Forum of International Respiratory Societies Report

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1 Forum of International Respiratory Societies Report Biomass Fuels and Respiratory Diseases A Review of the Evidence Carlos Torres-Duque, Darío Maldonado, Rogelio Pérez-Padilla, Majid Ezzati, and Giovanni Viegi, on behalf of the Forum of International Respiratory Societies (FIRS) Task Force on Health Effects of Biomass Exposure CONTENTS Foreword Introduction Background The Use of Biomass Fuels in the World Biomass Smoke Emissions and Chemical Composition Contribution of the Use of Biomass Fuels to Air Pollution Toxic Effects of Wood Smoke Exposure Assessment of Biomass Smoke Exposure and Risks Burden of Disease from Indoor Air Pollution Respiratory Effects of Biomass Fuel Combustion: Evidence and Burden Health Outcomes and Evidence ALRIs in Children COPD, Chronic Bronchitis, Respiratory Symptoms, and Lung Function Lung Cancer in Women Exposed to Coal and Biomass Smoke Tuberculosis Asthma Attacks Interstitial Lung Disease, Pneumoconiosis, and Other Respiratory Effects Suggestions for Prevention of Diseases Related to Solid Fuel Smoke Exposure Interventions and Education Research Globally, about 50% of all households and 90% of rural households use solid fuels (coal and biomass) as the main domestic source of energy, thus exposing approximately 50% of the world population close to 3 billion people to the harmful effects of these combustion products. There is strong evidence that acute respiratory infections in children and chronic obstructive pulmonary disease in women are associated with indoor biomass smoke. Lung cancer in women has been clearly associated with household coal use. Other conditions such as chronic obstructive pulmonary disease in men and tuberculosis could be also associated but evidence is scarce. According to estimates of the World Health Organization, more than 1.6 million deaths and over 38.5 million disability-adjusted life-years can be (Received in original form July 17, 2007; accepted in final form April 3, 2008) This is a report by a task force of the Forum of International Respiratory Societies (FIRS), currently formed by the American College of Chest Physicians (ACCP), the American Thoracic Society (ATS), the Asian Pacific Society of Respirology (APSR), Asociación Latinoamericana del Tórax (ALAT)*, the European Respiratory Society (ERS), and the International Union Against Tuberculosis and Respiratory Diseases (IUATLD). See the list of FIRS Working Group participants at the end of the article. *ULASTER (Unión Latinoamericana de Sociedades de Tisología y Enfermedades Respiratorias) is now merged into ALAT. Supported by the Forum of International Respiratory Societies and by the American Thoracic Society. Proc Am Thorac Soc Vol 5. pp , 2008 DOI: /pats RP Internet address: attributable to indoor smoke from solid fuels affecting mainly children and women. Interventions to suppress or reduce indoor exposure include behavior changes, improvements of household ventilation, improvements of stoves, and, outstandingly, transitions to better and cleaner fuels. These changes face personal and local beliefs and economic and sociocultural conditions. In addition, selection of fuels should consider cost, sustainability, and protection of the environment. Consequently, complex solutions need to be locally adapted, and involve the commitment and active participation of governments, scientific societies, nongovernmental organizations, and the general community. Keywords: solid fuels; indoor pollution; biomass; chronic obstructive pulmonary disease FOREWORD Presentation of FIRS and the Task Force The Forum of International Respiratory Societies (FIRS) was established on January 22, 2002, in Geneva with the aim of creating a structure for continuous cooperation among international scientific societies, active in the field of respiratory medicine. The founding societies were the Asociación Latinoamericana del Tórax (ALAT), the American Thoracic Society (ATS), the American College of Chest Physicians (ACCP), the Asian Pacific Society of Respirology (APSR), the European Respiratory Society (ERS), the International Union Against Tuberculosis and Lung Disease (IUATLD), and the Union Latinoamericana de Sociedades de Tisiología y Enfermedades Respiratorías (ULASTER) (now merged with ALAT). These societies felt the need to collaborate in the fight against the epidemics of respiratory diseases with a global approach. Indeed, the FIRS constitution states the following: 1. The objectives of the Forum of International Respiratory Societies are united advocacy in matters of global respiratory health and the identification of new areas for global initiatives. 2. These objectives will be attained by the consideration of needs and the proposal of projects to meet these needs, which would be implemented jointly or individually by the member organizations. Several task forces have been established that have enabled FIRS to collaborate with the World Health Organization (WHO) in the process of the Framework Convention on Tobacco Control ( in the development of International Standards for Tuberculosis Care ( and in the creation of the Global Alliance against Chronic Respiratory Diseases (GARD) ( as well as to prepare a document to help spread the use of simple spirometry worldwide.

