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Monica Calasans-Maia A randomized controlled clinical trial

Rodrigo Resende
Gustavo Fernandes
to evaluate a new xenograft for
Jose Calasans-Maia alveolar socket preservation
Adriana Terezinha Alves
Jose Mauro Granjeiro

Authors’ affiliations: Key words: bone implant interactions, bone substitutes, clinical research, clinical trials
Monica Calasans-Maia, Rodrigo Resende,
Department of Oral Surgery, Fluminense Federal
University, Niteroi, Brazil Abstract
Gustavo Fernandes, Cell and Molecular Biology Objective: The aim of this clinical trial was to compare the effect of Bio-Ossâ and a new bovine
Department, Fluminense Federal University,
xenograft (Osseusâ) in alveolar sockets after a 24-week healing period.
Niteroi, Brazil
Jose Calasans-Maia, Department of Orthodontics, Materials and methods: A total of 20 adult volunteers ages 30–60 were subjected to single tooth
Fluminense Federal University, Nova Friburgo, extraction. A tooth extraction was performed at the baseline. All sites were randomly allocated to
Brazil
two test groups (TG1: grafted using a new bovine xenograft, Osseusâ, and TG2: grafted using
Adriana Terezinha Alves, Department of Oral
Pathology, Gama Filho University, Rio de Janeiro, commercially available bovine xenograft-Bio-Ossâ). Six months later, a sample of the grafted area
Brazil was obtained and implants were inserted in the same site. Histological sections were examined
Jose Mauro Granjeiro, Fluminense Federal
University, Niteroi, Brazil focusing on the presence of fibrous connective tissue (CT), and newly formed bone in direct
Bioengineering Program, National Institute of contact with the graft. The HE-stained sections were subjected to histomorphometrical evaluation
Metrology Standardization and Industrial Quality, using Image Pro-Plusâ software (Release 7.0). The definitive crown was placed 3 months later.
Duque de Caxias, Brazil
Results: Upon completion of the study, no patients were removed from the study and all inserted
Corresponding author: implants (10 in each group) were eventually integrated. After 6 months, in the TG1, the mean
Monica Calasans-Maia value of new bone formation was 33.7 (7.1), for CT was 32.3 (8.9) and for the remaining
Department of Oral Surgery
Fluminense Federal University biomaterial was 10.7 (16.2). In the TG2, the mean value of new bone formation was 19.3 (22.6),
Rua Mario Santos Braga of the CT was 49.9 (14.1) and of the remaining biomaterial was 22.6 (7.9).
30. Centro
Conclusions: No statistically significant difference was observed between TG1 and TG2 after
Niteroi
Rio de janeiro 6 months (P > 0.05), and both biomaterials afforded a more favorable implant position.
CEP: 24020-140
Brazil
e-mail: monicacalasansmaia@gmail.com
The aim of implant dentistry is to restore (Schropp et al. 2003), primarily due to the
missing or extracted teeth by placing implants resorption of the buccal bone plate (Araujo &
in anatomical, esthetical, and long-term Lindhe 2011). The ridge preservation proce-
functional restorative positions (Kutkut et al. dures facilitate the preservation of the alveo-
2012). The amount of hard tissue resorption lar architecture to prevent hard and soft
following tooth extraction occasionally tissue collapse and minimize or eliminate
involves prosthetically driven implant place- the necessity for future augmentation proce-
ment; therefore, the development of ridge dures (Tan et al. 2012). Many graft materials,
preservation techniques that result in less such as autogenous bone grafts (Pelegrine
alveolar bone loss is of great interest (Sisti et al. 2010), allografts (Wood et al. 2012;
et al. 2012). Extraction socket wound healing xenografts (Calasans-Maia et al. 2009; Fernan-
is characterized by resorption of the alveolar des et al. 2011; Spinato et al. 2012; Festa
bone at the extraction site, which reduces et al. 2011), and alloplasts (Gonshor et al.
the bone volume available for implant place- 2011; Ruga et al. 2011; Brkovic et al. 2012),
ment. Major changes in the extraction socket have been used to maintain the dimensions
occur during the first year after tooth extrac- of the alveolar ridge after extraction in
Date: tion, with two-thirds of the bone loss occur- humans. Although some of these graft mate-
Accepted 3 July 2013 ring within the first 3 months (Schropp et al. rials preserved the post-extraction alveolar
To cite this article: 2003; Ara ujo et al. 2008; Van der Weijden ridge dimensions to some extent, the quan-
Calasans-Maia M, Resende R, Fernandes G, Calasans-Maia J, et al. 2009), although dimensional changes tity and the quality of the bone tissue forma-
Alves AT, Granjeiro JM. A randomized controlled clinical
trial to evaluate a new xenograft for alveolar socket are observed up to 1 year after tooth extrac- tion in the socket varied and the presence
preservation.
tion, resulting in a 50% reduction in the buc- of these materials has often affected the
Clin. Oral Impl. Res. 00, 2013, 1–6
doi: 10.1111/clr.12237 colingual dimension of the alveolar ridge usual healing process (Heberer et al. 2011).

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 1
Calasans-Maia et al  Alveolar socket preservation with xenograft

Xenografts are obtained from a species that is Table 1. List of volunteer subjects investigated clinical photographs, study casts, and clinical
different from that of the recipients, and as Experimental examinations of the extraction sites. Sub-
osteoconductors, these grafts are predomi- Patient Gender Age Tooth groups sequently, the volunteers were provided
nantly made from the inorganic portion of 1 Female 30 46* 1 with detailed oral hygiene instructions, and
animal bone tissue (Granjeiro et al. 2005; 2 Female 52 37* 2 customized surgical splints were fabricated
3 Female 53 37* 2
Munhoz et al. 2006; Calasans-Maia et al. on the study casts for use in reentry proce-
4 Male 44 21‡ 1
2009; Accorsi-Mendoncßa et al. 2011; Zam- 5 Female 34 46* 2 dures to accurately obtain bone biopsies from
buzzi et al. 2012). The processing of bovine 6 Male 58 46‡ 1 the center of the grafted sockets.
bone results in two distinct types of materi- 7 Male 50 47‡ 2
8 Female 51 46* 2
als: inorganic and organic (predominantly col- 9 Female 34 36* 1
Surgical procedures
lagen type I). Inorganic material is free of 10 Female 34 16* 1 The following implant procedure was used at
proteins and cells because it only consists of 11 Female 53 22† 1 all extraction sites. The extraction was
12 Male 50 27‡ 2 performed under local anesthesia, without the
hydroxyapatite. The proteins are removed
13 Male 60 15† 2
through heat treatment at temperatures 14 Male 52 36‡ 2
elevation of a mucoperiosteal flap (Fig. 1a,b,
above 300°C or alkali treatment, followed by 15 Male 23 47* 2 Data S1). A periotome and the appropriate
neutralization, thus eliminating the risk of 16 Female 56 36† 1 dental forceps were used to minimize surgical
17 Female 48 26* 1
disease transmission. However, the bioab- trauma of the surrounding tissue. The thor-
18 Female 45 24† 1
sorption of these materials is reduced with 19 Female 33 34† 2 ough curettage of all soft tissue debris in the
increasing temperature (Wenz et al. 2001). 20 Female 31 36† 1 alveolus was performed during the extraction
Indeed, bovine materials obtained from Brazil *Extraction due to periodontal reason.
at all extraction sites to ensure the removal of
are regarded favorably, as Brazilian cattle are †
caries. all granulation tissue and stimulate bleeding

free of spongiform encephalopathy (BSE or tooth/root fracture. from the osseous base to promote healing. A
mad cow disease). A new Brazilian bone sub- caliper (Dentaurumâ; Dentaurum Dental
stitute (Osseousâ; SIN, S~ao Paulo, SP, Brazil), size (10 subjects per group) was established Technology, Ispringen, Germany) was subse-
comprising an inorganic bovine bone matrix, in an attempt to minimize the publication quently used to measure the horizontal ridge
has been used as an alternative graft material bias (Vignoletti et al. 2012, Sisti et al. 2012). width (buccolingually) at the midpoint of the
for ridge preservation after tooth extraction alveolar crest using the mid-buccal and mid-
prior to implant placement. In previous in Patient selection palatal marks on the cervical bone surface as
vivo studies, we confirmed that this bovine All the patients were in general good health. published before (Mardas et al. 2011, Vigno-
xenograft is a biocompatible, bioabsorbable Any patient requiring one tooth extraction letti et al. 2012). After completion of the mea-
osteoconductor (Calasans-Maia et al. 2009; (hopeless tooth for periodontal, traumatic, or surements, the randomization envelope was
Jardelino-Lima et al. 2008). The aim of this caries reasons) and showing a bone defect opened and the assigned treatment test Osse-
study was to compare the effects of two between 3 and 5 mm at the buccal wall and ousâ (SIN) or control (Geistlich Biomaterials,
deproteinized bovine bone minerals in the no soft tissue recession was eligible for this Wollhusen, Switzerland) was revealed to the
healing of fresh extraction sockets using study according to specific exclusion and surgeon. The implant did not exceed the
clinical, histological, and histomorphometric inclusion criteria (Table 2). The recruitment height of the alveolar crest, and the site was
analyses. of the volunteers was carried out during visually inspected to ensure that the biomate-
6 months, and all volunteers were followed rial was saturated with blood (Fig. 1c). Pri-
up for a period of 12 months after prosthetic mary wound closure was performed following
Material and methods the elevation and rotation of the mucoperio-
rehabilitation. The volunteer subjects were
randomly assigned to the tests groups using steal flap (Fig. 1d,e). Postoperative antibiotic
This study was performed in compliance
an envelope system distribution provided by therapy (500-mg Azithromycin) was adminis-
with the principles outlined in the Declara-
the principal investigator. tered once a day for the first postoperative
tion of Helsinki concerning experimentation
week, and a disinfectant mouth rinse (0.12%
involving human subjects. Quality assess-
Presurgical procedures Chlorhexidine) was prescribed two times per
ment was carried out based on the RCT-
The medical and dental histories of the day, for the first two postoperative weeks.
checklist of the CONSORT-statements
patients were reviewed, and each patient Postoperative clinical evaluations of the
(Schulz et al. 2010). All procedures and mate-
was evaluated using periapical radiographs, patients were performed at 1, 7, 30, and
rials in the present study were approved
through the relevant independent committee
on the Ethics of Human Research of Flumin-
Table 2. Inclusion and exclusion criteria
ense Federal University (CEP/HUAP nº 118),
Inclusion criteria Exclusion criteria
and the volunteer subjects were informed
Age between 30 and 60 years Pregnancy or lactating period
about the study protocol and required to sign
Good general health Smoking
a consent form. Twenty patients (ten women Presence of a hopeless tooth requiring Chronic treatment with any medication known
and 10 men) participated in this randomized, extraction to affect oral status and bone turnover
controlled clinical trial, which took place in The extraction site would be suitable for Contraindicate surgical treatment
replacement by a dental implant Suffering from a known psychological disorder
the Dental Clinical Research Center at Flu-
Volunteer subjects had voluntarily signed
minense Federal University, Rio de Janeiro, the informed consent
Brazil (Table 1, Data S1). A minimum sample

2 | Clin. Oral Impl. Res. 0, 2013 / 1–6 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Calasans-Maia et al  Alveolar socket preservation with xenograft

(a) (b) Histological evaluation


Bone biopsy specimens (6 9 2 mm) obtained
from the grafted and ungrafted sockets were
fixed in 10% formalin for 2 days and subse-
quently decalcified in bone decalcification
solution (Alkimiaâ; Allkimia, Campinas, Bra-
zil) for 48 h. After routine processing, the tis-
sues were embedded in paraffin, sectioned
longitudinally into multiple 4lm-thick sec-
tions and stained with Hematoxylin and
Eosin (H&E) and Masson’s trichrome stain.
(d)
The two most central sections were obtained
from each specimen. For the qualitative and
morphologic analysis of the remodeling pro-
cess, the stained preparations were examined
under a light microscope (Zeiss Axioplan) at a
minimum 209 magnification and the entire
(c) section was evaluated. Ten digital images of
each section were acquired and used to trace
the areas identified as vital bone, biomaterial
particles, and connective tissue (CT)/other
non-bone components. Image analysis soft-
(f) ware (Image ProPlusâ, Release 7.0; MediaCy-
bernetics, Silver Spring, MD, USA) was used
to create individual layers of newly formed
bone, biomaterial particles, and CT/other non-
bone components, which were assessed by a
single observer blinded to the clinical data.

(e) Statistical analysis


The results were expressed as the means 
95%CI. The Mann–Whitney unpaired test were
(g) performed, considering significant differences if
P < 0.05.

Results

Clinical findings
Clinical healing was uneventful and free of
infection or symptoms in all volunteers from
both groups. Age and gender did not signifi-
cantly affect the clinical outcomes of this
Fig. 1. (a, b) Clinical and radiographic aspects of the hopeless tooth; (c) socket filled with the osseus xenograft; (d) study.
The flap was advanced coronally for primary closure; (e) radiographic aspect of the immediate area post grafting; (f, Almost complete soft tissue closure was
g) clinical and radiographic aspects at 6 months after grafting.
observed at 10 days after extraction in both
test groups. After 6 months of healing, when
90 days to determine the presence of compli- ridge width buccolingually. A core biopsy the bone specimen sample was obtained, both
cations, such as infection with inflammation, with a depth of 6 mm was obtained from the groups exhibited the same bone density and
wound dehiscence, or loss of graft material. center of the extraction site. A trephine bur showed the same resistance on trephine appli-
After 6 months, all sockets were evaluated (2 mm in diameter, SIN) was used to collect cation. Bone core samples were retrieved, and
through clinical and radiographic examination the biopsy specimen (Fig. 2a), followed by implants were placed in all sockets. The hori-
(Fig. 1f,g). dental implant placement according to the zontal ridge width (buccolingually) was mea-
manufacturer’s surgical protocol. Try-On or sured at the midpoint of the alveolar crest
Surgical reentry Strong implants (SIN) were used (Fig. 2b,c). using the mid-buccal and mid-palatal marks
At 24 weeks after extraction, the implants The mucoperiosteal flaps were closed with on the cervical bone crest before the tooth
were placed. A mucoperiosteal flap was interrupted sutures (Silk suture 4-0, Ethi- extraction and after 6 months of socket heal-
raised, and the site of extraction was identi- conâ). After 6 months, the implants were ing, and the results are showed in Table 3.
fied using a customized surgical splint. A successfully placed at all sites in the control Statically significant differences were not
caliper was used to measure the horizontal and test groups (Fig. 2d). observed between the groups.

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 3 | Clin. Oral Impl. Res. 0, 2013 / 1–6
Calasans-Maia et al  Alveolar socket preservation with xenograft

(a) (c) (a)

(b) (b)

(d)

(c)

Fig. 4. Histomorphometric evaluation of the alveolar


Fig. 2. (a) Before implant installation a 2-mm specimen was removed using a trephine; (b, c) Clinical and sockets grafted with Bio-Ossâ and Osseusâ, consider-
radiographic images of the installed implant; (d) Prosthetic rehabilitation. ing the volume density of (a) newly-formed bone; (b)
connective tissue and (c) residual biomaterial particles.
Points in the plot represent all data, mean 95% of confi-
Histological observations dence interval (bars).

Table 3. Clinical outcomes with respect to Test sites


width in millimeters (standard deviation in
parentheses) One experienced blinded pathologist performed mation of new well-mineralized vital trabecu-
the histological evaluation. Histological slides lar bone was observed in all examined sections.
Change in
Tooth Group Baseline End width (mm) were prepared, and the cores were examined at The new bone showed trabecular organization,
209 and 409 magnification, revealing new with collagen fibers arranged in a meshwork
46 1 11 10.6 0.4
37 2 10 9.5 0.5 bone formation in all grafted sockets. The for- pattern and osteocytes randomly distributed
37 2 9.5 9.1 0.4
21 1 8.0 7.8 0.2
46 2 11.2 10.9 0.3
46 1 12.1 11.6 0.5 (a) (b)
47 2 12.3 12 0.3
46 2 11 10.4 0.6
36 1 11.5 11.1 0.4
16 1 11 10.8 0.2
22 1 7.0 6.8 0.2
27 2 12.0 11.7 0.3
15 2 6.5 6.3 0.2
36 2 11.5 11.2 0.3
47 2 12.4 12 0.4
36 1 11.8 11.6 0.2
26 1 12.1 12 0.1
24 1 9.0 8.8 0.2
34 2 7.0 6.4 0.6
Fig. 3. (a, b) Photomicrographs of the interface between xenograft and the new formed bone, Stain HE, 109 and
36 1 11.9 11.4 0.5
409 augmentation.

4 | Clin. Oral Impl. Res. 0, 2013 / 1–6 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Calasans-Maia et al  Alveolar socket preservation with xenograft

within the trabeculae in large spindle-shaped first 3–6 months, followed by gradual reduc- osseous resorption and significant contour
lacunae (Fig. 3a,b). Loose fibrous tissue with tions in the dimensions. A previous study changes especially in the horizontal plane of
thin vessels filled the trabecular spaces. Dense, discussed so-called ridge preservation tech- the residual alveolar ridge (Schropp et al.
trabecular bone patterns were observed in both niques, which are categorized into two differ- 2003; Araujo & Lindhe 2011). These changes
test groups. The overall mean value of the ent groups: techniques for maintaining the may be limited because our sample is mainly
newly formed vital bone area fraction for TG1 ridge profile (ridge preservation) and tech- composed by molars. A shorter 3-month
was 33.6% (7.1) and 19.3% (22.5) for TG2. niques for enlarging the ridge profile (ridge healing period should be evaluated in future
For TG1, the mean value of the newly formed augmentation). The reasons for ridge preser- studies. A recent systematic review evalu-
CT was 32.3% (8.8), and the mean value vation include the maintenance of the exist- ated bone healing after tooth extraction,
of the remaining biomaterial was 10.6% ing soft and hard tissue envelope, with or without an intervention, and the
(16.2). For TG2, the mean value of the CT maintenance of a stable ridge volume for histological evaluation revealed a large pro-
was 49.9% (14.0), and the mean value of the optimizing the functional and esthetic out- portion of residual graft material that might
remaining biomaterial was 22.5% (7.9) comes, and the simplification of treatment account for some of the differences in the
(Fig. 4). procedures subsequent to ridge preservation alveolar ridge dimensions observed during
(Vignoletti et al. 2012). Contraindications for the follow-up exam (Morjaria et al. 2012).
Discussion ridge preservation were considered in patients Another recent systematic review evaluated
irradiated in the area planned for ridge preser- the effectiveness of bone preservation using
The present randomized clinical trial com- vation, patients taking biphosphonates and graft materials in non-molar alveolar regions
pared two bovine xenografts (Bio-Ossâ and when general contraindications against oral and suggested that the graft materials might
Osseusâ) for the preservation of the alveolar surgical interventions and infections at the not prevent physiological resorptive bone
ridge dimensions following tooth extraction. site planned for ridge preservation were processes after tooth extraction, although
The clinical, histological, and histomorpho- observed, which could not be treated during these materials might reduce changes in the
metrical evaluations did not show significant ridge preservation surgery (H€ammerle et al. resulting bone dimensions (Ten Heggeler
differences between the two materials. In the 2012). The volunteer subjects included in the et al. 2011).
present study, biopsy specimens were present clinical trial did not present contrain-
obtained and dental implants were placed dications for ridge preservation. In the pres- Conclusions
after a 6-month healing period. A healing ent study, mucoperiosteal flaps were raised
period of 6 months was selected because this to preserve the ridge profile and facilitate The alterations in the dimension of the alve-
time point was used in two previously primary wound closure. The primary closure olar ridge following tooth extraction were
reported systematic reviews. The first sys- of the wound is beneficial with respect to similar between the groups, affording a more
tematic review showed 29–63% horizontal the volume gained as a result of this favorable implant position.
bone loss and 11–22% vertical bone loss approach (H€ammerle et al. 2012). Cellular
after 6 months following tooth extraction differentiation, augmentation material break-
and demonstrated rapid reductions in the down, and bone replacement were evidenced Acknowledgements: The authors
first 3–6 months, followed by gradual reduc- at the grafted sites, largely preserving the thank Sistema de Implantes Nacional, S~ao
tions in the dimensions (Tan et al. 2012). dimensions of the alveolar ridge after Paulo, Brazil (SIN) for providing financial
The second systematic review showed a 6 months of healing. In the present study, a support for this study. We also want to
3.8 mm horizontal reduction in width and a very small horizontal resorption of the bone express our thanks to Dr. Alfredo Schnetzler
1.24 mm vertical reduction in height of the crest after the two types of treatments was Neto and Frederico, Prosthodontists, Rio de
alveolar ridge within 6 months after tooth observed in both groups, confirming previous Janeiro, Brazil for his significant
extraction (H€ ammerle et al. 2012). These clinical and preclinical reports that post- contributions to developing the
studies demonstrated rapid reductions in the extraction healing is always characterized by prosthodontic rehabilitation.

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6 | Clin. Oral Impl. Res. 0, 2013 / 1–6 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Clin Oral Invest (2013) 17:341–363
DOI 10.1007/s00784-012-0758-5

REVIEW

Alveolar ridge preservation. A systematic review


Attila Horváth & Nikos Mardas & Luis André Mezzomo &
Ian G. Needleman & Nikos Donos

Received: 31 December 2011 / Accepted: 14 May 2012 / Published online: 20 July 2012
# Springer-Verlag 2012

Abstract in six out of eight studies. Histological analysis indicated


Objective The objective of this paper is to examine the various degrees of new bone formation in both groups. Some
effect of alveolar ridge preservation (ARP) compared to graft interfered with the healing. Two out of eight studies
unassisted socket healing. reported statistically significantly more trabecular bone for-
Methods Systematic review with electronic and hand search mation in the ARP group. No superiority of one technique for
was performed. Randomised controlled trials (RCT), controlled ARP could be identified; however, in certain cases guided
clinical trials (CCT) and prospective cohort studies were bone regeneration was most effective. Statistically, signifi-
eligible. cantly less augmentation at implant placement was needed
Results Eight RCTs and six CCTs were identified. Clinical in the ARP group in three out of four studies. The strength of
heterogeneity did not allow for meta-analysis. Average change evidence was moderate to low.
in clinical alveolar ridge (AR) width varied between −1.0 Conclusions Post-extraction resorption of the AR might be
and −3.5 ± 2.7 mm in ARP groups and between −2.5 limited, but cannot be eliminated by ARP, which at histolog-
and −4.6±0.3 mm in the controls, resulting in statistically ical level does not always promote new bone formation. RCTs
significantly smaller reduction in the ARP groups in five out with unassisted socket healing and implant placement in the
of seven studies. Mean change in clinical AR height varied ARP studies are needed to support clinical decision making.
between +1.3±2.0 and −0.7±1.4 mm in the ARP groups and Clinical relevance This systematic review reports not only on
between −0.8±1.6 and −3.6±1.5 mm in the controls. Height the clinical and radiographic outcomes, but also evaluates the
reduction in the ARP groups was statistically significantly less histological appearance of the socket, along with site specific
factors, patient-reported outcomes, feasibility of implant
A. Horváth : N. Mardas : L. A. Mezzomo : I. G. Needleman : placement and strength of evidence, which will facilitate the
N. Donos (*)
decision making process in the clinical practice.
Unit of Periodontology, Department of Clinical Research,
UCL Eastman Dental Institute,
256 Gray’s Inn Road, Keywords Tooth extraction . Bone resorption . Implant site
London WC1X 8LD, UK development . Bone substitute . Bone regeneration .
e-mail: n.donos@ucl.ac.uk
Human histology
A. Horváth
Department of Periodontology, Semmelweis University,
Budapest, Hungary Introduction
L. A. Mezzomo
Pontifical Catholic University of Rio Grande do Sul, Periodontal disease, periapical pathology and mechanical trau-
Porto Alegre, Brazil ma often result in bone loss prior to tooth removal [1]. Further-
more, traumatic extraction has also been associated with
I. G. Needleman
additional loss of bone. In the healing phase after extraction,
International Centre for Evidence-Based Oral Health,
UCL Eastman Dental Institute, alveolar bone undergoes additional atrophy as a result of the
London, UK natural remodelling process [2–7]. This begins immediately
342 Clin Oral Invest (2013) 17:341–363

after extraction and may result in up to 50 % resorption of the Definition


alveolar ridge (AR) width even in 3 months [1]. Post-extraction
AR resorption may have an impact on dental implant place- Whilst ‘socket preservation’ has widely been employed to
ment, since sufficient vertical and horizontal volume of alveolar depict a certain procedure, we believe that the objective of
bone should ideally be present at the site of insertion [8]. these interventions is to preserve the dimension of the AR.
Alveolar ridge preservation (ARP) procedures have been Therefore, we have used the term ‘Alveolar Ridge Preser-
introduced to maintain an acceptable ridge contour in areas vation’ to define such procedures.
of aesthetic concern, as well as to prevent alveolar ridge
atrophy and maintain adequate dimensions of bone in order Types of studies
to facilitate implant placement in prosthetically driven posi-
tions [9, 10]. Several methods have already been investigat- Longitudinal prospective studies were included, i.e. RCTs,
ed for ARP in preclinical models [11–14] and clinical CCTs and cohort studies with control group.
studies, such as socket grafting with autogenous bone
[15], demineralised freeze-dried bone allograft (DFDBA) Populations of studies
[15–17], xenografts, like deproteinized bovine-bone
mineral (DBBM) [18], alloplasts [19] and bone morpho- Healthy individuals, without any age limit, who underwent
genic proteins (BMP) [20]. Guided bone regeneration any type of ridge preservation following permanent tooth
(GBR) with or without bone grafts has also been evaluated extraction, were included. Smokers and patients with history
[9, 10, 21–25]. of periodontal disease were not excluded. The minimum
Although some of the above bone substitutes were number of subjects per group was five. However, no limit
able to limit the resorption of post-extraction alveolar was set for study follow-up period.
ridge up to a certain extent, the quality of the new
tissue in the socket varied broadly. The remnants of Types of interventions
the grafts often interfered with the normal healing pro-
cess in line with preclinical results [15–17, 26]. A Test groups
number of review articles on ARP have been published
in the last decade [27–32]. However, a systematic as- Studies reporting on any of the following types of interven-
sessment of the nature and quality of the newly formed tions were included: socket grafting (autograft, allograft,
tissue alongside methodological quality and risk of bias xenograft, alloplastic materials); socket sealing (soft tissue
of the studies has not been carried out. Furthermore, grafts); GBR (resorbable/non-resorbable barriers); biological
non-controlled prospective and retrospective studies as active materials (growth factors) and combinations of the
well as case series were also included in most of the above techniques/materials.
previous reviews without the comparison to the control
group of unassisted socket healing [33–36]. Control groups
Therefore, the objective of the present systematic review
was to investigate the effect of ridge preservation on the The control groups of the included studies comprised empty
residual alveolar ridge dimensions and on histological char- sockets, i.e. unassisted socket healing.
acteristics, compared to unassisted socket healing.
Outcome variables

Methods The primary outcome was the change in oro-facial (horizontal)


and apico-coronal (vertical) AR dimensions. Secondary out-
Prior to commencement of the study, a detailed protocol was comes were the following: (1) change in buccal plate thickness;
developed and agreed upon by the authors based on the (2) bone volume alteration following extraction; (3) complica-
Cochrane Collaboration guidelines and previous reviews tions; (4) histological healing characteristics; (5) site eligibility
published by our group [37–41]. for placement of an adequate size dental implant with or
without further augmentation; (6) patient-reported outcomes,
Focused question such as quality of life and (7) health economics.

Following tooth/root extraction in humans, what is the effect Risk of bias and methodological quality assessment
of ridge preservation on the residual alveolar ridge dimension
and on histological characteristics, compared to unassisted In order to evaluate the methodological quality and risk of
socket healing? bias of individual studies, we used a combination of
Clin Oral Invest (2013) 17:341–363 343

parameters from the Cochrane Collaboration and Consoli- Exclusion criteria


dated Standards of Reporting Trials (CONSORT) statement.
The following parameters were assessed and taken into 1. Case reports, case series, retrospective analyses were
consideration in the final analysis: sample size calculation, excluded.
statement of eligibility criteria, ethics approval, informed 2. Studies without a control group comprising unassisted
consent, baseline homogeneity, randomisation method, allo- socket healing were excluded.
cation concealment, masking, calibration, follow up, protocol 3. Studies on medically compromised patients, e.g. uncon-
violation, method of statistics, unit of analysis, CONSORT trolled diabetes mellitus or cancer were excluded.
implementation, International Standard Randomised Con- 4. Studies reporting on immediate placement of dental
trolled Trial Number Register (ISRCTN) and funding disclo- implant were excluded.
sure. Methodology unique to RCTs was not assessed in CCTs, 5. Studies describing extraction of third molars were
i.e. randomisation and concealment of allocation. excluded.
Randomisation was accepted as adequate, in case the
allocation sequence was correctly generated either by Search strategy
computer, toss of a coin, throwing dice, etc. Quasi
randomisation, e.g. birth dates, hospital numbers were A sensitive search strategy was designed as we anticipated
not accepted. Adequacy of allocation concealment was that relevant studies might be difficult to locate. The search
accepted if the sequence was concealed, until interven- strategy incorporated both electronic and hand searches. The
tion was assigned (e.g. in sequentially numbered and following electronic databases were utilised in Apr 2010: (1)
sealed opaque envelopes, remote computer or central MEDLINE In-Process & Other Non-Indexed Citations
telephone). Statistical analysis was judged as adequate and MEDLINE 1950 to present via Ovid interface; (2)
if appropriate statistical method was selected to accom- EMBASE Classic + EMBASE 1947 to present via Ovid
modate to the characteristic of the each individual data interface; (3) The Cochrane Central Register of Controlled
(e.g. number of groups and investigated categories, size Trials (CENTRAL); (4) LILACS.
of samples, normally distributed or skewed data, para- The electronic search strategy used the following combi-
metric or non-parametric, paired or unpaired, numerical nation of key words and MeSH terms: (“tooth extraction”
or categorical variables). Statistical significance was ac- OR “tooth removal” OR “socket” OR “alveol$” OR “ridge”
cepted in case of confidence interval (CI) >95 % (p< OR “crest” OR “tooth socket” OR “alveolar bone loss” OR
0.05), while ‘statistically highly significant’ referred to “bone resorption” OR “bone remodeling”) AND (“preserv
CI>99.9 % (p<0.001). $” OR “reconstruct$” OR “augment$” OR “fill$” OR “seal
Based on the above, we attempted to categorize the $” OR “graft$” OR “repair$” OR “alveolar ridge augmen-
possible risk of bias as low, moderate or high. Low risk tation” OR “bone regeneration” OR “bone substitutes” OR
referred to studies with adequate randomisation method, “transplantation”).
sequence concealment and masking of examiner. Studies Cochrane search filters for RCTs and CCTs were imple-
were classified as moderate, if one of the above key mented. In addition, cohort trials were also searched. The
categories were missing, or high risk of bias, if more results were limited to humans only.
than one were lacking. An extensive hand search was also performed encom-
passing the bibliographies of the included papers and review
Inclusion criteria articles. Furthermore the following journals were screened
from 2001 to April 2010: Clinical Oral Implants Research,
1. All prospective longitudinal studies (i.e. RCTs, CCTs Clinical Implant Dentistry and Related Research, European
and cohort studies) were included, where one of the Journal of Oral Implantology, Implant Dentistry, Interna-
above mentioned types of interventions were carried tional Journal of Oral and Maxillofacial Implants, Interna-
out in the test group, whereas unassisted socket healing tional Journal of Periodontics and Restorative Dentistry,
served as control. Journal of Clinical Periodontology, Journal of Dental Re-
2. Studies on healthy individuals, without any age limit, search, Journal of Oral and Maxillofacial Surgery, Journal
who underwent ARP following tooth extraction, were of Periodontology, Oral Surgery, Oral Medicine, Oral Ra-
included. diology, Oral Pathology and Endodontics, Periodontology
3. Studies had to report on minimum of five patients per 2000. No language restrictions were applied. Translations
group. were carried out as necessary by two reviewers (AH, LAM).
4. Studies, performing clinical or three-dimensional (3D) The extracted data were copied into Reference Manager
radiographic evaluation of hard tissue or histological 10 software (Thomson Reuters, New York, NY, USA). Thus
assessment, were included. the further steps of screening were performed on this
344 Clin Oral Invest (2013) 17:341–363

interface. A three-stage selection of the resulted hits was 14 publications eligible for the review [17, 19–21, 23–25,
performed independently and in duplicate by two reviewers 42–48]. The excluded full text papers along with the reasons
(AH and LAM). In order to reduce errors and bias, a cali- for exclusion are listed in Table 1. The most typical reasons
bration exercise was performed with the first 500 titles, for exclusion were lack of control group with unassisted
resulting in 96.4 % agreement. In case of disagreement at socket healing; use of retrospective design; assessment of
the title selection stage, the trial was included in the abstract dimensional changes of the AR only on periapical two-
stage. At the abstract and full text selection any disagree- dimensional radiographs, or on casts taken from soft tissue
ments between the above reviewers were resolved by dis- level; and surgical removal of third molars.
cussion. If unresolved, a third reviewer (NM) was involved The Kappa score for agreement between the reviewers (AH,
for arbitration. The reasons for exclusion were recorded LAM) at the abstract and full text selection level, was 0.96 and
either in the Reference Manager (abstract stage) or in a 0.90, respectively, indicating a high level of agreement.
specific data extraction form (full text stage). The level of
agreement was determined by Kappa score calculation. Study characteristics

Research synthesis In the 14 included articles (eight RCTs and six CCTs) the
efficacy of ARP techniques was evaluated clinically by
Studies were grouped by research design and their chief means of direct measurements of the residual alveolar ridge
characteristics. Outcomes were recorded in evidence tables. dimensions during re-entry procedures, radiographically by
In view of the marked heterogeneity, no meta-analysis was means of computer tomography or histologically from tre-
conducted. Instead, a narrative synthesis was undertaken. phine biopsies taken at re-entry during osteotomies for
implant placement (Tables 3 and 4). No cohort studies were
indentified. Limited data were reported on confounding
Results factors, such as periodontitis, smoking, systemic disease
and medication. The extraction site distribution was fairly
Search sequence heterogeneous. In some studies ARP was performed only in
maxillary anterior sockets [42, 46, 47], whereas such restric-
The electronic search yielded 6,216 relevant hits after re- tion was not employed in other studies. The residual bone
moval of duplicates (Fig. 1). Subsequently, 157 titles were volume around the investigated sockets, e.g. the presence/
selected for the abstract stage. Following investigation of absence and width of the buccal bone plate varied from
the abstracts, 42 articles qualified for full text evaluation. severely compromised [20, 46], to completely intact, buccal
Four extra papers were then added as a result of the hand bone (Table 3) [17, 21, 42].
search. Assessment of these articles resulted in the following
Intervention characteristics
Electronic search
6.216 titles With regard to the techniques or materials used for ARP, the
6,059
Excluded based included studies were grouped into three categories (Table 3);
on the title
Relevant 1. Bone grafts/substitutes
abstracts 2. GBR
Kappa score 115
0.96 Excluded based 3. Biological active materials.
on the abstract
Relevant full-texts In the majority of the included studies, various bone
42 grafts were utilised, such as autologous bone marrow [47],
3 Included
as a result of plasma rich in growth factor (PRGF) with or without autol-
hand search
Full-text analysis ogous bone [43], DFDBA [17], DBBM [46], calcium sul-
45 phate hemihydrates [42, 45] and bioactive glass [17].
Kappa score 32 Alloplastic polyglycolide/polylactide (PGPL) sponge was
0.90 Excluded based
on the full-text also employed [19, 48]. GBR technique was applied using
non-resorbable expanded polytetrafluoroethylene (e-PTFE)
1 Included [24] or resorbable (PGPL) [25] barrier. Resorbable collagen
as a result of
final search membrane was also employed in combination with FDBA
Included publications [23] or corticocancellous porcine bone [21]. Biological ac-
14
tive material, namely bone morphogenic protein (rhBMP-2)
Fig. 1 Flow chart of the screening process was used on a collagen sponge carrier in one study [20].
Clin Oral Invest (2013) 17:341–363 345

Table 1 List of excluded full text papers and reasons for exclusion

First author Journal Reasons for exclusion


(year of publication)

Bianchi (2004) Int J Periodont Rest Dent Retrospective analysis


Single-arm of the included Fiorellini et al. (2005)
Bolouri (2001) Comp Cont Educ Dent Reported on optical density on two-dimensional radiographs
Brawn (2007) Impl Dent Case report
Brkovic (2008) J Can Dent Assoc Case report
Carmagnola (2003) Clin Oral Impl Res Lack of real control group, resembles to a retrospective analysis
(extreme difference in follow-up period between tests and controls.
T1: 4 months; T2: 7 months; C: 1-15 years, mean: 7.8 years)
Cranin (1988) J Biomed Mat Res Case series without control group
De Coster (2009) Clin Impl Dent Relat Res Case series
Retrospective study as stated by the authors in the discussion
Healing period varied between 1.5 months and 1.5 years
Neither histomorphometry nor clinical or radiographic measurements
reported in the results
Graziani (2008) J Cranofac Surg Extraction of fully impacted third molars
Linear measurements on OPG
Gulaldi (1998) Oral Surg Oral Med Extraction of fully impacted third molars
Oral Pat Oral Rad End Linear measurements on OPG and scintigraphy
Primary outcome was to analyze bone metabolism
Heberer (2008) Clin Oral Impl Res Case series without control group
Hoad-Reddick (1994) Eur J Prosth Rest Dent Two-dimensional linear measurements obtained from OPG and cephalometry
Lack of defined landmarks
Surgical procedure was not described
Hoad-Reddick (1999) Eur J Prosth Rest Dent Description of a method for measurements on casts
Neither socket preservation procedure nor the results were described.
Soft tissue punch technique only
Howell (1997) Int J Periodont Rest Dent Case series without control group
Jung (2004) Int J Periodont Rest Dent Case series without control group
Primary outcome was soft tissue healing
Kangvonkit (1986) Int J Oral Maxillofac Surg Based on OPG and lateral cephalogram only
Evaluation method remains unclear
Primary outcome was the biocompatibility of HA cones
Karapataki (2000) J Clin Periodontol Extraction of fully impacted third molars
Primary outcome was to assess the periodontal status of
second molars after extraction of third molars
Kerr (2008) J Periodontol No biomaterials were used to preserve the ridge dimensions,
therefore did not address the focused question
Kwon (1986) J Oral Maxillofac Surg Based on OPG and lateral cephalogram only
Evaluation method remains unclear
Lack of description of the measurement methods
Molly (2008) J Periodontol Control group was covered by an e-PTFE membrane,
thus lack of unassisted control sockets
Munhoz (2006) Dento Maxillofac Radiol Extraction of fully impacted third molars
Two-dimensional evaluation of periapical radiographs
Norton (2002) Int J Oral Maxillofac Impl Case series without control group
Resembles to a retrospective design
(healing period ranged from 3 to 11 months)
Page (1987) J Oral Maxillofac Surg Case report
Pape (1988) Deutsche Zahnarztliche Augmentation of a resorbed ridge
Zeitschrift
346 Clin Oral Invest (2013) 17:341–363

Table 1 (continued)

First author Journal Reasons for exclusion


(year of publication)

Case series without control group


Penteado (2005) Braz J Oral Sci Immunohistochemical analysis
Did not address the focused question
Quinn (1985) J Am Dent Assoc Clinical measurements at soft tissue level only based on tattoo points,
thus failed to address the focused question
Resembles to a retrospective analysis
Schepers (1993) Impl Dent Retrospective case series without control group
Simon (2004) Ind J Dent Res Extraction of fully impacted third molars
Evaluated soft tissue healing and radiographic analysis based
on the two-dimensional periapical radiographs
Simion (1994) Int J Periodont Rest Dent Titanium implants placed simultaneously
No control group
Primary outcome was microbiological analysis
Smukler (1999) Int J Oral Maxillofac Impl Healed edentulous ridge as control instead of empty socket
No compatibility of the follow-up periods of the different groups
Svrtecky (2003) J Prosth Dent Case report
Throndson (2002) Oral Surg Oral Med Extraction of fully impacted third molars
Oral Pat Oral Rad End Measurements based on two-dimensional periapical radiographs
Yilmaz (1998) J Clin Periodontol Measurement at soft tissue level on study casts

None of the included studies used the socket sealing tech- the control groups (p<0.05). In two out of the three studies,
nique. Primary flap closure was achieved in 9 out of 14 the width reduction was statistically significantly smaller in
studies, while the sockets left uncovered in the rests. Various the test groups compared to the controls [42, 47].
types and amounts of antibiotics and antiseptic rinses were Four studies investigated the mean change in ridge height
administered for different duration in studies reporting on at the mid-buccal aspect [19, 42, 44, 47]. The AR height
postoperative care. Finally, average healing period ranged changed from baseline to re-entry between +1.3±1.9 mm
from one to nine months. and −0.5 ± 1.1 mm following ARP, and between −0.8 ±
1.6 mm and −1.2±0.6 mm in the control groups. The height
Outcome characteristics reduction between baseline and re-entry was not statistically
significant in one study in both test and control groups [44],
Clinical outcomes while one study reported an increase in height instead of
loss following ARP with a PGPL sponge (p<0.05) [19]. In
Eight out of the 14 included studies investigated the efficacy two out of the four studies, the height reduction was statis-
of various ARP techniques to preserve the pre-extraction tically significantly smaller in the test groups compared to
ridge dimensions using intra-surgical hard tissue measure- the controls [42, 47].
ments taken during re-entry procedure [19, 21, 23–25, 42, The vertical dimension changes at the mesial and distal
44, 47]. In these studies, ARP was performed in 137 sockets aspects of the socket were measured in two studies [19, 42]
of 119 patients and compared to 120 sockets that left to heal and did not present any statistically significant difference for
without any treatment in a total of 92 patients (Table 3). both groups.
Three studies captured data on socket fill and reported
Bone ‘graft’ Four studies evaluated changes in AR dimen- statistically significant differences between baseline and re-
sions following grafting of the socket. Two studies were RCTs entry in both groups [42, 44, 47], but only one reported
[42, 47] and two were CCTs [19, 44]. Healing time varied statistically significantly higher socket fill, where bioactive
from 3 to 6 months [19, 42, 44, 47]. glass was covered by calcium sulphate, compared to the
The horizontal (bucco-lingual) changes of the alveo- unassisted healing [44].
lar ridge were assessed in three studies [42, 44, 47].
The AR reduced in width from baseline to re-entry GBR Four studies evaluated changes in AR dimensions
between −1.0 mm and −3.5±2.7 mm following ARP following ARP with GBR alone [24, 25], or in combination
(p<0.05) and between −2.5 mm and −3.2±1.8 mm in with bone graft [21, 23]. Three studies were RCTs [21, 23,
Clin Oral Invest (2013) 17:341–363 347

25] and one was CCT [24]. Healing time varied between 4 Histological results
and 9 months.
Horizontal (bucco-lingual) changes of the AR were Eleven studies carried out a histological analysis based on
assessed in all four studies. AR width reduction from base- trephine biopsies retrieved at re-entry [17, 19–21, 23, 42,
line to re-entry varied between −1.2±0.9 mm and −2.5± 43, 45–48]. Seven studies were RCTs [17, 20, 21, 23, 46,
1.2 mm in the GBR-treated sockets and between −2.6± 47] and four were CCTs [19, 43, 45, 48]. In these studies,
2.3 mm and −4.6±0.3 mm in the control groups. With the ARP was performed in 181 sockets of 158 patients and
exception of one study [23], a statistically significantly compared to 149 sockets that left to heal without any
smaller reduction of the alveolar ridge width was observed treatment in 131 patients (Table 4). Only two out of
when e-PTFE [24], PGPL [25], or collagen membranes in eight studies reported statistically significantly higher tra-
combination with xenograft [21] were used. becular bone volume following ARP in comparison to unas-
All the four studies investigated the mean change in AR sisted socket healing [21, 42] and two studies reported
height at the mid-buccal aspect. The AR height changed statistically significantly more connective tissue in the post-
from baseline to re-entry between +1.3±2.0 mm and −0.7± extraction socket when no ARP was performed [17, 21]. On
1.4 mm in the ARP groups and between −0.9±1.6 mm the contrary, one study reported more vital bone in the
and −3.6±1.5 mm in the control groups. The resorption in unassisted socket healing group compared to the ARP
the ARP group was not statistically significant in three out group [23]. None of the differences of the investigated
of four studies [23–25]. All studies reported a statistically histomorphometric parameters reached statistical signifi-
significantly less post-extraction reduction in AR height cance in other studies.
when the socket was treated by GBR compared to unassisted
healing. Bone ‘grafts’ Eight studies evaluated histologically the
Vertical dimension changes at mesial and distal aspects healing of post-extraction sockets following the application
of the socket were measured in two studies [21, 23]. The of some type of bone grafts/substitutes [17, 19, 42, 43,
observed differences between baseline and re-entry were not 45–48]. Four studies were RCTs [17, 42, 46, 47] and four
statistically significant in both groups. In one out of the two were CCTs [19, 43, 45, 48]. New mineralised bone was
studies the height reduction was statistically significantly observed at various levels in all studies in both ARP and
smaller in the test group compared to the control [23]. control groups in a healing period from 2.5 to 8 months.
Two studies captured data on the socket fill [24, 25] and Connective tissue occupied a portion of the socket in both
reported statistically significant socket fill in both groups groups. When DFDBA, bioactive glass or DBBM were
between baseline and re-entry, as well as between tests and used, the graft particles were embedded either in new bone
controls. or in connective tissue. In most studies, there was no sig-
No data were found on either initial buccal plate thick- nificant difference in the type of healing, or amount of bone
ness or alteration of bone volume. However, one study formation between bone grafts and unassisted socket
measured the buccal bone thickness loss and reported sta- healing.
tistically significantly less reduction in the ARP group [47].
GBR in combination with graft GBR in combination with
Radiographic measurements graft was utilised in two RCTs. ARP with a collagen mem-
brane and deproteinized porcine bone resulted in statistically
Two RCTs, reporting on 3D radiographic assessment, met significantly higher new bone and lower connective tissue
the inclusion criteria [20, 46]. The healing time varied from formation after 7 to 9 months of healing in comparison to
1 to 4 months. In one study, where the post-extraction socket unassisted socket healing [21]. However, residual graft
was grafted with a radiopaque material (DBBM), treatment materials were present in the ARP biopsies. FDBA and
resulted in significantly less reduction in radiographic AR collagen membrane resulted in similar amounts of new bone
height compared to unassisted socket healing [46]. The test formation to untreated sockets, although more vital bone
group in the other study, where the higher concentration was observed in the untreated sockets at 4 to 6 months of
(1.5 mg/ml) of RhBMP-2 was utilised [20], resulted in a healing (p>0.05) [23].
mean increase of the radiographic AR width by 3.27±
2.53 mm at the most coronal part, compared to the 0.57± Biological active material RhBMP-2 in a collagen sponge
2.56 mm increase in the group of unassisted healing. AR carrier was completely resorbed at 4 months following ARP
height was reduced by 0.02±1.2 mm in the same test group regardless of the concentration of the growth factor [20].
and by 1.17±1.23 mm in the control group (Table 3). The Mineralised tissue was found and trabecular bone formation
differences between test and control were statistically was noticed in two third of both the test and control biopsies
significant. in the RCT.
348 Clin Oral Invest (2013) 17:341–363

Adverse events, complications 43, 45, 46]. Sample size calculations were reported only in
three studies [20, 23, 42], although with insufficient data to
Adverse events were reported in six RCTs [17, 20, 21, 25, evaluate the validity of the calculations. Statistical analysis
42, 47] and four CCTs [19, 24, 44, 48] including oedema, was appropriately carried out and described in one study
pain, erythema and membrane exposure/infection. In two only [47]. Appropriate statistics were either not carried out
studies, more adverse events, i.e. oedema, erythema [20] or [17, 19–21, 43, 45, 46], or the reported data were insuffi-
membrane exposure [24] were observed in the ARP group cient to determine the validity [23–25, 42, 43, 48]. In addi-
compared to the natural socket healing. No comparison tion, no RCTs were either registered with ISRCTN or
between tests and controls were reported in the other studies reported using the CONSORT guidelines (Table 3).
(Table 3).
Risk of bias
Feasibility of implant placement
Four studies were classified as moderate risk of bias [17, 21,
Seven studies [17, 19, 23, 42, 45, 46, 48] reported that 23, 25] and the rest were categorised as high risk of bias
implant placement in the previous sockets were successful, (Table 2).
but no differences between the ARP and untreated sites were
revealed. The outcome of implant placement remained un-
clear in one article [43] and only re-entry without implanta- Discussion
tion was performed in three trials [24, 44]. Four studies
reported the need of further augmentation at the stage of Key findings
implant placement. Three of them favoured the ARP group
over the controls, since less [20] or no sites [21, 47] in the This systematic review has demonstrated that different ARP
ARP group presented with residual dehiscence or fenestra- techniques do not totally eliminate post-extraction alveolar
tion defects around the inserted implants (Table 3). ridge resorption or predictably promote new bone forma-
tion. However, the reduction in ridge width and height
Patient-reported outcome and health economics following ARP may be less than that which occurs follow-
ing natural socket healing. The clinical data suggest that the
No data were found for patient-reported outcome measures horizontal ridge contraction was most successfully limited
or health economic evaluation. in the two studies applying GBR without additional bone
grafts [24, 25], whereas the vertical shrinkage was most
Quality assessment efficiently limited by employing GBR with additional bone
graft [21, 23].
Considerable heterogeneity was found among the studies in
terms of methodological quality. Detailed description of the Strengths of the review
quality assessment of the included studies is presented in
Table 2. Among the 14 included controlled studies, eight The present systematic review was limited to randomised
were randomised [17, 20, 21, 23, 25, 42, 46, 47] although in controlled trials, controlled clinical trials and prospective
four of them the randomisation technique was not reported cohort studies with a control group of empty untreated
[20, 42, 46, 47]. None of the RCTs reported the method of sockets. Furthermore, the inclusion criteria of our systematic
allocation concealment. Masking of the examiner was review were based on the fact that the clinical merit of
reported at the clinical level in two out of eight [23, 25], at applying the different ARP techniques could only be vali-
radiological level in one out of two [20] and at histological dated, if the clinical and histological outcomes following the
level in four out of 11 studies [17, 21, 42, 43]. Examiner application of a technique are superior to that of unassisted
calibration was declared in three papers [20, 23, 42], whilst socket healing.
inclusion and exclusion criteria were defined in seven pub- In comparison to the previous systematic reviews [28,
lications [17, 21, 23, 42, 43, 46, 47]. Apart from three 32] the present review has evaluated the histological char-
studies [21, 43, 46] all the other reported the approval of acteristics of the alveolar socket healing with or without
the ethical committee. Three studies were funded by indus- ARP. The amount and the quality of the newly formed
try [17, 20, 44], two studies by academic institution [45, 48] osseous tissues in the socket area are essential, especially
and the remaining nine did not report the source of funding. when the justification of ARP is to facilitate the placement
Nine trials implemented patient-based analysis [20, 21, of a dental implant in the position of a previously extracted
23–25, 42, 44, 47, 48], whilst the extraction site served as tooth. It is doubtful, whether an ARP technique should be
unit of analysis in the rest of the five investigations [17, 19, claimed successful, if it only preserves the external contour
Table 2 Quality assessment of the included studies
Study Quality Criteria Estimated
First author risk of bias
Year of publication Randomisation Masking Calibration Eligibility Criteria Follow up Ethical considerations Funding Statistical analysis Miscellaneous
Type 1. Randomised 1. Therapist 1. Intra-examiner 1. Inclusion 1. Percentage 1. Ethics approval Source of 1. Appropriate 1. Comparable
Reference number 2. Adequate 2. Patient 2. Inter-examiner criteria defined of completed 2. Informed Funding sample size experimental groups
sequence generation 3. Examiner 2. Exclusion follow ups consent calculation and power 2. CONSORT
3. Allocation 4. Statistician criteria defined 2. Adequate 2. Unit of analysis implemented
concealment correction 3. Appropriate 3. ISRCTN registered
4. Concealment statistics applied 4. Other comments
adequate

Aimetti 1. Yes 1. N/R 1. Yes (histo), 1. Yes 1. N/R 1. Yes N/R 1. Insufficient data 1. Yes High
Clin Oral Invest (2013) 17:341–363

2009 2. N/R 2. N/R N/R (clin) 2. Yes 2. N/A 2. Yes to determine 2. N/R
RCT 3. N/R 3. Yes (histo), 2. N/A 2. Patient 3. N/R
.#42 4. N/A N/R (clin) 3. Insufficient data
4. N/R to determine
*Reported as
‘double blind’

Anitua 1. Yes (btw T-C) 1. N/R 1. N/R 1. Yes 1. 100% 1. N/R N/R 1. N/R 1. N/R High
1999 No (within T) 2. N/R 2. N/A 2. Yes 2. Yes 2. Yes 2. Patient + site 2. N/R
CCT 2. N/A 3. Yes 3. No statistical analysis 3. N/R
#43 3. N/R 4. N/R was carried out 4. At severe defects
4. N/A autogenous bone
was added to PRGF.
Different healing periods.

