Associations Between Periodontitis and Chronic Obstructive Pulmonary Disease; the 2010-2012 Korean National Health and Nutrition Examination Survey (KNHANES) Jae Ho Chung,* Hee-Jin Hwang,† Sun-Hyun Kim,† Tae Ho Kim‡ *Department of Internal Medicine, International St. Mary`s Hospital, Catholic Kwandong University College of Medicine, Incheon, Republic of Korea. †
Department of Family Medicine, International St. Mary`s Hospital, Catholic Kwandong University College of Medicine, Incheon, Republic of Korea. ‡
Department of Internal Medicine, Seoul Medical Center, Seoul, Republic of Korea.
Objectives: To examine whether the oral hygiene and self care especially in periodontal health are associated with chronic obstructive pulmonary disease (COPD) in a Korean population. Methods: Using data from the Korean National Health and Nutrition Examination Survey (KNHANES) between 2010 and 2012, we included 5,878 participants (normal lung function: 5181, obstructive spirometric pattern: 697) aged ≥40 years who underwent spirometry and assess the community periodontal index (CPI). Results: Participants with COPD brushed their teeth less frequently, used less frequently dental floss and / or interdental brush, mouthwash and electric toothbrush (p<0.001). The prevalence of periodontitis in COPD (58.1%) was significantly higher than without COPD (34.0%, p<0.001). The number of teeth was significantly lower in COPD patients when compared to the controls. DMF (decayed+missing+filled teeth) index is significantly lower in COPD patients. Table 3 showed risk of COPD by periodontal severity. Periodontitis (CPI 3 and 4) was associated in male COPD after adjustment for age, income, education, smoking, alcohol consumption, exercise, BMI, tooth brushing frequency, diabetes and number of teeth (CPI 3, RR 1.38; 95% confidence interval [CI], 1.12–2.05: CPI 4, RR 1.23; 95% CI, 1.06-1.56) . Conclusions: Findings of this cross-sectional study suggest that male COPD may be associated with the severe periodontitis and indicate the importance of promoting dental care in COPD patients.
Periodontitis is a common infectious disease affecting tissues supporting the teeth. 1 Risk factors for periodontal disease include poor oral hygiene, diabetes, smoking, low socioeconomic status, age, and stress. 2 Diabetes increases susceptibility to oral infections such as periodontitis and progresses more rapidly in poorly controlled diabetics. 3 Smoking is a well-established risk factor for periodontal disease. 4 Smoking tobacco is destructive effect on the periodontal system and increases the rate of periodontal disease aggravation. 5 Periodontal disease is also associated with socioeconomic status. 6 Gingival helath is better in those who received the more education and higher incomes. The prevalence and severity of periodontal disease increase with age. 7 Papapanou et al 7, demonstrated that the mean annual rate of dental bone loss was 0.07 mm in 25-year-olds and 0.28 mm in 70-year-olds. Stress is associated with increased risk of periodontitis. 8 Men who reported being angry had a 43% higher risk of periodontitis than did not.8 Although chronic obstructive pulmonary disease (COPD) is primarily a pulmonary disease characterized by airflow limitation, it is also often associated with a significant systemic inflammatory response. 9, 10 Poor periodontal status was also been associated with COPD.11 Several studies suggested an association between poor
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oral health (alveolar bone injury, periodontal attachment loss, oral hygiene index, and oral plaque colonization) and lung diseases.12-14 Case–control studies also found that poor periodontal health was significantly associated with increased risk of COPD. 15,16 A metaanalysis of 14 studies suggested that periodontal disease was a significant risk factor for COPD. 17 However, other studies showed uncertain associations between periodontal disease and COPD. 18,19 A recent review of research on the relationship between COPD and periodontitis found only a weak relationship, at best. 18 Another study 19 found no significant difference in periodontal variables between COPD and non-COPD groups. Because of this inconsistent data, we examined the relation of periodontal health status and oral health-related behaviors such as self-care, smoking, alcohol consumption with COPD in a representative sample of adults who were involved in the fifth Korean National Health and Nutrition Examination Survey (KNHANES).20