2 578 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL It was an idea of ALAT (C. Torres-Duque and D. Maldonado; at that time, President and International Relationships Chair, respectively) to launch in 2004 an initiative on biomass exposure, one of the most important indoor air pollutants and risk factor for respiratory disease for a large part of the world s inhabitants. In this context, FIRS is convinced that this document will be extremely useful for doctors, patients, and governmental authorities. It is important to emphasize that cost-affordable interventions have proven to be effective in abating or reducing biomass exposure and the consequent adverse health effects. The newly formed GARD, a partnership of WHO and more than 50 respiratory, allergologic, general medical, and patients organizations, may be an important instrument to disseminate the recommendations in this FIRS document beyond the readers of respiratory journals and to strongly promote the implementation of preventative measures. 1. INTRODUCTION Biomass fuels are extensively used for cooking and home heating in developing countries and have health adverse effects (1). Recent estimates (2, 3) attribute 1.5 to 2 million deaths per year worldwide to indoor air pollution, most of them (1 million) occurring in children younger than 5 years due to acute respiratory infections (ARI), but also in women due to chronic obstructive pulmonary disease (COPD) and lung cancer (4). Today, indoor air pollution ranks 10th among preventable risk factors contributing to the global burden of disease (5), and although predominant in underprivileged countries, where it ranks fourth, indoor air pollution is also present in the Western world (6). Half of the world s population uses solid fuels (coal and biomass) (7, 8). In developed countries, particularly Canada and Australia, and in some western states of the United States (9), the persistent rise of the costs of energy has prompted an increasing number of households to use wood or any other biomass product for heating. In addition, there are worldwide transient exposures to the products of biomass combustion during forest fires. On a global scale, the household use of solid fuels is the most important source of indoor air pollution (10), and the exposure to the by-products of the combustion of biomass fuels, particularly wood smoke, has been related to numerous respiratory problems (7, 10), and increased mortality and burden of disease (5). This article presents information about the evidence linking the exposure to solid biomass fuels, especially wood smoke, to respiratory diseases and the burden of disease attributable to that exposure, but it is not purported to be an original systematic review nor a meta-analysis. Recent World Health Organization (WHO) publications (7, 10) have been largely used. The article also presents a section of suggestions for prevention. The gap between the global relevance of the health impact from biomass fuels use and the research activity has been recently highlighted (11). Physicians and governments should be acquainted with this knowledge to intervene properly, and reduce the exposure and the connected risks. 2. BACKGROUND 2.1. The Use of Biomass Fuels in the World Biomass is defined as the group of biologic materials (living organisms, both animal and vegetable, and their derivates) present in a specific area, collectively considered. Some of this material is used as fuel for cooking or home heating (12). Close to 50% of the world population, around 3 billion people, use biomass fuels as their primary source of domestic energy for cooking, home heating, and light, ranging from near 0% in developed countries to more than 80% in China, India, and sub-saharan Africa (7, 10, 12, 13). In the rural areas of Latin America, approximately 30 to 75% of households use biomass fuels for cooking (2, 5). An estimation of the household use of solid fuels (in countries grouped as shown in Figure 1) based on the scarce available data and some demographic and development indicators obtained from the World Bank and United Nations data is presented in Table 1 and Figure 2 (10). Wood is the biomass fuel most frequently used both as unprocessed wood and as charcoal, the latter having far lower impact in indoor air pollution. In some regions, especially in sub-saharan Africa, roughly 20% of the wood energy harvest is processed into charcoal and could reach 50% in some countries (14). Use of animal dung, crop residues, corncobs, and grass increases when wood is scarce or the forests are situated far away from the community. The use of solid fuels is linked to the gross national product per capita (10), and in general, in the same geographic zone, the use of solid fuels is higher in households with lower income. The global energy derived from biomass fuels has fallen from 50% in 1900 to nearly 13% in 2000, but recently it seems to be increasing, especially among the poor. The current socioeconomic situation in many developing countries suggests that the use of biomass fuels will continue in the coming decades (2). In these countries, nearly 2 billion kilograms of biomass are burned every day (15). In rural India, nearly 90% of the primary energy is derived from biomass (wood, 56%; crop residues, 16%; dung, 21%) (16). The total annual average of wood production used for fuel in developing countries increased approximately 16.5% over the past decade to about 1.55 billion cubic meters (17) Biomass Smoke Emissions and Chemical Composition Table 2 shows a simplified classification of the fuels used for cooking and heating, divided into solid or nonsolid fuels. Sources of energy and fuels can be also classified in renewable and nonrenewable; renewable refers to energy derived from sources that are essentially inexhaustible, such as solar energy, wind, and TABLE 1. ESTIMATED HOUSEHOLD USE OF SOLID FUEL, BY WORLD HEALTH ORGANIZATION SUBREGION Subregion Subregional Population (in thousands) Household Use of Solid Fuel (% of population) Point Estimate (range) Africa D 293, ( ) Africa E 337, ( ) America A 320, ( ) America B 430, ( ) America D 71, ( ) Eastern Mediterranean B 139, ( ) Eastern Mediterranean D 357, ( ) Europe A 410, ( ) Europe B 216, ( ) Europe C 245, ( ) Southeast Asia B 292, ( ) Southeast Asia D 1,238, ( ) Western Pacific A 153, ( ) Western Pacific B 1,528, ( ) World 6,036, ( ) Definition of abbreviations:a5 very low child, very low adult mortality; B 5 low child, low adult mortality; C 5 low child, high adult mortality; D 5 high child, high adult mortality; E 5 high child, very high adult mortality. Regional country groupings for global assessment according to the World Health Organization (43, 157).

3 FIRS Report: Biomass Smoke and Health 579 Figure 1. Map of World Health Organization (WHO) regional offices. Regional office headquarters are marked with black squares. (Modified from: WHO regional offices [Internet]. Geneva, Switzerland: World Health Organization [Ó 2008]. Available from: some biomass fuels. Nonrenewable energy includes fossil fuels, such as petroleum and nuclear energy. The most efficient fuels generate more heat and fewer pollutants per unit of fuel used but tend to be more expensive, whereas more polluting fuels are inexpensive: a relationship called the household fuel ladder (18). Biomass materials are considered low-efficiency fuels because there are many pollutant products and they are low warming. There is a wide variation in the emission of pollutants produced when biomass is burned, depending principally on the characteristics of combustion and the cooking practices. Unfortunately, the production and the end use of biomass fuels are done under suboptimal conditions, contributing enormously to indoor air pollution and to greenhouse gas (GHG) burden (14). Wood smoke is a complex mixture of numerous volatile and particulate substances constituted by different organic and inorganic compounds (9, 19, 20), and its Figure 2. Worldwide solid fuel use for cooking. (Modified from: Children s environmental health. Part 2: Global environmental issues [Internet]. Geneva, Switzerland: World Health Organization [Ó 2008]. Map 9. Indoor smoke: breaking down respiratory defences. Available from: en/map09b.jpg.)

