Prevalence of metabolic syndrome and its association with oral health: First results from the Kurdish cohort study

Abstract Aims Investigate the association between oral and dental health (ODH) and metabolic syndrome (MetS) in adults aged 35–70 years. Methods The study utilized data from the enrollment phase of Dehgolan prospective cohort study in the west of Iran. A cross‐sectional assessment was conducted on a total of 3996 participants, involving a comprehensive oral examination and the assessment of their oral hygiene behavior (ODH). MetS was defined according to the updated National Cholesterol Education Program Adult Treatment Panel III. Logistic regression used to calculate odds ratios (ORs) and 95% confidence intervals (CIs), adjusting for sociodemographic characteristics. Results MetS was more prevalent among those who not daily brushing and flossing. Participants with missing teeth (MT) show higher prevalent of MetS. Being female, lower age, illiteracy, family history of diabetes, low physical activity, and salt at table were independently associated with increase odds of MetS (p < 0.05). Odds of MetS were significantly decreased with use flossing (OR = 0.75; CI = 0.60–0.93), decayed (OR = 0.83; CI = 0.72–0.97), filled (OR = 0.84; CI = 0.71–0.99), and increased with MT (OR = 1.45; CI = 1.16–1.81) as long as adjusted for ODH factors. When other potential confounder such as sociodemographic, personal and nutritional habits were adjusted, daily flossing was the only factor that still statistically decreased (OR = 0.79; CI = 0.62–0.99) the odds of MetS. Conclusion Daily flossing was the only factor that independently associated with MetS. Relationship of other ODH factors with Mets were confounded by sociodemographic characteristics of the participants.

In the current two decades, metabolic syndrome (MetS) are being increasingly recognized as the most common health problem affecting people of all ages. 1 MetS is associated with several factors including insulin resistance, visceral adiposity, dyslipidemia, endothelial dysfunction, genetic susceptibility, elevated blood pressure (BP), and chronic inflammation. 2e presence of MetS in general population is responsible for one-third of cardiovascular disease risk 3 and around 6%-7% of allcause.mortality. 4The overall prevalence of MetS varied from 12.5% to 31.4% in the adult population worldwide. 5Specifically, in Kurdish population the prevalence of MetS is reported to be 22.1%. 6's suggested that chronic inflammation associated with metabolic abnormality may leading to insulin resistance and MetS. 7rious studies reported that oral caries and MetS are interrelated and share common risk factors that include abdominal obesity, excess sugar intake, weight, age, smoking, alcohol consumption, income, and physical inactivity. 8,9Some studies have pointed out the link between chronic periodontitis with chronic diseases such as dyslipidemia, 10 diabetes, 11 and MetS.Likewise, it has been shown that dental caries process directly or indirectly related to the metabolic conditions.
Since both MetS and dental caries are correlated with common factors such as inflammation, it is reasonable to surmise they share the same causal pathways.Dental caries is a long-term and irreversible process, caused by lack of oral hygiene and past chronic infection and inflammation. 2,12So, it can be used as a suitable proxy for oral and dental health (ODH).
Another Index that directly associated with dental caries is DMFT (decayed, missing, filled teeth), the most common index used to evaluate ODH is based on a person's experience of decay (from the past to present) and indicates the oral health status of a person throughout his life. 13wever, the relationship between MetS and oral health remain controversial and limited studies 14,15 have investigated the relationship between oral health behaviors and MetS.The purpose of this study is to directly assess the relationship between DMFT with MetS and its component separately by taking into account the oral health behaviors.

| Study design and population
This study was used data of Dehgolan prospective cohort study (DehPCS) from individuals aged 35-70 years after enrollment phase.
Study detail and rational has published elsewhere. 16Briefly, DehPCS is a part of prospective epidemiological research in Iran (PERSIAN) a combination of population-based studies evaluating incidence, prevalence, mortality, and risk factors of common noncommunicable diseases.A total of 3996 permanent residents of Dehgolan town were selected.Subjected with severe illness unable to go through questioning process and/or those who were unwilling to participate were excluded.The DehPCS was gathered socioeconomic, selfreported health status such as medical history, sign and symptoms, and biomarker assessment.The research was performed ethically according to the principles of the Declaration of Helsinki and was approved by the Ethics Committee of the Kurdistan University of Medical Sciences, Kurdistan, Iran (IR.MUK.REC.1400.323).The participants to be included signed the informed consent form.Wealth index was used as a proxy for socioeconomic status of participants.It is a composite measure of household living standards, calculated using easy-to-collect data on family ownership of selected assets.We used principle correspondence analysis to calculate total wealth score of asset data.Then participants were ranked and distributed into three groups of poorest, middle, and richest.