Barone 1. Yes 1. N/R 1. N/R 1. Yes 1. 100% 1. N/R N/R, declared 1. N/R 1. Yes Moderate
2008 2. Yes 2. N/R 2. N/A 2. Yes 2. Yes 2. Yes no conflict 2. Patient 2. N/R
RCT 3. N/R 3. Yes (histo), of interest 3. No 3. N/R
#21 4. N/A N/R (clin) 4. Different healing
4. N/R periods.

Camargo N/A 1. N/R 1. N/R 1. Yes 1. 100% 1. Yes Industry 1. N/R 1. N/R High
2000 2. N/R 2. N/A 2. Yes 2. Yes 2. Yes 2. Patient 2. N/R
CCT 3. N/R 3. Insufficient data 3. N/R
#44 4. N/R to determine

Fiorellini 1. Yes 1. N/R 1. N/R 1. No 1. 100% 1. Yes Industry 1. Insufficient data 1. N/R High
2005 2. N/R 2. N/R 2. Yes 2. No 2. Unclear 2. Yes to determine 2. N/R
RCT 3. N/R 3. Yes (CT scans) 2. Patient 3. N/R
#20 4. N/A 4. N/R 3. No 4. Standardisation of
* Reported CT scans N/R.
as ‘double Final number
blind’ of sockets, patients
remain unclear.

Froum 1. Yes 1. N/R 1. N/R 1. Yes 1. 100% 1. Yes Industry 1. N/R 1. N/R Moderate
2002 2. Yes 2. N/R 2. N/A 2. Yes 2. Unclear 2. Yes 2. Site 2. N/R
RCT 3. N/R 3. Yes 3. No 3. N/R
#17 4. N/A 4. N/R 4. Different healing periods.
Enrolment of sites of
subjects inconsistent.
349
Table 2 (continued)
350

Study Quality Criteria Estimated


First author risk of bias
Year of publication Randomisation Masking Calibration Eligibility Criteria Follow up Ethical considerations Funding Statistical analysis Miscellaneous
Type 1. Randomised 1. Therapist 1. Intra-examiner 1. Inclusion 1. Percentage 1. Ethics approval Source of 1. Appropriate 1. Comparable
Reference number 2. Adequate 2. Patient 2. Inter-examiner criteria defined of completed 2. Informed Funding sample size experimental groups
sequence generation 3. Examiner 2. Exclusion follow ups consent calculation and power 2. CONSORT
3. Allocation 4. Statistician criteria defined 2. Adequate 2. Unit of analysis implemented
concealment correction 3. Appropriate 3. ISRCTN registered
4. Concealment statistics applied 4. Other comments
adequate

Guarnieri N/A 1. N/R 1. N/R 1. Yes 1. N/R 1. Yes Government; 1. N/R 1. N/R High
2004 2. N/R 2. N/A 2. No 2. N/A 2. Yes institution 2. Site 2. N/R
CCT 3. N/R 3. No 3. N/R
#45 4. N/R

Iasella 1. Yes 1. N/R 1. Yes 1. Yes 1. 100% 1. Yes N/R 1. Insufficient data 1. Yes Moderate
2003 2. Yes 2. N/R 2. N/A 2. Yes 2. Yes 2. Yes to determine 2. N/R
RCT 3. N/R 3. Yes 2. Patient 3. N/R
#23 4. N/A 4. N/R 3. Insufficient data
to determine

Lekovic N/A 1. N/R 1. N/R 1. No 1. 70% (premature 1. Yes N/R 1. N/R 1. Yes High
1997 2. N/R 2. N/A 2. No exposure of e-PTFE 2. N/R 2. Patient 2. N/R
CCT 3. N/R barrier in 3/10) 3. Insufficient data
#24 4. N/R 2. Yes to determine 3. N/R

Lekovic 1. Yes 1. N/R 1. N/R 1. No 1. 100% 1. Yes N/R 1. N/R 1. Yes Moderate
1998 2. Yes 2. N/R 2. N/A 2. No 2. Yes 2. Yes 2. Patient 2. N/R
RCT 3. N/R 3. Yes 3. Insufficient data 3. N/R
#25 4. N/A 4. Yes to determine

Nevins 1. Yes 1. N/R 1. N/R 1. Yes 1. 100% 1. N/R N/R 1. N/R 1. Yes High
2006 2. N/R 2. N/R 2. N/A 2. Yes 2. Yes 2. N/R 2. Site 2. N/R
RCT 3. N/R 3. N/R 3. No 3. N/R
#46 4. N/A 4. N/R 4. Standardisation of CT
scans N/R. Test material
radiopaque. Different
healing periods.

Pelegrine 1. Yes 1. N/R 1. N/R 1. Yes 1. 100% 1. Yes N/R 1. N/R 1. N/R High
2010 2. N/R 2. N/R 2. N/A 2. Yes 2. Yes 2. Yes 2. Patient 2. N/R
RCT 3. N/R 3. N/R 3. Yes 3. N/R
#47 4. N/A 4. N/R

Serino N/A 1. N/R 1. N/R 1. Yes 1. 80% 1. Yes N/R 1. N/R 1. N/R High
2003 2. N/R 2. N/A 2. No 2. Unclear 2. Yes 2. Site 2. N/R
CCT 3. N/R 3. No 3. N/R
#19 4. N/R 4. Molars only in T.
Clin Oral Invest (2013) 17:341–363
Clin Oral Invest (2013) 17:341–363 351

risk of bias

N/A not applicable; N/R not reported, T test; C control; RCT randomised controlled trial; CCT controlled clinical trial; PRGF platelet-rich growth factor; CONSORT Consolidated Standards of
Estimated
of the AR, but the newly formed tissue is of inferior quality

High
and quantity (percentage of matured trabecular bone) to
what is normally achieved following a tooth extraction.
Finally, the quality of the included studies has also been
meticulously assessed in this review. Such a quality evalu-
3. ISRCTN registered
experimental groups

4. Other comments
ation of the retrieved data is essential to estimate the source
1. Comparable
Miscellaneous

2. CONSORT
implemented

and magnitude of potential bias that may lead to delusive


conclusions.
1. N/R
2. N/R
3. N/R
Strength of evidence—risk of bias
calculation and power

3. Insufficient data
2. Unit of analysis
Statistical analysis

The quality assessment of the included studies in this sys-


statistics applied

to determine
1. Appropriate

3. Appropriate

tematic review revealed that none of the trials have qualified


sample size

2. Patient

for a low risk of bias category. Ten out of the 14 studies


1. N/R

presented with high risk of bias thus their results must be


evaluated with caution. The lack of clear reporting of re-
Government;
institution

search methodology elements, such as adequate randomiza-


Source of
Funding

Funding

tion and concealment and/or masking of the therapist and


the examiner were among the primary reasons for the high
risk of bias [49]. We did not contact authors for clarification
Ethical considerations
1. Ethics approval

of unclear methodology. Therefore, it is possible that actual


study conduct was better than that reported in the publica-
2. Informed

tion. Statistical considerations played important role as well,


consent

1. Yes
2. Yes

since appropriate analytical statistics was completed and


reported merely in one study [47]. Power calculation was
conducted in three trials only [21, 23, 42], nevertheless the
reported data were insufficient to determine the validity of
Reporting Trials; ISRCTN International Standard Randomised Controlled Trial Number Register
1. Percentage
of completed

2. Adequate
follow ups

2. Unclear
Follow up

the calculation.
correction

1. 80%

Dimensional changes and histological characteristics


Eligibility Criteria

criteria defined

criteria defined

Sufficient ridge width and height have been considered as


2. Exclusion
1. Inclusion

one of the key requirements for successful implant therapy


1. Yes
2. No

and for the establishment of an aesthetically pleasing emer-


gence profile at fixed partial dentures [8, 50, 51]. Therefore,
1. Intra-examiner
2. Inter-examiner

the alterations in oro-facial (horizontal) and apico-coronal


Calibration

(vertical) AR dimensions were selected as the primary out-


2. N/A
1. N/R

comes of the present review. Direct intra-surgical measure-


ments on the AR at re-entry are considered as the most
precise method to evaluate the bone volume changes fol-
4. Statistician

lowing ARP. It is desirable though to establish and validate a


3. Examiner
1. Therapist
2. Patient
Masking

surrogate measure that avoids the need for re-entry surgery,


1. N/R
2. N/R
3. N/R
4. N/R

while providing the clinician with a reliable measure. Two-


dimensional radiographs, such as periapical or panoramic
sequence generation

radiographs, are not ideal to estimate the 3D changes of the


4. Concealment
Quality Criteria

1. Randomised
Randomisation

AR [52]. Also, measurements of the alveolar mucosa level


3. Allocation
concealment
2. Adequate

adequate

or study casts incorporate not only the alveolar bone, but


N/A
Table 2 (continued)

also the overlaying soft tissue. For these reasons only


studies performing clinical or 3D radiographic evaluation
Year of publication

Reference number

of hard tissue were included in this review. Cone-beam


computerised tomography (CBCT) appears to offer a valid
First author

technique to assess alveolar ridge changes, with newer mod-


Serino
Study

2008
Type

CCT
#48

els greatly reducing radiation exposure [53]. However, a


352

Table 3
First author Trial Population Confounding Defect Test material Control Surgical Follow-up Alveolar ridge Alveolar ridge Implant
Year of characteristics characteristics factors characteristics (number of (number of management 1. Healing dimension dimension 1. Feasibility
publication 1. Country 1. Age range 1. Smoking 1. Socket sockets/ sockets/ 1. Type of flap period changes in changes in of implant
Type 2. Number of (mean) in 2. Periodontitis location subjects) subjects) 2. Soft tissue 2. Number horizontal width vertical height placement
Design centres years 2. Defect closure of drop-outs Mean/median mm Mean/median mm 2. Necessity of
Methodology 3. Setting 2. Number of morphology 3. Postoperative 3. Adverse 1. Whole ridge (reference point) simultaneous
Reference patients antimicrobials events 2. Buccal plate 1. Mid-buccal augmentation
number (sockets) 2. Mesial
3. Distal
4. Socket Fill

Aimetti 1. Italy 1. 36-68 1. No 1. Maxillary Calcium Empty 1. Flapless 1. 3 months 1. T: -2.0±1.1** 1. T: -0.5±1.1*, 1. Implants
2009 2. 1 (51.27 ±8.4) 2. N/R anterior sulphate (18/18) 2. No primary 2. N/R C: -3.2±1.8**, C: -1.2±0.6**, *** were
RCT 3. University 2. 40 (40) 2. 4-wall Hemihydrate closure 3. Uneventful *** 2. T: -0.2±0.6, inserted
Parallel configuration (22/22) 3. Amoxicillin healing 2. N/R C: -0.5±0.9 2. N/R
Clin+Histo 2g/day for 3. T: -0.4±0.9,
5 days, C: -0.5±1.1
#42 Chlorexidine 4. T: 11.3±2.8**,
0.12% for C: 10.0±2.3**
2 weeks (Acrylic stent)

Anitua 1999 1. Spain 1. T: 35-55 1. Yes 1. Any T1: PRGF Empty 1. Full-thickness 1. 2.5 – 4 N/A N/A 1. N/R
CCT 2. 1 (41) (5+3/5+3) (10+3/ months
Parallel+Split- 3. Private 2. Yes 2. Variable 2. Primary 2. N/R
C: 38-54 (42) T2: PRGF+ 10+3) closure 2. 0
mouth practice 2. 23 (26) Autologous 3. Amoxicillin 3. N/R
Histo
bone (5/5) 1.5g/day for
#43 5 days

Barone 1. Italy 1. 26-69 1. <10/day 1. Non-molars Corticocancellous Empty 1. Full-thickness 1. 7-9 months 1. T: -2.5±1.2*, 1. T: -0.7±1.4*, 1. ‘Implants were
2008 2. 1 2. 40 (40) 2. Yes 2. 4-wall porcine bone+ (20/20) 2. Primary closure 2. 0 C: -4.5±0.8*, *** C: -3.6±1.5*, *** inserted in
RCT 3. Hospital (treated) configuration collagen 3. Amoxicillin 3. Uneventful 2. N/R 2. T: -0.2±0.8, both groups’
Parallel membrane 2g/day for healing C: -0.4±1.2 2. Some GBR
Clin+Histo (20/20) 4 days+ (pain, swelling) 3. T: -0.4±0.8, were needed
#21 Chlorexidine C: -0.5±1.0 due to buccal
0.12% for dehiscence in
3 weeks 4. N/R
the control
(Acrylic stent) group

Camargo 1. USA, 1. 28-60 1. N/R 1. Maxillary Bioactive glass+ Empty 1. Full-thickness 1. 6 months 1. T: -3.48±2.68**, 1. T: -0.38±3.18, 1. Reentry only
2000 Yugoslavia (44±15.9) 2. N/R anterior, covered by (16/8) with 4 vertical 2. N/R C: -3.06±2.41** C: -1.00±2.25 2. N/A
CCT 3. University 2. 16 (32) premolars calcium releasing 3. Uneventful 2. N/R (titanium tack)
Split-mouth 2. N/R 2. N/R sulphate incisions healing 2. N/R
Clin layer (16/8) 2. No primary 3. N/R
#44 closure 4. T: 6.43±2.78**,
3. Penicillin C: 4.00±2.33**, ***
1.5g/day for (to buccal
7 days+ bone crest)
Chlorexidine
0.12% for
2 weeks
Clin Oral Invest (2013) 17:341–363
Table 3 (continued)
First author Trial Population Confounding Defect Test material Control Surgical Follow-up Alveolar ridge Alveolar ridge Implant
Year of characteristics characteristics factors characteristics (number of (number of management 1. Healing dimension dimension 1. Feasibility
publication 1. Country 1. Age range 1. Smoking 1. Socket sockets/ sockets/ 1. Type of flap period changes in changes in of implant
Type 2. Number of (mean) in 2. Periodontitis location subjects) subjects) 2. Soft tissue 2. Number horizontal width vertical height placement
Design centres years 2. Defect closure of drop-outs Mean/median mm Mean/median mm 2. Necessity of
Methodology 3. Setting 2. Number of morphology 3. Postoperative 3. Adverse 1. Whole ridge (reference point) simultaneous
Reference patients antimicrobials events 2. Buccal plate 1. Mid-buccal augmentation
number (sockets) 2. Mesial
3. Distal
4. Socket Fill

Fiorellini 1. USA 1. 47.4 1. N/R 1. Maxillary T1: 1.5mg/ml Empty 1. Full-thickness 1. 4 months 1. Coronal: 1. T1: -0.02±1.2, 1. N/R
Clin Oral Invest (2013) 17:341–363

2005 2. 8 centres 2. 80 (95) 2. N/R anterior, rhBMP-2 (?/20?) with vertical T1: +3.27±2.53*, T2: -0.62±1.39*,
2. No drop-outs 2. No need for
RCT 3. University premolars (?/21?) incisions reported. T2: +1.76±1.67*, T3: -1.00±1.40*, augmentation
Parallel 2. ≥50% T2: 0.75mg/ml 2. Primary (3 patients T3: +0.82±1.40, C: -1.17±1.23*,
C: +0.57±2.56, *** *** (T1 vs C) T1: 18/21 (86%)
Radiogr+ buccal bone rhBMP-2 closure incorrectly
Histo loss (?/22?) randomized, (T1 vs T2/T3/C) 2. N/R T2: 12/22 (55%)
3. Penicillin (?mg)
#20 T3: Collagen for 7-10 days+ 1 patient 2. N/R 3. N/R T3: 10/17 (59%)
sponge (?/17?) Chlorexidine received 4. N/R C: 9/20 (45%)
0.12% different
graft) (T1 vs T2/C)***
3. 250 (T>C)

Froum 1. USA 1. 35-77 1. No 1. Any T1: Bioactive Empty 1. Full-thickness 1. 6-8 months N/A N/A 1. ‘An implant
2002 2. Single (54.9±11.9) 2. N/R 2. 4-wall glass (10/8) (10/10) without vertical 2. 0 of appropriate
RCT centre 2. 19 (30) configuration, T2: DFDBA incisions 3. Uneventful size was placed
≤2mm buccal (10/8) 2. Primary healing in the healed
Split mouth 3. University
plate loss closure sockets.’
Histo 3. Doxycycline
100mg/day 2. N/R
#17
for 13 days+
Chlorexidine
0.12% for
30 days

Guarnieri 1. Italy 1. 35-58 1. N/R 1. Maxillary, Calcium Empty 1. Full-thickness 1. 3 months N/A N/A 1. ‘Bucco-lingual
2004 2. N/R 2. 10 (25) 2. Yes mandibular sulphate (5/5) without vertical 2. N/R dimensions of
CCT 3. N/R anteriors, Hemihydrate incisions 3. N/R the alveolar
Parallel+ premolars (10/10) 2. Primary closure ridge enabled
Split 2. socket with 3. Amoxicillin safe insertion of
mouth ridge (?mg) for titanium
Histo resorption 1 week+Chlorexidine implant.’
#45 ≥50% were 0.2% for 2 weeks 2. N/R
excluded

Iasella 2003 1. USA 1. 28-76 1. Yes 1. Maxillary Tetracycline Empty 1. Full-thickness 1. 4 or 6 months 1. T: -1.2±0.9*, 1. T: +1.3±2.0, 1. Implants
RCT 2. N/R (51.5±13.6) 2. N/R anteriors, hydrated (12/12) without vertical (combined) C: -2.6±2.3* C: -0.9±1.6*** successfully
Parallel 3. N/R 2. 24 (24) premolars FDBA + incisions 2. 0 2. N/R 2. T: -0.1±0.7, placed at all
Clin+Histo and collagen 2. No primary closure 3. N/R C:-1.0±0.8*** sites
#23 mandibular membrane 3. Doxycyclin 3. T: -0.1±0.7, 2. Some sites had
premolars (12/12) 200mg/day for C: -0.8±0.8*** slight dehiscence
2. N/R 1 week+ 4. N/R and required
Chlorexidine (Acrylic stent) further
0.12% for augmentation
2 weeks
353
Table 3 (continued)
354

First author Trial Population Confounding Defect Test material Control Surgical Follow-up Alveolar ridge Alveolar ridge Implant
Year of characteristics characteristics factors characteristics (number of (number of management 1. Healing dimension dimension 1. Feasibility
publication 1. Country 1. Age range 1. Smoking 1. Socket sockets/ sockets/ 1. Type of flap period changes in changes in of implant
Type 2. Number of (mean) in 2. Periodontitis location subjects) subjects) 2. Soft tissue 2. Number horizontal width vertical height placement
Design centres years 2. Defect closure of drop-outs Mean/median mm Mean/median mm 2. Necessity of
Methodology 3. Setting 2. Number of morphology 3. Postoperative 3. Adverse 1. Whole ridge (reference point) simultaneous
Reference patients antimicrobials events 2. Buccal plate 1. Mid-buccal augmentation
number (sockets) 2. Mesial
3. Distal
4. Socket Fill

Lekovic 1. Yugoslavia 1. (49.8) 1. N/R 1. Maxillary e-PTFE Empty 1. Full-thickness 1. 6 months 1. 10/10:, 1. 10/10: 1. Reentry only
1997 / USA 2. 10 (20) 2. N/R and membrane (10/10) with 4 vertical 2. 3/10 drop-outs T: -1.80±0.51, T: -0.5±0.22, 2. N/A
CCT 2. N/R mandibular (10/10) releasing due to premature C: -4.40±0.61**, C: -1.2±0.13**,
Split-mouth (presumably anteriors, incisions membrane *** ***
Clin single centre) premolars 2. Primary closure exposure 7/10: T: -1.71±0.75, 7/10:
#24 3. University 2. N/R 3. Penicillin 3. 3/10 exposed, C: -4.43±0.72**, T: -0.28±0.18,
1g/day for 7/10 no *** C: -1.0±0.0**,
7 days+ infection 3/10: T: -2.00±0.00, ***
Chlorexidine C: -4.33±0.88* 3/10: T: -1.0±0.58,
0.2% 2. N/R C: -1.66±0.33
(titanium tack)
2. N/R
3. N/R
4. 10/10:
T: 4.9±0.86*,
C: 3.0±0.63,
***
7/10: T: 5.43±1.1*,
C:2.92±1.61, ***
3/10: T: 3.66±1.20,
C: 4.33±1.45
(to buccal bone crest)

Lekovic 1. Yugoslavia 1. (52.6±11.8) 1. N/R 1. Maxillary PG/PL Empty 1. Full-thickness 1. 6 months 1. T: -1.31±0.24* 1. T: -0.38±0.22, 1. Reentry only
1998 2. 1 2. 16 (32) 2. Yes (treated) and membrane (16/16) with 4 vertical 2. 0 C:-4.56±0.33*, C: -1.50±0.26*, 2. N/A
RCT 3. University mandibular (16/16) releasing incisions 3. Uneventful *** *** (titanium tack)
Split-mouth anteriors, 2. Primary closure healing 2. N/R 2. N/R
Clin premolars 3. Penicillin 1g/day 3. N/R
#25 2. N/R for 7 days+
4. T: 5.81±0.29*,
Chlorexidine 0.12%
C: 3.94±0.35*, ***
for 2 weeks
(to buccal bone crest)

Nevins 2006 1. USA / Italy 1. N/R 1. N/R 1. Maxillary anterior DBBM (19/9) Empty (17/9) 1. Partial 1. 1 – 3 months N/A 1. T: -2.42±2.58, 1. Implants were
RCT 2. N/R 2. 9 (36) 2. Yes 2. Buccal plate was thickness (biopsies at 6M) C: -5.24±3.72*** placed, but
Split-mouth 3. N/R compromised 2. Primary 2. 0 2. N/R number
Radiogr+ closure 3. N/R 3. N/R unknown
Histo 3. N/R 4. N/R (At 6 mm 2. N/R
#46 ridge width)
Clin Oral Invest (2013) 17:341–363
Table 3 (continued)
First author Trial Population Confounding Defect Test material Control Surgical Follow-up Alveolar ridge Alveolar ridge Implant
Year of characteristics characteristics factors characteristics (number of (number of management 1. Healing dimension dimension 1. Feasibility
publication 1. Country 1. Age range 1. Smoking 1. Socket sockets/ sockets/ 1. Type of flap period changes in changes in of implant
Type 2. Number of (mean) in 2. Periodontitis location subjects) subjects) 2. Soft tissue 2. Number horizontal width vertical height placement
Design centres years 2. Defect closure of drop-outs Mean/median mm Mean/median mm 2. Necessity of
Methodology 3. Setting 2. Number of morphology 3. Postoperative 3. Adverse 1. Whole ridge (reference point) simultaneous
Reference patients antimicrobials events 2. Buccal plate 1. Mid-buccal augmentation
number (sockets) 2. Mesial
3. Distal
4. Socket Fill

Pelegrine 1. Brazil 1. 28-70 1. No 1. Maxillary Autologous Empty 1. Full-thickness 1. 6 months 1. T: -1.0*, 1. T: -0.5*, 1. All implants
Clin Oral Invest (2013) 17:341–363

2010 2. 1 (47.5±10.3) 2. N/R anteriors bone marrow (15/6) with 2 buccal 2. 0 C: -2.5*, *** C: -1.0*, *** osseointegrated
RCT 3. University 2. 13 (30) 2. Sockets with (15/7) vertical releasing 3. Uneventful 2. T: -0.75, (Titanium screw) 2. T: without
Parallel severe bone incisions healing C: -1.75, *** 2. N/R further
Clin+histo loss were 2. Primary closure 3. N/R augmentation,
#47 excluded 3. N/R 4. T: 10.33*, C: 10.32* C: At 5 sites
(to buccal bone crest) augmentation
or expansion
carried out

Serino 2003 1. Italy 1. 35-64 1. N/R 1. Any PG/PL sponge Empty 1. Full-thickness 1. 6 months N/A 1. T: +1.3±1.9*, 1. Placement of
CCT 2. 1 2. 45 (39) 2. Yes 2. Buccal plate (26/24) after (13/12) buccally and 2. 9 drop-outs C: -0.8±1.6 implants in all
Parallel+ 3. N/R before (treated) could be drop-out after drop-out lingually for reasons 2. T: -0.2±1.0, C and T sites
split-mouth drop-out partially or 2. No primary unrelated to C: -0.6±1.0 with good
Clin+Histo completely closure the therapy 3. T: -0.1±1.1, primary stability
#19 lost 3. No 3. Uneventful C: -0.8±1.5 2. N/R
antibiotics; healing 4. N/R
Chlorexidine (Acrylic stent)
0.2% for
2 weeks

Serino 2008 1. Italy 1. 32-64 1. N/R 1. Any PG/PL sponge Empty (9/9) 1. Full-thickness 1. 3 months N/A N/A 1. Placement of
CCT 2. 1 2. 20 (20) 2. Yes non-molars (7/7) after drop-out buccally and 2. 4 drop-outs implants in all
Parallel 3. N/R before (treated) 2. Alveolar after drop-out lingually for reasons C and T sites
Histo drop-out bone height 2. No primary unrelated to with good
#48 ≥8mm closure the therapy primary stability
3. No Antibiotics; 3. Uneventful 2. N/R
Chlorexidine healing
0.2% for 2 weeks

* p<0.05; statistically significant intra-group difference, baseline to final; ** p<0.001 statistically highly significant intra-group difference, baseline to final; *** p<0.05 statistically significant
inter-group difference, between test and control;
N/A not applicable; N/R not reported; T test; C control; M=month(s); Clin clinical analysis; Histo histological analysis; Radiogr radiographic analysis; RCT randomised controlled trial; CCT
controlled clinical trial; PRGF plasma rich in growth factors; DFDBA demineralised freeze-dried bone allograft; FDBA freeze-dried bone allograft; e-PTFE expanded-polytetrafluorethylen; PG/PL
polyglycolide/polylactide; DBBM demineralised bovine-bone mineral
355
356

Table 4

First author Number of Histomorphology Histomorphometry Statistical difference


biopsies between test and
Year of publication (test material) Test Control (mean or median %) control
Type
Healing period
Reference number
RCT
Aimetti 2009 T: N/R 22? No residual graft material. No inflammatory 100% living bone (mostly woven) Trabecular bone: Residual Woven bone: Lamellar T vs C*
3M (MGCSH) infiltrate. New bone formation in all in all biopsies. Lamellar bone T: 58.8±3.5 substitute Coronal: bone:
#42 C: N/R 18? specimens, 100% living trabecular bone remodeling was starting. C: 47.2±7.7 material: T: 83.6±6.6 Coronal:
with woven and lamellar structure. T: 0.0 C: 88.9±7.6 T: 16.4±6.6
C: N/A Middle: C: 11.1±7.6
T: 59.6±13.2 Middle:
C: 81.1±7.6 T: 40.4±13.2
Apical: C: 18.9±7.6
T: 56.4±10.9 Apical:
C: 77.8±8.1 T: 43.6±10.9
C: 22.2±8.1

Anitua T: N/R (PRGF± Compact mature bone with well-organized Connective tissue fills the main N/R
1999 autogen bone) trabeculae and morphology in 8/10 patients. part of the defect. No mature
CCT C: N/R Connective tissue with non-organized bone.
2.5 – 4 M trabeculae in 2/10 patients. Significant
#43 intra-group differences 10 vs. 16 weeks!

Barone 2008 T: 20 Residual graft material embedded in newly Typically trabecular bone pattern. Total bone Connective Residual graft Bone: T>C*
RCT (Corticocancellous formed bone in all specimens. Complete Large marrow spaces filled with volume: tissue: material: Connective tissue:
7–9M porcine bone+ bone fill. adipocytes. Lamellar bone was T: 35.5±10.4 T: 36.6±12.6 T: 29.2±10.1 T<C*
#21 collagen also present within the bone C: 25.7±9.5 C: 59.1±10.4 C: N/A
membrane) marrow.
C: 20

Fiorellini 2005 T1: 16 (rhBMP-2 No evidence of inflammation or residual graft. Trabecular bone formation in 2/3 N/R
RCT 1.5mg/ml) of the samples. Mineralized tissue formation presented with different level of
4M T2: 15 remodeling. Minor osteoclastic activity. No comparison reported between
#20 (0,75mg/ml) T and C!
T3: 11
(Collagen sponge)
C: 14

Froum 2002 T1: 10 T1: New bone formation. Osteoid surrounded N/R Vital bone: Connective Residual bone Connective tissue:
RCT (Bioactive glass) and penetrated the bioactive glass particles. T1: 59.5 tissue: substitute: T1<T2 or C*
6–8M T2: 10 (DFDBA) T2: Varying degrees of reossification T2: 34.7 T1: 35.3 T1: 5.5
#17 C: 10 around DFDBA. C: 32.4 T2: 51.6 T2: 13.5
C: 67.0 C: N/A
Clin Oral Invest (2013) 17:341–363
Table 4 (continued)
First author Number of Histomorphology Histomorphometry Statistical difference
biopsies between test and
Year of publication (test material) Test Control (mean or median %) control
Type
Healing period
Reference number

Guarnieri 2004 T: 10 (MGCSH) Almost complete absence of MGCSH. Less bone formation compared Trabecular bone No statistical significance
CCT C: 5 Absence of connective tissue and to test sites. area: could be drawn due
3M inflammatory cells. In all sections T: Coronal: 58.6±9.2 to small number of
#45 trabecular bone formation with no Middle: 58.1±6.2 control specimens.
Clin Oral Invest (2013) 17:341–363

differences between the apical, middle Apical: 58.3±7.8


and coronal levels. C: ≤ 46

Iasella 2003 T: 4M: 5, 6M:7 Residual graft particles surrounded by Similar amount of total bone and Vital bone: Non-vital bone: N/R
RCT (Tetracycline woven bone or by connective tissue. trabecular spaces as in test. 4M 4M
4–6M hydrated (No biopsy from 2 C sites due T: 31±9 T: 32±19
#23 FDBA+ to minimal bone fill) C: 58±11 C: N/A
Collagen 6M 6M
membrane) T: 25±17 T: 41±18
C: 4M: 5, 6M: 5 C: 50±14 C: N/A
Combined Combined
T: 28±14 T: 37±18
C: 54±12 C: N/A

Nevins 2005 T: 5 (DBBM) DBBM granules present. Apically integrated New bone formation No comparison made.
RCT C: 5 in cancellous bone but coronally in soft
6M tissue. No signs of inflammation or
#46 foreign body reaction.

Pelegrine 2010 T: 7 (Autologous Mineralized bone: No significant difference.


RCT bone marrow) T: 45.0
6M C: 6 C: 43.75
#47

Serino 2003 T: 10 No residual graft material. Presence of Presence of mineralized bone. Mineralized bone: Statistical comparison
CCT (PG/PL sponge) matured, mineralized bone. Lack of Wide marrow spaces. T: 66.7 cannot be made due
6M C: 3 coronal soft tissue ingrowth. C: 43.7 to the small number
#19 of control specimens.

Serino 2008 T: 7 No residual graft material. Scarce presence of Coronal: trabecular bone with wide Mineralized bone: No significant
CCT (PG/PL sponge) inflammatory tissue. Coronal: newly formed marrow spaces with connective T: 59.9±22.4 difference.
3M C: 9 trabecular bone with large marrow spaces. tissue. Apical: more mature and C: 48.8±14.4
#48 Apical: more mature and compact bone. compact bone.

*p<0.05; statistically significant difference between test and control


T test; C control; M month(s); N/R not reported; N/A not applicable; vs. versus; TBV total bone volume; MGCSH medical grade calcium sulphate hemihydrate; DFDBA demineralised freeze-dried
357

bone allograft; FDBA mineralised freeze-dried bone allograft; DBBM demineralised bovine-bone mineral; PG/PL polyglycolide/polylactide
358 Clin Oral Invest (2013) 17:341–363

prerequisite of this technique would be some type of stand- Based on the histological evaluation of these studies, the
ardisation, so that the captured image is being always taken above AR dimensional changes were not necessarily accom-
from exactly identical positions [54]. None of the two included panied by higher amount of new bone formation in the
radiographic studies reported on such standardisation [20, 46]. socket, since the quality of newly formed tissue in the
For the interpretation of the results we attempted to ARP sites was comparable to that in the control sites.
cluster the studies in respect to the type of intervention. Furthermore, the sockets were occupied by a mixture of
new bone and connective tissue which in many occasions
Unassisted sockets In the present review, the mean reduc- was surrounding the graft particles [17, 21, 46] (Table 4).
tion of the AR width of the untreated sites varied between
2.6±2.3 mm and 4.6±0.3 mm and the mean reduction of the GBR (membrane alone or in combination with ‘graft’) The
AR height was between 0.8±1.6 mm and 3.6±1.5 mm after conception of guided bone and tissue regeneration [62] was
1 to 9 months of healing. This corroborates the result of a translated to ARP procedures in order to exclude epithelial
previous clinical study which indicated that 95 % of AR cells from the extraction socket by the use of barrier mem-
reduction should be expected after three months of extrac- brane in four studies of the present review [21, 23–25].
tion [1]. Furthermore, it is in agreement with a recent sys-
(a) GBR with membrane alone
tematic review, which reported that the average reduction of
ARP with GBR resulted in statistically significantly
the AR width seemed to be higher (3.87 mm), than the
less resorption in ridge width and height compared to
reduction in AR height (1.67 mm) [55].
unassisted socket healing, regardless of the type of
Even though both AR width and height present resorp-
membrane [24, 25]. It should be noted that in one study
tion, histologically, new bone formation up to a variable
[24], in three out of 10 cases, the exposed non-
extent was also observed in some studies as result of unas-
resorbable e-PTFE barrier had to be removed prema-
sisted socket healing [19–21, 23, 42, 45, 46, 48]. In addi-
turely, highlighting the importance of sufficient soft
tion, a large area was occupied by bone marrow [19, 21, 48],
tissue closure and timing of removal of the barrier.
as reported in preclinical studies [11, 13, 56]. Only a single
The outcomes in these three cases were similar to the
study reported on connective tissue fill and lack of mature
control sites. Where healing was uncompromised, a
bone [43].
statistically significant difference was found after
6 months in width and height changes in favour of
Bone grafts and substitutes Effective grafting procedures for
the ARP group.
bone augmentation have been associated with the osteocon-
(b) GBR with membrane and ‘graft’
ductive, osteoinductive or osteogenetic properties of the graft
ARP resulted in statistically significantly less re-
[56–59]. This led to the assumption that the placement of these
sorption in width [21, 23] and height [23] in compar-
materials in the extraction socket may accelerate new bone
ison to unassisted socket healing. The histological
formation by the above biological properties and may also
evaluation of the GBR procedures in the included
reduce AR resorption by stabilising the blood clot, providing a
studies demonstrated new bone formation [21, 23],
scaffold and external source of minerals and/or collagen [11,
but the presence of graft particles was also evident in
12, 60, 61]. The placement of DBBM with collagen in fresh
both studies, embedded either in newly formed bone
extraction sockets resulted in limited reduction of the AR
[21] or in connective tissue [23]. This is in agreement
dimensions, although delayed initial socket healing in terms
with a recent trial, where a collagen membrane in
of new bone formation was also observed [11, 12]. Human
combination with DBBM or a biphasic bone substitute
studies reported similar unfavourable histological observa-
was used for ARP [9, 10].
tions when DFDBA was employed for ARP [15, 16].
In the present review of human experiments, two out of
three studies reported that socket grafting with autologous Biological active materials The potential benefit of biologi-
bone marrow [47] or alloplastic material [42] have signifi- cal active molecules was investigated in periodontal and bone
cantly limited the reduction of the AR width compared to regeneration through fostering the proliferation and differen-
the unassisted socket healing. Three out of five studies tiation of different mesenchymal cells in various preclinical
reported that reduction of the resorption in AR height was models [63, 64]. The safety and feasibility of rhBMP-2 on
significant [42, 46, 47], while the ridge height was even human ARP or ridge augmentation was evaluated and shown
increased in one study, where sockets were grafted with to be safe in a two-centre clinical study [35]. Dimensional
polymer sponge [19]. We should emphasise though that changes of the alveolar ridge were measured on CT scans in an
since the graft material (DBBM) in a CT study possessed RCT [20]. Treatment with recombinant BMP-2 resulted in an
radiopaque characteristic, the alteration of the AR contour increase in ridge width which was statistically significantly
on the CT image should be interpreted with caution [46]. greater than controls. However, this observation needs to be
Clin Oral Invest (2013) 17:341–363 359

interpreted in light of the surprise finding of an increase in Flap management All studies reporting statistically signifi-
ridge width of the untreated controls. This was a unique cant inter-group differences in both horizontal and vertical
finding amongst the studies that we reviewed. Histologically, clinical measurements achieved either primary flap closure
no comparison between ARP and controls sites was reported. [21, 24, 25, 47], or did not detach the periosteum in a
The human histological results of the included papers of flapless procedure [42]. Furthermore, none of the studies
the present review were generally found to be comparable to without primary closure demonstrated statistically signifi-
preclinical studies [11–13, 60, 65]. There are a number of cant differences between test and control in terms of both
aspects to consider in the interpretation of the results. First- horizontal and vertical clinical measurements [19, 23, 44].
ly, it has to be kept in mind that whilst the biopsies of the Therefore, both achieving and maintaining the epithelial
animal model incorporate the cross section of the whole AR, seal above the socket may be crucial to improving ARP.
the biopsy retrieval at human studies is limited to a trephine Further corroboration of this concept was suggested where
core sample of part of the former socket. This location may e-PTFE barriers were prematurely exposed. The healing of
not necessarily coincide with the exact position of the pre- these three exposed cases demonstrated no statistically sig-
vious extraction, thus making interpretation of the results nificant differences compared to the control sites [24].
challenging. Furthermore, the differentiation between api-
cal, mid and coronal, as well as the central and lateral
aspects of the biopsies was not always apparent. Other factors affecting interpretation of the findings
Another important parameter when considering a histo-
logical overview of the studies was the variation in healing Healing time
time. Due to the nature of post-extraction healing, the direct
comparison of the new tissue formation in studies between 1 The optimal timing of re-entry following ARP is determined
and 9 months of healing could be misleading. This was by the implant insertion. Since the volume of the AR is
highlighted in three studies which did not make a distinction gradually decreasing, while the quality of the newly formed
between the variable healing times within the groups, rang- tissue is gradually increasing during the post-extraction
ing from 2.5 months to 9 months [17, 21, 43]. It has to be remodelling [1, 6] the implant placement could be consid-
kept in mind also that the only study, which completed and ered as early as possible, but as late as necessary, in order to
reported appropriate statistical methodology [47], did not maintain AR volume, as well as to achieve complete epi-
observe statistically significant difference between the test thelial seal with some extent of osseous fill. The healing
and control biopsies. periods of the trials in the present review varied consider-
Furthermore, small sample sizes in the majority of the ably (one to nine months). Therefore, interpretation of the
studies may also limit the generalisability of the histological results was complicated by the heterogeneity present in the
findings. included studies.
Two studies found statistically significant histological
differences in new bone formation favouring the test group Antimicrobials
[21, 42]. Drawing conclusions across the studies is difficult
since the test groups differed in many respects compared Improvement of clinical parameters was demonstrated as a
with each other, including different technique (bone sub- result of regular rinsing with chlorhexidine following tooth
stitute only [42]/GBR + graft [21]), different material extraction [66]. Subjects of the included trials in the present
(MGCSH [42]/porcine bone with collagen membrane review were prescribed various types of antibiotics and
[21]), different flap management (flapless, no primary clo- instructed to rinse with chlorhexidine for 2 to 3 weeks.
sure [42]/mucoperiosteal flap, primary closure [21]), dif- Therefore, no conclusion could be drawn on the necessity
ferent healing time (3 months [42]/7–9 months [21]). One or benefit of employment of antibiotics/antimicrobials fol-
common feature was that both groups limited their inter- lowing ARP.
vention to sockets with four intact walls. It is noteworthy
that all three studies that included intact socket walls only, Smoking
reported statistically significant differences both on AR
width and height in favour of ARP [21, 42, 47], while only Smoking is associated with delayed socket healing and
one [20] out of two studies [19, 20] with initial buccal bone increased reduction in post-extraction alveolar width [67].
loss reported similar significant difference between test Three trials in this review included smokers [21, 23, 43] and
and control. Therefore, socket morphology could be an the half of the studies did not report on smoking as an
important predicator of improved ARP. The need for exclusion factor, thus any conclusions about the impact of
ARP in such sockets, in terms of future clinical success/ this well-recognised risk factor for impaired healing are
implant placement needs further investigation. difficult to draw [68].
360 Clin Oral Invest (2013) 17:341–363

