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Year : 2017  |  Volume : 21  |  Issue : 2  |  Page : 119-124  

Comparison of bone mineral density among pre- and post-menopausal women with and without chronic generalized periodontitis

1 Department of Periodontology, Meenakshi Ammal Dental College and Hospital, Chennai, Tamil Nadu, India
2 Department of Periodontology, Adiparasakthi Dental College, Chennai, Tamil Nadu, India

Date of Submission23-Feb-2016
Date of Acceptance22-Aug-2017
Date of Web Publication29-Dec-2017

Correspondence Address:
Jaideep Mahendra
Meenakshi Ammal Dental College and Hospital, Maduravoyal, Chennai - 600 095, Tamil Nadu
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jisp.jisp_43_16

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Background: There have been a very limited number of studies regarding the assessment of bone mineral density (BMD) using dual energy X-ray absorptiometry scan. Hence, the purpose of the study was to assess the relationship between BMD and periodontal health in three different study groups. Materials and Methods: The study comprised of thirty female individuals who were categorized into three groups: ten premenopausal women with healthy periodontium (Group A), ten premenopausal women with generalized chronic periodontitis (Group B), and ten postmenopausal women with generalized chronic periodontitis (Group C). Number of teeth, plaque index, probing depth, clinical attachment level, interproximal alveolar bone loss, T-score for dual femur and posteroanterior (PA) spine, and BMD for dual femur and PA spine of each individual were recorded in all the three groups. Results: The BMD and T-score of dual femur and PA spine were found to be low in Group C when compared to Group A and B which was statistically significant. Conclusion: Postmenopausal women with generalized chronic periodontitis (Group C) exhibited severe periodontal destruction with less BMD. Hence, it is suggested that periodontitis may be a risk indicator for osteoporosis in postmenopausal women and vice versa.

Keywords: Bone mineral density, dual femur/posteroanterior spine, osteoporosis, periodontitis, T-score

How to cite this article:
Svedha PR, Mahendra J, Theayarajar R, Namachivayam A. Comparison of bone mineral density among pre- and post-menopausal women with and without chronic generalized periodontitis. J Indian Soc Periodontol 2017;21:119-24

How to cite this URL:
Svedha PR, Mahendra J, Theayarajar R, Namachivayam A. Comparison of bone mineral density among pre- and post-menopausal women with and without chronic generalized periodontitis. J Indian Soc Periodontol [serial online] 2017 [cited 2022 Aug 13];21:119-24. Available from:

   Introduction Top

Periodontitis is a chronic inflammatory disease characterized by resorption of the alveolar bone as well as loss of soft tissue attachment resulting in edentulism in majority of the adults. Osteopenia and osteoporosis are progressive metabolic bone disorders which are closely associated with estrogen deficiency that causes reduction in the bone mass resulting in demineralization and deossification within 5–10 years from the cessation of ovarian function. Since alveolar bone loss is a salient feature of periodontitis, there is increasing evidence which suggests that severe osteoporosis may be an aggravating factor in periodontal tissue breakdown.

Conventional radiography is being used as a common diagnostic technique for estimation for bone loss; however, it is not a sensitive and accurate detector to diagnose osteoporosis until the total bone density has decreased by 50%.[1] The gold standard for traditional diagnosis of osteoporosis is the measurement of bone mineral density (BMD) by dual energy X-ray absorptiometry (DEXA) which is a two-dimensional projection system that uses an X-ray tube source as photon source.[2]

Postmenopausal osteoporosis may lead to the presence of less crestal alveolar bone per unit volume leading to more periodontal destruction.[3] Estrogen deficiency following menopause is associated with increased osteoclast (OC) differentiation and reduced OC apoptosis further contributing to bone loss. It has been hypothesized that a decreased alveolar bone density is more susceptible to resorption by the effect of coexisting or subsequent periodontal infection and inflammation due to osteoporosis; however, there is a limited literature to address the relationship. Hence, we aimed to compare clinically and radiographically, the BMD among pre- and post-menopausal women with and without generalized chronic periodontitis.