4 580 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL TABLE 2. SIMPLIFIED CLASSIFICATION OF FUELS USED FOR COOKING AND HEATING Solid fuels Coal Biomass fuels Wood: unprocessed and charcoal Dung Crop residues Nonsolid fuels Kerosene Liquefied petroleum gas Gas Electricity TABLE 3. CHEMICAL COMPOSITION OF WOOD SMOKE Species Grams per Kilogram of Wood Carbon monoxide 80 to 370 Methane 14 to 25 Volatile organic compounds (C2 C7) 7 to 27 Aldehydes 0.6 to 5.4 Substituted furans 0.15 to 1.7 Benzene 0.6 to 4.0 Alkyl benzenes 1 to 6 Toluene 0.15 to 1.0 Acetic acid 1.8 to 2.4 Formic acid 0.06 to 0.08 Nitrogen oxides (NO, NO 2 ) 0.2 to 0.9 Sulfur dioxide 0.16 to 0.24 Methyl chloride 0.01 to 0.04 Naphthalene 0.24 to 1.6 Substituted naphthalenes 0.3 to 2.1 Oxygenated monoaromatics 1 to 7 Total particle mass 7 to 30 Particulate organic carbon 2 to 20 Oxygenated PAHs 0.15 to 1 Varied PAHs Benzo[a]pyrene to Dibenzo[a,h]pyrene to l Dibenz[a,h]anthracene to Particulate elemental carbon 0.3 to 5 Normal alkanes (C24 C30) to Cyclic di- and triterpenoids Dehydroabietic acid 0.01 to 0.05 Isopimaric acid 0.02 to 0.10 Lupenone to Friedelin to Chlorinated dioxins to Particulate acidity to Definition of abbreviation: PAH 5 polycyclic aromatic hydrocarbon. Data are from Reference 19. composition varies with the fuel and the conditions of combustion. More than 200 chemical and compound groups have been identified (Table 3), which are almost all (.90%) in the inhalable size range with mean aerodynamic particulate matter diameters less than 10 mm (PM 10 ). A significant number of these wood smoke constituents are known to be toxic or irritants for the respiratory system, including respirable PM (PM 10 ), carbon monoxide (CO), nitrogen and sulfur oxides (NO 2,SO 2 ), aldehydes (e.g., formaldehyde), polycyclic aromatic hydrocarbons (e.g., benzopyrene), volatile organic compounds, chlorinated dioxins, and free radicals (19 22). Many substances can act as primary pollutants, irritants, and carcinogenic or cocarcinogenic compounds (20). The mean emission concentrations of PM 10 from charcoal combustion could be 87 and 92% less than emissions from unprocessed wood combustion, during the burning and smoldering period, respectively (23). On the contrary, non-co 2 GHG emissions from charcoal combustion are 6 to 13 times higher than those from woodstoves, when the emissions from the charcoal production are also included (24). Smoke from other types of biomass has a similar composition, although less well characterized than wood smoke (9, 25) Contribution of the Use of Biomass Fuels to Air Pollution In general, the household use of solid fuels (biomass or coal) is the main source of indoor air pollution and, in certain geographic zones and seasons, also of outdoor pollution. The pollutant emissions from burning solid fuels usually exceed considerably the health-based national standards for outdoor pollution (25) Indoor air pollution. Cooking is the most important activity contributing to indoor air pollution. However, in some regions, especially in Asia, heating is another important source (26). The majority of rural households in developing countries burn biomass fuels in open fireplaces or in nonairtight stoves, resulting in substantial emissions, which, in the presence of poor ventilation, produce very high levels of indoor pollution with 24-hour mean PM 10 levels in the range of 300 to 3,000 mg/m 3, which may reach 30,000 mg/m 3 during periods of cooking (2, 4). The mean 24-hour levels of CO in the same households are in the range of 2 to 50 ppm, and can reach 500 ppm during cooking. The measurement of indoor air pollution from biomass combustion is complex because of the temporal and spatial distribution within the household, and the characteristics of the ventilation. In developing countries, the levels of indoor air pollution in homes using biomass fuels for cooking far exceed the health-based standards in the whole household, in both cooking and sleeping or living areas, with repeated episodes of intense emissions (16, 23, 26 28). Cooking or heating with biomass fuels in stoves or fireplaces vented to the outdoors (airtight stoves) also produces high indoor air pollution, exceeding substantially the total global outdoor exposures to several important pollutants, including respirable particulates, although there is a substantial reduction in indoor concentration of pollutants compared with houses with unvented stoves. Studies from China (29) and from other developing countries (30) provide data supporting the large contribution of indoor pollution to total exposure, especially for women and children. In China, it has been estimated that 80 to 90% of the total exposure to PM 10 results from indoor air pollution due to solid fuel use in the rural population and this contribution is less than 60% in the urban population (31). The level of exposure of a population or an individual who uses solid fuels is extremely variable (7, 10, 12, 32 34). Up to half of the total exposure in women who cook with solid fuel may be derived by high-intensity episodes when they are close to the fire, especially when starting or stirring the fire Outdoor air pollution from indoor sources. Biomass burning, especially wood, also contributes to outdoor pollution (9, 24, 35). In developing countries, household solid fuel use is the main source of ambient (outdoor) pollution in rural areas and may significantly contribute to outdoor pollution in some urban areas (9). In developed countries, a substantial number of studies summarized recently (9) have measured the contribution of domestic and industrial wood burning to the environmental outdoor pollution. Wood smoke may be the major source of PM during winter months in several parts of the western United States (36 40), and comparable to that emitted from automobiles, industries, or power plants. Other sources of outdoor air pollution are forest fires and agricultural burning affecting mainly agricultural workers and firefighters with acute or subacute exposures. Some reviews (9),

