Next Article in Journal
Hemodynamic Response, Coughing and Incidence of Cerebrospinal Fluid Leakage on Awakening with an Endotracheal Tube or Laryngeal Mask Airway in Place after Transsphenoidal Pituitary Surgery: A Randomized Clinical Trial
Next Article in Special Issue
Comparison of the Effect of Oral Versus Intravenous Bisphosphonate Administration on Osteoclastogenesis in Advanced-Stage Medication-Related Osteonecrosis of the Jaw Patients
Previous Article in Journal
MDSC in Mice and Men: Mechanisms of Immunosuppression in Cancer
Previous Article in Special Issue
Analysing Complex Oral Protein Samples: Complete Workflow and Case Analysis of Salivary Pellicles
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JCM
Volume 10
Issue 13
10.3390/jcm10132873
jcm-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-Analysis

by
Cornelia Melinda Adi Santoso
1,2,
Fera Ketti
1,
Taufan Bramantoro
3,
Judit Zsuga
1 and
Attila Nagy
1,*
1
Faculty of Public Health, University of Debrecen, 4028 Debrecen, Hungary
2
Doctoral School of Health Sciences, University of Debrecen, 4028 Debrecen, Hungary
3
Department of Dental Public Health, Universitas Airlangga, Surabaya 60286, Indonesia
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2021, 10(13), 2873; https://doi.org/10.3390/jcm10132873
Submission received: 25 April 2021 / Revised: 14 June 2021 / Accepted: 18 June 2021 / Published: 28 June 2021
(This article belongs to the Special Issue Oral Conditions and Dental Behavior in Patients with Systemic Diseases)
Browse Figures
Versions Notes

Abstract

:
Emerging evidence has linked poor oral hygiene to metabolic syndrome (MetS), but previously, no summary of evidence has been conducted on the topic. This systematic review and meta-analysis aims to evaluate the associations of oral hygiene status and care with MetS. A systematic search of the PubMed and Web of Science databases from inception to 17 March 2021, and examination of reference lists was conducted to identify eligible observational studies. A random-effects model was applied to pool the effects of oral hygiene status and care on MetS. Thirteen studies met the inclusion criteria and had sufficient methodological quality. Good oral hygiene status (OR = 0.30 (0.13–0.66); I2 = 91%), frequent tooth brushing (OR = 0.68 (0.58–0.80); I2 = 89%), and frequent interdental cleaning (OR = 0.89 (0.81–0.99); I2 = 27%) were associated with a lower risk of MetS. Only one study examined the association between dental visits and MetS (OR = 1.10 (0.77–1.55)). Our findings suggested that there might be inverse associations of oral hygiene status, tooth-brushing frequency, and interdental cleaning with MetS. However, substantial heterogeneity for tooth-brushing frequency and inconsistent results for oral hygiene status in subgroup analyses were observed. There was insufficient evidence for the association between dental visits and MetS. Further longitudinal studies are needed to investigate these associations.

1. Introduction

Metabolic syndrome (MetS), a clustering of abdominal obesity, hyperglycemia, hypertension, and dyslipidemia, represents a growing public health concern globally [1]. Although the prevalence of MetS differs depending on diagnostic criteria, age group, and ethnicity [1,2], it is estimated to affect around 25% of the world population [2,3]. MetS raises the risk of type 2 diabetes mellitus (T2DM) and cardiovascular diseases [1] and is associated with a 20% increase in healthcare costs [4].
Several risk factors for MetS have been identified. Besides socioeconomic status (SES) [5], smoking [6], diet [7], and physical activity [8], oral diseases, such as periodontal diseases and dental caries, are associated with MetS [9,10,11]. The link between oral and systemic diseases is suggested due to common risk factors, subgingival biofilm harboring Gram-negative bacteria, and periodontium serving as a cytokine reservoir [12].
Poor oral hygiene is the primary cause of common oral diseases. Accumulation of dental plaque allows bacterial growth that may lead to inflamed periodontal tissues and eventually create bacteremia and systemic inflammation [13,14]. Invading bacteria from severe caries or endodontic infections is also thought to provoke similar mechanisms [10,15,16]. Chronic low-grade inflammation underlies the development of metabolic disorders [17,18], and a study found that systemic exposure to periodontal bacteria was associated with MetS [13].
Tooth brushing and interdental cleaning, which are the main forms of oral self-care, together with regular professional care, are important measures for plaque control or removal and maintaining optimal oral health [19,20,21]. Poor oral hygiene care is associated with low-grade inflammation [22], suggesting its potential link to MetS [23]. The association of poor oral hygiene care with a higher risk of the components of MetS, such as obesity [24], diabetes [25,26], hypertension [26,27], and dyslipidemia [26,28], as well as with cardiovascular disease [14,22], has been demonstrated.
Although several epidemiological studies have reported the association of oral hygiene status [29] and care [23,30] with MetS, some studies found no such association [31,32]. To date, there has not been a systematic review conducted on the topic. A summary of evidence can provide a better understanding of the potential relationship and help healthcare practitioners deliver more targeted care. It can provide more substance for the formulation of public health programs and policies, especially strategies for the prevention and management of MetS.
The aim of our study was to systematically review the association of oral hygiene status and care with MetS and to quantify the strength of associations.

2. Materials and Methods

The systematic review and meta-analysis were performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [33]. The protocol was registered on the PROSPERO database (No. CRD42021243292) [34]. The research question was: Is better oral hygiene status or care associated with a lower risk of MetS?

2.1. Eligibility Criteria

The inclusion criteria were as follows: (1) The design of the study was cross-sectional, case–control, or cohort; (2) the exposure was oral hygiene status (e.g., oral hygiene index (OHI), plaque index (PI), plaque score (PSc)) or care (i.e., tooth brushing, interdental cleaning, and dental visit); (3) the outcome was MetS, clearly defined using diagnostic criteria for the condition (e.g., National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III), International Diabetes Federation (IDF), Joint Interim Statement (JIS)); (4) the study assessed the association between exposures and outcome in multiple analysis. There was no limitation on the characteristics of the study population. Animal studies, clinical trials, reviews, editorial letters, commentaries, case series, and case reports were excluded.

2.2. Search Strategy

A systematic search was performed on the PubMed and Web of Science databases, with the following keywords: oral hygiene, dental deposit, OHI, PI, PSc, tooth brushing, interdental cleaning, dental visit, and MetS. While no date restrictions were imposed, the language was limited to English. The last search was on 17 March 2021. Details of the search strategy can be seen in Supplementary Table S1. Examination of reference lists of eligible studies and relevant systematic reviews were also conducted to identify further relevant studies.

