Mendelian randomisation study of smoking exposure in relation to breast cancer risk.
Journal
British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
03
08
2020
accepted:
28
04
2021
revised:
14
04
2021
pubmed:
4
8
2021
medline:
18
12
2021
entrez:
3
8
2021
Statut:
ppublish
Résumé
Despite a modest association between tobacco smoking and breast cancer risk reported by recent epidemiological studies, it is still equivocal whether smoking is causally related to breast cancer risk. We applied Mendelian randomisation (MR) to evaluate a potential causal effect of cigarette smoking on breast cancer risk. Both individual-level data as well as summary statistics for 164 single-nucleotide polymorphisms (SNPs) reported in genome-wide association studies of lifetime smoking index (LSI) or cigarette per day (CPD) were used to obtain MR effect estimates. Data from 108,420 invasive breast cancer cases and 87,681 controls were used for the LSI analysis and for the CPD analysis conducted among ever-smokers from 26,147 cancer cases and 26,072 controls. Sensitivity analyses were conducted to address pleiotropy. Genetically predicted LSI was associated with increased breast cancer risk (OR 1.18 per SD, 95% CI: 1.07-1.30, P = 0.11 × 10 Our MR study provides supportive evidence for a potential causal association with breast cancer risk for lifetime smoking exposure but not cigarettes per day among smokers.
Sections du résumé
BACKGROUND
Despite a modest association between tobacco smoking and breast cancer risk reported by recent epidemiological studies, it is still equivocal whether smoking is causally related to breast cancer risk.
METHODS
We applied Mendelian randomisation (MR) to evaluate a potential causal effect of cigarette smoking on breast cancer risk. Both individual-level data as well as summary statistics for 164 single-nucleotide polymorphisms (SNPs) reported in genome-wide association studies of lifetime smoking index (LSI) or cigarette per day (CPD) were used to obtain MR effect estimates. Data from 108,420 invasive breast cancer cases and 87,681 controls were used for the LSI analysis and for the CPD analysis conducted among ever-smokers from 26,147 cancer cases and 26,072 controls. Sensitivity analyses were conducted to address pleiotropy.
RESULTS
Genetically predicted LSI was associated with increased breast cancer risk (OR 1.18 per SD, 95% CI: 1.07-1.30, P = 0.11 × 10
CONCLUSION
Our MR study provides supportive evidence for a potential causal association with breast cancer risk for lifetime smoking exposure but not cigarettes per day among smokers.
Identifiants
pubmed: 34341517
doi: 10.1038/s41416-021-01432-8
pii: 10.1038/s41416-021-01432-8
pmc: PMC8505411
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1135-1145Subventions
Organisme : Medical Research Council
ID : MC_UU_00004/02
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 29186
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N003284/1
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P50 CA058223
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : Medical Research Council
ID : G0401527
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 14136
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P30 CA015083
Pays : United States
Organisme : Medical Research Council
ID : G1000143
Pays : United Kingdom
Investigateurs
Anne-Lise Børresen-Dale
(AL)
Grethe I Grenaker Alnæs
(GI)
Kristine K Sahlberg
(KK)
Lars Ottestad
(L)
Rolf Kåresen
(R)
Ellen Schlichting
(E)
Marit Muri Holmen
(MM)
Toril Sauer
(T)
