The origins of biomass exposure

Biomass is defined as an organic matter that can be used as a fuel including wood, animal waste (manure), crop, and forestry residues, among others⁹. Biomass, either wood or its derivatives, shares many properties and substances with tobacco. However, regarding their epidemiology, the main difference between biomass exposure and tobacco exposure and, therefore, with COPD expression, is related with the socioeconomic context in which these exposures occur. The tobacco epidemic developed as a result of innovations in the tobacco industry between 1913 and 1920; later, during the 60s, the cigarette industry experienced almost uninterrupted growth in the United States and over the world¹⁰, killing thousands of millions of people. In contrast, biomass exposure has existed since humans began using organic fuel materials for cooking and heating, affecting billions of women and children¹¹; unfortunately, for centuries, there has been no awareness of the impact on the health of exposed individuals¹². These individuals, especially women, have gone unnoticed by governments and also by the research community.

While tobacco smoking was promoted by the tobacco industry for recreational purposes, developing a need to smoke tobacco¹³, the use of biomass has been a necessity for women in rural areas for subsistence, cooking, and household heating since poverty has prevented them from having access to electricity and safer fuels¹⁴.

The World Health Organization has estimated that there are around 1100 billion persons exposed to tobacco globally, while for biomass exposure, it is half of the world’s population, or about 3 billion people, who rely on solid fuels for cooking and heating. This proportion is higher in developing countries, especially in rural areas¹⁴.

Biomass as an indoor air contaminant: a cause of COPD in women

As women tend to stay indoors most of the time, exposure to contaminants inside the homes dominates the list of exposure to various pollutants worldwide, especially in developing countries. In most cultures, women have a leading role in domestic cooking, while men are at work or away from home. Globally, almost 50% of deaths from COPD in developing countries could be attributed to biomass exposure, and approximately 75% of these are in women¹⁶.

COPD is the disease with the highest evidence, reported in different studies that women exposed to indoor smoke are 3 times more likely to suffer from COPD in the form of chronic bronchitis than women who cook with electricity, gas, or other cleaner fuels¹⁷. For example, in Colombia, it was found that the use of a biomass stove for 10 or more years was associated with a greater risk of COPD (GOLD Stage 1 or greater; OR, 1.5; 95% CI 1.22-1.86)¹⁸. At present, COPD associated with indoor air pollution from biofuels is considered a public health issue with a double significance: it is a gender-specific disease, occurring almost exclusively in women, and, on the other hand, an increasing number of women are being affected worldwide¹⁷.

Early COPD: factors that contribute to airway damage since childhood

It is very common for women to have several periods of exposure to intense cooking smoke each day, occurring indoors in unvented open fires that operate at low temperatures. This produces a great variety of air contaminants. The levels of pollutants inside homes burning biomass in unvented open fires are incredibly high, in the milligram per cubic meter range¹⁹-²². Women are exposed to biomass smoke at all stages of life, during pregnancy and childhood and especially during adolescence when they begin to cook. Therefore, women and girls receive the largest cumulative exposures throughout their lives, since they spend an average of 4-8 h daily in the kitchen, usually in an enclosed space with poor ventilation. Consequently, during their lifetime, women are exposed to biomass smoke for 30-40 years, the equivalent of 60,000 h of exposure, or inhaling a total volume of 25 million L of polluted indoor air²³.

Celli et al. recently wrote that the beginning of the disease is not a firmly defined concept³. The natural history of a disease is sometimes said to start at the moment of exposure to a causal agent in an individual susceptible to it³,²⁴. The age of onset of biomass and tobacco exposures is different. Biomass exposure begins much earlier in life (in utero and from the neonatal period) than does active smoking (usually in the teenage years), thereby increasing the risk for COPD in relative terms²⁵,²⁶. In addition, young children and infants, who are typically carried on the back or placed near their mother to sleep, are also exposed to biomass smoke¹⁴. There is a particular concern when young children are exposed to smoke because data suggest that smoke exposure during the window of developmental susceptibility in early life is particularly detrimental²⁶. Chronic insult beginning in childhood may act as an early stimulus that affects airway structure and function²⁷. The early years are crucial because diseases associated to exposure can affect lung function throughout life. Children exposed to biomass smoke have a larger number of acute respiratory infections, including pneumonia, and asthma compared to unexposed children²⁸,²⁹. The consequence is a lower growth in lung function, leading to COPD²⁵.