Periodontal treatment/health Conclusions

Four studies included patients whose periodontal treatment Within the limits of the above findings the following con-
was carried out prior to the ARP [19, 21, 25, 48]. ARP clusions can be drawn:
resulted in statistically significant difference between tests
and controls in clinical [21, 25] and in histological param- 1. The results of the control groups confirm that tooth
eters [21]. In addition, in the studies where periodontitis was extraction results in a statistically significant horizontal
present, but periodontal treatment was not reported, no and vertical resorption of the AR, as part of the natural
statistically significant histological differences were demon- remodelling.
strated [43, 44, 46]. This suggests that treated periodontitis 2. The magnitude of the horizontal shrinkage is more
may not hinder the success of ARP. pronounced than the vertical.
3. The resorption of the AR cannot be totally prevented
Hard and soft tissue morphology by ARP.
4. Dimensional changes of the AR may be limited by
No data were reported on factors, such as gingival biotype, some of the ARP techniques.
width of the keratinised gingiva, thickness of buccal plate or 5. No evidence was identified to inform on the possible
total volume of AR that may modify the outcome of ARP. impact of the following factors on ARP outcomes: (a)
Therefore, the possible impact of these factors on ARP site location, (b) buccal plate thickness, (c) healing
cannot be determined. time, (d) antibiotic regime, (e) light smoking, (f) his-
tory of treated periodontitis.
Clinical relevance 6. The presence of intact socket walls and primary flap
closure are often associated with favourable results.
The clinical rationale for ARP is to minimise the necessity 7. Conflicting evidence exists on the benefit of ARP
for one or two stage alveolar ridge reconstruction to allow at the histological level. ARP does not appear to
successful implant placement. If the ARP procedure fails promote de novo hard tissue formation routinely.
to meet this requirement, it may be considered as an un- In addition, some graft materials may interfere with
necessary or even unsuccessful procedure. Therefore, a healing.
statistical significance favouring ARP does not necessarily 8. Due to the broad variety of employed materials, tech-
lead to a clinical benefit, unless the whole treatment is niques, defect morphologies, healing periods, as well
simplified or made more successful [9]. In the present as the relatively small sample sizes, meta-analysis or
systematic review, seven out of ten studies did not report comparative assessment of ARP cannot be made. Con-
differences in feasibility of implant insertion at re-entry sequently no material or method can be claimed to
[17, 19, 23, 42, 45, 46, 48]. Only two studies reported that serve superior to another. However, in certain cases
there was no need for further reconstruction in the ARP GBR appeared to be most effective.
group, whilst GBR or ridge expansion were carried out in 9. Only limited evidence supports the clinical benefit of
some of the control sites alongside implant insertion [21, ARP, namely the reduction of necessity of further
47]. One study reported that statistically significantly less augmentation in conjunction with implant placement.
augmentation had to be performed in the ARP group, 10. No evidence exists on comparison of the survival or
compared to the control [20]. In relation to illuminating success rate of implants, placed in the former ARP or
the understanding of possible long term benefits of ARP, control sites.
the success rate of the inserted dental implants in the 11. No evidence exists on cost-effectiveness, patient’s
former test, versus control sites should be examined. No preference or quality of life following ARP.
studies have yet reported this. 12. The case selection criteria for performing ARP remain
still undetermined.
Patient-reported outcome and health economics 13. The strength of evidence ranges from weak to moder-
ate and therefore, the conclusions of this review should
It would be helpful to understand patient experiences such be interpreted with caution.
as concomitant discomfort at/following ARP in order to
avoid a further, extensive reconstructive surgery. On the Recommendations for further research
other hand, the additional costs of ARP at the time of
extraction may not be desirable if the outcome and benefit & Randomised controlled trials on adequately powered
of such extra treatment were not predictable. There are no sample sizes are needed where unassisted socket healing
data yet to inform on these questions. serves as the negative control.
Clin Oral Invest (2013) 17:341–363 361

& Appropriate follow-up periods are required. Ideally, this 9. Mardas N, Chadha V, Donos N (2010) Alveolar ridge preservation
with guided bone regeneration and a synthetic bone substitute or a
should reflect implant insertion protocols, such as six
bovine-derived xenograft: a randomized, controlled clinical trial.
weeks (Type 2), three to four months (Type 3) or Clin Oral Implants Res 21:688–698
>6 months (Type 4) placement following extraction. 10. Mardas N, D’Aiuto F, Mezzomo L, Arzoumanidi M, Donos N
& Clinical studies should be designed to perform not only (2011) Radiographic alveolar bone changes following ridge pres-
ervation with two different biomaterials. Clin Oral Implants Res
clinical (quantitative), but also histological (qualitative)
22:416–423
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& The role of additional factors like smoking, reason for bone formation in extraction sockets: an experimental study in dog.
extraction, tooth location, initial buccal plate thickness, Clin Oral Implants Res 20:1–6
flap reflection and closure, antimicrobial regime should 12. Araújo MG, Lindhe J (2009) Ridge preservation with the use of
Bio-Oss® collagen: a 6-month study in the dog. Clin Oral Implants
also be investigated. Res 20:433–440
& Comparative studies should also be designed in order to 13. Fickl S, Zuhr O, Wachtel H, Bolz W, Huerzeler MB (2008) Hard
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& It may be beneficial to seek for a cell occlusive barrier in the beagle dog. Clin Oral Implants Res 19:1111–1118
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Acknowledgments The authors wish to express their gratitude to 17. Froum S, Cho SC, Rosenberg E, Rohrer M, Tarnow D (2002)
Aviva Petrie for her invaluable contribution to the statistical assessment. Histological comparison of healing extraction sockets implanted
with bioactive glass or demineralized freeze-dried bone allograft: a
Conflict of interest and source of funding There was no known conflict pilot study. J Periodontol 73:94–102
of interest among the review team. The trial was self funded and supported 18. Artzi Z, Tal H, Dayan D (2000) Porous bovine bone mineral in
by the Research Discretionary Account of the Unit of Periodontology, UCL healing of human extraction sockets. Part 1: histomorphometric
Eastman Dental Institute. This work was undertaken at UCLH/UCL who evaluations at 9 months. J Periodontol 71:1015–1023
received a proportion of funding from the Department of Health’s NIHR 19. Serino G, Biancu S, Iezzi G, Piattelli A (2003) Ridge preservation
Biomedical Research Centres funding scheme. following tooth extraction using a polylactide and polyglycolide
sponge as space filler: a clinical and histological study in humans.
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Ren E. Wang Ridge preservation after tooth extrac-
Niklaus P. Lang
tion

Authors’ affiliations: Key words: bone substitutes, GBR, implant dentistry, membrane, ridge preservation, tooth
Ren E. Wang, Niklaus P. Lang, The University of extraction
Hong Kong, Prince Philip Dental Hospital,

Corresponding author: Abstract


Prof. Niklaus P. Lang, DDS, MS, PhD, Dr, odont.
hc.mult.
Background: Following tooth extraction, the alveolar ridge will undergo dimensional changes.
The University of Hong Kong Faculty of Dentistry This change may complicate the subsequent restorative procedure when oral implants are chosen.
Prince Philip Dental Hospital, “Alveolar ridge preservation” has been assessed in various studies.
34 Hospital Road, Sai Ying Pun, Hong Kong SAR
PR China Aim: To evaluate the more recent studies on this topic and to explore new insights under this
Tel.: +852 2859 0526 topic.
Fax: +852 2559 9013 Material and methods: Animal studies and clinical studies have addressed different techniques.
Mobile: + 41 79 301 5505
e-mail: nplang@dial.eunet.ch Results and conclusions: Implants placed into the fresh extraction sockets do not prevent the
resorption of the alveolar bone. Simultaneous guided bone regeneration could partially resolve
Conflicts of interest: alveolar bone resorption. The use of root-formed implants does not preserve alveolar ridges.
The authors declare no potential conflicts.
Moreover, various bone substitutes have been tested: magnesium-enriched hydroxyapatite, human
demineralized bone matrix, and deproteinized bovine bone mineral have been shown to be
effective in ridge preservation. Applying the guided bone regeneration principle using bone
substitutes together with a collagen membrane has shown clear effects on preserving alveolar
ridge height as well as ridge width. Soft tissue grafts or primary closure did not show beneficial
effect on preserving the alveolar bone.

Following tooth extraction, the alveolar ridge bridges separated the marginal mucosa from
will undergo structural changes. These the socket, and bone marrow replaced woven
changes in extraction sockets were amply bone at the center of the previous socket. At
demonstrated with histological observations day 90, woven bone was replaced by lamellar
in dog studies (Cardaropoli et al. 2003). At bone. At days 120 and 180, most of the woven
day 1 after extraction, the socket was occupied bone had been replaced by lamellar bone.
by a coagulum; this coagulum was comprised The role of bundle bone in the dimensional
mainly of erythrocytes and platelets that were change in the alveolar ridge was investigated in
trapped in a fibrous matrix. Immediately adja- several dog studies (Araùjo & Lindhe 2005;
cent to the hard tissue wall was the “bundle Araùjo et al. 2005) At 1 week after extraction
bone”, and principal fibers from periodontal (Araùjo & Lindhe 2005), the buccal bony crest
ligament (Sharpey’s fibers) could be found was 0.3 mm coronal to the lingual bony crest,
invested in the bundle bone. These were also but at 2 weeks after extraction, the buccal crest
in direct contact with the coagulum. At day became 0.3 mm apical to the lingual crest.
3, the coagulum had been replaced by a richly This relative distance was increased to 0.9 and
vascularized granulation tissue. At day 7, 1.9 mm at 4 and 8 weeks after extraction,
newly formed blood vessels were evident in respectively. It was also observed that the cres-
the primary matrix. Various types of leuko- tal region of the buccal bone wall was made up
cytes and collagen fibers had taken the place exclusively of bundle bone, whereas the corre-
of the residual periodontal ligament as well as sponding region of the lingual bone was made
the granulation tissue. At day 14, most of the of a combination of bundle bone and lamellar
bundle bone had disappeared, and instead, bone. Obviously, the function of bundle bone
adjacent to the newly formed blood vessels, is to anchor the tooth in the alveolar bone
Date:
Accepted 03 July 2012 “woven bone” started extending from the old through the invested periodontal ligament. As
bone of the socket walls toward the center of the tooth is extracted, the bundle bone will lose
To cite this article:
Wang RE, Lang NP. New insights into ridge preservation after the socket. At day 30, woven bone underwent its function, and subsequently, will resorb.
tooth extraction
resorption, suggesting that the remodeling This may explain the more pronounced resorp-
Clin. Oral Implants Res. 23(Suppl. 6), 2012, 147–156
doi: 10.1111/j.1600-0501.2012.02560.x process had begun. At day 60, hard tissue tion of the buccal than the lingual bony crest.

© 2012 John Wiley & Sons A/S 147


Wang & Lang  Ridge preservation revisited

A recent systematic review evaluated the omy and that the placement of a fixture in a would help to preserve the buccal bone
dimensional changes in the hard and soft tis- fresh extraction socket may help to maintain (Blanco et al. 2011). In a dog model, two
sues of the alveolar process up to 12 months the bony crest structure” (Paolantonio et al. implants were placed into the fresh extrac-
following tooth extraction (Tan et al. 2012). 2001). However, this statement has been tion sockets at the premolar sites on each
It was concluded that after 3 months of scrutinized later in a dog study (Araùjo et al. side of the mandible. At the time of the
healing, the horizontal resorption of the 2005). In the right jaw of five dogs, implants implantation, the implants on one side of the
alveolar bone was 2.2 mm at the crest, and were placed into the fresh extraction sockets, jaw received a prosthesis with occlusal con-
1.3, 0.59, and 0.3 mm at 3, 6, and 9 mm api- while in the left jaw, fresh sockets were left tacts, while the implants on the other side
cal to the crest, respectively; after 6 months for spontaneous healing. After 3 months of remained unloaded during the whole experi-
of healing, the vertical resorption of the healing, histological sections were obtained mental period. Three months later, the dogs
alveolar bone was 11–22%, whereas the hori- to assess the distance from the SLA level to were sacrificed. The histomorphometric
zontal resorption of the alveolar bone was 29 the first bone-to-implant contact under results showed that the vertical distance
–63%. When soft tissue was included microscope. On the buccal aspect, this dis- from the implant shoulder to the first bone-
together with the hard tissue in the dimen- tance was 2.6 mm at implant sites and to-implant contact was on average 3.66 mm
sional assessments at 3 months of healing, 2.2 mm at the corresponding extraction in the simultaneously loaded group and
there was even an increase of 0.4 mm in the socket sites. Hence, the immediate place- 4.11 mm in the unloaded group. This
vertical dimension. At 12 months of healing, ment of dental implants clearly failed to pre- difference was not statistically significant,
the vertical resorption of the alveolar ridge vent the resorption of the buccal bone walls. and hence it was concluded that “immediate
was 0.8 mm. Horizontally, the resorption of To further study the modeling of the buc- implant placement with or without loading
the soft and hard tissue together was 1.3mm cal bony plate, the same group of researchers does not prevent bone resorption that occurs
and 5.1mm after 3 and 12 months of heal- designed another dog study (Araùjo et al. following tooth extraction.”
ing, respectively. 2006). In that study, the implants were
This vertical as well as horizontal dimen- placed into the fresh extraction sockets in Immediate implant with bone grafts
sional changes of the alveolar ridge may com- the right jaw and 2 months later, the same The effect of bone fillers (magnesium-
plicate the subsequent restorative procedures procedure was performed again in the left enriched hydroxyapatite) on preservation of
when dental implants are chosen. Over the jaw. Following another 1 month, the dogs the alveolar bone around immediate implants
past 20 years, increasing interest has arisen were sacrificed, and it was observed that after was evaluated in a dog study (Caneva et al.
regarding a concept called “alveolar ridge 1 month of healing, at the buccal aspect, 2011). Implants with a sandblasted acid
preservation”, which was defined as “any good osseointegration had been achieved etched surface (Zirti®, Sweden & Martina,
procedure undertaken at the time of or fol- above the first thread of the implant. How- Due Carrare, PD, Italy) were placed into the
lowing an extraction that is designed to mini- ever, after 3 months of healing, the level of fresh extraction sockets bilaterally in the
mize external resorption of the ridge and this osseointegration had receded to below dogs’ jaws. The margin of the rough surface
maximize bone formation within the socket” the first thread as a result of the modeling of was placed at the level of the buccal bony
(Darby et al. 2008). As suggested by that the buccal bone. In the molar regions, the crest. On one side of the jaw, the bone filler
review, studies promoting various techniques degree of this modeling was much less was applied into the gaps around the
have been performed. Most of the studies compared with the premolar regions, most implants. The contralateral sites were left
included the measurements of dimensional likely because of the wider original combined unfilled as controls. After 4 months of sub-
changes of the alveolar ridge after a ridge defect and bone wall dimensions in the molar merged healing, the dogs were sacrificed. His-
preservation procedure. regions. This study provided strong evidence tomorphometric evaluations showed that the
The purpose of this review was to evaluate for the continued modeling process of the vertical distance from the junction between
these more recent studies and to explore new buccal bony wall leading to buccal bone loss rough and smooth surface to the buccal bony
insights under this topic. Within the context despite the good osseointegration that had crest was on average 0.7 mm in the group
of exploring new insights for ridge preserva- already been achieved in early healing with the bone filler and 1.2 mm in the
tion, also studies of lower levels in the phases. Obviously, this phenomenon was less control group with no statistically significant
evidence hierarchy may be of interest to shed pronounced in sites with thicker buccal bony differences between the groups. Obviously,
some light on the techniques designed to pre- walls. Again, immediate implant installation the use of bone fillers around implants
serve the alveolar ridge after tooth extraction. failed to preserve the alveolar bone. immediately placed into extraction sockets
These low evidence papers are generally case In a study aimed at observing bone- did not contribute significantly to the preser-
series that combine various protocols. How- to-implant contact of orthodontic implants vation of the buccal bone. In a recent experi-
ever, this approach, should lead to clinical subjected to horizontal loading (Wehrbein ment (Araújo et al. 2011), it has been
validation before recommendable for routine et al. 1998), immediately placed implants demonstrated that the use of Bio-OssÒ col-
clinical application. with simultaneous horizontal loading lagen as a bone substitute filler in the space
achieved better osseointegration than those between the implant and the buccal bony
Animal studies with delayed loading. Moreover, it was sug- wall resulted in the prevention of buccal soft
gested in another dog study that “a static tissue recession and a reduction in peri-
Implants for ridge preservation load may stimulate bone mineralization adja- implant bone loss and allowed the buccal
cent to titanium implants” (Gotfredsen et al. bone to be thicker at the marginal level.
Immediate implants alone 2001). Finally, the hypothesis was tested However, another similar animal study
A decade ago, it was proposed that “early whether or not immediate implant place- (Favero et al. 2012) was not able to confirm
implantation may preserve the alveolar anat- ment together with simultaneous loading these differences in outcomes.

148 | Clin. Oral Implants Res. 23, 2012 / 147–156 © 2012 John Wiley & Sons A/S
Wang & Lang  Ridge preservation revisited

Immediate implant with GBR limited contribution of DBBM particles was branes were placed below the buccal bony
In an AAP-commissioned review on bone obtained (Caneva et al. 2011). crests, and no primary closure was intended,
augmentation techniques, it was recom- In the second study on the same material which meant that the flaps healed without
mended that immediate implant placement the dimensional changes of the alveolar bony tension. Consequently, membrane exposure
together with GBR techniques may yield out- crest following the placement of DBBM parti- was absent during healing.
comes comparable to delayed placed implants cles into sockets immediately after tooth
(McAllister & Haghighat 2007). Recently, extraction, in conjunction of the placement Shape of implants and implant positioning
a dog study was conducted to evaluate the of a collagen membrane, were addressed Tapered or root-formed implants were
influence of absorbable membranes on hard (Caneva et al. 2012). After 4 months of heal- designed to reduce the gaps around implants
tissue alterations around the immediately ing, no differences in soft tissue dimensions that were placed immediately into the fresh
placed implants (Caneva et al. 2010a,b,c). were found based on histological evaluations. extraction sockets, thus filling the defect par-
Implants with a rough surface (zirconium Yet, the location of the soft tissue at the buc- tially with titanium. The question arises if
sandblasted acid etched) were placed immedi- cal aspect was more coronally at the test this type of implant design will help in pre-
ately following extraction on both sides of compared to the control sites. Hence, it was venting alveolar bone resorption around such
the mandibles, on the test side of the jaw, concluded that the application of DBBM con- implants. In a split-mouth design, mandibles
collagen resorbable membranes were placed comitantly with the placement of a collagen of dogs received cylindrical implants 3.3 mm
to cover the implants. On the control side of membrane at implant sites placed in the in diameter (Premium®, Sweden & Martina,
the jaw, the implants were left without socket immediately after tooth extraction Due Carrare, PD, Italy) immediately after
membranes. contributed positively to the preservation of tooth extraction (control) (Caneva et al.
After 4 months of intended submerged the alveolar process. 2010c). A similar procedure was carried out
healing, all implants were found exposed to In a similar study recently published (Park with root-formed implants 5 mm in diameter
the oral cavity because of soft tissue dehi- et al. 2011), immediate implants (Institute (Kohno®, Sweden & Martina, Due Carrare,
scences. The dogs were sacrificed and biop- Straumann AG, Basel, Switzerland) were PD, Italy) on the test sites. After 4 months of
sies were obtained. The distance between the placed bilaterally in the dogs’ jaws in the pre- non-submerged healing, the dogs were sacri-
most coronal margin of the implant and the molar region. On the experimental side, a ficed and histomorphometric evaluations
bone crest were measured. At the buccal non-resorbable ePTFE membrane (Tefgen®, were performed. The mean vertical buccal
aspect, this distance was 1.7 mm on the Lifecore Biomedical, Chaska, MN, USA) was bone resorption was significantly greater in
implants placed with GBR procedures, and placed on the buccal plate of the implant the test group (2.7 mm) than in the control
2.2 mm on the implants placed without sites without coverage of the bone crest and group (1.5 mm). In essence, the filling of gaps
GBR, and this difference was statistically sig- was fixed with mini screws. In the control with root-formed implants failed to preserve
nificant. At the lingual aspect, this distance site, no membrane was placed. After the buccal bone. On the contrary, the bone
was 0.6 and 0.4 mm on the test sites and 3 months of non-submerged healing, no resorption was more pronounced around the
control sites, the difference not reaching sta- membrane exposure occurred. The dogs were root-formed immediate implants that filled
tistical significance. There was no difference sacrificed and after histometric observation, the extraction socket to a greater extent than
between the groups regarding the level of the vertical distance from the rough and did the cylindrical implants. The root-formed
first bone-to-implant contact and the percent- smooth surface interface to the buccal bone implants with a wider diameter occupied the
age of bone-to-implant contact. This study crest was on average 1.72 mm in the control entire socket, leaving no space between the
provided evidence that the use of collagen group and 0.92 mm in the experimental implant and the buccal bony wall. In other
resorbable membranes at immediate implant group. This difference was statistically signif- words, the implant body was located closer
sites contributed partially (23%) to the pres- icant. Moreover, at the level 2 mm below the to the outer surface of the buccal bony wall.
ervation of the buccal bony wall. buccal bony crest, the mean thickness of the Consequently, a greater portion of the
Further studies of the same group of buccal bone walls was 0.4 mm in the control implant was exposed in the supracrestal
researchers (Caneva et al. 2011, 2012) group and 1.49 mm in the test group. Again, region after modeling and remodeling pro-
explored the effect of GBR based on deprotei- this difference was statistically significant. cess, as the distance between the implant
nized bovine bone mineral on alveolar ridge From the above two animal studies, it outline and the outer surface of the buccal
preservation and the reparation of defects appeared that the outcomes of using non- bone appears to be a crucial factor for the
around osseointegrated implants. After resorbable ePTFE membranes is superior to preservation of the buccal bone.
hemi-sectioning the third mandibular premo- that achieved by resorbable collagen mem- To evaluate the influence of implant posi-
lars and extracting the distal roots, a recipi- branes. It should be realized that the tech- tioning into extraction sockets on the main-
ent site was prepared for an implant. This niques applied in the two studies were tenance of the buccal bone level (Caneva
was placed lingually, leaving a defect of different. In the first study, the resorbable et al. 2010a), implants (Premium®, Sweden &
about 0.6mm in width and 3mm in depth at collagen membranes were placed on top of Martina, Due Carrare, PD, Italy) were placed
the buccal aspect. While the other side of the implants without fixation, and primary in the center of the sockets in control sites
the jaw was used as control without GBR, closure was achieved at the completion of of mandibles, whereas in the test sites, the
deproteinized bovine bone mineral (DBBM) the surgery. However, during the healing per- same implants were placed 0.8 mm deeper
was place into the defects of the test site and iod, all implants were exposed because of soft and more lingually. After 4 months of non-
covered with a collagen membrane. This tissue dehiscences. In the later study, the submerged healing, the histometric evalua-
treatment contributed to improved bone non-resorbable membrane was placed on the tions showed that the mean vertical distance
regeneration in the defects. However, regard- buccal bone wall and fixed with mini screws from the rough and smooth surface interface
ing the buccal bony crest preservation only a to avoid membrane exposure. The mem- to the buccal bone crest was significantly less

© 2012 John Wiley & Sons A/S 149 | Clin. Oral Implants Res. 23, 2012 / 147–156
Wang & Lang  Ridge preservation revisited

in the test group (0.6 mm) compared with untreated group had a significantly narrower coronal portions, the ridge underwent resorp-
the control group (2 mm). Hence, the posi- ridge width than the test group (3.7 mm vs. tion ( 25%) in the autogenous bone graft
tion of the implant had a greater impact on 4.4 mm). However, at 3 mm/5 mm below group. In the xenograft group, there was a posi-
the preservation of the buccal bone resorp- the crest, the ridge width was similar tive change (3.6%). The residual grafting mate-
tion than the shape of the implant. between the groups. Using digital image anal- rial was found to be 24.4%. Non-vital
ysis on study casts for the same material autogenous bone chips were found to be 1.9%.
Bone substitutes (Fickl et al. 2008a,b) at the buccal aspect, the It seemed that autologous bone did not pre-
volumetric differences from baseline to after serve the alveolar ridge.
Bone substitutes alone 4 months of healing was significantly greater
The effectiveness of ridge preservation with in the control group (-2.2mm) than the test Primary flap closure
bone grafting in the extraction sockets alone group (-1.5mm). These results showed small
was evaluated in a dog study (Boix et al. benefits toward using Bio-oss® collagen. Soft tissue grafts versus no soft tissue grafts
2006). The maxillary and mandibular premo- A similarly designed study (Araùjo & Lind- In five beagle dogs, the 3rd and 4th mandibu-
lars were extracted. The sockets of the distal he 2009) compared sockets healing without lar premolars were extracted (Fickl et al.
roots were filled with an injectable bone sub- treatment (control) and sockets treated with 2008a). In the test group, the sockets were
stitute (a polymer solution and granules of a Bio-oss® collagen (test). Flaps were coronally filled with Bio-oss® collagen, and free gingi-
biphasic calcium phosphate ceramic), and the replaced and primary closure was achieved in val grafts were obtained to cover the sockets.
sockets of the mesial roots were left unfilled both types of sockets. After 6 months of The control sites were also filled with
as controls. Primary closure was achieved by healing, biopsies were obtained. Histometric Bio-oss® collagen (Geistlich Biomaterials, W
overlapping hermetic sutures. After 3 months analysis revealed that the dimensional olhusen, LU, Switzerland). The collagen was
of healing, a tangent vector was drawn con- changes in the apical and middle portion of fixed with sutures, but no soft tissue grafts
necting the buccal and lingual crests, and the the sockets were moderate in both sites, but were applied. After 4 months of healing, the
distance from the highest point of the alveo- in the coronal portion, the ridge width reduc- histomorphometric evaluation showed a
lar ridge and this tangent vector was mea- tion was three times greater in the control mean vertical buccal bone loss that was sig-
sured. There was a significant difference sockets ( 35%) compared with the test sock- nificantly lower in the control group
between the groups in the mandible (0.5mm ets ( 12%). However, the composition (2.8 mm) than in the test group (3.3 mm). At
and 0.4mm in test and control, respectively) between two sites was similar. The xenograft 1mm below the crest, the control group had
and the maxilla ( 0.3 and 0.5 in the test (Bio-Oss®, Geistlich Biomaterials, W olhusen significantly narrower ridge width than the
and control, respectively). LU, Switzerland)) only served as a scaffold and test group (4.4 mm vs. 4.8 mm). But at
In another dog study (Shi et al. 2007), man- did not stimulate new bone formation. 3 mm/5 mm below the crest, the ridge width
dibular premolars and molars were extracted, Another histometric study (Rothamel et al. was similar between the test and control
the extraction sockets on the test side were 2008) compared sockets treated by Nanocrys- groups. In another study digital image analy-
treated with Surgical-Grade Calcium Sulfate talline hydroxyapatite paste (test) with un- sis on study casts from the same material
(SGCS) + platelet-rich plasma (PRP) or with filed sockets (control). Primary closure was (Fickl et al. 2008b), the remodeling process at
SGCS alone. On the control side, the sockets achieved in both groups. After 3 and the buccal aspect from baseline to after
were left unfilled. Primary closure was 6 months of healing, the dogs were sacrificed. 4 months of healing was similar between the
achieved by periosteal releasing incisions and Histometric analysis on lingual and buccal control and test groups ( 1.5 mm vs. 1.6
coronally advanced flaps. At baseline and bone height, alveolar wall, and total bone mm). These results, therefore, indicate the
2 months after healing, CT scans were taken. width showed no difference for any parame- need for further human research using free
Alveolar bone height was assessed on CT ters between groups. It could be concluded gingival grafts to obtain primary closure for
scans as the distance from the midpoint of that Nanocrystalline hydroxyapatite paste alveolar ridge preservation in well preserved
the cortical bone to the inferior border of the does not appear to be effective for ridge pres- alveoli.
mandible. It was found that the reduction in ervation.
the ridge height was significantly greater in
Clinical trials
the control group compared with the test Xenografts versus autografts
group (2.77, 1.39 mm, respectively), although For many years, the use of autologous bone Implants for ridge preservation
no difference was found between SGCS + was regarded as a “gold standard” for augmen-
PRP treatment and SGCS treatment alone. tation procedures. To evaluate its efficacy in Immediate implants alone
In five beagle dogs (Fickl et al. 2008a,b), ridge preservation, a dog study was conducted To observe the alteration of hard tissues fol-
the 3rd and 4th mandibular premolars were (Araùjo & Lindhe 2011). Extraction sockets in lowing tooth extraction and immediate
extracted. In the test sites, the sockets were the mandibles of dogs were filled with either implant placement, a clinical study was con-
filled with Bio-Oss® collagen (Geistlich anorganic bovine bone or autogenous bone ducted (Botticelli et al. 2004). In 18 patients,
Biomaterials, W olhusen, LU, Switzerland). chips. After 3 months of healing, a histomet- 21 SLA surface implants were placed. After
The collagen was fixed with sutures. The ric analysis was performed. The cross-sec- 4 months of non-submerged healing without
control sites were left untreated. After tional area of the ridge alteration was loading, a re-entry surgery was performed.
4 months of healing, the histomorphometric estimated by subtracting the cross-sectional The differences between the clinical mea-
evaluation documented a mean vertical buc- ridge area identified after extraction from the surements made before implant placement
cal bone loss that was significantly lower in corresponding area at the adjacent root. In the and after 4 months of healing yielded a hori-
the test (2.8 mm) than in the control sites apical and middle portions of the sockets, no zontal resorption of the buccal bone of about
(3.2 mm). At 1 mm below the crest, the resorption was observed. However, in the 56%. The corresponding resorption of the lin-

150 | Clin. Oral Implants Res. 23, 2012 / 147–156 © 2012 John Wiley & Sons A/S
Wang & Lang  Ridge preservation revisited

gual/palatal bone was 30%, whereas the ver- et al. 2009); 12 immediate transmucosal zontal bone resorption by 20% when
tical bone resorption was on average 0.3 mm implants with an sandblasted acid etched compared with the tapered implants (control).
at the buccal aspect and 0.6 mm at the lin- surface were placed in 12 patients. GBR was In three centers, 93 patients were included in
gual/palatal aspect. This amount of resorp- performed by placing a resorbable collagen the study. Forty-five cylindrical implants
tion is very similar with the resorption at membrane supported by a bone substitute (Astra Tech AB, Mölndal, Sweden) were
human alveolar ridges after extraction (Bio-oss®). The alveolar bone dimensions installed into extraction sockets in the test
reported recently in a systematic review (Tan around the implants were assessed at the group, and 48 tapered implants (Astra Tech
et al. 2012). This, in turn, means that time of implant surgery and at the re-entry AB, Mölndal, Sweden) were placed in the con-
implants immediately placed into extraction surgery after 6 months of healing. The gaps trol group. At baseline and at the re-entry sur-
sockets, also in humans, do not prevent the around the implants healed as expected. gery after 4 months healing, the results
resorption of the alveolar bony ridge. However, the horizontal distance from the indicated that there was a marked reduction
outer surface of the alveolar ridge to the in the distance from the outer surface of the
Immediate implant with bone GBR implant surface at the buccal aspect was ridge to the implant in both groups (43% and
The effect of membrane placement in con- reduced by 58% on average. Unfortunately, 30%, respectively), although this difference
junction with or without bone substitutes for no control group was provided in this study. was not statistically significant. Once again, it
preserving the alveolar bony around implants An interesting aspect of this study was the was evidenced that tapered implants cannot
immediately placed into extraction sockets of influence of bone thickness on the buccal preserve the alveolar bony ridge. On the con-
the anterior region (Chen et al. 2007) was bone resorption. If the buccal bony wall was trary, tapered implants were associated with
studied in 30 patients that randomly received initially 1-mm thick, the buccal bone resorp- more bone resorption.
immediate implants (SLA surface, Institute tion was as high as 52%. However, when the
Straumann AG, Basel, Switzerland) with Bio- buccal bone wall was initially 2-mm thick, Non-surgical treatment
oss® + collagen membrane (Geistlich Bioma- the buccal bone resorption was significantly
terials, W olhusen, LU, Switzerland), Bio-oss® reduced to 33%. Ultrasonic non-surgical treatment
alone, or were left un-grafted. The dimen- The effect of ultrasonic application on bone
sions of the alveolar bony crest were assessed Shape of implants and implant positioning healing has been studied in the orthopedic lit-
at baseline and at the re-entry surgery after As one of the proposed benefits of using root- erature. In vitro experiments showed a signifi-
6 months of healing. The implants were formed implants was to avoid the need for cant influence of ultrasound on the
loaded after further 2 months, and the bone augmentation, a multi-center random- proliferation of mandibular osteoblasts. Clini-
patients were followed up to 3 years after ized controlled clinical trial was conducted to cal evidence has also demonstrated that ultra-
completion of restoration delivery. Standard- test this hypothesis (Lang et al. 2007). In nine sound treatment may accelerate the healing
ized peri-apical radiographs and peri-implant centers, 216 patients received either cylindri- process of tibial diaphysis fractures by 38% in
examinations were performed every year. At cal or tapered implants (Institute Straumann time (Kerr et al. 2008). In a randomized con-
the re-entry surgery, there was no significant AG, Basel, Switzerland) installed into the trolled split-mouth clinical trial, 12 patients
difference between the groups on the vertical extraction sockets in non-molar regions. Dur- who were scheduled for tooth extraction on
and horizontal defect reduction around the ing the surgery, the type of implants was allo- both sides of the jaw were enrolled. At 7–
implants. On the other hand, the reduction cated at random and the need for guided bone 10 days following extraction, ultrasound ther-
in the horizontal distance from the outer sur- regeneration was assessed. Whenever the gap apy was delivered on the alveolar ridge of the
face of the buccal bony ridge to the implant around the implants was more than 0.5 mm test site for 20 min using a piezoelectric
surface was significantly greater in the con- or whenever buccal bony plate was thin (less transducer for 10 sessions over the subsequent
trol group (48.3 ± 9.5%) than in the bone than 1 mm), augmentation procedures were 4 weeks. Standardized cone-beam volumetric
graft alone group (15.8 ± 16.9%) and the bone performed. Questionnaires were given to both tomography (CBVT) scans were acquired at
graft with membrane group (20 ± 21.9%). patients and the operators to assess the prefer- baseline (7–10 days post extraction), comple-
During the 3-year post-restorative follow-up, ence to these two types of implants. The tion of ultrasound therapy (4 weeks after ther-
all patients kept excellent oral hygiene. No results revealed that 90% of both implant apy), and 3 months post extraction.
difference was found regarding the peri- designs required GBR procedures. Patient- Dimensional changes of the buccal and lin-
implant or radiographic parameters between reported outcomes did not show any prefer- gual bony plates were analyzed through
baseline and 1-year/3-year follow-ups or ence toward any type of the implants. How- CBVT. However, given the limitations of
among the groups. This clinical study dem- ever, the surgeons’ perception was in favor of small sample size and a short observational
onstrated that the bone defect around the the tapered implants. Therefore, it is evident period with CBVT scans in this study, no sig-
immediately placed implants will heal pre- that root-formed implants do not offer an nificant differences could be found in absolute
dictably irrespective of the usage of mem- advantage in the need for avoiding GBR bony dimensional changes.
branes or bone grafts. However, the procedures.
membrane or bone graft treatment may Another multi-center study aimed to a com- Bone substitutes
reduce the horizontal resorption of the buccal parison of the dimensional bony changes
bony plate by 25% of the original dimension. around the two types of implants (Sanz et al. Bone fillers alone
Another clinical study was performed in 2010). The hypothesis of the study was that, In a randomized controlled clinical trial (Nei-
the molar region, to examine the alteration by providing more space for the coagulum va et al. 2008), the effectiveness of an
of the alveolar bony ridge around implants around the implants, the cylindrical implants anorganic bovine-derived hydroxyapatite
immediately placed into molar extraction (test) should have a positive effect in preserv- matrix delivered in a putty-form combined
sockets after 6 months of healing (Matarasso ing the alveolar bone and to reduce the hori- with a synthetic cell-binding peptide P-15

© 2012 John Wiley & Sons A/S 151 | Clin. Oral Implants Res. 23, 2012 / 147–156
Wang & Lang  Ridge preservation revisited

(Putty P15) on ridge preservation was investi- sium-enriched hydroxyapatite was found to was found on ridge width reduction between
gated. Comparisons were made between be more useful in alveolar ridge preservation the single particle size group (1.4 mm) and
untreated control sockets and sockets treated than calcium sulfate. multiple particle size group (1.3 mm). The
with this putty-form matrix (test). Collagen In a recent clinical split-mouth design vertical buccal and lingual bone loss was less
dressing material was applied in both groups. study (Fernandes et al. 2011), sockets treated than 0.5 mm in both groups. Histological
After 4 months of healing, at the re-entry with anorganic bovine bone matrix (ABM) analysis did not find any difference between
surgery, no difference was found between the + synthetic cell-binding peptide P-15 (Test) the groups. Obviously, ridge preservation
groups in ridge width reduction ( 1.31 and were compared with unfiled sockets (control). using this grafting material irrespective of its
1.43mm in test and control, respectively). The sockets in both groups were covered particle sizes was effective.
However, significantly less ridge height with Acellular dermal matrix (ADM). Clini-
reduction was found in the test group cal measurements were made at baseline and Demineralized allografts versus mineralized allografts
(0.15 mm) compared with the control group after 6 months of healing. No statistically Although both demineralized freeze-dried
( 0.56 mm). The bone density assessed dur- significant differences could be found on bone allograft (DFDBA) and mineralized
ing implant surgery was found significantly ridge height reduction between the groups freeze-dried bone allograft (FDBA) are claimed
higher in the test group as well. (1.5 and 1.2 mm in the control and test to be osteoconductive; only DFDBA has been
Another biomaterial, medical-grade calcium groups, respectively). But the ridge width proven to be osteoinductive. Both DFDBA
sulfate hemihydrates (MGCSH) was evaluated resorption was significantly greater in the and FDBA contain bone morphogenic pro-
in a randomized controlled clinical trial (Ai- control (3.40 mm) compared with the test teins (BMP). As the process of demineraliza-
metti et al. 2009). In the test group, 22 group (2.52 mm). tion facilitates the release of soluble factors
patients received this material in their sock- The effectiveness of an allograft material like BMP, evidence suggested that a maxi-
ets. As control group, 18 patients did not in ridge preservation was recently tested in a mum of osteoinduction was observed when
receive any treatment after extraction at all. randomized controlled clinical trial (Brown- there was approximately 2% residual calcium
Clinical measurements were performed at field & Weltman 2012). Twenty patients in DFDBA. However, FDBA may serve as a
baseline and at the re-entry surgery (implant were divided into two groups. The extraction superior scaffold compared with DFDB for
surgery). After 3 months of healing, signifi- sockets in the test group were treated with space maintenance and may also be more os-
cantly greater reduction in ridge height was an allograft paste composed of “osteoinduc- teoconductive. When osteoclasts break down
found in the control group (1.2 mm) compared tive” demineralized bone matrix and cancel- the mineral content in FDBA until it is also
with test group (0.5 mm). Moreover, signifi- lous bone chips, and the sockets in the demineralized, there could be a prolonged os-
cantly greater ridge width reduction was found control group were left unfilled. The sockets teoinductive effect. To evaluate the clinical
in the control group (3.2 mm) compared with in both groups were covered with an absorb- effectiveness of these two materials on ridge
the test group (2.0 mm). A histological analy- able collagen wound dressing. No significant preservation, a randomized controlled clinical
sis also found less lamellar bone and more difference on ridge resorption was found trial was performed (Wood & Mealey 2011).
woven bone in the control group. between the two groups as studied by CBCT/ Forty patients were randomly allocated into
Two new materials were evaluated in a Micro CT and histological analysis, although two groups. The extraction sockets of the
split-mouth clinical trial (Crespi et al. 2009). CBCT analysis found a significant correlation patients were filled with FDBA or DFDBA,
In 15 patients, three teeth were extracted in between initial buccal bony plate thickness respectively. All grafting materials were
each patient. One of the sockets was treated and loss of ridge height. obtained from a single donor. Clinical mea-
with magnesium-enriched hydroxyapatite surements were performed at baseline and at
(Test 1). Another socket was treated with Different particle size re-entry surgery after 4–5 months of healing.
Calcium sulfate (Test 2). The third socket In general, smaller particles of bone substi- No difference between the groups was found
was left unfilled (control). The filling materi- tutes are preferred because they may be on ridge height reduction (1 mm in both
als in the two test groups were secured with resorbed more rapidly. They may enhance groups) or ridge width reduction (2 mm in
a collagen sheet covering and sutures to affix osteogenesis because of a greater surface area. both groups). However, histological analysis
the membrane. Applying standardized intra- On the other hand, the optimal particle size yielded that the vital bone content was signif-
oral radiographs obtained at baseline and may depend on the bony defect to be grafted. icantly higher in the DFDB group (38.42% vs.
3 months later at the re-entry surgery, signif- Extraction sockets may benefit more using 24.63%), while the residual graft content was
icant differences in ridge height reduction larger particles, as the sockets are usually lar- significantly lower in DFDBA group (8.88%
was found among all groups ( 0.48, 2.48, ger than the periodontal defects. vs. 25.42%). Although DFDBA may seem to
and 3.75 mm in the Test 1, Test 2, and To elaborate on the most appropriate parti- be more osteoinductive, its effect on ridge
control group, respectively). In histological cle size to be used in extraction sockets, a preservation is similar to that of FDBA.
analyses, the amount of vital bone was found randomized controlled clinical trial was
to be significantly different among all groups conducted (Hoang & Mealey 2012) in 20 Synthetic bone substitutes versus xenografts
(40.0, 45.0, and 32.8% in the Test 1, Test 2, patients. One molar was extracted in each Bone Ceramic® is a biphasic ceramic bone
and control group, respectively). The amount patient. The sockets were either filled with substitute. It is composed of a combination
of connective tissue was not different human demineralized bone matrix (DBM) of hydroxyapatite (HA) and b-tricalcium
between the test groups, but it was signifi- putty with a single particle size (2–4 mm) or phosphate (b-TCP). HA is insoluble.
cantly different between the test and control with multiple particle sizes (125–710 lm). Although it is well tolerated in bone, its os-
groups. Significantly, less residual grafting Clinical assessments of the ridge dimensions teoconductive properties have been ques-
material was found in sockets treated with were made at baseline and at re-entry surgery tioned. To be osteoconductive, the material
Calcium sulfate. Based on this study, magne- after 4–5 months of healing. No difference should leave space for new bone to be depos-

152 | Clin. Oral Implants Res. 23, 2012 / 147–156 © 2012 John Wiley & Sons A/S
Wang & Lang  Ridge preservation revisited

ited. Unlike HA, b-TCP is soluble. When it material appeared to interfere with the normal may increase in dimension to partially com-
slowly resorbs, it is replaced by new bone. healing process. Hence, using this material for pensate the hard tissue resorption, especially
The objective of combining the insoluble HA crestal bone preservation when implants are in vertical direction. Hence, the assessment of
with b-TCP, therefore, is that HA would considered, even after long healing time, study casts may not be appropriate to evaluate
maintain the space (scaffold function), while should be revised and based on additional the effectiveness of ridge preservation proce-
the b-TCP would resorb and promote new scientific studies. dures.
bone formation.
A randomized controlled clinical trial was Collagen plugs Guided Bone Regeneration (GBR)
conducted to compare the ability of preserving Ideally, ridge preservation procedures should
alveolar ridges with this synthetic material be easy and should not involve additional Ridge preservation with or without GBR
(Bone Ceramic®,Institute Straumann AG, surgery. The use of collagen plug was intro- A cohort study was performed to follow 30
Basel, Switzerland) and a xenograft material, duced, as it has the mentioned advantages. patients who received ridge preservation pro-
deproteinized bovine bone mineral (DBBM) To test its effectiveness on preserving alveo- cedures with resorbable b-TCP of small parti-
(Mardas et al. 2010). Thirty patients were ran- lar ridges, a randomized controlled clinical cle size and resorbable collagen barriers after
domly assigned to two groups. One non-molar trial was conducted (Kim et al. 2011). tooth extraction (Horowitz et al. 2009). Eval-
tooth in each patient was extracted, and the Twenty patients were divided into two uating clinically the alveolar ridge width at
sockets in one group were filled with Bone groups. After the extraction of one molar in baseline and at re-entry surgery 6 months
Ceramic®, whereas in the other group, the each patient, the sockets in one group were later, a mean reduction in the ridge width of
sockets were filled with DBBM. A resorbable grafted with Bio-oss® and a collagen plug. 12.4% was reported. Although there was no
bi-layer collagen membrane was applied to Sutures were applied to fix the material. The control group, it could be estimated from his-
cover each socket. Flaps were coronally sockets in the other group were left unfilled torical controls of a systematic review that
advanced to close the wound as well as possi- as controls. Study casts were obtained imme- reported on horizontal ridge resorption at
ble. Clinical assessments on ridge dimensions diately at baseline and after 3 months of 6 months after extraction (29–63%) (Tan
were made at baseline and at re-entry surgery healing. Assessments of the bony height and et al. 2012) that this ridge preservation proce-
after 8 months of healing. The reduction in ridge width were performed. After calcula- dure applying the guided tissue regeneration
the ridge width was significantly less in the tion, the average resorption rate of the bone principle was certainly effective.
Bone Ceramic® group ( 1.1 mm) than in height was 6.8% in the control group and In a randomized controlled clinical trial (Ba-
DBBM group ( 2.1 mm). The reduction in the 5.8% in the test group. There was no signifi- rone et al. 2008), 40 patients were randomly
ridge height was negligible in both groups. cant difference between the groups. The aver- allocated into two groups. After tooth extrac-
Both materials partially preserved the width age resorption rate of the alveolar ridge width tion, the sockets of the patients in test group
and interproximal bone height of the alveolar at 3 mm below the crest was 20.7% in the received guided bone regeneration procedures
ridge. Bone Ceramic® achieved a better out- control group and 14.3% in the test group. with cortico-cancellous porcine bone and col-
come in preserving the alveolar ridge. In a Although this technique may be advanta- lagen membranes. The sockets of the patients
clinical study (De Coster et al. 2011), whereby geous in preserving the alveolar ridge, no def- in the control group were left to heal sponta-
bone regeneration in healing extraction sock- inite recommendations may be made. neously. Clinical measurements were per-
ets substituted with Bone CeramicÒ was com- formed at baseline and at re-entry surgery
pared with unfilled sockets, biopsies were Collagen plugs with soft tissue grafts after 7 months of healing. It was found that
obtained from the sites during later performed To evaluate the effectiveness of a collagen the reduction in ridge width and height were
implant bed preparation. Healing was evalu- plug together with soft tissue graft on ridge significantly lower in the GBR group com-
ated using transmitted light microscopy after preservation (Oghli & Steveling 2010), 125 pared with control group (2.5 mm vs. 4.5 mm;
6–74 weeks (mean 22 weeks). 15 Bone cera- patients were divided into three groups. After 0.4 mm vs. 3 mm, respectively). Histological
micÒ sites were compared with 10 naturally tooth extraction, the sockets were treated analysis revealed that the amount of cancel-
healed sockets. During implant placement it with either a cone comprised of collagen (Test lous bone was significantly greater in the GBR
was clinically observed that bone at the sub- 1), a cone comprised of collagen and impreg- group (35.5% vs. 25.7%), and the amount of
stituted sites was softer than in control sites nated with gentamicin (Test 2), or left unfilled connective tissue was significantly less in the
and large amount of loose biomaterial were (control). In the two test groups, soft tissue GBR group (36.6% vs. 59.1%).
found requiring thorough debridement. Con- grafts were harvested from the palate, and the
sequently, some of the recipient beds were too sockets were covered with the sutured grafts. Membranes versus no membranes
large to get normal diameter implants initially Study casts were obtained at baseline and after To evaluate the adjunctive effect of resorb-
stable. Hence, wider implants were necessary, 3 months of healing. Assessments of the verti- able collagen membranes to bone substitutes,
and in 4 substituted sites, implants could not cal dimension of the alveolar ridge were made a randomized clinical study was conducted
be installed at all. Additionally, it was on the casts. No difference was found among (Brkovic et al. 2012). Twenty patients were
reported that 2 out of ten implants installed in the three groups on vertical ridge resorption randomly allocated into two groups. After
substituted sockets failed within 3 months (0.8, 0.1, and 0.3 mm in Test 1, Test 2, and tooth extraction, each socket was filled with
after insertion. The histology showed that 5/ control groups, respectively). However, cau- a cone that is comprised of b-tricalcium
15 substituted sites showed clearly incom- tion should be taken while interpreting these phosphate (b-TCP) and type I collagen. The
plete healing. Overall, new bone formation results. While using study casts to measure sockets in the test group were covered with
was consistently poorer than in controls and the ridge dimensions, soft and hard tissue collagen membranes, whereas the sockets in
presented with predominantly loose connec- alterations are included as indicated in a sys- the control group were not. Primary closure
tive tissue and less woven bone. The grafting tematic review (Tan et al. 2012). Soft tissue was achieved in both groups by muco-perio-

© 2012 John Wiley & Sons A/S 153 | Clin. Oral Implants Res. 23, 2012 / 147–156
Wang & Lang  Ridge preservation revisited

steal flaps. Clinical assessments were per-


formed at baseline and at re-entry surgery
• Immediate loading of the implants in dogs • Although DFDBA may be claimed to be
as well as in humans does not preserve the more osteoinductive, its effect on ridge
after 9 months of healing. No statistical sig-
alveolar bone ridge. The use of bone fillers preservation is similar to that of FDBA.
nificant differences were found between the
test and control groups on horizontal ridge
in residual defects around immediate • A combination of hydroxyapatite and b-tri-
implants placed in well preserved, intact calcium phosphate (Bone Ceramic®) was
resorption ( 0.86 mm vs. 1.29 mm, respec-
alveoli in dogs may reduce soft tissue twice as effective on preserving the alveo-
tively) or on vertical dimensional changes
recession as well as vertical and horizontal lar ridge width when compared with de-
(0.12 mm vs. 0.5 mm, respectively). Histo-
resoprtion of the buccal bony plate. proteinized bovine bone mineral (Bio-
metric analysis showed that there was no dif-
ference between the test and control groups
• Simultaneous guided bone regeneration oss®). However, the use of BoneCeramic®
procedures could partially resolve alveolar as a grafting material in fresh extraction
regarding the amount of new bone (45.3% vs.
bone resorption. However, this is sockets appears to interfere with normal
42.4%, respectively). Obviously, applying the
depended on the type of membrane as healing processes of the alveolar bone, and
cone material with or without membranes
well as the techniques applied. hence its indication as a material for bone
was effective in preserving the alveolar bone.
• The use of root-formed implants, aiming augmentation, when implant placement is
at closing the space between the implant considered, should be reconsidered (De
Primary flap closure
surface and alveolar bone of the extrac- Coster et al. 2011).

