Periodontology 2000, Vol.

32, 2003, 105110

Printed in Denmark. All rights reserved

Copyright # Blackwell Munksgaard 2003

PERIODONTOLOGY 2000
ISSN 0906-6713

Osteoporosis and periodontal

disease progression
Nico C. Geurs, Cora Elizabeth Lewis & Marjorie K. Jeffcoat

Osteopenia and osteoporosis are systemic skeletal

diseases characterized by low bone mass and
micro-architectural deterioration with a consequent
increase in bone fragility and susceptibility to fracture. According to the World Health Organization,
osteoporosis is considered to be present when bone
mineral density (BMD) is 2.5 standard deviations
(SD) below the young normal. Osteopenia is defined
as bone density levels between 1 SD and 2.5 SD
below normal BMD (29).
In the third National Health and Nutrition Examination Survey (NHANES III) the prevalence of osteoporosis when assessed at the femoral neck was 20%
of postmenopausal white women (16). An alternative
approach is to use morphological deformities in the
vertebrae to define osteoporosis. The prevalence of
the defined vertebral deformities was found to be
12% in both men and women. The increase in frequency with age was greater in women, from 5% at
age 5054 to 24% at age 7579. For men this was 10%
at age 5054 years, rising to 18% at age 7579 years
(18). The prevalence of this relatively silent disease is
very high and on the rise. Future projections indicate
a threefold increase in osteoporosis-related hip fractures (9).
The risk factors for osteoporosis can be divided
into non-modifiable and modifiable risk factors.
The non-modifiable include sex, age, early menopause, thin or small body frame, race, and heredity.
Lack of calcium intake, lack of exercise, smoking, and
alcohol are modifiable risk factors. Low bone mass,
certain medications, propensity to fall, and systemic
diseases such as hyperparathyroidism are modifiable
to some extent. These risk factors have been discussed previously (5, 6).
The risk factors for osteoporosis include many risk
factors associated with advanced periodontal disease. Since both osteoporosis and periodontal diseases are bone resorptive diseases, it has been

hypothesized that osteoporosis could be a risk factor

for the progression of periodontal disease.

Relation between systemic bone

mineral density and oral bone
mineral density
Studies discussing the relationship between systemic
BMD and oral BMD are summarized in Table 1. Most
studies reported to date concerning this relationship
are cross-sectional studies using different populations and different methods to assess BMD.
Kribbs et al. (15) was the first to address the relationship in osteoporotic women in a study assessing
total body calcium by neutron activation analysis. An
association was found with mandibular density when
measured by quantitative analysis on intraoral radiographs. In a comparison of 85 osteoporotic women
and 27 normal women, the osteoporotic group had
less mandibular bone mass and density and a thinner
cortex at the gonion than the normal group. The
osteoporotic group also had a greater percentage of
subjects who were edentulous. In dentate subjects a
greater amount of tooth loss was reported for the
osteoporotic group. No differences in clinical periodontal measurements were found between osteoporotic and normal groups (1214).
In a study of 12 osteoporotic subjects with a history
of fractures, von Wowern et al. (27) found less mandibular bone mineral content as measured by dual
photon absorptiometry than in 14 normal women.
In a longitudinal study of 69 women receiving
hormone replacement therapy, lumbar spine BMD
was assessed by dual photon absorptiometry. When
compared to quantitative measurements of standardized radiographs of the posterior region, a significant but moderate correlation was found only at the
second visit. During the observation period of an

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Geurs et al.

Table 1. Relation between systemic bone mineral density (BMD) and oral bone mineral density
Authors

Population

Major Result

Type of study

Jeffcoat et al. (6)

158 postmenopausal
women
Age 62.2  7.6 years

Significant correlation between

hip BMD and mandibular
basal BMD

Cross-sectional study

Shrout et al. (22)

45 postmenopausal
women with no or
mild periodontitis
Mean age 57.4  5.8

Complexity of the trabecular

pattern weakly correlated with
lumbar spine and femoral BMD

Cross-sectional study

Southard et al. (23)

41 dentate Caucasian
women aged
20 to 78 years

Significant correlation between the

density of maxillary and mandibular
alveolar process, lumbar spine,
hip, and radius in healthy women.