Conversely, exposure to tobacco usually begins in adolescence, is intermittent, for very short periods, and most of the time occurs in open spaces. Assuming that smoking exposure was the “only” causal agent of COPD, the absence of an early exposure in the first year of life would prevent the detrimental factors from damaging the airway in these children, i.e., lung growth in the first year of life is not affected in those future smokers³⁰.

In other words, TE-COPD begins when a young individual starts to smoke, most often in adolescence, while BE-COPD starts in early childhood³¹.

Variations in biomass and tobacco smokes inhalation lead to differences in damage location

The differences between biomass and tobacco COPD phenotypes begin with the smoke source. Although biomass smoke has many of the same constituents as tobacco smoke, the exact composition differs depending on the source of the fuel, combustion efficiency, and relative humidity. Although the particle size may be similar in both tobacco and biomass smoke²¹,³², differences in chemical composition could lead to variation in the pathophysiological processes. Another difference between BE-COPD and TE-COPD is the pattern of smoke inhalation. Individuals inhaling biomass smoke use a consistent tidal breathing pattern. This type of inhalation pattern probably prevents the damage from spreading beyond the small airway, leading to an airway-predominant COPD phenotype. The greatest damage from inhaling biomass components is located in the small airway that functions as the final part of the funnel, where an important inflammatory reaction takes place followed by remodeling of the small airway⁸.

Conversely, cigarette smokers usually smoke in a two-phase pattern: first, the smoke is drawn into the mouth without direct inhalation into the lungs, then there is a pause, and finally, the smoke is inhaled into the lungs with an additional volume of air³². The average inhalation volumes have been measured at nearly 25% of vital capacity; this corresponds to close to twice the average tidal volume³². The larger inhalation volume in cigarette smokers compared to those exposed to biomass smoke may allow the smoke to reach more deeply into the lungs and may increase the deposition of tobacco smoke in the lung parenchyma, leading to an emphysema-predominant COPD phenotype.

This contrasting epidemiological context between women using biomass fuel and smokers allows for a better understanding of the differences in the clinical picture and the functional, histologic, and tomographic findings of COPD between these two phenotypes³³.

AIRWAY DAMAGE IN COPD FROM EXPOSURE TO BIOMASS SMOKE

A growing body of evidence supports that COPD caused by chronic indoor exposure to biomass smoke, in contrast to COPD due to cigarette smoke, is predominantly a disease of the airways with mild or minimum emphysema⁶-⁸,³⁴-³⁸. Although recent studies have focused on the small airways’ damage in BE-COPD⁸,³⁸, bronchial anthracofibrosis affecting also the central airways seems a trait more frequent and severe in BE-COPD than in TE-COPD, which could cause bronchial stenosis⁸,³⁹-⁴¹. In the following paragraphs, we present some of the evidence and characteristics of the airways’ damage in BE-COPD.

Histological and tomographic findings

Pathological studies of samples obtained from bronchial and lung biopsies and from autopsies in persons chronically exposed to biomass smoke, with or without a diagnosis of COPD, revealed an important thickening of the bronchial wall, mainly of its basal membrane, squamous-cell metaplasia, goblet cell hyperplasia, peribronchiolar fibrosis, and bronchiectasis with a remarkable anthracotic pigment deposition in the bronchi and pulmonary interstitium⁷,⁸,³³,⁴²-⁴⁴. Among these findings, in the study by Rivera et al.,³³ the autopsies of 10 women with BE-COPD and 10 women with TE-COPD showed greater remodeling and more fibrosis in the small airway in BE-COPD compared to TE-COPD. This is a clear evidence that the damage to the small airway is the main pathological feature in BE-COPD. Figure 1 shows an example of the severity of damage to the small airway in BE-COPD.

Figure 1 Membranous bronchioles with structural remodeling from mild (1) to severe (4) in chronic obstructive pulmonary disease (COPD) secondary to biomass. Courtesy of Dr. Rivera. Material obtained from the autopsy of a woman with BE-COPD. 

