Prevalence of periodontitis in patients with pulmonary disease: A cross-sectional survey in the industrial district of India.

BACKGROUND: Evidence state that periodontitis may have a contributory role in the onset and progression of pulmonary diseases. However, very limited data are available till date, studying the coexistence of both the conditions. AIM AND
OBJECTIVE: The aim and objective of this study are to determine the prevalence of periodontitis among patients affected with various pulmonary diseases in Moradabad District, Uttar Pradesh, India.
MATERIALS AND METHODS: A total of 700 patients suffering from pulmonary diseases including tuberculosis (TB), chronic obstructive pulmonary disease, or pneumonia within the age group of 12-70 years were selected for the study. A detailed case-history for both pulmonary and periodontal status was taken. Periodontal Disease Index and Periodontal Index for Risk of Infectiousness were recorded for all patients. The scores were calculated and subjected to statistical analysis.
RESULTS: Individuals with pulmonary diseases showed a statistically significant prevalence of periodontal disease with higher values of periodontal disease index (31%) and periodontal index for risk of infectiousness (55%) at P < 0.05. Patients suffering from TB within the age group of 51-60 (42%) showed the highest prevalence of periodontitis with a more number of males (43%) being affected as compared to females at P < 0.01.
CONCLUSION: Most of the study population was diagnosed with periodontitis with a higher proportion categorized under high-risk category as per PIRI scores.

INTRODUCTION

Microbial plaque associated with periodontal infection, the chronic nature of these diseases, and the exuberant local and systemic host responses to the microbial assault are the influencing factors for the overall health and the course of various systemic diseases.[1] Miller suggested an extensive role of the oral cavity and oral infection such as periodontal disease for having systemic effects.[2] Since the very beginning of medical sciences, the association between the oral health and the general health of an individual has been a subject of interest.[13456] Contemporary studies of the association of periodontal diseases with systemic disorders and their mutual cause-effect relationships are one of the main areas of research in periodontology.[1678910]

Offenbacher, in 1996, first suggested that periodontal medicine is a broad term that defines a rapidly emerging branch of Periodontology focusing on the wealth of new data establishing a strong relationship between periodontal health or disease and systemic health or disease.[5] This implies a two-way relationship in which the periodontal status of an individual may influence an individual's health systemically as well as the role of systemic disease in influencing an individual's periodontal health.[511]

The possible contribution of oral pathogens especially those present in periodontal pockets to various systemic conditions have been acknowledged for decades.[1310] Focal infection theory describes a local infection site disseminating microorganisms and/or their toxins to distant locations, which might lead to secondary infections that initiate, sustain, or worsen systemic diseases, usually chronic, such as atherosclerosis or arthritis or cancer.[11213] Although an ancient concept, it took a modern form around 1900 and was accepted widely by 1989.[113]

With evolved understanding of disease pathogenesis and transmission, three possible mechanisms for focal infection theory were suggested. They were as follows: (1) metastasis of infection, (2) metastatic toxic injury, and (3) metastatic immunologic injury might occur simultaneously and even interact with each other.[12] It could thus be precluded that oral cavity might act as the focal site of origin for dissemination of pathogenic micro-organisms to distant locations especially in immunocompromised hosts and that “uncontrolled advanced periodontitis” presents a substantial infectious burden for the entire body by releasing bacteria, bacterial toxins, and other inflammatory mediators into the bloodstream causing systemic complications.[1213] An altogether shift in the paradigm regarding the directionality of oral and systemic associations was thus presented.[1111213]

It has also been established that systemic conditions such as cardiovascular diseases, diabetes mellitus, pregnancy, and various immunological disorders may also contribute toward the severity of periodontal disease.[911] A huge amount of evidence supports the notion that untreated periodontitis may lead to varieties of adverse systemic conditions in an individual.[111] Thus, good oral health maintenance is a key component to good systemic health, and individuals with periodontitis are more prone to develop various systemic conditions such as cardiovascular diseases including myocardial infarction, atherosclerosis, and stroke; adverse pregnancy outcomes such as pre-term low birth-weight babies, diabetes mellitus, osteoporosis; and respiratory disorders such as pulmonary tuberculosis (TB), chronic obstructive pulmonary disorder (COPD), pneumonia (PN), asthma, and influenza.[111] It has been hypothesized that in individuals with periodontitis, oral pathogens present in the gingival sulcus or the subsequently formed periodontal pockets may enter the lungs by inhalation or by aspiration of oropharyngeal secretions.[8] Therefore, it is possible that oral micro-flora might infect the respiratory tract, causing various respiratory diseases.[810]

