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Arch Osteoporos (2017) 12: 26

DOI 10.1007/s11657-017-0314-7

ORIGINAL ARTICLE

Use of cone beam computed tomography in identifying


postmenopausal women with osteoporosis
C. B. Brasileiro 1 & L. L. F. H. Chalub 2 & M. H. N. G. Abreu 2 & I. D Barreiros 1 & T. M. P. Amaral 1 &
A. M. Kakehasi 3 & R. A. Mesquita 1

Received: 2 December 2016 / Accepted: 6 February 2017 / Published online: 6 March 2017
# International Osteoporosis Foundation and National Osteoporosis Foundation 2017

Abstract used to compare the differences between the indices of the


Summary The aim of this study is to correlate radiometric groups’ intraclass correlation coefficient (ICC).
indices from cone beam computed tomography (CBCT) im- Results Statistical analysis showed a high degree of interob-
ages and bone mineral density (BMD) in postmenopausal server and intraobserver agreement for all measurements
women. Quantitative CBCT indices can be used to screen (ICC > 0.80). The mean values of CTMI, CTI (S), and CTI
for women with low BMD. (I) were lower in the osteoporosis group than in osteopenia
Purpose Osteoporosis is a disease characterized by the dete- and normal patients (p < 0.05). In comparing normal patients
rioration of bone tissue and the consequent decrease in BMD and women with osteopenia, there was no statistically signif-
and increase in bone fragility. Several studies have been per- icant difference in the mean value of CTI (I) (p = 0.075).
formed to assess radiometric indices in panoramic images as Conclusions Quantitative CBCT indices may help dentists to
low-BMD predictors. The aim of this study is to correlate screen for women with low spinal and femoral bone mineral
radiometric indices from CBCT images and BMD in postmen- density so that they can refer postmenopausal women for bone
opausal women. densitometry.
Methods Sixty postmenopausal women with indications for
dental implants and CBCT evaluation were selected. Dual- Keywords Cone beam computed tomography . Bone mineral
energy X-ray absorptiometry (DXA) was performed, and the density . Mandibular indices . Postmenopausal women
patients were divided into normal, osteopenia, and osteoporo-
sis groups, according to the World Health Organization
(WHO) criteria. Cross-sectional images were used to evaluate Introduction
the computed tomography mandibular index (CTMI), the
computed tomography index (inferior) (CTI (I)) and comput- Osteoporosis is a systemic skeletal disease characterized by
ed tomography index (superior) (CTI (S)). Student’s t test was compromised bone strength with the consequent increased
risk of fracture [1]. It is considered a public health concern
worldwide due to the high mortality rate, morbidity, and eco-
* C. B. Brasileiro
cbbrasileiro@gmail.com nomic impact related to osteoporotic fractures [2]. According
to the 2010 census of the Brazilian Institute of Geography and
Statistics, individuals older than 60 years were almost 20 mil-
1
Department of Oral Surgery and Pathology, School of Dentistry, lion people in 2010. The population of this age group is
Federal University of Minas Gerais, Av. Antônio Carlos, 6627,
Pampulha, Belo Horizonte, Minas Gerais 31270-901, Brazil
projected to exceed 60 million in 2050 [3].
2
Various techniques are used in BMD evaluation, such as
Department of Community and Preventive Dentistry, School of
Dentistry, Federal University of Minas Gerais, Av. Antônio Carlos,
dual-energy X-ray absorptiometry (DXA), quantitative com-
6627, Pampulha, Belo Horizonte, Minas Gerais 31270-901, Brazil puted tomography (QCT), and quantitative ultrasound (QUS).
3
Department of Locomotor System, School of Medicine, Federal
DXA is the gold standard method for BMD assessment [4].
University of Minas Gerais, Av. Alfredo Balena, 190/291, Santa According to international guidelines, all women over 65 years
Efigênia, Belo Horizonte, Minas Gerais 30130-100, Brazil old should perform bone densitometry, as should younger
26 Page 2 of 6 Arch Osteoporos (2017) 12: 26

