Association of Exposure to Biomass Fuels with Occurrence of Chronic Obstructive Pulmonary Disease in Rural Western China: A Real-World Nested Case-Control Study

Introduction

Chronic obstructive pulmonary disease (COPD) is a chronic lung disease that limits airflow in the lungs, leading to high mortality and disability.¹ The decline in lung function also reduces quality of life, and the chronic nature of the disease places a heavy burden on patients, their families and society.^2,3

In China, the incidence of COPD has been steadily increasing as the population ages and environmental pollution worsens, making it a serious public health crisis. The 2018 China Pulmonary Health Study (CPHS) surveyed 50 991 people from 10 provinces and cities, and found that the prevalence of COPD was 8.6% among adults 20–39 years old and 13.7% among adults at least 40 years old.⁴ A recent World Health Organization (WHO) report identified COPD as the third leading cause of death worldwide, causing 3.23 million deaths in 2019.⁵ The Chinese Center for Disease Control and Prevention, based on data from 1999 to 2017, COPD is the fourth cause of death in China.⁶ COPD is now considered a preventable and treatable disease, highlighting the importance of risk factor detection in order to enable early intervention,⁷ when it is more likely to be effective.⁸ However, the strongest risk factors for COPD in the rural Chinese population are unknown.

COPD risk factors can be genetic or environmental.⁵ One potential environmental factor is combustion of biomass fuels, mainly wood, charcoal, crop straw, animal excrement, corn cobs, and leaves,⁹ which create indoor air pollution. Smoke from biomass fuels has been linked to increased risk of COPD in various populations.^10,11 The WHO estimates that around 2.6 billion people cook using polluting open fires or simple stoves fuelled by kerosene, biomass and coal, and close to 4 million people die prematurely from illness attributable to household air pollution from inefficient cooking practices using polluting stoves paired with solid fuels and kerosene each year.¹² At the same time, environmental initiatives have led to the construction of large-scale biogas digesters in rural areas of China,¹³ which have substantially reduced the use of biomass fuels. The use of biomass fuels varies greatly across different regions. Therefore, the current situation of biomass fuels exposure in rural areas of western China is unclear, and a better understanding of the contribution of biomass fuels exposure to COPD in rural residents is urgently needed.

The purpose of this study was to determine the association between biomass fuels exposure and COPD occurrence in rural areas of western China. Our findings may provide a scientific basis for targeted strategies and measures to reduce biomass fuels exposure, especially in remote rural areas of China.

Methods

Study Design and Participants

The baseline survey- The National Science & Technology Pillar Program during the 12th Five-year Plan Period, implemented from June 1, 2013 to March 1, 2014, Chinese participants were recruited from the rural population (n = 48,109,000) of Mianyang, Sichuan Province in China. And the follow-up time ended between October 1, 2017 and October 1, 2018 (the 13th Five-year Plan).

At the baseline survey, we used a multistage, stratified cluster sampling procedure to enroll a nationally representative sample. In stage one, we stratified administrative divisions in Mianyang into two levels based on gross domestic product (GDP) data from the Mianyang Bureau of Statistics. In each of the two levels, we used a random number table to select one administrative division comprising Fucheng District and Jiangyou City. In stage two, we used GDP data to further stratify towns or subdistricts located in Fucheng District and Jiangyou City into two sublevels. From each of these sublevels, we randomly selected one town or subdistrict from Fucheng District (Qingyi and Xinzao) and Jiangyou City (Erlangmiao and Sanhe). In stage three, we selected all villages or residential communities from within Qingyi, Xinzao, Erlangmiao, and Sanhe. In stage four, proportional random sampling was used to select 15% of permanent residents at least 40 years old in each village or residential community for enrollment in the study (Figure 1).

Figure 1 The flow chart for sampling strategy. In stage one, we stratified administrative divisions in Mianyang into two levels based on gross domestic product (GDP) data from the Mianyang Bureau of Statistics. In stage two, we used GDP data to further stratify towns or subdistricts located in Fucheng District and Jiangyou City into two sublevels. In stage three, we selected all villages or residential communities. In stage four, proportional random sampling was used to select 15% of permanent residents at least 40 years old in each village or residential community for enrollment in the study.

