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Indoor air pollution and risk of lung cancer among Chinese female non-smokers

Cancer Causes & Control volume 24, pages 439–450 (2013)Cite this article

Abstract

Purpose

To investigate indoor particulate matter (PM) level and various indoor air pollution exposure, and to examine their relationships with risk of lung cancer in an urban Chinese population, with a focus on non-smoking women.

Methods

We conducted a case–control study in Taiyuan, China, consisting of 399 lung cancer cases and 466 controls, of which 164 cases and 218 controls were female non-smokers. Indoor PM concentrations, including PM1, PM2.5, PM7, PM10, and TSP, were measured using a particle mass monitor. Unconditional logistic regression models were used to calculate odds ratios (ORs) and 95 % confidence intervals after adjusting for age, education, annual income, and smoking.

Results

Among non-smoking women, lung cancer was strongly associated with multiple sources of indoor air pollution 10 years ago, including heavy exposure to environmental tobacco smoke at work (aOR = 3.65), high frequency of cooking (aOR = 3.30), and solid fuel usage for cooking (aOR = 4.08) and heating (aORcoal stove = 2.00). Housing characteristics related to poor ventilation, including single-story, less window area, no separate kitchen, no ventilator, and rarely having windows open, are associated with lung cancer. Indoor medium PM2.5 concentration was 68 μg/m3, and PM10 was 230 μg/m3. PM levels in winter are strongly correlated with solid fuel usage for cooking, heating, and ventilators. PM1 levels in cases are more than 3 times higher than that in controls. Every 10 μg/m3 increase in PM1 is associated with 45 % increased risk of lung cancer.

Conclusions

Indoor air pollution plays an important role in the development of lung cancer among non-smoking Chinese women.

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Fig. 1
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Abbreviations

PM:

Particulate matter

ETS:

Environmental tobacco smoke

OR:

Odds ratio

aOR:

Adjusted OR

95 % CI:

95 % confidence interval

IAP:

Indoor air pollution

PAH:

Polycyclic aromatic hydrocarbons

References

  1. IARC (2008) Cancer incidence, mortality and prevalence worldwide in 2008. Globocan 2008

  2. Wang JB, Jiang Y, Wei WQ, Yang GH, Qiao YL, Boffetta P (2010) Estimation of cancer incidence and mortality attributable to smoking in China. Cancer Causes Control 21(6):959–965

    PubMed  Article  Google Scholar 

  3. Franchini M, Mannucci PM (2007) Short-term effects of air pollution on cardiovascular diseases: outcomes and mechanisms. J Thromb Haemost 5(11):2169–2174

    PubMed  Article  CAS  Google Scholar 

  4. Mannino DM, Buist AS (2007) Global burden of COPD: risk factors, prevalence, and future trends. Lancet 370(9589):765–773

    PubMed  Article  Google Scholar 

  5. Boffetta P (2006) Human cancer from environmental pollutants: the epidemiological evidence. Mutat Res 608(2):157–162

    PubMed  Article  CAS  Google Scholar 

  6. Yang G, Fan L, Tan J, Qi G, Zhang Y, Samet JM, Taylor CE, Becker K, Xu J (1999) Smoking in China: findings of the 1996 national prevalence survey. JAMA 282(13):1247–1253

    PubMed  Article  CAS  Google Scholar 

  7. Wakai K, Inoue M, Mizoue T, Tanaka K, Tsuji I, Nagata C, Tsugane S (2006) Tobacco smoking and lung cancer risk: an evaluation based on a systematic review of epidemiological evidence among the Japanese population. Jpn J Clin Oncol 36(5):309–324

    PubMed  Article  Google Scholar 

  8. Alberg AJ, Ford JG, Samet JM (2007) Epidemiology of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 132(3 Suppl):29S–55S

    PubMed  Article  CAS  Google Scholar 

  9. Ellickson PL, Orlando M, Tucker JS, Klein DJ (2004) From adolescence to young adulthood: racial/ethnic disparities in smoking. Am J Public Health 94(2):293–299

    PubMed  Article  Google Scholar 

  10. Services UDoHaH (1987) Smoking and health: a national status report. In: US Government Printing Office, Washington, DC

