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In osteoporotic patients, the skeletal
condition is characterized by low
bone mass and microarchitectural
deterioration of bone tissue. Osteo-
porosis is associated with decreased
mechanical strength, thus making
the skeleton more likely to fracture.
Postmenopausal and age-related
osteoporosis are the most common
primary forms of bone loss.
1
In the
case of systemic osteoporosis, both
periodontal tissues and alveolar
processes can undergo silent resorp-
tion that often progresses with no
clear symptoms. Much research has
linked both osteoporosis/osteope-
nia and estrogen deficiency with
alveolar bone loss.
212
Most works,
however, have been cross-sectional
in design, and, even if they allow for
the identification of possible ele-
ments correlated to the systemic dis-
ease, they have not been as suc-
cessful in establishing irrefutable
links between the two diseases.
13
Although relationships between
maxillary bone loss and systemic
osteoporosis have not been clearly
demonstrated, a growing number
of studies suggest that postmeno-
pausal women run a greater risk of
Osteoporosis: The Effect on Maxillary
Bone Resorption and Therapeutic
Possibilities by Means of Implant
ProsthesesA Literature Review and
Clinical Considerations
Francesco Sanfilippo, DDS*
Andrea E. Bianchi, MD, MDM**
Osteoporosis is a systemic disease in which the skeletal condition is characterized
by a decreased mass of normally mineralized bone. It is considered the most
common metabolic bone disease, and it constitutes a major public health prob-
lem. Given the evidence that alveolar processes provide the bony framework for
tooth support, the decline of skeletal mass has to be correlated with an increased
risk of oral bone loss and has a negative consequence on tooth stability. Data
from past research confirm that aging and estrogen depletion have a negative
influence on both tooth retention and residual alveolar crest preservation. The
goal of the present article is, however, to underline how the morphostructural
evolution of the edentulous maxilla is mainly due to mechanical factors as the
result of alterations in maxillary function. The advantages of prosthetic rehabilita-
tion supported by osseointegrated implants are also considered, focusing the
therapeutic role of this procedure on preserving the residual alveolar ridge from
atrophy. (Int J Periodontics Restorative Dent 2003;23:447457.)
**Private Practice, Milan, Italy.
**Head, Department of Periodontology and Implantology, Istituto
Stomatologico Italiano, Milan, Italy.
**Reprint requests: Dr Francesco Sanfilippo, Via Friuli 2, 20135 Milano,
Italy. e-mail: bifasa@tiscalinet.it
447
Volume 23, Number 5, 2003
both systemic osteoporosis and
more rapid alveolar bone loss. A 10-
year review of publications between
1989 and 1998
14
confirmed a posi-
tive relationship between systemic
osteoporosis and oral alveolar bone
mass. The authors also reported a
positive effect of estrogen-replace-
ment therapy on alveolar bone and
tooth retention in osteoporotic pa-
tients, just as the therapy is success-
ful with other skeletal sites. Clinical
longitudinal research investigated,
over 2 years, alveolar bone height
and density changes in osteo-
porotic/osteopenic women.
15
Data
concerning alveolar bone height,
number of residual teeth, bleeding
on probing, and plaque were com-
pared with those of a control group
consisting of people with normal
spine bone mineral density. The rela-
tionship between alveolar bone
changes and estrogen status was
also explored. This research sug-
gested a strong correlation between
alveolar bone density reduction and
height loss in postmenopausal
women with a history of periodontal
disease. Moreover, an increase in
alveolar bone density loss was seen
in those subjects deficient in estro-
gen serum levels compared with
those with normal estrogen levels.
The response to plaque, demon-
strated by bleeding on probing, was
also more vivid in osteoporotic/
osteopenic women. Another work
provides data regarding an increase
in the negative influence of the sys-
temic disease on alveolar bone
metabolism in postmenopausal
female smokers.
16
Experimental animal
studies on osteoporosis
and alveolar bone loss
Works dealing with the association
of changes in oral bony mass and
structure with the metabolic status of
the skeletal mass in mammals are
currently available. It is interesting
to observe how data retrieved in
humans agree with the findings of
experimental animal models. Many
authors have documented that
estrogen deficiency results in bone
loss in small-sized rodents, as in
humans. The loss of both cortical
and cancellous bone in the gonad-
ectomized rat provides a useful
model of estrogen depletion
related osteoporosis with effects at
systemic
1719
and local levels.
