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Review

Association between Periodontal Disease and Obesity: Umbrella Review

by
Heber Isac Arbildo-Vega
1,2,
Fredy Hugo Cruzado-Oliva
3,
Franz Tito Coronel-Zubiate
4,
Rubén Aguirre-Ipenza
5,*,
Joan Manuel Meza-Málaga
6,7,
Sara Antonieta Luján-Valencia
6,8,
Eduardo Luján-Urviola
9 and
Carlos Alberto Farje-Gallardo
4
1
Faculty of Dentistry, Dentistry School, San Martin de Porres University, Chiclayo 14012, Peru
2
Faculty of Human Medicine, Human Medicine School, San Martín de Porres University, Chiclayo 14012, Peru
3
Faculty of Stomatology, Stomatology School, Nacional University of Trujillo, Trujillo 13001, Peru
4
Faculty of Health Sciences, Stomatology School, Toribio Rodríguez of Mendoza National University of Amazonas, Chachapoyas 01001, Peru
5
Faculty of Health Sciences, Continental University, Lima 15046, Peru
6
Faculty of Dentistry, Dentistry School, Catholic University of Santa Maria, Arequipa 04013, Peru
7
Faculty of Medicine, Medicine School, Catholic University of Santa Maria, Arequipa 04013, Peru
8
Postgraduate School, Catholic University of Santa Maria, Arequipa 04013, Peru
9
Faculty of Dentistry, Néstor Cáceres Velásquez Andean University, Juliaca 21104, Peru
*
Author to whom correspondence should be addressed.
Medicina 2024, 60(4), 621; https://doi.org/10.3390/medicina60040621
Submission received: 19 March 2024 / Revised: 5 April 2024 / Accepted: 5 April 2024 / Published: 11 April 2024
(This article belongs to the Special Issue Medicine and Dentistry: New Methods and Clinical Approaches)

Abstract

:
Objective: Determine the association between periodontal disease (PD) and obesity through an umbrella review. Materials and Methods: A search for information until March 2024 was carried out in the following electronic databases: PubMed, Cochrane library, Scopus, SciELO, Web of Science, Google Scholar, Proquest Dissertations and Theses, and OpenGrey. We included studies that were systematic reviews (SR) with or without meta-analysis, without time or language restrictions, that evaluated primary studies that associated PD with obesity. Literary or narrative reviews, rapid reviews, intervention studies, observational studies, preclinical and basic research, summaries, comments, case reports, protocols, personal opinions, letters, and posters were excluded. The AMSTAR-2 tool was used to determine the quality and overall confidence of the included studies. Results: The preliminary search yielded a total of 419 articles, discarding those that did not meet the selection criteria, leaving only 14 articles. All studies reported that PD was associated with obesity, with an OR and RR ranging from 1.1 to 1.46 and 1.64 to 2.21, respectively. Conclusions: Based on the results and conclusions of the SR with a high overall confidence level, PD is associated with obesity.

1. Introduction

In recent years, evidence has accumulated on the relationships between oral diseases such as periodontitis and various systemic diseases, known as periodontal medicine [1]. The strongest associations, supported by a significant amount of evidence, include cardiovascular disease, adverse pregnancy outcomes, respiratory disease, and diabetes mellitus [2,3,4,5]. In 2013, the European Federation of Periodontology (EFP) and the American Academy of Periodontology (AAP) organized workshops focusing on these associations, especially cardiovascular disease, diabetes, and adverse pregnancy outcomes [6,7,8,9]. However, Linden et al. [10] explored lesser-known associations, such as chronic kidney disease, rheumatoid arthritis, cognitive decline, inflammatory cancers, and obesity. Although some modest associations were found between periodontitis and obesity, connections with other diseases are weaker and are subject to limitations in the definition of periodontal disease (PD) and the control of confounding factors in the studies [10]. A systematic mapping of clinical trial registries conducted in 2016 reported that 57 systemic conditions are currently being investigated for possible links to PDs [11].
Obesity and being overweight represent a significant public health challenge in the modern era [12], with prevalence steadily increasing globally since 1980 [13]. This problem affects about a third of the world’s population, with higher rates among men for overweight and among women for obesity [13,14]. Furthermore, each year, obesity and being overweight cause the death of around 3.4 million people [13,15,16]. The World Health Organization (WHO) defines an adult as overweight if the body mass index (BMI) is greater than or equal to 25 and obese if the BMI is greater than or equal to 30 [17], while, for children and adolescents, it defines that they will be overweight if the BMI is greater than or equal to the 85th percentile and obese if the BMI is greater than or equal to the 95th percentile [18].
Obesity is associated with an increased risk of serious diseases, such as heart disease, hypertension, type 2 diabetes, and several types of cancer, and contributes to increased medical costs [13,19,20]. Despite genetic predisposition, environmental changes, availability of high-fat foods, and decreased physical activity have contributed to rising obesity rates worldwide [21]. The BMI is a commonly used measure to assess the relative amount of body fat in a person [22,23,24] and has been associated with metabolism [25,26] and oral health [27]. Obesity is associated with dental problems such as dental caries, periodontitis, and tooth loss, and inflammation is thought to play a key role in this relationship [27,28].
Only one umbrella systematic review [1] on the associations of PD with obesity has been published in the scientific literature. However, a general synthesis and evaluation of all systematic reviews taken together, including those published in recent years, has not yet been performed. Therefore, the purpose of this umbrella review was to summarize the available evidence and answer the following specific question: “What do we know so far about the association of PD and obesity?” and what is the overall confidence of systematic reviews assessing this topic?

2. Materials and Methods

2.1. Protocol and Registration

A protocol was carried out based on the Preferred Reporting Items for Systematic Reviews and Meta-Analysis Protocols (PRISMA-P) [29] and registered in the Prospective Registry of Systematic Reviews (PROSPERO) [30]. The registry is publicly available under the number CRD42024521090. In addition, the report of this study is based on the Preferred Reporting Items for Overview of Systematic Reviews Checklist (PRIO-harms) [31]. Ethical approval was not required for this umbrella review.
The focused question was formulated using the PECO format (population, exposure, comparison, and outcomes), as detailed below:
  • − Population: people of all ages.
  • − Exposure: people with obesity (BMI ≥ 30 or ≥95th percentile) and/or overweight (BMI ≥ 25 or ≥85th percentile).
  • − Comparison: people with normal weight (BMI ≥ 18.5 or ≥5th percentile).
  • − Outcomes: association with periodontal disease.

2.2. Eligibility Criteria and Results of Interest

The included studies were systematic reviews (SR) with or without meta-analysis, without time and language restrictions, that evaluated primary studies that reported the association between PD and obesity.
Literature or narrative reviews, rapid reviews, intervention studies, observational studies, preclinical and basic research, abstracts, commentaries, case reports, protocols, personal opinions, letters, and posters were excluded.

2.3. Sources of Information, Search Strategy, and Additional Search for Primary Studies

An electronic search was performed on 5 March 2024 in five databases (Pubmed, Cochrane database, Scielo, Web of Science, and Scopus). Gray literature was also consulted through Google Scholar, Proquest Dissertations and Theses, and OpenGrey. In addition, the reference lists of the included studies were reviewed. The found articles were exported to reference management software (Zotero® 6.0, Center for History and New Media, Fairfax, VA, USA) and duplicate articles were removed. The search strategy adopted for each database is shown in Table 1.

2.4. Data Management and Selection Process

The identified articles were entered into Rayyan® Online Software https://www.rayyan.ai/, accessed on 4 April 2024 (Qatar Research Institute of Computing, Doha, Qatar). The selection of the studies was performed in 2 phases; in phase 1, two reviewers (F.C.O. and F.C.Z.) independently selected the studies by reading the title and abstract; then, phase 2 was carried out, which consisted of reading the full text, performed independently by the same two reviewers. A third reviewer (H.A.) was consulted in case of disagreement.

2.5. Data Collection Process

Data from the studies were independently collected in duplicate using a table previously formulated by two reviewers (F.C.O. and R.A.). The data were cross-checked and disagreements resolved by the third review author (H.A.). The following information was extracted from the selected articles: authors, year of publication, study design, design of the primary studies included, number of studies included in the qualitative and quantitative analysis, results, main conclusions, mentions of what was used or carried out: PRISMA, PROSPERO, and Grading of Recommendations Assessment, Development and Assessment (GRADE), and meta-analysis.

2.6. Assessment of Methodological Quality, Quality of Evidence, and Meta-Bias

The evaluation of the methodological quality of the included SRs was performed independently in duplicate by two reviewers (J.M. and S.L.), calibrated (Kappa 0.85), using the AMSTAR-2 checklist (A MeaSurement Tool to Assess Systemic Reviews) [32]. The AMSTAR-2 evaluates the methodological quality of the SR through 16 questions that can be answered with three possible answers: “yes”, “no”, or “partially yes”. The overall confidence rating (high, moderate, low, and critically low) in the studies was assessed as suggested by Shea et al. [32].

2.7. Summary of Measures

In the case of an SR without meta-analysis, the results shown in odds ratio (OR), hazard ratio (HR), incidence risk ratio (IRR), or prevalence ratio (PR) in ranges or intervals were considered. If the SR presents meta-analysis, we consider the results that were shown with OR, risk/rate ratio (RR), or standardized mean difference (SMD) for the association between PD and obesity.

2.8. Summary of Results

The main results of the included SRs were summarized, categorizing their findings into the following points: general association, by age, sex, countries, or continents, BMI, type of PD, smoking, and by periodontal clinical parameters (plaque index, gingival index, bleeding on probing, probing depth, and sub- and supragingival calculus).

3. Results

3.1. Review and Selection of Primary Studies

The electronic database search retrieved 419 references, with 267 remaining after removal of duplicates. In phase 1, the title and abstract of the identified studies were assessed and 23 articles eligible for full-text reading were considered. Finally, 14 SRs remained for the qualitative synthesis. The reasons for the exclusion of the articles are shown in Table 2. The complete process of identification and selection of the studies is shown in Figure 1.

3.2. Review and Characteristics of Included Studies

The SRs included were published between 2010 and 2022. They were held in Brazil [42,43,44,45], South Korea [46], Qatar [47], Indonesia [48], Australia [49], Belgium [50], Spain [51], Denmark [52], China [53], United Kingdom [54], and United States [55]. Nine SRs [43,44,45,46,47,48,51,54,55] studied the association in adults, two in adolescents and adults [49,52], two in children and adolescents [50,53], and one in pregnant women [42]. More information on SR characteristics can be found in Table 3.

3.3. Assessment of Methodological Quality and Quality of Evidence

Nine SRs [42,43,44,46,49,52,53,54,55] were considered to have high confidence, four SRs [45,47,48,50] had low confidence, and one SR [51] had critically low confidence (Table 4).

3.4. Overlapping

A total of 397 primary studies were identified in the SRs. Of these, approximately 41.81% of the primary studies were included in more than one SR. Thirty studies were included twice; twenty-three were included three times; twelve were included four times; seven were included five times; four were included six times; and one was included seven times. More information on the overlap and characteristics of the primary studies is available in Table 5.

3.5. Synthesis of Results

The syntheses of the results are presented in Table 6.

3.5.1. General Association

Nine SRs [42,45,46,47,48,49,50,51,55] included reported that there was an association between PD and obesity. Six SRs [42,45,46,48,50,55] meta-analyzed the results and found that the OR ranged from 1.23 (CI: 1.15 to 1.33) [48] to 1.46 (CI: 1.20 to 1.77) [50] and the RR was 2.21 (CI: 1.53 to 3.17) [42]. Abu-Shawish et al. [47] reported that the OR ranged from 1.77 to 3.25 and the RR ranged from 1.64 to 1.84, while Khan et al. [49] reported that the OR ranged between 1.1 and 4.5 and Martínez-Herrera et al. [51] reported that the OR ranged from 0.99 to 4.3, the HR ranged between 1.03 and 3.24, and the RR ranged from 0.99 to 5.4.