However, only a few studies all over the world have reported an association between periodontal diseases and respiratory disorders such as COPD, PN, asthma.[135911] Studies on periodontal status in TB cases are even scarcer.[13] India being the highest TB burden country accounting for one-fifth of the global incidence with 1.98 million annual incidences of a total 9.4 million globally.[14] Despite such a scenario, a very limited number of studies have been conducted to evaluate the association of TB with periodontal diseases in India.

The release of brass and silica dust and gases ozone, nitrogen oxides, acetylene, and phosphine are also liberated during welding may pose a threat to the health of these workers, as well as the general population residing around, as there are no control measures such as personal protection (masks) as well as exhaust ventilation systems installed in this type of cottage industry.[15]

There is limited literature determining the prevalence of pulmonary diseases in industrial cities like Moradabad, as manufacture of brassware is one of the cottage industries in Moradabad. Therefore, the present study was conducted to evaluate the association by determining the prevalence of periodontal diseases in patients afflicted with various pulmonary diseases in Moradabad District.

MATERIALS AND METHODS

A cross-sectional epidemiological survey was conducted to assess the periodontal status among patients with various pulmonary diseases. The data were obtained from the out- and in-patient department of TB and chest. A total of 700 patients, both male and females, of age group 12–70 years were included in the study.

Ethical clearance

The Ethical clearance was obtained from the Institutional Ethical Committee (TMU/EC/302), along with the permission from the respective department to conduct the survey. A written informed consent was obtained from the participants or their attendees before carrying out the examination which was in accordance with the World Medical Association's Declaration of Helsinki.[16]

Inclusion criteria

Patients in the age group of 12–70 years diagnosed with pulmonary disease including TB, chronic obstructive pulmonary disease, or PN were included in the survey. Patients who were not willing to sign the consent, who had undergone periodontal therapy in the last 3 months, who were diagnosed with any other systemic diseases, edentulous patients, and/or patients on medications (e.g., antibiotics) known to influence the periodontal tissue for the last 6–8 weeks were not included in the study.

Study design

The present cross-sectional epidemiological survey was conducted to assess the prevalence of periodontitis in patients suffering from various pulmonary diseases including TB, chronic obstructive pulmonary disease, or PN in Moradabad district, over a period of 2 years, i.e., from August 2013 to July 2015.

A total of 700 patients suffering from pulmonary diseases, in the age group of 12–70 years were assessed for their periodontal status. A detailed Questionnaire/case-history was taken including the various clinical signs and symptoms, history, diagnosis, and periodontal status of each patient.

Sample size calculation

The sample size was calculated on the basis of the results of the pilot study which was done on 100 cases of the pulmonary disease. A total of 700 patients formed the final sample size to be recorded for the study, and the participants who were part of the pilot study were not included again in the main study to avoid bias.

Method of collection of data

The patients were screening at the Department of TB and Chest and those who satisfied the inclusion, and the exclusion criteria were selected. The medical condition of the patients under the study was confirmed from the medical records of the Department which included the clinical history as well as other investigations. The survey consisted of 700 patients including 430 males and 270 females. Out of 700, 266 were diagnosed with pulmonary TB, 231 for chronic obstructive pulmonary disease (COPD), and 203 for PN.

The data were collected by a single investigator using a questionnaire (Contact the corresponding author for a copy of the questionnaire), and clinical examination was done to record the periodontal disease index[17] (PDI) and periodontal index for risk of infectiousness[18] (PIRI). PDI includes the plaque, calculus, and gingival/periodontal components each with a scoring range of 0-3 that are recorded on index teeth, i.e., 16, 21, 24, 36, 41, and 44. PIRI includes two components, (1) Pocket lesions based on the number of pockets with a certain depth with scoring range of 1–6, and (2) Furcation involvement based on the number and degree of furcation involvements with scoring of 1–4.

