Breast Cancer Research and Treatment

, Volume 154, Issue 2, pp 213–224 | Cite as

Active and passive smoking and risk of breast cancer: a meta-analysis

  • Alina Macacu
  • Philippe Autier
  • Mathieu Boniol
  • Peter Boyle
Review

Abstract

Studies on active and passive tobacco smoking and breast cancer have found inconsistent results. A meta-analysis of observational studies on tobacco smoking and breast cancer occurrence was conducted based on systematic searches for studies with retrospective (case–control) and prospective (cohort) designs. Eligible studies were identified, and relative risk measurements were extracted for active and passive tobacco exposures. Random-effects meta-analyses were used to compute summary relative risks (SRR). Heterogeneity of results between studies was evaluated using the (I2) statistics. For ever active smoking, in 27 prospective studies, the SRR for breast cancer was 1.10 (95 % CI [1.09–1.12]) with no heterogeneity (I2 = 0 %). In 44 retrospective studies, the SRR was 1.08 (95 % CI [1.02–1.14]) with high heterogeneity (I2 = 59 %). SRRs for current active smoking were 1.13 (95 % CI [1.09–1.17]) in 27 prospective studies and 1.08 (95 % CI [0.97–1.20]) in 22 retrospective studies. The results were stable across different subgroup analyses, notably pre/post-menopause, alcohol consumption adjustments, including/excluding passive smokers from the referent group. For ever passive smoking, in 11 prospective studies, the SRR for breast cancer was 1.07 (95 % CI [1.02–1.13]) with no heterogeneity (I2 = 1 %). In 20 retrospective studies, the SRR was 1.30 (95 % CI [1.10–1.54]) with high heterogeneity (I2 = 74 %). Too few prospective studies were available for meaningful subgroup analyses. There is consistent evidence for a moderate increase in the risk of breast cancer in women who smoke tobacco. The evidence for a moderate increase in risk with passive smoking is more substantial than a few years ago.

Keywords

Breast cancer Environmental tobacco smoke Smoking Meta-analysis 

Supplementary material

10549_2015_3628_MOESM1_ESM.pdf (566 kb)
Supplementary material 1 (PDF 566 kb)

