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The effect of secondhand smoke exposure on the association between active cigarette smoking and colorectal cancer

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Abstract

Background

Studies published prior to 1980 failed to find an association between smoking and colorectal cancer, while subsequent studies reported an association after accounting for a three to four decade initiation period. The aims of this study were to determine the effect of accounting for secondhand smoke (SHS) exposure on the association between smoking and colorectal cancer and to determine the association between SHS and colorectal cancer.

Methods

Approximately 1,200 colorectal cancer cases treated at Roswell Park Cancer Institute between 1982 and 1998 were matched to 2,400 malignancy-free controls. The effect of accounting for SHS exposure was determined by comparing the odds ratios (OR) for each smoking variable in the overall sample and then for those who reported no current SHS exposure.

Results

A small, significant increase in colorectal cancer odds was noted for heavy, long-term smoking males when not accounting for SHS exposure (>45 PY: OR = 1.34; 95% CI 1.04–1.72). OR increased when the analyses were restricted to individuals reporting no current SHS exposure (>45 PY: OR = 2.40; 95% CI 1.36–4.23).

Conclusions

Accounting for SHS exposure resulted in a substantial increase in the odds of colorectal cancer for all smoking variables in this study. Future studies should account for SHS exposure when examining the association between smoking and colorectal cancer.

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References

  1. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, World Health Organization, International Agency for Research on Cancer (2004) Tobacco smoke and involuntary smoking. IARC Press, distributed by IARC Press and the World Health Organization Distribution and Sales, Lyon, France, Geneva

  2. Kune GA, Kune S, Vitetta L et al (1992) Smoking and colorectal cancer risk: data from the Melbourne Colorectal Cancer Study and brief review of literature. Int J Cancer 50:369–372

    Article  CAS  PubMed  Google Scholar 

  3. Potter JD (1999) Colorectal cancer: molecules and populations. J Natl Cancer Inst 91:916–932

    Article  CAS  PubMed  Google Scholar 

  4. Yamasaki E, Ames BN (1977) Concentration of mutagens from urine by absorption with the nonpolar resin XAD-2: cigarette smokers have mutagenic urine. Proc Natl Acad Sci USA 74:3555–3559

    Article  CAS  PubMed  Google Scholar 

  5. Peppone LJ, Mahoney MC, Cummings KM et al (2008) Colorectal cancer occurs earlier in those exposed to tobacco smoke: implications for screening. J Cancer Res Clin Oncol 134:743–751

    Article  PubMed  Google Scholar 

  6. Doll R, Gray R, Hafner B et al (1980) Mortality in relation to smoking: 22 years’ observations on female British doctors. Br Med J 280:967–971

    Article  CAS  PubMed  Google Scholar 

  7. Doll R, Peto R (1976) Mortality in relation to smoking: 20 years’ observations on male British doctors. Br Med J 2:1525–1536

    Article  CAS  PubMed  Google Scholar 

  8. Graham S, Dayal H, Swanson M et al (1978) Diet in the epidemiology of cancer of the colon and rectum. J Natl Cancer Inst 61:709–714

    CAS  PubMed  Google Scholar 

  9. Hammond EC, Horn D (1958) Smoking and death rates; report on forty-four months of follow-up of 187,783 men. II. Death rates by cause. J Am Med Assoc 166:1294–1308

    Google Scholar 

  10. Kahn HA (1966) The Dorn study of smoking and mortality among U.S. veterans: report on eight and one-half years of observation. Natl Cancer Inst Monogr 19:1–125

    CAS  PubMed  Google Scholar 

  11. Rogot E, Murray JL (1980) Smoking and causes of death among U.S. veterans: 16 years of observation. Public Health Rep 95:213–222

    CAS  PubMed  Google Scholar 

  12. Boutron MC, Faivre J, Dop MC et al (1995) Tobacco, alcohol, and colorectal tumors: a multistep process. Am J Epidemiol 141:1038–1046

    CAS  PubMed  Google Scholar 

  13. Giovannucci E, Colditz GA, Stampfer MJ et al (1994) A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. women. J Natl Cancer Inst 86:192–199

    Article  CAS  PubMed  Google Scholar 

  14. Giovannucci E, Rimm EB, Stampfer MJ et al (1994) A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men. J Natl Cancer Inst 86:183–191

    Article  CAS  PubMed  Google Scholar 

  15. Jacobson JS, Neugut AI, Murray T et al (1994) Cigarette smoking and other behavioral risk factors for recurrence of colorectal adenomatous polyps (New York City, NY, USA). Cancer Causes Control 5:215–220

    Article  CAS  PubMed  Google Scholar 

  16. Potter JD, Bigler J, Fosdick L et al (1999) Colorectal adenomatous and hyperplastic polyps: smoking and N-acetyltransferase 2 polymorphisms. Cancer Epidemiol Biomarkers Prev 8:69–75

    CAS  PubMed  Google Scholar 

  17. Terry MB, Neugut AI (1998) Cigarette smoking and the colorectal adenoma-carcinoma sequence: a hypothesis to explain the paradox. Am J Epidemiol 147:903–910

    CAS  PubMed  Google Scholar 

  18. Le Marchand L, Wilkens LR, Kolonel LN et al (1997) Associations of sedentary lifestyle, obesity, smoking, alcohol use, and diabetes with the risk of colorectal cancer. Cancer Res 57:4787–4794

    CAS  PubMed  Google Scholar 

  19. Luchtenborg M, White KK, Wilkens L et al (2007) Smoking and colorectal cancer: different effects by type of cigarettes? Cancer Epidemiol Biomarkers Prev 16:1341–1347

    Article  PubMed  CAS  Google Scholar 

  20. Newcomb PA, Storer BE, Marcus PM (1995) Cigarette smoking in relation to risk of large bowel cancer in women. Cancer Res 55:4906–4909

    CAS  PubMed  Google Scholar 

  21. Slattery ML, Potter JD, Friedman GD et al (1997) Tobacco use and colon cancer. Int J Cancer 70:259–264

    Article  CAS  PubMed  Google Scholar 

  22. Slattery ML, Samowtiz W, Ma K et al (2004) CYP1A1, cigarette smoking, and colon and rectal cancer. Am J Epidemiol 160:842–852

    Article  PubMed  Google Scholar 

  23. Slattery ML, West DW, Robison LM et al (1990) Tobacco, alcohol, coffee, and caffeine as risk factors for colon cancer in a low-risk population. Epidemiology 1:141–145

    Article  CAS  PubMed  Google Scholar 

  24. Chao A, Thun MJ, Jacobs EJ et al (2000) Cigarette smoking and colorectal cancer mortality in the cancer prevention study II. J Natl Cancer Inst 92:1888–1896

    Article  CAS  PubMed  Google Scholar 

  25. Heineman EF, Zahm SH, McLaughlin JK et al (1994) Increased risk of colorectal cancer among smokers: results of a 26-year follow-up of US veterans and a review. Int J Cancer 59:728–738

    Article  CAS  PubMed  Google Scholar 

  26. Hsing AW, McLaughlin JK, Chow WH et al (1998) Risk factors for colorectal cancer in a prospective study among U.S. white men. Int J Cancer 77:549–553

    Article  CAS  PubMed  Google Scholar 

  27. Knekt P, Hakama M, Jarvinen R et al (1998) Smoking and risk of colorectal cancer. Br J Cancer 78:136–139

    CAS  PubMed  Google Scholar 

  28. Hecht SS, Hoffmann D (1988) Tobacco-specific nitrosamines, an important group of carcinogens in tobacco and tobacco smoke. Carcinogenesis 9:875–884

    Article  CAS  PubMed  Google Scholar 

  29. Ito N, Hasegawa R, Sano M et al (1991) A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 12:1503–1506

    Article  CAS  PubMed  Google Scholar 

  30. Wu WK, Wong HP, Luo SW et al (2005) 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone from cigarette smoke stimulates colon cancer growth via beta-adrenoceptors. Cancer Res 65:5272–5277

    Article  CAS  PubMed  Google Scholar 

  31. Alexandrov K, Rojas M, Kadlubar FF et al (1996) Evidence of anti-benzo[a]pyrene diolepoxide-DNA adduct formation in human colon mucosa. Carcinogenesis 17:2081–2083

    Article  CAS  PubMed  Google Scholar 

  32. Giovannucci E (2001) An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 10:725–731

    CAS  PubMed  Google Scholar 

  33. Corbo GM, Agabiti N, Pistelli R et al (2007) Parental smoking and lung function: misclassification due to background exposure to passive smoking. Respir Med 101:768–773

    Article  PubMed  Google Scholar 

  34. Pell JP, Haw SJ, Cobbe SM et al (2008) Validity of self-reported smoking status: comparison of patients admitted to hospital with acute coronary syndrome and the general population. Nicotine Tob Res 10:861–866

    Article  PubMed  Google Scholar 

  35. Terry PD, Rohan TE (2002) Cigarette smoking and the risk of breast cancer in women: a review of the literature. Cancer Epidemiol Biomarkers Prev 11:953–971

    PubMed  Google Scholar 

  36. Johnson KC (2005) Accumulating evidence on passive and active smoking and breast cancer risk. Int J Cancer 117:619–628

    Article  CAS  PubMed  Google Scholar 

  37. Alberg AJ, Kouzis A, Genkinger JM et al (2007) A prospective cohort study of bladder cancer risk in relation to active cigarette smoking and household exposure to secondhand cigarette smoke. Am J Epidemiol 165:660–666

    Article  PubMed  Google Scholar 

  38. Jiang X, Yuan JM, Skipper PL et al (2007) Environmental tobacco smoke and bladder cancer risk in never smokers of Los Angeles County. Cancer Res 67:7540–7545

    Article  CAS  PubMed  Google Scholar 

  39. Samanic C, Kogevinas M, Dosemeci M et al (2006) Smoking and bladder cancer in Spain: effects of tobacco type, timing, environmental tobacco smoke, and gender. Cancer Epidemiol Biomarkers Prev 15:1348–1354

    Article  PubMed  Google Scholar 

  40. Gerhardsson de Verdier M, Plato N, Steineck G et al (1992) Occupational exposures and cancer of the colon and rectum. Am J Ind Med 22:291–303

    Article  CAS  PubMed  Google Scholar 

  41. Nishino Y, Tsubono Y, Tsuji I et al (2001) Passive smoking at home and cancer risk: a population-based prospective study in Japanese nonsmoking women. Cancer Causes Control 12:797–802

    Article  CAS  PubMed  Google Scholar 

  42. Sandler RS, Sandler DP, Comstock GW et al (1988) Cigarette smoking and the risk of colorectal cancer in women. J Natl Cancer Inst 80:1329–1333

    Article  CAS  PubMed  Google Scholar 

  43. Slattery ML, Edwards S, Curtin K et al (2003) Associations between smoking, passive smoking, GSTM-1, NAT2, and rectal cancer. Cancer Epidemiol Biomarkers Prev 12:882–889

    CAS  PubMed  Google Scholar 

  44. Verla-Tebit E, Lilla C, Hoffmeister M et al (2009) Exposure to environmental tobacco smoke and the risk of colorectal cancer in a case–control study from Germany. Eur J Cancer Prev 18:9–12

    Article  CAS  PubMed  Google Scholar 

  45. D’Avanzo B, La Vecchia C, Franceschi S et al (1995) Cigarette smoking and colorectal cancer: a study of 1,584 cases and 2,879 controls. Prev Med 24:571–579

    Article  PubMed  Google Scholar 

  46. Nyren O, Bergstrom R, Nystrom L et al (1996) Smoking and colorectal cancer: a 20-year follow-up study of Swedish construction workers. J Natl Cancer Inst 88:1302–1307

    Article  CAS  PubMed  Google Scholar 

  47. Olsen J, Kronborg O (1993) Coffee, tobacco and alcohol as risk factors for cancer and adenoma of the large intestine. Int J Epidemiol 22:398–402

    Article  CAS  PubMed  Google Scholar 

  48. Tavani A, Gallus S, Negri E et al (1998) Cigarette smoking and risk of cancers of the colon and rectum: a case–control study from Italy. Eur J Epidemiol 14:675–681

    Article  CAS  PubMed  Google Scholar 

  49. Baron JA, Gerhardsson de Verdier M, Ekbom A (1994) Coffee, tea, tobacco, and cancer of the large bowel. Cancer Epidemiol Biomarkers Prev 3:565–570

    CAS  PubMed  Google Scholar 

  50. Wong HP, Yu L, Lam EK et al (2007) Nicotine promotes cell proliferation via alpha7-nicotinic acetylcholine receptor and catecholamine-synthesizing enzymes-mediated pathway in human colon adenocarcinoma HT-29 cells. Toxicol Appl Pharmacol 221:261–267

    Article  CAS  PubMed  Google Scholar 

  51. Wong HP, Yu L, Lam EK et al (2007) Nicotine promotes colon tumor growth and angiogenesis through beta-adrenergic activation. Toxicol Sci 97:279–287

    Article  CAS  PubMed  Google Scholar 

  52. Haw SJ, Gruer L (2007) Changes in exposure of adult non-smokers to secondhand smoke after implementation of smoke-free legislation in Scotland: national cross sectional survey. BMJ 335:549 (Clinical research ed)

    Article  PubMed  Google Scholar 

  53. Jefferis BJ, Thomson AG, Lennon LT et al (2009) Changes in environmental tobacco smoke (ETS) exposure over a 20-year period: cross-sectional and longitudinal analyses. Addiction (Abingdon, England) 104:496–503

    Google Scholar 

  54. Martinez-Sanchez JM, Fernandez E, Fu M et al (2009) Assessment of exposure to secondhand smoke by questionnaire and salivary cotinine in the general population of Barcelona, Spain (2004–2005). Prev Med 48:218–223

    Article  CAS  PubMed  Google Scholar 

  55. Pirkle JL, Bernert JT, Caudill SP et al (2006) Trends in the exposure of nonsmokers in the U.S. population to secondhand smoke: 1988–2002. Environ Health Perspect 114:853–858

    Article  CAS  PubMed  Google Scholar 

  56. Schick S, Glantz SA (2006) Sidestream cigarette smoke toxicity increases with aging and exposure duration. Tob Control 15:424–429

    Article  PubMed  Google Scholar 

  57. Witschi H, Espiritu I, Peake JL et al (1997) The carcinogenicity of environmental tobacco smoke. Carcinogenesis 18:575–586

    Article  CAS  PubMed  Google Scholar 

  58. Jinot J, Bayard SP, United States, Environmental Protection Agency, Office of Health and Environmental Assessment et al (1992) Respiratory health effects of passive smoking: lung cancer and other disorders. Office of Health and Environmental Assessment, Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC

    Google Scholar 

  59. Menezes RJ, Swede H, Niles R et al (2006) Regular use of aspirin and prostate cancer risk (United States). Cancer Causes Control 17:251–256

    Article  PubMed  Google Scholar 

  60. Mettlin C, Croghan I, Natarajan N et al (1990) The association of age and familial risk in a case–control study of breast cancer. Am J Epidemiol 131:973–983

    CAS  PubMed  Google Scholar 

  61. Moysich KB, Mettlin C, Piver MS et al (2001) Regular use of analgesic drugs and ovarian cancer risk. Cancer Epidemiol Biomarkers Prev 10:903–906

    CAS  PubMed  Google Scholar 

  62. Morabia A, Stellman SD, Wynder EL (1996) Smoking prevalence in neighborhood and hospital controls: implications for hospital-based case–control studies. J Clin Epidemiol 49:885–889

    Article  CAS  PubMed  Google Scholar 

  63. Wynder EL, Stellman SD (1992) The “over-exposed” control group. Am J Epidemiol 135:459–461

    CAS  PubMed  Google Scholar 

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Acknowledgments

Source of Support

This work was supported by National Cancer Institute R03-CA097780 and R25-CA102618.

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Authors and Affiliations

  1. Department of Radiation Oncology, University of Rochester Medical Center, 601 Elmwood Ave., Box 704, Rochester, NY, 14642, USA

    Luke J. Peppone, Gary R. Morrow, Pascal Jean-Pierre, Supriya G. Mohile & Tom V. Darling

  2. Department of Medicine, Roswell Park Cancer Institute, Buffalo, NY, USA

    Mary E. Reid

  3. Department of Epidemiology, Roswell Park Cancer Institute, Buffalo, NY, USA

    Kirsten B. Moysich

  4. Department of Health Behavior, Roswell Park Cancer Institute, Buffalo, NY, USA

    Andrew Hyland

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  1. Luke J. Peppone
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Correspondence to Luke J. Peppone.

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Peppone, L.J., Reid, M.E., Moysich, K.B. et al. The effect of secondhand smoke exposure on the association between active cigarette smoking and colorectal cancer. Cancer Causes Control 21, 1247–1255 (2010). https://doi.org/10.1007/s10552-010-9552-3

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