Vilde Haakensen
(V)
Olav Engebråten
(O)
Bjørn Naume
(B)
Alexander Fosså
(A)
Cecile E Kiserud
(CE)
Kristin V Reinertsen
(KV)
Åslaug Helland
(Å)
Margit Riis
(M)
Jürgen Geisler
(J)
Christine Clarke
(C)
Deborah Marsh
(D)
Rodney Scott
(R)
Robert Baxter
(R)
Desmond Yip
(D)
Jane Carpenter
(J)
Alison Davis
(A)
Nirmala Pathmanathan
(N)
Peter Simpson
(P)
Dinny Graham
(D)
Mythily Sachchithananthan
(M)
David Amor
(D)
Lesley Andrews
(L)
Yoland Antill
(Y)
Rosemary Balleine
(R)
Jonathan Beesley
(J)
Ian Bennett
(I)
Michael Bogwitz
(M)
Leon Botes
(L)
Meagan Brennan
(M)
Melissa Brown
(M)
Michael Buckley
(M)
Jo Burke
(J)
Phyllis Butow
(P)
Liz Caldon
(L)
Ian Campbell
(I)
Deepa Chauhan
(D)
Manisha Chauhan
(M)
Georgia Chenevix-Trench
(G)
Alice Christian
(A)
Paul Cohen
(P)
Alison Colley
(A)
Ashley Crook
(A)
James Cui
(J)
Margaret Cummings
(M)
Sarah-Jane Dawson
(SJ)
Anna DeFazio
(A)
Martin Delatycki
(M)
Rebecca Dickson
(R)
Joanne Dixon
(J)
Ted Edkins
(T)
Stacey Edwards
(S)
Gelareh Farshid
(G)
Andrew Fellows
(A)
Georgina Fenton
(G)
Michael Field
(M)
James Flanagan
(J)
Peter Fong
(P)
Laura Forrest
(L)
Stephen Fox
(S)
Juliet French
(J)
Michael Friedlander
(M)
Clara Gaff
(C)
Mike Gattas
(M)
Peter George
(P)
Sian Greening
(S)
Marion Harris
(M)
Stewart Hart
(S)
Nick Hayward
(N)
John Hopper
(J)
Cass Hoskins
(C)
Clare Hunt
(C)
Paul James
(P)
Mark Jenkins
(M)
Alexa Kidd
(A)
Judy Kirk
(J)
Jessica Koehler
(J)
James Kollias
(J)
Sunil Lakhani
(S)
Mitchell Lawrence
(M)
Geoff Lindeman
(G)
Lara Lipton
(L)
Liz Lobb
(L)
Graham Mann
(G)
Deborah Marsh
(D)
Sue Anne McLachlan
(SA)
Bettina Meiser
(B)
Roger Milne
(R)
Sophie Nightingale
(S)
Shona O'Connell
(S)
Sarah O'Sullivan
(S)
David Gallego Ortega
(DG)
Nick Pachter
(N)
Briony Patterson
(B)
Amy Pearn
(A)
Kelly Phillips
(K)
Ellen Pieper
(E)
Edwina Rickard
(E)
Bridget Robinson
(B)
Mona Saleh
(M)
Elizabeth Salisbury
(E)
Christobel Saunders
(C)
Jodi Saunus
(J)
Rodney Scott
(R)
Clare Scott
(C)
Adrienne Sexton
(A)
Andrew Shelling
(A)
Peter Simpson
(P)
Melissa Southey
(M)
Amanda Spurdle
(A)
Jessica Taylor
(J)
Renea Taylor
(R)
Heather Thorne
(H)
Alison Trainer
(A)
Kathy Tucker
(K)
Jane Visvader
(J)
Logan Walker
(L)
Rachael Williams
(R)
Ingrid Winship
(I)
Mary Ann Young
(MA)
Informations de copyright
© 2021. The Author(s).
Références
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A. & Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394–424 (2018).
pubmed: 30207593
doi: 10.3322/caac.21492
Tobacco smoke and involuntary smoking, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 83, 1–1438 (2004).
Centers for Disease C, Prevention, National Center for Chronic Disease P, Health P, Office on S, Health. Publications and reports of the surgeon general. in How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General Centers for Disease Control and Prevention (US): Atlanta (GA) (2010).
Hecht, S. S. Tobacco smoke carcinogens and breast cancer. Environ. Mol. Mutagen. 39, 119–126 (2002).
pubmed: 11921179
doi: 10.1002/em.10071
Petrakis, N. L., Gruenke, L. D., Beelen, T. C., Castagnoli, N. Jr. & Craig, J. C. Nicotine in breast fluid of nonlactating women. Science 199, 303–305 (1978).
pubmed: 619458
doi: 10.1126/science.619458
Petrakis, N. L., Maack, C. A., Lee, R. E. & Lyon, M. Mutagenic activity in nipple aspirates of human breast fluid. Cancer Res. 40, 188–189 (1980).
pubmed: 7349898
Conway, K., Edmiston, S. N., Cui, L., Drouin, S. S., Pang, J., He, M. et al. Prevalence and spectrum of p53 mutations associated with smoking in breast cancer. Cancer Res. 62, 1987–1995 (2002).