2.3. Study Selection and Data Extraction

Two authors independently screened all titles and abstracts to evaluate eligibility. Relevant studies were then examined for full-text review. Any ambiguities or disagreements were resolved by consensus. JabRef 5.2 was used during the review process.
Data from included studies were extracted independently by two authors using a data extraction form. The following information was collected: first author, publication year, study country, study design, sample size, age, gender, type of oral hygiene assessment, diagnostic criteria used for MetS, number of MetS cases, adjusted odds ratio (OR) or risk ratio (RR) with 95% confidence interval (CI), and adjustment factors. Discrepancies in data extraction were resolved by consensus.

2.4. Quality Assessment

Two authors independently examined the quality of included studies using the Newcastle–Ottawa Scale for cross-sectional, case–control, and cohort studies, as applicable. The three main domains examined were the selection of participants, comparability of study groups, and assessment of exposure/outcome of interest. The total scores for case–control and cohort studies were 9 points, while cross-sectional studies were 8 points [35,36]. The included studies were then categorized into high (≥7 points), moderate (4–6 points), or low (0–3 points) quality. Any disagreements were resolved by consensus.

2.5. Statistical Analyses

Meta-analysis was conducted separately for different types of exposure (i.e., oral hygiene status, tooth brushing, and interdental cleaning). The OR was used as the common measure for the association between oral hygiene and MetS. The reported RR was considered approximately as OR [37]. The data utilized in the meta-analysis were the estimates and the corresponding 95% CI from the most adjusted model in the studies.
The categorization of exposure varied between studies. Poor oral hygiene status or care was used as the reference group, equivalent to the highest value of OHI, PI, and PSc or the lowest frequency category of tooth brushing, interdental cleaning, and dental visits in each study. If a study classified the exposure into more than two categories, a single effect estimate was produced by combining the results of the categories using a fixed-effects (FE) model [38]. An overall pooled OR for the main analysis was calculated using a random-effects (RE) model (DerSimonian and Laird).
Heterogeneity was assessed using the I2 statistic, with the value of ≥50% representing substantial heterogeneity [37,39]. Potential sources of heterogeneity were assessed using prespecified subgroup analyses by study design and country. Examination of publication bias using funnel plot and Egger’s test was only recommended if there were an adequate number of studies (>10) [40,41].
Meta-analysis was conducted using the generic inverse variance method in Review Manager (RevMan) 5.4 software (The Cochrane Collaboration, 2020) [42].

3. Results

3.1. Literature Search

Figure 1 shows the process and the results of study selection. A total of 595 records were identified, of which 144 were duplicates; 380 irrelevant studies were eliminated. Of the 71 studies selected for full-text review, 13 met the eligibility criteria and were included in the review and meta-analysis.

