Burden of lung cancer attributable to household air pollution in the Chinese female population: trend analysis from 1990 to 2019 and future predictions

Carga de doença devida a câncer de pulmão atribuível à poluição do ar domiciliar na população feminina chinesa: análise de tendências de 1990 a 2019 e previsões futuras

Carga de morbilidad del cáncer de pulmón atribuible a la contaminación del aire doméstico en la población femenina china: análisis de tendencias de 1990 a 2019 y predicciones futuras

Zhixue Li Yan Ma Ying Xu About the authors

Abstracts

This study analyzes the long-term trend of the burden of lung cancer attributable to household air pollution in the Chinese female population, from 1990 to 2019, and make predictions for the next decade. Based the data from the 2019 Global Burden of Diseases (GBD 2019), the joinpoint regression model was used to reflect the temporal trend of the burden of lung cancer attributable to household air pollution, and an autoregressive integrated moving average (ARIMA) model was used to predict the burden of disease over the next decade. From 1990 to 2019, the age-standardized mortality and disability-adjusted life years (DALYs) rates of the Chinese female population were higher than the global rates, and the gap due to residential radon increased over time. The burden of lung cancer attributable to solid fuels has shown a significant downward trend while that due to residential radon has increased slightly overall, but remains lower than the former. The burden of lung cancer increased with age, and the peak age of DALYs rates changed from 70 < 75 years in 1990 to 75 < 80 years in 2019. The model predicted that the burden of lung cancer attributable to solid fuels will gradually decrease over the next decade, whereas the burden of lung cancer due to residential radon will gradually increase and surpass the burden due to solid fuels in 2023. Residential radon will become a more important factor of household air pollution than solid fuels in the next decade for the Chinese female population. Future interventions targeted at household air pollution are needed to reduce the burden of lung cancer.

Keywords:
Lung Neoplasms; Cost of Illness; Air Pollution


O objetivo do texto foi analisar a tendência a longo prazo da carga da doença devida a câncer de pulmão atribuível à poluição atmosférica domiciliar na população feminina chinesa de 1990 a 2019 e fazer previsões para a próxima década. Com base nos dados da Carga Global de Doenças 2019 (GBD 2019), o modelo de regressão joinpoint foi utilizado para refletir a tendência temporal da carga da doença devida a câncer de pulmão atribuível à poluição atmosférica domiciliar e um modelo autorregressivo de média móvel integrada (ARIMA), para prevê-la na próxima década. Entre 1990 e 2019, as taxas de mortalidade padronizada por idade e esperança de vida corrigida pela incapacidade (DALYs) da população feminina chinesa foram maiores do que as taxas globais e a diferença devido à exposição residencial a radônio aumentou ao longo do tempo. A carga da doença atribuível a combustíveis sólidos mostrou uma tendência significativa à queda, enquanto aquela devida à exposição residencial a radônio aumentou ligeiramente no geral, mas permanece menor que a primeira. A carga da doença aumentou com a idade, e a idade máxima das taxas de DALYs passou de 70 < 75 anos em 1990 para 75 < 80 anos em 2019. Nosso modelo previu que a carga da doença atribuível aos combustíveis sólidos diminuirá gradualmente na próxima década, enquanto a carga da doença devida ao radônio aumentará paulatinamente e superará a carga devida aos combustíveis sólidos em 2023. A exposição residencial ao radônio se tornará um fator mais importante à poluição atmosférica domiciliar para a população feminina chinesa do que os combustíveis sólidos na próxima década. Futuras intervenções direcionadas à poluição atmosférica domiciliar são necessárias para reduzir a carga do câncer de pulmão.

Palavras-chave:
Neoplasias Pulmonares; Efeitos Psicossociais da Doença; Poluição do Ar


El objetivo fue analizar la tendencia a largo plazo de la carga de morbilidad del cáncer de pulmón atribuible a la contaminación del aire doméstico en la población femenina china de 1990 a 2019 y hacer predicciones para la próxima década. Según los datos de la Carga Global de Enfermedad de 2019 (GBD 2019), se utilizó el modelo de regresión joinpoint para reflejar la tendencia temporal de la carga de morbilidad pulmonar atribuible a la contaminación del aire doméstico y un modelo autorregresivo integrado de media móvil (ARIMA) para predecir la carga de morbilidad durante la próxima década. De 1990 a 2019, las tasas de mortalidad estandarizadas por edad y años de vida ajustados por discapacidad (AVAD) de la población femenina china fueron más altas que las tasas mundiales, y la brecha debida al radón residencial aumentó con el tiempo. La carga de morbilidad atribuible a los combustibles sólidos mostró una significativa tendencia decreciente, mientras que la del radón residencial aumentó ligeramente, pero en niveles inferiores a la anterior. La carga de morbilidad aumentó con la edad, y las tasas de edad máxima de AVAD cambiaron de 70 < 75 años en 1990 a 75 < 80 años en 2019. El modelo predijo que la carga de morbilidad atribuible a los combustibles sólidos disminuirá gradualmente durante la próxima década, mientras que la carga de morbilidad por radón residencial aumentará gradualmente y superará la carga debida a los combustibles sólidos en 2023. El radón residencial se convertirá en un factor más importante de contaminación del aire doméstico que los combustibles sólidos en la próxima década para la población femenina china. Se necesitan intervenciones futuras dirigidas a la contaminación del aire doméstico para reducir la carga del cáncer de pulmón.

