http://informahealthcare.com/iht ISSN: 0895-8378 (print), 1091-7691 (electronic) Inhal Toxicol, 2014; 26(14): 866–872 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/08958378.2014.965560

RESEARCH ARTICLE

Respiratory symptoms, lung function decrement and chronic obstructive pulmonary disease in pre-menopausal Indian women exposed to biomass smoke Sayali Mukherjee1, Sanghita Roychoudhury2, Shabana Siddique3, Madhuchanda Banerjee4, Purba Bhattacharya5, Twisha Lahiri5, and Manas Ranjan Ray5 Inhalation Toxicology Downloaded from informahealthcare.com by Emory University on 04/19/15 For personal use only.

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Amity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow, Uttar Pradesh, India, 2Central Pollution Control Board, New Delhi, India, Cancer Care Ontario, Ottawa, Ontario, Canada, 4University Of Calcutta, Kolkata, West Bengal, India, and 5Chittaranjan National Cancer Institute, Kolkata, West Bengal, India

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Abstract

Keywords

Background: The impact of chronic exposure to smoke from biomass burning on respiratory health has been examined. Methods: Six-hundred and eighty-one non-smoking women (median age 35 years) from eastern India who cook exclusively with biomass (wood, dung and crop residues) and 438 age-matched women from similar neighborhood who cook with liquefied petroleum gas (LPG) were examined. Pulmonary function test was done by spirometry. The concentrations of particulate matter having diameter of 5 10 mm (PM10) and 5 2.5 mm (PM2.5) in indoor air was measured by real-time aerosol monitor. Results: Compared with LPG users, biomass users had greater prevalence of upper (50.9 versus 28.5%) and lower respiratory symptoms (71.8 versus 30.8%) and dyspnea (58.4 versus 19.9%). They showed reduction in all parameters measured by spirometer especially in mid-expiratory volume. PM10 and PM2.5 concentration in biomass using kitchen were 2–3-times more than LPG-using kitchen, and the decline in spirometry values was positively associated PM10 and PM2.5 levels in indoor air after controlling education, family income and kitchen location as potential confounders. Overall, 29.7% of biomass users and 16.4% of LPG users had deficient lung function, and restrictive type of deficiency was predominant. Chronic obstructive pulmonary disease (COPD) was diagnosed in 4.6% of biomass and 0.9% of LPG users. Women who predominantly used dung cake and did not possess separate kitchen had poorer lung function. Conclusion: Cumulative exposure to biomass smoke causes lung function decrement and facilitates COPD development even in non-smoking and relatively young pre-menopausal women.

Biomass smoke, COPD, india, lung function, women

Introduction About 80% of rural households in India still depend on unprocessed solid biomass such as wood, animal dung and agricultural refuse for cooking and room heating. Biomass users are usually poor people who cannot afford cleaner fuel like electricity or liquefied petroleum gas (LPG). Biomass emits high level of smoke during burning. Smoke emission is even more during monsoon (June–September) when the moisture content of biomass is elevated. Moreover, cooking is usually done in traditional stoves that are not vented outside. As a result, smoke remains in cooking areas for prolonged period leading to high level of indoor air pollution (IAP). In a typical Indian household, the concentration of

Address for correspondence: Dr. Sayali Mukherjee PhD. Amity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow, Uttar Pradesh, India. E-mail: [email protected]

History Received 26 July 2014 Revised 28 August 2014 Accepted 2 September 2014 Published online 29 November 2014

particulate pollutant during cooking with biomass reaches levels several times higher than the National Ambient Air Quality Standard recommended by the US Environmental Protection Agency (Balakrishnan et al., 2002, 2011; Bruce et al., 2000). Another important point is that a large number of poor families in the villages do not possess separate kitchen. They usually do the cooking in a space adjacent to living room. Thus, not only do the housewives who usually prepare the family meals, but also other members of the family including the children who stay with their mothers and the elderly who remain indoor for most of the time get exposed to smoke emitted from burning biomass. Biomass smoke is essentially not different from cigarette smoke and it contains a large number of health-damaging chemicals including high level of particulate matter of different sizes, carbon monoxide, oxides of nitrogen, formaldehyde, acrolein, benzene, toluene, styrene, 1,3-butadiene and polycyclic organic hydrocarbons including benzo (a) pyrene and

