Anticipated Efficacy of HPV Vaccination in Prophylaxis Against Nongenital Cancers
Authors:
B. Sehnal 1; N. Vojáčková 2; D. Driák 1; E. Kmoníčková 3; D. Vaňousová 2; K. Maxová 1; H. Neumannová 1; J. Sláma 4
Authors‘ workplace:
Onkogynekologické centrum, Gynekologicko‑porodnická klinika 1. LF UK a Nemocnice Na Bulovce, Praha
1; Dermatovenerologická klinika 2. LF UK a Nemocnice Na Bulovce, Praha
2; Ústav radiační onkologie, Komplexní onkologické centrum, 1. LF UK a Nemocnice Na Bulovce, Praha
3; Onkogynekologické centrum, Gynekologicko-porodnická klinika 1. LF UK a VFN v Praze
4
Published in:
Klin Onkol 2014; 27(4): 239-246
Category:
Review
Overview
Background:
There is a considerable number of studies on the efficacy HPV (human papillomavirus) vaccination against different cancers but relevant information is scattered in diverse journals. This paper is a review summarizing current knowledge of the potential of HPV vaccination against all HPV related cancers.
Aim:
HPV infection is probably the most frequent sexually transmitted disease. At least 13 HPV genotypes are classified as carcinogenic or probably carcinogenic in respect to cervical cancer. Almost 100% of cervical cancers are linked to HPV infection. HPV 16 and HPV 18 are the most frequently involved genotypes and account together for approximately 70% of cervical cancer in the world. Persistent high‑risk HPV infection is responsible for a significant proportion of vulvar, vaginal, anal and penile carcinomas. The virus has also been implicated in oncogenesis of head and neck cancers, including oropharyngeal cancers. HPV infection can play an important role in cancerogenesis of lung, esophagus, breast, and colon and rectum. On the contrary, published results indicate that HPV infection is not associated with prostate oncogenesis. Strong predominance of HPV 16 has been reported for all HPV‑associated cancer sites. Generally, it is estimated that approximately 5.2% of all cancers are associated with oncogenic HPV infection. Currently, there are two vaccines on the market; quadrivalent Silgard® (Gardasil®) and bivalent CervarixTM. Large trials for both vaccines have shown efficacy against HPV‑related infection and disease. Efficacy has been very high in HPV naive subjects to vaccine related types. While HPV vaccination is currently approved for the prevention of cervical cancer, it also has the potential in the prevention of all HPV‑associated malignancies. The Czech republic belongs to countries that cover HPV vaccination of girls at the age of 13– 14 years by general health insurance. Overall impact of this vaccination remains to be evaluated. The new issues of the role of HPV in oncogenesis, as well as the potential effect of HPV vaccination against HPV‑related nongenital cancers are discussed.
Conclusion:
Approximately 5.2% of all human cancers are associated with oncogenic human papillomavirus infection. HPV vaccination against the most risky HPV oncotypes may cause a significant reduction of these cancers mainly in the HPV naive population.
Key words:
human papillomavirus – anal cancer – penile cancer – head and neck cancer – esophageal cancer – lung cancer – colorectal cancer – recurrent respiratory papillomatosis
This study was supported by grant of Integral Agency of the Czech Ministry of Health No. NT14079-3/2013 and by project PRVOUK-P27/LF1/1.
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.
Submitted:
2. 2. 2014
Accepted:
21. 5. 2014
Sources
1. Spitzer M. Human papillomavirus: epidemiology, natural history, and clinical sequelae. OBG Management 2006; 18 (Suppl): S5– S10.
2. Trollfors B. Human papillomavirus vaccines: an outsider’s point of view. Expert Rev Vaccines 2008; 7(8): 1131– 1133. doi: 10.1586/ 14760584.7.8.1131.
