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Abstract
Objective To investigate the association between biomass exposure and chronic obstructive pulmonary disease (COPD) in a representative sample of adults from the Moroccan population
Methods A cross-sectional study was conducted in Fez as part of the Burden of Obstructive Lung Disease (BOLD) study, which included apparently healthy subjects aged 40 years and above. Biomass exposure was defined as self-report use of various biomass types for heating or cooking. The Wood Heating Exposure Index, and the Cooking Biomass Exposure Index were used to assess biomass exposure. Participants underwent post-bronchodilator spirometry and COPD was defined as having a forced expiratory volume in 1 s/forced vital capacity ratio <0.7. Descriptive, univariate and multivariable statistical analyses adjusting for potential confounders including age, sex, smoking, education level, Mokken scale (wealth index) and occupational dust exposure were performed for the general population and separately for men and women.
Results A total of 760 subjects were included, comprising 350 men and 410 women. In the multivariable analyses, we found a statistically significant association between a higher Wood Heating Exposure Index and COPD in men (adjusted OR=3.8; 95% CI: 1.4 to 10.4). While for women, a high Cooking Biomass Exposure Index was the main factor potentially linked to the increased risk of COPD (adjusted OR=7.2; 95% CI: 1.7 to 30.0).
Conclusion This study suggests that biomass exposure is a significant risk factor for COPD development in both men and women, independently of the smoking status which is known as its main risk factor.
- COPD epidemiology
Data availability statement
All data relevant to the study are included in the article or uploaded as supplementary information.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
Chronic obstructive pulmonary disease (COPD) is a major cause of morbidity and mortality worldwide, particularly in low- and middle-income countries.
While tobacco smoking is the primary risk factor for COPD, exposure to biomass smoke is also recognised as a significant contributor, especially among non-smokers.
WHAT THIS STUDY ADDS
This study demonstrates a strong association between biomass exposure, particularly wood heating in men and biomass cooking in women and the occurrence of COPD in the Moroccan population, independent of smoking status.
The findings highlight the importance of considering gender-specific patterns of biomass exposure when assessing COPD risk.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
Public health initiatives should raise awareness about biomass smoke risks, promote cleaner cooking fuels and improve ventilation to reduce the burden of COPD, especially in rural communities and among women.
Introduction
Chronic respiratory disease constitutes one of the primary causes of morbidity in low- and middle-income countries (LMICs). One of these significant diseases is chronic obstructive pulmonary disease (COPD). It is characterised by an abnormal response of the lungs to toxic particles and gases, resulting in progressive and not completely reversible obstruction of the airways.1 COPD imposes a substantial burden on the death rate and high costs of care. According to global estimates, COPD ranks as the third leading cause of death worldwide, responsible for 3.23 million deaths in 2019,2 with over 80% of these fatalities occurring in LMIC.3
Although tobacco smoke remains the most common environmental risk factor associated with the development of COPD, population-based studies reveal a significant prevalence of COPD in those who have never smoked.4 5 Numerous studies have shown that exposure to biomass smoke can also be proposed as a significant risk factor for the development of COPD, particularly in non-smokers.6 7 Other studies have confirmed the relationship between biomass exposure and COPD development.8–11
Considering its low cost and easy availability, about 2.4 billion people worldwide, or roughly one-third of the world’s population, cook using unprocessed solid fuels, which results in domestic air pollution. The majority of this exposed population resides in less economically developed countries.12
Furthermore, statistics from the Global Initiative for Chronic Obstructive Lung Disease (GOLD) based on spirometric criteria reveal that 17–38.8% of patients with COPD worldwide are non-smokers,13 with exposure to biomass smoke being one of the most significant risk factors for the development of COPD in these patients is.14
In Morocco, the prevalence of tobacco in men is estimated at 23.4%, while in women, it does not exceed 0.4%.15 The prevalence of COPD in the country is estimated to be 16.6% and 8.3%, respectively,16 suggesting that smoking cannot be considered the leading cause of COPD in Morocco, particularly in women. Although national data on domestic air pollution is lacking, previous studies have shown that women and children in developing countries are the most heavily exposed to indoor pollution.17 Hence the primary objective of this study is to investigate the association between biomass exposure and COPD in the Moroccan population in general and in women in particular.