Importantly, these pathological changes are well correlated with the radiographic findings, whether in the chest X-ray or the computed tomography³⁶,³⁷,⁴²,⁴⁵,⁴⁶. High-resolution computed tomography (HRCT) scans show peribronchial thickening, bronchial dilation, laminar subsegmental atelectasis, mosaic perfusion pattern, parenchymal bands, and no significant emphysema³⁶-³⁸,⁴⁶. Using parametric response mapping, an imaging tool that allows the quantification of small airway disease and emphysema in COPD, Fernandes et al. confirmed the absence of important emphysema in patients with BE-COPD but, interestingly, suggested that these patients had a distinct pattern of small airway disease³⁸.

Clinical findings

The vast majority of persons with BE-COPD are women⁴⁷, who strikingly and consistently have a body mass index (BMI) higher than that of people with TE-COPD⁶,⁸,³⁴,⁴⁸. Individuals exposed to biomass smoke have a high risk of chronic bronchitis (cough and phlegm for ≥ 3 months per year for at least 2 consecutive years)⁴⁹,⁵⁰ and patients with BE-COPD frequently have respiratory symptoms: cough, expectoration, and dyspnea³⁶,⁴²,⁴⁵,⁵¹. Some studies show that these symptoms are more frequent or have more impact in BE-COPD than in TE-COPD³⁶,⁴⁵,⁵²,⁵³, but other studies do not⁴⁸,⁵¹,⁵⁴,⁵⁵. With regard to the physical examination, rhonchus and wheezing are relatively frequent in BE-COPD⁴⁵. The high frequency of cough, expectoration, rhonchus, and wheezing is clearly indicating the predominant damage to the airways in BE-COPD.

Quality of life

It is well known that COPD negatively affects the quality of life. Some studies have shown that this negative impact is higher in BE-COPD. Camp et al., using the St. George’s Respiratory Questionnaire, found worse symptoms and more compromised activity indexes in women with BE-COPD compared to those with TE-COPD³⁶. Another study including 138 women with COPD showed that among women with the same degree of obstruction, those with BE-COPD had worse health status (poorer quality of life and worse dyspnea) than those with TE-COPD, with no differences in comorbidities⁵².

Functional findings

By definition, patients with BE-COPD have post-bronchodilator airflow obstruction: FEV₁/FVC < 0.7 or < lower limit of normal. Compared with TE-COPD, obstruction in BE-COPD is milder, both overall and after adjusting for age³⁶,⁴²,⁴⁵,⁴⁸,⁵⁴,⁵⁶-⁵⁸. Regarding the annual decline in lung function, the time-course behavior of FEV₁ in a Mexican cohort of patients with COPD associated with biomass or tobacco during a 15-year follow-up period showed that the rate of FEV₁ decline was significantly slower in patients whose COPD was caused by biomass smoke than in those caused by tobacco exposure. The annual rate of decline was significantly higher in the TE-COPD group than in the BE-COPD group (42 mL vs. 23 mL, respectively, p < 0.001). The proportion of rapid decliners in patients with COPD caused by biomass fuel was very low (1%) compared with the one seen in patients whose COPD was caused by tobacco exposure (11%) (Fig. 2)⁵⁷.

Figure 2 A: FEV₁ annual decline in biomass smoke exposure-chronic obstructive pulmonary disease (BE-COPD) compared to tobacco-exposed chronic obstructive pulmonary disease (TE-COPD) and healthy subjects. This figure shows an annual decline of almost twice the value in patients with TE-COPD compared to BE-COPD. The variability in the mean annual decline in TE-COPD was broader. B: −41.7 ± 26.2 mL, while the variability in the BE-COPD was narrower. C: −23.1 ± 16.9 mL. 

With respect to gas exchange, some studies have shown that carbon dioxide arterial pressure (PaCO₂) is higher (lower ventilation) and oxygen arterial pressure (PaO₂) and oxygen arterial saturation (SaO₂) are lower in BE-COPD than in TE-COPD³⁶,⁴⁵,⁵⁴,⁵⁷. The lower oxygenation rates observed in BE-COPD may be explained in part by hypoventilation. It remains to be determined whether this behavior is related with a higher BMI in these patients, most of whom are women over 50 years of age. Recently, Olloquequi et al. found that patients with COPD exposed to both biomass and cigarette smoke exhibit significantly lower oxygen saturation than those exposed to only biomass or only cigarette smoke⁵⁵.

