Introduction

Nearly one-half of the world’s population continues to be exposed to biomass smoke, during cooking or heating with solid fuels such as dung, wood, agricultural residues and coal.^{1, 2} This exposure is most prevalent in less developed countries and rural areas, with indoor levels of particulate matter often reaching levels several times higher than accepted, safe air pollution standards. Biomass smoke has a variety of pollutants ^1,3-5 resembling those found in tobacco smoke. Tobacco smoke can be considered to be an addictive form of biomass smoke with both forms of smoke including carcinogens. Exposure to poverty-related biomass smoke6 has been associated with a variety of health effects.^7-12 In 2010, 3.2 million deaths, and 111 million disability-adjusted life-years (DALYs) were attributed to solid fuel use worldwide.¹³ Because the exposure is principally domestic, it predominantly affects women and infants, but may also affect men particularly when biomass is used for household heating. The use of biomass fuel can be attributed to a population’s geographic isolation and poor availability of cleaner fuels creating a low position on the energy or fuel ladder.⁴ This position can improve with economic development, reducing the use of biomass fuel and increasing the use of cleaner fuels such as liquid petroleum gas or electricity. An alternative or complementary model of energy use is the multiple fuel model in which a community simultaneously employs fuels high and low on the energy ladder. This may occur within the same family. ¹⁴ For example, in Mexico, homes with available gas stoves may still use open fires once or twice a week to cook tortillas or special dishes.

Among the adverse health effects described, COPD and chronic bronchitis are most prevalent^{7, 8, 10, 15, 16}; comprising the current third leading cause of global mortality and responsible for 2.9 million deaths in 2010.¹⁷ COPD also ranks fifth among the main causes of years lived with disability ¹⁸ and ninth in global causes of DALY´s.¹⁹

In the 2010 Global Burden of Disease study, 1.1 million COPD-related deaths were attributed to tobacco smoking, and 850,000 to indoor pollution, but in women slightly more deaths were attributed to indoor pollution than to smoking (445,000 vs. 417,000 deaths).²⁰ It is of interest that estimates for smoking-related deaths due to COPD are rising, whereas those related to indoor pollution are decreasing.

In a recent meta-analysis, risk of exposure to biomass smoke for COPD in women attained an odds ratio of between 2 and 3 ^7-10 with less evidence of an effect in men, as expected, because exposure is related to traditionally female-dominated domestic tasks. Use of cleaner fuels or improved biomass stoves for cooking and heating reduces exposure, ²¹ is cost-effective, ²² and would likely exert a significant positive impact on health. ²³ Unfortunately, because of economic conditions and cultural circumstances, the use of solid fuels, which are burnt inefficiently and produce increased amounts of pollutants, continues. ²⁴

Comparing COPD caused by smoking and COPD caused by exposure to biomass smoke is very relevant, and not only because of the global magnitude of exposure to biomass smoke. The pathogenesis of the disease and predisposing factors could differ; thus, clinical characteristics, response to treatment and disease prognosis could also differ. ²⁵ Analyzing in detail the pathogenesis of COPD and chronic bronchitis associated with biomass smoke may also identify key pathways for the development of COPD from different exposures.

Although information is scarce, over the past few years, a clearer picture of the main characteristics of the persons with biomass smoke-associated COPD (BSCOPD) has emerged, which allows for comparison with many aspects of the better understood individual with COPD caused by tobacco/cigarette smoking (TSCOPD), (See Table 1) forming 2 clearly separable COPD phenotypes.

Some of the differences between individuals with COPD who smoke and those who cook over open fires derive from the cultural and socioeconomic characteristics associated with the use of biomass as fuel and from the specific progression of the smoking epidemic in a given geographic area. Specifically, women in a community may be exposed only to biomass smoke if the majority of households cook with biomass open fires, and smoking in women is still uncommon. Thus, that community’s tobacco smoking epidemic would be at a stage in which the majority of smokers are men.²⁶ Later, a combined exposure of biomass smoke and tobacco smoke is possible if socioeconomic conditions and geographic isolation persist with little ascent on the energy ladder (towards using cleaner fuels), while the tobacco smoking epidemic advances further to include women. For example, in Mexico, that combination is observed in women born in rural areas who migrate to cities, where tobacco smoking by women has increased.