Palabras-clave:
Neoplasias Pulmonares; Costo de Enfermedad; Contaminación del Aire


Introduction

The health problems caused by household air pollution have gradually gained more widespread concern and recognition 11. Gordon SB, Bruce NG, Grigg J, Hibberd PL, Kurmi OP, Lam K, et al. Respiratory risks from household air pollution in low and middle income countries. Lancet Respir Med 2014; 2:823-60.,22. Junfeng Z, Smith KR. Household air pollution from coal and biomass cuels in China: measurements, health impacts, and interventions. Environ Health Perspect 2007; 115:848-55.. Since its inception in 1990, the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) has focused on household air pollution from solid fuels and residential radon 33. Murray CJL, Aravkin AY, Zheng P. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020; 396:1223-49.. Studies have found that the inadequate combustion of solid fuels is an important cause of household air pollution, especially in developing countries where houses are poorly ventilated 44. Bruce N, Perezpadilla R, Albalak R. Indoor air pollution in developing countries: a major environmental and public health challenge. Bull World Health Organ 1999; 78:1078-92.,55. Diette GB, Accinelli RA, Balmes JR, Buist AS, Checkley W, Garbe P, et al. Obstructive lung disease and exposure to burning biomass fuel in the indoor environment. Global Heart 2012; 7:265-70.. The World Health Organization (WHO) estimated that 3 billion people worldwide have been exposed to household air pollution from solid fuels 66. World Health Organization. Household air pollution and health. Geneva: World Health Organization; 2016.. GBD 2019 estimated that the magnitude of household air pollution from solid fuels dropped substantially in terms of the percentage of attributable disability-adjusted life years (DALYs) and rank by 2019 33. Murray CJL, Aravkin AY, Zheng P. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020; 396:1223-49.. Nevertheless, 2.31 million people die from the combustion of household solid fuels each year, making it the 10th leading risk factor for the loss of DALYs globally 33. Murray CJL, Aravkin AY, Zheng P. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020; 396:1223-49.,77. Institute for Health Metrics and Evaluation. Global Burden of Disease Study 2019 (GBD 2019): data resources. http://ghdx.healthdata.org/gbd-2019 (accessed on 26/Feb/2022).
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. Moreover, radon is a common and critical air pollutant in indoor environments that is mainly generated from water sources, fuels (e.g., coal and liquefied gas), soil, construction materials, and decorative materials 88. Su C, Pan M, Zhang Y, Kan H, Zhao Z, Deng F, et al. Indoor exposure levels of radon in dwellings, schools, and offices in China from 2000 to 2020: a systematic review. Indoor Air 2022; 32:e12920.,99. World Health Organization. Radon and health. https://www.who.int/news-room/fact-sheets/detail/radon-and-health (accessed on 22/Feb/2022).
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. The Environmental Burden of Disease in European Countries identified radon as one of the main indoor risk factors 1010. Hänninen O, Knol AB, Jantunen M, Lim TA, Conrad A, Rappolder M, et al. Environmental burden of disease in Europe: assessing nine risk factors in six countries. Environ Health Perspect 2014; 122:439-46.. The global environmental burden of disease attributable to residential radon has reached 1,979,000 DALYs for both sexes in the non-smoker population 1111. Noh J, Sohn J, Cho J, Kang DR, Joo S, Kim C, et al. Residential radon and environmental burden of disease among non-smokers. Ann Occup Environ Med 2016; 28:12.. Globally, the burden of lung cancer and summary exposure values of residential radon increased significantly each year from 1990 to 2019 33. Murray CJL, Aravkin AY, Zheng P. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020; 396:1223-49.. A systematic review estimated that the mean concentrations of indoor radon in China from 2000 to 2020 for housings, school buildings, and office buildings were 54.6, 56.1, and 54.9Bq/m3, respectively, which were much higher than the concentrations of the outdoor environment 88. Su C, Pan M, Zhang Y, Kan H, Zhao Z, Deng F, et al. Indoor exposure levels of radon in dwellings, schools, and offices in China from 2000 to 2020: a systematic review. Indoor Air 2022; 32:e12920.. The average indoor activity time of Chinese adults accounts for about 81% of each entire day 1212. Duan X, Zhao X, Wang B, Chen Y, Cao S. Exposure factors handbook of Chinese population (adults). Beijing: Science Press; 2013.. Therefore, indoor air quality may have a significant impact on the health of Chinese residents.

