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Longitudinal Study of Bone Density and Periodontal Disease in Men
1 Oregon Health & Science University, CR 113, 3181 SW Sam Jackson Park Road, Portland, OR 97239, USA; and Correspondence: * corresponding author, krp123{at}charter.net
Bone loss is a feature of both periodontitis and osteoporosis, and periodontal destruction may be influenced by systemic bone loss. This study evaluated the association between periodontal disease and bone mineral density (BMD) in a cohort of 1347 (137 edentulous) older men followed for an average of 2.7 years. Participants were recruited from the Osteoporotic Fractures in Men Study. Random half-mouth dental measures included clinical attachment loss (CAL), pocket depth (PD), calculus, plaque, and bleeding. BMD was measured at the hip, spine, and whole-body, by dual-energy x-ray absorptiometry, and at the heel by ultrasound. After adjustment for age, smoking, race, education, body mass index, and calculus, there was no association between number of teeth, periodontitis, periodontal disease progression, and either BMD or annualized rate of BMD change. We found little evidence of an association between periodontitis and skeletal BMD among older men.
Key Words: periodontal disease • osteoporosis • epidemiology • men
Bone loss is a common feature of both periodontitis and osteoporosis, and it is biologically plausible that periodontal destruction is influenced by systemic bone loss. Although numerous studies support the existence of a relationship between the two disease processes, most have been plagued by small sample sizes, inadequate control of confounding factors, and cross-sectional study design (Wactawski-Wende, 2001). In addition, almost all have focused on women, specifically post-menopausal women. The focus on post-menopausal women can be partially attributed to the fact that osteoporosis is more common in women than in men; however, osteoporosis in men is an enormous public health problem. Bone mass measurements performed in the National Health & Nutrition Examination Survey (NHANES) III revealed that from 1 to 2 million men over 50 have osteoporosis at the femoral neck, and from 8 to 13 million have osteopenia at that site (Looker et al., 1997). Low bone density is strongly linked to increased fracture risk. A longitudinal observational study in the community of Dubbo, Australia, found the lifetime risk of low trauma fracture in 60-year-old men to be 26% (Nguyen et al., 1996). The majority of this risk comes after 65, when vertebral and hip fracture rates begin to show an exponential increase. The care of fractures in men represents 20% of the annual economic burden of osteoporosis in the US (Ray et al., 1997). The reason for the rapid increase in fracture rates with aging in men is complex, but in large part reflects loss of skeletal mass. To date, only two published studies have evaluated the association between periodontal disease and osteoporosis in men. Using data from NHANES III, Ronderos et al. (2000) found an association between age- and race-adjusted femoral bone mineral density (BMD) and mean clinical attachment loss in men and women. Once smoking was controlled for, however, the association became non-significant in men. In contrast, a small (n = 86) longitudinal study found that Japanese men with low calcaneal BMD had significantly more periodontal sites with attachment loss of 3 mm or more after 3 yrs of follow-up (Yoshihara et al., 2004). The purpose of this study was to determine if skeletal BMD is associated with both the prevalence and progression of periodontal disease in a cohort of well-characterized older men.
The Osteoporotic Fractures in Men (MrOS) Study is a prospective, observational study designed to determine risk factors for osteoporosis and fractures in a cohort of community-dwelling men 65 yrs of age and older. During 2000–2002, MrOS recruited 5995 men at six clinical sites in the US: Birmingham, AL; Minneapolis, MN; Palo Alto, CA; Pittsburgh, PA; Portland, OR; and San Diego, CA (Blank et al., 2005; Orwoll et al., 2005). In 2002–2003, we invited MrOS study participants at two of the clinical sites, Portland and Birmingham, to participate in the MrOS Dental Study. Recruitment began by invitation letters sent to participants in the order in which they were initially enrolled. Staff then contacted participants by telephone to explain the study and schedule the visit. Men who completed the first MrOS Dental Study visit (Visit 1) were invited to a second visit (Visit 2) in 2005–2006, an average of 2.7 yrs after Visit 1 (SD = 0.2, range = 1.9–3.5). This study was approved by the Institutional Review Boards at Oregon Health & Science University and the University of Alabama at Birmingham; informed consent was obtained from all participants.