3.2. Characteristics of Studies

Table 1 shows the main characteristics of the included studies. They consisted of seven cross-sectional, three case–control, and three cohort studies. A study by Shearer et al. [32] examined data from a cohort study. However, because our exposure of interest (modified OHI-S) was measured simultaneously with the outcome (MetS) at age 38, we chose to consider it as cross-sectional and reported the results of their cross-sectional model.
Eleven studies were from Asian countries, and one study each was from Finland and New Zealand. All were conducted among adult populations. Publication years ranged from 2009 to 2020, and the mean sample size was 4251.
Six studies reported oral hygiene status, six studies reported tooth-brushing frequency, two studies reported interdental cleaning, and one study reported dental visits as study factors. In the meta-analysis, a study by Tsutsumi et al. [43] was treated as two separate studies, as it reported the results independently for males and females instead of total samples. A similar approach was applied to a study by Kim et al. [44], as it provided separate data on interdental brushing and flossing.
Health examination was performed in all included studies to ascertain MetS conditions. Four studies used the NCEP ATP III criteria or its adapted version, five studies used JIS criteria, two used IDF criteria, and two used other criteria to define MetS. The most common confounders adjusted in the studies were age, gender, SES, smoking status, alcohol consumption, physical activity, and periodontal parameters. All studies reported a measure of associations as ORs, except for one study [31].
Table
Table 1. Main characteristics of the 13 included studies.
Table 1. Main characteristics of the 13 included studies.
Author, Publication YearCountryStudy DesignSample Size (M, F)Age RangeType of Oral HygieneDiagnostic Criteria for MetSNumber of CasesStatistical Analysis; AdjustmentsAssociation
Fukui et al., 2012 [45]JapanCross-sectional6421 (M: 4944, F: 1477)34–77Tooth-brushing frequency (times/day)Modified NCEP ATP III *, except the use of BMI ≥ 25 kg/m2 to define obesity. Treatments for raised TG and reduced HDL were not recorded.958Logistic regression;
age, gender, smoking habit, alcohol consumption, C-reactive protein, number of teeth, periodontal parameter (PD or CAL).		OR (95% CI)
Adjusted by PD:
≤1 time daily (reference)
2 times daily = 0.67 (0.57–0.78)
≥3 times daily = 0.50 (0.40–0.64)
Adjusted by CAL:
≤1 time daily [reference]
2 times daily = 0.66 (0.57–0.77)
≥3 times daily = 0.50 (0.39–0.63)
Kim et al., 2013 [44]South KoreaCross-sectional18742 (M: 8034, F: 10708)≥19Tooth-brushing frequency (times/day), use of dental floss (yes or no), use of interdental brush (yes or no)Modified NCEP ATP III * for Asians.5878Logistic regression;
age, gender, income, education, smoking, alcohol intake, and physical activities.		OR (95% CI)
Tooth-brushing frequency:
≥3 times daily (reference)
2 times daily = 1.23 (1.12–1.34)
≤1 time daily = 1.23 (1.04–1.47)
Use of dental floss:
Yes [reference]
No = 1.23 (1.07–1.41)
Use of interdental brush:
Yes [reference]
No = 1.05 (0.92–1.20)
Tsutsumi and Kakuma, 2015 [43]JapanCross-sectional12548 (M: 7703, F: 4845)30–59Tooth-brushing frequency (times/day)Obesity (body mass percentage ≥ 20% in men or ≥30% in women, and/or BMI ≥ 25 kg/m2) and at least one of the following: TG ≥ 150 mg/dL and/or low HDL < 40 mg/dL or drug for hypertriglyceridemia, SBP ≥ 130 mm Hg and/or DBP ≥ 85 mm Hg or drug for hypertension, FPG ≥ 110 mg/dL or drug for diabetes).3624Logistic regression;
Males: age, exercise during holidays, favorite seasoning, eating soup, sugar in coffee, having an interest in losing weight, housekeeping during holidays;
Females: age, favorite seasoning, worrying about job, sugar in coffee, pickles and food boiled in soy sauce, exercise during holidays, eating quickly, preparation of dinner, solving problems immediately.		OR (95% CI)
Males:
None (reference)
1 time daily = 0.57 (0.40–0.81)
2 times daily = 0.50 (0.35–0.71)
≥3 times daily = 0.42 (0.29–0.61)
Females:
≤1 time daily (reference)
2 times daily = 0.65 (0.48–0.87)
≥3 times daily = 0.44 (0.32–0.62)
Kim et al., 2019 [46]South KoreaCross-sectional8314 (M: 3860, F: 4454)35–79Tooth-brushing frequency (times/day)Three or more of the following five: WC ≥ 90 cm in men or ≥85 cm in women, TG > 150 mg/dL or treatment for raised TG, HDL <40 mg/dL in men or <50 mg/dL in women or treatment for reduced HDL, SBP ≥ 130 mm Hg and DBP ≥ 85 mm Hg or antihypertensive medication, FPG ≥ 100 mg/dL or current use of antidiabetic medication.2834Logistic regression;
age, gender, household income, education, smoking, alcohol intake, physical activity, periodontitis.		OR (95% CI)
Frequency of daily tooth-brushing (continuous) = 0.887 (0.84–0.94)
Saito et al., 2019 [47]JapanCross-sectional2379 (M: 960, F: 1419)75 and 80Use of secondary oral hygiene products, such as dental floss or interdental brushes (none or sometimes or every day)JIS ǂ, except the use of BMI ≥ 25 kg/m2 to define obesity and the use of HbA1c levels ≥ 5.6% to additionally define elevated glucose. Treatments for raised TG and reduced HDL were not included.563Logistic regression;
age, gender, smoking, exercise, weight gain, eating speed, cholesterol drug intake, community periodontal index, number of teeth.		OR (95% CI)
None (reference)
Sometimes = 1.19 (0.92–1.54)
Everyday = 0.71 (0.55–0.92)
Shearer et al., 2018 [32]New ZealandCross-sectional83638Modified OHI-S (very low (0–0.5) or low (>0.5–1.0) or moderate (>1.0–1.5) or high (>1.5))NCEP ATP III ¤, except the use of HbA1c ≥ 5.7% (≥39 mmol/mol) to define elevated glucose and the use of antihypertensive drugs to additionally define elevated blood pressure.152Logistic regression;
gender, low socioeconomic status, smoking, dysglycemia, inflammatory load.		OR (95% CI)
Low (reference)
High = 0.95 (0.44, 2.01)
Chen et al., 2011 [48]TaiwanCross-sectional253 (M:117, F: 136)>18PIModified NCEP ATP III * for Asians, except the use of FPG ≥ 110 mg/dL or previously diagnosed T2DM to define elevated glucose.145Logistic regression;
age, gender, education, smoking, high-sensitivity C-reactive protein, and serum albumin.		OR (95% CI)
PI score (continuous) = 1.724 (1.135–2.615)
Kobayashi et al., 2012 [30]JapanCohort prospective, 3-year follow-up685 (M: 513, F: 172)-Tooth-brushing frequency (times/day)JIS ǂ for Asians, except not including treatments for raised TG, reduced HDL, and elevated glucose.99Logistic regression;
age, gender, smoking status, drinking status, breakfast eating, educational level, occupation (desk work or non-desk work), depressive symptoms, physical activity, and total caloric consumption.		OR (95% CI)
≤1 time daily (reference)
2 times daily = 0.80 (0.49–1.31)
≥3 times daily = 0.43 (0.19–0.97)
Tanaka et al., 2018 [23]JapanCohort retrospective, 5-year follow-up3722 (M: 2897, F: 825)35–64Tooth-brushing frequency (times/day), dental check-ups (regular or irregular)JIS ǂ for Asians, except the use of BMI ≥ 25 kg/m2 to define obesity.412Logistic regression;
age, gender, periodontal status, number of present teeth, occupational status, smoking quantity, alcohol consumption, physical activity, dietary behavior, food preference, tooth-brushing frequency, dental check-ups, and number of MetS components at baseline.		OR (95% CI)
Tooth-brushing frequency:
≤1 time daily (reference)
2 times daily = 0.83 (0.65–1.05)
≥3 times daily = 0.64 (0.45–0.91)
Dental check-ups:
Irregular (reference)
Regular = 1.10 (0.77–1.55)
Pussinen et al., 2020 [31]FinlandCohort prospective, 21-, 27-, 31-year follow-up586 (M: 270, F: 316)27–43Presence of visible plaque (yes or no)JIS ǂ for Europeans.153Poisson regression;
age, gender, childhood BMI, family income, adulthood smoking (ever) and socioeconomic status (education), and interaction terms between caries and periodontal parameters.		RR (95% CI)
No (reference)
Yes = 1.21 (0.87–1.86)
Pham, 2018 [29]VietnamCase–control (case = 206, control = 206)412 (M: 114, F: 298)50–78PI (≤2.5 or 2.51–2.90 or 2.91–3.26 or ≥3.27)JIS ǂ for Asians.206Logistic regression;
age, gender.		OR (95% CI)
≤2.5 (reference)
2.51–2.90 = 4.81 (1.74–13.27)
2.91–3.26 = 6.12 (2.24–16.70)
≥3.27 = 7.50 (2.80–20.12)
Li et al., 2009 [49]ChinaCase–control (case = 152, control = 56)208 (M: 85, F: 123)37–78PI
(≤1 or >1–1.5 or >1.5–2 or >2) 		IDF §152Logistic regression;
age, gender, smoking.		OR (95% CI)
≤1 (reference)
>1–1.5 = 4.81 (0.81–28.63)
>1.5–2 = 13.06 (2.24–76.18)
>2 = 47.4 (6.94–323.68)
Li et al., 2020 [50]ChinaCase–control (case = 114, control = 49)163 (M: 60, F: 103)37–78PIIDF §114Logistic regression (backward);
age, gender, smoking habits, bleeding index, PD, biomarkers (serum C-reactive protein, salivary IL-6, IL-1β).		OR (95% CI)
PI score (continuous) = 14.69 (5.56–38.84)
M, male; F, female; MetS, metabolic syndrome; WC, waist circumference; BMI, body mass index; TG, triglycerides; HDL, high-density lipoprotein; SBP, systolic blood pressure; DBP, diastolic blood pressure; FPG, fasting plasma glucose; HbA1c, glycated haemoglobin; T2DM, type 2 diabetes mellitus; OHI-S, simplified oral hygiene index; PI, plaque index; PD, probing depth; CAL, clinical attachment level; OR, odds ratio; RR, risk ratio; CI, confidence interval. ¤ The National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) (2001) definition is any three of the following five: WC > 102 cm (>40 in) in men or >88 cm (>35 in) in women, TG ≥ 150 mg/dL, HDL < 40 mg/dL in men or <50 mg/dL in women, blood pressure ≥ 130/85 mm Hg, FPG ≥ 110 mg/dL [51]. * The modified NCEP ATP III (2005) definition is any three of the following five: WC ≥ 102 cm (≥40 in) in men or ≥88 cm (≥35 in) in women (for Asians: ≥90 cm (≥35 in) in men and ≥80 cm (≥31 in) in women), TG ≥ 150 mg/dL (1.7 mmol/L) or treatment for raised TG, HDL < 40 mg/dL (1.03 mmol/L) in men or <50 mg/dL (1.3 mmol/L) in women or treatment for reduced HDL, SBP ≥ 130 mm Hg or DBP ≥ 85 mm Hg or treatment for hypertension, FPG ≥ 100 mg/dL or treatment for elevated glucose [52]. § The International Diabetes Federation (IDF) (2005) definition is increased WC (ethnicity specific) plus any two of the following four: TG ≥ 150 mg/dL (1.7 mmol/L) or treatment for raised TG, HDL < 40 mg/dL (1.03 mmol/L) in men or <50 mg/dL (1.29 mmol/L) in women or treatment for reduced HDL, SBP ≥ 130 mm Hg or DBP ≥ 85 mm Hg or treatment for hypertension, FPG ≥ 100 mg/dL (5.6 mmol/L) or previously diagnosed T2DM [53]. ǂ The Joint Interim Statement (JIS) (2009) definition is any three of the following five: increased WC (population- and country-specific), TG ≥ 150 mg/dL (1.7 mmol/L) or treatment for raised TG, HDL < 40 mg/dL (1.0 mmol/L) in men or <50 mg/dL (1.3 mmol/L) in women or treatment for reduced HDL, SBP ≥ 130 mm Hg and/or DBP ≥ 85 mm Hg or treatment for hypertension, FPG ≥100 mg/dL or treatment for elevated glucose [54].