COPD in biomass users

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DOI: 10.3109/08958378.2014.965560

transitional metals like Cu, Fe, Ni, Al and Zn (Morawska & Zhang, 2002; Zhang & Smith, 1996). Volatile organic compounds like benzene and polycyclic aromatic hydrocarbon such as benzo (a) pyrene are mutagenic and carcinogenic. It is reasonable to assume therefore that chronic exposures to these pollutants may cause cellular alterations in exposed cells particularly those at the direct line of exposure such as cells of the nasopharynx, oral cavity, airways and the lung. However, little is known about the impact of chronic biomass smoke exposure on respiratory health of Indian women who get married at an early age and become responsible for cooking of family meals with wood, cow dung and agricultural wastes that produce high level of smoke. Against this background, we have investigated in this study the impact of biomass smoke exposure on the prevalence of respiratory symptoms and dyspnea, lung function and chronic obstructive pulmonary disease (COPD) in a group of 681 never-smoking and pre-menopausal married women from the villages of West Bengal, a state in eastern India, who cook exclusively with biomass fuel. We have compared the findings with that of 438 age-matched rural women from similar neighborhood who cooked with cleaner fuel LPG. The study has shown greater prevalence of upper and lower respiratory symptoms, dyspnea, lung function decrement and COPD among biomass users and the changes were positively associated with particulate pollution in indoor air.

Materials and methods Participants and study areas Seven-hundred pre-menopausal women in the age group of 23–43 years residing in 14 villages of Burdwan, Birbhum, Hooghly, Nadia and South 24-Pargans districts of West Bengal, a state in eastern India, who cook exclusively with biomass fuel such as cow dung, wood, dried leaves, jute stick, hay, were invited to participate in this study through village panchayats (local administration) and non-government organizations. Out of them, 683 (97.5%) consented to participate. Another group of 450 pre-menopausal women aged between 23 and 43 years from the same villages but who used to cook with relatively clean fuel LPG were invited to participate and 443 (98.4%) consented. After scrutiny using inclusion and exclusion criteria as listed below, 681 biomass users and 438 LPG users were enrolled. Inclusion and exclusion criteria Inclusion criteria for the study were as follows: (1) cook at least five days/week, 2 h/day either with biomass or LPG for the past 5 years, (2) married, (3) pre-menopausal, (4) normal menstrual cycle length (28 ± 2 days) and (5) nonsmoker and non-chewer of tobacco. Exclusion criteria were: (1) pregnant or lactating, (2) under medication, (3) currently using contraceptive pills and (4) having past history of malignant diseases. The Ethics Committee of Chittaranjan National Cancer Institute approved this study protocol.