5 FIRS Report: Biomass Smoke and Health 581 including a WHO guideline (41), provide relevant information about this issue. There is a growing interest in the impact of GHG derived from production and end use (burning) of biomass. The use of charcoal significantly reduces indoor air pollution but increases non-co 2 GHG emissions, with their global warming potential (14, 42, 43) Toxic Effects of Wood Smoke Exposure Many wood smoke constituents (Table 3) can produce acute and/or chronic biologic, physiologic, and structural effects in exposed animal models (44 46) and humans (20). Naeher and colleagues (9) have summarized the principal published studies about the toxicologic effects of wood smoke. Table 4 presents the main effects described in animal models. Other toxicologic effects of chronic exposure to biomass smoke have been derived from clinical observations of exposed patients with chronic symptoms or respiratory disease. Table 5 summarizes the proposed mechanisms by which the most important pollutant in biomass and coal smoke may cause adverse health effects including cataracts (2) Assessment of Biomass Smoke Exposure and Risks Exposure is a function of both the pollutant concentration in an environment and the time spent by the subject in that environment (person-time). Some of the variables related to biomass combustion and derived exposure that can be measured include the following: indoor emissions, indoor concentrations, personal exposures, breath levels of pollutants, air exchange rate (ventilation), outdoor emissions, and outdoor concentrations. The pollutants more frequently measured are those regulated outdoors: PM (PM 10 and PM 2.5 ), CO, nitrogen oxides (NO 2 ), and sulfur oxides (SO 2 ). Pollutant concentrations exhibit an extremely wide temporal and spatial variability within the household, creating different microenvironments and variable exposures. In addition, the measurement of PM 10 and CO, as quantified in most studies evaluating exposures, might not be representative of the exposure to other dangerous compounds. In epidemiologic studies on the effects of biomass combustion products, the air pollutant concentrations should be measured continuously and for long enough periods in a representative sample of the at-risk population, in various environments together with the person-time spent in the environments, and the number of people exposed. Unfortunately, there may be residual misclassification of the exposure because of several TABLE 4. TOXICOLOGIC EFFECTS OF WOOD SMOKE EXPOSURE REPORTED IN ANIMAL MODELS Acute: single exposures Necrotizing tracheobronchial epithelial cell injury Acute tracheobronchial and bronchiolar inflammatory response Acute mucociliary dysfunction Alveolar macrophage dysfunction Airway hyperresponsiveness Lung compliance reduction Ventilatory response reduction Subchronic: repeated exposures Airway epithelial lining desquamation Pulmonary edema Neutrophilic peribronchiolar and perivascular infiltration Bronchiolitis Lymphoid follicles hyperplasia Late eosinophilia Bacterial clearance reduction Mild emphysema Lung cancer confounding factors that include lack of specificity for biomass smoke, poor correlation between personal and central monitor exposure metrics, inability to account for the modifying effect of personal behavior on the level of personal exposures, and failure to capture differences in personal exposure versus absorbed dose (9). The estimation of the health effects of indoor smoke from solid fuels by extrapolating the well-established exposure response relationships obtained from outdoor epidemiologic studies on the same pollutants has potential problems, such as the following: differences in pollutant mixtures and toxicity of inhaled PM, differences in exposure patterns, differences in exposure levels, and differences in relevance of the health outcomes addressed (10). An alternative strategy, used in most epidemiologic studies in developing countries, is to divide the population into people exposed or not exposed to biomass smoke on the basis of the biomass fuel use and ventilation (10), accepting that this method overlooks the large variability of exposures. Using a simple binary classification of the exposure (exposed or not exposed), selecting the suspected health outcomes (symptoms, specific diseases, mortality), and adjusting the confounding factors, it is possible to measure and test associations. The strength of the epidemiologic studies (evidence) evaluating these possible associations for biomass smoke exposure is shown in Table 6 (10). Detailed reviews on the assessment of solid fuel use, exposure, and relative risks for health outcomes have been presented by Smith and colleagues (10), Desai and colleagues (7), and Naeher and coworkers (9). 3. BURDEN OF DISEASE FROM INDOOR AIR POLLUTION Until recently, most of the worldwide research on air pollution focused on outdoor sources. Murray and Lopez (47) estimated that some 500,000 deaths from pneumonia, COPD, cardiovascular diseases, and all causes combined could be attributable to outdoor air pollution each year. The global burden of disease caused by the indoor use of solid fuels has been estimated taking into account acute lower respiratory infections (ALRIs), COPD, and lung cancer (i.e., the three specific diseases for which there is a strong evidence of an association with the exposure) (Table 6) (7, 10). More than 1.6 million deaths and over 38.5 million of disability-adjusted life-years (DALYs) were attributable to indoor smoke from solid fuels in 2000 (5, 10, 32). Cooking with solid fuels is considered to be responsible for about 2.6% of the global burden of disease (3.6% in developing countries). ALRIs in young children account