Background Better information on lung cancer occurrence in lifelong nonsmokers is needed to understand gender and racial disparities and to examine how factors other than active smoking influence risk in different time periods and geographic regions. Methods and Findings We pooled information on lung cancer incidence and/or death rates among self-reported never-smokers from 13 large cohort studies, representing over 630,000 and 1.8 million persons for incidence and mortality, respectively. We also abstracted population-based data for women from 22 cancer registries and ten countries in time periods and geographic regions where few women smoked. Our main findings were: (1) Men had higher death rates from lung cancer than women in all age and racial groups studied; (2) male and female incidence rates were similar when standardized across all ages 40+ y, albeit with some variation by age; (3) African Americans and Asians living in Korea and Japan (but not in the US) had higher death rates from lung cancer than individuals of European descent; (4) no temporal trends were seen when comparing incidence and death rates among US women age 40–69 y during the 1930s to contemporary populations where few women smoke, or in temporal comparisons of never-smokers in two large American Cancer Society cohorts from 1959 to 2004; and (5) lung cancer incidence rates were higher and more variable among women in East Asia than in other geographic areas with low female smoking. Conclusions These comprehensive analyses support claims that the death rate from lung cancer among never-smokers is higher in men than in women, and in African Americans and Asians residing in Asia than in individuals of European descent, but contradict assertions that risk is increasing or that women have a higher incidence rate than men. Further research is needed on the high and variable lung cancer rates among women in Pacific Rim countries.
References
[1]
World Health Organization (2002) World health report 2002. Geneva: World Health Organization.
[2]
U.S. Department of Health and Human Services, editor. (2004) The health consequences of smoking: a report of the surgeon general. Rockville (Maryland): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office On Smoking and Health. 941 p.
[3]
Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71–96.
[4]
Thun MJ, Henley SJ, Burns D, Jemal A, Shanks TG, et al. (2006) Lung cancer death rates in lifelong nonsmokers. J Natl Cancer Inst 98: 691–699.
[5]
Centers for Disease Control and Prevention (1994) Surveillance for selected tobacco-use behaviors - United States, 1900–1994. MMWR CDC Surveill Summ 43(No. SS-3): 1–43.
[6]
National Center for Health Statistics (2007) Health, United States, 2007 With Chartbook on Trends in the Health of Americans. Hyattsville (Maryland): National Center for Health Statistics.
[7]
Subramanian J, Govindan R (2007) Lung cancer in never smokers: a review. J Clin Oncol 25: 561–570.
[8]
Gazdar AF, Thun MJ (2007) Lung cancer, smoke exposure, and sex. J Clin Oncol 25: 469–471.
[9]
Henschke CI, Miettinen OS (2004) Women's susceptibility to tobacco carcinogens. Lung Cancer 43: 1–5.
[10]
Henschke CI, Yip R, Miettinen OS (2006) Women's susceptibility to tobacco carcinogens and survival after diagnosis of lung cancer. JAMA 296: 180–184.
[11]
Wakelee HA, Chang ET, Gomez SL, Keegan TH, Feskanich D, et al. (2007) Lung cancer incidence in never smokers. J Clin Oncol 25: 472–478.
[12]
Enstrom JE (1979) Rising lung cancer mortality among nonsmokers. J Natl Cancer Inst 62: 755–760.
[13]
Davis DL (1993) Trends in nonsmoking lung cancer. Epidemiology 4: 489–492.
[14]
Forastiere F, Perucci CA, Arca M, Axelson O (1993) Indirect estimates of lung cancer death rates in Italy not attributable to active smoking. Epidemiology 4: 502–510.
[15]
Parkin DM, editor. IARC (1992) Cancer incidence in five continents. Lyon: IARC.
[16]
Shafey O, Dolwick S, Guindon GE, editors. (2003) Tobacco control: country profiles. 2nd edition. Atlanta: American Cancer Society.
[17]
Griswold MH, editor. Connecticut State Department of Health (1955) Cancer in Connecticut, 1935–1951. Hartford (Connecticut): Connecticut State Department of Health.
[18]
Wingo P, Cardinez C, Landis S, Greenlee R, Ries L, et al. (2003) Long-term trends in cancer mortality in the United States, 1930–1998. Cancer 97(12 Suppl): 3133–3275.
[19]
Doll R, Peto R (1981) The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 66: 1191–1308.
[20]
Russell C, Palmer JR, Adams-Campbell LL, Rosenberg L (2001) Follow-up of a large cohort of Black women. Am J Epidemiol 154: 845–853.
[21]
Bain C, Feskanich D, Speizer FE, Thun M, Hertzmark E, et al. (2004) Lung cancer rates in men and women with comparable histories of smoking. J Natl Cancer Inst 96: 826–834.
[22]
Kolonel LN, Henderson BE, Hankin JH, Nomura AM, Wilkens LR, et al. (2000) A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol 151: 346–357.