Cross-sectional study

Streckfus et al. (23)

28 healthy women
aged 2378

Strong correlation between alveolar bone

and the second metacarpal densities.
Both reduced in postmenopausal women

Cross-sectional study

Jacobs et al. (4)

69 women receiving HRT

aged 3264 at entry

Correlation between spinal density and

mandibular bone mass at the second
examination (average follow-up 5.1 years)

longitudinal study

von Wowern
et al. (27)

12 women with
osteoporotic fractures

Osteoporotic subjects had less bone

mineral content

Cross-sectional study

Kribbs et al. (14)

50 normal women
aged 2090

Mandibular bone mass correlated with

bone mass at spine and wrist

Cross-sectional study

Kribbs (12)

85 osteoporotic women
and 27 normal
women aged 5085

Osteoporotic group had less mandibular

bone mass and density

Cross-sectional study

Kribbs et al. (13)

85 osteoporotic women

Total body calcium, bone mass at radius,

and bone density at spine correlated
with mandibular mass

Cross-sectional study

Kribbs et al. (15)

30 postmenopausal
women

Total body calcium associated with

mandibular bone density

Cross-sectional study

average of 5 years, a positive effect of estrogen replacement therapy on the bone mass of the mandible
and the lumbar spine was observed. Different estrogen regimens resulted in different increases in bone
mass (4).
Streckfus et al. (24) used quantitative measurements of vertical bitewing and hand radiographs in
patients with active periodontitis. The results of the
study showed that postmenopausal women on estrogen therapy had more alveolar bone loss (ABL), more
missing teeth, and reduced alveolar and second metacarpal bone density than premenopausal women.
Alveolar bone densities were also strongly correlated
to second metacarpal densities.
Most studies relate systemic BMD with mandibular mineral density. In a study of both maxilla and
mandible, 41 dentate Caucasian women aged 2078
were evaluated using quantitative intraoral radiography and systemic bone densities determined by dualenergy X-ray absorptiometry (DXA) (23). The density
of maxillary alveolar process bone was significantly

106

related to the density of the mandibular alveolar

process, lumbar spine, hip, and radius in healthy
women and maxillary alveolar process bone density
declined with age (23).
Shrout et al. (22) used morphologic measurements
from digitized images of bitewing radiographs to
correlate with lumbar and femoral BMD in 45 postmenopausal women who had no or only mild periodontal disease (no probing depths > 5 mm). The
complexity of the trabecular pattern weakly correlated with lumbar spine and femoral BMD.
In a preliminary report of the oral ancillary study of
the Womens Health Initiative, 158 patients with a
mean age of 62.2  7.6 years were evaluated (6).
Hipbone mineral density was confirmed by DXA
and mandibular bone density was measured by
quantitative digital intraoral radiography. A significant correlation was found between mandibular
basal bone and hipbone mineral density (6). The
authors posed the question whether intraoral radiography could serve as a screening tool for osteopenia.

Osteoporosis and periodontal disease progression

The usefulness of the alveolar trabecular pattern

analysis and mandibular alveolar bone mass for prediction of the skeletal BMD was further evaluated by
Jonasson et al. (8). They used an index to assess the
alveolar trabecular patterns and found a significant
correlation with skeletal BMD. The evaluation of the
coarseness of trabeculation of the alveolar bone as
seen on intraoral radiographs could be a helpful clinical indicator of skeletal BMD and better than densitometric measurements of the alveolar bone. Dense
trabeculation is a strong indicator of high BMD,
whereas sparse trabeculation may be used to predict
low BMD.
The data gathered on the mostly cross-sectional
studies appears to indicate a relationship between
systemic BMD and oral BMD. Additional data from
ongoing longitudinal studies will further elaborate
this relationship.

Periodontal disease and

osteoporosis
The relationship of tooth loss and BMD has been
studied. Several reports find a correlation between
tooth loss and diminished systemic BMD (5, 11, 24,
25). Other reports fail to find this correlation (1, 10,
19). The use of tooth loss as a surrogate for periodontal disease extent has several limitations. The
underlying reason for the loss of the teeth is often
unknown. The extent of the disease around the
remaining teeth is not taken into account in these
analyses. Therefore, an accurate measurement of the
extent of periodontal destruction can not be made by
using tooth loss as a variable in the analysis of the
relationship between osteoporosis and periodontitis.
Several mostly cross-sectional reports have used a
variety of parameters to evaluate the periodontal disease severity in subjects with decreased BMD. These
reports are summarized in Table 2.
In a report by Elders et al. (1), lumbar BMD and
metacarpal cortical thickness (MCT) were compared
to alveolar bone height measured on bitewing radiographs and clinical parameters of periodontitis. No
significant relation was observed between the bone
mass measurements and alveolar bone height or periodontal parameters. The mean age in this group was
relatively young, between 46 and 55 years of age,
which could have contributed to the lack of correlation.
Similar findings were reported in a study of tooth
loss and attachment loss when related to vertebral

