Skip to main content
Top
Published in: BMC Cancer 1/2017

Open Access 01-12-2017 | Research article

Cancer incidence in Germany attributable to human papillomavirus in 2013

Authors: Nina Buttmann-Schweiger, Yvonne Deleré, Stefanie J. Klug, Klaus Kraywinkel

Published in: BMC Cancer | Issue 1/2017

Login to get access

Abstract

Background

It is estimated that a total of 120,000 new cancer cases in men and in women in more developed countries could be avoided if exposure to HPV was prevented. We used the nationwide pool of German population-based cancer registry data to estimate the burden of HPV-attributable cancer in this population for the year 2013.

Methods

Incident cases of cervical cancer, squamous cell carcinoma of the anus, oropharynx (OP), as well as of the vulva, vagina and penis were classified as potentially HPV-associated and identified from the nationwide cancer registry data-pool. We calculated the incidence and proportions of cancer with potentially HPV-associated morphologies. Estimation of the HPV-attributable incidence was based on prevalence-estimates of viral DNA in tumor cells in the respective sites, as provided from the international literature.

Results

From the overall 15,936 incident cases of anogenital and OP cancers in 2013, 6239 female and 1358 male cancer cases were estimated to be attributable to HPV. The majority of HPV-attributable cases were contributed by cervical cancer (70.9% of female cancers) and oropharyngeal cancer (46.9% of male cancers).