3.5.2. Age

Three SRs [46,52,55] included reported that there was an association between PD and obesity according to age. Two SRs [46,55] meta-analyzed the results and found that the OR was 2.21 (CI: 1.26 to 3.89) [46], 1.53 (CI: 1.17 to 2.00) [46], 1.82 (CI: 1.16 to 2.83) [46], 1.35 (CI: 1.14 to 1.59) [55], and 1.21 (CI: 1.04 to 1.41) [55] for ages 18 to 34 years, 35 to 54 years, older and equal to 55 years, young, and old, respectively. Keller et al. [52] reported that the HR ranged from 1.30 to 3.24 and 1.09 to 1.70, the IRR was 1.3 and 1.2, and the PR was 1.01 and 0.99 for ages in obese and overweight people, respectively.

3.5.3. Sex

One SR [55] included reported that there was an association between PD and obesity according to sex. This study meta-analyzed its results and found that the OR was 1.50 (CI: 1.27 to 1.77) for men and 1.75 (CI: 1.26 to 2.43) for women.

3.5.4. Country or Continent

Two SRs [46,55] included reported that there was an association between PD and obesity depending on the country or continent. All of them meta-analyzed the results and found that the OR for the United States, Brazil, Korea, and Japan ranged from 0.59 (CI: 0.19 to 1.65) [46] to 1.75 (CI: 1.48 to 2.06) [46], while the OR for European countries, East Asia, Europe and the Middle East, and other Asian countries ranged from 0.98 (CI: 0.49 to 1.95) [46] to 2.46 (CI: 1.11 to 5.46) [46].

3.5.5. Obese

Three SRs [44,54,55] included reported that there was an association between PD and people with obesity, while one RS [43] reported that there was an association between gingivitis and obese people. They all meta-analyzed the results and found that the OR ranged from 1.52 (CI: 1.26 to 1.83) [55] to 1.81 (CI: 1.42 to 2.30) [54]. The SMD ranged from 0.05 (CI: −0.20 to 0.29) [43] to 1.10 (CI: 0.14 to 2.05) [43]. Furthermore, the RR was 1.34 (CI: 1.21 to 1.47) [44].

3.5.6. Overweight

Three SRs [44,54,55] included reported that there was an association between PD and overweight people, while one RS [43] reported that this association did not exist. They all meta-analyzed the results and found that the OR ranged from 1.18 (CI: 1.00 to 1.39) [55] to 1.27 (CI: 1.06 to 1.51) [54]. The SMD ranged from 0.30 (CI: −0.03 to 0.62) [43] to 2.08 (CI: −0.60 to 4.77) [43]. Furthermore, the RR was 1.13 (CI: 1.06 to 1.20) [44].

3.5.7. Smoker and Non-Smoker

One SR [55] included reported that there was an association between PD and obesity depending on whether the person did not smoke. This study meta-analyzed its results and found that the OR was 1.36 (CI: 0.98 to 1.88) for smokers and 2.08 (CI: 1.29 to 3.36) for non-smokers.

3.5.8. Bleeding on Probing

One SR [53] included reported that there was an association between PD and obesity when the BOP was greater than 25%, while one RS [43] reported that there was such an association when the BOP was from people with gingivitis and who were overweight. They all meta-analyzed their results and found that the OR was 5.41 (CI: 2.75 to 10.63) [53], while the SMD for the obese ranged from 0.03 (CI: −0.23 to 0.28) [43] to 0.64 (CI: −0.37 to 1.65) [43] and, for those who were overweight, it ranged from 0.13 (CI: −0.04 to 0.30) [43] to 0.78 (CI: 0.52 to 1.03) [43].

3.5.9. Gingival Index

One SR [43] included reported that there was an association between PD and overweight people according to their gingival index. This study meta-analyzed its results and found that the SMD for the obese ranged from 0.35 (CI: −0.21 to −0.91) to 2.13 (CI: −1.51 to 5.77) and, for overweight people, it ranged from 0.97 (CI: 0.45 to 1.49) to 3.52 (CI: 2.32 to 4.71).

3.5.10. Plaque Index

One SR [53] included reported that there was an association between PD and obesity when the plaque index was greater than 25%. This study meta-analyzed its results and found that the OR was 4.75 (CI: 2.42 to 9.34).

3.5.11. Probing Depth

One SR [53] included reported that there was an association between PD and obesity when probing depth was greater than 4 mm. This study meta-analyzed its results and found that the OR was 14.15 (CI: 5.10 to 39.25).

3.5.12. Subgingival Calculus

One SR [53] included reported that there was an association between PD and obesity according to subgingival calculus. This study meta-analyzed its results and found that the OR was 3.07 (CI: 1.10 to 8.62).

3.5.13. Supragingival Calculus

One SR [53] included reported that there was no association between PD and obesity according to supragingival calculus. This study meta-analyzed its results and found that the OR was 1.08 (CI: 0.60 to 1.94).

4. Discussion

In recent years, there has been increasing interest in evaluating and analyzing the relationship between PD and obesity. Numerous studies have investigated this topic and found evidence to support this association.
Currently, obesity and overweight are considered global health problems of epidemic proportions, classified as chronic inflammatory diseases by the National Institutes of Health (NIH) and the World Health Organization (WHO) [1]. The WHO has reported a significant increase in obesity rates worldwide in all age groups since 1975 [1]. Although initially attributed primarily to an energy imbalance between calories consumed and calories expended, it is now recognized that the causes of obesity and overweight are much more complex and involve environmental and genetic factors [1,130].
For more than 20 years, oral health researchers have investigated the possible relationship between obesity and PD. Several potential mechanisms linking the two conditions have been identified, including an exaggerated immune response in obese individuals [128,131], differences in the oral microbiome [132], and the release of proinflammatory cytokines by adipose tissue cells [133]. Other mechanisms include the role of several molecules, such as TNFα, leptin, and ghrelin, which are involved in inflammation and energy balance [130]. These findings support the possibility of a biological connection between PD and obesity.
An umbrella review in 2018 [130] that included 14 SRs on the relationship between periodontitis and obesity highlighted that obese people are more likely to suffer from periodontitis than those of normal weight. Furthermore, Khan et al. [49] also found a positive association between obesity and periodontitis in young adults and adolescents. These findings were supported by a longitudinal cohort study in Taiwan, that included more than 12,000 people and found a slightly increased risk of periodontitis in obese people, with an even higher risk in obese people over 65 years of age [134].
Previous studies of the relationship between periodontitis and obesity have been conducted primarily in animals or through cross-sectional, case–control, or cohort studies. Recently, however, intervention studies have recently emerged. For example, Suvan et al. [130] analyzed six SRs that included intervention studies, but the results were contradictory.
Most studies found no differences in gingival inflammation between obese and non-obese individuals, but higher levels were observed in obese people with periodontitis. In addition, there were variations in the measurement of obesity, with some studies using different measures such as waist–hip ratio (WHR) and waist circumference (WC), indicating the need for consistency in measurement tools in future studies [43]. It is also clear that there is a positive association between obesity and periodontitis at all age levels, although determination of a cause–effect relationship is premature at this time [1].
In the present study, a comprehensive literature search was conducted to summarize and analyze the available SRs on the association between PD and obesity, and 14 SRs were identified that met the selection criteria. Although SRs are a reliable source of scientific evidence, it is important to be cautious when interpreting their results due to the possibility of bias. The SRs included in this study showed certain limitations related to the selected primary studies: different types of study, different definition criteria for periodontal disease (gingivitis or periodontitis), and different population groups studied (children, adolescents, adults, and pregnant women). These limitations of the primary studies made it impossible to perform a meta-analysis.
Some studies included in the analysis had a high level of confidence, which could strengthen the evidence for the results and conclusions of the current study. However, the persistence of systematic reviews with lower confidence levels highlights the need for greater rigor in conducting research on this topic.
The assessment of the methodological quality of the included SRs was performed using the AMSTAR-2 tool, which is current and widely recognized. Some studies were found to have deficiencies in critical domains 7, 9, and 13 of this tool. These deficiencies included failure to provide a list of excluded studies with justification, inadequate use of techniques to assess risk of bias, and failure to consider such risk when interpreting or discussing results. These findings highlight the importance of addressing these elements in future SRs.
Furthermore, caution should be taken when interpreting the results of systematic reviews, as about 50% of the included primary studies are repeated in multiple reviews, which may lead to repeated re-evaluation of the same data. This may distort the perception of the amount of work conducted in the field. Although, it would be beneficial to conduct new SRs to address the methodological limitations recommended by Moher [135] due to the high degree of overlap between existing reviews.

4.1. Evidence Summary

In this umbrella review, we sought to clarify the association between PD and obesity through the collection and analysis of SRs and meta-analysis on this topic, identifying the following results:
The SRs included in this study suggest an overall positive and direct association between PD and obesity. This finding aligns with what was found by Suvan et al. [130] and Lavigne [1], who also reported on this association.
With regard to age, it was observed that the association between PD and obesity was stronger in young people. This may be due to the fact that young people today tend to adopt unhealthy eating habits, which may contribute to both obesity and oral health problems [136,137].
Regarding gender, it was observed that this association was more present in women. This may be because hormonal changes during the menstrual cycle, pregnancy, and menopause affect fat metabolism in women, generally resulting in a higher percentage of body fat in women compared to men [130,138,139,140].
In relation to the country or continent, it was observed that the association was present in most countries and continents. This may be attributed to globalization and the adoption of Western lifestyles in many countries, which has led to the increase in unhealthy eating habits, smoking, and lack of physical activity [130,141].
In obese and overweight individuals, this association was found to be more pronounced in obese individuals. This may be due to unhealthy eating habits and lack of physical activity in this population group [130].
In relation to smoking, the association is more present in non-smokers. This may be explained by the tendency of smokers to have a weakened immune response and a greater propensity to inflammation, which could obscure this association. On the other hand, non-smokers may have a more pronounced inflammatory response to the inflammatory effects of obesity [52].
Regarding periodontal clinical indicators, the association was observed in all clinical aspects. This could be due to the fact that obesity is linked to modifications in the immune response and systemic inflammation, which negatively impacts periodontal health [1].

4.2. Implications for Clinical Practice

Oral health professionals have a responsibility to raise awareness and educate patients about how overweight and obesity can increase the risk of developing PD. Promoting good oral hygiene, including regular tooth brushing, flossing, and mouthwash, can help prevent plaque buildup and reduce the risk of PD. In the era of personalized medicine, it is suggested to incorporate BMI measurement as part of routine risk assessment and educate patients about the complex, multiorgan nature of obesity. It is crucial to implement preventive interventions to modify risk factors such as diet, exercise, and weight control, which may decrease the likelihood of obesity and PD. Additionally, a monitoring and follow-up plan should be established for patients with obesity, including frequent visits to the dentist and specific evaluations to detect PD early and provide intervention when necessary. Collaboration with endocrinologists, nutritionists and other specialists is essential for a comprehensive approach to the management of patients with obesity, allowing for co-ordinated medical and dental care.

4.3. Implications for Research

This review highlights the need to improve the presentation of SRs. The authors suggest the use of quality assessment tools to guide the development of future SRs. They also emphasize the importance of conducting primary studies with high methodological rigor to obtain more reliable results.
For future research on this topic, it is recommended to standardize the diagnostic criteria for both PD and obesity, conduct high-quality prospective studies with larger samples and consistent measures, and conduct more robust research to understand the precise mechanisms and the magnitude of the association between PD and obesity.

5. Conclusions

Based on the results and conclusions of the SRs with a high overall confidence, PD is associated with obesity in children, adolescents, adults, and pregnant women.

