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RAPID COMMUNICATION |
1 Department of Diagnostic Sciences, University of Alabama at Birmingham School of Dentistry, SDB 219, 1530 3rd Avenue South, Birmingham, AL 35294-0007, USA; and
2 Department of Cariology, Restorative Sciences and Endodontics, University of Michigan School of Dentistry, Ann Arbor, USA;
* corresponding author, mafisher{at}uab.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: periodontal diseases • periodontal attachment loss • tobacco • smoking • smokeless tobacco
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Previous findings of the effect of smokeless tobacco on periodontal health have been limited to attachment loss manifested as gingival recession at the usual site of tobacco placement (Weintraub and Burt, 1987; USDHHS, 2000). The recession has been postulated to be a result of mechanical injury from either the abrasive nature of the smokeless tobacco products or from vigorous toothbrushing at the site of its placement (Robertson et al., 1990; Christen, 1992). Data are insufficient to support an association between smokeless tobacco use and severe periodontitis (Weintraub and Burt, 1987; Robertson et al., 1990). There is a gap in knowledge regarding the effect of smokeless tobacco on periodontal diseases; existing information has been derived from case reports (Christen et al., 1979) and several cross-sectional studies in young adults (Greer and Poulson, 1983; Offenbacher and Weathers, 1985; Robertson et al., 1990). There are no reports of an association between smokeless tobacco and severe active periodontal disease from large, population-based epidemiologic studies.
The purpose of this study was to assess the association between smokeless tobacco use and severe active periodontal disease using the population-based Third National Health and Nutrition Examination Survey (NHANES III), a dataset representative of the civilian, non-institutionalized US population.
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Description of the Dependent Variable
Severe active periodontal disease was defined as an individual having at least 1 tooth with 6 mm or more attachment loss, and bleeding on the same tooth. Because this definition could indicate gingivitis with severe mechanical gingival recession only, an interproximal definition which required the ‘6 mm or more’ attachment loss to be at the interproximal site (mesial), with bleeding on the same tooth, was also utilized, henceforth referred to as ‘interproximal severe active periodontal disease’. These definitions comply with the recommendation that severity of periodontal disease be categorized on the basis of the amount of attachment loss rather than on pocket depth, because the gingival margin is not a fixed reference point from which to measure (Armitage, 2004). Pocket depth is a reversible measure, while attachment loss is irreversible.
Description of Independent Variables
The main exposure variable, regular use of smokeless tobacco, was defined as a categorical variable: never, former, and current use. The potential explanatory variables included those previously recognized as important covariates: smoking history (never, former, or current regular smoker), age (18–34, 35–54, 44–74, or 75 yrs and older), race (minority or Non-Hispanic White), gender, education (high school graduate), diabetes (self-reported, or undiagnosed based on either one-hour fasting plasma glucose level of at least 126 mg/dL or the two-hour oral glucose tolerance test result of at least 200 mg/dL glucose after a 75-g glucose challenge), and having a dental visit in the past year.
Statistical Methods
The hypothesis that smokeless tobacco use is independently associated with severe active periodontal disease was tested by univariable (one dependent variable and one independent variable) and multivariable (one dependent variable and multiple independent variables) logistic regression modeling, with a separate model for smokeless tobacco and severe active periodontal disease among all adults, and for analyses restricted to never-smokers. Separate multivariable logistic regression models, for all adults or never-smokers, quantified the association of smokeless tobacco use with (1) severe active periodontal disease and (2) interproximal severe active periodontal disease. Analyses were conducted with SAS-Callable SUDAAN version 8.0.2 (Research Triangle Institute, 2003, Research Triangle Park, NC, USA) and SAS Systems for Windows®, version 9.00 (SAS Institute, Inc., 2002, Cary, NC, USA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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and 2 depict the descriptive summary with the corresponding crude odds ratios and 95% confidence intervals (ORCrude; 95%CI) for the univariable, unadjusted association between severe active periodontal disease and smokeless tobacco use, and the other potential explanatory variables. The adjusted, multivariable analyses of the association between severe active periodontal disease and smokeless tobacco use, adjusted for smoking (or restricted to never-smokers), diabetes, age, race, gender, and seeing a dentist in the past year are reported in Table 3.