Primary closure versus no primary closure


tion socket, does not preserve alveolar • Although collagen plugs were claimed to
bone ridges. On the contrary, their use have an advantage in avoiding surgery, no
Primary closure can also be attained by
with this association was associated with definite recommendations can be made
means of an implant-supported provisional
accentuated bone resorption. based on their poor outcome on preserv-
prostheses, or using a customized healing
abutment. In a recent split-mouth clinical • It was demonstrated that thicker bony ing the alveolar ridge.
walls results in less resorption.
trial (Engler-Hamm et al. 2011), molars or
premolars were extracted bilaterally in 11 • The position of the implants was also an
Guided bone regeneration
patients. The sockets on both sides were
essential factor for the alveolar bone ridge
preservation. Placing the immediate
• Applying the guided bone regeneration
filled with an inorganic bovine-derived principle using bone substitutes together
implant 0.8mm deeper and more lingually
hydroxyapatite matrix, cell-binding peptide with a collagen membrane has shown
led to a reduction in the vertical buccal
P-15 (ABM/P-15), DFDBA, and covered with clear effects on preserving alveolar ridge
bone resorption by 70% in dogs after
collagen membranes. Primary closure was height as well as ridge width.
4 months of healing.
achieved on one side (control). On the other
side, the membranes were left uncovered
Primary flap closure
(test). Clinical assessments of the ridge width
were made using a caliper through a stent at
Non-surgical treatment
• There is not enough evidence to recom-
• A dog study revealed that using free gingi-
val grafts in combination with bone sub-
baseline and at after 6 month of healing. In mend ultrasonic instrumentation for
stitutes did not provide additional effects
addition, questionnaires regarding the post- alveolar ridge preservation and no conclu-
on ridge preservation compared with bone
operative discomfort were filled by the sions on its clinical benefits can be made.
substitutes alone.
patients. No significant differences were
found on the ridge width changes (3 mm vs.
• A clinical trial showed that achieving pri-
mary flap closure did not present addi-
3.42 mm). However, the post-operative dis- Bone substitutes tional beneficial effects on preserving the
comfort was significantly lower in the group
• The only relevant dog study showed that ridge width. On the other hand, patients
without primary closure. The mucogingival unfilled sockets underwent three times experienced more discomfort with pri-
junction was significantly more coronally the amount of horizontal resorption as mary closed flaps. Moreover, the muco-
displaced in the group with primary closure. sockets filled with xenograft (Bio-oss®). gingival junction was significantly more
However, the xenograft only served as a coronally displaced in the primary closed
Conclusions scaffold and did not stimulate new bone flap sites.
formation.
Implants and associated techniques for alveolar • Various bone substitute materials have
ridge preservation been tested in clinical trials for their
• Implants placed into the fresh extraction effects on ridge preservation. Acknowledgements: This manuscript
sockets do not prevent the resorption of • Ridge preservation using human deminer- was supported by a grant of the Clinical
Research Foundation (CRF) for the Promotion
the alveolar bone. Although osseointegra- alized bone matrix was effective in ridge
tion is achieved in the early stage preservation irrespective of the particle of Oral Health, Brienz, Switzerland. The
(1 month in dogs), modeling of the bone sizes used, but allograft paste showed no senior author was an ITI Scholar 2010–2012
may cause this level to recede apically. effect. at the University of Hong Kong.

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21. (Suppl 5): 1–21.

156 | Clin. Oral Implants Res. 23, 2012 / 147–156 © 2012 John Wiley & Sons A/S
Wah Lay Tan A systematic review of post-extrac-
Terry L. T. Wong
May C. M. Wong
tional alveolar hard and soft tissue
Niklaus P. Lang dimensional changes in humans

Authors’ affiliations: Key words: alveolar bone, dimensional change, extraction, hard tissue, human, removal of
Wah Lay Tan, Terry L. T. Wong, May C. M. Wong, teeth, resorption, soft tissue, systematic review
Niklaus P. Lang, Implant Dentistry, The University
of Hong Kong, Prince Philip Dental Hospital,
Implant Dentistry, Hong Kong, China Abstract

Corresponding author:
Background: Removal of teeth results in both horizontal and vertical changes of hard and soft
Prof. Niklaus P. Lang, DMD, MS, PhD, Dr odont.h. tissue dimensions. The magnitude of these changes is important for decision-making and
c. mult. comprehensive treatment planning, with provisions for possible solutions to expected
The University of Hong Kong Faculty of Dentistry
Prince Philip Dental Hospital complications during prosthetic rehabilitation.
34 Hospital Road, Sai Ying Pun Objectives: To review all English dental literature to assess the magnitude of dimensional changes
Hong Kong, China of both the hard and soft tissues of the alveolar ridge up to 12 months following tooth extraction
Tel.:+852 2859 0526
Fax: +852 2858 6114 in humans.
e-mail: nplang@dial.eunet.ch Methods: An electronic MEDLINE and CENTRAL search complemented by manual searching was
conducted to identify randomized controlled clinical trials and prospective cohort studies on hard
Conflicts of interest and soft tissue dimensional changes after tooth extraction. Only studies reporting on undisturbed
The authors declare no conflict of interest. post-extraction dimensional changes relative to a fixed reference point over a clearly stated time
period were included. Assessment of the identified studies and data extraction was performed
independently by two reviewers. Data collected were reported by descriptive methods. Weighted
means and percentages of the dimensional changes over time were calculated where appropriate.
Results: The search provided 3954 titles and 238 abstracts. Full text analysis was performed for 104
articles resulting in 20 studies that met the inclusion criteria. In human hard tissue, horizontal
dimensional reduction (3.79 ± 0.23 mm) was more than vertical reduction (1.24 ± 0.11 mm on
buccal, 0.84 ± 0.62 mm on mesial and 0.80 ± 0.71 mm on distal sites) at 6 months. Percentage
vertical dimensional change was 11–22% at 6 months. Percentage horizontal dimensional change
was 32% at 3 months, and 29–63% at 6–7 months. Soft tissue changes demonstrated 0.4–0.5 mm
gain of thickness at 6 months on the buccal and lingual aspects. Horizontal dimensional changes of
hard and soft tissue (loss of 0.1–6.1 mm) was more substantial than vertical change (loss 0.9 mm to
gain 0.4 mm) during observation periods of up to 12 months, when study casts were utilized as a
means of documenting the changes.
Conclusions: Human re-entry studies showed horizontal bone loss of 29–63% and vertical bone
loss of 11–22% after 6 months following tooth extraction. These studies demonstrated rapid
reductions in the first 3–6 months that was followed by gradual reductions in dimensions
thereafter.

The periodontium is an important structure tion or extraction of the tooth. Subsequent to


that supports the tooth and is affected by any removal of a tooth, the periodontium under-
changes that the tooth may undergo, includ- goes atrophy (Cohn 1966; Schropp et al.
ing eruption and extraction (Cohn 1966; Pie- 2003), with the complete loss of attachment
trokovski & Massler 1967, 1971). The apparatus including cementum, periodontal
alveolar process is a tooth-dependent tissue; ligament fibres and bundle bone (Araujo &
the shape and volume of the alveolar process Lindhe 2005).
Date:
is influenced by tooth form, as well as the Tooth extraction is one of the most widely
Accepted 15 October 2011
direction of eruption of the tooth (Marks performed dental procedures. In general, post-
To cite this article: 1995; Marks & Schroeder 1996), and the pres- extraction healing of both the hard and soft
Tan WL, Wong TLT, Wong MCM, Lang NP. A systematic ence or absence of teeth (Tallgren 1972). Sim- tissues proceeds uneventfully. However, the
review of post-extractional alveolar hard and soft tissue
dimensional changes in humans. ilarly, gingival tissues undergo changes removal of a tooth will generally result in
Clin. Oral. Impl. Res. 23(Suppl. 5), 2012, 1–21 together with eruption and eventual exfolia- some alveolar bone loss, as well as structural
doi: 10.1111/j.1600-0501.2011.02375.x

© 2011 John Wiley & Sons A/S 1


Tan et al ! Dimensional tissue changes post extraction

and compositional changes in the overlying that alveolar bone loss can be quite marked OR
soft tissue (Schropp et al. 2003). Both hori- after tooth removal (Araujo & Lindhe 2009), <[text words] Tooth AND Extraction>)
zontal and vertical changes in dimensions are especially in the horizontal dimension (Botti- AND
expected in hard tissue (Van der Weijden celli et al. 2004). Soft tissue changes
et al. 2009) as well as soft tissue. Studies in post-extraction have largely been described Outcome:
the canine model (Araujo & Lindhe 2005; qualitatively, and usually as a single entity (<[MeSH terms/all subheadings] “Bone
Araujo et al. 2005) have demonstrated that together with the hard tissue changes Resorption “ OR “Alveolar Bone Loss” OR
there are marked dimensional changes of the assessed using serial study casts (e.g. Schropp “Periodontal Atrophy”>
alveolar ridge in the first 2–3 months post- et al. 2003). OR
extraction, with the changes more pro- In recent years, there has been one system- <[text words] Bone Defect OR Bone Resorp-
nounced on the buccal (Araujo et al. 2005). atic review addressing the dimensional tion OR Alveolar Bone Loss OR Alveolar
Critically, horizontal buccal bone resorption changes of the alveolar ridge after tooth Resorption OR Alveolar Healing OR Ridge
has been shown reach as much as 56% while extraction (Van der Weijden et al. 2009); Changes OR Ridge Alterations OR Ridge
lingual bone resorption has been reported to however, there is as yet no systematic review Resorption OR Ridge Healing OR Mucosal
be up to 30% (Botticelli et al. 2004); the over- addressing the dimensional changes of both Alterations OR Mucosal Changes OR Muco-
all reduction in width of the horizontal ridge the hard and soft tissues after tooth extrac- sal Atrophy OR Mucosal Healing OR Gingi-
has been reported to reach 50% (Schropp tion. val Alterations OR Gingival Changes OR
et al. 2003). This study aims to review all existing liter- Gingival Atrophy OR Gingival Healing OR
A narrower and shorter ridge can be an ature published between 1st January 1960 Socket Healing OR Socket>)
expected sequelae of the resorptive process and 30th January 2011, to assess the magni- The following journals between 2004 and
(Pinho et al. 2006), and in effect, the process tude of dimensional change of both the hard 2010 inclusive, were hand-searched for rele-
of resorption often results in the relocation of and soft tissues of the alveolar ridge after vant articles: Clinical Oral Implants
the ridge to a more lingual position (Botticelli tooth extraction. Research, International Journal of Oral &
et al. 2004). The process of ridge remodelling Maxillofacial Implants, Implant Dentistry,
is further complicated if the buccal bone wall Journal of Periodontology, Journal of Clinical
Material and methods
is lost (Iasella et al. 2003) as a result of Periodontology and Journal of Oral Implan-
inflammatory processes or the extraction tology.
The Preferred Reporting Items for Systematic
itself. Furthermore, the bibliographies of all pub-
Reviews and Meta-Analyses (PRISMA) state-
Extraction of one or more teeth results lications selected for inclusion in this review
ment was consulted throughout the process
not only in changes of the bony architec- were also scanned for potentially relevant
of this systematic review.
ture, but also affects the overlying soft tis- articles.
sues of the alveolus (Schropp et al. 2003). Focused question
Immediately following tooth extraction, Selection criteria
What is the magnitude of dimensional
there is absence of soft tissue covering over Studies were included if they were published
changes in the hard and soft tissues of the
the socket entrance, and hence the socket in English and conducted on human subjects,
alveolar process, up to 12 months following
defect is left to heal by secondary intention. with the intervention being tooth extraction,
tooth extraction?
In the subsequent weeks, cell proliferation and the outcome to be assessed in the form
will result in an increase in soft tissue vol- Search strategy
of changes in the clinical or radiographic
ume, and a soft tissue covering will seal the A comprehensive and systematic electronic alveolar bone dimensions, as well as dimen-
socket entrance. The changes in the muco- search of both the MEDLINE–Pubmed data- sional soft tissue changes. Similarly, exclu-
sal contours are dependent on the corre- base and the Cochrane Central Register of sion criteria were applied; letters and
sponding changes in the external profile of Controlled Trials (CENTRAL) was con- narrative or retrospective reviews, single case
the alveolar bone surrounding the extraction ducted, for articles published in English reports, case series with less than three cases,
site. between 1st January 1960 and 30th June and third molar extraction cases were all
The magnitude of these dimensional 2010 in the dental literature. The search excluded. Only studies reporting on undis-
changes are important for informed decision- was performed again at a later stage, to turbed post-extraction dimensional changes
making and comprehensive treatment plan- include any relevant new studies published relative to a fixed reference point over a
ning, with provisions for possible solutions between 1st July 2010 and 31st Janu- clearly stated time period were included. In
to expected complications during prosthetic ary 2011. The following key words were addition, in the event of duplicate publica-
rehabilitation. In addition, with the advent of used: tions, the study with the most inclusive data
greater emphasis on aesthetics in the last was preferentially selected.
decade, a thorough understanding of the Intervention:
resorptive pattern and alterations in bony and (<[MeSH terms/all subheadings] “Tooth Selection of studies
mucosal contours post-extraction would Extraction”> Screening was performed independently by
greatly enhance our ability to reconstruct our OR two reviewers (L. T. Wong and W. L. Tan);
patients to a level of optimal function cou- <[text words] Tooth Extraction OR Dental any disagreement between the reviewers was
pled with satisfactory aesthetics. Extraction OR Tooth Removal OR Tooth resolved by discussion. The initial electronic
There have been numerous studies that Pulling OR Tooth Loss OR Exodontia OR search resulted in the identification of 2843
have researched the magnitude of hard tissue Surgery OR Surgical Tooth Extraction OR titles from the MEDLINE–Pubmed database
changes post-extraction, with the consensus Surgical Tooth Removal> and 1111 titles from the Cochrane Central

2 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Potentially relevant Register of Controlled Trials (CENTRAL).


Potentially relevant
publications identified from After careful independent screening of the
publications identified from
electronic search of
electronic search of
Cochrane Central Register of
MEDLINE-Pubmed database
titles and elimination of duplicate titles by
Controlled Trials (CENTRAL) st th
st from 1 January 1960 to 30 both the examiners, a total of 238 titles were
database from 1 January
th June 2010
1960 to 30 June 2010 considered for possible inclusion. Retrieval of
(n = 2843)
(n = 1111)
the 238 abstracts and further perusal led to
104 full-text articles being selected. From
Publications excluded on the basis of title
and summary evaluation; also excluded these full-text articles, 19 were identified for
duplicate publications inclusion in the review.
(n = 3716)
Another article was deemed suitable from
Potentially relevant full texts the secondary electronic search, but no addi-
retrieved for detailed
evaluation tional publications from the hand-search or
(n = 104) the bibliography search of the selected arti-
Publications excluded on the basis of full
text evaluation cles were identified for inclusion.
(n = 85) In total, 20 articles were identified for
Studies included based on eventual inclusion in this review (Fig. 1).
the initial electronic search of A j-score of 0.84 was obtained, for consen-
the MEDLINE-Pubmed and
st
CENTRAL database from 1 sus between the two reviewers.
th
January 1969 to 30 June
2010
(n = 19) Exclusion of studies
Publications included based on the hand- Of the 104 full-text articles examined, 85
search and bibliography search of
relevant articles were excluded from the final analysis
(n = 0)
(Table 1). The main reasons for exclusion
were that there were no actual measure-
Publications included based on the ments of the dimensional changes of the
secondary electronic search of the
MEDLINE-Pubmed and CENTRAL alveolar ridge, the reported parameters were
st st
database from 1 July 2010 to 31
January 2011
not useful for this review and that there was
(n = 1) the presence of a foreign material in the
extraction site during the healing phase,
among other reasons.
Studies included in the
present systematic review
(n = 20)
Data collection
From the selected papers that met the crite-
Fig. 1. Search strategy. Post-extraction dimensional changes.
ria, data addressing dimensional changes

Table 1. Studies failing to meet inclusion criteria


Reference Rationale for exclusion
Richardson 1965; Guglielmotti & Cabrini 1985; Guglielmotti et al. 1985; Mathai et al. 1989; Reported parameters not relevant or not useful
Ubios et al. 1991; Boyne 1995; Gauthier et al. 1999; Teofilo et al. 2001; Brandao et al. 2002;
Indovina & Block 2002; Magro-Ernica et al. 2003; Altundal & Guvener 2004; Bianchi et al. 2004;
Gorustovich et al. 2004; Nevins et al. 2006; Ortega et al. 2007; Araujo et al. 2008; Iino et al. 2008;
Agbaje et al. 2009; Puia et al. 2009; Alissa et al. 2010; Normando et al. 2010
Pietrokovski & Massler 1967a; Matsumoto 1968 Length of observation period not reported
Amemori 1966; Mizutani & Ishihata 1976; Olson & Hagen 1982; Hahn et al. 1988; Oltramari et al. Studies carried out on animals
2007; Shi et al. 2007; Fickl et al. 2008a; Fickl et al. 2008b
Loo 1968; Ashman & Bruins 1985; Ashman & Bruins1987; Scheer & Boyne 1987; Sclar 1999; Descriptive report on procedure/ technique;
Minsk 2005 commentary
Guglielmotti et al. 1986; Hsieh et al. 1995; Fickl et al. 2008c; Rothamel et al. 2008; Araujo & No baseline data available for comparison, thus unable
Lindhe 2009a; Pessoa et al. 2009 to arrive at an estimate of dimensional change over
time
Carlsson & Persson 1967; Pietrokovski & Massler 1967b; Pietrokovski 1967; Green et al. 1969; No measurements of alveolar dimensional changes (e.g.
Huebsch & Hansen 1969; Berkovitz 1971; Pietrokovski & Massler 1971; Hars & Massler 1972; description of healing process or bony shape change,
Librus et al. 1973; Thilander & Astrand 1973; Horn et al. 1979; Olson et al. 1982; Quinn & or histology only)
Kent 1984; Lavelle 1985; Boyes-Varley et al. 1988; Magro-Filho & de Carvalho 1990; Dayan
et al. 1992; Alves-Rezende & Okamoto 1997; Anitua 1999; Pinto et al. 2002; Carmagnola
et al. 2003; Cardaropoli et al. 2005; Smith 1974; Ahn & Shin 2008; Serino et al. 2008; Sharan &
Madjar 2008; Luvizuto et al. 2010; Teofilo et al. 2010
Bergstedt et al. 1973; Michael & Barsoum 1976; Kangvonkit et al. 1986; Sattayasanskul et al. Study subjects had immediate dentures after extraction,
1988 hence they did not have undisturbed healing
post-extraction
Bahat et al. 1987; Iizuka et al. 1992; Yugoshi et al. 2002; Araujo et al. 2005; Lindeboom et al. Sample did not include untreated/undisturbed extraction
2006; Wu et al. 2008; Araujo & Lindhe 2009b; Nevins et al. 2009 sockets left to heal spontaneously
Araujo & Lindhe 2005 Only measured relative difference in height between
buccal and lingual plates of the alveolus

© 2011 John Wiley & Sons A/S 3 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

of both soft and hard tissues of the alveolar Assessment of heterogeneity including molar extraction sites and one
ridge were retrieved for analysis. Mean Statistical heterogeneity between all the study (Oghli & Steveling 2010) did not spec-
values and standard deviations, where included studies was not assessed because all ify where the extractions were performed.
available, were extracted in duplicate by the studies had different observation time Most of the data extracted concerned teeth in
the two reviewers (L. T. Wong and W. L. points as well as measurement methods, control groups of studies that evaluated vari-
Tan). making a statistical comparison impossible. ous ridge preservation procedures (Lekovic
However, assessment of heterogeneity et al. 1997, 1998; Yilmaz et al. 1998; Camar-
Quality assessment between studies with similar characteristics go et al. 2000; Iasella et al. 2003; Serino et al.
Assessment of study quality was performed were performed using Cochran’s Q-test: 2003; Fiorellini et al. 2005; Barone et al.
for all the included papers. The Cochrane 2008; Aimetti et al. 2009; Crespi et al. 2009;
X
Collaboration’s tool for assessing risk of bias Q¼ wi ðxi % x!Þ Oghli & Steveling 2010; Pelegrine et al. 2010;
was used in the case of randomized con- Rasperini et al. 2010), but other studies were
trolled clinical trials and controlled clinical The P-value was then calculated for the Q either designed specifically to evaluate post-
trials. Methodological quality assessment of statistic and a value of P < 0.05 would indi- extraction alveolar changes (Carlsson & Pers-
cohort studies was based on the Newcastle– cate significant statistical heterogeneity son 1967; Schropp et al. 2003; Rodd et al.
Ottawa Quality Assessment Scale for Cohort between the studies. 2007; Moya-Villaescusa & Sanchez-Perez
studies (Tables 2 and 3). When Q > df, where df is its degree of free- 2010) or the effect of smoking (Saldanha
dom, the I2 index was also calculated using et al. 2006) or ultrasound treatment (Kerr
Data synthesis the following formula: et al. 2008) on these changes. In addition,
Preliminary evaluation of the selected publi- one included study (Bragger et al. 1994) was
! "
cations revealed that there was considerable Q % df actually designed to test the effect of
I2 ¼ & 100%
heterogeneity between the studies with Q chlorhexidine mouthrinse on post-extraction
regard to study design, study population, healing. Each paper that was included in
study period, method of assessment of where, I2 = 0% to 40% would indicate this review contributed a number of extrac-
dimensional change of the alveolar ridge as there is little to no heterogeneity tion sites, ranging from three to over a
well as reference point from which the I2 = 30% to 60% would indicate there is hundred sites. The age range of the patients
changes were measured. Taking this into moderate heterogeneity in these studies was between 10.8 and
consideration, it was not appropriate to con- I2 = 50% to 90% would indicate there is 53.3 years.
duct a quantitative data synthesis for all substantial heterogeneity
studies, leading to a meta-analysis. In this I2 = 75% to 100% would indicate consider- Included studies
case, we attempted to report the data by able heterogeneity There were a total of 20 studies addressing
applying descriptive methods. In addition, Similarly, the P-value was calculated for the hard and soft tissue dimensional changes
as a selected few of the included studies the I2 statistic, and a value of P < 0.05 would of the alveolar ridge in humans, with sponta-
demonstrated some similarity in measure- indicate a result that is statistically signifi- neous undisturbed healing. The studies were
ment methods and reference points, we pre- cant. grouped according to the reported changes in
sented weighted means of the dimensional hard tissue, soft tissue, or a combination of
change of the alveolar ridge over time as Results both hard and soft tissue.
appropriate, taking into account the values
of the relevant standard deviation and Collectively, a total of 20 studies satisfied Hard tissue changes
applying inverse variance weighting (Meier the inclusion criteria and were included in Vertical and horizontal linear hard tissue
1953). this systematic review. changes in humans were reported indepen-
The 20 studies included 11 randomized dently or in combination by 17 studies
Inverse variance weighting controlled clinical trials, five controlled clini- (Tables 4 and 7).
For the weighted mean of the list of data for
cal trials and four cohort studies (Tables 2
which each mean xi comes from a different
and 3). The majority of studies did not state Vertical linear hard tissue alteration
probability distribution with a known
the reasons for tooth extraction, but in the All 17 studies that reported on post-extrac-
variance ri2, the weight for each study is
studies that did, they included fractures, car- tion hard tissue changes looked into the ver-
given by:
ies, trauma, endodontic, prosthodontic, tical linear dimensional change of the
orthodontic and periodontal reasons. Thirteen alveolus. Eight studies (Lekovic et al. 1997,
1
Wi ¼ papers only studied non-molar extraction 1998; Camargo et al. 2000; Iasella et al. 2003;
ri2
sites (Carlsson & Persson 1967; Lekovic et al. Serino et al. 2003; Barone et al. 2008; Aimetti
The weighted mean in this case is: 1997, 1998; Yilmaz et al. 1998; Camargo et al. 2009; Pelegrine et al. 2010) utilized
et al. 2000; Iasella et al. 2003; Serino et al. re-entry procedures with stents or titanium
Pn
ðxi =r2i Þ 2003; Fiorellini et al. 2005; Saldanha et al. pins as reference points (Fig. 2), one other
x! ¼ Pi¼1
n 2
i¼1 ð1=ri Þ
2006; Rodd et al. 2007; Barone et al. 2008; study (Rasperini et al. 2010) did not carry out
Aimetti et al. 2009; Pelegrine et al. 2010), a re-entry procedure but nevertheless utilized
and the variance of the weighted mean is: while six studies (Bragger et al. 1994; Schropp a stent for reference. An additional eight
et al. 2003; Kerr et al. 2008; Crespi et al. studies (Carlsson & Persson 1967; Bragger
1 2009; Moya-Villaescusa & Sanchez-Pérez et al. 1994; Schropp et al. 2003; Fiorellini
r2x! ¼ Pn 2
i¼1 ð1=ri Þ 2010; Rasperini et al. 2010) reported on data et al. 2005; Saldanha et al. 2006; Kerr et al.

4 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Table 2. Cochrane Collaboration’s tool for assessing risk of bias


Carlsson & Persson (1967) Brägger et al. (1994)
Controlled clinical trial Randomized controlled clinical trial
Study design Parallel Parallel
Adequate sequence generation No Unclear
Remark Quote “alternate patients were assigned to respective Quote “then randomly assigned”
groups”
Insufficient information about sequence generation
Allocation concealment Unclear Unclear
Remark No information provided. No information provided.
Blinding Unclear Yes
Remark Study did not address this outcome. Quote “ double-blind clinical trial”
Incomplete outcome data addressed Yes No
Remark Quote “one patient from each group had to be Initially mentioned that 40 patients were enrolled in
discarded….one had moved…other case first radiograph study, but subsequently only obtained radiographs for
unsuccessful and could not be repeated..” 23 patients with no explanation
Free of selective reporting Yes No
Remark Initially mentioned that 40 patients were enrolled in
study, but subsequently only obtained radiographs for
23 patients with no explanation
Free of other sources of bias Yes Yes
Remark
Overall risk of bias High High

Lekovic et al. (1997) Lekovic et al. (1998)


Controlled clinical trial Randomized controlled clinical trial
Study design Split-mouth Split-mouth
Adequate sequence generation Unclear Yes
Remark No information provided Quote “ control and experimental sites were assigned by
the flip of a coin”
Allocation concealment Unclear Unclear
Remark No information provided No information provided
Blinding Unclear Yes
Remark Study did not address this outcome Quote “clinical measurements were performed by one
clinician who did not have knowledge of control and
experimental sites”
Incomplete outcome data addressed Yes Yes
Remark Mentioned that three patient had dehiscence in test No missing outcome data
group, hence did not measure values at 6 months;
re-entry was planned at 6 months, but if membrane
exposure occurred, re-entry and measurements was
done at 3 months. Refer to Tables 3–5 and will see that
they analysed the results with various combinations,
including with or without the patients that exited early,
suggesting an intention-to-treat analysis
Free of selective reporting Yes Yes
Remark
Free of other sources of bias Yes Yes
Remark
Overall risk of bias Unclear Unclear

Camargo et al. (2000) Iasella et al. (2003) Serino et al. (2003) Fiorellini et al. (2005)
Randomized controlled Randomized controlled clinical
Controlled clinical trial clinical trial Controlled clinical trial trial
Study design Split-mouth Parallel Parallel and split-mouth Parallel
Adequate sequence Unclear Yes Unclear Unclear
generation
Remark No information provided Quote “randomly selected No information provided Quote “ cohorts of 40 patient
using a coin toss” randomized in a double-blind
manner”
Insufficient information about
sequence generation
Allocation Unclear Unclear Unclear Unclear
concealment
Remark No information provided No information provided No information provided No information provided
Blinding Unclear Yes Unclear Yes
Remark Study did not address this Quote “measurements were No information provided Quote “all the patients in the study
outcome taken by 2 masked underwent the same surgical
examiners” procedure, regardless of the
treatment
Incomplete outcome Yes Yes Yes Yes
data addressed

© 2011 John Wiley & Sons A/S 5 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Table 2. (continued)
Camargo et al. (2000) Iasella et al. (2003) Serino et al. (2003) Fiorellini et al. (2005)
Randomized controlled Randomized controlled clinical
Controlled clinical trial clinical trial Controlled clinical trial trial
Study design Split-mouth Parallel Parallel and split-mouth Parallel
Remark No missing outcome data Quote “implants were Quote “nine subjects Quote “ No subjects were
successfully placed at all dropped out from the withdrawn or lost to follow-up”
sites….none have been study for reasons unrelated
subsequently lost” to the therapy”
Free of selective Yes Yes Yes Yes
reporting
Remark
Free of other sources Yes Yes Yes Yes
of bias
Remark
Overall risk of bias Unclear Unclear Unclear Unclear

Barone et al. (2008) Kerr et al. (2008) Aimetti et al. (2009)


Randomized controlled clinical
Randomized controlled clinical trial Randomized controlled clinical trial trial
Study design Parallel Split-mouth Parallel
Adequate sequence generation Yes Unclear Unclear
Remark Quote “using a Quote “ one site was assigned Quote “ were consecutively
computer-generated randomly as test, whereas the selected..” and “ all sockets were
randomisation list…” other site was assigned as control” measured and assigned randomly
to test or control”
Insufficient information about Insufficient information about
sequence generation sequence generation
Allocation concealment Unclear Unclear No
Remark No information provided No information provided Assignment not explicitly
concealed
Blinding Yes Yes Yes
Remark Quote “all measurements were Quote “examiner was masked as to Quote “recorded by the same
taken by one examiner who was whether sites were test or control” examiner, who was not involved
not involved in performing the in providing therapy”
surgical treatment…”
Incomplete outcome data addressed Yes Yes Unclear
Remark No loss to follow-up in test and No missing outcome data Study did not address this
control group outcome
Free of selective reporting Yes Yes Yes
Remark
Free of other sources of bias Yes Yes Yes
Remark
Overall risk of bias Unclear Unclear High

Crespi et al. (2009) Pelegrine et al. (2010) Rasperini et al. (2010)


Randomized controlled clinical
Controlled clinical trial Randomized controlled clinical trial trial
Study design Split-mouth Parallel Parallel
Adequate sequence generation No Unclear Yes
Remark Quote “sockets on right side of jaw Quote “teeth to be extracted were Quote “treatment regimens were
received MHA….sockets on left randomized into two groups” assigned randomly to the subjects
side received CS…” with a balanced random permuted
block approach”
Allocation by left or right side Insufficient information about
of jaw sequence generation
Allocation concealment Unclear Unclear Yes
Remark No information provided. No information provided. Quote “treatment regimens
assigned randomly…
communicated to the operator
immediately after tooth
extraction”
Blinding Yes Unclear Yes
Remark Quote “a masked examiner Study did not address this outcome Quote “tubes included into the
measured the bone level changes.” stent by a blind examiner…..after
surgery, blinded examiner
positioned the stent.”
Incomplete outcome data addressed Yes Unclear Yes
Remark No missing outcome data Study did not address this outcome. Missing outcome data balanced in
numbers across groups
Free of selective reporting Yes Yes Yes
Remark
Free of other sources of bias Yes Yes Yes
Remark
Overall risk of bias High Unclear Low

6 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Table 2. (continued)
Yilmaz et al. (1998) Oghli & Steveling (2010)
Controlled clinical trial Randomized controlled clinical trial
Study design Parallel Parallel
Adequate sequence generation Unclear Unclear
Remark No information provided Quote “patients were divided randomly into three groups”
Insufficient information about sequence generation
Allocation concealment Unclear Unclear
Remark No information provided No information provided
Blinding Unclear Unclear
Remark Study did not address this outcome Study did not address this outcome
Incomplete outcome data addressed Unclear Yes
Remark Study did not address this outcome All exclusions accounted for
Free of selective reporting Yes Yes
Remark
Free of other sources of bias Yes Yes
Remark
Overall risk of bias Unclear Unclear

2008; Crespi et al. 2009; Moya-Villaescusa & tion of 0.9 ± 1.6 mm at the mid-buccal, were lost at time of extraction, there was a
Sanchez-Pérez 2010) utilized imaging meth- 0.4 ± 1.0 mm at the mid-lingual, 1.0 ± 0.8 corresponding gain of buccal bone height of 1
ods to obtain the required information. mm at the mesial and 0.8 ± 0.8 mm on the and 0.6 mm at 3 and 6 months respectively.
Only one re-entry study (Aimetti et al. distal sites; the latter study recorded a mean Radiographic methods used for the relevant
2009) addressed the vertical linear change of reduction of 0.7 ± 1.2 mm on the buccal. studies were: lateral cephalometric radiogra-
the alveolar hard tissue post-extraction at Taking into consideration the similarities phy in one study (Carlsson & Persson 1967),
3 months. In this study, 3 months after between these six re-entry studies that cone beam computed tomography in two
extraction of anterior maxillary teeth, a mean reported 6-month data (Lekovic et al. 1997, studies (Fiorellini et al. 2005 and Kerr et al.
vertical reduction of 1.2 ± 0.8 mm on the 1998; Camargo et al. 2000; Iasella et al. 2003; 2008), linear tomography in one study (Salda-
buccal, 0.9 ± 1.1 mm on the palatal and Serino et al. 2003; Pelegrine et al. 2010), the nha et al. 2006), and intraoral peri-apical radi-
0.5 ± 0.9 mm on the mesial and distal sites weighted mean was calculated for the rele- ography in four studies (Bragger et al. 1994;
were reported when an acrylic stent was used vant sites, using the inverse variance Schropp et al. 2003; Crespi et al. 2009 and
as a fixed reference during re-entry. method, to give a more robust value of the Moya-Villaescusa & Sanchez-Pérez 2010).
A total of six re-entry studies (Lekovic et al. 6-month post-extraction vertical change Carlsson & Persson (1967) attempted to
1997, 1998; Camargo et al. 2000; Iasella et al. (Fig. 3). On the buccal, all six studies were use lateral cephalometric radiography to dem-
2003; Serino et al. 2003; Pelegrine et al. 2010) included to give a weighted mean reduction onstrate the longitudinal height change in
reported data on 6-month post-extraction ver- of 1.24 ± 0.11 mm (Q = 1.3, P = 0.94). Only the mandibular alveolar ridge after extraction
tical linear hard tissue changes of the alveolus; two studies (Iasella et al. 2003; Serino et al. of at least five to six lower anterior teeth and
four studies (Lekovic et al. 1997, 1998; Camar- 2003) were included when mesial and distal loading with conventional full dentures
go et al. 2000; Pelegrine et al. 2010) utilized a sites were investigated; the respective 2 months post-extraction. The study had
titanium screw or pin, while two studies (Ia- weighted reductions were 0.84 ± 0.62 mm on observation time points at 2, 4, 6, 12, 24 and
sella et al. 2003 and Serino et al. 2003) used an the mesial (Q = 0.10, P = 0.75) and 60 months. The reductions in alveolar height
acrylic stent as a fixed reference point. 0.80 ± 0.71 mm on the distal (Q = 0, P = 1). were 2.0 mm at 2 months, 2.9 mm at
Six months following the extraction of After a 7-month undisturbed healing period 4 months, 3.4 mm at 6 months and 4.1 mm
anterior teeth or premolars, Lekovic et al. in non-molar extraction sites, Barone et al. at 12 month, compared to baseline. From this
(1997) reported a mean reduction of (2008) observed vertical linear reduction of study, we can see a trend where there is a
1.2 ± 0.13 mm in buccal vertical ridge height, 3.6 ± 1.5 mm, 3.0 ± 1.6 mm, 0.4 ± 1.2 mm large reduction in alveolar bone height in the
while Lekovic et al. (1998) and Camargo and 0.5 ± 1.0 mm on the mid-buccal, mid-lin- first 2 months post-extraction, followed by a
et al. (2000) reported a mean reduction of gual, mesial and distal sites respectively, at re- continual gradual resorption thereafter. Take
1.50 ± 0.26 mm and 1.00 ± 2.25 mm respec- entry. A stent was used as a fixed reference. note that we should interpret the values
tively. Later, Pelegrine et al. (2010) showed Rasperini et al. (2010) reported on 3- and 6- obtained in this study, with observation time
that 6 months after extraction of maxillary month dimensional changes of the alveolar points greater than 2 months, with caution;
anterior teeth, the mean buccal vertical alve- ridge after extraction of maxillary molar 2 months after teeth extraction, full dentures
olar ridge height reduction was teeth, using a custom acrylic stent and a peri- were inserted in the conventional group, and
1.17 ± 0.26 mm. All the four studies men- odontal probe or endodontic file to obtain the we cannot with full confidence, state that
tioned above measure changes relative to a measurements; measurements were made insertion and use of denture prostheses did
titanium pin or screw at re-entry. from the surface of the bone to the external not have an impact on the resorptive pattern
Iasella et al. (2003) and Serino et al. (2003) surface of the stent. The observed reduction and extent of the alveolar hard and soft tis-
utilized re-entry procedures and acrylic stents in height of the buccal plate at 3 and sues in this case.
as fixed references, 6 months after extraction 6 months were 2.2 and 5.7 mm respectively, Two studies (Fiorellini et al. 2005; Kerr
of non-molar teeth. The former study reported when the buccal plates were intact after et al. 2008) utilized computed tomography to
an average alveolar vertical hard tissue reduc- extraction. However, when the buccal plates detect vertical height changes in the alveolar

© 2011 John Wiley & Sons A/S 7 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Table 3. Newcastle–Ottawa Quality Assessment Scale for Cohort Studies (max 9*)
Schropp et al. (2003) Saldanha et al. (2006)
Study design Cohort Cohort
Selection
Representativeness of the exposed Truly representative of the average implant Representative of the average patient
cohort patient in the community requiring extraction in the community
Rating * *
Selection of non exposed cohort No description of the derivation of non-exposed No description of the derivation of the non-exposed
cohort cohort
Rating
Ascertainment of exposure Secure record (radiograph, study model, clinical Secure record (radiograph, linear tomography, clinical
exam) exam)
Rating * *
Demonstration that outcome of Yes Yes
interest was not present at
start of study
Rating * *
Comparability
Comparability of cohorts on the No mention of control of any confounding factors (e.g. Controlled for confounding factors (smoking, oral
basis of the design or analysis smoking, health) hygiene, ethnicity, systemic health)
Rating **
Outcome
Assessment of outcome Records (radiograph, study models) Independent blind assessment
Rating * *
Was follow-up long enough for Yes; 12 months follow up (early soft/hard tissue healing Yes; 6 months (early hard tissue healing usually
outcomes to occur usually 6–8 weeks) 6–8 weeks)
Rating * *
Adequacy of follow up of cohorts Description of those lost to follow-up No statement
Rating *
Overall 6* 7*

Rodd et al. (2007) Moya-Villaescusa & Sanchez-Pérez (2010)


Study design Cohort Cohort
Selection
Representativeness of the exposed Truly representative of the average young patient Representative of the average patient requiring
cohort with dental trauma in the community extraction in the community
Rating * *
Selection of non exposed cohort No description of the derivation of non-exposed No description of the derivation of non-exposed
cohort cohort
Rating
Ascertainment of exposure Secure record (study model, photograph, clinical Secure record (radiograph, clinical exam)
exam)
Rating * *
Demonstration that outcome of interest Yes Yes
was not present at start of study
Rating * *
Comparability
Comparability of cohorts on the basis Sample size too small to allow statistical Controlled for confounding factors (smoking, number
of the design or analysis adjustment of confounders of roots, oral hygiene, periodontal disease)
Rating **
Outcome
Assessment of outcome Records (study model, photograph) Records (radiograph)
Rating * *
Was follow-up long enough for Yes; 4–61 months follow up (early soft/hard tissue Yes; 3 months follow up (early hard tissue healing
outcomes to occur healing usually 6–8 weeks) usually 6–8 weeks)
Rating * *
Adequacy of follow up of cohorts No statement No statement
Rating
Overall 5* 7*

hard tissue. Fiorellini et al. (2005) reported a of the alveolar ridge were 1.01 ± 0.39 mm on Assessing interproximal bone height
4-month mean height reduction of the buccal, 0.62 ± 0.28 mm on the lingual at change on intraoral periapical radiographs,
1.17 ± 1.23 mm in patients after extraction 1 month and 0.95 ± 0.39 on the buccal, Bragger et al. (1994) demonstrated a vertical
of maxillary non-molar teeth; of note is that 1.12 ± 0.28 on the lingual at 3 months. reduction of 0.61 ± 0.67 mm, 0.67 ±
all the patients in this sample had a buccal Six months after extraction of upper ante- 0.66 mm, 1.19 ± 1.50 mm and 0.93 ± 0.74
defect of ' 50% bone loss of the extraction rior teeth, Saldanha et al. (2006) observed a mm at 1, 2, 3 and 6 months respectively,
socket at baseline. In the study by Kerr et al. vertical resorption of 1.5 mm in smokers and while Schropp et al. (2003) documented a
(2008), following extraction of a permanent 1.0 mm in non-smokers when using linear 0.3 mm loss at 12 months. Crespi et al.
tooth, the corresponding vertical resorption tomography. (2009) went on to show an overall 3-month

8 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Table 4. Characteristics of studies included for hard tissue change only


No. of
Author, Sample extraction
Title publishing year Species QA Tissue Methods size sites
Morphologic changes of the mandible after extraction Carlsson 1967 human CCT Hard Radio 17 5–6 per pt
and wearing of denture
Effect of chlorhexidine(0.12%) rinses on periodontal Bragger 1994 Human RCCT Hard Radio 12 21
tissue healing after tooth extraction(II)radiographic
parameters
A bone regeneration approach to alveolar ridge Lekovic 1997 Human CCT Hard Re-entry (pin) 10 10
maintenance following tooth extraction. Report of
10 cases
Preservation of alveolar bone in extraction sockets Lekovic 1998 Human RCCT Hard Re-entry 16 16
using bioabsorbable membranes (pin 2–5 mm)
Influence of bioactive glass on changes in alveolar Camargo 2000 Human CCT Hard Re-entry 16 16
process dimensions after exodontia (pin 1–8 mm)
Ridge preservation with freeze-dried bone allograft Iasella 2003 Human RCCT Soft Re-entry 12 12
and a collagen membrane compared to extraction + hard (stent)
alone for implant site development: a clinical and
histological study in humans
Ridge preservation following tooth extraction using Serino 2003 Human CCT Hard Re-entry 12 13
a polylactide and polyglycolide sponge as space filler: (stent)
a clinical and histological study in humans
Bone healing and soft tissue contour changes Schropp 2003 Human Cohort Hard Radio 46 46
following single-tooth extraction: a clinical and
radiographic 12-month prospective study
Randomized study evaluating recombinant human Fiorellini 2005 Human RCCT Hard CT scan 20 ?
bone morphogenetic protein-2 for extraction socket
augmentation
Smoking may affect the alveolar process dimensions Saldanha 2006 Human Cohort Hard Radio 21 21
and radiographic bone density in maxillary extraction
sites: a prospective study in humans
Xenograft vs. extraction alone for ridge preservation Barone 2008 Human RCCT Hard Re-entry 20 20
after tooth removal: a clinical and histomorphometric (stent)
study
The effect of ultrasound on bone dimension changes Kerr 2008 Human RCCT Hard CBVT (ref 12 12
following extraction: a pilot study plate)
Clinical and histological healing of human extraction Aimettl 2009 Human RCCT Hard Re-entry 18 18
sockets filled with calcium sulphate (stent)
Magnesium-enriched hydroxyapatite compared to Crespi 2009 Human RCCT Hard Radio 15 15
calcium sulphate in the healing of human extraction
sockets: radiographic and histomorphometric
evaluation at 3 months
Measurement of ridge alterations following tooth Moya-Villaescusa Human Cohort Hard Radio 100 100
removal:a radiographic study in humans 2010
Clinical and histomorphometric evaluation of Pelegrine 2010 Human RCCT Hard Re-entry (pin) 6 15
extraction sockets treated with an autologous bone
marrow graft
Socket grafting in the posterior maxilla reduces the Rasperini 2010 Human RCCT Hard Stent 3 3
need for sinus augmentation

loss of 3.75 ± 0.63 mm when the buccal plate percentage reduction of the vertical dimen- horizontal changes over time in the hard tis-
was lost during extraction. One study (Moya- sion of the alveolus post-extraction as fol- sue at the level of the alveolar crest (Fig. 5).
Villaescusa & Sanchez-Pérez 2010) further lows: Two studies (Kerr et al. 2008; Aimetti et al.
discerned between the bone loss at 3 months 2009) reported 3-month horizontal reduction
after extraction of single-rooted teeth %vertical linear change ðhard tissueÞ to be between 2.20 and 3.20 mm; another
(4.16 ± 0.32 mm) vs. multiple-rooted teeth vertical linear resortion ðhard tissueÞ study (Barone et al. 2008) reported 7-month
¼
(4.48 ± 0.39 mm loss), although the differ- baseline internal socket height reduction to be 4.5 ± 0.8 mm. Lekovic et al.
ence was not statistically significant. The (1997, 1998), Camargo et al. (2000), Iasella
average bone loss when both groups were The calculated percentage vertical change et al. (2003) and Pelegrine et al. (2010) docu-
combined was 4.32 ± 0.24 mm. of the alveolar hard tissue ranged from 11% mented 6-month horizontal reduction in the
to 22% (Fig. 4) at buccal sites, 6 months hard tissue of the alveolar ridge to be 4.40,
Percentage change of vertical linear hard tissue post-extraction. 4.56, 3.06, 2.63 and 2.46 mm respectively.
alteration The five latter studies (Lekovic et al. 1997,
All the four re-entry studies (Lekovic et al. Horizontal linear hard tissue alteration 1998; Camargo et al. 2000; Iasella et al. 2003
1997, 1998; Camargo et al. 2000; Pelegrine A total of eight studies (Lekovic et al. 1997, and Pelegrine et al. 2010) have quite a few
et al. 2010) utilizing a titanium pin or screw 1998; Camargo et al. 2000; Iasella et al. 2003; methodological similarities, however, results
had data on the baseline internal socket Barone et al. 2008; Kerr et al. 2008; Aimetti of the heterogeneity testing reveal that there
height. This facilitated a calculation of the et al. 2009; Pelegrine et al. 2010) reported on is considerable heterogeneity between the

© 2011 John Wiley & Sons A/S 9 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Fig. 5. Horizontal (linear) hard tissue change for re-


entry studies only.

