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Smoking and survival after breast cancer diagnosis: a prospective observational study and systematic review

  • Epidemiology
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Abstract

The association of smoking with outcomes following breast cancer prognosis is not well understood. In a cohort study called Life After Cancer Epidemiology (LACE), 2,265 women diagnosed with breast cancer were followed for a median of 12 years. We used multivariable proportional-hazards models to determine whether smoking, assessed approximately two years post-diagnosis, was associated with risk of death among these women. We also undertook a systematic review of all cohort studies to date that have examined the association between smoking and breast cancer mortality. Compared with never smokers, women who were current smokers had a twofold higher rate of dying from breast cancer [hazard ratio (HR) = 2.01, 95 % confidence interval (CI) 1.27–3.18] and an approximately fourfold higher rate of dying from competing (non-breast cancer) causes (HR = 3.84, 95 % CI 2.50–5.89). Among seven studies that met the inclusion criteria in the systematic review, three studies and our own reported significantly increased risk of breast cancer death with current smoking. We found little evidence of an association between former smoking and breast cancer mortality (HR = 1.24, 95 % CI 0.94–1.64). Consistent with findings from our prospective observational study, the systematic review of seven additional studies indicates positive association of current smoking with breast cancer mortality, but weak association with former smoking. Women who smoke following breast cancer diagnosis and treatment are at higher risk of death both from breast cancer and other causes.

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References

  1. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295(21):2492–2502. doi:10.1001/jama.295.21.2492

    Article  PubMed  CAS  Google Scholar 

  2. Daniell HW (1995) A worse prognosis for smokers with prostate cancer. J Urol 154(1):153–157

    Article  PubMed  CAS  Google Scholar 

  3. Myers RP (1995) Prostate cancer–neurovascular preservation; smoking cessation may enhance prognosis? J Urol 154(1):158–159

    Article  PubMed  CAS  Google Scholar 

  4. Jadallah F, McCall JL, van Rij AM (1999) Recurrence and survival after potentially curative surgery for colorectal cancer. N Z Med J 112(1091):248–250

    PubMed  CAS  Google Scholar 

  5. Kirschner CV, Yordan EL, De Geest K, Wilbanks GD (1995) Smoking, obesity, and survival in squamous cell carcinoma of the vulva. Gynecol Oncol 56(1):79–84. doi:10.1006/gyno.1995.1013

    Article  PubMed  CAS  Google Scholar 

  6. Archimbaud E, Maupas J, Lecluze-Palazzolo C, Fiere D, Viala JJ (1989) Influence of cigarette smoking on the presentation and course of chronic myelogenous leukemia. Cancer 63(10):2060–2065

    Article  PubMed  CAS  Google Scholar 

  7. Rigel DS, Friedman RJ, Levine J, Kopf AW, Levenstein M (1981) Cigarette smoking and malignant melanoma. Prognostic implications. J Dermatol Surg Oncol 7(11):889–891

    PubMed  CAS  Google Scholar 

  8. Yu GP, Ostroff JS, Zhang ZF, Tang J, Schantz SP (1997) Smoking history and cancer patient survival: a hospital cancer registry study. Cancer Detect Prev 21(6):497–509

    PubMed  CAS  Google Scholar 

  9. Holmes MD, Murin S, Chen WY, Kroenke CH, Spiegelman D, Colditz GA (2007) Smoking and survival after breast cancer diagnosis. Int J Cancer 120(12):2672–2677. doi:10.1002/ijc.22575

    Article  PubMed  CAS  Google Scholar 

  10. Ewertz M, Gillanders S, Meyer L, Zedeler K (1991) Survival of breast cancer patients in relation to factors which affect the risk of developing breast cancer. Int J Cancer 49(4):526–530

    Article  PubMed  CAS  Google Scholar 

  11. Calle EE, Miracle-McMahill HL, Thun MJ, Heath CW Jr (1994) Cigarette smoking and risk of fatal breast cancer. Am J Epidemiol 139(10):1001–1007