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). The associations between severe active periodontal disease and the potential explanatory variables were similar for all adults and adult never-smokers. All adults and never-smokers were approximately twice as likely to have severe active periodontal disease if they currently used smokeless tobacco (ORCrude = 2.1 or 2.3, respectively), currently used smoked tobacco (ORCrude = 1.7), formerly used smoked tobacco (ORCrude = 2.3), were in a minority group (ORCrude = 1.8), or were male (ORCrude = 1.7 or 1.2, respectively) (Table 1). Older adults were 4 to 23 times more likely to have severe active periodontal disease, with the association increasing as age increased: for all adult 35- to 54-year-olds (ORCrude = 5.8); 55- to 74-year-olds (ORCrude = 14.0); those 75 yrs old and older (ORCrude = 22.8), and for ‘never-smoker’ 35- to 54-year-olds (ORCrude = 4.0); 55- to 74-year-olds (ORCrude = 12.5); and those 75 yrs old and older (ORCrude = 23.9). All adults (ORCrude = 4.5) and never-smokers (ORCrude = 5.7) with diabetes were over 4 times more likely to have severe active periodontal disease. All adults and never-smokers who did not graduate from high school (ORCrude = 3.0 or 4.0, respectively), or who did not visit the dentist in the past year (ORCrude = 1.8 or 2.4, respectively), were more likely to have severe active periodontal disease (Table 1).
After simultaneously taking into account smokeless and smoked tobacco use, diabetes, age, minority status, gender, and visiting the dentist in the past year, we found that there were substantial differences in the association between severe active periodontal disease ORAdj (Table 3) and the ORCrude (Table 1) for all adults with diabetes (ORAdj = 2.2 vs. ORCrude = 4.5) and never-smokers with diabetes (ORAdj = 2.3 vs. ORCrude = 5.7), for all adults 75 yrs old and older (ORAdj = 31.2 vs. ORCrude = 22.8) and for never-smokers 75 yrs old and older (ORAdj = 40.0 vs. ORCrude = 23.9), and former smoked tobacco use was no longer significant (ORAdj = 1.4). While current smokeless tobacco use was not statistically significant for never-smokers (ORAdj = 2.1), it was consistent with that in the crude analysis (ORCrude = 2.3) and with all adults (ORAdj = 2.1), and was noteworthy in approaching significance (p = 0.0637). Because the analysis restricted to never-smokers substantially reduced the sample size of those with severe active periodontal disease from 596 to 240 (Table 1), this limited the power to detect a statistically significant difference.
Interproximal Severe Active Periodontal Disease
Among all 12,932 adults in this study, 1.9% had interproximal severe active periodontal disease, compared with 1.2% of the 7061 adult never-smokers (weighted percent, Table 2). The strength of the associations between interproximal severe active periodontal disease and the independent variables (Table 2) was similar to that of severe active periodontal disease (Table 1).
The comparison of the univariable and multivariable analyses for interproximal severe active periodontal disease [ORAdj (Table 3) with the ORCrude (Table 2)] was similar to that of severe active periodontal disease, with substantial changes in the associations with diabetes and age; ‘former smoked tobacco use’ was also no longer statistically significant (ORAdj = 1.5 vs. ORCrude = 2.4).
