Smoking and alcohol by HPV status in head and neck cancer: a Mendelian randomization study.

Humans Mendelian Randomization Analysis Alcohol Drinking / adverse effects Head and Neck Neoplasms / virology Smoking / adverse effects Papillomavirus Infections / virology Squamous Cell Carcinoma of Head and Neck / virology Male Female Risk Factors Papillomaviridae / genetics Middle Aged Case-Control Studies Polymorphism, Single Nucleotide

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
07 Sep 2024
Historique:
received: 12 02 2024
accepted: 12 08 2024
medline: 8 9 2024
pubmed: 8 9 2024
entrez: 7 9 2024
Statut: epublish

Résumé

HPV-positive and HPV-negative head and neck squamous cell carcinoma (HNSCC) are recognized as distinct entities. There remains uncertainty surrounding the causal effects of smoking and alcohol on the development of these two cancer types. Here we perform multivariable Mendelian randomization (MR) to evaluate the causal effects of smoking and alcohol on the risk of HPV-positive and HPV-negative HNSCC in 3431 cases and 3469 controls. Lifetime smoking exposure, as measured by the Comprehensive Smoking Index (CSI), is associated with increased risk of both HPV-negative HNSCC (OR = 3.03, 95%CI:1.75-5.24, P = 7.00E-05) and HPV-positive HNSCC (OR = 2.73, 95%CI:1.39-5.36, P = 0.003). Drinks Per Week is also linked with increased risk of both HPV-negative HNSCC (OR = 7.72, 95%CI:3.63-16.4, P = 1.00E-07) and HPV-positive HNSCC (OR = 2.66, 95%CI:1.06-6.68, P = 0.038). Smoking and alcohol independently increase the risk of both HPV-positive and HPV-negative HNSCC. These findings have important implications for understanding the modifying risk factors between HNSCC subtypes.

Identifiants

DOI: 10.1038/s41467-024-51679-x PMID: 39244563
pubmed: 39244563
doi: 10.1038/s41467-024-51679-x
pii: 10.1038/s41467-024-51679-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7835

Informations de copyright

© 2024. The Author(s).