2026
Speculative aspects concerning
experimental animal model usage
are covered in a previous article.
27
A histomorphometric analysis
conducted on both maxillary and
mandibular bones of completely
dentate male and female rats af-
fected by gonadectomy-induced
osteoporosis pointed out how alve-
olar bone loss occurred only in fe-
male maxillae.
28
No relevant signs
of alveolar bone depletion were
observed in the mandibles of either
sex or in male maxillae. To provide
at least a hypothetic explanation of
this peculiar behavior, the authors
suggest considering the physio-
logic rules governing bone metab-
olism. Skeletal and mineral home-
ostasis of bone tissue is under the
control of both systemic hormones,
such as gonadic estrogens, and lo-
cal mechanical conditions.
29,30
A
reduction of estrogen serum con-
centration or a decrease in load-
related strain promotes osteoclastic
erosion. In contrast, if estrogen
depletion occurs but local loading
conditions are strong enough to
produce an adequate strain, bone
structures will be preserved.
In accordance with this hypoth-
esis is the behavior of both maxillary
and mandibular bones. The maxilla
is a stable bone, anchored to the
rest of the skull, and receives load
mainly from occlusal contacts con-
ducted to the alveolar and basal
bone by the dental roots. The man-
dible is instead a moving bone, and
both occlusal contacts and muscle
actions perform proper strain con-
ditions in its structures. Microarchi-
tectural deterioration occurs in fe-
male maxillae only,
28
and it can be
linked to the evidence that strain
conditions in alveolar bone are not
strong enough to ward off ovariec-
tomy-related osteoporosis. The dif-
ferences observed in the maxillae of
the sexes can be explained by a
higher bony mass at the origin or a
lower influence of estrogen decrease
in males.
448
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.
Factors correlated to
edentulous crest resorption
The morphologic evidence of eden-
tulous alveolar bone adaptation pro-
vides proof of the long-term result of
tooth loss and configuration of resid-
ual ridges,
31
in which the quantity of
bone tissue is constantly reduced.
Moreover, the architectural structure
declines in quality and mechanical
properties. This evolutionary trend
suggests that on both a general and
local level, potential regulatory fac-
tors of residual ridge resorption
could have contrasting repercus-
sions on either the augmentation of
osteoclastic erosion or on the de-
cline of osteoblastic deposition.
With regard to the systemic vari-
ables, one must consider:
The primitive morphology of
completely dentate maxillae
32
depends on ethnic origin
33
and
individual genetic attributes.
Moreover, it is influenced by
other factors, such as the growth
and development of the alveolar
processes with regard to teeth
location and intermaxillary rela-
tionships.
Gender and sex have to be con-
sidered as important variables
in the increase of oral bone
loss.
34,35
The altered metabolic condi-
tion
36
in diseases like osteo-
porosis or other systemic path-
ol ogi es produces a bone
remodeling uncoupling; as a
consequence, a modification of
mineral homeostasis may occur,
and an i ncrease i n skel etal
osteoclastic erosion of the peri-
osteal antral floor brings about a
progressive hollowing out of the
alveolar process from the upper
side.
5559
Characteristics of eden-
tulous atrophic maxillae
It is widely accepted that, as with
other skeletal segments, the maxilla
undergoes menopause- and age-
related bone metabolic effects. The
unbalanced conditions in the remod-
eling processes, in which resorption
activity exceeds new bone forma-
tion, lead to a reduction in the oral
and alveolar bone. However, unlike
other skeletal segments, the maxilla
and mandible do not support the
body weight; their functions are
linked to chewing, swallowing, and
phonation. The evolution of these
bones is strictly related to the pres-
ence of the teeth that conduct forces
produced by the muscles to the can-
cellous and cortical supporting bone
architecture of the alveolar process
and basal structure.
The general resorption trend of
the edentulous alveolar ridge can
be understood by using two univer-
sally approved residual ridge classi-
fications that provide a description of
the evolutionary tendency of the
maxilla. The Cawood and Howell
60
classification considers the gross
anatomy of residual alveolar bone on
the vertical and transverse planes
and in volume. Although it offers
good support for surgical planning,
such as implant placement or bone
grafting, it does not clearly take into
impoverishment can generate
osteopenic effects on the maxilla
and mandible.
