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Chronic Obstructive Pulmonary Disease Secondary to Household Air Pollution Sumi Mehta, MPH, PhD4

1 Division of Pulmonary, Critical Care and Sleep Medicine, Department

of Internal Medicine, University of New Mexico Health Sciences Center School of Medicine, 1 University of New Mexico, Albuquerque, New Mexico 2 Division of Occupational and Environmental Medicine, Department of Internal Medicine, University of California San Francisco School of Medicine, San Francisco, California 3 Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley, California 4 Department of Research and Evaluation, Global Alliance For Clean Cookstoves, Pennsylvania, Washington, District of Columbia 5 Dow University of Health Sciences, Ojha Campus, Karachi, Pakistan

Umar Cheema5

Address for correspondence Akshay Sood, MD, MPH, Division of Pulmonary, Critical Care and Sleep Medicine, Department of Internal Medicine, University of New Mexico Health Sciences Center School of Medicine, 1 University of New Mexico, MSC 10 5550, Albuquerque, NM 87131 (e-mail: [email protected]).

Semin Respir Crit Care Med 2015;36:408–421.

Abstract

Keywords

► ► ► ►

emphysema chronic bronchitis pulmonary function bronchial anthracofibrosis ► particulate matter

Approximately 3 billion people around the world cook and heat their homes using solid fuels in open fires and rudimentary stoves, resulting in household air pollution. Household air pollution secondary to indoor combustion of solid fuel is associated with multiple chronic obstructive pulmonary disease (COPD) outcomes. The exposure is associated with both chronic bronchitis and emphysema phenotypes of COPD as well as a distinct form of obstructive airway disease called bronchial anthracofibrosis. COPD from household air pollution differs from COPD from tobacco smoke with respect to its disproportionately greater bronchial involvement, lesser emphysematous change, greater impact on quality of life, and possibly greater oxygen desaturation and pulmonary hypertensive changes. Interventions that decrease exposure to biomass smoke may decrease the risk for incident COPD and attenuate the longitudinal decline in lung function, but more data on exposure–response relationships from well-designed longitudinal studies are needed.

Approximately 3 billion people around the world cook and heat their homes using unprocessed solid fuels in open fires and rudimentary stoves, resulting in household air pollution (HAP) (►Fig. 1).1 Illnesses caused by HAP were responsible for approximately 4.3 million premature deaths worldwide in children and adults in 2012.1 HAP is a leading risk factor for noncommunicable diseases in developing countries, and arguably the leading risk factor among women. Over one-third of premature deaths from chronic obstructive pulmonary disease

Issue Theme Occupational and Environmental Pulmonary and Bronchiolar Disorders; Guest Editors: William N. Rom, MD, MPH; Joan Reibman, MD

(COPD) in low and middle income countries can be attributed to exposure to HAP from cooking with solid fuels.1 Clinical evidence of this association has been well documented for over three decades now2–4 and several recent reviews of the epidemiologic evidence have described the association between HAP and COPD.5,6 This nonsystematic review of the medical literature, with a more clinical focus, describes COPD outcomes secondary to HAP from the combustion of various types of indoor solid fuel (►Fig. 2).

Copyright © 2015 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.

DOI http://dx.doi.org/ 10.1055/s-0035-1554846. ISSN 1069-3424.

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Nour A. Assad, MD1 John Balmes, MD2,3 Akshay Sood, MD, MPH1

Assad et al.

Fig. 1 Global use of indoor solid fuels in 2012, as reported in percentage, by the World Health Organization (WHO). (Reproduced with permission from World Health Organization. Global Health observatory map gallery. Map on world populations using solid fuels (%), 2012: total. Available at: http://gamapserver.who.int/mapLibrary/Files/Maps/Global_iap_exposure_2012.png. Accessed January 5, 2015).

Household Solid Fuels In this review, we will focus on COPD secondary to HAP from indoor solid fuels used for cooking, namely, biomass and coal. Biomass fuel refers to any living or recently living plant- and/

or animal-based materials that are burnt by people for energy. Biomass fuel includes wood and charcoal (a product of incomplete burning of wood), twigs, grass, or agricultural crop residues (e.g., corn husk, straw, and bagasse which is biomass remaining after processing sugarcane) as well as

Fig. 2 Indoor sources of energy.

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dried animal dung (e.g., cow dung). Coal on the other hand is a solid fuel distinct from charcoal. It is a fossil fuel formed from preserved compressed and partially metamorphosed organic material, which occurs in both smoky (bituminous) and “smokeless” (anthracitic) types. “Clean” fuels include liquefied petroleum gas (LPG), methane, natural gas, biogas, ethanol, and electricity. While kerosene was previously considered a “clean” fuel, an emerging body of evidence suggests major health implications associated with kerosene combustion, and the World Health Organization (WHO) has cautioned against its use until further research can be conducted.7 Kerosene is a fractional distillate of petroleum that is similar to both jet and diesel fuels so the relative toxicity of its domestic combustion in inefficient cooking and lighting devices should not be surprising. Indoor solid fuels are used for heating and cooking. In developing countries, solid fuels are used mainly for cooking, often using unvented and inefficient stoves that are made of stones, a hole in the ground, or a rounded pit, often without ventilation. In developed countries and developing countries with cold climates, solid fuel (primarily wood) is used for heating, using fireplaces or wood-burning stoves, which are often poorly maintained and leaky (►Fig. 3).8

Contents of Household Air Pollution The combustion of solid fuels produces a complex mixture of air pollutants,9,10 including respirable particulate matter (PM). PM10 refers to particles with mass median aerodynamic diameter of less than 10 µm. These particles are small enough to be easily inhaled past the vocal cords and deposit primarily in the conducting airways. PM of aerodynamic diameter of less than 2.5 µm (PM2.5) is a subfraction of

PM10 that has even greater potential for lung toxicity because its smaller size allows penetration to the alveolar spaces. In addition to PM, solid fuel smoke contains carbon monoxide, oxides of nitrogen and sulfur, benzene, formaldehyde, 1,3butadiene, polycyclic aromatic hydrocarbons such as benzo (α)pyrene, free radicals, aldehydes, volatile organic compounds, chlorinated dioxins, oxygenated and chlorinated organic matter, and endotoxin.11 The U.S. Environmental Protection Agency (EPA) defines the 24-hour recommended standard for PM10 and PM2.5 of no more than 150 and 35 µg/m3, respectively.12 The comparable WHO guidelines are 50 and 25 µg/m3, respectively.12 In households with limited ventilation, as is common in developing countries, PM10 exposures experienced by household members may be 100 times higher than the WHO and EPA limits, with levels of PM10 as high as 20,000 µg/m3.13 Products of combustion of different types of solid fuel are not identical. For example, cooking with wood-burning stoves results in significantly higher amount of PM than either charcoal or LPG stoves (1,260, 540, and 200–380 µg/m3, respectively, in one study).14 Cow dung produces 23% more fine particulates (PM2.5) per unit mass of sample burned (8.5 vs. 6.9 g/kg) and as it also burns at a faster rate than wood (3.5 vs. 2.2 kg/h), cow dung combustion results in twice as much PM production than wood.15,16 Endotoxin levels can be high in emissions from burning maize crop residues and animal dung.11 This suggests that the type of solid fuel used has an impact on the type and level of exposure and consequently the severity of adverse outcomes. Two common features of emissions from solid fuel combustion are a particulate phase that is characterized by particles with a carbon core with complex organic compounds adsorbed onto their surfaces and a gas phase that contains airway irritants.

