Abstract
Background
To evaluate the association of dental diseases and oral hygiene care with incidence of heart failure (HF) among patients with type 2 diabetes.
Methods and Results
This study included 173 927 patients with type 2 diabetes aged ≥40 years, who underwent Korean National Health Insurance Service health examinations in 2008 and were followed up until the end of 2017. Hazard ratios (HRs) and 95% CIs for HF were estimated using multivariable Cox proportional hazards regression analysis. During a median follow‐up of 9.3 years, 1.94% of participants developed HF. An increased number of missing teeth was associated with a higher risk of HF (P<0.001). HRs of HF increased among individuals with ≥15 missing teeth (HR, 1.37 [95% CI, 1.14–1.64]) compared with those without missing teeth. Decreased risk of HF was observed in individuals with ≥1 time/year of professional dental cleaning (HR, 0.93 [95% CI, 0.87–0.99]) and in those with ≥2 times/d of toothbrushing (HR, 0.90 [95% CI, 0.82–0.98]) compared with those without these practices. While combined presence of missing teeth and periodontal disease (P=0.004) or dental caries (P=0.007) increased HF risk, combined oral hygiene care was associated with further HF risk reduction (P=0.024). Better oral hygiene care was associated with decreased HF risk, even as the number of missing teeth increased (P<0.001).
Conclusions
Among patients with type 2 diabetes, dental diseases and oral hygiene care are important determinants of HF development. Dental disease management and good oral care may prevent HF in patients with type 2 diabetes.
Keywords: dental caries, heart failure, missing teeth, oral hygiene care, periodontal disease, type 2 diabetes
Subject Categories: Heart Failure
Nonstandard Abbreviations and Acronyms
- NHIS
National Health Insurance Service
- RD
risk difference
Clinical Perspective.
What Is New?
In this large nationwide cohort study of patients with type 2 diabetes (n=173 927), the risk of heart failure (HF) increased among individuals with dental diseases compared with those without these conditions.
The risk of HF decreased with regular oral hygiene care among patients with type 2 diabetes.
While combined presence of dental diseases increased HF risk, combined oral hygiene care was associated with further risk reduction for HF among patients with type 2 diabetes.
What Are the Clinical Implications?
Dental diseases and oral hygiene care are important determinants of HF development among patients with type 2 diabetes.
Dental disease management and good oral care may prevent HF among patients with type 2 diabetes.
Periodontal diseases are caused by the formation of bacterial plaques between the tooth and gingiva, which triggers a host‐mediated inflammatory response that may damage the deeper dental support tissues and eventually result in dental caries and tooth loss. 1 As a widespread illness with chronic inflammatory properties, periodontal disease can cause not only transient bacteremia but systemic inflammation and endothelial dysfunction, which are possible underlying mechanisms of atherogenesis. 2 This disease may be influenced by several factors such as poor oral health behaviors, age, smoking, and socioeconomic status. 3 Of them, oral hygiene behaviors, such as toothbrushing and professional cleaning, are known to reduce periodontal diseases, dental caries, tooth loss, 4 and the pathogens of periodontal diseases. 5 Additionally, oral hygiene behaviors were reported to be associated with markers of systemic inflammation. 6
Heart failure (HF) is the leading cause of hospitalization and increasing health costs in Western countries. 7 Its prevalence in the United States is 2.4% in adults aged ≥19 years. Although the prevalence of HF in South Korea is low, it has increased from 0.8% in 2002 to 1.5% in 2015. 8 Type 2 diabetes is a well‐established risk factor of HF. 9 In this regard, HF prevalence is 11.8% among patients with type 2 diabetes and 3.2% among the general populations. 10 Compared with individuals without type 2 diabetes, those with type 2 diabetes have been reported to have a 2.5‐fold increase in HF incidence. 11 Moreover, type 2 diabetes increases the risk of adverse prognosis of HF, including hospitalization and mortality. 12 Therefore, it is important to prevent HF among the patients with type 2 diabetes.
Some studies have shown that dental diseases increase the risk of cardiovascular diseases (CVDs) 13 and that good oral hygiene behaviors reduce them. 14 However, few studies have evaluated representative nationwide data, and there is limited evidence regarding HF risk in relation to dental diseases and oral hygiene behaviors among patients with type 2 diabetes. Therefore, this study evaluated the association of dental diseases and oral hygiene care (alone or in combination) with incident HF among patients with type 2 diabetes using nationwide cohort data in Korea.
Methods
Data Availability
Restrictions apply to the availability of Korean National Health Insurance Service (NHIS) data because of ethical issues and data protection regulations according to the policy of Korean NHIS. Therefore, these data have been made accessible to qualified researchers who submitted a study protocol approved by official review committees.
Data Source and Study Population
This study retrospectively evaluated nationwide cohort data of patients with type 2 diabetes from the Korean NHIS database. The NHIS was established in 2000 as a single universal insurer in South Korea and provides at least biennial health examinations for all insured South Koreans. Therefore, it retains an extensive medical database of nearly the entire South Korean population on demographic characteristics, health examinations, disease diagnoses, medical treatments, and procedures based on medical claims according to International Classification of Diseases, Tenth Revision (ICD‐10) codes.