37,38
With regard to the local factors,
one must consider:
Biologic width injury following
alveolar wound healing, which
results from pathology treatment
and time-related tooth loss.
39
Resti ng condi ti on atrophy
caused by physiologic strain
shrinkage occurring after the loss
of occlusal load as a conse-
quence of tooth loss.
Changes in neuromuscular pat-
terns and reflexes because of
gender and edentulousness
4043
produce alterations in oral motor
performance (chewing, swallow-
ing, and speech) and in strain
conditions on the maxilla and
mandible.
4447
Intense occlusal loading condi-
tions in dentate subjects, as in
bruxism, may act positively to
preserve alveolar and oral bone
mass from extreme resorption
once edentulousness occurs.
48
The duration of removable pros-
thesis wearing is directly related
to an increase in residual ridge
resorption.
4954
Intermittent
compression forces, produced
by completely mucosa-support-
ed prosthetic devices, have a
negative effect on bone substra-
tum stability because of the
effect of augmented osteoclastic
activity from below.
Growth pattern and edentu-
lousness-related maxillary sinus
pneumati zati on caused by
449
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.
account the quality of cortical and
cancellous bone. This insufficiency
is partially compensated for by the
Lekholm and Zarb
61
classification,
which appears more efficient in
terms of the architectural aspects of
residual ridges. However, it is lacking
in its consideration of some funda-
mental biologic and biomechanical
structural features, such as the dis-
tribution of cortical bone thickness
along the crest perimeter and the
number, size, and degree of trabec-
ulae connectivity of cancellous bone.
In accordance with the general
principles of both classifications, a
detailed analysis of the evolutionary
trend of edentulous alveolar ridges
is still needed. Most of the above-
mentioned systemic and local vari-
ables have to be taken into account,
and every maxillary area probably
has to be considered as a structural
and functional unit with its own ten-
dencies in bone resorption. In this
regard, the age- and sex-related
alveolar structural evolution of corti-
cal and cancellous maxillary bone
has been investigated in edentulous
human skulls.
62
Histomorphometric
measurements in 52 edentulous
maxillae showed that trabecular
bone volume, thickness, number,
and connectedness are clearly lower
in the posterior than anterior areas.
Cortical bone, particularly in the
molar regions, often exhibits several
perforations crestally or buccally
rather than l i ngual l y, where i t
appears well-represented.
Important sex-specific differ-
ences were reported in all investi-
gated alveolar areas.
62
In female
maxillae, the bone volume, trabec-
ular thickness, and trabecular num-
ber were extremely reduced com-
pared with male maxillae. Moreover,
in females, a large amount of free-
ending trabeculae were reported,
denoting a serious decrease in con-
nectedness and biomechanical sta-
bility. In the female maxillae, both
cortical and cancellous bone exhib-
ited a similar tendency, appearing
thinner and with a larger number of
perforations. The advanced mean
age of the analyzed subjects sug-
gests that postmenopausal estrogen
depletion and the related presenta-
tion of systemic osteoporosis can
probably be linked with the evi-
dence of high bone loss and micro-
architecture deterioration in female
maxillae.
Histomorphometric data
56,62
help to clarify certain aspects of atro-
phy evolution of the maxilla, espe-
cially because morphology evidence
agrees with existing knowledge con-
cerning the original anatomic orga-
nization of the maxilla. In addition,
variables such as aging, osteoporo-
sis, and load loss have been taken
into adequate account (Figs 1 and 2).
Under normal anatomic conditions,
maxillary teeth are projected toward
the buccal side to reduce the differ-
ent inclination with the mandibular
teeth. In the posterior region, this
condition is strictly correlated in the
maintenance of the longitudinal axes
of the teeth optimally aligned with
the direction of the force vectors that
result from the muscular action of
the masseter and temporalis on the
external side and medial pterygoid
on the inner side. To maintain opti-
mal conditions in the mechanical
450
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.
system during function, premolars
and molars are structured to receive
the most intense occlusal forces on
their supporting cusps and direct
them to the palate by their lingual
roots. As a consequence, the lingual
bone lamina usually need to be
thicker and more resistant. On the
contrary, vestibular cusps normally
This role implies a vestibular tipping
toward the vestibular side, and, con-
sequently, the vestibular bone wall
appears thin. When tooth loss
related atrophy occurs, the buccal
bone lamina and crestal surface eas-
ily undergo faster resorption, while
the lingual wall can preserve, at least
partially, its original thickness.
have a cutting action and receive
less-intense occlusal forces. The cor-
responding vestibular roots work as
stabilizing elements of the mechan-
ical structure, and the buccal bone
wall appears thinner than the lingual
one. The behavior of the anterior
teeth, which primarily act in cutting
and mandibular guidance, is similar.
