Seminars in Oncology
Volume 36, Issue 6 , Pages 516-523 , December 2009

Sex Differences in Susceptibility to Carcinogens

  • Kavitha Ramchandran
    • ,
  • Jyoti D. Patel

      Affiliations

    • Corresponding Author InformationAddress correspondence to Jyoti D. Patel, MD, Division of Hematology/Oncology, Feinberg School of Medicine, Northwestern University, 676 N St Clair St, Chicago, IL 60611

References 

  1. In:  Horner MJ,  Ries LAG,  Krapcho M,  Neyman N,  Aminou R,  Howlader N, et al. editor. SEER cancer statistics review, 1975-2006. Bethesda, MD: National Cancer Institute; 2009;http://seer.cancer.gov/csr/1975_2006/, based on November 2008 SEER data submission; posted to the SEER web site
  2. Gan WQ, Man SF, Postma DS, Camp P, Sin DD. Female smokers beyond the perimenopausal period are at increased risk of chronic obstructive pulmonary disease: a systematic review and meta-analysis. Respir Res. 2006;7:52–60
  3. Ferguson MK, Skosey C, Hoffman PC, Golomb HM. Sex-associated differences in presentation and survival in patients with lung cancer. J Clin Oncol. 1990;8:1402–1407
  4. Radzikowska E, Glaz P, Roszkowski K. Lung cancer in women: Age, smoking, histology, performance status, stage, initial treatment and survival—population-based study of 20,561 cases. Ann Oncol. 2002;13:1087–1093
  5. 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
  6. Ferguson MK, Skosey C, Hoffman PC, Golomb HM. Sex-associated differences in presentation and survival in patients with lung cancer. J Clin Oncol. 1990;8:1402–1407
  7. Ramaswamy G, Page N, Morgensztern D, Read W, Tierney R, Vlahiotis A, et al. Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the Surveillance, Epidemiologic, and End Results Database. J Clin Oncol. 2006;24:4539–4544
  8. Edmonson JH, Lagakos SW, Selawry OS. Cyclosphosphamide and CCNU in the treatment of inoperable small cell carcinoma and adenocarcinoma of the lung. Cancer Treat Rep. 1976;60:925–932
  9. Ramalingam S, Pawlish K, Gadgeel S. Lung cancer in young patients: analysis of a Surveillance, Epidemiology, and End Results Database. Am J Clin Oncol. 1998;16:651–657
  10. Mitsudomi T, Tateishi M, Oka T, Yano T, Ishida T, Sugimachi K. Longer survival after resection of non-small cell lung cancer in Japanese women. Ann Thorac Surg. 1989;48:639–642
  11. Radzikowska E, Glaz P, Roszkowski K. Lung cancer in women: age, smoking, histology, performance status, stage, initial treatment and survival—population-based study of 20,561 cases. Ann Oncol. 2002;13:1087–1093
  12. 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
  13. Moore KA, Mery CM, Jaklitsch MT, Estocin AP, Bueno R, Swanson SJ, et al. Menopausal effects on presentation, treatment, and survival of women with non-small cell lung cancer. Ann Thorac Surg. 2003;76:1789–1795
  14. Moore R, Doherty D, Chamberlain R, Khuri F. Sex differences in survival in non-small cell lung cancer patients 1974-1998. Acta Oncol. 2004;43:57–64
  15. Risch HA, Howe GR, Jain M, Burch JD, Holowaty EJ, Miller AB. Are female smokers at higher risk for lung cancer than male smokers? (A case-control analysis by histologic type). Am J Epidemiol. 1993;138:281–293
  16. Zang EA, Wynder EL. Differences in lung cancer risk between men and women: examination of the evidence. J Natl Cancer Inst. 1996;88:183–192
  17. Henschke CI, Miettinen O. Women's susceptibility to tobacco carcinogens. Lung Cancer. 2004;43:1–5
  18. Bach PB, Kattan MW, Thornquist MD, Kris MG, Tate RC, Barnett MJ, et al. Variations in lung cancer risk among smokers. J Natl Cancer Inst. 2003;95:470–478
  19. 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
  20. 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
  21. Dunnill MS. The problem of lung growth. Thorax. 1982;37:561–564
