Seminars in Oncology
Volume 36, Issue 6 , Pages 506-515 , December 2009

Population-Based Trends in Lung Cancer Incidence in Women

  • Brian L. Egleston

      Affiliations

    • Biostatistics and Bioinformatics Facility, Fox Chase Cancer Center, Philadelphia, PA
  • ,
  • Sibele I. Meireles

      Affiliations

    • Cancer Prevention and Control Program, Fox Chase Cancer Center, Philadelphia, PA
  • ,
  • Douglas B. Flieder

      Affiliations

    • Department of Pathology, Fox Chase Cancer Center, Philadelphia, PA
  • ,
  • Margie L. Clapper

      Affiliations

    • Cancer Prevention and Control Program, Fox Chase Cancer Center, Philadelphia, PA
    • Corresponding Author InformationAddress correspondence to Margie L. Clapper, PhD, Fox Chase Cancer Center, 333 Cottman Ave, Philadelphia, PA 19111

References 

  1. US Department of Health and Human Services. Women and smoking: a report of the surgeon general. Washington, DC: Public Health Service, Office of the Surgeon General; 2001;
  2. American Cancer Society. Cancer facts and figures. Atlanta, GA: American Cancer Society; 2008;
  3. Adebonojo SA, Bowser AN, Moritz DM, Corcoran PC. Impact of revised stage classification of lung cancer on survival: a military experience. Chest. 1999;115:1507–1513
  4. Minami H, Yoshimura M, Miyamoto Y, Matsuoka H, Tsubota N. Lung cancer in women: sex-associated differences in survival of patients undergoing resection for lung cancer. Chest. 2000;118:1603–1609
  5. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database. Incidence—SEER 9 Regs Limited-Use, Nov 2007 Sub (1973-2005) <Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969-2005 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2008, based on the November 2007 submission.
  6. Surveillance Research Program. National Cancer Institute SEER*Stat software. wwwseercancergov/seerstatversion 6.4.4.
  7. International Agency for Research on Cancer. GLOBOCAN 2002. Lyon, France: International Agency for Research on Cancer; 2002;
  8. Alberg AJ, Ford JG, Samet JM. Epidemiology of lung cancer: ACCP evidence-based clinical practice guidelines. (2nd edition) Chest. 2007;132:29S–55S
  9. Bosetti C, Bertuccio P, Levi F, Lucchini F, Negri E, La Vecchia C. Cancer mortality in the European Union, 1970-2003, with a joinpoint analysis. Ann Oncol. 2008;19:631–640
  10. Levi F, Bosetti C, Fernandez E, Hill C, Lucchini F, Negri E, et al. Trends in lung cancer among young European women: the rising epidemic in France and Spain. Int J Cancer. 2007;121:462–465
  11. Toh C-K. The changing epidemiology of lung cancer. Methods Mol Biol. 2009;472:397–411
  12. Sun S, Schiller JH, Gazdar AF. Lung cancer in never smokers—a different disease. Nat Rev Cancer. 2007;7:778–790
  13. Bain C, Feskanich D, Speizer FE, Thun M, Hertzmark E, Rosner BA, et al. Lung cancer rates in men and women with comparable histories of smoking. J Natl Cancer Inst. 2004;96:826–834
  14. Ernster VL. Female lung cancer. Annu Rev Public Health. 1996;17:97–114
  15. Thun MJ, Heath CW. Changes in mortality from smoking in two American Cancer Society prospective studies since 1959. Prev Med. 1997;26:422–426
  16. Morabia A, Costanza MC, Bernstein MS, Rielle JC. Ages at initiation of cigarette smoking and quit attempts among women: a generation effect. Am J Public Health. 2002;92:71–74
  17. Davy M. Time and generational trends in smoking among men and women in Great Britain, 1972-2004/05. Health Stat Q. 2006;32:35–43
  18. Sarna L, Bialous SA, Jun HJ, Wewers ME, Cooley ME, Feskanich D. Smoking trends in the Nurses' Health Study (1976-2003). Nurs Res. 2008;57:374–382
  19. Doll R, Gray R, Hafner B, Peto R. Mortality in relation to smoking: 22 years' observations on female British doctors. Br Med J. 1980;280:967–971
