Skip to main content
Top
Published in: Cancer Causes & Control 3/2017

01-03-2017 | Original paper

Disease burden of human papillomavirus infection in the Netherlands, 1989–2014: the gap between females and males is diminishing

Authors: Scott A. McDonald, Venetia Qendri, Johannes Berkhof, Hester E. de Melker, Johannes A. Bogaards

Published in: Cancer Causes & Control | Issue 3/2017

Login to get access

Abstract

Purpose

Besides cervical cancer, HPV infection is linked to a multitude of diseases in both males and females, suggesting that vaccination programmes should be re-evaluated, with a judicious assessment made of the disease burden stratified by sex, age, and genotype. Projections of burden into the near future are also needed to provide a benchmark for evaluating the impact of vaccination programmes, and to assess the need for scaling-up preventive measures.

Methods

Using the disability-adjusted life-years (DALY) measure, we estimated the total HPV-associated disease burden in the Netherlands. Annual cancer registrations over the period 1989–2014 for all cancers with an aetiological link to HPV infection were retrieved, supplemented by incidence data on high-grade cervical intraepithelial neoplasia (CIN) and anogenital warts.

Results

Over the recent period 2011–2014, the average annual HPV disease burden was 10,600 DALYs (95% credible interval (CrI):10,260–10,960) in females and 3,346 DALYs (95% CrI: 2,973–3,762) in males. Burden was dominated by cervical cancer, but its share amongst women decreased from 89% in 1989 to 77% in 2014. The male share of the total disease burden increased from 9.8% in 1989 to 26% in 2014. In 2023 (before the expected clinical impact from vaccinating girls), total burden is forecasted at 1.3-fold larger than in 2014.