From this database, we initially identified 3 913 183 individuals who underwent national health examinations and oral health screening offered by the NHIS between January 1, 2008, and December 31, 2008. We excluded individuals with missing data for any of the study variables (n=736 081) and those aged <40 years (n=618 200). We then excluded individuals without type 2 diabetes (n=2 384 539). Type 2 diabetes was defined based on fasting serum glucose concentration of ≥126 mg/dL or at least 1 medication prescription claim per year with the ICD‐10 codes E11–E14. 15 Furthermore, we excluded patients who had been diagnosed with HF before 2008 (n=436). Finally, 173 927 individuals (125 948 men and 47 979 women) were eligible for the analyses and were followed up until December 31, 2017. This study adhered to the principles of the Declaration of Helsinki and was approved by the Institutional Review Board of Korea University Anam Hospital (No. 2020AN0293). The requirement for informed consent was waived because we used anonymized data of the participants.
Study Outcome
The outcome of our study was incident HF diagnosed between January 1, 2008 and December 31, 2017. HF presence was identified with ICD‐10 code I50 as the primary diagnosis during hospitalization.
Definitions of Dental Diseases and Oral Hygiene Care
Participants responded to a self‐reported survey, including dental visits and oral hygiene care, and an oral examination was conducted by professional dentists. Dental diseases included periodontal disease, dental caries, and tooth loss. Periodontal disease was classified as present or absent on the basis of oral examination results. The presence of dental caries was categorized as yes or no. The number of missing teeth was categorized as 0, 1–7, 8–14, or ≥15. Oral hygiene care consisted of dental check‐ups, professional dental cleaning, and toothbrushing. Dental check‐ups and professional dental cleaning were categorized as <1 or ≥1 time per year. The frequency of toothbrushing was categorized as 0–1 or ≥2 times per day.
Covariates
The NHIS database contains detailed information on demographic characteristics and lifestyles, which were evaluated using standardized self‐administered questionnaires. The lowest 20% of the income range of the participants was classified as low income, and the remaining was considered non‐low income. Smoking status was classified as either current smoker or nonsmoker based on smoking history. Alcohol drinkers were defined as individuals consuming >0 g per week of alcohol. Regular physical activity was defined as high‐intensity exercise for ≥3 days per week or moderate‐intensity exercise for ≥5 days per week. Health examinations were conducted by a qualified medical staff and included anthropometric and laboratory measurements. Height, weight, and waist circumference were measured, and body mass index was calculated as weight divided by height squared (kg/m2). Systolic and diastolic blood pressures were measured while the participants were seated after ≥5 minutes of rest. Blood samples were obtained after overnight fasting to determine the serum concentrations of glucose and total cholesterol.
Comorbidities were identified according to health examination results and medical claims for disease diagnoses and medication prescriptions. Hypertension was defined as a blood pressure of ≥140/90 mm Hg or at least 1 medication prescription claim per year with the ICD‐10 codes I10–I13 or I15. Dyslipidemia was defined as a total cholesterol concentration of ≥240 mg/dL or at least one medication prescription claim per year with the ICD‐10 code E78. Chronic kidney disease was defined by the ICD‐10 codes N18 or N19. CVD was identified based on the ICD‐10 codes for myocardial infarction (I21 or I22) or stroke (I63 or I64). The antidiabetic medications were assessed with insulin use (categorized as user or non‐user) and the number of oral antidiabetic medications (categorized as 0–1 or ≥2).
Statistical Analysis
All statistical analyses were performed using the SAS software (version 9.4; SAS Institute, Cary, NC). The baseline characteristics according to the prevalence of periodontal diseases are reported as means±SDs for continuous variables or numbers (percentages) for categorical variables. Continuous variables were compared using independent t‐test, and categorical variables using the Chi‐squared test. HF incidence was calculated by dividing the number of events by 1000 person‐years. We plotted Kaplan–Meier curves to identify cumulative incidence probabilities of HF according to dental diseases and oral hygiene care, and examined their differences by log‐rank test. We performed a multivariable Cox proportional hazards regression analysis to evaluate the association of dental diseases and oral hygiene care with the risk of HF incidence. The results were reported as hazard ratios (HRs) and 95% CIs. Two models were used: model 1 was not adjusted for any variables; model 2 was adjusted for age, sex, smoking status, alcohol consumption, physical activity, income, body mass index, hypertension, dyslipidemia, chronic kidney disease, CVD, and antidiabetic medication (number of oral antidiabetic medication and insulin use). We also presented 5‐year risk difference (RD) and SE to show effect size of difference according to dental diseases and oral hygiene care. Additionally, we analyzed the associations of combined dental diseases and oral hygiene care with the risk of incident HF incidence. Differences were considered statistically significant at P<0.05.
Results
Baseline Characteristics
Table 1 presents the baseline characteristics of 173 927 eligible participants with type 2 diabetes based on the presence of periodontal diseases. Among them, 22.6% (n=39 242) had periodontal diseases. The mean age and proportion of men were higher in individuals with periodontal diseases than those without. Individuals with periodontal diseases were less likely to be current smokers and alcohol drinkers, and more likely to perform regular exercise, compared with those without periodontal diseases. Individuals with periodontal diseases had higher proportions of hypertension, dyslipidemia, and CVD compared with those without periodontal diseases. The proportions of participants with the use of ≥2 oral antidiabetic medications and the use of insulin were higher among individuals with periodontal diseases than among those without. Participants with periodontal diseases were likely to have more missing teeth, to undergo regular dental check‐up and professional dental cleaning, and to brush their teeth frequently.
