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No Alteration in Bone Mineral Density in Patients with Periodontitis lu-Sönmez1aolu3
1 Department of Periodontology, Faculty of Dentistry, Correspondence: * corresponding author
Alveolar bone destruction can be magnified in the presence of generalized skeletal disorders. We questioned whether severe generalized periodontitis patients display signs of bone metabolism disturbances. Our objective was to assess skeletal bone mineral density (BMD) and biochemical bone parameters in premenopausal women with periodontitis. Forty-five patients and 40 control individuals were included in the study. We measured BMD by dual-energy x-ray absorptiometry. The results showed no difference in BMD values between the periodontitis and control groups (p > 0.05). A positive relationship between the clinical attachment level and Body Mass Index (BMI) scores was observed (p = 0.03). Increased serum creatinine levels were noted in the periodontitis group (p = 0.04). Analysis of the data suggests that there is no evidence for an association between skeletal BMD and severe periodontitis in premenopausal women. There may be a link between elevated creatinine levels and periodontitis. The persons with high BMI scores seemed to be at risk for periodontitis.
Key Words: alveolar bone • osteoporosis • premenopause • tooth loss • BMI
Periodontitis is an infectious disease characterized by inflammation within the supporting periodontal tissues. In periodontitis, the response of alveolar bone to local bacterial and host-mediated factors leads to a tipping of the bone-remodeling balance in favor of bone resorption and loss of periodontal attachment (Schwartz et al., 1997). Osteoporosis is a systemic skeletal disorder that is characterized by reduction of bone mass, deterioration of bony structure, increased bone fragility, and escalated fracture risk (Conference Report, 1993). Both primary and secondary forms of osteoporosis have been defined, whereby the former is classified as idiopathic or involutional. Involutional osteoporosis encompasses the postmenopausal (type I) and senile types (type II). Secondary osteoporosis occurs as a result of a particular etiologic mechanism, such as an endocrine or a renal disease (Riggs, 1991). It might be expected that the alveolar bone destruction seen in periodontitis could be magnified in the presence of generalized skeletal disturbances (Klemetti et al., 1994; Carranza, 2002). As a result, several studies have been carried out in the past decade to evaluate the potential role of postmenopausal and/or senile osteoporosis with regard to the onset and progression of inflammatory periodontal disease (Hildebolt et al., 1997; Payne et al., 1999; Reinhardt et al., 1999; Weyant et al., 1999; Tezal et al., 2000; Lundström et al., 2001; Pilgram et al., 2002; Mohammad et al., 2003). Yet, the pertinent literature lacks sufficient evidence to provide unequivocal conclusions on this issue, since the results of the studies may easily have been confounded by factors such as the participants’ age, race, smoking habits, and hormone intake. Epidemiological studies have yielded an increase in the prevalence, extent, and severity of periodontal attachment loss with aging (Albandar, 1990; Haffajee et al., 1991; Albandar et al., 1999). Consequently, many age-related factors, including osteoporosis, may contribute to the alveolar bone loss observed in postmenopausal or elderly women. Pre-menopausal osteoporosis may also lead to decreased bone mass in women, for idiopathic or secondary reasons. Although osteoporosis has been suspected of being an aggravating factor for alveolar bone loss, no direct evidence has been available with respect to skeletal bone status in premenopausal women with periodontitis. We believed that the patients with severe and generalized periodontal attachment loss could provide a good working model for studying the underlying reasons for extensive alveolar bone destruction, and we questioned whether severe generalized periodontitis patients display signs of skeletal bone metabolism disturbances. Therefore, we designed the current cross-sectional study to assess vertebral and femoral bone mineral density (BMD) and systemic factors that affect bone metabolism in patients with severe generalized periodontitis, and to compare the results with those in periodontally healthy control individuals. Additionally, the data were evaluated for the correlation of selected clinical and systemic parameters.
Sample Size (Power) Calculation Initially, we analyzed data we had collected for other clinical studies with respect to BMD values, and noted that the standard deviation of the values in question was approximately 0.16 g/cm2. Consequently, we concluded that, to detect a difference of 0.10 g/cm2 between the BMD values of the periodontitis and control groups, with a 0.05 significance level and a power of 0.80, each group needed 40 people to be included in the study.