METHODS Study Participants The present study was conducted using data acquired from Korean National Health and Nutrition Examination Surveys (KNHANES). The KNHANES analyses are periodically conducted to assess the health and nutritional status of Korea. These investigations are composed of a health interview survey, health examination survey, and nutrition survey, and are conducted by well-trained investigators. Annually, 10,000–12,000 individuals from 4,600 households are selected by a panel to represent Koreans that are 18 years of age and older using a multistage clustered and stratified random sampling method based on National Census Data. The sampling frame was developed based on the 2005 population and housing census in Korea, and the household units were selected by a stratified multistage probability sampling design created for the South Korean population. Thus, the KNHANES were nationally representative cross-sectional surveys conducted by the Division of Chronic Disease Surveillance of the Korea Centers for Disease Control and Prevention, and included data from approximately 260,000 primary sampling units that were each composed of approximately 60 households. Of these participants, 8,145 participants (normal lung function: 5181, obstructive spirometric pattern: 697) aged ≥40 years who underwent spirometry and assess the community periodontal index (CPI)21 were analyzed. Baseline Physical Health Self-reported smoking, alcohol, and physical activity were calculated from questionnaire, and education status, household income were categorized. Smokers were classified as current, former, or non-smokers. Risky alcohol drinking is defined as consuming ≥5 standard drinks consecutively on one occasion22 Regular exercise was defined as walking exercise (5 times per week for at least 30 min), or moderate exercise (5 times per week for at least 30 min) or strenuous exercise (3 times per week for at least 20 min), as defined by the American College of Sports Medicine Guidelines 23, during the survey period. The height and weight of the participants were measured and used to calculate body mass index (BMI) with the following formula: (weight [kg]/height [m2]). Diabetes mellitus (DM) was determined in selfadministration questionnaires as follows: “Have you ever been diagnosed with diabetes mellitus by doctor? Yes or no?”.
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Lung Function Measurement Spirometry was performed by well-trained technicians according to the 1994 American Thoracic Society recommendations 24. Airway obstruction was defined according to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) 25 criteria (GOLD Stage I) as FEV1/ FVC <70%. The severity of airway obstruction was based on the percentage predicted FEV1 in accordance with the GOLD criteria (FEV1 ≥80% predicted, mild; FEV1 = 50–79% predicted, moderate; FEV1 = 30–49% predicted, severe; FEV1 <30% predicted, very severe). Oral Hygiene and Self Care This study checked both time of day when tooth brushing (before or after breakfast, lunch, dinner, after snacks, or before bedtime) occurred and use of dental floss, mouthwash, interdental brush, and electric toothbrush. We calculated the frequency of daily toothbrushing by the sum of tooth brushing per day, use of dental floss, mouthwash, interdental brush, and electric toothbrush. Periodontitis Dentists conducted an oral health examination in the survey. The World Health Organization (WHO) community periodontal index (CPI) was used to assess periodontitis.21 CPI code is categorized as normal (CPI 0), gingival bleeding (CPI 1), calculus (CPI 2), shallow periodontal pocket (CPI 3), deep periodontal pocket (CPI 4). The index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46 and 47 according to the Federation Dentaire Internationale (FDI) system. 26 A CPI probe that met the WHO guidelines 27 was used (World Health Organization 1997). Periodontitis was defined as a CPI 3 ( >3.5 mm pocket) or CPI4 (>5.5 mm pocket). The mean of Kappa value of inter-examiner was 0.89 (0.55–1.00). Number of teeth (28 except for the wisdom teeth) was measured. Ethical Issues Korea Centers for Disease Control and Prevention approved the study protocol (nos. 2010– 02CON-21-C, 2011–02CON-06-C, 2012-01EXP-01-2C), and all of the participants signed informed consent forms. Data Analysis All sampling and weight variables used in the present study were stratified to ensure appropriate estimates and standard errors. In addition, survey sample weights were used to produce non-biased estimates for the descriptive and analytical data analyses. Descriptive statistical methods were used to describe the basic characteristics of the study population, and the numbers and percentages were reported for each variable. All of the characteristics were compared using student's t- tests for continuous variables and the Chi-squared test or Fisher’s exact test for categorical variables. A multivariate logistic regression analysis that was adjusted for sex, age, exercise, family income, education, alcohol, smoking, BMI and DM were also used to assess the data.