postmenopausal women with associated risk factors [5]. The Materials and methods
methods used to evaluate BMD are not accessible to all pa-
tients and in Brazil, and according to the last available Subjects
sociodemographic and health indicators collected in 2005
and published in 2009, there were only 1.5 instruments for This study was conducted in the Department of Oral Surgery
BMD evaluation per million inhabitants in the public health and Pathology, School of Dentistry, Federal University of
system [6]. Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Panoramic radiography is the most frequent type of X- Postmenopausal women with indications for dental implants
ray imaging requested in dentistry, and Klemetti et al. and CBCT evaluation were invited to participate. This study
(1994) [7] were the first to investigate the correlation be- was approved by the Ethics Committee of Federal University
tween mandibular cortical morphology and low BMD. of Minas Gerais (35869714.5.0000.5149). Written informed
The index proposed by Klemetti is called the Klemetti consent was obtained from all patients, and a questionnaire
index (KI) or mandibular cortical index (MCI). Many oth- about sociodemographic aspects and health and lifestyle
er studies have been proposed to evaluate this radiograph- habits was answered. Women with a history of oophorectomy,
ic index as a screening tool for osteoporosis [8–14]. metabolic bone diseases, hyperparathyroidism, hypoparathy-
Quantitative assessment of panoramic radiography as a roidism, diabetes, osteomalacia, renal disease, or the use of
low-BMD predictor based on radiometric indices has been drugs that can affect bone metabolism were excluded.
reported, and most such studies were performed in post- Moreover, patients in hormonal replacement therapy and pa-
menopausal women because the lack of estrogen increases tients supplemented with calcium and vitamin D for at least
the risk of osteoporosis. Mandibular cortical width 6 months were excluded.
(MCW), also called the mental index (MI), was described
by Ledgerton et al. (1997) [15] and is the measured thick- Evaluation of the bone mineral density
ness of the mandibular cortical bone at the mental fora-
men region. The panoramic mandibular index (PMI) pre- Bone mineral density at the femoral neck and lumbar spine
sented by Benson et al. (1991) [16] is the ratio between (L1–L4) was determined using the Hologic Discovery DXA
the mandibular cortical bone thickness and the distance System® (Hologic Inc., Bedford, MA, USA). Patients were
from the mental foramen to the lower edge of the mandi- classified as normal (T-score ≥ −1), osteopenia (−1 > T-
ble. Other linear measurements studied include the gonial score > −2.5), and osteoporosis (T-score ≤ −2.5) according
index (GI), antegonial index (AI), and antegonial depth to the WHO criteria [23].
(AD) [17]. Angular measurements including the gonial
angle (GA), antegonial angle (AA), and mandibular angle Cone beam computed tomography
(MA) were also investigated [18, 19].
Cone beam computed tomography (CBCT) can be a CBCT of all women was performed using the KODAK 9000C
useful tool in identifying patients with low BMD. CBCT 3D® (Kodak Dental Systems, Carestream Health, USA) with
provides structure images without overlapping, magnifica- a voxel size of 0.076 mm, field of view of 50 mm diameter ×
tion, or distortion and allows viewing in three dimensions 37 mm height, tube voltage of 72 kVp, tube current of 10 mA,
[20]. Thus, it is expected that tomographic images may and a scan time of 32.40 s. Digital Imaging and
facilitate the investigation of correlations between the Communications in Medicine (DICOM) files were evaluated
quantitative and qualitative indices and low BMD using the Implant Viewer software® (Anne Solutions, Brazil).
[20–22]. Koh and Kim (2011) [21] performed the first Two measurements were performed in cross-sectional images
study that evaluated CBCT and BMD in postmenopausal with an interval of 15 days, bilaterally, in the region of the
women, and it was based on quantitative and qualitative mental foramen by two previously calibrated radiologists. The
indices used in the evaluation of panoramic radiographs indices evaluated were as follows:
as low-BMD predictors. Gungor et al. (2016) [22] also CTMI: computed tomography mandibular index, which
studied radiomorphometric indices in CBCT images, but was the inferior cortical width of the mandible (Fig. 1a)
the authors did not report whether the study was conduct- CTI (I): computed tomography index (inferior), which was
ed only in postmenopausal women. Gomes et al. (2014) the ratio of the inferior cortical width to the distance from the
[20] evaluated panoramic and cross-sectional CBCT im- inferior margin of the mental foramen to the inferior border of
ages based on the Klemetti index. Thus, the aim of this the mandible (Fig. 1b)
study was to correlate radiometric indices from CBCT CTI (S): computed tomography index (superior), which
images and BMD in postmenopausal women and verify was the ratio of the inferior cortical width to the distance from
if these indices may be a useful tool in detecting patients the superior margin of the mental foramen to the inferior bor-
with low BMD. der of the mandible (Fig. 1c)
Arch Osteoporos (2017) 12: 26 Page 3 of 6 26