For the analyses reported in this article, data were analyzed using a nested case-control study. Participants were included in this study if they satisfied the following criteria: (i) they had been living in the sampled community for more than 6 months by the time of study enrollment; (ii) they had no prior COPD diagnosis, based on registry data or interviews; (iii) they were at least 40 years old; and (iv) they participated in the physical examination of the 12th Five-year Plan (baseline survey in 2014 to 2015). Furthermore, we excluded individuals if they were physically incapable of taking a spirometry test, eg due to thoracic, abdominal, or eye surgery, retinal detachment, or myocardial infarction in the past 3 months; if they had been admitted to hospital for any cardiac condition in the past month; if their heart rate was greater than 120 beats per min; if they were on antibacterial chemotherapy for tuberculosis; or if they were pregnant or breastfeeding. The subjects in this study were recruited by doctors, nurses and village doctors in the local township health center. The principle of convenience sampling was adopted to select subjects meeting the inclusion and exclusion criteria until the expected sample size of the study in the town was reached.

The present study was approved by the Ethics Committee of West China Hospital, Sichuan University (NO.2013–55 and NO.2019–151), and it conformed to the provisions of the Declaration of Helsinki. Each participant signed an informed consent form before enrollment.

Data Collection

Demographics and Clinical Parameters

Research staff received appropriate training and then collected data at examination centers in local health facilities and community clinics in the towns/subdistricts selected for inclusion in the study. The staff conducted standardized face-to-face interviews based on a custom-made questionnaire. The questionnaire collected the following sociodemographic characteristics and clinical information: sex, age, educational level, area of residence, medical history (chronic bronchitis, asthma, COPD, emphysema, tuberculosis), COPD-related symptoms (cough, wheezing, chest tightness, expectoration), and risk factors (smoking history, passive smoking, occupational exposure, childhood history of chronic cough, family history of chronic bronchitis/COPD/emphysema). Physical examination included height, weight, waist circumference, blood pressure, and heart rate. Each questionnaire was assigned a unique identification number.

Spirometry Test

Trained and certified technicians performed pulmonary function tests on all participants using a MasterScreen Pneumo PC spirometer (JAEGER, Wurzburg, Germany). The spirometer was calibrated daily before participants were tested. Participants were required to do up to eight forced expiratory maneuvers until the forced vital capacity (FVC) and forced expiratory volume in 1 s (FEV1) were reproducible within 150 mL.¹⁴ Then, 400 μg of the bronchodilator salbutamol (Glaxo Wellcome, Brentford, UK) was administered by inhalation with a 500-mL spacer. After 20 min, spirometry testing was repeated as above. We did all spirometric manoeuvres with the participant in a seated position, wearing a nose clip, and using a disposable mouthpiece. An expert panel performed quality control analysis on the test results based on criteria from the American Thoracic Society and European Respiratory Society. Tests were excluded if they were judged to be of poor quality¹⁴.

Data Upload and Storage

Questionnaires were converted into digital data through optical character recognition (OCR) technology (PS306U, Plustek, Taiwan, China). The digitized data and spirometry data were exported and stored securely on a data cloud platform at the College of Computer Science, Sichuan University.

Nested Case-Control Study

Definition of Cases

Cases were defined as patients diagnosed with COPD. COPD was diagnosed according to the 2023 Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines¹⁵ as a post-bronchodilator FEV1:FVC ratio less than 0.70. We calculated the FEV1:FVC ratio for each participant in this study. Calculated ratios were classified by stages reflecting the predicted degree of breathing obstruction. Stages were determined based on reference FEV1 values from the US general population (n=7429 adults):¹⁶ GOLD stage I, ≥ 80% predicted; GOLD stage II, ≥ 50% to < 80% predicted; GOLD stage III, ≥ 30% to < 50% predicted; and GOLD stage IV, < 30% predicted.

Definition of Controls

Controls were defined as individuals who did not occurrence of COPD during follow-up.

Exposure

Exposure to biomass fuels was the exposure of interest. The definition of biomass fuels in this study included crop straw, wood, firewood and animal manure. Subjects were considered to be exposed to biomass fuels if they cooked frequently (>5/week) using biomass fuels (wood/firewood/crop straw or animal dung), regardless of whether biomass fuels were the main cooking fuel. Subjects were considered to be exposed to coal if they cooked frequently using coal, regardless of whether coal was the primary cooking fuel. The rate of biomass exposure was defined as the proportion of subjects who were exposed to biomass fuels.

Outcomes

The primary outcomes of this study was the the occurrence of COPD.

Covariates

Covariates consisted of age, male or female sex, ethnicity, educational level, urbanisation, body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]), smoking history, History of tuberculosis, history of asthma, chronic cough during childhood, family history of chronic bronchitis/COPD/emphysema, house ventilation, dust, exposure to coal, kitchen ventilation, occupational exposure, and exposure to secondhand smoke.

