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Osteoporosis and Oral Infection: Independent Risk Factors for Oral Bone Loss
1 Department of Social and Preventive Medicine and Correspondence: * corresponding author
Studies have suggested that oral bone loss is independently influenced by local and systemic factors, including osteoporosis. This cross-sectional study of 1256 post-menopausal women, recruited from the Buffalo center of the Women’s Health Initiative Observational Study, evaluated the influence of oral infection and age on the associations between osteoporosis and oral bone loss. Systemic bone density was measured by dual-energy x-ray absorptiometry. Alveolar crestal height was measured from standardized dental radiographs. Oral infection was assessed from subgingival plaque samples. Total forearm density [β (SE) = –0.931 (0.447), p = 0.038] and presence of Tannerella forsythensis [β (SE) = 0.125 (0.051), p = 0.015] were independently associated with mean alveolar height among women aged < 70 years after confounder adjustment. Women aged 70+ years had worse oral bone loss, in general, but neither bone density nor oral infection was significantly associated with mean alveolar height in this age group. Systemic bone density and oral infection independently influenced oral bone loss in post-menopausal women aged < 70 years.
Key Words: bone density • osteoporosis • post-menopausal • dental plaque • periodontal diseases • alveolar bone loss
Periodontal disease may be associated with systemic diseases, including osteoporosis. A recent review described several mechanisms of association for periodontal disease and osteoporosis (Wactawski-Wende, 2001). Imbalanced bone remodeling associated with osteoporosis can lead to a net loss of bone density throughout the skeleton, including the oral cavity, possibly providing a more susceptible environment for insult by bacteria. Infection with certain subgingival bacteria can lead to periodontal disease through increased cytokine production and inflammation, which may be exacerbated by increased systemic cytokine levels associated with osteoporosis. The two diseases may have multiple risk factors in common. There may be multiple mechanisms by which osteoporosis and periodontal disease (and oral bacteria) are linked. Previous studies’ results of alveolar crestal height loss and systemic bone mineral density have been inconsistent. Some studies found low bone density (Payne et al., 1999; Hildebolt et al., 2000, 2002; Tezal et al., 2000; Wactawski-Wende et al., 2005) and post-menopausal status (Streckfus et al., 1997) to be significantly associated with alveolar crestal height. Other studies have not (Elders et al., 1992; Lundstrom et al., 2001). In general, studies found a trend that lower bone density was associated with worse alveolar crestal height. Different study populations, small sample sizes, and lack of consideration of confounding variables and effect modifiers may explain some of this inconsistency. In the present study, we explored the associations between osteoporosis and oral bone loss, assessing whether oral bacteria and age modify those associations. To our knowledge, studies evaluating the joint associations among oral bacteria, osteoporosis, and alveolar crestal height have not been previously published.
The cross-sectional study, "Risk Factors for Osteoporosis and Oral Bone Loss", was an ancillary study of the Buffalo, NY, center of the Women’s Health Initiative’s Observational Study. The Institutional Review Board at the University at Buffalo approved the study. Participants provided signed consent. Inclusion criteria were at least 6 teeth present and no history of other bone disease, bilateral hip replacement, cancer diagnosis (preceding 10 yrs), or other serious illness. A total of 1256 post-menopausal women met these criteria and had data for the main study variables. Participants completed self-administered questionnaires and had physical measurements and bone densitometry taken. An oral health examination included assessment of missing teeth (number and reason), subgingival microbiological sampling, and oral radiographs.
Bone Mineral Density
Oral Infection We used this formalin-fixed sample to assess the presence of micro-organisms by indirect immunofluorescence microscopy, using species-specific polyclonal and monoclonal serodiagnostic reagents according to a method described previously (Bonta et al., 1985; Zambon et al., 1985). Fluorescence was graded from 1+ to 4+, with 3+ and 4+ considered serologically positive reactions. Plaque smears were considered positive for a given bacterial species if they demonstrated 5 or more strongly fluorescent cells with well-defined cell outlines and dark or lightly fluorescing centers, and constituted more than 1% of the total cell count, determined by phase-contrast microscopy. Although some quantification was made and other species were assessed, only data on the presence or absence of Tannerella forsythensis were used in these analyses.
Oral Bone Loss
Statistical Analysis
Most post-menopausal women in this study were < 70 yrs old (65.6%), white (97.4%), educated beyond high school (79.1%), had never smoked cigarettes (53.0%), and were currently taking hormone therapy (46.1%), calcium (71.0%), or vitamin D (64.0%) supplements (Table 1  ). Subgingival infection with T. forsythensis was present in 37.9% of participants. Mean alveolar crestal height in the total study sample was 2.46 ± 0.77 mm (data not presented). Mean alveolar crestal height increased as the T-score group worsened (2.32 mm, 2.43 mm, and 2.65 mm, respectively, for normal, osteopenia, and osteoporosis) and was higher when T. forsythensis was present (2.56 mm vs. 2.39 mm when T. forsythensis was absent) (p < 0.001). Continuous bone density measures at all skeletal sites were inversely correlated with alveolar crestal height (p  0.001).
We evaluated associations between bone density and alveolar crestal height or T-score group and clinical oral bone loss after adjustment for age, smoking status, hormone therapy, weight, education, and calcium and vitamin D supplementation. Among all participants, results were non-significant based on continuous bone mineral density (Table 2 ), but were significant with T-score group [odds ratio (OR) (95% confidence interval (CI)]: 1.77 (1.10–2.85)) (Table 3). Further adjustment by T. forsythensis infection did not provide evidence of confounding by that variable in either set of analyses. We also did not find evidence of effect modification by T. forsythensis infection (p > 0.20).