References

  1. 1.
    Al-Delaimy WK, Cho E, Chen WY, Colditz G, Willet WC (2004) A prospective study of smoking and risk of breast cancer in young adult women. Cancer Epidemiol Biomarkers Prev 13:398–404PubMedGoogle Scholar
  2. 2.
    Aune D, Greenwood DC, Chan DS, Vieira R, Vieira AR, Navarro Rosenblatt DA, Cade JE, Burley VJ, Norat T (2012) Body mass index, abdominal fatness and pancreatic cancer risk: a systematic review and non-linear dose–response meta-analysis of prospective studies. Ann Oncol 23:843–852. doi:10.1093/annonc/mdr398 CrossRefPubMedGoogle Scholar
  3. 3.
    Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101CrossRefPubMedGoogle Scholar
  4. 4.
    Bjerkaas E, Parajuli R, Weiderpass E, Engeland A, Maskarinec G, Selmer R, Gram IT (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. doi:10.1007/s10552-013-0213-1 PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Boyle P, Gray N, Henningfield J, Seffrin J, Zatoński W (2010) Tobacco: science, policy and public health, 2nd edn. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. 6.
    Brown LM, Gridley G, Wu AH, Falk RT, Hauptmann M, Kolonel LN, West DW, Nomura AM, Pike MC, Hoover RN, Ziegler RG (2010) Low level alcohol intake, cigarette smoking and risk of breast cancer in Asian–American women. Breast Cancer Res Treat 120:203–210. doi:10.1007/s10549-009-0464-4 PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Catsburg C, Kirsh VA, Soskolne CL, Kreiger N, Rohan TE (2014) Active cigarette smoking and the risk of breast cancer: a cohort study. Cancer Epidemiol 38:376–381. doi:10.1016/j.canep.2014.05.007 CrossRefPubMedGoogle Scholar
  8. 8.
    Catsburg C, Miller AB, Rohan TE (2015) Active cigarette smoking and risk of breast cancer. Int J Cancer 136:2204–2209. doi:10.1002/ijc.29266 CrossRefPubMedGoogle Scholar
  9. 9.
    Collishaw NE, Boyd NF, Cantor KP, Hammond SK, Johnson KC, MIllar J, Miller AB, MIller M, Palmer JR, Salmon AG, Turcotte F (2009) Canadian expert panel on tobacco smoke and breast cancer risk., OTRU special report seriesOntario Tobacco Research Unit, TorontoGoogle Scholar
  10. 10.
    Cox DG, Dostal L, Hunter DJ, Le Marchand L, Hoover R, Ziegler RG, Thun MJ, Breast Prostate Cancer, Cohort C (2011) N-acetyltransferase 2 polymorphisms, tobacco smoking, and breast cancer risk in the breast and prostate cancer cohort consortium. Am J Epidemiol 174:1316–1322. doi:10.1093/aje/kwr257 PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M, Comparative Risk Assessment collaborating (2005) Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 366:1784–1793. doi:10.1016/S0140-6736(05)67725-2 CrossRefPubMedGoogle Scholar
  12. 12.
    Dossus L, Boutron-Ruault MC, Kaaks R, Gram IT, Vilier A, Fervers B, Manjer J, Tjonneland A, Olsen A, Overvad K, Chang-Claude J, Boeing H, Steffen A, Trichopoulou A, Lagiou P, Sarantopoulou M, Palli D, Berrino F, Tumino R, Vineis P, Mattiello A, Bueno-de-Mesquita HB, van Duijnhoven FJ, Bakker MF, Peeters PH, Weiderpass E, Bjerkaas E, Braaten T, Menendez V, Agudo A, Sanchez MJ, Amiano P, Tormo MJ, Barricarte A, Butt S, Khaw KT, Wareham N, Key TJ, Travis RC, Rinaldi S, McCormack V, Romieu I, Cox DG, Norat T, Riboli E, Clavel-Chapelon F (2014) Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int J Cancer 134:1871–1888. doi:10.1002/ijc.28508 CrossRefPubMedGoogle Scholar
  13. 13.
    Dumitrescu RG, Shields PG (2005) The etiology of alcohol-induced breast cancer. Alcohol 35:213–225. doi:10.1016/j.alcohol.2005.04.005 CrossRefPubMedGoogle Scholar
  14. 14.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Ferlay J, Soerjomataram I, Ervik M, Dikshit RP, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2012) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 In: International Agency for Research on Cancer, Lyon, FranceGoogle Scholar
  16. 16.
    Gram IT, Braaten T, Terry PD, Sasco AJ, Adami HO, Lund E, Weiderpass E (2005) Breast cancer risk among women who start smoking as teenagers. Cancer Epidemiol Biomarkers Prev 14:61–66PubMedGoogle Scholar
  17. 17.
    Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309PubMedGoogle Scholar
  18. 18.
    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 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. doi:10.1038/sj.bjc.6600596 CrossRefPubMedGoogle Scholar
  19. 19.
    Hartung J, Knapp G (2001) A refined method for the meta-analysis of controlled clinical trials with binary outcome. Stat Med 20:3875–3889CrossRefPubMedGoogle Scholar
  20. 20.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558. doi:10.1002/sim.1186 CrossRefPubMedGoogle Scholar
  21. 21.
    IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2004) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol 83., Tobacco smoke and involuntary smokingWorld Health Organization, International Agency for Research on Cancer, LyonGoogle Scholar
  22. 22.
    International Agency for Research on Cancer (2009) A review of human carcinogens. Part E: Personal habits and indoor combustions. Lyon, FranceGoogle Scholar
  23. 23.
    Johnson KC (2005) Accumulating evidence on passive and active smoking and breast cancer risk. Int J Cancer 117:619–628. doi:10.1002/ijc.21150 CrossRefPubMedGoogle Scholar
  24. 24.
    Johnson KC, Wells AJ (2002) Active and passive smoking in breast cancer. Epidemiology 13:745–746. doi:10.1097/01.ede.0000032423.06738.c4 CrossRefPubMedGoogle Scholar
  25. 25.
    Khuder SA, Simon VJ Jr (2000) Is there an association between passive smoking and breast cancer? Eur J Epidemiol 16:1117–1121CrossRefPubMedGoogle Scholar
  26. 26.
    Kropp S (2002) Active and passive smoking and risk of breast cancer by age 50 Years among German Women. Am J Epidemiol 156:616–626. doi:10.1093/aje/kwf093 CrossRefPubMedGoogle Scholar