Statistical Analysis

Demographic information included age, sex, and region. Since older adults are more likely to develop COPD, we divided participants into two age groups: 40–59 or ≥ 60 years old. Subjects reporting biomass fuels exposure were compared to those reporting no exposure in terms of sociodemographic and clinical parameters in addition to risk factors, domestic ventilation, cooking with coal, and occupational exposure.

The measurement data such as age and lung function followed a normal distribution and were described by means±standard deviation (SD). Data on demographic characteristics, COPD occurrence, and biomass fuels exposure were reported as frequencies or percentages. We assessed the statistical significance of differences using Student’s t-test and ANOVA for continuous variables, the χ2 test and Fisher’s exact test for categorical variables. The Cochran–Armitage trend test was used to identify the trend across ordered groups such as COPD rates across groups exposed to biomass fuels for different periods of time. Multivariate logistic regression was used to model the influence of biomass fuels exposure on COPD after adjusting for confounding factors. Bayes’ theorem¹⁷ was used to weight the relative contributions of various risk factors to the occurrence of COPD.

Data were analyzed using SPSS 20.0 (IBM, Armonk, NY, USA). Differences associated with a P < 0.05 were considered significant.

Results

Characteristics of the Study Participants

Between October 2017 and October 2018, 11421 individuals were invited to participate in this study. Of the11398individuals included in the final analysis, 4848 (42.45%) were male and the mean age was 57.67±9.58 years. Approximately 47.60% of participants were living in Fucheng district, while 52.40% were living in Jiangyou county. The majority of participants were Han Chinese (98.82%). Individuals with GOLD stage III and IV were combined because of the small sample sizes. General characteristics and risk factors of the study population are presented in Table 1.

Table 1 Demographic Characteristics and Lung Function of the People Over 40 Years Old in Rural Western China

According to the behavior and living habits reported by participants, most families used firewood/animal excrement for daily cooking (88.35%). Roughly half (52.36%) did not use coal for daily cooking. Most participants believed that their living environment was well ventilated (71.78%), whereas only 0.17% of the subjects considered it to be poor. Most participants believed that their kitchens were well ventilated (53.61%), whereas only 0.93% of the subjects considered the ventilation to be poor. Very few subjects (1.91%) considered their living environment dusty.

Factors Associated with COPD Occurrence

We newly diagnosed 500 participants with COPD according to the 2023 GOLD guidelines, which corresponded to an overall incidence of 4.39%. After standardizing the population composition of different age groups in Mianyang city in 2021, the standardized incidence of COPD increased to 4.51%.

Older age significantly increased likelihood of COPD (P < 0.001), as did being male (7.05% vs 2.41%) and living in a rural area (4.55% vs 3.56%). Conversely, higher levels of education were associated with lower incidence (2.85% vs 5.22%). Incidence was higher among underweight subjects than among those with normal body mass index (BMI) (12.55% vs 5.12%). A history of any of the following health conditions was associated with significantly higher incidence of COPD: tuberculosis (12.90 vs 4.32%), chronic inflammation (25.62% vs 3.67%), asthma (24.44% vs 4.10%), emphysema (31.46% vs 4.15%), chronic cough during adolescence (10.84% vs 4.34%), a family history of chronic bronchitis/COPD/emphysema (10.36% vs 4.36%), or exposure to secondhand smoke (10.90% vs 1.71%). Finally, the incidence of COPD was slightly higher among participants who were exposed to dust through their occupation than among those who were not (6.71% vs 4.35%) (Table 2).

Table 2 Demographics and Risk Factors for Chronic Obstructive Pulmonary Disease Aged 40 years Older, Stratified by Exposure History of Biomass Fuels

Among the subjects with COPD in this study, The proportion of GOLD stage I, II and III-IV was 25.20%, 40.8% and 34.00%, respectively. Those with GOLD grade III-IV disease had the most obvious clinical symptoms, including frequent cough (8.82%), expectoration (4.71%), wheezing (7.06%), air tightness (6.47%), and dyspnea (52.36%). Prevalence of these symptoms was lower among subjects with GOLD grade IorII. For example, self-reported cough in GOLD gradeIwas 3.97% and 5.88% in GOLD gradeII. As the GOLD grade increased, so did the degree of breathing difficulty (P<0.001), Those patients with GOLD grade III-IV, the mMRC score of dyspnea grade 3 accounted for 51.18% and grade 4 accounted for 1.18%. (Table 3).

