Introduction

Exercise has been shown to have numerous beneficial effects on the general health of human beings and increase life expectancy [1]. Furthermore, studies have indicated the protective effects and improvement of taking moderate exercise on various lifestyle-related diseases including obesity, arthritis, hypertension, depression, and coronary heart disease [2]. Taking regularly moderate exercise can alleviate systemic inflammatory reactions and reduce the risk of multiple traditional chronic diseases [3]. Moreover, regular exercise has a positive impact on the management of stress and anxiety [4]. In addition to these physical and mental benefits, taking exercise may also help reduce healthcare costs and the need for medications through lower hospital stays and physician visits [5].

Periodontal health is defined as a state free from inflammation and characterized by the absence of gingival bleeding and shallow pockets [6]. Periodontitis is a chronic multifactorial inflammatory disease characterized by progressive destruction of the tooth-supporting apparatus and combined with dysbiotic plaque biofilms [7]. This disease is prevalent worldwide, affecting approximately 20–50% of the global population, making it a significant public health concern [8]. Although periodontitis mainly threatens oral health, its association with systemic conditions such as cardiovascular diseases, diabetes, and arthritis has also been established in the literature [9, 10]. However, given the high physical, psychological, social, and economic impacts on individuals and communities, prevention and management of periodontitis are crucial globally. A previous study summarized data related to severe periodontitis and indicated that governments should pay attention to the growing burden of severe periodontitis because of the increasing population associated with a better life expectancy around the world and a reduction of tooth loss [11].

Various lifestyle factors, including diet quality, alcohol consumption, and smoking, have been found to impact the occurrence and severity of periodontitis [8]. Substantial evidence suggests that interventions targeting lifestyle behaviors are effective, underscoring the importance of behavioral support in managing periodontitis [12]. Significant factors such as diet and smoking have been thoroughly investigated regarding their role in the risk of periodontal tissue decay [13, 14]. Nevertheless, there is limited research on the potential role of exercise in preventing periodontitis. Most studies regarded exercise as a part of lifestyle variables when evaluating the risk of periodontitis. However, few researchers investigated the level of exercise in detail, and the intervention studies are also limited in current literature.

Given that exercise has been shown to modulate systemic inflammatory reactions and alter inflammatory markers such as protein C-reactive levels, there may be a potential relationship between exercise and periodontitis [15, 16]. However, it is unclear whether exercise has a direct impact on periodontitis. Previous studies have tried to summarize the potential relationship between exercise and periodontitis [17, 18]. For example, a meta-analysis investigated the influence of physical exercise on periodontitis [17]. Another study also suggested an association between periodontitis and physical activity [18]. However, only 6 studies were included in this previous study [18]. Accordingly, the results should be considered carefully due to the limited research available and the certain risk of bias. Furthermore, only observational researches were included in these previous studies. Thus, the goal of this study was to perform a comprehensive meta-analysis from both observational and intervention studies to investigate the potential relationship between exercise and the prevalence of periodontitis and provide references for future intervention programs aimed at preventing periodontitis.

Materials and methods

The present study was registered at PROSPERO under registration number CRD42023396334 and performed based on the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines [19]. Given that no human or animal subjects were involved in this study, medical ethics committee approval was not required.

The guiding question for this systematic review was formulated using the PICO format, with (P) indicating participants, (I) representing intervention, (C) standing for comparison, and (O) representing outcome [20]. Specifically, the guiding question was, “For individuals of all ages (P), what is the impact of exercise (I) or a sedentary lifestyle (C) on periodontitis (O)?” Participants of all ages were included. The intervention group contained subjects who engaged in regular or recommended exercise. The comparison group consisted of individuals who engaged in inadequate exercise or a sedentary lifestyle. The primary outcomes were the measurements of periodontitis.

Search strategy

To identify relevant publications in accordance with PRISMA guidelines, a systematic literature search was performed in Web of Science, PubMed/MEDLINE, Scopus, and Cochrane Library databases. The search was limited to English-language publications published From January 1993 to January 2023. The search strategy used predefined search terms related to exercise and periodontitis, and the specific search strategies used for each database are provided in Table 1. Gray literature searches were also conducted on the International Clinical Trials Registry Platform of the World Health Organization and SciELO. To complement the study, the search in the databases was combined with a manual retrieval of the reference lists from the selected studies.