Conclusions

Even if most HPV-attributable cases were contributed by cervical cancer, anogenital cancer at sites other than the cervix, and oropharyngeal cancer substantially contribute to the burden of HPV-associated cancer. Our nationwide cancer registry data-analyses provide the baseline for long-term population-based monitoring of vaccination-effects on cancer incidence in Germany.
Literature
1.
go back to reference Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189(1):12–9.CrossRefPubMed Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189(1):12–9.CrossRefPubMed
2.
go back to reference German Centre for Cancer Registry Data. Cancer in Germany 2011/2012. 10th ed. Robert Koch Institute (ed.) and the Association of Population-based Cancer Registries in Germany (ed.). Berlin: Robert Koch Institute; 2016. German Centre for Cancer Registry Data. Cancer in Germany 2011/2012. 10th ed. Robert Koch Institute (ed.) and the Association of Population-based Cancer Registries in Germany (ed.). Berlin: Robert Koch Institute; 2016.
3.
go back to reference de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13(6):607–15.CrossRefPubMed de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13(6):607–15.CrossRefPubMed
4.
go back to reference STIKO. Neuerungen in den aktuellen Empfehlungen der Ständigen Impfkommission (STIKO) am RKI vom August 2014. Epid Bull. 2014;35:343–47 STIKO. Neuerungen in den aktuellen Empfehlungen der Ständigen Impfkommission (STIKO) am RKI vom August 2014. Epid Bull. 2014;35:343–47
5.
go back to reference Villain P, Gonzalez P, Almonte M, Franceschi S, Dillner J, Anttila A, Park JY, De Vuyst H, Herrero R. European code against cancer 4th edition: infections and cancer. Cancer Epidemiol. 2015;39(Suppl 1):S120–38.CrossRefPubMed Villain P, Gonzalez P, Almonte M, Franceschi S, Dillner J, Anttila A, Park JY, De Vuyst H, Herrero R. European code against cancer 4th edition: infections and cancer. Cancer Epidemiol. 2015;39(Suppl 1):S120–38.CrossRefPubMed
6.
go back to reference Beachler DC, Kreimer AR, Schiffman M, Herrero R, Wacholder S, Rodriguez AC, Lowy DR, Porras C, Schiller JT, Quint W, et al. Multisite HPV16/18 vaccine efficacy against cervical, anal, and oral HPV infection. J Natl Cancer Inst. 2016;108(1). Beachler DC, Kreimer AR, Schiffman M, Herrero R, Wacholder S, Rodriguez AC, Lowy DR, Porras C, Schiller JT, Quint W, et al. Multisite HPV16/18 vaccine efficacy against cervical, anal, and oral HPV infection. J Natl Cancer Inst. 2016;108(1).
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: A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 2015;372(8):711–723. Joura EA, Giuliano AR, Iversen OE, Bouchard C, Mao C, Mehlsen J, Moreira ED, Jr., Ngan Y, Petersen LK, Lazcano-Ponce E et al: A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 2015;372(8):711–723.
8.
go back to reference Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu CW, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, et al. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. J Natl Cancer Inst. 2015;107(6):djv086.CrossRefPubMedPubMedCentral Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu CW, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, et al. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. J Natl Cancer Inst. 2015;107(6):djv086.CrossRefPubMedPubMedCentral
9.
go back to reference Drolet M, Benard E, Boily MC, Ali H, Baandrup L, Bauer H, Beddows S, Brisson J, Brotherton JM, Cummings T, et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2015;15(5):565–80.CrossRefPubMedPubMedCentral Drolet M, Benard E, Boily MC, Ali H, Baandrup L, Bauer H, Beddows S, Brisson J, Brotherton JM, Cummings T, et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2015;15(5):565–80.CrossRefPubMedPubMedCentral
10.
go back to reference IARC Monographs on the evaluation of carcinogenic risks to humans; v. 100B. Biological Agents. 2012. IARC Monographs on the evaluation of carcinogenic risks to humans; v. 100B. Biological Agents. 2012.
11.
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. Worldwide human papillomavirus genotype attribution in over 2000 cases of intraepithelial and invasive lesions of the vulva. Eur J Cancer. 2013;49(16):3450–61.CrossRefPubMed de Sanjose S, Alemany L, Ordi J, Tous S, Alejo M, Bigby SM, Joura EA, Maldonado P, Laco J, Bravo IG, et al. Worldwide human papillomavirus genotype attribution in over 2000 cases of intraepithelial and invasive lesions of the vulva. Eur J Cancer. 2013;49(16):3450–61.CrossRefPubMed
12.
go back to reference Alemany L, Cubilla A, Halec G, Kasamatsu E, Quiros B, Masferrer E, Tous S, Lloveras B, Hernandez-Suarez G, Lonsdale R, et al. Role of human papillomavirus in penile carcinomas worldwide. Eur Urol. 2016;69(5):953–61.CrossRefPubMed Alemany L, Cubilla A, Halec G, Kasamatsu E, Quiros B, Masferrer E, Tous S, Lloveras B, Hernandez-Suarez G, Lonsdale R, et al. Role of human papillomavirus in penile carcinomas worldwide. Eur Urol. 2016;69(5):953–61.CrossRefPubMed
13.
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. Large contribution of human papillomavirus in vaginal neoplastic lesions: a worldwide study in 597 samples. Eur J Cancer. 2014;50(16):2846–54.CrossRefPubMed Alemany L, Saunier M, Tinoco L, Quiros B, Alvarado-Cabrero I, Alejo M, Joura EA, Maldonado P, Klaustermeier J, Salmeron J, et al. Large contribution of human papillomavirus in vaginal neoplastic lesions: a worldwide study in 597 samples. Eur J Cancer. 2014;50(16):2846–54.CrossRefPubMed
