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Purpose: This study describes the development of a methodology for using three-dimensional
(3D) image superimposition to measure volumetric changes in bone level around dental implants
in comparison with linear measures. Materials and Methods: The sample was comprised of 46
dental implants of 6-mm length and 4.1-mm diameter placed in the posterior maxilla and posterior
mandible in 20 patients. All implants received screw-retained single crowns. Radiographic images
were taken using cone beam computed tomography (CBCT) and digital periapical radiography
after implantation and after 12 and 24 months of functional loading (after crown placement).
Tridimensional reconstructions of the bone perimeter closest to the implant were developed,
superimposed, and volumetrically measured. Linear measures of bone levels were recorded in
periapical radiography images. A multilevel regression model tested volumetric and linear bone loss.
Results: The mean peri-implant linear bone loss for the first and second years was 0.2 ± 0.4 mm
and 0.1 ± 0.2 mm, respectively, and the mean volumetric bone loss for the first and second years
was 7.2 ± 6.1 mm3 and 6.4 ± 7.8 mm3, respectively. It was estimated that an increase of 1 mm
of linear bone loss was associated with a mean volumetric bone loss of approximately 14 mm3
(P < .001). Conclusion: The findings showed that linear and volumetric bone loss measures are
related. Measuring volumetric bone changes around implants is possible provided that the CBCT
images have proper contrast and sharpness, particularly around the implant outline. Improvements
in image quality and in the filters for bone tissue detection would be important for this methodology
to be made faster and used clinically. Int J Prosthodont 2018;31:23–30. doi: 10.11607/ijp.5366
Table 1 D
escription of the Demographic and Clinical Methodology
Sample Data
Variable This work was conducted as a methodological de-
Patients (n) 20 velopment pilot study. Data were obtained from the
Female 8 sample of a prospective cohort study with clinical
Male 12
Age (y) (mean ± SD) 52 ± 10 and radiographic follow-up,23 which was approved
by the Institutional Review Board and registered
Implants (n) 46
In maxilla 23 (16 in molar and 7 in premolar region) at the National System of Information on Ethics for
In mandible 23 (18 in molar and 5 in premolar region) Research in Humans. The study sample consisted of
46 Standard Plus Regular Neck SLActive implants
(Straumann Dental Implant System) of 6-mm length
and spatial resolution than multi-slice computed to- and 4.1-mm diameter placed in a nonprobabilistic
mography (MSCT) and allows for distinguishing ob- sample of patients (Table 1) following the one-stage
jects separated by subtle differences in distance and surgical protocol, as recommended by the manufac-
radiopacity, which is ideal for detecting and visualiz- turer. After a 90-day osseointegration period, transfer
ing peri-implant defects.6–8 molding was carried out for manufacture of the met-
Previous clinical implant follow-up studies with CT al-ceramic crown. SynOcta abutments and castable
have assessed bone level changes; however, only lin- cylinders (Straumann Dental Implant System) were
ear changes in buccal and palatal bone plates were used to fabricate screw-retained crowns.
analyzed—which would not be possible with periapi- The exclusion criteria were: Previous episodes of
cal radiography—and do not utilize the volumetric failure of osseointegration at the region of interest,
reconstruction capability of CT to analyze volumetric uncontrolled type 2 diabetes, immunosuppression,
changes in the bone tissue adjacent to the implant head and neck radiotherapy, active periodontal dis-
during a given period of time.9–12 In vitro and animal ease at the remaining dentition, poor oral hygiene,
studies on volumetric measurement of bone defects and use of a removable partial denture (RPD) or com-
using CT have shown its potential to provide such plete denture (CD) in the opposing dentition.
measurements.3,7,8,13 Radiographic images were taken using CBCT and
Superimposition of different 3D images obtained by digital periapical radiography. CBCT images were
CBCT is a method that allows for analyzing the longi- acquired in Digital Imaging and Communications in
tudinal evolution of a given treatment, providing volu- Medicine (DICOM) format by CBCT scanner i-CAT
metric changes in a given area of interest. In dentistry, CBCT (Imaging Sciences International) and KODAK
this method has been used for monitoring mandibular 9500 Cone Beam 3D System (Kodak Dental Systems,
advancement,14,15 condylar remodeling in orthogna- Carestream Health) at two different clinics specialized
thic surgery patients,16–19 and synthetic grafting in in dental imaging diagnostics. Baseline periapical ra-
the malar region, along with orthognathic surgery20 diographic images were obtained immediately after
in segmented alveolar areas that have been subject- surgery, and baseline CBCT images were acquired
ed to different alveolar preservation methods with or within 1 week after surgery. Follow-up radiographic
without implant placement.21 In 2013, Ahmad et al22 and CBCT images were taken at 12 and 24 months
monitored the bone remodeling process through 3D after the prosthesis was in function.