Table 1 Electronic databases used and search strategies
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Eligibility criteria

The following criteria were applied to choose publications: (1) peer-reviewed research articles published in English, (2) studies conducted on human subjects with no age restrictions, and (3) observational or experimental studies that examined the relationship between exercise and periodontitis.

The following exclusion criteria were performed: (1) studies conducted on animals, case reports, letters, editorials, conference abstracts, and review articles; (2) studies with insufficient data to extract relevant information including the exercise measurement and evaluation of periodontitis; and (3) publications written in languages other than English.

Study selection

The information obtained by search strategy in each database was collated, and duplicate entries were eliminated. Two reviewers independently assessed the abstract and title of the retrieved articles based on eligibility criteria. Studies which were considered ineligible by both reviewers were promptly excluded, while studies deemed ineligible by one author but eligible by another were retained for full-text evaluation. The reviewers worked in tandem to analyze articles not excluded in their entirety. Publications that satisfied the eligibility criteria were used for further data extraction. Any discrepancies were resolved by means of discussion.

Data from the included studies were retrieved in detail. Report of the following variables was extracted: author(s), year of publication, study type, country, number of participants, gender, age, exercise assessment, evaluation of periodontitis, main findings, and conclusions.

Quality assessment

The risk of bias for observational studies was evaluated in accordance with the “Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies” and the “Quality Assessment of Case-Control Studies” from the National Institutes of Health (Available online at https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools). These tools comprise 14 criteria (12 for case-control studies) designed to appraise the internal validity of cross-sectional studies, case-control studies, and cohort studies. Responses to each criterion could be “yes,” “no,” “not applicable,” or “not reported.” Responses other than “yes” indicate a potential risk of bias. After evaluation, articles were defined as good, fair, or poor. Studies rated as “good” had a maximum of three domains that were not answered as “no” or “not applicable.” The domains of “Validity of outcomes” and “Adjustment for confounders” were considered the most critical factors in determining the classification of poor study quality.

Furthermore, the risk of bias for experimental researches was assessed based on the Cochrane Collaboration’s tool, using Review Manager 5.4 (The Nordic Cochrane Center, The Cochrane Collaboration, Copenhagen, Denmark) [21]. The tool contains the following criteria: allocation concealment, random sequence generation, blinding of outcome assessment, blinding of participants, incomplete outcome data, blinding of operator, and selective reporting. Each study’s risk of bias was classified as low, with some concerns, or high based on these criteria.

The same reviewers independently analyzed the included studies using the above tools. In case of any discrepancies, a consensus decision was made through further discussion with a third review author.

Data synthesis

Data on exercise and periodontitis were extracted and analyzed using Stata 17.0 Software (College Station, TX: StataCorp LLC, USA) to evaluate the underlying relationship between exercise and periodontitis. Specifically, the prevalence of periodontitis and the number of individuals in active and inactive groups were recorded to determine the odds ratio with a 95% confidence interval (95%CI). Heterogeneity was calculated using the I2 test, which measures the rate of variation among articles caused by heterogeneity instead of probabilistic chance. The fixed-effects model and the random-effects model were used to test the significance of treatment effects in case of absence and high heterogeneity, respectively [22]. The estimated effect was regarded as significant where P < 0.05.

Results

Study selection

4,098 papers were initially obtained through an electronic search, comprising 899 articles from PubMed/MEDLINE, 1,324 articles from Scopus, 1,681 articles from Web of Science, and 194 articles from Cochrane Library. Furthermore, a manual search of manufacturers’ reference lists yielded seven additional articles. None of the 243 references from gray literature was considered eligible. 2,995 studies remained after removing duplicates, and 2959 of them were excluded after assessing the titles and abstracts. After thoroughly examining the full texts, 13 studies were excluded since they did not meet the eligibility criteria. At last, 30 articles were selected for inclusion in this systematic review (Fig. 1).