3. Ciuffo G. Innesto positivo con filtrato di verruca volgare. Giorn Ital Mal Venereol 1907; 48: 12– 17.
4. Della Torre G, Pilotti S, de Palo G et al. Viral particles in cervical condylomatous lesions. Tumori 1978; 64(5): 549– 553.
5. Laverty CR, Booth N, Hills E et al. Noncondylomatous wart virus infection of the postmenopausal cervix. Pathology 1978; 10(4): 373– 378.
6. Muñoz N, Bosch FX, de Sanjose S et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348(6): 518– 527.
7. zur Hausen H. Papillomaviruses in the causation of human cancers‑ a brief historical account. Virology 2009; 384(2): 260– 265. doi: 10.1016/ j.virol.2008.11.046.
8. von Knebel Doeberitz M, Rittmüller C, zur Hausen H et al. Inhibition of tumorigenicity of cervical cancer cells in nude mice by HPV E6– E7 anti‑sense RNA. Int J Cancer 1992; 51(5): 831– 834.
9. Yee C, Krishnan‑ Hewlett I, Baker CC et al. Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am J Pathol 1985; 119(3): 361– 366.
10. Vonka V, Kanka J, Hirsch I et al. Prospective study on the relationship between cervical neoplasia and herpes simplex type‑ 2 virus. II. Herpes simplex type‑ 2 antibody presence in sera taken at enrollment. Int J Cancer 1984; 33(1): 61– 66.
11. Fehrmann F, Laimins LA. Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation. Oncogene 2003; 22(33): 5201– 5207.
12. White EA, Sowa ME, Tan MJ et al. Systematic identification of interactions between host cell proteins and E7 oncoproteins from diverse human papillomaviruses. Proc Natl Acad Sci USA 2012; 109(5): E260– E267. doi: 10.1073/ pnas.1116776109.
13. Viscidi RP, Schiffman M, Hildesheim A et al. Seroreactivity to human papillomavirus (HPV) types 16, 18, or 31 and risk of subsequent HPV infection: results from a population‑based study in Costa Rica. Cancer Epidemiol Biomarkers Prev 2004; 13(2): 324– 327.
14. Carter JJ, Koutsky LA, Hughes JP et al. Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J Inf Diseas 2000; 181(6): 1911– 1919.
15. Schwarz TF. ASO4- adjuvanted human papillomavirus – 16/ 18 vaccination: recent advances in cervical cancer prevention. Expert Rev Vaccines 2008; 7(10): 1465– 1473. doi: 10.1586/ 14760584.7.10.1465.
16. Bouvard V, Baan R, Straif K et al. A review of human carcinogens – part B: biological agents. Lancet Oncol 2009; 10(4): 321– 322.
17. Driák D, Sehnal B. Význam infekcí způsobených lidskými papilomaviry. Cas Lek Cesk 2013; 152(1): 15– 19.
18. De Vuyst H, Clifford GM, Nascimento MC et al. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta‑analysis. Int J Cancer 2009; 124(7): 1626– 1636. doi: 10.1002/ ijc.24116.
19. Kreimer AR, Clifford GM, Boyle P et al. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomarkers Prev 2005; 14(2): 467– 475.
20. Zandberg DP, Bhargava R, Badin S et al. The role of human papillomavirus in nongenital cancers. CA Cancer J Clin 2013; 63(1): 57– 81. doi: 10.3322/ caac.21167.
21. Weiss P, Zvěřina J (eds). Sexuální chování obyvatel v ČR. Praha: Dema 2003: 28– 32.
22. Zhou J, Sun XY, Stenzel DJ et al. Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cell is sifficient for assembly of HPV virion‑like particles. Virology 1991; 185(1): 251– 257.
23. Driák D, Dyrhonová M, Tachezy R. Vakcinace proti lidským papilomavirům a její kontroverze – II. Gynekolog 2009; 18: 176– 181.
24. Tomson TT, Roden RB, Wu TC. Human papillomavirus vaccines for the prevention and treatment of cervical cancer. Curr Op Invest Drugs 2004; 5(12): 1247– 1261.
