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Cancer Causes & Control

, Volume 28, Issue 9, pp 929–938 | Cite as

Active smoking and survival following breast cancer among African American and non-African American women in the Carolina Breast Cancer Study

  • Humberto ParadaJrEmail author
  • Xuezheng Sun
  • Chiu-Kit Tse
  • Andrew F. Olshan
  • Melissa A. Troester
  • Kathleen Conway
Original paper

Abstract

Purpose

To examine racial differences in smoking rates at the time of breast cancer diagnosis and subsequent survival among African American and non-African American women in the Carolina Breast Cancer Study (Phases I/II), a large population-based North Carolina study.

Methods

We interviewed 788 African American and 1,020 Caucasian/non-African American women diagnosed with invasive breast cancer from 1993 to 2000, to assess smoking history. After a median follow-up of 13.56 years, we identified 717 deaths using the National Death Index; 427 were breast cancer-related. We used Cox regression to examine associations between self-reported measures of smoking and breast cancer-specific survival within 5 years and up to 18 years after diagnosis conditional on 5-year survival. We examined race and estrogen receptor status as potential modifiers.

Results

Current (vs never) smoking was not associated with 5-year survival; however, risk of 13 year conditional breast cancer-specific mortality was elevated among women who were current smokers at diagnosis (HR 1.54, 95% CI 1.06–2.25), compared to never smokers. Although smoking rates were similar among African American (22.0%) and non-African American (22.1%) women, risk of breast cancer-specific mortality was elevated among African American (HR 1.69, 95% CI 1.00–2.85), but only weakly elevated among non-African American (HR 1.22, 95% CI 0.70–2.14) current (vs. never) smokers (P Interaction = 0.30). Risk of breast cancer-specific mortality was also elevated among current (vs never) smokers diagnosed with ER (HR 2.58, 95% CI 1.35–4.93), but not ER+ (HR 1.11, 95% CI 0.69–1.78) tumors (P Interaction = 0.17).

Conclusions

Smoking may negatively impact long-term survival following breast cancer. Racial differences in long-term survival, as related to smoking, may be driven by ER status, rather than by differences in smoking patterns.

Keywords

Smoking Breast cancer Survival analysis Mortality 

Notes

Funding

This research was funded in part by the University Cancer Research Fund of North Carolina and the National Cancer Institute Specialized Program of Research Excellence (SPORE) in Breast Cancer (NIH/NCI P50-CA58223) and by the National Institute of Environmental Health Sciences (T32 ES007018).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the Carolina Breast Cancer Study involving human participants were in accordance with the ethical standards of the Institutional Review Boards of the University of North Carolina at Chapel Hill and were in compliance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

10552_2017_923_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 43 kb)