[23]
Rexrode KM, Lee IM, Cook NR, Hennekens CH, Buring JE (2000) Baseline characteristics of participants in the Women's Health Study. J Womens Health Gend Based Med 9: 19–27.
[24]
Hirayama T (1990) Life-style and mortality. A large-scale census-based cohort study in Japan. Contributions to epidemiology and statistics. Basel: Karger.
[25]
Ando M, Wakai K, Seki N, Tamakoshi A, Suzuki K, et al. (2003) Attributable and absolute risk of lung cancer death by smoking status: findings from the Japan Collaborative Cohort Study. Int J Cancer 105: 249–254.
[26]
Marugame T, Sobue T, Satoh H, Komatsu S, Nishino Y, et al. (2005) Lung cancer death rates by smoking status: comparison of the Three-Prefecture Cohort study in Japan to the Cancer Prevention Study II in the USA. Cancer Sci 96: 120–126.
[27]
Jee SH, Sull JW, Park J, Lee SY, Ohrr H, et al. (2006) Body-mass index and mortality in Korean men and women. N Engl J Med 355: 779–787.
[28]
Calle EE, Rodriguez C, Jacobs EJ, Almon ML, Chao A, et al. (2002) The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer 94: 500–511.
[29]
Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, et al. (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 5: 1113–1124.
[30]
Boffetta P, Jarvholm B, Brennan P, Nyren O (2001) Incidence of lung cancer in a large cohort of non-smoking men from Sweden. Int J Cancer 94: 591–593.
[31]
Rothman KJ, Greenland S (1998) Modern epidemiology. Philadelphia: Lippincott Williams & Wilkins.
[32]
Ries L, Harkins D, Krapcho M, Mariotto A, Miller B, et al. (2006) SEER Cancer Statistics Review, 1975–2003. Bethesda (Maryland): National Cancer Institute.
[33]
World Health Organization (1999) WHO Mortality Database. Available: www.who.int/whosis/mort/en/. Accessed 15 January 2008.
[34]
U.S. Department of Health and Human Services (1989) Reducing the health consequences of smoking: 25 years of progress. A report of the Surgeon General. Rockville (Maryland): U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.
[35]
Shopland D, Eyre H, Pechacek T (1991) Smoking-attributable cancer mortality in 1991: is lung cancer now the leading cause of death among smokers in the United States. J Natl Cancer Inst 83: 1142–1148.
[36]
Thun M, Day-Lally C, Calle E, Flanders W, Heath C (1995) Excess mortality among cigarette smokers: changes in a 20-year interval. Am J Public Health 85: 1223–1230.
[37]
Thun M, Day-Lally C, Meyers D, Calle E, Flanders W, et al. (1997) Trends in tobacco smoking and mortality from cigarette use in Cancer Prevention Studies I (1959 through 1965) and II (1982 through 1988). In: Shopland D, Burns D, Garfinkel L, Samet J, editors. National Cancer Institute changes in cigarette-related disease risks and their implication for prevention and control smoking and tobacco control monograph number 8. Bethesda (Maryland): U.S. Department of Health and Human Services, National Institutes of Health, National Cancer Institute, National Institutes of Health publication number 97–4213. pp. 305–382.
[38]
Risch H, Howe G, Jain M, Burch J, Holowaty E, et al. (1993) Are female smokers at a higher risk for lung cancer than male smokers? A case-control analysis by histologic type. Am J Epidemiol 138: 281–293.
[39]
Osann K, Anton-Culver H, Kurosaki T, Taylor T (1993) Sex differences in lung-cancer risk associated with cigarette smoking. Int J Cancer 54: 44–48.
[40]
Zang E, Wynder E (1996) Differences in lung cancer risk between men and women: examination of the evidence. J Natl Cancer Inst 88: 183–192.
[41]
Thun M, Henley S, Calle E (2002) Tobacco use and cancer: an epidemiologic perspective for geneticists. Oncogene 21: 7307–7325.
[42]
Prescott E, Osler M, Hein H, Borch-Johnsen K, Lange P, et al. (1998) Gender and smoking-related risk of lung cancer. Epidemiology 79: 79–83.
[43]
Boffetta P, Clark S, Shen M, Gislefoss R, Peto R, et al. (2006) Serum cotinine level as predictor of lung cancer risk. Cancer Epidemiol Biomarkers Prev 15: 1184–1188.
[44]
Bach PB, Kattan MW, Thornquist MD, Kris MG, Tate RC, et al. (2003) Variations in lung cancer risk among smokers. J Natl Cancer Inst 95: 470–478.
[45]
Henschke CI, Yankelevitz DF, Libby DM, McCauley D, Pasmantier M, et al. (2001) Early lung cancer action project: annual screening using single-slice helical CT. Ann N Y Acad Sci 952: 124–134.