  20. Stellman SD, Garfinkel L. Smoking habits and tar levels in a new American Cancer Society prospective study of 1.2 million men and women. J Natl Cancer Inst. 1986;76:1057–1063
  21. Hoffmann D, Hoffmann I. The changing cigarette, 1950-1995. J Toxicol Environ Health. 1997;50:307–364
  22. Dresler C, Fratelli C, Babb J, Everley LC, Evans AA, Clapper ML. Gender differences in genetic susceptibility to lung cancer. Lung Cancer. 2000;30:153–160
  23. McDuffie HH, Klaassen DJ, Dosman JA. Female-male differences in patients with primary lung cancer. Cancer. 1987;59:1825–1830
  24. International Early Lung Cancer Action Program Investigators. Women's susceptibility to tobacco carcinogens and survival after diagnosis of lung cancer. JAMA. 2006;296:180–184
  25. Belani CP, Marts S, Schiller J, Socinski MA. Women and lung cancer: epidemiology, tumor biology, and emerging trends in clinical research. Lung Cancer. 2007;55:15–23
  26. Khuder SA. Effect of cigarette smoking on major histological types of lung cancer: a meta-analysis. Lung Cancer. 2001;31:139–148
  27. Freedman ND, Leitzmann MF, Hollenbeck AR, Schatzkin A, Abnet CC. Cigarette smoking and subsequent risk of lung cancer in men and women: analysis of a prospective cohort study. Lancet Oncol. 2008;9:649–656
  28. Sridhar KS, Thurer RJ, Markoe AM, Chatoor HT, Fountzilas G, Raub WJ, et al. Multidisciplinary approach to the treatment of locally and regionally advanced non-small cell lung cancer: University of Miami experience. Semin Surg Oncol. 1993;9:114–119
  29. Zell JA, Ou SH, Ziogas A, Anton-Culver H. Epidemiology of bronchioloalveolar carcinoma: improvement in survival after release of the 1999 WHO classification of lung tumors. J Clin Oncol. 2005;23:8396–8405
  30. Thun MJ, Hannan LM, Adams-Campbell LL, Boffetta P, Buring JE, Feskanich D, et al. Lung cancer occurrence in never-smokers: an analysis of 13 cohorts and 22 cancer registry studies. PLoS Med. 2008;5:e185
  31. Wakelee HA, Chang ET, Gomez SL, Keegan TH, Feskanich D, Clarke CA, et al. Lung cancer incidence in never smokers. J Clin Oncol. 2007;25:472–478
  32. Boffetta P, Jarvholm B, Brennan P, Nyren O. Incidence of lung cancer in a large cohort of non-smoking men from Sweden. Int J Cancer. 2001;94:591–593
  33. Enstrom JE. Rising lung cancer mortality among nonsmokers. J Natl Cancer Inst. 1979;62:755–760
  34. Thun MJ, Henley SJ, Burns D, Jemal A, Shanks TG, Calle EE. Lung cancer death rates in lifelong nonsmokers. J Natl Cancer Inst. 2006;98:691–699
  35. Stellman SD, Muscat JE, Thompson S, Hoffmann D, Wynder EL. Risk of squamous cell carcinoma and adenocarcinoma of the lung in relation to lifetime filter cigarette smoking. Cancer. 1997;80:382–388
  36. Thun MJ, Lally CA, Flannery JT, Calle EE, Flanders WD, Heath CW. Cigarette smoking and changes in the histopathology of lung cancer. J Natl Cancer Inst. 1997;89:1580–1586
  37. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350:2129–2139
  38. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304:1497–1500
  39. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol. 2007;25:561–570
  40. Weiss JM, Lacey JV, Shu XO, Ji BT, Hou L, Yang G, et al. Menstrual and reproductive factors in association with lung cancer in female lifetime nonsmokers. Am J Epidemiol. 2008;168:1319–1325
  41. Liu Y, Inoue M, Sobue T, Tsugane S. Reproductive factors, hormone use and the risk of lung cancer among middle-aged never-smoking Japanese women: a large-scale population-based cohort study. Int J Cancer. 2005;117:662–666
  42. Kabat GC, Miller AB, Rohan TE. Reproductive and hormonal factors and risk of lung cancer in women: a prospective cohort study. Int J Cancer. 2007;120:2214–2220
  43. Wysowski DK, Golden L, Burke L. Use of menopausal estrogens and medroxyprogesterone in the United States, 1982-1992. Obstet Gynecol. 1995;85:6–10
  44. Kennedy DL, Baum C, Forbes MB. Noncontraceptive estrogens and progestins: use patterns over time. Obstet Gynecol. 1985;65:441–446
