We found that PD showed an association with chronic bronchitis in Koreans. This is the first follow-up study in Korea to demonstrate that PD was associated with a higher incidence of chronic bronchitis after adjusting for various confounders. This association was accentuated in the middle age group (40–59 years) and in the subjects without periodontal treatment.
Table 1 shows that the subjects with PD were more likely to be male, older, and had a low income. The baseline systemic health including diabetes mellitus, hypertension, obesity, hypercholesterolemia, and ischemic heart disease also tended to increase with the severity of PD, which was consistent in other studies [13, 14, 32, 33].
Our results supported the previous 2 studies that showed a significant association between PD with respiratory disease :HR of 2.72 for respiratory disease [34] and an IRR of 4.21 for adverse respiratory events in the Taiwanese study [30]. Our association showing the impact of PD on CB was a bit lower than 2 studies, because Qian Y et al. only studied the impact of PD on respiratory disease for the elderly aged 75 and over [34] and the Taiwanese study was conducted only with COPD patients at the baseline [35]. However, while Qian Y et al. analyzed the overall risk of all respiratory diseases [34], this paper only analyzed CB, which is thought to have reduced the risk when considering the overall prevalence. In particular, while no risk was observed in COPD in that study [34], our paper showed that the risk increased 1.05 times in CB, a type of COPD. And significance was observed not in periodontitis but in completely edentulous patients in that study (aHR = 2.08, 95% CI = 1.46 to 3.58). Although other papers reported the risk of COPD related to PD, there is no paper that reported the risk of CB on PD yet. And, While the Taiwanese study studied the incidence of worsening respiratory tract in COPD patients [35], our study is more meaningful by examining the incidence of CB in the entire population cohort.
In respiratory disease with CB than without CB, the severity and exacerbation of the disease occur more frequently, and the fatality rate of respiratory diseases is higher. Therefore, it can be considered that the effect of systemic inflammation was more prevalent and more severe in patients with CB than without CB [36]. For this reason, I think it is meaningful to study not only the effect of CB on respiratory diseases, but also its association with PD. In this study, the result of the high incidence of CB in subjects with PD is thought to be consistent with other papers in which periodontitis negatively affects respiratory diseases [36]. Overall, the previous studies and our data confirmed that severe PD is associated with chronic bronchitis [36].
Our data showed that age modified the association of PD with chronic bronchitis. PD increased the incidence of chronic bronchitis from 5% in the total population to 6% in adults aged 40 to 59 years. We found that adults aged 40 to 59 years generally have poorer periodontal health, so chronic inflammation caused by periodontitis could negatively affect the chronic bronchitis. On the contrary, in the age of 60 years or older, the prevalence of systemic diseases as well as periodontitis increases, so the risk of chronic bronchitis due to PD could be evaluated as statistically low [37]. It is considered that further research is needed to determine the age-specific differences in the relationship between periodontitis and systemic diseases.
As a result of analyzing systemic factors affecting periodontitis by sex, there is no difference according to sex in the present study. Men have a higher prevalence of periodontitis and CB than women [38, 39], while women have an increasing prevalence of CB [39]. Since men are a risk group for periodontitis and CB, the HR analyzing the association between chronic bronchitis and periodontitis was also expected to be higher in men, but no gender difference was found. This reason may be due to the action of CRP, a predictor of systemic inflammation, in the associated pathway between periodontitis and chronic bronchitis. CRP is a representative chronic inflammatory factor, but it is found to be higher in women, which can be interpreted as being related to women's abdominal fat [40]. Therefore, there is a need for additional research on the lack of significant gender differences in chronic bronchitis.
Numerous data have already suggested a biological link between periodontitis and other systemic disease including cardiovascular disease, rheumatoid arthritis, respiratory disease, kidney disease, liver disease and DM [10–14]. It is meaningful to analyze the relationship more because CB is in close contact with the oral cavity and is prone to systemic chronic inflammation. There are several hypotheses about the relationship between CB and periodontitis. Firstly, dental plaque may provide nutrition to pathogens in the respiratory tract, particularly in patients with poor oral hygiene [41]. Secondly, mouth breathing, decreased salivary protection, and altered immune response in gingival tissue in individuals with periodontal disease may lead to respiratory disease [42]. Thirdly, studies have indicated that aspirated organisms from dental plaque, circulating inflammatory substances, and even organisms in periodontal lesions play an important role in chronic respiratory inflammation [43]. Fourthly, periodontal disease-associated enzymes and cytokines may modify the mucous secretions of the airway [44].
Table 4 shows that there were significant effects to reduce the occurrence of chronic bronchitis as a result of periodontal treatments. Thus, periodontal therapy may slow down the reduction in lung function and decrease the occurrence of CB. Our results may support initial periodontal therapy in patients with pulmonary disease and CP may decrease the exacerbation frequency [26]. Several mechanisms may be considered for the effect of periodontal therapy on pulmonary disease. First, periodontal treatment can remove plaque and lessen oral mucosa colonization with respiratory pathogens. Respiratory pathogens isolated from broncho-alveolar lavage fluid of the old patients were the same as pathogens isolated from their dental plaques [45, 46]. Second, periodontal treatment may reduce periodontal pathogen that can increase airway inflammation and exacerbations. It was suggested that the coexistence of multiple inflammatory stimuli may be a key factor leading to the development of more severe airway disease [47]. Periodontal lesions and peripheral mononuclear cells continuously release many inflammatory factors, which can cause more severe inflammatory response in respiratory diseases. Thus, it seems reasonable to speculate that periodontal treatment, which effectively reduces the dental plaque burden, could reduce exposure to pathogens in the respiratory tract. And, it subsequently could slow the progression of pulmonary dysfunction and decrease the frequency of chronic bronchitis exacerbation.
This study has several strengths. First, it is the first report conducted on a representative Korean national population. Second, we classified periodontal conditions of ICD codes [48]. Third, periodontal diagnosis and medical diagnosis were conducted by dentists and medical doctors, respectively.
Several limitations in this study were suspected. First, PD and chronic bronchitis are chronic diseases that barely show significant signs and symptoms at the early stage, and the patients may not seek dental or medical consultations until the PD and/or chronic bronchitis has/have been ongoing for some time. Thus, we used the expression of a potential risk factor instead of causality. Second, we could not use clinical attachment loss to define PD. Moreover, patients with mild periodontitis without dental visit could be misclassified into the periodontally healthy group. Fourth, for robust estimation, we set the incubating time of 3 years for the occurrence of chronic bronchitis due to the burden of periodontal inflammation without clear evidence, which could underestimate the association. However, there was a study that used a similar method for the robust incubation period [49, 50]. Notwithstanding these limitations, our data was sufficiently valid for the evaluation of a possible association between PD with chronic bronchitis. The findings support that prevention and management of PD could be beneficial for reducing the risk of chronic bronchitis.