Combined effects of smoking and HPV16 in oropharyngeal cancer

Devasena Anantharaman, David C Muller, Pagona Lagiou, Wolfgang Ahrens, Ivana Holcátová, Franco Merletti, Kristina Kjærheim, Jerry Polesel, Lorenzo Simonato, Cristina Canova, Xavier Castellsague, Tatiana MacFarlane, Ariana Znaor, Peter Thomson, Max Robinson, David I Conway, Claire M Healy, Anne Tjønneland, Ulla Westin, Johanna Ekström & 35 others Jenny Chang-Claude, Rudolf Kaaks, Kim Overvad, Dagmar Drogan, Göran Hallmans, Göran Laurell, H B Bueno-de-Mesquita, Petra H Peeters, Antonio Agudo, Nerea Larrañaga, Ruth C Travis, Domenico Palli, Aurelio Barricarte, Antonia Trichopoulou, Saitakis George, Dimitrios Trichopoulos, J Ramón Quirós, Sara Grioni, Carlotta Sacerdote, Carmen Navarro, María-José Sánchez, Rosario Tumino, Gianluca Severi, Marie-Christine Boutron-Ruault, Francoise Clavel-Chapelon, Salvatore Panico, Elisabete Weiderpass, Eiliv Lund, Inger T Gram, Elio Riboli, Michael Pawlita, Tim Waterboer, Aimée R Kreimer, Mattias Johansson, Paul Brennan

Research output: Contribution to journalArticle

22 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)752-761
Number of pages10
JournalInternational Journal of Epidemiology
Volume45
Issue number3
Early online date19 May 2016
DOIs
Publication statusPublished - Jun 2016

Fingerprint

Oropharyngeal Neoplasms
Smoking
Odds Ratio
Laryngeal Neoplasms
Smoking Cessation
Serology
Primary Prevention
Head and Neck Neoplasms
Mouth
Joints
Logistic Models

Keywords

  • human papillomavirus
  • tobacco smoking
  • interaction
  • head and neck cancer risk
  • oropharynx cancer

Cite this

Anantharaman, D., Muller, D. C., Lagiou, P., Ahrens, W., Holcátová, I., Merletti, F., ... Brennan, P. (2016). Combined effects of smoking and HPV16 in oropharyngeal cancer. International Journal of Epidemiology, 45(3), 752-761. https://doi.org/10.1093/ije/dyw069

Combined effects of smoking and HPV16 in oropharyngeal cancer. / Anantharaman, Devasena; Muller, David C; Lagiou, Pagona; Ahrens, Wolfgang; Holcátová, Ivana; Merletti, Franco; Kjærheim, Kristina; Polesel, Jerry; Simonato, Lorenzo; Canova, Cristina; Castellsague, Xavier; MacFarlane, Tatiana; Znaor, Ariana; Thomson, Peter; Robinson, Max; Conway, David I; Healy, Claire M; Tjønneland, Anne; Westin, Ulla; Ekström, Johanna; Chang-Claude, Jenny; Kaaks, Rudolf; Overvad, Kim; Drogan, Dagmar; Hallmans, Göran; Laurell, Göran; Bueno-de-Mesquita, H B; Peeters, Petra H; Agudo, Antonio; Larrañaga, Nerea; Travis, Ruth C; Palli, Domenico; Barricarte, Aurelio; Trichopoulou, Antonia; George, Saitakis; Trichopoulos, Dimitrios; Quirós, J Ramón; Grioni, Sara; Sacerdote, Carlotta; Navarro, Carmen; Sánchez, María-José; Tumino, Rosario; Severi, Gianluca; Boutron-Ruault, Marie-Christine; Clavel-Chapelon, Francoise; Panico, Salvatore; Weiderpass, Elisabete; Lund, Eiliv; Gram, Inger T; Riboli, Elio; Pawlita, Michael; Waterboer, Tim; Kreimer, Aimée R; Johansson, Mattias; Brennan, Paul.