Fig. 1
figure 1

Flow chart of the literature search and results

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Characteristics of the studies

Tables 2, 3 and 4 provide detailed information on the 30 studies included in this review, of which 4 were experimental studies and 26 were observational studies. 20 of the included articles were cross-sectional design and most of them were performed in developed countries. Subjects of all ages were included, with a minimum of 25 and a maximum of 16,726. There was considerable variation in the tools used to assess physical activity, including different versions of questionnaires, strength, and maximal oxygen consumption. 18 studies elaborated on the types of sports, and 14 studies reported the duration time of measurement. The frequency and intensity of exercise have also been included in most selected studies. The assessment of periodontitis included clinical attachment loss and periodontal probing depth in most studies, with additional measures including gingival index, plaque index, bleeding on probing, and community periodontal index. The selected studies also investigated sedentary behavior, diet quality, normal body weight, alcohol consumption, and cigarette smoking as potential co-factors. Overall, from the 30 included studies, 20 studies reported that taking exercise was combined with a low prevalence of periodontitis, while the remaining 10 studies did not reach conclusive findings. For example, a representative cross-sectional study indicated that a higher prevalence of periodontitis was found in those inactive individuals compared to partially active individuals and subjects took recommended exercise [25]. A low level of exercise combined with a poor diet demonstrated a significant association with increased odds of periodontitis in another included study [27]. Possible explanations can be obtained from the included intervention studies. One research concluded that taking exercise may alter total salivary antioxidants activity, which could eventually affect periodontal health status [44]. Another study indicated that leisure-time exercise may protect against an excessive inflammatory response in periodontitis [46]. In addition, none of the selected studies reported a negative effect. Other main potential co-factors reported in the selected studies include maintaining a normal weight, consuming a healthy diet, sedentary behavior, and cigarette smoking.

Table 2 Characteristics of the included studies
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Table 3 Details of exercise in the included studies
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Table 4 Main findings of the included studies
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Risk of bias

Table 5 presents a summary of the quality assessment of observational studies. Three publications were considered to be of good quality with low risk, providing adequate information about the population and objectives of the study, and how the outcomes and exposures were measured. 18 studies were rated as fair, while four publications were rated as poor. In terms of the experimental studies, two studies showed a high risk of random sequence generation since subjects were not randomly assigned to the experimental and control groups. Most studies also exhibited a high risk of bias in blinding of participants because participants were aware of their grouping under different intervention conditions. See Fig. 2 for a graphical representation of the risk of bias assessment.

Fig. 2
figure 2

Risk of bias of experimental studies using Cochrane Collaboration’s tool

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Table 5 Quality assessment of included observational studies
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Meta-analysis

Among 30 selected articles, 16 were included in the meta-analysis, while 14 publications were excluded due to variability in study outcomes and methodologies. The results presented high heterogeneity (I2 = 88) with statistical significance. Since the selected studies were not functionally equivalent, Random-effects models were used to generalize the results from meta-analysis. The prevalence of periodontitis was 27.85% in the active group and 33.88% in the inactive group, respectively. The Forest plot demonstrated a risk ratio of 0.84 (95%CI: 0.77, 0.91) between the active group and the inactive group (P < 0.01), which indicated a positive association between exercise and periodontitis (Fig. 3). The funnel plot did not reveal any publication bias (Fig. 4).

Fig. 3
figure 3

Forest plot of the relationship between exercise and prevalence of periodontitis

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Fig. 4
figure 4

Funnel plot of the relationship between exercise and prevalence of periodontitis

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Discussion

Regular exercise is considered an essential aspect of many individuals’ lives, and it has been postulated to positively impact periodontitis through various mechanisms, including improved insulin sensitivity, decreased incidence of lifestyle-related diseases and obesity, stress reduction, and decreased inflammation reactions [53]. Furthermore, lifestyle and obesity are closely linked to the development of periodontitis [54]. Despite this, few studies have investigated the relationship between exercise and periodontitis. Two previous published meta-analyses have tried to clarify the underlying relationship between exercise and periodontitis [17, 18]. However, the results should be considered carefully to some extent due to the limited research available and certain risk of bias. In addition, these previous meta-analyses only included observational studies. Conversely, after a comprehensive literature review, 30 studies were selected for inclusion in our study. Moreover, in this study, we included both experimental studies and observational studies. Following a systematic review, the included studies demonstrated a significant correlation between exercise and periodontitis. To our knowledge, this is one of the first reviews that focus on the influence of taking exercise on periodontitis.

