Association of periodontal status with lung function in patients with and without chronic obstructive pulmonary disease visiting a medical hospital in Pune: A comparative study.

BACKGROUND: The relationship between oral health and systemic conditions has been increasingly debated over recent decades with one such discussion existing about oral hygiene and periodontitis with chronic obstructive pulmonary disease (COPD). Hence, a study was conducted to assess and compare the oral hygiene status and periodontal status of age and gender-matched participants with and without COPD and to correlate oral hygiene status and periodontal status with lung function status among them.
MATERIALS AND METHODS: This hospital-based study included a study population of 117 participants (39 patients of COPD and 78 participants without COPD) 35-75 years of age with at least 20 natural teeth. Participant's demographic details and history of smoking were recorded. Lung function was recorded using a spirometer. Periodontal health was assessed by measuring Probing Pocket Depth (PPD), Clinical Attachment Loss (CAL), and Oral Hygiene Index (OHI) by a trained and calibrated examiner.
RESULTS: Higher mean of PPD, CAL, and OHI is being reported in the present study with 4.07 versus 3.50, 0.58 versus 0.24, and 5.24 versus 3.60, respectively, among patients with and without COPD which was statistically significant. The risk of having COPD was 0.4 times more in participants having poor oral hygiene and 0.07 times more in patients smoking. Smoking and oral hygiene, as independent variables, have a significant influence on COPD which is a dependent variable. A weak correlation was found of poor oral hygiene and loss of attachment among participants with COPD.
CONCLUSION: Periodontitis and respiratory disease share a common risk factor, i.e., smoking. Smoking has a definite relation with periodontitis and COPD. Oral hygiene is significantly associated with increased risk for COPD when age and gender effects have been matched and when adjusted for smoking. However, no association was found of PPD with COPD. Copyright:

INTRODUCTION

Chronic obstructive pulmonary disease (COPD) is a complex, multifactorial inflammatory disease of the airways, and the pulmonary parenchyma, caused by infection, air pollution, and particles.[1] COPD has made its presence felt globally as well as in India. COPD is likely to be the fourth leading cause of death worldwide by 2030.[2]

Periodontitis is quite often seen among adults as a result of poor oral hygiene. Periodontitis and COPD share common risk factors such as smoking. Oral pathogens such as Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans play a role in the pathogenesis of respiratory infections. The relationship between poor oral hygiene, periodontal, and respiratory disease has been increasingly debated over recent decades.[3] Studies have shown that there is a poor evidence of a weak association between COPD and oral health.[4]

The pathogens present in gingival sulcus or periodontal pockets in periodontal disease have direct access into the systemic blood; moreover, they also shed in the saliva and are further carried down into the respiratory tract where they cause irritation of the respiratory mucosa increasing the risk of COPD.[5] An irritation to a limit is acceptable by the immune response of our body, but when this crosses normal protective response, it leads to COPD causing lung injury.[6] Past literature has assessed the association between COPD and periodontal status.[78910] Periodontitis is a common oral problem observed among the patients visiting dentists. If a clear idea about their relation is understood, then it would become easy for the health-care professionals to direct their treatment accordingly as periodontitis is a preventable disease and can be avoided by proper awareness and oral hygiene modification in patients. Thus, a small effort of awareness can help to overcome the succeeding COPD risk. Although various studies have been reported in the literature regarding the same, still this topic remains controversial. Therefore, to get this clarity, first, a comparative study was conducted with an aim to associate the periodontal status with lung function status in adults with and without COPD. Second, the correlation was assessed between periodontal status and lung function status among the same patients with and without COPD.

MATERIALS AND METHODS

The sample size for the hospital-based comparative study among age- and sex-matched 117 patients was calculated, keeping the power 80% based on the previous literature by Deo et al.[7] Out of the total 117 patients, 39 patients were newly diagnosed with COPD and 78 patients were without COPD. The ratio was kept at 1:2. The study was approved by the Institution's Ethics Committee with Ref. No. of EC/DYPDCH/PHD/02, and written informed consent was obtained in local language (Marathi) prior to starting the study. The COPD patients were recruited from Outpatient Department, Department of Pulmonary Medicine of a Medical College, and the patients without COPD were recruited from the Outpatient Department of a College and the relatives accompanying them from April 2014 to September 2014.