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RESULTS Clinical characteristics of the study population are shown in Table 1. COPD patients were more likely to be older, less educated, more regular exercise and more likely to earn a lower income and to more current smoking and more alcohol intake. Table 2 showed the relationship between oral hygiene and self-care with COPD. Shallow (39.3% vs 24.5%) and deep periodontal pocket (18.7% vs 9.6%) were significantly increased in COPD patients than non-COPD patients (p<0.001). Despite of more prevalent periodontitis defined as a CPI ≧ 3 in COPD patients (58.1%) than non-COPD patients (34.0%, p<0.001), dental visit in last year in COPD were only 27.6% and 49% of COPD patients think their oral health status is in good condition. Participants who tooth brushed more than three times per day were 35.8% in the COPD patients and 44.4% in the non-COPD patients (p<0.001). The COPD patients also used dental floss, mouthwash, interdental brush, and electric toothbrush less frequently than non-COPD patients. The number of teeth was significantly lower in COPD patients when compared to the controls. DMF (decayed+missing+filled teeth) index is significantly lower in COPD patients. Table 3 showed risk of COPD by periodontal severity. After adjustment for age, income, education, smoking, alcohol, exercise, BMI, tooth brushing frequency, diabetes, number of teeth, periodontitis (CPI 3, CPI4) were associcated in male COPD (CPI 3, RR 1.38; 95% confidence interval [CI], 1.12–2.05: CPI 4, RR 1.23; 95% CI, 1.06-1.56).
DISCUSSION In this representative sample of Koreans aged 40 years and older, we found that the severe periodontitis was closely associated with COPD in males after adjusting for confounding factors. The findings of the present study consistent with other studies. 12, 14, 28, support an association between periodontitis and COPD. Hayes et al 12 found that, for every 20% increase in alveolar bone loss, there was a 60% increase in the risk of COPD. A crosssectional retrospective study 14 found that lung function was lower with poor periodontal health, and the most periodontitis scores was 1.45-fold greater odds ratio of concurrent COPD. There is a relationship between more severe periodontal status and severity of COPD. 28 However, other studies have shown uncertain associations between periodontal disease and COPD. Azarpazhooh 18 could showed only a weak association between COPD and periodontitis, and another study found no significant difference in periodontitis between COPD and nonCOPD patients. 19 Some periodontal status may be significantly worse in COPD, but such as clinical attachment level is not significant . 29 These inconsistent findings may result from differences in assessments of periodontal status and the use of different diagnostic criteria. The Hayes study 12 used a COPD criterion of FEV1 <65% instead of the GOLD criteria. In the Scannapieco 14 study, COPD was defined by a questionnaire rather than by spirometry. Our study included only those who underwent spirometry and met the GOLD COPD criteria. Our study showed that the prevalence of periodontitis, defined as community periodontal index code (CPI) ≥3, was significantly higher in those with than in those without COPD. Some mechanisms have been proposed to explain the association between periodontitis and COPD. COPD and periodontitis have a similar pathophysiology, specifically, inflammation
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of the local connective tissue. Neutrophils also play an important role in both COPD and periodontitis, as their proteases and ROS can promote inflammation and destroy connective tissue. Similar to Oztekin study 30, our study showed that the number of teeth was significantly lower in COPD patients than in controls. Furthermore, periodontal health was associated with dental loss, may have contributed to systemic inflammation, and was associated with COPD. The Oztekin study 30 also showed that serum and gingival crevicular fluid high-sensitive Creactive protein levels were significantly higher in COPD patients than in controls. Periodontitis may be linked to COPD through microbial species, by supporting colonization of respiratory pathogens in dental plaque 29 or by airway inflammation and exacerbation by periodontal organisms. COPD inflammatory status may be modified by dental plaque and/or hematogenous dissemination of inflammatory mediators and plaque microbials from periodontal pockets. 31 Pavord et al. suggested that multiple inflammations in the airway may be a key factor leading to the development of severe airway disease . 32 The present study has several limitations. First, because it was a cross-sectional study, it is not possible to determine a cause-and-effect relationship between COPD and periodontitis. Second, periodontal status was assessed by CPI only. Although CPI can assess the periodontitis and has been adopted as an index for periodontitis on the association between systemic disease and periodontal disease, 33, 34 the limitations of CPI should be considered because it can overestimate or underestimate the prevalence of periodontitis due to the use of representative teeth and pseudo pockets. 