  22. Merkus PJFM, ten Have-Opbroek AAW, Quanjer PH. Human lung growth: a review. Pediatr Pulmonol. 1992;21:383–397
  23. Tager IB, Segal MR, Speizer FE, Weiss ST. The natural history of forced expiratory volumes (The effect of cigarette smoking and respiratory symptoms). Am Rev Resp Dis. 1988;138:837–849
  24. Kanner RE, Connett JE, Altose MD, Buist AS, Lee WW, Tashkin DP, et al. Gender difference in airway hyperresponsiveness in smokers with mild COPD (The Lung Health Study). Am J Respir Crit Care Med. 1994;150:956–961
  25. Bakke PS, Baste V, Gulsvik A. Bronchial responsiveness in a Norwegian community. Am Rev Respir Dis. 1991;143:317–322
  26. Kanner RE, Connett JE, Altose MD, Buist AS, Lee WW, Tashkin DP, et al. Gender difference in airway hyperresponsiveness in smokers with mild COPD: the Lung Health Study. Am J Respir Crit Care Med. 1994;150:956–961
  27. Gold DR, Wang X, Wypig D, Spiezer FE, Ware JH, Dockery DW. Effects of cigarette smoking on lung function in adolescent boys and girls. N Engl J Med. 1996;335:931–937
  28. Prescott E, Bjerg AM, Andersen PK, Lange P, Vestbo J. Gender difference in smoking effects on lung function and risk of hospitalization for COPD: results from a Danish longitudinal population study. Eur Respir J. 1997;10:822–827
  29. Gan WQ, Man SF, Postma DS, Camp P, Sin DD. Female smokers beyond the perimenopausal period are at increased risk of chronic obstructive pulmonary disease: a systematic review and meta-analysis. Respir Res. 2006;29:52–607
  30. Centers for Disease Control and Prevention. Trends in cigarette smoking among high school students–United States, 1991-2001. Morb Mortal Wkly Rep. 2002;51:409–412
  31. Johnston L, Bachman J, O'Malley PM. Monitoring the future: questionnaire responses from the nation's high school seniors 1997. Ann Arbor, MI: Institute for Social Research, University of Michigan; 2001;
  32. Wiencke JK, Thurston SW, Kelsey KT, Varkonyi A, Wain JC, Mark EJ, et al. Early age of smoking initiation and tobacco carcinogen DNA damage in the lung. J Natl Cancer Inst. 1999;91:614–619
  33. Pierce L, Lee L, Gilpin EA. Smoking initiation by adolescent girls, 1944- 1988 (An association with targeted advertising). JAMA. 1994;271:608–611
  34. Hegmann KT, Fraser AM, Keaney RP, Moser SE, Nilasena DS, Sedlars M, et al. The age of smoking initiation on lung cancer risk. Epidemiology. 1993;4:444–448
  35. Busse WW, Lemanske RF. Asthma. N Engl J Med. 2001;344:350–362
  36. Chen Y, Stewart P, Johansen H, McRae L, Taylor G. Sex difference in hospitalization due to asthma in relation to age. J Clin Epidemiol. 2003;56:180–187
  37. Schatz M, Clark S, Camargo CA. Sex differences in the presentation and course of asthma hospitalizations. Chest. 2006;129:50–55
  38. Tantisira KG, Colvin R, Tonascia J, Strunk RC, Weiss ST, Fuhlbrigge AL. Airway responsiveness in mild to moderate childhood asthma: sex influences on the natural history. Am J Respir Crit Care Med. 2008;178:325–331
  39. Troisi RJ, Speizer FE, Willett WC, Trichopoulos D, Rosner B. Menopause, postmenopausal estrogen preparations and the risk of adult-onset asthma: a prospective cohort study. Am J Respir Crit Care Med. 1995;152:1183–1188
  40. Barr RD, Wentowski CC, Grodstein F, Somers SC, Stampfler JM, Schwartz J, et al. Prospective study of postmenopausal hormone use and newly diagnosed asthma and chronic obstructive pulmonary disease. Arch Intern Med. 2004;164:379–386
  41. Tan KS, McFarlane LC, Lipworth BJ. Modulation of airway reactivity and peak flow variability in asthmatics receiving the oral contraceptive pill. Am J Respir Crit Care Med. 1997;155:1273–1277
  42. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: executive summary 2006 (Global Initiative for Chronic Obstructive Lung Disease (GOLD)). http://www.goldcopd.orgAccessed March 16, 2009
