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518 Thorax 2000;55:518–532

Indoor air pollution in developing countries and
acute lower respiratory infections in children
Kirk R Smith, Jonathan M Samet, Isabelle Romieu, Nigel Bruce

Abstract Acute respiratory infection (ARI) is the most
Background—A critical review was con- common cause of illness in children and a
ducted of the quantitative literature link- major cause of death in the world. Among chil-
ing indoor air pollution from household dren under five years of age, three to five
use of biomass fuels with acute respira- million deaths annually have been attributed to
tory infections in young children, which is ARI, of which 75% are from pneumonia.1 The
focused on, but not confined to, acute World Health Organization estimates that
lower respiratory infection and pneumo- approximately three million children under five
nia in children under two years in less died from ARI in 1993, exclusive of measles,
developed countries. Biomass in the form pertussis, and diphtheria, and another 1.1 mil-
of wood, crop residues, and animal dung is lion died from conditions in association with
used in more than two fifths of the world’s these diseases (table 1).2 As shown in table 2,
households as the principal fuel. ARI is one of the leading causes of death in the
Methods—Medline and other electronic world, smaller only than heart disease, cancer,
databases were used, but it was also and cerebrovascular disease. In terms of lost
necessary to secure literature from col- healthy life years (measured as disability
leagues in less developed countries where adjusted life years, DALYs), however, table 2
not all publications are yet internationally shows that ARI is the chief cause of global ill
indexed. health today because its biggest impact is in
Results—The studies of indoor air pollu- young children.3 ARI is also a significant cause
tion from household biomass fuels are of death at other ages, particularly in the very
reasonably consistent and, as a group, old.
show a strong significant increase in risk Early in the 20th century ARI, in the form of
for exposed young children compared pneumonia, was also a major cause of death in
with those living in households using the currently developed countries, but its
cleaner fuels or being otherwise less importance diminished dramatically during the
exposed. Not all studies were able to adjust century, partly due to the development of vac-
for confounders, but most of those that did cines and antibiotics.4 A large decline had
so found that strong and significant risks already occurred before these medical inter-
remained. ventions became available, however, probably
Conclusions—It seems that the relative largely reflecting improvements in housing
risks are likely to be significant for the environments and nutrition.
exposures considered here. Since acute This report on indoor air pollution is part of
lower respiratory infection is the chief a series of reviews of the major determinants of
cause of death in children in less developed childhood pneumonia in developing countries
countries, and exacts a larger burden of that were initiated by the World Health
disease than any other disease category for Organization in association with the London
Environmental Health School of Hygiene and Tropical Medicine.5
Sciences, University of the world population, even small addi-
tional risks due to such a ubiquitous expo- There are a number of risk factors that aVect
California, Berkeley,
California 94720-7360, sure as air pollution have important public
USA Table 1 Annual mortality in children aged under five
health implications. In the case of indoor years from developing countries in 1993
K R Smith air pollution in households using biomass
Department of fuels, the risks also seem to be fairly ARI related: 4.1 million
strong, presumably because of the high ARI alone 3.0
Epidemiology, Johns ARI with measles 0.64
Hopkins University, daily concentrations of pollutants found in ARI with pertussis 0.26
Baltimore, Maryland, such settings and the large amount of time ARI with malaria or HIV 0.23
USA young children spend with their mothers Neonatal or perinatal 3.1 million
J M Samet (many involving ARI)
doing household cooking. Given the large Diarrhoea related: 3.0 million
Pan-American Health vulnerable populations at risk, there is an Diarrhoea alone 2.7
Diarrhoea with measles or HIV 0.27
Organization, Mexico urgent need to conduct randomised trials Measles/TB/tetanus/pertussis alone 1.2 million
City, Mexico to increase confidence in the cause-eVect Malaria alone 0.68 million
I Romieu relationship, to quantify the risk more Other 0.2 million
Total 12.2 million
precisely, to determine the degree of
Public Health
reduction in exposure required to signifi- ARI = acute respiratory infection.
Medicine, University Source: World Health Organization.2
of Liverpool, UK cantly improve health, and to establish the
Other ARI information:
N Bruce eVectiveness of interventions. ARI accounts for 33% of all deaths from infectious disease in the
(Thorax 2000;55:518–532) world and for 27% of the entire burden of infectious diseases.
Correspondence to: 80% of the ARI burden occurs in children under five years from
Dr K R Smith Keywords: acute respiratory infections; indoor air less developed countries, accounting for about 6.7% of the glo-
krksmith@uclink4.berkeley.edu pollution; biomass fuels; developing countries; children bal burden of disease from all causes.

2014 .6 exposures received to an agent. we concentrate on has been estimated to be dominated by house- pneumonia.10 Outdoor air smoking and outdoor air pollution from pollution has now been examined as a risk fac. perhaps Chen et al6 and Smith. When possible.9 Tuberculosis 2.2 0. rather.2 Malaria 2.3 are exposed to inhaled pollutants as they Cerebrovascular (stroke) 2.0 1. as well as in places where ambient about the contribution of household air pollu. total population exposure globally countries.7 accounting for about half of all fuels used daily to cook meals.5 9.12 15–17 polio.1 4. makes clear the health DALYs = disability adjusted life years. where solid fuels are used for cooking and sively address the sources and concentrations heating. and air pol.5 1.6 particles at levels that were previously consid- Diarrhoea 7. More details can be found in and coal are widely used globally.9 36. chilling.8 2.1 1. wood.5 significance for child health of exposures to air Malnutrition/anaemia (direct 3.3 1.2 4. the most polluted urban outdoor Early in the 20th century dramatic episodes of environments in the world are also in develop- outdoor air pollution in developed countries ing countries—notably.3 1.8 For example. the weights are proportional to the time Total (%) 72 73 64 Population (million) 5260 4120 1140 spent in each of these environments having Lost DALYs (million) 1380 1220 160 distinct pollutant concentrations.4 1. Infants and This review focuses on indoor exposures of young children as well as the elderly were noted the world’s children to pollution from combus- to be at higher risk than others and the tion of biomass fuels. but has been inconsistently related to res- levels have now declined in developed coun. including malnu.23–25 tion to the risk of ARI in young children world.bmj.4 8. pertussis.4 2.7 7.1 0.2 2.4 5.29–31 For example. Downloaded from thorax. In considering risk to health. an overview.2 0.3 1. exposure factors—that is. Those categories causing at least 1% of lost DALYs indicate adverse eVects on both respiratory World LDCs MDCs morbidity and mortality.26 thousand excess deaths occurred. this indoor young children are at risk for adverse pollutant has not been convincingly linked to eVects.8 11–14 Even though ambient pollution ARI. which causes the highest case hold environments in developing countries fatality rate. combustion of fossil fuels.1 2.2 2.6 cept of pollution exposure.4 1.9 breathe air in diverse indoor and outdoor loca- Motor vehicle accidents 2. (Companion reviews proportion of deaths attributed to respiratory have also been done on ARI risks to children causes was increased in comparison with the from indoor air pollution due to tobacco weeks before and after the fog. Using particulates as the indicator pollutant.2 2.3 environmental model.4 0. large populations tries.3 Perinatal eVects 6.003 personal exposure—which encompasses all Maternal 2.) The review does tor for respiratory morbidity and mortality in not address indoor air pollution by nitrogen numerous epidemiological studies and the evi.Published by group. levels are high.com Indoor air pollution in developing countries 519 Table 2 Global burden of death and diseases in 1990 tries.7 4. dung.21 Total personal exposure to War 1. tetanus. with particular focus on less developed for example.5 9.8 4.25 26 This is because of confluence of of indoor air pollutants in less developed coun. LDCs = less developed countries.3 Violence 1.8 3.22 This con- Deaths (million) 50. diphtheria) During the last two decades the potential Cancer 5.bmj.7 4.5 0. 5.com on September 7. new stud- ies are indicating adverse eVects of inhaled Acute respiratory infections 8.5 exposure measure.3 Chronic obstructive lung disease 2. which was due mainly to smoke tries are now static or declining while in the from coal burning household stoves.12 13 Indeed.4 2. in the course of examining the adjacent to frequently used devices with large strength of air pollution as a risk factor.1 2. total Congenital (birth defects) 2.27 From the standpoint of parti- Introduction to ARI and air pollution cle levels.3 1. wide.1 the locations and the medium—is the relevant Falls 1. of other diseases that aVect susceptibility. The depending on sources and time-activity pat- child’s environment also aVects risk through terns.1 0. lack of breast feeding. the epidemiological evidence continues to (%).008 in many urban areas.9 ered to be safe and are now frequently reached Child cluster (measles.4 2.6 0.8 0. during the London by developed countries but rates in these coun- fog of 1952.9 2.6 7 18–20 The world’s children Heart (ischaemic) 3. The review does not comprehen.26 28 Exposures to deaths and that children might be at particu.1 weighted average of the pollutant concentra- Alcohol (direct eVects) 1.7 Depression 4.2 8. exposures and the potential for widely varying contributions of indoor and outdoor exposures ARI rates in young children.1 0.9 several developing world they are growing steadily.2 5. Crop residues.7 an air pollutant can be estimated as the Suicide 1. to total personal exposures for children living trition. It emphasises that one must be sure to such factors as crowding. environmental tobacco smoke (ETS) track larly increased risk during the times of high tobacco consumption.5 time. termed the micro- Source: Murray and Lopez.3 2.0 tions in the environments where a child spends Drowning 1. this has been dominated pollution. examine pollution where the people spend lution. piratory symptoms. This review explores what is known most time. regardless of Sexually transmitted w/HIV 2. in showed that air pollution could cause excess the coal using cities of Asia.5 10. but not exclusively. a cohort .4 tions. it oVers emission factors. dioxide from cooking stoves and space heaters.0 13. MDCs = more relevance of both indoor and outdoor pollution developed countries.5 2. and the incidence in diVerent countries throughout the world.9 pollutants in indoor environments has also eVects) been recognised. dence continues to indicate that infants and In spite of intense investigation.