Table 1.
Baseline Characteristics According to the Presence of Periodontal Diseases in Individuals With Type 2 Diabetes
| Periodontal diseases | ||
|---|---|---|
| No | Yes | |
| n | 134 685 | 39 242 |
| Age, y | 62.8±11.1 | 65.3±10.1 |
| Male sex | 96 848 (71.9) | 29 100 (74.2) |
| Low income | 19 564 (14.5) | 5555 (14.2) |
| Current smoker | 39 983 (29.7) | 11 315 (28.8) |
| Alcohol drinker | 50 918 (37.8) | 14 476 (36.9) |
| Regular exerciser | 79 446 (59.0) | 24 515 (62.5) |
| Body mass index, kg/m2 | 25.0±3.2 | 25.0±3.1 |
| Waist circumference, cm | 85.6±8.4 | 85.8±8.0 |
| Systolic blood pressure, mm Hg | 129.0±15.6 | 128.4±15.3 |
| Diastolic blood pressure, mm Hg | 79.7±10.1 | 79.1±10.0 |
| Fasting glucose, mg/dL | 148.5±50.0 | 147.6±50.4 |
| Total cholesterol, mg/dL | 196.8±40.9 | 194.8±39.8 |
| Hypertension | 73 764 (54.8) | 22 620 (57.6) |
| Dyslipidemia | 46 378 (34.4) | 14 418 (36.7) |
| Chronic kidney disease | 1142 (0.9) | 327 (0.83) |
| Cardiovascular disease | 6872 (5.1) | 2526 (6.4) |
| ≥2 Oral antidiabetic medication | 46 656 (34.6) | 16 038 (40.9) |
| Insulin use | 11 569 (8.6) | 3725 (9.5) |
| Dental caries (yes) | 27 810 (20.7) | 5823 (14.8) |
| No. of missing teeth | ||
| 0 | 103 399 (76.8) | 27 526 (70.1) |
| 1–7 | 27 166 (20.2) | 10 260 (26.2) |
| 8–14 | 2404 (1.8) | 988 (2.5) |
| ≥15 | 1716 (1.3) | 468 (1.2) |
| Dental checkup (≥1/y) | 53 603 (39.8) | 30 006 (76.5) |
| Professional dental cleaning (≥1/y) | 33 015 (24.5) | 19 182 (48.9) |
| Frequency of toothbrushing | ||
| 0–1/d | 19 505 (14.5) | 5264 (13.4) |
| ≥2/d | 115 180 (85.5) | 33 978 (86.6) |
Values were presented as means±SDs or numbers (percentages).
Associations of Dental Diseases and Oral Hygiene Care With HF Risk
In Figure 1, the cumulative incidence probabilities of HF were higher in individuals with periodontal diseases and an increased number of missing teeth than those without, which were lower in individuals with good oral hygiene care than those without (log‐rank P<0.001).
Figure 1. Kaplan–Meier curves showing cumulative incidence probabilities of heart failure according to dental diseases and oral hygiene care.
Periodontal diseases (A), dental caries (B), number of missing teeth (C), professional dental cleaning (D), and toothbrushing among patients with type 2 diabetes (E).
Table 2 shows the longitudinal associations of dental diseases and oral hygiene care with the risk of HF. Of total participants with type 2 diabetes, 3379 (1.94%) individuals developed HF during a median follow‐up of 9.3 years (interquartile range, 9.1–9.6 years). HRs for HF increased by 37% among those with ≥15 missing teeth (HR, 1.37 [95% CI, 1.14–1.64]; 5‐year RD 0.36, SE 0.12), compared with those without missing teeth. The HRs for HF were significantly higher as the number of missing teeth increased (P<0.001). HRs of HF decreased by 7% among individuals who underwent professional dental cleaning ≥1 time/year of (HR, 0.93 [95% CI, 0.87–0.99]; 5‐year RD −0.07, SE 0.04) and by 10% among those who brushed their teeth ≥2 times/d (HR, 0.90 [95% CI, 0.82–0.98]; 5‐year RD −0.07, SE 0.05), compared with those who did not undergo regular professional dental cleaning or >1 time/d.
Table 2.