Periodontal Assessment The distance from the cemento-enamel junction to the base of the pocket (clinical attachment loss) and the distance from the gingival margin to the base of the pocket (pocket depth) were measured at 6 sites per tooth. All measurements were made in millimeters and rounded to the nearest whole millimeter. For plaque, calculus, and gingival bleeding, the worst score per tooth was recorded. We used the Silness and Löe Plaque Index (Löe, 1967) and the Löe and Silness Gingival Index (Löe and Silness, 1963). Calculus was classified as none, supragingival only, or subgingival.
We identified periodontitis and periodontitis progression based on the case definitions proposed by the European Workshop in Periodontology (Tonetti and Claffey, 2005), with one modification to account for our half-mouth design. Our criterion for a periodontitis case was the presence of proximal attachment loss of
Bone Mineral Density Measurements
Statistical Analysis We assessed inter-examiner reliability for the periodontal examination on a subset of 56 participants who had a second periodontal examination by the study periodontist ("gold standard") at each site. We used nested models to summarize the percentage of total variability explained by the examiner. The inter-examiner r2 was 62% for clinical attachment loss and 61% for pocket depth. To account for inter-examiner error, all statistical models with periodontal examination data included the examiner as a covariate. To optimize longitudinal measurement precision, we incorporated quality assurance measures into the DEXA and QUS protocols, including central training of technicians and daily phantom scanning. In addition, a single set of phantoms was scanned at both sites, to provide the cross-calibration data for multi-site data analyses. The intra-clinic coefficients of variation for DEXA hip phantoms (from 0.3% to 0.6%) and QUS phantoms (4.9%, 5.1%) were within acceptable limits. All statistical models with BMD included ’clinic’ as a covariate.
Baseline Characteristics Of the 1976 men enrolled in MrOS from Portland and Birmingham, 1347 (68%) attended Visit 1, including 137 edentulous (10%) and 1210 dentate men (90%). Compared with the dentate participants, a higher proportion of the edentulous men had less than a college education (47% vs. 17%, p < 0.01) and had smoked for 20+ pack-years (61% vs. 32%, p < 0.01). Edentulous men were less likely to report their overall health as excellent or good (78% vs. 88%, p < 0.01) and had a higher mean BMI (28.2 vs. 27.2, p < 0.01). There were no other differences between the edentulous and dentate men in terms of age, race, self-reported diabetes, daily calcium intake, or mean number of alcoholic drinks per week.
The dentate men had, on average, 23 teeth and a mean CAL and PD of 3.02 mm and 2.52 mm, respectively. The prevalence of CAL
Follow-up Characteristics Eighty-four percent (n = 1133) of the men who completed Visit 1 attended Visit 2. Reasons for not attending Visit 2 included death (n = 89), refusal because of health problems (n = 64), and refusal for other reasons (n = 61). The men who did not attend Visit 2 were older (77 vs. 74 years, p < 0.01), were less likely to have attended college (26% vs. 18%, p < 0.01), and were more likely to have smoked for 20+ pack-years (24% vs. 17%, p < 0.01). Of those who did not attend, 48% had periodontitis at baseline, compared with 36% of those who did attend Visit 2 (p < 0.01).
Bone Mineral Density and Number of Teeth
Bone Mineral Density, Periodontitis, and Periodontal Disease Progression Among the dentate men at Visit 1 (n = 1210), there was no association between adjusted BMD and number of teeth, mean CAL, or mean PD (data not shown). There was also no association between periodontitis at baseline, BMD, or rate of BMD change at any anatomical site (Table 3  ). Surprisingly, men with periodontal disease progression between Visit 1 and Visit 2 had greater mean total hip and femoral neck BMD at baseline (Table 3).