Studies have strongly associated household air pollution from solid fuels with the risk of lung cancer and noted that women are at greater risk than men 1313. Seow WJ, Hu W, Vermeulen R, Iii HDH, Downward GS, Chapman RS, et al. Household air pollution and lung cancer in China:a review of studies in Xuanwei. Chin J Cancer 2014; 33:471-5.,1414. Hosgood HD, Wei H, Sapkota A, Choudhury I, Bruce N, Smith KR, et al. Household coal use and lung cancer: systematic review and meta-analysis of case-control studies, with an emphasis on geographic variation. Int J Epidemiol 2011; 40:719-28.,1515. Kurmi OP , Arya PH, Lam KBH, Sorahan T, Ayres JG. Lung cancer risk and solid fuel smoke exposure: a systematic review and meta-analysis. Eur Respir J 2012; 40:1228-37.. A systematic evaluation and meta-analysis in Asia found an overall odds ratio (OR) of 1.17 (95% confidence interval [95%CI]: 1.01; 1.37) for cooking or heating with biofuels 1616. Bruce N, Dherani M, Liu R, Hosgood HD, Pope D. Does household use of biomass fuel cause lung cancer? A systematic review and evaluation of the evidence for the GBD 2010 study. Thorax 2015; 70:433-41.. Similarly, a case-control study in Nepal reported a slightly higher OR of 1.77 (95%CI: 1.00; 3.14) 1717. Raspanti GA, Hashibe M, Siwakoti B, Wei M, Thakur BK, Pun CB, et al. Household air pollution and lung cancer risk among never-smokers in Nepal. Environ Res 2016; 147:141-5.. Moreover, another study associated the household use of coal for cooking and heating with a combined OR of roughly 2 for lung cancer, with a slightly greater risk in women than men 1515. Kurmi OP , Arya PH, Lam KBH, Sorahan T, Ayres JG. Lung cancer risk and solid fuel smoke exposure: a systematic review and meta-analysis. Eur Respir J 2012; 40:1228-37.. Notably, radon pollution is the second most common cause of lung cancer in the general population, after smoking 1818. World Health Organization. WHO handbook on indoor radon: a public health perspective. Geneva: World Health Organization; 2009.. The risk of lung cancer increases proportionally with indoor radon exposure 1919. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, et al. Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. BMJ 2005; 330:223-6.. Cheng et al. 2020. Cheng ES, Egger S, Hughes S, Weber M, Yu XQ. Systematic review and meta-analysis of residential radon and lung cancer in never-smokers. Eur Respir Rev 2021; 30:200230. conducted a systematic review and meta-analysis, and they reported that the adjusted excess relative risk of lung cancer from residential radon exposure was 0.15 (95%CI: 0.06; 0.25) per 100Bq.m3 of the radon level for never-smokers. Residential radon exposure alone is estimated to have caused 84,000 lung cancer deaths worldwide, in 2019 77. Institute for Health Metrics and Evaluation. Global Burden of Disease Study 2019 (GBD 2019): data resources. http://ghdx.healthdata.org/gbd-2019 (accessed on 26/Feb/2022).
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. In some countries, it is among the leading causes of lung cancer 2121. World Health Organization. More countries act against exposure to radon and associated cancer risks. Geneva: World Health Organization ; 2021.. The attributable risk of lung cancer mortality due to residential radon exposure is 16.5% for the global population, and radon-attributable lung cancer deaths represent a median of 3% of all cancer deaths 2222. Gaskin J, Coyle D, Whyte J, Krewksi D. Global estimate of lung cancer mortality attributable to residential radon. Environ Health Perspect 2018; 126:057009.. However, the burden of lung cancer caused by residential radon has received relatively little attention in China.

An analysis of Chinese tumor registration data showed that lung cancer ranked second in the incidence and first in the mortality of female malignant tumors in 2015 2323. Zheng RS, Sun KX, Zhang SW, Zeng HM, Zou XN, Chen R, et al. Report of cancer epidemiology in China, 2015. Zhonghua Zhong Liu Za Zhi 2019; 41:19-28.. Therefore, we used the GBD database to analyze the long-term trend of the attributable burden of lung cancer caused by household air pollution in the Chinese female population from 1990 to 2019 and compare the results with the global levels. Additionally, we performed a model to predict the burden of lung cancer over the next decade. Our study aims to provide a reference for further research and the formulation of preventive and control policies for lung cancer, especially in women.