Fig. 2. Vertical (linear) hard tissue change for re-entry


studies only.

Fig. 3. Vertical (linear) hard tissue change for re-entry


Fig. 6. Horizontal (linear) hard tissue change for re-
studies (Q = 17.8, P < 0.05; I2 = 77.6%, studies only; weighted means shown.
entry studies only; weighted means shown.
P < 0.05). In this case, although the weighted
mean was calculated by applying the inverse
variance method to arrive at a value of
The calculated percentage horizontal
3.79 ± 0.23 mm horizontal reduction at
change of the alveolar hard tissue at the alve-
6 months (Fig. 6) across all five studies, the
olar crest ranged from 32% at 3 months, and
robustness and applicability of this value
between 29% and 63% after 6–7 months
should be questioned.
post-extraction (Fig. 8).
Saldanha et al. (2006) reported the horizon-
tal reduction of the alveolar bone at 0% and
Overall hard tissue changes
50% the distance from the crest. This study
In general, with regard to vertical dimen-
demonstrated a 6-month reduction of 0.6 and
sional change, we can see a trend where
1.3 mm for non-smokers and smokers respec-
there is a greater reduction on the buccal and
tively at 0% from the alveolar crest and cor-
lingual sites as compared to the mesial and
responding values of 0.1 and 0.8 mm at 50%
distal sites. Looking at the horizontal dimen-
from the crest. This study utilized linear
sional change, there is a distinct pattern of
tomography to track the changes. Fig. 4. Vertical (linear) hard tissue percentage change in resorption where the resorption decreases
Of note, Kerr et al. (2008) demonstrated four studies.
with increased distance from the alveolar
beautifully that 3 months after tooth extrac-
baseline ridge width immediately post-extrac- crest. Overall, the observed horizontal resorp-
tion, there was a relative decrease in horizon-
tion. This facilitated a calculation of the per- tion of the hard tissues (29–63%) is far
tal ridge reduction as the distance from the
centage reduction of the horizontal dimension greater than the resorption in the vertical
alveolar crest increased (Fig. 7).
of the alveolus post-extraction as follows: dimension (11–22%), over an observation per-
iod of 3–7 months. It can be seen that the
Percentage change of horizontal linear hard tissue
alteration %horizontallinear changeðhard tissueÞ bulk of the resorption occurs in the first
All but one study (Kerr et al. 2008) reporting horizontal linear resortionðhard tissueÞ 3 months post-extraction, and the changes
¼
changes in the ridge width also reported the baseline internal socket height are much more subtle thereafter.

10 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Fig. 9. Change in soft tissue dimensions over time.

pendently or in combination; in one study


(Rodd et al. 2007) the overall areal change of
Fig. 8. Horizontal (linear) hard tissue percentage the alveolar hard and soft tissue combined,
change. was reported.

Vertical linear combined hard and soft tissue


sue thickness at 6 months, measured at buc- alteration
cal and lingual sites 3 mm from the alveolar Three studies (Carlsson & Persson 1967; Yil-
crest. Occlusally, soft tissue with thickness maz et al. 1998 and Schropp et al. 2003)
of 2.1 mm developed after 6 months to com- addressed the combined hard and soft tissue
plete soft tissue coverage of the wound changes in the vertical dimension of the alve-
(Fig. 9). olus.
With the aid of lateral cephalometric radi-
Combined hard and soft tissue changes ography, Carlsson & Persson (1967) was able
To date, a total of five studies (Carlsson & to demonstrate the combined hard and soft
Persson 1967; Yilmaz et al. 1998; Schropp tissue changes of the mandibular alveolus in
et al. 2003; Rodd et al. 2007; Oghli & Stevel- the vertical dimension over time. The verti-
ing 2010) presented data on the longitudinal cal reductions of the conjugated tissue
Fig. 7. Horizontal (linear) hard tissue change with change in the combined hard and soft tissue dimension from baseline were 2.1 mm at
respect to distance from alveolar crest.
dimension of the alveolus post-extraction 2 months, 2.9 mm at 4 months, 3.4 mm at
(Tables 6 and 7). One study (Carlsson & Pers- 6 months and 4.0 mm at 12 month. This
Soft tissue changes son 1967) utilized lateral cephalometric radi- degree of resorption of the combined hard
Only a single study (Iasella et al. 2003) ography whereas study casts were employed and soft tissues followed a similar trend as
reported on longitudinal changes of soft tis- in the other four studies (Yilmaz et al. 1998; that of hard tissue alone.
sue dimensions in the alveolus post-extrac- Schropp et al. 2003; Rodd et al. 2007; Oghli Utilizing sectioned study casts, Yilmaz
tion (Tables 5 and 7). This study & Steveling 2010). Vertical and horizontal et al. (1998) demonstrated a vertical reduc-
demonstrated a 0.4–0.5 mm gain of soft tis- linear tissue alterations were reported inde- tion of 0.1 ± 0.52 mm and 0.5 ± 0.76 mm at

Table 5. Characteristic of study included for soft tissue change only


Author, No. of
Title Publishing Year Species QA Tissue Methods Sample size extraction site
Ridge preservation with freeze-dried bone allograft Iasella 2003 Human RCCT Soft + hard Re-entry (stent) 12 12
and a collagen membrane compared to extraction
alone for implant site development: a clinical and
histological study in humans

Table 6. Characteristics of studies included for both hard and soft tissue changes combined
No. of
Title Authors Species QA Tissue Method Sample size extraction sites
Morphologic changes of the mandible after extraction Carlsson 1967 Human CCT Soft + hard Radio 17 5/6 per pt
and wearing of denture
Alveolar ridge reconstruction and/or preservation Yilmaz 1998 Human CCT Soft + hard Cast 5 10
using root form bioglass cones
Bone healing and soft tissue contour changes Schropp 2003 Human CCT Soft + hard Cast 46 46
following single-tooth extraction: A clinical and
radiographic 12-month prospective study
Change in supporting tissue following loss of a Rodd 2007 Human Cohort Soft + hard Cast 16 16
permanent maxillary incisor in children
Ridge preservation following tooth extraction: Oghli 2010 Human RCCT Soft + hard Cast 72 101
A comparison between atraumatic extraction and
socket seal surgery

© 2011 John Wiley & Sons A/S 11 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Table 7. Overall results from all studies


No. of
Author, Sample extraction Vertical dimensional Horizontal dimensional
Publishing Year Species Tissue Methods size sites change change
Carlsson 1967 Human Hard Radio 17 5–6 per pt 2 month: %2.0(0.9) 2 month: %2.2(1.1)
4 month: %2.9(1.7) 12 month: %3.6(0.5)
6 month: %3.4(2.1) 60 month: %4.0(1.5)
12 month: %4.1(2.7)
24 month: %4.9(3.7)
60 month: %7.3(3.7)
Bragger 1994 Human Hard Radio 12 21 1 month: %0.61(0.67)
2 month: %0.67(0.66)
3 month: %1.19(1.50)
6 month: %0.93(0.74)
Lekovic 1997 Human Hard Re-entry (pin) 10 10 6 month: %1.2(0.13) 6 month: %4.4(0.61)
Lekovic 1998 Human Hard Re-entry (pin2– 16 16 6 month: %1.50(0.26) 6 month: %4.56(0.33)
5 mm)
Camargo 2000 Human Hard Re-entry (pin1– 16 16 6 month: %1.00(2.25) 6 month: %3.06(2.41)
8 mm)
Iasella 2003 Human Soft+ Re-entry (stent) 12 12 6 month: B %0.9(1.6) 6 month: %2.6(2.3)
hard L %0.4(1.0)
M %1.0(0.8)
D %0.8(0.8)
Iasella 2003 Human Soft Re-entry (stent) 12 12 6 month: B 0.4(0.6)
L 0.5(1.5)
(Soft tissue thickness change)
Serino 2003 Human Hard Re-entry (stent) 12 13 6 month: B %0.8(1.6)
M %0.6(1.0)
D %0.8(1.5)
Schropp 2003 Human Hard Radio 46 46 12 month: M %0.3
D %0.3
Schropp 2003 Human Soft+ Cast 46 46 3 month: B %0.1 3 month: %3.8
hard L %0.8 6 month: %5.1
6 month: B 0.1 12 month: %6.1
L %0.9
12 month: B 0.4
L %0.8
Fiorellini 2005 Human Hard CT scan 20 ? 4 month: %1.17(1.23)
Saldanha 2006 Human Hard Radio 21 21 6 month: %1.0 to 1.5 6 month: %0.1 to 1.3
Barone 2008 Human Hard Re-entry (stent) 20 20 7 month: B %3.6(1.5) 7 month: %4.5(0.8)
L %3.0(1.6)
M %0.4(1.2)
D %0.5(1.0)
Kerr 2008 Human Hard CBVT 12 12 1 month:B %1.01(0.39) 1 month: %0.16(0.96)
(ref plate) L %0.62(0.28) %0.62(0.24)
3 month:B %0.95(0.9) %0.26(0.17)
L %1.12(0.28) %0.10(0.10)
3 month: %2.20(0.81)
%1.30(0.24)
%0.59(0.17)
%0.28(0.10)
Aimettl 2009 Human Hard Re-entry (stent) 18 18 3 month: B%1.2(0.6)
L %0.9(1.1)
M %0.5(0.9)
D %0.5(1.1)
Crespi 2009 Human Hard Radio 15 15 3 month: %3.75(0.63)
Moya-Villaescusa Human Hard Radio 100 100 3 month: %4.32(0.23)
2010
Pelegrine 2010 Human Hard Re-entry (pin) 6 15 6 month: %1.17(0.26)
Rasperini 2010 Human Hard Stent 3 3 3 month: %2.2
6 month: %5.7(4.2)
Yilmaz 1998 Human Hard Cast 5 10 3 month: %0.1(0.52) 3 month: %0.1(0.23)
12 month: %0.5(0.76) 12 month: %0.4(0.48)
Rodd 2007 Human Hard Cast 16 16 3 month: 15.7%
6 month: 25.3%
9 month: 22%
(Bone surface area)
Oghli 2010 Human Hard Cast 72 101 3 month: %0.3(0.5)

3 and 12 months respectively, post-extrac- well as 3, 6 and 12 months after extraction was followed by a net gain of 0.1 mm at
tion of maxillary incisor teeth (Fig. 10). of maxillary posterior teeth. Taking the 6 months and 0.4 mm at 12 months of the
Schropp et al. (2003) took measurements occlusal surfaces of adjacent teeth as refer- buccal sites. Lingual sites demonstrated a
from study casts taken immediately after as ence, a reduction of 0.1 mm at 3 months loss of 0.8–0.9 mm between 3 and 6 months,

12 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

always more substantial than the vertical


change.

Discussion

The 20 included studies in this systematic


review were of different study designs and
measured dimensional change in various
ways.
Eleven randomized controlled clinical tri-
als, five controlled clinical trials and four
cohort studies were included in this review.
Fig. 11. Horizontal (linear) change of hard and soft tis- It is common knowledge that randomized
sues combined.
controlled clinical trials and the systematic
review of randomized controlled clinical tri-
als provide the highest level of evidence
provide any information on the standard related to intervention and therapy. However,
deviations in the study, so it was impossible in the case of post-extractional dimensional
to utilize the inverse variance method to cal- changes of the alveolar hard and soft tissues,
Fig. 10. Vertical (linear) change of hard and soft tissues
culate the weighted means. there are no randomized controlled clinical
combined.
trials where the control procedure is where
Cross-sectional surface area alteration of combined the tooth was left in situ and the test proce-
with a net loss of 0.8 mm at 12 months alveolar hard and soft tissues
dure was extraction. Hence, the cohort stud-
(Fig. 10). A single study reported on change in alveolar
ies where post-extraction alveolar hard and
surface area of the hard and soft tissues com-
soft tissues changes were monitored longitu-
Horizontal linear combined hard and soft tissue bined (Rodd et al. 2007); measurements were
dinally might provide better insight and be
alteration obtained from study casts acquired prior to,
the more appropriate study design.
Four studies (Carlsson & Persson 1967; Yil- and at 3, 6 and 9 months following extrac-
The three main measuring methods uti-
maz et al. 1998; Schropp et al. 2003; Oghli & tion of maxillary central incisors in children.
lized were: (i) re-entry (ii) imaging and (iii)
Steveling 2010) presented data on the com- The reductions in surface area were presented
study models. The re-entry method consti-
bined hard and soft tissue change in the hori- as a percentage of the surface area on the pre-
tuted of elevating a flap during extraction
zontal dimension following extraction. extraction cast, and were as follows: 15.7%
and again at re-evaluation. All the studies
The only study using radiographic methods at 3 months, 25.3% at 6 months and 22% at
using the re-entry method measured the
(Carlsson & Persson 1967) demonstrated a 9 months.
parameters from a fixed reference, namely an
reduction of the alveolar width in the magni-
acrylic stent or a titanium pin or screw. The
tude of 2.2 mm at 2 months, which subse- Overall combined hard and soft tissue changes
imaging method included the utilization of
quently increased to 3.6 mm at 12 months; With the aid of various assessment methods,
periapical radiographs, lateral cephalometric
this measurement was taken 3 mm from the a longitudinal change of the combined hard
radiography, or computer tomography. The
alveolar crest. and soft tissues in the vertical dimension
method where study models were utilized
Study casts were used in some of the stud- was found to be anywhere between a loss of
required that study impressions be taken
ies (Yilmaz et al. 1998; Schropp et al. 2003; 4.0 mm to a gain of 0.4 mm over a period of
before, or immediately after extraction, and
Oghli & Steveling 2010) to evaluate the 2–12 months.
again at re-evaluation.
change in the horizontal dimension (Fig. 11). Study casts and radiographs were employed
Re-entry studies evaluated hard tissue as
Yilmaz et al. (1998) showed a 3- and 12- to assess the reduction of the combined hard
well as soft tissues as separate entities, while
month reduction in width of 0.1 ± 0.23 mm and soft tissues in the horizontal dimension.
imaging studies evaluated either hard tissue
and 0.4 ± 0.48 mm respectively, while Oghli This reduction was demonstrated to be
dimension only, or the combined hard and
& Steveling (2010) reported a 3-month reduc- between 0.1 and 6.1 mm when the observa-
soft tissue changes. Study model studies
tion of 0.3 ± 0.5 mm. Horizontal resorption tion periods varied from 3 to 12 months, and
focused on combined hard and soft tissue
of the alveolar hard and soft tissue between 3 the measurements were taken at the alveolar
dimensional changes. During data analysis
and 12 months was also reported by Schropp crest. When the measurements were taken
process, we subdivided the data into different
et al. (2003); at 3 months the resorption was 3 mm apical to the alveolar crest, the corre-
groups, mainly according to measurement
3.8 mm, this increased to 5.1 mm at sponding horizontal reductions of the com-
methods and the tissues involved. The
6 months and culminated to a value of bined hard and soft tissues were 2.2 mm at
groups include (i) hard tissue group, (ii) soft
6.1 mm at 12 months. 2 months and 3.6 mm at 12 months. Reduc-
tissue group, and (iii) combined hard and soft
The latter three studies (Yilmaz et al. tions in cross-sectional surface area of the tis-
tissue group.
1998; Schropp et al. 2003; Oghli & Steveling sues were up to 22% after 9 months.
2010) had quite many similarities and an Mimicking the changes of the alveolar hard
Heterogeneity assessment
attempt to calculate the weighted means for tissue, there is a similar pattern of resorption
The 20 included studies had different obser-
these three studies was launched. However, when we look at the combined hard and
vation time points, methodologies, and
the study by Schropp et al. (2003) failed to soft tissue entity; the horizontal alteration is

© 2011 John Wiley & Sons A/S 13 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

measurement methods. Heterogeneity assess- of resorption can be explained by the bundle Hard tissue horizontal dimensional change
ment was performed in six re-entry studies bone concept as proposed by Araujo & Lind- Five re-entry studies (Lekovic et al. 1997,
(Lekovic et al. 1997, 1998; Camargo et al. he (2005). According to this theory, a larger 1998; Camargo et al. 2000; Iasella et al. 2003;
2000; Iasella et al. 2003; Serino et al. 2003 proportion of the buccal plate is made up of Pelegrine et al. 2010) showed that there was
and Pelegrine et al. 2010) calculating mean bundle bone relative to the lingual plate; as range of 2.46–4.56 mm horizontal bone loss
vertical hard tissue change, and five studies bundle bone is a tooth-dependent tissue, it is and weighted mean resorption of 3.79 mm at
(Lekovic et al. 1997, 1998; Camargo et al. quickly resorbed after tooth extraction and 6 months. However, theses studies only pro-
2000; Iasella et al. 2003 and Pelegrine et al. with its resorption, a substantial portion of vided data for horizontal resorption at the
2010,) calculating horizontal hard tissue the buccal plate is lost. In our review of the level of the alveolar crest, no data was avail-
change. These studies had similarity in terms literature, however, the relative height differ- able on magnitude of horizontal resorption a
of the method of measurements employed. ence between the buccal and lingual bone distance away from the alveolar crest. Kerr
The studies all employed re-entry methods, plates in humans was less marked compared et al. (2008) demonstrated a relative decrease
utilizing an acrylic stent or a titanium pin or to the canine model by Araujo & Lindhe in horizontal ridge reduction as the distance
screw as a fixed reference from which to (2005). The relative difference in height of from the alveolar crest increased. This find-
measure the dimensional changes. The differ- the buccal and lingual plate is estimated to ing was similar to a dog study done by Ara-
ences in sample sizes, different behaviours of be around 0.3–0.6 mm over a period of 3 and ujo & Lindhe (2009), which observed more
study populations, varied observation time 7 months, in our review. One possible expla- resorption at coronal third and least resorp-
points and measurement parameters contrib- nation for the observed differences between tion at apical third of the alveolar ridge.
uted to the heterogeneity. Although weighted human models and canine models is that the Hence, it is expected that the amount of hor-
means were calculated, the resultant values buccal plate in humans is on average equally izontal resorption might be less than
should really only be used for reference pur- prone to resorption as the lingual aspect of weighted mean of 3.79 mm at 6 months
poses. The robustness and applicability of the the ridge (Van der Weijden et al. 2009). when the measurement is taken at a distance
weighted means should be interpreted with from the alveolar crest.
caution. Mesial vs. distal
Four studies (Iasella et al. 2003; Serino et al. Hard tissue horizontal dimensional percentage
change
Hard tissue vertical dimensional change 2003; Barone et al. 2008 and Aimetti et al.
There was 32% reduction at 3 months, and
2009) measured vertical dimensional changes
29–63% reduction in horizontal dimension
Buccal/lingual vs. mesial/distal of both mesial and distal bone plates. All four
Three studies (Iasella et al. 2003; Barone at 6 months. This demonstrated that possi-
studies showed the extent of resorption to be
et al. 2008; Aimetti et al. 2009) measured bly more than half of the ridge width could
between 0.4 and 0.8 mm over an observation
vertical dimensional changes of all the buc- be resorbed after 6 months in some patients.
period of 3–7 months.
cal, lingual, mesial and distal bone plates. However, a definite conclusion cannot be
Two of the three studies, namely Barone drawn from these data, on whether the
Hard tissue vertical dimensional percentage
et al. (2008) and Aimetti et al. (2009), demon- change resorption was from the buccal or lingual.
strated that buccal/lingual sites (0.9–3.6 mm Lekovic et al. (1997, 1998), Camargo et al. Studies by Pietrokovski & Massler (1967),
loss at 3–7 months) had more resorption than (2000), Pelegrine et al. (2010) reported base- Schropp et al. (2003), Araujo & Lindhe
mesial/distal sites (0.4–0.5 mm loss at 3– line data of the internal socket height imme- (2005) and Barone et al. (2008) all suggest
7 months). Referring to the calculated values diately post-extraction. Internal socket height that tissue loss is more pronounced on the
of the respective weighted mean, buccal bone is a measurement from buccal bone crest to buccal aspect than from the lingual or pala-
plates (1.24 mm loss at 3–7 months) also had the bottom of the extraction socket. The pro- tal aspect.
a tendency to resorb more than mesial/distal vision of baseline internal socket height
bone sites (0.8–0.84 mm at 3–7 months) enabled us to calculate the percentage change Vertical hard tissue vs. horizontal hard tissue
change
(Fig. 2). One possible explanation for this in height of the buccal bone wall relative to
The amount of horizontal dimensional
trend is that the mesial and distal bone levels the baseline height of the buccal bone wall
change was found to be greater than that of
are partially determined by the presence or over time. The percentage change reflected
the vertical dimension, in both absolute val-
absence of neighbouring teeth; mesial/distal the amount of vertical resorption of the buc-
ues and percentage change. Horizontal reduc-
bone levels are held stable by the presence of cal plate only; this was found to be between
tion (3.79 ± 0.23 mm) was more than vertical
adjacent teeth. 11% and 22% six months post-extraction.
reduction (1.24 ± 0.11 mm on buccal, 0.84 ±
Percentage changes of lingual, mesial and
0.62 mm on mesial and 0.80 ± 0.71 mm on
Buccal vs. lingual distal bony plates could not be calculated due
distal) at 6 months. Percentage vertical
Iasella et al. (2003), Barone et al. (2008) and to lack of baseline data, but it is expected to
change was 11–22% at 6 months while per-
Aimetti et al. (2009) measured vertical be less than 11–22%, as the amount of
centage horizontal change was 32% at
dimensional changes at both buccal and lin- resorption in these areas have been shown to
3 months, and 29–63% between 6 and
gual bone plates. All three studies showed be of a comparatively lesser magnitude. Cor-
7 months.
that the buccal plate resorption (0.9–3.6 mm respondingly, from this this percentage, we
at 3–7 months) was of greater magnitude can interpret that there might be 78–89%
Soft tissue changes
than that of the lingual plate (0.4–3 mm at 3 bone fill of the original socket height, calcu-
Only one study by Iasella et al. (2003) was
–7 months). This finding was similar to pre- lated as percentage vertical bone fill equals
found to have measured soft tissue thickness
vious studies in the canine model (Araujo & one minus vertical dimensional percentage
change after extraction. There was a 0.4–
Lindhe 2005; Araujo et al. 2005). This pattern change.

14 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

0.5 mm gain in soft tissue thickness on buc- ited a trend where there was a rapid reduc- study were negligible after 6 months. Hence,
cal and lingual sites at 6 months. Interest- tion in first 3 months and gradual change raising a flap during extraction may only
ingly, from this study, a difference was found from thereafter, up to 12 months. Weighted affect the short-term dimensional alterations
in the change of soft tissue thickness over a mean reduction showed this change to be of the alveolar ridge.
natural healing socket, and sockets aug- 1.3 mm at 3 months and 5.1 mm at
mented using bio-resorbable membranes and 12 months. Overeruption of adjacent teeth
grafts. There was net gain of soft tissue Mizutani & Ishihata (1976) found that the
thickness in the natural healing group and a Vertical vs. horizontal combined hard and soft
over-eruption of teeth adjacent to the extrac-
net loss in the augmented group. One possi- change tion socket affected the overall dimensional
ble explanation for this observation was that Hard and soft tissue showed a combined hori- change of ridge. The vertical alveolar ridge
the membrane or graft placed might have zontal reduction of 0.1–3.8 mm and 5.1 mm height in this study decreased slightly ini-
interfered with the soft tissue vascularity in at 3 and 6 months respectively. Correspond- tially, followed by a gradual increase later on,
the augmented group. We must remember ingly, in the vertical dimension, this change which negated the previous reduction or even
that the vascular supply to the soft tissue is was between 0.1 and 0.8 mm reduction at surpassed the amount of resorption to result
derived from the underlying bone, and the 3 months, and 0.1 mm gain to 0.9 mm in a net gain. The study speculated that the
placement of membranes or grafts might reduction at 6 months. Overall, the demon- over-eruption of teeth adjacent to extraction
interfere with re-vascularization of the soft strated horizontal change was more substan- sites might have affected the pattern of
tissues. In contrast, there is no interposing tial than the vertical change. dimensional change observed.
material between the bone and the overlying
soft tissues in the naturally healing sockets. Combined hard and soft tissue change vs. hard Smoking
Although there was an observed gain in soft tissue change only Smoking may affect the extent of vertical
In the horizontal dimension, the combined
tissue thickness over a naturally healing reduction of the alveolar ridge after extrac-
hard and soft tissue reduction was 5.1 mm at
socket, a robust conclusion cannot be drawn tion. Saldanha et al. (2006) showed that
6 months, while the corresponding hard
from this single study. there was a significant difference in dimen-
tissue reduction was between 2.46 and
In addition, this study also demonstrated a sional reduction between smoking and non-
4.56 mm, with a weighted mean reduction of
trend where the lingual soft tissues were smoking groups. There was vertical alveolar
3.79 mm.
thicker than that on the buccal; lingual soft ridge reduction of 1.5 mm in smokers and
Hence, at 6 months post-extraction, the
tissues were nearly twice as thick. The meth- 1.0 mm in non-smokers, 6 months post-
combined hard and soft tissues demonstrated
ods and materials in the study could explain extraction.
a tendency towards a more substantial reduc-
this difference; majority of teeth extracted
tion than hard tissue only; this observation is
within the study were maxillary teeth where Single-rooted vs. multiple-rooted teeth
not corroborated in the vertical aspect. Moya-Villaescusa & Sanchez-Pérez (2010)
palatal soft tissue is expected to be much
In the vertical dimension, when consider- study showed there was no significant differ-
thicker than that of the buccal. Hence, this
ing only hard tissue change (loss of 0.4– ence in vertical dimensional change between
finding may only be applicable to the maxil-
1.5 mm at 6 months), the magnitude of this single-rooted (4.16 mm loss) and multi-rooted
lary extraction sockets, but not mandibular
change was greater than that of the hard and teeth (4.48 mm loss), although there was a
ones. Note that this study only had a sample
soft tissues combined (0.1 mm gain to tendency that multi-rooted teeth exhibited
size of 12 non-molar extraction sockets,
0.9 mm reduction at 6 months). A plausible greater resorption of the alveolar ridge.
hence we should be cautious when trying to
explanation might be that the increase in soft
interpret the results of this study.
tissue thickness (gain of 2.1 mm occlusally
Chlorhexidine
Vertical combined hard and soft tissue change
vs. gain of only 0.4–0.5 mm on buccal/lin- Rinsing with 15 ml of 0.12% chlorhexidine
Two studies by Yilmaz et al. (1998) and Sch- gual) compensated for the reduction in hard digluconate mouthrinse twice daily for
ropp et al. (2003) demonstrated very subtle tissue height. 1 month, starting 2 days after extraction may
changes in the vertical dimension of the hard have some effect on the observed vertical
and soft tissues combined, between 3 and Possible factors affecting dimensional change change of the mesial and distal bone. Bragger
after tooth extraction
12 months post-extraction. The changes ran- et al. (1994) showed that patients rinsing for
ged from a gain of 0.1 mm to a loss of 1 month with a placebo solution lost almost
Flap vs. flapless
0.9 mm at 6 months and a gain of 0.4 mm to 1 mm of bone height over a 6-month period
Using a canine model, Fickl et al. (2008a)
a loss of 0.8 mm at 12 months. Schropp et al. after extraction, while in patients rinsing
demonstrated that there was significant dif-
(2003) also observed a small increase buccally with the chlorhexidine solution, the crestal
ference of the extent of bone resorption
and a reduction orally. alveolar bone level was maintained.
between flap and flapless extractions. The
flapless group had lower extent of resorption
Horizontal combined hard and soft tissue Immediate denture
change compared to the flap group. Blanco et al.
Carlsson & Persson (1967) showed that there
Three studies (Yilmaz et al. 1998; Schropp (2008) also showed similar trend in another
was no significant difference in alveolar
et al. 2003 and Oghli & Steveling 2010) study, although the study was investigating
dimensional change between patients with
reported data on horizontal hard and soft tis- ridge alterations after immediate implants
immediate or conventional dentures in the
sue changes. The studies by Yilmaz et al. with or without flap. However, Araujo &
long-term. Take note, however, that the
(1998) and Schropp et al. (2003) had a follow- Lindhe (2009) found that the differences
usage of immediate dentures had a tendency
up of up to 12 months; both studies exhib- between the flap and flapless groups in their
to affect dimensional change in short-term,

© 2011 John Wiley & Sons A/S 15 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

but the effect would be negligible after Conclusions extraction may mask the real extent of hard
2 years post-extraction. tissue resorption and impact on the overall
In conclusion, the studies included in this outcome of any reconstructive efforts, espe-
Bone resorption pattern after 12 months review demonstrated that horizontal bone cially with regard to aesthetics. However,
Only one study (Carlsson & Persson 1967) loss (29–63%, 2.46–4.56 mm, weighted mean more studies might be required to arrive at a
followed dimensional changes in human 3.79 mm at 6 months) was more substantial more definitive value of soft tissue changes
alveolar ridge for up to 5 years. This study than vertical bone loss (11–22%, 0.8–1.5 mm, post-extraction, and clarify the influence of
displayed a similar pattern where there was a weighted mean 1.24 mm at 6 months) after this change.
relatively rapid reduction in the first tooth extraction. The buccal aspect generally Overall, dimensional alterations of the
6 months in both vertical and horizontal displayed more resorption than the lingual/ alveolar hard and soft tissues can be quite
dimension, followed by a gradual reduction palatal aspect. There is an observed resorp- extensive, and an astute clinician will do
thereafter; the reduction continued at a tion pattern of rapid reduction in the first 3– well to understand the pattern and sequelae
steady rate for up to 5 years. This finding 6 months, followed by gradual reduction of these changes, to arrive at predictable
could suggest that bone resorption will con- thereafter, throughout life. treatment outcomes
tinue throughout life once the teeth are Soft tissue on the buccal and lingual sur-
extracted. Take note, however, that all the faces of the alveolar ridge has a tendency to
patients in this study wore complete den- increase in thickness after extraction, as Acknowledgement: This study has
tures; dentures were inserted 2 months after reported in one study; the significance of this been made possible by an educational grant
extractions in the conventional group and finding is as yet unknown. The same study of the Osteology Foundation, Lucerne,
immediately after extractions in the immedi- also documented that 6 months post-extrac- Switzerland.
ate group. We can speculate that the usage of tion, a soft tissue cover of 2.1 mm in thick-
removable complete dentures may also affect ness developed over the original socket; this
the pattern of resorption of the alveolar tis- soft tissue thickness that develops post-
sues.

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implant placement in fresh extraction sockets: an Crespi, R., Cappare, P. & Gherlone, E. (2009) Mag- tenance following tooth extraction. Report of 10
experimental study in the dog. Journal of Clinical nesium-enriched hydroxyapatite compared to cal- cases. Journal of Periodontology 68: 563–570.
Periodontology 32: 645–652. cium sulfate in the healing of human extraction Marks, S.C. Jr (1995) The basic and applied biology
Barone, A., Aldini, N.N., Fini, M., Giardino, R., sockets: radiographic and histomorphometric of tooth eruption. Connective Tissue Research
Calvo Guirado, J.L. & Covani, U. (2008) Xenograft evaluation at 3 months. Journal of Periodontol- 32: 149–157.
versus extraction alone for ridge preservation after ogy 80: 210–218. Marks, S.C. Jr & Schroeder, H.E. (1996) Tooth erup-
tooth removal: a clinical and histomorphometric Fickl, S., Zuhr, O., Wachtel, H., Bolz, W. & Huerz- tion: theories and facts. Anatomical Record 245:
study. Journal of Periodontology 79: 1370–1377. eler, M. (2008a) Tissue alterations after tooth 374–393.
Blanco, J., Nuñez, V., Aracil, L., Muñoz, F. & Ra- extraction with and without surgical trauma: a Meier, P. (1953) Variance of a weighted mean. Bio-
mos, I. (2008) Ridge alterations following imme- volumetric study in the beagle dog. Journal of metrics 9: 59–73.
diate implant placement in the dog: flap versus Clinical Periodontology 35: 356–363. Mizutani, H. & Ishihata, N. (1976) Decrease and
flapless surgery. Journal of Clinical Periodontol- Fiorellini, J.P., Howell, T.H., Cochran, D., Malm- increase in residual ridges after extraction of
ogy 35: 640–648. quist, J., Lilly, L.C., Spagnoli, D., Toljanic, J., teeth in monkeys (part I). Bulletin of Tokyo Med-
Botticelli, D., Berglundh, T. & Lindhe, J. (2004) Jones, A. & Nevins, M. (2005) Randomized study ical & Dental University 23: 157–168.
Hard-tissue alterations following immediate evaluating recombinant human bone morphoge- Moya-Villaescusa, M.J. & Sanchez-Pérez, A. (2010)
implant placement in extraction sites. Journal of netic protein-2 for extraction socket augmenta- Measurement of ridge alterations following tooth
Clinical Periodontology 31: 820–828. tion. Journal of Periodontology 76: 605–613. removal: a radiographic study in humans. Clini-
Bragger, U., Schild, U. & Lang, N.P. (1994) Effect of Iasella, J.M., Greenwell, H., Miller, R.L., Hill, M., cal Oral Implants Research 21: 237–242.
chlorhexidine (0.12%) rinses on periodontal tissue Drisko, C., Bohra, A.A. & Scheetz, J.P. (2003) Oghli, A.A. & Steveling, H. (2010) Ridge preserva-
healing after tooth extraction. (II). Radiographic Ridge preservation with freeze-dried bone allo- tion following tooth extraction: a comparison
parameters. Journal of Clinical Periodontology graft and a collagen membrane compared to between atraumatic extraction and socket seal
21: 422–430. extraction alone for implant site development: a surgery. Quintessence International 41: 605–609.

16 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

Pelegrine, A.A., da Costa, C.E., Correa, M.E. & posterior maxilla reduces the need for sinus aug- Serino, G., Biancu, S., Iezzi, G. & Piattelli, A.
Marques, J.F. Jr (2010) Clinical and histomorpho- mentation. International Journal of Periodontics (2003) Ridge preservation following tooth extrac-
metric evaluation of extraction sockets treated & Restorative Dentistry 30: 265–273. tion using a polylactide and polyglycolide sponge
with an autologous bone marrow graft. Clinical Rodd, H.D., Malhotra, R., O’Brien, C.H., Elcock, C., as space filler: a clinical and histological study in
Oral Implants Research 21: 535–542. Davidson, L.E. & North, S. (2007) Change in sup- humans. Clinical Oral Implants Research 14:
Pietrokovski, J. (1967) Healing of the socket follow- porting tissue following loss of a permanent max- 651–658.
ing tooth extraction. Alpha Omegan 60: 126–129. illary incisor in children. Dental Traumatology Tallgren, A. (1972) The continuing reduction of
Pietrokovski, J. & Massler, M. (1967) Alveolar ridge 23: 328–332. the residual alveolar ridges in complete denture
resorption following tooth extraction. Journal of Saldanha, J.B., Casati, M.Z., Neto, F.H., Sallum, E. wearers: a mixed-longitudinal study covering
Prosthetic Dentistry 17: 21–27. A. & Nociti, F.H. Jr (2006) Smoking may affect 25 years. Journal of Prosthetic Dentistry 27: 120
Pietrokovski, J. & Massler, M. (1971) Residual ridge the alveolar process dimensions and radiographic –132.
remodeling after tooth extraction in monkeys. bone density in maxillary extraction sites: a pro- Van der Weijden, F., Dell’Acqua, F. & Slot, D.E.
Journal of Prosthetic Dentistry 26: 119–129. spective study in humans. Journal of Oral & (2009) Alveolar bone dimensional changes of
Pinho, M.N., Roriz, V.L., Novaes, A.B.Jr, Taba, M. Maxillofacial Surgery 64: 1359–1365. post-extraction sockets in humans: a systematic
Jr, Grisi, M.F., de Souza, S.L. & Palioto, D.B. Schropp, L., Wenzel, A., Kostopoulos, L. & Karring, review. Journal of Clinical Periodontology 36:
(2006) Titanium membranes in prevention of T. (2003) Bone healing and soft tissue contour 1048–1058.
alveolar collapse after tooth extraction. Implant changes following single-tooth extraction: a clini- Yilmaz, S., Efeoglu, E. & Kilic, A.R. (1998) Alveolar
Dentistry 15: 53–61. cal and radiographic 12-month prospective study. ridge reconstruction and/or preservation using
Rasperini, G., Canullo, L., Dellavia, C., Pellegrini, International Journal of Periodontics & Restor- root form bioglass cones. Journal of Clinical Peri-
G. & Simion, M. (2010) Socket grafting in the ative Dentistry 23: 313–323. odontology 25: 832–839.

List of included articles:


Aimetti, M., Romano, F., Griga, F.B. & Godio, L. Jones, A. & Nevins, M. (2005) Randomized study metric evaluation of extraction sockets treated
(2009) Clinical and histologic healing of human evaluating recombinant human bone morphoge- with an autologous bone marrow graft. Clinical
extraction sockets filled with calcium sulfate. netic protein-2 for extraction socket augmenta- Oral Implants Research 21: 535–542.
The International Journal of Oral & Maxillofa- tion. Journal of Periodontology 76: 605–613. Rasperini, G., Canullo, L., Dellavia, C., Pellegrini,
cial Implants 24: 902–929. Iasella, J.M., Greenwell, H., Miller, R.L., Hill, M., G. & Simion, M. (2010) Socket grafting in the
Barone, A., Aldini, N.N., Fini, M., Giardino, R., Drisko, C., Bohra, A.A. & Scheetz, J.P. (2003) posterior maxilla reduces the need for sinus aug-
Calvo Guirado, J.L. & Covani, U. (2008) Xenograft Ridge preservation with freeze-dried bone allo- mentation. International Journal of Periodontics
versus extraction alone for ridge preservation graft and a collagen membrane compared to & Restorative Dentistry 30: 265–273.
after tooth removal: a clinical and histomorpho- extraction alone for implant site development: a Rodd, H.D., Malhotra, R., O’Brien, C.H., Elcock, C.,
metric study. Journal of Periodontology 79: 1370– clinical and histologic study in humans. Journal Davidson, L.E. & North, S. (2007) Change in sup-
1377. of Periodontology 74: 990–999. porting tissue following loss of a permanent max-
Bragger, U., Schild, U. & Lang, N.P. (1994) Effect of Kerr, E.N., Mealey, B.L., Noujeim, M.E., Lasho, D. illary incisor in children. Dental Traumatology
chlorhexidine (0.12%) rinses on periodontal tissue J., Nummikoski, P.V. & Mellonig, J.T. (2008) The 23: 328–332.
healing after tooth extraction. (II). Radiographic effect of ultrasound on bone dimensional changes Saldanha, J.B., Casati, M.Z., Neto, F.H., Sallum, E.
parameters. Journal of Clinical Periodontology following extraction: a pilot study. Journal of A. & Nociti, F.H. Jr (2006) Smoking may affect
21: 422–430. Periodontology 79: 283–290. the alveolar process dimensions and radiographic
Camargo, P.M., Lekovic, V., Weinlaender, M., Klok- Lekovic, V., Camargo, P.M., Klokkevold, P.R., We- bone density in maxillary extraction sites: a pro-
kevold, P.R., Kenney, E.B., Dimitrijevic, B., inlaender, M., Kenney, E.B., Dimitrijevic, B. & spective study in humans. Journal of Oral &
Nadic, M., Jancovic, S. & Orsini, M. (2000) Influ- Nedic, M. (1998) Preservation of alveolar bone in Maxillofacial Surgery 64: 1359–1365.
ence of bioactive glass on changes in alveolar pro- extraction sockets using bioabsorbable mem- Schropp, L., Wenzel, A., Kostopoulos, L. & Karring,
cess dimensions after exodontia. Oral Surgery branes. Journal of Periodontology 69: 1044–1049. T. (2003) Bone healing and soft tissue contour
Oral Medicine Oral Pathology Oral Radiology & Lekovic, V., Kenney, E.B., Weinlaender, M., Han, T., changes following single-tooth extraction: a clini-
Endodontology 90: 581–586. Klokkevold, P., Nedic, M. & Orsini, M. (1997) A cal and radiographic 12-month prospective study.
Carlsson, G.E. & Persson, G. (1967) Morphologic bone regenerative approach to alveolar ridge main- International Journal of Periodontics & Restor-
changes of the mandible after extraction and tenance following tooth extraction. Report of 10 ative Dentistry 23: 313–323.
wearing of dentures. A longitudinal, clinical, and cases. Journal of Periodontology 68: 563–570. Serino, G., Biancu, S., Iezzi, G. & Piattelli, A.
x-ray cephalometric study covering 5 years. Od- Moya-Villaescusa, M.J. & Sanchez-Pérez, A. (2010) (2003) Ridge preservation following tooth extrac-
ontologisk Revy 18: 27–54. Measurement of ridge alterations following tooth tion using a polylactide and polyglycolide sponge
Crespi, R., Cappare, P. & Gherlone, E. (2009) Mag- removal: a radiographic study in humans. Clini- as space filler: a clinical and histological study in
nesium-enriched hydroxyapatite compared to cal- cal Oral Implants Research 21: 237–242. humans. Clinical Oral Implants Research 14:
cium sulfate in the healing of human extraction Oghli, A.A. & Steveling, H. (2010) Ridge preserva- 651–658.
sockets: radiographic and histomorphometric tion following tooth extraction: a comparison Yilmaz, S., Efeoglu, E. & Kilic, A.R. (1998) Alveolar
evaluation at 3 months. Journal of Periodontol- between atraumatic extraction and socket seal ridge reconstruction and/or preservation using
ogy 80: 210–218. surgery. Quintessence International 41: 605–609. root form bioglass cones. Journal of Clinical Peri-
Fiorellini, J.P., Howell, T.H., Cochran, D., Malm- Pelegrine, A.A., da Costa, C.E., Correa, M.E. & odontology 25: 832–839.
quist, J., Lilly, L.C., Spagnoli, D., Toljanic, J., Marques, J.F. Jr (2010) Clinical and histomorpho-

List of excluded full text articles and the reason for exclusion:
Agbaje, J.O., Jacobs, R., Michiels, K., Abu-Ta’a, M. study on a novel technique for volume assess- Exclusion criteria: reported parameters not
& van Steenberghe, D. (2009) Bone healing after ment of healing tooth sockets. Clinical Oral relevant or not useful.
dental extractions in irradiated patients: a pilot Investigations 13: 257–261.