Normal or mildly altered diffusing capacity (DL_CO) and DL_CO/alveolar volume (DLCO/AV) ratio are consistently observed in BE-COPD when they are compared to TE-COPD, in which these parameters are significantly reduced³⁷,⁴⁵,⁵⁵. This finding correlates with the lower grade of emphysema found in HRCT in patients with BE-COPD⁸,³⁶-³⁸,⁴⁶ at all levels of COPD severity. This functional picture of decreased DL_CO with normal DLCO/AV has been described in cases with significantly compromised small airways with little emphysema (pseudophysiological emphysema)⁵⁹. Compromised diffusion correlates better with decreased FEV₁ in women with TE-COPD than in those with BE-COPD, posing the greater contribution of emphysema to airflow obstruction in TE-COPD⁴⁵.

Women with BE-COPD have greater bronchial hyperreactivity than women with TE-COPD (Fig. 3)⁶⁰. Further, research is needed to determine if this correlates with the higher frequency of the asthma–COPD overlap phenotype observed in BE-COPD⁴⁸. There is evidence also that small airway resistance measured by oscillometry is considerably more affected in BE-COPD than in TE-COPD⁶¹.

Figure 3 Bronchial hyperreactivity evaluated by PC₂₀ by exposure (59). White circles: biomass smoke exposure-chronic obstructive pulmonary disease (BE-COPD); black circles: tobacco-exposed chronic obstructive pulmonary disease (TE-COPD). PC₂₀ geometric mean: BE-COPD versus TE-COPD: 0.39 (0.06-5.13) versus 1.24 (0.34-9.39), p = 0.028. PC₂₀: methacholine concentration causing ≥ 20% reduction in FEV₁. 

Exercise tolerance in BE-COPD

The walked distance in the 6 min walking test in BE-COPD does not seem significantly different compared to TE-COPD³⁶,⁵²,⁵⁴,⁵⁵, although Zhao et al. found a lower distance in BE-COPD⁸. Camp et al. reported lower SaO2 measured by pulse oximetry at the end of the test in women with BE-COPD³⁶.

Clinical phenotypes in BE-COPD

Golpe et al.⁴⁸ evaluated that the frequency of clinical phenotypes defined by the Spanish COPD guidelines⁶² in patients with COPD caused by biomass or tobacco smoke. The asthma–COPD overlap phenotype was more common in BE-COPD, but the difference disappeared after adjusting for sex. Similar to the findings discussed in the previous sections, they found a greater frequency of emphysema phenotype in TE-COPD. No difference was found in the frequencies of chronic bronchitis or exacerbator phenotypes⁴⁸.

Pulmonary hypertension in BE-COPD

A recent study found that pulmonary hypertension on echocardiography was more common in patients with BE-COPD than in those with TE-COPD⁶³. In previous studies, González et al. based on radiographic evaluation, and Sandoval et al. showed a higher rate of pulmonary hypertension among individuals with COPD related to wood smoke exposure compared to those exposed to tobacco smoke⁴⁵,⁶⁴. The origin of pulmonary hypertension in BE-COPD patients does not appear to be related only to hypoxic pulmonary vasoconstriction but also to direct effects caused by the inhaled substances or indirect inflammatory-mediated effects⁶⁵.

Exacerbations and survival in BE-COPD

Golpe et al. did not find differences in the annual rate of exacerbations comparing BE-COPD and TE-COPD⁴⁸, but it should be noted that no prospective data are available on this aspect. After adjusting for age, sex, and disease severity, Ramírez-Venegas et al. and Golpe et al. did not find differences in survival between BE-COPD and TE-COPD⁵⁴,⁵⁸.

Table 1 summarizes the most important epidemiological, clinical, functional, histological, and imaging differences between BE-COPD and TE-COPD.

Summary

No doubt BE-COPD is a disorder clearly associated with poverty and sociocultural issues. There is a direct impact on lung growth in these women that damage mainly the small airway.

However, in spite of these women being exposed to very high levels of pollutants while cooking, the consequent decline in FEV₁ seems not as detrimental as that induced by tobacco. These findings could indicate that BE-COPD may be classified as the benign version of COPD. Even so, despite having a higher baseline FEV₁, the histological and tomographic findings in BE-COPD show a more intense small airway damage in comparison with TE-COPD. Furthermore, in BE-COPD gas exchange abnormalities occur earlier, and patients have a worse quality of life than smokers. Moreover, mortality is similar to the one observed in smokers.