image superimposition in patients rehabilitated with Digital periapical radiographs were taken using the
implant-retained mandibular overdentures in the ca- long cone paralleling technique, with x-ray holders
nine (cuspid) region, comparing the images from be- (Rinn XCP) customized with silicone putty for each
fore the surgery and at 12 and 24 months after the patient. The Krystal X Easy (Owandy) digital sensor
prosthesis had been in function. However, analysis of and its software (Owandy Quick Vision) were used
dimensional changes was carried out in the most pos- for image acquisition. The Timex 70C (Gnatus, Brazil)
terior region—where the prosthesis was anchored— x-ray equipment was used, operating at 65 kVp and
and not in the region close to the implants, which may 7.5 mA and using exposure times of 0.10 seconds (for
be explained by the presence of artifacts in the im- maxillary and mandibular premolars and mandibular
plant region. molars) and 0.12 seconds (maxillary molars).
Therefore, this pilot study aimed to describe the
development of a new methodology for measuring Image Treatment and Measurement Procedures
volumetric changes in bone levels around osseoin-
tegrated implants using 3D image superimposition Image 3D reconstruction was performed using
and compared this new method with conventional Mimics (Materialise), a software for medical image
radiography. processing, and all DICOM images were imported
a b
c d a b
Fig 1 Mimics image with bone region selected around the implant, Fig 2 Stereolithography (STL) image of selected bone tissue import-
checking that only the bone tissue is selected in all sections, and sub- ed into Geometics. (a) Original imported image. (b) Selected image
sequent 3D reconstruction. (a) Coronal section. (b) Axial section. with closest perimeter to selected implant.
(c) Sagittal section. (d) 3D reconstruction of the selected area.
a b
Fig 3 (a) Bone perimeter around selected implant after removal of Fig 4 Images at different times, superimposed by alignment tool. The
area of no interest for measurement. (b) Image during mesh refine- blending of colors in the bottom image shows that superimposition is
ment for better image superimposition. being correctly made.
and processed. After uploading different sections, the Fig 5 Correct im-
age alignment is veri-
thresholding tool was applied. In bone scale mode, fied through a color
the area of interest around the implant was selected, map, where green
and then the image-processing tool crop mask was color means that im-
ages for the bone
applied. Within the selected area, each section was perimeter closest to
individually examined in the sagittal, axial, and coro- the implant are per-
nal planes, ensuring that only the bone tissue around fectly aligned or at a
distance < 0.041 mm.
the implant being assessed was highlighted in each
section. The processing of images of a single implant
at different times was performed in the same man-
ner by one trained operator, ensuring that all recon-
structions followed the same standards. After image
manipulation was completed, a 3D model of selected
peri-implant bone tissue was generated and saved in
Standard Tessellation Language (STL) format (Fig 1).
The STL model was exported to Geomagic Studio images were visually inspected to check the correct
(Geomagic), and the area of interest (ie, the bone pe- superimposition, showing areas of greater contact and
rimeter closest to the implant) was segmented (Fig 2). greater distance between images (Figs 4 and 5).
Then, the image mesh was refined, peaks were re- With this set of superimposed images of a single im-
moved, polygons were relaxed, and minor imperfec- plant, external walls were projected onto the selected
tions were manually corrected (ie, filled up) (Fig 3). area, creating a cube around the point of implant in-
Different image-processing routines were repeated sertion. In this cube, external walls were the same for
for all time points for a given single implant. Then, im- all images. As the cube walls were the same for all im-
ages were superimposed using an alignment tool with ages at different times, difference in cube volume was
semi-automatic registration wizard. Using a color map, due to the bone portion closest to the implant, which
Statistical Analysis
Table 3 M
ultilevel Regression Model to Evaluate Volumetric Changes in Bone Level Around Dental Implants in
Relation with Linear Measures
Volumetric bone loss (mm3)
Parameter Estimate Standard error 95% Confidence limits P
Intercept 183.5758 8.7877 166.3523 200.7994 < .0001
Linear bone loss 14.0200 3.2071 20.3059 7.7341 < .0001
Predictor: Linear bone loss (1 mm).