Références

Bray, F. et al. 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
Jethwa, A. R. & Khariwala, S. S. Tobacco-related carcinogenesis in head and neck cancer. Cancer Metastasis Rev. 36, 411–423 (2017).
pubmed: 28801840 pmcid: 5709040 doi: 10.1007/s10555-017-9689-6
Boffetta, P., Hecht, S., Gray, N., Gupta, P. & Straif, K. Smokeless tobacco and cancer. lancet Oncol. 9, 667–675 (2008).
pubmed: 18598931 doi: 10.1016/S1470-2045(08)70173-6
Gandini, S. et al. Tobacco smoking and cancer: a meta‐analysis. Int. J. Cancer 122, 155–164 (2008).
pubmed: 17893872 doi: 10.1002/ijc.23033
Hashibe, M. et al. Evidence for an important role of alcohol-and aldehyde-metabolizing genes in cancers of the upper aerodigestive tract. Cancer Epidemiol. Biomark. Prev. 15, 696–703 (2006).
doi: 10.1158/1055-9965.EPI-05-0710
Hashibe, M. et al. Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. J. Natl. Cancer Inst. 99, 777–789 (2007).
pubmed: 17505073 doi: 10.1093/jnci/djk179
Ang, K. K. et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N. Engl. J. Med. 363, 24–35 (2010).
pubmed: 20530316 pmcid: 2943767 doi: 10.1056/NEJMoa0912217
Elrefaey, S., Massaro, M., Chiocca, S., Chiesa, F. & Ansarin, M. HPV in oropharyngeal cancer: the basics to know in clinical practice. Acta Otorhinolaryngol. Italica 34, 299 (2014).
Fakhry, C. et al. Improved survival of patients with human papillomavirus–positive head and neck squamous cell carcinoma in a prospective clinical trial. J. Natl Cancer Inst. 100, 261–269 (2008).
pubmed: 18270337 doi: 10.1093/jnci/djn011
Kreimer, A. R. et al. Evaluation of human papillomavirus antibodies and risk of subsequent head and neck cancer. J. Clin. Oncol. 31, 2708 (2013).
pubmed: 23775966 pmcid: 3709056 doi: 10.1200/JCO.2012.47.2738
Lang Kuhs, K. A. et al. Human papillomavirus 16 E6 antibodies in individuals without diagnosed cancer: a pooled analysis. Cancer Epidemiol. Biomark. Prev. 24, 683–689 (2015).
doi: 10.1158/1055-9965.EPI-14-1217
Lydiatt, W. M. et al. Head and Neck cancers-major changes in the American Joint Committee on cancer eighth edition cancer staging manual. CA Cancer J. Clin. 67, 122–137 (2017).
pubmed: 28128848 doi: 10.3322/caac.21389
Anantharaman, D. et al. Combined effects of smoking and HPV16 in oropharyngeal cancer. Int. J. Epidemiol. 45, 752–761 (2016).
pubmed: 27197530 pmcid: 5841602 doi: 10.1093/ije/dyw069
Skoulakis, A. et al. Do smoking and human papilloma virus have a synergistic role in the development of head and neck cancer? A systematic review and meta-analysis. J. BUON 25, 1107–1115 (2020).
pubmed: 32521913
Arif, R. T., Mogaddam, M. A., Merdad, L. A. & Farsi, N. J. Does human papillomavirus modify the risk of oropharyngeal cancer related to smoking and alcohol drinking? A systematic review and meta-analysis. Laryngoscope Investig. Otolaryngol. 7, 1391–1401 (2022).
pubmed: 36258880 pmcid: 9575072 doi: 10.1002/lio2.877
Sanderson, E. et al. Mendelian randomization. Nat. Rev. Methods Prim. 2, 6 (2022).
doi: 10.1038/s43586-021-00092-5
de Leeuw, C., Savage, J., Bucur, I. G., Heskes, T. & Posthuma, D. Understanding the assumptions underlying Mendelian randomization. Eur. J. Hum. Genet. 30, 653–660 (2022).
pubmed: 35082398 pmcid: 9177700 doi: 10.1038/s41431-022-01038-5
Sanderson, E. Multivariable Mendelian randomization and mediation. Cold Spring Harb. Perspect. Med. 11, a038984 (2021).
pubmed: 32341063 pmcid: 7849347 doi: 10.1101/cshperspect.a038984
Auguste, A. et al. Joint effect of tobacco, alcohol, and oral HPV infection on head and neck cancer risk in the French West Indies. Cancer Med. 9, 6854–6863 (2020).
pubmed: 32750236 pmcid: 7520253 doi: 10.1002/cam4.3327
Liu, M. et al. Data related to 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).
Furberg, H. et al. Genome-wide meta-analyses identify multiple loci associated with smoking behavior. Nat. Genet. 42, 441–447 (2010).
doi: 10.1038/ng.571