Table 3 The Occurrence of COPD in People Over 40 Years Old in Rural Western China, by GOLD Stage

Associations Between Biomass Fuels Exposure and COPD

A total of 468 (4.65%) were newly diagnosed with COPD in the population exposed to biomass fuels, compared to 32 (2.41%) among those who were not exposed to biomass fuels. There was a significant difference in the incidence of COPD between the two groups (χ2 = 5.487, P < 0.05), and the odds risk (OR) was 1.83 (95% CI 1.19–2.68). Subjects with COPD in the biomass fuels exposure group showed significantly worse lower lung function than those in the non-exposure group in terms of mean FVC (75.81±27.30 vs 84.72±27.59), mean FEV1 (57.47±21.86 vs 63.93±23.79), and FEV1:FVC (57.00±8.01 vs 59.44±7.76) (all P < 0.05). Incidence of COPD increased with longer exposure to biomass fuels (χ2 trend = 9.263, P = 0.02) (Figure 2).

Figure 2 The incidence of COPD at different biomass fuel exposure times. Bars represent the incidence of COPD, and error bars 95% CI. The horizontal axis represents the exposure time of biomass fuels.

Exposure to biomass fuels was positively associated with COPD (OR= 2.58, 95% CI: 2.23–3.05, P < 0.001) after adjusting for the following potential confounding factors: age, sex, educational level, BMI, smoking, occupational exposure, use of coal in daily cooking, passive smoking, family history of chronic bronchitis/COPD/emphysema, history of tuberculosis, and childhood history of severe cough or asthma (Table 4).

Table 4 Multivariate Analysis for COPD Associated with Biomass Fuels Occurrence in Rural Western Chinese Population Over 40 Years Old

In subgroup analysis, exposure to biomass fuels increased the risk of COPD in men by 1.71 times (95% CI 1.09–2.68, P<0.001) and in women by 2.88 times (95% CI 2.01–3.48, P<0.001) (Table 5), and in never-smokers by 2.18 times (95% CI: 1.53–3.11, P<0.001) (Table 6).

Table 5 Subgroup Analysis of COPD Occurrence in Rural Western Chinese Population Over 40 Years Old by Sex

Table 6 Subgroup Analysis of COPD Occurrence in Rural Western Chinese Population Over 40 Years Old by Smoking History

Weighted Contributions of Risk Factors

Based on Bayes’ theorem, the following factors contributed most to risk of COPD: poor kitchen ventilation (W=31.13%), family history of chronic bronchitis/ emphysema/COPD (W=19.18%), biomass fuels exposure (W=18.08%), age (W=17.04%), sex (W=16.80%), and underweight (W=16.74%) (Table 7).

Table 7 Weight of Risk Factors for COPD Occurrence in Rural Western Chinese Population Over 40 Years Old

Discussion

This study found that the standardized incidence of COPD was 4.51%. The incidence of COPD varies greatly by country, region, age and sex, epidemiological studies in European, Asian and North American countries have estimated the incidence of COPD in their populations to be 1.40–8.92%.^18–22 In recent years, to the best of our knowledge, there were no reports on the incidence of COPD in China. Many cross-sectional surveys have reported the prevalence of COPD in China.^4,6,23 The CPH study found that the prevalence of COPD was 8.6% among adults 20–39 years old and 13.7% among adults at least 40 years old 4. It can be seen that COPD has become a major chronic noninfectious disease that seriously affects human health in the 21st century.

This study found evidence that biomass fuels exposure significantly increases risk of COPD, which meant 2.58 times higher risk in our sample, in never-smokers by 2.18 times. This relationship held true even after controlling for numerous potential confounders.

Our results are consistent with previous studies showing that indoor air pollution caused by biomass fuels contributes to respiratory tract infection, COPD, tuberculosis, asthma, cardiovascular disease and other diseases.^23–26 An epidemiological investigation of 25 627 residents at least 40 years old in seven provinces or cities in China found that those who used biomass fuels for cooking or heating were at significantly higher risk of COPD than those who did not (OR=1.35, 95% CI: 1.20–1.52), after adjusting for risk factors such as smoking, age, and sex.²³ A cross-sectional investigation into COPD prevalence among 50 991 people at least 20 years old in 10 provinces, municipalities or autonomous regions of China also found higher COPD risk among those who used biomass fuels for cooking or heating, after adjusting for several confounding factors (OR=1.25, 95% CI:0.95–1.65, P= 0.10).⁴ Similarly, meta-analyses have reported that women exposed to biomass fuels are at 2–3 times higher risk of COPD than those not exposed.^25,26