Methods
Study design and population
This is a cross-sectional study conducted in the city of Fez as part of the ‘Burden of Obstructive Lung Disease’ (BOLD) study with detailed methodology published elsewhere.18 The target population includes all individuals apparently healthy, aged 40 and above of both genders residing in the city of Fez. Individuals who were sick, bedridden or had mental illnesses were excluded from the study. A two-stage cluster sampling approach was employed to recruit participants. First, 10 administrative base units (ABUs) were randomly selected from a list of 31 ABUs within the Sais district. Within each selected ABU, households were systematically sampled using a pre-calculated sampling interval based on the total number of households in the ABU. Prior to data collection, selected households were contacted to schedule appointments and obtain informed consent. The target sample size was calculated by the BOLD Centre and estimated at 600 participants (300 men and 300 women). Those who agreed to participate signed a written consent form.
Data collection
Trained and certified staff administered a structured questionnaire through face-to-face interviews with study participants in their native language after a house-to-house visit to collect socio-demographic and biomass data. The questionnaire was translated from the original English version of the BOLD study, following standard translation and back-translation procedures. A pilot study was conducted to test the local pre-final version. The final version was administered to the participants, with sufficient time given for each to respond to the various questions.
The questionnaire included participants’ personal data, such as age and gender and risk factors, including tobacco, occupational exposure to dust and exposure to biomass, with specific exposure times.
Socioeconomic status was assessed using a wealth index (Mokken scale), an international scale based on household assets.19 We chose 10 items (household assets) for calculating the score, resulting in a total score ranging from 0 (no assets) to 10 (all assets). The details of the 10 selected items for score calculation, along with the percentage of ownership for each among the participants in this study, have already been published.20
Biomass exposure
Biomass exposure was defined as the use of different types of biomasses for cooking or heating, such as charcoal, wood or kerosene. During the study, all participants were asked about their exposure to different types of biomasses for heating. The questions were asked as follows: ‘Have you been exposed to wood heating?’ If yes, the participants were asked to specify ‘During how many years?’ and ‘Are you still exposed?’ These questions were repeated for each type of biomass. A Wood Heating Exposure Index was calculated based on the number of wood heating exposure years. This index was divided into three classes based on its median, corresponding to 20 years. Participants with no exposure were assigned an index of 0; low exposure (an index ≤20); high exposure (an index >20). Participants who had been exposed to other types of biomasses for heating (N=10) were excluded from this analysis.
Since women are traditionally responsible for cooking in Morocco, in addition to various questions regarding heating exposure which were asked to the entire study population, questions about the use of different biomasses for cooking were asked exclusively to women, in addition to asking about the years of exposure, we specifically inquired about the average number of hours per day that women spent cooking. To assess this exposure, we calculated a Cooking Biomass Exposure Index for Moroccan women, which corresponds to the average number of daily hours spent cooking multiplied by the total number of years spent cooking for each woman, which means that the higher the index, the greater the risk of exposure. This index was developed by Mahesh et al,21 and it was divided into three classes: low exposure (<60), medium exposure (between 60 and 120) and high exposure (>120).
Spirometry
To diagnose subjects with COPD, we adopted the GOLD definition.1 Spirometry was performed before and 15 min after administration of 200 µg of albuterol/salbutamol (Ventolin, GlaxoSmithKline, Brentford, UK) using a double-valve volumatic spacer (Volumatic; GlaxoSmithKline; Research Triangle Park, North Carolina, USA). Spirometric testing was conducted by trained and certified technicians who were regularly monitored for quality assurance, using the ‘nddEasyOne’ spirometer, which was approved for use in this study, meeting the highest levels of quality control while being accessible and suitable for field use.18
Each spirogram was assessed by the BOLD Pulmonary Function Reading Centre at Imperial College London, UK. To be included in the analysis, each spirogram had to meet the criteria of the American Thoracic Society/European Respiratory Society,22 requiring at least three acceptable and reproducible tests for forced vital capacity (FVC) and forced expiratory volume in 1 s (FEV1) (difference between the two highest FVC and FEVA values: 150 mL for quality grade A or, 200 mL for quality grade B), a peak expiratory flow time of at least 6 s and back-extrapolated volume, 150 or 5% of FVC.23 A subject was considered to have COPD if they had an FEV1/FVC ratio <0.7.
Patient and public involvement statement
Patients were not involved in the development of the research question, outcome measures, study design or conduct of this study.
Statistical analyses
We used descriptive statistics to describe the participants’ characteristics and the exposure type. Frequencies were used to describe qualitative variables, while means and SD were used to describe quantitative variables. We used simple logistic regression to investigate the association between different factors (age, sex, smoking, occupational dust exposure, education level, Mokken scale (wealth index), exposure to cooking or heating with wood or charcoal and cooking and heating biomass exposure indexes) and the risk of COPD. A multivariable analysis was then conducted, using binary logistic regression to determine the association between heating and cooking indices and the risk of COPD, adjusting for variables that are established as risk factors for COPD identified by previous literature, such as age, sex, occupational dust exposure, education level, the Mokken scale and active smoking (passive smoking for women since their exposure to active smoking was almost zero), which were thus forced in the model. The initial model included only the above-mentioned confounding factors and indexes.
