The antioxidant system of periodontal tissue is unbalanced in periodontitis, and appropriate supplementation of antioxidants can effectively prevent or alleviate periodontal tissue damage. However, a dearth of research exists on the association between dietary antioxidant intake and the prevalence of periodontitis.

Six dietary antioxidants (vitamins A, C, and E, zinc, selenium, and carotenoids) were extracted from two 24-h recall interviews utilizing data from the National Health and Nutrition Examination Survey (NHANES) conducted between 2009 and 2014. The composite dietary antioxidant index (CDAI) made calculations using data on the intake of these six dietary antioxidants. Periodontitis severity was categorized into mild, moderate, and severe classifications based on established consensus criteria. Additionally, a restricted cubic spline (RCS) regression model was applied to evaluate the potential non-linear dose–response relationship between CDAI and periodontitis prevalence.

A total of 9,378 adults were included in this analysis, of which 4,755 had periodontitis. Individuals within the highest CDAI quartile demonstrated a diminished prevalence of total periodontitis compared to those in the lowest quartile (OR = 0.70 [0.53–0.93], P_trend = 0.012). When moderate/severe periodontitis served as the outcome variable, those within the fourth CDAI quartile exhibited a 32% reduced prevalence compared to those in the first quartile (OR = 0.68 [0.52–0.88], P_trend = 0.006). RCS regression showed that CDAI was linearly and negatively related to the prevalence of periodontitis (both total and moderate/severe periodontitis). In subgroup analysis by gender, a significant association between CDAI and total periodontitis was discerned solely among females (OR = 0.60 [0.42–0.85], P_interaction = 0.015).

Elevated dietary antioxidant intake is associated with a diminished prevalence of periodontitis. These findings underscore the potential role of antioxidants in periodontal health.

Periodontitis is a chronic and heterogeneous inflammatory condition characterized by progressive degradation of the tooth support apparatus, encompassing the periodontal membrane and alveolar bone [1, 2]. With a global prevalence exceeding 40%, severe periodontitis affects approximately 11% of the population, making it a prevalent and challenging oral health concern [3, 4]. Recognized as a primary cause of tooth loss, periodontitis not only compromises masticatory function and quality of life [5], but also demonstrates associations with various systemic conditions such as cardiovascular disease, chronic kidney disease, and Parkinson's disease [6,7,8]. Presently, the principal objective of periodontitis management is disease prevention, involving interventions such as mechanical debridement, antibiotic therapy, anti-inflammatory medications, and surgical approaches [9,10,11]. However, due to the persistent challenges in eradicating local infection and inflammation, restoration of the periodontal tissue structure remains a formidable task [12].

In recent years, the relationship between diet and periodontitis has garnered increasing attention, with evidence suggesting a role for diet in disease progression [13]. A cross-sectional study revealed a positive correlation between the pro-inflammatory component of the diet and the likelihood of developing periodontitis [14]. In a controlled trial, individuals adopting a diet rich in omega-3 fatty acids, vitamins C and D, antioxidants, and fiber demonstrated a significantly reduced incidence of periodontal disease [15]. Notably, Nishida et al. identified a connection between decreased dietary vitamin C intake and an elevated risk of periodontal disease within the general population [16]. Additionally, Wright et al. observed that a diet enriched with salads, fruits, and vegetables was associated with lower levels of clinical attachment loss (CAL) [17]. Considering the protective role of antioxidants against free radicals, it has been hypothesized that enhancing antioxidant intake through diet may mitigate the risk of developing periodontitis [18].

The Composite Dietary Antioxidant Index (CDAI) serves as a comprehensive measure assessing the body's antioxidant capacity, considering the quantities and proportions of various antioxidants in the diet [19]. The index predominantly incorporates the intake of six dietary antioxidants, including zinc, selenium, carotenoids, vitamin A, vitamin C, and vitamin E [20]. CDAI scores, expressed numerically, reflect the body's antioxidant capacity through dietary intake, with higher scores indicative of greater antioxidant potential. Previous research has demonstrated associations between CDAI and the occurrence of various chronic diseases. Wu et al. established a negative association between CDAI and hypertension in adults [21], while Zhao et al. revealed that each unit increase in CDAI reduced the incidence of depression by 30% [22]. Consequently, CDAI emerges as a valuable indicator for studying the relationship between antioxidants and health, serving as a pivotal reference for researchers. Therefore, this study aims to elucidate the relationship between CDAI and periodontitis, with the objective of enhancing our comprehension of the role of diet in periodontitis development and potentially identifying targeted dietary interventions for individuals at risk of periodontitis.

