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Role of Human Papillomavirus Infection in Head and Neck Cancer in Italy: The HPV-AHEAD Study

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Division of Otolaryngology and Head and Neck Surgery, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy
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Cancer Epidemiology Research Program, Catalan Institute of Oncology-Bellvitge Biomedical Research Institute (ICO-IDIBELL), L’Hospitalet de Llobregat, 08908 Barcenola, Spain
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Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, 28029 Madrid, Spain
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Division of Pathology, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy
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Infections and Cancer Biology Group, International Agency for Research on Cancer (IARC), 69372 Lyon, France
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Deutsches Krebsforschungszentrum (DKFZ), 69120 Heidelberg, Germany
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Roche mtm laboratories, 69117 Mannheim, Germany
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Ventana Medical Systems Inc./Roche Tissue Diagnostics, Tucson, AZ 85755, USA
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Laboratory for Cell Biology and Histology, University of Antwerp, 2610 Antwerp, Belgium
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Hospital del Mar, 08003 Barcelona, Spain
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Kidwai Memorial Institute of Oncology, Bangalore, Karnataka 560029, India
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Mahatma Gandhi Institute of Medical Sciences, Sevagram, Wardha, Maharashtra State 442102, India
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Rajiv Gandhi Centre for Biotechnology, Poojappura, Thiruvananthapuram, Kerala 695012, India
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Section of Genetics, International Agency for Research on Cancer (IARC), 69372 Lyon, France
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Research Triangle Institute (RTI) International India, New Delhi 110001, India
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Unit of Cancer Epidemiology/Belgian Cancer Centre, Sciensano, 1050 Brussels, Belgium
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Data Management, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy
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Medical Oncology Department, Catalan Institute of Oncology (ICO), ONCOBELL, IDIBELL, L’Hospitalet de Llobregat, 08035 Barcelona, Spain
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Department of Experimental Oncology, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy
*
Authors to whom correspondence should be addressed.
Contributed equally as first authors.
Contributed equally as senior authors.
§
Lead author: [email protected] (S.C.).
HPV-AHEAD Study Group: Cindy Simoens, Ivana Gorbaslieva (University of Antwerp, Antwerp, Belgium); Christel Herold-Mende (Departmentof Neurosurgery and Department of Otorhinolaryngology, Head and Neck Surgery, University of Heidelberg, Germany); Gerhard Dyckhoff (Department of Otorhinolaryngology, Head and Neck Surgery, University of Heidelberg, Germany); George Mosialos (Aristotle University of Thessaloniki, Greece); Heiner Boeing (German Institute of Human Nutrition, Berlin, Germany); Xavier Castellsagué (Castellsagué passed away on June 12th, 2016), Silvia de Sanjosé, Francesc Xavier Bosch (Catalan Institute of Oncology—IDIBELL, L’Hospitalet de Llobregat, Spain); Pulikottil Okkuru Esmy (Christian Fellowship Community Health Centre, Ambillikai, India); Rudrapatna S. Jayshree, Kortikere S. Sabitha, Ashok M. Shenoy (Kidwai Memorial Institute of Oncology, Bangalore, India); Manavalan Vijayakumar (YEN ONCO Centre, Yenepoya University, Deralakatte, Mangalore 575018, Karnataka, India); Aruna S. Chiwate, Ranjit V. Thorat, Girish G. Hublikar, Shashikant S. Lakshetti, Bhagwan M. Nene (Nargis Dutt Memorial Cancer Hospital, Barshi 413401, India); Amal Ch Kataki, Ashok Kumar Das (B. Borooah Cancer Institute, Guwahati, Assam, India); Subha Sankaran, Anju Krishnan, Jinu Austin (Rajiv Gandhi Centre for Biotechnology, Thiruvananthapuram, India); Kunnambath Ramadas (Regional Cancer Centre, Thiruvananthapuram, India); Christine Carreira, Sandrine McKay-Chopin (International Agency for Research on Cancer (IARC), Lyon, France), Priya Ramesh Prabhu, Madhavan Radhakrishna Pillai (Rajiv Gandhi Centre for Biotechnology, Poojappura, Thiruvananthapuram 695014, Kerala, India), Thara Somanathan (Regional Cancer Centre, Thiruvananthapuram 695011, India).
Cancers 2020, 12(12), 3567; https://doi.org/10.3390/cancers12123567
Received: 28 October 2020 / Revised: 20 November 2020 / Accepted: 24 November 2020 / Published: 29 November 2020
(This article belongs to the Special Issue Human Papillomavirus and Head and Neck Cancer)
This is the largest and most comprehensive assessment of the role of human papillomavirus (HPV) in head and neck cancer (HNC) in Italy, which is a region currently considered bearing a low burden of HPV-driven HNC. p16INK4a, HPV-DNA, and HPV RNA biomarkers were used to assess the HPV status in head and neck cancer in a retrospective cohort of approximately 700 patients. In our study, HPV prevalence in oropharyngeal cancers was much higher than in oral and laryngeal cancers, and HPV positivity conferred better prognosis only in oropharyngeal cancers. Importantly, we have observed an increase of the prevalence of HPV positivity in oropharyngeal cancers in the most recent calendar periods, suggesting that this disease is increasing in Italy, as has happened before in other developed regions.
Literature on the role of human papillomavirus (HPV) in head and neck cancer (HNC) in Italy is limited, especially for non-oropharyngeal tumours. Within the context of the HPV-AHEAD study, we aimed to assess the prognostic value of different tests or test algorithms judging HPV carcinogenicity in HNC and factors related to HPV positivity at the European Institute of Oncology. We conducted a retrospective cohort study (2000–2010) on a total of 696 primary HNC patients. Formalin-fixed, paraffin-embedded cancer tissues were studied. All HPV-DNA-positive and a random sample of HPV-DNA-negative cases were subjected to HPV-E6*I mRNA detection and p16INK4a staining. Multivariate models were used to assess for factors associated with HPV positivity and proportional hazards for survival and recurrence. The percentage of HPV-driven cases (considering HPV-E6*I mRNA positivity) was 1.8, 2.2, and 40.4% for oral cavity (OC), laryngeal (LC), and oropharyngeal (OPC) cases, respectively. The estimates were similar for HPV-DNA/p16INK4a double positivity. Being a non-smoker or former smoker or diagnosed at more recent calendar periods were associated with HPV-E6*I mRNA positivity only in OPC. Being younger was associated with HPV-E6*I mRNA positivity in LC. HPV-driven OPC, but not HPV-driven OC and LC, showed better 5 year overall and disease-free survival. Our data show that HPV prevalence in OPC was much higher than in OC and LC and observed to increase in most recent years. Moreover, HPV positivity conferred better prognosis only in OPC. Novel insights on the role of HPV in HNC in Italy are provided, with possible implications in the clinical management of these patients. View Full-Text
Keywords: head and neck cancer; human papillomavirus; oropharyngeal cancer; virus-related cancers; human papillomavirus diagnosis head and neck cancer; human papillomavirus; oropharyngeal cancer; virus-related cancers; human papillomavirus diagnosis
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MDPI and ACS Style

