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Prevention and Epidemiology

No Causal Association Identified for Human Papillomavirus Infections in Lung Cancer

Devasena Anantharaman, Tarik Gheit, Tim Waterboer, Gordana Halec, Christine Carreira, Behnoush Abedi-Ardekani, Sandrine McKay-Chopin, David Zaridze, Anush Mukeria, Neonila Szeszenia-Dabrowska, Jolanta Lissowska, Dana Mates, Vladimir Janout, Lenka Foretova, Vladimir Bencko, Peter Rudnai, Eleonora Fabianova, Anne Tjønneland, Ruth C. Travis, Heiner Boeing, J. Ramón Quirós, Mikael Johansson, Vittorio Krogh, H. Bas Bueno-de-Mesquita, Anastasia Kotanidou, Françoise Clavel-Chapelon, Elisabete Weiderpass, Mattias Johansson, Michael Pawlita, Ghislaine Scelo, Massimo Tommasino and Paul Brennan
Devasena Anantharaman
Authors' Affiliations: Genetic Epidemiology Group;
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Tarik Gheit
Infections and Cancer Biology Group;
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Tim Waterboer
Infection and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg;
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Gordana Halec
Infection and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg;
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Christine Carreira
Molecular Pathology Group, International Agency for Research on Cancer, Lyon;
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Behnoush Abedi-Ardekani
Authors' Affiliations: Genetic Epidemiology Group;Digestive Disease Research Center, Tehran University of Medical Sciences, Tehran, Iran;
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Sandrine McKay-Chopin
Infections and Cancer Biology Group;
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David Zaridze
Department of Epidemiology and Prevention, Russian Cancer Research Center, Moscow, Russia;
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Anush Mukeria
Department of Epidemiology and Prevention, Russian Cancer Research Center, Moscow, Russia;
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Neonila Szeszenia-Dabrowska
Department of Environmental Epidemiology, Nofer Institute of Occupational Medicine, Lodz;
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Jolanta Lissowska
M. Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland;
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Dana Mates
Institute of Public Health, Bucharest, Romania;
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Vladimir Janout
Department of Preventive Medicine, Palacky University, Olomouc;
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Lenka Foretova
Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno;
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Vladimir Bencko
Institute of Hygiene and Epidemiology, 1st Faculty of Medicine, Charles University in Prague, Prague, Czech Republic;
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Peter Rudnai
National Institute of Environmental Health, Budapest, Hungary;
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Eleonora Fabianova
Regional Authority of Public Health, Banská Bystrica, Slovakia;
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Anne Tjønneland
Danish Cancer Society Research Center, Copenhagen, Denmark;
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Ruth C. Travis
Cancer Epidemiology Unit, Nuffield Department of Clinical Medicine, University of Oxford, Oxford;
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Heiner Boeing
Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany;
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J. Ramón Quirós
Public Health Directorate, Asturias, Spain;
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Mikael Johansson
Department of Radiation Sciences, Oncology, Umeå University, Umeå;
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Vittorio Krogh
Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy;
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H. Bas Bueno-de-Mesquita
The School of Public health, Imperial College London, London, United Kingdom;National Institute for Public Health and the Environment (RIVM), Bilthoven;Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, the Netherlands;
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Anastasia Kotanidou
First Department of Critical Care Medicine & Pulmonary Services, University of Athens Medical School, Evangelismos Hospital;Bureau of Epidemiologic Research, Academy of Athens, Athens, Greece;
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Françoise Clavel-Chapelon
INSERM, Centre for research in Epidemiology and Population Health (CESP), U1018, Nutrition, Hormones and Women's Health team;University Paris Sud;IGR, Villejuif, France;
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Elisabete Weiderpass
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden;Department of Community Medicine, Faculty of Health Sciences, The Artic University of Norway, Tromsø;Department of Research, Cancer Registry of Norway, Oslo, Norway; andSamfundet Folkhälsan, Helsinki, Finland
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Mattias Johansson
Authors' Affiliations: Genetic Epidemiology Group;
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Michael Pawlita
Infection and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg;
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Ghislaine Scelo
Authors' Affiliations: Genetic Epidemiology Group;
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Massimo Tommasino
Infections and Cancer Biology Group;
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Paul Brennan
Authors' Affiliations: Genetic Epidemiology Group;
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  • For correspondence: gep@iarc.fr
DOI: 10.1158/0008-5472.CAN-13-3548 Published July 2014
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Abstract