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areas with a portable, battery-operated laser photometer (DustTrakTM Aerosol Monitor, model 8520, TSI Inc., Shoreview, MN) that contained 10-mm nylon Dor-Oliver cyclone and operated at a flow rate of 1.7 lit/min, measuring particle load in the concentration range of 1 mg to 100 mg per cubic meter of air. The monitor was calibrated to the standard ISO 12103-1 A1 test dust. Monitoring was carried out for three consecutive days, 8 h per day (07:00–15:00 h), covering both cooking and non-cooking hours. The mean of three days was used as the indoor air quality of a single household. Air quality measurements were performed in 45 biomass-using and 42 LPG-using households during the study period. Since biomass-using women cook in a sitting position 2–3 ft away from the open chullah (oven), the monitor was placed in the breathing zone of the cook, 2.5 ft above floor level on a wooden stool and 3 ft away from the chullah. LPG users, on the other hand, cook in a standing position and the monitor was placed accordingly at a height of 4.5 ft. Prevalence of respiratory symptoms During personal interview with trained female members of the research team each participant was requested to furnish information about age, education, family size and income, habit, cooking time per day, years of cooking, fuel and oven type, location of kitchen, health problems in past three months and last one year, etc. As most of the participants were poorly educated, the researchers entered their responses in structured questionnaire forms on their behalf. Respiratory symptoms were ascertained from survey using structured questionnaire based on the respiratory questionnaire of British Medical Research Council (Cotes, 1987), American Thoracic Society (ATS) and National Heart and Lung Institute Division of Lung Diseases (DLD) questionnaire (ATS-DLD-78C) (Ferris, 1978). The symptoms were broadly grouped into two: upper respiratory symptoms (URS) and lower respiratory symptoms (LRS) (Pope & Dockery, 1999). Dyspnea Dyspnea was assessed following the modified, 6-point Medical Research Council (MRC) dyspnea scale that consists of six questions about perceived breathlessness (Eltayara et al., 1996). The degree of dyspnea was classified into six categories: category 0, no dyspnea; category 1, slight dyspnea (shortness of breath when hurrying on the level or walking up a slight hill); category 2, moderate dyspnea (walks slower than people of the same age on the level because of breathlessness); category 3, moderately severe dyspnea (has to stop because of breathlessness when walking at own pace on the level); category 4, severe dyspnea (stops for breath after walking about 100 yards or after a few minutes on the level) and category 5, very severe degree of dyspnea (too breathless to leave house or breathless when dressing or undressing). Pulmonary function test

Measurement of PM10 and PM2.5 in indoor air Particulate matter with aerodynamic diameter less than 10 mm (PM10) and 2.5 mm (PM2.5) were measured in the cooking

The age, standing height with shoe removed and body weight of each participant were recorded prior to pulmonary function test (PFT). PFT was done in a sitting position and nose closed

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Table 1. Demographic characteristics of the participants.

Parameter Age in year, median (range) Body mass index (kg/m2) Years of cooking, median (range) Cooking hours/day, median (range) Homes with separate kitchen (%) Smokers in the family (%) Years of schooling, median (range) Food habit, mixed (%) Members in family, median (range) Average family income per month (in US $)

LPG users (n ¼ 438)

Biomass users (n ¼ 681)

p Valuea

34 (21–45) 21.9 ± 1.7 16 (5–23) 2.5 (3–5) 91.8 63.9 8 (0–12) 100 4 (3–7) 75

35 (21–45) 21.3 ± 1.4 18 (5–24) 3 (3–6) 44.0 61.8 3 (0–10) 100 4 (4–9) 40

NS NS NS NS 50.001 NS 50.05 NS NS 50.05

a

Inhalation Toxicology Downloaded from informahealthcare.com by Emory University on 04/19/15 For personal use only.

In Chi-square test.

with nose clips by portable spirometer (Spirovit SP-1, Switzerland) following the recommendations of the American Thoracic Society – ATS (ATS, 1995). Forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), mid-expiratory flow (FEF25–75) and peak expiratory flow rate (PEFR) were adjusted for height, sex and age. The spirometers were calibrated daily in the morning before start of the procedure with 2.0 l syringe. Diagnosis of COPD COPD was initially diagnosed on the basis of symptoms of chronic bronchitis i.e. presence of cough and expectorations on most of the days for at least three months in a year for two consecutive years or more. Confirmation of diagnosis and further classification of COPD (stage I, mild; IIA, moderate; IIB severe and stage III, very severe) were based on spirometric measurements following the criteria of Global Initiative for Chronic Obstructive Lung Diseases (GOLD) (Pauwels et al., 2001). Statistical analysis Results are presented as mean ± standard deviation (SD) or median with range. The differences between groups and that between measurable parameters were determined by using Chi-square test, Student’s t-test, and Mann Whitney U test, as applicable. Statistical analyses were performed using SPSS statistical software (Statistical Package for Social Sciences for windows, release 10.0, SPSS Inc., Chicago, IL). Multivariate logistic regression analysis was done to find association between biomass smoke exposure and lung function parameters after controlling potential confounders. Statistical significance was assigned at p50.05.