© 2011 John Wiley & Sons A/S 17 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Ahn, J.J. & Shin, H.I. (2008) Bone tissue formation Exclusion criteria: no baseline data avail- vet monkey. The International Journal of Oral &
in extraction sockets from sites with advanced able for comparison, thus unable to arrive at Maxillofacial Surgery 17: 138–141.
periodontal disease: a histomorphometric study Exclusion criteria: no measurements of
an estimate of dimensional change over time.
in humans. The International Journal of Oral & alveolar dimensional changes (e.g. description
Araujo, M.G. & Lindhe, J. (2009b) Ridge preserva-
Maxillofacial Implants 23: 1133–1138.
tion with the use of bio-oss collagen: a 6-month of healing process or bony shape change, or
Exclusion criteria: no measurements of study in the dog. Clinical Oral Implants histology only).
alveolar dimensional changes (eg. description Research 20: 433–440. Boyne, P.J. (1995) Use of htr in tooth extraction
of healing process or bony shape change, or Exclusion criteria: sample did not include sockets to maintain alveolar ridge height and
histology only). untreated/undisturbed extraction sockets left increase concentration of alveolar bone matrix.
Alissa, R., Esposito, M., Horner, K. & Oliver, R. to heal spontaneously. General Dentistry 43: 470–473.
(2010) The influence of platelet-rich plasma on Araujo, M.G., Sukekava, F., Wennstrom, J.L. & Exclusion criteria: reported parameters not
the healing of extraction sockets: an explorative Lindhe, J. (2005) Ridge alterations following relevant or not useful.
randomised clinical trial. European Journal of implant placement in fresh extraction sockets: an Brandao, A.C., Brentegani, L.G., Novaes, A.B. Jr,
Oral Implantology 3: 121–134. experimental study in the dog. Journal of Clin Grisi, M.F., Souza, S.L., Taba Junior, M. & Salata,
Exclusion criteria: reported parameters not Periodontology 32: 645–652. L.A. (2002) Histomorphometric analysis of rat
relevant or not useful. Exclusion criteria: sample did not include alveolar wound healing with hydroxyapatite alone
Altundal, H. & Guvener, O. (2004) The effect of untreated/undisturbed extraction sockets left or associated to bmps. Brazilian Dental Journal
alendronate on resorption of the alveolar bone fol- 13: 147–154.
to heal spontaneously.
lowing tooth extraction. The International Jour- Exclusion criteria: reported parameters not
Ashman, A. & Bruins, P. (1985) Prevention of alveo-
nal of Oral & Maxillofacial Surgery 33: 286–293. relevant or not useful.
lar bone loss postextraction with htr grafting
Exclusion criteria: reported parameters not material. Oral Surgery Oral Medicine & Oral Cardaropoli, G., Araujo, M., Hayacibara, R., Sukek-
relevant or not useful. Pathology 60: 146–153. ava, F. & Lindhe, J. (2005) Healing of extraction
Alves-Rezende, M.C. & Okamoto, T. (1997) Effects Exclusion criteria: descriptive report on sockets and surgically produced – augmented and
of fibrin adhesive material (tissucol) on alveolar non-augmented – defects in the alveolar ridge. An
procedure/technique; commentary.
healing in rats under stress. Brazilian Dental experimental study in the dog.. Journal of Clini-
Ashman, A. & Bruins, P. (1987) Prevention of alveo-
Journal 8: 13–19. cal Periodontology 32: 435–440.
lar bone loss postextraction with htr polymer
Exclusion criteria: no measurements of grafting material. Journal of Oral Implantology Exclusion criteria: no measurements of
alveolar dimensional changes (eg. description 13: 270–281. alveolar dimensional changes (eg. description
of healing process or bony shape change, or Exclusion criteria: descriptive report on of healing process or bony shape change, or
histology only). procedure/technique; commentary. histology only).
Amemori, H. (1966) An experimental study of Bahat, O., Deeb, C., Golden, T. & Komarnyckij, O. Carlsson, G.E., Thilander, H. & Hedegard, B. (1967)
changes in the form of the mandible after extrac- (1987) Preservation of ridges utilizing hydroxyapa- Histologic changes in the upper alveolar process
tion of lower posterior teeth. I. The areal change tite. International Journal of Periodontics & after extractions with or without insertion of an
of mandibular frontal sections.. Bulletin of Tokyo Restorative Dentistry 7: 34–41. immediate full denture. Acta Odontolologica
Medical & Dental University 13: 59–74. Exclusion criteria: sample did not include Scandinavica 25: 21–43.
Exclusion criteria: study carried out on ani- untreated/undisturbed extraction sockets left Exclusion criteria: no measurements of
mals. to heal spontaneously. alveolar dimensional changes (eg. description
Anitua, E. (1999) Plasma rich in growth factors: pre- Bergstedt, H., Wictorin, L. & Lundquist, G. (1973) of healing process or bony shape change, or
liminary results of use in the preparation of Transplantation of bone treated with ethylenedia- histology only).
future sites for implants. The International Jour- mine into tooth sockets in immediate denture Carmagnola, D., Adriaens, P. & Berglundh, T.
nal of Oral & Maxillofacial Implants 14: 529– patients. Sven Tandlak Tidskr 66: 39–48. (2003) Healing of human extraction sockets filled
535.
Exclusion criteria: study subjects had with bio-oss. Clinical Oral Implants Research
Exclusion criteria: no measurements of 14: 137–143.
immediate dentures after extraction, hence
alveolar dimensional changes (eg. description Exclusion criteria: no measurements of
they did not have undisturbed healing post-
of healing process or bony shape change, or alveolar dimensional changes (eg. description
extraction.
histology only). Berkovitz, B.K. (1971) The healing process in the of healing process or bony shape change, or
Araujo, M., Linder, E., Wennstrom, J. & Lindhe, J. incisor tooth socket of the rat following root histology only).
(2008) The influence of bio-oss collagen on heal- resection and exfoliation. Archives of Oral Biol- Dayan, D., Bodner, L. & Horowitz, I. (1992) Effect
ing of an extraction socket: an experimental ogy 16: 1045–1054. of salivary gland hypofunction on the healing of
study in the dog. International Journal of Peri-
Exclusion criteria: no measurements of extraction wounds: a histomorphometric study in
odontics & Restorative Dentistry 28: 123–135. rats. Journal of Oral & Maxillofacial Surgery 50:
alveolar dimensional changes (eg. description
Exclusion criteria: reported parameters not 354–358.
of healing process or bony shape change, or
relevant or not useful. Exclusion criteria: no measurements of
histology only).
Araujo, M.G. & Lindhe, J. (2005) Dimensional ridge alveolar dimensional changes (eg. description
Bianchi, J., Fiorellini, J.P., Howell, T.H., Sekler, J.,
alterations following tooth extraction. An experi-
Curtin, H., Nevins, M.L. & Friedland, B. (2004) of healing process or bony shape change, or
mental study in the dog.. Journal of Clinical Peri-
Measuring the efficacy of rhbmp-2 to regenerate histology only).
odontology 32: 212–218.
bone: a radiographic study using a commercially Fickl, S., Zuhr, O., Wachtel, H., Bolz, W. & Huerz-
Exclusion criteria: only measured relative
available software program. International Journal eler, M. (2008b) Tissue alterations after tooth
difference in height between buccal and lin- of Periodontics & Restorative Dentistry 24: 579– extraction with and without surgical trauma: a
gual plates of the alveolus. 587. volumetric study in the beagle dog. Journal of
Araujo, M.G. & Lindhe, J. (2009a) Ridge alterations Exclusion criteria: reported parameters not Clinical Periodontology 35: 356–363.
following tooth extraction with and without flap Exclusion criteria: study carried out on ani-
relevant or not useful.
elevation: an experimental study in the dog. Clin-
Boyes-Varley, J.G., Cleaton-Jones, P.E. & Lownie, J. mals.
ical Oral Implants Research 20: 545–549.
F. (1988) Effect of a topical drug combination on Fickl, S., Zuhr, O., Wachtel, H., Stappert, C.F.,
the early healing of extraction sockets in the ver- Stein, J.M. & Hurzeler, M.B. (2008c) Dimensional

18 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

changes of the alveolar ridge contour after differ- wound healing in rats. Acta Odontologica Scan- socket healing in the rat. Archives of Oral Biol-
ent socket preservation techniques. Journal of dinavica 30: 511–522. ogy 18: 1283–1289.
Clinical Periodontology 35: 906–913. Exclusion criteria: no measurements of Exclusion criteria: no measurements of
Exclusion criteria: study carried out on ani- alveolar dimensional changes (eg. description alveolar dimensional changes (eg. description
mals. of healing process or bony shape change, or of healing process or bony shape change, or
Fickl, S., Zuhr, O., Wachtel, H., Bolz, W. & Huerz- histology only). histology only).
eler, M.B. (2008c) Hard tissue alterations after Horn, Y., Sela, M.N., Shlomi, B., Ulmansky, M. & Lindeboom, J.A., Tjiook, Y. & Kroon, F.H. (2006)
socket preservation: an experimental study in the Sela, J. (1979) Effect of irradiation-timing on the Immediate placement of implants in periapical
beagle dog. Clinical Oral Implants Research 19: initial socket healing in rats. International Jour- infected sites: a prospective randomized study in
1111–1118. nal of Oral Surgery 8: 457–461. 50 patients. Oral Surgery Oral Medicine Oral
Exclusion criteria: no baseline data avail- Exclusion criteria: no measurements of Pathology Oral Radiology & Endodontology 101:
able for comparison, thus unable to arrive at alveolar dimensional changes (eg. description 705–710.
an estimate of dimensional change over time. of healing process or bony shape change, or Exclusion criteria: sample did not include
Gauthier, O., Boix, D., Grimandi, G., Aguado, E., untreated/undisturbed extraction sockets left
histology only).
Bouler, J.M., Weiss, P. & Daculsi, G. (1999) A to heal spontaneously.
Hsieh, Y.D., Devlin, H. & McCord, F. (1995) The
new injectable calcium phosphate biomaterial for Loo, W.D. (1968) Ridge preservation with immedi-
effect of ovariectomy on the healing tooth socket
immediate bone filling of extraction sockets: a ate treatment dentures. Journal of Prosthetic
of the rat. Archives of Oral Biology 40: 529–531.
preliminary study in dogs. Journal of Periodontol- Dentistry 19: 5–11.
Exclusion criteria: no baseline data avail-
ogy 70: 375–383.
able for comparison, thus unable to arrive at Exclusion criteria: descriptive report on
Exclusion criteria: reported parameters not
an estimate of dimensional change over time. procedure/technique; commentary.
relevant or not useful. Luvizuto, E.R., Queiroz, T.P., Dias, S.M., Okamoto,
Huebsch, R.F. & Hansen, L.S. (1969) A histopatho-
Gorustovich, A., Veinsten, F., Costa, O.R. & Gug- T., Dornelles, R.C., Garcia, I.R. Jr & Okamoto, R.
logic study of extraction wounds in dogs. Oral
lielmotti, M.B. (2004) Histomorphometric evalua- (2010) Histomorphometric analysis and immunol-
Surgery Oral Medicine & Oral Pathology 28: 187
tion of the effect of bovine collagen granules on ocalization of rankl and opg during the alveolar
–196.
bone healing. An experimental study in rats. Acta healing process in female ovariectomized rats
Odontologica Latinoamericana 17: 9–13. Exclusion criteria: no measurements of
treated with oestrogen or raloxifene. Archives of
Exclusion criteria: reported parameters not alveolar dimensional changes (eg. description
Oral Biology 55: 52–59.
relevant or not useful. of healing process or bony shape change, or Exclusion criteria: no measurements of
Green, L.J., Gong, J.K. & Neiders, M.E. (1969) Rela- histology only). alveolar dimensional changes (eg. description
tionship between sr85 uptake and histological Iino, G., Nishimura, K., Omura, K. & Kasugai, S.
of healing process or bony shape change, or
changes during healing in dental extraction wounds (2008) Effects of prostaglandin e1 application on
rat incisal sockets. The International Journal of histology only).
in rats. Archives of Oral Biology 14: 865–872.
Oral & Maxillofacial Implants 23: 835–840. Magro Filho, O. & de Carvalho, A.C. (1990) Appli-
Exclusion criteria: no measurements of
cation of propolis to dental sockets and skin
alveolar dimensional changes (eg. description Exclusion criteria: reported parameters not
wounds. Journal of Nihon University School of
of healing process or bony shape change, or relevant or not useful.
Dentistry 32: 4–13.
Iizuka, T., Miller, S.C. & Marks, S.C. Jr (1992)
histology only). Exclusion criteria: no measurements of
Alveolar bone remodeling after tooth extraction
Guglielmotti, M.B. & Cabrini, R.L. (1985) Alveolar alveolar dimensional changes (eg. description
in normal and osteopetrotic (ia) rats. Journal of
wound healing and ridge remodeling after tooth
Oral Pathology & Medicine 21: 150–155. of healing process or bony shape change, or
extraction in the rat: a histologic, radiographic,
Exclusion criteria: sample did not include histology only).
and histometric study. Journal of Oral & Maxil-
untreated/undisturbed extraction sockets left Magro-Ernica, N., Magro-Filho, O. & Rangel-Garcia,
lofacial Surgery 43: 359–364.
I. (2003) Histologic study of use of microfibrillar
Exclusion criteria: reported parameters not to heal spontaneously.
collagen hemostat in rat dental sockets. Brazilian
relevant or not useful. Indovina, A. Jr & Block, M.S. (2002) Comparison of 3
Dental Journal 14: 12–15.
Guglielmotti, M.B., Ubios, A.M. & Cabrini, R.L. bone substitutes in canine extraction sites. Journal
of Oral & Maxillofacial Surgery 60: 53–58. Exclusion criteria: reported parameters not
(1985) Alveolar wound healing alteration under
Exclusion criteria: reported parameters not relevant or not useful.
uranyl nitrate intoxication. Journal of Oral
Mathai, J.K., Chandra, S., Nair, K.V. & Nambiar, K.
Pathology 14: 565–572. relevant or not useful.
K. (1989) Tricalcium phosphate ceramic as imme-
Exclusion criteria: reported parameters not Kangvonkit, P., Matukas, V.J. & Castleberry, D.J.
diate root implants for the maintenance of alveo-
relevant or not useful. (1986) Clinical evaluation of durapatite sub-
lar bone in partially edentulous mandibular jaws.
Guglielmotti, M.B., Ubios, A.M. & Cabrini, R.L. merged-root implants for alveolar bone preserva-
A clinical study. Australian Dental Journal 34:
(1986) Alveolar wound healing after x-irradiation: tion. The International Journal of Oral &
421–426.
a histologic, radiographic, and histometric study. Maxillofacial Surgery 15: 62–71.
Exclusion criteria: reported parameters not
Journal of Oral & Maxillofacial Surgery 44: 972– Exclusion criteria: study subjects had
relevant or not useful.
976. immediate dentures after extraction, hence
Matsumoto, M. (1968) Changes in residual ridge of
Exclusion criteria: no baseline data avail- they did not have undisturbed healing post-
the mandible after extraction and wearing exten-
able for comparison, thus unable to arrive at extraction. sion saddle type of removable partial dentures. (a
an estimate of dimensional change over time. Lavelle, C.L. (1985) Preliminary study of mandibu- longitudinal, clinical and roentgenographic inves-
Hahn, E., Sonis, S., Gallagher, G. & Atwood, D. lar shape after tooth loss. Journal of Prosthetic tigation). Bulletin of Tokyo Medical & Dental
(1988) Preservation of the alveolar ridge with Dentistry 53: 726–730. University 15: 67–89.
hydroxyapatite-collagen implants in rats. Journal Exclusion criteria: no measurements of Exclusion criteria: length of observation
of Prosthetic Dentistry 60: 729–734. alveolar dimensional changes (eg. description period not reported.
Exclusion criteria: study carried out on ani- of healing process or bony shape change, or Michael, C.G. & Barsoum, W.M. (1976) Comparing
mals. histology only). ridge resorption with various surgical techniques
Hars, E. & Massler, M. (1972) Effects of fluorides, Librus, H., Pietrokovski, J., Ulmanski, M. & Geda- in immediate dentures. Journal of Prosthetic
cortico-steroids and tetracyclines on extraction lia, I. (1973) The effect of fluoride on molar Dentisty 35: 142–155.

© 2011 John Wiley & Sons A/S 19 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Tan et al ! Dimensional tissue changes post extraction

Exclusion criteria: study subjects had Exclusion criteria: study carried out on ani- tite root implants. Oral Surgery Oral Medicine &
immediate dentures after extraction, hence mals. Oral Pathology 58: 511–521.
they did not have undisturbed healing post- Ortega, K.L., Rezende, N.P., Araujo, N.S. & Ma- Exclusion criteria: no measurements of
extraction. galhaes, M.H. (2007) Effect of a topical antimicro- alveolar dimensional changes (eg. description
Minsk, L. (2005) Extraction-site ridge preservation. bial paste on healing after extraction of molars in of healing process or bony shape change, or
Compendium of Continuing Education in Den- hiv positive patients: randomised controlled clini- histology only).
tistry 26: 272. cal trial. British Journal of Oral & Maxillofacial Richardson, A. (1965) The pattern of alveolar bone
Surgery 45: 27–29.
Exclusion criteria: descriptive report on resorption following extraction of anterior teeth.
Exclusion criteria: reported parameters not Dental Practitioner & Dental Record 16: 77–80.
procedure/technique; commentary.
Mizutani, H. & Ishihata, N. (1976) Decrease and relevant or not useful. Exclusion criteria: reported parameters not
increase in residual ridges after extraction of Pessoa, R.S., Oliveira, S.R., Menezes, H.H. & de relevant or not useful.
teeth in monkeys (part I). Bulletin of Tokyo Med- Magalhaes, D. (2009) Effects of platelet-rich Rothamel, D., Schwarz, F., Herten, M., Engelhardt,
ical & Dental University 23: 157–168. plasma on healing of alveolar socket: split-mouth E., Donath, K., Kuehn, P. & Becker, J. (2008)
histological and histometric evaluation in cebus
Exclusion criteria: study carried out on ani- Dimensional ridge alterations following socket
apella monkeys. Indian Journal of Dental preservation using a nanocrystalline hydroxyapa-
mals.
Research 20: 442–447. tite paste: a histomorphometrical study in dogs.
Nevins, M., Camelo, M., De Paoli, S., Friedland, B.,
Exclusion criteria: no baseline data avail- The International Journal of Oral & Maxillofa-
Schenk, R.K., Parma-Benfenati, S., Simion, M.,
Tinti, C. & Wagenberg, B. (2006) A study of the able for comparison, thus unable to arrive at cial Surgery 37: 741–747.
fate of the buccal wall of extraction sockets of an estimate of dimensional change over time. Exclusion criteria: no baseline data avail-
teeth with prominent roots. International Journal Pietrokovski, J. (1967) Healing of the socket able for comparison, thus unable to arrive at
of Periodontics & Restorative Dentistry 26: 19– following tooth extraction. Alpha Omegan 60: an estimate of dimensional change over time.
29. 126–129. Sattayasanskul, W., Brook, I.M. & Lamb, D.J. (1988)
Exclusion criteria: reported parameters not Exclusion criteria: no measurements of Dense hydroxyapatite root replica implantation:
relevant or not useful. alveolar dimensional changes (eg. description measurement of mandibular ridge preservation.
Nevins, M.L., Camelo, M., Schupbach, P., Kim, D. of healing process or bony shape change, or The International Journal of Oral & Maxillofa-
M., Camelo, J.M. & Nevins, M. (2009) Human his- histology only). cial Implants 3: 203–207.
tologic evaluation of mineralized collagen bone Pietrokovski, J. & Massler, M. (1967a) Alveolar Exclusion criteria: study subjects had
substitute and recombinant platelet-derived ridge resorption following tooth extraction. Jour- immediate dentures after extraction, hence
growth factor-bb to create bone for implant place- nal of Prosthetic Dentistry 17: 21–27. they did not have undisturbed healing post-
ment in extraction socket defects at 4 and Exclusion criteria: length of observation extraction.
6 months: a case series. International Journal of
period not reported. Scheer, P. & Boyne, P.J. (1987) Maintenance of alve-
Periodontics & Restorative Dentistry 29: 129–139.
Pietrokovski, J. & Massler, M. (1967b) Ridge remod- olar bone through implantation of bone graft sub-
Exclusion criteria: sample did not include eling after tooth extraction in rats. Journal of stitutes in tooth extraction sockets. Journal of
untreated/undisturbed extraction sockets left Dental Research 46: 222–231. the American Dental Association 114: 594–597.
to heal spontaneously. Exclusion criteria: no measurements of Exclusion criteria: descriptive report on
Normando, A.D., Maia, F.A., Ursi, W.J. & Simone, alveolar dimensional changes (eg. description procedure/technique; commentary.
J.L. (2010) Dentoalveolar changes after unilateral
of healing process or bony shape change, or Sclar, A.G. (1999) Preserving alveolar ridge anatomy
extractions of mandibular first molars and their following tooth removal in conjunction with
histology only).
influence on third molar development and posi- immediate implant placement. The bio-col tech-
Pietrokovski, J. & Massler, M. (1971) Residual ridge
tion. World Journal of Orthodontics 11: 55–60. nique. Atlas of the Oral & Maxillofacial Surgery
remodeling after tooth extraction in monkeys.
Exclusion criteria: reported parameters not Clinics of North America 7: 39–59.
Journal of Prosthetic Dentistry 26: 119–129.
relevant or not useful. Exclusion criteria: descriptive report on
Exclusion criteria: no measurements of
Olson, H.M. & Hagen, A. (1982) Inhibition of post- procedure/technique; commentary.
alveolar dimensional changes (eg. description
extraction alveolar ridge resorption in rats by di- Serino, G., Rao, W., Iezzi, G. & Piattelli, A. (2008)
chloromethane diphosphonate. Journal of Peri- of healing process or bony shape change, or
Polylactide and polyglycolide sponge used in
odontal Research 17: 669–674. histology only).
human extraction sockets: bone formation fol-
Exclusion criteria: study carried out on ani- Pinto, J.R., Bosco, A.F., Okamoto, T., Guerra, J.B. &
lowing 3 months after its application. Clinical
Piza, I.G. (2002) Effects of nicotine on the healing
mals. Oral Implants Research 19: 26–31.
of extraction sockets in rats. A histological study.
Olson, R.A., Roberts, D.L. & Osbon, D.B. (1982) A Exclusion criteria: no measurements of
Brazilian Dental Journal 13: 3–9.
comparative study of polylactic acid, gelfoam, alveolar dimensional changes (eg. description
and surgicel in healing extraction sites. Oral Sur- Exclusion criteria: no measurements of
of healing process or bony shape change, or
gery Oral Medicine & Oral Pathology 53: 441– alveolar dimensional changes (eg. description
histology only).
449. of healing process or bony shape change, or
Sharan, A. & Madjar, D. (2008) Maxillary sinus
Exclusion criteria: no measurements of histology only).
pneumatization following extractions: a radio-
alveolar dimensional changes (eg. description Puia, S.A., Renou, S.J., Rey, E.A., Guglielmotti, M.
graphic study. The International Journal of Oral
of healing process or bony shape change, or B. & Bozzini, C.E. (2009) Effect of bismuth sub-
& Maxillofacial Implants 23: 48–56.
gallate (a hemostatic agent) on bone repair; a his-
histology only). Exclusion criteria: no measurements of
tologic, radiographic and histomorphometric
Oltramari, P.V., Navarro Rde, L., Henriques, J.F., alveolar dimensional changes (eg. description
study in rats. The International Journal of Oral
Taga, R., Cestari, T.M., Janson, G. & Granjeiro, J.
& Maxillofacial Surgery 38: 785–789. of healing process or bony shape change, or
M. (2007) Evaluation of bone height and bone
density after tooth extraction: an experimental Exclusion criteria: reported parameters not histology only).
relevant or not useful. Shi, B., Zhou, Y., Wang, Y.N. & Cheng, X.R. (2007)
study in minipigs. Oral Surgery Oral Medicine
Quinn, J.H. & Kent, J.N. (1984) Alveolar ridge Alveolar ridge preservation prior to implant place-
Oral Pathology Oral Radiology & Endodontology
maintenance with solid nonporous hydroxylapa- ment with surgical-grade calcium sulfate and
104: 9–16.
platelet-rich plasma: a pilot study in a canine

20 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21 © 2011 John Wiley & Sons A/S
Tan et al ! Dimensional tissue changes post extraction

model. The International Journal of Oral & Max- Teofilo, J.M., Leonel, D.V. & Lamano, T. (2010) Exclusion criteria: reported parameters not
illofacial Implants 22: 656–665. Cola beverage consumption delays alveolar bone relevant or not useful.
Exclusion criteria: study carried out on ani- healing: a histometric study in rats. Brazilian Wu, Z., Liu, C., Zang, G. & Sun, H. (2008) The
mals. Oral Research 24: 177–181. effect of simvastatin on remodelling of the alveo-
Smith, N. (1974) A comparative histological and Exclusion criteria: no measurements of lar bone following tooth extraction. The Interna-
radiographic study of extraction socket healing in alveolar dimensional changes (eg. description tional Journal of Oral & Maxillofacial Surgery
the rat. Australian Dental Journal 19: 250–254. of healing process or bony shape change, or 37: 170–176.
Exclusion criteria: no measurements of histology only). Exclusion criteria: sample did not include
alveolar dimensional changes (eg. description Thilander, H. & Astrand, P. (1973) The effect of tet- untreated/undisturbed extraction sockets left
of healing process or bony shape change, or racyclines on socket healing. Acta Odontologica to heal spontaneously.
histology only). Scandinavica 31: 131–139. Yugoshi, L.I., Sala, M.A., Brentegani, L.G. & Lama-
Teofilo, J.M., Brentegani, L.G. & Carvalho, T.L. Exclusion criteria: no measurements of no Carvalho, T.L. (2002) Histometric study of
(2001) A histometric study in rats of the effect of alveolar dimensional changes (eg. description socket healing after tooth extraction in rats trea-
the calcium antagonist amlodipine on bone heal- of healing process or bony shape change, or ted with diclofenac. Brazilian Dental Journal 13:
ing after tooth extraction. Archives of Oral Biol- 92–96.
histology only).
ogy 46: 375–379. Ubios, A.M., Jares Furno, G. & Guglielmotti, M.B.
Exclusion criteria: sample did not include
Exclusion criteria: reported parameters not (1991) Effect of calcitonin on alveolar wound untreated/undisturbed extraction sockets left
relevant or not useful. healing. Journal of Oral Pathology & Medicine to heal spontaneously.
20: 322–324.

© 2011 John Wiley & Sons A/S 21 | Clin. Oral. Impl. Res. 23(Suppl. 5), 2012/1–21
Copyright of Clinical Oral Implants Research is the property of Wiley-Blackwell and its content may not be
copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written
permission. However, users may print, download, or email articles for individual use.
Osteology Consensus Report
Christoph H.F. Hämmerle Evidence-based knowledge on the
Mauricio G. Araujo
Massimo Simion
biology and treatment of extraction
Mauricio G. Araujo sockets

Authors’ affiliations: Key words: bone regeneration, clinical research, clinical trials, guided tissue regeneration,
Christoph H.F. Hämmerle, Center of Dental wound healing
Medicine, Clinic of Fixed and Removable
Prosthodontics and Dental Material Science,
University of Zurich, Zurich, Switzerland Abstract
Mauricio G. Araujo, Department of Dentistry, State
University of Maringá, Parana, Brazil
Objectives: The fresh extraction socket in the alveolar ridge represents a special challenge in
Massimo Simion, Departmet of Periodontology, everyday clinical practice. Maintenance of the hard and soft tissue envelope and a stable ridge
IRCCS Cà Granda Foundation – Ospedale Maggiore volume were considered important aims to allow simplifying subsequent treatments and
Policlinico, Department of Reconstructive, Surgical
and Diagnostic Science, University of Milan, optimizing their outcomes in particular, when implants are planned to be placed.
Department of Periodonology, College of Dentistry, Material and Methods: : Prior to the consensus meeting four comprehensive systematic reviews
King Saud University, Riyadh, Saudi Arabia were written on two topics regarding ridge alteration and ridge preservation following tooth
Mauricio G. Araujo, Department of Dentistry, State
University of Maringá, Parana, Brazil extraction and implant placement following tooth extraction. During the conference these
manuscripts were discussed and accepted thereafter. Finally, consensus statements and
Corresponding author: recommendations were formulated.
Mauricio G. Araujo
Department of Dentistry Results: : The systematic reviews demonstrated that the alveolar ridge undergoes a mean
State University of Maringá horizontal reduction in width of 3.8 mm and a mean vertical reduction in height of 1.24 mm
Parana, Brazil
within 6 months after tooth extraction. The techniques aimed at ridge preservation encompassed
Tel.: +41 44 634 32 51
Fax: +41 44 634 43 05 two different approaches: i) maintaining the ridge profile, ii) enlarging the ridge profile.
e-mail: christoph.hammerle@zzm.uzh.ch Regarding timing of implant placement the literature showed that immediate implant placement
leads to high implant survival rates. This procedure is primarily recommended in premolar sites
Conflicts of interest with low esthetic importance and favorable anatomy. In the esthetic zone, however, a high risk for
The authors declare no conflicts of interest. mucosal recession was reported. Hence, it should only be used in stringently selected situations
with lower risks and only by experienced clinicians. In molar sites a high need for soft and hard
tissue augmentation was identified.
Conclusions: : Future research should clearly identify the clinical and patient benefits resulting
from ridge preservation compared with traditional procedures. In addition, future research should
also aim at better identifying parameters critical for positive treatment outcomes with immediate
implants. The result of this procedure should be compared to early and late implant placement.

The fresh extraction socket in the alveolar the ridge following tooth extraction. Further-
ridge represents a special challenge in every- more, this consensus analyzed the clinical
day clinical practice. Regardless of the subse- outcomes of implant placement into sockets
quent treatment maintenance of the ridge at different time spans following tooth
contour will frequently facilitate all further extraction.
*Osteology Consensus Group 2011: Mauricio G. Araújo, steps of therapy. This is particularly true for
Maringa, Parana, Brazil; Dieter Bosshardt, Daniel Buser,
Berne, Switzerland; William V. Giannobile, Ann Arbor,
treatments involving the placement and
Michighan, USA; Reinhard Gruber, Vienna, Austria; Chr- reconstruction of dental implants. It has been Workshop discussion and
istoph H.F. Hämmerle, Ronald E. Jung, Zürich, Switzer-
land; Niklaus P. Lang, Hong Kong SAR PRC; Myron demonstrated in numerous animal and clini- consensus
Nevins, Boston, Massachusetts, USA; Friedrich Neukam, cal studies in humans that following tooth
Nuremberg, Germany; Mariano Sanz, Madrid, Spain;
Massimo Simion, Milano, Italy; Georg Watzek, Vienna, extraction undisturbed wound healing will The group discussing the evidence and gener-
Austria lead to loss of ridge volume and change in ating the consensus statements consisted of
Date: ridge shape. individuals competent in different disciplines
Accepted 8 October 2011 The aim of the present consensus report of medical dentistry with a special emphasis
To cite this article: was to critically evaluate the scientific evi- on implant therapy. Prior to the consensus
CHF Hämmerle, Araújo MG, Simion M, On Behalf of the
Osteology Consensus Group 2011. Evidence-based knowledge
dence regarding ridge alterations following meeting, two groups of researchers wrote
on the biology and treatment of extraction sockets. tooth extraction and to assess the effects of comprehensive systematic reviews on two
Clin. Oral Impl. Res. 23(Suppl. 5), 2012, 80–82
doi: 10.1111/j.1600-0501.2011.02370.x treatment strategies aiming at preservation of topics each regarding ridge alterations and

© 2011 John Wiley & Sons A/S 80


Hämmerle et al ! Evidence for treatment of extraction sockets

ridge preservation following tooth extraction (i) Generation of a good soft tissue volume Regarding indication other than the ones
and implant placement following tooth for the time of implant placement thus mentioned above, there is little or no evi-
extraction. simplifying implantation procedures at dence.
During the conference, the reviewers first earlier time points.
presented their manuscripts explaining how (ii) Generation of a good hard tissue volume Clinical recommendations regarding ridge
the literature search was conducted, how the for the time of implant placement thus preservation
In general, the group made the following clin-
data were extracted, analyzed, which results simplifying implantation procedures at
ical recommendations:
were found and which conclusions could be later time points.
drawn. The entire group then discussed these
No high level evidence was found in the • Raising of a flap and placement of bioma-
reports. Thereafter, all four manuscripts were terials (biomaterial for ridge contouring
literature regarding contraindications specific
accepted. Another thorough discussion fol- and/or barrier membrane).
for ridge preservation. Hence, the group made
lowed on published data on lower levels of
the following consensus. • Primary would closure.
evidence than the one included in the manu-
Contraindication for ridge preservation was • Materials with a low resorption and
scripts and its impact on the conclusions to replacement rate.
considered to encompass:
be drawn. Finally, the group formulated con- • Raising of flaps and placement of a
sensus statements and recommendations for • General contraindication against oral sur- device/devices for contouring the ridge
clinical practice and for future research. gical interventions. profile.
Furthermore: Regarding the different materials applied in
clinical studies the systematic review did not
Ridge preservation
• Infections at the site planned for ridge
show significant differences between the var-
preservation, which cannot be taken care
ious materials, (i.e., filler, membranes) except
of during the ridge preservation surgery.
for the collagen plug alone, which revealed
Definition of terms
The group considered it important to define
• Patients radiated in the area planned for
negative results.
ridge preservation.
terms regarding the various procedures, Although primary wound closure was gen-
which previously had been described in the
• Patients taking bisphosphonates.
erally considered an important factor for suc-
literature under the general term of “ridge Various techniques have been described in cess, the literature did not allow a
preservation.” It was obvious that a distinc- the literature for so called ridge preserva- meaningful comparison of different tech-
tion needed to be made as described below. tion. These techniques may be categorized niques for primary wound closure (soft tissue
Ridge preservation = preserving the ridge into two different groups: (i) techniques aim- punch, connective tissue graft, barrier mem-
volume within the envelope existing at the ing at maintaining the ridge profile (ridge brane, soft tissue replacement matrix).
time of extraction preservation), (ii) techniques aiming at
Ridge augmentation = increasing the ridge enlarging the ridge profile (ridge augmenta-
tion). Future research regarding ridge preservation
volume beyond the skeletal envelope existing
Regarding future research the consensus sta-
at the time of extraction To enlarge the ridge profile flaps have
ted the following:
generally been raised and augmentation pro-
Consensus statements regarding ridge cedures using biomaterials for ridge contour- • Focus on patient centered outcomes.
preservation
The systematic review by Lang et al. (2012)
ing with or without barrier membranes • Focus on clinical short-, medium-, and
have been performed. It appears that pri- long-term outcomes including biological,
demonstrated that based on clinical studies
mary closure of the wound is beneficial technical, phonetic, and esthetic parame-
the alveolar ridge undergoes the following
regarding the volume gained applying this ters.
dimensional changes within 6 months after
tooth extraction:
approach. • Studies regarding possible benefits during
These indications were identified for ridge subsequent implant therapy encompass-
• Mean horizontal reduction in ridge width: preservation: ing:
3.8 mm.
• Implant placement is planned at a time (i) Assessing the need for further hard and
• Mean vertical reduction in ridge height: point later than tooth extraction i.e., soft tissue augmentation
1.24 mm.
(ii) Assessing the amount of further hard
(i) When immediate or early implanta-
Based on the systematic review by Vigno- and soft tissue augmentation.
tion is not recommendable
letti et al. (2012) the group concluded that (iii) Assessing esthetic outcomes.
(ii) When patients are not available for
the reasons for ridge preservation included:
the immediate or early implant • Conditions of the soft tissues, i.e., dis-
• Maintenance of the existing soft and hard placement (pregnancy, holidays, …) placement of the muco-gingival junction,
tissue envelope. (iii) When primary stability of an color of the ridge mucosa, amount of ker-
• Maintenance of a stable ridge volume for implant cannot be obtained atinized mucosa.
optimizing functional and esthetic out- (iv) In adolescent people • Techniques for soft tissue management, i.
comes.
• Contouring of the ridge for conventional

e., raising of flaps yes/no.
• Simplification of treatment procedures prosthetic treatment.
Method for soft tissue closure.
subsequent to the ridge preservation
• Provided the cost/benefit ratio is positive. • Influence of the hard and soft tissue anat-

• Reducing the need for elevation of the


omy following tooth extraction: presence
or absence of bony socket walls, thick-
sinus floor.

© 2011 John Wiley & Sons A/S 81 | Clin. Oral Impl. Res. 23(Suppl. 5), 2012/80–82
Hämmerle et al ! Evidence for treatment of extraction sockets

ness of the bony socket walls, soft tissue • Several risk factors for the development In areas of esthetic priority implant installa-
area, volume, color, scars. of mucosal recession have been identified: tion into the fresh extraction socket (Type I
• Effect of various biomaterials applied for (i) Smoking placement) is not recommended.
ridge contouring. (ii) Presence of a thin buccal bone plate Several published prospective case series
• Effect of various biomaterials applied as (i.e., <1 mm thick) not included in the present systematic review
barrier membranes. (iii) Presence of a thin soft tissue biotype using the early implant placement protocol
• Methodological studies on the optimal (iv) Facial implant position have reported intermediate to long-term
type of measurements to assess the out- excellent esthetic results (Belser et al. 2009;
come of treatment regarding soft tissue • Augmentation of soft and hard tissues is Buser et al. 2011). These results lend addi-
and hard tissues. frequently necessary. tional support to the recommendation of type
• Development of consistent reference • The procedure of immediate implant place- II instead of type I implant placement follow-
points for 3D imaging technologies, when ment into extraction sockets should be ing tooth extraction in esthetic sites.
studying changes in ridge morphology used very restrictively in the esthetic area.
regarding soft and/or hard tissues. Limited to posterior sites the systematic
Future research regarding timing for implant
• Studies on the normal anatomy regarding review by Lau et al. 2012 lead to the follow-
placement
These recommendations are valid for both
bone and soft tissue thickness and types ing conclusions: anterior and posterior sites.
in different regions of the jaws.
• Studies on the effects of different extrac- • For single tooth implants high survival
• Reporting of frequency analyses of com-
tion techniques on subsequent healing. and low complication rates have been plication should become standard.
• Identify the most appropriate control reported.
• Studies addressing immediate implanta-
group for pre-clinical and clinical studies. • Molar sites present situations with lim- tion in the absence of risk factors.
ited indications due to anatomical rea-
sons.
• Comparison of surgical approaches with
and without the elevation of flaps.
Timing for implant placement • When immediate implants are placed in
• Comparison of surgical approaches with
molar sites, soft and hard tissue augmen- and without filler materials in the gap
Two systematic reviews were available (Lau tation is frequently necessary. between the buccal aspect of the implant
et al. 2012; Sanz et al. 2012) regarding timing • Premolars represent the sites with the and the buccal bone wall.
of implant placement into extraction sockets. most favorable indication due to the nor-
mally favorable anatomical situation and
• Assess the influence of the distance of
Both reviews focused on the highest level of the implant to the buccal bone wall on
scientific evidence and were conducted with the generally low esthetic demands. bone formation.
reasonable and clearly defined inclusion and The treatments of fully edentulous jaws • Comparison of different filler materials in
exclusion criteria. and of multiple extraction sites have not different clinical situations.
been duly addressed in the literature. • Comparison of type 1 (immediate) and
Consensus statements regarding timing for type 2 (early) implant placement in low
implant placement
Clinical recommendations regarding timing for risk situations.
Limited to esthetic sites the systematic
reviews lead to following conclusions:
implant placement
As based on the literature the group con-
• Comparison of type 2 (early) and type 3
(delayed) implant placement.
cluded that in situations, where no risk fac-
• Immediate implant placement leads to
tors are present (situations rarely occurring),
• Identify the ideal clinical protocols and
high implant survival rates. the best biomaterials for type 1, type 2,
this procedure may be recommended for
• Immediate implant placement is associ-
experienced clinicians.
and type 3 implant placement.
ated with a high risk for mucosal recession.
Immediate implant placement is primarily
• Changes in the contours of the ridge over
A wide range regarding the amount of extended periods of time.
recommended in premolar sites with low
recessions is reported in the literature.
esthetic importance and favorable anatomy.

References
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M., Weber, H.-P. & Buser, D. (2009) Outcome early implant placement postextraction. Journal Implants Research 23(Suppl. 5): 67–79.
evaluation of early placed maxillary anterior sin- of Periodontology 82: 342–349. Tan, W.L., Wong, T.W.L., Wong, M.C.M. & Lang,
gle-tooth implants using objective esthetic crite- Lang, N.P., Pun, B.L., Lau, I.K.Y., Li, K.Y. & Wong, N.P. (2012) A systematic review of post-extract-
ria: a cross-sectional, retrospective study in 45 M.C.M. (2012) A systematic review on survival ional alveolar bone dimensional changes in
patients with a 2- to 4-year follow-up using pink and success rates of implants placed immediately humans. Clinical Oral Implants Research 23
and white esthetic scores. Journal of Periodontol- into fresh extraction sockets after at least one (Suppl. 5): 1–21.
ogy 80: 140–151. year. Clinical Oral Implants Research 23(Suppl. Vignoletti, F., Matesanz, P., Rodrigo, D., Figuero,
Buser, D., Wittneben, J., Bornstein, M.M., Grütter, 5): 39–66. E., Martin, C. & Sanz, M. (2012) Surgical proto-
L., Chappuis, V. & Belser, U.C. (2011) Stability of Sanz, I., Garcia-Gargallo, M., Herrara, D., Martin, cols for ridge preservation after tooth extraction.
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82 | Clin. Oral Impl. Res. 23(Suppl. 5), 2012/80–82 © 2011 John Wiley & Sons A/S
Copyright of Clinical Oral Implants Research is the property of Wiley-Blackwell and its content may not be
copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written
permission. However, users may print, download, or email articles for individual use.
The International Journal of Periodontics & Restorative Dentistry
71

Ridge Preservation With and


Without Primary Wound Closure:
A Case Series

David M. Kim, DDS, DMSc1/Nicola De Angelis, DDS2/Marcelo Camelo, DDS3 Tooth extraction may lead to dif-
Marc L. Nevins, DMD, MMSc4/Peter Schupbach, PhD5/Myron Nevins, DDS6 ferent patterns of bone resorption,
apposition, and remodeling that
The purpose of this study was to determine the clinical and histologic efficacy make it difficult to predict the fi-
of the combination of alloplastic biphasic calcium phosphate composed of 30%
nal ridge contour and dimension.
hydroxyapatite and 70% β–tricalcium phosphate (Osteon II) and a cross-linked
collagen membrane used to reconstruct an extraction socket with new bone The clinician’s decision to augment
formation. Twelve patients, from two private dental practices, requiring extraction of extraction sockets is important be-
maxillary and mandibular nonmolar teeth (n = 30) received both Osteon II (0.5- to cause ungrafted extraction sockets
1.0-mm particle size) and the collagen membrane. The primary healing intention may undergo progressive bone
group (group A, n = 12) received primary flap closure over the membrane, while resorption without intervention.1–3
in the secondary healing intention group (group B, n = 18), the membrane was left
Complete bone regeneration to
exposed. Early wound healing seemed to be slower in group B when compared
to group A, but the difference was not noticeable after 4 weeks. Clinical reentry the pre-extraction crestal bone
revealed that the dimensions of the ridge appeared to be maintained in both level is not always possible, regard-
groups, and internal socket bone fill was evident. The grafted area appeared less of grafting materials or the use
to be well vascularized, but clinically visible graft particles were noted in some of barrier membranes.2–4
cases. Light microscopic analysis revealed the formation of new bone directly Autogenous bone has been
apposing the surfaces of graft particles and bridging the space between them,
considered the gold standard for
indicating that the graft material behaved as an osteoconductive scaffold. The
mean amount of vital bone in group A was 40.3% ± 7.8%, while the remaining bone grafting, but the morbidity
graft was 6.0% ± 4.0%. The mean amount of vital bone in group B was 47.3% ± and complications associated with
11.3%, while the remaining graft was 18.0% ± 20.0%. The absence of primary harvesting have provided a reason
flap closure did not affect the percentage of vital bone formation or residual graft. to consider alternatives. Alloplas-
(Int J Periodontics Restorative Dent 2013;33:71–78. doi: 10.11607/prd.1463) tic biomaterials such as hydroxy-
1Assistant Professor, Division of Periodontology, Department of Oral Medicine, Infection
apatite (HA) and β–tricalcium
and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USA. phosphate (β-TCP) are promising
2Assistant Professor, University of Genoa, Genoa, Italy.
bone substitutes because of their
3Institute for Advanced Dental Studies, Belo Horizonte, Brazil.