The PIRI scores were put together, and the patients were then classified into three categories of risk of metastatic injury from the periodontal niches; low-risk group: PIRI = 0; moderate risk group: 1 ≤ PIRI ≥ 5; and high-risk group: 6 ≤ PIRI ≤ 10. The data obtained from both the indices was subjected to statistical analysis.

Statistical evaluation

Statistical analysis was done using SPSS software version 19.0. IBM Inc., Chicago, IL, USA. Chi-square test was done to find the association between various categorical variables. The continuous variables were analyzed and expressed in descriptive statistics such as mean and standard deviation. The inferential statistics was done and expressed by the application of the test of significance to check and estimate if there is any significant difference of the mean of various measurements. The test of significance between the total score was done by regression analysis, and P < 0.05 was taken as significant level. The precision of the variability of the parameter and the risk of having the high-risk PIRI was estimated by odds ratio, expressed in the form of 95% confidence Interval (95% confidence interval).

RESULTS

The present cross-sectional survey consisted of 700 patients including 430 males and 270 females [Graph 1]. Out of 700, 266 were diagnosed for pulmonary TB, 231 for COPD, and 203 for PN. The maximum number of participants was under the age group of 51-60 years, while the minimum was observed in < 20 years of age group as shown in Graph 2.

Graph 1

Distribution of the study population based on sex. n – number of participants

Graph 2

Distribution of study population based on different age groups. n – number of participants

In Table 1, the age and gender distribution of the three pulmonary diseases among the study population are shown. The prevalence of COPD was higher in the 21–30 years age group whereas PN showed significantly high prevalence in the youngest age group of <20 years. Higher prevalence of TB was observed almost equally in the older age groups of 41–50 and 51–60 years. Among the males and females, higher prevalence of COPD and PN were observed in females and TB in males.

Table 1

Distribution of the study population based on age and gender in the three pulmonary diseases

	Respiratory disease
	COPD, n (%)	Pneumonia, n (%)	TB, n (%)	Total, n (%)
Age groups (years)
≤20	3 (23.1)	10 (76.9)	0	13 (100.0)
>60	30 (31.9)	36 (38.3)	28 (29.8)	94 (100.0)
21-30	23 (37.1)	18 (29.0)	21 (33.9)	62 (100.0)
31-40	45 (32.1)	41 (29.3)	54 (38.6)	140 (100.0)
41-50	64 (34.4)	44 (23.7)	78 (41.9)	186 (100.0)
51-60	66 (32.2)	54 (26.3)	85 (41.5)	205 (100.0)
Total	231 (33.0)	203 (29.0)	266 (38.0)	700 (100.0)
χ2, df, P	24.6, 10, 0.006 (strongly significant)
Sex
Female	99 (36.7)	91 (33.7)	80 (29.6)	270 (100.0)
Male	132 (30.7)	112 (26.0)	186 (43.3)	430 (100.0)
Total	231 (33.0)	203 (29.0)	266 (38.0)	700 (100.0)
χ2, df, P	13.2, 2, 0.001 (strongly significant)

COPD – Chronic obstructive pulmonary disease; TB – Tuberculosis; n – Number of participants; % – Percentage of participants; df – Degrees of freedom, P<0.05 – Statistically significant. Chi-square value 24.6 and 13.2 at ten and two degrees of freedom, respectively. χ2 – Chi-square test value; P – Statistical significance

Table 2 shows the highest number of participants recorded score 3 (435) followed by those recorded with score 2 (262) of the plaque component. Of particular interest was that only three participants recorded with score 1. However, based on the calculus component, maximum number of participants was recorded for Score 2 followed by Score 3.

Table 2

Distribution of study population based on plaque and calculus component scores of periodontal disease index

Scores	Plaque component, n (%)	Calculus component, n (%)
Score 1	3 (0.4)	99 (14.1)
Score 2	262 (37.4)	368 (52.6)
Score 3	435 (62.1)	233 (33.3)

n – Number of participants within each score; % – Percentage of participants within each score

Graph 3 and Table 3 show the gingival and periodontal components of the respiratory diseases, showing that the highest number of participants for scores 2 and 4 were recorded in COPD patients whereas the highest number for scores 3, 5, and 6 were recorded in TB patients. None of the study participants were recorded with scores 0 and 1.