  43. Stockely RA. Neutrophils and protease/antiprotease imbalance. Am J Respir Crit Care Med. 1999;160:S49–S52
  44. Mannino D, Homa D, Akinbami L, Ford E, Redd S. Chronic obstructive pulmonary disease surveillance: United States, 1971–2000. MMWR Surveill Summ. 2002;51:1–16
  45. Carrasco Garrido P, de Miguel Diez J, Rejas Gutierrez J. Characteristics of chronic obstructive pulmonary disease in Spain from a gender perspective. BMC Pulm Med. 2009;9:2
  46. Carter R, Nicotra B, Huber G. Differing effects of airway obstruction on physical work capacity and ventilation in men and women with COPD. Chest. 1994;106:1730–1739
  47. Wasswa-Kintu S, Gan WQ, Man SF, Pare PD, Sin DD. Relationship between reduced forced expiratory volume in one second and the risk of lung cancer: a systematic review and meta-analysis. Thorax. 2005;60:570–575
  48. Chapman KR, Tashkin DP, Pye DJ. Gender bias in the diagnosis of COPD. Chest. 2001;119:1691–1695
  49. McLemore TL, Adelber S, Liu MC, McMahon NA, Yu SJ, Hubbard WC, et al. Expression of CYP1A1 gene in patients with lung cancer: evidence for cigarrette smoke-induced gene expression in normal lung tissue and for altered gene regulation in primary pulmonary carcinomas. J Natl Cancer Inst. 1990;82:1333–1339
  50. Rossini A, de Almeida Simão T, Albano RM, Pinto LF. CYP2A6 polymorphisms and risk for tobacco-related cancers. Pharmacogenomics. 2008;9:1737–1752
  51. Mollerup S, Ryberg D, Hewer A, Phillips DH, Haugen A. Sex differences in lung CYP1A1 expression and DNA adduct levels among lung cancer patients. Cancer Res. 1999;59:3317–3320
  52. Han W, Pentecost BT, Pietropaolo RL, Fasco MJ, Spivack SD. Estrogen receptor alpha increases basal and cigarette smoke extract-induced expression of CYP1A1 and CYP1B1, but not GSTP1, in normal human bronchial epithelial cells. Mol Carcinog. 2005;44:202–211
  53. Hayes CL, Spink DC, Spink BC, Cao JQ, Walker NJ, Sutter TR. 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc Natl Acad Sci U S A. 1996;93:9776–9781
  54. Spink DC, Katz BH, Hussain MM, Pentecost BT, Cao Z, Spink BC. Estrogen regulates Ah responsiveness in MCF-7 breast cancer cells. Carcinogenesis. 2003;12:1941–1950
  55. Han W, Pentecost BT, Pietropaolo RL, Fasco MJ, Spivack SD. Estrogen receptor alpha increases basal and cigarette smoke extract-induced expression of CYP1A1 and CYP1B1, but not GSTP1, in normal human bronchial epithelial cells. Mol Carcinog. 2005;44:202–211
  56. Chichester CH, Buckpitt AR, Chang A, Plopper CG. Metabolism and cytotoxicity of naphthalene and its metabolites in isolated murine Clara cells. Mol Pharmacol. 1994;45:664–672
  57. Forkert PG, Dowsley TF, Lee RP, Hong JY, Ulreich JB. Differential formation of 1,1-dichloroethylene-metabolites in the lungs of adult and weanling male and female mice: correlation with severities of bronchiolar cytotoxicity. J Pharmacol Exp Ther. 1996;279:1484–1490
  58. Seymour BW, Friebertshauser KE, Peake JL, Pinkerton KE, Coffman RL, et al. Gender differences in the allergic response of mice neonatally exposed to environmental tobacco smoke. Dev Immunol. 2002;9:47–54
  59. Al Koudsi N, Mwenifumbo JC, Sellers EM, Benowitz NL, Swan GE, et al. Characterization of the novel CYP2A6*21 allele using in vivo nicotine kinetics. Eur J Clin Pharmacol. 2006;62:481–484
  60. Mollerup S, Ryberg D, Hewer A, Phillips DH, Haugen A. Sex differences in lung CYP1A1 expression and DNA adduct levels among lung cancer patients. Cancer Res. 1999;59:3317–3320
  61. Daniel V. Glutathione S-transferases: gene structure and regulation of expression. Crit Rev Biochem Mol Biol. 1993;28:173–207