3.3. Quality Aspects of Studies

All the included studies were of moderate to high quality. One cross-sectional study, two case–control studies, and three cohort studies were of high quality. Six cross-sectional studies and one case–control study were of moderate quality. Details of the quality assessment of included studies can be seen in Supplementary Table S2.

3.4. Association between Oral Hygiene Status, Care, and MetS

Figure 2 shows the results of the meta-analysis of associations of oral hygiene status, tooth-brushing frequency, and interdental cleaning with MetS. Good oral hygiene (OR = 0.30; 95% CI = 0.13–0.66), frequent tooth brushing (OR = 0.68; 95% CI = 0.58–0.80), and frequent interdental cleaning (OR = 0.89; 95% CI = 0.81–0.99) were associated with a lower risk of MetS. While heterogeneity was minimal for interdental cleaning (I2 = 27%), there was substantial heterogeneity for oral hygiene status (I2 = 91%) and tooth-brushing frequency (I2 = 89%).
The association between dental visits and MetS was evaluated only in a study by Tanaka et al. It was found that dental visits were not significantly associated with MetS (OR = 1.10; 95% CI = 0.77–1.55) [23].

3.5. Subgroup Analyses

Table 2 displays the results of subgroup analysis by study design for the association between oral hygiene status and MetS. The inverse association between oral hygiene status and MetS was only observed in the subgroup of case–control studies. Subgroup analysis by study design reduced heterogeneity to less than 50%.
Table 3 shows the results of subgroup analyses for the association between tooth-brushing frequency and MetS. Frequent tooth brushing was consistently associated with a lower risk of MetS in all subgroup analyses. However, high heterogeneity was still observed among studies with a cross-sectional design. While subgroup analysis by country reduced heterogeneity, it remained above 50%.

4. Discussion

Our systematic review and meta-analysis investigated the association of oral hygiene status and care with MetS. Better oral hygiene status, frequent tooth brushing, and frequent interdental cleaning were associated with a lower risk of MetS. However, substantial heterogeneity for tooth-brushing frequency and inconsistent results for oral hygiene status in subgroup analyses were noted. Our review identified only one study examining the association between dental visits and MetS, and found no association [23].
While our main analysis revealed an inverse association between better oral hygiene status and MetS, the finding was inconsistent in subgroup analysis by study design. Of all studies included in the meta-analysis for oral hygiene status, only studies by Shearer et al. [32] and Pussinen et al. [31], conducted in New Zealand and Finland, respectively, did not find an association. These different findings might be due to the age of the study samples. Both studies had relatively younger samples than the other studies, which had a sample mean age of more than 50 years. The stronger influence of periodontal inflammations on cardiometabolic health may only be observed in later life [32]. Moreover, Pussinen et al. [31] reported both the adjusted RRs for MetS and β values for the number of MetS components. While the adjusted RR for the association between the presence of plaque and MetS was not significant, the β value for the association between the number of teeth with plaque and the number of MetS components was significant [31].
Our overall findings are in line with other systematic reviews and meta-analyses that demonstrated an association between oral health or hygiene and metabolic conditions [9,37]. Poor oral hygiene not only leads to dental infections, such as periodontitis, but it may also affect systemic health [55]. Periodontal bacteria in plaque, their products, and resulting local inflammatory response may enter the bloodstream, directly contributing to systemic inflammation [56]. Chronic exposure to proinflammatory cytokines, such as TNF-α and IL-1β, may alter lipid metabolism, causing hyperlipidemia [57]. TNF-α may induce insulin resistance by directly affecting target organs (e.g., liver, muscle, and adipocytes) and by indirectly promoting the production of free fatty acids from adipocytes [58]. Elevated levels of proinflammatory cytokines may also contribute to pancreatic β-cells dysfunction, leading to the development of T2DM [57,59,60,61]. Moreover, recent evidence showed that Porphyromonas gingivalis might induce metabolic impairment by altering the gut microbiome [62].
Our study showed inverse relationships of tooth-brushing frequency and interdental cleaning with MetS. Despite substantial heterogeneity, the findings of all subgroup analyses of tooth-brushing frequency were consistent. Tooth brushing is the most crucial self-care measure to control plaque and is a protective factor against periodontal diseases [63,64]. While a suggestion for proper frequency of tooth brushing could not be given, most of the included studies used a cut-off point of twice or more daily. Another review showed similar findings and indicated that brushing less than twice daily might not be beneficial for the prevention of DM [37]. In addition to tooth brushing, interdental cleaning is recommended for maintaining oral health. The daily use of interdental brushes was found to decrease periodontal bacteria, promote symbiotic microbiota, and reduce interdental inflammation [65]. It was suggested that poor oral hygiene could exaggerate MetS by increasing local and systemic inflammation [66].
An alternative explanation for the association between oral hygiene care and MetS might be that it is due to shared risk factors [14] or biased health consciousness. People with a healthier lifestyle might tend to adopt better oral hygiene care [67]. The fact that oral hygiene care may merely be an indicator of general health awareness or behaviors underscores the complexity of oral epidemiology [68]. However, most of the included studies in our review accounted for important confounders, such as age, gender, SES, smoking status, alcohol consumption, and physical activity, minimizing the bias.
The association between dental visits and MetS was not demonstrated in the study by Tanaka et al. [23]. This finding was similar to another study demonstrating no associations between dental visits, professional dental cleaning, and diabetes. It was argued that other confounders had more important roles in the development of diabetes than professional dental cleaning [25]. However, an earlier review has demonstrated the benefit of scaling and root planing on metabolic control and systemic inflammation reduction in patients with T2DM [69].
This systematic review and meta-analysis was the first to explore the association of oral hygiene status and care with MetS. The topic is seen as recent in the scientific literature, with the earliest identified studies published in 2009. It is also related to an emerging interest in the interrelationships between oral pathogens, oral microbiome dysbiosis, and systemic conditions [70]. Exploring this topic is relevant considering the importance of formulating policies with common risk factors approach to address both oral and general health [71]. Another strength of our review was the quality of the studies, which was moderate to high.
Our review might be limited by the methodological weakness of the included studies with a cross-sectional design. The number of cohort studies was also limited. Moreover, the restriction of studies to those published in English and the exclusion of a grey literature search might introduce bias. The risk of publication bias could not be ruled out and was not assessed in our study due to an inadequate number of studies and high heterogeneity. Besides study design and country, the potential source of heterogeneity might be from the variability in measurement methods of oral hygiene status (e.g., the use of different indices) and the reporting of tooth-brushing frequency and interdental cleaning between studies. Moreover, the criteria used to define MetS varied.
Information on tooth-brushing frequency and interdental cleaning was self-reported, which might be prone to bias. However, it might only be the type of nondifferential misclassification, leading to the underestimation of true effect estimates. Regular brushing does not necessarily reflect effective brushing, as the studies did not adjust for the duration and method of tooth brushing and the type of dentifrice used.
Finally, most of the included studies in our review were conducted among an Asian population, which may influence the generalizability of the findings worldwide. Further research conducted among other populations is warranted to provide more evidence. Using a uniform protocol for reporting oral hygiene (e.g., tooth-brushing frequency) may also facilitate better comparison.

