Introduction

Exposure to household air pollution from domestic solid fuel use causes over 4 million deaths per year, and is the most important environmental risk factor for disability adjusted life years worldwide [1]. Household air pollution has been found to increase the risk of childhood acute lower respiratory tract infection (ALRI) by 78% (pooled odds ratio = 1.78 (95% CI 1.45 to 2.18) [2]) and is responsible for half a million deaths in young children every year. Over a third of the world’s population are exposed to high levels of household air pollution, with women and children experiencing the greatest burden [3].

Disease outcomes in adults attributed to household air pollution from solid fuels include chronic lung and cardiovascular disease [1]. Based on the evidence for an association between household air pollution and child ALRI [2], and evidence from ecological and toxicology studies regarding the health effects ambient air pollution in all ages [4], an association between household air pollution and ALRI in adults is biologically plausible but lacks a convincing evidence base. Although the Global Burden of Disease study 2013 incorporated adult ALRI as an outcome for household air pollution exposure, the risk estimate was derived from an integrated exposure-response curve for PM_2.5 (particulate matter <2.5μm diameter) from ambient and household air pollution, and tobacco smoke which has limitations [1,5]. It is important to determine whether or not there is an increased risk of ALRI associated with household air pollution in adults since the attributable risk is potentially high and the burden greatest in people living in low and middle income countries (LMICs). ALRI is a common cause of hospitalisation among adults in LMICs with high associated morbidity and mortality [6]. Mortality among adults with pneumonia in sub-Saharan Africa is around 10%, with over 50% of deaths seen in people under 35 [7–9].

To ensure that public health interventions are appropriately directed, the true burden of disease needs to be clarified [10, 11]. We systematically reviewed the literature, including studies of any design, to synthesise the evidence base for the relationship between household air pollution exposure from domestic solid fuel use and adult ALRI worldwide. We describe the current literature, identify knowledge gaps and future research opportunities.

Methods

This systematic review is registered with the Centre for Reviews and Dissemination (Registration number: CRD42015028042). The full protocol is available at http://www.crd.york.ac.uk/prospero.

Results

Database searches identified 8605 records and 331 records were identified from the alternative sources set out in the methods. After removal of duplicates 4617 records remained. The number of titles, abstracts and papers reviewed was 4617, 513 and 72 respectively, as summarised in the PRISMA flowchart (Fig 1), with the reasons for exclusion at the abstract and full text stages (see S1 File for PRISMA Checklist). Agreement between authors was 95–96% for the first 20% of titles reviewed, and 95–98% for the 10% overlap of remaining titles. It was not possible to locate 5 selected abstracts [13–17] and 2 selected full text papers—both published in Chinese [18, 19]—for review. Two authors were contacted for further details about their recent or ongoing studies identified at www.clinicaltrials.gov. One study is a prospective cohort study of febrile adults in Tanzania for which recruitment has been completed but the data are not yet available (NCT01947075). The second study is a randomized trial of smoke reduction interventions in Native American populations, but we were unable to obtain further details (NCT02240069). In addition, we are conducting a case-control study of the effects of air pollution exposure and chronic respiratory disease on pneumonia risk in Malawian adults [20].

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Fig 1. PRISMA Flow Chart A flow chart depicting the inclusion and exclusion of identified studies

https://doi.org/10.1371/journal.pone.0167656.g001

Ten papers met the criteria for inclusion; data from 2 of these were duplicated in other selected papers [21, 22], and therefore not extracted. The remaining 8 papers included 4 cross-sectional [23–26], 2 cohort [27, 28] and 2 case control studies [29, 30]. The articles covered study locations from 8 countries across 4 continents. The largest study was a retrospective cohort study from China, which reported on the causes of death in 42,422 farmers [28]. The main findings of all included studies are summarised in Table 1, which demonstrates the heterogeneity of study participants, exposure definitions and outcome definitions.

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Table 1. Summary of findings table for four studies investigating the effects of household air pollution on adult acute lower respiratory tract infections.

https://doi.org/10.1371/journal.pone.0167656.t001

Most studies were based in rural settings and recruited participants from communities. There were 3 exceptions, which were hospital or health-centre based studies, conducted in urban areas of Canada, Mexico and Serbia [25, 29, 30].