for 59% of all attributed premature deaths and 78% of DALYs. COPD accounts for almost all the remaining premature deaths due to indoor air pollution, with lung cancer as a relatively minor contributor (10), which can be important for people exposed to coal, especially in China. Tables 7 10 show the burden of disease from use of solid fuels in 2000, according to WHO regions (7). Five regions in descending order, Southeast Asia D, Western Pacific B, Africa E, Africa D, and eastern Mediterranean D (see abbreviations footnote in Table 10), contribute with 94% of the deaths and 93% of DALYs attributable to indoor air pollution from solid fuels (10). Others studies have focused on the burden of disease from indoor air pollution in developing countries (4, 29, 32, 48). In India, approximately 500,000 premature deaths, representing 6 to 7% of the national burden of disease, may be attributable to indoor air pollution (48). Extrapolating to the rest of the world on the basis of regional use of solid fuels and regional population and health conditions, solid fuel use in developing countries might be responsible for nearly 4% of the global burden of disease and

6 582 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL TABLE 5. DOMESTIC SMOKE POLLUTANTS AND POSSIBLE MECHANISMS FOR POTENTIAL HEALTH EFFECTS Pollutant Mechanism Potential Health Effects Particulate matter (small particles,10 mm, d Acute: bronchial irritation, inflammation d Wheezing, exacerbation of asthma and particularly,2.5 mm aerodynamic diameter) and increased reactivity d Reduced mucociliary clearance d Respiratory infections d Reduced macrophage response and (?) reduced local immunity d Chronic bronchitis and chronic obstructive pulmonary disease d (?) Fibrotic reaction d Exacerbation of chronic obstructive pulmonary disease Carbon monoxide d Binding with hemoglobin to produce carboxyhemoglobin, which reduces oxygen delivery to key organs and the developing fetus. d Low birth weight (fetal carboxyhemoglobin 2210% or higher) d Increase in perinatal deaths Polycyclic aromatic hydrocarbons (e.g., benzo[a]pyrene) d Carcinogenic d Lung cancer d Cancer of mouth, naso-pharynx and larynx Nitrogen dioxide d Acute exposure increases bronchial reactivity d Wheezing and exacerbation of asthma d Longer term exposure increases susceptibility to bacterial and viral lung infections d Respiratory infections d Reduced lung function in children Sulfur dioxide d Acute exposure increases bronchial reactivity d Wheezing and exacerbation of asthma d Longer term: difficult to dissociate from effects of particles d Exacerbation of chronic obstructive pulmonary disease, cardiovascular disease Biomass smoke condensates including polycyclic aromatics and metal ions d Absorption of toxins into lens, leading to oxidative changes d Cataracts Modified from Reference 2. more than 1 million premature deaths per year (32). A positive association between the use of biomass fuels (and indoor air pollution measured by PM 10 and CO) and infant mortality has been described in Ecuador (49). Lopez and coworkers (50) have estimated the deaths and DALYs due to COPD, comparing the impact of tobacco and biomass by sex, in developed and developing countries. Globally, close to 50% of the deaths from COPD in developing countries could be attributed to biomass, and about 75% of these are in women (Table 11). Taking into account the growing evidence from epidemiologic studies establishing a relationship between the use of biomass fuel household and ill health, the WHO included indoor air pollution among the 26 risk factors relevant to global burden of disease (5, 50, 51). Indoor air pollution was globally ranked 10th among preventable risk factors causing burden of disease, and fourth in developing countries (5). 4. RESPIRATORY EFFECTS OF BIOMASS FUEL COMBUSTION: EVIDENCE AND BURDEN 4.1. Health Outcomes and Evidence The quantity and quality of the available studies associating the exposure to biomass combustion products with respiratory diseases are limited but growing. Three outcomes were qualified by Smith and colleagues (10) as having strong evidence of association with exposure to solid fuel smoke: ALRIs in young children (,5 yr), COPD in women, and lung cancer in women exposed to coal smoke (Table 6). Evidence for associations with COPD and lung cancer (from coal smoke exposure) in men was considered moderate, and association of biomass smoke with lung cancer, asthma in children and adults, and tuberculosis in adults was considered scarce. Few studies have established an association between lower values of lung function, airflow obstruction, and chronic exposure to biomass fuel smoke. Confounding factors represent a substantial problem for observational studies of indoor air pollution and health (52). Interventions and cohort studies are required to determine more clearly the strength of the associations. However, available evidence supports a causal role for the observed associations ALRIs in Children ALRIs are a leading cause of the global burden of disease, accounting for 7% of the total (50). ALRIs are also the first cause of mortality from infectious diseases and are responsible for an estimated 4 million deaths worldwide (2 million in children younger than 5 yr) (50). Indoor air pollution from solid fuel use TABLE 6. RELATIVE RISKS FOR HEALTH OUTCOMES ASSOCIATED WITH SOLID FUEL SMOKE INHALATION Evidence Health Outcome Group, Age (yr) Relative Risk 95% CI Strong ALRI Children,, COPD Women, > Lung cancer (coal smoke exposure) Women, > Moderate I COPD Men, > Lung cancer (coal smoke exposure) Men, > Moderate II Lung cancer Women, > (biomass smoke exposure) Asthma Children, Asthma All, > Cataracts All, > Tuberculosis All, > Definition of abbreviations: ALRI 5 acute lower respiratory infection; CI 5 confidence interval; COPD 5 chronic obstructive pulmonary disease. Data are from Reference 7.