Burden of Adverse Health Effects Related to Household Air Pollution

Fig. 3 The energy ladder. Fuels lower in the energy ladder are less efficient and produce more pollution, but are less expensive. Conversely, fuels higher in the energy ladder are more efficient and produce less pollution, but are more expensive. (Reproduced with permission from Sood A. Indoor fuel exposure and the lung in both developing and developed countries: an update. Clin Chest Med 2012;33:649–665.) Seminars in Respiratory and Critical Care Medicine

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According to the Global Burden of Disease 2010 comparative risk assessment, tobacco smoking and HAP were the second and third leading risk factors for global burden of disease, responsible for 6.3 and 4.0 million annual deaths, respectively.17 Among the 4 million deaths in children and adults from illnesses attributed to HAP in 2010, 34% were due to stroke, 26% from ischemic heart disease, 22% from COPD, 12% from pneumonia, and 6% from lung cancer1 and approximately half of these deaths occurred in women and children.17 Using the same methodology and slightly different background disease estimates, the WHO estimated that HAP was responsible for around 4 million premature deaths in 2012.18 About 3 billion people, half the worldwide population, are exposed to HAP, as compared with 1 billion people who smoke tobacco.19 COPD of moderate-to-severe intensity affects 65 million people around the world.18 More than 3 million people died of COPD in 2005, which corresponds to 5% of all deaths globally.18 Already the third leading cause of death in the United States, COPD is expected to also become the third leading cause of death worldwide by 2020.6 HAP secondary to indoor combustion of solid fuel is the biggest risk factor for

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Effects of Household Air Pollution on Lung Function Airflow Obstruction HAP is associated with greater risk for having obstructive ventilatory defects, as demonstrated by multiple studies, mostly cross-sectional and a few case–control studies. Although this finding has been consistent across both developing and developed countries, data in developed countries is limited to very few studies.

Developing Countries In a large population-based study of over 5,500 adult Colombians, exposure to wood smoke for 10 years or longer was associated with 1.5-fold increase in odds ratio (OR) of COPD, as defined by the Global Initiative for Chronic Obstructive Lung Disease (GOLD) criteria,23 that is, postbronchodilator forced expiratory volume in one second/forced vital capacity (FEV1/FVC) ratio < 70%.24 Another study of over 1,600 young adults in Nepal demonstrated a 2.1-fold greater OR of COPD, as defined by the lower limit of normal FEV1/FVC value; although the amount and duration of smoke exposure was not quantified.25 In another study of 900 women in rural Southern India, the prevalence of COPD, as defined by GOLD criteria, in biomass users was 1.4-fold greater than that in clean fuel users.26 Liu et al in a population-based study, demonstrated higher prevalence rates of COPD in a rural area in China (mostly using biomass and charcoal—12%) versus an urban area (mostly using liquid petroleum gas— 7%). Using urban/rural area as a surrogate for fuel type, the study demonstrated that residence in a rural area was associated with 1.8-fold greater prevalence of GOLD-defined COPD in a multivariate analysis, and found similar results when analysis was restricted to nonsmoking women.27 In Brazil, a cross-sectional study found the prevalence of airflow obstruction, defined by GOLD criteria, in biomass smokeexposed nonsmokers to be 20%, similar to the prevalence in smokers who cook with clean fuel.28 One meta-analysis

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concluded that the pooled OR for developing COPD in subjects exposed to biomass smoke is 4.4 in smokers and 2.6 in nonsmokers, as compared with their unexposed counterparts.29 In summary, biomass smoke exposure is a consistently important risk factor for developing airflow obstruction in many developing countries across the world.

Developed Countries Few studies have analyzed the association between HAP and COPD in developed countries, reflective of the underestimation of the importance of this exposure in developed countries. In a population of smokers recruited from an urban center in New Mexico in southwestern United States, 28% reported exposure to wood smoke. This data suggest that biomass smoke exposure is not infrequent in selected populations in developed countries. In the same New Mexican cross-sectional study, self-reported wood smoke exposure was associated with low postbronchodilator percent predicted FEV1 and greater prevalence of GOLD-defined COPD with a remarkably similar OR for COPD of 2.0 as those described by published studies in the developing countries.22 A similar OR of 2.5 for the association between biomass smoke exposure and similarly defined COPD was demonstrated in a cross-sectional study of nonsmoking women in Turkey, technically a “developed” country, but one that still includes a substantial population living in rural, less developed areas with continued use of household biomass fuel.30 In a Spanish case–control study, combined wood and charcoal smoke exposure was associated with a 4.5-fold greater OR of having COPD, defined by irreversible airflow obstruction as per the GOLD criteria.31 Using a selfreported physician diagnosis of COPD rather than spirometry, another case–control study of Turkish nonsmoking women concluded that biomass smoke exposure for at least 30 years was associated with a 6.6-fold higher OR for COPD, a significantly higher strength of association than generally described in the literature.32 Although understudied and often ignored, these data suggest that HAP is an important cause of COPD in developed countries as well.

Dose–Response Relationship When biomass smoke exposure is quantified by hour-years, the product of number of hours of daily exposure and the total years of exposure, this metric shows a negative association with FEV1, suggesting that greater amount of exposure to biomass smoke is associated with greater respiratory impairment.28,33 Other studies have looked at the individual components of this metric and showed that the OR for COPD is greater in subjects with either longer duration of exposure (in years) or more heavy exposure (in hours per day).31

Household Air Pollution and Emphysema Prevalence The emphysema phenotype of COPD seems to be less strongly associated with HAP exposure than tobacco smoking.34–36 The prevalence of emphysema in nonsmokers exposed to biomass smoke has been reported to be 32% in one study compared with 46% in smokers.36 Seminars in Respiratory and Critical Care Medicine

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COPD globally.19 In communities that primarily depend on solid fuel for energy, HAP is responsible for a greater fraction of COPD risk than tobacco smoking or outdoor air pollution.18 Cooking with biomass fuels accounts for the high prevalence of COPD among nonsmoking women in parts of the Middle East, Africa, and Asia.18 The burden of disease may be greatest in sub-Saharan Africa.20,21 The absolute number of people using mainly solid fuel for cooking has remained stable over the past three decades at approximately 2.8 billion. The proportion of the world’s households relying mainly on solid fuels for cooking, however, has declined from 53% in 1990 to 41% in 2010.6 There is a large regional variation and sub-Saharan Africa and South Asia show the most widespread solid fuel use.6,20,21 Although the largest disease burden is reported in developing countries, solid fuels, primarily wood, are also used in developed countries. Overall, 28% of an urban cohort based in New Mexico in southwestern United States reported wood smoke exposure in a 2010 report.22

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Severity Besides being less prevalent, emphysema in subjects exposed to HAP tends to be less severe than that seen in subjects exposed to tobacco smoke. In one small study, the percent predicted diffusing capacity was significantly higher in wood smoke-associated COPD compared with tobacco smoke-associated COPD (58 vs. 35%).37 Furthermore, the radiological and macroscopic pathologic severity of emphysema in wood smoke-exposed subjects was less than that in cigarette smokers.34,35,37

Pathologic Data In a rat model, similar emphysematous changes were seen in the lungs of animals exposed to wood smoke as those exposed to tobacco smoke.38 In humans, a similar type of emphysema was seen in autopsies of women with COPD due to biomass smoke exposure and those with COPD due to tobacco smoking (mainly centrilobular emphysema), but more severe emphysema was reported in the tobacco smokers than biomass smoke-exposed women on macroscopic pathologic examination.35

1.2).40 Another study of women in rural Indian villages showed a linear increase in OR of chronic bronchitis with increase in biomass smoke exposure index.41

Effects of Host Characteristics on Solid Fuel Smoke-Associated COPD Sex Although studies from low-income countries suggest that women are at higher risk of COPD from solid fuel smoke exposure,49–51 this is likely reflective of the specific daily tasks of women in these countries that include long hours of indoor cooking compared with men, rather than a biologically based sex predilection to adverse outcomes. In a U.S.-based study, men were at a higher risk for wood smoke-related COPD than women.22

Ethnicity In New Mexico in the United States, Hispanic ethnicity may be protective against wood smoke-related COPD.22 Similarly, New Mexico Hispanics also show lower predilection to cigarette smoke-related COPD than non-Hispanic whites.52

Household Air Pollution and Chronic Bronchitis Symptoms of chronic bronchitis (chronic productive cough for 3 months in each of 2 successive years in a patient in whom other causes of chronic cough have been excluded39) seems to be the most common manifestation of HAP-associated respiratory condition.