4Assistant Clinical Professor, Division of Periodontology, Department of Oral Medicine, Infection unlimited supply, but a lack of evi-
and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USA. dence and inconsistent clinical re-
5Schupbach Ltd, Service and Research for Histology, Microscopy and Imaging, Horgen, Switzerland.
ports have made clinicians weary
6Associate Clinical Professor, Division of Periodontology, Department of Oral Medicine, Infection

and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USA.


of their use.5–8
A barrier membrane is com-
Correspondence to: Dr David M. Kim, Harvard School of Dental Medicine, 188 Longwood Ave, monly used in conjunction with a
Boston, MA 02115, USA; fax: 617-432-1897; email: dkim@hsdm.harvard.edu.
bone graft to maintain space and
©2013 by Quintessence Publishing Co Inc. foster selective osteogenic cells

Volume 33, Number 1, 2013


72

Fig 1 The patient presented with a failed root canal treatment Fig 2 Atraumatic extraction was performed to preserve the buccal
and recurrent caries beneath the crown margins on the maxillary plate, and both sockets were grafted with Osteon II.
left canine and second premolar. Implants were selected to replace
the two teeth.

to populate the defect while ex- tentional exposure of the collagen evaluations (periapical radiographs
cluding epithelial cells and fibro- membrane was investigated. and computed tomography [CT]
blasts.9 Resorbable membranes scans) were performed.
are accompanied by fewer adverse The surgical procedure was
events than nonresorbable mem- Method and materials performed under local anesthe-
branes when exposed because sia (2% xylocaine with 1:100,000
they degrade naturally.10,11 Ex- Twelve patients (2 men, 10 women; epinephrine). An intrasulcular inci-
posed non–cross-linked collagen age range, 33 to 70 years), from two sion was extended along the study
membranes may resorb too quickly private dental practices, requiring teeth followed by elevation of buc-
to accommodate bone formation, extraction of maxillary and mandib- cal and lingual full-thickness flaps
while cross-linked collagen mem- ular nonmolar teeth (n = 30) partici- (Fig 1). Atraumatic tooth extrac-
branes may allow stabilization of pated in this outpatient study. They tions were performed to minimize
the collagen fibers to maintain the required removal of one or more trauma to the socket walls, and
membrane’s integrity.11,12 teeth and expressed a desire for careful investigation was done to
The purpose of this study was replacement with dental implants. identify possible bone dehiscences
to determine the clinical and histo- Patients were systemically healthy and fenestrations. Sockets with a
logic efficacy of the combination of with no surgical contraindications. thin or partially missing labial plate
alloplastic biphasic calcium phos- Oral and written explanations of (< 50%) were selected to undergo
phate composed of 30% HA and the study, including the risks, bene- the proposed ridge regeneration.
70% β-TCP (Osteon II, Dentium) fits, and alternative therapies, were Thirty extraction sockets re-
and a cross-linked collagen mem- thoroughly discussed. All patients ceived both Osteon II (0.5- to
brane (Collagen Membrane, volunteered for the protocol and 1.0-mm particle size) and Collagen
Dentium) used to reconstruct an signed an informed consent form membrane. The primary healing
extraction socket with new bone based on the Helsinki Declaration intention group (group A, n = 12)
formation. In addition, the safety of 1975, as revised in 2000. Preop- received primary flap closure over
and efficacy of soft and hard tis- erative assessments including intra- the membrane, while in the sec-
sue regeneration in sites with in- oral examination, and radiographic ondary healing intention group

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73

Fig 3 Collagen membrane placed to protect the underlying graft Fig 4 Membrane intentionally exposed at both grafted sites.
material.

(group B, n = 18), the membrane either 3- or 4-mm trephine burs diamond-coated blade (Exakt).
was left exposed. All extraction (Dentium) along the long axis of the The final thickness of 40 μm was
sites were incrementally graft- treated sites prior to implant place- achieved by grinding and final pol-
ed with Osteon II until the graft ment. Twenty-three cores were ob- ishing steps with 1,200-, 2,400-,
was level with the existing crestal tained (11 from group A, 12 from and 4,000-grit sandpaper. Sec-
bone, and a barrier membrane group B). The collected cores were tions from each block were used
was trimmed and closely adapted kept in the trephine burs, placed for staining with Sanderson rapid
to fit the contours of the grafted in formalin, and shipped to a his- bone stain (methylene blue and so-
site (Figs 2 and 3). Simple inter- tologist. Tapered dental implants dium permanganate).
rupted sutures (Silk and Vicryl, (SuperLine, Dentium) were placed
Ethicon) were used to position into the biopsy sites, and primary
the flap over the augmented area stability was verified in all cases. Backscatter scanning electron
(Fig 4). Both verbal and written microscopy
postoperative instructions were
given to patients, and appropri- Light microscopy Following the light microscopic
ate antibiotics and analgesics were evaluation, the ground sections
prescribed. Sutures were removed The bone cores were embedded were destained by polishing with
7 to 10 days postsurgery, and pa- following complete dehydration 6-μm diamond paste. They were
tients were seen at regular intervals in ascending grades of ethanol in then washed and sputter-coated
during the 6 months of healing. a light-curing one-component res- with a 6-nm-thick carbon layer
Postoperative periapical ra- in (Technovit 7200 VLC, Heraeus and examined in the backscatter
diographs and a CT scan were Kulzer). Polymerized blocks were modus of a Supra 40VP scanning
obtained 6 months after the ridge initially ground to bring the tissue electron microscope (Zeiss). Back-
regeneration procedure prior to components closer to the cutting scatter scanning electron micros-
the implant surgery. Soft and hard surface. A 100-µm-thick section copy (BSEM) micrographs were
tissue biopsy specimens of the was cut away from the block us- produced from the same levels as
grafted areas were obtained using ing a bandsaw equipped with a those for light microcopy.

Volume 33, Number 1, 2013


74

Fig 5 Excellent soft tissue healing was observed at the 15-week


postoperative visit.

Figs 6a and 6b Six-month postoperative CT scans revealed


preserved ridge dimensions of the sockets as well as radiographic
maturation of bone grafts for the (a) canine and (b) second premolar.

Results The soft tissue that formed Light microscopy and BSEM
over the exposed membrane ap- analyses
Clinical and radiographic peared to be firm in texture at the
evaluations 6-month biopsy sampling. The re- Histologic evaluation of the bone
sistance of the regenerated bone cores from the augmented area
All 12 patients completed the study to trephine and osteotomy drills provided an opportunity to ex-
without significant adverse events or indicated that the regenerated amine the quality and quantity of
complications (Fig 5). Early wound bone was dense and firm. Clinical newly formed bone and remnants
healing seemed to be slower at the reentry was performed after rais- of grafting material (Figs 8 to 12).
intentionally exposed sites (group B) ing a full-thickness flap to assess The connective tissue was devoid
when compared to primary flap the quality of regenerated bone. of inflammatory cell infiltrate but
closure sites (group A), but the dif- The dimensions of the ridge ap- was characterized by the presence
ference was not noticeable after peared to be maintained in both of a dense network of collagen fi-
4 weeks. Continuous maturation of groups, and internal socket bone bers with no membrane remnants
the tissue covering the membrane fill was evident (Fig 7). The grafted (Figs 8b and 11b). Evidence of
was noted after 4 weeks in group B. area appeared to be well vascu- mature bone formation and resid-
No spontaneous membrane expo- larized, but clinically visible graft ual bone grafting material was ob-
sure was noted in group A. particles were noted in some cas- served to varying degrees (Figs 8b
Radiographic analysis revealed es. The buccolingual dimensions and 11b). Newly formed bone
that mesial and distal crestal bone of the augmented alveolar ridge seemed to be directly apposed to
levels were maintained in both allowed placement of dental im- the surfaces of graft particles and
groups. Sockets in both groups un- plants that were at least 4.5 mm bridged the space between them,
derwent similar radiographic matu- in width. indicating that the graft material
ration (Figs 6a and 6b). behaved as an osteoconductive

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75

500 μm
a
NB M NB G

500 μm
b
Fig 7 Clinical reentry with a full-thickness Figs 8a and 8b (a) BSEM and (b) light microscopic micrograph from the same section
flap revealed that the dimensions of the through a core showing new bone formation (NB), marrow space (M), and graft particles
ridge were maintained, and internal socket (G) (group A).
bone fill was evident.

Osteoblasts
Osteoid

NB
NB
NB

500 μm 50 μm

Fig 9 Light microscopic micrograph showing newly formed bone Fig 10 Ongoing bone formation was characterized by the pres-
(NB) and marrow space (M) (group A). ence of osteoblasts and osteoid (group A). NB = new bone.

Figs 11a and 11b (a) BSEM and (b) light


microscopic micrograph from the same
section through a core showing new bone
formation (NB), marrow space (M), and
graft particles (G) (group B). CT = connec-
500 μm
tive tissue. a
NB G G M NB G CT

500 μm
b

Volume 33, Number 1, 2013


76

Fig 12 Graft particles (G) were seen partially embedded in newly


formed bone (NB) (group B).
NB

G
G

G
NB

NB

scaffold (Fig 12). The presence of was 18.0% ± 20.0%. Therefore, the the combination of HA and β-TCP
both osteoblasts and osteoclasts absence of primary flap closure did have been previously reported.15–22
indicated active bone formation as not affect the percentage of vital Osteon II is composed of 30% HA
well as bone remodeling. bone formation or residual graft. and 70% β-TCP (granules are 70%
BSEM evaluation of cores porous with interconnected pores
confirmed the presence of newly of 250 μm). The reason to combine
formed bone surrounding the graft Discussion an insoluble HA with a resorbable
particles (Figs 8a and 11a). BSEM β-TCP is that the slow-resorbing
enabled the graft particles to be dis- Ridge preservation immediately HA will maintain the volume while
tinguished from bone and nonmin- after tooth extraction has been ad- the faster-resorbing β-TCP will pro-
eralized tissue by their more dense vocated to preserve the ridge and mote bone regeneration.
and whiter appearance and shape. soft tissue dimension to allow ideal This study provided a healing
implant placement.3,13 Ideal bone period of 6 months to induce incor-
substitutes should not only pre- poration of the grafts with subse-
Histomorphometric analysis serve the socket dimension but also quent maturation of newly formed
encourage new bone ingrowth into bone tissue. A similar amount of
Histomorphometric analysis was the grafted area, thereby forming a bone regeneration as well as pres-
performed on 10 selected speci- living bridge between the existing ervation of alveolar ridge dimen-
mens (5 from group A, 5 from bone, new bone, and remaining sions was observed in both primary
group B). There were no signifi- bone substitutes.14 With time, newly and secondary healing intention
cant differences between the two formed bone should penetrate and groups. It was apparent that after a
groups regarding the amount of vi- replace much of the graft through 6-month healing period, the graft-
tal bone and residual graft (P > .05). the bone remodeling process.14 ed area was stable enough to en-
The mean amount of vital bone in This study investigated the role sure successful implant placement.
group A was 40.3% ± 7.8%, while of an alloplastic biomaterial and Histologic analysis of obtained
the remaining graft was 6.0% ± collagen membrane in preserv- bone cores revealed intimate con-
4.0%. The mean amount of vi- ing the ridge dimension after the tact between mineralized bone
tal bone in group B was 47.3% ± extraction of teeth. The biocom- tissue and graft particles, confirm-
11.3%, while the remaining graft patibility and osteoconductivity of ing the osteoconductive property

The International Journal of Periodontics & Restorative Dentistry


77

of the biomaterial. The percent- posure of a resorbable membrane References


age of vital bone volume (40.3% does not adversely affect the re-
1. Schropp L, Wenzel A, Kostopoulos L,
for group A and 47.3% for group generative outcome.13,28 Primary Karring T. Bone healing and soft tissue
B) was equivalent to other studies flap closure was not necessary to contour changes following single-tooth
extraction: A clinical and radiographic
of HA and β-TCP composite bone achieve bone augmentation when
12-month prospective study. Int J Peri-
graft. For example, Froum et al16 healing was marked by minimal odontics Restorative Dent 2003;23:
reported a 28.35% mean vital bone inflammation and rapid epithelial 313–323.
2. Fiorellini JP, Howell TH, Cochran D, et
volume when a mixture of 60% HA migration over the exposed mem- al. Randomized study evaluating re-
and 40% β-TCP was used as a sinus brane.28 The similarity between the combinant human bone morphogenetic
protein-2 for extraction socket augmen-
augmentation material. While the treatments indicated that the ab-
tation. J Periodontol 2005;76:605–613.
amount of vital bone formed after sence of primary closure did not 3. Nevins M, Camelo M, De Paoli S, et al. A
the augmentation may not corre- affect the percentage of vital bone study of the fate of the buccal wall of ex-
traction sockets of teeth with prominent
late to implant survival, it can be regeneration or the difference in roots. Int J Periodontics Restorative Dent
an accurate indicator to assess and graft stability or osseointegration. 2006;26:19–29.
4. Araújo M, Linder E, Wennström J, Lindhe
compare the healing potential of
J. The influence of Bio-Oss Collagen on
the graft.16 Because of the higher healing of an extraction socket: An exper-
β-TCP content in Osteon II (70%), a Conclusions imental study in the dog. Int J Periodon-
tics Restorative Dent 2008;28:123–135.
significant amount of graft particles 5. Mellonig JT, Valderrama P, Cochran DL.
were resorbed histologically. Thus, The use of a composite alloplastic Clinical and histologic evaluation of cal-
cium-phosphate bone cement in inter-
it appeared as though new bone biomaterial in combination with
proximal osseous defects in humans: A
formation was occurring simultane- a collagen membrane allowed report in four patients. Int J Periodontics
ously with material degradation. postextraction ridge preservation Restorative Dent 2010;30:121–127.
6. Lupovici J. Regenerative strategies for
A barrier membrane is used as well as sufficient bone qual- anterior esthetic rehabilitation: A clini-
along with bone graft material to ity and quantity to place dental cal and histologic case report. Compend
Contin Educ Dent 2010;31:614–618,
stabilize the blood clot, exclude implants. Although intentional
620, 622–623.
epithelial and connective tissue, membrane exposure could have 7. Kim DM, Nevins M, Camelo M, et al. Hu-
and enable osteogenic cells to pro- resulted in compromised barrier man histologic evaluation of the use of
the dental putty for bone formation in
liferate and differentiate.9 Early or function to support regeneration, the maxillary sinus: Case series. J Oral
spontaneous membrane exposure the sites that healed by second- Implantol 2012;38:391–398.
8. De Coster P, Browaeys H, De Bruyn H.
may lead to bacterial colonization, ary intention revealed similar clini-
Healing of extraction sockets filled with
infection, or membrane degrada- cal, radiographic, and histologic BoneCeramic prior to implant placement:
tion with a poor regenerative out- findings as those that healed by Preliminary histological findings. Clin Im-
plant Dent Relat Res 2011;13:34–45.
come because soft tissue growth primary intention. The use of this 9. Melcher AH. On the repair potential of
progresses at the rate of 0.5 to alloplastic biomaterial can be con- periodontal tissues. J Periodontol 1976;
47:256–260.
1.0 mm per day and can take 7 to sidered as a viable alternative to
10. Fontana F, Maschera E, Rocchietta I,
10 days to granulate.23–27 Cross- the use of autogenous bone or Simion M. Clinical classification of com-
linked collagen membranes remain other bone substitutes. plications in guided bone regeneration
procedures by means of a nonresorb-
intact longer than non–cross- able membrane. Int J Periodontics Re-
linked membranes, but the non– storative Dent 2011;31:265–273.
11. Moses O, Pitaru S, Artzi Z, Nemcovsky
cross-linked or low–cross-linked Acknowledgments CE. Healing of dehiscence-type defects
collagen membranes may not pro- in implants placed together with different
This study was funded by a grant from barrier membranes: A comparative clini-
vide effective barrier function if ex-
Dentium. cal study. Clin Oral Implants Res 2005;16:
posed prematurely.27 210–219.
Recent publications support
the idea that the intentional ex-

Volume 33, Number 1, 2013


78

12. Bornstein MM, Bosshardt D, Buser D. 18. Kim YK, Yun PY, Kim SG, Lim SC. Analy- 24. Simion M, Baldoni M, Rossi P, Zaffe D. A
Effect of two different bioabsorbable sis of the healing process in sinus bone comparative study of the effectiveness of
collagen membranes on guided bone grafting using various grafting materials. e-PTFE membranes with and without ear-
regeneration: A comparative histomor- Oral Surg Oral Med Oral Pathol Oral Ra- ly exposure during the healing period. Int
phometric study in the dog mandible. diol Endod 2009;107:204–211. J Periodontics Restorative Dent 1994;14:
J Periodontol 2007;78:1943–1953. 19. Frenken JW, Bouwman WF, Braven- 166–180.
13. Cardaropoli D, Cardaropoli G. Preser- boer N, Zijderveld SA, Schulten EA, ten 25. Simion M, Maglione M, Iamoni F, Scar-
vation of the postextraction alveolar Bruggenkate CM. The use of Straumann ano A, Piattelli A, Salvato A. Bacterial
ridge: A clinical and histologic study. Int Bone Ceramic in a maxillary sinus floor penetration through Resolut resorbable
J Periodontics Restorative Dent 2008;28: elevation procedure: A clinical, radiologi- membrane in vitro. An histological and
469–477. cal, histological and histomorphometric scanning electron microscopic study.
14. Hing KA. Bioceramic bone graft substi- evaluation with a 6-month healing period. Clin Oral Implants Res 1997;8:23–31.
tutes: Influence of porosity and chem- Clin Oral Implants Res 2010;21:201–208. 26. Hämmerle CH, Jung RE. Bone augmen-
istry. Int J Appl Ceram Technol 2005;2: 20. Mardas N, Chadha V, Donos N. Alveo- tation by means of barrier membranes.
184–199. lar ridge preservation with guided bone Periodontol 2000 2003;33:36–53.
15. Cordaro L, Bosshardt DD, Palattella P, regeneration and a synthetic bone sub- 27. Oh TJ, Meraw SJ, Lee EJ, Giannobile
Rao W, Serino G, Chiapasco M. Maxillary stitute or a bovine-derived xenograft: A WV, Wang HL. Comparative analysis of
sinus grafting with Bio-Oss or Straumann randomized, controlled clinical trial. Clin collagen membranes for the treatment
Bone Ceramic: Histomorphometric re- Oral Implants Res 2010;21:688–698. of implant dehiscence defects. Clin Oral
sults from a randomized controlled mul- 21. Mardas N, D’Aiuto F, Mezzomo L, Ar- Implants Res 2003;14:80–90.
ticenter clinical trial. Clin Oral Implants zoumanidi M, Donos N. Radiographic 28. Kim DM, Nevins M, Camelo M, et al. The
Res 2008;19:796–803. alveolar bone changes following ridge feasibility of demineralized bone matrix
16. Froum SJ, Wallace SS, Cho SC, Elian N, preservation with two different bioma- and cancellous bone chips in conjunc-
Tarnow DP. Histomorphometric com- terials. Clin Oral Implants Res 2011;22: tion with an extracellular matrix mem-
parison of a biphasic bone ceramic to 416–423. brane for alveolar ridge preservation:
anorganic bovine bone for sinus aug- 22. Kim DM, Camelo M, Nevins M, Fateh A, A case series. Int J Periodontics Restor-
mentation: 6- to 8-month postsurgical Schupbach P, Nevins M. Alveolar ridge ative Dent 2011;31:39–47.
assessment of vital bone formation. A construction with a composite alloplastic
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Dent 2008;28:273–281. ative Dent 2012;32:e204–e209.
17. Kim YK, Yun PY, Lim SC, Kim SG, Lee 23. Engler WO, Ramfjord SP, Hiniker JJ. Heal-
HJ, Ong JL. Clinical evaluations of OS- ing following simple gingivectomy. A triti-
TEON as a new alloplastic material in si- ated thymidine radioautographic study. I.
nus bone grafting and its effect on bone Epithelialization. J Periodontol 1966;37:
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459

Socket Site Preservation Using Bovine


Bone Mineral With and Without a
Bioresorbable Collagen Membrane

Mally Perelman-Karmon, DMD, MS*/Avital Kozlovsky, DMD** Tooth extraction leads to morpho-
Roman Lilov, DMD***/Zvi Artzi, DMD**** logic changes and resorption of the
alveolar ridge as a result of a lack of
biomechanical forces on the bone.1,2
The purpose of this study was to compare extraction sites augmented with In the immediate postextraction
bovine bone mineral (BBM) with and without resorbable membrane coverage. phase, the fresh extraction socket
BBM particles were grafted in fresh human extraction sockets of 23 patients; possesses a unique wound-healing
in 12 of these patients, a guided tissue regeneration (GTR) membrane was cascade.3–5 Marked dimensional al-
applied. After 9 months of histomorphometric evaluation, cylindric hard terations occur in the edentulous
tissue specimens were obtained. Percent bone area fractions (BAFs) of the
ridge after extraction.1,5,6
crestal, middle, and apical sections from each specimen were calculated using
In the anterior maxilla, there is
the point-counting technique. Changes in values were compared. In sites
consistent bone resorption where
augmented with BBM, the mean BAF ranged from 22.8% (coronal) to 36.3%
(apical) compared to sites augmented with BBM and collagen membrane
the buccal plate is thin. Bone re-
(35.2% [coronal] to 47% [apical]). Comparison between the different depths sorption leads to palatal/lingual
and the two groups showed a distinct increase in BAF from coronal to apical and apical positioning of the alveo-
regions (P < .001). This pattern was observed in both groups (P < .001) and lar crest, since resorption is more
was significantly higher in the group augmented with BBM and collagen prominent in the buccal plate.1,5
membrane (P < .05). In the immediate postextraction phase, BBM as a grafted Thus, preserving the alveolar ridge
biomaterial preserved the socket volume and enabled newly formed bone for and achieving appropriate ridge
future implant site preparation. The amount of the osseous fraction increased dimensions are important7,8 when
with GTR membrane. (Int J Periodontics Restorative Dent 2012;32:459–465.) an implant-supported fixed partial
    *Department of Oral Sciences, School of Dental Medicine, State University of New York,
denture is required.
Buffalo, New York, USA; Formerly, Undergraduate Student, The Maurice and Gabriela The increasing demand for es-
Goldschleger Scool of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. thetic implant dentistry challenges
   **Associate Professor, Department of Periodontology, The Maurice and Gabriela
the clinician. The implant location
Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel.
  ***Private Practice, Netanya, Israel. should comply with the patient’s
****Associate Professor and Director of Graduate Periodontics, Department of esthetic, functional, and phonetic
Periodontology, The Maurice and Gabriela Goldschleger School of Dental Medicine, needs. Guided tissue regeneration
Tel Aviv University, Tel Aviv, Israel.
(GTR), a biologic principle based on
Correspondence to: Prof Zvi Artzi, School of Dental Medicine, Tel Aviv University, a selective cell population, achieves
Ramat Aviv, Tel Aviv 61390, Israel; email: zviartzi@tau.ac.il. sufficient volume of regenerated

Volume 32, Number 4, 2012

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460

bone.9 Different types of GTR mem- serves the alveolar ridge by stabiliz- ranged from 26 to 68 years of age
branes are used with and without a ing the blood clot, thus maintaining and were nonsmokers. The proce-
biomaterial scaffold10,11 to maintain the volume at the site and simulta- dure was explained, and patients
space over a bony defect (extrac- neously serving as an osteoconduc- signed consent forms. The study
tion socket void) and to prevent tive guide rail to facilitate continual was in accordance with the Helsinki
undesired cells from migrating into bone formation.12–17 BBM applied Declaration.
the defect. The membrane protects in conjunction with a bioresorbable Before extraction, clinical
the blood clot formed in the socket. membrane after a healing period of (probing) and radiographic param-
By protecting and secluding the 9 months has shown complete hori- eters were collected (Figs 1a and
socket from the adjacent interfer- zontal bone augmentation.11 1b). Sites exhibiting severe to com-
ing connective tissue cells, the While the significant contri- plete socket wall destruction were
membrane enables and promotes bution of applying a selective se- excluded.
osteogenic cell migration into the cluded barrier in GTR or guided Extracted teeth included max-
defect.9 bone regeneration (GBR) proce- illary incisors (n = 10) and maxil-
After extraction, the defined dures is evident, the application lary (n = 8) and mandibular (n = 5)
area serves as a wound-healing site. of membrane coverage at a fresh single-root premolars. At least 50%
The healing cascade of the socket extraction socket while at the same of sockets were partially resorbed/
is dominated by coagulum, which time obtaining complete soft tis- destructed at one to two walls, but
is gradually occupied by granula- sue closure is a challenge. Further- not circumferentially so that the
tion tissue followed by a provision- more, since bone tissue has been inclusion criteria of containing the
al matrix (connective tissue).4 One formed with and without the use of grafted particles and supporting
week postextraction, the socket is a membrane in animal and human the applied over-latticed resorb-
characterized by granulation tissue studies,7,8,12,13,16–18 the indication of able membrane could be met.
consisting of a vascular network, im- a GBR surgical modality in a unique Immediately following extraction,
mature connective tissue, osteoid healing site (ie, fresh extraction BBM particles (250 to 1,000 µm;
formation in the apical portion, socket) should be interpreted. Bio-Oss, Geistlich) were placed to
and epithelial coverage over the The objective of this study was fill the site completely (Fig 1c). The
wound. At 1 month postextrac- to compare the amount of bone decision to use sites with or with-
tion, the socket is characterized by area fraction in fresh extraction out the application of a resorbable
dense connective tissue overlying sites using BBM as the grafting membrane was determined ran-
the residual sockets and filled with biomaterial, protected or unpro- domly by flipping a coin before ex-
granulation tissue. A trabecular tected with a resorbable collagen traction. A double layer of collagen
pattern of bone starts to emerge. membrane, and by using a rotating membrane (Bio-Gide, Geistlich)
Epithelium used for wound cover- pedicle flap or coronally advanced was applied in 11 sites (Fig 1d). The
age is complete following the se- flap to achieve complete soft tissue membrane covered the entire site
quence of bone formation.3,4 closure. and was secured labially and lin-
In a periodontal deteriorating gually under soft tissue flaps.
situation, when destruction of par- In the maxilla, complete soft
tial or complete socket walls is evi- Method and materials tissue closure was obtained using a
dent, ingrowth of connective tissue rotating pedicle flap from the pala-
into the extraction site is unavoid- This study included 23 fresh single- tal side. Advanced coronal, buccal,
able, leading to a deficient ridge. root extraction sockets in 23 and lingual flaps ensured soft tissue
The use of bone substitute, such healthy patients (16 women, 7 men) closure in mandibular premolars.
as bovine bone mineral (BBM), pre- with no systemic diseases. Patients The distal superficial end of the

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461

pedicle flap was de-epithelialized with 5% formic acid for 2 weeks.


and sutured (4-0 Vicryl, Ethicon) to The decalcified cylindric speci-
the inner layer of the buccal flap mens were embedded in paraffin
to obtain complete soft tissue clo- and transversely cut into serial sec-
sure over the membrane-protected tions 5-µm wide using a microtome
grafted site (Fig 1e). The same soft (Leica RM 2245, Leica Microsys-
tissue management was performed tems). Each core was cut uniform-
in the unprotected group (n = 13) ly from the peripheral to deeper
but without applying the GTR regions. Slides were stained with
membrane. The exposed palatal hematoxylin-eosin. From each tis-
area was left for secondary healing. sue cylinder, six representative cuts
Patients were prescribed anal- undamaged during microtome cut-
gesics (naproxen 275 mg; Narocin, ting were selected for morphomet-
Teva Pharmaceutical) and instruct- ric analysis: two from the coronal
ed to rinse with 0.2% chlorhexidine portion (1 to 2 mm), two from the
gluconate (Tarodent, Taro Pharma- middle core, and two from the apical
ceutical) twice a day for 30 seconds end (1 to 2 mm). Data from each pair
for 2 weeks. Complete soft tissue were averaged and used as such.
healing was observed at 1 month
postgrafting (Fig 1f). Computed to-
mography scans were taken to plan Histomorphometry
the future implant prosthetic recon-
struction (Fig 1g). In each section, bone area fraction
Since BBM is a slow biodegrad- at membrane-protected (m-BAF)
able material,17 an extended heal- and biomaterial-only (BAF) grafted
ing phase was allowed for possible sites was measured using an adap-
interpretation between membrane- tation of the point-counting proce-
protected and unprotected healing dure.12,17,19–22 Briefly, each section
sites. At 9 months, at implant place- was examined in a projection mi-
ment, a midcrestal incision was croscope (Visopan, Reichart, Leica)
made to expose the grafted site at 20× magnification. A 64-square
(Fig 1h). At this stage, instead of (1.5 × 1.5 cm) graticule was su-
the usual sequence of step-up drill- perimposed on the screen for the
ing for implant site preparation, a point-counting calculation. Bone
2.5-mm–internal diameter trephine tissue was recorded whenever the
bur was applied to harvest a cylin- graticule center (marked with “+”)
dric hard tissue core approximately hit the bone tissue.12,21,22 The sum
8 mm in length. The apical end of (Pi) of the points overlying the bone
each specimen was marked for ori- tissue was calculated. Percentage
entation to identify the peripheral of bone tissue was evaluated as a
versus deep ends. portion of the entire section area
Specimens (n = 23) were fixed (Pi / Σi), where Σi represents the to-
in 10% neutral buffered formalin tal number of points superimposed
for 1 week and then decalcified on each section.

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462

Fig 1a (left)    Clinical appearance of a


maxillary right central incisor. The marginal
gingiva was inflamed, and the tooth had
migrated slightly labially and mesially be-
cause of the periodontal condition.

Fig 1b (right)    Periapical radiograph of the


maxillary central incisor. Severe periodontal
destruction is evident.

Fig 1c    Fresh extraction socket filled with Fig 1d    Bioresorbable membrane applied Fig 1e    Complete soft tissue closure was
BBM particles. to cover the augmented socket. obtained using a pedicle palatal rotated flap.

Fig 1f    At 1 month, soft tissue healing was Fig 1g    Buccolingual computed tomogra- Fig 1h    At reentry, a wide buccolingual os-
evident. phy section of the grafted extraction site. seous table had been established.

All measurements were taken measurements and the coefficient


by the same investigator. To de- of variation (CV) for each parameter,
termine the reproducibility of the 10 randomly selected slides were

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463

Fig 2a (left)    Typical coronal decalcified


section cut. An abundance of soft tissue
(ST) and grafted particles (P) surrounded
by newly formed bone (B) can be seen
B
(hematoxylin-eosin, original magnification B
ST ×25).

B B
P Fig 2b (right)    Apical section with a high B
P
P percentage of bone area fraction (B)
(hematoxylin-eosin, original magnification
B
×25).
ST

Fig 3    Mean BAF at the crestal, middle, and apical regions of the

membrane-protected and unprotected extraction sites augmented by †
70 † Membrane-protected
BBM particles. **P < .05; ***P < .001, †P < .001 (within-subject data). †

60 *** Unproteced
**
50

Mean BAF (%)


**
40
30
20
10
0
Crestal Middle Apical

measured 5 times, not consecu- Results group, total BAF ranged from 15%
tively, without reference to the pre- to 54% (mean, 29.7% ± 7.21%).
vious data. The mean CV of bone All patients were observed fre- BAF ranged from 15.0% to 33.0%
(2.2%), biomaterial particle (2%), and quently, and postoperative heal- (mean, 22.8% ± 5.11%), 16.5% to
remaining concavity area fractions ing was immaculate. Histologic 47.5% (mean, 29.9% ± 8.98%), and
(1.8%) indicated that these measure- examination revealed that all cores 21.5% to 54.0% (mean, 36.3% ±
ments were highly reproducible. harbored an abundance of BBM 11.3%) at the crestal, middle, and
During measurements, the in- particles surrounded by newly apical regions, respectively.
vestigator was masked to the type of formed bone. In the membrane- Mean m-BAF was significantly
site with respect to whether the mea- protected group, total bone frac- greater than BAF at all respective
surement was conducted on protect- tion ranged from 23% to 72% depths (P < .05). In both groups
ed or unprotected membrane sites; (mean, 40.8% ± 10.61%) (Figs 2a (m-BAF and BAF), a gradual in-
the same applied for its depth. and 2b). m-BAF ranged from 24.0% crease in bone area fraction was
Repeated-measures analysis to 52.5% (mean, 35.2% ± 9.18%), observed from the coronal to apical
of variance was used. The within- 24.5% to 59.5% (mean, 40.2% areas. Within each type, the bone
subject factor was depth, and the ± 10.74%), and 23.0% to 72.0% area fraction in the apical region was
between-subject factor was mem- (mean, 46.95% ± 12.83%) at the statistically greater than that in the
brane coverage. Values were con- crestal, middle, and apical regions, middle and crestal areas (P < .001)
sidered significant at P < .05. respectively. In the unprotected (Fig 3).

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464

Discussion entire site, in addition to its bio- ed. In a computed tomography–


logic contributions. In unprotected derived bone density study in
BBM, which has been used for over sites, some particulate biomate- dogs,29 similar findings were shown
20 years, has proven to be a suitable rial would be lost or reside in the with regard to the contribution
biomaterial in augmentation proce- overlying soft tissue. Nevertheless, of the GTR modality. Moreover,
dures. Clinical and histologic stud- in both sites, BBM particles were wound site stability and undesired
ies have shown the efficacy of this surrounded by newly formed bone, micromovement,30 which can occur
osteoconductive material.11,18,23,24 and all sites exhibited clinical hard in this region, might influence the
A high osteoconductive property tissue formation, which was suit- remodeling process.
by BBM has also been shown in a able for implant site preparation.
recent comparative study in human The slow resorption rate of
extraction sockets.15 BBM does not inhibit continuous Conclusions
BBM particles have been bone formation. On the contrary, it
shown to be well integrated with enhances it progressively.17 BBM, as a grafted biomaterial in
regenerated bone in extraction In unprotected grafted human fresh extraction sockets, preserved
and alveolar ridge deficiency sites sockets,12,26 BAF increases when its volume and enabled newly
in animal16,23,25 and human clinical approaching the apical area. In- formed bone for future implant
studies,11,18,24,26 as well as in mor- trabony defects healed with BBM site preparation. The application of
phometric studies.12,22 In a human alone or with BBM and a resorb- GBR increased the osseous fraction.
study,27 excellent osseointegration able membrane. It has been shown
and crestal bone level maintenance that the amount of bone regenera-
were shown when implant place- tion is further enhanced with the Acknowledgments
ment was combined with bone latter.28
The authors thank Mrs Ilana Gelerntner for
augmentation using BBM as the Caution should be taken when
the statistical analysis and Ms Rita Lazar for
grafting biomaterial. internalizing the morphometric
editorial assistance.
In the current study, all 23 con- data if the examined sites are nei-
secutive patients showed primary ther identical nor standardized
soft tissue closure and excellent before grafting. However, the re-
healing whether GTR membrane peated outcomes at the 12 versus
coverage was applied or not. 11 consecutively examined sockets
However, the point-counting his- should strengthen the findings.
tomorphometry disclosed a distin- In this study, the least BAF was
guishable observation. Regardless found in the crestal zone, regardless
of the depth of the examined his- of whether the site was membrane-
tologic section, a membrane- protected. This could be explained
protected grafted socket site by the distance between the socket
showed greater newly formed walls.12 In the extraction site, the
bone when compared with unpro- distance between the socket walls
tected grafted sites. It should be is reduced toward the apical region.
considered that a membrane-pro- Thus, this is an amply nourished
tected site is advantageous since site.
the GTR membrane confines the The fact that a membrane-pro-
grafted particles during the first tected socket site showed greater
period of healing and stabilizes the newly formed bone was anticipat-

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465

References 12. Artzi Z, Tal H, Dayan D. Porous bovine bone 22. Artzi Z, Kozlovsky A, Nemcovsky CE,
mineral in healing of human extraction Weinreb M. The amount of newly formed
 1. Carlsson GE, Bergman B, Hedegård B. sockets. Part 1: Histomorphometric eval- bone in sinus grafting procedures de-
Changes in contour of the maxillary alve- uation at 9 months. J Periodontol 2000; pends on tissue depth as well as the type
olar process under immediate dentures. 71:1015–1023. and residual amount of the grafted mate-
A longitudinal clinical and x-ray cepha- 13. Artzi Z, Nemcovsky CE, Tal H. Efficacy rial. J Clin Periodontol 2005;32:193–199.
lometric study covering 5 years. Acta of porous bovine bone mineral in vari- 23. Berglundh T, Lindhe J. Healing around
Odontol Scand 1967;25:45–75. ous types of osseous deficiencies: Clini- implants placed in bone defects treated
  2. Pietrokovski J, Massler M. Alveolar ridge cal observations and literature review. with Bio-Oss. An experimental study in
resorption following tooth extraction. Int J Periodontics Restorative Dent the dog. Clin Oral Implants Res 2007;8:
J Prosthet Dent 1967;17:21–27. 2001;21:395–405. 117–124.
  3. Amler MH, Johnson PL, Salman I. Histo- 14. Cardaropoli G, Araújo M, Hayaci- 24. Skoglund A, Hising P, Young C. A clinical
logical and histochemical investigation bara R, Sukekava F, Lindhe J. Healing and histologic examination in humans of
of human alveolar socket healing in un- of extraction sockets and surgically pro- the osseous response to implanted natu-
disturbed extraction wounds. J Am Dent duced—augmented and non-augment- ral bone mineral. Int J Oral Maxillofac Im-
Assoc 1960;61:32–44. ed—defects in the alveolar ridge. An plants 1997;12:194–199.
 4. Cardaropoli G, Araújo M, Lindhe J. experimental study in the dog. J Clin 25. Hockers T, Abensur D, Valentini P, Legrand
Dynamics of bone tissue formation in Periodontol 2005;32:435–440. R, Hämmerle CH. The combined use of
tooth extraction sites. An experimental 15. Lee DW, Pi SH, Lee SK, Kim EC. Com- bioresorbable membranes and xenografts
study in dogs. J Clin Periodontol 2003;30: parative histomorphometric analysis of or autografts in the treatment of bone de-
809–818. extraction sockets healing implanted with fects around implants. A study in beagle
  5. Araújo MG, Lindhe J. Dimensional ridge bovine xenografts, irradiated cancellous dogs. Clin Oral Implants Res 1999;10:
alterations following tooth extraction. allografts, and solvent-dehydrated al- 487–498.
An experimental study in the dog. J Clin lografts in humans. Int J Oral Maxillofac 26. Artzi Z, Tal H, Dayan D. Porous bovine
Periodontol 2005;32:212–218. Implants 2009;24:609–615. bone mineral in healing of human extrac-
 6. Schropp L, Wenzel A, Kostopoulos L, 16. Artzi Z, Givol N, Rohrer MD, Nemcovsky tion sockets: 2. Histochemical observa-
Karring T. Bone healing and soft tissue con- CE, Prasad HS, Tal H. Qualitative and tions at 9 months. J Periodontol 2001;
tour changes following single tooth extrac- quantitative expression of bovine bone 72:152–159.
tion: A clinical and radiographic 12-month mineral in experimental bone defects. Part 27. Meijndert L, Raghoebar GM, Schüpbach
prospective study. Int J Periodontics Re- 1: Description of a dog model and histo- P, Meijer HJ, Vissink A. Bone quality at the
storative Dent 2003;23:313–323. logical observations. J Periodontol 2003; implant site after reconstruction of a local
  7. Nevins M, Camelo M, De Paoli S, et al. A 74:1143–1152. defect of the maxillary anterior ridge with
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 8. Araújo MG, Lindhe J. Ridge preserva- Part 2: Morphometric analysis. J Peri- al. Clinical, radiographic, and histologic
tion with the use of Bio-Oss collagen: A odontol 2003;74:1153–1160. evaluation of human periodontal defects
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regeneration. Plast Reconstr Surg 1988; a case report. J Periodontol 1998;69: mineral with or without collagen mem-
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NP. Ridge augmentation by applying ramic hydroxyapatite bone derivative in odontol 1993;64:883–890.
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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

Ridge Preservation Comparing a Socket Allograft Alone to a


Socket Allograft Plus a Facial Overlay Xenograft: A Clinical and
Histologic Study in Humans
Evmenios Poulias, DDS, MS*, Henry Greenwell, DMD, MSD†,  Margaret Hill, DMD‡,  
Dean Morton, DMD, MS§, Ricardo Vidal, DDS, MS‖, Brian Shumway, DMD, MS¶,
Thomas L. Peterson, DDS, MS#

Private Practice, Athens, Greece.

Professor, Director of Graduate Periodontics, University of Louisville, Louisville, KY.

Associate Professor, Assoc Dean Postdoctoral Education, University of Louisville,


Louisville, KY.

Professor, Chair, Dept of Oral Health & Rehabilitation, University of Louisville,


Louisville, KY.

Assistant Professor, Periodontics, University of Louisville, Louisville, KY.

Assistant Professor, Oral Pathology, University of Louisville, Louisville, KY.

Private Practice, Macon, Georgia.


Background. Previous studies of ridge preservation showed a loss of about 18% or 1.5 mm of
crestal ridge width in spite of treatment. The primary aim of this randomized, controlled, blinded clinical
trial was to compare a socket graft to the same treatment plus a buccal overlay graft, both with a polylactide
membrane, to determine if loss of ridge width can be prevented by use of an overlay graft.
Methods. Twelve positive control patients received an intrasocket mineralized cancellous
allograft (Socket group) while twelve test patients received the same socket graft plus buccal overlay
cancellous xenograft (Overlay group). Horizontal ridge dimensions were measured with a digital caliper
and vertical ridge changes were measured from a stent. Prior to implant placement at 4 months a trephine
core was obtained for histologic analysis.
Results. The mean horizontal ridge width at the crest for the Socket group decreased from 8.7 ±
1.0 mm to 7.1 ± 1.5 mm for a mean loss of 1.6 ± 0.8 mm (p < 0.05) while the Overlay group decreased
from 8.4 ± 1.4 mm to 8.1 ± 1.4 mm for a mean loss of 0.3 ± 0.9 mm (p > 0.05). The Overlay group was
significantly different from the Socket group (p < 0.05). Histologic analysis revealed that the Socket group
had 35 ± 16% vital bone while the Overlay group had 40 ± 16% (p > 0.05).
Conclusions. The Overlay treatment significantly prevented loss of ridge width and preserved or
augmented the buccal contour. The Socket and Overlay groups healed with a high percentage of vital bone.

KEY WORDS:
allograft; xenograft; grafting, bone; socket graft; bone regeneration.
Following extraction there is substantial resorption of the alveolar ridge resulting
in compromised ridge dimensions. Araujo et al. have shown that bone resorption is most
pronounced on the buccal.1-5 This is due to loss of bundle bone that results in the loss of
a portion of the buccal plate. When human extraction alone studies are reviewed as a

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

group they show that, on average, approximately 3.7 mm or 45% of horizontal ridge
width is lost within a 4 to 6 month period.6-14 Ridge height, on the other hand, is less
affected and on average only about 1.6 mm is lost.6-14
In an effort to reduce post-extraction bone loss clinicians have performed what is
known as a ridge preservation procedure. This treatment utilizes an osseous graft and/or
a barrier membrane to manage the extraction socket. The goal of this procedure is to
ensure that adequate ridge width is preserved to allow implant placement totally within
bone and to avoid complications such as implant dehiscence and fenestration. In spite of
these efforts, most studies of ridge preservation show that there is still some loss of
horizontal ridge width that can lead to a concave buccal contour and may lead to a
dehiscence or fenestration at the time of implant placement. Ridge preservation studies
as a group show that, on average, about 1.5 mm or 18% of horizontal ridge width is lost.6-
9,11-32
Ridge height is minimally affected and, on average, less than about 0.5 mm of
height is lost.6-15,17,18,20,21,23,24,27,29-33
Wang et al. have described a "sandwich" technique of layered osseous grafting
that utilizes an outer layer that resists resorption and will remain in place for an extended
or indefinite period.34 The inner layer, on the other hand, is resorbed and replaced more
quickly by newly formed vital bone. These principles will be utilized in this study.
Bovine xenograft has been reported to resorb very slowly and become fibrous
encapsulated while cancellous allograft is resorbed and replaced more quickly through a
process known as creeping substitution.18,34-40 These two materials fulfill the principles
proposed by Wang et al.34 Therefore the cancellous allograft was chosen as a rapidly
resorbing socket graft while the bovine xenograft was chosen as a buccal overlay to resist
resorption and preserve the buccal contour. The specific aim of this study was to
determine if ridge preservation treatment can be performed in a manner that will prevent
the loss of crestal ridge width thereby preserving the original buccal contour. Comparing
a socket graft alone to a socket graft plus a facial overlay will provide a valid test of the
hypothesis that loss of crestal ridge width can be prevented when a slowly resorbing
facial overlay graft is utilized.

METHODS
Study Design
A total of 24 patients participated in this 4-month randomized, controlled, blinded clinical
study of ridge preservation in sequentially entered single extraction sites of nonmolar
teeth to be replaced by a dental implant. Twelve positive control patients were randomly
selected, using a coin toss, to receive ridge preservation treatment with an intrasocket,
mineralized, cancellous, particulate allograft (500-800 µm, Socket group).* The twelve
test patients received the same intrasocket allograft plus a facial overlay with a
mineralized, cancellous, particulate bovine xenograft (250-1000 µm, Overlay group).† A
bioresorbable polylactide membrane was used to cover the osseous graft in both groups.‡
Four months after the grafting procedure the implant placement surgery was performed
and a trephine core was removed from the osteotomy site for histologic analysis. All
surgical procedures were completed by one operator (EP) under the direction of one
mentor (HG). The surgeon was trained in the procedures until considered proficient. All

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

blinded measurements were performed by one blinded examiner (TP), who was unaware
of the treatment assignment at all time points. The mentor performed the coin toss after
flap reflection and immediately prior to graft placement and verified the measurements
taken by the blinded examiner. All patients signed an informed consent approved by the
University of Louisville Institutional Review Board in August 2011, when this study
11.0352 was also approved. This study was conducted in accordance with the Helsinki
Declaration of 1975, as revised in 2000. The study was conducted between September
2011 and July 2012 in the Graduate Periodontics clinic at the University of Louisville.

Outcome Variables
The primary outcome variable was crestal horizontal ridge width and the power analysis
was based on this variable. Other variables evaluated included vertical ridge dimension
change and histologic assessment of vital bone, non-vital bone and trabecular space.

Inclusion/Exclusion Criteria
Subjects met the eligibility criteria if they were at least 18 years of age and had one
nonmolar tooth requiring extraction that would be replaced by a dental implant.
Extraction sites were bordered by at least one tooth. Exclusion criteria included: 1)
debilitating systemic diseases, or diseases that have a clinically significant effect on the
periodontium; 2) molar extraction sites; 3) presence of or history of osteonecrosis of the
jaws; 4) history of IV bisphosphonate treatment; 5) history of oral bisphosphonate
treatment for more than three years; 6) pregnancy or lactation; 7) known allergy to any
material or medication used in the study; 8) required antibiotic prophylaxis; 9) previous
head and neck radiation therapy; 10) history of chemotherapy in the last 12 months; 11)
long term steroid or non-steroidal anti-inflammatory drug therapy; or 12) failure to sign
an informed consent approved by the Human Studies Committee. Patients were excluded
post-treatment if they developed infection or had an adverse reaction to any of the
materials used in the study.

