Introduction

Periodontitis is one of the most frequent chronic conditions in human adults, affecting more than 42% of US adults 30 years of age or older [1]. It is a leading cause of tooth loss among adults and has been reported to have a harmful impact on general health and wellbeing [2–7]; periodontitis has been associated with diabetes, cardiovascular disease and adverse pregnancy outcomes [3–7]. It is a multifactorial disease that entails complex infectious and immunological interactions [8]. Although bacterial plaque biofilm is an essential factor in development of periodontitis, it is insufficient by itself to initiate the disease process. The interplay between the host response and the periodontopathic bacteria is the key to initiation and progression of periodontal inflammation. In a susceptible host, repeated bacterial insult results in dysregulation of the inflammatory and immune pathways leading to persistent inflammation and tissue destruction of the connective attachment, periodontal ligament and alveolar bone [9]. Several environmental and systemic factors such as smoking, diabetes, stress and obesity have been linked to increased susceptibility to periodontitis [10].

Sleep is a natural physiologic process that has restorative and regulatory functions [11]. Sleep duration was found to have a U-shaped relationship with health outcomes. Sleep deficiency is frequently defined as having less than 6 or 7 hours of sleep, while sleep excess is defined as more than 8 or 9 hours [12]. Both deficient and excessive sleep durations are associated with poorer general health. Increased risk for all-cause mortality, diabetes, obesity, and coronary heart disease have been linked to both short and long sleep durations [12–16]. Sleep deprivation was also shown to impair function of the immune system, and could leads to metabolic and endocrine changes that mimic some of the hallmarks of ageing and obesity, which might explain the increase in the severity of age-related pathologies such as diabetes and hypertension [17–19]. Although insufficient nocturnal sleep has been reported to have a harmful impact on several body organs and systems, more than 30% of the American adults sleep less than the recommended 7 hours a night [20].

A few recent studies had investigated the association between sleep duration and periodontitis with conflicting results, reporting negative, positive and no associations between sleep duration and periodontitis [21–25]. These studies had major shortcomings in the classification of the exposure and/or the outcome. A number of them failed to appreciate the widely recognized non-linear (or U-shaped) relationship between sleep and health outcomes [12–16].The purpose of this investigation therefore was to determine if there is a relation between sleep duration and periodontitis in a large nationally representative US sample.

Methods

Results

The final analysis included 10,291 individuals, among whom 5,244 were periodontitis patients. Table 1 shows characteristics of the study population by categories of sleep duration. Most of the study participants were either in the sleep adequate or sleep deficient categories. The number of women who reported sleeping more than 8 hours was slightly higher than men. Most of the less than 7 hours group were in the 35–49 y age range, while most of the more than 8 hours category were older. More proportion of non-Hispanic Black participants tended to report sleep deficiency, while most of the non-Hispanic White where either in the sleep adequate or excessive categories. Most of the current smokers reported less than 7 hours of sleep. The proportion of diabetics in the excessive sleep group was somewhat higher. Higher proportion of obese were sleep deficient. Most of participants who reported 7–8 hours were in the higher socioeconomic level. Table 2 compared those with periodontitis to those with no periodontitis. About 42% of the study population had periodontitis. Periodontitis was higher among males, Mexican-American and non-Hispanic Black participants. Older individuals were more likely to have periodontitis. Never smokers were the least likely to have periodontitis, followed by former smokers; Current smokers had the highest risk. Diabetes and obesity were associated with a higher prevalence of periodontitis. Higher socioeconomic status and educational attainment were inversely associated with periodontitis. The average hours of sleep was marginally lower among participants with periodontal disease.

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Table 1. Characteristics of the study population by sleep duration groups.

https://doi.org/10.1371/journal.pone.0234487.t001

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Table 2. Characteristics of the study population by periodontal disease diagnosis.

https://doi.org/10.1371/journal.pone.0234487.t002

In the crude model, those who slept less than 7 hours had a statistically significant 36% higher risk of periodontitis (OR: 1.36, 95% CI: 1.23–1.50) when compared to the 7–8 hours reference group, while the odds of periodontitis for participants who slept more than 8 hours were 40% higher than the reference group (OR: 1.40, 95% CI: 1.16–1.71) (Table 3). The association was slightly attenuated in the age adjusted model. In the fully adjusted model, the odds of periodontitis among the sleep-deficient population were 19% significantly higher than the sleep-adequate participants (OR: 1.19, 95% CI: 1.06–1.38). The association among the sleep-excessive population was also attenuated and became statistically non-significant (OR: 1.16, 95% CI: 0.94–1.43).