Conventional and radiographic images are still com- the increase in micronuclei was not significant, and
plementary in clinics. Vandenberghe et al28 compared mutagenicity (which would cause permanent dam-
digital periapical radiographic images with CBCT im- age to patients subjected to the tests) did not occur.
ages using a corpse’s jaw and a dry skull as the gold These results corroborate the findings of Silva et al,32
standard and concluded that both methods are ef- who analyzed cell changes in patients subjected to
ficient to determine the defect depth, presenting the one or two panoramic radiographs and showed that
same rates for defect underestimation and overesti- increased radiation led to increased cell changes but
mation. However, they observed that the lamina dura, mutagenic changes did not occur (ie, there was no
trabecular bone characteristics, and contrast among permanent damage). In any case, when selecting the
tissues are best visualized in periapical radiographs, type of scanning, as well as the equipment and its
while defects in the furcation area and the descrip- adjustment, the principle of minimum-required dose
tion of defect morphology are best visualized by to- should be observed for correct and accurate diagnos-
mography. Thus, they concluded that one test does not tic imaging.
replace the other in every aspect and that, in some This pilot study presents only the use of 6-mm
cases, both tests are required for accurate testing. implants in the posterior regions of the maxilla and
In another comparative study, Corpas et al3 analyzed mandible, where, despite having a greater magnitude
bone levels around implants to compare periapical ra- of masticatory forces, the incidence of forces is pre-
diographs and CBCT in an animal model, having histo- dominantly axial. It is worth noting the importance of
logic sections as a gold standard. For both techniques, studies with a greater number and variety of implants
the image and histologic measurements were strongly located in different regions (eg, in the anterior re-
correlated; however, both tests underestimated actual gions, where a greater incidence of oblique forces is
values (variation was 1.17 mm for periapical radio- expected and a different tissue response is therefore
graphs and 1.20 mm for CT scans). The researchers potentially generated).
point out, however, that 50% of the deviations were In summary, this investigation developed a prom-
lower than 0.5 mm, which is clinically insignificant. ising methodology for volumetric bone measurement
The literature shows that CBCT is efficient for di- around dental implants. However, as medical image-
agnosis and measurement of peri-implant bone de- processing programs cannot properly distinguish tis-
fects.3,8,13,27 Additionally, only tomographic scans, sues automatically, this methodology still depends
which allow for 3D reconstruction, enable visualization on the examiner, making the process relatively slow,
of such defects in the buccal, palatal, or lingual bone subjective, and dependent on adequate training. This
plate, as well as follow-up of changes in bone levels in methodology requires high tomographic image qual-
these regions over time. Mengel et al13 proved the ac- ity to ensure that small tissue changes are not from
curacy of CBCT for measuring bone defects, reporting artifact-related errors and are instead from anatomi-
that CBCT was even more accurate than MSCT. cal changes in the area being studied. Improvements
CBCT provides clinical information that would not in image quality and in the filters for bone tissue de-
be possible using conventional radiography. However, tection would be important for this methodology to
its use should be judicious because of the potential become faster and able to be used clinically. These
risks related to ionizing radiation. In a literature re- issues should be addressed in further studies to im-
view, Lorenzoni et al29 reported that MSCT showed prove the technical procedures and to allow the use
the highest levels of radiation, followed by CBCT of this methodology for several clinical situations that
and conventional radiography. They reported that might benefit from 3D measurement of bone level
increased kV, mA, exposure time, and field of view changes over time.
(FOV) led to increased radiation doses, and a numeric
dose comparison between the different scans would Conclusions
not be possible because the number varies depend-
ing on the equipment used and its adjustment during Based on the findings and limitations of this study, it
image acquisition. Li30 reported that CBCT radiation can be concluded that:
doses could be on average 10 times lower than con-
ventional tomography, but also 100 times higher than •• Measuring volumetric bone changes around
conventional radiography. implants is possible provided that CBCT images
To compare the mutagenicity and cytotoxicity of have good contrast and sharpness, particularly in
ionizing radiation in CBCT and conventional radiog- the implant outline.
raphy, Lorenzoni et al31 reported increased nuclear •• It was estimated that an increase of 1 mm of linear
changes in patients after both tests. CBCT presented bone loss was associated with a mean volumetric
a higher number of changes and cell death; however, bone loss of approximately 14.02 mm3.