In: International Journal of Epidemiology, Vol. 45, No. 3, 06.2016, p. 752-761.

Research output: Contribution to journalArticle

Anantharaman, D, Muller, DC, Lagiou, P, Ahrens, W, Holcátová, I, Merletti, F, Kjærheim, K, Polesel, J, Simonato, L, Canova, C, Castellsague, X, MacFarlane, T, Znaor, A, Thomson, P, Robinson, M, Conway, DI, Healy, CM, Tjønneland, A, Westin, U, Ekström, J, Chang-Claude, J, Kaaks, R, Overvad, K, Drogan, D, Hallmans, G, Laurell, G, Bueno-de-Mesquita, HB, Peeters, PH, Agudo, A, Larrañaga, N, Travis, RC, Palli, D, Barricarte, A, Trichopoulou, A, George, S, Trichopoulos, D, Quirós, JR, Grioni, S, Sacerdote, C, Navarro, C, Sánchez, M-J, Tumino, R, Severi, G, Boutron-Ruault, M-C, Clavel-Chapelon, F, Panico, S, Weiderpass, E, Lund, E, Gram, IT, Riboli, E, Pawlita, M, Waterboer, T, Kreimer, AR, Johansson, M & Brennan, P 2016, 'Combined effects of smoking and HPV16 in oropharyngeal cancer', International Journal of Epidemiology, vol. 45, no. 3, pp. 752-761. https://doi.org/10.1093/ije/dyw069
Anantharaman D, Muller DC, Lagiou P, Ahrens W, Holcátová I, Merletti F et al. Combined effects of smoking and HPV16 in oropharyngeal cancer. International Journal of Epidemiology. 2016 Jun;45(3):752-761. https://doi.org/10.1093/ije/dyw069
Anantharaman, Devasena ; Muller, David C ; Lagiou, Pagona ; Ahrens, Wolfgang ; Holcátová, Ivana ; Merletti, Franco ; Kjærheim, Kristina ; Polesel, Jerry ; Simonato, Lorenzo ; Canova, Cristina ; Castellsague, Xavier ; MacFarlane, Tatiana ; Znaor, Ariana ; Thomson, Peter ; Robinson, Max ; Conway, David I ; Healy, Claire M ; Tjønneland, Anne ; Westin, Ulla ; Ekström, Johanna ; Chang-Claude, Jenny ; Kaaks, Rudolf ; Overvad, Kim ; Drogan, Dagmar ; Hallmans, Göran ; Laurell, Göran ; Bueno-de-Mesquita, H B ; Peeters, Petra H ; Agudo, Antonio ; Larrañaga, Nerea ; Travis, Ruth C ; Palli, Domenico ; Barricarte, Aurelio ; Trichopoulou, Antonia ; George, Saitakis ; Trichopoulos, Dimitrios ; Quirós, J Ramón ; Grioni, Sara ; Sacerdote, Carlotta ; Navarro, Carmen ; Sánchez, María-José ; Tumino, Rosario ; Severi, Gianluca ; Boutron-Ruault, Marie-Christine ; Clavel-Chapelon, Francoise ; Panico, Salvatore ; Weiderpass, Elisabete ; Lund, Eiliv ; Gram, Inger T ; Riboli, Elio ; Pawlita, Michael ; Waterboer, Tim ; Kreimer, Aimée R ; Johansson, Mattias ; Brennan, Paul. / Combined effects of smoking and HPV16 in oropharyngeal cancer. In: International Journal of Epidemiology. 2016 ; Vol. 45, No. 3. pp. 752-761.
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title = "Combined effects of smoking and HPV16 in oropharyngeal cancer",
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.",
keywords = "human papillomavirus, tobacco smoking, interaction, head and neck cancer risk, oropharynx cancer",
