Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Modification of association between prior lung disease and lung cancer by inhaled arsenic: A prospective occupational-based cohort study in Yunnan, China

Journal of Exposure Science & Environmental Epidemiology volume 26, pages 464–470 (2016)Cite this article

Subjects

Abstract

Arsenic and prior lung diseases have been shown to increase lung cancer risk; however, little is known about their joint effects. The aim of our study was to analyze the joint effects of inhaled arsenic and prior lung diseases on lung cancer risk within a occupational cohort. The interactions of prior lung diseases and inhaled arsenic were analyzed based on multiplicative and additive scales in the Cox proportional hazards model. Compared with low arsenic exposure and no history of asthma, the hazard ratios (HRs) of high arsenic exposure with asthma, high arsenic exposure without asthma and low arsenic exposure with asthma were 2.61 (95% CI: 1.71–4.00), 2.60 (95% CI: 1.93–3.51) and 2.49 (95% CI: 1.53–4.06), respectively. Based on the multiplicative scale in the Cox proportional hazards model, the HR of the interaction of asthma and arsenic on lung cancer risk was 0.45 (95% CI: 0.25–0.80). Based on the additive scale, the relative excess risk due to interaction between asthma and arsenic was −1.41 (95% CI: −2.81 to −0.02). Our study provides strong evidence that arsenic exposure is associated with lung cancer risk. A significant negative interaction between asthma and arsenic on lung cancer risk is observed.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  1. Zheng R, Zeng H, Zuo T, Zhang S, Qiao Y, Zhou Q et al. Lung cancer incidence and mortality in China, 2011. Thorac Cancer 2016; 7: 94–99.

    Article  Google Scholar 

  2. Wang JB, Fan YG, Jiang Yong, Ping Li, Xiao HJ, Chen WQ et al. Attributable causes of lung cancer incidence and mortality in China. Thoracic Cancer 2011; 2: 156–163.

    Article  CAS  Google Scholar 

  3. Krewski D, Lubin JH, Zielinski JM, Alavanja M, Catalan VS, Field RW et al. Residential radon and risk of lung cancer: a combined analysis of 7 North American case-control studies. Epidemiology 2005; 16: 137–145.

    Article  Google Scholar 

  4. Steenland K, Loomis D, Shy C, Simonsen N . Review of occupational lung carcinogens. Am J Ind Med 1996; 29: 474–490.

    Article  CAS  Google Scholar 

  5. Yokota J, Shiraishi K, Kohno T . Genetic basis for susceptibility to lung cancer: recent progress and future directions. Adv Cancer Res 2010; 109: 51–72.

    Article  CAS  Google Scholar 

  6. Guo Y, Zeng H, Zheng R, Li S, Barnett AG, Zhang S et al. The association between lung cancer incidence and ambient air pollution in China: a spatiotemporal analysis. Environ Res 2016; 144: 60–65.

    Article  CAS  Google Scholar 

  7. Brenner DR, McLaughlin JR, Hung RJ . Previous lung diseases and lung cancer risk: a systematic review and meta-analysis. PLoS One 2011; 6: e17479.

    Article  CAS  Google Scholar 

  8. Biesalski HK, Bueno de Mesquita B, Chesson A, Chytil F, Grimble R, Hermus RJ et al. European Consensus Statement on Lung Cancer: risk factors and prevention. Lung Cancer Panel. CA Cancer J Clin 1998; 48: 167–176; discussion 164-166.

    Article  CAS  Google Scholar 

  9. Fan YG, Jiang Y, Chang RS, Yao SX, Jin P, Wang W et al. Prior lung disease and lung cancer risk in an occupational-based cohort in Yunnan, China. Lung Cancer 2011; 72: 258–263.

    Article  Google Scholar 

  10. Wang XR, Yu IT, Chiu YL, Qiu H, Fu Z, Goggins W et al. Previous pulmonary disease and family cancer history increase the risk of lung cancer among Hong Kong women. Cancer Causes Control 2009; 20: 757–763.

    Article  Google Scholar 

  11. Turner MC, Chen Y, Krewski D, Calle EE, Thun MJ . Chronic obstructive pulmonary disease is associated with lung cancer mortality in a prospective study of never smokers. Am J Respir Crit Care Med 2007; 176: 285–290.

    Article  Google Scholar 

  12. Bae JM, Li ZM, Shin MH, Kim DH, Lee MS, Ahn YO . Pulmonary tuberculosis and lung cancer risk in current smokers: the Seoul Male Cancer Cohort Study. J Korean Med Sci 2013; 28: 896–900.

    Article  Google Scholar 

  13. Hosgoodiii HD, Chapman RS, He X, Hu W, Tian L, Liu LZ et al. History of lung disease and risk of lung cancer in a population with high household fuel combustion exposures in rural China. Lung Cancer 2013; 81: 343–346.

    Article  Google Scholar 

  14. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Arsenic and arsenic compounds. In: IARC Some Metals and Metallic Compounds, 23rd edn. IARC: Lyon, 1980.