Exposure to biomass fuel creates clinical characteristics in individuals with COPD or chronic bronchitis that may be somewhat different from the typical characteristics found in individual’s with COPD who have inhaled tobacco smoke. It is important to identify both of these. Interactions between exposures are complex, because exposure to biomass smoke increases the risk of airflow obstruction in smokers. ²⁷ Combined exposures are rising, as the smoking epidemic reaches women in developing countries.

General Description of the Patients with BSCOPD

A detailed description of the clinical characteristics of women with BSCOPD was recently published.²⁸

Due to the circumstances of exposure, patients with BSCOPD or chronic bronchitis are commonly women born in rural areas who have a lifetime exposure to biomass smoke while cooking. Their exposure includes prenatal and childhood exposure, ²⁹ potentially causing an adverse impact on lung development and recurring respiratory infections during infancy, ³⁰ which may increase the risk of airway injury and disease later in life. As adults, these women may have migrated to urban areas, or even to a different country.³¹ Although customs for cooking vary from country to country and within different areas of the same country, kitchens in developing countries tend to be similar with poor ventilation, especially in cold areas, stoves comprised of unvented, open fires, and walls smudged with stove smoke. The kitchen is often the room in the house where everyone sleeps often creating a prolonged exposure, as open fires may additionally be used for household heating. The type of biomass burned tends to change over time. As forests near the village recede, the quality of the biomass decreases, causing a descent on the energy ladder to crop residues, and later dung or garbage. As these biomass are burned, pollution and health risks increase. Gathering and carrying the biomass is also the women´s responsibility, which progressively adds to their burden of domestic activities.

Exposure to biomass smoke leads to chronic irritation and is clearly and consistently associated with respiratory symptoms. Cough, phlegm^{8, 16, 28, 32} and symptoms of chronic bronchitis are prevalent in women exposed to biomass smoke. Although meta-analyses based on case-control and cross-sectional studies confirm the association between biomass exposure and airflow obstruction, ^7-10 more evidence exists for an association between biomass smoke inhalation and chronic bronchitis or respiratory symptoms than for spirometric abnormalities.¹⁶

Irritation of the eyes and nose mucosa can also be present.^33-37 Bacterial colonization of sputum is similar to that described in smokers. ²⁸ Dyspnea is common in women arriving at referral hospitals. ^{28, 32}

Wheezing may be present, ^{28, 32} and is consistent with studies finding more methacholine hyperresponsiveness in women with BSCOPD than in smokers.³⁸ The relationship of asthma with exposure to biomass smoke is controversial. Some studies have found an increased risk of asthma in those exposed to biomass smoke,^{39, 40} but results have been inconsistent. Bronchial hyperreactivity (BHR) can be present in any disease producing airflow obstruction, and is not necessarily due to bronchial asthma. ⁴¹ On physical examination, low-pitched crackles may be heard. Chest roentgenogram may be normal or with increased bronchovascular markings. In a formal comparison, no significant differences between individuals exposed to biomass smoke and smokers were found, with the exception that biomass exposed individuals exhibited more common features of pulmonary hypertension. ²⁸ Yet less common in Latin America is an interstitial lung disease pattern, which is likely associated with inhalation of, not only biomass smoke, but also fibrogenic dusts. ^{11, 12}

In developing countries, the presence of bronchiectasis and tuberculosis (TB) must be ruled out as a cause of chronic respiratory symptoms or airflow obstruction, especially in countries where prevalence for these illnesses is high.⁴² In one study, cylindrical bronchiectasis was identified via HRCT in 14% of BSCOPD patients . Yet, no bronchiectasis was found in those exposed to tobacco, with patients matched by age and severity of airflow obstruction. ⁴³ However, the former may be present in autopsies ^{28, 44} and has been identified in one half of patients with moderate or severe COPD. ⁴⁵ It is worth noting that exposure to biomass smoke, as well as exposure to tobacco smoke, may be an important risk factor for developing TB ^46-48 and lung infections ^49-52 although evidence for an increase in risk for TB is scarce and controversial. ^{53, 54} The presence of TB is also associated with irreversible airflow obstruction. ⁵⁵