  62. Bell D, Taylor J, Paulson D, Robertson CN, Mohler JL, Lucier GW. Genetic risk and carcinogen exposure: a common inherited defect of the carcinogen-metabolism gene glutathione S-transferase M1 (GSTM1) that increases susceptibility to bladder cancer. J Natl Cancer Inst. 1993;85:1159–1164
  63. McWilliams JE, Sanderson BJ, Harris EL, Richert-Boe KE, Henner WD. Glutathione S-transferase M1 (GSTM1) deficiency and lung cancer risk. Cancer Epidemiol Biomarkers Prev. 1995;4:589–594
  64. Tang D, Rundle A, Warburton D, Santella RM, Tsai WY, Chiamprasert S, et al. Associations between both genetic and environmentals biomarkers and lung cancer: evidence of a greater risk of lung cancer in women in smokers. Carcinogenesis. 1998;19:1949–1953
  65. Zhang G, Liu X, Farkas AM, Parwani AV, Lathrop KL, Lenzner D, et al. Estrogen receptor beta functions through non-genomic mechanisms in lung cancer cells. Mol Endocrinol. 2009;23:146–156
  66. Nose N, Sugio K, Oyama T. Association between estrogen receptor-β expression and epidermal growth factor receptor mutation in the postoperative prognosis of adenocarcinoma of the lung. J Clin Oncol. 2009;27:411–417
  67. Kawai H, Ishii A, Washiya K, Konno T, Kon H, Yamaya C, et al. Estrogen receptor alpha and beta are prognostic factors in non-small cell lung cancer. Clin Cancer Res. 2005;11:5084–5089
  68. Márquez-Garbán DC, Chen HW, Fishbein MC, Goodglick L, Pietras RJ. Estrogen receptor signaling pathways in human non-small cell lung cancer. Steroids. 2007;72:135–143
  69. 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
  70. 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
  71. Ganti A, Sahmoun AE, Panwalker AW. Hormone replacement therapy is associated with decreased survival in women with lung cancer. J Clin Oncol. 2006;24:59–63
  72. Adami HO, Persson I, Hoover R, Schairer C, Bergkvist L. Risk of cancer in women receiving hormone replacement therapy. Int J Cancer. 1989;44:833–839
  73. Taioli E, Wynder EL. Endocrine factors and adenocarcinoma of the lung in women. J Natl Cancer Inst. 1994;86:869–870
  74. Wei Q, Cheng L, Amos CI, Wang LE, Guo Z, Hong WK, et al. Repair of tobacco carcinogen-induced DNA adducts and lung cancer risk: a molecular epidemiologic study. J Natl Cancer Inst. 2000;92:1764–1772
  75. Travis WD, Travis LB, Devesa SS. Lung cancer. Cancer. 1995;75:S191–S202
  76. Ikeda T, Kurita Y, Inutsuka S, Tanaka K, Nakanishi Y, Shigematsu N, et al. The changing pattern of lung cancer by histological type—a review of 1151 cases from a university hospital in Japan, 1970–1989. Lung Cancer. 1991;7:157–164
  77. Janssen-Heijnen ML, Nab HW, van Reek J, van der Heijden LH, Schipper R, Coebergh JW. Striking changes in smoking behaviour and lung cancer incidence by histological type in south-east Netherlands, 1960–1991. Eur J Cancer. 1995;31A:949–952
  78. Wynder EL, Muscat JE. Environmental health issues. Environ Health Perspect Suppl. 1995;103:
  79. Djordjevic MV, Hoffmann D, Hoffmann I. Nicotine regulates smoking patterns. Prev Med. 1997;26:435–440
  80. Fischer S, Spiegelhalder B, Preussmann R. Influence of smoking parameters on the delivery of tobacco-specific nitrosamines in cigarette smoke—a contribution to relative risk evaluation. Carcinogenesis. 1989;10:1059–1066
  81. Thun MJ, Lally CA, Flannery JT, Calle EE, Dana Flanders W, Health CW. Cigarette smoking and changes in the his-topathology of lung cancer. J Natl Cancer Inst. 1997;89:1580–1586
  82. Le Marchand L, Sivaraman L, Pierce L, Seifried A, Lum A, Wilkens LR, et al. Associations of CYP1A1, GSTM1, and CYP2E1 polymorphisms with lung cancer suggest cell type specificities to tobacco carcinogens. Cancer Res. 1998;58:4858–4863

PII: S0093-7754(09)00167-5

doi: 10.1053/j.seminoncol.2009.09.005

Seminars in Oncology
Volume 36, Issue 6 , Pages 516-523 , December 2009

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