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  • Review
  • Open Access

The role of environmental exposure to non-cigarette smoke in lung disease

Clinical and Translational Medicine20187:39

https://doi.org/10.1186/s40169-018-0217-2

  • Received: 3 October 2018
  • Accepted: 23 November 2018
  • Published:

Abstract

Chronic exposure to household indoor smoke and outdoor air pollution is a major contributor to global morbidity and mortality. The majority of these deaths occur in low and middle‐income countries. Children, women, the elderly and people with underlying chronic conditions are most affected. In addition to reduced lung function, children exposed to biomass smoke have an increased risk of developing lower respiratory tract infections and asthma-related symptoms. In adults, chronic exposure to biomass smoke, ambient air pollution, and opportunistic exposure to fumes and dust are associated with an increased risk of developing chronic bronchitis, chronic obstructive pulmonary disease (COPD), lung cancer and respiratory infections, including tuberculosis. Here, we review the evidence of prevalence of COPD in people exposed to non-cigarette smoke. We highlight mechanisms that are likely involved in biomass-smoke exposure-related COPD and other lung diseases. Finally, we summarize the potential preventive and therapeutic strategies for management of COPD induced by non-cigarette smoke exposure.

Keywords

  • Non-cigarette smoke
  • Biomass smoke
  • Occupational exposure
  • Air pollution
  • Lung disease
  • Chronic obstructive pulmonary disease (COPD)

Introduction

Worldwide, in 2016, approximately 9 million deaths were attributed to lung diseases, including COPD, lung cancer and lower respiratory tract infections, among which 82.4% occurred in low and middle-income countries [1]. Tobacco smoking is one of the most well-characterized risk factors for lung disease development, killing more than 7 million people each year [2]. However, compared to 1.1 billion tobacco smokers globally, nearly 3 billion people are exposed to biomass smoke [3, 4]. Moreover, data from epidemiologic studies conducted in Asia, Europe, South America and Africa have consistently shown associations between biomass smoke exposure and lung diseases, even after controlling for the primary risk factor, tobacco smoking [5, 6]. Here, we review the association of lung diseases, including COPD, with exposure to biomass smoke, fumes, dust, gases and outdoor air pollution.

Methods

We conducted a qualitative examination of the published peer-reviewed literature from 1980 to June 2018 using the Medline database (https://www.nlm.nih.gov/bsd/medline.html). We used the search terms “biomass fuel”, “biomass smoke”, “wood smoke”, “solid fuel”, “coal smoke”, “indoor smoke”, household pollutants”, “outdoor air pollution”, “occupational exposure” combined using the Boolean logic ‘OR’. Similarly, the search terms “lung disease”, “pulmonary disease”, “airway disease”, “bronchitis”, “emphysema”, “asthma”, “lung cancer”, “acute respiratory tract infection” were also combined using the Boolean logic ‘OR’. The two subsets were combined using the Boolean logic ‘AND’, and the results were restricted to meta-analyses, systematic reviews, observational studies, comparative studies and original articles published in English. The search resulted in 1953 articles that were screened from which 168 studies were selected as being relevant to the review.

Prevalence and burden of biomass smoke exposure

Annually, nearly 4 million people die prematurely from illness attributable to household biomass smoke exposure, among which an estimated 55% die due to respiratory diseases, including pneumonia (lower respiratory tract infections), COPD and lung cancer [7]. Nearly half of the world’s population rely on biomass, such as wood, animal dung, and crop residues as a primary fuel source for cooking and heating purposes [7]. The proportion of households using clean fuels (liquid petroleum gas, biogas and electricity) varies considerably across the globe (and even in the same continent) [8]. The access to clean fuels is especially limited to relatively smaller populations in the low- and middle-income countries (Fig. 1). Consequently, populations residing in the regional and rural households in developing countries are heavily reliant on biomass fuel for cooking or heating purposes (Fig. 1) [9].
Fig. 1
Fig. 1

Global use of clean fuels in 2014, by the World Health Organization. Countries with the lowest (< 5%) and the highest (> 95%) proportion of people using clean fuels as the primary domestic source of energy are shaded dark and light blue, respectively.

Reproduced with permission from the World Health Organization [8], Copyright (2016)

The particular concern with energy from biomass fuel is the use of inefficient stoves for combustion, which generates toxic gases like carbon monoxide and nitrogen oxides; suspended particulate matter containing volatile organic compounds (VOCs) such as methane, aldehydes, benzene and its derivatives; and polycyclic aromatic hydrocarbons (PAHs) like benzo[a]pyrene and anthracene [10]. Particulate matter (PM) with an aerodynamic diameter of < 2.5 microns (PM2.5) is light and can remain suspended in the air for longer periods [11]. These particles can be inhaled deep into the lungs, and have been linked to oxidative stress and inflammation induced damage of the respiratory system [11]. Moreover, in developing countries, the cultural practice of indoor cooking in housing with poor air ventilation potentially exposes women and children to PM2.5 up to the levels that are 1000 times higher than the threshold recommended by WHO (25 µg/m3) [12, 13].

Wood is the most common biomass fuel, however, use of animal dung, such as cow, sheep and horse, as a source of fuel is also widespread, especially in rural areas of low- and middle-income countries, including India, Nepal, and sub-Saharan Africa due to its availability in areas with limited vegetation and its lower cost [14]. Despite this, animal dung is the least efficient biofuel and burns faster as compared to wood [15]. Relative to wood smoke, combustion of animal dung produces more particulate matter (23% more PM2.5 per kilogram), toxic byproducts, such as PAHs and oxidizing species, such as redox active metals (copper and iron) and quinones [16, 17].

Nonetheless, exposure to biomass smoke is not exclusively an issue in low- and middle-income countries. Use of indoor wood fires for heating purposes and for imparting flavor during cooking processes, such as barbecuing and wood-smoking of food, is becoming more popular in high-income countries, thus, increasing biomass smoke exposure [18]. In 2014, in a survey carried out in Australia, approximately 10% of households used wood as the main source of heating [19]. However, in developed countries, use of biomass fuel is primarily seasonal and exposure is largely limited by better ventilation [20]. Besides indoor biomass smoke exposure, people in developed countries such as Australia, Canada and the USA are also exposed to outdoor biomass smoke from frequent bushfires [21]. Importantly, individuals exposed to biomass smoke are more likely to have respiratory symptoms and reduced lung function [2224].

Association of biomass smoke exposure with respiratory diseases

Chronic airway disease

Worldwide, COPD claimed more than 3 million deaths in 2016, among which 81.8% occurred in low- and middle-income countries [1]. Tobacco smoking is still the main causative factor of COPD in high-income countries where only 15–25% of COPD cases are never smokers (Table 1). However, in low and middle countries more than 45% of COPD patients have been found to be never smokers (Table 1). The existing literature provides strong evidence that smoke from biomass fuels is an independent risk factor for the development of COPD, particularly in low- and middle-income countries where the reliance on biomass fuel is still very high. The noxious particles in biomass smoke induce an inflammatory response through: upregulation of pro-inflammatory cytokines such as interleukin 6 (IL-6), tumor necrosis factor alpha (TNFα), and granulocyte colony stimulatory factor (G-CSF); recruitment of immune cells, such as macrophages and neutrophils; upregulation of gelatinases (matrix metalloproteinase 2 and 9); and epithelial-mesenchymal transition (EMT), thereby reducing lung function and contributing to the onset/progression of COPD [2527]. Da Silva et al. in a case–control study in Brazil, evaluated the effect of exposure to biomass combustion PM2.5 on lung function [22]. There was a significant loss in pulmonary function in non-smoker biomass users compared to non-smoker liquefied petroleum gas (LPG) users (forced expiratory volume in one second to forced vital capacity ratio (FEV1/FVC) 0.79 versus 0.85, p < 0.05, respectively). In addition, pulmonary function was negatively correlated with the level and duration of PM2.5 exposure (FEV1/FVC: r = − 0.63, p < 0.05 and − 0.52, p < 0.05, respectively) [22]. A minor reduction in FEV1/FVC was observed in women in Mexico using biomass fuel compared to clean gas (0.80 vs 0.83, p = 0.03, respectively) [24].
Table 1

Proportion of never smokers among COPD patients and associated risk factors

Study center and design

Participants

Age (years)

Proportion of never smokers among COPD patients (%)

Risk factors for COPD in never-smokers

References

Overall

Male

Female

Multinational (35 centres, 16 countries; ECRHS)

17,966

20–44

17.0

13.4

21.6

Occupational exposure to vapours, gas, dust, or fumes

Cerveri et al. [33]