Nonambulatory participants having minimum 20 natural teeth and between 35 and 75 years having chronic periodontitis were part of the study. Only newly diagnosed cases of COPD were included in the COPD group while non-COPD group patients were recruited from OPD who were not having COPD or any other respiratory disease. Smokers, nonsmokers, participants with exposure to agriculture dust, burning of wood, coal fumes, biomass fuel, and vehicle carbon exhaust were also included in the study in both the groups. Participants with any history of periodontal treatment in the past 6 months, participants having history of all types of diabetes, tuberculosis, recent eye surgery (last 1 month), recent myocardial infarction (within last 1 month), and stroke that affects the face, pleural effusion, pneumonia, and hospitalized patients were excluded from the study. A consecutive sampling technique was used to select the participants meeting the inclusion and exclusion criteria. The study was conducted in two phases as follows:

Phase I

The first phase of the study comprised identifying the patients with COPD based on the previously published criteria (forced expiratory volume after 1 s [FEV1]/forced vital capacity [FVC] <0.70, FEV1 ≥80%).[11] The patients diagnosed as COPD by the physician and fulfilling the inclusion and exclusion criteria were selected as cases, whereas the patients not having COPD and fulfilling the inclusion and exclusion criteria were classified as controls. Information regarding patient's demographic characteristics, yearly income and lifestyle, oral hygiene, and periodontal status was recorded in the study.

Phase II

In the second phase, the clinical examination was conducted by an oral health expert and technician. Respiratory examination of the study participant was done by a chest physician in the Pulmonology Department of Medical College. Spirometry is a pulmonary function test that measures the presence and severity of airflow obstruction. In symptomatic patients, spirometry is helpful for determining whether the symptoms are due to respiratory disease or other conditions. COPD is diagnosed when spirometry demonstrates airflow obstruction that is not fully reversible. Lung function was assessed by a trained technician using a spirometer (Cosmed). Before performing spirometry test, the technician recorded the patient's height, weight, sex, age, and smoking history into the patient profile in the spirometer. Lung function was estimated by calculating the ratio of FeV1/FVC × 100 by expert physician.

Training and calibration

Before commencing the study, the examiner underwent clinical training and calibration with regard to probing pocket depth (PPD), clinical attachment loss (CAL), and oral hygiene index (OHI) in the Department of Public Health Dentistry. The agreement between examiner and benchmark was (k = 0.8). Duplicate examinations were carried out among 12 study participants after 3 months' and after 6 months' time during the study period to check for the consistency in recording of the PPD, CAL, and OHI which was found to be 0.8.

Assessment

Patient's periodontal status was assessed with the help of OHI, PPD, and CAL. Periodontal health was assessed by measuring PPD from the crest of gingival margin to the base of periodontal pocket and CAL from cementoenamel junction to base of the periodontal pocket using WHO CPI probe. Six surfaces (distofacial, facial, mesiofacial, mesiolingual, lingual, and distolingual) of the tooth were examined for measuring periodontal pocket and loss of attachment. Except the third molar, all the teeth which present in the mouth were examined and the tooth having >3 mm of pocket depth was considered as diseased. For each tooth, the pocket depth was calculated at the six sites and the mean value was taken as the mean pocket depth of the tooth. Similarly, mean pocket depth was calculated for all the teeth present. The mean pocket depth of all the diseased teeth was calculated, which was considered as the mean pocket depth for that individual. The calculation of mean CAL was done similarly. The lung function was recorded by the expert technician on the same day and was noted by the principal investigator from the patient's medical records.