| Measurements and data collection
Salt at table and added sugar were used as a marker of the poor dietary habits.We divided added sugar into the two categories of low (women <25 & men <38) and high (women≥ 25 & men ≥ 38). 17

| Definition of MetS
MetS is a cluster of risk factors that often occur together and increase the risk of developing various health conditions, including cardiovascular diseases and type 2 diabetes.We defined MetS according to the National Cholesterol Education Program Adult Treatment Panel III which was revised by American Heart Association/National Heart, Lung, and Blood Institute in 2005. 18To establish a positive diagnosis of the MetS, three out of five criteria have to be met, as follows: (1) elevated WC ≥ 102 cm in men and ≥88 cm in women, (2) elevated serum triglyceride (TG) ≥ 150 mg/dL and/or on drug treatment for elevated TG, (3) reduced high-density lipoproteincholesterol (HDL-C) < 40 mg/dL in men and <50 mg/dL in women and/or on drug treatment for reduced HDL-C, (4) elevated BP ≥ 130 mmHg systolic BP or 85 mmHg diastolic BP and/or on antihypertensive drug treatment in a patient with a history of hypertension, and (5) elevated fasting plasma glucose ≥ 100 mg/dL and or on drug treatment for elevated glucose.BP was measured using a standard protocol by trained nurses with the participants in sitting position twice in right arm after at least 15 min of resting before measuring.
The mean of two measurements was used as Systolic and diastolic BP.

| Oral health measurement
The oral cavity of all participant undertook a comprehensive clinical examination.The number of decayed teeth (DT), missing teeth (MT), and filled teeth (FT) was diagnosed according to WHO criteria using DMFT index.In line with standard guidelines published by WHO, 19 participants with MT due to reason other than carious extraction such as trauma were excluded from the analysis.Teeth with restoration on one surface and caries on the other were counted as decayed.DMFT score was estimated for the total sample according to the following criteria: 0 = free from any form of dental decay, missing or FT and ≥1 = having one or more of dental decay, missing or FT.Subsequently, subjects were divided into three groups of low (<9), moderate (9-13.9),and high (≥14) DMFT.Participants were also asked about their ODH behavior such as daily brushing, flossing, and use of mouthwash.

| Statistical analysis
Prevalence of MetS was defined across the different oral heath variable as the number of participants with positive criteria for MetS in nominator divided by all participants.The characteristics of participants were reported by count (proportion) and were compared between those with and without MetS using χ 2 test.Logistic regression model was used for calculate odds ratio (OR) with 95% confidence intervals (CI) for MetS, elevated WC, reduced HDL-C, elevated BP, and elevated fast blood sugar (FBS).All analyses were conducted by using Stata software, version 16.0 (Stata Corp).The p < 0.05 was considered a statistically significant, clinically relevant level of association.

| RESULTS
In total, 3992 participates were enrolled in the study.A total of 56.26% of participants were females.Mean ages of female and male participants were 47.98 ± 8.91 and 48.78 ± 8.91, respectively.
T A B L E 1 Prevalence of MetS based on the socioeconomic characteristics, personal and nutritional habit of the participants in DehPCS.Approximately, 91% of participants were married, 31% were illiterate, and 13% had university education.At least 75% of participants had a BMI of 25 or higher, and 46% comorbid with hypertension or dyslipidemia.