Malataya, Turkey (CS)

1160

> 18

22.5

  

Exposure to biomass smoke

Gunen et al. [34]

China (CPH; nationwide CS)

50,991

> 20

50.5

10.1

91.7

Exposure to biomass fuel smoke and PM2.5, parental history of respiratory disease

Wang et al. [28]

South Africa (nationwide survey)

13,826

> 18

47·6

24.8

61.0

Biomass fuel, occupational exposure, history of pulmonary tuberculosis

Ehrlich et al. [35]

Maswa, Tanzania (CS)

869

> 35

62.1

 

Magitta et al. [36]

Västra Götaland and Norrbotten, Sweden (CS)

1839

21–78

21

Occupational exposure to gas, dust and fumes

Hagstad et al. [37]

Copenhegen, Denmark (CS)

68,501

20–100

22.3

18.9

25.5

 

Thomsen et al. [38]

Multinational 12 countries; population-based survey)

73,745

> 40

36 (24 USA-64 Mexico)

21

49

 

Landis et al. [39]

ECRHS European Community Respiratory Health Survey; CS cross-sectional study; CPH China Pulmonary Health; COPD chronic obstructive pulmonary disease

In a recent nationwide cross-sectional study conducted in 50,991 individuals from ten provinces of China, more than half of the COPD patients were never smokers [28]. Importantly, the proportion of never smokers in female COPD patients was markedly high (91.7%). Additionally, individuals exposed to indoor biomass smoke were 62% more likely to develop COPD than unexposed individuals who used clean fuel sources (age and sex adjusted OR = 1.6, p = 0.003) [28].

A meta-analysis of 11 cross-sectional and four case–control studies covering a wide range of countries identified household biomass smoke exposure as an independent risk factor for developing COPD in both men (OR 4.30, 95% CI 1.85–10.01) and women (OR 2.73, 95% CI 2.28–3.28), and in both the Asian population (OR 2.31, 95% CI 1.41–3.78) and the non-Asian population (OR 2.56, 95% CI 1.71–3.83) [5]. This finding is supported by another recent cross-sectional study, the PUMA (Prevalence Study and Regular Practice, Diagnosis, and Treatment Among General Practitioners in Populations at Risk of COPD in Latin America), which assessed 1740 individuals from multiple nations in South America, who were at greater risk of developing COPD [6]. The PUMA study reported that individuals exposed to household biomass smoke are twice as likely to develop COPD than unexposed people (adjusted OR 2.28, 95% CI 1.18–4.41) [6]. Moreover, a systematic review of 24 epidemiological studies revealed that household biomass smoke exposure was associated with COPD development in both urban (OR 1.6, 95% CI 1.2–2.0) and rural women (OR 2.0, 95% CI 1.5–2.8) [29].

In terms of COPD phenotypes, biomass smoke exposed individuals were found to have more lung fibrosis and bronchiolitis and less emphysema whereas tobacco smokers exhibited higher levels of emphysema (radiologist CT score—a measure of the extent of emphysema based on computed tomography (CT) at inspiration and expiration) 0.7 versus 2.3, p = 0.001; emphysema on CT 19% versus 27%, p = 0.046) [30, 31]. This finding is further supported by Fernandes et al. who reported a significantly lower level of emphysema in biomass exposed women than in women who were tobacco smokers (PRMEmph (parametric response mapping, an image tool used to quantify emphysema based on paired CT images at inspiration and expiration) 1.84% (0.69 ± 3.72%) versus 9.85% (2.40–16.34%); p = 0.001) [32].

Lung cancer

Globally, 1.7 million deaths in 2016 were attributed to lung cancer, among which 66% occurred in low- and middle-income countries [1]. The combustion products of biomass fuel emissions such as dibenz[a,h]anthracene, cyclopenta[cd]pyrene and 1,3-butadiene have been grouped as a probable human carcinogen (group 2A) by the International Agency for Research on Cancer [40]. Saldana and colleagues, in a hospital based case–control study with 136 cases of primary lung cancer and 137 controls, reported a significant association between the magnitude of biomass smoke exposure in hour-years (years of exposure multiplied by average hours of exposure per day) and the risk of lung cancer after adjusting for sex, smoking, socioeconomic status and housing with asbestos sheet roof (OR for an exposure > 300 h-years 3.01, 95% CI 1.12–8.36) [41]. A systematic review including 13 case control studies summarized an increased risk (OR 1.17, 95% CI 1.01–1.37) of lung cancer with biomass exposure associated with cooking/heating, in particular, among women in developing countries [42]. In a retrospective cohort study conducted in Xuanwei city of China, mortality from lung cancer was compared between lifelong users of smoky coal (27,310 individuals) and smokeless coal (9962 individuals). Individuals exposed to smoky coal were at greater risk of death from lung cancer when compared to those exposed to smokeless coal (for men, HR 36, 95% CI 20–65; for women, 99, 95% CI 37–266) [43]. A similar observation was reported in a meta-analysis from 28 epidemiological studies where a significantly higher risk of lung cancer was observed in females (OR 1.81, 95% CI 1.54–2.12; p = 0.034) exposed to biomass/solid fuel smoke compared to males (OR 1.16, 95% CI 0.79–1.69) with related exposure [44]. The increased susceptibility of women to biomass/coal carcinogens compared to men may be due to differences in base-line exposure (women being exposed to biomass/coal smoke for extended periods of time) or due to differences in lung size (women having smaller lungs than men, hence more damage done for the similar amount of smoke inhaled) [45]. The association was even more prominent in individuals using coal (OR 1.82, 95% CI 1.60–2.06) compared to biomass (OR 1.50, 95% CI 1.17–1.94), which may be due to the production of predominant Group 1 carcinogenic PAHs during coal combustion [44, 46]. Although the studies included in this review have either been adjusted for smoking or studied a population of non-smokers, none of these studies commented on the presence of other co-morbid conditions, such as COPD, at the time of lung cancer diagnosis.

Lower respiratory tract infections

In addition to COPD and lung cancer, the other major respiratory cause of global mortality is lower respiratory tract infection (LRI) and tuberculosis, which was directly implicated in 2.96 and 1.29 million deaths in 2016, respectively [1]. Of the approximate 4 million deaths globally, around 89% of the mortality was reported in low- and middle-income countries alone [47]. An evaluation of 14 studies in developing countries indicates that young children living in households where biomass fuels are utilized, have a two to three times higher risk of respiratory infections than unexposed children after adjustment of potential confounding factors [48, 49]. A recent systematic review of 77 studies from 39 low- and middle-income countries evaluated the risk factors for mortality from acute lower respiratory infections in children under 5 years of age and found that biomass smoke exposure is significantly associated with an increased risk of death from LRI (OR 3.0, 95% CI 2.1–4.3) [50]. However, only a small number of studies have focused on the association between biomass smoke exposure and risk of lower respiratory tract infection in the adult population. Ezzati et al. evaluated the risk of LRI in 229 individuals between 5 and 49 years of age in Central Kenya upon exposure to biomass fuel derived PM10 [51]. The risk of LRI was positively correlated with the level of PM10 exposure, however, the odds ratio was significant only above 2000 µg/m3 (adjusted OR 3.3, 95% CI 1.1–9.9) [51]. Exposure to household biomass smoke was associated with risk of hospitalization due to pneumonia in older adults aged 65 and above (adjusted OR 3.3, 95% CI 1.6–6.9) [52]. On the other hand, although the prevalence of acute respiratory infection was higher among biomass users (15–45%), after controlling for major confounding factors such as age and smoking, the risk of LRI was not significant when including adults aged less than 65 [5355]. In addition, biomass smoke exposure is significantly associated with the risk of developing tuberculosis. For example, a close correlation between biomass fuel usage and tuberculosis (OR 3.14, 95% CI 1.15–8.56) has been reported from northern India compared to usage of liquid petroleum gas in kitchens after adjusting for confounding variables, such as tobacco smoking and close contact with TB cases (6).

Other respiratory conditions

Several studies have highlighted the effect of biomass smoke exposure in respiratory symptoms, such as cough, wheeze, mucus overproduction and dyspnoea [2224]. A case–control study in Brazil reported an increased risk of developing chronic cough (OR 2.9, 95% CI 1.68–5.10), wheeze (OR 2.33, 95% CI 1.25–4.38) and dyspnoea (OR 2.59, 95% CI 1.32–5.09) in adults exposed to biomass smoke as compared to LPG users [22]. Similarly, a study in Eastern India assessed the impact of chronic exposure to indoor biomass smoke on respiratory health in 681 non-smoking women and 438 age matched women not exposed to biomass smoke [23]. Compared to LPG users, biomass users had a higher prevalence of cough, mucus production and wheeze (71.8% versus 30.8%, p = 0.001), and dyspnoea (58.4% versus 19.9%, p = 0.001) [23].