Data and methods

Data resources

This study used data from GBD 2019, which applied DALYs and indicators of variables such as morbidity, prevalence, and mortality to comprehensively assess the burden of diseases of 369 diseases and 87 risk factors in 204 countries and regions. To determine the burden of lung cancer in China, this study utilized GBD 2019 data collected from cause-of-death reports, national nutrition and health surveys, chronic diseases and risk factor reports, and other literature reviews. In the database, the factors of lung cancer attributable to household air pollution included solid fuels and residential radon. Details can be found on the website of the Global Health Data Exchange (http://ghdx.healthdata.org).

Disease classification and encoding

Disease classification followed the International Classification of Disease (ICD). In the 10th revision of the ICD, cancers encoded as C34.0, C34.1, C34.2, C34.3, C34.8, C 34.8, and C34.9 were considered as bronchial and lung cancers (collectively “lung cancer”).

Methods for assessing the burden of lung cancer attributable to household air pollution

For each risk factor, GBD 2019 quantified the proportion of the burden of lung cancer that could have been prevented if the exposure levels were maintained at the lowest risk level, which is defined as the theoretical minimum risk exposure level. The population attributable fraction (PAF) was analyzed by comparing the theoretical minimum risk exposure levels and the population-specific exposure levels, assuming constant exposure levels for other risk factors. Based on the framework of comparative risk assessment theory, GBD 2019 calculated the burden of lung cancer attributable to household air pollution by using indicators of PAF and mortality, DALYs, and similar measures.

Statistical method

This study applied age-standardized mortality and DALYs rates to evaluate and compare the burden of lung cancer attributable to household air pollution in the global and Chinese female populations from 1990 to 2019. Joinpoint Regression Program version 4.9.0.1 (https://surveillance.cancer.gov/joinpoint/), developed by the American Institute of Cancer and Research, was used to analyze the long-term trends of the burden of lung cancer 2424. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 2000; 19:335-51.. Log-linear regression was performed to estimate the annual percentage change (APC) and average annual percentage of change (AAPC). The Monte Carlo permutation test determined the number of segmented points, location, and corresponding p-values. The burden of lung cancer was described for different age groups in 1990 and 2019. An ARIMA (autoregressive integrated moving average) model 2525. Linden A, Adams JL, Roberts N. Evaluating disease management program effectiveness: an introduction to time-series analysis. Dis Manag 2003; 6:243-55.,2626. Chaurasia V, Pal S. COVID-19 pandemic: ARIMA and regression model-based worldwide death cases predictions. SN Comput Sci 2020; 1:288. was constructed in SPSS version 24.0 (https://www.ibm.com/), to predict the burden of lung cancer over the next decade. The basic form was ARIMA (p,d,q), in which “p” is the order for autoregressive expression, “q” is the order for the moving average expression, and “d” is the number of differences required for making the time arrangement fixed. White noise test was used to evaluate the model. Additionally, the standardized Bayesian information criterion (BIC) was used to select the optimal model. The test level was set to 0.05.

Results

Trends in the burden of lung cancer attributable to household air pollution in the Chinese female population

From 1990 to 2019, the age-standardized mortality and DALYs rates attributable to household air pollution in China were higher than the global rates. The gap due to solid fuels gradually decreased over time, while the gap due to residential radon tended to increase gradually. The burden of lung cancer due to solid fuels showed a significant decreasing trend (Figures 1 and 2). The standard mortality rate decreased from 4.56 (95%CI: 2.95; 6.47) per 100,000 inhabitants, in 1990, to 1.39 (95%CI: 2.66; 2.43), in 2019; and the AAPC was -3.98% (t = -15.708, 95%CI: -4.47%; -3.48%, p < 0.001) (Figure 1; Table 1). The age-standardized DALYs rate decreased from 112.08 (95%CI: 72.51; 158.56) per 100,000 inhabitants, in 1990, to 30.22 (95%CI: 14.30; 52.55), in 2019; and the AAPC was -4.42% (t = -26.824, 95%CI: -4.74; -4.11, p < 0.001) (Figure 2; Table 2). The burden of lung cancer due to residential radon increased slightly overall, while still remaining lower than the burden due to solid fuels (Figures 1 and 2). The age-standardized mortality rate increased from 0.70 (95%CI: 0.13; 1.49) per 100,000 inhabitants, in 1990, to 0.88 (95%CI: 0.15; 1.85), in 2019; and the AAPC was 0.79% (t = 7.094, 95%CI: 0.57; 1.00, p < 0.001) (Figure 1; Table 1). The age-standardized DALYs rate increased from 17.34 (95%CI: 3.17; 35.85) per 100,000 inhabitants, in 1990, to 19.06 (95%CI: 3.21; 39.82) per 100,000, in 2019; and the AAPC was 0.33% (t = 3.440, 95%CI: 0.14; 0.51, p < 0.001) (Figure 2; Table 2).

Figure 1
Trend of age-standardized mortality rate of lung cancer attributed to household air pollution in the female population.