5. Conclusions

Our study found that there might be inverse associations of oral hygiene status, tooth-brushing frequency, and interdental cleaning with MetS. However, substantial heterogeneity for tooth-brushing frequency and inconsistent results for oral hygiene status in subgroup analyses were observed. There was insufficient evidence on the association between dental visits and MetS. Further well-conducted studies, preferably of longitudinal design, are needed to confirm the associations of oral hygiene status and care with MetS and to explore their underlying mechanisms. Research on this topic will provide a valuable contribution to our current understanding of the interrelationship between oral health and MetS.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/jcm10132873/s1, Table S1: Database search strategy, Table S2: Quality assessment of the 13 included studies.

Author Contributions

Conceptualization, C.M.A.S.; methodology, C.M.A.S. and A.N.; formal analysis, C.M.A.S.; investigation, C.M.A.S., F.K. and A.N.; data curation, C.M.A.S. and F.K.; writing—original draft preparation, C.M.A.S.; writing—review and editing, C.M.A.S., F.K., T.B., J.Z., A.N.; supervision, A.N. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the European Union, cofinanced by the European Social Fund and European Regional Development Fund (Grant No. EFOP-3.6.1-16-2016-00022 “Debrecen Venture Catapult Program”). Project No. TKP2020-NKA-04 has been implemented with the support provided by the National Research, Development, and Innovation Fund of Hungary, financed under the 2020-4.1.1-TKP2020 funding scheme.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design, execution, interpretation, or writing of the study.