451
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.
Fig 2a Serial tomographic transverse section at lowest level of
maxillary alveolar ridge highlights low bone quantity in anterior area
beside incisal fossa. In premolar region, residual ridge is reduced in
thickness and knife edged. In right molar region, sinus is greatly ex-
panded; on the left, it is absent because of fusion with nasal cavity.
Fig 2b Some millimeters above, section at anterior nasal spine
level highlights reduction of residual ridge to thin lamina. On the
right side, because of pneumatization, sinus extends from premolar
area until, posteriorly, frontal wall of the pterygoid process.
Fig 1 Orthopantomograph of 68-year-old man shows systemic
disease, early tooth loss, and long-standing denture wearing con-
tributing to high bone resorption. Maxillary alveolar process is com-
pletely destroyed, and basal bone is particularly reduced in height.
Elevated atrophic involution also occurred in the posterior areas of
the mandibular alveolar process; in the mandibular anterior area,
where some teeth are retained, supporting bone is preserved.
452
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.
Fig 3 Reconstructions obtained by elab-
orating tomographic sections show pro-
found changes undergone by alveolar
bone.
Fig 4d Serial coronal sections of the left
side at canine and lateral incisor level. Re-
sidual ridge is similar to opposite side as a
result of significant resorption. Another ex-
acerbating element could be stronger
pressure forces transmitted by maxillary
anterior denture because of survival of
some anterior mandibular teeth.
Fig 4e Serial coronal sections of the left
side at premolar level with greatly resorbed
knife-edged residual crest. Sinus pneumati-
zation not directed down alveolar process-
es, but extended medially toward the nasal
cavity and fused with it. Schneiderian mem-
brane is thick because of altered conditions.
Fig 4f Serial coronal sections of the left
side at molar level. Behind hard palate,
residual ridge is preserved in height and
width, probably because the morphology
acquired by pneumatic cavities interrupted
further antral expansion below.
Fig 4a Serial coronal sections of the right
side at molar level. Compact bone in section
one is the anterior wall of major nasolingual
channel. Several millimeters in front, under
sinus floor, some cancellous bone, such as
vestibular and lingual thecae, is preserved.
Fig 4b Serial coronal sections of the
right side at premolar level. Profile of
residual crest is clearly visible and recalls
Cawood and Howells Class V classifica-
tion. Wide, expanded monocameral sinus
dominates residual ridge at this level.
Fig 4c Serial coronal sections of the right
side at canine and lateral incisor level.
Atrophic conditions of crest demonstrate
strong resorption despite no hypothetic
expansion of the nasal cavity.
Another fundamental point is
that the maxilla is anchored to the
skull, while the mandible can move.
This condition, static versus dynamic
bone, imposes some different sys-
tems of adaptation. Muscles pro-
duce the movement of the mandible
and can adapt i ts posi ti on by
changes in force magnitude during
both action and rest. The maxilla,
meanwhile, can only deal with
changes in dynamic and static load
by virtue of the flexibility of its own
bone architecture. Cancellous bone
is prevalent in the maxilla because
the high degree of vascularization
allows a faster adaptation of the
bone substratum, which consists of
well-organized and well-connected
trabeculae that follow the force tra-
jectories departing from the alveoli.
These structural advantages make
maxillary bone highly sensitive to
force magnitude reduction after
tooth loss and the decrease in es-
trogen serum levels during post-
menopause. After molar extraction
in maxillary posterior regions, the
opposing bony walls of the residual
alveolar cavity have to supply the
new local metabolic requirements at
a wider distance than in premolar
and anterior regions. This con-
tributes to unfavorable conditions in
wound healing, and consequently
an increase in bone loss. The pres-
ence of the maxillary sinus just above
the molar roots and its enlargement
after tooth loss contribute to the
extreme reduction of residual alve-
olar bone height and volume (Figs 3
and 4).