Study Population Inclusion criteria were that the individual must be: a non-smoker, having regular menstrual periods, and 45 yrs old or younger. Exclusion criteria were that the individual: showed systemic risk factors for periodontal diseases like diabetes, immunological, hematological, or malignant disorders; had received initial periodontal treatment in the preceding 6 mos; had a history of surgical periodontal therapy, taking antibiotics, anti-inflammatory, immunosuppressive, or cytotoxic drugs for at least 6 mos prior to the evaluation; or was receiving active treatment for osteoporosis (estrogen hormone, calcium, calcitonin, vitamin D, fluorides, or biphosphonates). The protocol for this study was approved by the Ethics Committee of Hacettepe University (#LUT 01/1), and informed consent was obtained from all the participants.
Study Design
First, following clinical periodontal parameters, we recorded: number of missing teeth, plaque index (Silness and Löe, 1964), calculus index (Greene and Vermillion, 1964), sulcus bleeding index (Mühlemann and Son, 1971), probing depth, and clinical attachment level (CAL). Calculus index/sulcus bleeding index scores and probing depth/CAL measurements were obtained from 6 points per tooth. The recordings were performed by a single examiner and included all the teeth except third molars (Table 1
Body Mass Index We calculated the participants’ body mass index (BMI), used as an indicator of overall adiposity, by dividing weight (kg) by the square of height (m2).
Assessment of Bone Mineral Density
Laboratory Evaluation
Statistical Analysis We used Pearson’s correlation coefficient to study the relationships among BMD, CAL, BMI, and number of missing teeth.
Statistical significance was accepted at p
Body Mass Index In the periodontitis group, the mean BMI score was 27.16 ± 5.01 kg/m2. For the control group, it was 25.11 ± 3.63 kg/m2. The difference was not found to be statistically significant (p = 0.06).
Bone Mineral Density
Biochemical Parameters The mean serum creatinine level was significantly higher in the periodontitis group than in the control group (p = 0.04) (Table 3  ).
There was no statistically significant difference in serum estradiol, osteocalcin, and urine deoxypyridinoline levels between the groups (p > 0.05) (Table 3  ). Similarly, no significant differences were noted between the groups with respect to liver and renal function tests, thyroid/parathyroid hormone, Vitamin D3 levels, and urinary calcium and creatinine excretions (p > 0.05) (Table 3).
Distribution of Osteoporotic, Osteopenic, and Healthy Individuals
Correlations of Selected Clinical and Systemic Parameters No significant correlation was found between the CAL and femoral (r = 0.075, p = 0.494) and lumbar (r = 0.034, p = 0.757) BMD values. However, a weak but statistically significant positive relationship between the CAL and BMI scores was observed (r = 0.243, p = 0.03).
Bone mineral density values from lumbar vertebrae (total L1-L4) were positively correlated with the number of missing teeth (r = 0.208, p = 0.05) as well as BMI scores (r = 0.312, p
In the present study, we aimed to assess skeletal BMD and systemic factors that affect bone metabolism in pre-menopausal women with severe generalized periodontitis, and to compare the results with those from periodontally healthy controls. Our findings revealed no significant difference between these two groups as to the mean BMD values of both the lumbar vertebrae and the hip. In addition, no significant correlation was noted between the CAL and femoral/lumbar BMD values. Collectively, analysis of these data suggests that there is no evidence for an association between skeletal BMD and severe periodontitis in pre-menopausal women. Noteworthy in the relevant literature are two studies, one by Von Wowern et al.(2001) and one by Inagaki et al.(2001). The former study measured bone mineral content from the mandible and forearm in 24 young adults (17 women and seven men) with severe periodontitis. They reported that severe periodontitis in young adults is a local disorder without systemic alterations of bone mineral status. Nevertheless, this study was limited by the fact that no control group was included, and some confounding factors, such as sex and smoking, were disregarded. Inagaki et al.(2001) analyzed the relationship between periodontitis and BMD in Japanese women. They determined bone mass by measuring metacarpal bone mineral density (m-BMD) and found a positive association between decreasing m-BMD and prevalence of periodontal disease in both pre- and post-menopausal women. The distinguishing features of our study are that it was primarily designed to evaluate BMD in pre-menopausal women with severe generalized periodontitis, and that the BMD measurements were accomplished with DXA, a well-accepted gold-standard technique. In this study, seven pre-menopausal women (six with periodontitis and one control individual) had BMD values that were considered to be osteoporotic. Among these women, one had hyperparathyroidism—thus, secondary osteoporosis—and the other six women had an idiopathic type of osteoporosis. Recently, Peris et al.