Statistical analysis

For analysis, the data were entered into the Excel sheet and analyzed using IBM ® SPSS 17. One-Sample Kolmogorov–Smirnov test was used to check the normalcy of the data. Comparison of PPD, CAL, and OHI between the two groups was tested by Mann–Whitney test, and smoking exposure was tested by Pearson's Chi-square test. P < 0.05 was taken as statistically significant. To evaluate the effect of predictor variables (PPD, CAL, OHI, and smoking) on the two groups, a logistic regression model was run. Correlation of PPD, CAL, and OHI with lung function in both the groups was tested by Spearman's correlation coefficient test.

RESULTS

A total of 93 males and 24 females in the age range of 35–75 years participated in the study. When exposure to smoking was assessed, the COPD group had 20 smokers, while non-COPD group had 75 smokers. In this study, all the participants had similar family income and oral hygiene practice and had exposure to environmental pollutants.

The mean score for PPD, CAL, and OHI was higher in COPD group with a score of 4.07, 0.58, and 5.24, respectively, as compared to non-COPD group with mean score of 3.50, 0.24, and 3.60, respectively. The difference between the groups for these parameters showed statistical significance with P < 0.001 [Table 1]. When the Chi-square test was applied to assess the difference of smokers in between both the groups, the COPD groups noted a higher number of smokers than non-COPD group with P = 0.00 [Table 2].

Table 1

Comparison of periodontal parameters between the groups

Parameter	With COPD	Without COPD	P
PPD*
Mean	4.07	3.50	<0.001
SD	1.03	0.98
Mean rank	83.96	46.52
CAL*
Mean	0.58	0.24	<0.001
SD	0.29	0.19
Mean rank	88.33	44.33
OHI*
Mean	5.24	3.60	<0.001
SD	1.12	1.04
Mean rank	89.95	43.53

*Significant at P<0.001; Mann–Whitney test. SD – Standard deviation; COPD – Chronic obstructive pulmonary disease; PPD – Probing Pocket Depth; CAL – Clinical Attachment Loss; OHI – Oral Hygiene Index

Table 2

Exposure to smoking among the two groups

	With COPD	Without COPD	P
Smoking	19	3	0.00*
No smoking	20	75

*Significant at P<0.001; Pearson Chi-square test. SD – Standard deviation; COPD – Chronic obstructive pulmonary disease

Since smoking was associated with both periodontitis and COPD and was a significant confounding factor, hence the logistic regression analysis was done to adjust for this covariate. After adjusting for smoking, the logistic regression model was run and a significant difference was found with only poor oral hygiene. The risk of having COPD was 0.4 times more in patients having poor oral hygiene as compared to the ones having healthy oral hygiene. Later, smoking was also put into the model to know its independent risk effect. Smoking too showed a significant value, and the risk of having COPD was 0.07 times more in patients smoking as compared to the ones who did not smoke [Table 3]. Correlation of periodontal parameters with lung function was done for the COPD and non-COPD group [Table 4]. PPD showed negligible correlation in COPD and non-COPD group, whereas CAL and OHI showed weak correlation in both the groups.

Table 3

Effect of predictor variables on patients with and without chronic obstructive pulmonary disease

Predictor variables	B	Significance	Exp(B)
PPD	−0.39	0.17	0.67
CAL	−1.95	0.18	0.14
OHI*	−0.91	0.00	0.40
Smoking*	−2.56	0.00	0.07

*Significant at P<0.001; logistic regression analysis. B – Coefficient for constant; Exp(B) – Exponential of B called as odds ratio; PPD – Periodontal Pocket Depth; CAL – Clinical Attachment Loss; OHI – Oral Hygiene Index

Table 4

Correlation of probing pocket depth, Clinical Attachment Loss, and Oral Hygiene Index status with lung function status among patient with and without chronic obstructive pulmonary disease

	Correlation coefficient with lung function among patients with COPD	Correlation coefficient with lung function among patients without COPD
PPD	−0.02 (negligible)	−0.03 (negligible)
CAL	−0.32 (weak)	−0.19 (weak)
OHI	−0.17 (weak)	−0.19 (weak)

Unadjusted for smoking. COPD – Chronic obstructive pulmonary disease; PPD – Periodontal Pocket Depth; CAL – Clinical Attachment Loss; OHI – Oral Hygiene Index

DISCUSSION

In the present study, lung function was recorded using spirometry which is a gold standard for diagnosing COPD. The patient enrolled as cases were those having COPD and no other systemic disease that influenced periodontal status. Since all the patients recruited from the hospital had similar socioeconomic background (low) and oral hygiene practice (brushing once in a day with toothbrush and toothpaste), it was not considered as a confounding factor in this study. Age and gender matching was done in controls to avoid bias.