Associations of Dental Diseases and Oral Hygiene Care With the Risk of Heart Failure Among Patients With Type 2 Diabetes
| n | Event | Person‐years | IR* | HR (95% CI) | 5‐Year risk difference (SE) | ||
|---|---|---|---|---|---|---|---|
| Model 1† | Model 2‡ | ||||||
| Periodontal diseases | |||||||
| No | 134 685 | 2523 | 1 213 068 | 2.1 | 1 (reference) | 1 (reference) | … |
| Yes | 39 242 | 856 | 352 792 | 2.4 | 1.17 (1.08–1.26) | 1.03 (0.95–1.11) | 0.03 (0.04) |
| P value | <0.001 | 0.473 | |||||
| Dental caries | |||||||
| No | 140 294 | 2814 | 1 262 210 | 2.2 | 1 (reference) | 1 (reference) | … |
| Yes | 33 633 | 565 | 303 650 | 1.9 | 0.84 (0.76–0.91) | 1.02 (0.93–1.12) | 0.02 (0.05) |
| P value | <0.001 | 0.678 | |||||
| No. of missing teeth | |||||||
| 0 | 130 925 | 2424 | 1 182 832 | 2.0 | 1 (reference) | 1 (reference) | … |
| 1–7 | 37 426 | 705 | 336 296 | 2.1 | 1.02 (0.94–1.11) | 0.92 (0.85–1.00) | −0.08 (0.04) |
| 8–14 | 3392 | 123 | 29 175 | 4.2 | 2.06 (1.72–2.47) | 1.16 (0.97–1.39) | 0.16 (0.11) |
| ≥15 | 2184 | 127 | 17 557 | 7.2 | 3.56 (2.98–4.26) | 1.37 (1.14–1.64) | 0.36 (0.12) |
| P value | <0.001 | <0.001 | |||||
| Professional dental cleaning | |||||||
| <1/y | 121 730 | 2536 | 1 091 825 | 2.3 | 1 (reference) | 1 (reference) | … |
| ≥1/y | 52 197 | 843 | 474 035 | 1.8 | 0.77 (0.71–0.83) | 0.93 (0.87–0.99) | −0.07 (0.04) |
| P value | <0.001 | 0.033 | |||||
| Frequency of toothbrushing | |||||||
| 0–1/d | 24 769 | 615 | 219 570 | 2.8 | 1 (reference) | 1 (reference) | … |
| ≥2/d | 149 158 | 2764 | 1 346 290 | 2.1 | 0.73 (0.67–0.80) | 0.90 (0.82–0.98) | −0.11 (0.05) |
| P value | <0.001 | 0.018 | |||||
HR indicates hazard ratio; and IR, incidence rate.
Incidence per 1000 person‐years.
Model 1 was not adjusted for any variables.
Model 2 was adjusted for age, sex, smoking status, alcohol consumption, physical activity, income, body mass index, dyslipidemia, chronic kidney disease, cardiovascular disease, number of oral antidiabetic medication used, and insulin use.
Associations Between the Combined Dental Diseases or Oral Hygiene Care and the Risk of HF
Table 3 presents the association of the combined presence of dental diseases or combined oral hygiene care with HF risk. The HRs for HF increased by 20% among individuals with both periodontal diseases and dental caries (HR, 1.20 [95% CI, 1.01–1.43]; 5‐year RD 0.20, SE 0.10), even after adjusting for potential confounding variables, compared with those without any of these diseases. HRs for HF increased in participants with both periodontal diseases and a higher number of missing teeth (P=0.004). HR for HF significantly increased by 46% in individuals with periodontal disease and ≥15 missing teeth (HR, 1.46 [95% CI, 1.01–2.13]; 5‐year RD 0.45, SE 0.27) compared with those without any of these conditions. A similar trend was observed for the combined presence of dental caries and missing teeth. Dental caries and a higher number of missing teeth were associated with higher HF risk (P=0.007).
Table 3.
Associations of Combined Presence of Dental Diseases or Combined Oral Hygiene Care With the Risk of Heart Failure Among Patients With Type 2 Diabetes
| n | Event | IR* | HR (95% CI)† | 5‐Year risk difference (SE) | ||
|---|---|---|---|---|---|---|
| Combined dental diseases | ||||||
| Periodontal disease | Dental caries | |||||
| No | No | 106 875 | 2095 | 2.2 | 1 (reference) | … |
| Yes | 27 810 | 428 | 1.7 | 0.97 (0.88–1.08) | −0.03 (0.05) | |
| Yes | No | 33 419 | 719 | 2.4 | 1.00 (0.92–1.08) | −0.00 (0.04) |
| Yes | 5823 | 137 | 2.6 | 1.20 (1.01–1.43) | 0.20 (0.10) | |
| P value | 0.177 | |||||
| Periodontal disease | No. of missing teeth | |||||
| No | 0 | 103 399 | 1832 | 2.0 | 1 (reference) | … |
| 1–7 | 27 166 | 508 | 2.1 | 0.95 (0.86–1.04) | −0.05 (0.05) | |
| 8–14 | 2404 | 84 | 4.1 | 1.12 (0.90–1.40) | 0.12 (0.12) | |
| ≥15 | 1716 | 99 | 7.2 | 1.37 (1.11–1.68) | 0.35 (0.14) | |
| Yes | 0 | 27 526 | 592 | 2.4 | 1.05 (0.96–1.15) | 0.05 (0.05) |
| 1–7 | 10 260 | 197 | 2.1 | 0.91 (0.78–1.05) | −0.09 (0.07) | |
| 8–14 | 988 | 39 | 4.6 | 1.30 (0.95–1.79) | 0.29 (0.20) | |
| ≥15 | 468 | 28 | 7.3 | 1.46 (1.01–2.13) | 0.45 (0.27) | |
| P value | 0.004 | |||||
| Dental caries | No. of missing teeth | |||||
| No | 0 | 109 040 | 2101 | 2.1 | 1 (reference) | … |
| 1–7 | 26 904 | 515 | 2.1 | 0.91 (0.83–1.00) | −0.09 (0.05) | |
| 8–14 | 2445 | 87 | 4.1 | 1.17 (0.95–1.45) | 0.16 (0.12) | |
| ≥15 | 1905 | 111 | 7.2 | 1.38 (1.14–1.67) | 0.37 (0.13) | |
| Yes | 0 | 21 885 | 323 | 1.6 | 1.02 (0.91–1.15) | 0.02 (0.06) |
| 1–7 | 10 522 | 190 | 2.0 | 0.96 (0.83–1.12) | −0.04 (0.07) | |
| 8–14 | 947 | 36 | 4.5 | 1.16 (0.83–1.61) | 0.15 (0.19) | |
| ≥15 | 279 | 16 | 7.4 | 1.32 (0.81–2.16) | 0.31 (0.32) | |
| P value | 0.007 | |||||
| Combined oral hygiene care | ||||||
| Professional dental cleaning | Toothbrushing | |||||
| <1/y | 0–1/d | 18 791 | 477 | 2.9 | 1 (reference) | … |
| ≥2/d | 102 939 | 2059 | 2.2 | 0.92 (0.83–1.02) | −0.08 (0.05) | |
| ≥1/y | 0–1/d | 5978 | 138 | 2.6 | 1.01 (0.83–1.22) | 0.01 (0.10) |
| ≥2/d | 46 219 | 705 | 1.7 | 0.85 (0.75–0.95) | −0.17 (0.06) | |
| P value | 0.024 | |||||
HR indicates hazard ratio; and IR, incidence rate.