References

  1. Cornier, M.A.; Dabelea, D.; Hernandez, T.L.; Lindstrom, R.C.; Steig, A.J.; Stob, N.R.; Van Pelt, R.E.; Wang, H.; Eckel, R.H. The metabolic syndrome. Endocr. Rev. 2008, 29, 777–822. [Google Scholar] [CrossRef] [PubMed]
  2. Lear, S.A.; Gasevic, D. Ethnicity and metabolic syndrome: Implications for assessment, management and prevention. Nutrients 2020, 12, 15. [Google Scholar] [CrossRef] [Green Version]
  3. Saklayen, M.G. The Global Epidemic of the Metabolic Syndrome. Curr. Hypertens. Rep. 2018, 20, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Curtis, L.H.; Hammill, B.G.; Bethel, M.A.; Anstrom, K.J.; Gottdiener, J.S.; Schulman, K.A. Costs of the metabolic syndrome in elderly individuals: Findings from the Cardiovascular Health Study. Diabetes Care 2007, 30, 2553–2558. [Google Scholar] [CrossRef] [Green Version]
  5. Blanquet, M.; Legrand, A.; Pélissier, A.; Mourgues, C. Socio-economics status and metabolic syndrome: A meta-analysis. Diabetes Metab. Syndr. Clin. Res. Rev. 2019, 13, 1805–1812. [Google Scholar] [CrossRef] [PubMed]
  6. Sun, K.; Liu, J.; Ning, G. Active Smoking and Risk of Metabolic Syndrome: A Meta-Analysis of Prospective Studies. PLoS ONE 2012, 7, e47791. [Google Scholar] [CrossRef] [Green Version]
  7. Fabiani, R.; Naldini, G.; Chiavarini, M. Dietary patterns and metabolic syndrome in adult subjects: A systematic review and meta-analysis. Nutrients 2019, 11, 2056. [Google Scholar] [CrossRef] [Green Version]
  8. Joseph, M.S.; Tincopa, M.A.; Walden, P.; Jackson, E.; Conte, M.L.; Rubenfire, M. The impact of structured exercise programs on metabolic syndrome and its components: A systematic review. Diabetes Metab. Syndr. Obes. Targets Ther. 2019, 12, 2395–2404. [Google Scholar] [CrossRef] [Green Version]
  9. Gobin, R.; Tian, D.; Liu, Q.; Wang, J. Periodontal Diseases and the Risk of Metabolic Syndrome: An Updated Systematic Review and Meta-Analysis. Front. Endocrinol. 2020, 11, 1035–1057. [Google Scholar] [CrossRef]
  10. Cao, X.; Wang, D.; Zhou, J.; Yuan, H.; Chen, Z. Relationship between dental caries and metabolic syndrome among 13 998 middle-aged urban Chinese. J. Diabetes 2017, 9, 378–385. [Google Scholar] [CrossRef]
  11. Ojima, M.; Amano, A.; Kurata, S. Relationship between decayed teeth and metabolic syndrome: Data from 4716 middle-aged male Japanese employees. J. Epidemiol. 2015, 25, 204–211. [Google Scholar] [CrossRef] [Green Version]
  12. Li, X.; Kolltveit, K.M.; Tronstad, L.; Olsen, I. Systemic diseases caused by oral infection. Clin. Microbiol. Rev. 2000, 13, 547–558. [Google Scholar] [CrossRef] [PubMed]
  13. Hyvärinen, K.; Salminen, A.; Salomaa, V.; Pussinen, P.J. Systemic exposure to a common periodontal pathogen and missing teeth are associated with metabolic syndrome. Acta Diabetol. 2015, 52, 179–182. [Google Scholar] [CrossRef] [PubMed]
  14. Chang, Y.; Woo, H.G.; Park, J.; Lee, J.S.; Song, T.J. Improved oral hygiene care is associated with decreased risk of occurrence for atrial fibrillation and heart failure: A nationwide population-based cohort study. Eur. J. Prev. Cardiol. 2020, 27, 1835–1845. [Google Scholar] [CrossRef] [PubMed]
  15. Gomes, M.S.; Blattner, T.C.; Sant’Ana Filho, M.; Grecca, F.S.; Hugo, F.N.; Fouad, A.F.; Reynolds, M.A. Can apical periodontitis modify systemic levels of inflammatory markers? A systematic review and meta-analysis. J. Endod. 2013, 39, 1205–1217. [Google Scholar] [CrossRef] [PubMed]
  16. Scannapieco, F.A.; Cantos, A. Oral inflammation and infection, and chronic medical diseases: Implications for the elderly. Periodontol. 2000 2016, 72, 153–175. [Google Scholar] [CrossRef]
  17. De Rooij, S.R.; Nijpels, G.; Nilsson, P.M.; Nolan, J.J.; Gabriel, R.; Bobbioni-Harsch, E.; Mingrone, G.; Dekker, J.M. Low-grade chronic inflammation in the relationship between insulin sensitivity and cardiovascular disease (RISC) population: Associations with insulin resistance and cardiometabolic risk profile. Diabetes Care 2009, 32, 1295–1301. [Google Scholar] [CrossRef] [Green Version]
  18. León-Pedroza, J.I.; González-Tapia, L.A.; del Olmo-Gil, E.; Castellanos-Rodríguez, D.; Escobedo, G.; González-Chávez, A. Low-grade systemic inflammation and the development of metabolic diseases: From the molecular evidence to the clinical practice. Cir. Cir. 2015, 83, 543–551. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Claydon, N.C. Current concepts in toothbrushing and interdental cleaning. Periodontol. 2000 2008, 48, 10–22. [Google Scholar] [CrossRef]
  20. Ainamo, J. Prevention of periodontal disease in the dental office. Int. Dent. J. 1984, 34, 56–61. [Google Scholar]
  21. Lim, L.P.; Davies, W.I.R. Comparison of various modalities of “simple” periodontal therapy on oral cleanliness and bleeding. J. Clin. Periodontol. 1996, 23, 595–600. [Google Scholar] [CrossRef] [PubMed]
  22. De Oliveira, C.; Watt, R.; Hamer, M. Toothbrushing, inflammation, and risk of cardiovascular disease: Results from Scottish Health Survey. BMJ 2010, 340, 1400. [Google Scholar] [CrossRef] [Green Version]
  23. Tanaka, A.; Takeuchi, K.; Furuta, M.; Takeshita, T.; Suma, S.; Shinagawa, T.; Shimazaki, Y.; Yamashita, Y. Relationship of toothbrushing to metabolic syndrome in middle-aged adults. J. Clin. Periodontol. 2018, 45, 538–547. [Google Scholar] [CrossRef] [PubMed]
  24. Nijakowski, K.; Lehmann, A.; Rutkowski, R.; Korybalska, K.; Witowski, J.; Surdacka, A. Poor oral hygiene and high levels of inflammatory cytokines in saliva predict the risk of overweight and obesity. Int. J. Environ. Res. Public Health 2020, 17, 6310. [Google Scholar] [CrossRef] [PubMed]
  25. Chang, Y.; Lee, J.S.; Lee, K.J.; Woo, H.G.; Song, T.J. Improved oral hygiene is associated with decreased risk of new-onset diabetes: A nationwide population-based cohort study. Diabetologia 2020, 63, 924–933. [Google Scholar] [CrossRef] [PubMed]
  26. Fujita, M.; Ueno, K.; Hata, A. Lower frequency of daily teeth brushing is related to high prevalence of cardiovascular risk factors. Exp. Biol. Med. 2009, 234, 387–394. [Google Scholar] [CrossRef]
  27. Choi, H.M.; Han, K.; Park, Y.-G.; Park, J.-B. Associations Among Oral Hygiene Behavior and Hypertension Prevalence and Control: The 2008 to 2010 Korea National Health and Nutrition Examination Survey. J. Periodontol. 2015, 86, 866–873. [Google Scholar] [CrossRef]
  28. Song, T.J.; Kim, J.W.; Kim, J. Oral health and changes in lipid profile: A nationwide cohort study. J. Clin. Periodontol. 2020, 47, 1437–1445. [Google Scholar] [CrossRef]