Besides lower respiratory tract symptoms, other lung diseases, such as asthma and pneumoconiosis have been correlated with exposure to indoor biomass smoke. Oluwole et al. reported an increased prevalence of asthma-related symptoms, such as wheezing or whistling in the chest, cough, dyspnoea and chest tightness in rural school children in Nigeria exposed to biomass smoke (OR 2.37, 95% CI 1.16–4.84) [56]. However, evidence of its association with asthma is inconclusive. A meta-analysis of 25 studies did not find any significant association of biomass smoke exposure and asthma in children (OR 0.5, 95% CI 0.1–2.0) or women (1.34, 95% CI 0.9–1.9) [57]. However, a significant difference has been reported between bronchiectasis (diagnosed by computed tomography scans) in women and exposure to biomass fuel, compared to exposure to tobacco smoke (14% versus 0%, p = 0.009) [30]. Particularly, the “Hut lung disease” or domestically acquired pneumoconiosis has been noted as a particulate lung disease in women exposed to biomass fuel smoke or agricultural activities but not associated with mining [5860].

Exposure to other types of air pollutants

Environmental exposure to noxious particles and gases

High levels of air pollution have also been implicated as risk factors for the development of COPD, although it is less potent than active smoking. Approximately 25–60% of COPD patients are never-smokers in developing countries [28, 36, 61]. Increasing population, urbanization, economic profile and pollution are several factors that contribute substantially to the COPD burden [62]. The role of outdoor air pollution (including traffic-related fine particulate matter) as a causative factor for airflow limitation is gaining attention in recent times, due to increased vehicular pollution, as well as industrialization of the two most populated countries, China and India [63].

PM2.5 is considered to be the most health-damaging of the particulate matter, as it can penetrate deep into the lungs and initiate deleterious effects on the airway, including but not limited to airway oxidative stress, pulmonary and systemic inflammation, ciliary dysfunction, amplification of infections, and increases in bronchial reactivity [64]. The main components of PM10 are sulfate, nitrates, ammonia, sodium chloride, black carbon, mineral dust and water [4].

Several investigators have assessed the effect of air pollution as a potential risk factor for COPD. In children and young adults, cross-sectional studies have shown a relationship between higher outdoor pollutant levels (especially traffic related pollution) and lower lung function [65, 66]. Kulkarni et al. reported a likely causative dose-dependent inverse association between the carbon content (as a biomarker of particulate matter exposure, PM10) of airway macrophages with lung function in children [67]. Furthermore, exposure to traffic-related pollution, indicated by residential distance from a highway, was associated with impaired lung growth and lung function deficits at 18 years of age [68]. Also, higher traffic density and proximity to highways was significantly associated with lower lung function (FEV1) and FVC, but only in females [69], who are also at a greater risk of developing COPD than for those living farther away [70].

Long-term exposure to airborne particles and particulate matter is significantly associated with the risk of premature death and acute care hospitalizations, especially in patients with severe disease [71, 72]. Moreover, daily variation in exposure to outdoor air pollution (mainly the particulate matter) significantly correlates with acute exacerbations of COPD [73]. The mechanisms that underlie obstruction due to air pollution are likely to be similar to those caused by cigarette smoking, but we do not yet have conclusive evidence for this, despite the detrimental effects of air pollution on lung health.

Occupational exposure to dusts and fumes

Several longitudinal studies have shown an association between certain dusty occupational exposures and COPD, i.e., coal mining [74], gold mining [75], work related to tunnel-construction [76], low levels of concrete dust containing crystalline silica exposure (concrete production industries) [77], exposure to cotton in textile industries [78], workers exposed to welding fumes [79], grain handlers and postal workers (exposure to endotoxins) [80] and animal feed industry [81]. Moreover, chronic exposure to metallic dust (primarily, cobalt and chromium) was found to be associated with deterioration of lung function [82]. In addition, exposure to chemical vapors, irritants and fumes can also contribute to accelerated loss of airflow [83]. Another study involving railroad workers reported a positive association between COPD mortality and occupational exposure to diesel exhaust [84]. A population-based study found positive associations between several occupational exposure measures (mineral dusts, metal dusts and fumes, organic dusts, irritant gases or vapors, sensitizers, organic solvents, diesel exhaust, and environmental tobacco smoke) with COPD, among both ever-smokers and never-smokers [85].

Experimental studies in animal models have demonstrated that exposures to several agents, such as sulphur dioxide, mineral dusts, vanadium and endotoxin, are capable of inducing chronic obstructive bronchitis [83]. Intratracheally instilled silica (quartz) produces airflow obstruction (functional change), which correlates with the presence of both emphysema and small-airway lesions [86]. Inorganic dusts containing silica are also associated with neutrophil and macrophage accumulation and morphological changes in the rat lung [86]. These morphological changes in small airways and lung parenchyma were similar to those in rats treated with elastase, which represents a well-established model of experimental COPD [87].

Mechanisms of lung damage due to biomass smoke exposure

Despite the immense burden of chronic airway disease, only a limited number of mechanistic studies have examined the immunomodulatory effects of biomass smoke exposure. Sussan et al. explored the mechanisms of pulmonary responses in mice after acute (6 and 24 h) or sub-chronic (3 times a week for 8 weeks) exposure to wood or cow dung PM [17]. Acute exposure to wood smoke elicited a stronger pro-inflammatory response, as indicated by increased expression of G-CSF, Keratinocyte chemoattractant (KC), C-X-C motif chemokine 10 (CXCL10), IL-6, TNFα and interleukin 12 p70 subunit (IL12p70) [17]. The induction of pro-inflammatory cytokine expression was higher with cow dung than wood smoke PM [17]. On the other hand, sub-chronic exposures exhibited differences in pulmonary response, where wood smoke elicited an eosinophilic response in contrast to a predominantly neutrophilic response induced by cow dung smoke [17]. The inflammatory response elicited by both wood and cow dung smoke was mediated via nuclear factor kappa B (NF-κB) signaling [17]. In addition, in an in vitro study, c-Jun N-terminal kinase-activator protein-1 (JNK-AP-1) signaling, and not the NFκB regulatory pathway, was found to be involved in mediating inflammatory responses in human primary small airway epithelial cells upon exposure to dung biomass smoke [88].

Moreover, in a case–control study conducted in India with 142 biomass users and 126 age-matched LPG user women, a significant neutrophilic inflammatory response was observed in the biomass using group [89]. Also, compared to LPG users, reactive oxygen species (ROS) generation by leukocytes (in both blood and sputum) and the systemic level of antioxidant enzyme superoxide dismutase (SOD) were higher and lower, respectively in women using biomass fuel [89]. A similar increase in systemic oxidative stress was reported in rats exposed to biomass smoke, as indicated by an increased plasma level of malondialdehyde and a reduced level of SOD [90]. Several in vitro studies reported depletion of antioxidants, such as ascorbate, urate and reduced glutathione in respiratory tract lining fluid when incubated with wood and animal dung smoke extracts [16, 91]. Therefore, biomass smoke exposure induces inflammation and oxidative stress mediated lung damage which potentially contributes to the development/progression of COPD.

In terms of lung cancer, biomass smoke induced ROS directly damages DNA and promotes lung cell proliferation and turnover, resulting in fibrosis and development of lung tumours in rats [92]. Furthermore, biomass exposure upregulates the production of extracellular matrix proteins, including perlecan and fibronectin with a capacity to induce fibrosis in cultured cells [93]. In addition, PAHs released by incomplete combustion of biomass fuels are evidently carcinogenic in both in vitro and in vivo studies [9497]. Metabolism of PAHs leads to the formation of active carcinogens diol-epoxides, radical cations and o-quinones [94, 98]. These activated PAH metabolites can form adducts with DNA, resulting in mutations, alteration of gene expression profiles, and tumorigenesis [94]. Gene ‘hotspots’ for adduct formation by PAH metabolites include oncogenes such as p53, K-ras and the H-ras [99, 100]. PAH-DNA adducts are associated with a two-fold increased risk of lung cancer [101].