Fig. 1 Radiometric index. a CTMI: inferior cortical width of the border of the mandible (W/I). c CTI (S): ratio of the inferior cortical width
mandible (W). b CTI (I): ratio of the inferior cortical width to the to the distance from the superior margin of the mental foramen to the
distance from the inferior margin of the mental foramen to the inferior inferior border of the mandible (W/S)

The mean values were calculated for each index. groups, the mean age was 57.5, ranging between 50 and
The indices evaluated in this study were in accordance with 66 years, and 62.4, ranging between 52 and 80 years, respec-
Koh and Kim (2011) [21]. CTMI is related to the MCW, also tively. The results showed a higher average age of groups with
called the MI, described by Ledgerton et al. (1997) [15]. low BMD (osteopenia and osteoporosis) compared to the nor-
MCW or MI represents the measured thickness of the man- mal group. The low-BMD groups had equivalent ages.
dibular cortical bone at the mental foramen region. A line Table 2 presents the mean values of the computed tomog-
parallel to the long axis of the mandible and tangential to the raphy indices evaluated. The results showed that the mean
inferior border of the mental foramen is drawn. A line perpen- values of CTMI, CTI (S), and CTI (I) were lower in the oste-
dicular to this tangent intersecting the inferior border of the oporosis group than in the osteopenia and normal patients.
mental foramen is then drawn, along which the mandibular The CTMI mean values in osteoporosis patients were signif-
cortical width is measured. CTI (S) and CTI (I) are related to icantly lower than those in the osteopenia and normal groups
the PMI. The PMI is a radiometric measurement introduced (p = 0.000). For CTI (S), the mean values in the osteoporosis
by Benson et al. (1991) [16] and is the ratio between the group were also lower than those in the osteopenia and normal
mandibular cortical bone thickness and the distance from the patients, and the differences were statistically significant
superior or inferior margin of the mental foramen to the infe- (p = 0.017 and p = 0.000, respectively). Similarly, for CTI
rior border of the mandible. (I), the mean values in the osteoporosis group were lower than
those in the osteopenia group (p = 0.021) and the normal
Data analyses group (p = 0.002). Considering normal patients and women
with osteopenia, the mean values of CTI (S) (p = 0.022) and
Interobserver and intraobserver agreement was calculated by CTMI (p = 0.015) were significantly lower in the osteopenia
the intraclass correlation coefficient (ICC). Statistical analysis group. However, there was no statistically significant differ-
showed a high degree of interobserver and intraobserver ence in the mean value of CTI (I) (p = 0.075) when comparing
agreement for all measurements (ICC > 0.80). The mean and these groups.
confidence interval of the indices were determined for the
three groups. The statistical analyses were performed using
the SAEG System for Statistical Analysis 9.1® (Federal Discussion
University of Viçosa, Viçosa, Minas Gerais, Brazil) and
SPSS® for Windows 17.0 (Statistical Package for the Social Panoramic radiography is an imaging method routinely used
Sciences, Chicago, IL, USA). The Kolmogorov-Smirnov and in dental practice, and most studies evaluating quantitative
Lilliefors tests were used to verify the normal distribution of radiometric indices in panoramic radiographs, such as
the values. Statistical analysis showed a normal distribution, MCW, have demonstrated statistically significant correlations
and Student’s t test was used to compare the differences be- between these indices and low BMD in postmenopausal wom-
tween the indices of the groups. en [14, 19, 24]. The mean cortical thickness of the osteopenia/
osteoporotic groups was lower than that of the normal group
[8, 25, 26]. Previous studies reported that a mandibular corti-
Results cal width below 3 mm at the mental foramen region may be
considered a threshold value when predicting low BMD and is
The characteristics of the study subjects by age are shown in a cutoff for referring patients for densitometric evaluation [27,
Table 1. The mean age of the normal group was 55.6, ranging 28]. However, the measurement of the thickness of the lower
between 47 and 78 years. For the osteopenia and osteoporosis mandible cortical bone in panoramic radiography is limited by
26 Page 4 of 6 Arch Osteoporos (2017) 12: 26