  11. Peto R (1985) Control of tobacco-related disease. Ciba Found Symp 110:126–142

    PubMed  CAS  Google Scholar 

  12. Tang N, Wu Y, Zhou B, Wang B, Yu R (2009) Green tea, black tea consumption and risk of lung cancer: a meta-analysis. Lung Cancer 65(3):274–283

    PubMed  Article  Google Scholar 

  13. Boehm K, Borrelli F, Ernst E, Habacher G, Hung SK, Milazzo S, Horneber M (2009) Green tea (Camellia sinensis) for the prevention of cancer. Cochrane Database Syst Rev (3):CD005004

  14. Li Y, Chang SC, Goldstein BY, Scheider WL, Cai L, You NC, Tarleton HP, Ding B, Zhao J, Wu M et al (2011) Green tea consumption, inflammation and the risk of primary hepatocellular carcinoma in a Chinese population. Cancer Epidemiol 35(4):362–368

    PubMed  Article  Google Scholar 

  15. Wu M, Liu AM, Kampman E, Zhang ZF, Van’t Veer P, Wu DL, Wang PH, Yang J, Qin Y, Mu LN (2009) Green tea drinking, high tea temperature and esophageal cancer in high- and low-risk areas of Jiangsu Province, China: a population-based case-control study. Int J Cancer 124(8):1907–1913

    PubMed  Article  CAS  Google Scholar 

  16. Mu LN, Lu QY, Yu SZ, Jiang QW, Cao W, You NC, Setiawan VW, Zhou XF, Ding BG, Wang RH et al (2005) Green tea drinking and multigenetic index on the risk of stomach cancer in a Chinese population. Int J Cancer 116(6):972–983

    PubMed  Article  CAS  Google Scholar 

  17. Wang N, Chen WQ, Zhu WX, Xing XM, Lu AP, Yang L (2011) Incidence trends and pathological characteristics of lung cancer in urban Beijing during period of 1998–2007. Zhonghua Yu Fang Yi Xue Za Zhi 45(3):249–254

    PubMed  Google Scholar 

  18. Wang X, Qin Y, Gu J, Wang F, Jia P, Wang H, Yao Q, Zhu S (2011) Systematic review of studies of workplace exposure to environmental tobacco smoke and lung cancer risk. Zhongguo Fei Ai Za Zhi 14(4):345–350

    PubMed  Google Scholar 

  19. Eisner MD (2010) Secondhand smoke at work. Curr Opin Allergy Clin Immunol 10(2):121–126

    PubMed  Article  Google Scholar 

  20. Zhao H, Gu J, Xu H, Yang B, Han Y, Li L, Liu S, Yao H (2010) Meta-analysis of the relationship between passive smoking population in China and lung cancer. Zhongguo Fei Ai Za Zhi 13(6):617–623

    PubMed  Google Scholar 

  21. Wen W, Shu XO, Gao YT, Yang G, Li Q, Li H, Zheng W (2006) Environmental tobacco smoke and mortality in Chinese women who have never smoked: prospective cohort study. BMJ 333(7564):376

    PubMed  Article  Google Scholar 

  22. Trichopoulos D, Kalandidi A, Sparros L, MacMahon B (1981) Lung cancer and passive smoking. Int J Cancer 27(1):1–4

    PubMed  Article  CAS  Google Scholar 

  23. Boffetta P (2002) Involuntary smoking and lung cancer. Scand J Work Environ Health 28(Suppl 2):30–40

    PubMed  CAS  Google Scholar 

  24. Boffetta P, Agudo A, Ahrens W, Benhamou E, Benhamou S, Darby SC, Ferro G, Fortes C, Gonzalez CA, Jockel KH et al (1998) Multicenter case-control study of exposure to environmental tobacco smoke and lung cancer in Europe. J Natl Cancer Inst 90(19):1440–1450

    PubMed  Article  CAS  Google Scholar 

  25. Zhong L, Goldberg MS, Parent ME, Hanley JA (2000) Exposure to environmental tobacco smoke and the risk of lung cancer: a meta-analysis. Lung Cancer 27(1):3–18

    PubMed  Article  CAS  Google Scholar 

  26. Taylor R, Najafi F, Dobson A (2007) Meta-analysis of studies of passive smoking and lung cancer: effects of study type and continent. Int J Epidemiol 36(5):1048–1059