40 The complex worldwide there are no uniformly accepted cri. ALRI include severe ARI hyperplasia. epithelial cell therapy at home. developed. For ARI comprise a set of clinical conditions of example. there is a suY- tory illness during the first 18 months of life cient basis of understanding of the toxicologi- found no evidence of increased risk with cal properties of these mixtures to conclude exposure. sel exhaust has been related to chronic inflam- ally be treated successfully with supportive mation of the respiratory tract. pul- involving infection of the lungs.com 520 Smith. alveolar macrophages. specific host defences of the respiratory tract then infections might become more severe as against pathogens (table 3). the particulate phase of cigarette various aetiologies and severities that are smoke and gas phase components adversely generally divided into two main forms: upper aVect ciliary function in in vitro models. The increased severity might be treated with antimicrobial therapy. et al Table 3 Host defences against respiratory infections spective. On the other hand. and even to increase morbidity and stridor. monary fibrosis. severe ARI. acrolein. fibronectin been characterised to some extent. Romieu. Samet. URI can usu.42 infections are most commonly caused by Exposure to air pollutants might also act to bacteria. increased combination of the following symptoms: cough bronchoalveolar permeability. Most housing in developed coun- phages. inflammation. mixture of sulphur dioxide and particulates teria and the definitions in use are not fully may reduce the eYcacy of host defences consistent. cell impact of indoor emissions on air quality mediated immunity is required to kill organ. For research and case management against microbial agents and respiratory tract under field conditions in less developed coun. exposure of animals to wood smoke signifi- cytosis promoting components of the epithelial cantly altered both the local and systemic lining fluid. The chemical and + Secretory IgA physical characteristics of these mixtures have + Surfactant + Opsonising IgG. of the space.35 face of the tracheobronchial tree caused by the Air pollutants could increase the incidence irritant pollutants. phago.bmj. Severe ALRI caused by bacteria are mortality. cyanides. although they may sometimes be increase the severity of respiratory infections viral.36 The non-specific the infecting organisms further damage already mechanisms include filtration and removal of inflamed and possibly narrowed airways. low emission rates in such housing can result in . Gase- respiratory tract infections (URI) and lower ous components that appear to be important respiratory tract infections (ALRI). and to impair with or without fever. is highest in aldehydes. impaired alveolar clearance.34 Serious function. If sustained exposure to air of ARI by adversely aVecting specific and non. without mediated by inflammation of the epithelial sur- which they can sometimes be fatal. tries lies at temperate latitudes and has relatively Smoke from household solid fuels is a com. plex mixture which contains many potentially typically one air change per hour or less. and phagocytosis and killing of immune response associated with bacterial infecting organisms by cells in the airways and infection. and acids.13 Ozone has been shown to tries the WHO defines URI to include any cause respiratory tract inflammation. The specific mecha- nisms involve various components of humoral INDOOR AIR POLLUTION and cellular immunity. Clinical signs of ALRI include any of the and thereby increase the proportion of illnesses above symptoms of URI with the addition of considered clinically to involve the lower respi- rapid breathing and/or chest indrawing and/or ratory tract.32 Ackermann-Liebrich and Rap33 that they could plausibly increase the risk of have recently reviewed the evidence on indoor ARI. blocked or runny nose. + Polymorphonuclear leucocytes + Plasma components Thus. which can be fatal. Re- particles by the upper airway. Clinical gen dioxide has been shown to adversely aVect and epidemiological criteria are available for both the mucociliary apparatus and humoral separating URI from ALRI but. and/or ear discharge. with pneumo. ketones.41 In animal studies die- sore throat.bmj. and compromised pulmonary nia being the most serious form. Thomas and ZelikoV43 have shown that apparatus of the trachea and bronchi. time since genera- + Mucociliary clearance tion. pollutants produces chronic inflammation. the mucociliary cently.44 Even relevant components from a toxicologic per. unfortunately. exposure to nitrogen dioxide. ammonia. A number of pollutants commonly found in indoor and outdoor air have been shown to adversely aVect components of the defence A brief discussion of mechanisms mechanisms against infectious organisms. The risk of include nitrogen dioxide. depends directly on ventilation and air mixing isms capable of living within alveolar macro. Downloaded from thorax.Published by group. low exchange rates of indoor with outdoor air. and other factors. only generalisations can be oVered con- + Vasoactive mediators cerning mechanisms by which particular air pollutants could increase the risk for ARI and Based on Reynolds and Elias. materials burned. and cellular immune defences. macrophage functions.com on September 7. the immunoglobulins promote phagocytosis. Organism specific In addition to the strength of sources.39 Nitro- very young children and in the elderly. 2014 .36 mixture-specific arguments cannot readily be study of nitrogen dioxide exposure and respira. These mixtures are inherently highly variable with characteristics determined by + Anatomical barriers + Angulation of airways sources.7 37 38 par- + Complement ticularly in the form of wood smoke from metal + Alveolar macrophages heating stoves used in developed countries.