Author Contributions

Conceptualization, H.I.A.-V.; methodology, H.I.A.-V. and F.H.C.-O.; software, F.T.C.-Z. and E.L.-U.; validation, S.A.L.-V., J.M.M.-M. and R.A.-I.; formal analysis, H.I.A.-V.; investigation, F.H.C.-O.; resources, C.A.F.-G.; data curation, R.A.-I.; writing—original draft preparation, H.I.A.-V. and F.H.C.-O.; writing—review and editing, R.A.-I. and H.I.A.-V.; visualization, J.M.M.-M.; supervision, H.I.A.-V.; project administration, S.A.L.-V.; funding acquisition, R.A.-I. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Lavigne, S.E. Evolving evidence for relationships between periodontitis and systemic diseases: Position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2022, 56, 155–171. [Google Scholar] [PubMed]
  2. Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews of the evidence of a causal relationship between periodontal disease and cardiovascular diseases: Position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2020, 54, 32–41. [Google Scholar] [PubMed]
  3. Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews of the evidence of a causal relationship between periodontal disease and adverse pregnancy outcomes: A position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2020, 54, 92–100. [Google Scholar] [PubMed]
  4. Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews of the evidence of a causal relationship between periodontal microbes and respiratory diseases: Position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2020, 54, 144–155. [Google Scholar] [PubMed]
  5. Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews examining the relationship between type 2 diabetes and periodontitis: Position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2021, 55, 57–67. [Google Scholar]
  6. Tonetti, M.S.; Van Dyke, T.E.; Working Group 1 of the Joint EFP/AAP Workshop. Periodontitis and atherosclerotic cardiovascular disease: Consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J. Periodontol. 2013, 84, S24–S29. [Google Scholar] [CrossRef] [PubMed]
  7. Chapple, I.L.C.; Genco, R.; Working Group 2 of the Joint EFP/AAP Workshop. Diabetes and periodontal diseases: Consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J. Periodontol. 2013, 84, S106–S112. [Google Scholar] [CrossRef]
  8. Sanz, M.; Kornman, K.; Working Group 3 of the Joint EFP/AAP Workshop. Periodontitis and adverse pregnancy outcomes: Consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J. Periodontol. 2013, 84, S164–S169. [Google Scholar] [CrossRef] [PubMed]
  9. Linden, G.J.; Herzberg, M.C.; Working Group 4 of the Joint EFP/AAP Workshop. Periodontitis and systemic diseases: A record of discussions of working group 4 of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J. Clin. Periodontol. 2013, 40, S20–S23. [Google Scholar] [CrossRef]
  10. Linden, G.J.; Lyons, A.; Scannapieco, F.A. Periodontal systemic associations: Review of the evidence. J. Clin. Periodontol. 2013, 40, S8–S19. [Google Scholar] [CrossRef]
  11. Monsarrat, P.; Blaizot, A.; Kémoun, P.; Ravaud, P.; Nabet, C.; Sixou, M.; Vergnes, J.-N. Clinical research activity in periodontal medicine: A systematic mapping of trial registers. J. Clin. Periodontol. 2016, 43, 390–400. [Google Scholar] [CrossRef] [PubMed]
  12. Ebbeling, C.B.; Pawlak, D.B.; Ludwig, D.S. Childhood obesity: Public-health crisis, common sense cure. Lancet 2002, 360, 473–482. [Google Scholar] [CrossRef] [PubMed]
  13. Issrani, R.; Reddy, J.; Bader, A.K.; Albalawi, R.F.H.; Alserhani, E.D.M.; Alruwaili, D.S.R.; Alanazi, G.R.A.; Alruwaili, N.S.R.; Sghaireen, M.G.; Rao, K. Exploring an Association between Body Mass Index and Oral Health—A Scoping Review. Diagnostics 2023, 13, 902. [Google Scholar] [CrossRef] [PubMed]
  14. Seidell, J.C.; Flegal, K.M. Assessing obesity: Classification and epidemiology. Br. Med. Bull. 1997, 53, 238–252. [Google Scholar] [CrossRef] [PubMed]
  15. Idrees, M.; Hammad, M.; Faden, A.; Kujan, O. Influence of body mass index on severity of dental caries: Cross-sectional study in healthy adults. Ann. Saudi Med. 2017, 37, 444–448. [Google Scholar] [CrossRef] [PubMed]
  16. Adams, K.F.; Schatzkin, A.; Harris, T.B.; Kipnis, V.; Mouw, T.; Ballard-Barbash, R.; Hollenbeck, A.; Leitzmann, M.F. Overweight, Obesity, and Mortality in a Large Prospective Cohort of Persons 50 to 71 Years Old. N. Engl. J. Med. 2006, 355, 763–778. [Google Scholar] [CrossRef] [PubMed]
  17. Zeb, A.; Sivarajan Froelicher, E.; Pienaar, A.J.; Dhamani, K. Effectiveness of Community-based Obesity Intervention for Body Weight, Body Mass Index, and Waist Circumference: Meta-analysis. Iran. J. Nurs. Midwifery Res. 2024, 29, 16–22. [Google Scholar] [PubMed]
  18. Carullo, N.; Zicarelli, M.; Michael, A.; Faga, T.; Battaglia, Y.; Pisani, A.; Perticone, M.; Costa, D.; Ielapi, N.; Coppolino, G.; et al. Childhood Obesity: Insight into Kidney Involvement. Int. J. Mol. Sci. 2023, 24, 17400. [Google Scholar] [CrossRef] [PubMed]
  19. Deshpande, N.C.; Amrutiya, M.R. Obesity and oral health—Is there a link? An observational study. J. India Soc. Periodontol. 2017, 21, 229. [Google Scholar] [CrossRef]
  20. Prospective Studies Collaboration; Whitlock, G.; Lewington, S.; Sherliker, P.; Clarke, R.; Emberson, J.; Halsey, J. Body-mass index and cause-specific mortality in 900 000 adults: Collaborative analyses of 57 prospective studies. Lancet 2009, 373, 1083–1096. [Google Scholar] [CrossRef]
  21. Galgani, J.; Ravussin, E. Energy metabolism, fuel selection and body weight regulation. Int. J. Obes. 2008, 32, S109–S119. [Google Scholar] [CrossRef] [PubMed]
  22. Suvan, J.; Petrie, A.; Moles, D.R.; Nibali, L.; Patel, K.; Darbar, U.; Donos, N.; Tonetti, M.; D’Aiuto, F. Body Mass Index as a Predictive Factor of Periodontal Therapy Outcomes. J. Dent. Res. 2014, 93, 49–54. [Google Scholar] [CrossRef] [PubMed]
  23. Eknoyan, G. Adolphe Quetelet (1796–1874)—The average man and indices of obesity. Nephrol. Dial. Transplant. 2008, 23, 47–51. [Google Scholar] [CrossRef] [PubMed]
  24. Kapila, Y.L. Oral health’s inextricable connection to systemic health: Special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontology 2000 2021, 87, 11–16. [Google Scholar] [CrossRef] [PubMed]
  25. Finucane, M.M.; Stevens, G.A.; Cowan, M.J.; Danaei, G.; Lin, J.K.; Paciorek, C.J.; Singh, G.M.; Gutierrez, H.R.; Lu, Y.; Bahalim, A.N.; et al. National, regional, and global trends in body-mass index since 1980: Systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9·1 million participants. Lancet 2011, 377, 557–567. [Google Scholar] [CrossRef] [PubMed]
  26. McMurray, R.G.; Soares, J.; Caspersen, C.J.; McCurdy, T. Examining variations of resting metabolic rate of adults: A public health perspective. Med. Sci. Sports Exerc. 2014, 46, 1352–1358. [Google Scholar] [CrossRef] [PubMed]
  27. Chang, Y.; Jeon, J.; Kim, J.-W.; Song, T.-J.; Kim, J. Association between Findings in Oral Health Screening and Body Mass Index: A Nation-Wide Longitudinal Study. Int. J. Environ. Res. Public Health 2021, 18, 11062. [Google Scholar] [CrossRef]
  28. Wood, N.; Johnson, R.B.; Streckfus, C.F. Comparison of body composition and periodontal disease using nutritional assessment techniques: Third National Health and Nutrition Examination Survey (NHANES III). J. Clin. Periodontol. 2003, 30, 321–327. [Google Scholar] [CrossRef] [PubMed]
  29. Shamseer, L.; Moher, D.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A.; PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation. BMJ 2015, 350, g7647. [Google Scholar] [CrossRef] [PubMed]
  30. Booth, A.; Clarke, M.; Ghersi, D.; Moher, D.; Petticrew, M.; Stewart, L. An international registry of systematic-review protocols. Lancet 2011, 377, 108–109. [Google Scholar] [CrossRef]
  31. Bougioukas, K.I.; Liakos, A.; Tsapas, A.; Ntzani, E.; Haidich, A.-B. Preferred reporting items for overviews of systematic reviews including harms checklist: A pilot tool to be used for balanced reporting of benefits and harms. J. Clin. Epidemiol. 2018, 93, 9–24. [Google Scholar] [CrossRef] [PubMed]
  32. Shea, B.J.; Reeves, B.C.; Wells, G.; Thuku, M.; Hamel, C.; Moran, J.; Moher, D.; Tugwell, P.; Welch, V.; Kristjansson, E.; et al. AMSTAR 2: A critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 2017, 358, j4008. [Google Scholar] [CrossRef] [PubMed]
  33. Paranhos, K.; Oliveira, S.; Bonato, R.; Niknami, N.; Vinayak, S.; Loomer, P. The impact of obesity on the outcome of periodontal disease treatment: Systematic review and meta-analysis. Dent. Res. J. 2023, 20, 108. [Google Scholar]
  34. Zhang, Y.; Jia, R.; Zhang, Y.; Sun, X.; Mei, Y.; Zou, R.; Niu, L.; Dong, S. Effect of non-surgical periodontal treatment on cytokines/adipocytokines levels among periodontitis patients with or without obesity: A systematic review and meta-analysis. BMC Oral Health 2023, 23, 717. [Google Scholar] [CrossRef] [PubMed]
  35. Joseph, P.; Prabhakar, P.; Holtfreter, B.; Pink, C.; Suvan, J.; Kocher, T.; Pitchika, V. Systematic review and meta-analysis of randomized controlled trials evaluating the efficacy of non-surgical periodontal treatment in patients with concurrent systemic conditions. Clin. Oral Investig. 2023, 28, 21. [Google Scholar] [CrossRef] [PubMed]
  36. Akram, Z.; Safii, S.H.; Vaithilingam, R.D.; Baharuddin, N.A.; Javed, F.; Vohra, F. Efficacy of non-surgical periodontal therapy in the management of chronic periodontitis among obese and non-obese patients: A systematic review and meta-analysis. Clin. Oral Investig. 2016, 20, 903–914. [Google Scholar] [CrossRef] [PubMed]
  37. Nascimento, G.G.; Leite, F.R.M.; Correa, M.B.; Peres, M.A.; Demarco, F.F. Does periodontal treatment have an effect on clinical and immunological parameters of periodontal disease in obese subjects? A systematic review and meta-analysis. Clin. Oral Investig. 2016, 20, 639–647. [Google Scholar] [CrossRef]