Graph 3

Gingival and periodontal scores of periodontal disease index among respiratory diseases. COPD – Chronic obstructive pulmonary disease, TB – Tuberculosis

Table 3

Distribution of study population based on gingival and periodontal component scores of periodontal disease index

Gingival and periodontal component score	Respiratory disease
	COPD, n (%)	Pneumonia, n (%)	TB, n (%)	Total, n (%)
0	0	0	0	0
1	0	0	0	0
2	16 (41.0)	14 (35.9)	9 (23.1)	39 (100.0)
3	16 (23.5)	25 (36.8)	27 (39.7)	68 (100.0)
4	62 (33.0)	65 (34.6)	61 (32.4)	188 (100.0)
5	74 (34.3)	53 (24.5)	89 (41.2)	216 (100.0)
6	63 (33.3)	46 (24.3)	80 (42.3)	189 (100.0)
Total	231 (33.0)	203 (29.0)	266 (38.0)	700 (100.0)
χ2, df, P	15, 8, 0.058 (nonsignificant)

COPD – Chronic obstructive pulmonary disease; TB – Tuberculosis; n – number of participants with COPD, pneumonia or TB within each score; % – Percentage of participants with COPD, pneumonia or TB within each score; df – Degrees of freedom, P<0.05 – Statistically significant. Chi-square value 15 at eight degrees of freedom. χ2 – Chi-square test value; P – Statistical significance

Based on PIRI scores as shown in Table 4, majority of the population was recorded under high-risk category with highest risk observed in TB patients followed by COPD and pneumonia. The presence of hypertension and diabetes mellitus were significantly associated with the high-risk category for total score as P < 0.001 at 5% significance level. Smoking was not associated with total score high-risk category [Table 5].

Table 4

Distribution of risk categories within study population based on periodontal index for risk of infectiousness scores

	Respiratory disease			Total
	COPD	Pneumonia	TB
Risk category, n (%)
High	131 (33.9)	97 (25.1)	159 (41.1)	387 (100.0)
Moderate	67 (32.2)	71 (34.1)	70 (33.7)	105 (100.0)
Low	33 (31.4)	35 (33.3)	37 (35.2)	208 (100.0)
χ2, df, P	7, 4, 0.133 (nonsignificant)

COPD – Chronic obstructive pulmonary disease; TB – Tuberculosis; n – Number of participants with COPD, pneumonia or TB within each category; % – Percentage of participants with COPD, pneumonia or TB within each category; df – Degrees of freedom, P<0.05 – Statistically significant. Chi-square value 7 at four degrees of freedom.χ2 – Chi-square test value; P – Statistical significance

Table 5

Association of the high-risk periodontal index for risk of infectiousness category with heart diseases, diabetes mellitus, and smoking, taking moderate risk category as a reference

Parameter estimates
Total scorea=6≤ PIRI ≤10	B	SE	Wald	df	Significant	OR	95% CI for OR
							Lower	Upper
Intercept	1.306	0.276	22.395	1	0.000
Hypertension	1.650	0.349	22.288	1	0.000	5.206	2.625	10.328
Diabetes mellitus	1.102	0.268	16.901	1	0.000	3.012	1.780	5.094
Smoking	0.501	0.262	3.655	1	0.056	1.650	0.987	2.758

aThe reference category is: 1

DISCUSSION

The present cross-sectional study was conducted to determine the prevalence of periodontitis and to evaluate the risk of infectiousness for periodontal diseases in patients suffering from pulmonary diseases such as TB, COPD, and PN. Among the pulmonary diseases, distribution of the study population suffering from TB, chronic obstructive pulmonary disease (COPD), and PN was 38%, 33%, and 29% respectively.