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Table 3. Odd ratios and 95% CI relating duration of sleep to periodontitis.

https://doi.org/10.1371/journal.pone.0234487.t003

Discussion

The results of the present investigation showed that short sleep duration of 6 hours or less compared to sleeping the recommended 7–8 hours a night was associated with 19% increase in prevalence of periodontitis. These results are consistent with recent findings in a Turkish population in which sleep duration was found to be associated with the stage and grade of periodontitis [22]. It also supports the findings of a study that used the Taiwan National Health Insurance database and found a 36% increase in the probability of developing periodontitis among the study sample [25]. Our results are also in line with an animal study that found an increase of gingival inflammation and alveolar bone loss in sleep deprived rats. In contrast, our findings differ from results of a recent analysis by Romandini et al in which participants who slept 5 hours or less were less likely to have periodontitis [24]. The Romandini et al study used the community periodontal index (CPI) for periodontal assessment which has major limitations as it depends on few index teeth which might underestimate the prevalence of periodontitis. Furthermore, in that study, sleep duration was classified into 5 categories with the “less than 5 hours” as the reference category. This contrasts the majority of human sleep studies in which 7–8 hours, as was done in our study, were considered to be the adequate sleep duration. Lastly, the populations of the two studies are different which could explain in part the dissimilar findings.

Our findings also differ from a study by Wiener in which no significant association between sleep duration and periodontitis was found [23]. The sleep duration in Weiner’s study was dichotomized into less than 7 hours, and 7 hours or more which combine those with adequate (7–8 hours a night) and long (> 8 hour a night) sleep duration into a single category. This method of categorization fails to appreciate the U-shaped relationship between sleep and periodontitis. Long sleep duration of 9 hours or more has been shown, in several epidemiological studies to be related to an increased morbidity and mortality [32–34]. In addition, it was shown to be associated with a higher periodontitis prevalence among women and fewer remaining teeth among elderly [35, 36]. As long sleep duration might have harmful effect, combining adequate and long sleeper into a single category would probably dilute any significant results, which would explain the inconsistency in the results between the present study and Weiner’s results.

There are several plausible mechanisms to explain the observed association between short sleep duration and higher prevalence of periodontitis. Sleep is known to affect the immune system function; hence insufficient sleep could have altered the balance between the immune system and the periodontal microflora. Sleep deprivation has been linked to elevated level of pro-inflammatory cytokines that are important in regulating the inflammatory cascade such as interleukin-6 (IL-6), C-reactive protein (CRP), and tumor necrosis factor-alpha (TNF-⍺) [37–39]. Pink et al prospectively investigated the association between systemic inflammation, using fibrinogen and white blood cell counts, and periodontal disease [40]. They found systemic inflammation to be a significant predictor of periodontal tissue loss [40]; thus activation of pro-inflammatory pathways is a possible mechanism by which short sleep duration could affect periodontitis. In addition, sleep is linked to psychosocial stress and obesity which have been shown to be associated with higher periodontitis prevalence [41–43]. Since the present study was cross sectional, it could also be possible that insufficient sleep is a consequence rather than a cause of periodontitis or that the reported association between the two conditions is coincidental.

The present study has several strengths including the large representative sample size, the sophisticated sampling methods and application of the full-mouth clinical periodontal examinations protocol. Our study however has some limitations. Although research has shown that self-reported sleep duration has acceptable validity [28–30], bias due to measurement error cannot be ruled out. In addition, due to the observational nature of the study, the likelihood of confounding cannot be excluded. However, we adjusted for the established risk factors of periodontal disease which should mitigate any bias due to confounding. The cross-sectional design of our study is another limitation; Longitudinal cohort studies are warranted to confirm the findings of the present analysis, and to explore the potential causality.

In conclusion, findings of the present study showed an association between short sleep duration and higher prevalence of periodontitis in a nationally representative United States population. If these results were confirmed in longitudinal prospective studies, this might have significant health implications considering the high prevalence of periodontitis and increased number of individuals who sleep less than 7 hours, in the contemporary society.

Supporting information