Conclusions

The HPV-associated disease burden is higher than that reported for any other infectious disease in the Netherlands, with a larger burden observed in women than in men. The rapidly rising male share of the total burden underlines the prioritization of male HPV-related disease in prevention programmes.
Appendix
Available only for authorised users
Literature
2.
go back to reference Munoz N, Castellsague X, de Gonzalez AB, Gissmann L (2006) Chap. 1: HPV in the etiology of human cancer. Vaccine 24(Suppl 3):1–10 Munoz N, Castellsague X, de Gonzalez AB, Gissmann L (2006) Chap. 1: HPV in the etiology of human cancer. Vaccine 24(Suppl 3):1–10
3.
go back to reference Leemans CR, Braakhuis BJ, Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nat Rev Cancer 11(1):9–22CrossRefPubMed Leemans CR, Braakhuis BJ, Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nat Rev Cancer 11(1):9–22CrossRefPubMed
4.
go back to reference Plummer M, de Martel C, Vignat J, Ferlay J, Bray F, Franceschi S (2016) Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health 4:e609–e616CrossRefPubMed Plummer M, de Martel C, Vignat J, Ferlay J, Bray F, Franceschi S (2016) Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health 4:e609–e616CrossRefPubMed
6.
go back to reference Hawkins MG, Winder DM, Ball SL, Vaughan K, Sonnex C, Stanley MA, Sterling JC, Goon PK (2013) Detection of specific HPV subtypes responsible for the pathogenesis of condylomata acuminata. Virol J 10:137CrossRefPubMedPubMedCentral Hawkins MG, Winder DM, Ball SL, Vaughan K, Sonnex C, Stanley MA, Sterling JC, Goon PK (2013) Detection of specific HPV subtypes responsible for the pathogenesis of condylomata acuminata. Virol J 10:137CrossRefPubMedPubMedCentral
7.
go back to reference Joura EA, Giuliano AR, Iversen OE, Bouchard C, Mao C, Mehlsen J, Moreira ED Jr, Ngan Y, Petersen LK, Lazcano-Ponce E et al (2015) A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 372(8):711–723CrossRefPubMed Joura EA, Giuliano AR, Iversen OE, Bouchard C, Mao C, Mehlsen J, Moreira ED Jr, Ngan Y, Petersen LK, Lazcano-Ponce E et al (2015) A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 372(8):711–723CrossRefPubMed
8.
go back to reference zur Hausen H (1977) Human papillomaviruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol 78:1–30 zur Hausen H (1977) Human papillomaviruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol 78:1–30
9.
go back to reference Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189(1):12–19CrossRefPubMed Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189(1):12–19CrossRefPubMed
10.
go back to reference Sinisgalli E, Bellini I, Indiani L, Sala A, Bechini A, Bonanni P, Boccalini S (2015) HPV vaccination for boys? A systematic review of economic studies. Epidemiol Prev 39(4 Suppl 1):51–58PubMed Sinisgalli E, Bellini I, Indiani L, Sala A, Bechini A, Bonanni P, Boccalini S (2015) HPV vaccination for boys? A systematic review of economic studies. Epidemiol Prev 39(4 Suppl 1):51–58PubMed
11.
go back to reference Brisson M, Laprise JF, Chesson HW, Drolet M, Malagon T, Boily MC, Markowitz LE (2016) Health and economic impact of switching from a 4-valent to a 9-valent HPV vaccination program in the United States. J Natl Cancer Inst 108(1):djv282CrossRefPubMed Brisson M, Laprise JF, Chesson HW, Drolet M, Malagon T, Boily MC, Markowitz LE (2016) Health and economic impact of switching from a 4-valent to a 9-valent HPV vaccination program in the United States. J Natl Cancer Inst 108(1):djv282CrossRefPubMed
12.
go back to reference Bogaards JA, Wallinga J, Brakenhoff RH, Meijer CJ, Berkhof J (2015) Direct benefit of vaccinating boys along with girls against oncogenic human papillomavirus: bayesian evidence synthesis. Bmj 350:h2016CrossRefPubMedPubMedCentral Bogaards JA, Wallinga J, Brakenhoff RH, Meijer CJ, Berkhof J (2015) Direct benefit of vaccinating boys along with girls against oncogenic human papillomavirus: bayesian evidence synthesis. Bmj 350:h2016CrossRefPubMedPubMedCentral
13.
go back to reference Ault KA (2007) Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 369(9576):1861–1868CrossRefPubMed Ault KA (2007) Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 369(9576):1861–1868CrossRefPubMed
14.
go back to reference Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR et al (2009) Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374(9686):301–314CrossRefPubMed Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR et al (2009) Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374(9686):301–314CrossRefPubMed
15.