Therapeutic possibilities of
implant prostheses
Just as tooth loss leads to a decrease
in alveolar bone function and, con-
sequently, triggers maxillary atrophy,
so the reinstatement of adequate
strain conditions inside the bone
protects the residual ridge from
extensive resorption. In partial or
complete edentulism, the only pros-
thetic devices able to reproduce
loading conditions in a similar way to
dental roots are endosseous im-
plants. It should be observed that
the induced-osteoporosis animal
model revealed a lower efficacy in
bone repair around dental implants.
Particularly in comparison with
sham-operated controls, new bone
formation in ovariectomized rats
showed a decrease; osseointegra-
tion did, however, occur, albeit in
delayed fashion.
63,64
Taking into
account that animals received no
estrogen-replacement therapy or
other antiosteoporotic drugs, this
research helps one understand the
biologic effect on the wound healing
processes, but may prove lacking
when applied to osteoporotic hu-
mans who receive implant rehabili-
tation after a pharmacologic and
dietary control. Furthermore, the
experiments did not consider the
functionalization of implants a fun-
damental factor in bone existence.
A retrospective case-control
study examining osteoporosis and
implant failure
65
reported no associ-
ation between dental implant loss
and peripheral bone density T
scores. The prevalence of the sys-
temic bone metabolic disease
453
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among cases and controls was only
24% and 18%, respectively, thus con-
firming data emerging from the
Toronto Study in 1993.
66
The results
reveal, however, that clinical ap-
praisal of local bone quality at sur-
gery may jeopardize the likelihood
of implant longevity more than
would peripheral bone density mea-
surement. Poor bone crest quality,
such as type 3 and 4 of the Lekholm
and Zarb classification,
61
demon-
strates implant retention 3.7 times
lower than type 1 and 2 bone sites.
Although osteoporotic patients do
not appear at a higher risk of implant
loss,
67
the prevalence of type 3 and
4 bone in the edentulous maxilla
and the moderate resistance of the
trabecular framework need evalua-
tion at treatment planning.
If the residual ridge exhibits
reduced bone volume, height, and
width, reinstatement of adequate
crest conditions by bone grafting
and sinus lifting may be indicated
prior to implant placement.
68,69
Ana-
tomic features in the maxillary resid-
ual ridge may represent a limit for
setting up fixed prosthetic rehabili-
tation. Nevertheless, it cannot be
disputed that the only way to save
bone from tooth loss, age-, and
osteoporosis-related atrophy is via
the maintenance of adequate strain
conditions inside the residual alveo-
lar processes. Implant devices, com-
bined with highly controlled load-
ing conditions
70,71
and correct
management of both surgical
72
and
prosthetic steps,
73
can supply this
physiologic requirement. Stanford
and Brand
74
provide useful evidence
of the positive influence of function-
alized implants on bone mainte-
nance and adaptation in moderate
and poor substratum quality. The
authors postulate that the ability
for dental implants to maintain a
long-term stable interface in the
maxilla lies in the ability of trabecu-
lar bone to maintain adequate local
material (strength) and architectural
(connectivity) properties.
If patient selection and periop-
erative management are controlled
in the therapeutic approach with
regard to systemic status
75
and local
indications,
76
endosseous implants
to support and retain dental pros-
theses become predictable and offer
the osteoporotic patient a realistic
treatment option. If surgical, techni-
cal, and hygiene factors are carried
further while respecting bone phys-
iology and biomechanics, tissue
modeling and remodeling and evi-
dent changes in bone morphostruc-
ture occur around the implant.
77,78
Comparative microscopic analy-
sis may only reveal the tissue orga-
nization.
79
When bone undergoes
positive conditioning in both cortical
and trabecular architecture, changes
are both drastic and macroscopic,
and evidence of compacting of the
peri-implant cancellous bone can be
easily observed radiographically.
80
Although large-scale longitudinal
studies dealing with implant survival
in osteoporotic subjects still need to
be carried out, the only limit in the
application of implant prosthetic
protocols may be the morphostruc-
tural condition of the residual alve-
olar ridge, as long as adequate sup-
porting therapy of the systemic
disease is provided.
454
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