| DISCUSSION
The prevalence of MetS among 3992 participants was 34.62%.
According to the results, the MetS prevalence in this study was higher than the national estimate of 23.8% in 2018 28 and 30.4% in 2019, 29 and less than national studies which reported the prevalence of MetS as 38.3% in 2021 30 and 36.9% in 2015 31 in Iran.Similar studies with the same age groups, Ravansar in Kermanshah (33.82%), 32 and Kashan (35.9%) 24 reported equal prevalence of MetS.Studies in Southeast Iran, Zahedan (21.0%), 33 Rural Population in Fasa (24.2%), 34 Sistan and Baluchestan Province (18.3%), 29 Tehran (27%) 35 were low.The prevalence was higher in northern Iran (42.3%) 36 and Bushehr Province (57.8%), 29 and among in food insecurity population (45.5%). 37Also, the prevalence varies throughout the world, as it was reported as 30.6% in Japan, 38 48.8% in Qatar, 39 34.7% in the United States, 40 33.5% in Turkey, 41 and 23% in Sweden. 23Various statistics on the prevalence of MetS may be due to differences in people's age distribution, demographic characteristics, and lifestyles.
In the primary results of the present study, a significant association between moderate and high MT and the increasing MetS has been found.It was associated with three components of the MetS.According to a study in Finland, MT were related to several components of MetS. 42Studies by Zhu in the United States and Hyvärinen stated participants with MT were more likely to have MetS. 43In agreement with previous studies, 42,43 the number of MT was associated with WC, BP, and FBS in this study.A causal relationship may be bidirectional.On the one hand, altered dietary patterns due to tooth MT 44 or uncontrolled BP and FBS in patients may contribute to tooth loss. 20Similarly, the daily brush was related to the WC and HDL-C.Also, MetS was significantly higher in the case with a lower frequency of brushing per day. 14These findings are supported by the results of this study.However, in the presence of demographic and socioeconomic factors, this study failed to observe significant associations.
The findings of this research indicated that individuals with daily flossing, DT, and filled teeth significantly had lower odds of developing MetS.Similar studies reported that the lack of daily flossing was associated with obesity and no dental flossing may increase the likelihood of MetS. 14In contrast, another study shows people with DT and FT had a higher prevalence of MetS than those without.Data from 4716 middle-aged male Japanese indicated decayed teeth were significantly linked to central obesity, high BP, and fasting blood sugar. 9,20A study on MetS and DT in Finland revealed no connection between the two conditions. 45However, these findings are not supported by the results of the present study, and there is no explanation for these contrasts.Untreated tooth decay can indirectly contribute to MetS due to chronic inflammation and infection in the oral cavity.Periodontitis and untreated DT share common risk factors with MetS, such as poor oral hygiene, unhealthy diet, smoking, and certain demographic factors. 9,20It should be noted that there is a direct causal relationship between oral hygiene and long-term tooth decay.
In the presence of demographic and socioeconomic factors, none of them are related to MetS, and only daily flossing significantly decreases the odds of MetS.Data from previous studies suggest that daily flossing is associated with a lower prevalence of periodontitis 25 and inflammation which may contribute directly to the development of MetS. 12The inflammation from periodontitis spreads throughout the body, causing systemic inflammation.This inflammation disrupts metabolic processes, promotes insulin resistance, and contributes to the development of MetS. 46Poor oral health, including untreated T A B L E 3 OR for MetS and its components according to the oral and dental correlates of participants in DehPCS.Adjusted ORs for MetS according to the demographic and socioeconomic factors showed that similarly in other studies, the prevalence of MetS was higher in females than men. 28Although a study in India 47 reported that MetS is higher in men than in women or in Chinese 48 and the Canadian 22 revealed that the prevalence of MetS in men and women is equal, in Iran, women are less active, overweight, and obese. 49Furthermore, in some countries in the region, the traditional dressing may indirectly contribute to obesity.The traditional long and wide dress for women in Iran especially among Kurdish people may hide the fatness of people and decrease their motivation to lose weight.The traditional dressing makes it difficult to observe the size and shape of a woman's body and even it encourages women to gain more weight. 50 the present study, odds of MetS directly increased across age groups.In studies inside and outside Iran, the prevalence of MetS steadily increased with aging. 28,29In South Korea, 51 the incidence of the MetS increased in people with a lower education level.In Swedish, education level was significantly correlated with BP, waistto-hip ratio, HDL-C level, and serum TG level. 26Also, a family history of diabetes was a risk factor for MetS.Previous studies had also found that a history of diabetes is a risk factor for body fatness, Type 2 DM, high BP, lipid abnormalities. 52,53Zuo et al. showed that family history of diabetes was independently associated with MetS. 54though, family history represents the ramifications of numerous genetic variables and the family's clustered lifestyle variables 55 as well, in a cohort study, no association was found. 56 the present study, however, the odds of MetS were higher in people who use salt and excessive added sugar intake was inversely related to the MetS.In a study of Iran, salty and sweet increased the incidence of MetS. 57A study in Korea revealed that high sodium intake is associated with MetS. 58There is strong evidence of the association between the use of salt and high BP/MetS 59,60 which is supported by the present study.However, inversely in other studies, there is a positive association between sugar intake and MetS. 27,61evious studies had also found that total sugar intake is a risk factor for being overweight 27 and incidence of type 2 diabetes. 21May be due to more adherences to the diet and the recommendations of the nutritionist among people with diabetes or high blood sugar, high BP, and obese people, sugar consumption was reduced and in the present study, no connection was found.