8 that may adversely aVect health.7 47 Biomass fuel smoke gas from the ground beneath a home may con. Dung Crop Wood Kerosene Gas Electricity residues gas stoves have been the most common indoor pollution source of concern in studies in devel- Figure 1 Emissions along the household fuel ladder. and indoor concentrations Solid fuels (biomass and coal) and associated exposures can be high as a Figure 2 World distribution of household fuel use.2 insects. Strong sources can be exposed to smoke from coal fuels burned in readily identified in developing countries. nitrogen and proper conditions. optimum conditions for complete environmental tobacco smoke (ETS). viruses. which also have high emission ever. one of the cleaner biofuels. and Oceania. A wide combustion are diYcult to create with inexpen- variety of semi-volatile and volatile organic sive household devices.6 many biological agents in indoor environments 35 PM10 including. The next rungs in the sequence are crop residues. and pollutants generated by biological generally contain few intrinsic contaminants processes. and chemical products.45 The principal combustion pollut. biomass fuels gas. In general. and charcoal.2 sources. the bulk of the emissions is released into the living area. although the blends of compounds in the ings. unvented space heating houses in developing countries. The first non- India biomass fuel on the ladder is kerosene or coal.4 1.46 On the lowest rungs are dried animal dung and scavenged twigs and grass as cooking fuels (fig Subsaharan Africa 1). and ash) and. Such complex mixtures are ucts. Africa. cleanliness. In addition. Reproduced with permission from result. The and unstable mixture. Un- by tobacco smoking has been referred to as fortunately. After tobacco smoking. and bottled and piped gases and electricity are South-east Asia and Islands highest. furnish. 30 1. Latin America the world and are often open to the outdoors. (sulphur. and dung) and coal burning for cooking and Incomplete combustion of unprocessed solid heating. For combustion 5 0.com on September 7. sometimes called the energy ladder. crop residues.20 In the global context. it is likely that the relative 0. how- simple stoves. each successive rung on this ladder is associated with increases in the tech- nology of the cooking system. biomass fuels or coal (fig 2).com Indoor air pollution in developing countries 521 40 1. produced by burning of both coal and biomass pounds released by building materials. the focus of this review.38 ever. Ventilation rates for (fig 1).0 20 unavailable. and bacteria.8 15 importance of the four types of indoor air pol- 0. including biomass (wood.Published by group.25 Large populations in China are are likely to be greater.4 and level of development. they can be burned without sulphur oxides. trace metals. rates.bmj. North Africa and Middle East Biomass fuel Nearly half the world’s households are thought Latin America and Caribbean to cook daily with unprocessed solid fuels— that is. fuels produces hundreds of chemical com- Indoor pollutants can be grouped by source pounds under the operating conditions of sim- into four principal classes: combustion prod. eY- China ciency. the pollutant emission rates for such fuels are also high. wood. compounds can be found in indoor air. There are CO 1.27 using wood. releases other than the products of complete The complex mixture in indoor air produced combustion (carbon dioxide and water).bmj. 2014 . some generali- 0 0 sations can be made. ple cooking stoves.6 lution varies throughout the world with climate 10 0. Unlike coal. there Smoke from cooking stoves is a complicated are diverse sources of these compounds. Compared with gas stoves.7 Although rates of Established Market Economies exchange of indoor with outdoor air are relatively high in most housing in developing Non-solid fuel countries. Reproduced with permission from oped countries. In a significant proportion of the households using Former Soviet Union and East Europe biomass fuels. semi-volatile and volatile organic com. and cost. 25 Although systematically collected data are g/meal g/meal 1. pollutants in soil smokes are diVerent. Downloaded from thorax. for example. gas stoves are near the upper end of a his- Population in 1990 (million) torical evolution in the quality of household 0 200 400 600 800 1000 1200 fuels. how- Smith et al. particles. pollens and moulds. under ants include carbon monoxide. contains significant quantities of several pollut- tain pollutants such as radon and termidicides ants for which many countries have set outdoor . can indoor pollutant concentrations at levels of release 50 times more pollution during cooking public health significance. and volatile organics. which lie with biomass fuels is common in much of primarily in tropical and subtropical regions of South Asia and in the highland areas of devel- oping countries of Asia. even stoves Reddy et al. fuels.

the number of people exposed at benzene. Samet. and nitro.7 m to ceiling) 390 4000–21 000 Menon108 Nepal 1986 Cooking . et al Table 4 Indoor air pollution from biofuel combustion in developing countries Particulate concentration Location and year Description n (µg/m3) Reference Kitchen area concentration Papua New Guinea 1968 Overnight at floor level 9 200–4900 Cleary & Blackburn101 1974 Overnight at sitting level 6 200–9000 Anderson102 Kenya 1971–72 Overnight . Area concentrations are measured with stationary instruments placed indoors at breathing height.bmj. either total (TSP) or respirable. greater than from ambient pollution. unfortunately. the aerosol contains tions indoors.winter 95 6800 Saksena et al113 .25 the findings of studies from diVerent parts of the world provide an indication of typical EPIDEMIOLOGY indoor concentrations of the major pollutants. hydrocarbons. 2014 . Some of the studies listed here also measured other pollutants.charcoal 10 5500 1988 Cooking (0. There is ample evidence that particles are gen. as well as nitrogen and sulfur oxides and formaldehyde. Downloaded from thorax. nevertheless. or combustion characteristics. cities. with far more time spent indoors than erally of the small sizes thought to be most outdoors.49 air quality standards—for example. not to be exceeded more than once per year. are fairly consistent. there was no control group of infants.49 and Smith. The unacceptable levels indoors is expected to rival composition of the smoke varies with even or exceed the number exposed to unacceptable minor changes in fuel quality. standards. significant extent and fuel burning indoors may kerosene.52 Extremely high mean levels of vari- can we readily apportion the contributions to ous gaseous pollutants were measured and a total personal exposure of indoor and outdoor mean exposure time of 3.com on September 7. and polyaromatic hydrocarbons. particles. Exposure rates were measured with instruments worn by the cook during food preparation. For comparisons.1 hours per day was sources. carbon tion.bmj.wood 22 15 800 Aggarwal et al106 . Modified from Pandey et al. recognised standards for pollutant concentra- gen oxides. Additionally.lowlands 3 300–1500 CliVord104 1988 24 hours 64 1200–1900 (RSP) Boleij et al105 India 1982 15 min cooking . the diVerences in outdoor pollution penetrates indoors to a exposure levels among households using wood. suggests that the total global dose damaging to health. The first report in the biomedical literature WHO recommendations.wood ? 2600 (RSP) Mumford et al110 The Gambia 1988 24 hours 36 1000–2500 (RSP) Boleij et al105 Exposures during cooking (2–5 hours per day) India 1983 4 villages 65 6800 Smith et al111 1987 8 villages 165 3700 Ramakrishna et al66 1987 2 villages 44 3600 Ramakrishna112 1988 5 villages 129 4700 Menon108 1991 3 villages . to describe an association between indoor centrations typical of the most polluted of cooking smoke and childhood pneumonia in cities. which were found in concentrations roughly equal to the high end of those measured in indoor developed country conditions.com 522 Smith. has been 260 µg/m3 and the Japanese one-hour standard is 200 µg/m3. b Cooks’ exposures measure before and after introduction of improved stoves. coal. cooking stove ambient concentrations in all of the world’s configuration. including carbon monoxide and benzo(a)pyrene.after 20 3000 (RSP) a Approximately half “improved cookstoves”.highlands 5 2700–7900 Hofmann & Wynder103 . Furthermore. In addition. these indoor levels are dramatically high. there are no internationally monoxide. nor Hospital. developing countries reported measurements We cannot presently derive an accurate esti.Published by group. and gas were not reported and be a prominent contributor to outdoor pollu. the US 24-hour standard. Assuming that indoor standards many organic compounds considered to be should be at least as stringent as outdoor toxic or carcinogenic. or even outdoor con. such as formaldehyde.beforeb 20 8200 (RSP) Pandey et al115 . (For an annotated bibliography of ARI and Table 4 lists studies that have measured indoor air quality (non-ETS) see McCracken particles. Romieu. of indoor pollution levels in the homes of mate of the total population in developing infants diagnosed with bronchiolitis and bron- countries exposed to indoor concentrations chopneumonia at Lagos University Teaching that would be considered unacceptable.monsoon 4800 Nepal a 1986 2 villages 49 2000 Reid et al114 1990 1 village . which were sometimes found in concentra- tions well above those found in public settings in developed countries. in some rural areas estimated but.50 Consideration of time-activity patterns. It is thus . The studies are not completely comparable because of diVerent measurement protocols and equipment but.51) Compared with various national standards.7 48 equivalent (amount actually inhaled) for in- Although a large scale worldwide survey of door pollution could be an order of magnitude smoke concentrations has not been conducted.dung 32 18 300 Patel et al107 .wood (geometric mean) 17 4700 Davidson et al109 China 1987 All day .summer 5400 .