Most studies predominantly or exclusively recruited females (accounting for 48–100% of participants within studies). In the study from Tanzania, the cooks were mainly female but the gender and age of the unexposed group were not reported [24].

Except for the study from Canada, which restricted recruitment to individuals over 65 [29], and the study from China [28], in which deaths occurred between 25 and 80 years of age, all studies recruited younger adults. Five studies restricted participants to adults over 18, whilst the 3 remaining studies—from Sierra Leone, Tanzania and Kenya—included younger participants but were conducted in predominantly adult populations.

One study evaluated coal use (Shen et al) and the 7 others evaluated biomass fuel use, predominantly wood. Four studies measured levels of household pollutants directly, but only 1 presented an estimate for the effect of pollutants on ALRI risk. In Kenya, Ezzati et al. measured particulate matter <10μm diameter (PM₁₀) for 14–15 hours per day for 200 days in 55 households, and demonstrated a dose-response relationship between exposure to PM₁₀ and ALRI risk [27]. The authors report that this finding was supported by analysis with a continuous-exposure variable and inverse-quadratic relation, although have not published these results. All studies monitoring air pollution levels measured PM₁₀ rather than PM_2.5. This may misrepresent the true harmful exposure, as smaller PM_2.5 particles are inhaled deeper in to the lungs than PM₁₀ and are therefore thought to be more pathogenic [31].

The 7 studies that did not provide an effect estimate for measured pollutants all used questionnaire data to classify exposure to household air pollution, based on a variety of self-reported measures including fuel or stove type, quantification of fuel use, ventilation, cooking frequency and location.

Two studies defined the outcome using prospective health care worker diagnosis of ALRI; in Canada, hospitalised cases had symptoms or signs, and radiological changes consistent with pneumonia [29]; in Kenya, the outcome was defined as nurse-diagnosed ALRI following review and physical examination at 1–2 weekly visits over a 2 year period [32]. A third study, from Nepal, included a physician’s review to diagnose ALRI, but no further definition was provided and it is unclear whether retrospective diagnoses were included [23]. The study from China used retrospective review of death certificate records, which had been completed by physicians on the basis of clinical and radiological investigations [32]. Similarly, the study in Mexico used a retrospective review of hospital records by specialists to identify cases [30]. The remaining studies used self-reported symptoms or past diagnoses, with varying recall periods, to define the outcome [24–26].

Six of the 8 studies made some adjustment for potential confounders in their analysis of the effect of household air pollution on ALRI [23, 25, 26, 28, 30, 32], but several studies failed to make adjustments for important potential confounders, such as economic status and smoking.

The effect estimates quantified by the studies are shown in Table 1 and in a Forest Plot (Fig 2). There were inconsistent findings across the studies. Whilst the 2 cohort studies have marked differences in study design, they demonstrated statistically significant harmful effects of household air pollution exposure on ALRI after adjustment for confounders. A dose-dependent relationship between PM₁₀ and ALRI was detected in Kenya, (OR = 7.10, (95% CI 2.26 to 22.32) for exposure to >7000μg/m³ PM₁₀ (highest exposure category) vs. 200–500 μg/m³ PM₁₀) [32], and a reduction in risk of pneumonia deaths was observed in participants using an improved coal stove instead of a traditional coal stove (OR = 0.49 (95% CI 0.31 to 0.80) and 0.53 (95% CI 0.32 to 0.88)) in Chinese men and women respectively [28]. The studies from Mexico and Tanzania both reported harmful effects of household air pollution exposure in univariate analysis [24, 30], but these were no longer significant after adjustment for confounders in the Mexican study. The studies from Nepal, Serbia and Sierra Leone did not identify a significant association between household air pollution and risk of ALRI [23, 25, 26]. The study from Canada found that fireplace use was associated with a reduction in the risk of pneumonia, although this was unadjusted [29].

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Fig 2. Forest Plot A forest plot showing the Odds Ratio (and lower and upper 95% Confidence Intervals) for different exposures and outcome in the included studies.

