Devasena Anantharaman1, David C Muller1, Pagona Lagiou2, Wolfgang Ahrens3, Ivana Holcátová4, Franco Merletti5, Kristina Kjærheim6, Jerry Polesel7, Lorenzo Simonato8, Cristina Canova8, Xavier Castellsague9, Tatiana V Macfarlane10, Ariana Znaor11, Peter Thomson12, Max Robinson12, David I Conway13, Claire M Healy14, Anne Tjønneland15, Ulla Westin16, Johanna Ekström17, Jenny Chang-Claude18, Rudolf Kaaks18, Kim Overvad19, Dagmar Drogan20, Göran Hallmans21, Göran Laurell22, H B Bueno-de-Mesquita23, Petra H Peeters24, Antonio Agudo25, Nerea Larrañaga26, Ruth C Travis27, Domenico Palli28, Aurelio Barricarte29, Antonia Trichopoulou30, Saitakis George31, Dimitrios Trichopoulos32, J Ramón Quirós33, Sara Grioni34, Carlotta Sacerdote35, Carmen Navarro36, María-José Sánchez37, Rosario Tumino38, Gianluca Severi39, Marie-Christine Boutron-Ruault40, Francoise Clavel-Chapelon40, Salvatore Panico41, Elisabete Weiderpass42, Eiliv Lund43, Inger T Gram43, Elio Riboli44, Michael Pawlita45, Tim Waterboer45, Aimée R Kreimer46, Mattias Johansson1, Paul Brennan47. 1. Genetic Epidemiology Group, International Agency for Research on Cancer, Lyon, France. 2. Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens, Greece. 3. Leibniz Institute for Prevention Research and Epidemiology, BIPS, Bremen, Germany, Faculty of Mathematics and Computer Science, University of Bremen, Bremen, Germany. 4. Institute of Hygiene and Epidemiology, First Faculty of Medicine, Charles University of Prague, Prague, Czech Republic. 5. Unit of Cancer Epidemiology, Department of Medical Sciences, University of Turin, Turin, Italy. 6. Cancer Registry of Norway, Oslo, Norway. 7. Unit of Epidemiology and Biostatistics, CRO Aviano National Cancer Institute, Aviano, Italy. 8. Laboratory of Public Health and Population Studies, Department of Molecular Medicine, University of Padova, Padova, Italy. 9. Unit of Infections and Cancer, Institut Català d'Oncologia (ICO), IDIBELL, CIBERESP, L'Hospitalet de Llobregat, Barcelona, Spain. 10. School of Medicine and Dentistry, University of Aberdeen, Aberdeen, UK. 11. Croatian National Cancer Registry, Croatian National Institute of Public Health, Zagreb, Croatia, Section of Cancer Surveillance, International Agency for Research on Cancer, Lyon, France. 12. Centre for Oral Health Research, Newcastle University, Newcastle-upon-Tyne, UK. 13. Dental School, College of Medicine, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK. 14. School of Dental Science, Trinity College Dublin, Dublin, Ireland. 15. Danish Cancer Society, Institute of Cancer Epidemiology, Copenhagen, Denmark. 16. Department of Otorhinolaryngology of Malmö and Lund. 17. Department of Clinical Sciences, Lund University, Lund, Sweden. 18. Division of Cancer Epidemiology, German Cancer Research Centre (DKFZ), Heidelberg, Germany. 19. Institute of Public Health, Aarhus, Denmark. 20. German Institute of Human Nutrition Potsdam Rehbruecke (DIfE), Nuthetal, Germany. 21. Department of Biobank Research, Umeå University, Umeå, Sweden. 22. Department of Surgical Sciences, Uppsala University, Uppsala, Sweden. 23. Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands, Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, The Netherlands, Department of Epidemiology and Biostatistics, Imperial College London, School of Public Health, London, UK, Department of Social & Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia. 24. Department of Epidemiology, Julius Centre for Health Sciences and Primary Care, University Medical Centre, Utrecht, The Netherlands, MRC-PHE, Imperial College London, School of Public Health, London, UK. 25. Unit of Nutrition and Cancer, Institut Català d'Oncologia (ICO), L'Hospitalet de Llobregat, Barcelona, Spain. 26. Public Health Division of Gipuzkoa, BIODonostia Research Institute, Basque Health Department, San Sebastián, Spain, CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain. 27. Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK. 28. Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, Florence, Italy. 29. CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain, Navarre Public Health Institute, Pamplona, Spain. 30. Hellenic Health Foundation, Athens, Greece, Bureau of Epidemiologic Research, Academy of Athens, Athens, Greece. 31. Hellenic Health Foundation, Athens, Greece, Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens, Greece. 32. Hellenic Health Foundation, Athens, Greece, Bureau of Epidemiologic Research, Academy of Athens, Athens, Greece, Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA. 33. Public Health Directorate Asturias, Oviedo, Spain. 34. Epidemiology and Prevention Unit, Fondazione IRCCS, Istituto Nazionale dei Tumori, Milan, Italy. 35. Unit of Cancer Epidemiology, Citta' della Salute e della Scienza Hospital, University of Turin and Centre for Cancer Prevention (CPO), Turin, Italy. 36. CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain, Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain, Department of Health and Social Sciences, Universidad de Murcia, Murcia, Spain. 37. CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain, Instituto de Investigación Biosanitaria, Universidad de Granada, Granada, Spain. 38. Cancer Registry and Histopathology Unit, Civic - M P Arezzo Hospital, ASP Ragusa, Ragusa, Italy. 39. Human Genetics Foundation (HuGeF), Torino, Italy, Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, VIC, Australia, Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, VIC, Australia. 40. INSERM, Centre for research in Epidemiology and Population Health (CESP), Villejuif, France, Université Paris Sud, Villejuif, France, Institut Gustave Roussy, Villejuif, France. 41. Dipartimento di Medicina Clinica e Chirurgia, Federico II University, Naples, Italy. 42. Department of Community Medicine, Faculty of Health Science, University of Tromsø, Arctic University of Norway, Tromsø, Norway, Cancer Registry of Norway, Oslo, Norway, Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden, Department of Genetic Epidemiology, Folkhälsan Research Centre, Helsinki, Finland. 43. Department of Community Medicine, Faculty of Health Science, University of Tromsø, Arctic University of Norway, Tromsø, Norway. 44. School of Public Health, Imperial College London, London, UK. 45. German Cancer Research Centre (DKFZ), Heidelberg, Germany and. 46. National Cancer Institute, NIH, Bethesda, MD, USA. 47. Genetic Epidemiology Group, International Agency for Research on Cancer, Lyon, France, gep@iarc.fr.
Abstract
BACKGROUND: Although smoking and HPV infection are recognized as important risk factors for oropharyngeal cancer, how their joint exposure impacts on oropharyngeal cancer risk is unclear. Specifically, whether smoking confers any additional risk to HPV-positive oropharyngeal cancer is not understood. METHODS: Using HPV serology as a marker of HPV-related cancer, we examined the interaction between smoking and HPV16 in 459 oropharyngeal (and 1445 oral cavity and laryngeal) cancer patients and 3024 control participants from two large European multi-centre studies. Odds ratios and credible intervals [CrI], adjusted for potential confounders, were estimated using Bayesian logistic regression. RESULTS: Both smoking [odds ratio (OR [CrI]: 6.82 [4.52, 10.29]) and HPV seropositivity (OR [CrI]: 235.69 [99.95, 555.74]) were independently associated with oropharyngeal cancer. The joint association of smoking and HPV seropositivity was consistent with that expected on the additive scale (synergy index [CrI]: 1.32 [0.51, 3.45]), suggesting they act as independent risk factors for oropharyngeal cancer. CONCLUSIONS: Smoking was consistently associated with increase in oropharyngeal cancer risk in models stratified by HPV16 seropositivity. In addition, we report that the prevalence of oropharyngeal cancer increases with smoking for both HPV16-positive and HPV16-negative persons. The impact of smoking on HPV16-positive oropharyngeal cancer highlights the continued need for smoking cessation programmes for primary prevention of head and neck cancer.
BACKGROUND: Although smoking and HPV infection are recognized as important risk factors for oropharyngeal cancer, how their joint exposure impacts on oropharyngeal cancer risk is unclear. Specifically, whether smoking confers any additional risk to HPV-positive oropharyngeal cancer is not understood. METHODS: Using HPV serology as a marker of HPV-related cancer, we examined the interaction between smoking and HPV16 in 459 oropharyngeal (and 1445 oral cavity and laryngeal) cancerpatients and 3024 control participants from two large European multi-centre studies. Odds ratios and credible intervals [CrI], adjusted for potential confounders, were estimated using Bayesian logistic regression. RESULTS: Both smoking [odds ratio (OR [CrI]: 6.82 [4.52, 10.29]) and HPV seropositivity (OR [CrI]: 235.69 [99.95, 555.74]) were independently associated with oropharyngeal cancer. The joint association of smoking and HPV seropositivity was consistent with that expected on the additive scale (synergy index [CrI]: 1.32 [0.51, 3.45]), suggesting they act as independent risk factors for oropharyngeal cancer. CONCLUSIONS: Smoking was consistently associated with increase in oropharyngeal cancer risk in models stratified by HPV16 seropositivity. In addition, we report that the prevalence of oropharyngeal cancer increases with smoking for both HPV16-positive and HPV16-negative persons. The impact of smoking on HPV16-positive oropharyngeal cancer highlights the continued need for smoking cessation programmes for primary prevention of head and neck cancer.
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