Table 1
Joinpoint results of age-standardized mortality rate attributed to household air pollution for lung cancer in Chinese female population from 1990 to 2019 (per 100,000 inhabitants).

Figure 2
Trend of age-standardized disability-adjusted life years (DALYs) rate of lung cancer attributed to household air pollution in the female population.

Table 2
Joinpoint results of age-standardized disability-adjusted life years (DALYs) rate attributed to household air pollution for lung cancer in Chinese female population from 1990 to 2019 (per 100,000 inhabitants).

Mortality of lung cancer attributable to household air pollution in different age groups of the Chinese female population in 1990 and 2019

In 1990, the mortality of lung cancer attributable to household air pollution in the Chinese female population increased gradually with age. The mortality due to solid fuels peaked at 80-85 years of age for 41.71 per 100,000 inhabitants, and the mortality due to residential radon peaked at 80 years of age and above for 5.71 per 100,000 inhabitants. The 2019 trend for all age groups was consistent with the 1990 trend. In 2019, people aged 80 and over had the highest rates of mortality due to solid fuels and residential radon: 17.48 and 10.50 per 100,000 inhabitants, respectively. From 1990 to 2019, mortality was mainly caused by solid fuels in all age groups, but it also decreased significantly over time. The age-standardized mortality rate due to residential radon increased among people aged 60 years and older (Figure 3).

Figure 3
Mortality rates of lung cancer attributed to household air pollution in different age groups of the Chinese female population in 1990 and 2019.

The DALYs rates of lung cancer attributable to household air pollution in different age groups of the Chinese female population in 1990 and 2019

In 1990, the DALYs rate of lung cancer attributable to household air pollution in the Chinese female population increased gradually with age, and it peaked in people aged 70-75 years. The DALYs rates of lung cancer due to solid fuels and residential radon were 552.05 and 84.17 per 100,000 inhabitants, respectively. The 2019 trend for all age groups was similar to the 1990 trend. The DALYs rate increased gradually with age and peaked in people aged 75-80 years. The DALYs rates of lung cancer due to solid fuels and residential radon were 205.11 and 125.62 per 100,000 inhabitants, respectively. From 1990 to 2019, the DALYs rates attributable to household air pollution from solid fuels were extremely high for all age groups, but they also decreased significantly. The DALYs rate due to residential radon increased among people aged 60 years and older (Figure 4).

Figure 4
Disability-adjusted life years (DALYs) rates of lung cancer attributed to household air pollution in different age groups of the Chinese female population in 1990 and 2019.

Model construction and prediction

After testing, each selected optimal model is ARIMA (2,0,0). According to the ARIMA model, the burden of lung cancer attributable to household air pollution from solid fuels in the Chinese female population will gradually decrease over the next decade. Furthermore, the age-standardized mortality and age-standardized DALYs rates will decrease to 0.02 and 1.07 per 100,000 inhabitants, in 2029, respectively (Table 3). In contrast, the burden of lung cancer due to residential radon will gradually increase. In 2023, the age-standardized mortality and DALYs rates will reach 0.96 and 20.71 per 100,000 inhabitants, respectively (Table 4). Furthermore, the burden of lung cancer due to residential radon will exceed that of solid fuel, becoming the prevalent part of the total household air pollution burden of lung cancer (Table 3).

Table 3
Forecast of burden of lung cancer in Chinese female population due to solid fuels from 2020 to 2029.
Table 4
Forecast of burden of lung cancer in Chinese female population due to residential radon from 2020 to 2029.

Discussion

This study provides basic data to improve preventive and control strategies for lung cancer, especially in women. Based on the latest data from GBD 2019 2727. Institute for Health Metrics and Evaluation. Global health data exchange. http://ghdx.healthdata.org/ (accessed on 28/Feb/2022).
http://ghdx.healthdata.org/...
, we used the age-standardized mortality and DALYs rates to analyze the burden of lung cancer attributable to household air pollution in the Chinese female population from 1990 to 2019. Additionally, we constructed an ARIMA model to predict the burden of lung cancer over the next decade. The results showed that the burden of lung cancer in China was higher than the global burden from 1990 to 2019. The gap attributable to residential radon increased gradually over time. Although the burden of lung cancer due to solid fuels decreased, it was still higher than the burden due to residential radon, which slightly increased overall. The higher rate of burden of lung cancer among the elderly suggests that the burden of lung cancer in the female population will continue to increase with age and with the aggravation of indoor pollution. According to our model, the estimated age-standardized mortality and DALYs rates due to residential radon will reach 0.96 and 20.71 per 100,000 inhabitants, in 2023, respectively, and exceed the rates due to solid fuels. The above results indicate that the prevention and control of female lung cancer caused by household air pollution in China still requires the long-term joint efforts of all parties.