| Limitation
The assessment of oral hygiene behavior and other variables relies on self-reported data, which can introduce recall bias or subjective interpretation.While the study adjusts for sociodemographic characteristics, there may be additional confounding factors that influence both ODH and MetS but were not fully accounted for.It's important to note that due to the cross-sectional design of this study and the unclear temporal relationship between the variables, the effect size values should be interpreted cautiously.
Data collection was carried out via a face-to-face interview by local trained interviewer who spoke Kurdish.First, participant were taken a sample of blood and urine after 8-12 h of fasting.Afterward, weight and height and waist circumference (WC) were measured by Seca scale and Stadiometer with accuracy of 0.1 cm.Then, body mass index (BMI) was categorized (body mass [kg]/height [m 2 ]) as: normal weight ≤ 24.9, overweight = 25.0-29.9,and obese ≥ 30.0.They were classified as "smoker" if had a history of smoking ≥ 100 cigarettes life time, ex-smoker, or never smoker.Use of 200 mL of beer or 45 mL of other alcoholic beverage once a week for at least 6 month was considered as "alcohol user."Illicit/illegal drug use including once a week for at least 6 months was classified as "use drugs."Self-reported time on leisure, work, sport, and other activity during 1 week was registered by standard questionnaire.Metabolic equivalent task score per hour per day was calculated based on participant's weight, type, and duration of activities.Then physical activity (PhA) as an everyday practice was categorized into low (24-36.5),moderate (36.6-44.9),and vigorous (≥45).Education level was classified in the following four categories that is, illiterate (zero school years), 1-6 school years, 7-12 school years, and university (>12 school years).
tooth decay, can lead to chronic inflammation and infection within the oral cavity.On the other hand, periodontitis and untreated DT share common risk factors with MetS.These risk factors include poor oral hygiene practices, unhealthy dietary habits, smoking, and certain demographic and socioeconomic factors.What is clear is the direct and causal relationship between oral hygiene and tooth decay in the long term.

Table 1
Vigorous physically active participants have shown less prevalence of MetS.In terms of healthy diet behaviors, participants who use salt at table present higher MetS.Inversely, those who use high amount of add sugar have shown less proportion of MetS.
prevalence was increased by about 25% in the ages over 60 and decreases with education and socioeconomic levels by approximately 31% and 7%, respectively.MetS decreased in current smoker, illicit/ illegal drug user, and alcohol user by 44.47%, 27.72%, and 33.35%, respectively.Proportion of MetS linearly increased with reporting family history of diabetes in first degree and both first and second degree.

Table 3
presents model 1 of crude and adjusted OR for MetS and its component according to the ODH factors.Among all participants, daily brushing, moderate and high MT were significantly increased adjusted odds of high WC by 46%, 58%, and 68%, respectively.Daily flossing and DT were decreased odds of WC by 18% and 15%, independently of other oral and dental factors.Those who have FT had a lower odd of developing high BP.People with moderate and high MT were approximately 1.5 and 2 times likely to develop hypertension.Adjusted odds of elevated FBS were decreased significantly by 18% among those with DT.Like hypertension, elevated FBS was directly affected by moderate and high MT.They added sugar intake was inversely related to the MetS (adjusted OR = 0.8, CI = 0.68-0.95).In the univariable analysis daily brushing, flossing, DT, and FT were inversely related to the MetS and MT directly increased odds of MetS.But in the presence of demographic and socioeconomic factors, multivariable analysis revealed none of them related to the T A B L E 1 (Continued) Abbreviations: BMI, body mass index; DehPCS, Dehgolan prospective cohort study; MET, metabolic equivalent task; MetS, metabolic syndrome.
T A B L E 2 Prevalence of MetS based on ODH factors of the participants in DehPCS.
OR for MetS according to the sociodemographic, ODH factors, personal and nutritional habits in participants of DehPCS.
CI, confidence interval; DehPCS, Dehgolan prospective cohort study; DMFT, decayed, missing, filled teeth; MET, metabolic equivalent task; MetS, metabolic syndrome; ODH, oral and dental health; OR, odds ratio.a Adjusted for gender; age groups; marital status; education years; economic status; illicit/illegal drug use; alcohol use; family history of diabetes; METhour; number of meals per day; salt at table; added sugar; daily brush; use moth wash; use flossing; has denture; DT; FT; and MT.