7 FIRS Report: Biomass Smoke and Health 583 TABLE 7. MORTALITY AND DISABILITY-ADJUSTED LIFE-YEARS ATTRIBUTABLE TO SOLID FUELS USE ACCORDING TO WORLD HEALTH ORGANIZATION REGIONS Subregion Attributable Mortality (in thousands) Percentage of Total Mortality in the Region Attributable DALYs (in thousands) Percentage of Total DALYs in the Region AFR D , AFR E , AMR A AMR B AMR D EMR B EMR D , EUR A EUR B EUR C SEAR B SEAR D , WPR A WPR B , World 1, , Definition of abbreviations: A5 very low child, very low adult mortality; AFR 5 Africa; AMR 5 Americas; B 5 low child, low adult mortality; C 5 low child, high adult mortality; D 5 high child, high adult mortality; DALYs 5 disability-adjusted life-years; E 5 high child, very high adult mortality; EMR 5 eastern Mediterranean; EUR 5 Europe; SEAR 5 Southeast Asia; WPR 5 Western Pacific. Data are from References 5 and 7. is a confirmed risk factor for ALRIs, especially in children, in developing countries (53). The relative risk of ALRIs for children exposed to household biomass smoke has been quantified in several studies (53 62), the majority from developing countries, but also in studies from the United States (61, 62). Most of the studies were case-control studies and there were a few cohort studies. They show a consistent and significant relationship between the exposure to solid fuel use and an increase of the risk of ALRIs with odds ratios (ORs) ranging from 1.8 to 5.5 (95% confidence interval [CI], ). The overall estimate of the risk of ALRIs, from the eight selected studies by Smith and colleagues (10), was 2.3 (95% CI, ): 1.8 for children younger than 5 years and 2.5 for children younger than 2 years. The highest OR was found in children carried on their mother s back while cooking (OR, 3.1; 95% CI, ). Frequency of ARI and ALRIs increase in an exponential fashion when PM 10 concentrations increase above 2,000 mg/m 3 (54). Impaired mechanisms of defense are a plausible explanation for the increased risk of ALRIs in exposed children (20, 53) COPD, Chronic Bronchitis, Respiratory Symptoms, and Lung Function COPD is one of the most important causes of global burden of disease in people older than 40 years (63) and is increasing. It has been estimated that COPD will be the fifth cause of DALYs and the third cause of mortality in the world (64, 65). In developed countries, most COPD cases are related to cigarette smoking. In developing countries, COPD is also a prevalent condition. In TABLE 8. ESTIMATED POPULATION ATTRIBUTABLE FRACTIONS FOR SOME DISEASES ASSOCIATED WITH SOLID FUEL USE Disease Male (%) Female (%) Both Sexes (%) Chronic obstructive pulmonary disease Acute lower respiratory infection Tracheobronchial cancers Data are from References 5 and 7. TABLE 9. ATTRIBUTABLE MORTALITY AND DISABILITY-ADJUSTED LIFE-YEARS FROM SOLID FUEL USE, BY AGE GROUP AND SEX Distribution of attributable Deaths, % attributable events Distribution of attributable DALYs, % attributable events Age Group (yr) Latin America, the prevalence of COPD varies from 7.8 to 19.7% in the urban population aged 40 years and older (66, 67). In these countries, a significant fraction of COPD, which could reach 50%, especially in women, occurs in never-smokers, and could be attributed predominantly to biomass (wood) burned in open stoves for cooking (and heating in the colder, higher altitudes) (66 68). A large number of mainly cross-sectional and case-control studies (52, 69 89) have found association of exposure to solid fuel smoke with COPD, chronic bronchitis, chronic airway disease, and airflow obstruction, especially in women. The overall risk of COPD in women exposed to indoor air pollution from domestic solid fuel use, especially wood, estimated by Smith and coworkers (10), was consistently higher (OR, 3.2; 95% CI, ) than in men (OR, 1.8; 95% CI, ), who were likely less exposed. Two recent probabilistic, population-based studies ratified a clear association between the exposure to smoke from biomass fuels and COPD defined by a post-bronchodilator FEV 1 to FVC ratio less than 70% (66, 86). One of these studies (66), which included 5,539 people, demonstrated that cooking 10 years or more with a wood stove was an independent risk factor for COPD after adjusting by age, sex, active and passive smoking, education level, history of tuberculosis, and exposure to charcoal or dust at work (OR, 1.50; 95% CI, ; P, 0.001). Interestingly, only a small sex difference was found, with an OR Sex Male Female Definition of abbreviation: DALYs 5 disability-adjusted life-years. Data are from References 5 and 7. TABLE 10. BURDEN OF DISEASE FROM USE OF SOLID FUEL 2000 Subregion ALRI Deaths (in thousands) COPD Lung cancer All causes ALRI COPD DALYs (in thousands) Lung Cancer All Causes AFR D NA NA 5,394 AFR E NA NA 6,924 AMR A 0 0 NA NA 6 AMR B 6 9 NA NA 444 AMR D 9 2 NA NA 329 EMR B 2 0 NA NA 64 EMR D NA 116 3, NA 3,508 EUR A 0 0 NA NA 0 EUR B 12 5 NA NA 477 EUR C 1 4 NA NA 67 SEAR B NA NA 990 SEAR D ,506 1, ,237 WPR A 0 0 NA NA 0 WPR B ,275 3, ,097 World ,619 31,919 6, ,539 Definition of abbreviations: A 5 very low child, very low adult mortality; AFR 5 Africa; AMR 5 Americas; B 5 low child, low adult mortality; C 5 low child, high adult mortality; D 5 high child, high adult mortality; DALYs 5 disability-adjusted life-years; E 5 high child, very high adult mortality; EMR 5 eastern Mediterranean; EUR 5 Europe; SEAR 5 Southeast Asia; WPR 5 Western Pacific. Data are from References 5 and 10.