Lung cancer is one of the most serious malignant tumors; causing death and disability in women all over the world, especially in China 2828. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394-424.. The burden of lung cancer has only increased in severity 2929. GBD 2019 Respiratory Tract Cancers Collaborators. Global, regional, and national burden of respiratory tract cancers and associated risk factors from 1990 to 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Respir Med 2021; 9:1030-49.. Studies have shown that household air pollution, especially when caused by solid fuel combustion or residential radon, is a main risk factor for lung cancer 1919. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, et al. Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. BMJ 2005; 330:223-6.,3030. Vermeulen R, Downward GS, Zhang J, Hu W, Portengen L, Bassig BA, et al. Constituents of household air pollution and risk of lung cancer among never-smoking women in Xuanwei and Fuyuan, China. Environ Health Perspect 2019; 127:97001.. This study found that the age-standardized mortality and DALYs rates of lung cancer due to household air pollution in the Chinese female population were higher than the global rates. Regarding household air pollution due to solid fuels, the burden of lung cancer gap between China and the world has decreased over time, which reflects China’s efforts to promote clean energy and reduce the use of solid fuels 3131. Meng W, Shen G, Shen H, Chen Y, Yun X, Li J, et al. Synergistic health benefits of household stove upgrading and energy switching in rural China. Environ Sci Technol 2021; 55:14567-75.. Notably, the Chinese age-standardized mortality and DALYs rates were roughly double the global rates in 2019, indicating that China still had a large burden of lung cancer due to household air pollution from solid fuels. In terms of residential radon, the overall difference in burden of lung cancer between China and the world increased. In 2019, the Chinese age-standardized mortality and DALYs rates were about 40% higher than the global rates, which may be related to the changes in living and working styles, building types, construction and decorative materials, furniture, and fuel types in recent years 88. Su C, Pan M, Zhang Y, Kan H, Zhao Z, Deng F, et al. Indoor exposure levels of radon in dwellings, schools, and offices in China from 2000 to 2020: a systematic review. Indoor Air 2022; 32:e12920.,3232. Yazzie SA, Davis S, Seixas N, Yost MG. Assessing the impact of housing features and environmental factors on home indoor radon concentration levels on the Navajo Nation. Int J Environ Res Public Health 2020; 17:2813..

Currently, many studies in China have focused on outdoor air pollution. However, there has been relatively little research on household air pollution, which involves studying the relationships between indoor pollutants and their health effects on residents, particularly the impact of indoor air pollutants on the burden of lung cancer of the population. Our study systematically analyzed the burden of lung cancer attributable to household air pollution factors in the Chinese female population over a period of 30 years. The results demonstrated that the burden of lung cancer attributable to household air pollution from solid fuels presented an overall decreasing trend from 1990 to 2019. The AAPCs of the age-standardized mortality and DALYs rates were -3.98% and -4.42%, respectively. The previous data based on GBD 2013 showed that the population attribution fractions (PAFs), deaths, and DALYs due to solid fuels in China decreased significantly from 1990 to 2013 3333. Yin P, Cai Y, Liu JM, Liu YN, Qi JL, Wang LJ, et al. Disease burden attributable to household air pollution in 1990 and 2013 in China. Zhonghua Yu Fang Yi Xue Za Zhi 2017; 51:53-7., when most areas in China gradually began to use cleaner and more effective electricity or natural gas sources for cooking and heating 3131. Meng W, Shen G, Shen H, Chen Y, Yun X, Li J, et al. Synergistic health benefits of household stove upgrading and energy switching in rural China. Environ Sci Technol 2021; 55:14567-75.. However, solid fuels, such as coal and carbon, have been the main materials used for heating and cooking by Chinese residents for a long time. The World Health Organization (WHO) estimated that about 50% of the 3 billion people exposed to household air pollution from solid fuels are in China and India 66. World Health Organization. Household air pollution and health. Geneva: World Health Organization; 2016.. Moreover, women have a higher risk than men of developing lung cancer from solid fuels, such as domestic coal and biofuel 1515. Kurmi OP , Arya PH, Lam KBH, Sorahan T, Ayres JG. Lung cancer risk and solid fuel smoke exposure: a systematic review and meta-analysis. Eur Respir J 2012; 40:1228-37.. In rural areas in low- and middle-income countries, most lung cancer patients are now non-smoker women who cook with solid fuels 3434. Gordon SB , Bruce NG , Grigg J , Hibberd PL , Kurmi OP , Lam KB, et al. Respiratory risks from household air pollution in low and middle income countries. Lancet Respir Med 2014; 2:823-60..