(2002) studied the etiologic factors of pre-menopausal osteoporosis in 52 women. They found, as did we, that idiopathic osteoporosis is the most frequent diagnosis for pre-menopausal osteoporosis. Since it is the principal active circulating metabolite, in our study, we assessed individuals’ estrogen status by measuring plasma 17β estradiol levels. Analysis of our data indicated that no significant difference was observed in estradiol levels between the periodontitis patients and the control individuals. Sex steroids, such as estradiol, have been known for their positive effect on bone metabolism (Morgan et al., 2001). Herein, it is worthwhile to note that almost comparable estrogen levels could have contributed to our finding of no BMD differences between the periodontitis and control groups. Leanness is considered to be a risk factor for osteoporosis. Therefore, BMI scores of the participants included in the present study were interpreted. Our findings may suggest an association between being overweight and having periodontitis in pre-menopausal women. Similarly, Saito et al.(2001) have reported that waist-hip ratio, BMI, and body fat were significant risk indicators for periodontitis. More recently, Al-Zahrani et al.(2003) have also reported a significant association between the measures of body fat and the prevalence of periodontal disease among young adults. In accordance with the classic literature, analysis of our data showed a positive correlation between vertebral/femoral BMD values and BMI scores. This could be attributed to the surrounding fat tissue acting as a cushion, and thus decreasing the mechanical stress on the bones, as well as to ongoing estrogen metabolism in the adipose tissues (Morgan et al., 2001). In the present study, serum creatinine levels were found to be significantly higher in periodontitis patients than in the controls. Similarly, an association between elevated serum creatinine levels and periodontitis has been reported (Kshirsagar et al., 2005). These results may suggest an association of periodontitis with renal insufficiency. Further studies are needed to address the exact nature of this relationship. The relationship between tooth loss and BMD has long been evaluated in post-menopausal women (Elders et al., 1992; Klemetti and Vainio, 1993; Krall et al., 1994, 1996; Earnshaw et al., 1998; Taguchi et al., 1999). Several studies have suggested an association between tooth loss and diminished systemic BMD (Krall et al., 1994, 1996; Taguchi et al., 1999). In contrast, some studies, conducted in early post-menopausal women, failed to find such an association (Elders et al., 1992; Klemetti and Vainio, 1993; Earnshaw et al., 1998). To date, no direct evidence has been available about this relationship in pre-menopausal women. In the present study, BMD values were positively correlated with the number of missing teeth. These findings revealed that skeletal bone loss may not be a risk factor for tooth loss in pre-menopausal women. This study was limited by its cross-sectional design. Additionally, a wider range of study participants could not be achieved, since severe and generalized periodontitis is rarely seen. In conclusion, the results of this study suggest that there is no evidence of an association between skeletal BMD and severe periodontitis in pre-menopausal women. There may be a link between elevated creatinine levels and periodontitis. Also, the individuals with high BMI scores seem to be at risk for periodontitis. Further studies examining periodontal status in osteoporotic males or persons with idiopathic or secondary osteoporosis may provide valuable information about the relationship between periodontitis and osteoporosis.
The authors acknowledge the contribution of Prof. Hakan S. Orer. This study was supported by the Hacettepe University Scientific Research Unit (grant No. 01.01.201.001). This paper is based on a PhD thesis submitted to the Institute of Health Sciences, Hacettepe University.
4 present address, Haci Emin Efendi Sokak, Ugur Apartmani, No. 45/2, Nisantasi-Sisli, 34365, Istanbul, Turkey, haviye{at}ttnet.net.tr  Received for publication July 21, 2006. Revision received June 2, 2007. Accepted for publication August 29, 2007.
Journal of Dental Research, Vol. 87, No. 1,
79-83 (2008)
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ABSTRACT
INTRODUCTION
5 mm in vertical axis) and generalized (more than 30% of the sites in the horizontal axis) periodontal attachment loss. The control group was comprised of 40 pre-menopausal women (mean age, 36.17 yrs; range, 26–45 yrs) with no clinical evidence of periodontal disease. These individuals did not show any sites with probing depth > 3 mm and periodontal attachment loss > 1 mm. 
0.05. All analyses were performed with the SPSS for Windows 11.5 (SPSS Inc., Chicago, IL, USA) software package.