Chronic obstructive pulmonary disease and altered risk of lung cancer in a population-based case-control study

Jill Koshiol, Melissa Rotunno, Dario Consonni, Angela Cecilia Pesatori, Sara De Matteis, Alisa M Goldstein, Anil K Chaturvedi, Sholom Wacholder, Maria Teresa Landi, Jay H Lubin, Neil E Caporaso, Jill Koshiol, Melissa Rotunno, Dario Consonni, Angela Cecilia Pesatori, Sara De Matteis, Alisa M Goldstein, Anil K Chaturvedi, Sholom Wacholder, Maria Teresa Landi, Jay H Lubin, Neil E Caporaso

Abstract

Background: Chronic obstructive pulmonary disease (COPD) has been consistently associated with increased risk of lung cancer. However, previous studies have had limited ability to determine whether the association is due to smoking.

Methodology/principal findings: The Environment And Genetics in Lung cancer Etiology (EAGLE) population-based case-control study recruited 2100 cases and 2120 controls, of whom 1934 cases and 2108 controls reported about diagnosis of chronic bronchitis, emphysema, COPD (chronic bronchitis and/or emphysema), or asthma more than 1 year before enrollment. We estimated odds ratios (OR) and 95% confidence intervals (CI) using logistic regression. After adjustment for smoking, other previous lung diseases, and study design variables, lung cancer risk was elevated among individuals with a history of chronic bronchitis (OR = 2.0, 95% CI = 1.5-2.5), emphysema (OR = 1.9, 95% CI = 1.4-2.8), or COPD (OR = 2.5, 95% CI = 2.0-3.1). Among current smokers, association between chronic bronchitis and lung cancer was strongest among lighter smokers. Asthma was associated with a decreased risk of lung cancer in males (OR = 0.48, 95% CI = 0.30-0.78).

Conclusions/significance: These results suggest that the associations of personal history of chronic bronchitis, emphysema, and COPD with increased risk of lung cancer are not entirely due to smoking. Inflammatory processes may both contribute to COPD and be important for lung carcinogenesis.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