Biomass smoke exposure is also implicated in increased susceptibility to bacterial infection through several mechanisms, including alterations in alveolar macrophage phagocytosis and/or upregulation of host surface receptors on the respiratory epithelium [102, 103]. In an in vitro study, the phagosomal function of wood smoke particle exposed human alveolar macrophages was tested with respect to uptake of fluorescently-labelled beads, Streptococcus pneumoniae and Mycobacterium tuberculosis [102]. Wood smoke exposed macrophages demonstrated reduced phagocytosis of fluorescent beads, S. pneumoniae and M. tuberculosis with a negative linear correlation between macrophage particulate content and phagocytosis [104]. Furthermore, oxidative stress is believed to upregulate expression of intercellular adhesion molecule-1 (ICAM-1), and platelet activating factor receptors (PAFR) allowing attachment and invasion of respiratory bacteria, including S. pneumoniae, Haemophilus influenzae and Pseudomonas aeruginosa, which are also important bacterial pathogens in COPD [105107]. Although airway ICAM-1 and PAFR expression were markedly upregulated in tobacco smokers and COPD patients, further studies are warranted to demonstrate the effect of biomass smoke exposure on inducing the expression of these host surface receptors [108110]. Recently, KC et al. developed a method to generate batches of biomass smoke extracts that can be preserved for longer periods for use in multiple exposure experiments, thus minimizing inter-assay variation [103]. This will facilitate further research on mechanistic role of smoke extracts in the inflammatory response and the pathogenesis of respiratory diseases including COPD, lung cancer and LRI.

Preventive and therapeutic measures

Biomass smoke is one of the major risk factors for the onset/progression of COPD in developing countries [61]. To reduce the exposure to smoke generated from combustion of biomass fuel, several preventive interventions have been recommended, with some already implemented.

Based on previous intervention studies, the use of efficient cooking stoves and the promotion of cleaner fuel use (e.g., biogas, liquefied petroleum gas and electricity) has been effective in preventing biomass smoke exposure, at least to some extent [111113]. The use of improved cooking stoves (ICS) has been found to reduce the mean PM2.5 levels by 63.2% in Nepal, 37.0% Senegal, 32.8% in the Gambia and 18–45% in Kenya [111, 112, 114]. Although the decrease in mean PM2.5 levels was significantly high, none of the improved cooking stoves achieved the WHO guideline level of mean kitchen PM2.5 of 25 µg/m3 for 24-h. A recent 9-year prospective cohort study in China evaluated the effect of intervention with improved cooking fuels and kitchen intervention [113]. Use of clean fuels and improved ventilation were associated with a lower decline in FEV1 (12 mL/year, 4–20 mL/year versus 13 mL/year, 4–23 mL/year) compared to those with neither intervention, after adjusting for confounders [113]. In addition, the duration of improved fuel use and ventilation was negatively correlated with the decline of FEV1 (p < 0.05) [113]. Moreover, the fuel and ventilation improvement intervention were associated with a reduction in the risk of COPD, with an odds ratio of 0.28 (95% CI, 0.11–0.73) [113]. Despite the perception that biomass is a cheap fuel source, the annual health-related cost per household associated with biomass smoke exposure (16.94 USD) in Nepal is 61.3% higher than the annual cost of biogas usage (10.38 USD), an alternative cleaner fuel [14]. In addition, the findings of the study suggest that providing community education and creating rural employment and income generation opportunities are important measures in promoting the sustainable use of clean fuels [14].

In terms of therapeutic intervention, exposure to household and outdoor air pollutants are found to reduce antioxidant defense by decreasing the levels of ascorbate, urate, SOD and reduced glutathione resulting in inflammation of the airways [115]. Antioxidants and anti-inflammatory drugs are potential therapeutics for the prevention of biomass smoke induced inflammation-mediated lung injury [116, 117]. Based on the evidence that wood and cow dung smoke upregulated the expression of PAFR on human bronchial epithelial cells, we believe that the induction of microbial adhesion receptors on respiratory epithelia could be targeted therapeutically to prevent LRIs. Several in vitro studies have shown that the use of PAFR antagonists such as CV-3988 and WEB-2086 abrogates the adhesion of S. pneumoniae and nontypeable H. influenzae to cigarette smoke exposed human bronchial and alveolar epithelial cells [118, 119]. In addition, ICAM-1, a major receptor for rhinoviruses and nontypeable H. influenzae could be another important target with therapeutic potential [120, 121]. However, we stress the point that further research is needed to elucidate the mechanisms of biomass smoke induced susceptibility to LRI, as well as development of COPD and lung cancer. But while new therapeutics may be possible with regard to reducing the progression or symptoms of biomass smoke-related lung disease, the major focus needs to be maintained on a global reduction in the exposure of human populations to biomass smoke.

Strengths and limitations

There are several strengths of our review. Our narrative review comes at a time when the United Nations and the World Health Organization have specifically focused on the urgent need to limit non-communicable diseases, which has also garnered support from various Heads-of-Countries and Governments [122]. In addition, we have examined the epidemiology of non-cigarette smoke etiologies (biomass smoke, air pollution and multiple occupational exposures) implicated in heightened risk of developing a range of lung diseases, most notably, COPD, lung cancer and respiratory infections. We have reviewed and summarized potential mechanisms involved in the pathogenesis of non-cigarette smoke exposure and lung disease. Finally, we have highlighted the potential preventive, as well as therapeutic strategies to limit lung diseases related to these exposures.

One of the limitations is that there may be variability across epidemiological studies in terms of data collection and analyses. In particular, factors such as geographical locations, sampling points within a city as well as multiple cities in a specific country, the type of sampling (longitudinal versus one time-point sampling) contributes significantly to heterogeneity of results obtained. In addition, participant recruitment criteria (i.e., from general population or community healthcare centers), reliability of self-reported duration of exposure are crucial factors that need to be standardized globally. Notably, variability of spirometry technique and the threshold cut-off for COPD (i.e., FEV1/FVC < 0.70 or FEV1/FVC < LLN) vary across studies. In addition, it is difficult to tease out contributions of individual exposure(s)-related causations and hence the results may represent disease associated with mixed exposures. The heterogeneity in future epidemiological studies could be addressed by utilizing standardized and validated research methodologies/strategies to ascertain burden of lung diseases associated with non-cigarette smoke exposures. We are not concluding direct causation of lung diseases due to non-cigarette smoke exposures in our review; however, our intent was to direct policymakers and researchers towards the possible mechanisms reported to date. Clearly, focused and detailed mechanistic studies are needed to establish direct causation of non-cigarette smoke exposures and lung pathologies, which should be further validated in large-scale epidemiological studies, as well as mechanistic models of experimental animal models. Finally, we limited our analysis to published literature and did not include media/analytical reports from recently initiated preventive strategies (such as Ujjwala yojana in India; [123]). However, this could be followed up once the government reports are released by various countries.

Summary and conclusions

The prevalence of COPD amongst non-smokers is a worrying concern globally, as almost half the World’s population is chronically exposed to biomass smoke, air pollution and other exposures (chemicals, dusts, and fumes). Evidently, low socio-economic status drives large sections of societies living in low- and middle-income countries towards biomass fuels for cooking/heating purposes. In addition, poor awareness about respiratory health and lack of implementation of adequate safety measures (e.g., poorly ventilated homes) predispose these individuals to heightened risk of developing biomass smoke-induced lung diseases, including COPD, lung cancer and respiratory infections. Chronic biomass smoke (and other non-cigarette exposures) delivers deleterious compounds (PMs, PAHs etc.) that activate an inflammatory cascade in the lungs, which may potentially spill over systemically. This is coupled with marked immune cell dysfunction, activation of oncogenes and upregulation of microbial receptors in the respiratory tract, which contribute to onset/progression of COPD and other related diseases (lung cancer and infections). Preventive strategies should include awareness about the long-term health benefits of using cleaner fuels over biomass-fuels, use of more efficient cooking equipment, and the importance of adequate ventilation in low socioeconomic localities. Although research has only begun to unravel the underlying molecular and pathological mechanisms involved in biomass smoke-induced COPD, anti-oxidants, anti-inflammatory and anti-microbial drugs may be promising new therapeutics to limit the effects of non-smoking related COPD.