  29. Pham, T. The association between periodontal disease severity and metabolic syndrome in Vietnamese patients. Int. J. Dent. Hyg. 2018, 16, 484–491. [Google Scholar] [CrossRef]
  30. Kobayashi, Y.; Niu, K.; Guan, L.; Momma, H.; Guo, H.; Cui, Y.; Nagatomi, R. Oral health behavior and metabolic syndrome and its components in adults. J. Dent. Res. 2012, 91, 479–484. [Google Scholar] [CrossRef]
  31. Pussinen, P.J.; Paju, S.; Viikari, J.; Salminen, A.; Taittonen, L.; Laitinen, T.; Burgner, D.; Kahonen, M.; Lehtimaki, T.; Hutri-Kahonen, N.; et al. Childhood Oral Infections Associate with Adulthood Metabolic Syndrome: A Longitudinal Cohort Study. J. Dent. Res. 2020, 99, 1165–1173. [Google Scholar] [CrossRef]
  32. Shearer, D.M.; Thomson, W.M.; Cameron, C.M.; Ramrakha, S.; Wilson, G.; Wong, T.Y.; Williams, M.J.A.; McLean, R.; Theodore, R.; Poulton, R. Periodontitis and multiple markers of cardiometabolic risk in the fourth decade: A cohort study. Community Dent. Oral Epidemiol. 2018, 46, 615–623. [Google Scholar] [CrossRef] [PubMed]
  33. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009, 6, e1000097. [Google Scholar] [CrossRef] [Green Version]
  34. Santoso, C.M.A.; Ketti, F.; Nagy, A. Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-analysis. PROSPERO 2021 CRD42021243292. Available online: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42021243292 (accessed on 17 April 2021).
  35. Wells, G.; Shea, B.; O’Connell, D.; Peterson, J.; Welch, V.; Losos, M.; Tugwell, P. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses. Available online: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed on 5 February 2021).
  36. Yuan, T.; Zou, H.; Zhao, J.; Yang, Z.; Li, L.; Cai, W.; Gu, J.; Hao, C.; Li, J.; Hao, Y.; et al. Circumcision to prevent HIV and other sexually transmitted infections in men who have sex with men: A systematic review and meta-analysis of global data. Artic. Lancet Glob. Health 2019, 7, e436–e447. [Google Scholar] [CrossRef] [Green Version]
  37. Fu, W.; Lv, C.; Zou, L.; Song, F.; Zeng, X.; Wang, C.; Yan, S.; Gan, Y.; Chen, F.; Lu, Z.; et al. Meta-analysis on the association between the frequency of tooth brushing and diabetes mellitus risk. Diabetes Metab. Res. Rev. 2019, 35, e3141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Bae, J.M. Comparison of methods of extracting information for meta-analysis of observational studies in nutritional epidemiology. Epidemiol. Health 2016, 38, e2016003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Higgins, J.P.; Green, S. (Eds.) Analysing data and undertaking meta-analyses. In Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]; The Cochrane Collaboration: Melbourne, Australia, 2011. [Google Scholar]
  40. Higgins, J.P.T.; Green, S. (Eds.) Addressing reporting biases. In Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]; The Cochrane Collaboration: Melbourne, Australia, 2011. [Google Scholar]
  41. Alzahrani, H.; Mackey, M.; Stamatakis, E.; Zadro, J.R.; Shirley, D. The association between physical activity and low back pain: A systematic review and meta-analysis of observational studies. Sci. Rep. 2019, 9, 1–10. [Google Scholar] [CrossRef]
  42. Review Manager (RevMan) [Computer Program], Version 5.4; The Cochrane Collaboration: Melbourne, Australia, 2020; Available online: https://training.cochrane.org/online-learning/core-software-cochrane-reviews/revman/revman-non-cochrane-reviews (accessed on 16 March 2021).
  43. Tsutsumi, C.; Kakuma, T. Regular Tooth Brushing is Associated with a Decreased Risk of Metabolic Syndrome According to a Medical Check-Up Database. Kurume Med. J. 2015, 61, 43–52. [Google Scholar] [CrossRef] [Green Version]
  44. Kim, Y.-H.; Kim, D.-H.; Lim, K.S.; Ko, B.-J.; Han, B.-D.; Nam, G.-E.; Park, Y.-G.; Han, K.D.; Kim, J.-H.; Cho, K.-H. Oral health behaviors and metabolic syndrome: The 2008-2010 Korean National Health and Nutrition Examination Survey. Clin. Oral Investig. 2014, 18, 1517–1524. [Google Scholar] [CrossRef]
  45. Fukui, N.; Shimazaki, Y.; Shinagawa, T.; Yamashita, Y. Periodontal Status and Metabolic Syndrome in Middle-Aged Japanese. J. Periodontol. 2012, 83, 1363–1371. [Google Scholar] [CrossRef]
  46. Kim, J.S.; Kim, S.Y.; Byon, M.J.; Lee, J.H.; Jeong, S.H.; Kim, J.B. Association between periodontitis and metabolic syndrome in a korean nationally representative sample of adults aged 35–79 years. Int. J. Environ. Res. Public Health 2019, 16, 2930. [Google Scholar] [CrossRef] [Green Version]
  47. Saito, M.; Shimazaki, Y.; Nonoyama, T.; Tadokoro, Y. Number of teeth, oral self-care, eating speed, and metabolic syndrome in an aged Japanese population. J. Epidemiol. 2019, 29, 26–32. [Google Scholar] [CrossRef] [Green Version]
  48. Chen, L.-P.; Hsu, S.-P.; Peng, Y.-S.; Chiang, C.-K.; Hung, K.-Y. Periodontal disease is associated with metabolic syndrome in hemodialysis patients. Nephrol. Dial. Transplant. 2011, 26, 4068–4073. [Google Scholar] [CrossRef] [Green Version]
  49. 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]
  50. Li, P.; He, L.; Chen, Z.B.; Luan, Q.X. Biomarkers in Metabolic Syndrome Patients with Chronic Periodontitis. Chin. J. Dent. Res. 2020, 23, 191–197. [Google Scholar] [CrossRef]
  51. Expert Panel. Third Report of the Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III); NIH Publication: Bethesda, MD, USA, 2002.
  52. Grundy, S.M.; Cleeman, J.I.; Daniels, S.R.; Donato, K.A.; Eckel, R.H.; Franklin, B.A.; Gordon, D.J.; Krauss, R.M.; Savage, P.J.; Smith, S.C.; et al. Diagnosis and management of the metabolic syndrome: An American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Circulation 2005, 112, 2735–2752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Alberti, K.G.M.M.; Zimmet, P.; Shaw, J. The metabolic syndrome—A new worldwide definition. Lancet 2005, 366, 1059–1062. [Google Scholar] [CrossRef]
  54. Alberti, K.G.M.M.; Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; Cleeman, J.I.; Donato, K.A.; Fruchart, J.C.; James, W.P.T.; Loria, C.M.; Smith, S.C. Harmonizing the Metabolic Syndrome: A Joint Interim Statement of The International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009, 120, 1640–1645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Bui, F.Q.; Almeida-da-Silva, C.L.C.; Huynh, B.; Trinh, A.; Liu, J.; Woodward, J.; Asadi, H.; Ojcius, D.M. Association between periodontal pathogens and systemic disease. Biomed. J. 2019, 42, 27–35. [Google Scholar] [CrossRef]