   Materials and Methods Top

Sixty female individuals were recruited for the study, out of which 10 individuals were above 55 years of age hence were excluded from the present investigation, 9 individuals were not willing to participate in the study, 6 individuals were under hormonal replacement therapy, 4 individuals had <15 teeth, and 1 patient was already under antibiotic prophylaxis hence could not meet the inclusion criteria. The inclusion criteria included pre- and post-menopausal women with generalized chronic periodontitis, age ranging from 45 to 55 years with at least 15 natural teeth present. Patients who were under antibiotic prophylaxis, long-term steroid medication, hormone replacement therapy, calcium supplements, or the use of contrast agents or participation in nuclear medicine studies seven days before BMD assessment, early onset of menopause before 45 years of age or any chronic infection, and metabolic bone diseases such as parathyroid disease and malignancy were excluded from the study. Finally, 30 systemically healthy pre- and post-menopausal women within the age group of 45–55 years were selected for the present study [Figure 1]. The “Institutional Review Board” (MADC/IRB/2014/015) approved this study. The individuals were verbally informed, and written consent was obtained from them. These individuals underwent periodontal examination for the diagnosis of generalized chronic periodontitis.[4] Based on the periodontal screening, they were categorized into three groups: Groups A, B, and C. The control Group A consisted of ten premenopausal women who exhibited healthy periodontium with no attachment loss and the study Groups B and C consisted of ten pre- and post-menopausal women who exhibited alveolar bone loss due to generalized chronic periodontitis, respectively.
Figure 1: Flow chart; HRT: Hormone replacement therapy

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Clinical data collection

To assess the periodontal status, all 30 participants underwent thorough periodontal examination. Clinical parameters such as plaque index (PI)[5] were scored as being present or absent at four sites per tooth (mesiobuccal, buccal, distobuccal, and lingual surfaces) after air drying. The probing pocket depth [5] was measured clinically using Williams probe at six sites (mesiobuccal, midbuccal, distobuccal, mesiolingual, distolingual, and midlingual) of each tooth. The probe was inserted parallel to the vertical axis of the tooth from the gingival margin to the base of the pocket, and the probing pocket depth was measured to the nearest millimeter at the gingival margin. The pocket depth for the deepest probing site was recorded for each individual tooth. Clinical attachment level (CAL)[5] was recorded which is the distance between the base of the pocket and a fixed point on the crown such as cementoenamel junction. DEXA scores (BMD through T-score of posteroanterior spine (PA) and dual femur) were recorded.

Radiographic examination

Interproximal alveolar bone was determined from six intraoral periapical radiographs and two posterior bitewing radiographs. The radiographs were scanned and digitized.[6] A grid calibrated in millimeters was superimposed on the radiographs using CorelDRAW software. The interproximal alveolar bone loss was measured from the cementoenamel junction to most coronal aspect of interproximal alveolar bone on the mesial and distal aspects of all teeth except for 3rd molars.

Estimation of bone mineral density

Before assessing the BMD, a short interview was conducted from all the participants to rule out any contraindication such as inability to remain supine on the imaging table without movement or spinal deformity or disease. Patients were then instructed to remove all the metal items from their body. BMD of spine, left, and right femurs was estimated by DEXA scan using LUNAR DPA DXA SCANNER (GE Medical Systems) by a trained operator according to the manufacturer's instruction. The precision of DEXA to measure BMD at PA spine was 1% (effective dosage – 1–10 μSV) and proximal femur was 1%–2% (effective dosage – 1–10 μSV).[7]