Abbreviations

AP-1: 

activator protein 1

CI: 

confidence interval

COPD: 

chronic obstructive pulmonary disease

CS: 

cross-sectional study

CPH: 

China Pulmonary Health

CT: 

computed tomography

CXCL10: 

C-X-C motif chemokine 10

DNA: 

deoxyribonucleic acid

ECRHS: 

European Community Respiratory Health Survey

FEV1

forced expiratory volume in one second

FVC: 

forced vital capacity

OR: 

odds ratio

G-CSF: 

granulocyte colony-stimulating factor

HR: 

hazard ratio

ICAM-1: 

intercellular adhesion molecule-1

ICS: 

improved cook stoves

IL-12p70: 

interleukin 12 p70 subunit

IL-6: 

interleukin 6

JNK: 

c-Jun N-terminal kinase

KC: 

keratinocyte chemoattractant

LPG: 

liquefied petroleum gas

LRI: 

lower respiratory tract infection

NFkB: 

nuclear factor kappa B

PAFR: 

platelet activating factor receptor

PAHs: 

polycyclic aromatic hydrocarbons

PM: 

particulate matter

PRM: 

parametric response mapping

PUMA: 

Prevalence Study and Regular Practice, Diagnosis, and Treatment Among General Practitioners in Populations at Risk of COPD in Latin America

ROS: 

reactive oxygen species

SOD: 

superoxide dismutase

TB: 

tuberculosis

TNFα: 

tumour necrosis factor alpha

VOCS: 

volatile organic compounds

WHO: 

World Health Organization

Declarations

Authors’ contributions

SDS and RFOT conceived the review. RKC, SDS, SSG, and RFOT drafted the review. RKC, SSG and RFOT revised the review for submission. All authors read and approved the final manuscript.

Acknowledgements

RKC is a recipient of Tasmania Graduate Research Scholarship.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

Not applicable to this manuscript.

Consent for publication

This declaration is not applicable to this manuscript.

Ethics approval and consent to participate

This declaration is not relevant to this manuscript.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
School of Medicine, College of Health and Medicine, University of Tasmania, Hobart, Tasmania, Australia
(2)
Department of Clinical Microbiology, School of Medicine, Trinity College Dublin, Dublin, Ireland
(3)
Priority Research Centre for Healthy Lungs, Hunter Medical Research Institute, School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, Australia
(4)
Centenary Institute and University of Technology Sydney, Sydney, New South Wales, Australia