The National Health and Nutrition Examination Survey (NHANES) is a comprehensive research program in the United States designed to evaluate the health and nutritional status of both adults and children [23]. Initiated in the early 1960 s, the NHANES Program originally comprised a series of surveys targeting diverse population groups and health themes. Since 1999, the program has consistently assessed the health status of the U.S. population. Each survey involves approximately 10,000 participants in the United States who undergo home interviews, subsequent physical examinations, and laboratory assessments at the Mobile Examination Center (MEC). Ethical approval for NHANES research protocols was obtained from the National Center for Health Statistics (NCHS) Research Ethics Review Board, and all participants provided signed informed consent.

A total of 30,468 individuals participated in NHANES from 2009 to 2014. We excluded participants ineligible for oral examination (age < 30 years, n = 16,397) and those with incomplete periodontal data (n = 3,357). Additionally, 618 participants without data for calculating the Composite Dietary Antioxidant Index (CDAI), 62 pregnant participants, 107 individuals with extreme energy intakes, and 107 participants displaying outliers in the CDAI were excluded. Ultimately, our analytical cohort comprised 9,378 participants (Figure S1).

The CDAI was computed based on the intake data of six dietary antioxidants, namely vitamins A, C, and E, zinc, selenium, and carotenoids, following previously published methodology [19]. For each antioxidant, the daily intake was standardized using the z-score method:

where X_i represents the individual intake of the i-th antioxidant, and μ_i and σ_i denote the mean and standard deviation of intake in the study population, respectively. The CDAI was then calculated as the sum of the z-scores of these six antioxidants:

Higher CDAI scores indicate a diet richer in antioxidant micronutrients. Dietary intake data were collected using two non-consecutive 24-h dietary recall interviews, conducted in person at the mobile examination centers (MECs) and by telephone follow-up, as part of the NHANES dietary assessment. Detailed information on NHANES dietary methods is available from the official NHANES website: https://wwwn.cdc.gov/nchs/nhanes/. Nutrient intakes, including vitamins A, C, and E, zinc, selenium, and carotenoids, were calculated based on reported food and beverage consumption using the USDA Food and Nutrient Database for Dietary Studies. The average daily intake of each antioxidant nutrient was derived from the two recalls, and intake from dietary supplements over the past 30 days was also included. To mitigate the impact of aberrant values, participants with abnormal total energy intake (> 4200 or < 800 kcal/day in males; > 3500 or < 500 kcal/day in females) were excluded in this study.

Within the NHANES database, periodontal probing depth (PPD) and CAL were measured at six sites (mesiobuccal, mid-buccal, distobuccal, distolingual, mid-lingual, and mesiolingual) per tooth for each participant, resulting in 12 data points per tooth (6 PPD values and 6 CAL values at different sites). Consequently, a total of 28 teeth were measured for each individual. Periodontitis classification followed the consensus guidelines established by the Centers for Disease Control and Prevention (CDC) and the American Academy of Periodontology for epidemiologic studies [24]. In this study, periodontitis was categorized into mild, moderate, and severe forms according to the criteria outlined in a prior investigation [25]. Total periodontitis was defined as the cumulative presence of mild, moderate, and severe periodontitis.