References

    1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.
    1. Thun MJ, Henley SJ, Burns D, Jemal A, Shanks TG, et al. Lung cancer death rates in lifelong nonsmokers. J Natl Cancer Inst. 2006;98:691–699.
    1. Dubey S, Powell CA. Update in lung cancer 2007. Am J Respir Crit Care Med. 2008;177:941–946.
    1. Sun S, Schiller JH, Gazdar AF. Lung cancer in never smokers–a different disease. Nat Rev Cancer. 2007;7:778–790.
    1. Amos CI, Wu X, Broderick P, Gorlov IP, Gu J, et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet. 2008;40:616–622.
    1. Hung RJ, McKay JD, Gaborieau V, Boffetta P, Hashibe M, et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature. 2008;452:633–637.
    1. Thorgeirsson TE, Geller F, Sulem P, Rafnar T, Wiste A, et al. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature. 2008;452:638–642.
    1. Mallia P, Message SD, Kebadze T, Parker HL, Kon OM, et al. An experimental model of rhinovirus induced chronic obstructive pulmonary disease exacerbations: a pilot study. Respir Res. 2006;7:116.
    1. Papi A, Bellettato CM, Braccioni F, Romagnoli M, Casolari P, et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med. 2006;173:1114–1121.
    1. Engels EA. Inflammation in the development of lung cancer: epidemiological evidence. Expert Rev Anticancer Ther. 2008;8:605–615.
    1. Schottenfeld D, Beebe-Dimmer J. Chronic inflammation: a common and important factor in the pathogenesis of neoplasia. CA Cancer J Clin. 2006;56:69–83.
    1. Holtzman MJ, Tyner JW, Kim EY, Lo MS, Patel AC, et al. Acute and chronic airway responses to viral infection: implications for asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2005;2:132–140.
    1. Cohen BH, Diamond EL, Graves CG, Kreiss P, Levy DA, et al. A common familial component in lung cancer and chronic obstructive pulmonary disease. Lancet. 1977;2:523–526.
    1. Samet JM, Humble CG, Pathak DR. Personal and family history of respiratory disease and lung cancer risk. Am Rev Respir Dis. 1986;134:466–470.
    1. Osann KE. Lung cancer in women: the importance of smoking, family history of cancer, and medical history of respiratory disease. Cancer Res. 1991;51:4893–4897.
    1. Wang SY, Hu YL, Wu YL, Li X, Chi GB, et al. A comparative study of the risk factors for lung cancer in Guangdong, China. Lung Cancer. 1996;14(Suppl 1):S99–105.
    1. Landi MT, Consonni D, Rotunno M, Bergen AW, Goldstein AM, et al. Environment And Genetics in Lung cancer Etiology (EAGLE) study: an integrative population-based case-control study of lung cancer. BMC Public Health. 2008;8:203–213.
    1. Boutin-Forzano S, Moreau D, Kalaboka S, Gay E, Bonnefoy X, et al. Reported prevalence and co-morbidity of asthma, chronic bronchitis and emphysema: a pan-European estimation. Int J Tuberc Lung Dis. 2007;11:695–702.
    1. Lugogo NL, Kraft M. Epidemiology of asthma. Clin Chest Med. 2006;27:1–15, v.
    1. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, et al. Global burden of COPD: systematic review and meta-analysis. Eur Respir J. 2006;28:523–532.
    1. Mattison S, Christensen M. The pathophysiology of emphysema: considerations for critical care nursing practice. Intensive Crit Care Nurs. 2006;22:329–337.
    1. Pelkonen M. Smoking: relationship to chronic bronchitis, chronic obstructive pulmonary disease and mortality. Curr Opin Pulm Med. 2008;14:105–109.
    1. Petty TL. The history of COPD. Int J Chron Obstruct Pulmon Dis. 2006;1:3–14.
    1. Lubin JH, Caporaso NE. Cigarette smoking and lung cancer: modeling total exposure and intensity. Cancer Epidemiol Biomarkers Prev. 2006;15:517–523.
    1. Lubin JH, Kogevinas M, Silverman D, Malats N, Garcia-Closas M, et al. Evidence for an intensity-dependent interaction of NAT2 acetylation genotype and cigarette smoking in the Spanish Bladder Cancer Study. Int J Epidemiol. 2007;36:236–241.
    1. Lubin JH, Virtamo J, Weinstein SJ, Albanes D. Cigarette smoking and cancer: intensity patterns in the alpha-tocopherol, beta-carotene cancer prevention study in Finnish men. Am J Epidemiol. 2008;167:970–975.
    1. Global Initiative for Chronic Obstructive Lung Disease. Global-strategy for the diagnosis, management and prevention of chronic obstructive pulmonary disease. 2008 Available: . Accessed 2009 Sep 11.
    1. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol. 2007;25:561–570.
    1. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci U S A. 2001;98:13784–13789.
    1. Yamamoto H, Shigematsu H, Nomura M, Lockwood WW, Sato M, et al. PIK3CA mutations and copy number gains in human lung cancers. Cancer Res. 2008;68:6913–6921.
    1. 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.
    1. Alberg AJ, Samet JM. Epidemiology of lung cancer. Chest. 2003;123:21S–49S.
    1. Gao Y, Goldstein AM, Consonni D, Pesatori AC, Wacholder S, et al. Family history of cancer and nonmalignant lung diseases as risk factors for lung cancer. Int J Cancer. 2009;125:146–152.
    1. Yang P, Sun Z, Krowka MJ, Aubry MC, Bamlet WR, et al. Alpha1-antitrypsin deficiency carriers, tobacco smoke, chronic obstructive pulmonary disease, and lung cancer risk. Arch Intern Med. 2008;168:1097–1103.
    1. Holtzman MJ, Tyner JW, Kim EY, Lo MS, Patel AC, et al. Acute and chronic airway responses to viral infection: implications for asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2005;2:132–140.
    1. Papi A, Contoli M, Caramori G, Mallia P. Models of infection and exacerbations in COPD. Curr Opin Pharmacol. 2007;7:259–265. Epub 2007 May 2001.
    1. Wu AH, Fontham ET, Reynolds P, Greenberg RS, Buffler P, et al. Previous lung disease and risk of lung cancer among lifetime nonsmoking women in the United States. Am J Epidemiol. 1995;141:1023–1032.
    1. Brownson RC, Alavanja MC. Previous lung disease and lung cancer risk among women (United States). Cancer Causes Control. 2000;11:853–858.
    1. Brenner AV, Wang Z, Kleinerman RA, Wang L, Zhang S, et al. Previous pulmonary diseases and risk of lung cancer in Gansu Province, China. Int J Epidemiol. 2001;30:118–124.
    1. Schabath MB, Delclos GL, Martynowicz MM, Greisinger AJ, Lu C, et al. Opposing effects of emphysema, hay fever, and select genetic variants on lung cancer risk. Am J Epidemiol. 2005;161:412–422.
    1. 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.
    1. Castaing M, Youngson J, Zaridze D, Szeszenia-Dabrowska N, Rudnai P, et al. Is the risk of lung cancer reduced among eczema patients? Am J Epidemiol. 2005;162:542–547.
    1. Turner MC, Chen Y, Krewski D, Ghadirian P, Thun MJ, et al. Cancer mortality among US men and women with asthma and hay fever. Am J Epidemiol. 2005;162:212–221.
    1. Vena JE, Bona JR, Byers TE, Middleton E, Jr, Swanson MK, et al. Allergy-related diseases and cancer: an inverse association. Am J Epidemiol. 1985;122:66–74.
    1. Schabath MB, Gorlova OY, Spitz MR. Re: “Cancer mortality among US men and women with asthma and hay fever”. Am J Epidemiol. 2006;163:394–395; author reply 395–396. Epub 2005 Dec 2021.
    1. Littman AJ, Jackson LA, Vaughan TL. Chlamydia pneumoniae and lung cancer: epidemiologic evidence. Cancer Epidemiol Biomarkers Prev. 2005;14:773–778.
    1. McCallister JW, Mastronarde JG. Sex differences in asthma. J Asthma. 2008;45:853–861.
    1. Barr RG, Herbstman J, Speizer FE, Camargo CA., Jr Validation of self-reported chronic obstructive pulmonary disease in a cohort study of nurses. Am J Epidemiol. 2002;155:965–971.
    1. Viegi G, Baldacci S, Vellutini M, Carrozzi L, Modena P, et al. Prevalence rates of diagnosis of asthma in general population samples of northern and central Italy. Monaldi Arch Chest Dis. 1994;49:191–196.

Source: PubMed

3
Abonneren