Clinical and Radiographic Parameters


Each patient received a diagnostic work-up that included standardized periapical
radiographs, study casts, clinical photographs, and a full periodontal examination.
Radiographic and study cast data will not be presented or discussed. Customized occlusal
stents were fabricated on the study casts to serve as fixed reference guides for the vertical
measurements.9
Clinical parameters on adjacent teeth assessed at baseline and at the 4-month re-
entry included Plaque Index, Gingival Index, bleeding on probing (dichotomous),
keratinized tissue width, recession, probing depth, clinical attachment level, CEJ to
alveolar crest distance, and tooth mobility.41,42 Horizontal ridge width was recorded with
a modified digital caliper measuring to the nearest 10-2 at the mid-socket crestal level and
5 mm apically. Vertical distance from the acrylic stent to the alveolar crest was measured
mesially, mid-socket and distally on all buccal, occlusal and lingual surfaces using a 15
mm North Carolina periodontal probe.9

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

Surgical Treatment
Full thickness flaps were elevated to expose both the facial and the palatal/lingual aspects
of the alveolar ridge. The flaps were extended one tooth mesial and distal to the
preservation site on the buccal and vertical incisions were placed on the buccal and
palatal. Papillae preservation incisions were used to keep the papilla intact.43 The teeth
were extracted as atraumatically as possible using periotomes, elevators and forceps.
After the extraction, the socket was carefully curetted to remove all soft tissue.
The allograft and xenograft materials were hydrated in a 50 mg/ml solution of
tetracycline. The socket allograft was placed to the level of the alveolar crest and the
facial overlay xenograft was placed over the buccal wall of the extraction socket from the
alveolar crest to about 12 mm apical and was extended about half a tooth to the mesial
and distal. The polylactide barrier membrane was trimmed to completely cover the socket
and extended at least 3 mm past the alveolar crest and at least 3 mm past the lateral and
apical borders of the facial xenograft. The membrane overlying the central portion of the
socket was left exposed. Flaps were replaced or slightly coronally positioned. If needed,
an apical periosteal split was performed to permit adequate flap release for tension-free
closure. Flaps were sutured with a 4-0 polytetrafluoroethylene suture.§ Compression of
the facial overlay graft was avoided by ensuring that flap closure was tension free.
Patients were given a post-surgical regimen consisting of 375 mg naproxen (twice a day
for one week), 50 mg doxycycline hyclate (once a day for two weeks) and narcotic
analgesics as needed. Patients were seen every two weeks until soft tissue closure was
complete and then monthly until the 4-month implant placement.

Implant Placement
Full-thickness flaps were elevated on the buccal and palatal/lingual using a papilla
preservation technique. All baseline clinical measurements were repeated and a
standardized radiograph was taken. A 2.7 x 6.0 mm trephine was used with copious
chilled saline irrigation to remove a core from the osteotomy site prior to implant
placement.║ The core was subsequently placed in 10% buffered formalin for histologic
processing. A dental implant was placed and flaps were replaced and sutured with 4-0
silk or the polytetrafluoroethylene sutures described previously.

Contour Data
Pre- and post-treatment unlabelled occlusal clinical photographs were compared to
determine the initial and final buccal contour. Each contour was subjectively categorized
as a concave, flat or convex contour. Two blinded examiners (HG, EP) had to agree on
each contour categorization. Since this was a subjective evaluation it was considered
important to use two examiners. Subsequently the pre-and post-treatment categories
were compared to determine if there was a loss, no change or a gain in terms of contour.

Tooth Type Data


Data from previous studies of ridge preservation at this institution (this study, 2
publications, and 5 Master's theses) that were measured using the same technique as in
this study were grouped according to tooth type to determine initial and final ridge

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

dimensions, the change and the percent change.9,18 Data for this analysis came from sites
that received socket treatment alone without an overlay graft.

Histologic Analysis
Trephine cores (2.7 X 6 mm) were decalcified and 12-15 step serial sections were taken
from the center of each longitudinally sectioned core. The sections were stained with
hematoxylin and eosin. Ten slides per patient were prepared, each containing at least 4
sections. Six randomly selected fields, 1 per section if possible, were used to obtain
percent cellular bone, acellular bone, and trabecular space using an American Optics light
microscope at 150x with a 10x objective and 15x reticle eyepieces.9

Statistical Methods
Means and standard deviations were calculated for all parameters. A paired t-test was
used to evaluate the statistical significance of the differences between initial and final
data. An unpaired t-test was used to evaluate statistical differences between the test and
control groups. The sample size of 11 per group gave 80% statistical power to detect a
difference of 1 mm between groups for crestal ridge width. Power calculations were
based on data from previous studies.9,18

RESULTS
A total of 24 patients were entered in this study. For the Socket group 8 females
and 4 males with a mean age of 52 ± 16, ranging from 26 to 77 years, were enrolled
while 5 females and 7 males with a mean age of 58 ± 11, ranging from 38 to 71 years,
were enrolled in the Overlay group. All sites were bordered by at least one tooth mesially
or distally. The Socket group consisted of 1 maxillary incisor, 2 maxillary canines, 8
maxillary premolars, and 1 mandibular premolar. The Overlay group consisted of 5
maxillary incisors, 1 maxillary canine, and 6 maxillary premolars. There were 2 smokers
enrolled in the Socket group and 2 in the Overlay group. The reason for extraction in the
Socket group was 9 due to caries, 2 due to root fracture and 1 due to root resorption; in
the Overlay group 6 were extracted due to caries, 5 due to root fracture and 1 due to root
resorption. There were no adverse events that occurred due to this treatment.
All 24 patients completed the study, however, one patient in the Overlay group
(1/12) was excluded following data analysis. This patient had a buccal wall missing at the
time of extraction and the amount of ridge width gain was large. This represented an
outlier value that skewed the data and did not represent what typically happens following
a ridge preservation procedure.

Clinical Indices
Plaque index, gingival index and bleeding on probing had low initial values for both
groups, about 0.1 ± 0.1, and were virtually unchanged at the 4-month implant placement
visit. There were no significant differences between initial and final values or between
the test and the control groups (p > 0.05).

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

Horizontal Ridge Width Changes


The Socket group had a statistically significant mean loss of crestal width of 1.6 ± 0.8
mm (p < 0.05) while the Overlay group had mean loss of only 0.3 ± 0.9 mm, which was
not statistically significant (p > 0.05, Table 1). The difference between the 2 groups was
statistically significant (p < 0.05). At 5 mm apical to the crest the Socket group had a
significant mean loss of 0.8 ± 0.5 mm (p < 0.05) while the Overlay showed a statistically
significant mean gain of 0.5 ± 0.6 mm (p < 0.05). The difference between the test and
control groups was statistically significant (p < 0.05, Table 1).

Vertical Ridge Height Change


On the mid-buccal the Socket group gained a mean of 0.5 ± 2.9 mm while the Overlay
group gained 0.3 ± 2.6 mm, which was not statistically significant for either group (p >
0.05). The difference between the test and control groups was not statistically significant
(p > 0.05, Table 2). Data and statistical significance for the mid-lingual, the mesial and
the distal portion of the socket are shown in Table 2.

CEJ to Osseous Crest Changes


Mesial CEJ to osseous crest distance for the Socket group showed a significant mean loss
of 0.3 ± 0.3 mm (p < 0.05), while the Overlay group also had a significant mean loss of
0.5 ± 0.4 mm (p < 0.05). Distal CEJ to osseous crest distance for the Socket group
showed a significant mean loss of 0.5 ± 0.7 mm (p < 0.05), while the Overlay group had a
mean loss of 0.3 ± 0.5 mm, which was not statistically significant (p > 0.05). There were
no statistically significant differences between groups for either mesial or distal sites.

Buccal Contour
For the Socket group 5 sites ended with a concave contour while 7 were flat. For the
Overlay group 4 sites ended with a flat contour while 7 were convex. In the Socket group
this represented a loss of contour for 9 sites and no change for 3. For the Overlay group 4
sites had no change in contour while 7 showed a gain.

Histologic evaluation
The Socket group healed with a mean of 35 ± 16% vital bone, 21 ± 13% non-vital bone
and 44 ± 9% trabecular space, while the Overlay group healed with a mean of 40 ± 16%
vital bone, 17 ± 11% non-vital bone, and 43 ± 12% trabecular space. There were no
statistically significant differences between the Socket and Overlay groups for vital or
non-vital bone or trabecular space (p > 0.05, Table 3).

DISCUSSION
The primary aim of this 4-month randomized, controlled, blinded clinical study
was to test the hypothesis that crestal ridge width could be preserved when a facial
overlay xenograft that resists resorption was used. It was demonstrated that crestal ridge
width can be almost entirely preserved when a slowly resorbing buccal overlay xenograft
is used therfore the hypothesis should be accepted. This is in contrast to previous ridge

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

preservation studies where about 18% of crestal ridge width was lost.6-9,11-32 Furthermore
at 5 mm apical to the crest there was a gain of 0.5 mm of ridge width. This supports the
concept proposed by Wang et al. that a slowly resorbing outer layer of grafting material
may resist resorption and have a beneficial effect on the final result.34 They also
proposed that a rapidly resorbing inner graft layer is beneficial since it will be replaced
by newly formed vital bone. In this study the socket graft was mineralized particulate
cancellous allograft that healed with a high percentage of vital bone present. This means
that at the site of implant placement, the previous socket area, there was a high
percentage of vital bone present to promote osseointegration.
One question that needs to be considered is when an overlay graft is indicated. It
adds time and expense to the ridge preservation procedure so there should be a
compelling reason to complicate the grafting procedure by using an additional graft
material. Data from ridge preservation sites from this study and other studies at the
University of Louisville (2 publications and 5 Master's theses) indicate that maxillary
sites tend to have more resorption than mandibular sites and that maxillary anterior sites
tend to have the highest percentage of lost ridge width when compared to other sites
(Table 4).9,18 Another consideration in maxillary anterior sites is that there is often a
significant undercut or ridge concavity that extends corono-apically. This phenomenon
can lead to a fenestration at the time of implant placement while narrow crestal ridge
width may lead to dehiscence.
According to Woelfel's Dental Anatomy textbook maxillary incisors are about 6.0
mm in buccal-palatal width at the cervix, canines are about 7.5, premolars are about 8.1
and molars are about 10.7 mm.44 Mandibular dimensions are about 5.5 mm for incisors,
7.5 for canines, 7.1 for premolars and 8.9 mm for molars. This means that the smaller the
initial ridge (socket) dimension the more likely that the site will need an overlay graft.
Thus incisor, canine and premolar sites are the most likely candidates for an overlay
graft, especially if a significant undercut is present. Mandibular incisor sites are the
narrowest, however, the greatest percent resorption occurs in the maxilla (Table 4). Thus
initial site width, likely percent resorption, and depth of the undercut are all factors that
may influence the decision to use an overlay graft. Site analysis following tooth
extraction utilizing these factors will lead to the best treatment decision.
Another advantage of the bovine xenograft is preservation of the original buccal
contour in a mesio-distal direction. Without an overlay graft this contour is likely to
become concave (Figure 1a) while use of the overlay most often results in a convex
(Figure 1b) or at least a flat contour. In this study all pre- and post-op contour clinical
photos were evaluated and scored for initial and final contour. This demonstrated that the
overlay graft preserved or gained ridge contour, which is an esthetic advantage, while the
Socket group lost contour at most sites.
If the goal of implant surgery is to place the implant totally within vital bone with
no dehiscence or fenestration defects then the selection of a ridge preservation procedure
can be an important decision. Development of an adequate ridge is also important if
implant placement will be done using a flapless procedure, which may have esthetic
advantages for the soft tissue and papillae. Another advantage of adequate ridge width is
that following implant placement having 2 mm of bone buccal to the implant will help
prevent soft tissue recession.45,46 Inadequate crestal ridge width, on the other hand, could

7
Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

lead to implant dehiscence and potentially peri-implantitis. While additional grafting can
be performed at the time of implant placement, the goal of the initial grafting procedure
should be to establish adequate ridge dimensions so that no further grafting will be
necessary at the time of implant placement. Therefore the overlay graft may be useful in
successful development of adequate ridge width.
The most difficult aspect of the ridge preservation procedure is maintaining or
gaining crestal ridge width. This means graft compression at the crest must be avoided
and graft displacement either apically or laterally must be prevented. This was
accomplished in this study by extending the flap one tooth mesial and distal to the
extraction site. For the papilla preservation flap, the papillary incision was similar to that
recommended by Bernimoulin et al. for a coronally positioned flap.43 Thus a new papilla
tip was created about 3 mm apical to the existing papilla tip. The existing papilla was
then de-epithelialized and the new papilla tip was positioned coronally to the tip of the
existing papilla. An apical periosteal release gave adequate flap mobility to allow
coronal positioning and to accommodate a thick layer of xenograft.
About 3 to 4 mm of xenograft thickness was placed as a buccal overlay, and
perhaps more thickness was achieved apically. Also the graft was extended mesially and
distally to the mid-root prominence of the adjacent teeth. This helped prevent apical and
lateral displacement of the graft. Crestally the flap was closed with minimal tension to
avoid graft compression. Another factor may have been the slight rigidity of the
polylactide membrane, which also helped resist crestal compression.
Two previous studies tested the effect of an overlay graft.16,17 One showed a gain
and one showed a slight loss of ridge width. Simon et al. showed a gain and the overlay
graft was applied to the buccal, the crest and to the palatal/lingual.16 The gain was about
1.1 mm of ridge width, however, the measurement was at 3 mm apical to the crest rather
than at the crest as was done in this study. Also different graft and membrane materials
were used. Thus, although the data are not directly comparable, the present study
confirms that the overlay graft approach can have a beneficial effect. Zubillaga et al. was
performed in a similar fashion to Simon et al. but they used different graft materials,
which resulted in a slight loss of about 0.5 mm of ridge width at 3 mm apical to the
crest.17
Histologic analysis showed a high percentage of vital bone in the mid-socket area
where the trephine core was harvested, which is where the cancellous allograft was
placed (Table 3). This indicated that the goal of the Wang et al. layered graft had been
achieved and that the implant would be placed in an area with a high percentage of vital
bone.34 None of the histologic sections showed any signs of the xenograft. This
indicates that it served to maintain and gain space and did not collapse into the socket
area as the bundle bone and the allograft resorbed. The cancellous allograft used
followed the healing pattern described by Burchardt et al. for cancellous autograft.37
Figure 2a-c demonstrates the vital bone, osteoblasts and appositional bone growth they
reported as prominent features of cancellous graft healing.
A resorbable polylactide barrier membrane was used to contain the graft particles
and to fulfill the objectives of guided bone regeneration. Thus the membrane was used to
promote more rapid bone formation by preventing the ingrowth of connective tissue or

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Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

epithelium due to its barrier function. Since the primary objective of this study was to
compare two grafting techniques the same membrane was used at all sites. The
membrane was easy to use and all sites healed without any membrane associated
complications. The portion of the membrane overlying the socket opening was left
exposed and this resorbed by 6 to 8 weeks. Soft tissue had formed in this area by the
time of membrane resorption and thus the graft was completely covered by either
membrane or soft tissue at all times.
While there are many different ridge preservation procedures to choose from, the
buccal overlay approach using a xenograft appears to be a viable option. When site
analysis is used it can be determined whether the overlay or the intrasocket approach is
the most appropriate treatment. The choice of graft materials to accomplish different
purposes within the same graft as proposed by Wang et al. appears to be a valid and
useful concept in implant site development surgery.34 Preservation of the original buccal
contour is an esthetic advantage of this periodontal plastic surgery procedure.

Conflict of Interest Statement:


This study was performed in Graduate Periodontics, University of Louisville without any grant funding.
No commercial interests were involved and the authors report no conflict of interest. Dr. Greenwell has
previously performed research for Sunstar Americas. Their membranes were used in this study but they
supplied no funding or materials for this study.

Sources of support:
This study received no support from outside sources. Drs. Poulias, Greenwell, Hill, Morton, Vidal,
Shumway and Peterson report no financial relationships related to any products involved in this study. Dr.
Greenwell performs research for Sunstar Americas, Chicago, IL.

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44. Scheid RC, Weiss G. Woelfel's Dental Anatomy. Eighth Edition. Philadelphia: Lippincott Williams &
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Address correspondence and requests for reprints to Dr. Henry Greenwell, Graduate
Periodontics, School of Dentistry, University of Louisville, Louisville, KY 40292
(address is complete); Phone 502 852-6928; Fax 502 852-1317; email
henry.greenwell@louisville.edu
Submitted September 26, 2012; accepted for publication December 12, 2012.

Figure 1a.
Concave ridge contour associated with intrasocket graft alone treatment at 4 months associated with the
extraction of tooth #5.

Figure 1b.
Convex ridge contour associated with the overlay graft treatment at 4 months associated with the
extraction of tooth #4.

Figure 2a.
Vital bone harvested from the cancellous allograft site, which contains osteocytes in the lacunae. 100X.

Figure 2b.
Osteoblasts lined up along the surface of vital bone. Arrows indicate osteoblasts. 200X.

Figure 2c.
Appositional bone growth with vital bone growing on non-vital residual graft particles. Arrows indicate
vital bone that has formed on non-vital bone. 200X.
Table 1
Horizontal Ridge Width for Intrasocket and Overlay Sites Mean ± sd in mm
Group Initial Final Change % Change Range
Intrasocket at Crest 8.7 ± 1.0 7.1 ± 1.5 -1.6 ± 0.8* -19 ± 11 -3.4 to - 0.5
Overlay at Crest 8.4 ± 1.4 8.1 ± 1.4 -0.3 ± 0.9† -3 ± 10 -2.0 to 0.9

Intrasocket at 5 mm 9.1 ± 0.9 8.4 ± 0.9 -0.8 ± 0.5* -8 ± 5 -1.8 to 0.0


Overlay at 5 mm 8.6 ± 1.9 9.1 ± 2.0 0.5 ± 0.6*† 7±8 -0.8 to 1.5

* = p < 0.05 between initial and 4-month values


† = p < 0.05 between overlay and intrasocket groups

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Table 2
Vertical Ridge Height Change for Intrasocket and Overlay Sites Mean ± sd in mm
Location Intrasocket Overlay Intrasocket Overlay

Mean Change ± sd in mm Range in mm

Mid-Buccal 0.5 ± 2.9 0.3 ± 2.6 -2.0 to 8.0 -3.0 to 5.0

Mid-Lingual -0.4 ± 0.6 -0.5 ± 0.7* -1.5 to 0.5 -1.5 to 0.5

Mesial -0.5 ± 0.4* -0.6 ± 0.4* -1.2 to 0.0 -1.1 to 0.0

Distal -0.8 ± 0.3* -0.4 ± 0.4*† -1.3 to -0.1 -1.0 to 0.0

* = p < 0.05 between initial and 4-month values


† = p < 0.05 between overlay and intrasocket groups
Table 3
Histologic Data at Implant Placement for Intrasocket and Overlay Sites Mean ± sd
Group Time n % Vital % Non-vital % Trabecular

Intrasocket 4 month 12 35 ± 16 21 ± 13 44 ± 9

Overlay 4 month 11 40 ± 16 17 ± 11 43 ± 12

Table 4
Ridge Dimensions by Tooth Type Mean ± sd in mm
Tooth Type n Initial Final Change % Change

Maxillary Incisor 38 7.7 ± 1.0 5.8 ± 1.4 -1.9 ± 1.2 -24 ± 15


Mandibular Incisor 2 5.9 ± 0.2 5.1 ± 0.0 -0.9 ± 0.2 -15 ± 3
Maxillary Canine 8 8.8 ± 0.7 6.4 ± 2.1 -2.4 ± 2.0 -28 ± 22
Mandibular Canine 3 7.8 ± 1.8 7.0 ± 2.5 -0.8 ± 1.7 -10 ± 23
Maxillary Premolar 99 9.4 ± 1.2 8.0 ± 1.3 -1.4 ± 1.1 -14 ± 11
Mandibular Premolar 24 7.8 ± 1.3 7.4 ± 1.3 -0.4 ± 1.0 -4 ± 13
*
RegenerOssTM, BioMet 3i, Palm Beach Gardens, FL 33410

Bio-Oss, Geistlich Pharma North America, Inc, Princeton, NJ 08540

Guidor®, Sunstar Americas, Inc, Chicago, IL 60630
§
Cytoplast® PTFE Suture, Osteogenics Biomedical, Inc, Lubbock, TX 79424

H & H Company, Ontario, CA 91761

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14
Journal of Periodontology; Copyright 2013 DOI: 10.1902/jop.2013.120585

15
J Clin Periodontol 2013; doi: 10.1111/jcpe.12111

Dimensional alterations of Tobias Thalmair1, Stefan Fickl2,


David Schneider4, Marc Hinze1 and
Hannes Wachtel1,3

extraction sites after different 1


Private Institute for Periodontology and
Implantology, Munich, Germany; 2Department

alveolar ridge preservation


of Periodontology, Julius-Maximilians
University, Wurzburg, Germany; 3Department
of Prosthodontics, Dental School, Free
University of Berlin, Berlin, Germay; 4Clinic of

techniques – a volumetric study Fixed and Removable Prosthodontics and


Dental Material Science, University of Zurich,
Zurich, Switzerland

Thalmair T, Fickl S, Schneider D, Hinze M, Wachtel H. Dimensional alterations of


extraction sites after different alveolar ridge preservation techniques – a volumetric
study. J Clin Periodontol 2013; doi: 10.1111/jcpe.12111.

Abstract
Objectives: The aim of this randomized controlled clinical study was to assess
soft tissue contour changes after different alveolar ridge preservation procedures.
Material and Methods: Following tooth extraction, 30 patients were randomly
assigned to the following treatments (Tx) - Tx 1: xenogenic bone substitute (pre-
hydrated collagenated cortico-cancellous porcine bone) and free gingival graft; Tx
2: free gingival graft alone; Tx 3: xenogenic bone substitute; Tx 4: no further
treatment (control). Impressions were obtained before tooth extraction (baseline)
and 4 months after surgery. Cast models were optically scanned, digitally super-
imposed and horizontal measurements of the contour alterations between time
points were performed using digital imaging analysis.
Results: All groups displayed contour shrinkage at the buccal aspect ranging
from a mean horizontal reduction of !0.8 " 0.5 mm (Tx 1) to !2.3 " 1.1 mm
(control). Statistically significant differences were found between Tx 1 and Tx 4
as well as Tx 2 and Tx 4. A significant positive influence of the free gingival graft
on the maintenance of the ridge width was recorded (p < 0.001).
Conclusion: In this study, alveolar ridge preservation techniques were not able to
Key words: alveolar ridge preservation;
entirely compensate for alveolar ridge reduction. Covering the orifice of the dimensional alterations; extraction socket;
extraction socket with a free gingival tissue graft seems to have the potential to soft tissue punch
limit but not avoid the post-operative external contour shrinkage based on optical
scans. Accepted for publication 28 March 2013

Marked morphological and dimen- changes in dimensions are expected the lingual aspect of the extraction
sional alterations of the alveolar in hard tissue as well as soft tissue socket (Araujo and Lindhe, 2005)
ridge occur after tooth extraction (Van der Weijden et al. 2009). The and limited to the marginal one-
(Cardaropoli et al. 2003, Schropp resulting dimensional changes have third of the post-extraction site (Ara-
et al. 2003, Araujo and Lindhe, been evaluated by volumetric analy- ujo et al. 2008). It was suggested
2005). Both horizontal and vertical sis in a clinical study (Schropp et al. that the higher amount of resorption
2003). The loss of volume in the hor- at the buccal aspect is due to the
Conflict of interest and source of izontal dimension amounts 5–7 mm relatively greater proportion of bun-
funding statement: within the first 12 months. This cor- dle or “tooth-derived” bone facially
responds with approximately 50% of that loses its function after tooth
The authors declare that they have no
the original width of the alveolar extraction and undergoes atrophy
conflicts of interest. This study was
bone (Schropp et al. 2003). The (Araujo and Lindhe, 2005). As the
supported in part by Tecnoss, Torino,
Italy.
resorption of the ridge is more buccal wall of the tooth socket is
pronounced on the buccal than on frequently partially or completely
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 1
2 Thalmair et al.

resorbed (Araujo and Lindhe, 2005), is the most predictable. Therefore, All patients received instructions
consequently a collapse of the the aim of this clinical investigation in oral hygiene and underwent initial
buccal soft tissue leads to marked was to evaluate, to which extent a periodontal evaluation including
bucco-oral alterations (Schropp filler or a soft tissue socket seal professional tooth cleaning with scal-
et al. 2003). In particular, in the contributes to ridge preservation. ing and polishing until full-mouth
anterior zone the mentioned altera- plaque score and full-mouth bleeding
tions of the extraction socket can score <20% were reached.
Materials and Methods
jeopardize the aesthetic outcome of
any dental treatment involving tooth The research protocol and the con-
Inter-examiner accuracy control
extraction. sent form of this clinical investiga-
To reduce volumetric changes tion were approved by the ethical All surgical procedures were per-
occurring after tooth extraction, committee of the Julius-Maximilians formed by four operators (H.W.,
different treatment modalities have University, Wuerzburg, Germany T.T., S.F. and M.H.) in the same
been recommended. As implant (183/11). clinic (Private Institute for Periodon-
installation was not able to alter tology and Implantology, Munich,
biological procedures (Ara! ujo et al. Germany).
Study population
2005, Botticelli et al. 2004), it was To control the accuracy and
suggested that incorporation of Subjects selected for participating in repeatability between surgeons, a cali-
biomaterials into a fresh extraction this prospective clinical study were bration meeting was held in Munich
socket could be a suitable technique counselled and written informed (October 2010). Procedures were
for socket augmentation with the consent was obtained prior to the explained using digital images and sur-
ability to maintain the ridge dimen- surgical procedure (Helsinki Declara- gical videos. Within the discussion at
sion to a certain extent (Nevins et al. tion of 1975 as revised in 2000). The the calibration meeting, it was decided
2006, Cardaropoli et al. 2005). Sev- patients were enrolled and treated in to make a variation to the original
eral studies have proposed various a period of time between January approved protocol (two-arm study
ridge preservation techniques follow- 2011 and September 2011. with Tx 1 and Tx 3) and to add two
ing tooth extraction including the The study population consisted additional groups (Tx 2 and Tx 4).
placement of graft materials and/or of 30 adult patients (mean age 46.2,
the use of occlusive membranes range 24–72 years, 13 females)
Clinical procedure
(Camargnola et al. 2003, Lekovic requiring treatment of tooth extrac-
et al. 1998, Lekovic et al. 1997, tion in the anterior zone ranging to Before surgery, impressions of the
Cardaropoli et al. 2005) showing the second bicuspid. The reasons for jaws were obtained in a one-step/
that a significant reduction in alveo- extraction included root fractures, two-viscosity technique with polye-
lar bone resorption could be endodontic treatment failures and ther impression materials (Perma-
avoided. However, data obtained advanced caries lesions. dyne Garant 2:1/Permadyne Penta
from experimental studies showed The following exclusion criteria H; 3M Espe, St. Paul, MN, USA).
that incorporation of biomaterials were applied: Following the administration of
into the extraction socket is not able (1) Age <18 years. local anaesthesia, an intra-sulcular
to diminish the biological process of (2) Smoking status of more than 10 incision was performed and the teeth
the buccal bone plate (Fickl et al. cigarettes/day. were gently extracted without
2008a, Fickl et al. 2008b). (3) Presence of relevant medical con- elevation of a mucoperiosteal flap or
Techniques to achieve soft tissue ditions: Patients with diabetes mell- compromising the marginal gingiva.
closure of extraction sites have been itus, unstable or life-threatening Care was taken to produce as little
developed, mainly related to conditions, or requiring antibiotic trauma as possible to the bone
immediate implant placement. Jung prophylaxis. Patients with medica- around the alveolus. If necessary, the
et al. (2004) introduced the soft tissue tion of drugs influencing the bone teeth were sectioned to allow atrau-
punch technique, the extraction metabolism were also excluded. matic extraction and, more impor-
socket was filled with a bone substi- (4) Pregnant or lactating women. tantly, preservation of all bone walls.
tute and covered with an epithelial- (5) History of malignancy, radiother- In case of deep fractured teeth, when
ized free connective tissue graft. It apy, or chemotherapy for malignancy the remaining supragingival tooth
was proposed that stabilizing the soft in the past 5 years. structure was insufficient for the use
tissue architecture with a free gingival (6) History of autoimmune disease. of a forceps, a specific root extraction
graft has beneficial effects on mini- (7) Presence of acute periodontal or device with intra-canalicular anchor-
mizing the soft tissue shrinkage (Jung periapical pathology. age (Benex-Extractor, Zepf Medizin-
et al. 2004). It was demonstrated that technik GmbH, Seitingen-Oberflacht,
placing a deproteinized bovine bone Only teeth with an intact buccal Germany) was used to avoid trauma
material (DBBM) into the extraction bone plate were included in the to the surrounding tissues. The extr-
socket and closing the socket with a study population. The condition of action sockets were carefully curetted
free gingival graft was beneficial in the buccal bone plate was evaluated to remove granulation tissue.
limiting the volumetric shrinkage intra-surgically after tooth extrac- Patients were enrolled sequen-
(Fickl et al. 2008b, Fickl et al. 2008a). tion. All extraction sites presented a tially. A randomization list was
To date, it is still uncertain which minimum width of 2 mm of kerati- generated. Randomization envelopes
alveolar ridge preservation technique nized gingival tissue. were supplied and numbered sequen-
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Different alveolar ridge preservation techniques 3

tially containing the treatment


allocation according to the randomi-
zation list.
The extraction sites were ran-
domly assigned to one of the follow-
ing treatments:
Treatment 1 (Tx 1): The extrac-
tion socket was treated using the
socket seal technique (Jung et al.
2004). The internal marginal gingiva (a) (b)
of the extraction socket was deepi-
thelialized with a diamond bur until
bleeding was evident. The extraction
socket was filled with a xenogenic
bone substitute (pre-hydrated colla-
genated cortico-cancellous porcine
bone; mp3 OsteoBiol, Tecnoss, Tor-
ino, Italy) to the level of the bone
crest. A free gingival graft with a
thickness of 3 mm was harvested (c) (d)
from the palate/tuberosity and
sutured to the marginal gingiva of the Fig. 1. Treatment group 1. (a) after gentile extraction of tooth 21 the buccal wall is
extraction socket with several inter- intact, (b) a xenogenic bone substitute is applied into the extraction socket, (c) a gingi-
rupted sutures (Seralene 7–0, Serag val autograft is sutured to the marginal soft tissue, (d) clinical situation 4 months
Wiesner, Naila, Germany) (Fig. 1). post-surgically.
Treatment 2 (Tx 2): The internal
marginal gingiva of the extraction Penta H; 3M Espe) were obtained mesial and distal papilla, by the
socket was deepithelialized with a 4 months after tooth extraction. mucogingival line and the most coro-
diamond bur and a free gingival nal contour line of the alveolar ridge.
graft was sutured into the orifice of Evaluation of tissue contour changes As the size of this area differed from
the extraction socket in the same site due to the difference in tooth/gap
manner as in Tx 1, however, without The analysis of the soft tissue contour size, the mean volume change per
the use of a filler material. changes was performed at the Clinic area was calculated as a distance in
Treatment 3 (Tx 3): The extrac- of Fixed and Removable Prosthodon- buccal direction (∆d [mm] = ∆vol
tion socket was filled with mp3 tics and Dental Material Science, [mm3]/area [mm2]) to allow a direct
(OsteoBiol, Tecnoss, Torino, Italy) University of Zurich, according to comparison of dimensional changes
and secured with a non-resorbable previous studies (Fickl et al. 2009, between the sites.
suture material (Gore-Tex CV5, Thoma et al. 2010). Before the beginning of the evalua-
W.L. Gore & Associates, Putzbrunn, Master casts of each patient were tion, a calibration exercise was per-
Germany) without the use of a gingi- made with dental stone (CAM-Base, formed to obtain reproducibility for
val graft (Fig. 2). Dentona AG, Dortmund, Germany) the measurement of the relevant buccal
Treatment 4 (Tx 4): The extrac- utilizing the pre-extraction and fol- area. This analysis was conducted by
tion socket remained with its blood low-up impressions after 4 months. two examiners (D.S. and T.T.), one of
clot only (control). The cast models were optically them was blinded (D.S.).
Consecutively, a pre-fabricated scanned and digitized (Iscan D101,
resin-bonded bridge was fixed to the Imetric GmbH, Courgenay, Switzer-
land) creating STL files (Standard Statistical analysis
adjacent teeth without any contact
of the pontics to the extraction Tessellation Language). The STL files Sample size calculation was per-
socket with an auto-polymerizing of these digital models representing formed on the results of previous
resin material (Clearfil Cores; Kura- the two treatment time points were studies (Fickl et al. 2009, Fickl
ray, Tokyo, Japan). imported into a specific software et al. 2008b) and resulted in seven
(SMOP, Swissmeda, Zurich, Switzer- subjects per group. For the primary
land) and were superimposed accord- outcome variable (mean dimensional
Post-surgical protocol ing to the buccal surface of the change) it was assumed that the
The patients were instructed to rinse adjacent teeth using the best-fit algo- true difference between groups
with 0.2% chlorhexidine digluconate rithm. The same software was used to would amount to 0.75 mm with a
twice a day for at least 2 weeks measure the dimensional changes in SD of 0.5. The Type I error proba-
(Vaughan and Garnick, 1989). To the relevant buccal alveolar ridge area bility was set at 0.05, the statistical
reduce swelling, Ibuprofen (600 mg) comparing the contour before tooth power at 80%.
was prescribed (Pearlman et al. extraction and 4 months after ther- Statistical analysis was performed
1997). Sutures were removed 7 days apy (Fig. 3). The area of measure- using a statistical software program
after surgery. Polyether impressions ment was defined by a line parallel to (SPSS 20, IBM Corporation, Arm-
(Permadyne Garant 2:1/Permadyne the tooth axis in the middle of the onk, NY, USA) by a statistician (M.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
4 Thalmair et al.

on the mean distance change. Spear-


man correlation was computed to
indicate associations between the
mean distance change and variables
(age, gender, jaw, jaw location and
method of extraction). Fisher’s exact
test was applied to find associations
between two binary variables. Krus-
kal–Wallis tested the influence of the
(a) (b) surgeons. The level of significance
was set at p < 0.05.

Results
All patients completed the study. Thirty
patients were included (13 females);
eight were smokers. The mean age was
46.2 years, ranging from 24 to 72 years
(Table 1 and Appendix S1).
(c) (d)
Qualitative assessment
Fig. 2. Treatment group 3. (a) tooth 14 needs to be extracted, (b) a xenogenic bone
substitute is applied into the extraction socket, (c) buccal view and (d) occlusal view at Healing of all treatment groups was
4 months post-surgically display the contour preservation. uneventful. No intra-operative or post-
operative complications occurred.
Clinically, 1 week after insertion of the
gingival graft, all areas were vascular-
ized, some parts were covered with
fibrin and responded by bleeding after
removal of the fibrinoid surface.
Necrotic parts or incomplete wound
closure were not observed.
After 4 months, all free gingival
grafts of group Tx 1 and Tx 2 were
(a) (b) fully integrated.

Quantitative assessment

The results of the dimensional evalua-


tion are displayed in Tables 2 and 3
and Appendix S1.
Horizontal contour shrinkage at the
buccal aspect during the 4 month heal-
ing period was observed in all groups
(c) (d) and ranged from !0.8 " 0.5 mm (Tx
1) to !2.3 " 1.1 mm (Tx 4/Control).
Fig. 3. Measured area of tissue volume changes. (a) and (b) superimposed images dem- The following dimensional changes
onstrating volumetric changes between baseline (yellow colour area) and 4 months occurred according to the treatment
(green colour area). (c) and (d) buccal and occlusal view of the measured area (region
of interest) in blue colour.
option (descriptive data between
stages):
Treatment 1 (Tx 1): Mean
Roos) at the Division of Biostatistics, rectness of the normality assumption. dimensional differences between
University of Zurich. Differences in mean distance change baseline and the 4 month scan were
The primary outcome variable was between groups were tested by apply- !0.79 " 0.5 mm (range: !0.13 to
horizontal soft tissue dimensional ing one-way analysis of variance !1.33 mm) buccally.
change at 4 months after tooth (ANOVA) and post hoc Scheffe test. Treatment 2 (Tx 2): Four
extraction. Influence of bone filler material months after tooth extraction, the
Descriptive statistics including box and soft tissue seal and other variables following dimensional changes were
plots were used to indicate the mean, like age, gender, jaw or tooth type recorded for the buccal aspect:
median, minimum, maximum values were the secondary outcome variables. !0.85 " 0.6 mm (range: !0.15 to
and the standard deviation in each Two-way ANOVA was used to iden- !1.60 mm).
treatment group. Kolmogorov–Smir- tify possible influence of the bone Treatment 3 (Tx 3): The mean
nov Test was used to check the cor- substitute filler and the soft tissue seal differences between baseline and the
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Different alveolar ridge preservation techniques 5

Table 1. Randomization of treatment options per extraction sites the application of a free gingival
Group Number Gender Smoker Maxilla Mandibula Reason for graft with or without a xenogenic
(M/F) (anter/ (premol) tooth bone substitute reduced post-opera-
premol) extraction tive tissue shrinkage to a certain
(endo/ extent. The outcome of this random-
fract/caries) ized controlled clinical investigation
demonstrated that the different alve-
Tx 1 8 3/5 2 7 (4/3) 1 5/3/–
olar ridge preservation techniques
Tx 2 8 7/1 1 7 (4/3) 1 4/2/2
Tx 3 7 5/2 2 5 (2/3) 2 3/2/2
resulted in less contour reduction
Tx 4 7 3/4 2 5 (2/3) 2 3/2/2 from the buccal aspect when com-
pared with unassisted socket healing.
endo, endodontic reason; fract, root fracture; caries, advanced caries lesion. The findings of this study can be
well compared to previous animal
Table 2. Descriptive statistics with measured area (mm2/mm3) and volume changes (mean, studies using a similar volumetric
minimum and maximum) data analysis. The horizontal contour
Group Area (mm2) ∆ Vol (mm3) Mean ∆ distance Min/max ∆ distance changes on the buccal aspect, after
(mm) (mm) extraction the socket was filled with
DBBM and covered with a free gin-
Tx 1 22.04 " 3.70 19.92 " 3.77 !0.79 " 0.5 !0.13 " 0.17/!1.33 " 0.21 gival graft, demonstrated !1.5 mm.
Tx 2 23.46 " 2.16 24.89 " 7.68 !0.85 " 0.6 !0.15 " 0.20/!1.60 " 0.19
Tx 3 19.63 " 1.29 32.89 " 6.96 !1.45 " 0.7 !0.73 " 0.15/!2.14 " 0.35
It was concluded that the application
Tx 4 19.72 " 3.35 41.41 " 15.96 !2.29 " 1.1 !1.23 " 0.26/!3.34 " 0.54 of DBBM seemed to limit the tissue
shrinkage (Fickl et al. 2008b).
A xenogenic porcine bone substi-
Table 3. Volumetric data describing the distribution according to mean dimensional change tute was used in this clinical trial, it
Group <0.5 mm 0.5–1.0 mm 1.0–1.5 mm 1.5–2.0 mm >2.0 mm was investigated as natural scaffold for
new bone formation. An almost com-
Tx 1 3 2 3 – – plete incorporation of the cortico-can-
Tx 2 2 3 2 1 – cellous particles surrounded by vital
Tx 3 – 2 2 2 1 bone was observed (Barone et al.
Tx 4 – – 2 1 3
2008). Compared to ridge preservation
with a bovine bone substitute, the
grafted sites comprised connective tis-
4 month scans were !1.45 " 0.7 mm Spearman correlation did not sue including the graft particles and
(range: !0.73 to !2.14 mm). show any significant association small amounts of newly formed bone
Treatment 4 (Tx 4): The mean between predictors (age, gender, (Carmagnola et al. 2003).
difference of the dimensional con- smoking, jaw, jaw location and The results of this study indicate
tour changes was !2.29 " 1.1 mm method of extraction) and the mean that the free gingival graft for cover-
(range: !1.23 to !3.34 mm). distance difference. ing the extraction socket revealed
The comparison of the groups by Kruskal–Wallis test revealed no statistically significant superior
unpaired t-tests (one-way ANOVA) statistically significant difference results in minimizing the buccal con-
resulted in significant differences in among the different surgeons tour shrinkage, irrespective of addi-
dimensional change between the test (p = 0.964). tionally a xenogenic bone substitute
groups Tx 1 and Tx 2 compared was applicated or not. The biological
with control group Tx 4. No other integration of the free gingival graft
Discussion
significant differences were observed was successful as no complication
between groups (Fig. 4). Indications for ridge preservation regarding graft necrosis could be
Two-way ANOVA showed a signifi- are maintaining a stable ridge vol- observed. It can be assumed that the
cant influence of the soft tissue ume for optimizing functional and soft tissue cover at the extraction site
socket seal leading to a lower degree aesthetic outcome and simplifying has the potential to limit the post-
in shrinkage (B = 1.05; p < 0.001). the treatment procedures subsequent operative contour alterations to a
The influence of the filler was esti- to ridge preservation. certain extent.
mated to be not significant This study evaluated different This is in accordance with the
(B = 0.42; p = 0.125). techniques for alveolar ridge preser- clinical study of Jung et al. (2004),
The extraction procedure – sepa- vation following tooth extraction, who reported that 3 weeks after sur-
ration of the root, extraction with generating sufficient soft tissue vol- gery, 99.7% of the soft tissue grafts
forceps or with a mechanical device ume for the time of implant place- were fully integrated (Jung et al.
– had no influence on the buccal ment thus simplifying implantation 2004). Landsberg and Bichacho
contour changes. procedures at earlier time points. (1994) stated that due to primary
There was no difference in the The use of xenogenic bone substi- wound closure and the additional
volume alterations regarding the tute, a free gingival graft and the mechanical stability of the free auto-
location of the tooth. No difference combination of both for alveolar graft, the soft tissue collapse might
was found between teeth located in ridge preservation were assessed. be avoided to a certain extent. A sta-
maxilla or mandibula. Preserving the extraction socket by tistically significant effect of the
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
6 Thalmair et al.

of this clinical trial did not show a


difference in location and type of
tooth.
The most important clinical
impact of alveolar ridge preservation
techniques on patient-related out-
come should be to optimize implant
placement in the correct position and
to avoid additional augmentation
procedure. However, a statistical sig-
nificance favouring one alveolar ridge
preservation technique does not nec-
essarily lead to a clinical benefit for
the patient, unless the whole treat-
ment is simplified or made more suc-
cessful. There is still a lack of
sufficient evidence on implant-related
outcome. Only few studies reported
Fig. 4. Volumetric changes indicated as mean change distance in millimetres. on a possible influence of alveolar
ridge preservation on placing
implants and need of further augmen-
gingival autograft with respect to the compartment of the experimental tation therapies (Serino et al. 2008,
maintenance of the tissue contours sites was analysed. This is a limita- Fiorellini et al. 2005). Therefore, the
at the buccal aspect was found tion of the study. Because measure- positive influence of alveolar ridge
(Landsberg and Bichacho, 1994). ments were based on master models, preservation techniques on patient-
Within the limits of this study no statements can be made as to related outcome may be attributed
evaluating the soft tissue contour vol- whether the documented horizontal more to achieving enhanced restor-
ume, primary wound closure by volume resorption was caused by ative and aesthetic outcomes, as well
means of a free gingival graft to seal loss of soft tissue or underlying as better maintenance of healthy peri-
the orifice of the extraction socket bone. However, no complete preser- implant soft tissues (Vignoletti et al.
might be more beneficial compared to vation of the outline of the alveolar 2012).
healing by secondary intention. This crest could be assessed in particular In conclusion, the present clinical
is contrary to several clinical trials at the buccal aspect. study demonstrates that the investi-
reporting successful treatment out- The applied technique showed a gated alveolar ridge preservation
comes with secondary wound healing high reproducibility and an excellent techniques were not able to prevent
(Camargnola et al. 2003, Serino et al. accuracy for measuring volume soft tissue contour alterations entirely
2003, Serino et al. 2008). changes with a measurement error after tooth extraction. It appears that
Ridge preservation by simply below 10 mm (Mehl et al. 1997, complete ridge preservation is not
using a xenogenic bone substitute Windisch et al. 2007). This method possible with the alveolar ridge pres-
seemed to be more effective than offers advantages including its non- ervation techniques evaluated. The
healing by clot alone, but this differ- invasive character, absence of radia- use of a free gingival graft covering
ence was statistically not significant tion and the fact that it can easily be the extraction socket was beneficial
in the present investigation. This applied. Currently, there is one for maintaining soft tissue volume.
lack of evidence may be due to the shortcoming of the technique More studies including a higher num-
small number of subjects. This find- because optical scans were per- ber of patients or sites are needed to
ing would be in accordance with sev- formed on study casts in this study. further investigate these findings.
eral clinical trials indicating a strong The accuracy of the method is highly
evidence that ridge preservation with influenced by the accuracy of the
grafting materials is more effective impressions and the casts. References
(Barone et al. 2008, Cardaropoli and Another limitation of the study is Araujo, M. G., Liljenberg, B. & Lindhe, J. (2010)
Cardaropoli, 2008). However, it was the small number of patients in each Dynamics of Bio-Oss Collagen incorporation in
demonstrated that in marginal por- group. Further clinical investigation fresh extraction wounds: an experimental study
tions of some sockets bone substitute should be conducted to recruit a in the dog. Clinical Oral Implants Research 21,
55–64.
particles surrounded by granulation larger patient collective to increase Araujo, M. G. & Lindhe, J. (2009) Ridge preser-
tissue occurred (Araujo et al. 2010, the statistical power of clinical inves- vation with the use of Bio-Oss collagen: a
Araujo and Lindhe, 2009). tigations. 6-month study in the dog. Clinical Oral
According to previous studies It is generally assumed that the Implants Research 20, 433–440.
Araujo, M., Linder, E., Wennstrom, J. & Lindhe, J.
showing that the resorption of the anterior segment of the dentition (2008) The influence of Bio-Oss Collagen on heal-
alveolar ridge is more pronounced responded differently than premolar ing of an extraction socket: an experimental study
on the buccal than on the lingual sites to horizontal ridge reduction. in the dog. The International Journal of Periodon-
aspect of the extraction socket (Ara- This may indicate that anterior sites tics & Restorative Dentistry 28, 123–135.
Araujo, M. & Lindhe, J. (2005) Dimensional ridge
ujo and Lindhe, 2005, Schropp et al.