Estimation of bone mineral density in lumbar spine

PA spine scan was taken with the patient lying supine on the imaging table. The patient was aligned in the middle of the table, with the spine straight and parallel to longitudinal table axes. Important anatomical markers were taken into consideration such as the upper border of the pelvis and the twelfth rib, clearly visible on the image. After the imaging was over, the analysis was done by identifying L5, visualized as letter “M” or butterfly shape. If there were artifacts overlying bone, that part of the bone was excluded from region of interest (ROI) [Figure 2].
Figure 2: Dual energy X-ray absorptiometry report – posteroanterior spine bone density

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Estimation of bone mineral density in femur

The patient was instructed to lie supine on the table. The leg was slightly abducted and internally rotated, using a positioning device to bring the femoral neck parallel to the scan table. It was clearly instructed to rotate the entire length and not just the foot or lower leg to avoid errors. Femoral ROI, neck, Ward's triangle, and trochanter region were chosen to capture the different bone loss patterns that can occur in femur. Other ROIs were intertrochanter and total hip. The latter was an area weighed mean of the trochanter, intertrochanter, and femoral neck [Figure 3]. The BMD of the focused area, in spine, and dual femur were expressed in units of grams/cm 2 [Figure 4].
Figure 3: Dual energy X-ray absorptiometry report – dual femur bone density

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Figure 4: Important landmarks of femur

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Based on the results of the BMD of each patient, T-score was calculated. The T-score is represented by taking the difference between a patient's measured BMD and the mean BMD of healthy young adults, matched for gender and ethnic group, and expressing the difference relative to the young adult population standard deviation (SD).[8]

As according to the World Health Organization based on bone density levels, a T-score between +1 and −1 is considered normal or healthy, T-score between −1 and −2.5 indicates low bone mass, although not low enough to be diagnosed with osteoporosis, and T-score of −2.5 or lower indicates osteoporosis. The greater the negative number, the more severe the osteoporosis. Therefore, a T-score result indicates the difference between the patients' BMD and the ideal peak bone mass achieved by a young adult.

Statistical analysis

The statistical analysis was done using G*Power version 3.1.7 (computer software), Uiversität Kiel, Germany. The mean values of demographic, clinical, and radiographic parameters were compared within the groups by one-way ANOVA. Individual percentage was estimated among the groups with respect to osteoporosis. Tukey honest significant difference post hoc test was used for pair-wise comparisons.

   Results Top

On comparing the demographic variables such as age and body mass index, Group C was found to be statistically significant (P< 0.001) when compared to Groups A and B. Clinical parameters such as PI and CAL were highly significant in Group C (P< 0.001). On comparing the radiographic parameters such as interproximal alveolar bone loss, BMD, and T-score of PA spine and dual femur, Group C was found to have a greater alveolar bone loss (P< 0.001) and less BMD (P< 0.017) when compared to Groups A and B [Table 1]. It was also found that there were no osteoporotic individuals in Group A, 10% in Group B, and 30% in Group C [Table 2].
Table 1: Comparison of mean values of variables between control and study groups

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Table 2: Proportions of normal, osteopenia, and osteoporosis cases in the control and study groups

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   Discussion Top

Periodontitis is a microbial infection which is characterized by gingival inflammation, epithelial and connective tissue attachment loss, and subsequently, loss of alveolar bone. The host responds to the microbial challenge with the production of cytokines such as interleukin (IL)-1α, IL-1 β, IL-6, tumor necrosis factor-alpha (TNF-α), and matrix metalloproteinase, which leads to connective tissue and bone destruction.[9]

Studies state that the postmenopausal women undergo hormonal changes such as estrogen deficiency which further increases IL-6, IL-1α, IL-1 β, and TNF-α concentration in bone marrow that stimulates OC bone resorption and decreases OC apoptosis.[10] Similar mechanism is also involved in the pathogenesis of periodontitis. Since alveolar bone loss is the hallmark of periodontal disease, reduced BMD may predispose to aggravated alveolar bone loss in periodontitis. Age, hormonal imbalance, nutrition, smoking, and genetic factors which are indicated as risk factors in periodontitis are also indicated in reducing the systemic BMD.