  45. Hemminki E, Kennedy DL, Baum C, McKinlay SM. Prescribing of noncontraceptive estrogens and progestins in the United States, 1974-86. Am J Public Health. 1988;78:1479–1481
  46. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA. 2002;288:321–333
  47. Beral V, Hermon C, Kay C, Hannaford P, Darby S, Reeves G. Mortality associated with oral contraceptive use: 25 year follow up of cohort of 46 000 women from Royal College of General Practitioners' oral contraception study. BMJ. 1999;318:96–100
  48. Vessey M, Painter R, Yeates D. Mortality in relation to oral contraceptive use and cigarette smoking. Lancet. 2003;362:185–191
  49. Taioli E, Wynder EL. Endocrine factors and adenocarcinoma of the lung in women. [letter] J Natl Cancer Inst. 1994;86:869–870
  50. Ganti AK, Sahmoun AE, Panwalkar AW, Tendulkar KK, Potti A. Hormone replacement therapy is associated with decreased survival in women with lung cancer. J Clin Oncol. 2006;24:59–63
  51. Kreuzer M, Gerken M, Heinrich J, Kreienbrock L, Wichmann HE. Hormonal factors and risk of lung cancer among women?. Int J Epidemiol. 2003;32:263–271
  52. Schabath MB, Wu X, Vassilopoulou-Sellin R, Vaporciyan AA, Spitz MR. Hormone replacement therapy and lung cancer risk: a case-control analysis. Clin Cancer Res. 2004;10:113–123
  53. Syrjanen KJ. Condylomatous changes in neoplastic bronchial epithelium (Report of a case). Respiration. 1979;38:299–304
  54. Giuliani L, Favalli C, Syrjanen K, Ciotti M. Human papillomavirus infections in lung cancer (Detection of E6 and E7 transcripts and review of the literature). Anticancer Res. 2007;27:2697–2704
  55. Bohlmeyer T, Le TN, Shroyer AL, Markham N, Shroyer KR. Detection of human papillomavirus in squamous cell carcinomas of the lung by polymerase chain reaction. Am J Respir Cell Mol Biol. 1998;18:265–269
  56. Brouchet L, Valmary S, Dahan M, Didier A, Galateau-Salle F, Brousset P, et al. Detection of oncogenic virus genomes and gene products in lung carcinoma. Br J Cancer. 2005;92:743–746
  57. Clavel CE, Nawrocki B, Bosseaux B, Poitevin G, Putaud IC, Mangeonjean CC, et al. Detection of human papillomavirus DNA in bronchopulmonary carcinomas by hybrid capture II: a study of 185 tumors. Cancer. 2000;88:1347–1352
  58. Cook JR, Hill DA, Humphrey PA, Pfeifer JD, El-Mofty SK. Squamous cell carcinoma arising in recurrent respiratory papillomatosis with pulmonary involvement: emerging common pattern of clinical features and human papillomavirus serotype association. Mod Pathol. 2000;13:914–918
  59. Guillou L, Sahli R, Chaubert P, Monnier P, Cuttat JF, Costa J. Squamous cell carcinoma of the lung in a nonsmoking, nonirradiated patient with juvenile laryngotracheal papillomatosis (Evidence of human papillomavirus-11 DNA in both carcinoma and papillomas). Am J Surg Pathol. 1991;15:891–898
  60. Jain N, Singh V, Hedau S, Kumar S, Daga MK, Dewan R, et al. Infection of human papillomavirus type 18 and p53 codon 72 polymorphism in lung cancer patients from India. Chest. 2005;128:3999–4007
  61. Lele SM, Pou AM, Ventura K, Gatalica Z, Payne D. Molecular events in the progression of recurrent respiratory papillomatosis to carcinoma. Arch Pathol Lab Med. 2002;126:1184–1188
  62. Welt A, Hummel M, Niedobitek G, Stein H. Human papillomavirus infection is not associated with bronchial carcinoma: evaluation by in situ hybridization and the polymerase chain reaction. J Pathol. 1997;181:276–280
  63. Yousem SA, Ohori NP, Sonmez-Alpan E. Occurrence of human papillomavirus DNA in primary lung neoplasms. Cancer. 1992;69:693–697
  64. Klein F, Kotb WF, Petersen I. Incidence of human papilloma virus in lung cancer. Lung Cancer Epub 2008 101016/jlungcan200810003. Available from wwwelseviercom/locate/lungcan.
  65. Syrjanen KJ. HPV infections and lung cancer. J Clin Pathol. 2002;55:885–891