Prevalence Several cross-sectional and case–control studies have shown a high prevalence of chronic bronchitis in populations exposed to biomass smoke.30,40–47 One study reported a prevalence as high as 72% in nonsmoking women with more than 10 years of exposure to biomass smoke in rural Pakistan.46 Another study among Turkish women exposed to biomass smoke showed a prevalence of chronic bronchitis of 58% without significant difference between smokers and nonsmokers.42

Strength of Association The risk of developing chronic bronchitis in populations exposed to biomass smoke is estimated to be approximately twofold higher than the risk in populations using clean fuel. In one meta-analysis, the random pooled effect size was 2.3.48 The effect size was slightly greater in wood burners compared with mixed biomass fuel burners (OR ¼ 2.6 vs. 2.5, respectively).48 The strength of the association, however, would be better understood with longitudinal studies, which are limited in this field.

Dose–Response Relationship Higher biomass smoke exposure index (calculated by houryears of exposure, as discussed above) is associated with higher OR for developing chronic bronchitis. For example, in a study of Mexican women, the OR for chronic bronchitis in women with > 200 hour-years exposure was 15 as compared with women with < 100 hours-years of exposure (OR of Seminars in Respiratory and Critical Care Medicine

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Tobacco Smoking Cigarette smoking potentiates the effect of solid fuel smoke exposure on COPD. This was demonstrated by multiple epidemiologic studies where a greater prevalence of respiratory symptoms and a more severe airway obstruction were seen in tobacco smokers who also were exposed to biomass smoke than either nonbiomass smoke-exposed smokers or nonsmokers exposed to biomass smoke.3,22,29,53 While most studies were done in developing countries, Sood et al, in a U.S.-based study, also demonstrated an additive interaction between wood smoke and cigarette smoke exposures on COPD.22

Computed Tomography Abnormalities Associated with Biomass Smoke Exposure Data on high-resolution computed tomography (CT) scan (HRCT) findings in biomass smoke-exposed subjects are limited. In a Turkish study of women without a COPD diagnosis, Kara et al compared HRCT scans of 32 biomass smokeexposed asymptomatic subjects, 30 exposed symptomatic subjects, and 30 unexposed asymptomatic subjects.54 The study showed that HRCT scans of exposed subjects had greater prevalence of ground glass opacities, fibrotic bands, mosaic pattern, and peribronchovascular thickening than unexposed subjects. Further, exposed symptomatic subjects had a greater prevalence of mosaic pattern than exposed asymptomatic subjects. This study establishes that CT changes develop early in exposed subjects, often before symptoms develop or a diagnosis of lung disease is established. In another descriptive study of 30 rural Turkish nonsmoking women with a clinical diagnosis of COPD secondary to biomass smoke exposure, multiple radiological abnormalities were described by Ozbay et al.55 These abnormalities

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Histopathological Changes in Biomass Smoke-Associated COPD Pathological changes that have been described in subjects with COPD due to biomass smoke exposure include emphysema (as noted above), inflammation and smooth muscle hyperplasia of the small airway wall, anthracosis, bronchiectasis, pulmonary thromboembolism/infarctions, and pulmonary artery structural changes.35,57 While tobacco smokerelated COPD has been associated with more severe emphysema and more pronounced goblet cell metaplasia, biomass smoke-related COPD was characterized with more fibrosis in the lung parenchyma and in the walls of the bronchi, bronchioles, and blood vessels, and greater anthracosis.35

Bronchial Hyperresponsiveness Studies evaluating presence of bronchial hyperreactivity and extent of bronchial hyperresponsiveness in COPD related to HAP are limited and the findings are contradictory. In one cross-sectional study in Colombia, bronchial hyperresponsiveness was greater in patients with wood smoke-related COPD than in patients with tobacco smoke-related COPD. In this study, bronchial hyperresponsiveness was determined by the concentration of inhaled methacholine required to cause a  20% decline in FEV1 (methacholine PC20 of 0.39 vs. 1.24 mg/mL respectively; a lower methacholine PC20 value suggests greater bronchial hyperresponsiveness).58 On the other hand, when prevalence of bronchial hyperreactivity defined by spirometric response to inhaled bronchodilator was studied, Moreira et al showed the opposite results; the group exposed to tobacco smoke had higher prevalence of positive bronchodilator response than the wood smoke-exposed group (25.4 vs. 5.9%, respectively).59 Due to a limited number of studies examining this outcome, no definitive conclusions in this regard can be made.

Lung Growth and Development

Fig. 4 FEV1 decline during follow-up in milliliters (A) and as percentage change from baseline (B). Vertical bar is the range of variation, whereas closed diamonds show the mean change. BD, bronchodilator. (Reprinted with permission from Ramirez-Venegas A, Sansores RH, Quintana-Carrillo RH, et al. FEV1 decline in patients with chronic obstructive pulmonary disease associated with biomass exposure. Am J Respir Crit Care Med 2014;190(9):996–1002).

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Early exposure to biomass smoke has been linked to poor growth and development of the lung. In a cross-sectional study in rural Nepal, young adults (16–25 years of age) with biomass exposure had lower FEV1, FVC, and higher prevalence of airflow obstruction25 than those not similarly exposed. Two cross-sectional studies of school children (age range 7– 13 years) showed lower lung function parameters in exposed children as compared with unexposed children.60,61 Furthermore, higher indoor air pollution scores from coal- and gasbased heating in the early postnatal period (first 6 months of life) had a strong negative association with lung function later in life at 9 years of age in a retrospective Polish study.62 These findings suggest that the detrimental effect of biomass smoke exposure on lung function may start in the postnatal period or perhaps even earlier, although longitudinal studies that can better assess this effect are limited. A low lung function value at an early age, even in the absence of overt obstruction, is a risk factor for developing COPD later in life.63 This may explain the occurrence of HAP-related COPD in younger adults, as compared with tobacco smoke-related COPD that primarily occurs at a relatively older age.21 Seminars in Respiratory and Critical Care Medicine

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included not only classical changes of COPD, such as increased lung volume or diffuse emphysema (76%), focal emphysema (73%), and bullae/blebs (15%), but also included changes of other obstructive lung diseases, such as bronchiectasis (40%) as well as changes of restrictive lung diseases, such as honeycombing (30%), ground glass opacities (40%), reticulonodular pattern, and/or thickening of interlobular septa (76%). Further, cardiovascular changes were also commonly noted such as increased cardiothoracic ratio (73%) and increased bronchovascular arborization (70%). This study emphasizes that mixed obstructive–restrictive changes are common on CT imaging in biomass smoke-associated COPD. On the other hand, Moreira et al in a case–control study of Brazilian nonsmokers compared wood smoke-exposed COPD rural subjects with unexposed healthy controls from urban areas, and demonstrated predominantly bronchial changes, particularly bronchial wall thickening (►Fig. 5).56 This finding is corroborated by two other studies that compared HRCT scan findings in biomass smoke-associated COPD versus tobacco smoke-associated COPD. Biomass smoke-associated COPD was found to be disproportionately bronchial and small airway predominant and less emphysema predominant. Thus, biomass-associated COPD subjects were more likely to demonstrate peribronchial thickening, bronchial dilation, and subsegmental atelectasis (features suggestive of bronchial involvement),37 as well as more air trapping (a feature suggestive of small airway disease)34 and lower CT emphysema score37 than tobacco smoke-associated COPD. While all CT imaging studies are limited by their small sample size, they suggest that biomass smoke exposure results in early pulmonary changes, mixed changes of both obstructive and restrictive pulmonary diseases, and the resulting COPD phenotype may show greater small and large airway changes and less emphysematous change than cigarette smoke-associated COPD.