Lesseur, C. et al. Genome-wide association analyses identify new susceptibility loci for oral cavity and pharyngeal cancer. Nat. Genet. 48, 1544–1550 (2016).
pubmed: 27749845 pmcid: 5131845 doi: 10.1038/ng.3685
Gormley, M. et al. A multivariable Mendelian randomization analysis investigating smoking and alcohol consumption in oral and oropharyngeal cancer. Nat. Commun. 11, 6071 (2020).
pubmed: 33247085 pmcid: 7695733 doi: 10.1038/s41467-020-19822-6
Karlsson Linnér, R. et al. Genome-wide association analyses of risk tolerance and risky behaviors in over 1 million individuals identify hundreds of loci and shared genetic influences. Nat. Genet. 51, 245–257 (2019).
pubmed: 30643258 doi: 10.1038/s41588-018-0309-3
Cogliano, V. J. et al. Preventable exposures associated with human cancers. J. Natl Cancer Inst. 103, 1827–1839 (2011).
pubmed: 22158127 pmcid: 3243677 doi: 10.1093/jnci/djr483
Hashibe, M. et al. Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. Cancer Epidemiol. Biomark. Prev. 18, 541–550 (2009).
doi: 10.1158/1055-9965.EPI-08-0347
Vineis, P. et al. Tobacco and cancer: recent epidemiological evidence. J. Natl Cancer Inst. 96, 99–106 (2004).
pubmed: 14734699 doi: 10.1093/jnci/djh014
Sturgis, E. M. & Ang, K. K. The epidemic of HPV-associated oropharyngeal cancer is here: is it time to change our treatment paradigms? J. Natl Compr. Canc Netw. 9, 665–673 (2011).
pubmed: 21636538 doi: 10.6004/jnccn.2011.0055
Eldridge, R. C. et al. Smoking and subsequent human papillomavirus infection: a mediation analysis. Ann. Epidemiol. 27, 724–730.e721 (2017).
pubmed: 29107447 pmcid: 5705255 doi: 10.1016/j.annepidem.2017.10.004
Sinha, P., Logan, H. L. & Mendenhall, W. M. Human papillomavirus, smoking, and head and neck cancer. Am. J. Otolaryngol. 33, 130–136 (2012).
pubmed: 21546122 doi: 10.1016/j.amjoto.2011.02.001
Rees, J. M., Foley, C. N. & Burgess, S. Factorial Mendelian randomization: using genetic variants to assess interactions. Int. J. Epidemiol. 49, 1147–1158 (2020).
pubmed: 31369124 doi: 10.1093/ije/dyz161
Ference, B. A., Majeed, F., Penumetcha, R., Flack, J. M. & Brook, R. D. Effect of naturally random allocation to lower low-density lipoprotein cholesterol on the risk of coronary heart disease mediated by polymorphisms in NPC1L1, HMGCR, or both: a 2× 2 factorial Mendelian randomization study. J. Am. Coll. Cardiol. 65, 1552–1561 (2015).
pubmed: 25770315 pmcid: 6101243 doi: 10.1016/j.jacc.2015.02.020
Ference, B. A. et al. Variation in PCSK9 and HMGCR and risk of cardiovascular disease and diabetes. N. Engl. J. Med. 375, 2144–2153 (2016).
pubmed: 27959767 doi: 10.1056/NEJMoa1604304
Davies, N. M., Holmes, M. V. & Davey Smith, G. Reading Mendelian randomisation studies: a guide, glossary, and checklist for clinicians. BMJ 362, k601 (2018).
pubmed: 30002074 pmcid: 6041728 doi: 10.1136/bmj.k601
Heck, J. E. et al. Sexual behaviours and the risk of head and neck cancers: a pooled analysis in the International Head and Neck Cancer Epidemiology (INHANCE) consortium. Int. J. Epidemiol. 39, 166–181 (2010).
pubmed: 20022926 doi: 10.1093/ije/dyp350
Gormley, M. et al. Investigating the effect of sexual behaviour on oropharyngeal cancer risk: a methodological assessment of Mendelian randomization. BMC Med. 20, 40 (2022).
pubmed: 35094705 pmcid: 8802428 doi: 10.1186/s12916-022-02233-3
Budhathoki, S. et al. A risk prediction model for head and neck cancers incorporating lifestyle factors, HPV serology and genetic markers. Int. J. Cancer 152, 2069–2080 (2023).
pubmed: 36694401 pmcid: 10006331 doi: 10.1002/ijc.34444
Castellsagué, X. et al. HPV involvement in head and neck cancers: comprehensive assessment of biomarkers in 3680 patients. J. Natl Cancer Inst. 108, djv403 (2016).
pubmed: 26823521 doi: 10.1093/jnci/djv403
Ferreiro-Iglesias, A. et al. Germline determinants of humoral immune response to HPV-16 protect against oropharyngeal cancer. Nat. Commun. 12, 5945 (2021).
pubmed: 34642315 pmcid: 8511029 doi: 10.1038/s41467-021-26151-9