75 For focused attention in this review we were 1. (Nepal53) were consistent with larger relative Exposure to household smoke pollution was risks for more severe disease.9 2–3.9 1–1.com on September 7.bmj. 2.0 cussed below. (B) Based on three months data in late 1984 and early 1985 in same exposures to biomass fuel smoke. Reproduced with marises the results of these 15 studies. but few details were 50% of children with symptoms and signs of provided.00 relationship between exposure to household 0. carriage on confirmed ALRI.57 however.00 case selection reasonably corresponded to 0–0. Figure 3 Acute respiratory infections (ARI) and exposure although confirmed by diVerent means. Bar 1 = Moderate cases (grade II) These 15 studies are chosen for particular Bar 2 = Severe cases (grades III & IV) attention because they address actual ALRI. 2014 .9 4+ established WHO or other authoritative crite. used maternally reported time spent Incidence of ALRI in young children of developing near the cooking stove as a categorical exposure countries measure in exploring the dose-response rela- Outcome measures diVered among the 13 tionship of exposure to smoke with lower studies (table 5).bmj. In addition.3 1. or by ver. bia suggested that conditions were not favour- tory rate and assessing for chest indrawing and able for detecting a relationship between signs of cardiorespiratory failure.9 2–3. were too small to exclude chance as an Broadly.6 however. (A) Based on six months data children under five years old and involve indoor in about 250 infants in early 1984. Only one and the one prospective case-control study55 study actually measured pollutant levels and used reported shortness of breath to screen for only in a subset of study households. O’Dempsey concentrations of pollutants and lower respira- et al55 confirmed cases by laboratory tests and tory disease in children because of the radiography.57 behav- addressing respiratory symptoms but not ioural practices—for example. 0 Only one dealt with case fatality and the others 0–0. or bronchiolitis factory because of the diYculty of controlling diagnosed clinically or according to WHO rec. or not providing enough mother’s back while cooking53 55 56 58–61—or information to calculate odds ratios. All but one of the eight morbidity studies bal autopsy. and Nepal. 2.00 1. These outcome measures would finding significant associations were in Africa. Argentina. that the protocols in these 13 studies have been suYciently rigorous to warrant 0. 0. tend to include children with more severe The data in the one non-African study illness. Downloaded from thorax. are not examined in detail here of the outcome measure with cooking practices because they only meet some of the criteria— such as use of an open wood fire compared for example. but proved unsatis- nia.62–64 Pandey et al. population but with separate teams diagnosing ARI and ciently quantitative to allow calculation of odds determining smoke exposure. Two of the cohort studies53 54 respiratory disease in children (fig 3). in to biomass smoke in Nepal. presence of sources. The Air pollution studies in Kenya and the Gam- first two assessed severity by counting respira. for time since exposure. have not been entirely consistent among the studies. Nine were conducted in Africa and one each in India.57 children with lower respiratory disease.75 biomass smoke and ALRI in young children in 0.56 The remaining moglobin as a marker of smoke exposure was studies were based on children with pneumo. severe wheezy bronchitis. The possibility of using carboxyhae- lower respiratory disease. Age specific data available in the .57 ommendations in a hospital setting.4 ria in use at the time the study was done. but the numbers also assessed using diVerent approaches. In an expanded study of the same cooking in households of 20 children with region in the Gambia studied by Campbell et lower respiratory disease and 20 with upper al54 pneumonia was confirmed radiologically in respiratory disease.9 1–1.1 pool.50 able to identify 13 more recently published 1.25 0. we found two Reported hours per day near stove studies from a developed country (USA) of the Line = Mild cases (grade I) relationship between household wood smoke and ALRI among Navaho children (table 6). with cleaner fuels such as kerosene. diVerence in levels of total particles during respectively). 2. also explored in one study. although discussed briefly below.25 Episodes per infant the incidence of pneumonia. addressing risks to older children. as dis. severe cases are significant in both studies. Brazil.50 A about the relationship between exposure and 2. the studies examined the relationship explanation.25 studies which quantitatively addressed the 1.53 Some related studies.65 for moderate and severe lower respiratory Collings et al. found a significant infections (grade II and grade III/IV ARI.2 treating them as part of the same evidence 0.com Indoor air pollution in developing countries 523 diYcult to draw any quantitative conclusions 2. Table 7 sum. Each is suY. Pandey et al53 presented analyses homogeneity of levels among households. Such B Episodes per infant criteria have evolved over time and thus. Trends for moderate and ratios and confidence intervals. permission from Pandey et al. It is our judgement.53 for example.9 4+ dealt with morbidity.50 developing countries (table 5) in which ALRI 0.Published by group.

Cases: Hospitalised for ALRI Interview None Age. n=103+103. and residence.6) Natal (Kossove)58 132 cases. Outpatient cases: Wheezing. Controls: Non-respiratory = 33% + economic status was small.bmj.9 and Campbell)56 cooking + crowding back quite a distinct behaviour so (1. In study 1. Samet. TSP means: ALRI cooking): 20 ALRI and 20 + school age sibs (n=18) 1915 µg/m3 AURI (n=15) 546 AURI cases 73% exposed + paternal occupation not adjusted µg/m3 to open fire Rural Gambia (?) Upper Cohort. x ray.8 (1. ETS not significant for 2. date of either cooking in outpatients visit. 2014 . crowding.com Ibadan (Johnson and 0–59 months (croup. (a) Questionnaire on Questionnaire: Confounding: only diVerence was 2. of clinic visits Adjusted in MLR Urban Nigeria (1985–86) Case control. but success of matching verified. bronchiolitis. same team asked about exposure and ARI > possible bias 77% exposed over 1 hour Rural Gambia (1987–88) Cohort. of health centre visits + ethnic group + maternal education + other Urban. Exposure assessment was problems Examined. 455 (study 2) grades I–IV (Goroka) hours per day the child confounding not taken into account Exposure assessment not validated (Pandey et al)53 Breathlessness near fireplace.1 to 34.bmj.0 + sharing bedroom misclassification (1. ETS. 0–12 months. 0–35 months.4) for Buenos Aires (Cerqueiro et Cases: 516 inpatients.com on September 7.4 to 3.6 (1. but not al)57 Local well baby clinic woodsmoke (b) COHb + overcrowding adjusted.5–2. 0–59 months Three hospitals: Cases: ALRI Interview with mother: None.0) for any vaccination. of wives + no. age and sex matched. et al .0) Kathmandu Valley (study 1). 0–11 months. Rural Zimbabwe (?) Case control.3) Marondera (Collings et 244 cases.2 (1. and gas) biolab workup. Control group x ray.3 to 6.1) Basse (Campbell et al)54 history of “diYculty with on the mother’s back + birth interval factor. Argentina (1984–87) Case-control. No data available re charcoal heating in 9.Table 5 Biomass fuel use and ALRI in children under 5 in developing countries 524 Study Design Case definition Exposure Confounding adjusted Comments OR (95% CI) Rural South Africa (1980) Case control.2) F: 1.6 to 3. Chimney charcoal heat for inpatients al)67 outpatients. matched by age. COHb not diVerent between (all) (c) TSP (2 h during + housing conditions ALRI and AURI. nutritional status. breathing” over subsequent 3 Prevalence = 37% + parental ETS ability to deal with confounding.0 to 3.5 (0.9 (1. 18 controls bronchiolitis & ALRI. 0–23 months. based on clinical. Clinical + in the smoke?” Prevalence + number of siblings pneumonic changes. not adjusted vague. and to month period + crowding establish causation where exposure and + socioeconomic score incidence high + nutritional indicators + vaccination status + no. 280 Weekly surveillance. Report carriage on M: 0.2 (1. Romieu. Asked: “Does the child stay Routine data collection: Only 63% of 123 x rayed had 4. significant. Controls: infant welfare clinic.3 to 2.2) + vitamin A intake + no. nutritional status. Cautious about interpretation. 780 Two-weekly home visits: ARI Asked mothers for average Since homes were “homogeneous” Dose response relationship found 2. fuel.8 (1. kerosene.2 to 1.8 to 31. 500 controls clinical and x ray.5 (0. heating with any underway” smoke nearby found to be associated 1. cooking of patients.7 to 13. empyema thoracis) at home (wood. 500 Weekly home visits: ALRI Questionnaire: Carriage on Questionnaire: Boy/girl diVerence could be due to Approach (1) (all episodes) River Division (Armstrong (approx.2 (1. no respiratory disease Smith. Controls: 669 Controls: well baby clinic or charcoal. NS Downloaded from thorax.9) + socioeconomic index should define the two groups fairly Approach (2) (1st episode) + number of siblings clearly with low level of M: 0. Type of cooking fuel used and location of cooking area also not Aderele)62 pneumonia. Controls: cooking/exposure to + maternal ETS number of school age sibs.7) with ARLI in both kinds heating fuel in inpatients sex.2 to 3.9) for gas socioeconomic level. 0–59 months.Published by group. Mother’s Reported carriage of child Adjusted for Father’s ETS only other significant 2.3) F: 6. Rural Nepal (1984–85) Cohort. Hospital: Cases: Hosp ALRI.) clinical and x ray mother’s back while + parental ETS greater exposure. bottled gas for (OR 2. 153 within previous 12 days Household heating by Multivariate analysis “currently outpatient households.2 to 1.