Although the earlier studies have focused on the estimation of BMD among pre- and post-menopausal women with and without generalized chronic periodontitis, this is one of the few studies to compare pre- and post-menopausal chronic periodontitis women with premenopausal women having healthy periodontium to find out the influence of osteoporosis on periodontium.

Among all three Groups A, B, C, mean age was found to be highest in postmenopausal group with chronic periodontitis (Group C) (51.7 ± 2.214) than Group A (46.80 ± 1.619) and B (46.3 ± 1.337) and was statistically significant [Table 1]. In our study, the age range was between 45 and 55 years since in Indian women, most common prevalence of the menopause is suspected to be between this age group.[11] Study conducted by Dutta et al.[12] also found that postmenopausal generalized chronic periodontitis women fell into the age range of 45 and 55 years. El-Sayed et al.[13] noted the intrinsic alterations in human marrow stromal cells (hMSCs) with aging which included decrease in the proliferation and differentiation, an increase in senescence-associated β-galactosidase-positive cells and apoptosis in hMSCs, and an upregulation of the p53 pathway, all contributing to impaired osteoblast function and an age-related impairment in bone formation.

On comparing mean body mass index, patients in Group C (27.21 ± 0.843) were found to be overweight and showed statistically significant differences than Groups A and B [Table 1]. This is consistent with the studies done by Felson et al.[14] and Nguyen et al.,[15] who stated that overweight and obese females are more likely to have osteoporosis and osteopenia. This may be due to high level of the obesity hormone “adiponectin” in the blood that might increase the fragility of skeletons and the risk of fractures because of reduced muscle strength and lower muscle mass. It was also reported that adipose tissue from obese individuals preferentially releases pro-inflammatory cytokines such as TNF-α, IL-6, leptin, visfatin, resistin, angiotensin II, and plasminogen activator inhibitor-1 that modulate insulin resistance as well as immunity and inflammation. In our study, one individual in Group A was found to be underweight and shown to have less systemic BMD. This could be due to reduced calcium intake.

The mean number of teeth present in all the three groups was similar and hence found to be nonsignificant. This study was similar to Slaidina et al.[16] who also did not find any correlation of the number of teeth between the groups. However, the present study was in contrast with the study done by Kribbs [17] who compared patients with and without osteoporosis and observed less number of teeth present in postmenopausal women as compared to premenopausal women. He suggested that the osteoporosis may be a very important factor in tooth loss. However, it may be noted that considering tooth loss as one of the parameters for periodontitis has its own limitations. Tooth loss may also occur due to dental caries [Table 1].

The patients in Group C (1.98 ± 0.3066) had high PI score which was found to be statistically significant when compared to Groups B (1.748 ± 0.2676) and A (0.8522 ± 0.1099). The results of the present study were concurrent with the studies done by Geurs [18] and Klemetti et al.[19] They also found a higher PI score in postmenopausal periodontitis women as compared to controls. It is suggested that higher PI in these postmenopausal women can further worsen their periodontal status. The mean probing depth (PD) and CAL were found to be statistically significant in Group C when compared to Groups A and B [Table 1]. Similar findings were drawn by Reinhardt et al. who reported high clinical attachment loss in osteoporotic women with estrogen deficiency [Table 1].[20]

In Group C, when we correlated the clinical parameters such as PD, CAL, with BMD, we found that with decrease in BMD, there was increase in CAL and PD [Table 1]. This was in accordance with the study conducted by Shen et al.[21] who also showed an increased attachment loss in osteoporotic sites in postmenopausal women suggesting that osteoporosis may act as a risk factor for periodontitis. Klemetti et al.[19] found that women with higher skeletal BMDs retained teeth with deeper periodontal pockets more easily than those with osteoporosis. However, osteoporosis does not seem to be the only major etiological factor in the pathogenesis or progression of periodontal disease as in the present study; greater PD and attachment loss were noted in sites with poor plaque control [22]. This implies that the dental bacterial plaque still plays a very important role in the progression of periodontal disease than the bone loss due to other systemic factors.