8 584 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL TABLE 11. ESTIMATES OF DEATHS, IN THOUSANDS, DUE TO CHRONIC OBSTRUCTIVE PULMONARY DISEASE, COMPARING THE IMPACT OF TOBACCO AND BIOMASS BY SEX Countries Males Females Tobacco Biomass Tobacco Biomass Poor and middle income Rich All Data are from Reference 50. of 1.84 for females and 1.53 for males, suggesting that biomass fuel smoke may also be an important risk factor for men, which is consistent with small sex differences in total exposures to PM 10 from indoor air pollution in China (31). This finding could be partially explained by the persistent high levels of pollutants in living and sleeping areas at homes where biomass fuels are used. An increased risk for COPD in people exposed to wood and charcoal smoke (OR, 4.5; 95% CI, ) was found in Spain (83), and it would be important to confirm this association in other developed countries. The report of respiratory symptoms, especially phlegm and cough, is consistently higher in women cooking with biomass fuels in comparison with those using cleaner fuels (charcoal, gas, kerosene) (81, 84, 85). This finding has been associated with the PM 10 concentrations, which often exceed 2,000 mg/m 3 (84). For example, wood users (mean PM 10, 1,200 mg/m 3 ) had significantly more cough than charcoal (PM 10, 540 mg/m 3 ), liquefied petroleum gas (LPG), and electricity users (PM 10, mg/m 3 ) (85). The use of biomass fuels, mainly wood, has been also associated with an impairment of pulmonary function. Mild to moderate reductions of FEV 1 /FVC, FEV 1,FEV 1 %, PEF, and FEF have been associated with the exposure to indoor biomass burning in cross-sectional studies (80, 84). Other studies, mainly hospitalbased case-control studies, confirm that people exposed to biomass smoke have a high risk for developing airflow obstruction with significant reduction of FEV 1 and FEV 1 /FVC (69, 82, 88). The exposure response curves for COPD related to indoor biomass smoke exposure have not been established, but in a casecontrol study (88), the risk for chronic bronchitis and chronic airway disease increased linearly with the exposure estimated as hour-years (average hours a day cooking with a wood stove multiplied by years of cooking), and the risk of airflow obstruction increased briskly above 200 hour-years. Maternal exposure to biomass smoke has been associated with low birth weight in infants (90), with possible impairment of lung growth and development and impact on adult respiratory function and diseases Comparison between COPD related to smoking and to biomass smoke exposure. COPD related to chronic indoor (domestic) inhalation of wood smoke has similarities and differences with COPD due to cigarette smoking (68, 91, 92). Wood smoke attributable COPD presents clinically with minimal emphysema as a chronic obstructive disease with persistent cough, phlegm, dyspnea, and cor pulmonale (93, 94). The women with wood smoke attributable COPD tend to be older, shorter, and have a greater body mass index than those with cigarette smoking attributable COPD (68, 93); they also have milder reduction of CO diffusing capacity of the lung (DL CO ), a normal or near normal ratio of DL CO /alveolar volume (93, 95), and minimal or no emphysema on high-resolution computed tomography (CT) of the chest (95). Hyperresponsiveness to methacholine challenge was more severe in women with wood smoke attributable COPD than in women with cigarette (tobacco) smoking attributable COPD (94); however, most clinical characteristics, quality of life, and mortality were similar in both groups once severity of airflow obstruction was taken into account (68). Lung morphology in necropsies from women with COPD only exposed to tobacco smoke and from those only exposed to biomass smoke (96) shows varying severities of similar alterations. For example, anthracosis and scarring were more frequent and emphysema milder in wood smoke attributable COPD compared with smokers. Widespread mucosal swelling and anthracotic plaques of the airways have also been described in women exposed to biomass smoke (97). These clinical descriptions, still scarce, clearly show the possibility of developing severe and even fatal airflow obstruction in neversmokers with cor pulmonale with lifelong domestic exposure to biomass smoke (96) Lung Cancer in Women Exposed to Coal and Biomass Smoke A strong association between coal smoke exposure and lung cancer has been described in China in women who cook using coal in open stoves (29, ). Analyzing available studies, Smith and coworkers (10) and Zhang (29) have estimated that the risk for lung cancer associated with solid fuel exposure is significantly higher in women than in men (see Table 12). On the other hand, an increased lung cancer risk in subjects exposed to biomass smoke has been found at a mild level and only inconsistently (116, 117). A weak association between biomass smoke exposure, especially wood, and lung cancer in women, especially lung adenocarcinoma, was reported (117), which was not present for men. An excess risk for lung cancer (OR, 2.5; 95% CI, ) was also found in women residing in Montreal, Canada, an area in which women in the past (and currently in some areas) used coal and wood stoves for heating and gas and wood for cooking (118) Tuberculosis Few studies (119, 120, 121) have suggested a link between indoor air pollution from the use of solid fuels and tuberculosis. Mishra and associates (119) described an OR of 2.7 (95% CI, ) for people exposed indoors, but it was not adjusted for smoking. Pérez-Padilla and coworkers (120) found an OR of 2.4 (95% CI, ) adjusted for age, sex, level of education, crowding, smoking, socioeconomic level, zone of residence, and state of birth. A reasonable mechanism for the association would be, as in the case of ARI, impairment of respiratory defenses against mycobacteria (20), which was also found for tobacco exposure. A recent systematic review and meta-analysis (122) supported a mild or moderate association between indoor air pollution and the risk of tuberculosis. Tuberculosis is associated with airflow obstruction in population-based studies (66, 123); therefore, the development of tuberculosis may be another mechanism by which exposure to indoor pollution may derive to COPD Asthma Attacks Desai and colleagues (7), taking into account three studies ( ), have estimated that exposure to solid fuel smoke exacerbates asthma with a relative risk of 1.6 (95% CI, %) for children between 5 and 14 years and of 1.2 (95% CI, ) for persons older than 15 years. TABLE 12. ODDS RATIOS FOR LUNG CANCER IN PERSONS EXPOSED TO COAL SMOKE Subgroup (reference) Odds Ratio (95% CI) Males and females (29) 2.55 ( ) Males only (10) 1.51 ( ) Females only (10) 1.94 ( ) Definition of abbreviation: CI5 confidence interval.