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Rate of Decline in Lung Function

Hypoxia

The time-course of decline in FEV1 from baseline in subjects with COPD was recently studied in a longitudinal Mexican cohort followed over 15 years. The annual rate of FEV1 decline was lower in biomass smoke-exposed subjects compared with tobacco smoke-exposed subjects (23 vs. 42 mL, respectively) (►Fig. 4).64

In one small Mexican study (n ¼ 43), subjects with COPD secondary to biomass smoke exposure had significantly lower resting arterial oxygen saturation than subjects with COPD secondary to tobacco smoking (SaO2 of 82 vs. 87%, p ¼ 0.01). Both the groups showed similar exertional drops in their arterial oxygen saturation.34 On the other hand, a larger Turkish study found no differences between the two groups with respect to PaO2 or PaCO2 levels despite a higher FEV1 percent predicted in the biomass smoke-exposed group.67 While not conclusive, taken together the data from these two studies suggest a relatively greater level of oxygen desaturation for a given degree of spirometric impairment in subjects with COPD related to HAP. This finding cannot be explained away by the extent of emphysema. One potential explanation may be a greater prevalence of pulmonary hypertension in the biomass smoke-exposed group.

Quality of Life HAP is associated with several chronic respiratory symptoms that may interfere with the exposed individual’s quality of life, including cough, phlegm production, dyspnea, wheezing, and chest tightness.34,44,50,65,66 In one Mexican study using the St. George’s Respiratory Questionnaire (SGRQ), subjects with COPD secondary to biomass smoke exposure reported significantly more respiratory symptoms, more activity limitation and less control over their disease (despite less CTassessed emphysema) than tobacco smoke-related COPD subjects.34 These data suggest a disproportionately greater impact of biomass smoke exposure on quality of life than tobacco smoke exposure.

Pulmonary Hypertension Pulmonary hypertension, characterized by elevated mean pulmonary arterial pressures, is a common and well-

Fig. 5 Axial high-resolution computed tomography (HRCT) scans of the chest (lung window) at the level of the lower lung fields. (A) Bronchiectasis and bronchial wall thickening (thick arrow), parenchymal bands (thin arrow), and mosaic perfusion pattern (asterisks) are seen in a 66-year-old female patient. (B) Middle lobe atelectasis (thick arrow) and bronchial wall thickening (thin arrow) are seen in a 76-year-old female patient. (C) Parenchymal bands (thick arrow), moderate bronchial wall thickening (thin arrow), and mosaic perfusion pattern (asterisks) are seen in a 57-year-old female patient. (D) Centrilobular micronodules with tree-in-bud pattern are seen in an 81-year-old female patient. (Reprinted with permission from Moreira MA, Barbosa MA, Queiroz MC, et al. Pulmonary changes on HRCT scans in nonsmoking females with COPD due to wood smoke exposure. J Bras Pneumol 2013;39(2):155–163.)

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Mortality One study followed 520 COPD patients over 7 years in the city of Mexico to assess their mortality risk. Multivariable survival analysis showed that HAP-exposed COPD subjects experienced a similar mortality rate as tobacco smoke-exposed COPD subjects, after adjusting for severity of disease.68

Bronchial Anthracofibrosis Bronchial anthracofibrosis (BAF), an obstructive airway disease related to HAP, refers to the bronchoscopic finding of multiple dark anthracotic pigments of the large airways that is typically associated with bronchial narrowing or obliteration.69 This finding has been described in older adults, predominantly nonsmoking women from rural Southeast Asia69 and the Middle East70 who regularly cook using biomass fuel in poorly ventilated spaces. Clinically, HAP-induced BAF usually presents as obstructive airway disease,69,71 with chronic productive cough, hemoptysis, dyspnea, and chest pain representing the most commonly reported symptoms.69,71 The most common spirometric finding is an obstructive ventilatory defect (defined as FEV1/FVC < 0.7) reported in almost half of the cases.69,71 Normal spirometry and mixed obstructive–restrictive ventilatory defects have also been described.71 The disease has characteristic radiological findings including bronchial wall thickening, bronchial narrowing or atelectasis, peribronchial cuffing, and hilar lymphadenopathy.71,72 The diagnosis is confirmed by bronchoscopy, the principal finding being multiple pigmented anthracotic lesions and bronchial stenosis more commonly involving the bilateral upper and the right middle lobes.70,71 BAF was classically described to be a presentation of active or old tuberculosis.69,73 More recent evidence, however, suggests that heavy HAP exposure is the main risk factor for this disease.15,71 Other than tuberculosis, BAF has also been associated with COPD, pneumonia, and lung malignancy.71 Although BAF may be viewed as a variant of HAP-associated

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COPD, the distinct radiological and bronchoscopic features suggest that it might be a somewhat distinct pulmonary response to heavy HAP exposure.

Hut Lung Case series of “hut lung,” an interstitial lung disease characterized by carbon deposition, dust macules, and fibrosis, are reported primarily in women with chronic high-level exposure to HAP in developing countries.55,74–77 This disease has also been described from North Carolina, United States, where it was attributed to a malfunctioning indoor woodburning heater.78 The clinical manifestations of this disease is best described in a case series by Sandoval et al of 30 rural Mexican nonsmoking women with a mean exposure to biomass smoke of 400 hour-years.75 Pulmonary function tests usually showed obstructive or mixed obstructive–restrictive pattern (although other case series have also described normal lung function74 or a restrictive pattern77). Abnormal chest radiographs were found in 90% of the subjects—the most common finding was the presence of 2 to 3 mm wide reticulonodular opacities resembling those seen in pneumoconiosis. A large majority had evidence of cor pulmonale. Bronchoscopy revealed grossly visible anthracotic plaques, usually seen at the bifurcations of lobar bronchi. Histopathological examination of transbronchial biopsy specimens showed thickened basement membranes with diffuse deposition of fine anthracotic particles. Open lung biopsy specimens confirmed the presence of diffuse anthracosis and areas of interstitial fibrosis. Other case series have described the fibrosis as bronchiolocentric in distribution.77 Although the treatment of this disease is not known, improvement with systemic corticosteroids followed by inhaled corticosteroids has been reported.77

Mechanistic Bases for the Association between HAP and COPD Studies that evaluate possible mechanisms by which HAP leads to COPD are limited. Proposed mechanisms are however outlined below.

Increased Airway Inflammation, Fibrosis, and Remodeling Acute Exposure Exposure of mice to PM from cow dung and wood smoke elicits a dose-dependent neutrophilic inflammatory response in the airways in the first 24 hours of exposure. The increase in neutrophils in the bronchoalveolar lavage (BAL) of acutely exposed mice is greater with cow dung than wood smoke exposure. Additionally, proinflammatory mediators that increase in the BAL of exposed mice in the first 24 hours of the exposure include neutrophil chemokines (granulocyte-colony stimulating factor, keratinocyte chemoattractant, macrophage inflammatory protein [MIP-2], and MIP-1a), macrophage chemokines (MIP-1b, interferon-g–induced protein-10, monocyte chemotactic protein-1, and cytokines (interleukin [IL]-6, Seminars in Respiratory and Critical Care Medicine

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established complication of COPD. It has been suggested that subjects with biomass smoke-related COPD have a higher prevalence of pulmonary hypertension than smokers with tobacco smoke-related COPD.57,67 In one Turkish study employing echocardiographic systolic pulmonary artery pressure measurements, women with COPD due to biomass smoke exposure were compared with men with COPD due to tobacco smoking. This study concluded that the prevalence of pulmonary hypertension was substantially higher in the group with biomass smoke-related COPD than tobacco smoke-related COPD, particularly in the subgroup with moderate COPD (56.2 vs. 37.5%, p ¼ 0.03).67 It is plausible that due to the chronic bronchitis phenotype which is predominant in biomass smoke-related COPD, the latter has a greater prevalence of pulmonary hypertension than tobacco smoke-related COPD. It is also plausible that the diagnosis of COPD in biomass smoke-exposed subjects is delayed as compared with tobacco smokers, which in turn may lead to delayed treatment of hypoxia and consequently pulmonary hypertension.

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tumor necrosis factor-α, IL-12p70, and monokine-induced by gamma interferon16). Similar findings are seen in humans, where acute exposure to wood smoke in healthy subjects leads to increased neutrophilic influx in BAL79 and increased levels of the neutrophilic chemokine IL-8.80 In vitro, biomass smoke exposure causes similar effects on human lung fibroblasts as cigarette smoke exposure, including increase in fibronectin and perlecan deposition in the extracellular matrix.80 This observation indicates possible shared inflammatory pathways in response to HAP and cigarette smoke.