    PubMed  Article  Google Scholar 

  27. Mohtashamipur E, Mohtashamipur A, Germann PG, Ernst H, Norpoth K, Mohr U (1990) Comparative carcinogenicity of cigarette mainstream and sidestream smoke condensates on the mouse skin. J Cancer Res Clin Oncol 116(6):604–608

    PubMed  Article  CAS  Google Scholar 

  28. Denissenko MF, Pao A, Tang M, Pfeifer GP (1996) Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 274(5286):430–432

    PubMed  Article  CAS  Google Scholar 

  29. Hoh E, Hunt RN, Quintana PJ, Zakarian JM, Chatfield D, Wittry BC, Rodriguez E, Matt GE (2012) Environmental tobacco smoke as a source of polycyclic aromatic hydrocarbons in settled household dust. Environ Sci Technol 46(7):4174–4183

    Google Scholar 

  30. Oberg M, Jaakkola MS, Woodward A, Peruga A, Pruss-Ustun A (2011) Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet 377(9760):139–146

    PubMed  Article  Google Scholar 

  31. Hosgood HD III, Boffetta P, Greenland S, Lee YC, McLaughlin J, Seow A, Duell EJ, Andrew AS, Zaridze D, Szeszenia-Dabrowska N et al (2010) In-home coal and wood use and lung cancer risk: a pooled analysis of the international lung cancer consortium. Environ Health Perspect 118(12):1743–1747

    PubMed  Article  CAS  Google Scholar 

  32. Galeone C, Pelucchi C, La Vecchia C, Negri E, Bosetti C, Hu J (2008) Indoor air pollution from solid fuel use, chronic lung diseases and lung cancer in Harbin, Northeast China. Eur J Cancer Prev 17(5):473–478

    PubMed  Article  Google Scholar 

  33. Lan Q, He X, Costa DJ, Tian L, Rothman N, Hu G, Mumford JL (2000) Indoor coal combustion emissions, GSTM1 and GSTT1 genotypes, and lung cancer risk: a case-control study in Xuan Wei, China. Cancer Epidemiol Biomarkers Prev 9(6):605–608

    PubMed  CAS  Google Scholar 

  34. Xu ZY, Blot WJ, Li G, Fraumeni JF Jr, Zhao DZ, Stone BJ, Yin Q, Wu A, Henderson BE, Guan BP (1991) Environmental determinants of lung cancer in Shenyang, China. IARC Sci Publ 105:460–465

    PubMed  Google Scholar 

  35. Zhang JJ, Smith KR (2007) Household air pollution from coal and biomass fuels in China: measurements, health impacts, and interventions. Environ Health Perspect 115(6):848–855

    PubMed  Article  Google Scholar 

  36. Dai XD, Lin CY, Sun XW, Shi YB, Lin YJ (1996) The etiology of lung cancer in nonsmoking females in Harbin, China. Lung Cancer 14(Suppl 1):S85–S91

    PubMed  Article  Google Scholar 

  37. Luo RX, Wu B, Yi YN, Huang ZW, Lin RT (1996) Indoor burning coal air pollution and lung cancer—a case-control study in Fuzhou, China. Lung Cancer 14(Suppl 1):S113–S119

    PubMed  Article  Google Scholar 

  38. Sun X, Dai X, Shi Y, Lin Y (2002) A case-control study on the relationship among indoor air pollution, depression and oncogenesis of lung cancer. Zhongguo Fei Ai Za Zhi 5(2):101–103

    PubMed  Google Scholar 

  39. Kleinerman RA, Wang Z, Wang L, Metayer C, Zhang S, Brenner AV, Xia Y, Shang B, Lubin JH (2002) Lung cancer and indoor exposure to coal and biomass in rural China. J Occup Environ Med 44(4):338–344

    PubMed  Article  Google Scholar 

  40. Zhao Y, Wang S, Aunan K, Seip HM, Hao J (2006) Air pollution and lung cancer risks in China—a meta-analysis. Sci Total Environ 366(2–3):500–513

    PubMed  Article  CAS  Google Scholar 

  41. Zhang J, Smith KR, Ma Y, Ye S, Jiang F, Qi W, Liu P, Khalil MAK, Rasmussen RA, Thorneloe SA (2000) Greenhouse gases and other airborne pollutants from household stoves in China: a database for emission factors. Atmos Environ 34(26):4537–4549

    Article  CAS  Google Scholar 

  42. Zhang J, Smith KR (1996) Hydrocarbon emissions and health risks from cookstoves in developing countries. J Expo Anal Environ Epidemiol 6(2):147–161

    PubMed  Google Scholar 

  43. Chen H, Goldberg MS, Villeneuve PJ (2008) A systematic review of the relation between long-term exposure to ambient air pollution and chronic diseases. Rev Environ Health 23(4):243–297

    PubMed  CAS  Google Scholar 

  44. Turner MC, Krewski D, Pope CA III, Chen Y, Gapstur SM, Thun MJ (2011) Long-term ambient fine particulate matter air pollution and lung cancer in a large cohort of never-smokers. Am J Respir Crit Care Med 184(12):1374–1381

    PubMed  Article  Google Scholar 

  45. Heidi Elizabeth Satff Medtl JF (2003) Air quality estimate in Taiyuan, Shanxi Province, China. In: CICERO report

  46. Xie RK, Seip HM, Liu L, Zhang DS (2009) Characterization of individual airborne particles in Taiyuan City, China. Air Qual Atmos Health 2(3):123–131

    PubMed  Article  CAS  Google Scholar 

  47. Tseng CY, Huang YC, Su SY, Huang JY, Lai CH, Lung CC, Ho CC, Liaw YP (2012) Cell type specificity of female lung cancer associated with sulfur dioxide from air pollutants in Taiwan: an ecological study. BMC Public Health 12:4

    PubMed  Article  CAS  Google Scholar 

  48. Lin HH, Murray M, Cohen T, Colijn C, Ezzati M (2008) Effects of smoking and solid-fuel use on COPD, lung cancer, and tuberculosis in China: a time-based, multiple risk factor, modelling study. Lancet 372(9648):1473–1483

    PubMed  Article  CAS  Google Scholar 

  49. Wang XR, Chiu YL, Qiu H, Au JS, Yu IT (2009) The roles of smoking and cooking emissions in lung cancer risk among Chinese women in Hong Kong. Ann Oncol 20(4):746–751

    PubMed  Article  Google Scholar 

  50. Lee CH, Yang SF, Peng CY, Li RN, Chen YC, Chan TF, Tsai EM, Kuo FC, Huang JJ, Tsai HT et al (2010) The precancerous effect of emitted cooking oil fumes on precursor lesions of cervical cancer. Int J Cancer 127(4):932–941

    PubMed  CAS  Google Scholar 

  51. Li M, Yin Z, Guan P, Li X, Cui Z, Zhang J, Bai W, He Q, Zhou B (2008) XRCC1 polymorphisms, cooking oil fume and lung cancer in Chinese women nonsmokers. Lung Cancer 62(2):145–151

    PubMed  Article  Google Scholar 

  52. Yu IT, Chiu YL, Au JS, Wong TW, Tang JL (2006) Dose-response relationship between cooking fumes exposures and lung cancer among Chinese nonsmoking women. Cancer Res 66(9):4961–4967

    PubMed  Article  CAS  Google Scholar 

  53. Metayer C, Wang Z, Kleinerman RA, Wang L, Brenner AV, Cui H, Cao J, Lubin JH (2002) Cooking oil fumes and risk of lung cancer in women in rural Gansu, China. Lung Cancer 35(2):111–117

    PubMed  Article  Google Scholar 

  54. Ko YC, Cheng LS, Lee CH, Huang JJ, Huang MS, Kao EL, Wang HZ, Lin HJ (2000) Chinese food cooking and lung cancer in women nonsmokers. Am J Epidemiol 151(2):140–147

    PubMed  Article  CAS  Google Scholar 

  55. Zhong L, Goldberg MS, Parent ME, Hanley JA (1999) Risk of developing lung cancer in relation to exposure to fumes from Chinese-style cooking. Scand J Work Environ Health 25(4):309–316

    PubMed  Article  CAS  Google Scholar 

  56. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Cogliano V (2006) Carcinogenicity of household solid fuel combustion and of high-temperature frying. Lancet Oncol 7(12):977–978

    PubMed  Article  Google Scholar 

  57. Hecht SS, Seow A, Wang M, Wang R, Meng L, Koh WP, Carmella SG, Chen M, Han S, Yu MC et al (2010) Elevated levels of volatile organic carcinogen and toxicant biomarkers in Chinese women who regularly cook at home. Cancer Epidemiol Biomarkers Prev 19(5):1185–1192

    PubMed  Article  CAS  Google Scholar 

  58. Pan CH, Chan CC, Wu KY (2008) Effects on Chinese restaurant workers of exposure to cooking oil fumes: a cautionary note on urinary 8-hydroxy-2′-deoxyguanosine. Cancer Epidemiol Biomarkers Prev 17(12):3351–3357

    PubMed  Article  CAS  Google Scholar 

  59. Tao F, Gonzalez-Flecha B, Kobzik L (2003) Reactive oxygen species in pulmonary inflammation by ambient particulates. Free Radic Biol Med 35(4):327–340

    PubMed  Article  CAS  Google Scholar 

  60. Brauer M, Avila-Casado C, Fortoul TI, Vedal S, Stevens B, Churg A (2001) Air pollution and retained particles in the lung. Environ Health Perspect 109(10):1039–1043

    PubMed  Article  CAS  Google Scholar 

  61. Lippmann M, Yeates DB, Albert RE (1980) Deposition, retention, and clearance of inhaled particles. Br J Ind Med 37(4):337–362

    PubMed  CAS  Google Scholar 

  62. Squadrito GL, Cueto R, Dellinger B, Pryor WA (2001) Quinoid redox cycling as a mechanism for sustained free radical generation by inhaled airborne particulate matter. Free Radic Biol Med 31(9):1132–1138

    PubMed  Article  CAS  Google Scholar 

  63. Moller P, Folkmann JK, Forchhammer L, Brauner EV, Danielsen PH, Risom L, Loft S (2008) Air pollution, oxidative damage to DNA, and carcinogenesis. Cancer Lett 266(1):84–97

    PubMed  Article  CAS  Google Scholar 

  64. Scapellato ML, Lotti M (2007) Short-term effects of particulate matter: an inflammatory mechanism? Crit Rev Toxicol 37(6):461–487

    PubMed  Article  CAS  Google Scholar 

  65. Lewtas J (2007) Air pollution combustion emissions: characterization of causative agents and mechanisms associated with cancer, reproductive, and cardiovascular effects. Mutat Res 636(1–3):95–133 (Epub 2007 Aug 2017)

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported in part by the National Nature Science Foundation of China grant award to Dr. Lina Mu (NSFC-30500417). The work is also partially supported by NIH grants (ES06718, CA09142, DA11386) and the Alper Research Center for Environmental Genomics of the UCLA Jonsson Comprehensive Cancer Center.

Conflict of interest

We have no financial relationship with the organizations that sponsored the research.

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Authors and Affiliations

  1. Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, SUNY, 270 Farber Hall, Buffalo, NY, 14214, USA

    Lina Mu, Yanli Li, Mya Swanson & William Scheider

  2. Taiyuan City Center for Disease Control and Prevention (CDC), 89 Xinjian Road, Taiyuan, Shanxi, China

    Li Liu, Baoxing Zhao & Jianping Shi

  3. Shanxi Tumor Hospital, 3 Zhigongxin Street, Taiyuan, Shanxi, China

    Rungui Niu

  4. School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai, China

    Jia Su & Shunzhang Yu

  5. Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles (UCLA), 71-225 CHS, 650 Charles E. Young Drive, Los Angeles, CA, USA

    Shen-Chih Chang & Zuo-Feng Zhang

Authors
  1. Lina Mu
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  2. Li Liu
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  3. Rungui Niu
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  9. Jia Su
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  10. Shen-Chih Chang
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  11. Shunzhang Yu
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  12. Zuo-Feng Zhang
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Correspondence to Lina Mu.

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Mu, L., Liu, L., Niu, R. et al. Indoor air pollution and risk of lung cancer among Chinese female non-smokers. Cancer Causes Control 24, 439–450 (2013). https://doi.org/10.1007/s10552-012-0130-8

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Keywords

  • Indoor air pollution
  • Lung cancer
  • Particulate matter
  • Chinese non-smoking female