Chi, A. C., Day, T. A. & Neville, B. W. Oral cavity and oropharyngeal squamous cell carcinoma–an update. CA Cancer J. Clin. 65, 401–421 (2015).
pubmed: 26215712 doi: 10.3322/caac.21293
Combes, J.-D. & Franceschi, S. Role of human papillomavirus in non-oropharyngeal head and neck cancers. Oral. Oncol. 50, 370–379 (2014).
pubmed: 24331868 doi: 10.1016/j.oraloncology.2013.11.004
Mirghani, H., Amen, F., Moreau, F. & Lacau St Guily, J. Do high-risk human papillomaviruses cause oral cavity squamous cell carcinoma? Oral. Oncol. 51, 229–236 (2015).
pubmed: 25488179 doi: 10.1016/j.oraloncology.2014.11.011
Consortium, O. Consortium launches genotyping effort. Cancer Discov. 3, 1321–1322 (2013).
Mailman, M. D. et al. The NCBI dbGaP database of genotypes and phenotypes. Nat. Genet. 39, 1181–1186 (2007).
pubmed: 17898773 pmcid: 2031016 doi: 10.1038/ng1007-1181
Wrayner, N. (Accessed 09/20/2021). Strand. Wellcome Centre for Human Genetics. https://www.well.ox.ac.uk/~wrayner/strand/ .
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 17701901 pmcid: 1950838 doi: 10.1086/519795
Patterson, N., Price, A. L. & Reich, D. Population Structure and Eigenanalysis. PLOS Genet. 2, e190 (2006).
pubmed: 17194218 pmcid: 1713260 doi: 10.1371/journal.pgen.0020190
Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).
pubmed: 16862161 doi: 10.1038/ng1847
Das, S. et al. Next-generation genotype imputation service and methods. Nat. Genet. 48, 1284–1287 (2016).
pubmed: 27571263 pmcid: 5157836 doi: 10.1038/ng.3656
Loh, P.-R. et al. Reference-based phasing using the Haplotype Reference Consortium panel. Nat. Genet. 48, 1443–1448 (2016).
pubmed: 27694958 pmcid: 5096458 doi: 10.1038/ng.3679
Fuchsberger, C., Abecasis, G. R. & Hinds, D. A. minimac2: faster genotype imputation. Bioinformatics 31, 782–784 (2015).
pubmed: 25338720 doi: 10.1093/bioinformatics/btu704
Leffondré, K., Abrahamowicz, M., Xiao, Y. & Siemiatycki, J. Modelling smoking history using a comprehensive smoking index: application to lung cancer. Stat. Med. 25, 4132–4146 (2006).
pubmed: 16998807 doi: 10.1002/sim.2680
Wootton, R. E. et al. Evidence for causal effects of lifetime smoking on risk for depression and schizophrenia: a Mendelian randomisation study. Psychol. Med. 50, 2435 (2020).
pubmed: 31689377 doi: 10.1017/S0033291719002678
Prentice, R. L., Vollmer, W. M. & Kalbfleisch, J. D. On the use of case series to identify disease risk factors. Biometrics 4, 445-458 (1984).
Hemani, G. et al. The MR-Base platform supports systematic causal inference across the human phenome. Elife 7, e34408 (2018).
pubmed: 29846171 pmcid: 5976434 doi: 10.7554/eLife.34408
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. Genet. Epidemiol. 40, 304–314 (2016).
pubmed: 27061298 pmcid: 4849733 doi: 10.1002/gepi.21965
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
Rees, J. M. B., Wood, A. M. & Burgess, S. Extending the MR-Egger method for multivariable Mendelian randomization to correct for both measured and unmeasured pleiotropy. Stat. Med. 36, 4705–4718 (2017).
pubmed: 28960498 pmcid: 5725762 doi: 10.1002/sim.7492
Burgess, S. & Thompson, S. G. Multivariable Mendelian randomization: the use of pleiotropic genetic variants to estimate causal effects. Am. J. Epidemiol. 181, 251–260 (2015).
pubmed: 25632051 pmcid: 4325677 doi: 10.1093/aje/kwu283
Mariosa, D. et al. Body size at different ages and risk of 6 cancers: a Mendelian randomization and prospective cohort study. J. Natl Cancer Inst. 114, 1296–1300 (2022).
pubmed: 35438160 pmcid: 9468294 doi: 10.1093/jnci/djac061
Sanderson, E., Spiller, W. & Bowden, J. Testing and correcting for weak and pleiotropic instruments in two‐sample multivariable Mendelian randomization. Stat. Med. 40, 5434–5452 (2021).
pubmed: 34338327 pmcid: 9479726 doi: 10.1002/sim.9133
Kleiber, C. & Zeileis, A. Applied econometrics with R. (Springer Science & Business Media, 2008).
Thrakal, A. et al. mrhnscc/MRHNSCC: v1 (Version v1). Zenodo. https://doi.org/10.5281/zenodo.12558118 (2024).

