Digital panoramic radiographs are useful for diagnosis of osteoporosis in Korean postmenopausal women

Or ig ina l a r t i c le

Digital panoramic radiographs are useful for diagnosis ofosteoporosis in Korean postmenopausal women

Ok-Su Kim1,*, Min-Ho Shin2,*, In-Hwa Song1, Il-Gu Lim1, Suk-Ja Yoon3, Ok-Joon Kim4,Young-Hoon Lee5, Young-Joon Kim1 and Hyun-Ju Chung1

1Department of Periodontology, School of Dentistry, Dental Science Research Institute, Chonnam National University, Gwangju, Korea;2Department of Preventive Medicine, Chonnam National University, Medical School, Hak1dong, Donggu, Gwangju, Korea; 3Department of

Oral and Maxillofacial Radiology, School of Dentistry, Dental Science Research Institute, Chonnnam National University, Gwangju, Korea;4Department of Oral Pathology, School of Dentistry, Dental Science Research Institute, Chonnnam National University, Gwangju, Korea;5Department of Preventive Medicine and Institute of Wonkwang Medical Science, Wonkwang University College of Medicine, Iksan, Korea

Gerodontology 2014; doi: 10.1111/ger.12134

Digital panoramic radiographs are useful for diagnosis of osteoporosis in Korean post-menopausalwomen

Objective: The purpose of this study was to determine whether digital panoramic radiographs could be

used for the diagnosis of osteoporosis through evaluation of the radiographs based on the correlation

with bone mineral density (BMD).

Methods: One hundred and ninety-four post-menopausal women were selected from participants who

had participated in the Dong-gu study. Panoramic radiographic indices measured are mental index (MI),

mandibular cortical index (MCI) and simple visual estimation (SVE). BMD at the lumbar spine and

proximal femur was measured by dual-energy X-ray absorptiometry (DXA). The Pearson’s correlation

test was performed to analyse the correlation between MI and age and BMD at the lumbar spine, femo-

ral neck and total hip. Multiple linear regression analysis was performed to analyse the association of

MI, MCI and SVE with BMD after adjusting for age, height and weight. To determine the optimal cut-

off point of MI for the diagnosis of osteoporosis, the receiver operating characteristic analysis was per-

formed.

Results: The MI was positively correlated with BMDs: lumbar spine: r = 0.36, femoral neck: r = 0.59

and total hip: r = 0.58 (p < 0.001). As age increased, MI decreased (r = �0.46). BMD at the lumbar

spine and total hip were significantly lower in participants with reduction of mandibular width, thinning

and resorption of mandibular cortex by the MI, SVE and MCI, respectively. The optimal cut-off value of

MI for the diagnosis of spinal osteoporosis was 2.22 mm.

Conclusion: Thickness and morphological changes of mandibular inferior cortical bone are associated

with BMD, independent of age, height and weight. These results suggest that MI, MCI and SVE may be

useful indices for the diagnosis of osteoporosis in a Korean population.

Keywords: radiography, panoramic, bone density, osteoporosis, mandible.

Accepted 1 May 2014

Introduction

The increasing average lifespan of people in most

industrialised countries has led to increased preva-

lence of bone disorders and fractures in post-men-

opausal women1–3. Osteoporosis is a complex and

multifactorial chronic disease that can progress

silently for decades until characteristic fractures

result in life-threatening situations4. In general,

the risk of fractures in post-menopausal women

can be identified by osteoporosis prevention pro-

grammes. These programmes allow early detec-

tion of osteoporosis to maintain as much bone

mass and as good bone quality as possible to

reduce the risk of fractures5.

Osteoporosis is usually diagnosed by measure-

ment of bone mineral density (BMD). Dual-

energy X-ray absorptiometry (DXA) is a standard*These two authors contribute equally to this work.

© 2014 John Wiley & Sons A/S and The Gerodontology Association. Published by John Wiley & Sons Ltd 1

method for BMD evaluation and fracture risk

prediction6–10. However, DXA is not recom-

mended as a routine screening test for the gen-

eral population. Most guidelines limit the use of

DXA for post-menopausal women aged 65 years

or older and men aged 70 years or older, with

the exception of younger adults with known risk

factors6.