author = "Devasena Anantharaman and Muller, {David C} and Pagona Lagiou and Wolfgang Ahrens and Ivana Holc{\'a}tov{\'a} and Franco Merletti and Kristina Kj{\ae}rheim and Jerry Polesel and Lorenzo Simonato and Cristina Canova and Xavier Castellsague and Tatiana MacFarlane and Ariana Znaor and Peter Thomson and Max Robinson and Conway, {David I} and Healy, {Claire M} and Anne Tj{\o}nneland and Ulla Westin and Johanna Ekstr{\"o}m and Jenny Chang-Claude and Rudolf Kaaks and Kim Overvad and Dagmar Drogan and G{\"o}ran Hallmans and G{\"o}ran Laurell and Bueno-de-Mesquita, {H B} and Peeters, {Petra H} and Antonio Agudo and Nerea Larra{\~n}aga and Travis, {Ruth C} and Domenico Palli and Aurelio Barricarte and Antonia Trichopoulou and Saitakis George and Dimitrios Trichopoulos and Quir{\'o}s, {J Ram{\'o}n} and Sara Grioni and Carlotta Sacerdote and Carmen Navarro and Mar{\'i}a-Jos{\'e} S{\'a}nchez and Rosario Tumino and Gianluca Severi and Marie-Christine Boutron-Ruault and Francoise Clavel-Chapelon and Salvatore Panico and Elisabete Weiderpass and Eiliv Lund and Gram, {Inger T} and Elio Riboli and Michael Pawlita and Tim Waterboer and Kreimer, {Aim{\'e}e R} and Mattias Johansson and Paul Brennan",
note = "Funding The ARCAGE study was supported by a grant from the European Commission’s 5th Framework Program (contract QLK1-2001- 00182). The EPIC study has been supported by the Europe Against Cancer Program of the European Commission (SANCO); Deutsche Krebshilfe, Deutsches Krebsforschungszentrum, German Federal Ministry of Education and Research; Danish Cancer Society; Health Research Fund (FIS) of the Spanish Ministry of Health, Spanish Regional Governments of Andalucia, Asturias, Basque Country, Murcia and Navarra; Catalan Institute of Oncology, Spain; the ISCIII of the Spanish Ministry of Health (RETICC DR06/0020); Cancer Research UK; Medical Research Council, UK; Greek Ministry of Health; Stavros Niarchos Foundation; Hellenic Health Foundation; Italian Association for Research on Cancer (AIRC); Italian National Research Council, Fondazione-IstitutoBanco Napoli, Italy; Associazione Italiana per la Ricerca sul Cancro-AIRC Milan; Compagnia di San Paolo; Dutch Ministry of Public Health Welfare and Sports; World Cancer Research Fund; Swedish Cancer Society; Swedish Scientific Council; Regional Government of Vasterbotten, Sweden; NordForsk (Centre of excellence programme HELGA), Norway; French League against Cancer (LNCC), France; National Institute for Health and Medical Research (INSERM), France; Mutuelle Generale de l’Education Nationale (MGEN), France; 3M Co, France; Gustave Roussy Institute (IGR), France; and General Councils of France. The serology testing of EPIC prospective study was supported by the National Cancer Institute Intramural Research Program. The work done in this study was supported in part by a grant from the European Commission’s 7th Framework Program (contract FP7-HEALTH-2011–282562) and partly by the Health General Directorate of the French Social Affairs and Health Ministry.",
year = "2016",
month = "6",
doi = "10.1093/ije/dyw069",
language = "English",
volume = "45",
pages = "752--761",
journal = "International Journal of Epidemiology",
issn = "0300-5771",
publisher = "OXFORD UNIV PRESS",
number = "3",