Incidence per 1000 person‐years.
Hazard ratios (95% CIs) were calculated using a multivariable Cox hazards regression model that was adjusted for age, sex, smoking status, alcohol consumption, physical activity, income, body mass index, dyslipidemia, chronic kidney disease, cardiovascular disease, number of oral antidiabetic medication used, and insulin use.
The impact of combined oral hygiene care on HF risk is also shown in Table 3. Compared with those who did not receive regular professional dental cleaning per year and did brush their teeth 0–1 time per day, individuals who both received ≥1 time of professional dental cleaning annually and performed ≥2 times of daily toothbrushing had an ≈15% decrease in HF risk (HR, 0.85 [95% CI, 0.75–0.95]; 5‐year RD −0.17, SE 0.06).
Associations of the Combined Presence of Dental Diseases and Oral Hygiene Care With HR Risk
In Figure 2, better oral hygiene care was associated with decreased risk of HF, even when individuals had periodontal diseases (P=0.047 for daily toothbrushing) or an increasing number of missing teeth (P<0.001 for professional dental cleaning and daily toothbrushing). Compared with those without missing teeth but with poor oral hygiene care, individuals with ≥15 missing teeth and poor oral hygiene care had an increased HF risk (HR, 1.46 [95% CI, 1.20–1.77] for <1 time/year of professional dental cleaning; HR, 1.50 [95% CI, 1.09–2.06] for 0–1 time of daily toothbrushing). However, these associations were not observed among individuals with ≥15 missing teeth and better oral hygiene care (HR, 0.88 [95% CI, 0.52–1.49] for ≥1 time/year of professional dental cleaning; HR, 1.16 [95% CI, 0.92–1.47] for ≥2 times of daily toothbrushing).
Figure 2. Associations between combined status of dental diseases and oral hygiene care and the risk of heart failure among patients with type 2 diabetes.
Hazard ratios (95% CIs) were calculated using a multivariable Cox hazards regression model that was adjusted for age, sex, smoking status, alcohol consumption, physical activity, income, body mass index, dyslipidemia, chronic kidney disease, cardiovascular disease, number of oral antidiabetic medication used, and insulin use.
Discussion
This large population‐based cohort study revealed that the presence of a higher number of missing teeth were associated with increased HF risk among patients with type 2 diabetes. Furthermore, the combined presence of dental diseases increased the HF risk. Conversely, oral hygiene care, such as professional dental cleaning and toothbrushing, were associated with a decreased HF risk, and the combination of these practices further reduced the risk of HF. Moreover, the increased HF risks caused by combined dental diseases and poor oral hygiene care were attenuated by better oral hygiene care. Therefore, our findings suggest that dental diseases may be independent risk factors for incident HF among patients with type 2 diabetes, and good oral hygiene care may play a protective role against HF development.
There has been no study on the association between oral health factor and HF incidence in patients with type 2 diabetes. However, several previous studies have shown that periodontal diseases, dental caries, and missing teeth were associated with increased risks of CVDs in the general population. 13 A systematic review of 12 studies showed that patients with periodontal diseases and dental caries had an increased risk of atherosclerotic CVD compared with those without these conditions. 16 A study which compared the panoramic radiographs of 850 patients with and without myocardial infarction, the myocardial infarction risk among patients with periodontal diseases was 1.3 times higher than that among those without this condition after adjusting for confounding variables (odds ratio: 1.28 [95% CI, 1.03–1.60]). 17 A study on 514 866 Koreans revealed that the greater number of dental diseases and missing teeth was associated with increased risk of major cardiovascular events, including cardiovascular mortality, myocardial infarction, HF, and stroke. 18 Further, a study of 15 456 patients with stable coronary disease reported that every increase in the number of missing teeth was associated with an increased risk of cardiovascular mortality (HR, 1.17 [95% CI, 1.04–1.24]). 19 In line with these previous findings, our study found that dental diseases such as periodontal diseases and missing teeth were associated with higher risk of HF in patients with type 2 diabetes. Although significant associations between periodontal diseases and dental caries and the risk of HF was not observed in our study, HF risk was significantly associated with the combined presence of these diseases and increased number of missing teeth.