  38. Gerber, F.A.; Sahrmann, P.; Schmidlin, O.A.; Heumann, C.; Beer, J.H.; Schmidlin, P.R. Influence of obesity on the outcome of non-surgical periodontal therapy—A systematic review. BMC Oral Health 2016, 16, 90. [Google Scholar] [CrossRef] [PubMed]
  39. Papageorgiou, S.N.; Reichert, C.; Jaeger, A.; Deschner, J. Effect of overweight/obesity on response to periodontal treatment: Systematic review and a meta-analysis. J. Clin. Periodontol. 2015, 42, 247–261. [Google Scholar] [CrossRef]
  40. Deng, Q.; Wong, H.M.; Peng, S. Salivary and gingival crevicular fluid biomarkers of periodontal health and/or obesity among children and adolescents: A systematic review and meta-analysis. Heliyon 2024, 10, e23782. [Google Scholar] [CrossRef]
  41. Akram, Z.; Abduljabbar, T.; Abu Hassan, M.I.; Javed, F.; Vohra, F. Cytokine Profile in Chronic Periodontitis Patients with and without Obesity: A Systematic Review and Meta-Analysis. Dis. Markers 2016, 2016, 4801418. [Google Scholar] [CrossRef]
  42. Foratori-Junior, G.A.; Pereira, P.R.; Gasparoto, I.A.; de Sales-Peres, S.H.C.; de Souza, J.M.S.; Khan, S. Is overweight associated with periodontitis in pregnant women? Systematic review and meta-analysis. Jpn. Dent. Sci. Rev. 2022, 58, 41–51. [Google Scholar] [CrossRef]
  43. Da Silva, F.G.; Pola, N.M.; Casarin, M.; de Silva, C.F.; Muniz, F.W.M.G. Association between clinical measures of gingival inflammation and obesity in adults: Systematic review and meta-analyses. Clin. Oral Investig. 2021, 25, 4281–4298. [Google Scholar] [CrossRef] [PubMed]
  44. Nascimento, G.G.; Leite, F.R.M.; Do, L.G.; Peres, K.G.; Correa, M.B.; Demarco, F.F.; Peres, M.A. Is weight gain associated with the incidence of periodontitis? A systematic review and meta-analysis. J. Clin. Periodontol. 2015, 42, 495–505. [Google Scholar] [CrossRef]
  45. De Moura-Grec, P.G.; Marsicano, J.A.; Paz de Carvalho, C.A.; de Carvalho Sales-Peres, S.H. Obesity and periodontitis: Systematic review and meta-analysis. Cien Saude Colet. 2014, 19, 1763–1772. [Google Scholar] [CrossRef] [PubMed]
  46. Kim, C.M.; Lee, S.; Hwang, W.; Son, E.; Kim, T.W.; Kim, K.; Kim, Y.H. Obesity and periodontitis: A systematic review and updated meta-analysis. Front. Endocrinol. 2022, 13, 999455. [Google Scholar] [CrossRef] [PubMed]
  47. Abu-Shawish, G.; Betsy, J.; Anil, S. Is Obesity a Risk Factor for Periodontal Disease in Adults? A Systematic Review. Int. J. Environ. Res. Public Health 2022, 19, 12684. [Google Scholar] [CrossRef] [PubMed]
  48. Khairunnisa, L.; Dewi, Y.L.R.; Pamungkasari, E.P. Meta-Analysis the Association between Obesity and Periodontitis in Adults. J. Epidemiol. Public Health 2021, 6, 201–210. [Google Scholar] [CrossRef]
  49. Khan, S.; Barrington, G.; Bettiol, S.; Barnett, T.; Crocombe, L. Is overweight/obesity a risk factor for periodontitis in young adults and adolescents?: A systematic review. Obes. Rev. 2018, 19, 852–883. [Google Scholar] [CrossRef]
  50. Martens, L.; De Smet, S.; Yusof, M.Y.P.M.; Rajasekharan, S. Association between overweight/obesity and periodontal disease in children and adolescents: A systematic review and meta-analysis. Eur. Arch. Paediatr. Dent. 2017, 18, 69–82. [Google Scholar] [CrossRef]
  51. Martinez-Herrera, M.; Silvestre-Rangil, J.; Silvestre, F.-J. Association between obesity and periodontal disease. A systematic review of epidemiological studies and controlled clinical trials. Med. Oral Patol. Oral Cir. Bucal 2017, 22, E708–E715. [Google Scholar] [CrossRef] [PubMed]
  52. Keller, A.; Rohde, J.F.; Raymond, K.; Heitmann, B.L. Association Between Periodontal Disease and Overweight and Obesity: A Systematic Review. J. Periodontol. 2015, 86, 766–776. [Google Scholar] [CrossRef] [PubMed]
  53. Li, L.-W.; Wong, H.M.; Sun, L.; Wen, Y.F.; McGrath, C.P. Anthropometric Measurements and Periodontal Diseases in Children and Adolescents: A Systematic Review and Meta-Analysis. Adv. Nutr. 2015, 6, 828–841. [Google Scholar] [CrossRef] [PubMed]
  54. Suvan, J.; D’Aiuto, F.; Moles, D.R.; Petrie, A.; Donos, N. Association between overweight/obesity and periodontitis in adults. A systematic review. Obes. Rev. 2011, 12, e381–e404. [Google Scholar] [CrossRef] [PubMed]
  55. Chaffee, B.W.; Weston, S.J. Association Between Chronic Periodontal Disease and Obesity: A Systematic Review and Meta-Analysis. J. Periodontol. 2010, 81, 1708–1724. [Google Scholar] [CrossRef]
  56. Khader, Y.S.; Bawadi, H.A.; Haroun, T.F.; Alomari, M.; Tayyem, R.F. The association between periodontal disease and obesity among adults in Jordan. J. Clin. Periodontol. 2009, 36, 18–24. [Google Scholar] [CrossRef] [PubMed]
  57. Kongstad, J.; Hvidtfeldt, U.A.; Grønbaek, M.; Stoltze, K.; Holmstrup, P. The relationship between body mass index and periodontitis in the Copenhagen City Heart Study. J. Periodontol. 2009, 80, 1246–1253. [Google Scholar] [CrossRef] [PubMed]
  58. Ekuni, D.; Yamamoto, T.; Koyama, R.; Tsuneishi, M.; Naito, K.; Tobe, K. Relationship between body mass index and periodontitis in young Japanese adults. J. Periodontal Res. 2008, 43, 417–421. [Google Scholar] [CrossRef]
  59. Dalla Vecchia, C.F.; Susin, C.; Rösing, C.K.; Oppermann, R.V.; Albandar, J.M. Overweight and obesity as risk indicators for periodontitis in adults. J. Periodontol. 2005, 76, 1721–1728. [Google Scholar] [CrossRef]
  60. Al-Zahrani, M.S.; Bissada, N.F.; Borawskit, E.A. Obesity and periodontal disease in young, middle-aged, and older adults. J. Periodontol. 2003, 74, 610–615. [Google Scholar] [CrossRef]
  61. Pataro, A.L.; Costa, F.O.; Cortelli, S.C.; Cortelli, J.R.; Abreu, M.H.N.G.; Costa, J.E. Association between severity of body mass index and periodontal condition in women. Clin. Oral Investig. 2012, 16, 727–734. [Google Scholar] [CrossRef]
  62. Han, D.-H.; Lim, S.-Y.; Sun, B.-C.; Paek, D.-M.; Kim, H.-D. Visceral fat area-defined obesity and periodontitis among Koreans. J. Clin. Periodontol. 2010, 37, 172–179. [Google Scholar] [CrossRef] [PubMed]
  63. Saxlin, T.; Ylöstalo, P.; Suominen-Taipale, L.; Aromaa, A.; Knuuttila, M. Overweight and obesity weakly predict the development of periodontal infection. J. Clin. Periodontol. 2010, 37, 1059–1067. [Google Scholar] [CrossRef]
  64. Haffajee, A.D.; Socransky, S.S. Relation of body mass index, periodontitis and Tannerella forsythia. J. Clin. Periodontol. 2009, 36, 89–99. [Google Scholar] [CrossRef] [PubMed]
  65. Linden, G.; Patterson, C.; Evans, A.; Kee, F. Obesity and periodontitis in 60–70-year-old men. J. Clin. Periodontol. 2007, 34, 461–466. [Google Scholar] [CrossRef]
  66. Saito, T.; Shimazaki, Y.; Koga, T.; Tsuzuki, M.; Ohshima, A. Relationship between upper body obesity and periodontitis. J. Dent. Res. 2001, 80, 1631–1636. [Google Scholar] [CrossRef] [PubMed]
  67. Ekuni, D.; Mizutani, S.; Kojima, A.; Tomofuji, T.; Irie, K.; Azuma, T.; Yoneda, T.; Furuta, M.; Eshima, N.; Iwasaki, Y.; et al. Relationship between increases in BMI and changes in periodontal status: A prospective cohort study. J. Clin. Periodontol. 2014, 41, 772–778. [Google Scholar] [CrossRef]
  68. Amin, H.E.-S. Relationship between overall and abdominal obesity and periodontal disease among young adults. East. Mediterr. Health J. 2010, 16, 429–433. [Google Scholar] [CrossRef]
  69. Dumitrescu, A.L.; Kawamura, M. Involvement of psychosocial factors in the association of obesity with periodontitis. J. Oral. Sci. 2010, 52, 115–124. [Google Scholar] [CrossRef]
  70. Furuta, M.; Ekuni, D.; Yamamoto, T.; Irie, K.; Koyama, R.; Sanbe, T.; Yamanaka, R.; Morita, M.; Kuroki, K.; Tobe, K. Relationship between periodontitis and hepatic abnormalities in young adults. Acta Odontol. Scand. 2010, 68, 27–33. [Google Scholar] [CrossRef]
  71. Kumar, S.; Dagli, R.J.; Dhanni, C.; Duraiswamy, P. Relationship of body mass index with periodontal health status of green marble mine laborers in Kesariyaji, India. Braz. Oral Res. 2009, 23, 365–369. [Google Scholar] [CrossRef] [PubMed]
  72. Kushiyama, M.; Shimazaki, Y.; Yamashita, Y. Relationship between metabolic syndrome and periodontal disease in Japanese adults. J. Periodontol. 2009, 80, 1610–1615. [Google Scholar] [CrossRef]
  73. Sarlati, F.; Akhondi, N.; Ettehad, T.; Neyestani, T.; Kamali, Z. Relationship between obesity and periodontal status in a sample of young Iranian adults. Int. Dent. J. 2008, 58, 36–40. [Google Scholar] [PubMed]
  74. Borges-Yáñez, S.A.; Irigoyen-Camacho, M.E.; Maupomé, G. Risk factors and prevalence of periodontitis in community-dwelling elders in Mexico. J. Clin. Periodontol. 2006, 33, 184–194. [Google Scholar] [CrossRef] [PubMed]
  75. Reeves, A.F.; Rees, J.M.; Schiff, M.; Hujoel, P. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Arch. Pediatr. Adolesc. Med. 2006, 160, 894–899. [Google Scholar] [CrossRef]
  76. Genco, R.J.; Grossi, S.G.; Ho, A.; Nishimura, F.; Murayama, Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J. Periodontol. 2005, 76, 2075–2084. [Google Scholar] [CrossRef] [PubMed]
  77. Saito, T.; Shimazaki, Y.; Kiyohara, Y.; Kato, I.; Kubo, M.; Iida, M.; Yamashita, Y. Relationship between obesity, glucose tolerance, and periodontal disease in Japanese women: The Hisayama study. J. Periodontal Res. 2005, 40, 346–353. [Google Scholar] [CrossRef]
  78. Torrungruang, K.; Tamsailom, S.; Rojanasomsith, K.; Sutdhibhisal, S.; Nisapakultorn, K.; Vanichjakvong, O.; Prapakamol, S.; Premsirinirund, T.; Pusiri, T.; Jaratkulangkoon, O.; et al. Risk indicators of periodontal disease in older Thai adults. J. Periodontol. 2005, 76, 558–565. [Google Scholar] [CrossRef]
  79. Gulati, N.N.; Masamatti, S.S.; Chopra, P. Association between obesity and its determinants with chronic periodontitis: A cross-sectional study. J. Indian. Soc. Periodontol. 2020, 24, 167–172. [Google Scholar] [CrossRef]