Exposure to biomass smoke was described as a risk factor for cor pulmonale in a series of articles by Padmavati, et al,^{56, 57} who were puzzled by the frequency of the disease in women with no cardiovascular risks.^{57, 58} In fact, abnormalities of small pulmonary arterioles with intimal thickening may lead to pulmonary hypertension in individuals exposed to biomass smoke to a greater degree than in smokers.^28,44 Patients with BSCOPD are commonly hypoxemic, contributing to pulmonary hypertension ^{32, 57} which is mainly mild or moderate. However, some individuals may develop more severe pulmonary hypertension and need to be identified and treated.⁵⁹ Pulmonary hypertension and cor pulmonale may b leading causes of complications and death in BSCOPD.

In a comparison of individuals with BSCOPD and individuals with TSCOPD, in which all exhibited airflow obstruction, Ramirez-Venegas et al, found similarities and important differences.³² Airflow obstruction in women exposed to biomass was less severe than in smokers, ⁴² but their quality of life (QOL) was similarly affected.³² In fact, on matching by age and severity of airflow obstruction, women exposed to biomass smoke had a lower QOL and more hypoxemia than smokers.⁴³

In addition, evidence from computed tomography (CT) scanning^{43, 60, 61} and DLCO ^{43, 61} shows that the clinical presence of emphysema is particularly unusual in women exposed to biomass smoke. However, in lung pathology, emphysema is present in never-smoking women dying of COPD, exposed to biomass, ⁴⁴ but it was milder than in smokers. Other alterations in lung morphology have been described differently in persons exposed to biomass smoke than in persons exposed to tobacco smoke.^{28, 44} Specifically, those exposed to tobacco smoke exhibit more goblet cell hyperplasia and those exposed to biomass smoke exhibit more anthracosis (in airways and in blood vessel walls), small airway fibrosis and intimal thickening in small pulmonary arterioles.⁴⁴

In Mexico, women exposed to biomass smoke tend to be of short stature and overweight. These traits are reflective of a general high prevalence of obesity, and a link between short stature and indigenous ancestry, both common in deprived communities. The combination of obesity and COPD adds to the burden of COPD, including adding the long list of comorbidities associated with obesity such as hypoxemia, sleep apnea, diabetes, and cardiovascular risks among many others. Treatment for these comorbidities strains the health system to an even greater extent and requires health personnel receive additional education and training on simultaneous comorbid conditions.

The crude survival rate of male smokers with COPD was lower than in women smokers and in those exposed to biomass, but differences disappeared after adjusting for forced expiratory volume in 1 second (FEV₁ ) and oxygen saturation (SaO₂).³² Specifically, irreversible airflow obstruction in never-smokers with lifelong exposure to biomass creates a similar risk for death as that of the typical smoker with COPD, once adjustments have been carried out for hypoxemia and lung function. QOL is worse in BSCOPD if adjusted for airflow obstruction and age.

A summary of differences and similarities among these different expressions of COPD is depicted in Table 2 and was assembled from the Camp, et al, and Rivera, et al studies. In the Camp et al study at the same age and FEV₁, individuals in both groups had similar QOL and dyspnea, but women with BSCOPD were more hypoxemic.