9 FIRS Report: Biomass Smoke and Health 585 TABLE 13. RESEARCH PRIORITIES ON EFFECTS OF BIOMASS EXPOSURE AND INTERVENTIONS Health Effects d Basic Genetic susceptibility to various health effects Similarities and differences to mechanisms involved in the injury, compared with those found for tobacco smoke Heterogeneity of the health responses d Epidemiologic Standardization of exposure measurements and its longitudinal monitoring Dose response curves of health effects Systemic health effects, and health effects outside the respiratory system Health benefits of reducing exposure d Clinical Characterization and early diagnosis of health effects of biomass exposure Similarities and differences of the diseases associated with inhalation of biomass smoke and those associated with tobacco smoke Social, Environmental, and Economic Effects d Short- and long-term socioeconomic impact of exposure and interventions d Short- and long-term environmental impact of solid fuel use and interventions (including sustainability) d Socioeconomic and environmental factors that facilitate or impede the use of improved stoves and other interventions Interventions Longitudinal monitoring of technical performance of improved biomass or solid fuel stoves d Impact of massive educational programs on the exposure to solid fuel smoke and acceptance to health interventions d New biomass (and other solid fuel) stove technology d Multiple-stove/multiple-fuels scenarios d Impact of the improved-stove programs: resistance to implementation, funding, health effects d Inexpensive and cleaner fuels or sources of heat The relationship between indoor air pollution and the development of asthma is even more controversial. Mishra and colleagues (127) determined that elderly men and women living in households using biomass fuels have a significantly higher prevalence of asthma than those living in households using cleaner fuels, with an OR of 1.59 (95% CI, ); the adjusted effect was higher among women (OR, 1.83; 95% CI, ) than among men (OR, 1.46; 95% CI, ) Interstitial Lung Disease, Pneumoconiosis, and Other Respiratory Effects A listing of studies describing reticular or reticulonodular opacities in the lungs of subjects exposed to solid fuel smoke has been compiled (2), but usually there is no difficulty in excluding typical fibrosing diseases, such as the idiopathic pulmonary fibrosis, either clinically, with CT scanning, or in biopsies or necropsies. Anecdotic reports and short case series have linked exposure to biomass smoke with interstitial lung disease (92, 128, 129). Restrepo and associates (128) and Sandoval and colleagues (92) coincided in describing women chronically exposed to wood smoke who had interstitial inflammation and fibrosis, suggesting the possibility of a wood smoke pneumoconiosis related to anthracosis (128). Despite the high number of substances in wood smoke, mineral particles are not commonly found (130, 131) and only traces of silicon have been described (19). However, taking into account the huge variety of wood fuels, stoves, floor materials, and cooking and heating practices, a wide variation of the composition of wood smoke and the possibility of additional inhalation of dusts might be expected. In fact, the term hut lung has been used to describe a form of domestically acquired pneumoconiosis or particulate lung disease in people, almost all women, never exposed to mining or industry but exposed to biomass fuel smoke or some agricultural activities (maize grinding) ( ). Radiologic findings ranged from a miliary pattern with nodules less than 3 mm to extensive infiltrates (linear and reticular), and lung tissue included interstitial inflammation with anthracotic deposits, fibrosis, and a mixture of fibroblast and macrophages heavily laden with carbon and inorganic inclusions ( ), similar to the histopathologic descriptions by Restrepo and colleagues (128) and Sandoval and coworkers (92). Inflammatory and fibrous interstitial responses due to anthracotic deposits or other components of the biomass smoke have been suggested and called fly ash lung (135). Chest radiographs and CT in women chronically exposed to wood smoke may show linear shadows and nodular opacities supporting an interstitial involvement (91, 97, 136) but not as important as to be confused with classical fibrosing diseases. 5. SUGGESTIONS FOR PREVENTION OF DISEASES RELATED TO SOLID FUEL SMOKE EXPOSURE The ideal way to prevent or reduce the health impacts is the withdrawal or reduction of the exposure. However, the selection of the strategies to achieve this aim is very complex because it should take into consideration not only the personal exposure but also cultural and economic aspects at individual and local levels: the level of development, resources, technical capacity, the domestic needs of energy, the sustainability of the considered sources of energy, and the protection of the environment. Interventions and research should consider all these aspects to offer feasible solutions (2, 137). A logical first step for many of the poorest countries and communities is the development of projects to define the local resources and capacity to offer widespread and sustainable improvements in household energy (137). Although a change to cleaner and sustainable fuels is the main recommendation, substantial improvements can be obtained even when dirty biomass fuels are used, such as simple changes in ventilation characteristics of housing (locations and placement of windows and doors, cooking locations, space configuration, construction materials) and ventilation practices (keeping doors and windows open after cooking) (33). Some of these arrangements are within the means of poor families and may be of considerable cost-effectiveness (33). From a public health point of view, these local measures and the continued promotion of improved stoves can significantly reduce exposures within solid fuel using households (138) because the use of cleaner fuels for most people exposed seems unlikely in the near future despite a global clean cooking fuel initiative (139) Interventions and Education The introduction and success of a selected intervention require habits and behavioral changes. Even after electrification in a traditionally wood-burning area of South Africa, the more polluting fuels continued being used, particularly for cooking and heating (140). Almost a decade after the introduction of electricity in the Bushbuck Ridge region of South Africa, over 90% of households still used fuel wood for thermal purposes, especially cooking, and the mean household consumption rates over a 11- year period had no change, even with a policy of 6 kw/hour per month of free electricity (141). Therefore, education and cultural modification are necessary components of any intervention that must adapt to users needs, which include both practical and sociocultural considerations (142). The education level has shown a strong correlation with the risk of respiratory diseases from biomass exposure in women; illiterate women are at three to six times higher risk for all respiratory diseases compared with literate women (143). Edu-