References

  1. World Health Organisation (2018) Disease burden and mortality estimates. Cause-specific mortality, 2000–2016. WHO, Geneva. http://www.who.int/healthinfo/global_burden_disease/estimates/en/. Accessed 11 Aug 2018
  2. World Health Organisation (2018) Tobacco; key facts. WHO, Geneva. http://www.who.int/en/news-room/fact-sheets/detail/tobacco. Accessed 06 Aug 2018
  3. World Health Organisation (2018) Prevalence of tobacco smoking. WHO, Geneva. http://www.who.int/gho/tobacco/use/en/. Accessed 29 July 2018
  4. World Health Organisation (2018) Ambient (outdoor) air quality and health. WHO, Geneva. http://www.who.int/news-room/fact-sheets/detail/ambient-(outdoor)-air-quality-and-health. Accessed 06 Aug 2018
  5. Hu G, Zhou Y, Tian J, Yao W, Li J, Li B et al (2010) Risk of COPD from exposure to biomass smoke: a metaanalysis. Chest 138(1):20–31View ArticlePubMedGoogle Scholar
  6. Montes de Oca M, Zabert G, Moreno D, Laucho-Contreras ME, Lopez Varela MV, Smoke Surmont F (2017) Biomass exposure, and COPD risk in the primary care setting: The PUMA Study. Respiratory care. 62(8):1058–1066View ArticlePubMedGoogle Scholar
  7. World Health Organisation (2018) Household air pollution and health. WHO, Geneva. http://www.who.int/news-room/fact-sheets/detail/household-air-pollution-and-health. Accessed 06 Aug 2018
  8. Global Health Observatory Map Gallery; Map on “World: Proportion of population with primary reliance on clean fuels (%), 2014”. Geneva: World Health Organisation; 2014. http://gamapserver.who.int/mapLibrary/Files/Maps/Global_CleanFuels_2014.png. Accessed 31 Aug 2018
  9. Hall DO, Barnard GW, Moss P (2013) Biomass for energy in the developing countries: current role, potential, problems, prospects. Elsevier, AmsterdamGoogle Scholar
  10. Leavey A, Patel S, Martinez R, Mitroo D, Fortenberry C, Walker M et al (2017) Organic and inorganic speciation of particulate matter formed during different combustion phases in an improved cookstove. Environ Res 158:33–42View ArticlePubMedGoogle Scholar
  11. Xing YF, Xu YH, Shi MH, Lian YX (2016) The impact of PM2.5 on the human respiratory system. J Thorac Dis. 8(1):E69–E74PubMedPubMed CentralGoogle Scholar
  12. World Health Organisation (2006) WHO Air quality guidelines for particulate matter, ozone, nitrogen dioxide and sulfur dioxide; Global update 2005. WHO, Geneva. http://apps.who.int/iris/bitstream/handle/10665/69477/WHO_SDE_PHE_OEH_06.02_eng.pdf?sequence=1. Accessed 11 Aug 2018
  13. Saksena STL, Smith KR (2003) Database of household air pollution studies in developing countries, protection of the human environment. World Health Organization, GenevaGoogle Scholar
  14. Pant KP (2012) Cheaper fuel and higher health costs among the poor in rural Nepal. Ambio 41(3):271–283View ArticlePubMedGoogle Scholar
  15. Pahla G, Mamvura T, Ntuli F, Muzenda E (2017) Energy densification of animal waste lignocellulose biomass and raw biomass. S Afr J Chem Eng 24:168–175Google Scholar
  16. Mudway IS, Duggan ST, Venkataraman C, Habib G, Kelly FJ, Grigg J (2005) Combustion of dried animal dung as biofuel results in the generation of highly redox active fine particulates. Part Fibre Toxicol 2:6View ArticlePubMedPubMed CentralGoogle Scholar
  17. Sussan TE, Ingole V, Kim JH, McCormick S, Negherbon J, Fallica J et al (2014) Source of biomass cooking fuel determines pulmonary response to household air pollution. Am J Respir Cell Mol Biol 50(3):538–548View ArticlePubMedPubMed CentralGoogle Scholar
  18. Naeher LP, Brauer M, Lipsett M, Zelikoff JT, Simpson CD, Koenig JQ et al (2007) Woodsmoke health effects: a review. Inhalation Toxicol 19(1):67–106View ArticleGoogle Scholar
  19. Environmental Issues: Energy Use and Conservation Canberra: Australian Bureau of Statistics; 2014. http://www.abs.gov.au/ausstats/abs@.nsf/mf/4602.0.55.001. Accessed 03 Dec 2014
  20. Rogalsky DK, Mendola P, Metts TA, Martin WJ 2nd (2014) Estimating the number of low-income americans exposed to household air pollution from burning solid fuels. Environ Health Perspect 122(8):806–810View ArticlePubMedPubMed CentralGoogle Scholar
  21. Reisen F, Brown SK (2009) Australian firefighters’ exposure to air toxics during bushfire burns of autumn 2005 and 2006. Environ Int 35(2):342–352View ArticlePubMedGoogle Scholar
  22. da Silva LF, Saldiva SR, Saldiva PH, Dolhnikoff M (2012) Impaired lung function in individuals chronically exposed to biomass combustion. Environ Res 112:111–117View ArticlePubMedGoogle Scholar
  23. Mukherjee S, Roychoudhury S, Siddique S, Banerjee M, Bhattacharya P, Lahiri T et al (2014) Respiratory symptoms, lung function decrement and chronic obstructive pulmonary disease in pre-menopausal Indian women exposed to biomass smoke. Inhalation Toxicol 26(14):866–872View ArticleGoogle Scholar
  24. Regalado J, Perez-Padilla R, Sansores R, Paramo Ramirez JI, Brauer M, Pare P et al (2006) The effect of biomass burning on respiratory symptoms and lung function in rural Mexican women. Am J Respir Crit Care Med 174(8):901–905View ArticlePubMedGoogle Scholar
  25. Zou Y, Li S, Zou W, Hu G, Zhou Y, Peng G et al (2014) Upregulation of gelatinases and epithelial-mesenchymal transition in small airway remodeling associated with chronic exposure to wood smoke. PLoS ONE 9(5):e96708View ArticlePubMedPubMed CentralGoogle Scholar
  26. Olloquequi J, Silva OR (2016) Biomass smoke as a risk factor for chronic obstructive pulmonary disease: effects on innate immunity. Innate Immunity. 22(5):373–381View ArticlePubMedGoogle Scholar
  27. Ramos D, Proenca M, Leite MR, Ferreira AD, Trevisan IB, Brigida GFS et al (2017) Effects of exposure to biomass burning on pulmonary inflammatory markers and pulmonary function in individuals with COPD. Rev Port de Pneumol 23(5):273–279Google Scholar
  28. Wang C, Xu J, Yang L, Xu Y, Zhang X, Bai C et al (2018) Prevalence and risk factors of chronic obstructive pulmonary disease in China (the China Pulmonary Health [CPH] study): a national cross-sectional study. Lancet 391(10131):1706–1717View ArticlePubMedGoogle Scholar
  29. Sana A, Somda SMA, Meda N, Bouland C (2018) Chronic obstructive pulmonary disease associated with biomass fuel use in women: a systematic review and meta-analysis. BMJ Open Respir Res 5(1):e000246View ArticlePubMedPubMed CentralGoogle Scholar
  30. Camp PG, Ramirez-Venegas A, Sansores RH, Alva LF, McDougall JE, Sin DD et al (2014) COPD phenotypes in biomass smoke-versus tobacco smoke-exposed Mexican women. Eur Respir J 43(3):725–734View ArticlePubMedGoogle Scholar
  31. Rivera RM, Cosio MG, Ghezzo H, Salazar M, Perez-Padilla R (2008) Comparison of lung morphology in COPD secondary to cigarette and biomass smoke. Inte J Tuberc Lung Dis 12(8):972–977Google Scholar
  32. Fernandes L, Gulati N, Fernandes Y, Mesquita AM, Sardessai M, Lammers JJ et al (2017) Small airway imaging phenotypes in biomass- and tobacco smoke-exposed patients with COPD. ERJ Open Res. 3(2):00124–2016View ArticlePubMedPubMed CentralGoogle Scholar
  33. Cerveri I, Accordini S, Verlato G, Corsico A, Zoia MC, Casali L et al (2001) Variations in the prevalence across countries of chronic bronchitis and smoking habits in young adults. Eur Res J 18(1):85–92View ArticleGoogle Scholar
  34. Gunen H, Hacievliyagil SS, Yetkin O, Gulbas G, Mutlu LC, Pehlivan E (2008) Prevalence of COPD: first epidemiological study of a large region in Turkey. Eur J Intern Med 19(7):499–504View ArticlePubMedGoogle Scholar
  35. Ehrlich RI, White N, Norman R, Laubscher R, Steyn K, Lombard C et al (2004) Predictors of chronic bronchitis in South African adults. Int J Tuberc Lung Dis 8(3):369–376PubMedGoogle Scholar
  36. Magitta NF, Walker RW, Apte KK, Shimwela MD, Mwaiselage JD, Sanga AA et al (2018) Prevalence, risk factors and clinical correlates of COPD in a rural setting in Tanzania. Eur Respir J. 51(2):1700182View ArticlePubMedGoogle Scholar
  37. Hagstad S, Backman H, Bjerg A, Ekerljung L, Ye X, Hedman L et al (2015) Prevalence and risk factors of COPD among never-smokers in two areas of Sweden–Occupational exposure to gas, dust or fumes is an important risk factor. Respir Med 109(11):1439–1445View ArticlePubMedGoogle Scholar
  38. Thomsen M, Nordestgaard BG, Vestbo J, Lange P (2013) Characteristics and outcomes of chronic obstructive pulmonary disease in never smokers in Denmark: a prospective population study. Lancet Respir Med. 1(7):543–550View ArticlePubMedGoogle Scholar
  39. Landis SH, Muellerova H, Mannino DM, Menezes AM, Han MK, van der Molen T et al (2014) Continuing to Confront COPD International Patient Survey: methods, COPD prevalence, and disease burden in 2012-2013. Int J Chronic Obstr Pulm Dis 9:597–611Google Scholar
  40. International Agency for Research on Cancer (2010) Household use of solid fuels and high-temperature frying. International Agency for Research on Cancer, LyonGoogle Scholar
  41. Baez-Saldana R, Rumbo-Nava U, Canseco-Raymundo A, Castillo-Gonzalez P, Leon-Duenas S, Rivera-Rosales R et al (2018) 35PD Magnitude of exposure to biomass fuel smoke and risk of lung cancer in women: cases and controls study. J Thorac Oncol 13(4):S20View ArticleGoogle Scholar
  42. Bruce N, Dherani M, Liu R, Hosgood HD, Sapkota A, Smith KR et al (2015) Does household use of biomass fuel cause lung cancer? A systematic review and evaluation of the evidence for the GBD 2010 study. Thorax. 70:433–441View ArticlePubMedGoogle Scholar