This literature and the present study strengthen the association between biomass fuels exposure and development of COPD. We found that biomass fuels exposure and poor kitchen ventilation are among the greatest contributors to COPD in western rural areas. Our Bayesian weighting identified age, sex and family history of chronic bronchitis/COPD/emphysema as unmodifiable COPD risk factors, while biomass fuels exposure and kitchen ventilation emerged as the most important modifiable risk factors for COPD. In terms of the global burden of disease, household use of solid fuels (biomass fuels, coal) ranks 10th among all major risk factors and second among environmental risk factors.²⁷ The WHO lists indoor air pollution caused by biomass fuels exposure as the 10th most important risk factor worldwide, and the fourth greatest preventable contributor to disease burden in developing countries.¹² Exposure to biomass fuels and the associated indoor air pollution pose significant problems to public health, particularly in populations still using rudimentary equipment or “dirty energy”. Our data highlight the need for initiatives at local and national levels to improve living conditions in those populations, thereby lowering their COPD risk.

Subgroup analysis showed that biomass fuels exposure was more closely associated with COPD in women (OR 2.88) than in men (OR 1.71). This may be because women are more sensitive to smoke^28,29 and/or are more exposed to biomass fuels, especially those living in rural areas, where they often help the mother in the kitchen from an early age. Children exposed to biomass fuels are at greater risk of respiratory tract infection,^30,31 which in turn increases their risk of COPD in adulthood.³² Moreover, pregnant women exposed to smoke from biomass fuels tend to give birth to smaller babies³³ who are at higher risk of adverse lung development and therefore higher risk of COPD later in life.^34,35

In this study, 88.35% of our sample was exposed to biomass fuels. This exposure rate is higher than that in previous studies. One 2018 study³⁶ showed that the rate of biomass fuels exposure from cooking among women at least 40 years old in China was 56.3% in rural areas and 19.9% in urban areas. Exposure rates due to cooking among women in other regions in China have ranged from a low of 27.9% in eastern regions to 45.0% in western regions. A 2014 study inferred from national census data that 59–75% of households in rural areas of China still used biomass fuels as the main cooking fuels.³⁷ The reason why our incidence is higher than in other studies may be that our sample was from rural areas in Sichuan Province, located in the west of China, where people have access to abundant local crop and timber resources for biomass fuels.

Due to the large number of people affected by biomass fuels, sufficient attention should be paid to its impact on COPD burden in the population. The WHO estimates that about 2.6 billion people worldwide use biomass fuels and coal as the main source of energy for cooking, heating and other household needs 12, even more numerous than the 1.1 billion smokers of cigarettes worldwide.³⁸ Polluting fuels such as biomass will continue to be used in China and globally for a long time, especially in rural areas, because they are inexpensive and they support traditional cooking and heating practices. Greater attention should be paid to the impact of biomass fuels on the disease burden in developing countries, particularly among children and women.

The present study had several limitations. First, our data on exposure history, family history were based on self-reporting, creating risk of recall bias. Second, the exposure to biomass fuels has not been quantified accurately, it was divided into 5 groups: “<6 months”, “1~2 years”, “3~5 years”, “5~10 years”, and more than 10 years, it is not possible to pinpoint the specific exposure time of each individual. At the same time, this study did not measure the exposure concentration of biomass fuels. Third, several known risk factors of COPD were not investigated in the present study, such as PM2.5. Fourth, this study was carried out in the rural area of Mianyang city, which is located in Sichuan Province, the west of China. The results of this study may be representative of rural areas in western China, but the incidence of COPD in rural areas across the country needs to be further explored by multi-center, large-sample cohort studies. Finally, similar to other large-scale population-based surveys, the diagnosis of COPD was based only on spirometry tests done in our study. Many participants might have airflow limitation but not clinical COPD.

Conclusion

The data from this study show that COPD is still increasing rapidly in rural areas of western China, and exposed to biomass fuels during cooking or heating are at greater risk of developing COPD. In rural areas where incomes are low and energy sources limited, residents often use inexpensive but easily accessible local materials as the main energy source for daily living. Efforts should be made to strengthen the construction of clean energy infrastructure, so as to reduce the use of biomass fuels and thereby help prevent COPD.