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ABSTRACT
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 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.
Key Words: solid fuels • indoor pollution • biomass • chronic obstructive pulmonary disease
CONTENTS
Foreword
Introduction
Background
Burden of Disease from Indoor Air Pollution
Respiratory Effects of Biomass Fuel Combustion: Evidence and Burden
Suggestions for Prevention of Diseases Related to Solid Fuel Smoke Exposure
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:
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 (www.who.int/tobacco/framework/en), in the development of International Standards for Tuberculosis Care (www.who.int/tb/publications/2006/istc_report_shortversion.pdf), and in the creation of the Global Alliance against Chronic Respiratory Diseases (GARD) (www.who.int/gard), as well as to prepare a document to help spread the use of simple spirometry worldwide.
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.
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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).
2.2. 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 some biomass fuels. Nonrenewable energy includes fossil fuels, such as petroleum and nuclear energy.
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The mean emission concentrations of PM10 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-CO2 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).
2.3. 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).
2.3.1. 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 PM10 levels in the range of 300 to 3,000 µg/m3, which may reach 30,000 µg/m3 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 PM10 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.
2.3.2. 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), 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-CO2 GHG emissions, with their global warming potential (14, 42, 43).
2.4. 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).
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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).
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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).
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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).
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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.
4.2. 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 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], 1.3–8.5). The overall estimate of the risk of ALRIs, from the eight selected studies by Smith and colleagues (10), was 2.3 (95% CI, 1.9–2.7): 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, 1.8–5.3).
Frequency of ARI and ALRIs increase in an exponential fashion when PM10 concentrations increase above 2,000 µg/m3 (54). Impaired mechanisms of defense are a plausible explanation for the increased risk of ALRIs in exposed children (20, 53).
4.3. 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 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, 2.3–4.8) than in men (OR, 1.8; 95% CI, 1.0–3.2), 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 FEV1 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, 1.36–2.36; P < 0.001). Interestingly, only a small sex difference was found, with an OR 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 PM10 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, 1.4–14.2) 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 PM10 concentrations, which often exceed 2,000 µg/m3 (84). For example, wood users (mean PM10, 1,200 µg/m3) had significantly more cough than charcoal (PM10, 540 µg/m3), liquefied petroleum gas (LPG), and electricity users (PM10, 200–380 µg/m3) (85). The use of biomass fuels, mainly wood, has been also associated with an impairment of pulmonary function. Mild to moderate reductions of FEV1/FVC, FEV1, FEV1%, PEF, and FEF25–75 have been associated with the exposure to indoor biomass burning in cross-sectional studies (80, 84). Other studies, mainly hospital-based case-control studies, confirm that people exposed to biomass smoke have a high risk for developing airflow obstruction with significant reduction of FEV1 and FEV1/FVC (69, 82, 88).
The exposure–response curves for COPD related to indoor biomass smoke exposure have not been established, but in a case-control 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.
4.3.1. 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 (DLCO), a normal or near normal ratio of DLCO/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 never-smokers with cor pulmonale with lifelong domestic exposure to biomass smoke (96).
4.4. 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, 98–115). 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, 1.5–3.6) 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).
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4.6. Asthma Attacks
Desai and colleagues (7), taking into account three studies (124–126), have estimated that exposure to solid fuel smoke exacerbates asthma with a relative risk of 1.6 (95% CI, 1.0–2.5%) for children between 5 and 14 years and of 1.2 (95% CI, 1.0 – 1.5) for persons older than 15 years.
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, 1.30–1.94); the adjusted effect was higher among women (OR, 1.83; 95% CI, 1.32–2.53) than among men (OR, 1.46; 95% CI, 1.14–1.88).
4.7. 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) (132–134). 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 (132–134), 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).