  43. Barone-Adesi F, Chapman RS, Silverman DT, He X, Hu W, Vermeulen R et al (2012) Risk of lung cancer associated with domestic use of coal in Xuanwei, China: retrospective cohort study. BMJ 345:e5414View ArticlePubMedPubMed CentralGoogle Scholar
  44. Kurmi OP, Arya PH, Lam K-BH, Sorahan T, Ayres JG (2012) Lung cancer risk and solid fuel smoke exposure: a systematic review and meta-analysis. Eur Respir J 40(5):1228–1237View ArticlePubMedGoogle Scholar
  45. Bellemare F, Jeanneret A, Couture J (2003) Sex differences in thoracic dimensions and configuration. Am J Respir Crit Care Med 168(3):305–312View ArticlePubMedGoogle Scholar
  46. Petrilli FL, Kanitz S (1971) Medico-social aspects of air pollution. Minerva Med 62(18):870–923PubMedGoogle Scholar
  47. Naghavi M, Abajobir AA, Abbafati C, Abbas KM, Abd-Allah F, Abera SF, Aboyans V, Adetokunboh O, Afshin A, Agrawal A, Ahmadi A (2017) Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 390(10100):1151–1210View ArticleGoogle Scholar
  48. Smith KR, Samet JM, Romieu I, Bruce N (2000) Indoor air pollution in developing countries and acute lower respiratory infections in children. Thorax 55(6):518–532View ArticlePubMedPubMed CentralGoogle Scholar
  49. Mishra V (2003) Indoor air pollution from biomass combustion and acute respiratory illness in preschool age children in Zimbabwe. Int J Epidemiol 32(5):847–853View ArticlePubMedGoogle Scholar
  50. Sonego M, Pellegrin MC, Becker G, Lazzerini M (2015) Risk factors for mortality from acute lower respiratory infections (ALRI) in children under five years of age in low and middle-income countries: a systematic review and meta-analysis of observational studies. PLoS ONE 10(1):e0116380View ArticlePubMedPubMed CentralGoogle Scholar
  51. Ezzati M, Kammen D (2001) Indoor air pollution from biomass combustion and acute respiratory infections in Kenya: an exposure-response study. Lancet 358(9282):619–624View ArticlePubMedGoogle Scholar
  52. Loeb M, Neupane B, Walter SD, Hanning R, Carusone SC, Lewis D et al (2009) Environmental risk factors for community-acquired pneumonia hospitalization in older adults. J Am Geriatr Soc 57(6):1036–1040View ArticlePubMedGoogle Scholar
  53. Shrestha IL, Shrestha SL (2005) Indoor air pollution from biomass fuels and respiratory health of the exposed population in Nepalese households. Int J Occup Environ Health 11(2):150–160View ArticlePubMedGoogle Scholar
  54. Taylor ET, Nakai S (2012) Prevalence of acute respiratory infections in women and children in Western Sierra Leone due to smoke from wood and charcoal stoves. Int J Environ Res Public Health 9(6):2252–2265View ArticlePubMedPubMed CentralGoogle Scholar
  55. Kilabuko JH, Matsuki H, Nakai S (2007) Air quality and acute respiratory illness in biomass fuel using homes in Bagamoyo, Tanzania. Int J Environ Res Public Health 4(1):39–44View ArticlePubMedPubMed CentralGoogle Scholar
  56. Oluwole O, Arinola GO, Huo D, Olopade CO (2017) Household biomass fuel use, asthma symptoms severity, and asthma underdiagnosis in rural schoolchildren in Nigeria: a cross-sectional observational study. BMC Pulm Med 17(1):3View ArticlePubMedPubMed CentralGoogle Scholar
  57. Po JY, FitzGerald JM, Carlsten C (2011) Respiratory disease associated with solid biomass fuel exposure in rural women and children: systematic review and meta-analysis. Thorax 66(3):232–239View ArticlePubMedGoogle Scholar
  58. Diaz JV, Koff J, Gotway MB, Nishimura S, Balmes JR (2006) Case report: a case of wood-smoke-related pulmonary Disease. Environ Health Perspect 114(5):759–762View ArticlePubMedPubMed CentralGoogle Scholar
  59. Gold JA, Jagirdar J, Hay JG, Addrizzo-Harris DJ, Naidich DP, Rom WN (2000) Hut lung. A domestically acquired particulate lung disease. Medicine 79(5):310–317View ArticlePubMedGoogle Scholar
  60. Grobbelaar JP, Bateman ED (1991) Hut lung: a domestically acquired pneumoconiosis of mixed aetiology in rural women. Thorax 46(5):334–340View ArticlePubMedPubMed CentralGoogle Scholar
  61. Salvi SS, Barnes PJ (2009) Chronic obstructive pulmonary disease in non-smokers. Lancet 374(9691):733–743View ArticlePubMedGoogle Scholar
  62. Chan KY, Li X, Chen W, Song P, Wong NWK, Poon AN et al (2017) Prevalence of chronic obstructive pulmonary disease (COPD) in China in 1990 and 2010. J Glob Health 7(2):020704View ArticlePubMedPubMed CentralGoogle Scholar
  63. Eisner MD, Anthonisen N, Coultas D, Kuenzli N, Perez-Padilla R, Postma D et al (2010) An official American Thoracic Society public policy statement: novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 182(5):693–718View ArticlePubMedGoogle Scholar
  64. Donaldson K, Brown D, Clouter A, Duffin R, MacNee W, Renwick L et al (2002) The pulmonary toxicology of ultrafine particles. J Aerosol Med 15(2):213–220View ArticlePubMedGoogle Scholar
  65. Holguin F, Flores S, Ross Z, Cortez M, Molina M, Molina L et al (2007) Traffic-related exposures, airway function, inflammation, and respiratory symptoms in children. Am J Respir Crit Care Med 176(12):1236–1242View ArticlePubMedGoogle Scholar
  66. Janssen NA, Brunekreef B, van Vliet P, Aarts F, Meliefste K, Harssema H et al (2003) The relationship between air pollution from heavy traffic and allergic sensitization, bronchial hyperresponsiveness, and respiratory symptoms in Dutch schoolchildren. Environ Health Perspect 111(12):1512–1518View ArticlePubMedPubMed CentralGoogle Scholar
  67. Kulkarni N, Pierse N, Rushton L, Grigg J (2006) Carbon in airway macrophages and lung function in children. N Engl J Med 355(1):21–30View ArticlePubMedGoogle Scholar
  68. Gauderman WJ, Vora H, McConnell R, Berhane K, Gilliland F, Thomas D et al (2007) Effect of exposure to traffic on lung development from 10 to 18 years of age: a cohort study. Lancet 369(9561):571–577View ArticlePubMedGoogle Scholar
  69. Kan H, Heiss G, Rose KM, Whitsel E, Lurmann F, London SJ (2007) Traffic exposure and lung function in adults: the Atherosclerosis Risk in Communities study. Thorax 62(10):873–879View ArticlePubMedPubMed CentralGoogle Scholar
  70. Schikowski T, Sugiri D, Ranft U, Gehring U, Heinrich J, Wichmann HE et al (2005) Long-term air pollution exposure and living close to busy roads are associated with COPD in women. Respir Res 6:152View ArticlePubMedPubMed CentralGoogle Scholar
  71. Wordley J, Walters S, Ayres JG (1997) Short term variations in hospital admissions and mortality and particulate air pollution. Occup Environ Med 54(2):108–116View ArticlePubMedPubMed CentralGoogle Scholar
  72. Zanobetti A, Bind MA, Schwartz J (2008) Particulate air pollution and survival in a COPD cohort. Environ Health 7:48View ArticlePubMedPubMed CentralGoogle Scholar
  73. Sunyer J (2001) Urban air pollution and chronic obstructive pulmonary disease: a review. Eur Respir J 17(5):1024–1033View ArticlePubMedGoogle Scholar
  74. Attfield MD (1985) Longitudinal decline in FEV1 in United States coalminers. Thorax 40(2):132–137View ArticlePubMedPubMed CentralGoogle Scholar
  75. Gantt RC, Lincoln JE (1988) Determinants of chronic bronchitis and lung dysfunction in Western Australian gold miners. Br J Ind Med 45(7):503PubMedPubMed CentralGoogle Scholar
  76. Ulvestad B, Bakke B, Eduard W, Kongerud J, Lund MB (2001) Cumulative exposure to dust causes accelerated decline in lung function in tunnel workers. Occup Environ Med 58(10):663–669View ArticlePubMedPubMed CentralGoogle Scholar
  77. Meijer E, Kromhout H, Heederik D (2001) Respiratory effects of exposure to low levels of concrete dust containing crystalline silica. Am J Ind Med 40(2):133–140View ArticlePubMedGoogle Scholar
  78. Niven RM, Fletcher AM, Pickering CA, Fishwick D, Warburton CJ, Simpson JC et al (1997) Chronic bronchitis in textile workers. Thorax 52(1):22–27View ArticlePubMedPubMed CentralGoogle Scholar
  79. Bradshaw LM, Fishwick D, Slater T, Pearce N (1998) Chronic bronchitis, work related respiratory symptoms, and pulmonary function in welders in New Zealand. Occup Environ Med 55(3):150–154View ArticlePubMedPubMed CentralGoogle Scholar
  80. Schwartz DA, Thorne PS, Yagla SJ, Burmeister LF, Olenchock SA, Watt JL et al (1995) The role of endotoxin in grain dust-induced lung disease. Am J Respir Crit Care Med 152(2):603–608View ArticlePubMedGoogle Scholar
  81. Post W, Heederik D, Houba R (1998) Decline in lung function related to exposure and selection processes among workers in the grain processing and animal feed industry. Occup Environ Med 55(5):349–355View ArticlePubMedPubMed CentralGoogle Scholar
  82. Hamzah NA, Mohd Tamrin SB, Ismail NH (2016) Metal dust exposure and lung function deterioration among steel workers: an exposure-response relationship. Int J Occup Environ Health 22(3):224–232View ArticlePubMedPubMed CentralGoogle Scholar
  83. Boschetto P, Quintavalle S, Miotto D, Lo Cascio N, Zeni E, Mapp CE (2006) Chronic obstructive pulmonary disease (COPD) and occupational exposures. J Occup Med Toxicol 1:11View ArticlePubMedPubMed CentralGoogle Scholar
  84. Hart JE, Laden F, Schenker MB, Garshick E (2006) Chronic obstructive pulmonary disease mortality in diesel-exposed railroad workers. Environ Health Perspect 114(7):1013–1017View ArticlePubMedPubMed CentralGoogle Scholar