Information on covariates, including age, sex, race, education level, and total energy intake, was collected through standardized, interviewer-administered questionnaires conducted by trained interviewers at the MECs. The poverty income ratio (PIR) was computed by dividing household income by factors specific to household size and composition, subsequently categorized into three groups (≤ 1.0, 1.1–3.0, or > 3.0) [26]. Smoking status was delineated as never smokers (< 100 cigarettes), current smokers (> 100 cigarettes), and former smokers (> 100 cigarettes and cessation of smoking) [27]. Drinking status was categorized as nondrinker, low-to-moderate drinker, or heavy drinker (male: ≥ 2 drinks/day; female: ≥ 1 drinks/day) [27]. Physical activity levels were classified as inactive (no leisure-time physical activity), insufficiently active (moderate activity 1–5 times per week with metabolic equivalents [MET] 3–6 or vigorous activity 1–3 times per week with MET > 6), and active (individuals engaging in more moderate or vigorous activity than described above) [27, 28]. The body-mass index (BMI) was calculated as the weight in kilograms divided by the square of the height in meters, serving as a measure that reflects body density. Participants were categorized as underweight or normal weight (BMI < 25.0 kg/m²), overweight (BMI 25.0–29.9 kg/m²), and obese (BMI ≥ 30.0 kg/m²). Self-reported questionnaires were employed to collect information on the prevalence of hypertension, diabetes, cardiovascular disease (CVD), and cancer.

Appropriate sample weights were applied to all data analyses to account for the complex, multistage sampling design of NHANES and to obtain nationally representative estimates. Continuous variables with a normal distribution are presented as means ± standard errors, while continuous data without a normal distribution are expressed as medians [interquartile ranges]. Concentration and distribution analyses were also performed on CDAI and its constituent components. Pair-wise Spearman correlation analysis was employed to determine association coefficients among dietary antioxidant micronutrients. The study population was stratified into quartiles based on CDAI.

Multifactorial logistic regression was utilized to examine the association between CDAI (both continuous and categorical variables) and the prevalence of periodontitis (both total and moderate/severe) within the U.S. population. Potential non-linear associations between CDAI and periodontitis prevalence were explored using a restricted cubic spline (RCS) regression with nodes set at the 10 th, 50 th, and 90 th percentiles. Stratified analyses were employed to investigate the impact of different characteristics on the associations between CDAI and periodontitis prevalence. These characteristics included age categories (continuous), sex (female or male), race (non-Hispanic White or other), family poverty income ratio (PIR) (≤ 1.0, 1.1–3.0, or > 3.0), smoking status (never, former, or current smoker), drinking status (nondrinker, low-to-moderate drinker, or heavy drinker), physical activity levels (inactive, insufficiently active, or active), BMI (< 25.0, 25.0–29.9, or > 29.9 kg/m2), and self-reported conditions including hypertension, diabetes, cardiovascular disease (CVD), and cancer (no or yes). All statistical analyses were conducted using R (version 4.2.0), and P-values less than 0.05 were considered statistically significant.

The analysis included 9,378 participants aged 30 years or older, with 4,755 identified as having periodontitis (Table 1). The weighted mean CDAI level was 0.50. Periodontitis exhibited a higher prevalence in older male participants (P < 0.05). Except for total energy intakes and self-reported cancer (P > 0.05), all baseline variables demonstrated significant differences between individuals with and without periodontitis. Those with periodontitis exhibited lower education levels and household incomes. Moreover, patients with periodontitis were more likely to be current smokers, heavy drinkers, participants with obesity, and physically inactive (P < 0.01). The prevalence of hypertension, diabetes, and CVD was notably higher in participants with periodontitis (P < 0.01). Classification based on CDAI level revealed significant associations with age, gender, race, education level, PIR, smoking status, drinking status, self-reported hypertension, and CVD (P < 0.01) (Table S2). Subjects adhering to the antioxidant-rich diet (fourth group) tended to be younger and potentially had higher levels of education, non-smoking, and low-to-moderate alcohol consumption, among other factors (P < 0.01). Additionally, those with the highest CDAI demonstrated a lower prevalence of periodontitis, hypertension, and CVD compared to those with the lowest CDAI (P < 0.01).