Human papillomavirus (HPV) infections have been implicated in lung carcinogenesis, but causal associations remain uncertain. We evaluated a potential causal role for HPV infections in lung cancer through an analysis involving serology, tumor DNA, RNA, and p16 protein expression. Association between type-specific HPV antibodies and risk of lung cancer was examined among 3,083 cases and 4,328 controls in two case–control studies (retrospective) and one nested case–control study (prospective design). Three hundred and thirty-four available tumors were subjected to pathologic evaluation and subsequent HPV genotyping following stringent conditions to detect all high-risk and two low-risk HPV types. All HPV DNA-positive tumors were further tested for the expression of p16 protein and type-specific HPV mRNA. On the basis of the consistency of the results, although HPV11 and HPV31 E6 antibodies were associated with lung cancer risk in the retrospective study, no association was observed in the prospective design. Presence of type-specific antibodies correlated poorly with the presence of the corresponding HPV DNA in the tumor. Although nearly 10% of the lung tumors were positive for any HPV DNA (7% for HPV16 DNA), none expressed the viral oncogenes. No association was observed between HPV antibodies or DNA and lung cancer survival. In conclusion, we found no supportive evidence for the hypothesized causal association between HPV infections and lung cancer. Cancer Res; 74(13); 3525–34. ©2014 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • Received December 17, 2013.
  • Revision received March 28, 2014.
  • Accepted April 4, 2014.
  • ©2014 American Association for Cancer Research.
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Cancer Research: 74 (13)
July 2014
Volume 74, Issue 13
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No Causal Association Identified for Human Papillomavirus Infections in Lung Cancer
Devasena Anantharaman, Tarik Gheit, Tim Waterboer, Gordana Halec, Christine Carreira, Behnoush Abedi-Ardekani, Sandrine McKay-Chopin, David Zaridze, Anush Mukeria, Neonila Szeszenia-Dabrowska, Jolanta Lissowska, Dana Mates, Vladimir Janout, Lenka Foretova, Vladimir Bencko, Peter Rudnai, Eleonora Fabianova, Anne Tjønneland, Ruth C. Travis, Heiner Boeing, J. Ramón Quirós, Mikael Johansson, Vittorio Krogh, H. Bas Bueno-de-Mesquita, Anastasia Kotanidou, Françoise Clavel-Chapelon, Elisabete Weiderpass, Mattias Johansson, Michael Pawlita, Ghislaine Scelo, Massimo Tommasino and Paul Brennan
Cancer Res July 1 2014 (74) (13) 3525-3534; DOI: 10.1158/0008-5472.CAN-13-3548

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No Causal Association Identified for Human Papillomavirus Infections in Lung Cancer
Devasena Anantharaman, Tarik Gheit, Tim Waterboer, Gordana Halec, Christine Carreira, Behnoush Abedi-Ardekani, Sandrine McKay-Chopin, David Zaridze, Anush Mukeria, Neonila Szeszenia-Dabrowska, Jolanta Lissowska, Dana Mates, Vladimir Janout, Lenka Foretova, Vladimir Bencko, Peter Rudnai, Eleonora Fabianova, Anne Tjønneland, Ruth C. Travis, Heiner Boeing, J. Ramón Quirós, Mikael Johansson, Vittorio Krogh, H. Bas Bueno-de-Mesquita, Anastasia Kotanidou, Françoise Clavel-Chapelon, Elisabete Weiderpass, Mattias Johansson, Michael Pawlita, Ghislaine Scelo, Massimo Tommasino and Paul Brennan
Cancer Res July 1 2014 (74) (13) 3525-3534; DOI: 10.1158/0008-5472.CAN-13-3548
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