Clinical measures of periodontal status (number of teeth, mean CAL, mean PD, percent of sites with CAL  5 mm, percent of sites with PD 6 mm, percent of men with a history of periodontitis, and percent of men with periodontal disease progression) did not differ by quartile of total hip BMD measured at Visit 1 (Table 4), or by quartile of BMD at any other skeletal site (data not shown). There was also no difference in the clinical measures of periodontal status among osteoporotic, osteopenic, and men with normal BMD (data not shown).
The MrOS Dental Study is the first to evaluate the relationship among clinical measures of periodontal status, periodontal disease progression, and skeletal BMD in a large, well-characterized cohort of older men. By incorporating periodontal examinations into an ongoing study of osteoporosis and fractures, we were able to evaluate the relationship between these two disease processes while controlling for known confounding variables. We found no association between clinical measures of periodontal disease and BMD measured at a variety of skeletal sites. Our findings are similar to those of Ronderos et al. (2000), who found (after adjusting for smoking and calculus) no association between femoral BMD and clinical attachment loss in the 5733 men aged 20 yrs and older examined during NHANES III. While few studies have focused on this issue in men, several cross-sectional studies have attempted to assess the relationship between BMD and CAL in women. Of such studies published since 1990, three reported no relationship (Weyant et al., 1999; Tezal et al., 2000; Pilgram et al., 2002), while two found significant negative correlations between BMD and CAL (Mohammad et al., 1997, 2003). It should be noted that the sample sizes for all of these studies were small (from 30 to 292 participants). The relationship between BMD and CAL in women examined during NHANES III was more complex. After adjustment for confounders, women with high calculus scores and low BMD had significantly more CAL than women with normal BMD and similar calculus scores, while no association was observed among women with low and intermediate levels of calculus. This led the authors to speculate that, in the presence of calculus, osteoporosis increases the risk of CAL in women (Ronderos et al., 2000).
Cross-sectional studies, although useful, have inherent limitations, including the investigators’ inability to determine temporality, which can be better established through prospective studies. The only other prospective cohort study to evaluate the relationship between periodontal disease and BMD in men (n = 86) found that Japanese men with low calcaneal BMD had more periodontal sites with Our one unexpected finding was the relationship between baseline hip BMD and periodontal disease progression. Total hip and femoral neck BMD were 2.1% and 2.6% higher in men with periodontal disease progression, compared with percentages in men without progression. The biological basis for higher rates of periodontal progression in men with higher BMD was not apparent. Since BMD at other skeletal sites was not lower in men without disease progression, and there was no difference in the rate of BMD change between the two groups, we believe that this finding may have occurred by chance. Our study included a large number of well-characterized participants with careful periodontal assessments and measures of BMD at multiple skeletal sites. However, there are at least 3 limitations. First, our study population may not be representative of the general population of older men. Compared with the general US population of men aged 65 yrs and older, MrOS Dental Study participants were less often edentulous, more highly educated, and less likely to smoke. Because of this, our study cohort may have arrived into old age being "periodontitis-resistant". Nevertheless, a large fraction (38%) had periodontitis, and it is unlikely that a strong relationship between periodontal status and BMD was not detected. Second, our periodontal assessment was limited to a half-mouth, and our analysis did not include radiographic measures of oral BMD or bone height. In addition, the majority of our study participants were white non-Hispanic, so the results may not reflect the association between periodontal disease and BMD in other racial groups. In conclusion, we found no association among tooth loss, clinical periodontal status, and skeletal BMD in older men.
The MrOS is supported by grants from the NIH: UO1AG18197-02, UO1AR45580-02, UO1AR45614, UO1AR45632, UO1AR45647, UO1AR45654, UO1AR45583, M01RR00334, and R01DE14386-01. A preliminary report was presented at the AADR Annual Meeting in Orlando, FL, March, 2006. Received for publication December 27, 2006. Revision received May 29, 2007. Accepted for publication June 21, 2007.
Journal of Dental Research, Vol. 86, No. 11,
1110-1114 (2007) This article has been cited by other articles:
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ABSTRACT
INTRODUCTION
–2.5), osteopenic (T-score > –2.5 and 