References

  1. 1.
    Siegel RL, Miller KD, Jemal A (2016) Cancer statistics, 2016. CA Cancer J Clin 66:7–30CrossRefPubMedGoogle Scholar
  2. 2.
    Smigal C, Jemal A, Ward E et al (2006) Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin 56:168–183CrossRefPubMedGoogle Scholar
  3. 3.
    National Cancer Institute (2017) SEER Stat Fact Sheets: Breast Cancer. http://seer.cancer.gov/statfacts/html/breast.html. Accessed 19 Jun 2017
  4. 4.
    Shavers VL, Brown ML (2002) Racial and ethnic disparities in the receipt of cancer treatment. J Natl Cancer Inst 94:334–357CrossRefPubMedGoogle Scholar
  5. 5.
    Joslyn SA (2002) Racial differences in treatment and survival from early-stage breast carcinoma. Cancer 95:1759–1766CrossRefPubMedGoogle Scholar
  6. 6.
    O’Brien KM, Cole SR, Tse C-K et al (2010) Intrinsic breast tumor subtypes, race, and long-term survival in the Carolina Breast Cancer Study. Clin Cancer Res 16:6100–6110CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492–2502CrossRefPubMedGoogle Scholar
  8. 8.
    Jamal A, King BA, Neff LJ et al (2016) Current Cigarette Smoking Among Adults—United States, 2005–2015. MMWR Morb Mortal Wkly Rep 65:1205–1211CrossRefPubMedGoogle Scholar
  9. 9.
    Geronimus AT, Neidert LJ, Bound J (1993) Age patterns of smoking in US black and white women of childbearing age. Am J Public Health 83:1258–1264CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Gaudet MM, Gapstur SM, Sun J et al (2013) Active smoking and breast cancer risk: original cohort data and meta-analysis. J Natl Cancer Inst 105:515–525CrossRefPubMedGoogle Scholar
  11. 11.
    Bérubé S, Lemieux J, Moore L et al (2014) Smoking at time of diagnosis and breast cancer-specific survival: new findings and systematic review with meta-analysis. Breast Cancer Res 16:R42CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Dal Maso L, Zucchetto A, Talamini R et al (2008) Effect of obesity and other lifestyle factors on mortality in women with breast cancer. Int J Cancer 123:2188–2194CrossRefGoogle Scholar
  13. 13.
    Braithwaite D, Izano M, Moore DH et al (2012) Smoking and survival after breast cancer diagnosis: a prospective observational study and systematic review. Breast Cancer Res Treat 136:521–533CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Boone SD, Baumgartner KB, Baumgartner RN et al (2015) Active and passive cigarette smoking and mortality among Hispanic and non-Hispanic white women diagnosed with invasive breast cancer. Ann Epidemiol 25:824–831CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Holmes MD, Murin S, Chen WY et al (2007) Smoking and survival after breast cancer diagnosis. Int J Cancer 120:2672–2677CrossRefPubMedGoogle Scholar
  16. 16.
    IARC (2004) IARC Monographs on evaluation of carcinogenic risks to humans: Tobacco smoke and involuntary smoking. International Agency for Research on Cancer, LyonGoogle Scholar
  17. 17.
    Zhan M, Flaws JA, Gallicchio L et al (2007) Profiles of tamoxifen-related side effects by race and smoking status in women with breast cancer. Cancer Detect Prev 31:384–390CrossRefPubMedGoogle Scholar
  18. 18.
    Bishop JD, Killelea BK, Chagpar AB et al (2014) Smoking and breast cancer recurrence after breast conservation therapy. Int J Breast Cancer 2014:1–5CrossRefGoogle Scholar
  19. 19.
    Neugut AI, Murray T, Santos J et al (1994) Increased risk of lung cancer after breast cancer radiation therapy in cigarette smokers. Cancer 73:1615–1620CrossRefPubMedGoogle Scholar
  20. 20.
    Newman B, Moorman PG, Millikan R et al (1995) The Carolina Breast Cancer Study: integrating population-based epidemiology and molecular biology. Breast Cancer Res Treat 35:51–60CrossRefPubMedGoogle Scholar
  21. 21.
    Butler EN, Tse C-K, Bell ME et al (2016) Active smoking and risk of luminal and basal-like breast cancer subtypes in the Carolina Breast Cancer Study. Cancer Causes Control 27:775–786CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Millikan RC, Pittman GS, Newman B et al (1998) Cigarette smoking, N-acetyltransferases 1 and 2, and breast cancer risk. Cancer Epidemiol Biomarkers Prev 7:371–379PubMedGoogle Scholar
  23. 23.
    Soerjomataram I, Louwman MWJ, Ribot JG et al (2008) An overview of prognostic factors for long-term survivors of breast cancer. Breast Cancer Res Treat 107:309–330CrossRefPubMedGoogle Scholar
  24. 24.
    Centers for Disease Control and Prevention (2014) National Death Index. http://www.cdc.gov/nchs/ndi.htm. Accessed 29 Jun 2016
  25. 25.
    Sagiv SK, Gaudet MM, Eng SM et al (2007) Active and passive cigarette smoke and breast cancer survival. Ann Epidemiol 17:385–393CrossRefPubMedGoogle Scholar
  26. 26.