go back to reference Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Penny ME, Aranda C, Vardas E, Moi H, Jessen H, Hillman R et al (2011) Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N Engl J Med 364(5):401–411CrossRefPubMedPubMedCentral Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Penny ME, Aranda C, Vardas E, Moi H, Jessen H, Hillman R et al (2011) Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N Engl J Med 364(5):401–411CrossRefPubMedPubMedCentral
16.
go back to reference Palefsky JM, Giuliano AR, Goldstone S, Moreira ED Jr, Aranda C, Jessen H, Hillman R, Ferris D, Coutlee F, Stoler MH et al (2011) HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med 365(17):1576–1585CrossRefPubMed Palefsky JM, Giuliano AR, Goldstone S, Moreira ED Jr, Aranda C, Jessen H, Hillman R, Ferris D, Coutlee F, Stoler MH et al (2011) HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med 365(17):1576–1585CrossRefPubMed
17.
go back to reference Kretzschmar ME, Mangen M-J, Pinheiro P, Jahn B, Fèvre EM, Longhi S, Lai T, Havelaar AH, Stein C, Cassini A et al (2012) New methodology for estimating the burden of communicable diseases in Europe. PLoS Med 9(4):e1001205CrossRefPubMedPubMedCentral Kretzschmar ME, Mangen M-J, Pinheiro P, Jahn B, Fèvre EM, Longhi S, Lai T, Havelaar AH, Stein C, Cassini A et al (2012) New methodology for estimating the burden of communicable diseases in Europe. PLoS Med 9(4):e1001205CrossRefPubMedPubMedCentral
18.
go back to reference Murray CJ (1994) Quantifying the burden of disease: the technical basis for disability-adjusted life years. Bull World Health Organ 72(3):429–445PubMedPubMedCentral Murray CJ (1994) Quantifying the burden of disease: the technical basis for disability-adjusted life years. Bull World Health Organ 72(3):429–445PubMedPubMedCentral
20.
go back to reference Bogaards JA, Coupe VM, Xiridou M, Meijer CJ, Wallinga J, Berkhof J (2011) Long-term impact of human papillomavirus vaccination on infection rates, cervical abnormalities, and cancer incidence. Epidemiology 22(4):505–515CrossRefPubMed Bogaards JA, Coupe VM, Xiridou M, Meijer CJ, Wallinga J, Berkhof J (2011) Long-term impact of human papillomavirus vaccination on infection rates, cervical abnormalities, and cancer incidence. Epidemiology 22(4):505–515CrossRefPubMed
21.
go back to reference Devleesschauwer B, Havelaar AH, Maertens de Noordhout C, Haagsma JA, Praet N, Dorny P, Duchateau L, Torgerson PR, Van Oyen H, Speybroeck N (2014) DALY calculation in practice: a stepwise approach. Int J Public Health 59(3):571–574CrossRefPubMed Devleesschauwer B, Havelaar AH, Maertens de Noordhout C, Haagsma JA, Praet N, Dorny P, Duchateau L, Torgerson PR, Van Oyen H, Speybroeck N (2014) DALY calculation in practice: a stepwise approach. Int J Public Health 59(3):571–574CrossRefPubMed
22.
go back to reference Perez L, Kunzli N (2009) From measures of effects to measures of potential impact. Int J Public Health 54(1):45–48CrossRefPubMed Perez L, Kunzli N (2009) From measures of effects to measures of potential impact. Int J Public Health 54(1):45–48CrossRefPubMed
23.
go back to reference Rietbergen MM, Leemans CR, Bloemena E, Heideman DA, Braakhuis BJ, Hesselink AT, Witte BI, Baatenburg de Jong RJ, Meijer CJ, Snijders PJ et al (2013) Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer 132(7):1565–1571CrossRefPubMed Rietbergen MM, Leemans CR, Bloemena E, Heideman DA, Braakhuis BJ, Hesselink AT, Witte BI, Baatenburg de Jong RJ, Meijer CJ, Snijders PJ et al (2013) Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer 132(7):1565–1571CrossRefPubMed
24.
go back to reference O’Rorke MA, Ellison MV, Murray LJ, Moran M, James J, Anderson LA (2012) Human papillomavirus related head and neck cancer survival: a systematic review and meta-analysis. Oral Oncol 48(12):1191–1201CrossRefPubMed O’Rorke MA, Ellison MV, Murray LJ, Moran M, James J, Anderson LA (2012) Human papillomavirus related head and neck cancer survival: a systematic review and meta-analysis. Oral Oncol 48(12):1191–1201CrossRefPubMed
25.
go back to reference Soerjomataram I, Lortet-Tieulent J, Ferlay J, Forman D, Mathers C, Parkin DM, Bray F (2012) Estimating and validating disability-adjusted life years at the global level: a methodological framework for cancer. BMC Med Res Methodol 12:125CrossRefPubMedPubMedCentral Soerjomataram I, Lortet-Tieulent J, Ferlay J, Forman D, Mathers C, Parkin DM, Bray F (2012) Estimating and validating disability-adjusted life years at the global level: a methodological framework for cancer. BMC Med Res Methodol 12:125CrossRefPubMedPubMedCentral
26.
go back to reference Soerjomataram I, Lortet-Tieulent J, Parkin DM, Ferlay J, Mathers C, Forman D, Bray F (2012) Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. The Lancet 380(9856):1840–1850CrossRef Soerjomataram I, Lortet-Tieulent J, Parkin DM, Ferlay J, Mathers C, Forman D, Bray F (2012) Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. The Lancet 380(9856):1840–1850CrossRef