The mean interproximal alveolar bone loss was higher in Group C (7.65 ± 0.960) than in Groups B and A. This was in accordance with Payne et al.[23] and Streckfus et al.[24] who also found more alveolar bone loss in postmenopausal women with estrogen deficiency. It is suggested that the estrogen deficiency increases OC formation by increasing hematopoietic progenitors and providing a large recruited OC precursor pool. The upregulated formation and activation of OCs lead to cortical porosity and enlarged resorption areas in trabecular surfaces. Furthermore, the surface concentration of receptor activator of nuclear factor kappa-B ligand (RANKL) per cell is increased in postmenopausal women compared to premenopausal women by two to threefold for MSCs, T-cells, B-cells, and total RANKL expressing cells.[25]

There was a decrease in BMD of dual femur and spine in postmenopausal periodontitis women (Group C) as compared to Groups A and B which was found to be statistically significant [Table 1]. This is in accordance with the NHANES III study done by Ronderos et al.,[26] Inagaki et al.[27] who also found a low BMD with high PI and CAL. It is stated there is a higher concentration of circulating sclerostin, produced by osteocyte which has antianabolic effects on bone formation in postmenopausal women. In estrogen deficiency, TNF-α is increased which may stimulate the expression of sclerostin through the MEF2 transcription factor. Thus, TNF-mediated increase in sclerostin may partially contribute to postmenopausal osteoporosis.[28]

To ensure accurate measurements of BMD in our study, dual energy X-ray absorptiometry was used in both dual femur and the lumbar area (L2–L4) since it is still considered as the “gold standard” for diagnosis of osteoporosis which is in concurrence with the study by Tezal et al.[29]

The T-score of dual femur of Group A, Group B and Group C was found to be 0.78 ± 0.964, −1.420 ± 1.413, −3.050 ± 1.00 respectively. Similarly the T-score of PA spine of Group A, Group B and Group C was found to be −0.270 ± 0.0.384, −1.760 ± 1.718, −3.070 ± 1.31, respectively. The T-score dual femur (−3.050 ± 1.00) and AP spine (−3.070 ± 1.31) was found to be lower in Group C when compared with Groups A (0.78 ± 0.964, −0.270 ± 1.204) and B (−1.420 ± 1.413, −1.760 ± 1.718) which indicates that bone density was below the “young adult mean” (−2.5 or lower) in Group C, suggestive of osteoporosis. The T-score value of dual femur and lumbar spine in Group A women were between the reference range and found to be normal, whereas one patient reported to have osteopenia (10%).

Out of 10 postmenopausal women in Group C, the proportion of osteopenia and osteoporosis was found to be 60% and 30%, respectively, higher than Group B [Table 2]. This is in accordance with the Suresh et al.[30] who also showed higher proportions of osteopenia than osteoporosis in postmenopausal women. This shows that there may be an association between systemic osteopenia and periodontal status in postmenopausal women.

On comparing PI, probing pocket depth, CAL, and interproximal alveolar bone loss, Group C was found to have higher values when compared to Groups A and B which was statistically significant [Table 1]. Furthermore, the BMD and T-score (dual femur and PA spine) were found to be low in Group C when compared to Groups A and B suggesting the positive correlation between the systemic BMD and periodontal status.

   Conclusion Top

Postmenopausal women with generalized chronic periodontitis exhibited severe periodontal destruction with less BMD. Hence, it is suggested that periodontitis may be a risk indicator for osteoporosis in postmenopausal women and vice versa. It is suggested that the pro-inflammatory cytokines and prostaglandins are increased in both periodontitis and osteoporosis. Hence, the severity and extent of alveolar bone loss in postmenopausal women may be a risk indicator for systemic bone loss. The risk of periodontal disease progression that would prevent the further progression of systemic osteoporosis for women who are at a higher potential risk for osteopenia and osteoporosis.

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Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2]

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