  56. Leite, F.R.M.; Nascimento, G.G. The Relationship Between Periodontal Diseases and Chronic Diseases. In Oral Epidemiology—A Textbook on Oral Health Conditions, Research Topics and Methods; Peres, M.A., Antunes, J.L.F., Watt, R.G., Eds.; Springer: Cham, Switzerland, 2021; pp. 379–393. [Google Scholar]
  57. Iacopino, A.M. Periodontitis and diabetes interrelationships: Role of inflammation. Ann. Periodontol. 2001, 6, 125–137. [Google Scholar] [CrossRef]
  58. Nishimura, F.; Iwamoto, Y.; Mineshiba, J.; Shimizu, A.; Soga, Y.; Murayama, Y. Periodontal Disease and Diabetes Mellitus: The Role of Tumor Necrosis Factor-α in a 2-Way Relationship. J. Periodontol. 2003, 74, 97–102. [Google Scholar] [CrossRef]
  59. Wang, C.; Guan, Y.; Yang, J. Cytokines in the progression of pancreatic β-cell dysfunction. Int. J. Endocrinol. 2010, 2010, 515136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Cieślak, M.; Wojtczak, A.; Cieślak, M. Role of pro-inflammatory cytokines of pancreatic islets and prospects of elaboration of new methods for the diabetes treatment. Acta Biochim. Pol. 2015, 62, 15–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Grover, H.S.; Luthra, S. Molecular mechanisms involved in the bidirectional relationship between diabetes mellitus and periodontal disease. J. Indian Soc. Periodontol. 2013, 17, 292–301. [Google Scholar] [CrossRef] [PubMed]
  62. Watanabe, K.; Katagiri, S.; Takahashi, H.; Sasaki, N.; Maekawa, S.; Komazaki, R.; Hatasa, M.; Kitajima, Y.; Maruyama, Y.; Shiba, T.; et al. Porphyromonas gingivalis impairs glucose uptake in skeletal muscle associated with altering gut microbiota. FASEB J. 2020, 35, e21171. [Google Scholar] [CrossRef]
  63. Lertpimonchai, A.; Rattanasiri, S.; Arj-Ong Vallibhakara, S.; Attia, J.; Thakkinstian, A. The association between oral hygiene and periodontitis: A systematic review and meta-analysis. Int. Dent. J. 2017, 67, 332–343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Zimmermann, H.; Zimmermann, N.; Hagenfeld, D.; Veile, A.; Kim, T.S.; Becher, H. Is frequency of tooth brushing a risk factor for periodontitis? A systematic review and meta-analysis. Community Dent. Oral Epidemiol. 2015, 43, 116–127. [Google Scholar] [CrossRef]
  65. Bourgeois, D.; Bravo, M.; Llodra, J.C.; Inquimbert, C.; Viennot, S.; Dussart, C.; Carrouel, F. Calibrated interdental brushing for the prevention of periodontal pathogens infection in young adults—A randomized controlled clinical trial. Sci. Rep. 2019, 9, 1–13. [Google Scholar] [CrossRef] [Green Version]
  66. Kim, S.W.; Cho, K.H.; Han, K.D.; Roh, Y.K.; Song, I.S.; Kim, Y.H. Tooth loss and metabolic syndrome in South Korea: The 2012 Korean national health and nutrition examination survey. Medicine 2016, 95. [Google Scholar] [CrossRef] [PubMed]
  67. Yeung, C.A. Gums and heart disease: Healthy gums, healthy heart? BMJ 2010, 341, 113. [Google Scholar] [CrossRef]
  68. 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]
  69. Baeza, M.; Morales, A.; Cisterna, C.; Cavalla, F.; Jara, G.; Isamitt, Y.; Pino, P.; Gamonal, J. Effect of periodontal treatment in patients with periodontitis and diabetes: Systematic review and meta-analysis. J. Appl. Oral Sci. 2020, 28. [Google Scholar] [CrossRef] [PubMed]
  70. Santarelli, A.; Wong, D.T.W.; Lo Muzio, L. Editorial: Saliva and Oral Microbiota: From Physiology to Diagnostic and Therapeutic Implications. Front. Physiol. 2021, 11, 637599. [Google Scholar] [CrossRef]
  71. Souza, M.L.; Massignan, C.; Peres, K.G.; Peres, M.A. Association between metabolic syndrome and tooth loss: A systematic review and meta-analysis. J. Am. Dent. Assoc. 2019, 150, 1027–1039.e7. [Google Scholar] [CrossRef]
Jcm 10 02873 g001 550
Figure 1. PRISMA flow diagram of the literature search and study selection [33]. MetS, metabolic syndrome.
Figure 1. PRISMA flow diagram of the literature search and study selection [33]. MetS, metabolic syndrome.
Jcm 10 02873 g001
Jcm 10 02873 g002 550
Figure 2. Meta-analysis of the associations of (a) oral hygiene status, (b) tooth-brushing frequency, and (c) interdental cleaning with metabolic syndrome.
Figure 2. Meta-analysis of the associations of (a) oral hygiene status, (b) tooth-brushing frequency, and (c) interdental cleaning with metabolic syndrome.
Jcm 10 02873 g002
Table
Table 2. Subgroup analysis by study design for the association between oral hygiene status and MetS.
Table 2. Subgroup analysis by study design for the association between oral hygiene status and MetS.
SubgroupNumber of StudiesOR (95% CI)I2 (%)p
Cross-sectional20.72 (0.41–1.26)460.17
Case–control30.11 (0.06–0.20)390.19
Cohort10.83 (0.59–1.15)--
MetS, metabolic syndrome; OR, odds ratio; CI, confidence interval; I2, percentage of variation due to heterogeneity; p, p-value for heterogeneity.
Table
Table 3. Subgroup analyses for the association between tooth-brushing frequency and MetS.
Table 3. Subgroup analyses for the association between tooth-brushing frequency and MetS.
SubgroupNumber of StudiesOR (95% CI)I2 (%)p
Study design
Cross-sectional50.67 (0.55–0.81)93<0.001
Cohort20.74 (0.62–0.89)00.64
Country
Japan50.61 (0.52–0.70)550.06
Korea20.85 (0.78–0.93)730.06
MetS, metabolic syndrome; OR, odds ratio; CI, confidence interval; I2, percentage of variation due to heterogeneity; p, p-value for heterogeneity.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Santoso, C.M.A.; Ketti, F.; Bramantoro, T.; Zsuga, J.; Nagy, A. Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-Analysis. J. Clin. Med. 2021, 10, 2873. https://doi.org/10.3390/jcm10132873

AMA Style

Santoso CMA, Ketti F, Bramantoro T, Zsuga J, Nagy A. Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-Analysis. Journal of Clinical Medicine. 2021; 10(13):2873. https://doi.org/10.3390/jcm10132873

Chicago/Turabian Style

Santoso, Cornelia Melinda Adi, Fera Ketti, Taufan Bramantoro, Judit Zsuga, and Attila Nagy. 2021. "Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-Analysis" Journal of Clinical Medicine 10, no. 13: 2873. https://doi.org/10.3390/jcm10132873

APA Style

Santoso, C. M. A., Ketti, F., Bramantoro, T., Zsuga, J., & Nagy, A. (2021). Association between Oral Hygiene and Metabolic Syndrome: A Systematic Review and Meta-Analysis. Journal of Clinical Medicine, 10(13), 2873. https://doi.org/10.3390/jcm10132873

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop