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. 2024 Apr 4;19(4):e0297545. doi: 10.1371/journal.pone.0297545

Association between dental scaling and metabolic syndrome and lifestyle

TaeYeon Lee 1, Kyungdo Han 2, Kyoung-In Yun 3,*
Editor: Gustavo G Nascimento4
PMCID: PMC10994476  PMID: 38573898

Abstract

Purpose

Periodontal disease is a risk factor for diabetes and metabolic syndrome, and non-surgical periodontal treatment has been shown to help maintain stable blood sugar in diabetic patients. Determining the level of preventive scaling in patients with metabolic syndrome will help manage the disease. The purpose of this study was to investigate the extent to which people with metabolic syndrome or bad lifestyle performed scaling and the association between preventive scaling and metabolic syndrome or lifestyle in a large population.

Methods

This study was conducted on adults aged 20 years or older from January 2014 to December 2017 in the National Health Insurance System (NHIS) database. Among 558,067 people who underwent health checkups, 555,929 people were included. A total of 543,791 people were investigated for preventive scaling. Metabolic syndrome components were abdominal obesity, lower high density lipoprotein cholesterol (HDL)-C, high triglycerides, high blood pressure and hyperglycemia. Unhealthy lifestyle score was calculated by assigning 1 point each for current smokers, drinkers, and no performing regular exercise.

Results

When multiple logistic regression analysis was performed after adjusting for age, sex, income, body mass index (BMI), smoking, drinking and regular exercise, the Odds ratios (OR) and 95% confidence intervals (CI) of the group with 5 metabolic syndrome components were 0.741 (0.710, 0.773) (p<0.0001). After adjustment for age, sex, income, BMI, smoking, drinking, regular exercise, diabetes, hypertension and dyslipidemia, the OR (95% CI) of the group with unhealthy lifestyle score = 3 was 0.612 (0.586, 0.640) (p<0.0001).

Conclusions

The more metabolic syndrome components, and the higher unhealthy lifestyle score, the less scaling was performed.

Introduction

Periodontal inflammation results from the interaction of the host immune system and a dysbiotic subgingival plaque biofilm and modified by lifestyle and environmental factors [1, 2]. Although plaque deposition is not a major risk factor for periodontitis, periodontal disease can be initiated by bacterial plaque [1, 3]. Microbiota in plaque biofilms release the inflammatory tissue breakdown products into the gingival crevice and inflammatory reactions in gingival sulcus can induce microbiota imbalance (dysbiosis) [4]. Dysbiosis can increase the inflammatory potential and ultimately cause the periodontitis in susceptible persons [4]. If the initial subgingival infection and tissue damage localized to the gingiva are not resolved, the epithelial barrier may be destroyed and clinical loss of periodontal attachment can occur [1].

If the bacterial plaque is not removed and remains on the tooth surface for a long time, it becomes calcified and becomes calculus [3]. The mineralized mass of gingival calculus is actually very porous and may play a secondary role in bacterial retention and a reservoir of various endotoxins [2, 5]. Because surface biofilm is always present, it is difficult to determine the causal relationship of subgingival calculus to the initiation and progression of periodontal disease [2]. Nevertheless, the presence of calculus is closely associated with inflammation of the subgingival pocket walls [2].

Periodontal disease is initiated by bacterial biofilm, but clinical manifestations vary depending on the individual’s host inflammatory response and other predisposing factors such as lifestyle and systemic conditions. Various clinical studies have reported increased susceptibility and severity of periodontitis and more severe periodontal disease progression in smokers compared to non-smokers, suggesting that smoking-induced alterations in the host’s inflammatory response and microbiological changes may be involved [6, 7]. The negative effects of smoking on periodontitis can be further exacerbated by excessive drinking [7].

Periodontal pathogens do not remain only in tissues around the teeth, but can move through the bloodstream and cause low-grade inflammation throughout the body. Various previous studies have estimated that periodontal disease acts as a risk factor for cardiovascular disease, diabetes, and metabolic syndrome [811]. Patients with periodontitis are known to have more severe endothelial dysfunction, increased arterial calcification scores, and increased risk of myocardial infarction compared to patients without periodontitis [11]. Glycated hemoglobin increased over time in people with periodontitis [9]. The presence of periodontal pockets was associated with increased metabolic syndrome components [9]. However, the association between metabolic syndrome and periodontitis could be bi-directional. Diabetes is a high-level risk factor for gingivitis and periodontitis, and glycaemia and periodontal disease risk show a dose-response relationship [12]. Periodontitis seems to occur in conjunction with a number of diabetes-related complications and is even considered a complication of diabetes [13]. It has been reported that people with metabolic syndrome are twice as likely to develop periodontitis than those without it [9].

As discussed above, many studies report an association between systemic diseases and periodontitis, but the causal relationship is not clear. This potential association between periodontitis and metabolic syndrome may be related to common risk factors such as smoking and diet. Smoking increases the risk of metabolic syndrome, regardless of the age of onset or duration of smoking [14, 15]. Compared to non-smokers, smokers have more unhealthy lifestyle habits such as alcohol consumption and physical inactivity, which are known to increase the risk of metabolic disease [15]. A healthy lifestyle may prevent or delay the onset of metabolic syndrome in people who are susceptible to it.

Periodontal disease causes local and systemic inflammatory reactions, so proper prevention and treatment are very important. Treatment of periodontal disease includes non-surgical treatment and surgical treatment. Scaling is the gold standard of non-surgical periodontal treatment and a preventive treatment. Scaling alone can reduce bleeding and periodontal pockets in teeth with severe periodontitis [12]. It is known that the treatment of periodontal disease can improve not only the local inflammatory condition around the tooth but also the systemic inflammatory condition. After treatment for periodontal disease, systemic markers related to cardiovascular disease were reported to decrease [12]. Non-surgical periodontal treatment has been shown to reduce HbA1C levels in diabetic patients and help maintain stable blood sugar [16]. After regular scaling, surgical site infection in knee arthroplasty patients was reported to be reduced [17].

Dental scaling not only serves as a treatment for local inflammation around the teeth, but also plays an important role in the treatment of various systemic diseases and reduction of complications. However, most of the studies so far have observed changes in clinical indicators or test values related to the disease after scaling on patients with systemic diseases. There has been no study on the relationship between the scaling performed for preventive purposes and metabolic syndrome or lifestyle in a large population.

The purpose of this study was to investigate the extent to which people with metabolic syndrome or bad lifestyle performed scaling, a basic periodontal disease management program and the association between preventive scaling and metabolic syndrome or lifestyle in a large population.

Methods

Study population and design

In this study, the National Health Insurance Service-National Sample Cohort (NHIS-NSC) database produced by the National Health Insurance System (NHIS) was used. NHIS is the single mandatory health insurance program that covers approximately 97% of the Korean population. NHIS-NSC was launched in 2000 by integrating 375 insurance societies, and provides longitudinal data on 97% of the Korean population in connection with the national death registry and national health examination program [18, 19]. The remaining 3% of the low-income population is covered by health assistance programs and their data have been integrated into the NHIS database. Therefore, since 2006, the NHIS database has included information on comorbidities, drug prescriptions, treatment claims, and demographic characteristics of virtually the entire population of Korea. The NHIS database is based on the ICD-10-CM (International Classification of Disease, Tenth Revision, Clinical Modification) codes. The National Health Screening program, launched in 2009 and administered by the government, includes a medical interview and blood pressure test, chest X-ray, blood test, urine test, and dental exam. Health checkups are managed by the government and are practiced by almost all Koreans. NHIS-NSC data can only be analyzed by the analysis office within the National Health Insurance Service for studies that have passed the study protocol, and the original data are deleted after a certain period of time. (https://nhiss.nhis.or.kr/bd/ab/bdaba000eng.do;jsessionid=vlpHYbY2GAeotWKtU4XI9S8JvdHRUXclZxYlCu25G8htHNZaxz4zeBP3Q1VDIaSs.primrose22_servlet_engine10).

From July 2013, adults 20 years of age and older are covered by the NHIS-NSC for preventive scaling once a year. Scaling for preventive purposes is performed to prevent periodontal disease or to prevent deterioration of it, and means to be performed when additional periodontal treatment is not required after scaling. Scaling for therapeutic purposes is defined as being performed before curettage or periodontal surgery. Scaling for preventive purposes is managed as a separate prescription code to distinguish it from scaling for therapeutic purposes. This study was conducted on adults aged 20 years or older from January 2014 to December 2017 in the NHIS-NSC database. Those under 20 years of age or missing data were excluded. From January 2014 to December 2017, among 558,067 people who underwent health checkups, 555,929 people aged 20 years or older were included. A total of 543,791 people, excluding double missing persons, were investigated for preventive scaling considering various confounders.

Variables

Age, gender, and family income level were used as sociodemographic variables. Household income was corrected for the number of family members and divided into quintiles: < 20%, 20%~39%, 40%~59%, 60~79% and > 80% of the total equivalized income in the survey. We consider < 20% as low-income group. From the health behaviors survey data, we utilized smoking, drinking, and regular exercise. The drinking status was classified to never, mild (<30g alcohol per day) and heavy (≥30g alcohol per day). The smoking status was categorized into three groups: non-smoker, ex-smoker (those who had smoked in the past but had ceased smoking) or current smoker. The regular exercise was defined as moderate-intensity physical activity for at least 30 minutes at least 5 days a week or high-intensity exercise for at least 20 minutes at least 3 days a week.

Body weight and height were measured with the participants in light in door clothing without shoes. Waist circumference (WC) was measured at the narrowest point between the lower border of the rib cage and the iliac crest. Body mass index (BMI) was calculated by the following formula: weight/height2 (kg/m2). Systolic and diastolic blood pressure (BP) were measured on the right arm two times with five-minute interval, and the average value were used for the analysis. A blood sample was collected from antecubital vein of each subject after fasting for more than eight hours. Serum glucose, total cholesterol, triglyceride, high density lipoprotein (HDL) cholesterol, and low-density lipoprotein (LDL) cholesterol were measured. Hypertension was defined as ICD-10 codes I10 to I13 or I15 and treatment with antihypertensive medications, systolic BP ≥ 140mmHg, or diastolic BP ≥ 90mmHg). Type 2 diabetes was defined as ICD-10 codes E11 to E14 and anti-diabetic drugs, or fasting glucose level ≥ 126mg/dL) and hyperlipidemia was defined as ICD-10 code E78 with lipid-lowering agents, or serum total cholesterol ≥ 240mg/dL.

Metabolic syndrome was defined based on the modified criteria of the National Cholesterol Education Program Adult Treatment Panel III, while abdominal obesity was based on the Asian-specific WC cutoff [20]. Individuals were diagnosed with Metabolic syndrome if they had three or more of the following: (1) a WC of ≥ 90 cm for men and ≥ 85 cm for women [21]; (2) a serum triglyceride level of ≥ 150 mg/dL or were treated with lipid-lowering medication; (3) a serum HDL-C level of < 40 mg/dL for men or < 50 mg/dL for women; (4) a BP of ≥ 130/85 mmHg or were treated with antihypertensive medication; and (5) a fasting blood glucose level of ≥ 100 mg/dL or were treated with antidiabetic medication.

Based on the results of preliminary analyses, unhealthy lifestyle was defined as smoking, alcohol consumption, and non-regular exercise [22]. Unhealthy lifestyle score was calculated by assigning 1 point each for current smokers, drinkers, and no performing regular exercise. The study population was categorized into four groups according unhealthy lifestyle score from patients with score 0 who did not have any unhealthy lifestyle behaviors to patients with score 3 who met all three unhealthy lifestyle behaviors.

Scaling for preventive purposes is managed with a separate prescription code from scaling for treatment purposes. Because the outcome variable for this study was preventive dental scaling, prescription code for therapeutic scaling, regardless of referral, was excluded. The outcome variable, preventive dental scaling, was defined as whether or not the person had a preventive scaling in the same year as the year of the health checkup (Binary variable).

Statistical analyses

Baseline characteristics were analyzed using descriptive statistics. Categorical variables were described as frequencies (%). Continuous variables were described as means ± standard deviation (SD). An independent t-test for continuous variables or a chi-square test of categorical variables were used to analyze the relationship with scaling.

Multiple logistic regression analysis was used to assess the association between metabolic syndrome, lifestyle and scaling. Odds ratios (OR) and 95% confidence intervals (CI) were estimated after adjustment for potential confounders. The variables in the final model were age, sex, BMI, income level, smoking, alcohol consumption, regular exercise, diabetes, hypertension, and dyslipidemia (variables in Table 2). The variables in the final model were grouped into groups (demographics, body composition, socio-economics, lifestyle, comorbidities). The variables were added to the model progressively from non-adjusted to fully adjusted.

Three types of model were used to multiple logistic regression analysis according to metabolic syndrome. Model 1 was not adjusted. Model 2 was adjusted for demographic variables (age and sex). Model 3 was adjusted for the variables in model 2 plus body composition variable (BMI) and socio-economic variables (income level) and lifestyle variables (smoking, alcohol consumption and regular exercise). Four types of model were used to multiple logistic regression analysis according to lifestyle. Model 1 was not adjusted. Model 2 was adjusted for age and sex (demographic variables). Model 3 was adjusted for the variables in model 2 plus income level (socio-economic variables), and BMI (body composition variable). Model 4 was adjusted for the variables in model 3 plus comorbidities such as diabetes, hypertension and dyslipidemia (Fig 1). We used SAS version 9.2 (SAS institute Inc., Cary, NC, USA) for statistical analysis. Two-sided P- values of < 0.05 were considered statistically significant,

Fig 1. Study population and design.

Fig 1

Results

The general characteristics of the population categorized by with and without scaling are shown in Table 1. Among 543,791 people, 105,966 people were in the group that performed scaling for preventive purposes. The mean age of the scaling group was lower than that of the non-scaling group (50.29±14.91 vs. 46.34±13.11, p<0.0001). The prevalence of diabetes, hypertension, and dyslipidemia was lower in the scaling group than in the non-scaling group (p<0.0001). Systolic and diastolic blood pressure and fasting blood glucose levels were lower in the scaling group (p<0.0001). There was no difference in weight between the two groups, but BMI and waist circumference were lower in the scaling group (p<0.0001). The regular exercise execution rate was higher in the scaling group than in the non-scaling group.

Table 1. The clinical characteristics of study participants.

Preventive scaling
No Yes p-value
(n = 437,825) (n = 105,966)
Age groups < 0.0001
 < 40 104,807 (23.94) 32,009 (30.21)
 40–64 254,166 (58.05) 64,829 (61.18)
 ≥ 65 78,852 (18.01) 9,128 (8.61)
Age, years 50.29±14.91 46.34±13.11 < 0.0001
Sex < 0.0001
 Male 218,627 (49.93) 50,933 (48.07)
 Female 219,198 (50.07) 55,033 (51.93)
Income, Lower 20% 75,137 (17.16) 15,766 (14.88) < 0.0001
Body mass index (BMI) Level < 0.0001
 < 18.5 16,597 (3.79) 4,272 (4.03)
 < 23` 162,913 (37.21) 42,992 (40.57)
 < 25 103,212 (23.57) 24,860 (23.46)
 < 30 132,631 (30.29) 29,530 (27.87)
 ≥ 30 22,472 (5.13) 4,312 (4.07)
Smoking < 0.0001
 Non 271,372 (61.98) 67,852 (64.03)
 Ex 67,259 (15.36) 17,808 (16.81)
 Current 99,194 (22.66) 20,306 (19.16)
Drinking < 0.0001
 Non 231,298 (52.83) 52,953 (49.97)
 Mild 172,676 (39.44) 45,839 (43.26)
 Heavy 33,851 (7.73) 7,174 (6.77)
Regular exercise 83,472 (19.07) 22,762 (21.48) < 0.0001
Diabetes mellitus 51,868 (11.85) 8,269 (7.8) < 0.0001
Hypertension 128,111 (29.26) 22,076 (20.83) < 0.0001
Dyslipidemia 113,820 (26) 24,358 (22.99) < 0.0001
Systolic blood pressure, mmHg 122.65±15 119.87±14.07 < 0.0001
Diastolic blood pressure, mmHg 76.12±10.03 74.86±9.77 < 0.0001
Fasting glucose, mg/dL 100.37±25.79 97.29±20.83 < 0.0001
Total Cholesterol, mg/dL 194.63±37.94 194.72±36.92 0.4936
HDL -C, mg/dL 55.83±15.38 57.07±16.07 < 0.0001
LDL -C, mg/dL 113.61±35.66 113.91±34.41 0.0115
Height, cm 163.53±94 164.57±8.89 < 0.0001
Weight, kg 64.34±12.46 64.37±12.35 0.4566
BMI, kg/m2 23.95±3.48 23.64±3.35 < 0.0001
Waist Circumference, cm 80.87±9.68 79.62±9.66 < 0.0001

Data are presented as frequencies (%) in categorical variables and means ± standard deviation (SD) in continuous variables.

P-values were obtained by an independent t-test for continuous variables or a chi-square test of categorical variables. P< 0.05 is statistically significant.

HDL, high density lipoprotein cholesterol; LDL, low-density lipoprotein cholesterol

Table 2 shows the OR (95% CI) results of multivariate analysis for scaling trials. The lower the income and the older the age, the less scaling (p<0.0001). Males were doing less scaling than females (p<0.0001). Groups with BMI < 18.5 or BMI ≥ 23 received less preventive scaling, but in the case of BMI ≥ 23, as the BMI level increased, they received less preventive scaling (p<0.0001). Ex-smokers were found to be scaling more than non-smokers, but current smokers were found to be scaling less (p<0.0001). Mild drinkers performed more scaling than non-drinkers, but heavy drinkers did less (p<0.0001). The group that exercised regularly performed more preventive scaling than the group that did not (p<0.0001). People with diabetes, hypertension, and dyslipidemia were doing less scaling than those without these conditions (p<0.0001).

Table 2. Association of clinical characteristics with scaling in univariate analyses.

Event N (%) OR (95% C.I) p-value
Age groups < 0.0001
 < 40 32,009 (23.4) 1 (Ref.)
 40~64 64,829 (20.32) 0.835 (0.823, 0.848)
 ≥ 65 9,128 (10.38) 0.379 (0.370, 0.389)
Sex < 0.0001
 Male 50,933 (18.89) 0.928 (0.916, 0.940)
 Female 55,033 (20.07) 1 (Ref.)
Income < 0.0001
 Quintile 1 15,766 (17.34) 1 (Ref.)
 Quintile 2 16,497 (18.4) 1.075 (1.049, 1.101)
 Quintile 3 19,569 (18.77) 1.101 (1.076, 1.127)
 Quintile 4 23,827 (19.72) 1.170 (1.145, 1.197)
 Quintile 5 30,307 (21.94) 1.339 (1.311, 1.368)
BMI Level < 0.0001
 < 18.5 4,272 (20.47) 0.975 (0.942, 1.010)
 < 23 42,992 (20.88) 1 (Ref.)
 < 25 24,860 (19.41) 0.913 (0.897, 0.929)
 < 30 29,530 (18.21) 0.844 (0.830, 0.858)
 ≥ 30 4,312 (16.1) 0.727 (0.703, 0.753)
Smoking < 0.0001
 Non 67,852 (20) 1 (Ref.)
 Ex 17,808 (20.93) 1.059 (1.039, 1.079)
 Current 20,306 (16.99) 0.819 (0.805, 0.833)
Drinking < 0.0001
 Non 52,953 (18.63) 1 (Ref.)
 Mild 45,839 (20.98) 1.160 (1.143, 1.176)
 Heavy 7,174 (17.49) 0.926 (0.901, 0.951)
Regular exercise < 0.0001
 No 83,204 (19.02) 1 (Ref.)
 Yes 22,762 (21.43) 1.161 (1.142, 1.181)
Diabetes < 0.0001
 No 97,697 (20.2) 1 (Ref.)
 Yes 8,269 (13.75) 0.630 (0.615, 0.645)
Hypertension < 0.0001
 No 83,890 (21.31) 1 (Ref.)
 Yes 22,076 (14.7) 0.636 (0.626, 0.647)
Dyslipidemia < 0.0001
 No 81,608 (20.12) 1 (Ref.)
 Yes 24,358 (17.63) 0.850 (0.836, 0.863)

CI, confidence interval; OR, odds ratio.

P< 0.05 is statistically significant.

Fig 2 shows the OR (95% CI) of multiple logistic regression analysis stratified by metabolic syndrome and classified by scaling presence. Even after adjusting for various variables, the group with obesity, hypertension, diabetes, dyslipidemia, and metabolic syndrome showed less scaling, and the more metabolic syndrome components, the less scaling. As a result of analysis after adjustment for age, sex, income, BMI, smoking, drinking and regular exercise, the OR (95% CI) of the group with 5 metabolic syndrome components was 0.74 (0.71, 0.77) (p<0.0001).

Fig 2. Multiple logistic regression analysis according to metabolic syndrome.

Fig 2

P< 0.05 is statistically significant.

This forest plot is the result of analysis by adjusting for age, gender, income, BMI, smoking, drinking, and regular exercise. This forest plot was created based on the results in Appendix Table 1 in S1 Appendix.

Fig 3 shows the OR (95% CI) of multiple logistic regression analysis stratified by lifestyle and classified by the presence or absence of scaling. Even after adjusting the variables, the higher the unhealthy lifestyle score, the lower the scaling. As a result of analysis after adjustment for age, sex, income, BMI, smoking, drinking, regular exercise, diabetes, hypertension and dyslipidemia, the OR (95% CI) of the group with unhealthy lifestyle score = 3 was 0.61 (0.59, 0.64) (p<0.0001).

Fig 3. Multiple logistic regression analysis according to lifestyle.

Fig 3

P< 0.05 is statistically significant.

This forest plot is the result of analysis by adjusting for age, sex, income, BMI, smoking, drinking, regular exercise, diabetes, hypertension and dyslipidemia. This forest plot was created based on the results in Appendix Table 2 in S1 Appendix.

Discussion

As a result of adjusting and analyzing potential confounding variables, this study showed that the more metabolic syndrome components, and the higher the unhealthy lifestyle score, the less scaling was performed.

Periodontitis is a chronic multifactorial inflammatory disease associated with dysbiotic plaque biofilms and characterized by the progressive destruction of the tooth-supporting apparatus [23, 24]. It’s progression is related with individual’s immunity and lifestyle, especially smoking and poor oral hygiene [25]. If the inflammatory response is not controlled, extensive periodontal destruction is occurred. The periodontal pocket epithelium is involved in systemic spread of local inflammation because of its direct contact with subgingival biofilm [25]. Pro-inflammatory cytokines and enzymes from periodontitis may migrate into the circulation and cause distant systemic inflammation although systemic inflammation can also contribute to periodontitis [25, 26]. Patients with periodontitis have higher values of white blood cells, interleukin (IL)-1, IL-6, tumor necrosis factor (TNF)-α and C-reactive protein (CRP) [25, 26]. Long-term retention of these cytokines may alter the systemic inflammatory state. In this way, periodontitis may exacerbate pre-existing systemic diseases such as diabetes and cardiovascular disease [25].