Results

Table 2. Prevalence (%) of respiratory symptoms and bronchial asthma.

Group

LPG users (n ¼ 438)

Upper respiratory symptoms (URS, Sinusitis Sore throat Runny or stuffy nose Sneezing URS, overall Lower respiratory symptoms (LRS, Dry cough Cough with phlegm Chest discomfort Breathlessness on exertion Wheeze LRS, overall Medically diagnosed asthma

%) 12.3 20.1 10.0 2.7 28.5 %) 15.7 20.3 17.4 22.1 3.2 30.8 2.0

Biomass users (n ¼ 681)

pa

13.1 35.3 31.7 15.8 50.9

0.717 0.001 0.001 0.001 0.001

29.4 37.6 31.1 60.2 9.1 71.8 3.8

0.002 0.001 0.003 0.001 0.001 0.001 0.058

Results are expressed as percentage of individuals with symptoms; many individuals had more than one symptoms. a In Chi-square test.

households lacked separate kitchen compared with 8.2% of LPG-using households (p50.05). Air quality During cooking time, PM10 and PM2.5 concentrations in air of biomass-using kitchen were 552 ± 154 mg/m3 and 298 ± 83 mg/m3, respectively, in contrast to 143 ± 36 mg/m3 and 79 ± 22 mg/m3 in LPG-using kitchen. In non-cooking hours, biomass-using kitchen had 146 ± 44 mg/m3 of PM10 and 82 ± 28 mg/m3 of PM2.5 compared with 72 ± 18 mg/m3 and 42 ± 12 mg/m3, respectively, in LPG-using kitchen. The differences in particulate pollution between biomass and LPG-using households during cooking as well as non-cooking time were highly significant (p50.001) in Student’s t-test.

Demographic characteristics of the participants

Respiratory symptoms

Demographic characteristics of LPG- and biomass-using women who participated in this study are compared in Table 1. It is evident that the two groups were well-matched with respect to age, body mass index, cooking years, average cooking hours per day and number of family members. However, biomass users had lower education and family income than LPG users, and 56% of biomass-using

Self-reported respiratory symptoms prevalence data are presented in Tables 2 and 3. During personal interview more than half (50.9%) of biomass-using women, all neversmokers, declared that they had experienced one or more upper respiratory symptoms in past one month. In contrast, 28.5% of age-matched and never-smoking LPG-using control women from same locality complained of URS. The most

COPD in biomass users

DOI: 10.3109/08958378.2014.965560

Table 3. Prevalence (%) of dyspnea.

Table 5. Comparison of overall lung function between biomass and LPG-using women.

LPG users (n ¼ 438) Dyspnea, overall prevalence (%) MRC category 1 Category 2 Category 3 Category 4 Category 5

19.9 16.7 1.8 1.4 0 0

Biomass users (n ¼ 681) 58.4 37.9 16.5 3.4 0.6 0

pa 0.001 0.001 0.001 0.039 – –

Results are expressed as percentage of individuals with dyspnea. a In Chi-square test.

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Table 4. Comparison of spirometric lung function measurements between biomass and LPG-using women.

Parameter FVC (l) FVC (% predicted) FEV1 (l) FEV1 (% predicted) FEV1/FVC  100 (ratio) FEF25–75% (l/s) PEFR (l/s)

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LPG users (n ¼ 438)

Biomass users (n ¼ 681)

pa

2.38 ± 0.54 85.8 ± 2.93 1.96 ± 0.46 89.9 ± 2.37 82.35 ± 1.12 2.47 ± 0.46 2.84 ± 0.48

2.14 ± 0.35 68.8 ± 5.16 1.77 ± 0.37 71.8 ± 6.82 82.74 ± 1.24 1.92 ± 0.67 2.45 ± 0.86

50.0001 50.0001 50.0001 50.0001 50.0001 50.0001 50.0001

Results are expressed as mean + SD. p50.05 compared with LPG users in Student’s t-test.

