Association of Tobacco Exposure Patterns with Periodontal Health: A Cross-Sectional Analysis of NHANES Data

1. INTRODUCTION

Periodontitis is a chronic inflammatory disease and a leading cause of adult tooth loss [1]. It is a multifactorial condition, with Porphyromonas gingivalis recognized as a key pathogen within the periodontal biofilm, and microbial dysbiosis regarded as a primary contributor to the initiation and progression of the disease [2]. Disease progression is also driven by the host immune response to pathogenic microorganisms, leading to the destruction of gingival connective tissue and the resorption of alveolar bone. This process is associated with a shift from aerobic, Gram-positive bacteria to Gram-negative “red complex” pathogens, which are linked to elevated levels of pro-inflammatory cytokines [3]. The impact of periodontitis extends beyond the oral cavity. Chronic periodontal inflammation contributes to systemic inflammatory burden and has been associated with increased risk of cardiovascular disease, diabetes complications, dementia, adverse pregnancy outcomes, and respiratory conditions, highlighting that periodontitis is not only a local oral disease but also a significant public health concern with systemic implications [4-6]. There are various risk factors that can contribute to the development of periodontitis, including poor or inadequate oral hygiene, genetic predisposition, osteoporosis, diabetes, and environmental influences such as tobacco use, which can exacerbate disease progression.

Tobacco smoke is a common environmental exposure factor and remains a significant global public health concern due to its well-established role in the development and progression of numerous diseases [7, 8]. The association between smoking and periodontitis has been extensively documented, with current literature consistently demonstrating that tobacco use contributes to both the onset and advancement of periodontal disease [9-11]. Exposure to tobacco smoke and aerosols has been shown to impair microcirculatory function, alter immune responses, and disrupt normal wound healing, thereby accelerating periodontal breakdown. Additionally, evidence indicates that individuals exposed to tobacco, whether through active smoking, vaping, or environmental (secondhand) exposure, are at increased risk for periodontitis compared to those with no exposure [11-13].

The risk of periodontal disease from smoking is not unique to cigarette smoking. Public awareness of the harms of cigarette smoking has further contributed to the adoption of alternative nicotine delivery devices, particularly beginning in the mid-2000s. Electronic Nicotine Delivery Systems (ENDS), also known as electronic cigarettes (e-cigarettes), were introduced into the United States market in 2007 and have since experienced substantial growth in popularity [14]. These products were developed and marketed as potentially safer alternatives to traditional cigarette smoking and as tools for smoking cessation, in response to increasing evidence of the cancer risk and other health complications associated with conventional tobacco use [15, 16]. In recent years, the prevalence of e-cigarette use has risen notably among young adults, current and former smokers, and individuals of lower socioeconomic status [17]. One study estimated that approximately 600,000 Americans under 21 years of age used JUUL, a brand of electronic cigarette, daily in 2019 [18]. And in 2021, individuals aged 18 to 24 years demonstrated a consistently high prevalence of e-cigarette use, with more than 18.6% reporting current use and over 9.0% reporting daily use [19]. Despite their widespread adoption, the latest guidance from the Centers for Disease Control and Prevention (CDC) does not support e-cigarettes as approved smoking cessation aids and emphasizes that more definitive evidence is needed to determine their effectiveness in promoting long-term cessation [20]. For the purposes of this study, electronic cigarettes (e-cigarettes) and vapes are collectively referred to as e-cigarettes. The increased use of e-cigarette products has brought a new public health concern, with emerging evidence indicating that their use can contribute to increased risk of periodontal disease [21-23]. Recent systematic reviews and meta-analyses have further demonstrated that e-cigarette users exhibit greater risk of periodontal disease compared to non-smokers, although with generally less severe outcomes than conventional cigarette smokers [24, 25].

The association between conventional cigarette smoking and periodontitis is well established and has been demonstrated in prior NHANES-based investigations; using NHANES III data, Tomar and Asma estimated that current smoking accounted for 41.9% of periodontitis cases among U.S. adults [26]. Secondhand smoke exposure and periodontal disease have similarly been examined using national survey data, including a NHANES III analysis by Arbes et al. reporting 60% higher odds of periodontitis among never-smokers exposed to environmental tobacco smoke [27]. However, evidence regarding e-cigarette use and periodontal health remains comparatively limited and inconsistent [28]. Analyses of the Population Assessment of Tobacco and Health (PATH) study have examined self-reported gum disease in relation to tobacco-use patterns and electronic nicotine product use [28, 29]. Additionally, mechanistic reviews have shown biological pathways by which e-cigarette aerosol exposure may affect periodontal tissues [30]. There are few studies that have evaluated multiple forms of tobacco exposure, including conventional smoking, e-cigarette use, dual use, and secondhand smoke exposure, within a single analytic framework using clinically assessed, AAP-classified periodontal status. The purpose of this study is to evaluate whether active smoking, passive smoking, e-cigarette use, and combined exposures are associated with greater severity of periodontitis. We hypothesize that individuals with any of these exposures exhibited significantly more severe periodontal disease compared with those unexposed. To test this hypothesis, we analyzed data from the 2013–2014 National Health and Nutrition Examination Survey (NHANES) to assess the prevalence and severity of periodontitis across exposure groups.