    Hellmann SS, Thygesen LC, Tolstrup JS, Grønbæk M (2010) Modifiable risk factors and survival in women diagnosed with primary breast cancer: results from a prospective cohort study. Eur J Cancer Prev 19:366–373CrossRefPubMedGoogle Scholar
  27. 27.
    Kakugawa Y, Kawai M, Nishino Y et al (2015) Smoking and survival after breast cancer diagnosis in Japanese women: a prospective cohort study. Cancer Sci 106:1066–1074CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Fentiman IS, Allen DS, Hamed H (2005) Smoking and prognosis in women with breast cancer. Int J Clin Pract 59:1051–1054CrossRefPubMedGoogle Scholar
  29. 29.
    Vander Weg MW, Howren MB, Cai X (2012) Use of routine clinical preventive services among daily smokers, non-daily smokers, former smokers, and never-smokers. Nicotine Tob Res 14:123–130CrossRefPubMedGoogle Scholar
  30. 30.
    Passarelli MN, Newcomb PA, Hampton JM et al (2016) Cigarette smoking before and after breast cancer diagnosis: mortality from breast cancer and smoking-related diseases. J Clin Oncol 34:1–8CrossRefGoogle Scholar
  31. 31.
    Tominaga K, Andow J, Koyama Y et al (1998) Family environment, hobbies and habits as psychosocial predictors of survival for surgically treated patients with breast cancer. Jpn J Clin Oncol 28:36–41CrossRefPubMedGoogle Scholar
  32. 32.
    Manjer J (2000) Survival of women with breast cancer in relation to smoking. Eur J Surg 166:852–858CrossRefPubMedGoogle Scholar
  33. 33.
    Warren GW, Kasza KA, Reid ME et al (2012) Smoking at diagnosis and survival in cancer patients. Int J Cancer 132:401–410CrossRefPubMedGoogle Scholar
  34. 34.
    Sopori M (2002) Effects of cigarette smoke on the immune system. Nat Rev Immunol 2:372–377CrossRefPubMedGoogle Scholar
  35. 35.
    Singh S, Pillai S, Chellappan S (2011) Nicotinic acetylcholine receptor signaling in tumor growth and metastasis. J Oncol 2011:456743CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Gingras I Jr, Ignatiadis M (2015) Immunology and breast cancer: toward a new way of understanding breast cancer and developing novel therapeutic strategies. Clin Adv Hematol Oncol 13:372–385PubMedGoogle Scholar
  37. 37.
    Desmedt C, Haibe-Kains B, Wirapati P et al (2008) Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 14:5158–5165CrossRefPubMedGoogle Scholar
  38. 38.
    Teschendorff AE, Miremadi A, Pinder SE et al (2007) An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 8:R157CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Pfeifer GP, Denissenko MF, Olivier M et al (2002) Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 21:7435–7451CrossRefPubMedGoogle Scholar
  40. 40.
    Bertheau P, Lehmann-Che J, Varna M et al (2013) p53 in breast cancer subtypes and new insights into response to chemotherapy. Breast 22:S27–S29CrossRefPubMedGoogle Scholar
  41. 41.
    Rakha EA, Reis-Filho JS, Ellis IO (2008) Basal-like breast cancer: a critical review. J Clin Oncol 26:2568–2581CrossRefPubMedGoogle Scholar
  42. 42.
    Conway K, Edmiston SN, Parrish E et al (2017) Breast tumor DNA methylation patterns associated with smoking in the Carolina Breast Cancer Study. Breast Cancer Res Treat. doi: 10.1007/s10549-017-4178-8 PubMedGoogle Scholar
  43. 43.
    Browman GP, Wong G, Hodson I et al (1993) Influence of cigarette smoking on the efficacy of radiation therapy in head and neck cancer. N Engl J Med 328:159–163CrossRefPubMedGoogle Scholar
  44. 44.
    Cooley ME, Sipples RL, Murphy M, Sarna L (2008) Smoking cessation and lung cancer: oncology nurses can make a difference. Semin Oncol Nurs 24:16–26CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Krall EA, Valadian I, Dwyer JT, Gardner J (1989) Accuracy of recalled smoking data. Am J Public Health 79:200–202CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Centers for Disease Control and Prevention (CDC) (2011) Vital signs: current cigarette smoking among adults aged ≥18 years–United States, 2005–2010. MMWR Morb Mortal Wkly Rep 60:1207–1212Google Scholar
  47. 47.
    Westmaas JL, Newton CC, Stevens VL et al (2015) Does a recent cancer diagnosis predict smoking cessation? An analysis from a large prospective US cohort. J Clin Oncol 33:1647–1652CrossRefPubMedGoogle Scholar
  48. 48.
    Newcomb P, Passarelli M, Hampton J et al (2014) Smoking history in relation to survival after a breast cancer diagnosis. Cancer Epidemiol Biomarkers Prev 23:569–570CrossRefGoogle Scholar
  49. 49.
    Howlader N, Altekruse SF, Li CI et al (2014) US incidence of breast cancer subtypes defined by joint hormone receptor and HER2 status. J Natl Cancer Inst 106:dju055CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of EpidemiologyUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Lineberger Comprehensive Cancer CenterUniversity of North Carolina at Chapel HillChapel HillUSA

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