    PubMed  CAS  Google Scholar 

  12. Hellmann SS, Thygesen LC, Tolstrup JS, Gronbaek 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(5):366–373. doi:10.1097/CEJ.0b013e32833b4828

    Article  PubMed  Google Scholar 

  13. Warren GW, Kasza KA, Reid ME, Cummings KM, Marshall JR (2012) Smoking at diagnosis and survival in cancer patients. Int J Cancer. doi:10.1002/ijc.27617

    Google Scholar 

  14. Bradley CJ, Given CW, Roberts C (2002) Race, socioeconomic status, and breast cancer treatment and survival. J Natl Cancer Inst 94(7):490–496

    Article  PubMed  Google Scholar 

  15. Franzini L, Williams AF, Franklin J, Singletary SE, Theriault RL (1997) Effects of race and socioeconomic status on survival of 1,332 black, Hispanic, and white women with breast cancer. Ann Surg Oncol 4(2):111–118

    Article  PubMed  CAS  Google Scholar 

  16. Sternfeld B, Weltzien E, Quesenberry CP Jr, Castillo AL, Kwan M, Slattery ML, Caan BJ (2009) Physical activity and risk of recurrence and mortality in breast cancer survivors: findings from the LACE study. Cancer Epidemiol Biomarkers Prev 18(1):87–95. doi:10.1158/1055-9965.EPI-08-0595

    Article  PubMed  Google Scholar 

  17. Irwin ML, Smith AW, McTiernan A, Ballard-Barbash R, Cronin K, Gilliland FD, Baumgartner RN, Baumgartner KB, Bernstein L (2008) Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study. J Clin Oncol 26(24):3958–3964. doi:10.1200/JCO.2007.15.9822

    Article  PubMed  Google Scholar 

  18. Tammemagi CM, Nerenz D, Neslund-Dudas C, Feldkamp C, Nathanson D (2005) Comorbidity and survival disparities among black and white patients with breast cancer. JAMA 294(14):1765–1772. doi:10.1001/jama.294.14.1765

    Article  PubMed  CAS  Google Scholar 

  19. Satariano WA, Ragland DR (1994) The effect of comorbidity on 3-year survival of women with primary breast cancer. Ann Intern Med 120(2):104–110

    PubMed  CAS  Google Scholar 

  20. Braithwaite D, Moore DH, Satariano WA, Kwan ML, Hiatt RA, Kroenke C, Caan BJ (2012) Prognostic impact of comorbidity among long-term breast cancer survivors: results from the LACE study. Cancer Epidemiol Biomarkers Prev 21(7):1115–1125. doi:10.1158/1055-9965.EPI-11-1228

    Article  PubMed  Google Scholar 

  21. Wells AJ (1991) Breast cancer, cigarette smoking, and passive smoking. Am J Epidemiol 133(2):208–210

    PubMed  CAS  Google Scholar 

  22. Zhu BQ, Heeschen C, Sievers RE, Karliner JS, Parmley WW, Glantz SA, Cooke JP (2003) Second hand smoke stimulates tumor angiogenesis and growth. Cancer Cell 4(3):191–196