and proximal femoral BMD. In that study, 135

women with at least 10 teeth and no evidence of
moderate or severe periodontal disease were examined. Attachment loss was correlated with tooth loss
but not with vertebral or proximal femur bone density (3).
When comparing the number of sites with loss of
attachment with BMD in 292 dentate women (average age 75.5 years) no statistically significant association was found (28).
In an age cohort of 70-year-old women, 15 subjects
with osteoporosis were compared to 21 subjects with
normal BMD (17). No statistically significant differences were found in gingival bleeding, probing
pocket depths, gingival recession, or marginal bone
level between the women with osteoporosis and the
women with normal BMD (17).
In contrast to these reports, other authors have
reported a significant relation between systemic
osteopenia and periodontal bone loss. Von Wowern
et al. (27) found greater amounts of loss of attachment in osteoporotic women in a small population
with a mean age of 68. Osteoporosis was assessed
using bone mineral content of the mandible and
forearm determined by dual photon scanning.
In a study population of 70 postmenopausal
Caucasian women aged 5178, skeletal systemic
BMD was assessed by DXA (26). Clinical attachment
loss and interproximal ABL represented periodontal
disease severity. Mean ABL significantly correlated
with systemic BMD. A trend for a correlation
between clinical attachment levels and BMD was
found (26).
The cross-sectional studies have limitations. No
information about the diseases studied prior to the
exam is available. Although both osteopenia and periodontal disease are chronic diseases and can be
assumed to have been present prior to the observations, it is incorrect to conclude that both diseases
have been present. To better evaluate this relationship, prospective longitudinal studies are needed. To
date, few longitudinal studies have been performed.
In a 2-year longitudinal clinical study, the alveolar
bone height and density changes in 21 osteoporotic/
osteopenic women compared with 17 women with
normal lumbar spine BMD were studied. The subjects were postmenopausal women enrolled in a
periodontal maintenance program. Osteoporotic/
osteopenic women exhibited a higher frequency of
alveolar bone height loss and crestal and subcrestal
density loss relative to women with normal BMD.
Estrogen deficiency was associated with increased
frequency of alveolar bone crestal density loss in

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Geurs et al.

Table 2. Relationship of periodontal destruction and bone mineral density (BMD)

Authors

Population

Major result

Type of study

Lundstrom et al. (17) 15 women with

osteoporosis, 21 women
with normal BMD

No statistically significant
differences in gingival bleeding,
probing pocket depths, gingival
recession and marginal bone level

Cross-sectional
study

Tezal et al. (26)

70 postmenopausal Caucasian
women aged 5178

Mean ABL was significantly

correlated with BMD.

Cross-sectional
study

Weyant et al. (28)

292 dentate women (average

age 75.5 years)

No statistically significant association

between periodontal disease and
systemic BMD.

Cross-sectional
study

Payne (20)

Female periodontal maintenance

patients within 5 years of
menopause; 21 with normal
BMD, 17 osteoporotic women

Greater ABL, crestal and

subcrestal density loss in the
osteoporotic and estrogen-deficient
women.

2-year longitudinal
clinical study

Reinhardt et al. (21)

Women within 5 years of

menopause, 59 with adult
periodontitis and 16
non-periodontitis. Stratified
by serum estradiol levels

In non-smoking osteopenic/
osteoporotic periodontitis patients
with estrogen deficiency had
more bleeding on probing and
clinical attachment levels

2-year prospective
longitudinal study

Hildebolt et al. (3)

135 postmenopausal women

aged 4170 years, no moderate,
severe periodontitis

Attachment loss was correlated with

tooth loss but not with BMD.

Cross-sectional
study

Streckfus et al. (24)

28 healthy women
aged 2378

More ABL, more missing teeth, in

postmenopausal women on
estrogen therapy than
premenopausal women.