Simultaneously adjusted for smoking, diabetes, age, minority status, gender, and having a dental visit in the past year (Table 3), all adults who currently used smokeless tobacco were 2.1 times more likely to have interproximal severe active periodontal disease, but current smokeless tobacco use was not statistically significant for never-smokers (ORAdj = 2.3), although the 95% confidence interval (0.9 to 6.3) was very consistent with that in the crude analysis and was noteworthy in approaching significance (p = 0.1001). Because the analysis restricted to never-smokers substantially reduced the sample size of those with interproximal severe active periodontal disease from 433 to 173 (Table 2), this limited the power to detect a statistically significant difference. Hence, given the limitation in sample size, we reduced the number of parameters and tested another candidate model for never-smokers. When only those covariates with the strongest associations were included, smokeless tobacco was statistically significant; never-smokers who currently used smokeless tobacco were almost three times more likely to have interproximal severe active periodontal disease (ORAdj = 2.8), simultaneously adjusted for diabetes, age, and race (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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The definition of periodontal disease used in this study follows the recommendation that periodontal disease severity be measured based on irreversible attachment loss rather than on reversible pocket depth (Armitage, 2004). Attachment loss is an important component of the periodontal disease measure that defines past history of disease. To address the concern that any association between attachment loss and smokeless tobacco is limited to mechanical trauma, we also analyzed attachment loss restricted to interproximal sites. However, measuring attachment loss, per se, does not indicate present disease activity (Burt and Eklund, 1999; Beck and Elter, 2000). Adding a clinical parameter of current disease activity provides a more useful measure of periodontal disease (Burt and Eklund, 1999) that is especially pertinent in the assessment of current exposure to tobacco. Thus, the use of a proxy measure of severe active periodontal disease, that adds bleeding on probing as a measure of current disease status, helps to address a potential shortcoming of previously published reports that measured only past history of disease. Bleeding on probing has been shown to be an important risk predictor for increased attachment loss (Lang et al., 1986; Armitage, 1996), although this has not been universally reported. While bleeding on probing may be related to many factors—such as probing force and depth, probe diameter, and the presence of inflammation—its absence is a good indicator of periodontal disease stability (Tu et al., 2004).
It has been reported that smokers have less bleeding on probing than do never-smokers (Dietrich et al., 2004). If this is due to nicotine, then there may be an underestimate of the prevalence of severe active periodontal disease among smokeless tobacco users (and smokers). This potential misclassification would bias the estimate of the association toward the null value. Thus, the true estimate of the association of smokeless tobacco use with severe active periodontal disease may actually be greater than that reported herein. A limitation of this study is the potential misclassification of self-reported smokeless tobacco use among those with and those without severe active periodontal disease. Upon further evaluation of the adult never-smokers, we detected differential misclassification in which those with severe active periodontal disease were more likely to report that they never used smokeless tobacco, although their level of serum cotinine was above that of environmental tobacco smoke exposure (Pirkle et al., 1996), indicating that our findings may actually underestimate the true association.
The consistent odds ratios for the presence of severe active periodontal disease associated with smokeless tobacco use in both the crude and adjusted models suggest that smokeless tobacco use is a strong risk indicator, even after adjustment for other important explanatory variables known to be associated with periodontal disease prevalence. In addition, we considered the recent recommendation that rigorous methodological and analytical control of smoking is necessary when associations with periodontal disease are studied (Hujoel, 2002), and the suggestion that never-smokers and smokers should be analyzed separately (Spiekerman et al., 2003), particularly since smoking has a strong association with most clinical measures of periodontal disease (Hujoel et al., 2003). To remove the effect of smoking, we also conducted additional analyses limited to never-smokers. Using the same set of covariates as used for all adults, we observed an association of similar magnitude between either interproximal or severe active periodontal disease and smokeless tobacco in our candidate model for never-smokers. These observations for never-smokers provide additional evidence to support our finding of a significant association between smokeless tobacco use and severe active periodontal disease. Taken in their entirety, our findings indicate that smokeless tobacco may be an important risk factor for severe active periodontal disease in US adults.
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ACKNOWLEDGMENTS |
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Received August 17, 2004; Last revision February 1, 2005; Accepted May 10, 2005
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REFERENCES |
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