The mean OHI and mean periodontal parameters were poorer in COPD group as compared to non-COPD group [Table 1]. Similar results were found in the study conducted by Lopez-de-Andrés et al., wherein periodontal disease prevalence was higher among COPD patients over non-COPD patients.[9] The cross-sectional study conducted by Sharma N [12] on association between respiratory disease and periodontal disease also found that patients with COPD had significantly greater poor oral hygiene (OHI) and periodontal health (PPD and CAL) as compared to controls. The study conducted on potential association between chronic respiratory disease and periodontal disease depicted that oral health parameters (attachment loss and oral health status) were poorer in participants with COPD as compared to participants without COPD.[13] Similar results were found in study conducted by Deo et al.[7] which is in accordance with the present study. A meta-analysis conducted by Zeng et al.[14] on periodontal disease and risk of COPD concluded that periodontal disease is a significant and independent risk factor of COPD. The systematic review conducted by Agado and Bowen [15] on periodontal disease and respiratory disease depicted a fair evidence (Grade B, Level II-2) to support an association between COPD and periodontal disease.

Statistical analysis of exposure to smoking among both the groups showed that it was a significant confounder in this study [Table 2]. Similar findings were seen in the systematic review conducted by Garcia et al.[16] where it was observed that periodontal health status was associated with COPD. However, the observed result could have been due to residual confounding by tobacco smoking. The prevalence of smokers was also found on a higher side among COPD patients as compared to non-COPD patients.[9]

Regression analysis was done to adjust for the smoking exposure [Table 3]. Only mean OHI was significantly associated with COPD, and no association was found with mean PPD and mean CAL after adjusting for smoking. However, a study conducted by Peter et al.[17] had significantly worse PD, CAL, and OHI in case group when compared to control group when adjusted for smoking. Lung function declined rapidly among patients with increase in the mean CAL and PPD levels after adjusting for smoking.[10] In the study conducted by Mojon,[8] he could not find any causal association between oral hygiene and respiratory infection (COPD). However, Scannapieco et al.[18] found a residual effect of OHI on chronic respiratory disease. An association between COPD and oral health was first noted by the National Health and Nutrition Examination Survey I data. In this study, the logistic regression analysis revealed that poor oral hygiene was statistically associated with COPD, which substantiates our results. Exposure to smoking acted as an effect modifier in this study. Similar results were also seen in study conducted by Hayes et al.[19] in which he found that elevation in risk of COPD due to periodontal disease was not significant in participants who were never smokers and smoking had to be present as a cofactor for periodontal disease to have an effect.

Scannapieco et al.[18] could not establish any association between periodontal index and respiratory diseases, but they did report poorer oral hygiene among patients with COPD. In the present study, individuals with COPD are likely to have more severe periodontal disease than individuals without COPD, but the negative correlation established in non-COPD individuals between OHI and lung function status justifies that an association exists between OHI and lung function among individuals without COPD which can be studied further.