0 (1. This list is confined to quantitative studies that have used internationally standardised criteria for diagnosing ALRI. Poor nutrition exposed to kerosene and gas = 3) (1. and nutrition indicators plus ever visited welfare clinic OR = 0. Exposure assessment + education was vague and invalidated + birth weight etc.9) for cases vs. + other children in hh representative of other settings in (0. parental logistic regression was whether child 270 live controls group. physician diagnosed pneumonia ETS OR = 3. Village. age. of ALRI with other diseases (e. No diVerence in source of treatment by location where child sleeps. low income (1. 0–59 months respiratory rate. deaths (e. There are additional studies that have noted a relationship with various respiratory symptoms including cough. Adjusted in MLR Rural Gambia (1989–1991) Prospective case-control. and while cooking. and sore throat—for example.5 (1. 2. neighbourhood of cases. Attending clinic. and non-pneumonia deaths all had same significant risk factors. + Any source of indoor + housing quality good access to health care. Hospital: Cases: Admitted for History taken. wood = 16.1×) were more frequent in wood burning homes. Downloaded from thorax.bmj.0005) for those Ibadan (Johnson and months ALRI patients (see above) Type of cooking fuel used deaths were from wood burning homes. and immunisation + socioeconomic conditions were significant. Urban population with relatively 1. No eVect of bednets.Published by group. (Shah et al)63 definition).bmj. Yet paternal income. season of death. and ETS. live controls: Adjusted for Only other significant risk factor 5. whether mother alone distances from road. transported to Mother carries child while child’s weight slope. fireplaces) + income/education developing countries + Usually in kitchen while + day centre attendance cooking + history of respiratory illness + (other) Hierarchical model/MLR Urban and rural India (1991) Case control. one additional death had partial compared with those gas = 5. as the controls have (0. the study in Lucknow.8 (1.06 to 0. with + smokers in house increased severity. No significant factors (0.com (O’Dempsey et al)55 Medical Research Council where cooking significant illness in last six months. 4. Cases: ALRI admitted to Trained field worker Interview: Only 6% of children exposed to indoor Indoor smoke: 1. Aetiological after lab tests and x ray.97 neighborhood smoke (open fires.1 to 8. paternal occupation. recent illness.4 for other deaths months ALRI were excluded measles). Maternal education.3 for pneumonia Controls = 1160 0–59 (40 of 76 villages). On MLR. n=103. clinical and X-ray. by age May be reverse causality. dead controls. noisy respiration. ETS rates were similar. runny nose. Division (de Francisco et Cases: 129 ALRI deaths by 2 of 3 physicians.g. 2014 . 0–23 months. maternal education. 2.46 to 1.2 (1. Urban Brazil (1990) Porto Case control. confusion with malaria) is possible reason for lack of significant diVerence between cases and dead controls. interview: + cigarettes smoked smoke. 0–59 Cases: Death in hospital among Interview None Overall case fatality rate = 7.26) woodstoves. Models with all Indoor air pollution in developing countries deaths. age of weaning. Perhaps confusion cooking. and nutritional status. ethnic of stove.6) Upper River Division n=80+159.43). 5 of 8 12. No tendency to be diVerent for sleeping in room with (Mtango et al)60 Other deaths = 456 Controls: Multistage sampling where cooking is done child eating habit. About 95% of all groups cook with All deaths: 2.9 (5. and parental education. sex. other exposure to wood smoke.7 to 15.75 to 1. low maternal literacy (2. i. crowding. India by Awasthi et al68 which is discussed in the text. water source. Children with + Cook with wood decides treatment. only age. + Child sleeps in room maternal education. parity. ETS.e. ETS not related to case fatality rate Rural Tanzania (1986–87) Case-control Cases: Verbal autopsy certified by Household interview. not significant Rural Gambia Upper River Case-control Cases: Verbal autopsy confirmed Indoor air pollution index Cases vs. Cases: if high Household questionnaire: Adjusted for mother’s income.com on September 7. pneumonia deaths.98) Controls: Age matched.3) Bagamoyo District Cases: ALRI deaths = 154 physician of all deaths in period.36) Misclassification of ALRI for cases vs. Water not from tap had OR = 11. 2–60 months.g. Controls: (preventive) fraction for eliminating selected randomly from maternal carriage while cooking = 39%. wood. carrying of child socioeconomic score. including History: This is a study of the risk factors for “Smokeless” stove: 0. household crowding.2 (p<0. Controls: Outpatients “smokeless” category + number of siblings ARI (non-severe). only. Not Usually in the kitchen: 0.7). with non-severe ARI + outdoor pollution + house characteristics sharing a bedroom.8%.5×). sick children being more likely to be carried.5 to 25. Controls: based on location and type significant factors in univariate analysis: remaining after multiple conditional live controls al)61 Controls: 144 other deaths Matched by age.82 South Kerala-Trivandrum 400 total severe/very severe ARI (WHO + type of stove.Urban Nigeria (1985–86) Case fatality.61 to Alegre (Victora et al)64 510 cases. matched for eliminating ETS in house = 31%. crowding. questionnaire respondent.0 to 6. exposed to wood smoke Aderele)62 at home (79 = kerosene.8×).1). wealth.8 to 4. 525 .14 0–23 months geographic area ETS (details not provided) maternal education. crowding. 510 controls hospital. religion. and parental ETS.1 (0.