Tagliabue, M.; Mena, M.; Maffini, F.; Gheit, T.; Quirós Blasco, B.; Holzinger, D.; Tous, S.; Scelsi, D.; Riva, D.; Grosso, E.; Chu, F.; Lucas, E.; Ridder, R.; Rrehm, S.; Bogers, J.P.; Lepanto, D.; Lloveras Rubio, B.; Vijay Kumar, R.; Gangane, N.; Clavero, O.; Pawlita, M.; Anantharaman, D.; Radhakrishna Pillai, M.; Brennan, P.; Sankaranarayanan, R.; Arbyn, M.; Lombardi, F.; Taberna, M.; Gandini, S.; Chiesa, F.; Ansarin, M.; Alemany, L.; Tommasino, M.; Chiocca, S.; The HPV-AHEAD Study Group. Role of Human Papillomavirus Infection in Head and Neck Cancer in Italy: The HPV-AHEAD Study. Cancers 2020, 12, 3567. https://doi.org/10.3390/cancers12123567

AMA Style

Tagliabue M, Mena M, Maffini F, Gheit T, Quirós Blasco B, Holzinger D, Tous S, Scelsi D, Riva D, Grosso E, Chu F, Lucas E, Ridder R, Rrehm S, Bogers JP, Lepanto D, Lloveras Rubio B, Vijay Kumar R, Gangane N, Clavero O, Pawlita M, Anantharaman D, Radhakrishna Pillai M, Brennan P, Sankaranarayanan R, Arbyn M, Lombardi F, Taberna M, Gandini S, Chiesa F, Ansarin M, Alemany L, Tommasino M, Chiocca S, The HPV-AHEAD Study Group. Role of Human Papillomavirus Infection in Head and Neck Cancer in Italy: The HPV-AHEAD Study. Cancers. 2020; 12(12):3567. https://doi.org/10.3390/cancers12123567

Chicago/Turabian Style

Tagliabue, Marta, Marisa Mena, Fausto Maffini, Tarik Gheit, Beatriz Quirós Blasco, Dana Holzinger, Sara Tous, Daniele Scelsi, Debora Riva, Enrica Grosso, Francesco Chu, Eric Lucas, Ruediger Ridder, Susanne Rrehm, Johannes P. Bogers, Daniela Lepanto, Belén Lloveras Rubio, Rekha Vijay Kumar, Nitin Gangane, Omar Clavero, Michael Pawlita, Devasena Anantharaman, Madhavan Radhakrishna Pillai, Paul Brennan, Rengaswamy Sankaranarayanan, Marc Arbyn, Francesca Lombardi, Miren Taberna, Sara Gandini, Fausto Chiesa, Mohssen Ansarin, Laia Alemany, Massimo Tommasino, Susanna Chiocca, and The HPV-AHEAD Study Group. 2020. "Role of Human Papillomavirus Infection in Head and Neck Cancer in Italy: The HPV-AHEAD Study" Cancers 12, no. 12: 3567. https://doi.org/10.3390/cancers12123567

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