Good oral hygiene care has been reported to reduce periodontal diseases, dental caries, and missing teeth. 4 , 14 Therefore, some guidelines recommend oral hygiene care, such as toothbrushing ≥2/d and regular professional dental cleaning, to reduce dental diseases. 20 Furthermore, several Asian studies reported good oral hygiene care (toothbrushing) may reduce the risk of major risk factors for HF such as dyslipidemia and diabetes. 21 , 22 A previous national population‐based study of 11 869 adults showed that less frequent toothbrushing was associated with higher concentrations of C‐reactive protein and fibrinogen, 2 markers of systemic inflammation. 6 Therefore, infrequent toothbrushing has been suggested to be associated with an increased risk of CVDs. Meanwhile, a study reported that the risk of cardiovascular events decreased by 9% among participants who performed toothbrushing ≥1 time per day and 14% among those who received professional dental cleaning ≥1 times per year. 19 These findings suggest that good oral hygiene care might prevent CVDs. In addition, a few studies showed that good oral hygiene care in dental diseases was associated with decreased risk of cardiovascular events including HF in the general population. 2 , 18 Therefore, our study provides further evidence that good oral hygiene care decreased HF risk when dental diseases progressed irreversibly among patients with type 2 diabetes.
Some pathological mechanisms of dental diseases may induce atherosclerosis, CVD, and HF. 23 , 24 First, dental diseases cause systemic inflammation, which releases C‐reactive protein and interleukin‐6, subsequently resulting in atherosclerotic CVD. One study showed that patients with more tooth loss had higher levels of C‐reactive protein. 25 Second, the human microbiota participated in HF development. 26 Various bacteria species of the oral microbiome produce trimethylamine‐N‐oxide, and a higher level of circulating trimethylamine‐N‐oxide represented a significant risk factor for atherosclerosis and HF. 27 Several bacterial toxins in the oral cavity, such as Fusobacterium and members of the Lachnospiraceas families, were associated with increased cholesterol level, leading to atherosclerotic plaques. 28 Conversely, oral hygiene care might attenuate chronic inflammation and modify the oral microbiome. 29 , 30
Despite its many advantages, our study had several limitations. First, underdiagnosis or overdiagnosis was possible in some cases, as the NHIS database relies on the diagnostic code assigned by physicians to identify diseases. Second, the observational study design might prevent causality‐related conclusions. However, we excluded individuals with previous HF diagnosis to reduce the reverse causality issue. Third, data on inflammation or microbial environment which may affect HF risk, could not be considered because they were not included in the Korean NHIS database. In addition, the data on echocardiography results including ejection fraction were not available from the database, we could not assess the types of HF. Fourth, because oral hygiene care was evaluated using a questionnaire, recall bias could not be excluded. Finally, our study was conducted in a South Korean population, and similar results may not be observed in other regional or ethnic populations. Nevertheless, this study evaluated a large nationwide representative cohort of South Koreans, allowing the assessment of the associations of dental diseases and oral hygiene care with the risk of HF in patients with type 2 diabetes. In particular, although previous studies had focused on the association between oral health and CVD in the general population, our study showed the associations between combined status of various oral health variables and HF risk in patients with type 2 diabetes who are more vulnerable to both dental disease and CVDs. HF may be the first symptom of CVD among patients with type 2 diabetes. 31 Hospitalization due to HF increased among patients with type 2 diabetes compared with that of patients without type 2 diabetes. 12 Our study showed that dental disease management and good oral hygiene care might help decrease HF risk in type 2 diabetes.
In conclusion, we found that dental diseases and poor oral hygiene care were associated with HF incidence among South Korean patients with type 2 diabetes. While a further increase in HF risk was observed in patients with combined dental diseases, HF risk was lowered by a combination of better oral health practices. Furthermore, even in the presence of dental diseases, good oral hygiene care decreased HF risk. Therefore, dental diseases and oral hygiene care may be important determinants of HF development among patients with type 2 diabetes. Improving oral health by the dental disease management and good oral health care might help prevent HF in patients with type 2 diabetes.
Sources of Funding
This study was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (NRF‐2020R1A2C2009296) and the Bio & Medical Technology Development Program of the NRF and funded by the Korean government (MSIT) (NRF‐2017M3A9F1027902) (Sang Ho Jun). This study was also supported by the Seokchunnanum Foundation (SCY2112P) (Ga Eun Nam). The study funders had no role in the study design, data collection, data analyses, and interpretation of the study data.
Disclosures
None.
Acknowledgments
Y.H. and J.E.Y. contributed to the study conception, literature search, collection and assembly of data, and wrote the original draft. S.M.K., H.S.P., K.H.C., and J.‐S.A. discussed the results and commented on the manuscript. S.H.P. and K.H. contributed data analyses and interpretation. S.H.J. and G.E.N. contributed to the concept, design, data collection, critical revision of the manuscript, supervised the study, and take responsibility for the study. All authors approved the final version of the manuscript and agreed to its submission for publication.