Parameter Reduced PFT (%) Type of lung function deficits (%) Restrictive (FVC 580% predicted) Obstructive (FEV1/FVC 570% predicted) Combined (restrictive + obstructive)

LPG users (n ¼ 438)

Biomass users (n ¼ 681)

pa

16.4

29.7

0.001

11.4 4.3

17.9 8.4

0.003 0.008

0.7

3.4

0.003

Results are expressed as percentage of individuals with reduced lung function as measured by spirometry. a In Chi-square test.

Table 6. Prevalence of lung function deficits in non-smoking premenopausal women of eastern India in relation to type of biomass used as cooking fuel.

Parameter Reduced PFT (%) Restrictive type (%) Obstructive type (%) Combined type (%)

Wood (n ¼ 314)

Dung (n ¼ 148)

Crop wastes (n ¼ 219)

28.3 17.2 7.6 3.5

37.8 20.2 10.1 7.4

26.0 16.4 8.2 1.4

a

frequent URS among biomass users was sore throat and runny or stuffy nose. Lower respiratory symptoms were also more prevalent among biomass users and the most frequent complaint was breathlessness on exertion (Table 2). This finding was corroborated by dyspnea prevalence data (Table 3). Complaints of dyspnea (MRC score 40) were made by more than half (58.4%) of biomass-using women in contrast to one-fifth (19.9%) of control women (p50.001). Besides higher prevalence, the degree of dyspnea was more severe among biomass users (Table 3). The biomass-using women had higher prevalence of doctor-diagnosed asthma than control women prevalent among biomass users (Table 2). Reduction in pulmonary function Spirometric lung function data are presented in Table 4. Compared with age-matched LPG users, biomass using women had 240 ml (10.0%) reduction in mean FVC and 190 ml reduction (9.7%) in mean FEV1 with no appreciable change in FEV1/FVC ratio. However, there was 22% decline in mid-expiratory flow rate (FEF25–75%) and 14% reduction in PEFR. After controlling education, family income and kitchen location as potential confounders, PM10 and PM2.5 levels in indoor air, particularly the latter, were positively associated with decline in FVC (odds ratio [OR] ¼ 1.27, 95% confidence interval [95% CI]: 1.07–1.42 for PM10; OR ¼ 1.39, 95% CI: 1.12–1.71 for PM2.5); fall in FEV1 (OR ¼ 1.25, 95%CI: 1.03– 1.45 for PM10; OR ¼ 1.29, 95% CI: 1.06–1.61 for PM2.5), reduction in FEF25–75% (OR ¼ 1.33, 95% CI: 1.09–1.62 for PM10; OR ¼ 1.45, 95% CI: 1.12–1.74 for PM2.5) and decline in PEFR (OR ¼ 1.25, 95% CI: 1.03–1.45 for PM10; OR ¼ 1.29, 95% CI: 1.06–1.61 for PM2.5).

Results are expressed as percentage of individuals with reduced lung function as measured by spirometry; n, number of individuals.

Overall, 29.7% of biomass users had reduced lung function in contrast to 16.4% of LPG-using controls (p50.001). Restrictive type of lung function deficits (FVC 580% predicted) was predominant among biomass as well as LPG users. Obstructive (FEV1/FVC 570% predicted) and combined type (FVC 580% predicted and FEV1/FVC 570% predicted) of lung function deficits was also more frequent among biomass users (Table 5). Type of biomass used as cooking fuel was found to have influence on lung function as prevalence of reduced lung function was highest in women who predominantly used dung cake (Table 6). Difference in the prevalence of overall lung function deficits between dung and wood users (p ¼ 0.04) and between dung and crop residue users (p ¼ 0.01) was significant in Chi-square test. But the difference between wood and crop residue users in this regard was not significant (p ¼ 0.55). The reduction in spirometric values was more pronounced in biomass-using women who did not possess separate kitchen and cooked in a space adjacent to living room. Compared with biomass-using women with separate kitchen, the difference in all the parameters was significant in Student’s t-test (Table 7). Overall, 33.1% women who cooked in adjacent kitchen had deficient lung function compared with 25.3% of women having separate kitchen, and the difference was significant (p ¼ 0.028 in Chi-square test). Women with larger family (four or more members, n ¼ 405) had higher frequency of deficient lung function than those with smaller (up to three, n ¼ 276) family (30.6 versus. 28.3%), but the difference was not statistically significant (p ¼ 0.381 in Chi-square test).