  80. Buduneli, N.; Bıyıkoğlu, B.; Ilgenli, T.; Buduneli, E.; Nalbantsoy, A.; Saraç, F.; Kinane, D.F. Is obesity a possible modifier of periodontal disease as a chronic inflammatory process? A case-control study. J. Periodontal Res. 2014, 49, 465–471. [Google Scholar] [CrossRef]
  81. Fadel, H.T.; Pliaki, A.; Gronowitz, E.; Mårild, S.; Ramberg, P.; Dahlèn, G.; Yucel-Lindberg, T.; Heijl, L.; Birkhed, D. Clinical and biological indicators of dental caries and periodontal disease in adolescents with or without obesity. Clin. Oral Investig. 2014, 18, 359–368. [Google Scholar] [CrossRef] [PubMed]
  82. Altay, U.; Gürgan, C.A.; Ağbaht, K. Changes in inflammatory and metabolic parameters after periodontal treatment in patients with and without obesity. J. Periodontol. 2013, 84, 13–23. [Google Scholar] [CrossRef] [PubMed]
  83. Irigoyen-Camacho, M.E.; Sanchez-Perez, L.; Molina-Frechero, N.; Velazquez-Alva, C.; Zepeda-Zepeda, M.; Borges-Yanez, A. The relationship between body mass index and body fat percentage and periodontal status in Mexican adolescents. Acta Odontol. Scand. 2014, 72, 48–57. [Google Scholar] [CrossRef]
  84. Al-Zahrani, M.S.; Alghamdi, H.S. Effect of periodontal treatment on serum C-reactive protein level in obese and normal-weight women affected with chronic periodontitis. Saudi Med. J. 2012, 33, 309–314. [Google Scholar] [PubMed]
  85. De Castilhos, E.D.; Horta, B.L.; Gigante, D.P.; Demarco, F.F.; Peres, K.G.; Peres, M.A. Association between obesity and periodontal disease in young adults: A population-based birth cohort. J. Clin. Periodontol. 2012, 39, 717–724. [Google Scholar] [CrossRef] [PubMed]
  86. Gorman, A.; Kaye, E.K.; Apovian, C.; Fung, T.T.; Nunn, M.; Garcia, R.I. Overweight and Obesity Predict Time to Periodontal Disease Progression in Men. J. Clin. Periodontol. 2012, 39, 107–114. [Google Scholar] [CrossRef] [PubMed]
  87. Jimenez, M.; Hu, F.B.; Marino, M.; Li, Y.; Joshipura, K.J. Prospective Associations Between Measures of Adiposity and Periodontal Disease. Obesity 2012, 20, 1718–1725. [Google Scholar] [CrossRef] [PubMed]
  88. Zeigler, C.C.; Persson, G.R.; Wondimu, B.; Marcus, C.; Sobko, T.; Modéer, T. Microbiota in the oral subgingival biofilm is associated with obesity in adolescence. Obesity 2012, 20, 157–164. [Google Scholar] [CrossRef] [PubMed]
  89. Franchini, R.; Petri, A.; Migliario, M.; Rimondini, L. Poor oral hygiene and gingivitis are associated with obesity and overweight status in paediatric subjects. J. Clin. Periodontol. 2011, 38, 1021–1028. [Google Scholar] [CrossRef] [PubMed]
  90. Modéer, T.; Blomberg, C.; Wondimu, B.; Lindberg, T.Y.; Marcus, C. Association between obesity and periodontal risk indicators in adolescents. Int. J. Pediatr. Obes. 2011, 6, e264–e270. [Google Scholar] [CrossRef]
  91. Morita, I.; Okamoto, Y.; Yoshii, S.; Nakagaki, H.; Mizuno, K.; Sheiham, A.; Sabbah, W. Five-year incidence of periodontal disease is related to body mass index. J. Dent. Res. 2011, 90, 199–202. [Google Scholar] [CrossRef]
  92. Zuza, E.P.; Barroso, E.M.; Carrareto, A.L.V.; Pires, J.R.; Carlos, I.Z.; Theodoro, L.H.; Toledo, B.E.C. The role of obesity as a modifying factor in patients undergoing non-surgical periodontal therapy. J. Periodontol. 2011, 82, 676–682. [Google Scholar] [CrossRef]
  93. Morita, T.; Ogawa, Y.; Takada, K.; Nishinoue, N.; Sasaki, Y.; Motohashi, M.; Maeno, M. Association Between Periodontal Disease and Metabolic Syndrome. J. Public Health Dent. 2009, 69, 248–253. [Google Scholar] [CrossRef]
  94. Saxlin, T.; Suominen-Taipale, L.; Leiviskä, J.; Jula, A.; Knuuttila, M.; Ylöstalo, P. Role of serum cytokines tumour necrosis factor-alpha and interleukin-6 in the association between body weight and periodontal infection. J. Clin. Periodontol. 2009, 36, 100–105. [Google Scholar] [CrossRef]
  95. Wang, T.-T.; Chen, T.H.-H.; Wang, P.-E.; Lai, H.; Lo, M.-T.; Chen, P.Y.-C.; Chiu, S.Y.-H. A population-based study on the association between type 2 diabetes and periodontal disease in 12,123 middle-aged Taiwanese (KCIS No. 21). J. Clin. Periodontol. 2009, 36, 372–379. [Google Scholar] [CrossRef]
  96. D’Aiuto, F.; Sabbah, W.; Netuveli, G.; Donos, N.; Hingorani, A.D.; Deanfield, J.; Tsakos, G. Association of the Metabolic Syndrome with Severe Periodontitis in a Large U.S. Population-Based Survey. J. Clin. Endocrinol. Metab. 2008, 93, 3989–3994. [Google Scholar] [CrossRef]
  97. Saxlin, T.; Suominen-Taipale, L.; Kattainen, A.; Marniemi, J.; Knuuttila, M.; Ylöstalo, P. Association between serum lipid levels and periodontal infection. J. Clin. Periodontol. 2008, 35, 1040–1047. [Google Scholar] [CrossRef]
  98. Ylöstalo, P.; Suominen-Taipale, L.; Reunanen, A.; Knuuttila, M. Association between body weight and periodontal infection. J. Clin. Periodontol. 2008, 35, 297–304. [Google Scholar] [CrossRef]
  99. Shimazaki, Y.; Saito, T.; Yonemoto, K.; Kiyohara, Y.; Iida, M.; Yamashita, Y. Relationship of metabolic syndrome to periodontal disease in Japanese women: The Hisayama Study. J. Dent. Res. 2007, 86, 271–275. [Google Scholar] [CrossRef]
  100. Machado, A.C.P.; de Quirino, M.R.S.; Nascimento, L.F.C. Relation between chronic periodontal disease and plasmatic levels of triglycerides, total cholesterol and fractions. Braz. Oral. Res. 2005, 19, 284–289. [Google Scholar] [CrossRef]
  101. Caracho, R.A.; Foratori-Junior, G.A.; Fusco, N.D.S.; Jesuino, B.G.; Missio, A.L.T.; Sales-Peres, S.H. de C. Systemic conditions and oral health-related quality of life of pregnant women of normal weight and who are overweight. Int. Dent. J. 2020, 70, 287–295. [Google Scholar] [CrossRef]
  102. Foratori-Junior, G.A.; da Silva, B.M.; da Silva Pinto, A.C.; Honório, H.M.; Groppo, F.C.; de Carvalho Sales-Peres, S.H. Systemic and periodontal conditions of overweight/obese patients during pregnancy and after delivery: A prospective cohort. Clin. Oral Investig. 2020, 24, 157–165. [Google Scholar] [CrossRef]
  103. Fusco, N.D.S.; Foratori-Junior, G.A.; Missio, A.L.T.; Jesuino, B.G.; Sales-Peres, S.H. de C. Systemic and oral conditions of pregnant women with excessive weight assisted in a private health system. Int. Dent. J. 2019, 69, 472–479. [Google Scholar] [CrossRef]
  104. Kim, Y.-S.; Kim, J.-H. Body mass index and oral health status in Korean adults: The Fifth Korea National Health and Nutrition Examination Survey. Int. J. Dent. Hyg. 2017, 15, 172–178. [Google Scholar] [CrossRef]
  105. Martinez-Herrera, M.; Silvestre, F.J.; Silvestre-Rangil, J.; Bañuls, C.; Rocha, M.; Hernández-Mijares, A. Involvement of insulin resistance in normoglycaemic obese patients with periodontitis: A cross-sectional study. J. Clin. Periodontol. 2017, 44, 981–988. [Google Scholar] [CrossRef]
  106. Nascimento, G.G.; Peres, K.G.; Mittinty, M.N.; Mejia, G.C.; Silva, D.A.; Gonzalez-Chica, D.; Peres, M.A. Obesity and Periodontal Outcomes: A Population-Based Cohort Study in Brazil. J. Periodontol. 2017, 88, 50–58. [Google Scholar] [CrossRef]
  107. Al Habashneh, R.; Azar, W.; Shaweesh, A.; Khader, Y. The relationship between body mass index and periodontitis among postmenopausal women. Obes. Res. Clin. Pract. 2016, 10, 15–23. [Google Scholar] [CrossRef]
  108. Balli, U.; Ongoz Dede, F.; Bozkurt Dogan, S.; Gulsoy, Z.; Sertoglu, E. Chemerin and interleukin-6 levels in obese individuals following periodontal treatment. Oral Dis. 2016, 22, 673–680. [Google Scholar] [CrossRef]
  109. Öngöz Dede, F.; Bozkurt Doğan, Ş.; Ballı, U.; Avcı, B.; Durmuşlar, M.C. The effect of initial periodontal treatment on plasma, gingival crevicular fluid and salivary levels of 8-hydroxy-deoxyguanosine in obesity. Arch. Oral Biol. 2016, 62, 80–85. [Google Scholar] [CrossRef]
  110. Bouaziz, W.; Davideau, J.-L.; Tenenbaum, H.; Huck, O. Adiposity Measurements and Non-Surgical Periodontal Therapy Outcomes. J. Periodontol. 2015, 86, 1030–1037. [Google Scholar] [CrossRef]
  111. Gonçalves, T.E.D.; Feres, M.; Zimmermann, G.S.; Faveri, M.; Figueiredo, L.C.; Braga, P.G.; Duarte, P.M. Effects of scaling and root planing on clinical response and serum levels of adipocytokines in patients with obesity and chronic periodontitis. J. Periodontol. 2015, 86, 53–61. [Google Scholar] [CrossRef]
  112. Peng, S.M.; McGrath, C.; Wong, H.M.; King, N.M. The relationship between oral hygiene status and obesity among preschool children in Hong Kong. Int. J. Dent. Hyg. 2014, 12, 62–66. [Google Scholar] [CrossRef]
  113. Nascimento, G.G.; Seerig, L.M.; Vargas-Ferreira, F.; Correa, F.O.B.; Leite, F.R.M.; Demarco, F.F. Are obesity and overweight associated with gingivitis occurrence in Brazilian schoolchildren? J. Clin. Periodontol. 2013, 40, 1072–1078. [Google Scholar] [CrossRef]
  114. Scorzetti, L.; Marcattili, D.; Pasini, M.; Mattei, A.; Marchetti, E.; Marzo, G. Association between obesity and periodontal disease in children. Eur. J. Paediatr. Dent. 2013, 14, 181–184. [Google Scholar]
  115. Benguigui, C.; Bongard, V.; Ruidavets, J.-B.; Sixou, M.; Chamontin, B.; Ferrières, J.; Amar, J. Evaluation of oral health related to body mass index. Oral Dis. 2012, 18, 748–755. [Google Scholar] [CrossRef]
  116. Kim, E.-J.; Jin, B.-H.; Bae, K.-H. Periodontitis and obesity: A study of the Fourth Korean National Health and Nutrition Examination Survey. J. Periodontol. 2011, 82, 533–542. [Google Scholar] [CrossRef]
  117. Modéer, T.; Blomberg, C.C.; Wondimu, B.; Julihn, A.; Marcus, C. Association between obesity, flow rate of whole saliva, and dental caries in adolescents. Obesity 2010, 18, 2367–2373. [Google Scholar] [CrossRef]
  118. Shimazaki, Y.; Egami, Y.; Matsubara, T.; Koike, G.; Akifusa, S.; Jingu, S.; Yamashita, Y. Relationship between obesity and physical fitness and periodontitis. J. Periodontol. 2010, 81, 1124–1131. [Google Scholar] [CrossRef]
  119. Li, P.; He, L.; Sha, Y.-Q.; Luan, Q.-X. Relationship of metabolic syndrome to chronic periodontitis. J. Periodontol. 2009, 80, 541–549. [Google Scholar] [CrossRef]