  27. 27.
    Land SR, Liu Q, Wickerham DL, Costantino JP, Ganz PA (2014) Cigarette smoking, physical activity, and alcohol consumption as predictors of cancer incidence among women at high risk of breast cancer in the NSABP P-1 trial. Cancer Epidemiol Biomarkers Prev 23:823–832. doi:10.1158/1055-9965.EPI-13-1105-T PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Liu L, Wu K, Lin X, Yin W, Zheng X, Tang X, Mu L, Hu Z, Wang J (2000) Passive smoking and other factors at different periods of life and breast cancer risk in chinese women who have never smoked—a case–control study in Chongqing, People’s Republic of China. Asian Pac J Cancer Prev 1:131–137PubMedGoogle Scholar
  29. 29.
    Luo J, Margolis KL, Wactawski-Wende J, Horn K, Messina C, Stefanick ML, Tindle HA, Tong E, Rohan TE (2011) Association of active and passive smoking with risk of breast cancer among postmenopausal women: a prospective cohort study. BMJ 342:d1016. doi:10.1136/bmj.d1016 PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Macaskill P, Walter SD, Irwig L (2001) A comparison of methods to detect publication bias in meta-analysis. Statist Med 20:641–654CrossRefGoogle Scholar
  31. 31.
    Manjer J, Johansson R, Lenner P (2004) Smoking is associated with postmenopausal breast cancer in women with high levels of estrogens. Int J Cancer 112:324–328. doi:10.1002/ijc.20409 CrossRefPubMedGoogle Scholar
  32. 32.
    Miller MD, Marty MA, Broadwin R, Johnson KC, Salmon AG, Winder B, Steinmaus C, California Environmental Protection A (2007) The association between exposure to environmental tobacco smoke and breast cancer: a review by the California Environmental Protection Agency. Prev Med 44:93–106. doi:10.1016/j.ypmed.2006.08.015 CrossRefPubMedGoogle Scholar
  33. 33.
    Moore AA, Gould R, Reuben DB, Greendale GA, Carter MK, Zhou K, Karlamangla A (2005) Longitudinal patterns and predictors of alcohol consumption in the United States. Am J Public Health 95:458–465. doi:10.2105/AJPH.2003.019471 PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Nyante SJ, Gierach GL, Dallal CM, Freedman ND, Park Y, Danforth KN, Hollenbeck AR, Brinton LA (2014) Cigarette smoking and postmenopausal breast cancer risk in a prospective cohort. Br J Cancer 110:2339–2347. doi:10.1038/bjc.2014.132 PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Olson JE, Vachon CM, Vierkant RA, Sweeney C, Limburg PJ, Cerhan JR, Sellers TA (2005) Prepregnancy exposure to cigarette smoking and subsequent risk of postmenopausal breast cancer. Mayo Clin Proc 80:1423–1428. doi:10.4065/80.11.1423 CrossRefPubMedGoogle Scholar
  36. 36.
    Palmer JR, Rosenberg L (1993) Cigarette smoking and the risk of breast cancer. Epidemiol Rev 15:145–156PubMedGoogle Scholar
  37. 37.
    Prescott J, Ma H, Bernstein L, Ursin G (2007) Cigarette smoking is not associated with breast cancer risk in young women. Cancer Epidemiol Biomarkers Prev 16:620–622. doi:10.1158/1055-9965.EPI-06-0873 CrossRefPubMedGoogle Scholar
  38. 38.
    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. JNCI J Natl Cancer Inst 96:29–37. doi:10.1093/jnci/djh002 CrossRefPubMedGoogle Scholar
  39. 39.
    Roddam AW, Pirie K, Pike MC, Chilvers C, Crossley B, Hermon C, McPherson K, Peto J, Vessey M, Beral V (2007) Active and passive smoking and the risk of breast cancer in women aged 36–45 years: a population based case–control study in the UK. Br J Cancer 97:434–439. doi:10.1038/sj.bjc.6603859 PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Sanchez-Meca J, Marin-Martinez F (2008) Confidence intervals for the overall effect size in random-effects meta-analysis. Psychol Methods 13:31–48. doi:10.1037/1082-989X.13.1.31 CrossRefPubMedGoogle Scholar
  41. 41.
    Slattery ML, Curtin K, Giuliano AR, Sweeney C, Baumgartner R, Edwards S, Wolff RK, Baumgartner KB, Byers T (2008) Active and passive smoking, IL6, ESR1, and breast cancer risk. Breast Cancer Res Treat 109:101–111. doi:10.1007/s10549-007-9629-1 PubMedCentralCrossRefPubMedGoogle Scholar
  42. 42.
    Surgeon General (2014) Cancer. In: The health consequences of smoking—50 years of progressGoogle Scholar
  43. 43.
    Terry PD, Rohan TE (2002) Cigarette smoking and the risk of breast cancer in women: a review of the literature. Cancer Epidemiol Biomarkers Prev 11:953–971PubMedGoogle Scholar
  44. 44.
    van Houwelingen HC, Arends LR, Stijnen T (2002) Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 21:589–624CrossRefPubMedGoogle Scholar
  45. 45.
    Viechtbauer W (2005) Bias and efficiency of meta analytic variance estimators in the random effects model. J Educ Behav Stat 30:261–296CrossRefGoogle Scholar
  46. 46.
    Wells AJ (1991) Breast cancer, cigarette smoking, and passive smoking. Am J Epidemiol 133:208–210PubMedGoogle Scholar
  47. 47.
    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. doi:10.1001/archinternmed.2010.503 PubMedCentralPubMedGoogle Scholar
  48. 48.
    Young E, Leatherdale S, Sloan M, Kreiger N, Barisic A (2009) Age of smoking initiation and risk of breast cancer in a sample of Ontario women. Tob Induc Dis 5:4. doi:10.1186/1617-9625-5-4 PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Alina Macacu
    • 1
    • 3
  • Philippe Autier
    • 1
    • 2
  • Mathieu Boniol
    • 1
    • 2
  • Peter Boyle
    • 1
    • 2
  1. 1.International Prevention Research Institute (iPRI)LyonFrance
  2. 2.Strathclyde Institute of Global Public Health at iPRIEcully Ouest LyonFrance
  3. 3.International Prevention Research InstituteEcully Ouest LyonFrance

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