According to meta-analyses of the relationship between periodontitis and metabolic syndrome, the odds ratio between metabolic syndrome and periodontitis shows a slight difference between countries, but shows that periodontitis and metabolic syndrome are related [27, 28]. In addition, it was found that the relationship between periodontitis and metabolic syndrome increased as the severity of periodontitis and the number of metabolic syndrome factors increased [29]. Patients with metabolic syndrome had more severe periodontal disease than those without, and the pattern of oral bacteria was different [30, 31]. In the case of metabolic syndrome accompanied by periodontitis, more major bacteria of periodontal disease were detected than in the group with only metabolic syndrome, and the difference in treatment effect was significant [31]. Changes in oral flora were thought to increase the risk of metabolic syndrome due to periodontal disease [31].

Although the exact mechanism by which local inflammation caused by periodontal pathogens and cytokines induce systemic inflammation is unknown, it is thought that removing the cause of local inflammation can help treat diabetes and metabolic syndrome. Dental scaling is not only non-surgical periodontal therapy to control local inflammation around the teeth by mechanically removing bacterial plaque and calculus attached to the teeth, but also prophylactic treatment to prevent the occurrence and progression of local inflammation around the teeth. Removing the bacterial biofilm through dental scaling can help to stop the progression of inflammation in its earlier stages. Non-surgical periodontal therapy was associated with a progressive decrease in CRP in healthy individuals [32]. It has been reported that dental scaling affects the control of diabetes and hyperlipidemia. After scaling in patients with type 2 diabetes, high-sensitivity C-reactive protein (hs-CRP), IL-1ß, IL-6 concentrations and HbA1c decreased [3335]. In patients with hyperlipidemia, pro-inflammatory cytokine levels and serum lipid levels decreased after periodontal disease treatment [36, 37]. Recent study reported that moderate-certainly evidence that periodontal therapy is helpful in reduction of HbA1c in diabetic patients [38].

As seen above, there are many previous studies showing that systemic diseases such as diabetes, cardiovascular disease, and metabolic syndrome improve disease-related values after scaling, so it is important to actively manage periodontal disease from the diagnosis stage of these diseases. The present study investigated the extent to which patients with metabolic syndrome performed scaling, a basic periodontal disease management program. According to this study, the group with diabetes, dyslipidemia, hypertension, obesity, and metabolic syndrome received less scaling than the group without these conditions. In addition, the more metabolic syndrome factors, the less preventive scaling was received. The results of this study indicate that the group with poorly controlled systemic diseases neglected oral hygiene management more than the well-controlled group. The results of this study cannot accurately determine the cause. However, judging from the results of this study, it is necessary to check whether the accessibility of dental treatment for patients with metabolic syndrome, including diabetes, has decreased, and whether there is a lack of education on the importance of oral hygiene management and regular scaling to prevent periodontal disease. Dental clinicians may ask physicians to recommend that patients with metabolic syndrome visit the dental clinics.

The present study also investigated the association between bad lifestyle and dental scaling. Lifestyle factors such as smoking and physical exercise affect the development and exacerbation of periodontitis as well as metabolic syndrome [3, 39]. It has been reported that people with a healthy lifestyle have a lower incidence of metabolic syndrome and periodontitis [39, 40]. According to this study, it was found that the higher the unhealthy lifestyle score, the less scaling was received.

Smoking is a major risk factor for periodontal disease [6]. Smoking may affect periodontal destruction through the microcirculatory, inflammatory and immune systems [6]. Smoking may lead to change of composition of the subgingival biofilm, formation of specific periodontal pathogen colonization and compromising the immune response [6, 41]. Many previous studies have shown that smokers have more periodontal tissue destruction than non-smokers and do not respond well to nonsurgical periodontal treatment [42]. However, scaling alone presents improving periodontal clinical parameters and reducing the levels of periodontal pathogens in smokers [6]. It is known that when smoking cessation periodontal pathogens change to the same pattern as non-smokers, and the effect of periodontal treatment is improved [6, 43]. In this study, it was found that current smokers received less preventive scaling. However, former smokers received more prophylactic scaling than non-smokers or current smokers. The cause of quitting smoking of former smokers is not known, but it is presumed that attention to systemic and oral health may have contributed to their decision to stop smoking.

Alcohol consumption is also known to be associated with the development of periodontitis. Drinkers had a higher incidence of periodontitis than non-drinkers [44]. The risk of periodontitis increased as the amount of alcohol consumed or the frequency of drinking increased [4446]. However, some authors reported that periodontal parameters of moderate drinkers were not different from non-drinkers [47, 48]. This result was thought to be related to the heterogeneity of assessment methods or same mechanism, down regulation of pro-inflammatory cytokines as the beneficial effects of light drinking on cardiovascular disease and type 2 diabetes [47]. In this study, it was found that mild drinkers received more preventive scaling than non-drinkers, but heavy drinkers received less preventive scaling than non-drinkers or mild drinkers. It seems that clinicians need to help heavy drinkers reduce the amount and frequency of alcohol consumption, not only for their systemic health, but also for their oral health. It also seems that dental clinicians need to find way to make it easier for heavy drinkers to participate in oral healthcare program including preventive scaling.

This study showed that the more metabolic syndrome components, and the higher unhealthy lifestyle score, the less scaling was performed. The results of this study suggest that clinicians need to find ways to make periodontal disease prevention and management programs more accessible to people with metabolic syndrome or unhealthy lifestyles.