  120. Pitiphat, W.; Savetsilp, W.; Wara-Aswapati, N. C-reactive protein associated with periodontitis in a Thai population. J. Clin. Periodontol. 2008, 35, 120–125. [Google Scholar] [CrossRef]
  121. Saito, T. Obesity may be Associated with Periodontitis in Elderly Men. J. Evid. Based Dent. Pract. 2008, 8, 97–98. [Google Scholar] [CrossRef]
  122. Saito, T.; Yamaguchi, N.; Shimazaki, Y.; Hayashida, H.; Yonemoto, K.; Doi, Y.; Kiyohara, Y.; Iida, M.; Yamashita, Y. Serum levels of resistin and adiponectin in women with periodontitis: The Hisayama study. J. Dent. Res. 2008, 87, 319–322. [Google Scholar] [CrossRef]
  123. Wood, N.; Johnson, R.B. The relationship between smoking history, periodontal screening and recording (PSR) codes and overweight/obesity in a Mississippi dental school population. Oral Health Prev. Dent. 2008, 6, 67–74. [Google Scholar]
  124. Alabdulkarim, M.; Bissada, N.; Al-Zahrani, M.; Ficara, A.; Siegel, B. Alveolar bone loss in obese subjects. J. Int. Acad. Periodontol. 2005, 7, 34–38. [Google Scholar]
  125. Chapper, A.; Munch, A.; Schermann, C.; Piacentini, C.C.; Fasolo, M.T.M. Obesity and periodontal disease in diabetic pregnant women. Braz. Oral Res. 2005, 19, 83–87. [Google Scholar] [CrossRef]
  126. Nishida, N.; Tanaka, M.; Hayashi, N.; Nagata, H.; Takeshita, T.; Nakayama, K.; Morimoto, K.; Shizukuishi, S. Determination of smoking and obesity as periodontitis risks using the classification and regression tree method. J. Periodontol. 2005, 76, 923–928. [Google Scholar] [CrossRef]
  127. Socransky, S.S.; Haffajee, A.D. Periodontal microbial ecology. Periodontology 2005, 38, 135–187. [Google Scholar] [CrossRef]
  128. Lundin, M.; Yucel-Lindberg, T.; Dahllöf, G.; Marcus, C.; Modéer, T. Correlation between TNFalpha in gingival crevicular fluid and body mass index in obese subjects. Acta Odontol. Scand. 2004, 62, 273–277. [Google Scholar] [CrossRef]
  129. Buhlin, K.; Gustafsson, A.; Pockley, A.G.; Frostegård, J.; Klinge, B. Risk factors for cardiovascular disease in patients with periodontitis. Eur. Heart J. 2003, 24, 2099–2107. [Google Scholar] [CrossRef]
  130. Suvan, J.E.; Finer, N.; D’Aiuto, F. Periodontal complications with obesity. Periodontology 2018, 78, 98–128. [Google Scholar] [CrossRef]
  131. Amar, S.; Zhou, Q.; Shaik-Dasthagirisaheb, Y.; Leeman, S. Diet-induced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proc. Natl. Acad. Sci. USA 2007, 104, 20466–20471. [Google Scholar] [CrossRef]
  132. Maciel, S.S.; Feres, M.; Gonçalves, T.E.D.; Zimmermann, G.S.; da Silva, H.D.P.; Figueiredo, L.C.; Duarte, P.M. Does obesity influence the subgingival microbiota composition in periodontal health and disease? J. Clin. Periodontol. 2016, 43, 1003–1012. [Google Scholar] [CrossRef] [PubMed]
  133. Falagas, M.E.; Kompoti, M. Obesity and infection. Lancet Infect. Dis. 2006, 6, 438–446. [Google Scholar] [CrossRef] [PubMed]
  134. Chen, T.-P.; Yu, H.-C.; Lin, T.-H.; Wang, Y.-H.; Chang, Y.-C. Association between obesity and chronic periodontitis. Medicine 2021, 100, e27506. [Google Scholar] [CrossRef] [PubMed]
  135. Moher, D. The problem of duplicate systematic reviews. BMJ 2013, 347, f5040. [Google Scholar] [CrossRef] [PubMed]
  136. Mizia, S.; Felińczak, A.; Włodarek, D.; Syrkiewicz-Świtała, M. Evaluation of Eating Habits and Their Impact on Health among Adolescents and Young Adults: A Cross-Sectional Study. Int. J. Environ. Res. Public Health 2021, 18, 3996. [Google Scholar] [CrossRef]
  137. Bogaard, L. Parent Influences on the Dietary Habits of Young Adults. Berkeley Undergr. J. 2023, 37, 1–14. [Google Scholar] [CrossRef]
  138. Mao, L.; Xu, J.; Zou, J. Effects of follicle-stimulating hormone on fat metabolism and cognitive impairment in women during menopause. Front. Physiol. 2022, 13, 1043237. [Google Scholar] [CrossRef] [PubMed]
  139. Palla, G.; Ramírez-Morán, C.; Montt-Guevara, M.M.; Salazar-Pousada, D.; Shortrede, J.; Simoncini, T.; Grijalva-Grijalva, I.; Pérez-López, F.R.; Chedraui, P. Perimenopause, body fat, metabolism and menopausal symptoms in relation to serum markers of adiposity, inflammation and digestive metabolism. J. Endocrinol. Investig. 2020, 43, 809–820. [Google Scholar] [CrossRef] [PubMed]
  140. Williams, C.M. Lipid metabolism in women. Proc. Nutr. Soc. 2004, 63, 153–160. [Google Scholar] [CrossRef]
  141. Ferretti, F.; Mariani, M.; Sarti, E. Is the development of obesogenic food environments a self-reinforcing process? Evidence from soft drink consumption. Glob. Health 2021, 17, 91. [Google Scholar] [CrossRef] [PubMed]
Figure 1. PRISMA diagram showing the process of inclusion and exclusion of studies.
Figure 1. PRISMA diagram showing the process of inclusion and exclusion of studies.
Medicina 60 00621 g001
Table 1. Database search strategy.
Table 1. Database search strategy.
DatabaseSearch StrategyNumber of Studies
Pubmed((“periodontitis”) OR (“periodontal disease”) OR (“furcation defect”) OR (“gingival disease”) OR (“gingivitis”) OR (“tooth loss”) OR (“tooth migration”) OR (“tooth mobility”) OR (“missing teeth”) OR (“periodontal inflammation”) OR (“gum disease”) OR (“gum inflammation”)) AND ((“Obesity”) OR (“overweight”) OR (“body weight”) OR (“body mass index”) OR (“abdominal fat”) OR (“obese”) OR (“BMI”)) AND ((“systematic review”) OR (“meta-analysis”))76
Cochrane database#1 MeSH descriptor: [Periodontal Diseases] explode all trees42
#2 MeSH descriptor: [Periodontitis] in all MeSH products
#3 MeSH descriptor: [Furcation Defects] explode all trees
#4 MeSH descriptor: [Gingival Diseases] explode all trees
#5 MeSH descriptor: [Gingivitis] explode all trees
#6 MeSH descriptor: [Tooth Loss] explode all trees
#7 MeSH descriptor: [Tooth Migration] explode all trees
#8 MeSH descriptor: [Tooth Mobility] explode all trees
#9 (“periodontitis”) OR (“periodontal disease”) OR (“furcation defect”) OR (“gingival disease”) OR (“gingivitis”) OR (“tooth loss”) OR (“tooth migration”) OR (“tooth mobility”) OR (“missing teeth”) OR (“periodontal inflammation”) OR (“gum disease”) OR (“gum inflammation”) (Word variations have been searched)
#10 #1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7 OR #8 OR #9
#11 MeSH descriptor: [Obesity] explode all trees
#12 MeSH descriptor: [Overweight] explode all trees
#13 MeSH descriptor: [Body Weight] explode all trees
#14 MeSH descriptor: [Body Mass Index] explode all trees
#15 MeSH descriptor: [Abdominal Fat] explode all trees
#16 (“obesity”) OR (“overweight”) OR (“body weight”) OR (“body mass index”) OR (“abdominal fat”) (Word variations have been searched) OR (“obese”) OR (“BMI”) (Word variations have been searched)
#17 #11 OR #12 OR #13 OR #14 OR #15 OR #16
#18 MeSH descriptor: [Systematic Reviews as Topic] explode all trees
#19 MeSH descriptor: [Meta-Analysis as Topic] explode all trees
#20 (“systematic review”) OR (“meta-analysis”) (Word variations have been searched)
#21 #18 OR #19 OR #20; #22 #10 AND #17 AND #21
Scielo((((“periodontitis”) OR (“periodontal disease”) OR (“furcation defect”) OR (“gingival disease”) OR (“gingivitis”) OR (“tooth loss”) OR (“tooth migration”) OR (“tooth mobility”) OR (“missing teeth”) OR (“periodontal inflammation”) OR (“gum disease”) OR (“gum inflammation”))) AND (((“Obesity”) OR (“overweight”) OR (“body weight”) OR (“body mass index”) OR (“abdominal fat”) OR (“obese”) OR (“BMI”)))) AND (((“systematic review”) OR (“meta-analysis”)))3
Scopus(TITLE-ABS-KEY (((“periodontitis”) OR (“periodontal disease”) OR (“furcation defect”) OR (“gingival disease”) OR (“gingivitis”) OR (“tooth loss”) OR (“tooth migration”) OR (“tooth mobility”) OR (“missing teeth”) OR (“periodontal inflammation”) OR (“gum disease”) OR (“gum inflammation”))) AND TITLE-ABS-KEY (((“Obesity”) OR (“overweight”) OR (“body weight”) OR (“body mass index”) OR (“abdominal fat”) OR (“obese”) OR (“BMI”))) AND TITLE-ABS-KEY (((“systematic review”) OR (“meta-analysis”)))) AND (LIMIT-TO (DOCTYPE, “re”) OR LIMIT-TO (DOCTYPE, “ar”)) AND (LIMIT-TO (PUBSTAGE, “final”)) AND (LIMIT-TO (SRCTYPE, “j”))174
Web of Science(TS=(“periodontitis”) OR TS=(“periodontal disease”) OR TS=(“furcation defect”) OR TS=(“gingival disease”) OR TS=(“gingivitis”) OR TS=(“tooth loss”) OR TS=(“tooth migration”) OR TS=(“tooth mobility”) OR TS=(“missing teeth”) OR TS=(“periodontal inflammation”) OR TS=(“gum disease”) OR TS=(“gum inflammation”)) AND (TS=(“obesity”) OR TS=(“overweight”) OR TS=(“body weight”) OR TS=(“body mass index”) OR TS=(“abdominal fat”) OR TS=(“obese”) OR TS=(“BMI”)) AND (TS=(“systematic review”) OR TS=(“meta-analysis”))79
Google Scholarallintitle: ((“periodontal disease”) OR (“periodontitis”)) + ((“Obesity”) OR (“overweight”)) + ((“systematic review”) OR (“meta-analysis”))22
Proquest Dissertations and Theses((“periodontal disease”) OR (“periodontitis”)) AND ((“Obesity”) OR (“overweight”)) AND ((“systematic review”) OR (“meta-analysis”)) AND NOT ((“cardiovascular”) OR (“obstructive sleep apnea”) OR (“cancer”) OR (“pregnant”) OR (“dementia”) OR (“in vitro”) OR (“dental caries”) OR (“fractures”) OR (“rat”) OR (“diabetes mellitus”) OR (“periodontal treatment”) OR (“pulpotomy”) OR (“treatment”))23
OpenGrey((“periodontitis”) OR (“periodontal disease”) OR (“furcation defect”) OR (“gingival disease”) OR (“gingivitis”) OR (“tooth loss”) OR (“tooth migration”) OR (“tooth mobility”) OR (“missing teeth”) OR (“periodontal inflammation”) OR (“gum disease”) OR (“gum inflammation”)) AND ((“Obesity”) OR (“overweight”) OR (“body weight”) OR (“body mass index”) OR (“abdominal fat”) OR (“obese”) OR (“BMI”)) AND ((“systematic review”) OR (“meta-analysis”))0
Table 2. Reason for exclusion of studies.
Table 2. Reason for exclusion of studies.
AuthorReason for Exclusion
Paranhos et al. [33]They associated obesity with periodontal treatment
Zhang et al. [34]
Joseph et al. [35]
Akram et al. [36]
Nascimento et al. [37]