Although DXA is the most widely accepted

bone density measuring method, the cost is rela-

tively expensive with limitations for public

screening. Panoramic radiographs are routinely

taken in dental clinics for initial diagnosis and

treatment planning. Recently, several studies also

showed that panoramic X-ray examination is a

cost-effective method for identifying patients with

high risks of osteoporosis4–22. In general, intraoral

radiographs are taken more frequently than den-

tal panoramic radiographs. However, trabecular

bone shown in the intraoral film is easily remod-

elled by local inflammation, which makes it

inadequate for osteoporosis or skeletal triage

screening20. Horner et al.15 reported a valid corre-

lation between the mandibular cortex analysis of

panoramic radiographs and lumbar spine and hip

BMDs. Devlin et al.13 proposed panoramic radiog-

raphy examination as a method for identifying

osteoporosis as it is relatively inexpensive and

could be used on the elderly. In addition,

Taguchi suggested using panoramic radiographs

for dental triage screening for osteoporosis in

dental clinics20.

Until now, previous studies including OSTEO-

DENT projects were developed in the Japanese9,22

or Western population14–16,21, but the study for

panoramic radiographic indices and BMDs by

DXA in the Korean population has not been

reported. In this study of urban Korean post-men-

opausal women, the correlation between pano-

ramic radiographic indices and BMD score was

evaluated and investigated to determine whether

panoramic radiography would be helpful in the

diagnosis of osteoporosis.

Materials and methods

Study participants

The Dong-gu Study is an ongoing prospective

study designed to investigate the prevalence,

incidence and risk factors for chronic disease in

urban population23. A total of 9260 participants

aged 50 or older were enrolled from 2007 to

2010. Periodontal examination was carried out

for 5621 participants (2357 men; 3264 women)

among 7577 people who attended the study from

2008 to 2010. Of 3264 women aged 50 years or

older, 248 participants were excluded: no meno-

pausal (n = 115) and not taken panoramic radio-

graphs (n = 133). Panoramic radiographs from

2982 participants were used; of them, 200 partic-

ipants were randomly selected. Of 200 partici-

pants, participants whose panoramic radiograph

did not include the mandibular border com-

pletely or not clearly show the mental foramen

were excluded. Finally, data of 194 participants

were used. This study was approved by the Insti-

tutional Review Board of Chonnam National

University Hospital (IRB No: I-2008-05-056). All

participants provided written consent after

receiving a full and clear explanation of the

study in detail.

Panoramic radiographic indices

Digital panoramic radiographs (Planmeca ProOne,

Planmeca Oy, Helsinki, Finland) were taken at

the following exposure conditions 66 kV, 9 mA

and 18.0 s. For cortical thickness measurements,

the ‘Twice’ software (Osstem, Korea) was used.

Cortical width was measured by the length with

angle tool of the ‘Twice’ software.

In this study, three panoramic radiographic

indices, mental index (MI), mandibular cortical

index (MCI) and simple visual estimation (SVE),

were measured. MI is a measurement of cortical

width at the mental foramen region. A line paral-

lel to the long axis of the mandible and tangential

to the inferior border of the mandible was drawn.

A line perpendicular to this tangent intersecting

the inferior border of the mental foramen was

constructed, along which mandibular cortical

width was measured (Fig. 1, Table 1)5,24. Pano-

ramic radiographs were measured by the ‘Twice’

software, and the values were rounded up to the

second decimal place. For MCI, depending on the

classification of Klemetti25,26, mandibular cortical

border based on the type of the bone below the

mental foramen was classified as one of three

groups, C1–C3. In other words, C1 if the endos-

teal margin is even and sharp, C2 if the endosteal

margin presents semilunar defects or appears to

form endosteal cortical or C3 if the cortical layer

forms heavy endosteal cortical residues and is

clearly porous (Fig. 2, Table 1). SVE is evaluated

by observing the site (the inferior border of the

mandible) with the naked eye. Mandibular infe-

rior cortical widths were classified into three

groups: 1 = normal, 2 = medium and 3 = very

thin (Table 1)5.