Limitations and strengths

This study has several limitations. First of all, it is difficult to generalize the results of this study because the survey data from only one Asian country. Second, because this study targeted people who had undergone a health examination registered in the NHIS database, those who had not undergone a health examination were not included. Third, the analysis period was short, about 4 years. Fourth, it is difficult to determine a causal relationship. Forth, because this study focused on preventive care, data from people who received only therapeutic scaling without preventive scaling were not included.

Nevertheless, this study has the following strengths. First, there is almost no bias based on culture and race because this study was conducted on a relatively ethnically homogenous population. Second, population-based data were used, in which more than 97% of the total population of Korea participated. Third, because this study used the results of a targeting a large population, it can provide epidemiological evidence that the more metabolic syndrome components, and the higher the unhealthy lifestyle score, the less scaling was performed.

Conclusions

As a result of analysis after adjusting for potential confounding variables, it was found that the more metabolic syndrome components, and the higher unhealthy lifestyle score, the less scaling was performed. These findings suggest that plans are needed to increase access to preventive scaling for people with metabolic syndrome or unhealthy lifestyles.

Supporting information

S1 Appendix

(DOCX)

pone.0297545.s001.docx (17.2KB, docx)
S1 Checklist. STROBE statement—Checklist of items that should be included in reports of observational studies.

(DOCX)

pone.0297545.s002.docx (31.7KB, docx)

Data Availability

Data cannot be shared publicly because of the legal restrictions, concerns for patient privacy, and third party owner ship of the data by the Korea National Health Insurance Service (NHIS). However, the introduction and details of dataset are obtainable by accessing the Korean National Health Insurance Service homepage at https://nhiss.nhis.or.kr/. It can also be requested via nhiss@nhis.or.kr, +82-1577-1000, or from 32 Gungang-ro, Wonju-si, Gangwon-do 26464.

Funding Statement

This research was supported by grant of the Institute of Clinical Medicine Research in the Yeouido St. Mary’s Hospital, College of Medicine, The Catholic University of Korea(Grant Number: YSI22H007). The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Gustavo G Nascimento

20 Jun 2023

PONE-D-23-15887Association between dental scaling and metabolic syndrome and lifestyle: A national cohort studyPLOS ONE

Dear Dr. Yun,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. 

Dear authors,

Three experts in the field have reviewed your manuscript and raised serious concerns regarding the conceptual model underlying your study. Particular attention should be given to the presentation of the results, as all referees indicated issues related to lack of clarity and the exceeding number of tables. Please consider including a figure, as suggested by one of the referees. 

I look forward to receiving your revised manuscript. 

Please submit your revised manuscript by Aug 04 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

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Gustavo G. Nascimento, PhD

Academic Editor

PLOS ONE

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Reviewers' comments:

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Comments to the Author

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The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: No

Reviewer #2: Partly

Reviewer #3: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: No

Reviewer #3: Yes

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

**********

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Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The paper has the potential to enrich the literature by promoting a discussion about whether preventive scaling would indeed have any impact on indicators of metabolic syndrome in a population-based study.

I recommend that the authors reconsider the theoretical concept underlying the analyses and reorganize the presentation of the paper. In an epidemiological study like this, clarifying the outcomes and exposures according to your aims is crucial.

In a deep reflection, I suggest revisiting some assumptions still unclear in the literature. There is no consensus on the role of periodontitis in chronic disease causation. Studies show that, most likely, both share the same risk factors, such as an unhealthy diet. In this sense, preventive scaling would have little impact on periodontitis and even less on other metabolic risks.

Reviewer #2: The study uses a national database to report the associations of metabolic syndrome and unhealthy lifestyle (as exposures) and preventive scaling (as the outcome). The topic is clinically relevant as there is a need to identify the utilization rates of preventive dental care in such individuals at risk of periodontal disease. However, there are major methodological issues that need to be addressed before it can be considered for publication. Below are a few points for the consideration of the authors:

1. The statistical plan addresses the main objectives of the study using too many multivariable models and is rather confusing to follow. For instance, it is difficult to understand what Table 2 adds in the overall analysis, besides identifying the significant covariates associated with the outcome. If that is the case, the univariate analysis should suffice. As such, the multivariable analysis in Table 2 only adds to the ambiguity, for example, dyslipidemic individuals are shown to be at higher odds of preventive scaling which is in contrast to what has been reported in Table 3, where individuals with high triglycerides and low HDL-C levels are at lower odds of preventive scaling.

2. In Table 3, metabolic syndrome is categorized as a binary variable (yes/no), ordinal variable (with its five components together), and also as individual components tested separately with the outcome. The rationale of having so many definitions of metabolic syndrome to test this association is unclear. Also, the rationale behind having a stepwise inclusion of confounders as Models 1,2,3 needs to be clearly mentioned if it adds anything to the overall results, in contrast to reporting only model 3 which includes all the potential confounders.

3. Similarly, Table 4 also reports multiple models as well as definitions of exposure to test the association which either needs to be justified or needs to be trimmed down substantially. More so, some of the models are very perplexing. For example, Model 3 in Table 4 adjusts for smoking, drinking and regular exercise while testing the association of the same exposures with the outcome. The authors would need to re-organize the tables, to highlight main findings they believe helps to test their study objective.

4. Minor points:

i) The current Table 1 is unclear and confusing. In Table 1, it would be more informative if the comparative proportion of individuals is reported by row and not by column. For instance, how many proportions of males had/did not undergo preventive scaling, etc. Also, Table 1 needs to be re-organized into categorical variables, which is reported as N (%) and continuous variables, reported as Mean (SD).

ii) In Tables 1 and 2, remove the term “baseline” as this is a cross-sectional data with no baseline and follow-ups.

iii) In the Discussion, the authors need to discuss the potential role of dental visits for more complex procedures (such as surgical/non-surgical periodontal therapy) in those with metabolic syndrome and/or unhealthy lifestyle, which would confound the absence of codes for preventive scaling in this group of people.

iv) Also, potential explanations for the associations observed in the study needs further corroboration with evidence from literature.