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Table 7. Comparison of spirometric lung function measurements of biomass-using women in relation to kitchen location. Biomass user

Parameter FVC (l) FEV1 (l) FEV1/FVC  100 (ratio) FEF25–75% (l/s) PEFR (l/s)

Table 8. Comparison of spirometric lung function measurements. LPG users (n ¼ 438)

Parameter

With separate kitchen (n ¼ 300)

Adjacent kitchen (n ¼ 381)

pa

2.16 ± 0.37 1.83 ± 0.38 84.78 ± 5.45 2.06 ± 0.72 2.60 ± 0.89

2.10 ± 0.32 1.71 ± 0.35 81.43 ± 6.86 1.78 ± 0.61 2.30 ± 0.82

0.026 50.0001 50.0001 50.0001 50.0001

COPD, total GOLD stage GOLD stage GOLD stage GOLD stage

I, mild COPD IIA, moderate COPD IIB, severe COPD III, very severe COPD

4 (0.9) 4 (0.9) 0 0 0

Biomass users (n ¼ 681) 31 18 10 3

(4.6) (2.6) (1.5) (0.4) 0

Results are expressed as mean + SD; p50.05 compared with LPG users in Student’s t-test.

a

In Student’s t-test.

% women with COPD

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6 4 .6

dung and wood users (4.7 versus 4.4%; p ¼ 0.16), dung and crop residue users (4.7 versus 4.5%; p ¼ 0.13) and between wood and crop residue users (4.4 versus 4.5%; p ¼ 0.78) was not significant in Chi-square test. Similarly, women who cooked in adjacent kitchen had slightly higher COPD prevalence (18/381; 4.7%) than those with separate kitchen (13/300, 4.3%), but the difference was not significant (p40.05).

Discussion

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2 0 .9 0 LPG user

Biomass user

Figure 1. Prevalence of chronic obstructive pulmonary disease (COPD) among non-smoking and pre-menopausal women from eastern India who cook daily with either LPG or unprocessed solid biomass such as wood, dung and crop residues for the past five years or more. COPD was found 5-times more prevalent among biomass users and the difference was highly significant (p50.001) in Chi-square test.

Prevalence of COPD COPD was diagnosed in 31 (4.6%) of never-smoking women who used to cook regularly with biomass fuel compared with four (0.9%) age-matched women cooked with LPG (p50.001 in chi-square test, Figure 1). Among biomass users, the severity of the disease was mild (GOLD stage I) in 2.6% women, moderate (GOLD stage IIA) in 1.5% women and severe (GOLD stage IIB) in 0.4% women. In contrast, COPD was mild in all four LPG users and no one had moderate or severe form of the disease (Table 8). The median age of biomass-using women having COPD was 39 years (range 34–43 years) which was significantly lower than that of LPGusing women with COPD (median age 42 years, range 41–43 years; p50.0001 in Mann–Whitney U test). Thus, COPD was more prevalent and develops at a younger age among biomass users compared with LPG-using control women. The type of biomass used as cooking fuel also had some influence in the disease prevalence as COPD was most prevalent in women who predominantly used dung cake. However, the difference in the prevalence of COPD between