    Article  PubMed  CAS  Google Scholar 

  23. Hamajima N, Hirose K, Tajima K, Rohan T, Calle EE, Heath CW Jr, Coates RJ, Liff JM, Talamini R, Chantarakul N, Koetsawang S, Rachawat D, Morabia A, Schuman L, Stewart W, Szklo M, Bain C, Schofield F, Siskind V, Band P, Coldman AJ, Gallagher RP, Hislop TG, Yang P, Kolonel LM, Nomura AM, Hu J, Johnson KC, Mao Y, De Sanjose S, Lee N, Marchbanks P, Ory HW, Peterson HB, Wilson HG, Wingo PA, Ebeling K, Kunde D, Nishan P, Hopper JL, Colditz G, Gajalanski V, Martin N, Pardthaisong T, Silpisornkosol S, Theetranont C, Boosiri B, Chutivongse S, Jimakorn P, Virutamasen P, Wongsrichanalai C, Ewertz M, Adami HO, Bergkvist L, Magnusson C, Persson I, Chang-Claude J, Paul C, Skegg DC, Spears GF, Boyle P, Evstifeeva T, Daling JR, Hutchinson WB, Malone K, Noonan EA, Stanford JL, Thomas DB, Weiss NS, White E, Andrieu N, Bremond A, Clavel F, Gairard B, Lansac J, Piana L, Renaud R, Izquierdo A, Viladiu P, Cuevas HR, Ontiveros P, Palet A, Salazar SB, Aristizabel N, Cuadros A, Tryggvadottir L, Tulinius H, Bachelot A, Le MG, Peto J, Franceschi S, Lubin F, Modan B, Ron E, Wax Y, Friedman GD, Hiatt RA, Levi F, Bishop T, Kosmelj K, Primic-Zakelj M, Ravnihar B, Stare J, Beeson WL, Fraser G, Bullbrook RD, Cuzick J, Duffy SW, Fentiman IS, Hayward JL, Wang DY, McMichael AJ, McPherson K, Hanson RL, Leske MC, Mahoney MC, Nasca PC, Varma AO, Weinstein AL, Moller TR, Olsson H, Ranstam J, Goldbohm RA, van den Brandt PA, Apelo RA, Baens J, de la Cruz JR, Javier B, Lacaya LB, Ngelangel CA, La Vecchia C, Negri E, Marubini E, Ferraroni M, Gerber M, Richardson S, Segala C, Gatei D, Kenya P, Kungu A, Mati JG, Brinton LA, Hoover R, Schairer C, Spirtas R, Lee HP, Rookus MA, van Leeuwen FE, Schoenberg JA, McCredie M, Gammon MD, Clarke EA, Jones L, Neil A, Vessey M, Yeates D, Appleby P, Banks E, Beral V, Bull D, Crossley B, Goodill A, Green J, Hermon C, Key T, Langston N, Lewis C, Reeves G, Collins R, Doll R, Peto R, Mabuchi K, Preston D, Hannaford P, Kay C, Rosero-Bixby L, Gao YT, Jin F, Yuan JM, Wei HY, Yun T, Zhiheng C, Berry G, Cooper Booth J, Jelihovsky T, MacLennan R, Shearman R, Wang QS, Baines CJ, Miller AB, Wall C, Lund E, Stalsberg H, Shu XO, Zheng W, Katsouyanni K, Trichopoulou A, Trichopoulos D, Dabancens A, Martinez L, Molina R, Salas O, Alexander FE, Anderson K, Folsom AR, Hulka BS, Bernstein L, Enger S, Haile RW, Paganini-Hill A, Pike MC, Ross RK, Ursin G, Yu MC, Longnecker MP, Newcomb P, Kalache A, Farley TM, Holck S, Meirik O (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(11):1234–1245. doi:10.1038/sj.bjc.6600596

    Article  PubMed  Google Scholar 

  24. Hiatt RA, Fireman BH (1986) Smoking, menopause, and breast cancer. J Natl Cancer Inst 76(5):833–838

    PubMed  CAS  Google Scholar 

  25. Reynolds P, Hurley S, Goldberg DE, Anton-Culver H, Bernstein L, Deapen D, Horn-Ross PL, Peel D, Pinder R, Ross RK, West D, Wright WE, Ziogas A (2004) Active smoking, household passive smoking, and breast cancer: evidence from the California Teachers Study. J Natl Cancer Inst 96(1):29–37

    Article  PubMed  CAS  Google Scholar 

  26. Egan KM, Stampfer MJ, Hunter D, Hankinson S, Rosner BA, Holmes M, Willett WC, Colditz GA (2002) Active and passive smoking in breast cancer: prospective results from the Nurses’ Health Study. Epidemiology 13(2):138–145

