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.
Similar content being viewed by others
References
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
Daniell HW (1995) A worse prognosis for smokers with prostate cancer. J Urol 154(1):153–157
Myers RP (1995) Prostate cancer–neurovascular preservation; smoking cessation may enhance prognosis? J Urol 154(1):158–159
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
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
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
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
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
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
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
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
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
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
Bradley CJ, Given CW, Roberts C (2002) Race, socioeconomic status, and breast cancer treatment and survival. J Natl Cancer Inst 94(7):490–496
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
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
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
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
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
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
Wells AJ (1991) Breast cancer, cigarette smoking, and passive smoking. Am J Epidemiol 133(2):208–210
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
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
Hiatt RA, Fireman BH (1986) Smoking, menopause, and breast cancer. J Natl Cancer Inst 76(5):833–838
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
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
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
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
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
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
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
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
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
Fleming ID, Cooper JS, Henson DE (1997) AJCC cancer staging manual, 5th edn. Lippincott-Raven, New York
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
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
Greenland S (1989) Modeling and variable selection in epidemiologic analysis. Am J Public Health 79(3):340–349
Cox DR, Oakes D (1994) Analysis of survival data. Monographs in statistics and applied probability 21. Chapman & Hill, New York
Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Statistics for Biology and Health. Springer, New York
Prentice RL, Kalbfleisch JD (1979) Hazard rate models with covariates. Biometrics 35:25–39
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
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
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
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
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
Murin S, Inciardi J (2001) Cigarette smoking and the risk of pulmonary metastasis from breast cancer. Chest 119(6):1635–1640
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
Daniell HW (1980) Estrogen receptors, breast cancer, and smoking. N Engl J Med 302(26):1478
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
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-012-2276-1