Poor people living in the villages of this part of the world had one or two rooms with mud walls and straw or tin roof. In half of the families kitchen was absent. They cook either in the open courtyard or in the veranda close to the living room. Although cooking in the open helps dispersion of smoke resulting in lesser exposure, it becomes difficult during monsoon and in extreme climatic conditions. So, in most of the days of the year women who do not possess separate kitchen cook in areas closer to the living room. High emission of smoke by biomass coupled with poor ventilation contributes to longer retention of smoke in cooking as well as living areas. The consequence is high level of indoor air pollution that we observed even during non-cooking hours. The impact of chronic biomass smoke exposure on respiratory health of the women has been found widespread. They had greater prevalence of URS and LRS, had deficient lung function and 4.6% women had COPD despite the fact that they were all never-smokers. Respiratory symptoms in general reflect underlying illness or problem in the airways and the alveoli. Therefore, greater prevalence of URS and LRS in biomass users perhaps indicates higher incidence of respiratory diseases and/or airway and alveolar damage following cumulative exposure to smoke emitted from burning biomass. This is not unlikely because earlier studies have associated biomass smoke exposure with a host of respiratory diseases in humans including acute respiratory infections (Smith et al., 2000), chronic bronchitis (Albalak et al., 1999; Pandey, 1984) and tuberculosis (Mishra et al., 1999). But the association of biomass smoke with asthma, a multifactorial disease having both environmental and genetic component, is not conclusive (Bruce et al., 2000). Present finding of a non-significant rise in the prevalence of doctor-diagnosed asthma prevalence among biomass-using women is in conformity with this. Like the present findings, smoke produced by burning biomass has been shown to induce respiratory symptoms and lung function decrement (Ellegard, 1996; Golshan et al., 2002). Reduction of FVC and FEV1 values, especially the

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DOI: 10.3109/08958378.2014.965560

earlier, has been reported in women who cooked with biomass fuel in northern India (Behera et al., 1994) and Turkey (Ozbay et al., 2001). Poorer lung function in women having a larger family, as observed in this study, could be related to greater duration of smoke exposure because it takes a longer time of cooking to prepare meals for a larger family. COPD consisting of chronic bronchitis and emphysema is a progressive lung disease that could be life threatening. It is found mainly among smokers. But we found COPD in 4.6% of biomass-using women who never smoked in their life. It appears that development of the disease was intimately related to cumulative biomass smoke exposure because the prevalence was 5-times less in LPG users. Like the present observation, biomass smoke exposure-related chronic bronchitis and COPD have been reported in non-smoking women of Nepal (Pandey, 1984), Turkey (Ozbay et al., 2001) and Iran (Amoli, 1998). COPD was diagnosed in Iranian (Amoli, 1998) and Turkish women (Ozbay et al., 2001) at an older age of 46–72 years and 59 ± 11 years, respectively. Aging-related decrement in lung function and adverse effect of 26–50 years’ cumulative smoke exposure could have worked together to bring in obstructive lung disease (Lopez, 2014). Women with the diagnosis of COPD in our study, however, were young and pre-menopausal and were cooking with biomass for a lesser period of 16–18 years. It suggests that sustained exposure to biomass smoke even for 15–20 years significantly increases the risk of COPD development among nonsmokers. This observation lends credence to the hypothesis that women who have been cooking with biomass for 15 years are at 2–4-times greater risk of developing COPD (Smith et al., 2001). Although the precise mechanism by which biomass smoke elicits adverse lung reaction is not clear, oxidative stress and airway inflammation have been recognized as possible mediators (Dutta et al., 2012, 2013; Golshan et al., 2002; Laffron et al., 1999). Biomass is less combustible and more polluting than LPG (Zhang & Smith, 1996). It emits smoke that contains coarse (diameter 2.5–10 mm), fine (diameter 0.1–2.5 mm) and ultra-fine (diameter less than 0.1 mm) particles. The majority of particles in biomass smoke are ultra-fine and only a small fraction is in the larger size range (Morawska & Zhang, 2002). Ultra-fine particles induce greater inflammatory response per given mass than larger particles (Oberdorster, 2000). Biomass smoke inhalation affects both endothelial and epithelial barriers in the lung leading to neutrophilic airway inflammation (Banerjee et al., 2012) and acute lung injury with symptoms like cough, dyspnea and wheeze (Laffron et al., 1999). Inflammation has been suggested for respiratory symptoms generated by smoke from burning of crop wastes (Golshan et al., 2002). Although not sensitive or specific for inflammation, decline in FEV1 is usually associated with inflammation. Moreover, we have detected sputum neutrophilia in two-third of sputum samples from biomass-using women along with markedly elevated serum levels of pro-inflammatory cytokine tumor necrosis factor – alpha and neutrophil chemoattractant interleukin-8 (data not shown) that suggest inflammation in the airways which, in turn, can mediate respiratory symptoms and lung function deficits. Besides particulate matter, biomass smoke contains several other pollutants including carbon monoxide,