Primary energy source asthma. and house type not significant.9 to 57) Controls: Age-sex + diYculty of variance. Gambia (2). Inadequate control diVered. 1. in the study of Zulu chil. No eVect conditions + house type for coal use or wood for heating. India. this scenario is quite was much higher in cases.com on September 7. breast feeding patterns and socioeconomic status of cases and controls proaches (tables 6 and 7). recent chimneys but exposure Arizona. but were just as likely as others to bring also occur in prospective studies when collec. Cohort studies (n = 4) however. Arizona. . Samet. Median PM10 matched. though the from the clinics. although such bias can care. dirt floor.0 USA (Robin et al)70 pneumonia levels (5 pm–8 am) + electricity only explained 10% of (0. In principle.bmj. disease only other factor Controls: Age-sex presence of remaining significant (OR matched. Nepal study did not show greater eVects in Bias in case-control studies from diVerential use of infants than during the second year of life.57 58 62 This source 1 not significant Odds ratios = 2. lack of run- Odds ratio = 4.6 to 43) Defiance. Navaho reservation Case-control Hospital: Interview: cook with Interview No variation in PM10 levels Cook with wood (1993) Fort 1–24 months Cases: ALRI.0 completed routine immunisation. developing countries In practice it is diYcult to assess whether this bias has contributed to the risk estimates in the Case-control studies (n = 9) studies quoted since care seeking has not been (South Africa. or from other constraints associated child to smoke (determined by questionnaire) with poverty. Romieu. services for serious paediatric illnesses. whose children were more heavily exposed to Other possible sources of bias include indoor air pollution were less likely than others misclassification of exposure through recall to bring their children to these services when bias. In a health services detailed analysis of data from the Gambia. for heating and exposure to levels not validated.9) (1988) Tuba City. Nigeria. DiVerential use of health services could Armstrong and Campbell56 found that the risk introduce bias if the subjects who use health of pneumonia in association with smoke expo. since the use of open trols were less sick. This approach to control fires and biomass fuels is associated with selection could introduce bias if caretakers poverty and associated risk factors for ALRI. Other studies have just looked at the relationship of wood burning with respiratory symptoms.8 ning water) were poorer among cases. Kenya. n=45+45 bronchiolitis. this list is confined to those quantitative studies using standardised protocols for determining ALRI.bmj. In studies variably considered potential con. but not sure was increased in girls but not in boys. however. well child running water. not the others.8–7.Published by group.2–6. From information available on 3 not significant Odds ratios = 2. etc. wood + children/hh with ETS. Humidifiers.2–9. one of the case-control studies from Africa. 1998).g. Type of cooking/heating PM >65 µg/m3 7. Measured 15 h PM10 + running water etc. there appears to be little diVerence (Nepal. This would tion of exposure data follows the occurrence of result in heavily exposed children being under- illness.116 clinic was likely to represent the population. but founding in their design and analytical ap. are also authors suggested that this diVerence resulted those who use unprocessed biomass fuels for from greater exposure of females and not from cooking and who take no measures to avoid biological diVerences between the sexes. e. Honicky et al. ETS. Case-control studies are more likely to be they were only mildly unwell or for preventive subject to recall bias. 22 not for other + ETS µg/m3 (controls). possible since those households with the high- est exposures are also those most likely to be Table 7 Summary of studies of ALRI in young children and indoor biomass smoke in poor. with less access to transport.0 (0. Tanzania. The for mild illnesses or preventive care. The exposing their young children to the smoke.72 and Browning et al73 which are discussed in the text. 5. et al Table 6 Wood burning and ALRI in children under five in developed countries Confounding Study Design Case definition Exposure adjusted Comments OR (95% CI) Navaho reservation Case-control Hospital: Interview: Family history of Wood burning stoves with 4.9 socioeconomic circumstances in three studies. crowding. Downloaded from thorax. USA n=58+58 bronchiolitis. pets. Recent (Morris et al)69 pneumonia clinical cooking respiratory exposure to respiratory and x ray disease. inability to aVord the cost of proportion of women reporting exposure of the transport. For example. It was Developed countries (n = 2) (USA (2)) reported. sought care transport to clinic levels 24 µg/m3 (cases). Gambia (2)) 2 adjusted for confounders n=910 between cases and controls. 0–24 months Cases: ALRI.8 (1.7 to 12. Brazil.4) after multivariate clinic analysis. represented in the control groups and bias of dren in Natal by Kossove58 the reported the odds ratio away from unity. Zimbabwe.57 In the case-control study by of confounding is likely to result in an overesti- Kossove58 it is not clear whether the clinic con- mate of the odds ratios. but sample sizes small As in table 5. Argentina) 6 adjusted for confounders n=4311 studied directly. type of home. their children when seriously ill. 2014 . that over 90% of children Case-control n=206 born in the catchment area of the hospital Adjusted for confounders Odds ratios = 4.com 526 Smith. suggesting The dividing line between developed and developing countries = $1000 per capita purchasing that the control sample from the well baby power in 1995 (UNDP. This situation duration of smoke exposure was remarkably could arise due to distance of such households similar in cases and controls.0 of bias was discussed by Morris et al69 as in their Case-fatality study (n = 1) (Nigeria) study there was some evidence that socioeco- Hospitalised patients n=103 nomic circumstances (dirt floor.71 Butterfield et al.

com on September 7. 95% CI 1. a significant association of socioeconomic status and district of residence.bmj. crowding nor smoking were related to case sive case definition was an observational study fatality rates. but Mortality from pneumonia in developing countries did find a strong relationship of fuel type with An association between exposure to household case fatality. The loca.01.64 The case-control study however.Published by group. 1. 95% CI 1.62 Although a case-control study in the A study of ARI in infants aged less than one year in India.7 to 2.com Indoor air pollution in developing countries 527 The study by Shah et al63 provided limited associated with respiratory symptoms in this information on socioeconomic circumstances study. or noisy respiration.53 As 95% CI 1. With fortnightly queiro et al67 matched on five factors including household visits.6 (coal). months in the same area. India. life threatening ALRI.00 to 1. found between type of cooking fuel and hospital somewhat conflicting results in urban slum admissions for ALRI. India the measure of exposure was a A large national household survey in India question about the existence of a “smokeless” found a statistically significant relationship stove (with a flue) at home. 95% The study by Cerqueiro et al67 found a large CI 1. sex.2 times (p<0.3) between reported use of household however. sore throat. income.bmj. Downloaded from thorax.4 to 5. 95% CI 1. after multivariate analysis. gas (rather than electricity) also produced a related to evidence of uncollected refuse significant odds ratio (2.4) were also significantly associ- odds ratio (9. incidence of pneumonia and mortality. such stoves in India often do not biomass fuel and reported incidence of respira- actually lower indoor air pollution levels. No pollution measurements were reported Jakarta found that. weight.0.1 to 1.76 Kerala. and other factors often addressed only 1. (OR 1. or wood were not concern.7. Another study not qualify. although respiratory symp- and little information was provided about the type of stove and fuel involved. no multivariate of 650 randomly chosen pre-school children analysis was reported and the case sample size aged 1–59 months in Lucknow.2. it appears that this bias was probably found with outdoor TSP measurements. Somewhat diVerent results were ob- for cases and controls. they were not It is intriguing to note that the three studies related to the type of cooking fuel used. Even though wood burning outdoor “neighbourhood” pollution from the homes were characterised as a group by poorer cooking stoves themselves and other neigh.9). and less bourhood sources.77 Since the survey did not prevalence of household cooking with wood distinguish cases by ALRI. URI.6). 2014 . found no significant association of ALRI mor- bidity with reported type of household fuel. neither these factors nor ing for inclusion in table 5 because of its inclu. kerosene. although without specific information the solid fuels (ORs 1. nutritional status. and in any case did not tained in the previously discussed six month report an increased odds ratio for smoke expo. nutritional significantly related to the use of dung fuel (OR status. maternal literacy.74 which did not qualify for table 5 same hospital did not reveal a relationship because of its broad definition of ALRI. lower income. of whom were found to have respiratory disease Morbidity studies indicate that smoke pollu- as defined by runny nose. the impact of the refuse may be a result of the mation about family behaviour patterns. cough.0005) more likely to die than possibly due to strong interference by large those coming from homes using kerosene or scale urban outdoor pollution and local gas (table 5). more of these respiratory symptoms. and and exposure to smoke pollution will remain of cooking with coal.2 to 3. by multivariate analysis in other studies (table A study of 658 children aged 0–6 years in 5).4) and being error.8 to 31) for home ated. Cooking with tom rates were. ETS.9. tion is a risk factor for both milder and more breathlessness. indoors while cooking took place (OR 2. symptoms and/or duration of symptoms was Overall. the children with ALRI communities where some households used who came from homes that burnt wood were biomass fuels and others kerosene.66 The tory infection in the previous week among chil- Brazil study took place in a city where the dren under five years. Morbidity due to “probable pneumonia” heating with “charcoal” in patients with hospi.3 (wood). was also determined by cough and diYculty in tal diagnosed ALRI compared with controls breathing and was found only to be weakly but matched by socioeconomic level.62 biomass pollution and mortality from pneumo- nia has been shown in one study of ALRI in Other studies Nigeria. was quite low (6%). and that was used at home without additional infor. 1. This was 12. it probably is not a good predictor of reported by Johnson and Aderele in Nigeria the risk of severe. . In smoke generated by its frequent burning. 14.76 The that found no significant association were the author speculates that the sample size of only ones which relied on questionnaires to households using wood burning stoves (not determine what type of cooking stove or fuel given) was too small to find an eVect. The study from urban Argentina by Cer. EVec- adjusting for age.2. cooking with any of studies. or severity.63 Unfortunately.5% was small (eight deaths in 100 ALRI cases). and tive strategies for pneumonia case management house type. 95% CI 1.02). an association between pneumonia mortality tion of the child during cooking. use of dung as cooking fuel (OR will modify the relationship between the 2. prospective study of 650 children aged 1–53 sure. Unfortunately.75 not important in this group of case-control After multivariate analysis.68 After severe cases of lower respiratory disease.3) and crowding (OR 1.5 on care seeking it remains a possible source of (dung)) or kerosene (OR 1.4) were associated with one or long as pneumonia fatality rates remain high. around the house (OR 1.