Reviewer #3: This is an interesting manuscript on the association between metabolic syndrome, unhealthy lifestyle habits and preventive dental scaling using a huge dataset from Korea. As results, authors showed that these characteristics are interconnected and clustered in the sample, and that dose-response relationships with dental scaling for preventive purposes occur.

Introduction:

*There are some sentences that called my attention:

"Calculus, which is not removed by routine oral hygiene practices such as brushing, is the CAUSE of periodontitis along with the bacterial plaque that covers it."

"Periodontitis bacteria in dental calculus and bacterial plaque locally DESTROY not only the soft tissues around the teeth but also the alveolar bone, resulting in tooth loss."

"Periodontal pathogens, which CAUSE periodontal disease..."

In my opinion, these sentences should be accurately reviewed. Current knowledge shows that periodontitis causation are not so simply as stated.

*State study's hypotheses.

Methods:

*It would be interesting to see how variables were hierarchically organized. Consider to use a flowchart for that.

Results:

*I am not convinced on the way how authors reported their results. In table 1, for instance, authors showed all independent variables assessed, and described these as "baseline characteristics". In table 2, they also called "baseline characteristics" but selected some to report. Additionally, tables 3 and 4 showed some data also previously presented in table 2 (as the effect measures are the same). For instance, high blood pressure/hypertension, drinking, smoking and regular exercise.

My point is that these tables can be simplified and data could be accommodated in two tables (one for unhealthy lifestyle and another for metabolic syndrome).

*As authors described dose-response relationships, I would suggest to remove such findings from tables and present the odds ratios graphically.

Discussion:

*Authors centered the discussion (and introduction as well) on the microbiological path that links exposures and periodontitis. What about the inflammatory pathway?

*Indeed, what about behavioral pathways? Authors described that metabolic syndrome components, unhealthy lifestyle habits and lack of preventive oral care are clustered in the same individuals. What health professionals should do in this respect?

*Language revision would be useful to avoid some redundancies such as "treatment to treat".

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: Yes: Leandro Machado Oliveira

**********

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PLoS One. 2024 Apr 4;19(4):e0297545. doi: 10.1371/journal.pone.0297545.r002

Author response to Decision Letter 0


15 Aug 2023

I appreciate your kind advice about this manuscript. I did my best to correct the flaws. The corrected items were marked as yellow color in the manuscript. Please let me know if there are any more revisions.

Attachment

Submitted filename: response to reviewer comments_ Plos One.docx

pone.0297545.s003.docx (22.7KB, docx)

Decision Letter 1

Gustavo G Nascimento

13 Sep 2023

PONE-D-23-15887R1Association between dental scaling and metabolic syndrome and lifestylePLOS ONE

Dear Dr. Yun,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

Dear authors,

Thank you for sending your revised manuscript.

While the referees have noticed an improvement in your manuscript, inconsistencies remain to be further addressed. The definition of periodontitis merits attention and should be revised according to the current understanding of the disease.

In addition, please clarify some methodological aspects, such as the nature of the periodontal treatment variable (e.g., binary or discrete).

Thank you.

==============================

Please submit your revised manuscript by Oct 28 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Gustavo G. Nascimento, PhD

Academic Editor

PLOS ONE

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Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

Reviewer #2: All comments have been addressed

Reviewer #3: (No Response)

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: No

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: It must be acknowledged that the authors have made progress in the construction of the text and have greatly improved the way it is presented. Nevertheless, I suggest clarifying some of the study's important points.

Abstract/Results

The sentence: "Multiple logistic regression analysis showed that after adjustment for age, sex, income, body mass index (BMI), smoking, drinking and regular exercise, the Odds ratios (OR) and 95% confidence intervals (CI) of" is part of the methods and not the results.

Introduction

The authors approached a quite obvious pathway in which periodontal bacteria would cause cardiometabolic diseases. But right after that, the authors say sentences like “It has been reported that people with metabolic syndrome are twice as likely to develop periodontitis than those without it” demonstrating that perhaps periodontitis is caused by these diseases. It seems more plausible to believe that both periodontitis and cardiometabolic diseases have common causes such as smoking, alcohol, diet, etc. As there is no consensus on this, this should be expressed in the text. In the last two hypotheses, the low demand for dental scaling would be a clear demonstration that individuals have an unhealthy lifestyle, both in terms of general health and oral health.

Methods

The outcome variable preventive dental scaling needs to be better defined. Firstly, it needs to be stated in the text that this is the outcome studied, for example, "The outcome variable in this study was the preventive dental scaling...". Subsequently, the authors do not make it clear how this very important variable in the study was measured. Apparently, it was considered as a binary (y/n) variable, but this is not stated in the text. Furthermore, I have some doubts: Was it considered as “at least one visit”? Was it considered as the total number of visits (continuous)?

Were participants who were referred directly for therapeutic dental scaling excluded from the analysis? This may seem obvious, but it is important to clarify in the text, since the participant may not have carried out the preventive phase because their periodontal health had already deteriorated and therefore the preventive approach would no longer make sense in this situation.

Understanding that the frequency of visits for periodontal treatment is strongly linked to a healthy lifestyle, performing models adjusted for the number of medical visits (or another healthy lifestyle indicators) is necessary to help control confounding bias.

Discussion

The sentence: “Periodontitis is a chronic inflammatory infectious disease” does not make sense based on the WHO division of diseases, i.e. chronic (chronic inflammatory) or infectious diseases. From the relationship between periodontitis and other chronic diseases, it seems to be more of a chronic disease than an infectious disease, which is confirmed in the first 6 lines of the third paragraph of the discussion. Bear in mind that the relationship between periodontitis and other diseases is not clear from the literature.

P17: “The present study also investigated how many times the people with bad lifestyle habits were dental scaling.” The authors do not mention in the methodology that the outcome was considered to be the number of times the participant underwent (continuous) treatment. If dental scaling was considered as being binary, this sentence should be rewritten, as what was assessed was the probability/odds of having or not having undergone dental scaling.