© 2014 John Wiley & Sons A/S and The Gerodontology Association. Published by John Wiley & Sons Ltd

2 O. Kim et al.

Intra- and interobserver agreement

To quantify intraobserver agreements, 30 pano-

ramic radiographs were randomly selected from

the sample and analysed twice by the main obser-

ver. There was a period of 2 weeks between read-

ings. Two observers also measured the same

radiographs to verify interobserver reliability.

Observers were not aware of the DXA results and

had no access to information about the partici-

pants, such as age. Each observer independently

measured MI, MCI and SVE on both sides. For

the qualitative indices, agreements were calcu-

lated as a Cohen’s kappa index. For a quantitative

index, agreements were calculated as ICC (intra-

class correlation coefficient).

Intraclass correlation coefficient values for in-

traobserver agreement were 0.83, 0.99 and 0.76

for MI, and the kappa values for intraobserver

agreement were 0.64, 0.92 and 0.56 for the MCI,

0.7, 0.95 and 0.59 for the SVE, respectively. ICC

value for interobserver agreement was 0.81, and

the kappa values for interobserver agreement

were 0.34 and 0.52 for the MCI and SVE, respec-

tively. Inter- and intra-agreements for MI were

very good but for MCI and SVE were moderate

level. As a result, only the measurements and

classifications of the main observer were used to

analyse parameters.

Measurement of bone mineral density

BMD of participants were measured using Lunar

Prodigy bone densitometer (GE, Madison, WI,

USA) at total hip, femoral neck and lumbar spine.

BMD of the lumbar spine represents the average

BMD of L1–L4. The device was calibrated daily

with a physical phantom. All BMD scans were

conducted by certified examiners using standar-

dised procedures, by following the protocols rec-

ommended by the manufacturer. Any scans with

metal or other attenuating materials in the region

of interest, as well as any scans of poor quality,

were excluded. T scores were calculated using

manufacturer’s normative data for the lumbar

spine.

Statistical analysis

Data are presented as mean � standard deviation

(SD) or number (%). Each measurement was

repeated twice on the left and the right side,

respectively, and the average value of the four

measurements was calculated.

Scatter plot and Pearson’s correlation analysis

were used to determine the relationship between

Figure 2 Classification of mandibular cortex index

(C1–C3)25 C1: even and sharp, C2: semilunar defects

and C3: clearly porous.

Figure 1 The measurement method of mental index.

Table 1 Panoramic radiographic indices (MI, MCI and SVE).

Index

1 2 3

Mental index MI Cortical width measurement – –Mandibular. cortical index MCI Even and sharp Semilunar defects Clearly porous

Simple visual estimation SVE Normal Intermediate Very thin


Panoramic index and osteoporosis 3

MI and age and BMD at the lumbar spine, right

femoral neck and total hip. Multiple linear regres-

sion analysis was performed to analyse the associ-

ation between panoramic radiographic indices and

BMD at the lumbar spine, right femoral neck and

total hip. The receiver operating characteristic

(ROC) analysis was used to evaluate the ability of

the MI to classify lumbar spine osteoporosis,

defined as a lumbar spine BMD T score of �2.5 or

less, and area under curve (AUC) computed using

the method of Hanley and McNeil27. The optimal

MI cut-off value for the diagnosis of spinal osteo-

porosis was determined using Youden’s index. We

did not use data of femoral BMD for ROC analysis

because of low prevalence of osteoporosis in the

femoral neck and total hip and small sample size

of our study. All statistical analyses were

conducted with STATA 12 software (STATA

Corp, Texas, College Station, USA). The value of

p < 0.05 was considered significant.

Results

The demographic characteristics are summarised

in Table 2.Scatter plot and Pearson’s correlation

analysis showed that the mental index was

positively correlated with BMDs: lumbar spine:

r = 0.36, femoral neck: r = 0.59 and total

hip: r = 0.58 (Figs 3–5) (p < 0.001). Negative

correlations were observed in the analysis of cor-

relation between age and MI (r = �0.46,

p < 0.001, Fig. 6).

Table 2 Demographic characteristics of participants.