5.1. 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). Education requires a systematic and comprehensive program to have massive impact; it should be addressed to the general community (people exposed), health personnel (e.g., general practitioners, nurses, health promoters), governmental staff involved in health care, nongovernmental organizations, and potential donors or benefactors. Education is aimed to encourage behavioral changes in cooking and heating, in ventilation characteristics of housing and practices, and in the acceptance of new, cleaner fuels and improved stoves.
Certain habits, such as remaining unnecessarily close to the fire or cooking certain foods, increase significantly the exposure (28) and should be changed. Women should also be encouraged to keep their children far away from the fire or to consider improvements or changes in the ventilation conditions or the stoves and fuels used.
5.1.2. Improvements in household ventilation and area distribution.
Simple improvements in ventilation of houses could significantly reduce PM10 (33) and could be cost-effective interventions (33, 138). An open window in the cooking area could reduce the indoor CO by 85% (137). Large and better-placed windows in the whole household and/or gaps between roof and wall (137, 144) may help, as well as maintaining the windows open while cooking. A kitchen physically separated from the living and sleeping area could reduce significantly the average exposure (16, 26, 28). In households in which the heating stove is different from the cooking stove, like in China (26), reducing exposures requires improvements in the stoves.
5.1.3. Improvements in stoves.
Improved stoves favor a more complete combustion of fuels, increasing the generated heat and decreasing the harmful by-products (high-efficiency/low-emission stoves). Chimneys directing the fumes to the outside of the household can be added and enhance the benefits in reducing the particulate indoor air pollution.
Reductions from 40 to 85% in PM2.5, PM10, and CO concentrations have been described using improved stoves (23, 145). Although the concentrations of indoor pollutants from improved stoves are reduced, they still remain significantly higher than international standards.
The information about the impact of the improved-stove programs on health is scarce and large-scale rural stove programs have been questioned (146). Under the Chinese program, which began in 1980, improved stoves had been installed in over 172 million homes by the end of 1995 (147).
However, recent information supports the benefits of improved stoves in terms of health outcomes. Ezzati and associates estimated a reduction by 24 to 64% of acute respiratory infections and 21 to 44% for ALRIs in children younger than 5 years in Kenya, which was attributable to the transitions in household energy, including improvements of stoves (148). A recent study in Pakistan showed that dry cough, sneezing, and tears while cooking are less likely to occur in women using improved stoves compared with traditional stoves (149). In Guatemala, several health benefits were also observed after a change to improved wood stoves (so-called "plancha" stoves) relative to the group remaining with open fire stoves (150–153).
5.1.4. Changes of the fuels for cooking and heating.
Replacing wood or other biomass fuels used for cooking or heating with cleaner fuels, such as petroleum-derived fuels (LPG, kerosene), industrially processed biomass, thermoelectric energy, electricity, and, eventually, nuclear energy, may solve the health problems associated with exposure to biomass smoke and the ecological threat of deforestation linked with an uncontrolled increase in the population using wood as a fuel (2, 4, 154). Electricity and solar energy (solar cookers) are highly efficient and clean, but they are expensive and limited. Other, less expensive, high-efficiency/low-emission fuels include LPG and kerosene.
The reduction of particulate indoor air pollution using LPG as fuel ranges from 50 to 90% (145, 149); a similar reduction has been found using kerosene, but the quality of the fuel and therefore of the cleanliness may vary widely (137).
Because of the costs of electricity and the costs and availability of LPG and kerosene, charcoal, a biomass fuel, which is cleaner than other unprocessed biomass, has been used as a transitional fuel, especially in sub-Saharan Africa (24). Concentrations of PM10 in households using charcoal are close to 90% lower than in those using open wood fires. Bailis and colleagues (24) have estimated that gradual and rapid transitions from open wood fires to charcoal would delay 1 million and 2.8 million deaths by 2030. Gradual and rapid transitions to petroleum fuels would delay 1.3 and 3.7 million deaths, respectively. Approximately 83 to 85% of the avoidable deaths are in children and the remaining in women.