2. MATERIALS AND METHODS

3. RESULTS

A total of 3,618 individuals were initially included in the study. The mean age of study participants was 51.9 years, and 48.4% of the sample were male. As shown in Table 1, 53.5% of individuals were never smokers, and 0.7% were current e-cigarette-only smokers (Table 1).

For regression analyses, 6 individuals were excluded due to missing data on model covariates, resulting in a final analytic sample of 3,612 participants. Multivariable ordinal logistic regression was used to estimate the odds of being in a more severe stage of periodontitis for each smoking exposure group, adjusting for age, gender, diabetes status, socioeconomic status, race/ethnicity, and education level.

Compared to never smokers, current tobacco-only smokers had significantly higher odds of more severe periodontitis (odds ratio [OR], 2.95; 95% confidence interval [CI], [2.45-3.57]; P<0.001). Past tobacco smokers also had higher odds of more severe periodontitis compared to never smokers (OR, 1.27; 95% CI, [1.08-1.50]; P=0.003). Individuals exposed to secondhand smoke had significantly higher odds of more severe periodontitis compared with never smokers (OR, 1.54; 95% CI, [1.04-2.27]; P=0.028). Current e-cigarette-only users had significantly higher odds of more severe periodontitis compared to never smokers (OR, 2.70; 95% CI [1.25-5.80]; P=0.011), as did dual users of tobacco and e-cigarettes (OR, 2.51; 95% CI [1.25-5.04]; P=0.010) (Table 2).

Diabetes status was independently associated with periodontitis severity. Participants with diabetes had 1.51 times higher odds of more severe staging compared to those without diabetes (P<0.001), after adjusting for smoking status, age, gender, SES, race/ethnicity, and education level (Table 2). No significant difference in periodontitis severity was observed between individuals without diabetes and those with borderline diabetes.

Socioeconomic status was also associated with periodontitis severity. Participants with Poverty-Income Ratio (PIR) between >1 and <4 had lower odds of more severe periodontitis compared to those with PIR≤1 (OR, 0.66; 95% CI [0.55-0.79]; P<0.001), and participants with PIR≥4 had significantly lower odds compared with those with PIR≤1 (OR, 0.41; 95% CI [0.33-0.50]; P<0.001).

A chi-square test indicated that binary serum cotinine levels (≥3 ng/mL vs. <3 ng/mL) were significantly associated with smoking status (P<0.001). Median serum cotinine levels differed significantly between most smoking status groups based on Kruskal-Wallis tests and Dunn’s post hoc comparisons with Bonferroni correction, except for comparisons between current tobacco only, current e-cigarette only, and dual-users, which were not statistically significant (P>0.999).

Serum cotinine data were available for 3,492 of the 3,618 individuals and are presented descriptively in Table 3. The highest percentages of individuals with serum cotinine ≥3 ng/mL were observed among current tobacco and e-cigarette smokers (100.0%), current tobacco-only smokers (96.6%), and current e-cigarette-only smokers (96.2%) (Table 3).

4. DISCUSSION

The purpose of this study was to evaluate whether active conventional smoking, passive smoking, e-cigarette use, and combined exposures were associated with greater severity of periodontitis. It was hypothesized that individuals with any of these exposures would demonstrate significantly more severe periodontitis compared to those with no exposure. We addressed this hypothesis by analyzing data from the 2013-2014 National Health and Nutrition Examination Survey (NHANES) to compare the prevalence and severity of periodontitis across exposure groups. The findings support the hypothesis that individuals with any of these exposures demonstrate significantly greater odds of more severe periodontitis compared to never smokers. All five exposure groups demonstrated statistically significant associations with greater periodontitis severity, with current tobacco-only smokers showing the highest odds (OR 2.95), followed by e-cigarette-only users (OR 2.70) and dual users (OR 2.51). These results cannot establish causation given the cross-sectional design; however, they provide evidence that both direct and indirect tobacco exposure patterns are associated with adverse periodontal outcomes across multiple exposure types.

The present findings demonstrate that both e-cigarette-only users and dual users had significantly greater odds of more severe periodontitis compared to never smokers, highlighting the growing public health concern of e-cigarette use and its association with periodontal disease. Although e-cigarettes are often marketed as a safer alternative to conventional smoking, studies show that they produce similar harmful effects on oxidative stress markers and inflammatory cytokines [32].