pubmed: 11929815
Li, D., Zhang, W., Sahin, A. A. & Hittelman, W. N. DNA adducts in normal tissue adjacent to breast cancer: a review. Cancer Detect. Prev. 23, 454–462 (1999).
pubmed: 10571655
doi: 10.1046/j.1525-1500.1999.99059.x
Rundle, A., Tang, D., Hibshoosh, H., Estabrook, A., Schnabel, F., Cao, W. et al. The relationship between genetic damage from polycyclic aromatic hydrocarbons in breast tissue and breast cancer. Carcinogenesis 21, 1281–1289 (2000).
pubmed: 10874004
doi: 10.1093/carcin/21.7.1281
Warren, G. W., Alberg, A. J., Kraft, A. S. & Cummings, K. M. The 2014 Surgeon General’s report: “the health consequences of smoking–50 years of progress”: a paradigm shift in cancer care. Cancer 120, 1914–1916 (2014).
pubmed: 24687615
doi: 10.1002/cncr.28695
Band, P. R., Le, N. D., Fang, R. & Deschamps, M. Carcinogenic and endocrine disrupting effects of cigarette smoke and risk of breast cancer. Lancet 360, 1044–1049 (2002).
pubmed: 12383984
doi: 10.1016/S0140-6736(02)11140-8
Clemons, M. & Goss, P. Estrogen and the risk of breast cancer. New Engl. J. Med. 344, 276–285 (2001).
pubmed: 11172156
doi: 10.1056/NEJM200101253440407
Gaudet, M. M., Carter, B. D., Brinton, L. A., Falk, R. T., Gram, I. T., Luo, J. et al. Pooled analysis of active cigarette smoking and invasive breast cancer risk in 14 cohort studies. Int. J. Epidemiol. 46, 881–893 (2017).
pubmed: 28031315
Smith, G. D. & Ebrahim, S. ‘Mendelian randomization’: can genetic epidemiology contribute to understanding environmental determinants of disease? Int. J. Epidemiol. 32, 1–22 (2003).
pubmed: 12689998
doi: 10.1093/ije/dyg070
Evans, D. M. & Davey Smith, G. Mendelian randomization: new applications in the coming age of hypothesis-free causality. Annu. Rev. Genomics Hum. Genet. 16, 327–350 (2015).
pubmed: 25939054
doi: 10.1146/annurev-genom-090314-050016
Burgess, S., Bowden, J., Fall, T., Ingelsson, E. & Thompson, S. G. Sensitivity analyses for robust causal inference from mendelian randomization analyses with multiple genetic variants. Epidemiology 28, 30–42 (2017).
pubmed: 27749700
doi: 10.1097/EDE.0000000000000559
Michailidou, K., Lindstrom, S., Dennis, J., Beesley, J., Hui, S., Kar, S. et al. Association analysis identifies 65 new breast cancer risk loci. Nature 551, 92–94 (2017).
pubmed: 29059683
pmcid: 5798588
doi: 10.1038/nature24284
Michailidou, K., Hall, P., Gonzalez-Neira, A., Ghoussaini, M., Dennis, J., Milne, R. L. et al. Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Nat. Genet. 45, 353–361 (2013).
pubmed: 23535729
pmcid: 3771688
doi: 10.1038/ng.2563
Howie, B., Fuchsberger, C., Stephens, M., Marchini, J. & Abecasis, G. R. Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat. Genet. 44, 955–959 (2012).
pubmed: 22820512
pmcid: 3696580
doi: 10.1038/ng.2354
Wootton, R. E., Richmond, R. C., Stuijfzand, B. G., Lawn, R. B., Sallis, H. M., Taylor, G. M. J. et al. Evidence for causal effects of lifetime smoking on risk for depression and schizophrenia: a Mendelian randomisation study. Psychol Med, 50, 2435–2443 (2020).
pubmed: 31689377
doi: 10.1017/S0033291719002678
Liu, M., Jiang, Y., Wedow, R., Li, Y., Brazel, D. M., Chen, F. et al. Association studies of up to 1.2 million individuals yield new insights into the genetic etiology of tobacco and alcohol use. Nat. Genet. 51, 237–244 (2019).