All statistical analyses (descriptive, univariable and multivariable) were performed in the whole study sample and stratified by sex. Effect sizes are presented as OR and 95% CI.
The significance level was set at 5%. Statistical analysis was performed using SPSS software V.26.
Results
Table 1 presents the characteristics of the entire study population, which consisted of 760 subjects with an average age of 55.3±10.3 years (with a median of 54 years, Q1=48 years and Q3=61 years). Among these, 53.9% were women, 14.1% had spirometrically defined COPD and 8.6% were active smokers.
General characteristics and associated factors with COPD in the entire study population (N=760)
Regarding exposure to biomass, none of the participants used kerosene for heating or cooking. However, 1.3% of patients used charcoal for heating, with an average exposure of 17.5±11.1 years and 22.9% heated their homes using wood, with an average exposure of 20.1±12.9 years. Based on the Wood Heating Exposure Index, 77.7% of participants had no exposure, 15.3% had low exposure and 6.9% had high exposure.
The association between COPD and different factors was statistically significant for age (OR=1.06; 95% CI: 1.04 to 1.08), men (OR=2.3; 95% CI: 1.5 to 3.5), active smoking (OR=2.6; 95% CI: 1.4 to 4.7), as well as a high Wood Heating Exposure Index (OR=3.4; 95% CI: 1.8 to 6.5).
The multivariate analysis, after adjusting for the previously mentioned confounding factors, did not reveal a significant association between COPD and the Wood Heating Exposure Index (p=0.054), although a higher risk was observed in individuals with a high index (adjusted OR=2.3; 95% CI: 1.1 to 4.7).
Table 2 presents the characteristics of men in the study, which included 350 individuals with an average age of 56.7±10.3 years. Among these, 18.3% were active smokers, 8% were passive smokers and 19.4% had COPD. Concerning exposure to biomass, 1.4% used charcoal for heating, with an average exposure of 17.6±8.9 years and 23.7% were exposed to wood heating, with an average exposure of 20.1±13.6 years. Based on the Wood Heating Exposure Index, 77.1% had no exposure to wood heating, 16.5% had low exposure and 6.4% had high exposure.
General characteristics and associated factors with COPD in men (N=350)
While the association between COPD and active smoking approached the limit of significance (OR=1.9; 95% CI: 0.9 to 3.4), statistically significant associations were observed for age (OR=1.06; 95% CI: 1.03 to 1.09) and a high Wood Heating Exposure Index (OR=4.9; 95% CI: 2.0 to 12.0). Multivariate analysis showed that a high Wood Heating Exposure Index was significantly associated with the risk of COPD in men (adjusted OR=3.8; 95% CI: 1.4 to 10.4), after adjusting for confounding factors (age, active smoking, education level, Mokken scale and occupational dust exposure).
Table 3 presents the characteristics of women in the study, which consisted of 420 individuals with an average age of 54.1±10.1 years. Among these, 9.5% had COPD, 0.2% were active smokers, and 19% were exposed to passive smoking. Regarding biomass exposure: 1.2% used charcoal for heating, with an average exposure of 17.4±13.9 years, 22.2% used wood for heating, with an average exposure of 13.8±11.4 years. According to the Wood Heating Exposure Index, 78.3% had no exposure, 14.3% had low exposure and 7.4% had high exposure. For cooking habits, 46.7% of the women cooked with wood, with an average exposure of 17.7±11.5 years. Among them, 13.7% had a Cooking Biomass Exposure Index between 60 and 120 and 2.7% had an index greater than 120.
General characteristics and associated factors with COPD in women (N=410)
The statistical analysis revealed a significant association between the presence of COPD and age (OR=1.06; 95% CI: 1.02 to 1.09), cooking with wood (OR=1.9; 95% CI: 1.0 to 3.8) and Cooking Biomass Exposure Index (OR=2.9; 95% CI: 1.3 to 6.4 for medium exposure and OR=11.1; 95% CI: 3.1 to 38.9 for high exposure). However, no significant association was observed for Wood Heating Exposure Index.
Multivariate analysis was performed to adjust for potential confounders such as age, passive smoking, education level, wealth index and occupational exposure to dust. The results showed that a high Cooking Biomass Exposure Index is the main factor that may increase the risk of COPD (adjusted OR=7.2; 95% CI: 1.7 to 30.0).