  15. Sekeres MA . New data with arsenic trioxide in leukemias and myelodysplastic syndromes. Clin Lymph Myeloma 2007; 8 (Suppl. 1): S7–S12.

    Article  CAS  Google Scholar 

  16. Hertz-Picciotto I, Smith AH, Holtzman D, Lipsett M, Alexeeff G . Synergism between occupational arsenic exposure and smoking in the induction of lung cancer. Epidemiology 1992; 3: 23–31.

    Article  CAS  Google Scholar 

  17. Fan YG, Hu P, Jiang Y, Chang RS, Yao SX, Wang W et al. Association between sputum atypia and lung cancer risk in an occupational cohort in Yunnan, China. Chest 2009; 135: 778–785.

    Article  Google Scholar 

  18. Ratnasinghe D, Yao SX, Tangrea JA, Qiao YL, Andersen MR, Barrett MJ et al. Polymorphisms of the DNA repair gene XRCC1 and lung cancer risk. Cancer Epidemiol Biomarkers Prev 2001; 10: 119–123.

    CAS  PubMed  Google Scholar 

  19. Taylor PR, Qiao YL, Schatzkin A, Yao SX, Lubin J, Mao BL et al. Relation of arsenic exposure to lung cancer among tin miners in Yunnan Province, China. Br J Ind Med 1989; 46: 881–886.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Qiao YL, Taylor PR, Yao SX, Erozan YS, Luo XC, Barrett MJ et al. Risk factors and early detection of lung cancer in a cohort of Chinese tin miners. Ann Epidemiol 1997; 7: 533–541.

    Article  CAS  Google Scholar 

  21. Wu ZZ, Liu YT, Wei XY, Chen Z, Wang AD . Chemical etiology study among tin miners. J Hyg Res 1980; 9: 15–20.

    Google Scholar 

  22. J RK. Epidemiology: An Introduction. Oxford University Press: New York. 2002.

  23. Li R, Chambless L . Test for additive interaction in proportional hazards models. Ann Epidemiol 2007; 17: 227–236.

    Article  Google Scholar 

  24. Agency for Toxic Substances and Disease Registry (ATSDR) USPHS, U.S. Department of Health and Human Services. Toxicological Profile for Arsenic (Update). Atlanta, GA, 2007.

  25. Santillan AA, Camargo CA, Jr, Colditz GA . A meta-analysis of asthma and risk of lung cancer (United States). Cancer Causes Control 2003; 14: 327–334.

    Article  Google Scholar 

  26. Koshiol J, Rotunno M, Consonni D, Pesatori AC, De Matteis S, Goldstein AM et al. Chronic obstructive pulmonary disease and altered risk of lung cancer in a population-based case-control study. PLoS One 2009; 4: e7380.

    Article  Google Scholar 

  27. Ballaz S, Mulshine JL . The potential contributions of chronic inflammation to lung carcinogenesis. Clin Lung Cancer 2003; 5: 46–62.

    Article  CAS  Google Scholar 

  28. Azad N, Rojanasakul Y, Vallyathan V . Inflammation and lung cancer: roles of reactive oxygen/nitrogen species. J Toxicol Environ Health B Crit Rev 2008; 11: 1–15.

    Article  CAS  Google Scholar 

  29. IARC. A Review of Human Carcinogens: Arsenic, Metals, Fibres, and Dusts. Lyon, 2012.

  30. Enterline PE, Henderson VL, Marsh GM . Exposure to arsenic and respiratory cancer. A reanalysis. Am J Epidemiol 1987; 125: 929–938.

    Article  CAS  Google Scholar 

  31. Lubin JH, Moore LE, Fraumeni JF, Jr, Cantor KP . Respiratory cancer and inhaled inorganic arsenic in copper smelters workers: a linear relationship with cumulative exposure that increases with concentration. Environ Health Perspect 2008; 116: 1661–1665.

    Article  CAS  Google Scholar 

  32. Jarup L, Pershagen G . Arsenic exposure, smoking, and lung cancer in smelter workers—a case-control study. Am J Epidemiol 1991; 134: 545–551.

    Article  CAS  Google Scholar 

  33. Cocco P, Rice CH, Chen JQ, McCawley M, McLaughlin JK, Dosemeci M . Non-malignant respiratory diseases and lung cancer among Chinese workers exposed to silica. J Occup Environ Med 2000; 42: 639–644.

    Article  CAS  Google Scholar 

  34. Love RG, Muir DC . Aerosol deposition and airway obstruction. Am Rev Respir Dis 1976; 114: 891–897.

    CAS  PubMed  Google Scholar 

  35. Laube BL, Swift DL, Wagner HN, Jr . Norman PS, Adams GK, 3rd . The effect of bronchial obstruction on central airway deposition of a saline aerosol in patients with asthma. Am Rev Respir Dis 1986; 133: 740–743.