Gerber et al. [38]
Papageorgiou et al. [39]
Deng et al. [40]They associated obesity with salivary biomarkers of PD
Akram et al. [41]
Table 3. Characteristics of included studies.
Table 3. Characteristics of included studies.
AuthorsYearStudy DesignCountryIncluded Study DesignNumber of Studies in the Qualitative AnalysisNumber of Studies in the Quantitative AnalysisOutcomesConclusions
Foratori-Junior et al. [42]2022SR with MABrazilCS, C, and CC1111GeneralRR = 2.21 (1.53–3.17)There is an association between overweight/obesity and periodontitis during pregnancy.
Kim et al. [46]2022SR with MASouth KoreaCS, C, and CC3729GeneralOR = 1.35 (1.05–1.75)A positive association was found between obesity and periodontitis regardless of country or age.
18–34 yearsOR = 2.21 (1.26–3.89)
35–54 yearsOR = 1.53 (1.17–2.00)
≥ 55 yearsOR = 1.82 (1.16–2.83)
United StatesOR = 0.59 (0.19–1.65)
BrazilOR = 1.70 (0.78–3.72)
European countriesOR = 2.46 (1.11–5.46)
KoreaOR = 1.34 (1.00–1.80)
JapanOR = 1.75 (1.48–2.06)
Other Asian countriesOR = 0.98 (0.49–1.95)
Abu-Shawish et al. [47]2022SRQatarCS, C, and CC150GeneralOR = 1.77–3.25This SR found a positive association between obesity in terms of increased BMI and periodontitis in adults.
RR = 1.64–1.84
Khairunnisa et al. [48]2021SR with MAIndonesiaCS1111GeneralOR = 1.23 (1.15–1.33)Obesity increases periodontitis in adults.
da Silva et al. [43]2021SR with MABrazilCS, CT, C, and CC9090ObeseSMD = 0.05 (−0.20–0.29)Higher measures of gingival inflammation can be expected for those with higher BMI.
OverweightSMD = 0.30 (−0.03–0.62)
Overweight or obeseSMD = 0.20 (−0.09–0.48)
BOP (obese)SMD = 0.03 (−0.23–0.28)
BOP (Overweight)SMD = 0.13 (−0.04–0.30)
BOP (Overweight or obese)SMD = 0.20 (−0.05–0.45)
GI (obese)SMD = 0.35 (−0.21–0.91)
GI (Overweigh)SMD = 0.97 (0.45–1.49)
GI (Overweight or obese)SMD = 0.22 (−0.24–0.68)
Obese—GSMD = 1.10 (0.14–2.05)
Overweight—GSMD = 2.08 (−0.60–4.77)
Overweight or obese—GSMD = 2.91 (−0.89–6.72)
BOP (obese)—GSMD = 0.64 (−0.37–1.65)
BOP (Overweight)—GSMD = 0.78 (0.52–1.03)
BOP (Overweight or obese)—GSMD = 1.02 (0.77–1.27)
GI (obese)—GSMD = 2.13 (−1.51–5.77)
GI (Overweight)—GSMD = 3.52 (2.32–4.71)
GI (Overweight or obese)—GSMD = 4.91 (3.64–6.17)
Khan et al. [49]2018SRAustraliaCS, C, and CC250GeneralOR = 1.1–4.5There was evidence to suggest that obesity is associated with periodontitis in adolescents and young adults.
Martens et al. [50]2017SR with MABelgiumCS, C, and CC127GeneralOR = 1.46 (1.20–1.77)The available evidence suggests a significantly positive association between periodontal disease and obesity in children.
Martinez-Herrera et al. [51]2017SRSpainC, CC, and CT280GeneralOR = 0.99–4.3The association between obesity and periodontitis was consistent with a compelling pattern of increased risk of periodontitis in overweight or obese individuals.
HR = 1.03–3.24
RR = 0.99–5.4
Nascimento et al. [44]2015SR with MABrazilO55OverweightRR = 1.13 (1.06–1.20)A clear positive association between weight gain and new cases of periodontitis was found.
ObeseRR = 1.34 (1.21–1.47)
Keller et al. [52]2015SRDenmarkC and CT130Age (obese)HR = 1.30–3.24Overweight and obesity can be risk factors for the development or worsening of periodontal health.
IRR = 1.3
PR = 1.01
Age (overweight)HR = 1.09–1.70
IRR = 1.2
PR = 0.99
Li et al. [53]2015SR with MAChinaCS and CC165PI > 25%OR = 4.75 (2.42–9.34)Obesity is associated with some signs of periodontal disease in children and adolescents.
BOP > 25%OR = 5.41 (2.75–10.63)
SBCOR = 3.07 (1.10–8.62)
SPCOR = 1.08 (0.60–1.94)
PD > 4 mmOR = 14.15 (5.10–39.25)
de Moura-Grec et al. [45]2014SR with MABrazilCS3131GeneralOR = 1.30 (1.25–1.35)Obesity was associated with periodontitis; however, the risk factors that aggravate these diseases should be better clarified to elucidate the direction of this association.
Suvan et al. [54]2011SR with MAUnited KingdomCS, C, and CC3319ObeseOR = 1.81 (1.42–2.30)These results support an association between BMI overweight and obesity and periodontitis although the magnitude is unclear.
OverweightOR = 1.27 (1.06–1.51)
Overweight and obeseOR = 2.13 (1.40–3.26)
Chaffee et al. [55]2010SR with MAUnited StatesO7028GeneralOR = 1.35 (1.23–1.47)There is a positive association between periodontal disease and obesity, which was consistent and coherent with a biologically plausible role of obesity in the development of periodontal disease.
ObeseOR = 1.52 (1.26–1.83)
OverweightOR = 1.18 (1.00–1.39)
East AsiaOR = 1.32 (1.19–1.47)
Europe and Middle EastOR = 1.87 (1.17–2.99)
United StatesOR = 1.30 (1.16–1.46)
MenOR = 1.50 (1.27–1.77)
WomenOR = 1.75 (1.26–2.43)
YoungOR = 1.35 (1.14–1.59)
OlderOR = 1.21 (1.04–1.41)
SmokerOR = 1.36 (0.98–1.88)
Non-smokerOR = 2.08 (1.29–3.36)
SR = systematic review; MA = meta-analysis; O = observational study; CT = clinical trial; CS = cross-sectional; C = cohort; CC = case and control; BMI = body mass index; G = gingivitis; BOP = bleeding on probing; PD = probing depth; PI = plaque index; GI = gingival index; SBC = subgingival calculus; SPC = supragingival calculus; OR = odds ratio; RR = risk/rate ratio; HR = hazard ratio; PR = prevalence ratio; IRR = incidence risk ratio.
Table 4. Assessment of the methodological quality and the quality of the evidence of the included studies.
Table 4. Assessment of the methodological quality and the quality of the evidence of the included studies.
AuthorsYearAMSTAR-2Overall Confidence
12 *34 *567 *89 *1011 *1213 *1415 *16
Foratori-Junior et al. [42]2022YesYesYesYesYesYesYesYesYesYesYesYesYesYesYesYesHigh
Kim et al. [46]2022YesYesYesYes partialYesYesYes partialYesYesYesYesYesYesYesYesYesHigh
Abu-Shawish et al. [47]2022YesYesYesYes partialYesYesNoYesYesYesNo meta-analysisYesYesNo meta-analysisYesLow
Khairunnisa et al. [48]2021YesYes partialYesYes partialNoNoYes partialNoYes partialYesYesNoNoNoYesYesLow
da Silva et al. [43]2021YesYes partialYesYes partialYesYesYesYesYesYesYesYesYesYesYesYesHigh
Khan et al. [49]2018YesYesYesYes partialYesYesYes partialYesYesYesNo meta-analysisYesYesNo meta-analysisYesHigh
Martens et al. [50]2017YesYes partialYesYesYesYesNoYesYes partialYesYesYesYesYesYesYesLow
Martinez-Herrera et al. [51]2017YesYes partialYesYes partialNoNoNoYesNoNoNo meta-analysisNoNoNo meta-analysisYesCritically low
Nascimento et al. [44]2015YesYes partialYesYes partialYesYesYesYesYesYesYesYesYesYesYesYesHigh
Keller et al. [52]2015YesYes partialYesYes partialYesYesYesYesYes partialYesNo meta-analysisYesYesNo meta-analysisYesHigh
Li et al. [53]2015YesYes partialYesYes partialYesYesYes partialYesYes partialYesYesYesYesYesYesYesHigh
de Moura-Grec et al. [45]2014YesYes partialYesYes partialYesYesYes partialYesNoYesYesYesYesYesYesNoLow
Suvan et al. [54]2011YesYes partialYesYesYesYesYes partialYesYesYesYesYesYesYesYesYesHigh
Chaffee et al. [55]2010YesYes partialYesYesYesYesYes partialYesYes partialYesYesYesYesYesYesYesHigh
AMSTAR = A MeaSurement Tool to Assess Systemic Reviews. 1 = Did the research questions and inclusion criteria for the review include the components of PICO? 2 = Did the report of the review contain an explicit statement that the review methods were established prior to the conduct of the review and did the report justify any significant deviations from the protocol? 3 = Did the review authors explain their selection of the study designs for inclusion in the review? 4 = Did the review authors use a comprehensive literature search strategy? 5 = Did the review authors perform study selection in duplicate? 6 = Did the review authors perform data extraction in duplicate? 7 = Did the review authors provide a list of excluded studies and justify the exclusions? 8 = Did the review authors describe the included studies in adequate detail? 9 = Did the review authors use a satisfactory technique for assessing the risk of bias (RoB) in individual studies that were included in the review? 10 = Did the review authors report on the sources of funding for the studies included in the review? 11 = If meta-analysis was performed, did the review authors use appropriate methods for statistical combination of results? 12 = If meta-analysis was performed, did the review authors assess the potential impact of RoB in individual studies on the results of the meta-analysis or other evidence synthesis? 13 = Did the review authors account for RoB in primary studies when interpreting/discussing the results of the review? 14 = Did the review authors provide a satisfactory explanation for, and discussion of, any heterogeneity observed in the results of the review? 15 = If they performed quantitative synthesis, did the review authors carry out an adequate investigation of publication bias (small study bias) and discuss its likely impact on the results of the review? 16 = Did the review authors report any potential sources of conflict of interest, including any funding they received for conducting the review? * = Critical domain.
Table 5. Overlapping of primary studies in systematic reviews.
Table 5. Overlapping of primary studies in systematic reviews.
Primary StudiesSystematic Reviews That Included the Primary StudiesTimes That Primary Studies Were Included
Khader et al. [56]Kim et al. [46], Abu-Shawish et al. [47], Khairunnisa et al. [48], da Silva et al. [43], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]7
Kongstad et al. [57]Kim et al. [46], Khairunnisa et al. [48], Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]6
Ekuni et al. [58]Kim et al. [46], Khairunnisa et al. [48], Khan et al. [49], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]6
Dalla Vecchia et al. [59]Kim et al. [46], Abu-Shawish et al. [47], Khairunnisa et al. [48], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]6
Al-Zahrani et al. [60]Kim et al. [46], Khan et al. [49], Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]6