  85. Weinmann S, Vollmer WM, Breen V, Heumann M, Hnizdo E, Villnave J et al (2008) COPD and occupational exposures: a case-control study. J Occup Environ Med 50(5):561–569View ArticlePubMedGoogle Scholar
  86. Wright JL, Harrison N, Wiggs B, Churg A (1988) Quartz but not iron oxide causes air-flow obstruction, emphysema, and small airways lesions in the rat. Am Rev Respir Dis 138(1):129–135View ArticlePubMedGoogle Scholar
  87. Churg A, Hobson J, Wright J (1989) Functional and morphologic comparison of silica- and elastase-induced airflow obstruction. Exp Lung Res 15(6):813–822View ArticlePubMedGoogle Scholar
  88. McCarthy CE, Duffney PF, Gelein R, Thatcher TH, Elder A, Phipps RP et al (2016) Dung biomass smoke activates inflammatory signaling pathways in human small airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 311(6):L1222–L1233View ArticlePubMedPubMed CentralGoogle Scholar
  89. Banerjee A, Mondal NK, Das D, Ray MR (2012) Neutrophilic inflammatory response and oxidative stress in premenopausal women chronically exposed to indoor air pollution from biomass burning. Inflammation. 35(2):671–683View ArticlePubMedGoogle Scholar
  90. Hu G, Zhou Y, Hong W, Tian J, Hu J, Peng G et al (2013) Development and systematic oxidative stress of a rat model of chronic bronchitis and emphysema induced by biomass smoke. Exp Lung Res 39(6):229–240View ArticlePubMedGoogle Scholar
  91. Kurmi OP, Dunster C, Ayres JG, Kelly FJ (2013) Oxidative potential of smoke from burning wood and mixed biomass fuels. Free Radic Res 47(10):829–835View ArticlePubMedGoogle Scholar
  92. Warheit DB, Hansen JF, Yuen IS, Kelly DP, Snajdr SI, Hartsky MA (1997) Inhalation of high concentrations of low toxicity dusts in rats results in impaired pulmonary clearance mechanisms and persistent inflammation. Toxicol Appl Pharmacol 145(1):10–22View ArticlePubMedGoogle Scholar
  93. Krimmer D, Ichimaru Y, Burgess J, Black J, Oliver B (2013) Exposure to biomass smoke extract enhances fibronectin release from fibroblasts. PLoS ONE 8(12):e83938View ArticlePubMedPubMed CentralGoogle Scholar
  94. Moorthy B, Chu C, Carlin DJ (2015) Polycyclic aromatic hydrocarbons: from metabolism to lung cancer. Toxicol Sci 145(1):5–15View ArticlePubMedPubMed CentralGoogle Scholar
  95. Mastrangelo G, Fadda E, Marzia V (1996) Polycyclic aromatic hydrocarbons and cancer in man. Environ Health Perspect 104(11):1166–1170View ArticlePubMedPubMed CentralGoogle Scholar
  96. Siddens LK, Larkin A, Krueger SK, Bradfield CA, Waters KM, Tilton SC et al (2012) Polycyclic aromatic hydrocarbons as skin carcinogens: comparison of benzo[a]pyrene, dibenzo[def, p]chrysene and three environmental mixtures in the FVB/N mouse. Toxicol Appl Pharmacol 264(3):377–386View ArticlePubMedPubMed CentralGoogle Scholar
  97. Rengarajan T, Rajendran P, Nandakumar N, Lokeshkumar B, Rajendran P, Nishigaki I (2015) Exposure to polycyclic aromatic hydrocarbons with special focus on cancer. Asian Pac J Trop Biomed 5(3):182–189View ArticleGoogle Scholar
  98. Lim WY, Seow A (2012) Biomass fuels and lung cancer. Respirology (Carlton, Vic). 17(1):20–31View ArticleGoogle Scholar
  99. Denissenko MF, Pao A, Tang M, Pfeifer GP (1996) Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 274(5286):430–432View ArticlePubMedGoogle Scholar
  100. Ross JA, Nesnow S (1999) Polycyclic aromatic hydrocarbons: correlations between DNA adducts and ras oncogene mutations. Mutat Res 424(1–2):155–166View ArticlePubMedGoogle Scholar
  101. Peluso M, Munnia A, Hoek G, Krzyzanowski M, Veglia F, Airoldi L et al (2005) DNA adducts and lung cancer risk: a prospective study. Can Res 65(17):8042–8048View ArticleGoogle Scholar
  102. Rylance J, Fullerton DG, Scriven J, Aljurayyan AN, Mzinza D, Barrett S et al (2015) Household air pollution causes dose-dependent inflammation and altered phagocytosis in human macrophages. Am J Respir Cell Mol Biol 52(5):584–593View ArticlePubMedPubMed CentralGoogle Scholar
  103. Kc R, Zosky GR, Shukla SD, O’Toole RF (2018) A cost-effective technique for generating preservable biomass smoke extract and measuring its effect on cell receptor expression in human bronchial epithelial cells. Biol Methods Protocol 3:bpy010Google Scholar
  104. Gordon SB, Bruce NG, Grigg J, Hibberd PL, Kurmi OP, Lam KB et al (2014) Respiratory risks from household air pollution in low and middle income countries. Lancet Respir Med 2(10):823–860View ArticlePubMedPubMed CentralGoogle Scholar
  105. Roebuck KA, Rahman A, Lakshminarayanan V, Janakidevi K, Malik AB (1995) H2O2 and tumor necrosis factor-alpha activate intercellular adhesion molecule 1 (ICAM-1) gene transcription through distinct cis-regulatory elements within the ICAM-1 promoter. J Biol Chem 270(32):18966–18974View ArticlePubMedGoogle Scholar
  106. Ishizuka S, Yamaya M, Suzuki T, Nakayama K, Kamanaka M, Ida S et al (2001) Acid exposure stimulates the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells: effects on platelet-activating factor receptor expression. Am J Respir Cell Mol Biol 24(4):459–468View ArticlePubMedGoogle Scholar
  107. Kc R, Shukla SD, Walters EH, O’Toole RF (2017) Temporal upregulation of host surface receptors provides a window of opportunity for bacterial adhesion and disease. Microbiology 163(4):421–430View ArticlePubMedGoogle Scholar
  108. Shukla SD, Mahmood MQ, Weston S, Latham R, Muller HK, Sohal SS et al (2017) The main rhinovirus respiratory tract adhesion site (ICAM-1) is upregulated in smokers and patients with chronic airflow limitation (CAL). Respir Res 18(1):6View ArticlePubMedPubMed CentralGoogle Scholar
  109. Lopez-Campos JL, Calero C, Arellano-Orden E, Marquez-Martin E, Cejudo-Ramos P, Ortega Ruiz F et al (2012) Increased levels of soluble ICAM-1 in chronic obstructive pulmonary disease and resistant smokers are related to active smoking. Biomark Med 6(6):805–811View ArticlePubMedGoogle Scholar
  110. Shukla SD, Muller HK, Latham R, Sohal SS, Walters EH (2016) Platelet-activating factor receptor (PAFr) is upregulated in small airways and alveoli of smokers and COPD patients. Respirology 21(3):504–510View ArticlePubMedGoogle Scholar
  111. Singh A, Tuladhar B, Bajracharya K, Pillarisetti A (2012) Assessment of effectiveness of improved cook stoves in reducing indoor air pollution and improving health in Nepal. Energy Sustain Dev 16(4):406–414View ArticleGoogle Scholar
  112. Pilishvili T, Loo JD, Schrag S, Stanistreet D, Christensen B, Yip F et al (2016) Effectiveness of six improved cookstoves in reducing household air pollution and their acceptability in rural Western Kenya. PLoS ONE 11(11):e0165529View ArticlePubMedPubMed CentralGoogle Scholar
  113. Zhou Y, Zou Y, Li X, Chen S, Zhao Z, He F et al (2014) Lung function and incidence of chronic obstructive pulmonary disease after improved cooking fuels and kitchen ventilation: a 9-year prospective cohort study. PLoS Med 11(3):e1001621View ArticlePubMedPubMed CentralGoogle Scholar
  114. Sota CD, Lumbreras Martin J, Mazorra Aguiar J, Narros Sierra A, Fernández L, Borge García R. Effectiveness of improved cookstoves to reduce indoor air pollution in developing countries. The case of the cassamance natural subregion, western Africa. 2014Google Scholar
  115. Oluwole O, Arinola GO, Ana GR, Wiskel T, Huo D, Olopade OI et al (2013) Relationship between household air pollution from biomass smoke exposure, and pulmonary dysfunction, oxidant-antioxidant imbalance and systemic inflammation in rural women and children in Nigeria. Glob J Health Sci 5(4):28–38View ArticlePubMedPubMed CentralGoogle Scholar
  116. Rahman I (2012) Pharmacological antioxidant strategies as therapeutic interventions for COPD. Biochem Biophys Acta 1822(5):714–728PubMedGoogle Scholar
  117. Mui TS, Man SP, Sin DD (2008) Developments in drugs for the treatment of chronic obstructive pulmonary disease. Expert Rev Clin Immunol 4(3):365–377View ArticlePubMedGoogle Scholar
  118. Grigg J, Walters H, Sohal SS, Wood-Baker R, Reid DW, Xu CB et al (2012) Cigarette smoke and platelet-activating factor receptor dependent adhesion of Streptococcus pneumoniae to lower airway cells. Thorax 67(10):908–913View ArticlePubMedGoogle Scholar
  119. Shukla SD, Fairbairn RL, Gell DA, Latham RD, Sohal SS, Walters EH et al (2016) An antagonist of the platelet-activating factor receptor inhibits adherence of both nontypeable Haemophilus influenzae and Streptococcus pneumoniae to cultured human bronchial epithelial cells exposed to cigarette smoke. Int J Chron Obstr Pulm Dis 11:1647–1655View ArticleGoogle Scholar
  120. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA (1989) A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56(5):849–853View ArticlePubMedGoogle Scholar
  121. Avadhanula V, Rodriguez CA, Ulett GC, Bakaletz LO, Adderson EE (2006) Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression. Infect Immun 74(2):830–838View ArticlePubMedPubMed CentralGoogle Scholar
  122. Heads of State commit to lead response to beat noncommunicable diseases, promote mental health. Geneva: World Health Organisation; 2018. http://www.who.int/news-room/detail/27-09-2018-heads-of-state-commit-to-lead-response-to-beat-noncommunicable-diseases-promote-mental-health. Accessed 27 Sept 2018
  123. Dabadge A (2018) What has the Pradhan Mantri Ujjwala Yojana achieved so far?Google Scholar

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