25. Svod.cz [internetova stranka]. Česky národní webový portál epidemiologie nádorů. Masarykova univerzita, Česká republika; c2006. Dostupné z: http:/ / www.svod.cz.
26. Tachezy R, Rob L. Skrínink pro prevenci karcinomu děložního hrdla v České republice. Cas Lek Ces 2007; 146(12): 939– 944.
27. Medicines.org.uk [homepage on the Internet]. Silgard SPC. Available from: http:/ / www.medicines.org.uk/ emc/ medicine/ 19016/ SPC/ gardasil/ .
28. Medicines.org.uk [homepage on the Internet]. Cervarix SPC. Available from: http:/ / www.medicines.org.uk/ emc/ medicine/ 20204/ SPC/ cervarix/ .
29. Tjalma WA, Fiander A, Reich O et al. Differences in human papillomavirus type distribution in high‑grade cervical intraepithelial neoplasia and invasive cervical cancer in Europe. Int J Cancer 2013; 132(4): 854– 867. doi: 10.1002/ ijc.27713.
30. Johnson LG, Madeleine MM, Newcomer LM et al. Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973– 2000. Cancer 2004; 101(2): 281– 288.
31. Goodman MT, Shvetsov YB, McDuffie K et al. Sequential acquisition of human papillomavirus (HPV) infection of the anus and cervix: the Hawaii HPV Cohort Study. J Infect Dis 2010; 201(9): 1331– 1339. doi: 10.1086/ 651620.
32. Tachezy R, Smahelova M, Salakova J et al. Human papillomavirus genotype distribution in Czech women and men with diseases etiologically linked to HPV. PLoS One 2011; 6(7): e21913. doi: 10.1371/ journal.pone.0021913.
33. Palefsky JM, Holly EA, Ralston ML et al. Prevalence and risk factors for anal human papillomavirus infection in human immunodeficiency virus (HIV)- positive and high‑risk HIV-negative women. J Infect Dis 2001; 183(3): 383– 391.
34. Frisch M, Olsen JH, Melbye M. Malignancies that occur before and after anal cancer: clues to their etiology. Am J Epidemiol 1994; 140(1): 12– 19.
35. Edgren G, Sparén P. Risk of anogenital cancer after diagnosis of cervical intraepithelial neoplasia: a prospective population‑based study. Lancet Oncol 2007; 8(4): 311– 316.
36. Goodman MT, Shvetsov YB, McDuffie K et al. Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort study. J Infect Dis 2008; 197(7): 957– 966. doi: 10.1086/ 529207.
37. Melbye M, Sprogel P. Aetiological parallel between anal cancer and cervical cancer. Lancet 1991; 338(8768): 657– 659.
38. Daling JR, Weiss NS, Hislop TG et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317(16): 973– 977.
39. Daling J, Madeleine M, Johnson L et al. Penile cancer: importance of circumcision, human papillomavirus and smoking in in situ and invasive disease. Int J Cancer 2005; 116(4): 606– 616.
40. Fda.gov [homepage on the Internet]. U.S. Food and Drug Administration, USA. Available from: http:/ / www.fda.gov/ BiologicsBloodVaccines/ Vaccines/ ApprovedProducts/ ucm094042.htm.
41. Parkin DM, Bray F. Chapter 2: the burden of HPV‑related cancers. Vaccine 2006; 24 (Suppl 3): S11– S25.
42. Shabbir M, Barod R, Hegarty PK et al. Primary prevention and vaccination for penile cancer. Ther Adv Urol 2013; 5(3): 161– 169. doi: 10.1177/ 1756287212465456.
43. Gillison ML, Alemany L, Snijders PJ et al. Human papillomavirus and diseases of the upper airway: head and neck cancer and resipiratory papillomatosis. Vaccine 2012; 30 (Suppl 5): F34– F54. doi: 10.1016/ j.vaccine.2012.05.070.