Cross-sectional
study

von Wowern
et al. (27)

12 women with osteoporotic

fractures

Osteoporotic subjects had more

loss of attachment than normal
subjects

Cross-sectional
study

Elders et al. (1)

216 females between 46

and 55 years

No significant correlation was

observed between probing depth,
bleeding on probing, missing
teeth, alveolar bone height and
bone mass

Cross-sectional
study

the osteoporotic/osteopenic women. The authors

concluded that osteoporosis/osteopenia and estrogen deficiency are risk factors for alveolar bone density loss in postmenopausal women with a history of
periodontitis.
Fifty-nine moderate/advanced adult periodontitis
patients and 16 non-periodontitis subjects, all within
5 years after menopause at baseline, were stratified
based on serum estradiol levels. Attachment loss was
assessed over a 2-year period and correlated to BMD
and serum estradiol levels. Serum estradiol levels did
not influence the percentage of sites losing attachment for either periodontitis or non-periodontitis
groups. The estradiol-deficient group had a trend
toward a higher frequency of sites with attachment
loss 2 mm.
Larger prospective longitudinal studies are needed
to further evaluate osteoporosis as a risk factor for

108

periodontal disease progression. The oral ancillary

study of the Womens Health Initiative at the
University of Alabama at Birmingham was designed
to determine if there is an association between systemic osteoporosis and oral bone loss. In this report,
preliminary prospective longitudinal data will be
presented. The Womens Health Initiative is a study
of womens health after menopause in the United
States. Risk factors for diseases in this population
are being studied nationwide and include heart disease and osteoporosis. Utilizing the unique opportunity for collaboration with the Womens Health
Initiative at the University of Alabama at Birmingham, an oral ancillary study was established.
All subjects enrolled in the study were post-menopausal females. Hipbone mineral density was confirmed with DXA. Comprehensive medical histories
and examinations were linked with the results of oral

Osteoporosis and periodontal disease progression

Table 3. Alveolar bone loss (ABL) by periodontal and

osteoporosis status
Osteoporosis

Periodontitis

ABL (mm)

SD

No

No

14 0.18

0.21

No

Yes

11 0.31

0.20

Yes

No

23 0.66

0.62

Yes

Yes

10 1.08

0.46

examinations and quantitative digital intraoral radiography. The intraoral techniques used in this study
have been validated and are over 90% sensitive and
specific in detecting small changes in bone mass and
density (2, 7). Standardized vertical bitewing radiographs were taken at baseline and the 3-year followup visit. The radiographs were digitized and corrected for small angulation errors and contrast. Subtraction radiography was used for the enhancement
of the standardized radiographs. Alveolar bone
height was measured using Periovision software.
Measurements were made on the mesial and distal
aspects of posterior teeth. Alveolar bone height was
defined as the measurement from the cementoenamel junction to the point of bony attachment to
the root of teeth. The patients were recalled and a
similar examination including the radiographic surveys was performed every 3 years.
The amount of ABL along the root surface over the
3-year period was calculated for 58 subjects using
digital subtraction radiography. The subjects were
divided into two groups based on BMD at the hip
measured at baseline. The osteoporosis group was
defined as hipbone mineral density 2.5 SD below
the normal as confirmed by DXA. Subjects with
BMD above this level were considered the nonosteoporosis group. The subjects were also stratified
based on ABL as a measure of the periodontal disease
status at baseline. A subject was considered to have
periodontitis when 3 mm or greater of alveolar bone
height was measured at baseline.
Figure 1 and Table 3 represent the 3-year longitudinal ABL data for the subjects based on periodontal and osteoporosis status. Subjects with
osteoporosis presented with greater progression of
ABL than subjects with no osteoporosis over the 3year period. The subjects with periodontal disease at
baseline exhibited greater amounts of ABL than subjects with periodontal disease. The greatest amount
of ABL was found in the group of subjects with
periodontal disease and osteoporosis. A general linear model was constructed for the outcome variable
change in logarithmic alveolar bone height. Indepen-

Fig. 1. Three-year alveolar bone loss.

dent variables included smoking, age, current hormone replacement therapy, calcium intake, and
ethnicity (P < 0.0008). In the post hoc comparison
of subjects without periodontitis at baseline, the subjects with osteoporosis had greater mean ABL (0.18 
0.21 mm versus 0.66  62 mm; P < 0.02). This was
statistically significant. When periodontitis was present at baseline, the difference in mean ABL between
the osteoporosis and non-osteoporosis groups was
even greater. The mean ABL for patients with periodontitis and osteoporosis was 1.08  0.46 mm compared with 0.31  0.20 mm in the non-osteoporosis
group. This was statistically significant (P < 0.01).
These data present a preliminary report of this
ongoing study and indicate a greater propensity to
lose alveolar bone in subjects with osteoporosis especially in subjects with preexisting periodontitis. This
would indicate that osteoporosis or low systemic
BMD should be considered a risk factor for periodontal disease progression. In the future we will report
the data of the ongoing study for the complete study
population and duration.

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