  66. Gorgoulis VG, Zacharatos P, Kotsinas A, Kyroudi A, Rassidakis AN, Ikonomopoulos JA, et al. Human papilloma virus (HPV) is possibly involved in laryngeal but not in lung carcinogenesis. Hum Pathol. 1999;30:274–283
  67. Hirayasu T, Iwamasa T, Kamada Y, Koyanagi Y, Usuda H, Genka K. Human papillomavirus DNA in squamous cell carcinoma of the lung. J Clin Pathol. 1996;49:810–817
  68. Miyagi J, Tsuhako K, Kinjo T, Iwamasa T, Hirayasu T. Recent striking changes in histological differentiation and rate of human papillomavirus infection in squamous cell carcinoma of the lung in Okinawa, a subtropical island in southern Japan. J Clin Pathol. 2000;53:676–684
  69. Papadopoulou K, Labropoulou V, Davaris P, Mavromara P, Tsimara-Papastamatiou H. Detection of human papillomaviruses in squamous cell carcinomas of the lung. Virchows Arch. 1998;433:49–54
  70. Tsuhako K, Nakazato I, Hirayasu T, Sunakawa H, Iwamasa T. Human papillomavirus DNA in adenosquamous carcinoma of the lung. J Clin Pathol. 1998;51:741–749
  71. International Agency for Research on Cancer. IARC monographs on the evaluation of the carcinogenic risks to humans (Vol. 90 Human papillomaviruses). Lyon, France: IARC; 2007;
  72. Hsu NY, Cheng YW, Chan IP, Ho HC, Chen CY, Hsu CP, et al. Association between expression of human papillomavirus 16/18 E6 oncoprotein and survival in patients with stage I non-small cell lung cancer. Oncol Rep. 2009;21:81–87
  73. Sasco AJ, Secretan MB, Straif K. Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer. 2004;45(Suppl 2):S3–S9
  74. Czene K, Tiikkaja S, Hemminki K. Cancer risks in hairdressers: assessment of carcinogenicity of hair dyes and gels. Int J Cancer. 2003;105:108–112
  75. Sjodahl K, Jansson C, Bergdahl IA, Adami J, Boffetta P, Lagergren J. Airborne exposures and risk of gastric cancer: a prospective cohort study. Int J Cancer. 2007;120:2013–2018
  76. Pascual D, Borque A. Epidemiology of kidney cancer. Adv Urol Epub. 2008 November 4;10.1155/2008/782381. Available from www.hindawi.com.
  77. Laukkanen P, Koskela P, Pukkala E, Dillner J, Laara E, Knekt P, et al. Time trends in incidence and prevalence of human papillomavirus type 6, 11 and 16 infections in Finland. J Gen Virol. 2003;84:2105–2109
  78. US Department of Health and Human Services. Reducing the health consequences of smoking: 25 years of progress (A report of the Surgeon General). DHHS publication no. (CDC) 89-8411 Washington, DC: US 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; 1989;
  79. Raymond JS, Hogue CJ. Multiple primary tumours in women following breast cancer, 1973-2000. Br J Cancer. 2006;94:1745–1750
  80. Matesich SM, Shapiro CL. Second cancers after breast cancer treatment. Semin Oncol. 2003;30:740–748
  81. Roychoudhuri R, Evans H, Robinson D, Moller H. Radiation-induced malignancies following radiotherapy for breast cancer. Br J Cancer. 2004;91:868–872
  82. Bergfeldt K, Silfversward C, Einhorn S, Hall P. Overestimated risk of second primary malignancies in ovarian cancer patients. Eur J Cancer. 2000;36:100–105
  83. Hulley S, Furberg C, Barrett-Connor E, Cauley J, Grady D, Haskell W, et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA. 2002;288:58–66
  84. Beral V, Banks E, Reeves G. Evidence from randomised trials on the long-term effects of hormone replacement therapy. Lancet. 2002;360:942–944

 This work was supported by USPHS Grant No. CA-06927 from the National Cancer Institute, the Kitty Jackson Fund, the Estate of Jane Villon, the Jerome M. Spencer and Arnold Zaslow Family Foundation, the Fox Chase Cancer Center Keystone Program in Personalized Risk and Prevention, and by an appropriation from the Commonwealth of Pennsylvania. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute.

PII: S0093-7754(09)00165-1

doi: 10.1053/j.seminoncol.2009.09.003

Seminars in Oncology
Volume 36, Issue 6 , Pages 506-515 , December 2009