25. Chuang SK, Cai T, Douglass CW, Wei LJ, Dodson TB. Frailty 29. Lorenzoni DC, Bolognese AM, Garib DG, Guedes FR, Sant’anna
approach for the analysis of clustered failure time observations EF. Cone-beam computed tomography and radiographs in
in dental research. J Dent Res 2005;84:54–58. dentistry: Aspects related to radiation dose. Int J Dent 2012;
26. Kamburoglu K, Kolsuz E, Murat S, Eren H, Yüksel S, Paksoy 2012:813768.
CS. Assessment of buccal marginal alveolar peri-implant and 30. Li G. Patient radiation dose and protection from cone-beam
periodontal defects using a cone beam CT system with and computed tomography. Imaging Sci Dent 2013;43:63–69.
without the application of metal artefact reduction mode. 31. Lorenzoni DC, Fracalossi AC, Carlin V, Ribeiro DA, Sant’anna
Dentomaxillofac Radiol 2013;42:20130176. EF. Mutagenicity and cytotoxicity in patients submitted to ion-
27. Draenert FG, Coppenrath E, Herzog P, Müller S, Mueller-Lisse izing radiation. Angle Orthod 2013;83:104–109.
UG. Beam hardening artefacts occur in dental implant scans 32. da Silva AE, Rados PV, da Silva Lauxen I, Gedoz L, Villarinho EA,
with the NewTom cone beam CT but not with the dental 4-row Fontanella V. Nuclear changes in tongue epithelial cells follow-
multidetector CT. Dentomaxillofac Radiol 2007;36:198–203. ing panoramic radiography. Mutat Res 2007;632:121–125.
28. Vandenberghe B, Jacobs R, Yang J. Diagnostic validity (or
acuity) of 2D CCD versus 3D CBCT-images for assessing
periodontal breakdown. Oral Surg Oral Med Oral Pathol Oral
Radiol Endod 2007;104:395–401.
Literature Abstract
Body-Mass Index and Risk of 22 Specific Cancers: A Population-Based Cohort Study of 5·24 Million UK Adults
High body mass index (BMI) predisposes individuals to several site-specific cancers, but a large-scale systematic and detailed
characterization of patterns of risk across all common cancers, adjusted for potential confounders, has not been previously undertaken.
The authors therefore aimed to investigate the links between BMI and the most common site-specific cancers. With primary care and BMI
data from individuals in the Clinical Practice Research Datalink, Cox models were fitted to investigate associations between BMI and 22
of the most common cancers, adjusting for potential confounders. Linear and then non-linear (spline) models were fitted to the data, and
effects of sex, menopausal status, smoking, age, and population were investigated. A total of 5.24 million individuals were included, and
166,955 developed cancers of interest. BMI was associated with 17 of 22 cancers, but effects varied substantially by site. Using a BMI scale
of < 18.5 to > 25, each increase in BMI of 5 kg/m2 was roughly linearly associated with cancers of the uterus (hazard ratio [HR] 1.62; 99%
CI 1.56–1.69; P < .0001), gallbladder (HR 1.31; 99% CI 1.12–1.52; P < .0001), kidney (HR 1.25; 99% CI 1.17–1.33; P <. 0001), cervix (HR 1.10;
99% CI 1.03–1.17; P = . 00035), thyroid (HR 1.09; 99% CI 1.00–1.19; P = .0088), and leukemia (HR 1.09, 99% CI 1.05–1.13; P ≤ .0001). BMI
was positively associated with liver (HR 1.19; 99% CI 1.12–1.27), colon (HR 1.10; 99% CI 1.07–1.13), ovarian (HR 1.09; 99% CI 1.04–1.14),
and postmenopausal breast cancers (HR 1.05; 99% CI 1.03–1.07) overall (all P < .0001), but these effects varied by BMI or individual-level
characteristics. Prostate and premenopausal breast cancer risk showed inverse associations with BMI, both overall (prostate HR 0.98,
99% CI 0.95–1.00; premenopausal breast cancer HR 0.89, 99% CI 0.86–0.92) and in never-smokers (prostate HR 0.96, 99% CI 0.93–0.99;
premenopausal breast cancer HR 0.89, 99% CI 0.85–0.94). By contrast, for lung and oral cavity cancer, no association was observed in
never-smokers (lung HR 0.99, 99% CI 0.93–1.05; oral cavity HR 1.07, 99% CI 0.91–1.26). Overall inverse associations were driven by current
smokers and ex-smokers, probably because of residual confounding by smoking amount. Assuming causality, 41% of uterine and 10%
or more of gallbladder, kidney, liver, and colon cancers could be attributable to excess weight. It was estimated that a population-wide
increase in BMI of 1 kg/m2 would result in 3,790 additional annual UK patients developing 1 of the 10 cancers positively associated with
BMI. BMI is associated with cancer risk, with substantial population-level effects. The heterogeneity in the effects suggests that different
mechanisms are associated with different cancer sites and different patient subgroups.
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Bhaskaran, Krishnan.bhaskaran@lshtm.ac.uk —Steven Sadowsky, USA