44. Jemal A, Bray F, Center MM et al. Global cancer statistics. CA Cancer J Clin 2011; 61(2): 69– 90. doi: 10.3322/ caac.20107.
45. Syrjanen KJ, Pyrhonen S, Syrjanen SM et al. Immunohistochemical demonstration of human papilloma virus (HPV) antigens in oral squamous cell lesions. Br J Oral Surg 1983; 21(2): 147– 153.
46. Weinberger PM, Yu Z, Haffty BG et al. Molecular classification identifies subset of human papillomavirus‑associated oropharyngeal cancers with favorable prognosis. J Clin Oncol 2006; 24(5): 736– 747.
47. Ostwald C, Müller P, Barten M et al. Human papillomavirus DNA in oral squamous cell carcinomas and normal mucosa. J Oral Pathol Med 1994; 23(5): 220– 225.
48. Klozar J, Tachezy R, Rotnáglová E et al. Human papillomavirus in head and neck tumors: epidemiological, molecular and clinical aspects. Wien Med Wochenschr 2010; 160(11– 12): 305– 309. doi: 10.1007/ s10354‑ 010‑ 0782‑ 5.
49. Näsman A, Attner P, Hammarstedt L et al. Incidence of human papillomavirus (HPV) positive tonsillar carcinoma in Stockholm, Sweden: an epidemic of viral‑induced carcinoma? Int J Cancer 2009; 125(2): 362– 366. doi: 10.1002/ ijc.24339.
50. Simard EP, Ward EM, Siegel R et al. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J Clin 2012; 62: 118– 128. doi: 10.3322/ caac.20141.
51. Mazur S, D‘Souza G, Westra WH et al. HPV‑ asscociated head and neck cancer: a virus related cancer epidemic. Lancet Oncology 2010; 11(8): 781– 789. doi: 10.1016/ S1470‑ 2045(10)70017‑ 6.
52. D’Souza G, Dempsey A. The role of HPV in head and neck cancer and review of the HPV vaccine. Prev Med 2011; 53 (Suppl 1): S5– S11. doi: 10.1016/ j.ypmed.2011.08.001.
53. Bajos N, Bozon M, Beltzer N et al. Changes in sexual behaviours: from secular trends to public health policies. AIDS 2010; 24(8): 1185– 1191. doi: 10.1097/ QAD.0b013e328336ad52.
54. Mork J, Lie AK, Glattre E et al. Human papillomavirus infection as a risk factor for squamous‑ cell carcinoma of the head and neck. N Engl J Med 2001; 344(15): 1125– 1131.
55. Jayaprakash V, Reid M, Hatton E et al. Human papillomavirus types 16 and 18 in epithelial dysplasia of oral cavity and oropharynx: a meta‑analysis, 1985– 2010. Oral Oncol 2011; 47(11): 1048– 1054. doi: 10.1016/ j.oraloncology.2011.07.009.
56. Chaturvedi AK, Engels EA, Pfeiffer RM et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011; 29(32): 4294– 4301. doi: 10.1200/ JCO.2011.36.4596.
57. Gillison ML, D’Souza G, Westra W et al. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16- negative head and neck cancers. J Natl Cancer Inst 2008; 100(6): 407– 420. doi: 10.1093/ jnci/ djn025.
58. Hafkamp HC, Manni JJ, Haesevoets A et al. Marked differences in survival rate between smokers and nonsmokers with HPV 16‑associated tonsillar carcinomas. Int J Cancer 2008; 122(12): 2656– 2664. doi: 10.1002/ ijc.23458.
59. Ang KK, Harris J, Wheeler R et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010; 363(1): 24– 35. doi: 10.1056/ NEJMoa0912217.
