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Breast cancer and exposure to tobacco smoke during potential windows of susceptibility

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Abstract

Purpose

An association between smoking and breast cancer is unresolved, although a higher risk from exposure during windows of susceptibility has been proposed. The objective of this prospective study was to evaluate the association between tobacco smoke and breast cancer with a focus on timing of exposure, especially during early life.

Methods

Sister study participants (n = 50,884) aged 35–74 were enrolled from 2003 to 2009. Women in the United States and Puerto Rico were eligible if they were breast cancer-free but had a sister with breast cancer. Participants completed questionnaires on smoking and environmental tobacco smoke (ETS) exposure. Cox regression was used to estimate adjusted hazard ratios (HRs) and 95% confidence intervals (95% CIs) for breast cancer risk.

Results

During follow-up (mean = 6.4 years), 1,843 invasive breast cancers were diagnosed. Neither active smoking nor adult ETS was associated with breast cancer risk. However, never smoking women exposed to ETS throughout their childhood had a 17% higher risk of breast cancer (95% CI 1.00–1.36) relative to those with no exposure. In utero ETS exposure was also associated with breast cancer (HR = 1.16, 95% CI 1.01–1.32) and the HR was most elevated for women born in earlier birth cohorts (<1940, HR = 1.44, 95% CI 1.02–2.02; 1940–1949, HR = 1.28, 95% CI 1.01–1.62).

Conclusion

In utero ETS and ETS exposure during childhood and adolescence were associated with increased risk of breast cancer and associations varied by birth cohort.

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References

  1. Smith CJ, Perfetti TA, Rumple MA, Rodgman A, Doolittle DJ (2000) “IARC group 2A Carcinogens” reported in cigarette mainstream smoke. Food Chem Toxicol 38:371–383

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  3. Hecht SS (2002) Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen 39:119–126

    Article  CAS  PubMed  Google Scholar 

  4. Li DH, Wang MY, Dhingra K, Hittelman WN (1996) Aromatic DNA adducts in adjacent tissues of breast cancer patients: clues to breast cancer etiology. Cancer Res 56:287–293

    CAS  PubMed  Google Scholar 

  5. Perera FP, Estabook A, Hewer A et al (1995) Carcinogen-DNA adducts in human breast-tissue. Cancer Epidemiol Biomark Prev 4:233–238

    CAS  Google Scholar 

  6. Conway K, Edmiston SN, Cui L et al (2002) Prevalence and spectrum of p53 mutations associated with smoking in breast cancer. Cancer Res 62:1987–1995

    CAS  PubMed  Google Scholar 

  7. US Department of Health and Human Services (2014 Printed with corrections, January 2014) The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. US 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. Atlanta, GA

  8. Gaudet MM, Gapstur SM, Sun J, Diver WR, Hannan LM, Thun MJ (2013) Active smoking and breast cancer risk: original cohort data and meta-analysis. J Natl Cancer Inst 105:515–525

    Article  CAS  PubMed  Google Scholar 

  9. Bjerkaas E, Parajuli R, Weiderpass E et al (2013) Smoking duration before first childbirth: an emerging risk factor for breast cancer? Results from 302,865 Norwegian women. Cancer Causes Control 24:1347–1356

    Article  PubMed  PubMed Central  Google Scholar 

  10. Rosenberg L, Boggs DA, Bethea TN, Wise LA, Adams-Campbell LL, Palmer JR (2013) A prospective study of smoking and breast cancer risk among African-American women. Cancer Causes Control 24:2207–2215

    Article  PubMed  Google Scholar 

  11. Dossus L, Boutron-Ruault MC, Kaaks R et al (2014) Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int J Cancer 134:1871–1888

    Article  CAS  PubMed  Google Scholar 

  12. Nyante SJ, Gierach GL, Dallal CM et al (2014) Cigarette smoking and postmenopausal breast cancer risk in a prospective cohort. Br J Cancer 110:2339–2347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gram IT, Little MA, Lund E, Braaten T (2016) The fraction of breast cancer attributable to smoking: the Norwegian women and cancer study 1991–2012. Br J Cancer 9:154

    Google Scholar 

  14. Gram IT, Park SY, Kolonel LN et al (2015) Smoking and risk of breast cancer in a racially/ethnically diverse population of mainly women who do not drink alcohol: the MEC study. Am J Epidemiol 182:917–925

    Article  PubMed  PubMed Central  Google Scholar 

  15. Catsburg C, Miller AB, Rohan TE (2015) Active cigarette smoking and risk of breast cancer. Int J Cancer 136:2204–2209

    Article  CAS  PubMed  Google Scholar 

  16. Hiatt RA, Haslam SZ, Osuch J (2009) The breast cancer and the environment research centers: transdisciplinary research on the role of the environment in breast cancer etiology. Environ Health Perspect 117:1814–1822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Colditz GA, Frazier AL (1995) Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus. Cancer Epidemiol Biomark Prev 4:567–571

    CAS  Google Scholar 

  18. DeRoo LA, Cummings P, Mueller BA (2011) Smoking before the first pregnancy and the risk of breast cancer: a meta-analysis. Am J Epidemiol 174:390–402

    Article  PubMed  PubMed Central  Google Scholar 

  19. Nichols HB, Baird DD, DeRoo LA, Kissling GE, Sandler DP (2013) Tubal ligation in relation to menopausal symptoms and breast cancer risk. Br J Cancer 109:1291–1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. National Institutes of Environmental Health Sciences. Breast Cancer Validation. https://sisterstudy.niehs.nih.gov/English/brca-validation.htm. Accessed 1 Dec 2015

  21. Greenland S, Pearl J, Robins JM (1999) Causal diagrams for epidemiologic research. Epidemiology 10:37–48

    Article  CAS  PubMed  Google Scholar 

  22. Xu X, Dailey AB, Peoples-Sheps M, Talbott EO, Li N, Roth J (2009) Birth weight as a risk factor for breast cancer: a meta-analysis of 18 epidemiological studies. J Womens Health. 18:1169–1178

    Article  Google Scholar 

  23. Hilakivi-Clarke L (2014) Maternal exposure to diethylstilbestrol during pregnancy and increased breast cancer risk in daughters. Breast Cancer Res 16:208

    Article  PubMed  PubMed Central  Google Scholar 

  24. Bernstein L, Pike MC, Lobo RA, Depue RH, Ross RK, Henderson BE (1989) Cigarette smoking in pregnancy results in marked decrease in maternal hCG and oestradiol levels. Br J Obstet Gynaecol 96:92–96

    Article  CAS  PubMed  Google Scholar 

  25. Tomatis L (1989) Overview of perinatal and multigeneration carcinogenesis. IARC Sci Publ 96:1–15

    Google Scholar 

  26. Sandler DP, Everson RB, Wilcox AJ (1985) Passive smoking in adulthood and cancer risk. Am J Epidemiol 121:37–48

    Article  CAS  PubMed  Google Scholar 

  27. Sanderson M, Williams MA, Malone KE et al (1996) Perinatal factors and risk of breast cancer. Epidemiology 7:34–37

    Article  CAS  PubMed  Google Scholar 

  28. Sanderson M, Williams M, Daling J et al (1998) Maternal factors and breast cancer risk among young women. Paediatr Perinat Epidemiol 12:397–407

    Article  CAS  PubMed  Google Scholar 

  29. Weiss HA, Potischman NA, Brinton LA et al (1997) Prenatal and perinatal risk factors for breast cancer in young women. Epidemiology 8:181–187

    Article  CAS  PubMed  Google Scholar 

  30. Hodgson ME, Newman B, Millikan RC (2004) Birthweight, parental age, birth order and breast cancer risk in African-American and white women: a population-based case–control study. Breast Cancer Res 6:R656–R667

    Article  PubMed  PubMed Central  Google Scholar 

  31. Park SK, Garcia-Closas M, Lissowska J et al (2006) Intrauterine environment and breast cancer risk in a population-based case–control study in Poland. Int J Cancer 119:2136–2141

    Article  CAS  PubMed  Google Scholar 

  32. Park SK, Kang D, McGlynn KA et al (2008) Intrauterine environments and breast cancer risk: meta-analysis and systematic review. Breast Cancer Res 10:R8

    Article  PubMed  PubMed Central  Google Scholar 

  33. Strohsnitter WC, Noller KL, Titus-Ernstoff L et al (2005) Breast cancer incidence in women prenatally exposed to maternal cigarette smoke. Epidemiology. 16:342–345

    Article  PubMed  Google Scholar 

  34. Sanderson M, Daling JR, Doody DR, Malone KE (2006) Perinatal factors and mortality from breast cancer. Cancer Epidemiol Biomark Prev 15:1984–1987

    Article  Google Scholar 

  35. Lin Y, Kikuchi S, Tamakoshi K et al (2008) Active smoking, passive smoking, and breast cancer risk: findings from the Japan Collaborative Cohort Study for Evaluation of Cancer Risk. J Epidemiol. 18:77–83

    Article  PubMed  PubMed Central  Google Scholar 

  36. Luo J, Margolis KL, Wactawski-Wende J, et al (2011) Association of active and passive smoking with risk of breast cancer among postmenopausal women: a prospective cohort study. BMJ 342:d1016

    Article  PubMed  PubMed Central  Google Scholar 

  37. Xue F, Willett WC, Rosner BA, Hankinson SE, Michels KB (2011) Cigarette smoking and the incidence of breast cancer. Arch Intern Med 171:125–133

    PubMed  PubMed Central  Google Scholar 

  38. Reynolds P, Goldberg D, Hurley S et al (2009) Passive smoking and risk of breast cancer in the California teachers study. Cancer Epidemiol Biomark Prev 18:3389–3398

    Article  CAS  Google Scholar 

  39. Russo J, Tay LK, Russo IH (1982) Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 2:5–73

    Article  CAS  PubMed  Google Scholar 

  40. Hamajima N, Hirose K, Tajima K et al (2002) Alcohol, tobacco and breast cancer—collaborative reanalysis of individual data from 53 epidemiological studies, including 58,515 women with breast cancer and 95,067 women without the disease. Br J Cancer 87:1234–1245

    Article  CAS  PubMed  Google Scholar 

  41. Cui Y, Miller AB, Rohan TE (2006) Cigarette smoking and breast cancer risk: update of a prospective cohort study. Breast Cancer Res Treat 100:293–299

    Article  PubMed  Google Scholar 

  42. Gram IT, Braaten T, Terry PD et al (2005) Breast cancer risk among women who start smoking as teenagers. Cancer Epidemiol Biomark Prev 14:61–66

    Google Scholar 

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Acknowledgments

The authors recognize the helpful feedback from Drs. Lauren Wilson and Katie O’Brien.

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Correspondence to Alexandra J. White.

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Conflicts of interest

The authors have no conflicts of interest to declare.

Sources of financial support

This research was supported in part by the Intramural Research Program of the NIH, National Institute of Environmental Health Sciences (Z01-ES044005).

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White, A.J., D’Aloisio, A.A., Nichols, H.B. et al. Breast cancer and exposure to tobacco smoke during potential windows of susceptibility. Cancer Causes Control 28, 667–675 (2017). https://doi.org/10.1007/s10552-017-0903-1

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  • DOI: https://doi.org/10.1007/s10552-017-0903-1

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