In 2019, the age-standardized mortality and DALYs rates of lung cancer due to solid fuels were 1.39 and 30.22 per 100,000 inhabitants, which are significantly higher than the rates, due to residential radon, of 0.88 and 19.06 per 100,000 inhabitants, respectively. This implies that household air pollution from solid fuels is still a main factor for the burden of lung cancer in the Chinese female population and will be a main factor in the future for a considerable period. It also suggests that in some areas of China, such as the western provinces, household air pollution from solid fuels may still be responsible for a large portion of the burden of lung cancer 3333. Yin P, Cai Y, Liu JM, Liu YN, Qi JL, Wang LJ, et al. Disease burden attributable to household air pollution in 1990 and 2013 in China. Zhonghua Yu Fang Yi Xue Za Zhi 2017; 51:53-7..

While tobacco is the main risk factor for lung cancer, residential radon is the leading cause in never-smokers and the second-leading cause in ever-smokers 3535. Lorenzo-González M, Torres-Durán M, Barbosa-Lorenzo R, Provencio-Pulla M, Barros-Dios JM, Ruano-Ravina A. Radon exposure: a major cause of lung cancer. Expert Rev Respir Med 2019; 13:839-50.. Radon is estimated to cause from 3-14% of all cases of lung cancer within a country, depending on the national average radon level and the prevalence of smoking 1818. World Health Organization. WHO handbook on indoor radon: a public health perspective. Geneva: World Health Organization; 2009.. In buildings, such as homes, schools, and offices, radon levels can vary substantially from 10Bq/m3 to more than 10,000Bq/m399. World Health Organization. Radon and health. https://www.who.int/news-room/fact-sheets/detail/radon-and-health (accessed on 22/Feb/2022).
https://www.who.int/news-room/fact-sheet...
. Given the properties of radon, the occupants of these buildings could unknowingly be living or working in environments with very high radon levels. Moreover, even low concentrations of radon, such as those commonly found in residential settings, pose health risks, and contribute to the occurrence of lung cancer worldwide 3636. Obenchain R, Young SS, Krstic G. Low-level radon exposure and lung cancer mortality. Regul Toxicol Pharmacol 2019; 107:104418.. The risk of lung cancer increases by about 16% per each 100Bq/m3 increase in the long-term average radon concentration 1919. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, et al. Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. BMJ 2005; 330:223-6..

This study determined that the overall burden of lung cancer attributable to residential radon increased in the Chinese female population from 1990 to 2019. The AAPCs of the age-standardized mortality and DALYs rates were 0.79% and 0.33%, respectively, and the APCs were 2.42% and 2.31% from 2016 to 2019, respectively. These results imply that the annual average growth rate was high in recent years, which was consistent with the increasing trend of indoor radon concentration in China during the last two decades 88. Su C, Pan M, Zhang Y, Kan H, Zhao Z, Deng F, et al. Indoor exposure levels of radon in dwellings, schools, and offices in China from 2000 to 2020: a systematic review. Indoor Air 2022; 32:e12920.. However, indoor radon concentrations vary greatly between different areas. This is largely dependent on the radon concentration of a building’s foundation and the surrounding soil 3737. Carrion-Matta A, Lawrence J, Kang CM, Wolfson JM, Li L, Vieira CLZ, et al. Predictors of indoor radon levels in the Midwest United States. J Air Waste Manag Assoc 2021; 71:1515-28., building materials 3838. Yarmoshenko I, Vasilyev A, Malinovsky G, Bossew P, Žunić ZS, Onischenko A, et al. Variance of indoor radon concentration: major influencing factors. Sci Total Environ 2016; 541:155-60., domestic fuels 3939. Zhang Y, Chen B-S, Liu G-Q, Wang J-N, Zhao Z-H, Lin L-Q. Natural gas and indoor air pollution: a comparison with coal gas and liquefied petroleum gas. Biomed Environ Sci 2003; 16:227-36., water 4040. Tan W, Li Y, Tan K, Xie Y, Han S, Wang P. Distribution of radon and risk assessment of its radiation dose in groundwater drinking for village people nearby the W-polymetallic metallogenic district at Dongpo in southern Hunan province, China. Appl Radiat Isot 2019; 151:39-45., and air of the outdoor environment 4141. Park TH, Kang DR , Park SH, Yoon DK, Lee CM. Indoor radon concentration in Korea residential environments. Environ Sci Pollut Res Int 2018; 25:12678-85.. Plus, radon is much more likely to cause lung cancer in people who smoke. In fact, smokers are estimated to be 25 times more at risk from radon than non-smokers 1919. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, et al. Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. BMJ 2005; 330:223-6.. The low rates of smoking among women in developing countries may be increasing, as younger women are taking up smoking at alarming rates 4242. Fronczak A, Polańska K, Makowiec-Dabrowska T, Kaleta D. Smoking among women: strategies for fighting the tobacco epidemic. Przeglad Lekarski 2012; 69:1103-7.. Therefore, national strategies related to cancer control, tobacco control, and indoor air quality should consider including radon exposure as a risk factor 99. World Health Organization. Radon and health. https://www.who.int/news-room/fact-sheets/detail/radon-and-health (accessed on 22/Feb/2022).
https://www.who.int/news-room/fact-sheet...
.