pubmed: 30643251
pmcid: 6358542
doi: 10.1038/s41588-018-0307-5
Zhou, W., Liu, G., Hung, R. J., Haycock, P. C., Aldrich, M. C., Andrew, A. S. et al. Causal relationships between body mass index, smoking and lung cancer: univariable and multivariable Mendelian randomization. Int. J. Cancer https://doi.org/10.1002/ijc.33292 (2020).
doi: 10.1002/ijc.33292
pubmed: 33245569
pmcid: 8048589
Dumitrescu, R. G. & Shields, P. G. The etiology of alcohol-induced breast cancer. Alcohol 35, 213–225 (2005).
pubmed: 16054983
doi: 10.1016/j.alcohol.2005.04.005
Hamajima, N., Hirose, K., Tajima, K., Rohan, T., Calle, E. E., Heath, C. W. Jr. et al. 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 (2002).
pubmed: 12439712
doi: 10.1038/sj.bjc.6600596
Moore, A. A., Gould, R., Reuben, D. B., Greendale, G. A., Carter, M. K., Zhou, K. et al. Longitudinal patterns and predictors of alcohol consumption in the United States. Am. J. Public Health 95, 458–465 (2005).
pubmed: 15727977
pmcid: 1449202
doi: 10.2105/AJPH.2003.019471
Brion, M. J., Shakhbazov, K. & Visscher, P. M. Calculating statistical power in Mendelian randomization studies. Int. J. Epidemiol. 42, 1497–1501 (2013).
pubmed: 24159078
doi: 10.1093/ije/dyt179
Mavaddat, N., Michailidou, K., Dennis, J., Lush, M., Fachal, L., Lee, A. et al. Polygenic risk scores for prediction of breast cancer and breast cancer subtypes. Am. J. Hum. Genet. 104, 21–34 (2019).
pubmed: 30554720
doi: 10.1016/j.ajhg.2018.11.002
Lawlor, D. A., Tilling, K. & Davey Smith, G. Triangulation in aetiological epidemiology. Int. J. Epidemiol. 45, 1866–1886 (2016).
pubmed: 28108528
Bowden, J., Davey Smith, G. & Burgess, S. Mendelian randomization with invalid instruments: effect estimation and bias detection through Egger regression. Int. J. Epidemiol. 44, 512–525 (2015).
pubmed: 26050253
pmcid: 4469799
doi: 10.1093/ije/dyv080
Bowden, J., Davey Smith, G., Haycock, P. C. & Burgess, S. Consistent estimation in Mendelian randomization with some invalid instruments using a weighted median estimator. Genetic Epidemiol. 40, 304–314 (2016).
doi: 10.1002/gepi.21965
Hartwig, F. P., Davey Smith, G. & Bowden, J. Robust inference in summary data Mendelian randomization via the zero modal pleiotropy assumption. Int. J. Epidemiol. 46, 1985–1998 (2017).
pubmed: 29040600
pmcid: 5837715
doi: 10.1093/ije/dyx102
Zhao, Q., Wang, J., Hemani, G., Bowden, J. & Small, D. Statistical inference in two-sample summary-data Mendelian randomization using robust adjusted profile score. Annals of Statistics, 48, 1742–1769 (2020).
doi: 10.1214/19-AOS1866
Burgess, S., Butterworth, A. & Thompson, S. G. Mendelian randomization analysis with multiple genetic variants using summarized data. Genetic Epidemiol. 37, 658–665 (2013).
doi: 10.1002/gepi.21758
Sanderson, E., Davey Smith, G., Windmeijer, F. & Bowden, J. An examination of multivariable Mendelian randomization in the single-sample and two-sample summary data settings. Int. J. Epidemiol. 48, 713–727 (2019).
pubmed: 30535378
doi: 10.1093/ije/dyy262
Pulit, S. L., Stoneman, C., Morris, A. P., Wood, A. R., Glastonbury, C. A., Tyrrell, J. et al. Meta-analysis of genome-wide association studies for body fat distribution in 694 649 individuals of European ancestry. Hum. Mol. Genet. 28, 166–174 (2019).
pubmed: 30239722
doi: 10.1093/hmg/ddy327
Lee, J. J., Wedow, R., Okbay, A., Kong, E., Maghzian, O., Zacher, M. et al. Gene discovery and polygenic prediction from a genome-wide association study of educational attainment in 1.1 million individuals. Nat. Genet. 50, 1112–1121 (2018).
pubmed: 30038396
pmcid: 6393768
doi: 10.1038/s41588-018-0147-3
Haycock, P. C., Burgess, S., Wade, K. H., Bowden, J., Relton, C. & Davey Smith, G. Best (but oft-forgotten) practices: the design, analysis, and interpretation of Mendelian randomization studies. Am. J. Clin. Nutr. 103, 965–978 (2016).
pubmed: 26961927
pmcid: 4807699
doi: 10.3945/ajcn.115.118216
Verbanck, M., Chen, C. Y., Neale, B. & Do, R. Detection of widespread horizontal pleiotropy in causal relationships inferred from Mendelian randomization between complex traits and diseases. Nat. Genet. 50, 693–698 (2018).
pubmed: 29686387
pmcid: 6083837
doi: 10.1038/s41588-018-0099-7
Larsson, S. C., Carter, P., Kar, S., Vithayathil, M., Mason, A. M., Michaëlsson, K. et al. Smoking, alcohol consumption, and cancer: a Mendelian randomisation study in UK Biobank and international genetic consortia participants. PLoS Med. 17, e1003178–e1003178 (2020).
pubmed: 32701947
pmcid: 7377370
doi: 10.1371/journal.pmed.1003178
Russo, J., Hu, Y. F., Yang, X. & Russo, I. H. Developmental, cellular, and molecular basis of human breast cancer. J. Natl Cancer Inst. Monographs. 27, 17–37 (2000).
doi: 10.1093/oxfordjournals.jncimonographs.a024241
Dossus, L., Boutron-Ruault, M., Kaaks, R., Gram, I., Vilier, A., Fervers, B. et al. Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int. J. Cancer 134, 1871–1888 (2014).
pubmed: 24590452
doi: 10.1002/ijc.28508
Gram, I. T., Little, M. A., Lund, E. & Braaten, T. The fraction of breast cancer attributable to smoking: the Norwegian women and cancer study 1991–2012. Br. J. Cancer 115, 616–623 (2016).
pubmed: 27280631
pmcid: 4997535
doi: 10.1038/bjc.2016.154
Gram, I. T., Park, S. Y., Kolonel, L. N., Maskarinec, G., Wilkens, L. R., Henderson, B. E. et al. 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 (2015).
pubmed: 26493265
pmcid: 4836396
doi: 10.1093/aje/kwv092
Gaudet, M. M., Gapstur, S. M., Sun, J., Diver, W. R., Hannan, L. M. & Thun, M. J. Active smoking and breast cancer risk: original cohort data and meta-analysis. J. Natl Cancer Inst. 105, 515–525 (2013).
pubmed: 23449445
doi: 10.1093/jnci/djt023
Catsburg, C., Miller, A. B. & Rohan, T. E. Active cigarette smoking and risk of breast cancer. Int. J. Cancer 136, 2204–2209 (2015).
pubmed: 25307527
doi: 10.1002/ijc.29266
Rosenberg, L., Boggs, D. A., Bethea, T. N., Wise, L. A., Adams-Campbell, L. L. & Palmer, J. R. A prospective study of smoking and breast cancer risk among African-American women. Cancer Causes Control 24, 2207–2215 (2013).
pubmed: 24085586
doi: 10.1007/s10552-013-0298-6
Egan, K. M., Stampfer, M. J., Hunter, D., Hankinson, S., Rosner, B. A., Holmes, M. et al. Active and passive smoking in breast cancer: prospective results from the Nurses’ Health Study. Epidemiology 13, 138–145 (2002).
pubmed: 11880753
doi: 10.1097/00001648-200203000-00007
Terry, P. D. & Rohan, T. E. Cigarette smoking and the risk of breast cancer in women: a review of the literature. Cancer Epidemiol. Biomark. Prev. 11, 953–971 (2002).
World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Diet, nutrition, physical activity and breast cacner. Avaiable at https://dietandcancerreport.org .