As the fourth leading risk factor for global mortality, physical inactivity has been identified as a modifiable risk factor for various diseases, such as diabetes mellitus, hypertension, cardiovascular disease, and osteoporosis [55]. Exercise and physical activity have been shown to enhance life quality and increase life expectancy, resulting in an increasing focus on these activities by organizations [56]. The terms exercise and physical activity have been currently used interchangeably in the literature [57]. Therefore, we included both of them in the systematic review to improve the reliability. Previous research has indicated that exercise is linked to a favorable inflammatory profile, which may provide some protection against oral diseases [58]. The World Health Organization (WHO) recommends a moderate exercise pattern, defined as at least 75 min of running or 150 min of brisk walking per week, which has been associated with a lower prevalence of lifestyle-related diseases [3]. However, there are still a significant number of individuals who fail to meet these recommendations, which needs to be taken seriously.

Periodontitis refers to pathologic loss of alveolar bone and periodontal ligament, involving complex dynamic interactions among destructive immune responses and specific bacterial pathogens [59]. Our results showed that taking exercise is considered a health-promoting measure, which results in a decrease in the prevalence and severity of periodontitis. The underlying mechanism accounting for this reduction in prevalence may be associated with the influence of taking exercise on cytokine production and immune modulation [60, 61]. C-reactive protein (CRP), a by-product of vitamin K metabolism, is significantly correlated with periodontitis. Studies have revealed that physical exercise can modulate several cytokines, including CRP [13]. Thus, maintaining regular physical activity should be encouraged to improve periodontitis.

This study performed a literature review and meta-analysis, which confirmed the relationship between exercise and periodontitis. Among the 30 studies included, 20 reported a positive relationship between the level of exercise and periodontitis, the remaining 10 articles did not report significant differences. Notably, none of the included studies reported any negative effects regarding the influence of exercise on periodontitis. The meta-analysis revealed a risk ratio of 0.84 (95% CI: 0.77, 0.91) between the exercise group and the inactive group (P < 0.01), although there was considerable heterogeneity, which indicates that engaging in physical exercise is inversely associated with the presence and severity of periodontitis.

The selected studies proposed several influential factors that may impact periodontitis, including maintaining a healthy weight, consuming a nutritious diet, reducing sedentary behavior, and avoiding cigarette smoking. Among the studies, 7 evaluated diet quality and found a strong association between consuming a high-quality diet and improving periodontitis. In addition, 4 studies suggested that maintaining normal body weight is important in preventing periodontitis, as obesity-related inflammation can induce bacterial proliferation and produce inflammatory markers in fat tissues, which may exacerbate periodontitis. 3 studies analyzed the influence of tobacco smoking habits on periodontitis and concluded that cigarette smoking may affect the periodontal status through total salivary antioxidant activity. Furthermore, higher sedentary behavior was found to be associated with higher odds of periodontitis. Accordingly, in addition to emphasizing exercise, interventions should also focus on the factors mentioned above, including improving diet quality, maintaining normal body weight, reducing sedentary behavior, and avoiding cigarette smoking.

The present study has several limitations. Firstly, the measurement of exercise involved multiple tools, including different versions of questionnaires, strength, and maximal oxygen consumption, resulting in challenges in drawing definitive conclusions. Additionally, the included studies had varying sample sizes, with a significant gap between the smallest and largest numbers, and were mostly conducted in developed countries, which may have affected the quality of data analysis. Finally, most selected studies were observational and did not employ measures to reduce bias such as random allocation. Accordingly, in order to address existing gaps in evidence, future researches in larger population samples with a longer follow-up time are needed to understand the real role of exercise on the prevalence of periodontitis. Moreover, more intervention researches are needed to establish a possible cause-effect association between exercise and the management of periodontitis.

Conclusion

Despite current knowledge gaps, the present review and meta-analysis systematically summarized current epidemiological data, providing evidence of a significant correlation between exercise and a lower occurrence of periodontitis. Therefore, taking exercise is proposed as a critical component of periodontitis management. Future researches in larger population samples with a longer follow-up time are needed to understand the real role of exercise on the prevalence of periodontitis. Moreover, more intervention researches are needed to establish a possible cause-effect association between exercise and the management of periodontitis, to help dental health providers take measures in clinical scenarios.