Figure S2 illustrates the distribution of data before and after the removal of CDAI outliers. Following the exclusion of outliers, the distribution of CDAI approximated normality. Table S1 presented the distribution and concentration of CDAI and its components among adults with periodontitis. The mean CDAI was 0.22 (−2.20, 2.12). The average daily intake of vitamins A, C, and E, zinc, selenium, and carotenoids in the study population was approximately 576.52 (264.00, 760.25) μg/day, 80.77 (21.70, 111.90) mg/day, 7.83 (4.33, 9.92) mg/day, 10.70 (6.73, 13.32) mg/day, 109.82 (70.90, 138.00) μg/day, and 8748.27 (1934.75, 11,528.50) μg/day, respectively. Figure S3 depicted the Spearman correlation coefficients among dietary antioxidant micronutrients, revealing a robust correlation between zinc and selenium (r = 0.62).

This study employed three models to investigate the relationship between the CDAI and the prevalence of total periodontitis (Table 2). In the crude model, the odds ratios (ORs) for the association between continuous CDAI and the prevalence of total periodontitis was 0.94, indicating a decrease in total periodontitis prevalence with each unit increase in CDAI. This association persisted in both model 1 (OR = 0.94 [0.92–0.96], P < 0.001) and model 2 (OR = 0.96 [0.93–0.99], P = 0.007). Within the total population, the ORs for the prevalence of total periodontitis in subjects belonging to the second, third, and fourth CDAI quartiles were 0.80, 0.66, and 0.57, respectively (P_trend < 0.001), when compared to the lowest CDAI group. Notably, compared to the first quartile, the fourth quartile of CDAI exhibited a negative association with the prevalence of total periodontitis (OR = 0.56 [0.45–0.70], P_trend < 0.001) after adjusting age, sex, and race. After adjusting for all variables, individuals in the fourth quartile of CDAI demonstrated a 30% lower prevalence of total periodontitis than those in the first quartile (OR = 0.70 [0.53–0.93], P_trend = 0.012). Moreover, a negative and linear association between CDAI and the prevalence of total periodontitis was observed (P for nonlinearity = 0.269) (Fig. 1A). Regarding individual nutrients, increased dietary intake of vitamin A, vitamin E, and carotenoids were independently associated with a decreased prevalence of total periodontitis after multivariate adjustment (P_trend < 0.001) (Table S3).

The exposure–response association of the composite dietary antioxidant index (CDAI) with the prevalence of periodontitis by restricted cubic spline (RCS). A Total periodontitis. B Moderate/severe periodontitis. Analyses were adjusted for covariates age (continuous), sex (male or female), race (Mexican American, Other Hispanic, Non-Hispanic White, Non-Hispanic Black or Other), education level (below high school, high school, or above high school), family income-to-poverty ratio (≤ 1.0, 1.1–3.0, or > 3.0), smoking status (never smoker, former smoker, or current smoker), drinking status (nondrinker, low-to-moderate drinker, or heavy drinker), BMI (< 25.0, 25.0–29.9, or > 29.9), energy intake levels (in quartiles), physical activity (inactive, insufficiently active, or active), diabetes (yes or no), hypertension (yes or no), CVD (yes or no), and cancer (yes or no)

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Similar to the investigation into total periodontitis, this study employed three models to explore the association between the CDAI and the prevalence of moderate/severe periodontitis (Table 3). In the crude model, the ORs between CDAI and moderate/severe periodontitis was 0.94, signifying a consistent pattern. This association persevered in both model 1 (OR = 0.94 [0.92–0.96], P < 0.001) and model 2 (OR = 0.96 [0.93–0.98], P = 0.003). Individuals in the second, third, and fourth quartiles of CDAI exhibited ORs of 0.97, 0.66, and 0.56, respectively, in comparison to the lowest CDAI group (P_trend < 0.001). Noteworthy is the negative association of the fourth quartile of CDAI with the prevalence of moderate/severe periodontitis (OR = 0.56 [0.45–0.69], P_trend < 0.001) after adjusting for age, sex, and race. With comprehensive variable control, individuals in the fourth CDAI quartile displayed a 32% lower prevalence of moderate/severe periodontitis compared to those in the first quartile (OR = 0.68 [0.52–0.88], P_trend = 0.006). Furthermore, an observed negative and linear association between CDAI and the prevalence of moderate/severe periodontitis was evident (P for nonlinearity = 0.139) (Fig. 1B). Regarding individual nutrients, heightened dietary intake of vitamin A, vitamin C, vitamin E, and carotenoids remained independently associated with a decreased prevalence of moderate/severe periodontitis after meticulous multivariate adjustment (P_trend < 0.001) (Table S4).