Combustion of petroleum derivates and incomplete combustion of biomass generate a significant burden of GHGs impacting the global warming (155). Transition to charcoal in Africa, using the current practices, could increase GHG emissions by 140 to 190% (24). This increase can be reduced to 5 to 36% using the currently available technologies for sustainable production.
In summary, transition to high-efficiency/low-emission fuels will have substantial health benefits. This transition should be adapted to the particular conditions of each region and country (154). Many urban and periurban solid fuel–using populations may move to using LPG and kerosene, whereas the poorest rural populations should consider the use of charcoal and improved solid fuel stoves.
5.2. Research
Despite their unquestionable importance, research and information in many aspects of the exposures, risks, and health effects of biomass fuel–combustion smoke and the interventions to reduce or avoid it are lacking or very scarce (2, 4, 154). Table 13 shows several areas lacking enough information regarding the wide impact of use of solid fuels, especially their health effects, and these areas could be worthwhile research projects. Given the study done in Spain by Orozco-Levy (83), further research on lung disease attributable to biomass smoke exposure should be performed in other developed countries. More information is needed on the relationships of health outcomes with measured pollutants produced by biomass fuel use (i.e., PM and CO). Because CO principally affects tissue oxygenation due to carboxyhemoglobin production, with consequent cardiovascular effects, particular attention should be devoted to PM with aerodynamic diameter less than 10 µm, which can penetrate the lower respiratory airways. Lacking specific thresholds for indoor air quality with concern to indoor PM, the American Society of Heating, Refrigerating, and Air-conditioning Engineers has adopted the standards suggested by the U.S. Environmental Protection Agency for outdoor air (PM10 = 150 µg/m3 for 24 h; PM2.5 = 35 and 15 µg/m3 for 24 h and 1 yr, respectively) (156). Because people spend most of their lives indoors, it is important to better define the time spent in specified indoor environments, to establish exposure standards specifically concerning long-term indoor exposure, and to quantitate the contribution and risk of concomitant presence of other important sources of indoor PM, such as environmental tobacco smoke.
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One priority is to increase awareness about the health effects of solid fuel smoke inhalation in physicians and health administrators, which may improve not only research but also preventive actions as well as diagnosis and treatment of affected patients. In developing countries, another priority is the evaluation of the local conditions and strategies to adopt massive interventions (fuels and stoves) to reduce exposure.
ACKNOWLEDGMENTS
The authors acknowledge the reviewers from the FIRS member societies: V. Theodore Barnett, Richard Beasley, Dan Gerardi, Yuh-Chin Tony Huang, Enrique Jolly, Steven M. Koenig, Ware G. Kuschner, María Victorina López, Holger Schuneman, and Marzia Simoni.
FOOTNOTES
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.
Conflict of Interest Statement: None of the authors has a financial relationship with a commercial entity that has an interest in the subject of this manuscript.
FIRS Working Group Participants: Kalpana Balakhrisnan, Sri Ramachandra Medical College and Research Institute, Porur, India; Nigel Bruce, Department of Public Health, University of Liverpool, Liverpool, UK; Majid Ezzati, Department of Population and International Health and Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts; Vijay Laxmi Pandey, Indira Gandhi Institute for Development Research, Mumbai, India; Darío Maldonado, Fundación Neumológica Colombiana, Bogotá, Colombia; Isabelle Romieu, Instituto Nacional de Salud Pública, Pan American Health Organization–PAHO, Cuernavaca, Mexico; Kirk Smith, Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley, California; Carlos Torres-Duque (former president, Latin American Thoracic Association), Fundación Neumológica Colombiana, Bogotá, Colombia; Giovanni Viegi (2005–2006 President European Respiratory Society and FIRS Leader), Pulmonary Environmental Epidemiology Unit, National Research Council (CNR) Institute of Clinical Physiology, Pisa, Italy.
(Received in original form July 17, 2007; accepted in final form April 3, 2008)
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