Discussion
This study aimed to investigate the relationship between biomass exposure and the risk of COPD in the Moroccan population. The multivariable analysis, adjusted for known COPD risk factors such as age, smoking, education level, wealth index and occupational exposure to dust, revealed that the association with the Wood Heating Exposure Index was as strong as the association with active smoking in men. Conversely, in women, the odds of COPD increased with a rising Cooking Biomass Exposure Index.
While smoking has traditionally been considered the primary COPD risk factor, this study suggests that wood exposure increases the risk of COPD independently of smoking status, especially in men. Sood et al24 also showed that wood smoke exposure was independently associated with lower FEV1, a higher prevalence of airflow obstruction and chronic bronchitis, in a population of current smokers. Additionally, a study involving over 5500 Colombian adults demonstrated that exposure to wood smoke for at least 10 years was associated with a COPD risk, with an OR of 1.5.25
The specific association of wood in the increased likelihood of COPD can be attributed to its particular toxicity, compared with all other forms of biomass. Not only does it increases the risk of COPD, but it also increases the risk of other major respiratory diseases, such as severe bronchial hyper-reactivity.26 27
In women, the risk of COPD is associated with a high Cooking Biomass Exposure Index. This finding agrees with the results of an Indian study that demonstrated an increase in the prevalence of chronic bronchitis as the biomass exposure index rises.21 In Turkey, a study comparing the respiratory function of women exposed and not exposed to biomass smoke indicated that women exposed to biomass smoke have a higher risk of developing impaired respiratory function. Moreover, the duration of exposure to biomass smoke was identified as a significant factor affecting the likelihood of altered pulmonary function.28
A study has shown that non-smokers with COPD are more often women.29 This is particularly relevant in the Moroccan context, where smoking prevalence among women is very low. This observation is consistent with the findings from the latest national survey, which reported a smoking prevalence of only 0.4% among Moroccan women.15 Notably, in our study, exposure to active smoking among women was nearly zero, despite a COPD prevalence of 9.5%.
The association between the risk of COPD and exposure to a high biomass cooking index remained statistically significant even after adjusting for confounders, including passive smoking, which was not found to be associated with COPD risk in either univariate or adjusted analysis. These findings were confirmed by a meta-analysis,30 revealing that biomass smoke was the main risk factor for COPD in non-smoking patients, with an OR of 2.5 and a 95% CI of 2.06 to 3.15.
In addition to biomass exposure, the risk of COPD in women is linked to indicators of reproductive health, including markers of endogenous hormone exposure (age at menarche, age at menopause and duration of reproductive life), exogenous hormone exposure (use of oral contraceptives and hormone replacement therapy), as well as pregnancy history. Studies have shown that reduced lung function is associated with early menstruation,31 32 nulliparity,33 a younger age at first pregnancy,32 as well as postmenopausal status.34 35 In our study, the average age of women was 54 years, suggesting that most of them were in the menopausal stage, indicating an additional increase in the risk of COPD associated with this specific stage of life.
Overall, the results of this study support the growing body of evidence indicating that biomass exposure is associated with a higher risk of COPD, as seen in other studies.14 36 37 Moreover, previous studies have demonstrated a negative association between exposure duration and FEV1, suggesting that prolonged exposure to biomass smoke may lead to greater respiratory impairment.38 39
Numerous studies have confirmed the link between exposure to biomass and COPD risk, independent of tobacco, prompting investigations into the underlying mechanisms of this association. Unlike COPD resulting from cigarette smoke, which mainly affects the respiratory system with emphysema,40–43 COPD caused by biomass smoke was initially identified for its damaging effects on small airways.40 43 Rivera et al44 demonstrated greater remodelling and fibrosis of small airways in autopsies of 10 women with post-biomass COPD compared with 10 women with post-smoking COPD, supporting this finding. Recent studies have also reported damage to both small and central airways in post-biomass COPD, potentially leading to bronchial stenosis.40 45 46
The detrimental effects of exposure to biomass smoke on the respiratory tract can be attributed to the combustion of various materials present in biomass, releasing numerous air pollutants, including methane, volatile organic compounds, nitrogen oxides, sulphur oxides, hydrogen chloride, polyaromatic hydrocarbons, furans, dioxins and inorganic aerosol particles known as particulate matter (PM).47 The composition of these PM is variable, but usually includes aeroallergens, such as pollen, and other biological products, such as fungal or bacterial elements, containing endotoxin.48 It is worth noting that some of these components are similar to those found in cigarette smoke,49 50 highlighting the effect of exposure to biomass smoke on the respiratory tract and the occurrence of COPD. Unlike cigarettes, exposure to biomass smoke can occur very young, increasing the likelihood of suffering from COPD as an adult. Therefore, exposure to both smoking and biomass may be responsible for a higher risk of COPD. A meta-analysis confirmed that biomass smoke was a significant risk factor for COPD for both cigarette smokers and non-smokers, with a higher OR observed for smokers than non-smokers (4.39; 95% CI: 3.38 to 5.70 vs 2.55; 95% CI: 2.06 to 3.15).30