60. Herrero R, Quint W, Hildesheim A et al. Reduced prevalence of oral human papillomavirus (HPV) 4 years after bivalent HPV vaccination in a randomized clinical trial in Costa Rica. PLoS One 2013; 8(7): e68329. doi: 10.1371/ journal.pone.0068329.
61. Gholipour C, Shalchi RA, Abbasi M. A histopathological study of esophageal cancer on the western side of the Caspian littoral from 1994 to 2003. Dis Esophagus 2008; 21(4): 322– 327. doi: 10.1111/ j.1442‑ 2050.2007.00776.x.
62. Chang F, Syrjänen SM, Wang L et al. Infectious agents in the etiology of esophageal cancer. Gastroenterology 1992; 103(4): 1336– 1348.
63. Franceschi S, Munoz N, Bosch XF et al. Human papillomavirus and cancers of the upper aerodigestive tract: a review of epidemiological and experimental evidence. Cancer Epidemiol Biomarkers Prev 1996; 5(7): 567– 575.
64. Syrjänen K, Pyrhönen S, Aukee S et al. Squamous cell papilloma of the esophagus: a tumour probably caused by human papilloma virus (HPV). Diagn Histopathol 1982; 5(4): 291– 296.
65. Chang F, Syrjanen S, Shen Q et al. Human papillomavirus involvement in esophageal carcinogenesis in the high incidence area of China. A study of 700 cases by screening and type‑ specific in situ hybridization. Scand J Gastroenterol 2000; 35(2): 123– 130.
66. Syrjänen KJ. HPV infections and oesophageal cancer. J Clin Pathol 2002; 55(10): 721– 728.
67. El‑ Serag HB, Hollier JM, Gravitt P et al. Human papillomavirus and the risk of Barrett’s esophagus. Dis Esophagus 2013; 26(5): 517– 521. doi: 10.1111/ j.1442‑ 2050.2012.01392.x.
68. Ribeiro U Jr, Posner MC, Safatle‑ Ribeiro AV et al. Risk factors for squamous cell carcinoma of the oesophagus. Br J Surg 1996; 83(9): 1174– 1185.
69. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol 2007; 25(5): 561– 570.
70. Syrjänen K. Detection of human papillomavirus in lung cancer: systematic review and meta‑analysis. Anticancer Res 2012; 32(8): 3235– 3250.
71. Yu Y, Yang A, Hu S et al. Correlation of HPV‑ 16/ 18 infection of human papillomavirus with lung squamous cell carcinomas in Western China. Oncol Rep 2009; 21(6): 1627– 1632.
72. Yu Y, Yang A, Hu S et al. Significance of human papillomavirus 16/ 18 infection in association with p53 mutation in lung carcinomas. Clin Respir J 2013; 7(1): 27– 33. doi: 10.1111/ j.1752‑ 699X.2011.00277.x.
73. Klein F, Amin Kotb WF, Petersen I. Incidence of human papilloma virus in lung cancer. Lung Cancer 2009; 65(1): 13– 18. doi: 10.1016/ j.lungcan.2008.10.003.
74. Cheng YW, Wu MF, Wang J et al. Human papilloma-virus 16/ 18 E6 oncoprotein is expressed in lung cancer and related with p53 inactivation. Cancer Res 2007; 67(22): 10686– 10693.
75. Park MS, Chang YS, Shin JH et al. The prevalence of human papillomavirus infection in Korean non‑small cell lung cancer patients. Yonsei Med J 2007; 48(1): 69– 77.
76. Aguayo F, Anwar M, Koriyama C et al. Human papillomavirus‑ 16 presence and physical status in lung carcinomas from Asia. Infect Agent Cancer 2010; 5: 20. doi: 10.1186/ 1750‑ 9378‑ 5‑ 20.
77. Iwakawa R, Kohno T, Enari M et al. Prevalence of human papillomavirus 16/ 18/ 33 infection and p53 mutation in lung adenocarcinoma. Cancer Sci 2010; 101(8): 1891– 1896. doi: 10.1111/ j.1349‑ 7006.2010.01622.x.