In the present study, distribution of patients suffering from all the three pulmonary diseases was found to be highest in the age group of 51–60 years and the least in the individuals who were of <20 years of age. The overall sex ratio was 1.59:1 (male:female). A similar study conducted in various parts of India reported the overall prevalence rates of various pulmonary diseases in males and females of over 35 years of age as 5.0% and 3.2%, respectively. It is distinctly more common among men and smokers. Since tobacco smoking is the most known and established risk factor for COPD, the male predominance is partly explained on the basis of the male: female differences in smoking habits particularly in India.[67] Significantly, both the male: female and the smoker: nonsmoker ratios for COPD in India are not as high as in the Western populations.[56] This is largely attributed to the indoor air pollution from domestic combustion of solid fuels for cooking and heating to which the women are significantly more exposed.[8] This is particularly true in the rural and hilly areas where the solid biomass fuels are primarily used. Exposure to environmental tobacco smoke (Passive smoking) from male smokers in the house is another important risk factor for COPD in nonsmoker women. COPD is more commonly seen in people living in polluted areas as well in those engaged in dusty occupations. Continued exposure to environmental and occupational dusts is an important cause of chronic bronchial irritation which may also progress to airway obstruction after prolonged and persistent injury to the airways.

Based on the gingival and periodontal component scores of the Periodontal Disease Index, it was observed that the majority of the study population suffered from severe form of periodontitis while the least recorded for mild-to-moderately severe gingivitis. In a similar study conducted by Katancik et al., patients with obstructive airway disease were found to have worse indices of periodontal health. All periodontal indices were elevated in smokers regardless of pulmonary status. Periodontal disease as a chronic bacterial infection may provide a direct source of aspirated bacterial organisms that may lead to the progression and exacerbation of respiratory disease.[19] These bacteria of oral origin may stimulate the respiratory tissues, resulting in the inflammatory response associated with the obstructive pulmonary disease.[78] Periodontal disease as a chronic inflammatory disease is associated with multiple inflammatory cells such as neutrophils and monocytes and inflammatory mediators such as interleukin (IL)-1, IL-6, IL-8, and tumor necrosis factor-a. This chronic inflammatory state may indirectly contribute to respiratory inflammation through mediators released into the saliva and carried to the respiratory epithelium.[13] This could explain the potential link between periodontal health and pulmonary diseases.

Based on the PIRI scores, highest proportion of the study population was categorized as high-risk category, followed by medium risk category, and the least as low-risk category. In a study by Prasanna, PIRI scores for patients afflicted with COPD were significantly higher than those without the disease. This indicates that periodontal disease which may act as a risk factor for COPD, even slight elevations in risk, if true, can have major implications. Such associations could also be accountable for the hypothesis that the co-occurrence of COPD and periodontal disease may be due to a common underlying host susceptibility factor. The release of bacterial endotoxins from periodontal pockets in the bloodstream supports the hypothesis that periodontal disease could play a causative role in the development of systemic pathologies. The periodontal index for risk of infectiousness (PIRI)[20] is an individual index that takes into account the number of periodontal pockets per patient as well as their depth. Hence, the PIRI gives an indirect quick and rough estimation of the surface area of contact between the subgingival bacterial biofilm and the epithelial walls of the periodontal pockets and is representative of the risk of release of pro-inflammatory mediators (such as endotoxins) from the periodontal sites into the bloodstream. It suggests that the periodontal status may serve as a useful risk marker to identify persons at higher risk for various pulmonary diseases.

In the present study, the highest number of patients under High-risk category based on PIRI suffered from TB, depicting an association between the two conditions. However, to best of our knowledge, there is no literature supporting this correlation.

A significantly higher proportion of the study population suffering from diabetes mellitus, heart diseases, and smoking was found to have poor periodontal status in all the three pulmonary conditions, we considered them as important confounding factors[202122] in this study.

Limitations

Several limitations of the present study need to be considered. Despite the presence of a significant population of brass workers in Moradabad, a direct link between periodontal status and pulmonary diseases could not be exclusively established in this study. In addition, this study is cross-sectional, an exact cause-effect relation between the pulmonary diseases and periodontal status could not be elucidated. Moreover, patients suffering from two or more pulmonary diseases simultaneously were not included in the study. Had such participants been taken into consideration, the outcome of the study would have been significantly different.

CONCLUSION

The survey was conducted to determine the prevalence of periodontitis in patients suffering from various pulmonary diseases in Moradabad district. The results suggested that the majority of the study population suffered from severe form of periodontitis and the highest proportion of study population was categorized as high-risk category, followed by medium risk category, and the least as low-risk category. Within the limitations of this study, it can be concluded that a majority of the study population had pre-existing periodontitis. Further studies, both cross-sectional and longitudinal, preferably with larger sample sizes should be undertaken to reinforce the findings of the present study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.