This study has some limitations. First, it is a cross-sectional study, which does not allow us to confirm a causal relationship between biomass exposure and the development of COPD. Second, there may be a memory bias as participants had to recall the duration of their exposure in years or hours per day. Third, the lack of data on hormonal profiles and menopausal conditions has hindered our ability to incorporate and account for these factors in the multivariate analysis conducted on female participants. Despite these limitations, the study has several strengths. First, it included a large sample representing the general population, independent of their COPD status at the time of recruitment. Second, although the study was conducted in an urban setting, a region with a high level of rural migration was chosen. Third, spirometry was performed on all subjects by trained and certified staff to confirm or rule out COPD. All spirometry was performed according to the required recommendations. The survey was conducted in the patients’ homes to provide them with reassurance and adequate time to complete simplified and well-adapted questionnaires, ensuring the reliability of the collected data.
In conclusion
Exposure to biomass smoke mainly wood appears to be a significant factor in the development of COPD in both men and women, independent to the smoking status, which is known as its main risk factor. Further studies, mainly longitudinal ones, are needed to confirm and understand the incrimination of biomass in the risk of COPD.
Recommendations
Given the significant impact of exposure to biomass smoke on respiratory health, particularly in rural areas where it is still widely used, targeted public health interventions are crucial to mitigate this issue:
Raising public awareness of the dangers of biomass smoke, especially among rural communities and women.
Encouraging the adoption of cleaner cooking fuels and devices, such as improved stoves, liquefied petroleum gas or biogas, can significantly reduce harmful emissions and improve indoor air quality.
Improving kitchen ventilation by installing extractor hoods and windows to minimise exposure to smoke inside homes.
While it is known that tobacco smoking is the primary risk factor for the development of COPD, it is imperative to reduce its prevalence to decrease the risk of COPD. This can be achieved through:
Combating tobacco use through national campaigns and programmes, and enforcing the anti-smoking legislation, Law 15/91,51 to prohibit tobacco use in public places.
The establishment of smoking cessation centres across the different regions of the Kingdom, and the training of health professionals on this topic.
Implementing MPOWER measures from the Framework Convention on Tobacco Control in Morocco. Strengthening these measures has the potential to reduce smoking prevalence by 37% by 2030, compared with 2010.52
Increasing taxes, as Morocco has been doing since 2013. In 2019, total taxes on tobacco accounted for 76.1% of the price of the most sold cigarette brand.53
Data availability statement
All data relevant to the study are included in the article or uploaded as supplementary information.
Ethics statements
Patient consent for publication
Ethics approval
This study involves human participants and was approved by the Hospital University Ethics Committee of Fez (Serial Number: AR MOR v4_14 Sep 2009). Participants gave informed consent to participate in the study before taking part.
Acknowledgments
The authors would like to thank the Burden of Obstructive Lung Disease (BOLD) Coordinating Centre (London, UK) for their advice and technical support with this project; the director of Hassan II University Hospital Centre of Fez for technical support provided with the execution of the BOLD study in Fez; the Faculty of Medicine of Fez, Morocco, and Boehringer Laboratory-Morocco (Fez, Morocco) for funding part of this study. The BOLD Centre was funded by a Wellcome Grant 085790/Z/08/Z.
References
Footnotes
Contributors IELH: Conducted the statistical analysis and drafted the manuscript. VG-L: Contributed to the development of the Burden of Obstructive Lung Disease (BOLD) study. SB: Assisted with the statistical analysis. CN: Contributed to the development of the BOLD study and oversaw its implementation in Morocco. MEIB: Supervised the spirometry measurements and the implementation of the BOLD study in Morocco. MCB: Supervised the spirometry measurements and the implementation of the BOLD study in Morocco. KEIR: Contributed to the development of the BOLD study, oversaw its implementation in Morocco and supervised the writing of this manuscript. All authors reviewed and edited the final version of the manuscript. Guarantor: IELH.
Competing interests None declared.
Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.
Provenance and peer review Not commissioned; externally peer reviewed.