N = 194

Age, years 65.6 � 8.6

Weight, kg 57.3 � 8.4

Height, cm 152.1 � 6.2

Radiologic indices

MI 2.7 � 0.7

MCI

Even and sharp 46 (23.7)

Semilunar defects 89 (48.9)

Cleary porous 59 (30.4)

SVE

Normal 68 (35.0)

Intermediate 82 (42.3)

Very thin 44 (22.7)

Bone mineral density (g/cm2)a

Lumbar spine 0.973 � 0.171

Femoral neck 0.774 � 0.116

Total hip 0.848 � 0.132

Data are mean � SD or n (%).

MI, mental index; MCI, mandibular cortical index; and

SVE, simple visual estimation.aOf 194 participants, 186 had lumbar spine BMD and

193 had femoral neck and total hip BMD.

Figure 3 Scatter plot and Pearson’s correlation

between mental index (mm) and lumbar spine BMD.


between mental index (mm) and femoral neck BMD.


between mental index (mm) and total hip BMD.


4 O. Kim et al.

Multiple linear regression analysis for the asso-

ciation between panoramic radiographic indices

and BMD showed that association of MI with

BMD was detected at the lumbar spine

(p = 0.013) and total hip (p = 0.007), but not at

the femoral neck. Association of MCI with BMD

was detected at the lumbar spine, femoral neck

and total hip (p < 0.05). SVE was associated with

BMD at the lumbar spine and total hip, but not at

the femoral neck. BMD at the lumbar spine and

total hip were significantly lower in participants

with reduction of mandibular width, thinning and

resorption of mandibular cortex by the MI, SVE

and MCI, respectively (Table 3).

The area under the ROC curve for identifying

women with spinal osteoporosis (T ≤ �2.5) was

0.737 for the mental index (Fig. 7). In the ROC

analysis, the optimal cut-off value of MI for the

diagnosis of spinal osteoporosis was 2.22 mm

(sensitivity 67.9% and specificity 78.5%) (Table 4,

Fig. 7).

Discussion

Osteoporosis is an important public health prob-

lem in Korea28. According to the 2009 Korean

Health Statistics, among participating women aged

50 years or older, the prevalence of osteoporosis

was 38.7%29. According to the National Health

Insurance database, which includes almost all pre-

scription and treatment claims with diagnostic

codes in Korea, the number of patients being trea-

ted for osteoporosis substantially increased by

26.7% between 2005 and 200830. Among women

with osteoporosis, 30.3% were diagnosed with

osteoporosis by a physician, and only 14.3%

reported being treated29. Accordingly, it is critical

to find more easily accessible and effective meth-

ods for detection of osteoporosis. Until now, there

is no report for triage screening of osteoporosis

using panoramic radiographs in Korean popula-

tion. In this study, the significance of digital pano-

ramic radiographs is routinely taken in dental

clinics was evaluated through the correlation

between BMD and three panoramic indices in

Korean post-menopausal women aged 50 years or

older. We know that mandibular lower cortex

evaluation in digital panoramic radiographs is a

useful method for the prediction of osteoporosis

in post-menopausal women.

This study used three panoramic radiographic

indices. Leite et al.5 reported that the most

accurate indices were MI, MCI and SVE. MI is a


between mental index (mm) and age.

Table 3 Association of panoramic radiographic indices and bone mineral density by multiple linear regression

analysis.

Lumbar spine Femoral neck Total hip

Coefficient p-value Coefficient p-value Coefficient p-value

MI (mm) 0.045 � 0.018 0.013 0.016 � 0.011 0.136 0.032 � 0.012 0.007

MCI

Even and sharp Reference Reference Reference

Semilunar defects �0.066 � 0.027 0.015 �0.040 � 0.016 0.015 �0.058 � 0.018 0.001

Cleary porous �0.113 � 0.032 0.001 �0.036 � 0.019 0.064 �0.075 � 0.021 <0.001P between groups 0.002 0.045 <0.001SVE

Normal Reference Reference Reference

Intermediate �0.034 � 0.025 0.181 �0.032 � 0.015 0.035 �0.043 � 0.016 0.009

Very thin �0.098 � 0.034 0.005 �0.037 � 0.020 0.069 �0.061 � 0.022 0.006

P between groups 0.002 0.071 0.001

Adjusted for age, weight and height.



quantitative index, whereas MCI and SVE are

qualitative indices for evaluation of mandibular

cortical area. To this end, the indices that are able

to detect changes of the mandibular cortex

were used. In the present study, we proved that

MI, MCI and SVE may be useful osteoporosis

predictors.

It was difficult to determine the location of the

mental foramen when measuring MI on pano-

ramic radiographs. It can be measured only when

it was possible to definitely determine the location

of the mental foramen, and thus blurred or over-

lapped participants were excluded upon measur-

ing cortical bone thickness. In addition, it was

difficult to determine the upper border of mandib-

ular cortical bone, and in such cases, the thinnest

thickness of compact cortical bone was mea-

sured10. While MI measures the thickness of the

mandibular inferior border, MCI and SVE (which

are the suspected cause of experimental errors

incurred) simply allow the observation and evalu-

ation of the mandibular inferior border by the

naked eye. When it was unclear for the determi-

nation of MCI by the classification of Klemetti

et al.25, it was classified as C1 for cases between

C1 and C2, and C3 for cases between C2 and

C324.

Because MCI and SVE are objective indices,

many studies have examined intra- and interob-

server agreement on MCI. Some studies found

sufficient agreement5,10, but other studies failed

to find sufficient agreement15. The results of

these studies varied because of sample sizes and

differences in the ability of observers with regard

to accurate diagnosis using MCI and SVE. Leite

et al.5 reported that the kappa indices for intra-

observer agreement were 0.783 and 0.751 for

the MCI and SVE, respectively, and the kappa

values for interobserver agreement were 0.661

and 0.717 for the MCI and SVE, respectively, in

Brazilian study. In our study, ICC value for inte-

robserver agreement for MI was 0.81 and the

kappa values for interobserver agreement were

0.34 and 0.52 for the MCI and SVE, respectively.

Inter- and intra-agreements for MI were very

good but for MCI and SVE were moderate level.

From fair level of interobserver agreement for

MCI, adequate exercise should be needed

the determination of MCI. Taguchi20 also

reported that intraobserver agreement for MCI

was much better for oral radiologists than for

other dentists.

The thickness of mandibular cortical bone

decreased as age increased12,24. Kim et al.24 report

that MI was measured in five age categories for

subjects of Korean men and women; the mean

MI of subjects of 50–59 years was 3.7 mm, while

the mean MI of subjects of 60–69 years was

2.3 mm. They showed that MI of subjects of 60–69 years steeply declined. Even though the com-

parison is difficult, the mean MI in this study was

2.7 mm for Korean menopausal women (mean

age 65.6 years). We suggest that the mandibular

cortex evaluation on digital panoramic radio-

graphs should be enforced for the diagnosis of

osteoporosis in Korean women aged over

65 years.

The MI was the only quantitative index whose

accuracy was analysed. The area under the ROC

curve for identifying women with lumbar spine

osteoporosis (T ≤ �2.5) was 0.737. This indicates

moderate accuracy for the mental index, and the

results were similar to those of Leite et al.5. The

optimal cut-off value of MI for the diagnosis of

osteoporosis was 2.22 mm (sensitivity 67.9% and

Figure 7 The receiver operating characteristic (ROC)

analysis to evaluate the ability of the MI to classify

lumbar spine osteoporosis.

Table 4 Diagnostic performance of mental index in

predicting lumbar spine osteoporosis using receiver

operating characteristics curve.

MI

Sensitivity

(%)

Specificity

(%)

Youden’s

indexa

≤1.5 mm 14.3 96.2 0.105

≤2.0 mm 35.7 91.8 0.275

≤2.5 mm 67.9 69.6 0.375

≤3.0 mm 85.7 43.7 0.294

≤3.5 mm 96.4 17.7 0.141

Optimal (2.22 mm)b 67.9 78.5 0.464

aYouden’s index = sensitivity + specificity – 1.bOptimal cut-off value that maximised Youden’s index.