Auteurs

Abhinav Thakral (A)

Department of Biostatistics, Princess Margaret Cancer Centre-University Health Network, University of Toronto, Toronto, Ontario, Canada.

John Jw Lee (JJ)

Department of Otolaryngology-Head and Neck Surgery, University of Toronto, Toronto, Ontario, Canada. Jongwook.lee@utoronto.ca.
Department of Otolaryngology - Head and Neck Surgery, Sinai Health System, Toronto, Ontario, Canada. Jongwook.lee@utoronto.ca.
ORCID: 0000-0002-3364-9960

Tianzhichao Hou (T)

Department of Biostatistics, Princess Margaret Cancer Centre-University Health Network, University of Toronto, Toronto, Ontario, Canada.

Katrina Hueniken (K)

Department of Biostatistics, Princess Margaret Cancer Centre-University Health Network, University of Toronto, Toronto, Ontario, Canada.

Tom Dudding (T)

MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, BS8 1TL, UK.
University of Bristol Dental School, 1 Trinity Walk, Avon Street, Bristol, BS2 0PT, UK.
ORCID: 0000-0003-3756-040X

Mark Gormley (M)

MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, BS8 1TL, UK.
University of Bristol Dental School, 1 Trinity Walk, Avon Street, Bristol, BS2 0PT, UK.
ORCID: 0000-0001-5733-6304

Shama Virani (S)

Genomic Epidemiology Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.
ORCID: 0000-0002-1163-432X

Andrew Olshan (A)

Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, USA.

Brenda Diergaarde (B)

Department of Human Genetics, School of Public Health, University of Pittsburgh, and UPMC Hillman Cancer Center, Pittsburgh, PA, 15260, USA.

Andrew R Ness (AR)

University Hospitals Bristol and Weston NHS Foundation Trust National Institute for Health Research Bristol Biomedical Research Centre, University of Bristol, Bristol, BS1 3NU, UK.

Tim Waterboer (T)

Infections and Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
ORCID: 0000-0002-0616-6963

Karl Smith-Byrne (K)

Genomic Epidemiology Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.
ORCID: 0000-0002-1932-7463

Paul Brennan (P)

Genomic Epidemiology Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.

D Neil Hayes (DN)

Division of Medical Oncology and Center for Cancer Research, University of Tennessee Health Science Center, Memphis, TN, USA.
ORCID: 0000-0001-6203-7771

Eleanor Sanderson (E)

MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, BS8 1TL, UK.
ORCID: 0000-0001-5188-5775

M Catherine Brown (MC)

Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.
ORCID: 0000-0003-0184-7732

Sophie Huang (S)

Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.
Department of Radiation Oncology, University of Toronto, Toronto, Ontario, Canada.

Scott V Bratman (SV)

Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.
Department of Radiation Oncology, University of Toronto, Toronto, Ontario, Canada.

Anna Spreafico (A)

Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.
Division of Medical Oncology and Hematology, Department of Medicine, University of Toronto, Toronto, Ontario, Canada.
ORCID: 0000-0002-3034-3042

John De Almeida (J)

Department of Otolaryngology-Head and Neck Surgery, University of Toronto, Toronto, Ontario, Canada.
Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.

Joel C Davies (JC)

Department of Otolaryngology-Head and Neck Surgery, University of Toronto, Toronto, Ontario, Canada.
Department of Otolaryngology - Head and Neck Surgery, Sinai Health System, Toronto, Ontario, Canada.

Laura Bierut (L)

Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, USA.
ORCID: 0000-0002-9952-4810

Gary J Macfarlane (GJ)

Epidemiology Group, School of Medicine, Medical Sciences and Nutrition, University of Aberdeen, Aberdeen, UK.