14.
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. Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. Int J Cancer. 2015;136(1):98–107.CrossRefPubMed Alemany L, Saunier M, Alvarado-Cabrero I, Quiros B, Salmeron J, Shin HR, Pirog EC, Guimera N, Hernandez-Suarez G, Felix A, et al. Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. Int J Cancer. 2015;136(1):98–107.CrossRefPubMed
15.
go back to reference Castellsague X, Alemany L, Quer M, Halec G, Quiros B, Tous S, Clavero O, Alos L, Biegner T, Szafarowski T, et al. HPV Involvement in Head and Neck Cancers: Comprehensive Assessment of Biomarkers in 3680 Patients. J Natl Cancer Inst. 2016;108(6):djv403.CrossRefPubMed Castellsague X, Alemany L, Quer M, Halec G, Quiros B, Tous S, Clavero O, Alos L, Biegner T, Szafarowski T, et al. HPV Involvement in Head and Neck Cancers: Comprehensive Assessment of Biomarkers in 3680 Patients. J Natl Cancer Inst. 2016;108(6):djv403.CrossRefPubMed
16.
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. Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer. 2013;132(7):1565–71.CrossRefPubMed Rietbergen MM, Leemans CR, Bloemena E, Heideman DA, Braakhuis BJ, Hesselink AT, Witte BI, Baatenburg de Jong RJ, Meijer CJ, Snijders PJ, et al. Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer. 2013;132(7):1565–71.CrossRefPubMed
17.
go back to reference Boyle P, Parkin DM. Cancer registration: principles and methods. Statistical methods for registries. IARC Sci Publ. 1991;95:126–58. Boyle P, Parkin DM. Cancer registration: principles and methods. Statistical methods for registries. IARC Sci Publ. 1991;95:126–58.
19.
go back to reference Antonsson A, Wilson LF, Kendall BJ, Bain CJ, Whiteman DC, Neale RE. Cancers in Australia in 2010 attributable to infectious agents. Aust N Z J Public Health. 2015;39(5):446–51.CrossRefPubMedPubMedCentral Antonsson A, Wilson LF, Kendall BJ, Bain CJ, Whiteman DC, Neale RE. Cancers in Australia in 2010 attributable to infectious agents. Aust N Z J Public Health. 2015;39(5):446–51.CrossRefPubMedPubMedCentral
20.
go back to reference Ndiaye C, Mena M, Alemany L, Arbyn M, Castellsague X, Laporte L, Bosch FX, de Sanjose S, Trottier H. HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol. 2014;15(12):1319–31.CrossRefPubMed Ndiaye C, Mena M, Alemany L, Arbyn M, Castellsague X, Laporte L, Bosch FX, de Sanjose S, Trottier H. HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol. 2014;15(12):1319–31.CrossRefPubMed
21.
go back to reference Tinhofer I, Johrens K, Keilholz U, Kaufmann A, Lehmann A, Weichert W, Stenzinger A, Stromberger C, Klinghammer K, Becker ET, et al. Contribution of human papilloma virus to the incidence of squamous cell carcinoma of the head and neck in a European population with high smoking prevalence. Eur J Cancer. 2015;51(4):514–521. Tinhofer I, Johrens K, Keilholz U, Kaufmann A, Lehmann A, Weichert W, Stenzinger A, Stromberger C, Klinghammer K, Becker ET, et al. Contribution of human papilloma virus to the incidence of squamous cell carcinoma of the head and neck in a European population with high smoking prevalence. Eur J Cancer. 2015;51(4):514–521.
22.
23.
go back to reference Chaturvedi AK, Engels EA, Anderson WF, Gillison ML. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol. 2008;26(4):612–9.CrossRefPubMed Chaturvedi AK, Engels EA, Anderson WF, Gillison ML. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol. 2008;26(4):612–9.CrossRefPubMed
24.
go back to reference Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, Rosenberg PS, Bray F, Gillison ML. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol. 2013;31(36):4550–9.CrossRefPubMedPubMedCentral Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, Rosenberg PS, Bray F, Gillison ML. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol. 2013;31(36):4550–9.CrossRefPubMedPubMedCentral
25.
go back to reference Buttmann-Schweiger N, Klug SJ, Luyten A, Holleczek B, Heitz F, du Bois A, Kraywinkel K. Incidence patterns and temporal trends of invasive nonmelanotic vulvar tumors in Germany 1999-2011. A population-based cancer registry analysis. PLoS One. 2015;10(5):e0128073.CrossRefPubMedPubMedCentral Buttmann-Schweiger N, Klug SJ, Luyten A, Holleczek B, Heitz F, du Bois A, Kraywinkel K. Incidence patterns and temporal trends of invasive nonmelanotic vulvar tumors in Germany 1999-2011. A population-based cancer registry analysis. PLoS One. 2015;10(5):e0128073.CrossRefPubMedPubMedCentral
26.
go back to reference Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49(6):1374–403.CrossRefPubMed Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49(6):1374–403.CrossRefPubMed
27.
go back to reference World Health Organization. WHO classification of Tumours of the urinary system and male genital organs, vol. 4; 2016. World Health Organization. WHO classification of Tumours of the urinary system and male genital organs, vol. 4; 2016.
28.