There was an interaction between age group (< 70 or 70+ yrs) and bone densities of the total forearm (p = 0.016), one-third radius (p = 0.005), and whole-body (p = 0.090) and worst-site T-score groups (p = 0.103 and 0.098 for osteopenia and osteoporosis, respectively) (data not presented). Linear regression results were stratified by age. Among women < 70 yrs of age, total forearm and one-third radius bone densities and T. forsythensis infection were significantly and independently associated with mean alveolar crestal height, even after adjustment for each other and additional confounding variables (Table 2  ). Whole-body bone density was marginally significant in this model (p = 0.06). A decrease of 0.2 g/cm2 in total forearm, one-third radius, or whole-body bone density was associated with an increased mean alveolar crestal height of 0.19 mm, 0.17 mm, or 0.10 mm, respectively. T. forsythensis infection was associated with approximately 0.12 mm worse mean alveolar crestal height. Among women 70+ yrs of age, neither bone density nor infection was significantly associated with mean alveolar crestal height.
In logistic regression results (Table 3
We found significant inverse associations between systemic bone density variables and oral bone loss variables, which were highly attenuated (no longer statistically significant) after adjustment for confounding factors. We determined that T. forsythensis infection was not a confounder of the association between systemic bone density and alveolar crestal height. We also investigated a potential interaction between systemic bone density and T. forsythensis infection, but this was not statistically significant. Importantly, we found a significant interaction between systemic bone density and age. The adjusted associations between bone density and alveolar crestal height were stronger among women aged < 70 yrs. Half of these women were at least 13 yrs past menopause. Since the first 5 to 10 yrs after menopause are associated with a period of estrogen depletion and consequent rapid bone loss, it is conceivable to find an association between bone density and alveolar crestal height recently after or during this period of bone loss. In logistic regression analyses, the association between worst-site T-score group and clinical oral bone loss also differed by age, but a stronger association existed among women aged 70+ yrs. Because of our results, we examined our definition of clinical oral bone loss ("disease"). Most women with disease had a mean alveolar crestal height > = 2 mm, regardless of whether they had one or more sites of alveolar crestal height 4+ mm or tooth loss due to periodontal disease, making this the most influential criterion defining disease. This cut-point is a relatively low level of alveolar crestal height. Our intent in setting this cut-point was to separate health and disease. If we used mean alveolar crestal height > = 3 mm to define disease in logistic regression, odds of disease for worse T-score levels were stronger and significant among women aged < 70 yrs, but not among older women. This helps to explain why we did not find a linear relationship among older women, as we did among younger women. T. forsythensis infection was significant only among younger women when alveolar crestal height > = 3 mm defined disease. We assessed bone density at several skeletal sites. For women aged < 70 yrs, associations with alveolar crestal height were consistently found for total forearm, one-third radius, and whole-body bone densities. These regions of the skeleton are less likely to be influenced by body weight and physical activity, compared with weight-bearing sites, such as the hip (Inagaki et al., 2001), and they have a greater proportion of cortical bone than other skeletal sites assessed (Jacobs et al., 1996). Perhaps this may explain why we found these sites to have the strongest associations with oral bone loss. Most other studies have assessed associations between alveolar crestal height and hip or spine bone density. This may be of interest, because bone density is commonly measured at these sites in clinical settings, but these studies did not consistently find a significant association with alveolar bone loss (Elders et al., 1992; Lundstrom et al., 2001). To our knowledge, no other studies have been published that assessed the association between forearm or whole-body bone density and alveolar crestal height specifically, though other periodontal disease measures have been studied. A longitudinal study found an increased risk of tooth loss with decreasing whole-body bone density (Krall et al., 1996). Other studies found that radius bone density was associated with number of teeth (Krall et al., 1994), second metacarpal bone density was associated with number of teeth and the community periodontal index of treatment needs (an index based on calculus, bleeding, and pocket depth) (Inagaki et al., 2001), and radius bone mass correlated with mandibular bone density and number of mandibular teeth (Kribbs et al., 1989, 1990). Associations between osteoporosis and periodontal disease may manifest in highly cortical skeletal sites compared with highly trabecular sites. Regression models adjusted for several confounding factors, but it is possible that residual confounding by these and other factors, such as passive smoking, may exist. A limitation of this cross-sectional study is that we cannot determine the temporality of these associations. Longitudinal studies are needed and are currently under way. It is also of interest to study systemic measures of immuno-inflammatory responses, as well as genetic factors, in relation to these associations, to improve our understanding of the potential mechanisms involved. Our study offers new evidence of associations between osteoporosis and periodontal disease in a relatively large group of post-menopausal women. Bacterial infection was not a confounder or effect modifier of the associations between systemic bone density and oral bone loss in this study. Systemic bone density and bacterial infection were independently, yet modestly, associated with oral bone loss among post-menopausal women aged < 70 yrs.
This study was supported by funding from NIH contract N01WH32122, NIH/NIDCR grants 1R01-DE13505 and DE04898, and USARMC grant DAMD 17-96-1-6319. This paper is based on a thesis submitted to the graduate faculty, University at Buffalo, in partial fulfillment of the requirements for the PhD degree.
5 (current address) Utah Department of Health, PO Box 142104, Salt Lake City, UT 84114, USA, gdn7{at}cdc.gov  Received for publication May 1, 2007. Revision received October 12, 2007. Accepted for publication December 20, 2007.
Journal of Dental Research, Vol. 87, No. 4,
323-327 (2008)
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ABSTRACT
INTRODUCTION