Keywords osteoporosis - climacteric - mandible - panoramic radiograph - menopause
Palavras-Chave osteoporose - climatério - mandíbula - radiografia panorâmica - menopausa
Introduction
Osteoporosis is characterized by low bone mass and microarchitectural alterations
of the bone tissue, leading to enhanced fragility and increased risk of fracture.
The cortical layer of the bone becomes thinner, while the trabecular structure becomes
more porous.[1 ] Several predictors of risk of osteoporosis must be considered in the clinical practice,
such as: age, body mass index, family history and hypoestrogenism. The risk of osteoporosis
clearly increases after menopause. Osteoporosis is reported to occur more commonly
in the lumbar spine, ranging from 15% to 38%, and lower in the femoral neck, in which
it ranges from 10% to 18%.[2 ]
[3 ]
[4 ] Recently, mineral bone loss was reported to affect 35–52% of women aged over 50
years.[5 ] Osteoporosis involves the whole skeleton, also affecting the mandibular bones, in
which it is associated with tooth loss and failure of dental implants.[6 ]
Bone mineral density (BMD), measured by dual-energy X-ray absorptiometry (DXA), is
the standard technique for the diagnosis of osteoporosis. Regarding the oral health
assistance for postmenopausal women, the dental panoramic radiograph is utilized for
a variety of purposes, as part of the assessment of the status of the mandible.[7 ] A good correlation between panoramic mandibular indices and BMD results at the femur[8 ] and lumbar spine has been found.[9 ]
[10 ] In fact, the association of osteoporosis in the spine and femur with bone loss in
the mandible has been described over the past 50 years.[11 ] Many studies have correlated mandibular bone mass with general skeletal bone mass,[12 ]
[13 ] and have tried to anticipate the diagnosis of osteoporosis using panoramic radiograph
indices.[14 ]
[15 ]
Currently, the exact role of the mandibular panoramic radiograph in discriminating
osteoporotic women from those not affected by the condition is debatable.[3 ]
[16 ] Since many postmenopausal women over 50 years of age with no previous diagnosis
of osteoporosis in the spine and femur might have low skeletal bone mineral density,
the mandibular status should be verified before any dental treatment to reduce complications
or failures. This conduct is more important before tooth implants. The primary objective
of the present study is to verify whether the panoramic radiograph presents an adequate
concordance with the DXA in the diagnosis of low bone density.
Methods
Patient Selection
This cross-sectional study using accessibility sampling was conducted at a university
hospital in the Brazilian Midwest, and it included 198 postmenopausal volunteers between
the ages of 40 and 53 years, who were treated at a climacteric outpatient clinic between
January 2014 and July 2016. The study was approved by the Ethics Committee of the
institution (under CAAE 33915914.7.0000.5541). Only toothed women were included, excluding
those who did not agree to sign the free and informed consent form, the users of sex
steroids, thyroid hormones, corticosteroids, anticoagulants, or those using osteoporosis
medications. The sample size was calculated assuming a prevalence of osteoporosis
of 15%[17 ] and an imprecision of 5%, using the equation n = Z2 × p(1-p)/(d2 ).
Panoramic Radiograph
Panoramic radiographs were performed using the Kodak 8000 Digital Panoramic System
(Eastman Kodak Company, Rochester, NY, US) with 2 mA, 13.9 and kV ranging from 60
to 80. The examinations were performed by the same radiologist, and the images were
identified only with the initials of the names, so that no personal information was
disclosed to the examiner at the time of the evaluation. Moreover, the examiner had
no access to the patients' medical history and bone mineral density (BMD) results.
The panoramic radiographs were evaluated using the Radio Imp (Radio Memory, Belo Horizonte,
MG, Brazil) software, version 2.0. Two aspects were analyzed in the mandibular panoramic
radiograph: a qualitative aspect regarding the aspect of the mandibular cortical bone,
and a quantitative aspect regarding the width of the mandibular cortical bone. The
measurements were taken from the right and left sides of each mandible. In the diagnosis
of low mandibular bone mass, the panoramic radiograph was reported to present sensitivity
and specificity of over 80% and 73% respectively.[18 ]
Mandibular Cortical Index
The mandibular cortical index (MCI, [Figs. 1A ], [1B ], [1C ]),[19 ] is a qualitative index used to evaluate the inferior cortical bone of the mandible
posterior to the mental foramen on both the left and right sides. There are three
possible results. C1 = normal cortex: the endosteal margin of the cortex is matched
and tapered on both sides; C2 = moderately eroded cortex: the endosteal margin shows
semilunar defects resulting from lacunar resorption, or forms endosteal cortical residues;
C3 = severely eroded or porous cortex: the cortex forms dense layers of endosteal
and clearly porous cortical residues.