To discern potential effect modifiers and enhance the depth of our investigation, we conducted a stratified analysis, systematically evaluating the study population across various subgroups based on key demographic and health-related factors (Table 4). In our comprehensive analyses, gender emerged as a notable factor significantly influencing the relationship between CDAI and the prevalence of total periodontitis (OR = 0.60 [0.42–0.85], P_interaction = 0.015). This observation underscores the importance of considering gender-specific nuances when interpreting the impact of dietary antioxidant intake on periodontal health. Intriguingly, in the remaining subgroups, we did not identify any factors that exerted a significant influence on the observed results, suggesting the robustness and consistency of the overall findings across diverse demographic and health-related strata.

Our investigation involved 9,378 participants, including 4,755 diagnosed with periodontitis. The primary findings of our study revealed a significant and consistent negative correlation between the CDAI and the prevalence of both total and moderate/severe periodontitis. Notably, individuals in the fourth quartile of CDAI demonstrated a substantial 30% lower prevalence of total periodontitis compared to those in the first quartile. This association held even more robustly when considering moderate/severe periodontitis as the outcome variable. Furthermore, gender emerged as a noteworthy moderator, influencing the relationship between CDAI and total periodontitis prevalence in subgroup analyses.

The CDAI, a quantitative measure of dietary antioxidants, plays a pivotal role in chronic disease recurrence, emphasizing the crucial balance of antioxidants in the diet [29]. A high CDAI score indicates a diet rich in antioxidants such as vitamins A, C, E, and carotenoids, which contribute to scavenging free radicals, protecting cellular structures, and preserving DNA integrity [30]. Elevated CDAI levels are consistently associated with a lower risk of chronic diseases in healthy populations, preventing conditions such as cardiovascular disease, diabetic nephropathy, and specific malignancies [21, 31, 32]. However, individuals with chronic diseases may exhibit decreased CDAI, suggesting an already antioxidant-rich diet [33]. In this case, improving antioxidant balance through dietary modification or antioxidant supplementation could aid in managing chronic disease symptoms and complications [34]. Our findings underscore a negative correlation between antioxidant intake, as indicated by CDAI, and the prevalence of periodontitis. The CDAI, encapsulating vitamins A, C, and E, zinc, selenium, and carotenoid intake, emerges as a potentially valuable biomarker for assessing periodontitis risk. Nevertheless, the intricate relationship between CDAI and periodontitis is multifactorial, influenced by factors such as genetic background, lifestyle, and environmental conditions.

The investigation revealed a significantly enhanced efficacy of basic treatment with topical antioxidants compared to periodontal basic treatment alone, suggesting a promising application of antioxidants in periodontitis therapy [18, 35]. Prior research has established a negative correlation between the prevalence of inflammatory periodontitis and serum antioxidant concentrations [36]. Vitamin A, a fat-soluble micronutrient crucial for maintaining epithelial cell integrity, has been incorporated into periodontal therapy [37]. Vitamin C, a water-soluble antioxidant, exhibits antioxidant, anti-tumorigenic, and immunomodulatory activities [38]. Clinical studies have found a negative link between vitamin C levels and loss of periodontal attachment [39]. Adequate dietary vitamin C intake is imperative for promoting periodontal health in adults [40]. In a rat model, vitamin C supplementation demonstrated the potential to mitigate periodontitis-induced oxidative stress by reducing inflammatory gene transcription [41]. Vitamin C application in periodontitis may also impede alveolar bone resorption and periodontal tissue destruction [38]. Research suggests that vitamin C, functioning as a reducing agent, exerts a protective influence on the periodontal ligament, rendering it an effective remedy for periodontitis [42]. Oral vitamin C therapy has been shown to enhance postoperative healing of dental implants in patients with persistent periodontitis [43]. Vitamin E, characterized by anti-inflammatory properties attributed to its capacity to lower C-reactive protein and inhibit pro-inflammatory cytokine release [44], exhibits diminished levels in periodontally diseased patients compared to healthy subjects [45]. Singh et al. demonstrated that the application of vitamin E after root planing improved periodontal probing depth, clinical attachment levels, and bleeding on probing, concurrently increasing plasma antioxidant levels in patients [46]. Behfarnia et al. provided further evidence by illustrating that vitamin E supplementation reduced inflammation and enhanced periodontal clinical parameters in individuals with periodontitis [47].

Periodontitis is characterized by an imbalance in the generation of reactive oxygen species (ROS) and the antioxidant defense system, leading to oxidative stress [48]. Plaque adhering to the tooth surface harbors various bacterial pathogens capable of activating host macrophages and other inflammatory cells, inducing the production of diverse pro-inflammatory cytokines [49]. These cytokines play a pivotal role as mediators of the inflammatory response, recruiting additional neutrophils to the periodontitis site and promoting the substantial generation of ROS facilitated by the catalytic action of NADPH oxidase [50]. While ROS produced by immune cells typically exhibit antimicrobial properties, an excess of ROS exerts cytotoxic effects, inducing oxidative stress and triggering a cascade of periodontal inflammatory responses [51]. Oxidative stress, through various mechanisms encompassing DNA damage, tissue injury, and immunological activation, significantly contributes to the etiology of periodontitis [52]. Moreover, oxidative stress has been identified to augment the production of virulence factors by periodontal bacteria, thereby contributing to the progression of periodontitis [53]. Previous research has demonstrated that antioxidants can effectively scavenge free radicals, mitigating oxidative stress-induced damage to periodontal tissue cells and subsequently alleviating periodontitis symptoms [54]. In addition to their direct impact, dietary antioxidants have been observed to modulate the immune response by reducing pro-inflammatory cytokines and enhancing anti-inflammatory cytokines, thereby lowering the risk of periodontitis [55]. Furthermore, dietary antioxidants may exert an influence on the composition of the oral microbiota, a crucial factor in the development of periodontitis [56].

The study exhibits several notable strengths. Firstly, the NHANES survey, conducted from 2009 to 2014, provides substantial data on the health status of a representative sample of the US population. This dataset uniquely facilitates the exploration of potential associations between periodontitis, diagnosed through comprehensive oral examinations, and CDAI scores among survey participants. Secondly, the periodontal diagnosis relies on a low-risk whole-mouth examination of each tooth, ensuring a comprehensive assessment. Thirdly, the CDAI introduces a novel approach to evaluating dietary antioxidant intake, encompassing the assessment of six key antioxidants, surpassing the scope of a single indicator.

However, the study is not without limitations. First, its cross-sectional design impedes the establishment of causal relationships, restricting the ability to infer causality between variables. Moreover, the dietary nutrient intakes are derived from the average of two 24-h dietary reviews, potentially failing to capture daily dietary variations accurately. Third, while the CDAI comprehensively evaluates six key antioxidants, its scope may still lack the full spectrum of dietary antioxidants. Future investigations might consider expanding the assessment to include a broader range of antioxidants, accounting for the complex interplay of various micronutrients in the context of periodontal health. Lastly, although the NHANES oral health examinations were performed by trained and licensed dental examiners who underwent standardized training and calibration procedures, detailed information on inter-examiner and intra-examiner reliability is not publicly available. Therefore, the potential for measurement variability among examiners cannot be entirely excluded.

NHANES data described in this manuscript are available at https://wwwn.cdc.gov/nchs/nhanes/.

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Author notes

The authors’ responsibilities were as follows—JX: designed the research, and had primary responsibility for the final content; XC: conducted analyses and wrote the first draft of the paper; RH, and XL: revised the manuscript; and all authors: read and approved the final manuscript and approved the final submitted version.

Correspondence to Jincheng Xu.

All participants provided written informed consent and study procedures were approved by the National Center for Health Statistics Research Ethics Review Board (Protocol Number: Protocol #2005–06 and Protocol #2011–17). The study was conducted in accordance with the ethical principles outlined in the Declaration of Helsinki.

Not applicable.

The authors declare no competing interests.

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