In this study, the periodontal parameters were also correlated with lung function in both with and without COPD group [Table 4]. Interestingly, a trend was noted in which the periodontal indices worsened as the lung function value decreased, suggesting a negative correlation between periodontal parameters and lung function values. This observed correlation was weak negative between CAL, OHI, and lung function in the groups, whereas for PPD, a negligible negative correlation was observed in the groups. However, Peter et al.[17] found a significant negative correlation between periodontal parameters (CAL, PD, and GI) and lung function. The risk of rapid decline in lung function increased significantly with increase in CAL values.[10] Association between periodontal health and systemic health or lack of association is still a sensitive and debatable issue. Existing clinical and epidemiological studies had shown the weak association between periodontal health and respiratory diseases, and this study also adds support to the existing literature.[1620]

Travis et al.[21] had described a biologically plausible mechanism to explain the theoretical association between periodontal disease and COPD. It was noted that both emphysema and periodontal disease may share common pathophysiologic processes. However, there is no existence of direct evidence for a causal relationship between periodontal disease and respiratory disease. Although hypotheses are generated through research, to explain the causal relationship of oral bacteria in the pathogenesis of respiratory disease, the causality may not be concluded.[3] However, it is yet confusing whether oral bacteria do contribute independently in the pathogenesis of respiratory diseases or remains as a surrogate cause of diminished lung functioning. This study was conducted to know whether an association existed between COPD and periodontal disease. However, definite cause and effect relationship could not be established. To determine whether the association between previously existing periodontal disease and COPD exist or not, several factors are needed to be considered. Among these are the strength of the claimed association, temporality, dose effect, biologic plausibility, and experimental evidence. The demonstration that periodontitis was present before the onset of COPD can be referred to as temporality which is essential to establish an association, especially causality.[1318] To establish such temporality, studies with more appropriate study designs such as randomized control trial in which an intervention to reduce oral infection could be tested in regard to ability to lower the risk of respiratory disease outcome or prospective cohort studies should be conducted. Unfortunately, such studies are complicated to undertake. The dose effect, i.e., the risk for respiratory disease increases with increase in severity and duration of periodontitis, could not be established as it is likely to be impossible.[1022] A 3-year cohort study among Japanese adults concluded that periodontitis is a risk factor for the decline in lung function test which may lead to COPD in the future.[10]

To summarize, based on the results of this study and available literature, it suggests that poor health has its own role to play in causation of respiratory diseases because bacteria comprise an important component of respiratory disease, but alone poor oral health is not responsible for COPD. As controlling for smoking in studies becomes difficult, it is doubtful whether the observed association results from periodontitis and not from the confounding effect of exposure to smoking. Other factors such as environmental factors and genetic factors help to promote the progression of COPD.

COPD is preventable, and dentists have a role to play. Controlling the progression of periodontitis in patients already having periodontitis can help to reduce the incidence of COPD and thereby the health disparity. The efforts of dentist will not only help in providing good oral health but also eventually it might help in reducing the disabling respiratory and other systemic diseases which will help in extending the lifespan and reduce the burden on our health-care system. To prevent COPD, good oral hygiene and periodontal health are essential.[23]

Thus, the present study has shown that poor periodontal status and oral health status are associated with lung functioning in COPD patients. Adjusted analysis for confounder (smoking) showed that OHI was significantly different in patients with and without COPD, suggesting that poor oral hygiene did influence COPD.

One of the limitations of the present study was the use of Community Periodontal Index Probe. The use of periodontal probe (William's graduated probe) to measure the PPD and CAL would have been more sensitive.

In this study, patients without COPD had negligible to weak correlation where OHI, PPD, and CAL with lung function are concerned, suggesting the importance of promoting good oral health. Poor oral hygiene practices have shown association with COPD.[3]

Oral hygiene courses for caregivers in the hospitals can improve the oral health of patients with respiratory infection.[10] Importance of educating the staff of pulmonary medicine (teaching and nonteaching) on the importance of good oral health should be emphasized.

A weak correlation has been seen between OHI, CAL, and lung function status among non-COPD patients, whereas PPD has negligible correlation with lung function. Future studies can be directed in knowing the effect and cause relation between oral hygiene, PPD and CAL with lung function.

CONCLUSION

Periodontitis and respiratory disease share a common risk factor, i.e., smoking which cannot be ruled out, as it constitutes the link between periodontitis and respiratory disease. Thus, on the basis of observed results from the study, it can be concluded that there is an association between PPD, CAL, and OHI with COPD, and OHI is significantly associated with COPD when adjusted for smoking.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.