The age-specific results revealed that the peak mortality ages were 80 years and above in 1990 and 2019. The ages associated with the peak DALYs rate increased with time from 70-75 years in 1990 to 75-80 years in 2019. This may suggest that the burden of female lung cancer caused by household air pollution in China mainly affects middle-aged and elderly women. Solid fuels accounted for most of the burden of lung cancer attributable to household air pollution in all age groups, but the burden of lung cancer decreased significantly in 2019, when compared with 1990. Among the population aged 60 years and older, the burden of lung cancer due to residential radon increased significantly from 1990 to 2019. This was consistent with changes in indoor radon pollution. Moreover, this result indicates that indoor radon pollution increasingly impacts the prevention and control of lung cancer in middle-aged and elderly women. Following the national cancer registry data in China, the age-specific incidence and mortality of lung cancer in the Chinese female population increases from the age of 35 2323. Zheng RS, Sun KX, Zhang SW, Zeng HM, Zou XN, Chen R, et al. Report of cancer epidemiology in China, 2015. Zhonghua Zhong Liu Za Zhi 2019; 41:19-28.. At the same time, the population prediction data from the United Nations provide evidence of an aging Chinese population, and it is expected for the elderly to make up more than 35.1% of the total population of China in 2050 4343. Population Division, Department of Economic and Social Affairs, United Nations. World population prospects 2019. https://population.un.org/wpp/Download/Standard/Population/ (accessed on 28/Feb/2022).
https://population.un.org/wpp/Download/S...
. It can be inferred that the burden of lung cancer caused by lung cancer in the Chinese female population will continue to increase if household air pollution preventive and control measures remain unchanged.

This study found that the burden of lung cancer attributable to household air pollution from residential radon was lower than that from solid fuels, but also showed a long-term increasing trend. According to the model, the burden of lung cancer due to solid fuels will continue to decrease, while the burden of lung cancer due to residential radon will increase significantly. In 2023, the age-standardized mortality and DALYs rates due to residential radon are predicted to reach 0.96 and 20.71 per 100,000 inhabitants, respectively, which are both higher than the rates due to solid fuels. Therefore, preventive and control measures must be strengthened to address household air pollution, specifically household air pollution caused by residential radon. For example, it is urgent to improve public awareness of radon protection 4444. Vogeltanz-Holm N, Schwartz GG. Radon and lung cancer: what does the public really know? J Environ Radioact 2018; 192:26-31., provide relevant information about household radon levels and their health risks 4545. Samet JM. Indoor radon and lung cancer. Estimating the risks. West J Med 1992; 156:25-9., promote the implementation of radon prevention and radon reduction measures, and strengthen the corresponding laws and market regulations 1818. World Health Organization. WHO handbook on indoor radon: a public health perspective. Geneva: World Health Organization; 2009..

This study is limited since the household air pollution data from GBD 2019 only focused on residential solid fuels and radon. Hence, there is still a lack of research data on other indoor air pollutants 4646. Roth GA, Mensah GA, Johnson CO, Addolorato G, Ammirati E, Baddour LM, et al. Global burden of cardiovascular diseases and risk factors, 1990-2019: update from the GBD 2019 study. J Am Coll Cardiol 2020; 76:2982-3021.. The extensive and in-depth development of household air pollution research will gradually improve the lists, quality standards, and systems of household air pollutants that increase burden of lung cancer in China 4747. Gao XH, Chen RJ, Kan HD, Liu W, Deng FR, Li JG, et al. Review on methods in the disease burden assessment attributable to household air pollution. Zhonghua Yu Fang Yi Xue Za Zhi 2018; 52:1315-20.. Currently, solid fuels and residential radon remain the priority for further research and control measures of household air pollution.

This study determined that the overall burden of lung cancer attributable to household air pollution from solid fuels in the Chinese female population decreased significantly from 1990 to 2019. However, the burden of lung cancer due to residential radon is on the rise and will become the main factor of household air pollution in the next decade. Due to the aging population, there is an urgent need for the long-term improvement of household air pollution to prevent and control lung cancer in the Chinese female population.

Acknowledgments

Shenzhen Fundamental Research Program JCYJ20210324125202006.

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Publication Dates

  • Publication in this collection
    10 Oct 2022
  • Date of issue
    2022

History

  • Received
    29 Mar 2022
  • Reviewed
    02 Aug 2022
  • Accepted
    01 Sept 2022
Escola Nacional de Saúde Pública Sergio Arouca, Fundação Oswaldo Cruz Rio de Janeiro - RJ - Brazil
E-mail: cadernos@ensp.fiocruz.br