78. Simen‑ Kapeu A, Surcel HM, Koskela P et al. Lack of association between human papillomavirus type 16 and 18 infections and female lung cancer. Cancer Epidemiol Biomarkers Prev 2010; 19(7): 1879– 1881. doi: 10.1158/ 1055‑ 9965.EPI‑ 10‑ 0356.
79. Koshiol J, Rotunno M, Gillison ML et al. Assessment of human papillomavirus in lung tumor tissue. J Natl Cancer Inst 2011; 103(6): 501– 507. doi: 10.1093/ jnci/ djr003.
80. Srinivasan M, Taioli E, Ragin CC. Human papillomavirus type 16 and 18 in primary lung cancers – a meta‑analysis. Carcinogenesis 2009; 30(10): 1722– 1728. doi: 10.1093/ carcin/ bgp177.
81. Bishop JA, Ogawa T, Chang X et al. HPV analysis in distinguishing second primary tumors from lung metastases in patients with head and neck squamous cell carcinoma. Am J Surg Pathol 2012; 36(1): 142– 148. doi: 10.1097/ PAS.0b013e3182395c7b.
82. Cheng YW, Chiou HL, Sheu GT et al. The association of human papillomavirus 16/ 18 infection with lung cancer among nonsmoking Taiwanese women. Cancer Res 2001; 61(7): 2799– 2803.
83. Doxtader EE, Katzenstein AL. The relationship between p16 expression and high‑risk human papillomavirus infection in squamous cell carcinomas from sites other than uterine cervix: a study of 137 cases. Hum Pathol 2012; 43(3): 327– 332. doi: 10.1016/ j.humpath.2011.05.010.
84. Simões PW, Medeiros LR, Simões PD et al. Prevalence of human papillomavirus in breast cancer: a systematic review. Int J Gynecol Cancer 2012; 22(3): 343– 347. doi: 10.1097/ IGC.0b013e31823c712e.
85. Damin DC, Ziegelmann PK, Damin AP. Human papillomavirus infection and colorectal cancer risk: a meta‑analysis. Colorectal Dis 2013; 15(8): e420– e428. doi: 10.1111/ codi.12257.
86. Lin Y, Mao Q, Zheng X et al. Human papillomavirus 16 or 18 infection and prostate cancer risk: a meta‑analysis. Ir J Med Sci 2011; 180(2): 497– 503. doi: 10.1007/ s11845‑ 011‑ 0692‑ 6.
87. Tachezy R, Hrbacek J, Heracek J et al. HPV persistence and its oncogenic role in prostate tumors. J Med Virol 2012; 84(10): 1636– 1645. doi: 10.1002/ jmv.23367.
88. Dedo HH, Yu KC. CO(2) laser treatment in 244 patients with resiratory papillomas. Laryngoscope 2001; 111(9): 1639– 1944.
89. Silverberg MJ, Thorsen P, Lindeberg H et al. Condyloma in pregnancy is strongly predictive of juvenile‑ onset respiratory papillomatosis. Obstet Gynecol 2003; 101(4): 645– 652.
90. Kashima HK, Shah F, Lyles A et al. A comparison of risk factors in juvenile‑ onset and adult‑ onset recurrent respiratory papillomatosis. Laryngoscope 1992; 102(1): 9– 13.
91. Buchinsky FL, Donfack J, Derkay CS et al. Age of child, more than HPV type, is associated with clinical course in recurrent respiratory papillomatosis. PLoS One 2008; 3(5): e2263. doi: 10.1371/ journal.pone.0002263.
92. Wiatrak BJ, Wiatrak DW, Broker TR et al. Recurrent respiratory papillomatosis: longitudinal study comparing severity associated with papilloma viral type 6 and 11 and other risk factors in a large pediatric population. Laryngoscope 2004; 114 (11 Pt 2 Suppl 104): 1– 23.
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