Adjusted results are shown where available. Key: ICS: improved cookstove; kero: kerosene; *indicates that the study is assessing for the protective effect of an intervention.

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All of the case-control and cross-sectional studies were found to be at high risk of bias in at least 2 out of the 4 domains assessed, leading to an overall assessment of “moderate/high” or “high” risk of bias. Exposure assessments were weak. The cohort studies were of a generally higher standard, although their risk of bias was moderate in at least 2 out of 4 domains.

Discussion

This paper synthesises the current evidence base for the relationship between household air pollution and adult ALRI, identifying 8 eligible studies that have quantified this relationship. Despite a paucity of available studies, the available data provides some evidence for an increased risk of adult ALRI from exposure to household air pollution. The review has highlighted disparities between the findings of the studies, although these are unsurprising given the methodological heterogeneity seen. Methodological limitations were also noted, including poor exposure and outcome classifications, and potential biases including selection and recall biases. Although suggestive of an association, the current evidence is not sufficient to make a direct assessment of the potential impact of household air pollution on adult ALRI.

Methodological differences in exposure classification are a likely source of variation between study findings in this review. Indirect classification of exposure to household air pollution was common, and may have resulted in exposure misclassification. Accurate measurement of exposure to pollutants such as PM_2.5 is challenging in the field. Monitoring is becoming more practical, with a variety of devices now available, which will benefit future population studies of health impacts such as ALRI. Exposure, however, needs to be measured at repeated intervals to accurately classify levels for diseases with a long latency period from defined exposures and this remains a challenge.

With regards to major sources of bias and error, the quality of studies identified was varied. Two studies used retrospective records of patients, and none of the prospective studies reported response or refusal rates of participants, so may have been subject to selection bias. Several studies used some form of random sampling but the cross-sectional study from Serbia only recruited women who attended a health centre so the findings are not generalisable to the wider population. The case-control study from Mexico used patients with otolaryngeal disease as controls, but as household air pollution can also be a risk factor for this outcome [3], this may have biased the findings towards the null. Only 1 study directly measured exposure to household pollutants [32]. All other studies relied on questionnaire responses regarding exposures, which are prone to recall bias, with varying recall periods and often poor definitions of exposure. Similarly, several studies relied on potentially biased and inaccurate recall of previous illness; outcome misclassification may have diluted the true effect. Three studies used prospective assessment of patients by a health-care worker for the outcome classification, although the quality of definitions used varied. Two studies made no adjustment for confounders, and other studies failed to adjust for some important confounders such as smoking, and so their findings may be misleading. Four studies were cross-sectional and are therefore unable to establish temporality between exposure and outcome.

Although the literature was previously reviewed as part of the Comparative Risk Assessment conducted for the GBD 2010 [33], this review provides an update, adding 5 studies to the evaluation. This review also provides a narrative summary of the current evidence which was not previously available, and a critical appraisal of methodological limitations. The review included a comprehensive search of published bibliographic databases—including databases from Africa and Latin America—and available grey literature, including contact with known researchers in the field undertaking relevant research. A limitation of this review is that we were unable to include literature published in Chinese. Due to the paucity of evidence, publication bias was not assessed.

Diseases associated with household air pollution disproportionately affect those living in poverty, who rely on solid fuels to meet their energy needs [34]. To consolidate GBD estimates—which currently use modelled data from other sources of air pollution—we set out to quantify the association between household air pollution and adult ALRI. Whilst it is likely that the burden of disease from household air pollution in adults includes ALRI, the published literature does not provide definitive evidence of this. Further research, using robust direct exposure measurement and accurate classification of outcome, is required to improve the evidence base. Exposure to household air pollution is preventable but resources are limited in low-income populations with competing health priorities: with high quality evidence of the true scale of the problem and cost-effectiveness of interventions, resources to reduce the global burden of disease can be effectively allocated.

Supporting Information

Acknowledgments

We are grateful to Dr Christine Kelly (University of Liverpool) and Mariana Gallo for their assistance with translating French and Spanish language papers.