go back to reference Bruni L, Barrionuevo-Rosas L, Albero G, Aldea M, Serrano B, Valencia S, Brotons M, Mena M, Cosano RMJ, et al. Human Papillomavirus and Related Diseases in Germany. Summary Report. ICO Information Centre on HPV and Cancer (HPV Information Centre). Accessed 23 Dec 2015. Bruni L, Barrionuevo-Rosas L, Albero G, Aldea M, Serrano B, Valencia S, Brotons M, Mena M, Cosano RMJ, et al. Human Papillomavirus and Related Diseases in Germany. Summary Report. ICO Information Centre on HPV and Cancer (HPV Information Centre). Accessed 23 Dec 2015.
29.
go back to reference Daling JR, Sherman KJ, Hislop TG, Maden C, Mandelson MT, Beckmann AM, Weiss NS. Cigarette smoking and the risk of anogenital cancer. Am J Epidemiol. 1992;135(2):180–9.CrossRefPubMed Daling JR, Sherman KJ, Hislop TG, Maden C, Mandelson MT, Beckmann AM, Weiss NS. Cigarette smoking and the risk of anogenital cancer. Am J Epidemiol. 1992;135(2):180–9.CrossRefPubMed
30.
go back to reference Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370(9581):59–67.CrossRefPubMed Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370(9581):59–67.CrossRefPubMed
31.
go back to reference Adami J, Gabel H, Lindelof B, Ekstrom K, Rydh B, Glimelius B, Ekbom A, Adami HO, Granath F. Cancer risk following organ transplantation: a nationwide cohort study in Sweden. Br J Cancer. 2003;89(7):1221–7.CrossRefPubMedPubMedCentral Adami J, Gabel H, Lindelof B, Ekstrom K, Rydh B, Glimelius B, Ekbom A, Adami HO, Granath F. Cancer risk following organ transplantation: a nationwide cohort study in Sweden. Br J Cancer. 2003;89(7):1221–7.CrossRefPubMedPubMedCentral
32.
go back to reference Ferenczy A, Coutlee F, Franco E, Hankins C. Human papillomavirus and HIV coinfection and the risk of neoplasias of the lower genital tract: a review of recent developments. CMAJ. 2003;169(5):431–4.PubMedPubMedCentral Ferenczy A, Coutlee F, Franco E, Hankins C. Human papillomavirus and HIV coinfection and the risk of neoplasias of the lower genital tract: a review of recent developments. CMAJ. 2003;169(5):431–4.PubMedPubMedCentral
33.
go back to reference Jemal A, Simard EP, Dorell C, Noone AM, Markowitz LE, Kohler B, Eheman C, Saraiya M, Bandi P, Saslow D, et al. Annual report to the nation on the status of cancer, 1975-2009, featuring the burden and trends in human papillomavirus(HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst. 2013;105(3):175–201.CrossRefPubMedPubMedCentral Jemal A, Simard EP, Dorell C, Noone AM, Markowitz LE, Kohler B, Eheman C, Saraiya M, Bandi P, Saslow D, et al. Annual report to the nation on the status of cancer, 1975-2009, featuring the burden and trends in human papillomavirus(HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst. 2013;105(3):175–201.CrossRefPubMedPubMedCentral
34.
go back to reference Islami F, Ferlay J, Lortet-Tieulent J, Bray F, Jemal A. International trends in anal cancer incidence rates. Int J Epidemiol. 2016;46(3):924–38. Islami F, Ferlay J, Lortet-Tieulent J, Bray F, Jemal A. International trends in anal cancer incidence rates. Int J Epidemiol. 2016;46(3):924–38.
35.
go back to reference Baandrup L, Varbo A, Munk C, Johansen C, Frisch M, Kjaer SK. In situ and invasive squamous cell carcinoma of the vulva in Denmark 1978-2007-a nationwide population-based study. Gynecol Oncol. 2011;122(1):45–9.CrossRefPubMed Baandrup L, Varbo A, Munk C, Johansen C, Frisch M, Kjaer SK. In situ and invasive squamous cell carcinoma of the vulva in Denmark 1978-2007-a nationwide population-based study. Gynecol Oncol. 2011;122(1):45–9.CrossRefPubMed
36.
go back to reference Schuurman MS, van den Einden LC, Massuger LF, Kiemeney LA, van der Aa MA, de Hullu JA. Trends in incidence and survival of Dutch women with vulvar squamous cell carcinoma. Eur J Cancer. 2013;49(18):3872–80.CrossRefPubMed Schuurman MS, van den Einden LC, Massuger LF, Kiemeney LA, van der Aa MA, de Hullu JA. Trends in incidence and survival of Dutch women with vulvar squamous cell carcinoma. Eur J Cancer. 2013;49(18):3872–80.CrossRefPubMed
37.
go back to reference Helou A. Early detection of cancer in the German National Cancer Plan: health policy and legal regulations. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2014;57(3):288–93.CrossRefPubMed Helou A. Early detection of cancer in the German National Cancer Plan: health policy and legal regulations. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2014;57(3):288–93.CrossRefPubMed
38.
go back to reference Zentrum für Krebsregisterdaten (ZfKD) im Robert Koch-Institut. Population-based cancer registry dataset from the German Center for Cancer Registry Data Epi2015_1. [Datensatz des ZfKD auf Basis der epidemiologischen Landeskrebsregisterdaten, verfügbare Diagnosejahre bis 2013 Epi2015_1]. doi:10.18444/5.03.01.0005.0011.0001 . Zentrum für Krebsregisterdaten (ZfKD) im Robert Koch-Institut. Population-based cancer registry dataset from the German Center for Cancer Registry Data Epi2015_1. [Datensatz des ZfKD auf Basis der epidemiologischen Landeskrebsregisterdaten, verfügbare Diagnosejahre bis 2013 Epi2015_1]. doi:10.​18444/​5.​03.​01.​0005.​0011.​0001 .
Metadata
Title
Cancer incidence in Germany attributable to human papillomavirus in 2013
Authors
Nina Buttmann-Schweiger
Yvonne Deleré
Stefanie J. Klug
Klaus Kraywinkel
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2017
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-017-3678-6

Other articles of this Issue 1/2017

BMC Cancer 1/2017 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