35 Our study only used CPI and only measured index teeth to diagnose periodontal disease. In an adult population, CPI should be measured for all teeth; it can be measured from index teeth in population-based surveys only in patients under 18 years, where periodontitis (CPI 3 and 4) is not as prevalent as in older patients. Consensus and uniformity in the definition of periodontitis are lacking in epidemiological studies, as is uniformity of methods used. The consequence is that data from studies using differing case definitions and differing survey methods are not readily interpretable or comparable. In 2003, the American Association of Periodontology developed methods for assessing periodontal disease. This classification defines severe and moderate periodontitis in terms of probing depth (PD) and clinical attachment level (CAL) to enhance case definitions; this approach also stresses the importance of thresholds of PD and CAL and the number of affected sites when defining periodontitis. 36 In Europe, two threshold criteria for the diagnosis of periodontitis were proposed during the 5th European Workshop in Periodontology: 1. the presence of proximal attachment loss of ≥3 mm in ≥2 non-adjacent teeth, and 2. the presence of proximal attachment loss of ≥5 mm in ≥30% of teeth. 37 Finally, a limitation of KNHANES is that the participants in the survey generally have mild comorbidities. Thus, the small number of COPD patients in GOLD stages III and IV may influence the analysis of risk for periodontitis. Despite these limitations, our study is important for clinical practice. Strengths of our study were that the data were obtained from a nationwide population, which made higher precision and could multiple statistical adjustments. Second, the natural teeth numbers and oral condition were objectively assessed by dentists using the same criteria. Additionally, several confounding variables were precisely recorded by well-trained examiners. Survey participants with COPD reported more periodontitis than did participants in the general population. Thus, it is important for practicing general physicians to be aware that
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patients with COPD are at risk of significant periodontitis. In our study, only 27.6% of COPD patients visited dental clinics in the last year, and 49% of COPD patients reported that their oral health status was good, despite the high prevalence of periodontitis.
CONCLUSIONS We found that COPD in males may be associated with the periodontitis. Thus, healthcare workers should be screen for and promptly diagnose these problems and refer patients to appropriate oral health professionals, who may be able to prevent periodontitis and arrest the progression of periodontitis in COPD. However, it will require randomized controlled trials to investigate cause-and-effect relationship and understand the pathological basis and correlates of the disease. CONFLICT OF INTEREST: The authors declare no conflict of interest.
ACKNOWLEDGMENTS: The authors declare no acknowledgement.
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Corresponding Authors: Sun-Hyun Kim, MD and Tae Ho Kim, MD , Address: Sun Hyun Kim, MD, PhD; Department of Family Medicine, International St. Mary`s Hospital, Catholic Kwandong University College of Medicine, Simgokro 100gil 25 Seo-gu, Incheon, Republic of Korea, Tel +82 32 290 2932 fax: +82 32 290 2660. E-mail:[email protected], Tae Ho Kim, MD; Department of Internal Medicine, Seoul Medical Center, 156 Sinnae-ro, Joongrang-gu, Seoul, Republic of Korea, 131-795 Tel.: +82 2 2276 8864; fax: +82 2 2276 8504. E-mail: [email protected] Submitted November 16, 2015; accepted for publication February 19, 2016.
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Table 1. Clinical characteristics of study participants. COPD (n = 697 na=0.68) Age (years) GOLD classification Stage 1 Stage 2 Stage 3 Stage 4 FEV1 (l) FEV1(% predicted) Smoking status Never Ex-former Current Alcohol drinking Regular exercise Family income Low Moderate-low Moderate-high High Education ≤Elementary Middle school High school ≥College BMI DM
Calculus Shallow periodontal pocket Deep periodontal pocket
166 (23.8) 274 (39.3)
1868 (36.1) 1267 (24.5)
117 (22.3) 213 (40.6)
709 (34.0) 591 (28.3)
49 (28.3) 61 (35.3) 25 (14.5)
1159 (37.4) 676 (21.8) 205 (16.6)
n :unweighted sample size, n a :weighted sample size in millions. Table 3. Risk of COPD on periodontal severity Gingival bleeding (CPI 1) Model 1 Model 2 Model 3 Model 4 Calculus (CPI 2) Model 1 Model 2 Model 3 Model 4 Shallow Periodontal Pocket (CPI 3) Model 1 Model 2 Model 3 Model 4 Deep periodontal pocket (CPI 4) Model 1 Model 2 Model 3 Model 4
Results represent risk ratio (95% confidence interval). Adjusted for age variable in model 1. Adjusted for age, family income, education variables in model 2. Adjusted for age, family income, education, smoking, alcohol, exercise, BMI, tooth brushing frequency variables in model 3. Adjusted for age, income, education, smoking, alcohol, exercise, BMI, tooth brushing frequency, diabetes, number of natural teeth in model 4.
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