Table 1 Characterization of the


sample by age Groups Number Lower Upper Mean Confidence interval (95%)

Lower Upper

Normal 20 47 78 55.6 52.00 59.20


Osteopenia 20 50 66 57.5 55.20 59.81
Osteoporosis 20 52 80 62.4 58.66 66.14

the difficulty of precisely locating the mental foramen and radiographs. Khojastehpour et al. (2011) [8] and Kim
determining the upper border of the mandibular cortical bone et al. (2014) [14] showed that age was significantly cor-
[14]. Thus, these limitations may be overcome by CBCT, related with mandibular thickness and that as age in-
because the tomographic images make it possible to precisely creased, MCW decreased. Although differences were ob-
locate and view the mental foramen. served in the results of the three studies that investigated
The study of Koh and Kim (2011) [21] was the first to CBCT as a low-BMD predictor, it can be inferred that a
evaluate CBCT as a low-BMD predictor, and the authors CTMI thinner than 3 mm at the mental foramen region
found that the mean value of the CTMI in the osteoporo- may be considered a threshold value when predicting low
sis group (2.33 mm) was lower than that in the normal spinal and femoral BMD, as well as many panoramic
patients (3.22 mm), but there was no significant correla- radiographic studies [14, 19, 24, 27–29].
tion between the groups. In this study, the patients with In relation to CTI (I) and CTI (S), Koh and Kim (2011)
low BMD were divided into osteopenia and osteoporosis [21] found statistically significant differences between os-
patients, and the mean values of CTMI in the osteopenia teoporosis and normal groups. Gungor et al. (2016) [22]
and osteoporosis groups (3.68 and 2.93 mm, respectively) demonstrated similar results considering low-BMD and
were lower than those in the normal group (4.24 mm). In control groups, but the comparison between the
contrast to Koh and Kim (2011) [21], the results were osteopenia and normal groups revealed no significant dif-
statistically significant. The difference in sample size ferences. In this study, the mean values of CTI (I) and
and how the groups were divided may explain the dis- CTI (S) were significantly lower in the osteoporosis group
crepancy in the results of the studies. Gungor et al. than in the osteopenia and normal groups. However, we
(2016) [22] also used cross-sectional CBCT images, such did not find any significant difference between the
as this study, to evaluate CTMI, CTI (I), and CTI (S) and osteopenia and normal groups in the CTI (I) mean values.
demonstrated that the CTMI measurements in the osteo- These differences can be explained by the sample size.
porosis group (2.76 mm) were lower than those in the Studies that evaluated the correlation between PMI and
osteopenia (3.42 mm) and normal groups (3.62 mm). BMD in panoramic radiography also showed controver-
However, in contrast with the results of this study, these sial results. Some authors found a significant correlation
differences were not significant when comparing between PMI and BMD [19, 30], but others do not show
osteopenia with the control patients. The differences in this correlation [10, 25, 31].
the results may be explained by the fact that Gungor A limitation of the study is that it was conducted by the
et al. (2016) [22] did not evaluate postmenopausal women analysis of cross-sectional images in CBCT, while most stud-
and the normal group age range was considerably less ies were performed using panoramic radiography.
than the age range of the patients evaluated in this study. Considering that only three studies evaluated radiometric in-
The influence of age in the mandibular cortical width has dices in CBCT images, further studies should be conducted to
previously been reported in studies with panoramic confirm the reliability of the results.