COPD in biomass users

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oxides of nitrogen and sulphur, and trace metals and volatile organic compounds that could have played a role in impairing respiratory health of the users (Morawska & Zhang, 2002). Another potential smoke constituent that can inflict lung injury is the volatile organic compound benzene. Wood burning emits 10-times more benzene than that of LPG (Zhang & Smith, 1996), and chronic exposure to benzene increases both URS and LRS in human subjects (Pappas et al., 2000). To our knowledge, this is the pioneer study on COPD in relation to IAP from biomass burning in pre-menopausal women in India except for one study being done in South India (Johnson et al., 2011). Besides IAP, however, socioeconomic factors can influence lung function. In fact, social class and poor air quality are independently associated with decreased lung function (Wheeler et al., 2005). Biomass users in this study were less educated and poorer, and poverty is generally linked with malnutrition that affects lung development during childhood via respiratory muscle weakness and overall energy deficiency (Glew et al., 2004). There was little difference in BMI between biomass and LPG users in our study population. Moreover, after controlling education and family income as potential confounders, the positive association between particulate pollution, especially PM2.5, and lung function decrement remained. Admittedly, it is difficult to completely exclude the influence of confounding factors that may be related to adverse lung response such as differing socio-economic status, nutrition, personal hygiene, medical care and quality of life influences through statistical procedures. Despite these limitations, it seems that chronic inhalation of biomass smoke is a major risk factor for lung function reduction and COPD. Biomass smoke exposure has been widespread among rural women in India. In a male-dominated society the task of preparing food for the entire family is the responsibility of the women. They start cooking with highly polluting biomass usually from their early teens and often help their mothers in the kitchen in their childhood. After marriage they take charge of cooking from their mother-in-laws. In most cases the lung was still developing at that time, as lung development becomes complete in the age of 18–20 years in females (Tager et al., 1988). Since developing lung is more vulnerable to air toxics, the impact of IAP could be more harmful and the present findings have confirmed this apprehension. Our observations have wider implications as restrictive type of lung function deficits, the predominant type we observed in this study, is associated with insulin resistance and type-2 diabetes (Fimognari et al., 2007), and both obstructive and restrictive impairments in pulmonary function are associated with increased lung cancer risk (Purdue et al., 2007). It has been also reported that ultrafine particles from biomass combustion can cross the lung–alveolar barrier and cause several haematological changes (Ray et al., 2006), increases the risk of lung carcinogenesis via oxidative stress-mediated activation of Akt signal transduction pathway (Roychoudhury et al., 2012) and reduction in DNA mismatch repair proteins (Mukherjee et al., 2014). Incidentally, type-2 diabetes is steadily increasing among women in India and lung cancer is the fifth leading site of cancer among non-smoking women in eastern India after breast, cervix, gall bladder and ovary

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(National Cancer Registry Programme, 2001–2002), and its incidence is rapidly increasing.

Conclusion This study has shown that indoor air pollution from biomass fuel combustion is a matter of serious concern for women in rural households of Eastern India. But, this issue of utter public health hazard which affects the majority of Indian population is being neglected. The study underscore the express need for improvement of indoor air quality in rural areas through improved stoves that emit fewer pollutants than traditional stoves, better ventilation in cooking areas, and fuel switching from biomass to LPG, biogas or solar energy.

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Declaration of interest The authors report no conflicts of interest.

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