Reviewer #2: (No Response)

Reviewer #3: The authors are commended for their thoughtful review of the manuscript. Few issues remain to be addressed in the manuscript:

Introduction:

*There are STILL some sentences that called my attention:

"Calculus, which is not removed by routine oral hygiene practices such as brushing, is the CAUSE of periodontitis along with the bacterial plaque that covers it." - you may consider dental plaque (dysbiosis) as a causal component of periodontitis, however, to the best of my knowledge, there is no evidence to support such a role for calculus;

"Periodontitis bacteria in dental calculus and bacterial plaque locally DESTROY not only the soft tissues around the teeth but also the alveolar bone, resulting in tooth loss." - periodontopathogens are responsible for a small part of tissue destruction. The major contributor is host immune response;

"Periodontal pathogens, which CAUSE periodontal disease..." - current knowledge shows that periodontitis causation are not so simply as stated. Please, follow current definitions of periodontitis etiology.

Methods:

*Authors described their modeling strategy. However, there is no clear explanation on why such arrangement was done. For instance, why "unhealthy lifestyle" variables were combined with the socioeconomic ones for metabolic syndrome, and another block (exclusive for comorbidities) was used when unhealthy lifestyle was the outcome? Additionally, BMI is not a socioeconomic variable.

*Was there any criteria for variable retention? Or all variables were included?

Discussion:

*Language revision would still be useful.

"(...) preventive treatment to prevent (...)"

"(...) people with bad lifestyle habits were dental scaling."

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: Yes: Leandro Machado Oliveira

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While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Apr 4;19(4):e0297545. doi: 10.1371/journal.pone.0297545.r004

Author response to Decision Letter 1


24 Oct 2023

I appreciate your kind advice about this manuscript. I did my best to correct the flaws. The corrected items were marked as yellow color in the manuscript.

Attachment

Submitted filename: response to reviewer comments 2nd.docx

pone.0297545.s004.docx (21.7KB, docx)

Decision Letter 2

Gustavo G Nascimento

26 Oct 2023

PONE-D-23-15887R2Association between dental scaling and metabolic syndrome and lifestylePLOS ONE

Dear Dr. Yun,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Dear authors, Thank you for submitting your revised manuscript. I read with interest the corrections you have made. While the methodology became clearer in this version, the Introduction section, more specifically, the concepts of periodontitis causation and its relationship with systemic diseases, should be carefully revised. While a dysbiotic biofilm has been associated with periodontitis, it has been known that plaque deposits account for approx. 20% of periodontitis causation, while the remaining 80% relate to the host's ability to deal with the inflammatory process. You can find more details elsewhere (1). On a similar note, the authors assume periodontitis as a cause for several systemic diseases, such as endothelial dysfunction, myocardial infarction, and diabetes, among others. While studies have shown associations between these conditions, causation still neeeds to be established (2). In addition, referee #3 mentioned that a potential link between periodontitis and systemic diseases relies on their shared risk factors, such as smoking and diet, among others. This has not been included in the manuscript, and, given the aim of this study - to investigate lifestyle factors in addition to MetS - this should be included and discussed (3).  Once you revise your theoretical background accordingly, a final editorial decision can be made.   Thank you for taking an extra mile. Kind regards,Gustavo.  References: 1. Bartold PM, Van Dyke TE. An appraisal of the role of specific bacteria in the initial pathogenesis of periodontitis. J Clin Periodontol. 2019;46(1):6-11. doi:10.1111/jcpe.130462. Raittio E, Farmer J. Methodological Gaps in Studying the Oral-Systemic Disease Connection. J Dent Res. 2021;100(5):445-447. doi:10.1177/00220345209829723. Frandsen Lau E, Peterson DE, Leite FRM, et al. Embracing multi-causation of periodontitis: Why aren't we there yet?. Oral Dis. 2022;28(4):1015-1021. doi:10.1111/odi.14107

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Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Apr 4;19(4):e0297545. doi: 10.1371/journal.pone.0297545.r006

Author response to Decision Letter 2


28 Nov 2023

I appreciate your kind review and comments. Following your advice, we've revised the Introduction section to reflect the recent articles.

Attachment

Submitted filename: response to reviewer comments 3rd.docx

pone.0297545.s005.docx (14.4KB, docx)

Decision Letter 3

Gustavo G Nascimento

9 Jan 2024

Association between dental scaling and metabolic syndrome and lifestyle

PONE-D-23-15887R3

Dear Dr. Yun,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Gustavo G. Nascimento, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Gustavo G Nascimento

25 Mar 2024

PONE-D-23-15887R3

PLOS ONE

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on behalf of

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Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Appendix

    (DOCX)

    pone.0297545.s001.docx (17.2KB, docx)
    S1 Checklist. STROBE statement—Checklist of items that should be included in reports of observational studies.

    (DOCX)

    pone.0297545.s002.docx (31.7KB, docx)
    Attachment

    Submitted filename: response to reviewer comments_ Plos One.docx

    pone.0297545.s003.docx (22.7KB, docx)
    Attachment

    Submitted filename: response to reviewer comments 2nd.docx

    pone.0297545.s004.docx (21.7KB, docx)
    Attachment

    Submitted filename: response to reviewer comments 3rd.docx

    pone.0297545.s005.docx (14.4KB, docx)

    Data Availability Statement

    Data cannot be shared publicly because of the legal restrictions, concerns for patient privacy, and third party owner ship of the data by the Korea National Health Insurance Service (NHIS). However, the introduction and details of dataset are obtainable by accessing the Korean National Health Insurance Service homepage at https://nhiss.nhis.or.kr/. It can also be requested via nhiss@nhis.or.kr, +82-1577-1000, or from 32 Gungang-ro, Wonju-si, Gangwon-do 26464.


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