}

TY - JOUR

T1 - Combined effects of smoking and HPV16 in oropharyngeal cancer

AU - Anantharaman, Devasena

AU - Muller, David C

AU - Lagiou, Pagona

AU - Ahrens, Wolfgang

AU - Holcátová, Ivana

AU - Merletti, Franco

AU - Kjærheim, Kristina

AU - Polesel, Jerry

AU - Simonato, Lorenzo

AU - Canova, Cristina

AU - Castellsague, Xavier

AU - MacFarlane, Tatiana

AU - Znaor, Ariana

AU - Thomson, Peter

AU - Robinson, Max

AU - Conway, David I

AU - Healy, Claire M

AU - Tjønneland, Anne

AU - Westin, Ulla

AU - Ekström, Johanna

AU - Chang-Claude, Jenny

AU - Kaaks, Rudolf

AU - Overvad, Kim

AU - Drogan, Dagmar

AU - Hallmans, Göran

AU - Laurell, Göran

AU - Bueno-de-Mesquita, H B

AU - Peeters, Petra H

AU - Agudo, Antonio

AU - Larrañaga, Nerea

AU - Travis, Ruth C

AU - Palli, Domenico

AU - Barricarte, Aurelio

AU - Trichopoulou, Antonia

AU - George, Saitakis

AU - Trichopoulos, Dimitrios

AU - Quirós, J Ramón

AU - Grioni, Sara

AU - Sacerdote, Carlotta

AU - Navarro, Carmen

AU - Sánchez, María-José

AU - Tumino, Rosario

AU - Severi, Gianluca

AU - Boutron-Ruault, Marie-Christine

AU - Clavel-Chapelon, Francoise

AU - Panico, Salvatore

AU - Weiderpass, Elisabete

AU - Lund, Eiliv

AU - Gram, Inger T

AU - Riboli, Elio

AU - Pawlita, Michael

AU - Waterboer, Tim

AU - Kreimer, Aimée R

AU - Johansson, Mattias

AU - Brennan, Paul

N1 - Funding The ARCAGE study was supported by a grant from the European Commission’s 5th Framework Program (contract QLK1-2001- 00182). The EPIC study has been supported by the Europe Against Cancer Program of the European Commission (SANCO); Deutsche Krebshilfe, Deutsches Krebsforschungszentrum, German Federal Ministry of Education and Research; Danish Cancer Society; Health Research Fund (FIS) of the Spanish Ministry of Health, Spanish Regional Governments of Andalucia, Asturias, Basque Country, Murcia and Navarra; Catalan Institute of Oncology, Spain; the ISCIII of the Spanish Ministry of Health (RETICC DR06/0020); Cancer Research UK; Medical Research Council, UK; Greek Ministry of Health; Stavros Niarchos Foundation; Hellenic Health Foundation; Italian Association for Research on Cancer (AIRC); Italian National Research Council, Fondazione-IstitutoBanco Napoli, Italy; Associazione Italiana per la Ricerca sul Cancro-AIRC Milan; Compagnia di San Paolo; Dutch Ministry of Public Health Welfare and Sports; World Cancer Research Fund; Swedish Cancer Society; Swedish Scientific Council; Regional Government of Vasterbotten, Sweden; NordForsk (Centre of excellence programme HELGA), Norway; French League against Cancer (LNCC), France; National Institute for Health and Medical Research (INSERM), France; Mutuelle Generale de l’Education Nationale (MGEN), France; 3M Co, France; Gustave Roussy Institute (IGR), France; and General Councils of France. The serology testing of EPIC prospective study was supported by the National Cancer Institute Intramural Research Program. The work done in this study was supported in part by a grant from the European Commission’s 7th Framework Program (contract FP7-HEALTH-2011–282562) and partly by the Health General Directorate of the French Social Affairs and Health Ministry.

PY - 2016/6

Y1 - 2016/6

N2 - 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.

AB - 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.

KW - human papillomavirus

KW - tobacco smoking

KW - interaction

KW - head and neck cancer risk

KW - oropharynx cancer

U2 - 10.1093/ije/dyw069

DO - 10.1093/ije/dyw069

M3 - Article

VL - 45

SP - 752

EP - 761

JO - International Journal of Epidemiology

JF - International Journal of Epidemiology

SN - 0300-5771

IS - 3

ER -