    CAS  PubMed  Google Scholar 

  36. Liu YT . In vivo distribution and metabolism of arsenide in mineral dust. J Hyg Res 1981; 9: 53–56.

    Google Scholar 

  37. Chu KH, Lee CC, Hsin SC, Cai BC, Wang JH, Chiang BL . Arsenic trioxide alleviates airway hyperresponsiveness and eosinophilia in a murine model of asthma. Cell Mol Immunol 2010; 7: 375–380.

    Article  CAS  Google Scholar 

  38. Xu ZP, Huo JM, Sang YL, Kang J, Li X . Effects of arsenic trioxide (As(2)O(3)) on airway remodeling in a murine model of bronchial asthma. Can J Physiol Pharmacol 2012; 90: 1576–1584.

    Article  CAS  Google Scholar 

  39. Li K, Gong SB, Xu Li, Xiang Xu-dong . Regulation on immunity and airway inflammation of bronchial asthma by arsenic trioxide. Chin J Asthma (Electronic Version) 2011; 2: 130–133.

    Google Scholar 

  40. Zhou LF, Zhu Y, Cui XF, Xie WP, Hu AH, Yin KS . Arsenic trioxide, a potent inhibitor of NF-kappaB, abrogates allergen-induced airway hyperresponsiveness and inflammation. Respir Res 2006; 7: 146.

    Article  Google Scholar 

  41. Yang MH, Zang YS, Huang H, Chen K, Li B, Sun GY et al. Arsenic trioxide exerts anti-lung cancer activity by inhibiting angiogenesis. Curr Cancer Drug Targets 2014; 14: 557–566.

    Article  CAS  Google Scholar 

  42. Qu GP, Xiu QY, Li B, Liu YA, Zhang LZ . Arsenic trioxide inhibits the growth of human lung cancer cell lines via cell cycle arrest and induction of apoptosis at both normoxia and hypoxia. Toxicol Ind Health 2009; 25: 505–515.

    Article  CAS  Google Scholar 

  43. Binks K, Doll R, Gillies M, Holroyd C, Jones SR, McGeoghegan D et al. Mortality experience of male workers at a UK tin smelter. Occup Med 2005; 55: 215–226.

    Article  CAS  Google Scholar 

  44. Sorahan T . Lung cancer mortality in arsenic-exposed workers from a cadmium recovery plant. Occup Med 2009; 59: 264–266.

    Article  Google Scholar 

  45. IARC Some Metals and Metallic Compounds (IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, Vol. 84). International Agency for Research on Cancer: Lyon, France. 2004.

  46. Jin Y, Liang C, He G, Cao J . [Study on distribution of endemic arsenism in China]. Wei sheng yan jiu=J Hyg Res 2003; 32: 519–540.

    Google Scholar 

  47. George CM, Smith AH, Kalman DA, Steinmaus CM . Reverse osmosis filter use and high arsenic levels in private well water. Arch Environ Occup Health 2006; 61: 171–175.

    Article  CAS  Google Scholar 

  48. Heck JE, Andrew AS, Onega T, Rigas JR, Jackson BP, Karagas MR et al. Lung cancer in a U.S. population with low to moderate arsenic exposure. Environ Health Perspect 2009; 117: 1718–1723.

    Article  CAS  Google Scholar 

  49. Smith AH, Ercumen A, Yuan Y, Steinmaus CM . Increased lung cancer risks are similar whether arsenic is ingested or inhaled. J Expo Sci Environ Epidemiol 2009; 19: 343–348.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Cancer Institute/National Institute of Health, contract no. 263-MQ-511694. We thank the staff of The Third People’s Hospital of Honghe prefecture, Gejiu city, Yunnan province, PR China for their efforts in the collection of the baseline and follow-up data of the YTC screening cohort.

Author information

Authors and Affiliations

  1. Tianjin Key Laboratory of Lung Cancer Metastasis and Tumor Microenvironment, Tianjin Lung Cancer Institute, Tianjin Medical University General Hospital, Tianjin, 300052, PR China

    Yaguang Fan, Xuebing Li & Qinghua Zhou

  2. Department of Cancer Epidemiology, National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 10021, PR China

    Yong Jiang & Youlin Qiao

  3. Divisions of Cancer Prevention, National Cancer Institute, NIH, Bethesda, Maryland, USA

    Ping Hu

  4. Third People’s Hospital of Honghe Autonomous District, Yunnan, PR China

    Runsheng Chang & Bin Wang

  5. Kunming Medical University, Yunnan, PR China

    Shuxiang Yao

  6. Lung cancer Center, West China Hospital, Sichuan University, Chengdu, PR China

    Qinghua Zhou

Authors
  1. Yaguang Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ping Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Runsheng Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuxiang Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xuebing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qinghua Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Youlin Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qinghua Zhou or Youlin Qiao.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, Y., Jiang, Y., Hu, P. et al. Modification of association between prior lung disease and lung cancer by inhaled arsenic: A prospective occupational-based cohort study in Yunnan, China. J Expo Sci Environ Epidemiol 26, 464–470 (2016). https://doi.org/10.1038/jes.2016.22

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/jes.2016.22

Keywords

This article is cited by

Search

Advanced search

Quick links