Subchronic Exposure In contrast to the acute neutrophilic response, the subchronic 8-week exposure results in significantly elevated airway eosinophils, macrophages, and lymphocytes in mice exposed to solid fuel smoke.16 The clinical significance of the subchronic airway eosinophilic response is uncertain among humans.

Chronic Exposure Chronic exposure to wood smoke in guinea pigs leads to marked upregulation and production of matrix metalloproteinases (MMP-9, MMP-12) and tissue inhibitors of MMPs in the airway epithelial cells.38,81 Those proteins are believed to play a role in the development of emphysema.82 Peribronchiolar fibrosis was also seen in the lungs of exposed rats to biomass and cigarette smoke, as evident by increased number of fibroblasts around the small airways accompanied by type I collagen deposition in the airway walls.38 These findings in rodents are similar to the limited studies done in humans that demonstrate increased expression of MMP-9 and MMP-12 in the sputum samples of exposed women exposed to open fire stoves.83 However, exposure of rats for 3 months to wood smoke concentrations that resemble those found in developing countries (10 mg/m3) did not change rodent pulmonary function.84,85 This may reflect the difficulty of translating the effects of a similar dose of inhaled pollutant exposure in rats to humans. For example, ozone exposure in rodents causes much less respiratory tract toxicity for a given dose than it does in primates.

Increased Systemic Inflammation COPD is associated with systemic inflammation and HAP may further augment this effect. Systemic inflammation, in turn, may accelerate airway inflammation as well as enhance extrapulmonary side effects. In one study, serum concentrations of MMPs as well as C-reactive protein (CRP) were higher in subjects with COPD due to biomass smoke than either COPD due to tobacco smoke or healthy subjects. Further higher serum MMPs and CRP were independently associated with low FEV1.86

Increased Oxidative Stress The capacity of solid fuel smoke particles to elicit oxidative stress was illustrated in one study by incubating solid fuel smoke particles with synthetic respiratory tract lining fluid. This resulted in loss of ascorbate and depletion of glutathione in the synthetic respiratory tract lining fluid, suggestive of the Seminars in Respiratory and Critical Care Medicine

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oxidative potential of solid fuel smoke.87 Other studies demonstrated upregulation of arginase activity in platelets and erythrocytes of subjects with COPD secondary to biomass smoke exposure, which is also linked to greater oxidative stress.88 Moreover, it is plausible that high levels of oxidative stress related to wood smoke exposure mediate apoptosis in human cells, as shown in one study using pulmonary artery endothelial cells.89 A recent study reported that wood smoke exposure enhances cigarette smoke-induced inflammation by suppressing the anti-inflammatory pathway that cigarette smoke activates through the aryl-hydrocarbon receptor pathway.90 This pathway involves a strong induction of aryl hydrocarbon receptor repressor by wood smoke.

Other Mechanisms Other mechanisms such as pulmonary surfactant deactivation, decreased bacterial clearance, impaired phagocytosis, and impaired mucociliary clearance have also been suggested.91–93 In one study, human monocyte-derived macrophages exposed in vitro to respirable-sized particles generated by combustion of wood demonstrated a dosedependent impairment of phagocytosis of pneumococci and mycobacteria.94

Effects of Interventions on Respiratory Outcomes The adverse respiratory effects of HAP could be simply avoided by using “clean” fuel (e.g., liquid propane gas or natural gas) or electricity rather than biomass fuel. This however may not be applicable or affordable in many lowincome population groups. Other interventions have been described in the literature, such as outdoor relocation of cooking using biomass fuel,95,96 adding a window to the kitchen97 and using improved cook stoves that are characterized by a better ventilation system such as a chimney, a higher efficiency in thermal conversion, a higher heat transfer ratio, and a more complete combustion.98–102 Another suggested method is partitioning of the kitchen from the living space.95 This may not reduce the exposure of the cook, but reduces exposure to other members of the household. Interventions that improve kitchen ventilation and use cleaner fuels improve household air quality, as confirmed via measurements of indoor air pollutants (e.g., SO2, CO, CO2, NO2, and PM10).98,100 In a randomized wood stove intervention trial in highland Guatemala, the intervention group received an improved stove with chimney, whereas the control group continued using open indoor fires (►Fig. 6). A 50% mean reduction in 48-hour average personal carbon monoxide exposure levels among children 0 to 18 months of age101 as well as a 39% reduction in pregnant women103 was associated with the improved stove intervention. Interventions also yield improvements in air quality in developed countries. In the United States (in a Rocky Mountain Valley community), the replacement of woodstoves with Environmental Protection Agency (EPA)-certified woodstoves led to over 70% reduction in the ambient levels of PM2.5.102

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Fig. 6 Traditional open fire used for cooking (panel A) and the locally developed and constructed chimney woodstove, the plancha (panel B) in Guatemala. The chimney woodstove has a thick metal heating surface for cooking tortillas and holes with removable concentric rings for pots, a firebrick combustion chamber with baffling, a concrete and brick body, tile surfaces around the cooking area, dirt and pumice stone insulation, a metal fuel door, and a metal chimney with damper. Infants and toddlers are highly exposed to combustion smoke as they are carried on their mother’s back while she cooks, a common cultural practice in Guatemala and other regions. (Reprinted with permission from Smith KR, McCracken JP, Weber MW, et al. Effect of reduction in household air pollution on childhood pneumonia in Guatemala (RESPIRE): a randomised controlled trial. Lancet 2011;378(9804):1717–1726.)

Limited data suggest an improvement in COPD-relevant outcomes following these interventions, including reducing COPD incidence, reducing the rate of decline in lung function, and improving health-related quality of life. It is further hoped that reducing exposure in children may favorably impact their long-term lung growth and development and cut down their risk for COPD in adulthood.

COPD Incidence A significant reduction in COPD incidence in middle-aged adults (42% risk reduction in men and 25% in women) was seen in a large retrospective cohort study between 1976 and 1992 in China after installing chimneys in previously unvented household coal stoves.99 In a prospective Chinese study, the use of either a clean fuel (i.e., biogas from a household digester) or improved ventilation (i.e., a chimney with an exhaust fan) was associated with lower incidence of COPD over a 9-year period. The OR for developing COPD when both biogas and improved ventilation were used for 5 to 9 years was 0.28 as compared with when neither was used over the study period.100

Effect on Lung Function Based on data showing that smoking cessation reduces the rate of decline in lung function among tobacco smokers, one would expect reductions in biomass smoke exposure to have a similar effect. A significantly slower decline in FEV1 was demonstrated in individuals from households that switched to biogas from biomass fuel or added kitchen ventilation to biomass stoves over the 9-year prospective Chinese study referred to above.100 The decline in FEV1 was reduced by 12 mL/y for a switch to biogas, 13 mL/y for adding kitchen

ventilation and 16 mL/y for both interventions, compared with a lack of either intervention. Additionally, an exposure– response relationship was found; the longer the duration of biogas and ventilation, use the slower the decline in FEV1.100 Two longitudinal studies of lung function decline in the context of randomized controlled trials also found a protective effect of chimney stoves on decline in lung function. Although a study in Mexico did not find a difference in FEV1 decline over a 12-month period between chimney stove intervention and control groups with an intention-to-treat (ITT) analysis, there was a significant difference between those who reported actually using the chimney stove compared with those who did not (31 vs. 62 mL).104 In the randomized controlled trial of a chimney stove in Guatemala described above, while there was again no effect of the stove on FEV1 decline in an ITT analysis, an exposure–response analysis using exhaled breath carbon monoxide (EBCO) as the exposure metric did show an effect of exposure, 35 mL for a 100% increase in EBCO, again supporting the benefit of reduced exposure. Respiratory symptoms were also associated with EBCO.105 A weakness of both the Mexican and Guatemalan studies is a short follow-up period (12 and 18 months, respectively) which limits the interpretation of the apparent effect of reduction of exposure on lung function decline. Another limitation of these two studies is that although the chimney stove interventions did reduce exposure to some extent, levels of HAP were still relatively high by air quality standards of developed countries.