Table 2 Radiometric index (mean ± standard deviation) of the groups according to bone mineral density: normal, osteopenia, and osteoporosis

Group Normal Osteopenia Osteoporosis Normal × Normal × Osteopenia ×


mean (mm) ± SD mean (mm) ± SD mean (mm) ± SD osteopenia (p) osteoporose (p) osteoporose (p)

CTMI 4.27 ± 0.88 3.68 ± 0.55 2.93 ± 0.67 0.015 0.000 0.000
CTI (I) 0.33 ± 0.91 0.29 ± 0.47 0.24 ± 0.69 0.075* 0.002 0.021
CTI (S) 0.27 ± 0.81 0.22 ± 0.37 0.18 ± 0.56 0.022 0.000 0.017

*Mean that there was no statistically significant difference considering p < 0.05, when comparing groups
Arch Osteoporos (2017) 12: 26 Page 5 of 6 26

Conclusions 11. Gaur B, Chaudhary A, Wanjari PV, Sunil M, Basavaraj P (2013)


Evaluation of panoramic radiographs as a screening tool of osteo-
porosis in post menopausal women: a cross sectional study. J Clin
The results of this study suggest that quantitative CBCT indi- Diagn Res 7:2051–2055
ces may be useful in identifying postmenopausal women with 12. Mansour S, AlGhamdi AS, Javed F, Marzouk H, Khan EA (2013)
low BMD and as a screening tool for osteoporosis. These Panoramic radiomorphometric indices as reliable parameters in
indices are able to help dentists screen women with low spinal predicting osteoporosis. Am J Med Sci 346:473–478. doi:10.
1097/MAJ.0b013e3182972148
and femoral bone mineral density so that they can refer post- 13. Valerio CS, Trindade AM, Mazzieiro ET, Amaral TP, Manzi FR
menopausal women for bone densitometry. (2013) Use of digital panoramic radiography as an auxiliary means
of low bone mineral density detection in post-menopausal women.
Acknowledgments This study was supported by the Research Support Dentomaxillofac Radiol 42:1–6. doi:10.1259/dmfr.20120059
Foundation of the State of Minas Gerais (FAPEMIG, #CDS-BPD-00178- 14. Kim OS, Shin MH, Song IH, Lim IG, Yoon SJ, Kim OJ, Lee YH,
14) and the National Council of Technological and Scientific Kim YJ, Chung HJ (2014) Digital panoramic radiographs are useful
Development (CNPq, # 309322/2015-4), Brazil. for diagnosis of osteoporosis in Korean postmenopausal women.
Gerodontology 33:185–192. doi:10.1111/ger.12134
Compliance with ethical standards This study was approved by the 15. Ledgerton D, Horner K, Devlin H, Worthington H (1997)
Ethics Committee of Federal University of Minas Gerais Panoramic mandibular index as a radiomorphometric tool: an as-
(35869714.5.0000.5149). Written informed consent was obtained from sessment of precision. Dentomaxillofac Radiol 26:95–100. doi:10.
all patients. 1038/sj.dmfr.4600215
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Surg Oral Med Oral Pathol 71:349–356. doi:10.1016/0030-
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