Mechanistically, tobacco smoke and e-cigarette aerosol exposure have each been shown to impair periodontal tissue homeostasis through related but distinct pathways. Conventional cigarette smoke contains thousands of chemical constituents, including nicotine and carbon monoxide, that impair gingival microvascular blood flow and reduce neutrophil chemotaxis and phagocytic function, blunting the local immune response to periodontal pathogens. E-cigarette aerosol, although free of combustion byproducts, still delivers nicotine and contains reactive carbonyl compounds and ultrafine particulates that have been shown to increase oxidative stress and pro-inflammatory cytokine release in gingival epithelial and fibroblast cell lines, and to alter the oral microbiome toward a more dysbiotic, pathogen-favoring profile [33]. These pathways provide biological plausibility for the associations observed in the present study, although direct evidence in human periodontal tissue, particularly for e-cigarette aerosol, remains more limited than for conventional smoke [30, 34].

One study that analyzed data from the 2016 Behavioral Risk Factor Surveillance System found that poor oral health was more prevalent than good oral health among both daily e-cigarette users and intermittent e-cigarette users [35]. Another study using data from the Korean NHANES between 2013-2015 found that e-cigarettes and conventional tobacco smoking were each significantly associated with increased periodontal disease rates [36]. A systematic review that pooled 13 studies found that clinical attachment loss was higher in e-cigarette users compared to non-smokers and former smokers, but higher in smokers compared to e-cigarette users [34]. While e-cigarette use has been found to adversely affect periodontal health and increase the severity of periodontitis, it is also important to recognize that in many cases individuals who are smoking e-cigarettes are also traditional tobacco smokers. A study by AlQobaly et al. analyzed NHANES data from 2015-2018 that included self-reported periodontal status rather than diagnosis from a dental professional, and initially found that e-cigarette use was associated with self-reported periodontal disease. After further analyses, the authors found that although e-cigarette use was associated with periodontitis, the association was significant only among current smokers [37]. Similarly, a clinical study examining response to non-surgical periodontal therapy found that e-cigarette users showed impaired treatment response compared to non-smokers, further supporting an adverse periodontal effect of e-cigarette use [38]. This pattern is broadly consistent with the present findings, in which all active tobacco exposure groups, including e-cigarette-only users and dual users, demonstrated significantly greater odds of periodontitis severity compared to never smokers, while the magnitude of association was greatest for current tobacco-only smokers. This finding indicates that detailed analysis in further studies can aid in determining the exact adverse effects of e-cigarette-only use on periodontal health versus the effects on periodontal health of dual users.

In contrast to the comparatively limited and mixed evidence on e-cigarette use, the association between secondhand smoke exposure and periodontal disease risk is more consistently established. A cross-sectional study conducted by Liu et al. using NHANES data from 2009-2014 found that individuals with tobacco smoke exposure compared to participants without tobacco smoke exposure had increased odds of having periodontitis [11]. In another study that used NHANES data from the 2009-2012 examination cycle, the authors found that there was a 28% increase in the odds of having periodontitis for individuals exposed to secondhand smoke compared to those who were not [13]. These findings further demonstrate the detrimental impact of environmental smoke exposure on individuals who do not smoke. This highlights the continued importance of addressing secondhand smoke as a significant public health concern and the need for ongoing preventive and educational initiatives. Approximately one-quarter of non-smokers in our present study demonstrated elevated serum cotinine levels, showing that exposure to secondhand smoke remains a prevalent and concerning issue.

5. STUDY LIMITATIONS

The present study has several limitations that should be noted. The cross-sectional design reduces confidence in causal associations, and survey-weighted analyses were not conducted. As a result, the reported odds ratios and confidence intervals describe associations within the analytic sample and should not be interpreted as nationally representative estimates of the U.S. population. Smoking behavior and type were self-reported, introducing potential reporting bias due to reliance on participant answers and honesty. Furthermore, many current e-cigarette users may have been former conventional cigarette smokers, which could introduce exposure misclassification and confound the observed associations. The number of participants who reported exclusive e-cigarette use and dual use was relatively small, which may limit the precision of effect estimates for these subgroups despite reaching statistical significance in the current analysis. These exposure groups represent emerging populations of considerable public health interest, and future studies with larger samples would allow for more precise estimation of these associations. Additionally, some potential periodontal risk factors were not incorporated into the regression model. Although the models adjusted for key confounders, residual confounding from unmeasured or unmodeled factors cannot be excluded. The 2013-2014 NHANES cycle was the most recent dataset containing e-cigarette use information and therefore may not fully capture the rapid increase in e-cigarette use in more recent years.

Although the number of e-cigarette–only users in the sample was limited, future studies using more current samples and a larger number of e-cigarette-only users could allow for weighted analyses and more definitive conclusions. Despite these limitations, collecting and analyzing data on e-cigarette use and secondhand smoke exposure remains critical for understanding their impact on periodontal health and for informing public health initiatives.

CONCLUSION

All tobacco exposure groups, including conventional smokers, e-cigarette-only users, dual users, past smokers, and individuals exposed to secondhand smoke, were significantly associated with increased odds of more severe periodontal disease. These findings highlight the importance of raising public health awareness about the oral health risks of tobacco use in all forms, including e-cigarettes and secondhand smoke exposure.

REFERENCES