Pataro et al. [61]Kim et al. [46], Abu-Shawish et al. [47], Khairunnisa et al. [48], da Silva et al. [43], Martínez-Herrera et al. [51]5
Han et al. [62]Kim et al. [46], Khairunnisa et al. [48], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]5
Saxlin et al. [63]Kim et al. [46], Martínez-Herrera et al. [51], Nascimento et al. [44], Keller et al. [52], de Moura-Grec et al. [45]5
Haffajee et al. [64]Kim et al. [46], da Silva et al. [43], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]5
Linden et al. [65]Abu-Shawish et al. [47], Martínez-Herrera et al. [51], Keller et al. [52], Suvan et al. [54], Chaffee et al. [55]5
Wood et al. [28]Khan et al. [49], Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]5
Saito et al. [66]Kim et al. [46], Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]5
Ekuni et al. [67]da Silva et al. [43], Martínez-Herrera et al. [51], Nascimento et al. [44], Keller et al. [52]4
Amin et al. [68]Abu-Shawish et al. [47], da Silva et al. [43], Khan et al. [49], Chaffee et al. [55]4
Dumitrescu et al. [69]Kim et al. [46], da Silva et al. [43], de Moura-Grec et al. [45], Chaffee et al. [55]4
Furuta et al. [70]Kim et al. [46], Khan et al. [49], de Moura-Grec et al. [45], Chaffee et al. [55]4
Kumar et al. [71]Kim et al. [46], Khairunnisa et al. [48], de Moura-Grec et al. [45], Chaffee et al. [55]4
Kushiyama et al. [72]Kim et al. [46], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]4
Sarlati et al. [73]Abu-Shawish et al. [47], Khan et al. [49], Suvan et al. [54], Chaffee et al. [55]4
Borges-Yañez et al. [74]Kim et al. [46], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]4
Reeves et al. [75]Khan et al. [49], Martens et al. [50], Li et al. [53], Chaffee et al. [55]4
Genco et al. [76]Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]4
Saito et al. [77]Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]4
Torrungruang et al. [78]Kim et al. [46], de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]4
Gulati et al. [79]Kim et al. [46], Khairunnisa et al. [48], da Silva et al. [43]3
Buduneli et al. [80]Abu-Shawish et al. [47], da Silva et al. [43], Martínez-Herrera et al. [51]3
Fadel et al. [81]Khan et al. [49], Martens et al. [50], Li et al. [53]3
Suvan et al. [22]da Silva et al. [43], Martínez-Herrera et al. [51], Keller et al. [52]3
Altay et al. [82]da Silva et al. [43], Martínez-Herrera et al. [51], Keller et al. [52]3
Irigoyen-Camacho et al. [83]Khan et al. [49], Martens et al. [50], Li et al. [53]3
Al-Zahrani et al. [84]da Silva et al. [43], Martínez-Herrera et al. [51], Keller et al. [52]3
de Castilhos et al. [85]da Silva et al. [43], Khan et al. [49], Keller et al. [52]3
Gorman et al. [86]Martínez-Herrera et al. [51], Nascimento et al. [44], Keller et al. [52]3
Jimenez et al. [87]Martínez-Herrera et al. [51], Nascimento et al. [44], Keller et al. [52]3
Zeigler et al. [88]Khan et al. [49], Martens et al. [50], Li et al. [53]3
Franchini et al. [89]Khan et al. [49], Martens et al. [50], Li et al. [53]3
Modéer et al. [90]Khan et al. [49], Martens et al. [50], Li et al. [53]3
Morita et al. [91]Martínez-Herrera et al. [51], Nascimento et al. [44], Keller et al. [52]3
Zuza et al. [92]da Silva et al. [43], Martínez-Herrera et al. [51], Keller et al. [52]3
Morita et al. [93]Kim et al. [46], de Moura-Grec et al. [45], Chaffee et al. [55]3
Saxlin et al. [94]Kim et al. [46], de Moura-Grec et al. [45], Chaffee et al. [55]3
Wang et al. [95]Martínez-Herrera et al. [51], Suvan et al. [54], Chaffee et al. [55]3
D’aiuto et al. [96]Kim et al. [46], de Moura-Grec et al. [45], Chaffee et al. [55]3
Saxlin et al. [97]Martínez-Herrera et al. [51], de Moura-Grec et al. [45], Chaffee et al. [55]3
Ylöstalo et al. [98]Martínez-Herrera et al. [51], Suvan et al. [54], Chaffee et al. [55]3
Shimazaki et al. [99]de Moura-Grec et al. [45], Suvan et al. [54], Chaffee et al. [55]3
Machado et al. [100]Kim et al. [46], de Moura-Grec et al. [45], Chaffee et al. [55]3
Caracho et al. [101]Foratori-Junior et al. [42], da Silva et al. [43]2
Foratori-Junior et al. [102]Foratori-Junior et al. [42], da Silva et al. [43]2
Fusco et al. [103]Foratori-Junior et al. [42], da Silva et al. [43]2
Deshpande et al. [19]Abu-Shawish et al. [47], da Silva et al. [43]2
Kim et al. [104]Kim et al. [46], Khairunnisa et al. [48]2
Martínez-Herrera et al. [105]Kim et al. [46], da Silva et al. [43]2
Nascimento et al. [106]Abu-Shawish et al. [47], da Silva et al. [43]2
Al Habashneh et al. [107]Kim et al. [46], da Silva et al. [43]2
Balli et al. [108]da Silva et al. [43], Martínez-Herrera et al. [51]2
Öngöz Dede et al. [109]da Silva et al. [43], Martínez-Herrera et al. [51]2
Bouaziz et al. [110]da Silva et al. [43], Martínez-Herrera et al. [51]2
Gonçalves et al. [111]da Silva et al. [43], Martínez-Herrera et al. [51]2
Peng et al. [112]Martens et al. [50], Li et al. [53]2
Nascimento et al. [113]Martens et al. [50], Li et al. [53]2
Scorzetti et al. [114]Martens et al. [50], Li et al. [53]2
Benguigui et al. [115]Kim et al. [46], da Silva et al. [43]2
Kim et al. [116]Khairunnisa et al. [48], Martínez-Herrera et al. [51]2
Modéer et al. [117]Martens et al. [50], Li et al. [53]2
Shimazaki et al. [118]Kim et al. [46], Chaffee et al. [55]2
Li et al. [119]Kim et al. [46], de Moura-Grec et al. [45]2
Pitiphat et al. [120]de Moura-Grec et al. [45], Chaffee et al. [55]2
Saito [121]Kim et al. [46], de Moura-Grec et al. [45]2
Saito et al. [122]Suvan et al. [54], Chaffee et al. [55]2
Wood et al. [123]de Moura-Grec et al. [45], Chaffee et al. [55]2
Alabdulkarin et al. [124]Suvan et al. [54], Chaffee et al. [55]2
Chapper et al. [125]Suvan et al. [54], Chaffee et al. [55]2
Nishida et al. [126]Suvan et al. [54], Chaffee et al. [55]2
Socransky et al. [127]Suvan et al. [54], Chaffee et al. [55]2
Lundin et al. [128]Khan et al. [49], de Moura-Grec et al. [45]2
Buhlin et al. [129]Suvan et al. [54], Chaffee et al. [55]2
Table 6. Synthesis of the results of the included studies.
Table 6. Synthesis of the results of the included studies.
AuthorsOutcomeAssociation
Foratori-Junior et al. [42]GeneralRR = 2.21 (1.53–3.17)Yes
Kim et al. [46]GeneralOR = 2.21 (1.26–3.89)Yes
18–34 yearsOR = 1.35 (1.05–1.75)Yes
35–54 yearsOR = 1.53 (1.17–2.00)Yes
≥55 yearsOR = 1.82 (1.16–2.83)Yes
United StatesOR = 0.59 (0.19–1.65)No
BrazilOR = 1.70 (0.78–3.72)No
European countriesOR = 2.46 (1.11–5.46)Yes
KoreaOR = 1.34 (1.00–1.80)Yes
JapanOR = 1.75 (1.48–2.06)Yes
Other Asian countriesOR = 0.98 (0.49–1.95)No
Abu-Shawish et al. [47]GeneralOR = 1.77–3.25Yes
RR = 1.64–1.84Yes
Khairunnisa et al. [48]GeneralOR = 1.23 (1.15–1.33)Yes
da Silva et al. [43]ObeseSMD = 0.05 (−0.20–0.29)No
OverweightSMD = 0.30 (−0.03–0.62)No
Overweight or obeseSMD = 0.20 (−0.09–0.48)No
BOP (obese)SMD = 0.03 (−0.23–0.28)No
BOP (Overweight)SMD = 0.13 (−0.04–0.30)No
BOP (Overweight or obese)SMD = 0.20 (−0.05–0.45)No
GI (obese)SMD = 0.35 (−0.21–0.91)No
GI (Overweight)SMD = 0.97 (0.45–1.49)Yes
GI (Overweight or obese)SMD = 0.22 (−0.24–0.68)No
Obese—GSMD = 1.10 (0.14–2.05)Yes
Overweight—GSMD = 2.08 (−0.60–4.77)No
Overweight or obese—GSMD = 2.91 (−0.89–6.72)No
BOP (obese)—GSMD = 0.64 (−0.37–1.65)No
BOP (Overweight)—GSMD = 0.78 (0.52–1.03)Yes
BOP (Overweight or obese)—GSMD = 1.02 (0.77–1.27)Yes
GI (obese)—GSMD = 2.13 (−1.51–5.77)No
GI (Overweight)—GSMD = 3.52 (2.32–4.71)Yes
GI (Overweight or obese)—GSMD = 4.91 (3.64–6.17)Yes
Khan et al. [49]GeneralOR = 1.1–4.5Yes
Martens et al. [50]GeneralOR = 1.46 (1.20–1.77)Yes
Martinez-Herrera et al. [51]GeneralOR = 0.99–4.3Yes
HR = 1.03–3.24Yes
RR = 0.99–5.4Yes
Nascimento et al. [44]OverweightRR = 1.13 (1.06–1.20)Yes
ObeseRR = 1.34 (1.21–1.47)Yes
Keller et al. [52]Age (obese)HR = 1.30–3.24Yes
IRR = 1.3Yes
PR = 1.01Yes
Age (overweight)HR = 1.09–1.70Yes
IRR = 1.2Yes
PR = 0.99Yes
Li et al. [53]PI > 25%OR = 4.75 (2.42–9.34)Yes
BOP > 25%OR = 5.41 (2.75–10.63)Yes
SBCOR = 3.07 (1.10–8.62)Yes
SPCOR = 1.08 (0.60–1.94)No
PD > 4 mmOR = 14.15 (5.10–39.25)Yes
de Moura-Grec et al. [45]GeneralOR = 1.30 (1.25–1.35)Yes
Suvan et al. [54]ObeseOR = 1.30 (1.25–1.35)Yes
OverweightOR = 1.81 (1.42–2.30)Yes
Overweight and obeseOR = 1.27 (1.06–1.51)Yes
Chaffee et al. [55]GeneralOR = 1.35 (1.23–1.47)Yes
ObeseOR = 1.52 (1.26–1 83)Yes
OverweightOR = 1.18 (1.00–1.39)Yes
East AsiaOR = 1.32 (1.19–1.47)Yes
Europe and Middle EastOR = 1.87 (1.17–2.99)Yes
United StatesOR = 1.30 (1.16–1.46)Yes
MenOR = 1.50 (1.27–1.77)Yes
WomenOR = 1.75 (1.26–2.43)Yes
YoungOR = 1.35 (1.14–1.59)Yes
OlderOR = 1.21 (1.04–1.41)Yes
SmokerOR = 1.36 (0.98–1.88)No
Non-smokerOR = 2.08 (1.29–3.36)Yes
G = gingivitis; BOP = bleeding on probing; PD = probing depth; PI = plaque index; GI = gingival index; SBC = subgingival calculus; SPC = supragingival calculus; OR = odds ratio; RR = risk/rate ratio; HR = hazard ratio; PR = prevalence ratio; IRR = incidence risk ratio.
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Arbildo-Vega, H.I.; Cruzado-Oliva, F.H.; Coronel-Zubiate, F.T.; Aguirre-Ipenza, R.; Meza-Málaga, J.M.; Luján-Valencia, S.A.; Luján-Urviola, E.; Farje-Gallardo, C.A. Association between Periodontal Disease and Obesity: Umbrella Review. Medicina 2024, 60, 621. https://doi.org/10.3390/medicina60040621

AMA Style

Arbildo-Vega HI, Cruzado-Oliva FH, Coronel-Zubiate FT, Aguirre-Ipenza R, Meza-Málaga JM, Luján-Valencia SA, Luján-Urviola E, Farje-Gallardo CA. Association between Periodontal Disease and Obesity: Umbrella Review. Medicina. 2024; 60(4):621. https://doi.org/10.3390/medicina60040621

Chicago/Turabian Style

Arbildo-Vega, Heber Isac, Fredy Hugo Cruzado-Oliva, Franz Tito Coronel-Zubiate, Rubén Aguirre-Ipenza, Joan Manuel Meza-Málaga, Sara Antonieta Luján-Valencia, Eduardo Luján-Urviola, and Carlos Alberto Farje-Gallardo. 2024. "Association between Periodontal Disease and Obesity: Umbrella Review" Medicina 60, no. 4: 621. https://doi.org/10.3390/medicina60040621

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