Health-Related Quality of Life In a small interventional study in rural Bolivia, the simple intervention of installing chimneys in 20 households led to a Seminars in Respiratory and Critical Care Medicine

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significant improvement in health-related quality of life of exposed women, demonstrated by a significant reduction in SGRQ score after the intervention (lower scores correlate with better quality of life). In this study, the greatest improvement was noted with respect to the SGRQ activity subscale. Although the total SGRQ symptoms score did not significantly improve, the attacks of wheezing and the severity and duration of these attacks were significantly lower after the intervention.98

there is currently insufficient data to be sure of this hopedfor effect. More data are needed from longitudinal intervention studies that measure both exposure to biomass emissions and postbronchodilator lung function repeatedly over a sufficiently long time interval, that is, at least several years. It is also important to increase awareness of the respiratory effects of HAP among physicians and patients and to promote preventive initiatives through education, applied research, and policy changes.

Effects on Lung Growth and Development Although studies demonstrate improved respiratory outcomes in children after implementing wood stove interventions such as reduction in incidence of severe pneumonia101 and reported wheezing,106 the effect of the interventions on lung growth and development in children and young adults is not known.

1 World Health Organization (WHO). Media Center. Fact sheet no:

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Conclusions HAP secondary to indoor combustion of solid fuel may be the biggest risk factor for COPD globally.19 About 3 billion people, half the worldwide population, are exposed to HAP compared with 1 billion people who smoke tobacco.19 Exposure to HAP is associated with the chronic bronchitis and emphysema phenotypes of COPD as well as with a distinct form of obstructive airway disease called BAF. COPD from HAP differs from COPD from tobacco smoke with respect to its disproportionately greater bronchial involvement, lesser emphysematous change, greater impact on quality of life, and possibly greater oxygen desaturation and pulmonary hypertensive changes. The current knowledge of this topic has a few critical gaps including inadequate quantification of exposure resulting in misclassification bias, limited number of longitudinal and interventional studies, small sample sizes in most studies, lack of adjustment for important covariates such as poverty, limited understanding of the mechanistic bases for the association, inadequate study of the role of genetics and epigenetics, and likely underestimation of the disease burden in developed countries. Perhaps the most critical gap in knowledge that needs to be addressed involves the nature of the exposure–response relationship. A better understanding of this relationship would inform efforts to reduce the burden of COPD due to HAP. Some would argue that only truly clean energy solutions to cooking and heating, such as electricity or natural gas (►Fig. 2), will have a substantial impact on the burden of COPD. Certainly, from a public health perspective, the cleanest possible energy sources should be scaled up wherever possible. At the same time, it is likely that penetration of such energy technologies to the rural areas of relatively poor countries in sub-Saharan Africa will take decades. In this context, until clean energy is universally available, it is hoped that even modest interventions, such as advanced, extremely low emission biomass stoves, may decrease exposure to biomass smoke sufficiently to reduce the risk for incident COPD and attenuate longitudinal decline in lung function. However, at present Seminars in Respiratory and Critical Care Medicine

References

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8

9 10

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292: Available at: http://www.who.int/mediacentre/factsheets/ fs292/en/. Accessed January 1, 2015 Pandey MR. Domestic smoke pollution and chronic bronchitis in a rural community of the Hill Region of Nepal. Thorax 1984;39(5): 337–339 Anderson HR. Chronic lung disease in the Papua New Guinea Highlands. Thorax 1979;34(5):647–653 Rai UC, Srinivasan V, Veliath S, Krishnan B, Rao AS. Cow dung smoke—A causative factor for chronic bronchitis & emphysema. Indian J Exp Biol 1982;20(9):696–700 Gordon SB, Bruce NG, Grigg J, et al. Respiratory risks from household air pollution in low and middle income countries. Lancet Respir Med 2014;2(10):823–860 Smith KR, Bruce N, Balakrishnan K, et al; HAP CRA Risk Expert Group. Millions dead: how do we know and what does it mean? Methods used in the comparative risk assessment of household air pollution. Annu Rev Public Health 2014;35:185–206 World Health Organization. Indoor air quality guidelines: household fuel combustion. Available at: http://www.who.int/indoorair/ guidelines/hhfc/en/. Accessed January 1, 2015 Sood A. Indoor fuel exposure and the lung in both developing and developed countries: an update. Clin Chest Med 2012;33(4): 649–665 Zhang J, Smith KR. Indoor air pollution: a global health concern. Br Med Bull 2003;68:209–225 Sällsten G, Gustafson P, Johansson L, et al. Experimental wood smoke exposure in humans. Inhal Toxicol 2006;18(11): 855–864 Kurmi OP, Lam KB, Ayres JG. Indoor air pollution and the lung in low- and medium-income countries. Eur Respir J 2012;40(1): 239–254 Environmental Protection Agency. National ambient air quality standards for particulate matter. Fed Register 2013;78(10): 3086–3089 Ezzati M, Kammen DM. The health impacts of exposure to indoor air pollution from solid fuels in developing countries: knowledge, gaps, and data needs. Environ Health Perspect 2002;110(11): 1057–1068 Ellegård A. Cooking fuel smoke and respiratory symptoms among women in low-income areas in Maputo. Environ Health Perspect 1996;104(9):980–985 Kim KH, Jahan SA, Kabir E. A review of diseases associated with household air pollution due to the use of biomass fuels. J Hazard Mater 2011;192(2):425–431 Sussan TE, Ingole V, Kim JH, et al. Source of biomass cooking fuel determines pulmonary response to household air pollution. Am J Respir Cell Mol Biol 2014;50(3):538–548 Lim SS, Vos T, Flaxman AD, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012;380(9859):2224–2260

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

418

Assad et al.

18 World Health Organization. Media Center. Fact sheet no: 315.

39 Celli BR, MacNee W; ATS/ERS Task Force. Standards for the

Available at: http://www.who.int/mediacentre/factsheets/fs315/ en/. Accessed January 1, 2015 Salvi S, Barnes PJ. Is exposure to biomass smoke the biggest risk factor for COPD globally? Chest 2010;138(1):3–6 Salvi S. The silent epidemic of COPD in Africa. Lancet Glob Health 2015;3(1):e6–e7 van Gemert F, Kirenga B, Chavannes N, et al. Prevalence of chronic obstructive pulmonary disease and associated risk factors in Uganda (FRESH AIR Uganda): a prospective cross-sectional observational study. Lancet Glob Health 2015;3(1):e44–e51 Sood A, Petersen H, Blanchette CM, et al. Wood smoke exposure and gene promoter methylation are associated with increased risk for COPD in smokers. Am J Respir Crit Care Med 2010;182(9): 1098–1104 Vestbo J, Hurd SS, Agustí AG, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 2013;187(4):347–365 Caballero A, Torres-Duque CA, Jaramillo C, et al. Prevalence of COPD in five Colombian cities situated at low, medium, and high altitude (PREPOCOL study). Chest 2008;133(2):343–349 Kurmi OP, Devereux GS, Smith WC, et al. Reduced lung function due to biomass smoke exposure in young adults in rural Nepal. Eur Respir J 2013;41(1):25–30 Johnson P, Balakrishnan K, Ramaswamy P, et al. Prevalence of chronic obstructive pulmonary disease in rural women of Tamilnadu: implications for refining disease burden assessments attributable to household biomass combustion. Glob Health Action 2011;4:7226 Liu S, Zhou Y, Wang X, et al. Biomass fuels are the probable risk factor for chronic obstructive pulmonary disease in rural South China. Thorax 2007;62(10):889–897 da Silva LF, Saldiva SR, Saldiva PH, Dolhnikoff M; Bandeira Científica Project. Impaired lung function in individuals chronically exposed to biomass combustion. Environ Res 2012; 112:111–117 Hu G, Zhou Y, Tian J, et al. Risk of COPD from exposure to biomass smoke: a metaanalysis. Chest 2010;138(1):20–31 Ekici A, Ekici M, Kurtipek E, et al. Obstructive airway diseases in women exposed to biomass smoke. Environ Res 2005;99(1): 93–98 Orozco-Levi M, Garcia-Aymerich J, Villar J, Ramírez-Sarmiento A, Antó JM, Gea J. Wood smoke exposure and risk of chronic obstructive pulmonary disease. Eur Respir J 2006;27(3):542–546 Sezer H, Akkurt I, Guler N, Marakoğlu K, Berk S. A case-control study on the effect of exposure to different substances on the development of COPD. Ann Epidemiol 2006;16(1):59–62 Köksal H, Saygı A, Sarıman N, et al. Evaluation of clinical and functional parameters in female subjects with biomass smoke exposure. Respir Care 2013;58(3):424–430 Camp PG, Ramirez-Venegas A, Sansores RH, et al. COPD phenotypes in biomass smoke- versus tobacco smoke-exposed Mexican women. Eur Respir J 2014;43(3):725–734 Rivera RM, Cosio MG, Ghezzo H, Salazar M, Pérez-Padilla R. Comparison of lung morphology in COPD secondary to cigarette and biomass smoke. Int J Tuberc Lung Dis 2008;12(8):972–977 Golpe R, Sanjuán López P, Cano Jiménez E, Castro Añón O, Pérez de Llano LA. Distribution of clinical phenotypes in patients with chronic obstructive pulmonary disease caused by biomass and tobacco smoke. Arch Bronconeumol 2014;50(8):318–324 González-García M, Maldonado Gomez D, Torres-Duque CA, et al. Tomographic and functional findings in severe COPD: comparison between the wood smoke-related and smoking-related disease. J Bras Pneumol 2013;39(2):147–154 Zou Y, Li S, Zou W, et al. Upregulation of gelatinases and epithelialmesenchymal transition in small airway remodeling associated with chronic exposure to wood smoke. PLoS ONE 2014;9(5):e96708

diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J 2004;23(6):932–946 Pérez-Padilla R, Regalado J, Vedal S, et al. Exposure to biomass smoke and chronic airway disease in Mexican women. A casecontrol study. Am J Respir Crit Care Med 1996;154(3 Pt 1): 701–706 Mahesh PA, Jayaraj BS, Prabhakar AK, Chaya SK, Vijaysimha R. Identification of a threshold for biomass exposure index for chronic bronchitis in rural women of Mysore district, Karnataka, India. Indian J Med Res 2013;137(1):87–94 Uzun K, Ozbay B, Ceylan E, Gencer M, Zehir I. Prevalence of chronic bronchitis-asthma symptoms in biomass fuel exposed females. Environ Health Prev Med 2003;8(1):13–17 Malik SK. Exposure to domestic cooking fuels and chronic bronchitis. Indian J Chest Dis Allied Sci 1985;27(3):171–174 Desalu OO, Adekoya AO, Ampitan BA. Increased risk of respiratory symptoms and chronic bronchitis in women using biomass fuels in Nigeria. J Bras Pneumol 2010;36(4):441–446 Kiraz K, Kart L, Demir R, et al. Chronic pulmonary disease in rural women exposed to biomass fumes. Clin Invest Med 2003;26(5): 243–248 Akhtar T, Ullah Z, Khan MH, Nazli R. Chronic bronchitis in women using solid biomass fuel in rural Peshawar, Pakistan. Chest 2007; 132(5):1472–1475 Golshan M, Faghihi M, Marandi MM. Indoor women jobs and pulmonary risks in rural areas of Isfahan, Iran, 2000. Respir Med 2002;96(6):382–388 Kurmi OP, Semple S, Simkhada P, Smith WC, Ayres JG. COPD and chronic bronchitis risk of indoor air pollution from solid fuel: a systematic review and meta-analysis. Thorax 2010;65(3): 221–228 Po JY, FitzGerald JM, Carlsten C. Respiratory disease associated with solid biomass fuel exposure in rural women and children: systematic review and meta-analysis. Thorax 2011;66(3): 232–239 Moreira MA, Barbosa MA, Jardim JR, Queiroz MC, Inácio LU. Chronic obstructive pulmonary disease in women exposed to wood stove smoke. Rev Assoc Med Bras 2013;59(6):607–613 Xu F, Yin X, Shen H, Xu Y, Ware RS, Owen N. Better understanding the influence of cigarette smoking and indoor air pollution on chronic obstructive pulmonary disease: a case-control study in Mainland China. Respirology 2007;12(6):891–897 Bruse S, Sood A, Petersen H, et al. New Mexican Hispanic smokers have lower odds of chronic obstructive pulmonary disease and less decline in lung function than non-Hispanic whites. Am J Respir Crit Care Med 2011;184(11):1254–1260 Behera D, Jindal SK. Respiratory symptoms in Indian women using domestic cooking fuels. Chest 1991;100(2):385–388 Kara M, Bulut S, Tas F, Akkurt I, Seyfikli Z. Evaluation of pulmonary changes due to biomass fuels using high-resolution computed tomography. Eur Radiol 2003;13(10):2372–2377 Ozbay B, Uzun K, Arslan H, Zehir I. Functional and radiological impairment in women highly exposed to indoor biomass fuels. Respirology 2001;6(3):255–258 Moreira MA, Barbosa MA, Queiroz MC, et al. Pulmonary changes on HRCT scans in nonsmoking females with COPD due to wood smoke exposure. J Bras Pneumol 2013;39(2):155–163 Moran-Mendoza O, Pérez-Padilla JR, Salazar-Flores M, VazquezAlfaro F. Wood smoke-associated lung disease: a clinical, functional, radiological and pathological description. Int J Tuberc Lung Dis 2008;12(9):1092–1098 González-García M, Torres-Duque CA, Bustos A, Jaramillo C, Maldonado D. Bronchial hyperresponsiveness in women with chronic obstructive pulmonary disease related to wood smoke. Int J Chron Obstruct Pulmon Dis 2012;7:367–373 Moreira MA, Moraes MR, Silva DG, et al. Comparative study of respiratory symptoms and lung function alterations in patients

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72

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Assad et al.

with chronic obstructive pulmonary disease related to the exposure to wood and tobacco smoke. J Bras Pneumol 2008;34(9): 667–674 Shen S, Qin Y, Cao Z, et al. Indoor air pollution and pulmonary function in children. Biomed Environ Sci 1992;5(2):136–141 Azizi BH, Henry RL. Effects of indoor air pollution on lung function of primary school children in Kuala Lumpur. Pediatr Pulmonol 1990;9(1):24–29 Jedrychowski W, Maugeri U, Jedrychowska-Bianchi I, Flak E. Effect of indoor air quality in the postnatal period on lung function in pre-adolescent children: a retrospective cohort study in Poland. Public Health 2005;119(6):535–541 Kalhan R, Arynchyn A, Colangelo LA, Dransfield MT, Gerald LB, Smith LJ. Lung function in young adults predicts airflow obstruction 20 years later. Am J Med 2010;123(5):468.e1–468.e7 Ramirez-Venegas A, Sansores RH, Quintana-Carrillo RH, et al. FEV1 decline in patients with chronic obstructive pulmonary disease associated with biomass exposure. Am J Respir Crit Care Med 2014;190(9):996–1002 Díaz E, Bruce N, Pope D, et al. Lung function and symptoms among indigenous Mayan women exposed to high levels of indoor air pollution. Int J Tuberc Lung Dis 2007;11(12):1372–1379 Alim MA, Sarker MA, Selim S, Karim MR, Yoshida Y, Hamajima N. Respiratory involvements among women exposed to the smoke of traditional biomass fuel and gas fuel in a district of Bangladesh. Environ Health Prev Med 2014;19(2):126–134 Sertogullarindan B, Gumrukcuoglu HA, Sezgi C, Akil MA. Frequency of pulmonary hypertension in patients with COPD due to biomass smoke and tobacco smoke. Int J Med Sci 2012;9(6): 406–412 Ramírez-Venegas A, Sansores RH, Pérez-Padilla R, et al. Survival of patients with chronic obstructive pulmonary disease due to biomass smoke and tobacco. Am J Respir Crit Care Med 2006; 173(4):393–397 Kim YJ, Jung CY, Shin HW, Lee BK. Biomass smoke induced bronchial anthracofibrosis: presenting features and clinical course. Respir Med 2009;103(5):757–765 Sigari N, Mohammadi S. Anthracosis and anthracofibrosis. Saudi Med J 2009;30(8):1063–1066 Gupta A, Shah A. Bronchial anthracofibrosis: an emerging pulmonary disease due to biomass fuel exposure. Int J Tuberc Lung Dis 2011;15(5):602–612 Kim HY, Im JG, Goo JM, et al. Bronchial anthracofibrosis (inflammatory bronchial stenosis with anthracotic pigmentation): CT findings. AJR Am J Roentgenol 2000;174(2):523–527 Chung MP, Lee KS, Han J, et al. Bronchial stenosis due to anthracofibrosis. Chest 1998;113(2):344–350 Gold JA, Jagirdar J, Hay JG, Addrizzo-Harris DJ, Naidich DP, Rom WN. Hut lung. A domestically acquired particulate lung disease. Medicine (Baltimore) 2000;79(5):310–317 Sandoval J, Salas J, Martinez-Guerra ML, et al. Pulmonary arterial hypertension and cor pulmonale associated with chronic domestic woodsmoke inhalation. Chest 1993;103(1):12–20 Grobbelaar JP, Bateman ED. Hut lung: a domestically acquired pneumoconiosis of mixed aetiology in rural women. Thorax 1991;46(5):334–340 Churg A, Myers J, Suarez T, et al. Airway-centered interstitial fibrosis: a distinct form of aggressive diffuse lung disease. Am J Surg Pathol 2004;28(1):62–68 Ramage JE Jr, Roggli VL, Bell DY, Piantadosi CA. Interstitial lung disease and domestic wood burning. Am Rev Respir Dis 1988; 137(5):1229–1232 Ghio AJ, Soukup JM, Case M, et al. Exposure to wood smoke particles produces inflammation in healthy volunteers. Occup Environ Med 2012;69(3):170–175 Krimmer D, Ichimaru Y, Burgess J, Black J, Oliver B. Exposure to biomass smoke extract enhances fibronectin release from fibroblasts. PLoS ONE 2013;8(12):e83938