Y. Huh and J. E. Yoo contributed equally.
For Sources of Funding and Disclosures, see page 9.
Contributor Information
Sang Ho Jun, Email: junsang@korea.ac.kr.
Ga Eun Nam, Email: namgaaa@hanmail.net.
References
- 1. Cotti E, Dessì C, Piras A, Mercuro G. Can a chronic dental infection be considered a cause of cardiovascular disease? A review of the literature. Int J Cardiol. 2011;148:4–10. doi: 10.1016/j.ijcard.2010.08.011 [DOI] [PubMed] [Google Scholar]
- 2. Friedewald VE, Kornman KS, Beck JD, Genco R, Gold A, Libby P, Offenbacher S, Ridker PM, Van Dyke TE, Roberts WC, et al. The American Journal of Cardiology and Journal of Periodontology Editors' Consensus: periodontitis and atherosclerotic cardiovascular disease. Am J Cardiol. 2009;104:59–68. doi: 10.1016/j.amjcard.2009.05.002 [DOI] [PubMed] [Google Scholar]
- 3. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366:1809–1820. doi: 10.1016/S0140-6736(05)67728-8 [DOI] [PubMed] [Google Scholar]
- 4. Chapple IL, Van der Weijden F, Doerfer C, Herrera D, Shapira L, Polak D, Madianos P, Louropoulou A, Machtei E, Donos N, et al. Primary prevention of periodontitis: managing gingivitis. J Clin Periodontol. 2015;42:S71–S76. doi: 10.1111/jcpe.12366 [DOI] [PubMed] [Google Scholar]
- 5. Socransky SS, Haffajee AD, Teles R, Wennstrom JL, Lindhe J, Bogren A, Hasturk H, van Dyke T, Wang X, Goodson JM. Effect of periodontal therapy on the subgingival microbiota over a 2‐year monitoring period. I. Overall effect and kinetics of change. J Clin Periodontol. 2013;40:771–780. doi: 10.1111/jcpe.12117 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. de Oliveira C, Watt R, Hamer M. Toothbrushing, inflammation, and risk of cardiovascular disease: results from Scottish Health Survey. BMJ. 2010;340:c2451. doi: 10.1136/bmj.c2451 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Ambrosy AP, Fonarow GC, Butler J, Chioncel O, Greene SJ, Vaduganathan M, Nodari S, Lam CSP, Sato N, Shah AN, et al. The global health and economic burden of hospitalizations for heart failure: lessons learned from hospitalized heart failure registries. J Am Coll Cardiol. 2014;63:1123–1133. doi: 10.1016/j.jacc.2013.11.053 [DOI] [PubMed] [Google Scholar]
- 8. Lee JH, Lim NK, Cho MC, Park HY. Epidemiology of heart failure in Korea: present and future. Korean Circ J. 2016;46:658–664. doi: 10.4070/kcj.2016.46.5.658 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Groenewegen A, Rutten FH, Mosterd A, Hoes AW. Epidemiology of heart failure. Eur J Heart Fail. 2020;22:1342–1356. doi: 10.1002/ejhf.1858 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Thrainsdottir IS, Aspelund T, Thorgeirsson G, Gudnason V, Hardarson T, Malmberg K, Sigurdsson G, Ryden L. The association between glucose abnormalities and heart failure in the population‐based Reykjavik study. Diabetes Care. 2005;28:612–616. doi: 10.2337/diacare.28.3.612 [DOI] [PubMed] [Google Scholar]
- 11. Nichols GA, Gullion CM, Koro CE, Ephross SA, Brown JB. The incidence of congestive heart failure in type 2 diabetes: an update. Diabetes Care. 2004;27:1879–1884. doi: 10.2337/diacare.27.8.1879 [DOI] [PubMed] [Google Scholar]
- 12. MacDonald MR, Petrie MC, Varyani F, Ostergren J, Michelson EL, Young JB, Solomon SD, Branger CB, Swedberg K, Yusuf S, et al. Impact of diabetes on outcomes in patients with low and preserved ejection fraction heart failure: an analysis of the Candesartan in Heart failure: Assessment of Reduction in Mortality and morbidity (CHARM) programme. Eur Heart J. 2008;29:1377–1385. doi: 10.1093/eurheartj/ehn153 [DOI] [PubMed] [Google Scholar]
- 13. Dietrich T, Webb I, Stenhouse L, Pttni A, Ready D, Wanyonyi K, White S, Gallagher JE. Evidence summary: the relationship between oral and cardiovascular disease. Br Dent J. 2017;222:381–385. doi: 10.1038/sj.bdj.2017.224 [DOI] [PubMed] [Google Scholar]
- 14. Axelsson P, Nyström B, Lindhe J. The long‐term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults: results after 30 years of maintenance. J Clin Periodontol. 2004;31:749–757. doi: 10.1111/j.1600-051X.2004.00563.x [DOI] [PubMed] [Google Scholar]
- 15. Bae JH, Han K, Ko SH, Yand YS, Choi JH, Choi KM, Kwon HS, Won KC. Diabetes fact sheet in Korea 2021. Diabetes Metab J. 2022;46:417–426. doi: 10.4093/dmj.2022.0106 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Dietrich T, Sharma P, Walter C, Weston P, Beck J. The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. J Periodontol. 2013;84:S70–S84. doi: 10.1902/jop.2013.134008 [DOI] [PubMed] [Google Scholar]
- 17. Rydén L, Buhlin K, Ekstrand E, de Faire U, Gustafsson A, Holmer J, Kjellström B, Lindahl B, Norhammar A, Nygren A, et al. Periodontitis increases the risk of a first myocardial infarction: a report from the PAROKRANK study. Circulation. 2016;133:576–583. doi: 10.1161/CIRCULATIONAHA.115.020324 [DOI] [PubMed] [Google Scholar]
- 18. Park SY, Kim SH, Kang SH, Yoon CH, Lee HJ, Yun PY, Youn TJ, Chae IH. Improved oral hygiene care attenuates the cardiovascular risk of oral health disease: a population‐based study from Korea. Eur Heart J. 2019;40:1138–1145. doi: 10.1093/eurheartj/ehy836 [DOI] [PubMed] [Google Scholar]
- 19. Vedin O, Hagström E, Budaj A, Denchev S, Harrington RA, Koenig W, Soffer J, Sritara P, Stebbins A, Stewart RH, et al. Tooth loss is independently associated with poor outcomes in stable coronary heart disease. Eur J Prev Cardiol. 2016;23:839–846. doi: 10.1177/2047487315621978 [DOI] [PubMed] [Google Scholar]
- 20. Herrera D, Meyle J, Renvert S, Jin L. White Paper on Prevention and Management of Periodontal Diseases for Oral Health and General Health. FDI World Dental Federation; 2018. Accessed date: November 1, 2022. https://www.fdiworlddental.org/sites/default/files/2020‐11/gphp‐2018‐white_paper‐en.pdf [Google Scholar]
- 21. Kuwabara M, Motoki Y, Sato H, Fujii M, Ichiura K, Kuwabara K, Nakamura Y. Low frequency of toothbrushing practices is an independent risk factor for diabetes mellitus in male and dyslipidemia in female: a large‐scale, 5‐year cohort study in Japan. J Cardiol. 2017;70:107–112. doi: 10.1016/j.jjcc.2016.10.008 [DOI] [PubMed] [Google Scholar]
- 22. Chang Y, Lee JS, Lee K, Woo HG, Song TJ. Improved oral hygiene is associated with decreased risk of new‐onset diabetes: a nationwide population‐based cohort study. Diabetologia. 2020;63:924–933. doi: 10.1007/s00125-020-05112-9 [DOI] [PubMed] [Google Scholar]
- 23. Niedzielska I, Janic T, Cierpka S, Swietochowska E. The effect of chronic periodontitis on the development of atherosclerosis: review of the literature. Med Sci Monit. 2008;14:RA103–RA106. [PubMed] [Google Scholar]
- 24. Wrigley BJ, Lip GY, Shantsila E. The role of monocytes and inflammation in the pathophysiology of heart failure. Eur J Heart Fail. 2011;13:1161–1171. doi: 10.1093/eurjhf/hfr122 [DOI] [PubMed] [Google Scholar]
- 25. Vedin O, Hagström E, Gallup D, Neely ML, Stewart R, Koenig W, Budaj A, Sritara P, Wallentin L, White HD, et al. Periodontal disease in patients with chronic coronary heart disease: prevalence and association with cardiovascular risk factors. Eur J Prev Cardiol. 2015;22:771–778. doi: 10.1177/2047487314530660 [DOI] [PubMed] [Google Scholar]
- 26. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–2379. doi: 10.1056/NEJMra1600266 [DOI] [PubMed] [Google Scholar]
- 27. Tang WW, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575–1584. doi: 10.1056/NEJMoa1109400 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Koren O, Spor A, Felin J, Fak F, Stombaugh J, Tremaroli V, Behre CJ, Knight R, Fagerberg B, Ley RE, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci USA. 2011;108:4592–4598. doi: 10.1073/pnas.1011383107 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Teeuw WJ, Slot DE, Susanto H, Gerdes VEA, Abbas F, D'Aiuto F, Kastelein JJP, Loos BG. Treatment of periodontitis improves the atherosclerotic profile: a systematic review and meta‐analysis. J Clin Periodontol. 2014;41:70–79. doi: 10.1111/jcpe.12171 [DOI] [PubMed] [Google Scholar]
- 30. Huang S, Li Z, He T, Cunpei B, Chang J, Li L, He Y, Liu J, Charbonneau D, Li R, et al. Microbiota‐based signature of gingivitis treatments: a randomized study. Sci Rep. 2016;6:24705. doi: 10.1038/srep24705 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Shah AD, Langenberg C, Rapsomaniki E, Denaxas S, Pujades‐Rodriguez M, Gale CP, Deanfield J, Smeeth L, Timmis A, Hemingway H. Type 2 diabetes and incidence of cardiovascular diseases: a cohort study in 1·9 million people. Lancet Diabetes Endocrinol. 2015;3:105–113. doi: 10.1016/S2213-8587(14)70219-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Restrictions apply to the availability of Korean National Health Insurance Service (NHIS) data because of ethical issues and data protection regulations according to the policy of Korean NHIS. Therefore, these data have been made accessible to qualified researchers who submitted a study protocol approved by official review committees.