Fig. 1 Region below the foramen. C1–Panel A, smooth and regular cortical bone. C2–Panel
B, semilunar defects. C3–Panel C, clearly thin cortical bone with porosity. Source:
Klemetti et al (1994).[19 ]
Mental Index
The mental index (MI, [Fig. 2 ]) was used to evaluate the thickness of the mandibular cortical bone through a perpendicular
line drawn from the base of the mandible (a) at the height of the center of the mental
foramen; another line (b) is drawn tangent to the inferior border of the mandible,
and a third line (c), which is parallel to the second one (b), is drawn at the superior
border of the mandible. The measurement of the cortical bone thickness (mental index)
is made along horizontal lines b and c (Ledgerton et al, 1997).[20 ] The data are expressed in millimeters, with a normal value ≥ 3.0 mm.
Fig. 2 Mental index. One line (B ) is tangent to the lower border of the mandible, and another line is perpendicular
(A ) to the first one, passing through the center of the mental foramen. The measurement
of the cortical bone thickness (mental index) is made along the horizontal line (C ). Source: the authors.
Bone Mineral Density
The individual BMD results were compared with established standards for age and sex.
Despite the fact that the BMD can be measured in any part of the body, two regions
(the lumbar spine and the proximal femur) were established as more representative
and important. The result is a graph with the quantification of some areas expressed
in g/cm2 . The World Health Organization (WHO) established the diagnostic standardization criteria
for the clinical use of BMD.[20 ] Thus, BMD values below 2.5 standard deviations (SDs) from the mean peak value in
young adults (T ≤ −2.5) are compatible with the diagnosis of osteoporosis. A T-score
≤ −1 SD indicates a healthy individual, and a T-score between −1 SD and −2.5 SDs identifies
individuals with osteopenia.
Statistical Analysis
Data distribution was examined using the Shapiro-Wilk test, and those with Gaussian
distribution are shown as the mean (p < 0.05 were considered statistically significant.
Results
Among the women included in the study, 64.6% were white, 2.5% were black, and 32.8%
were of other ethnicities. The mean age (
[Table 1 ] shows that in the lumbar spine the BMD identified osteoporosis in 20/198 (10.1%)
patients; in the femoral neck, the condition was identified in 11/198 (5.5%) patients
(p < 0.001). In the lumbar spine, osteopenia was diagnosed in 101/198 (51%) patients;
in the femur, it was identified in 77/198 (38.8%) patients (p < 0.001). The changes in bone mass of the mandible examined by panoramic radiograph
were similar on the right and left sides (p > 0.05). Considering both sides, and using the MCI, osteoporosis was diagnosed in
approximately 9.6–10.1% of the patients, and osteopenia was diagnosed in approximately
50–54% of the patients. A mental index > 3.0 mm was found in 66–71% of the patients.
Table 1
Comparison of the absolute and relative frequencies of the bone mineral density findings
in the lumbar spine and femoral neck
Lumbar spine
Femoral neck
Bone mass
n
%
N
%
p *
Osteoporosis
20
10.10
11
5.55
0.000
Osteopenia
101
51.00
77
38.89
0.000
Normal
77
38.90
110
55.56
0.000
Total
198
100
198
100
Note: * Z-test for the proportions.
[Tables 2 ] and [3 ] show the degree of agreement between the mandibular radiomorphometric indices and
the T-scores for the diagnosis of bone mass changes. When the mental index results
were compared with the BMD findings in the lumbar spine, the agreement index was of
0.718 (95%CI: 0.618–0817). The comparison of the results obtained with the MCI and
the BMD in the lumbar spine showed a concordance of 0.912 (95%CI: 0.859–0.965). The
Kappa index between the MCI and the BMD of the femoral neck was of 0.579 (95%CI: 0.482–0.676).
When the MI results were compared with the BMD results of the femoral neck, the agreement
found was 0.443 (95%CI: 0.343–0.544).
Table 2
Comparison of bone mineral density results in the lumbar spine and femoral neck with
the results of the mental index for the diagnosis of osteoporosis in postmenopausal
women
Mental index
Kappa (95% confidence interval)
BMD
Abnormal
Normal
Total
Lumbar spine
Abnormal
121
00
121
Normal
25
52
77
Total
146
52
198
0.718 (0.618–0.817)
Femoral neck
Abnormal
88
00
88
Normal
58
52
110
Total
146
52
198
0.443 (0.343–0.544)
Abbreviation: BMD, bone mineral density.