those from homes with wood heating stoves. Ambient monitoring showed year-olds in Jordan found that open wood . Turkey found by respiratory symptoms in 59 children aged less questionnaire in a group of 617 9–12-year-olds than 66 months. et al Incidence of ALRI in young children from an approximate diVerence of 20 µg/m3 in PM10 developed countries levels between the two neighbourhoods. Three other US studies of respiratory symp. Samet. (An earlier review can be found in Hon- Nevertheless. Romieu.0.70 Cases included association with stove type was no longer LRI. bronchitis. were ETS with chest illness (OR 1.25 risks. A similar study of 1905 7–13- aged 1–5 years.82 A more detailed analysis of 1501 tained from the hospital’s inpatient records. significantly more cough than those using tween respiratory symptoms in 823 children kerosene.com 528 Smith. ascer. and/or hospital than those found in village homes using open visits in studies of school aged children in the fires. housing.9) after multivariate airways and impaired host defences. In did not qualify for inclusion in table 6. forced expiratory volume in one second to include the diYculty of reaching the clinic in (FEV1). pneumonia.69 Cases studies in Malaysia. FEF25) were in children from wood non-significant trend was observed in those burning homes. higher rates of asthma and wheeze were et al71 performed a historical prospective study found in coastal children. a PEFR. Morbidity in school aged children holds using enclosed metal heating or cooking Exposure to pollution from wood stoves has stoves with chimneys. analysis that included passive smoking the ure indoor air pollution levels. 12-year-old children the presence of a wood or monia. wheeze or that of non-Hispanic white children. Fur. residence. ate analysis was reported.8.7). the impact on ALRI has been icky and Osborne. found use of wood stoves to be associated with the age adjusted ALRI mortality rate of Native a 30% increase in respiratory illness (chronic American children has been some six times cough. In a study involving 12147 were thus confirmed as bronchiolitis or pneu. Although not increased to the extent suf. 2014 . both groups variance. chest illness. A study in Adana.7 to 12. changes in lung function.79) The one study lacking shown in the two studies summarised in table statistical significance80 was based on telephone 6.73 on the other that those in homes heated with coal had hand. ETS. FEV1. 95% CI 1. 95% CI 0. Downloaded from thorax. half of whom came study involving 112 highland children.Published by group.bmj. but with a broad confidence band (OR ing children exposed to diVerent levels of 7. interviews with 399 households. Honicky fact. In Papua New Guinea Anderson84 also failed ther analysis revealed that PM10 levels over to show a diVerence in rates of respiratory 65 µg/m3 (90th percentile) were related to symptoms or lung function in studies compar- ALRI. significant. the Harvard Six Cities study of air pollution fered by children from developing countries. wood smoke neighbourhoods. but no information was given on the kerosene stove in the home was inversely asso- mix. 95% CI 0.4) and households (measured once).4) and asthma (OR 1. and bronchiolitis. The indoor pollutant been associated with chronic respiratory symp- concentrations are normally substantially less toms. Similar associations were not found in two pitalised patients using radiographs. In 7–12-year-old children found. The nificantly related to maternally reported median 15 hour PM10 levels in both sets of wheeze (OR 1. that use of mosquito coils was sig- ratio was found (5. adventitia and past chest illness. In addition. but in a multiple logistic regression the multivariate analysis and to actually meas.85 The lowest statis- aged over one year and location in high or low tically diVerent lung functions (FVC. No associ- quite similar (table 6) and were much lower ation was found with type of cooking fuel. In the first study of 1650 highland and cooking/heating only explained 10% of the lowland children under 10 years.9 to 57). Studies of the health eVects of biomass smoke in developed countries have focused on house.6 to 43). In a much smaller of 68 preschool children.com on September 7. have found eVects in school aged of reported wood stove use and five of 10 children.83 than those found in developing countries. after multivari- this case a similar but non-significant odds ate analysis.81 Such studies suggest an adverse eVect household cooking/heating with woodstoves of biomass pollution on lung function and are (with flues) produced a significant odds ratio consistent with irritation and inflammation of (4. and exposed to smoke in their village homes were found significantly more respiratory symptoms found to have the same prevalence of respira- in the exposed group. Butterfield et al72 More recent studies in developing countries. A study of asthma) in a large sample of children aged 7–10 young Navaho children in Arizona found that years. Browning et al. asthmatics and five of which found significant lage homes cooking with biomass fuel. Careful matching was tory symptoms and similar lung function as done to assure that the groups did not diVer by their counterparts living in nearby government income. their own home and/or their neighbourhoods. despite higher toms in young children exposed to wood smoke levels of smoke exposure in the highlands. found a significant correlation between hours however. etc. analysis for physician-confirmed ALRI in hos. However.47 Peak indoor particulate concentrations USA exposed to wood smoke from stoves in resulting from leaky heating stoves in devel. however. and that type of smoke. A second study was designed to address ciated with the forced vital capacity (FVC) and factors not covered in the first—in particular. found no significant relationship be. two of which dealt with the peak values of many thousand µg/m3 in vil. oil. but no multivari. or electricity. were found to have similar rates of loose cough.bmj. oped country homes are at most several Larson and Koenig78 reviewed six such studies hundred µg/m3 and are typically much less than in school aged children.0.

95 = measurements Given that indoor biomass use commonly = primary cause-effect results in 24 hour indoor CO levels of many tens of ppm. decrease in birth weight for each 100 µg/m3 of ethnic group. which is also associated with biomass use. India88 found after multivariate the well documented adverse eVects of ETS on analysis that cooking with biomass fuel was the respiratory health of children complement associated with a statistically significant in. 26–29 February 1992. function.com on September 7.5 ppm ambient CO during their last trimester. Adjustment was made for a Birthweight Gestational range of socioeconomic and other potential Length age confounders. air polution. particle levels may be PaO2 serving as surrogates for carbon monoxide Reduced O2 SaO2 24hr (CO) exposures in these birth outcome studies. work • Cigarette smoke indoor TSP exposures in wood burning homes FVC environment.9 g components Socioeconomic status.bmj. among other Cooking Smoke on Health’. and SO2 levels. Invited paper presented at WHO Workshop on ‘The Impact of Indoor developed countries leading to. aldehydes.7 These other pollutants include known ARI risk factors1 through reduced ETS and ambient pollution with particles by immunocompetence and/or impaired lung fossil fuel combustion. physical of highland Guatemala are probably at least activity 1000 µg/m3 higher than those in homes using Reduced O2 gas. to justify considering this large additional body nancy outcomes such as low birth weight are of evidence. Indeed.91 Given that FEV gain. mass fuels should be interpreted with consid- eration of data from studies of other indoor Impact on known precursors of ARI pollutants that may act through comparable One mechanism by which biomass smoke and toxicological mechanisms to adversely aVect other air pollution exposures could enhance respiratory illness.0 to 2. an extensive 1. transport across diet recall CO. although even stronger associations with an index combining CO. and other irritant gases37 96 97 adverse pregnancy outcomes may result from that are also found in ETS.22 Impaired delivery (95% CI 1. there are several Smokes from biomass fuels contain parti- pathways by which low birth weight and other cles.14) for low cigarette smoke. NO2. A study in high- Maternal alcohol. excess disease risk in infancy. anaemia. lead. Geneva. Adverse preg. As discussed earlier. placenta and fetal uptake has well established mechanisms for producing Placental low birthweight infants. 95% CI biomass fuel.022 increase per birthweight ppm). founding.5. problems. can be heavily exposed. and/or kerosene burning was statistically re- Agreement with ETS and outdoor pollution lated to lower lung function with about twice studies the negative impact of ETS. Downloaded from thorax.89 A recent cohort study of smoke Confounders Other nearly 75 000 births in Beijing90 found a 6.7 there would seem to be potential Figure 4 Pathways relating smoke exposure and childhood health. Switzerland.Published by group. a recent cross macro and micro sectional study of 125 000 birth weights in Preterm morphology southern California found an odds ratio of 1. stature.bmj. 2014 .03 to 1. ‘Potential mechanisms for the eVect of indoor cooking smoke on for high in utero risks in households in less fetal growth’.com Indoor air pollution in developing countries 529 born to women exposed to increased levels of Indoor cooking small particles. land Guatemala found. epidemiological literature documents an as- cant intrauterine growth retardation in babies sociation between exposure to ETS and . There is suYcient overlap the risk of ARI in young children would be by between some components of biomass smoke in utero exposures via their mothers who. which translated to an odds ratio Carbon diet. but not active smoking or ETS. caffeine. Lower birth rates have placenta content of also been associated with ETS exposures to maternal Reduced nutrient intake pregnant women.05 to 1. also the result of burning a form of biomass. a statistically significant decrease of Effect modifiers house ventilation.1 (95% CI 1. A study in Bohemia found signifi.87 As shown in fig 4.93 blood CoHb As indicated in fig 4.92 the results of these two studies are delivery to Reduced O2 remarkably consistent. ing evidence of such in utero eVects. Particulate monoxide of 1. which of course is heavy maternal air pollution exposures.1). a While undoubtedly there are diVerences be- case-control study of 451 stillbirths in tween ETS and these other biomass smokes. when and components of other investigated mixtures cooking. • Anaemia 63 g in birth weight of infants born to mothers gestational weight • Altitude cooking with wood rather than gas. Provid. Reproduced with permission from Hass JD. after adjusting for con- lung disease altitude.86 No multivariate The evidence on health eVects from use of bio- analyses were reported for these studies. Ahmedabad.44) for low birthweight fetal growth infants (1000–2499 g) born to mothers experi- encing more than 5. the epidemiological findings on smoke from creased chance of stillbirth (OR 1. ambient TSP. birthweight babies (<2500 g).94 A time series study in Sao Paulo found similar levels of CO to be associated with excess Low intrauterine mortality (0.

ironically. the justice”—that is. Samet. or other contaminated environments. even more egregious examples of this Risk estimates from individual studies are injustice prevail. class of health impacts from air pollution expo- venting ARI in general. such as cooking stoves. tion of pneumonia/ARI mortality due to air may contribute to the increased risk of ARI pollution is not yet certain. respiratory defence mechanisms and the geo.com 530 Smith. Adverse eVects of these exposures factors: (1) the relatively high odds ratios would be anticipated on a toxicological basis. eVective intervention strategies. Thus. cigarettes. Indeed. closer to the “gold standard” of randomised which place children near sources of pollution clinical trials. and (3) the high base rate of the disease in these onstrated between exposure measures and nations (table 2). (2) the seemingly Although the epidemiological evidence on high and prevalent exposures in less developed smoke from biomass fuels and pneumonia is countries. This conclusion contrasts with the attributable ARI. vehicle Globally. pollution. and their young children. et al increased ALRI in infants and young children. We suggest that this seeming patterns of children under the age of five years paradox reflects a failure to systematically . and house- children are particularly susceptible to these holder education and. ever. this disease outcome represents the largest This review documents the potential for pre. how- terised. of even higher priority than and particles that are produced by combustion. Infants and young as clean fuels. and pneumonia in par. however. particularly in households (fig 2). Combustion of household solid fuels because much of the burden falls on young in developing countries produces exposures to children. quantitative risk assessments lutants. in children by reducing exposures to air terms of total morbidity and mortality but. Given the imprecision and uncer. associations have been dem. both engineering and contaminated by complex mixtures of gases behavioural. Patterns of time-activity. apparently involved (table 5).98 Globally. further observational studies is the promotion Components of these mixtures have been of well designed randomised intervention trials shown to adversely aVect host defences against in households in less developed countries in respiratory infections and it is thus plausible conjunction with careful exposure assessment. also shows adverse eVects of The resulting data would facilitate the design particles and gases on the respiratory health of of additional case-control and cohort studies to children. Unlike most sources of ambient air pollu- als within populations. Existing studies are likely to under. household sources of exposure such as cooking and heating oVer the oppor- Conclusions tunity for conducting randomised trials of Indoor and outdoor environments are widely potential interventions.32 personal exposures and the contributions of Similarly. countries to issues related to “environmental cal evidence on inhaled pollutants and ARI. because of the lack of information on the evidence driving policy for air pollution exposure-response relationships. who experience the tainty in characterising the risk of biomass bulk of global airborne exposures to many pol- smoke exposure.bmj.bmj. vincingly demonstrate to policy makers the tory infections by causing inflammation of the health benefits of practical interventions such lung airways and alveoli. given past sci- adverse eVects because of the immaturity of entific inattention to this particular problem. classification of the exposure status of individu. tion. disadvantaged populations. in urban settings. not yet abundant. tion and ARI in developed countries. few if any large groups imprecise because of relatively small sample are more disenfranchised and disadvantaged sizes and misclassification of exposure and than poor rural women in developing countries outcome. This is due to three countries. the major health consequences of air pollution els of exposure implies a significant burden of globally. On Some readers may be surprised by our con- the other hand. con- ants might also increase the severity of respira. Romieu. Indeed. This is likely to be the case in ticular. cannot be oVered with great confidence. that such pollutant mixtures increase the Data from intervention studies could quantify incidence of respiratory infections. the large population of children clusion that ARI in children represents one of exposed and even our limited database on lev. is almost certainly the case with smoke components that are remarkably high by regard to measures of ill health that consider the standards set for outdoor air in developed the lost life years involved. better quantify the relationship between smoke estimate the size of the association between exposure and ARI and to identify the most ambient pollution and health as a result of mis. Relatively recently there has been a signifi- ratory tract. exposure-response relationships for ARI.Published by group. however. even though the attributable frac- exhaust. the unfortunate tendency for association of smoke from biomass fuels with the highest exposures to environmental pollut- ARI should be considered as causal. it is probable that from airborne pollutants in young children. control at present derives largely from studies ther research directed at the time-activity of elderly persons. 2014 . The extent to which excess limited epidemiological research on air pollu- biomass smoke can be prevented is uncertain. We urge fur. primarily based indoor and outdoor pollution sources to on studies of various pollutants in outdoor air children’s exposures in developing countries.com on September 7. improved stoves. Downloaded from thorax. move air pollution epidemiology in general metry of the airways. although ants to be experienced by some of the most the quantitative risk has not been fully charac. a large literature. as well as studies designed to characterise total an association that has been judged as causal. When interpreted within the broad cant increase in attention in many developed framework of epidemiological and toxicologi. indicators of illnesses involving the lower respi. Air pollut. sure worldwide.

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