Pathogenesis

Scarce information is available on the possible differences in pathogenesis between damage caused by tobacco smoke and that due to biomass smoke.^62-66 Exposure to biomass smoke induces oxidative stress in animal models ^{67, 68} and also in individuals with COPD⁶³ to as great a degree as exposure to tobacco smoke creates. Specifically, in comparison with healthy individuals, individuals with BSCOPD have increased levels of malonylaldehide and superoxide dismutase which correlates inversely with FEV₁ .⁶³ In addition, both individuals exposed to tobacco and those exposed to biomass showed increased elastolytic activity of macrophages⁶² and of serum C-reactive protein.⁶⁹ Recently a group of individuals with TSCOPD were compared with a group of individuals with BSCOPD. Both groups showed an increased proportion of T helper 2 cells (T_H2) and T helper 17 cells (T_H17) as compared with controls. However, there were some quantitative differences, with the TSCOPD group having a higher blood percentage of T_H17 cells (10.3% vs. 3.5%) and the BSCOPD group having more T_H2 cells (4.4% vs. 2.5%) and serum concentrations of interleukin 4 (IL-4) and interleukin 10 (IL-10).⁷⁰ Whether or not these mild or moderate differences in inflammatory responses are relevant and whether they may explain the differences in the clinical and pathological presentations of COPD due to smoking or biomass, or whether the differences depend on susceptibility, or on the type and dose of smoke exposure, has yet to be determined. Alpha-1 antitrypsin deficiency, the genetic form of COPD is uncommon in Mexico, and not present in women with wood smoke exposure and chronic bronchitis ²⁸ however, some differences between BSCOPD and TSCOPD in the pattern of gene association were recently described. ⁷¹ In addition, exposure to biomass smoke and its associated gene promoter methylation increase the risk of airflow obstruction in smokers.²⁷ This finding may explain additive risks between exposures to tobacco smoke and to biomass smoke.

Prevention

Prevention must focus on reduction of exposure, by using a cleaner fuel higher on the energy ladder. If costs prohibit this, an improved biomass stove, which is vented to the exterior, is more energy-efficient, and permits the consumption of less wood per the same energy released, creating less pollution, should be used. In a short-term intervention study, a reduction in respiratory symptoms and a decrease in FEV₁ decline was observed in women regularly using an improved biomass stove.²¹ The use of vented coal stoves has decreased the risk of COPD in China. ⁷² The use of improved wood stoves, often implemented in official government programs with lots of publicity and with little or no community participation, has sadly decreased over time and has been abandoned altogether in some communities. Several factors contributed to this including the lack of perception of a health risk with open fires among the targeted population, preference for open fire stoves as a traditional way to cook and the requirement of maintenance of the improved stove at the individual level, which often created follow-up expenses for the household. The reduction of pollutants with improved biomass stoves may be as much as one-half ⁷³ however, this may be insufficient for significantly decreasing or eliminating some adverse health effects that depend on the exposure-health risk response. ^{74, 75} Without doubt, the use of cleaner fuels or the development of improved biomass stoves, more efficient than current models and with more community acceptance for use over the long term, is required.

Treatment

Recommendations for patients with BSCOPD include receiving treatment based on current COPD guidelines^76-78 and avoiding further exposure to biomass smoke if possible. Initial evaluation and follow-up, a prescription of bronchodilators, rehabilitation, oxygen for hypoxemic patients, antibiotics in case of infectious exacerbations, vaccination against influenza and pneumococcus, and other measures are recommended based on current COPD guidelines. However, scientific evidence of treatment effectiveness in BSCOPD is lacking. It is contradictory that these large, dispossessed populations of COPD patients lack relevant clinical trials to prove the effectiveness and cost-effectiveness of the recommended measures. Conversely, many trials have been conducted with tobacco smokers in developed or middle-income countries, often leading to therapeutic recommendations. Guidelines usually list a variety of interventions and medicines that may have proven effectiveness, but each country, according to its resources, should propose specific guidelines that take into account the cost-effectiveness of medicines and interventions. International agencies could be of assistance with this important activity.

Perspective

Information related to biomass smoke exposure and its health effects is lacking key components. The majority of observational studies lack quantitative measures of exposure. Upon review, no randomized clinical trials describing therapeutic interventions with this group of patients were found. Additionally, to our knowledge, no longitudinal study to observe the health impact of exposure on a cohort of individuals has been published or initiated: epidemiological information to date derives from cross-sectional or case-control studies. Pathogenic studies are also needed. In summary, exposure to biomass smoke predominantly and inequitably affects women, to whom domestic activities are usually assigned, and small children, adding to the burden of poverty. Reducing or eliminating exposure is challenging, but would likely improve health significantly not only through the reduction of lung disease but through the improvement of other quality of life measures, many of which may be unexpected.