Table 3
Comparison of bone density results in the lumbar spine and femoral neck with the results
of the mandibular cortical index for the diagnosis of osteoporosis in postmenopausal
women
Bone mineral density
Mandibular cortical index
Kappa (95% confidence interval)
Osteoporosis
Osteopenia
Normal
Total
Lumbar spine
Osteoporosis
19
01
00
20
Osteopenia
02
99
00
101
Normal
00
07
70
77
Total
21
107
70
77
0.912 (0.859–0.965)
Femoral neck
Osteoporosis
11
00
00
11
Osteopenia
09
68
00
77
Normal
01
39
70
110
Total
21
107
70
198
0.579 (0.482–0.676)
Discussion
The present study investigated the role of the mandibular panoramic radiograph in
the identification of mandibular bone mass in Brazilian postmenopausal women. In addition,
the results obtained with the panoramic radiograph were compared with those obtained
using DXA in the lumbar spine and femoral neck. The degrees of agreement between the
two tools are provided. Using DXA, the prevalence of osteoporosis was twice higher
in the lumbar spine than in the femoral neck. Using the panoramic radiograph, the
prevalence of abnormal MCIs was similar to the results found with DXA in the lumbar
spine. However, abnormal MIs were found in ∼ 70% of postmenopausal women. The panoramic
radiograph showed similar results in the right and left sides of the mandible. Regarding
the BMD findings, the panoramic radiograph and the DXA demonstrated a moderate to
good agreement, mainly when the results of the mandibular panoramic radiograph were
compared with the DXA in the lumbar spine.
Even though DXA is the standard procedure to measure general bone mass and its results
are predictive of the risk of fracture, the procedure is limited to a small part of
the population, and whether its results could also be expanded to the mandible is
debatable. Dental panoramic radiographs are frequently taken for the examination of
the mandibles in the general dental practice. It is possible that osteoporotic women
are accurately identified using the status of the mandibular inferior cortex as a
criteria to expand the investigation.[10 ] The patients' age should be taken into consideration when osteoporosis is diagnosed
using the panoramic radiograph; therefore, in early postmenopausal women, this procedure
might not detect small changes in the mandibular microarchitecture.
For over 50 years, the efficiency of the panoramic radiograph in identifying mandibular
osteoporosis was shown in different populations,[2 ]
[10 ]
[11 ]
[21 ]
[22 ] and the current results confirm previous findings in early postmenopausal Brazilian
women.[8 ] In the dental practice, a cortical bone width ≥ 3–4 mm seems not to be an appropriate
threshold for referral for DXA examination in postmenopausal women.[8 ]
[21 ]
[23 ]
[24 ] In addition, it was shown that a 1-mm decrease in cortical bone width increases
the likelihood of low BMD to 40% using DXA.[24 ] The MI has shown a long-term positive correlation with skeletal bone loss and tooth
loss,[10 ]
[23 ] but it has presented inconsistent sensitivity. Regarding the cortical bone width
(MI), 90% of the patients with width < 3 mm may present low BMD, and 30% of them have
osteoporosis.[3 ] Using this criterion, in the present study, the mandibular cortical bone width suffered
a 30% decrease in young postmenopausal women, corroborating similar results found
in another study including Caucasian women.[23 ]
Using the MCI, osteoporosis was diagnosed in 10% of the patients, and osteopenia,
in 50% of the patients in the current study. A similar prevalence was found for the
lumbar spine using DXA. Several studies have shown that postmenopausal women with
eroded mandibular cortical bones have elevated bone resorption and are more likely
to present low BMD in the DXA evaluation.[3 ]
[4 ]
[5 ] The correlation between the panoramic radiograph and DXA has been examined by other
authors, but the results are inconsistent.[5 ]
[25 ]
[26 ] An early study found a poor correlation between these tools,[13 ] but other studies found that the mandibular cortical bone mass is well-correlated
with the overall skeletal body mass.[12 ]
[27 ]
[28 ]
Too little data are available regarding the degree of agreement between the dental
panoramic radiograph and the skeletal DXA in the identification of low BMD in postmenopausal
women. Even though both methods present a moderate to good sensitivity, they have
never been used as interchangeable tools.[3 ]
[23 ] In the present study, the MCI presented an excellent and significant agreement with
the DXA at the lumbar spine, and a moderate agreement with the DXA at the femoral
neck. The MI and DXA showed a moderate and poor agreement at the lumbar spine and
femoral neck respectively. These results are consistent and even better than those
found in another study with postmenopausal Brazilian women.[12 ]
[28 ]
A few limitations must be considered in the present study: the women included in it
were not healthy volunteers from the community, but subjects recruited from an outpatient
tertiary academic menopause clinic. The cut-off threshold of cortical bone width of
3 mm might not be as appropriate for multi-ethnic young Brazilian postmenopausal women
as it was for Asian, Greek and Caucasian ethnicities.[23 ] As strengths, the current study used the two mandibular indices that have previously
demonstrated high reproducibility and good association with DXA T-scores.[21 ]
[29 ]
[30 ]
[31 ]
[32 ]
Conclusion
The prevalence rates of osteoporosis found in the lumbar spine and femoral neck in
the present study are consistent with other reports on early postmenopausal women.
There were moderate to excellent agreements between the mandibular panoramic radiograph
and the DXA findings in the lumbar spine and femoral neck regarding BMD. The results
of the current study demonstrated that the panoramic radiograph can be used in young
postmenopausal women as a tool to diagnose precocious loss of mandibular cortical
bone density, and to give support for dental treatment. In addition, it serves as
an instrument for the referral of those patients to a specialist for a specific examination,
definitive diagnosis, and possibly an early and adequate treatment of the disease.