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M. Increase of matrix metalloproteinases in woodsmoke-induced lung emphysema in guinea pigs. Inhal Toxicol 2009;21(2): 119–132 Mehra D, Geraghty PM, Hardigan AA, Foronjy R. A comparison of the inflammatory and proteolytic effects of dung biomass and cigarette smoke exposure in the lung. PLoS ONE 2012;7(12): e52889 Guarnieri MJ, Diaz JV, Basu C, et al. Effects of woodsmoke exposure on airway inflammation in rural Guatemalan women. PLoS ONE 2014;9(3):e88455 Tesfaigzi Y, McDonald JD, Reed MD, et al. Low-level subchronic exposure to wood smoke exacerbates inflammatory responses in allergic rats. Toxicol Sci 2005;88(2):505–513 Tesfaigzi Y, Singh SP, Foster JE, et al. Health effects of subchronic exposure to low levels of wood smoke in rats. Toxicol Sci 2002; 65(1):115–125 Montaño M, Sansores RH, Becerril C, et al. FEV1 inversely correlates with metalloproteinases 1, 7, 9 and CRP in COPD by biomass smoke exposure. Respir Res 2014;15:74 Kurmi OP, Dunster C, Ayres JG, Kelly FJ. Oxidative potential of smoke from burning wood and mixed biomass fuels. Free Radic Res 2013;47(10):829–835 Guzmán-Grenfell A, Nieto-Velázquez N, Torres-Ramos Y, et al. Increased platelet and erythrocyte arginase activity in chronic obstructive pulmonary disease associated with tobacco or wood smoke exposure. J Investig Med 2011;59(3):587–592 Liu PL, Chen YL, Chen YH, Lin SJ, Kou YR. Wood smoke extract induces oxidative stress-mediated caspase-independent apoptosis in human lung endothelial cells: role of AIF and EndoG. Am J Physiol Lung Cell Mol Physiol 2005;289(5):L739–L749 Awji EG, Chand H, Bruse S, et al. Wood Smoke Enhances Cigarette Smoke-Induced Inflammation by Inducing the Aryl Hydrocarbon Receptor Repressor in Airway Epithelial Cells. Am J Respir Cell Mol Biol 2014 (e-pub ahead of print). doi: 10.1165/rcmb.20140142OC Loke J, Paul E, Virgulto JA, Smith GJ. Rabbit lung after acute smoke inhalation. Cellular responses and scanning electron microscopy. Arch Surg 1984;119(8):956–959 Fick RB Jr, Paul ES, Merrill WW, Reynolds HY, Loke JS. Alterations in the antibacterial properties of rabbit pulmonary macrophages exposed to wood smoke. Am Rev Respir Dis 1984;129(1):76–81 Zelikoff JT, Chen LC, Cohen MD, Schlesinger RB. The toxicology of inhaled woodsmoke. J Toxicol Environ Health B Crit Rev 2002; 5(3):269–282 Rylance J, Fullerton DG, Scriven J, et al. Household Air Pollution Causes Dose-dependent Inflammation and Altered Phagocytosis in Human Macrophages. Am J Respir Cell Mol Biol 2014 (e-pub ahead of print). doi: 10.1165/rcmb.2014-0188OC Balakrishnan K, Sankar S, Parikh J, et al. Daily average exposures to respirable particulate matter from combustion of biomass fuels in rural households of southern India. Environ Health Perspect 2002;110(11):1069–1075 Albalak R, Frisancho AR, Keeler GJ. Domestic biomass fuel combustion and chronic bronchitis in two rural Bolivian villages. Thorax 1999;54(11):1004–1008 Kodgule R, Salvi S. Exposure to biomass smoke as a cause for airway disease in women and children. Curr Opin Allergy Clin Immunol 2012;12(1):82–90 Alexander D, Linnes JC, Bolton S, Larson T. Ventilated cookstoves associated with improvements in respiratory health-related quality of life in rural Bolivia. J Public Health (Oxf) 2014;36(3): 460–466 Chapman RS, He X, Blair AE, Lan Q. Improvement in household stoves and risk of chronic obstructive pulmonary disease in Xuanwei, China: retrospective cohort study. BMJ 2005; 331(7524):1050

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Assad et al.

104 Romieu I, Riojas-Rodríguez H, Marrón-Mares AT, Schilmann A,

obstructive pulmonary disease after improved cooking fuels and kitchen ventilation: a 9-year prospective cohort study. PLoS Med 2014;11(3):e1001621 101 Smith KR, McCracken JP, Weber MW, et al. Effect of reduction in household air pollution on childhood pneumonia in Guatemala (RESPIRE): a randomised controlled trial. Lancet 2011; 378(9804):1717–1726 102 Ward T, Palmer C, Bergauff M, Hooper K, Noonan C. Results of a residential indoor PM2.5 sampling program before and after a woodstove changeout. Indoor Air 2008;18(5):408–415 103 Thompson LM, Bruce N, Eskenazi B, Diaz A, Pope D, Smith KR. Impact of reduced maternal exposures to wood smoke from an introduced chimney stove on newborn birth weight in rural Guatemala. Environ Health Perspect 2011;119(10):1489–1494

Perez-Padilla R, Masera O. Improved biomass stove intervention in rural Mexico: impact on the respiratory health of women. Am J Respir Crit Care Med 2009;180(7): 649–656 105 Pope D, Diaz E, Smith-Sivertsen T, et al. Associations of Respiratory Symptoms and Lung Function with Measured Carbon Monoxide Concentrations among Nonsmoking Women Exposed to Household Air Pollution: The RESPIRE Trial, Guatemala. Environ Health Perspect 2014 (e-pub ahead of print). doi: 10.1289/ ehp.1408200 106 Noonan CW, Ward TJ, Navidi W, Sheppard L. A rural community intervention targeting biomass combustion sources: effects on air quality and reporting of children’s respiratory outcomes. Occup Environ Med 2012;69(5):354–360

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100 Zhou Y, Zou Y, Li X, et al. Lung function and incidence of chronic

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