6 O. Kim et al.

specificity 78.5%). From our results, Korean post-

menopausal women with mandibular cortical

thickness <2.5 mm should be referred for osteo-

porosis evaluation. These results for the diagnosis

of osteoporosis were lower than those found by

other authors. Compared with the osteoporosis

group, the group with MI of 3.15 mm or less and

the group with MI of 3 mm or less had the high-

est value of specificity and sensitivity in the study

by Leite et al.5 and by Ledgerton et al.10, respec-

tively. Taguchi et al.22 and Devlin31,32 suggested

that a follow-up evaluation is needed for the diag-

nosis of osteoporosis when the thickness of the

mandibular cortex is equal to or less than 2.8

(Taguchi22), following the criteria of T ≤ �1.0 or

MI is <3 mm (Devlin31,32). It is surmised that the

reasons for lower cut-off value in this study than

in other studies would be the use of digital pano-

ramic radiographs obtaining a good quality image,

the difference of statistical analysis for determin-

ing cut-off value, the difference of radiographic

magnifying ratio and ethnic/racial differences.

Nam et al.33 reported substantial race/ethnic dif-

ferences in BMD even within African or Asian

origin and illustrated the important role of body

size and oestrogen use to the geographic and

racial/ethnic variation in BMD in a cross-sectional

study, which compared BMD in older men across

seven race/ethnic groups in four countries. Fur-

ther, body composition, lifestyle and socio-eco-

nomic status would contribute differently to

BMD. In a Brazilian menopausal women study,

with a mean age of 63.5 � 4.7 years, the mean

values of MI were 3.32 � 1.02 mm5. In our study

for Korean menopausal women, with a mean age

of 65.6 � 8.6, the mean values of MI were

2.7 � 0.7 mm. Even if both groups had a similar

mean age, mandibular cortical width showed

racial differences. In addition, various definitions

of osteoporosis among the studies can lead to

some differences in the results. In this study, we

used the lumbar spine BMD in determining the

cut-off value of MI for the diagnosis of osteoporo-

sis. However, the OSTEODENT study by Horner

et al.21 used the femoral neck BMD for the hip

fracture risk assessment.

Our study has several limitations. First, our

study was cross-sectional in design, thus we could

not determine the temporal relationship. Longitu-

dinal studies may help clarify the mandibular cor-

tical resorption process due to osteoporosis over

time. Secondly, this study presented that pano-

ramic measurements may be useful in predicting

osteoporosis in post-menopausal women, but did

not include elderly men. Further studies with

above considerations are needed to know the

mechanism of resorption process and critical

index for diagnosing osteoporosis.

Clinicians should be aware of the risk of bone

density reduction when the thickness and mor-

phological changes of cortical bone of the man-

dibular lower border are detected on panoramic

radiographs. In such cases, more detailed investi-

gations to identify osteoporosis should be recom-

mended to the patients.

In conclusion, thickness and morphological

changes of mandibular inferior cortical bone on

digital panoramic radiographs are associated with

BMD in Korean post-menopausal women aged

50 years or older participants. In addition, the

thickness of the inferior mandibular cortex in

mental region is influenced by ageing. Finally,

MI, MCI and SVE are useful indices for the diag-

nosis of osteoporosis.

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Zmuda JM, Leung PC, Lui LY

et al. Race/ethnic differences in bone

mineral densities in older women. J

Bone Miner Metab 2013; 31: 190–8.

Correspondence to:

Ok-Su Kim, Department of

Periodontology, School of

Dentistry, Dental Science

Research Institute, Chonnam

National University, Gwangju,

South Korea.

Tel.: +82 62 530 5576

Fax: +82 62 530 5649

E-mail: [email protected].

kr

and

Min-Ho Shin, Department of

Preventive Medicine, Chonnam

National University, Medical

School, 5, Hak1dong, Donggu,

Gwangju, South Korea.

Tel.: +82 62 220 4166

Fax: +82 62 233 0305

E-mail: [email protected]


8 O. Kim et al.

Documents

Digital panoramic radiographs are useful for diagnosis of osteoporosis in Korean postmenopausal women