[46]
Li JY, Liu BQ, Li G, Rong S, Cao D, et al., editors. (1979) Atlas of cancer mortality in the Peoples' Republic of China. Shanghai: China Map Press.
[47]
Li L, Lu F, Zhang S (1996) [Analysis of cancer mortality and distribution in China, 1990–1992]. Zhonghua Zhong Liu Za Zhi 18: 403–407.
[48]
Li L, Zhang S, Lu F (1997) [Research on characteristics of mortality spectrum and type composition of malignant tumors in China]. Zhonghua Zhong Liu Za Zhi 19: 323–328.
[49]
Liu BQ, Peto R, Chen ZM, Boreham J, Wu YP, et al. (1998) Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. BMJ 317: 1411–1422.
[50]
Ministry of Health of the People's Republic of China. Available: http://www.moh.gov.cn/menunews/C30401.ht?m. Accessed 2 November 2007.
[51]
Mumford JL, He XZ, Chapman RS, Cao SR, Harris DB, et al. (1987) Lung cancer and indoor air pollution in Xuan Wei, China. Science 235: 217–220.
[52]
Wu-Williams AH, Dai XD, Blot W, Xu ZY, Sun XW, et al. (1990) Lung cancer among women in north-east China. Br J Cancer 62: 982–987.
[53]
Gao YT, Blot WJ, Zheng W, Ershow AG, Hsu CW, et al. (1987) Lung cancer among Chinese women. Int J Cancer 40: 604–609.
[54]
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: 4961–4967.
[55]
Zhong L, Goldberg MS, Gao YT, Jin F (1999) Lung cancer and indoor air pollution arising from Chinese-style cooking among nonsmoking women living in Shanghai, China. Epidemiology 10: 488–494.
[56]
Metayer C, Wang Z, Kleinerman RA, Wang L, Brenner AV, et al. (2002) Cooking oil fumes and risk of lung cancer in women in rural Gansu, China. Lung Cancer 35: 111–117.
[57]
Gu D, Wu X, Reynolds K, Duan X, Xin X, et al. (2004) Cigarette smoking and exposure to environmental tobacco smoke in China: the international collaborative study of cardiovascular disease in Asia. Am J Public Health 94: 1972–1976.
[58]
Geng G, Liang Z, Zhang A, Wu G (1988) On the relationship between smoking and female lung cancer risk. In: Aoki M, Hisamichi S, Tominaga S, editors. Smoking and health. Amsterdam: Elsevier. pp. 483–486.
[59]
Lee CH, Ko YC, Goggins W, Huang JJ, Huang MS, et al. (2000) Lifetime environmental exposure to tobacco smoke and primary lung cancer of non-smoking Taiwanese women. Int J Epidemiol 29: 224–231.
[60]
Chiu YL, Yu IT, Wong TW (2004) Time trends of female lung cancer in Hong Kong: age, period and birth cohort analysis. Int J Cancer 111: 424–430.
[61]
Seow A, Duffy S, Ng T, McGee M, Lee H (1998) Lung cancer among Chinese females in Singapore 1969–1002: time trends, dialect group differences and implications for aetiology. Int J Epidemiol 27: 167–172.
[62]
Lee C, Kang KH, Koh Y, Chang J, Chung HS, et al. (2000) Characteristics of lung cancer in Korea, 1997. Lung Cancer 30: 15–22.
[63]
Toh CK, Wong EH, Lim WT, Leong SS, Fong KW, et al. (2004) The impact of smoking status on the behavior and survival outcome of patients with advanced non-small cell lung cancer: a retrospective analysis. Chest 126: 1750–1756.
[64]
Cechner RL, Chamberlain W, Carter JR, Milojkovic-Mirceta L, Nash NP (1980) Misdiagnosis of bronchogenic carcinoma: the role of cigarette smoking, surveillance bias, and other factors. Cancer 46: 190–199.
[65]
Axelson O, Davis DL, Forestiere F, Schneiderman M, Wagener D (1990) Lung cancer not attributable to smoking. Ann N Y Acad Sci 609: 165–176.
[66]
Schneiderman MA, Davis DL, Wagener DK (1989) Lung cancer that is not attributable to smoking. JAMA 261: 2635–2636.
[67]
Bureau of the Census (1916) Mortality from cancer and other malignant tumors in the registration area of the United States. Washington (D.C.): U.S. Department of Commerce, U.S. Government Printing Office.
[68]
Wolfbane Cybernetic Ltd (2007) International classification of diseases. Available: http://www.wolfbane.com/icd/index.html. Accessed 15 December 2007.
[69]
Armstrong GL, Conn LA, Pinner RW (1999) Trends in infectious disease mortality in the United States during the 20th century. JAMA 281: 61–66.
[70]
Hoffman F (1929) Cancer of the lungs. Am Rev TBC 19: 392–406.
[71]
Hoffman F (1931) Cancer and smoking habits. Ann Surg 93: 50–67.