    Article  PubMed  Google Scholar 

  27. 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(10 Pt 1):953–971

    PubMed  Google Scholar 

  28. Johnson KC, Miller AB, Collishaw NE, Palmer JR, Hammond SK, Salmon AG, Cantor KP, Miller MD, Boyd NF, Millar J, Turcotte F (2011) Active smoking and secondhand smoke increase breast cancer risk: the report of the Canadian Expert Panel on Tobacco Smoke and Breast Cancer Risk (2009). Tob Control 20(1):e2. doi:10.1136/tc.2010.035931

    Article  PubMed  Google Scholar 

  29. Lee CH, Huang CS, Chen CS, Tu SH, Wang YJ, Chang YJ, Tam KW, Wei PL, Cheng TC, Chu JS, Chen LC, Wu CH, Ho YS (2010) Overexpression and activation of the alpha9-nicotinic receptor during tumorigenesis in human breast epithelial cells. J Natl Cancer Inst 102(17):1322–1335. doi:10.1093/jnci/djq300

    Article  PubMed  CAS  Google Scholar 

  30. Caan B, Sternfeld B, Gunderson E, Coates A, Quesenberry C, Slattery ML (2005) Life After Cancer Epidemiology (LACE) Study: a cohort of early stage breast cancer survivors (United States). Cancer Causes Control 16(5):545–556. doi:10.1007/s10552-004-8340-3

    Article  PubMed  Google Scholar 

  31. Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults (1998) Arch Intern Med 158(17):1855–1867

    Google Scholar 

  32. Staten LK, Taren DL, Howell WH, Tobar M, Poehlman ET, Hill A, Reid PM, Ritenbaugh C (2001) Validation of the Arizona Activity Frequency Questionnaire using doubly labeled water. Med Sci Sports Exerc 33(11):1959–1967

    Article  PubMed  CAS  Google Scholar 

  33. Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O’Brien WL, Bassett DR Jr, Schmitz KH, Emplaincourt PO, Jacobs DR Jr, Leon AS (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 32(9 Suppl):S498–S504

    PubMed  CAS  Google Scholar 

  34. Fleming ID, Cooper JS, Henson DE (1997) AJCC cancer staging manual, 5th edn. Lippincott-Raven, New York

    Google Scholar 

  35. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40(5):373–383

    Article  PubMed  CAS  Google Scholar 

  36. Katz JN, Chang LC, Sangha O, Fossel AH, Bates DW (1996) Can comorbidity be measured by questionnaire rather than medical record review? Med Care 34(1):73–84

    Article  PubMed  CAS  Google Scholar 

  37. Greenland S (1989) Modeling and variable selection in epidemiologic analysis. Am J Public Health 79(3):340–349

    Article  PubMed  CAS  Google Scholar 

  38. Cox DR, Oakes D (1994) Analysis of survival data. Monographs in statistics and applied probability 21. Chapman & Hill, New York

    Google Scholar 

  39. Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Statistics for Biology and Health. Springer, New York

    Google Scholar 

  40. Prentice RL, Kalbfleisch JD (1979) Hazard rate models with covariates. Biometrics 35:25–39

    Article  PubMed  CAS  Google Scholar 

  41. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012. doi:10.1016/j.jclinepi.2009.06.005

    Article  PubMed  Google Scholar 

  42. Dal Maso L, Zucchetto A, Talamini R, Serraino D, Stocco CF, Vercelli M, Falcini F, Franceschi S (2008) Effect of obesity and other lifestyle factors on mortality in women with breast cancer. Int J Cancer 123(9):2188–2194. doi:10.1002/ijc.23747

    Article  PubMed  CAS  Google Scholar 

  43. Manjer J, Andersson I, Berglund G, Bondesson L, Garne JP, Janzon L, Malina J, Matson S (2000) Survival of women with breast cancer in relation to smoking. Eur J Surg 166(11):852–858. doi:10.1080/110241500447227

    Article  PubMed  CAS  Google Scholar 

  44. Ambrosone CB, Freudenheim JL, Graham S, Marshall JR, Vena JE, Brasure JR, Michalek AM, Laughlin R, Nemoto T, Gillenwater KA, Shields PG (1996) Cigarette smoking, N-acetyltransferase 2 genetic polymorphisms, and breast cancer risk. JAMA 276(18):1494–1501

    Article  PubMed  CAS  Google Scholar 

  45. Morabia A, Bernstein MS, Bouchardy I, Kurtz J, Morris MA (2000) Breast cancer and active and passive smoking: the role of the N-acetyltransferase 2 genotype. Am J Epidemiol 152(3):226–232

    Article  PubMed  CAS  Google Scholar 

  46. Murin S, Inciardi J (2001) Cigarette smoking and the risk of pulmonary metastasis from breast cancer. Chest 119(6):1635–1640

    Article  PubMed  CAS  Google Scholar 

  47. Daniell HW (1988) Increased lymph node metastases at mastectomy for breast cancer associated with host obesity, cigarette smoking, age, and large tumor size. Cancer 62(2):429–435

    Article  PubMed  CAS  Google Scholar 

  48. Daniell HW (1980) Estrogen receptors, breast cancer, and smoking. N Engl J Med 302(26):1478

    PubMed  CAS  Google Scholar 

  49. Daniell HW, Tam E, Filice A (1993) Larger axillary metastases in obese women and smokers with breast cancer—an influence by host factors on early tumor behavior. Breast Cancer Res Treat 25(3):193–201

    Article  PubMed  CAS  Google Scholar 

  50. Abramowitz MC, Li T, Morrow M, Anderson PR, Bleicher RJ, Goldstein LJ, Swaby R, Nicoloau N, Freedman GM (2010) History of smoking is associated with younger age at diagnosis of breast cancer. Breast J. doi:10.1111/j.1524-4741.2010.00921.x

    PubMed  Google Scholar 

  51. Manjer J, Malina J, Berglund G, Bondeson L, Garne JP, Janzon L (2001) Smoking associated with hormone receptor negative breast cancer. Int J Cancer 91(4):580–584. doi: 10.1002/1097-0215(200002)9999:9999<::AID-IJC1091>3.0.CO;2-V

    Article  PubMed  CAS  Google Scholar 

  52. Scanlon EF, Suh O, Murthy SM, Mettlin C, Reid SE, Cummings KM (1995) Influence of smoking on the development of lung metastases from breast cancer. Cancer 75(11):2693–2699

    Article  PubMed  CAS  Google Scholar 

  53. Lilla C, Ambrosone CB, Kropp S, Helmbold I, Schmezer P, von Fournier D, Haase W, Sautter-Bihl ML, Wenz F, Chang-Claude J (2007) Predictive factors for late normal tissue complications following radiotherapy for breast cancer. Breast Cancer Res Treat 106(1):143–150. doi:10.1007/s10549-006-9480-9

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by Grant# KG110940 from Susan G. Komen for the Cure and by Grant# 121891-MRSG-12-007-01-CPHPS from the American Cancer Society. Additional support was obtained from the National Institutes of Health, National Cancer Institute, Bay Area Breast Cancer SPORE (P50 CA 58207). The data were derived from the Life after Cancer Epidemiology (LACE) study, which is supported by the National Cancer Institute (RO1 CA129059-05 to B. J. Caan). We thank Dr. Stanton Glantz for helpful comments on an earlier draft of this manuscript.

Conflict of interest

The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript. The authors have no further financial relationship with the funders. The authors have full control of all primary data and the Journal may review the data if requested.

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Correspondence to Dejana Braithwaite.

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Braithwaite, D., Izano, M., Moore, D.H. et al. Smoking and survival after breast cancer diagnosis: a prospective observational study and systematic review. Breast Cancer Res Treat 136, 521–533 (2012). https://doi.org/10.1007/s10549-012-2276-1

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