28.
go back to reference Department of Human Services (DHS) (2005) The Victorian burden of disease study: mortality and morbidity in 2001. Department of Human Services, Melbourne Department of Human Services (DHS) (2005) The Victorian burden of disease study: mortality and morbidity in 2001. Department of Human Services, Melbourne
29.
go back to reference Jayatilleke N, Pashayan N, Powles JW (2012) Burden of disease due to cancer in England and Wales. J Public Health (Oxf) 34(2):287–295CrossRef Jayatilleke N, Pashayan N, Powles JW (2012) Burden of disease due to cancer in England and Wales. J Public Health (Oxf) 34(2):287–295CrossRef
30.
go back to reference Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: Evolution, critique and future directions. Stat Med 28(25):3049–3067CrossRefPubMed Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: Evolution, critique and future directions. Stat Med 28(25):3049–3067CrossRefPubMed
31.
go back to reference Thomas A, O’Hara B, Ligges U, Sturtz S (2006) Making BUGS Open. R News 6(1):12–17 Thomas A, O’Hara B, Ligges U, Sturtz S (2006) Making BUGS Open. R News 6(1):12–17
32.
go back to reference R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
33.
go back to reference Dyba T, Hakulinen T (2000) Comparison of different approaches to incidence prediction based on simple interpolation techniques. Stat Med 19(13):1741–1752CrossRefPubMed Dyba T, Hakulinen T (2000) Comparison of different approaches to incidence prediction based on simple interpolation techniques. Stat Med 19(13):1741–1752CrossRefPubMed
34.
go back to reference de Kok IM, van der Aa MA, van Ballegooijen M, Siesling S, Karim-Kos HE, van Kemenade FJ, Coebergh JW (2011) Trends in cervical cancer in the Netherlands until 2007: has the bottom been reached? Int J Cancer 128(9):2174–2181CrossRefPubMed de Kok IM, van der Aa MA, van Ballegooijen M, Siesling S, Karim-Kos HE, van Kemenade FJ, Coebergh JW (2011) Trends in cervical cancer in the Netherlands until 2007: has the bottom been reached? Int J Cancer 128(9):2174–2181CrossRefPubMed
35.
go back to reference Berkhof J, Coupe VM, Bogaards JA, van Kemenade FJ, Helmerhorst TJ, Snijders PJ, Meijer CJ (2010) The health and economic effects of HPV DNA screening in The Netherlands. Int J Cancer 127(9):2147–2158CrossRefPubMed Berkhof J, Coupe VM, Bogaards JA, van Kemenade FJ, Helmerhorst TJ, Snijders PJ, Meijer CJ (2010) The health and economic effects of HPV DNA screening in The Netherlands. Int J Cancer 127(9):2147–2158CrossRefPubMed
37.
go back to reference Chaturvedi AK (2012) Epidemiology and clinical aspects of HPV in head and neck cancers. Head Neck Pathol 6(Suppl 1):S16–S24CrossRefPubMed Chaturvedi AK (2012) Epidemiology and clinical aspects of HPV in head and neck cancers. Head Neck Pathol 6(Suppl 1):S16–S24CrossRefPubMed
38.
go back to reference Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W et al (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29(32):4294–4301CrossRefPubMedPubMedCentral Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W et al (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29(32):4294–4301CrossRefPubMedPubMedCentral
39.
go back to reference Marur S, D’Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11(8):781–789CrossRefPubMedPubMedCentral Marur S, D’Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11(8):781–789CrossRefPubMedPubMedCentral
40.
go back to reference van Monsjou HS, Schaapveld M, van den Brekel MW, Balm AJ (2015) The epidemiology of head and neck squamous cell carcinoma in The Netherlands during the era of HPV-related oropharyngeal squamous cell carcinoma. Is there really evidence for a change? Oral Oncol 51(10):901–907CrossRefPubMed van Monsjou HS, Schaapveld M, van den Brekel MW, Balm AJ (2015) The epidemiology of head and neck squamous cell carcinoma in The Netherlands during the era of HPV-related oropharyngeal squamous cell carcinoma. Is there really evidence for a change? Oral Oncol 51(10):901–907CrossRefPubMed
41.
go back to reference Zevallos JP, Mazul AL, Rodriguez N, Weissler MC, Brennan P, Anantharaman D, Abedi-Ardekani B, Neil Hayes D, Olshan AF (2016) Previous tonsillectomy modifies odds of tonsil and base of tongue cancer. Br J Cancer 114(7):832–838CrossRefPubMed Zevallos JP, Mazul AL, Rodriguez N, Weissler MC, Brennan P, Anantharaman D, Abedi-Ardekani B, Neil Hayes D, Olshan AF (2016) Previous tonsillectomy modifies odds of tonsil and base of tongue cancer. Br J Cancer 114(7):832–838CrossRefPubMed
42.