Pagona Lagiou (P)

Department of Hygiene, Epidemiology and Medical Statistics, Medical School, National and Kapodistrian, University of Athens, Goudi, Greece.

Areti Lagiou (A)

Department of Public and Community Health, School of Public Health, University of West Attica, Athens, Greece.

Jerry Polesel (J)

Unit of Cancer Epidemiology, Centro di Riferimento Oncologico di Aviano (CRO) IRCCS, Aviano, Italy.
ORCID: 0000-0001-9381-1520

Antonio Agudo (A)

Cancer Epidemiology Research Programme, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona, Spain; Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública, Madrid, Spain.

Laia Alemany (L)

Cancer Epidemiology Research Programme, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona, Spain; Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública, Madrid, Spain.

Wolfgang Ahrens (W)

Department of Epidemiological Methods and Etiological Research, Leibniz Institute for Prevention Research and Epidemiology-BIPS, Bremen, Germany; Department of Mathematics and Computer Science, University of Bremen, Bremen, Germany.
ORCID: 0000-0003-3777-570X

Claire M Healy (CM)

Department of Oral and Maxillofacial Surgery, Oral Medicine and Oral Pathology, Dublin Dental University Hospital, Trinity College Dublin, Dublin, Ireland.

David I Conway (DI)

School of Medicine, Dentistry, and Nursing, University of Glasgow, Glasgow, UK.

Mari Nygard (M)

Department of Research, Cancer Registry of Norway, Norwegian Institute of Public Health, Oslo, Norway.

Cristina Canova (C)

University of Padua, Padova, Italy.

Ivana Holcatova (I)

Institute of Hygiene & Epidemiology, 1st Faculty of Medicine, Charles University, Prague, Czech Republic.
ORCID: 0000-0002-1366-0337

Lorenzo Richiardi (L)

Department of Medical Sciences, University of Turin and CPO-Piemonte, Turin, Italy.
ORCID: 0000-0003-0316-9402

Ariana Znaor (A)

Cancer Surveillance Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.

David P Goldstein (DP)

Department of Otolaryngology-Head and Neck Surgery, University of Toronto, Toronto, Ontario, Canada.
Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.
ORCID: 0000-0001-9390-7928

Rayjean J Hung (RJ)

Prosserman Centre for Population Health Research, Lunenfeld-Tanenbaum Research Institute, Sinai Health, Toronto, Canada.
Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada.

Wei Xu (W)

Department of Biostatistics, Princess Margaret Cancer Centre-University Health Network, University of Toronto, Toronto, Ontario, Canada.
Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada.

Geoffrey Liu (G)

Infections and Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany. Geoffrey.Liu@uhn.ca.
Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada. Geoffrey.Liu@uhn.ca.
Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada. Geoffrey.Liu@uhn.ca.

Osvaldo Espin-Garcia (O)

Department of Biostatistics, Princess Margaret Cancer Centre-University Health Network, University of Toronto, Toronto, Ontario, Canada.
Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada.
Department of Epidemiology and Biostatistics, University of Western Ontario, London, Ontario, Canada.
ORCID: 0000-0003-2052-2626

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Techniques d'investigation › Analyse de randomisation mendélienne › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Comportement dipsique › Consommation d'alcool › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Tumeurs › Tumeurs par siège › Tumeurs de la tête et du cou › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Fumer › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Caractéristiques de la maladie › Maladies transmissibles › Maladies sexuellement transmissibles › Maladies sexuellement transmissibles virales › Infections à papillomavirus › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Tumeurs › Tumeurs par siège › Tumeurs de la tête et du cou › Carcinome épidermoïde de la tête et du cou › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Statistiques comme sujet › Probabilité › Risque › Facteurs de risque › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Virus › Virus oncogènes › Virus tumoraux à ADN › Papillomaviridae › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Adulte d'âge moyen › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Caractéristiques des études épidémiologiques › Études épidémiologiques › Études cas-témoins › Smoking and alcohol by HPV status in head and...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Polymorphisme génétique › Polymorphisme de nucléotide simple › Smoking and alcohol by HPV status in head and...