go back to reference Chaturvedi AK, Song H, Rosenberg PS, Ramqvist T, Anderson WF, Munck-Wikland E, Ye W, Dalianis T (2016) Tonsillectomy and incidence of oropharyngeal cancers. Cancer Epidemiol Biomark Prev 25(6):944–950CrossRef Chaturvedi AK, Song H, Rosenberg PS, Ramqvist T, Anderson WF, Munck-Wikland E, Ye W, Dalianis T (2016) Tonsillectomy and incidence of oropharyngeal cancers. Cancer Epidemiol Biomark Prev 25(6):944–950CrossRef
43.
go back to reference Chesson HW, Markowitz LE, Hariri S, Ekwueme DU, Saraiya M (2016) The impact and cost-effectiveness of nonavalent HPV vaccination in the United States: estimates from a simplified transmission model. Hum Vaccin Immunother 12:1–10CrossRef Chesson HW, Markowitz LE, Hariri S, Ekwueme DU, Saraiya M (2016) The impact and cost-effectiveness of nonavalent HPV vaccination in the United States: estimates from a simplified transmission model. Hum Vaccin Immunother 12:1–10CrossRef
44.
go back to reference van Lier A, McDonald SA, Bouwknegt M, Kretzschmar ME, Havelaar AH (2016) Disease burden of 32 infectious diseases in the Netherlands, 2007–2011. PLoS One 11(4):e0153106CrossRefPubMedPubMedCentral van Lier A, McDonald SA, Bouwknegt M, Kretzschmar ME, Havelaar AH (2016) Disease burden of 32 infectious diseases in the Netherlands, 2007–2011. PLoS One 11(4):e0153106CrossRefPubMedPubMedCentral
45.
go back to reference Tjalma WA, Fiander A, Reich O, Powell N, Nowakowski AM, Kirschner B, Koiss R, O’Leary J, Joura EA, Rosenlund M et al (2013) Differences in human papillomavirus type distribution in high-grade cervical intraepithelial neoplasia and invasive cervical cancer in Europe. Int J Cancer 132(4):854–867CrossRefPubMed Tjalma WA, Fiander A, Reich O, Powell N, Nowakowski AM, Kirschner B, Koiss R, O’Leary J, Joura EA, Rosenlund M et al (2013) Differences in human papillomavirus type distribution in high-grade cervical intraepithelial neoplasia and invasive cervical cancer in Europe. Int J Cancer 132(4):854–867CrossRefPubMed
46.
go back to reference de Sanjose S, Alemany L, Ordi J, Tous S, Alejo M, Bigby SM, Joura EA, Maldonado P, Laco J, Bravo IG et al (2013) Worldwide human papillomavirus genotype attribution in over 2000 cases of intraepithelial and invasive lesions of the vulva. Eur J Cancer 49(16):3450–3461CrossRefPubMed de Sanjose S, Alemany L, Ordi J, Tous S, Alejo M, Bigby SM, Joura EA, Maldonado P, Laco J, Bravo IG et al (2013) Worldwide human papillomavirus genotype attribution in over 2000 cases of intraepithelial and invasive lesions of the vulva. Eur J Cancer 49(16):3450–3461CrossRefPubMed
47.
go back to reference Alemany L, Saunier M, Tinoco L, Quiros B, Alvarado-Cabrero I, Alejo M, Joura EA, Maldonado P, Klaustermeier J, Salmeron J et al (2014) Large contribution of human papillomavirus in vaginal neoplastic lesions: a worldwide study in 597 samples. Eur J Cancer 50(16):2846–2854CrossRefPubMed Alemany L, Saunier M, Tinoco L, Quiros B, Alvarado-Cabrero I, Alejo M, Joura EA, Maldonado P, Klaustermeier J, Salmeron J et al (2014) Large contribution of human papillomavirus in vaginal neoplastic lesions: a worldwide study in 597 samples. Eur J Cancer 50(16):2846–2854CrossRefPubMed
48.
go back to reference Alemany L, Saunier M, Alvarado-Cabrero I, Quiros B, Salmeron J, Shin HR, Pirog EC, Guimera N, Hernandez-Suarez G, Felix A et al (2015) Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. Int J Cancer 136(1):98–107CrossRefPubMed Alemany L, Saunier M, Alvarado-Cabrero I, Quiros B, Salmeron J, Shin HR, Pirog EC, Guimera N, Hernandez-Suarez G, Felix A et al (2015) Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. Int J Cancer 136(1):98–107CrossRefPubMed
49.
go back to reference Braakhuis BJ, Snijders PJ, Keune WJ, Meijer CJ, Ruijter-Schippers HJ, Leemans CR, Brakenhoff RH (2004) Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. J Natl Cancer Inst 96(13):998–1006CrossRefPubMed Braakhuis BJ, Snijders PJ, Keune WJ, Meijer CJ, Ruijter-Schippers HJ, Leemans CR, Brakenhoff RH (2004) Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. J Natl Cancer Inst 96(13):998–1006CrossRefPubMed
50.
go back to reference Combes JD, Franceschi S (2014) Role of human papillomavirus in non-oropharyngeal head and neck cancers. Oral Oncol 50(5):370–379CrossRefPubMed Combes JD, Franceschi S (2014) Role of human papillomavirus in non-oropharyngeal head and neck cancers. Oral Oncol 50(5):370–379CrossRefPubMed
Metadata
Title
Disease burden of human papillomavirus infection in the Netherlands, 1989–2014: the gap between females and males is diminishing
Authors
Scott A. McDonald
Venetia Qendri
Johannes Berkhof
Hester E. de Melker
Johannes A. Bogaards
Publication date
01-03-2017
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 3/2017
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-017-0870-6

Other articles of this Issue 3/2017

Cancer Causes & Control 3/2017 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine