Penile carcinoma and HPV infection (Review)
- Authors:
- Lucian Iorga
- Radu Dragos Marcu
- Camelia Cristina Diaconu
- Ana Maria Alexandra Stanescu
- Anca Pantea Stoian
- Dan Liviu Dorel Mischianu
- Mihaela Surcel
- Simona Bungau
- Traian Constantin
- Daniel Boda
- Laszlo Fekete
- Ovidiu Gabriel Bratu
-
Affiliations: Urology Department, Emergency University Central Military Hospital, 010825 Bucharest, Romania, ‘Carol Davila’ University of Medicine and Pharmacy, 050474 Bucharest, Romania, Immunology Department, Victor Babes National Institute of Pathology, 050096 Bucharest, Romania, Department of Pharmacy, University of Oradea, 410073 Oradea, Romania, Dermatology Research Laboratory, ‘Carol Davila’ University of Medicine and Pharmacy, 050474 Bucharest, Romania, Dermamed Private Clinic, 211 E60 Targu Mures, Romania - Published online on: November 11, 2019 https://doi.org/10.3892/etm.2019.8181
- Pages: 91-96
This article is mentioned in:
Abstract
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2019. CA Cancer J Clin. 69:7–34. 2019.PubMed/NCBI View Article : Google Scholar | |
Favorito LA, Nardi AC, Ronalsa M, Zequi SC, Sampaio FJ and Glina S: Epidemiologic study on penile cancer in Brazil. Int Braz J Urol. 34:587–593. 2008.PubMed/NCBI View Article : Google Scholar | |
Couto TC, Arruda RM, Couto MC and Barros FD: Epidemiological study of penile cancer in Pernambuco: Experience of two reference centers. Int Braz J Urol. 40:738–744. 2014.PubMed/NCBI View Article : Google Scholar | |
Pow-Sang MR, Ferreira U, Pow-Sang JM, Nardi AC and Destefano V: Epidemiology and natural history of penile cancer. Urology. 76 (Suppl 1):S2–S6. 2010.PubMed/NCBI View Article : Google Scholar | |
Misra S, Chaturvedi A and Misra NC: Penile carcinoma: A challenge for the developing world. Lancet Oncol. 5:240–247. 2004.PubMed/NCBI View Article : Google Scholar | |
Mosconi AM, Roila F, Gatta G and Theodore C: Cancer of the penis. Crit Rev Oncol Hematol. 53:165–177. 2005.PubMed/NCBI View Article : Google Scholar | |
Cubilla AL, Dillner J and Schellhammer PF: Tumours of the penis. In: Tumors of the Urinary System and Mail Genital Organs. Eble JN, Sauter G and Epstein JI (eds). World Health Organization, Lyon. p279:2010. | |
Sanchez DF, Soares F, Alvarado-Cabrero I, Cañete S, Fernández-Nestosa MJ, Rodríguez IM, Barreto J and Cubilla AL: Pathological factors, behavior, and histological prognostic risk groups in subtypes of penile squamous cell carcinomas (SCC). Semin Diagn Pathol. 32:222–231. 2015.PubMed/NCBI View Article : Google Scholar | |
Dunne EF, Nielson CM, Stone KM, Markowitz LE and Giuliano AR: Prevalence of HPV infection among men: A systematic review of the literature. J Infect Dis. 194:1044–1057. 2006.PubMed/NCBI View Article : Google Scholar | |
Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJ and Meijer CJ: International Agency for Research on Cancer Multicenter Cervical Cancer Study Group: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 348:518–527. 2003.PubMed/NCBI View Article : Google Scholar | |
Hammarstedt L, Lindquist D, Dahlstrand H, Romanitan M, Dahlgren LO, Joneberg J, Creson N, Lindholm J, Ye W, Dalianis T, et al: Human papillomavirus as a risk factor for the increase in incidence of tonsillar cancer. Int J Cancer. 119:2620–2623. 2006.PubMed/NCBI View Article : Google Scholar | |
Wiener JS, Effert PJ, Humphrey PA, Yu L, Liu ET and Walther PJ: Prevalence of human papillomavirus types 16 and 18 in squamous-cell carcinoma of the penis: A retrospective analysis of primary and metastatic lesions by differential polymerase chain reaction. Int J Cancer. 50:694–701. 1992.PubMed/NCBI View Article : Google Scholar | |
Ingles DJ, Pierce Campbell CM, Messina JA, Stoler MH, Lin HY, Fulp WJ, Abrahamsen M, Sirak BA, O'Keefe MT, Papenfuss M, et al: Human papillomavirus virus (HPV) genotype- and age-specific analyses of external genital lesions among men in the HPV Infection in Men (HIM) Study. J Infect Dis. 211:1060–1067. 2015.PubMed/NCBI View Article : Google Scholar | |
Sudenga SL, Ingles DJ, Pierce Campbell CM, Lin HY, Fulp WJ, Messina JL, Stoler MH, Abrahamsen M, Villa LL, Lazcano-Ponce E, et al: Genital human papillomavirus infection progression to external genital lesions: The HIM Study. Eur Urol. 69:166–173. 2016.PubMed/NCBI View Article : Google Scholar | |
Lu B, Wu Y, Nielson CM, Flores R, Abrahamsen M, Papenfuss M, Harris RB and Giuliano AR: Factors associated with acquisition and clearance of human papillomavirus infection in a cohort of US men: A prospective study. J Infect Dis. 199:362–371. 2009.PubMed/NCBI View Article : Google Scholar | |
Giuliano AR, Lee J-H, Fulp W, Villa LL, Lazcano E, Papenfuss MR, Abrahamsen M, Salmeron J, Anic GM, Rollison DE, et al: Incidence and clearance of genital human papillomavirus infection in men (HIM): A cohort study. Lancet. 377:932–940. 2011.PubMed/NCBI View Article : Google Scholar | |
Spiess PE, Dhillon J, Baumgarten AS, Johnstone PA and Giuliano AR: Pathophysiological basis of human papillomavirus in penile cancer: Key to prevention and delivery of more effective therapies. CA Cancer J Clin. 66:481–495. 2016.PubMed/NCBI View Article : Google Scholar | |
Chaux A, Velazquez EF, Algaba F, Ayala G and Cubilla AL: Developments in the pathology of penile squamous cell carcinomas. Urology. 76 (Suppl 1):S7–S14. 2010.PubMed/NCBI View Article : Google Scholar | |
Gregoire L, Cubilla AL, Reuter VE, Haas GP and Lancaster WD: Preferential association of human papillomavirus with high-grade histologic variants of penile-invasive squamous cell carcinoma. J Natl Cancer Inst. 87:1705–1709. 1995.PubMed/NCBI View Article : Google Scholar | |
Alemany L, Cubilla A, Halec G, Kasamatsu E, Quirós B, Masferrer E, Tous S, Lloveras B, Hernández-Suarez G, Lonsdale R, et al: HPV VVAP study group: Role of human papillomavirus in penile carcinomas worldwide. Eur Urol. 69:953–961. 2016.PubMed/NCBI View Article : Google Scholar | |
Rubin MA, Kleter B, Zhou M, Ayala G, Cubilla AL, Quint WG and Pirog EC: Detection and typing of human papillomavirus DNA in penile carcinoma: Evidence for multiple independent pathways of penile carcinogenesis. Am J Pathol. 159:1211–1218. 2001.PubMed/NCBI View Article : Google Scholar | |
Aynaud O, Ionesco M and Barrasso R: Penile intraepithelial neoplasia. Specific clinical features correlate with histologic and virologic findings. Cancer. 74:1762–1767. 1994.PubMed/NCBI View Article : Google Scholar | |
Backes DM, Kurman RJ, Pimenta JM and Smith JS: Systematic review of human papillomavirus prevalence in invasive penile cancer. Cancer Causes Control. 20:449–457. 2009.PubMed/NCBI View Article : Google Scholar | |
Miralles-Guri C, Bruni L, Cubilla AL, Castellsagué X, Bosch FX and de Sanjosé S: Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol. 62:870–878. 2009.PubMed/NCBI View Article : Google Scholar | |
Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tân PF, Westra WH, Chung CH, Jordan RC, Lu C, et al: Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 363:24–35. 2010.PubMed/NCBI View Article : Google Scholar | |
Serup-Hansen E, Linnemann D, Skovrider-Ruminski W, Høgdall E, Geertsen PF and Havsteen H: Human papillomavirus genotyping and p16 expression as prognostic factors for patients with American Joint Committee on Cancer stages I to III carcinoma of the anal canal. J Clin Oncol. 32:1812–1817. 2014.PubMed/NCBI View Article : Google Scholar | |
Lont AP, Kroon BK, Horenblas S, Gallee MP, Berkhof J, Meijer CJ and Snijders PJ: Presence of high-risk human papillomavirus DNA in penile carcinoma predicts favorable outcome in survival. Int J Cancer. 119:1078–1081. 2006.PubMed/NCBI View Article : Google Scholar | |
Djajadiningrat RS, Jordanova ES, Kroon BK, van Werkhoven E, de Jong J, Pronk DT, Snijders PJ, Horenblas S and Heideman DA: Human papillomavirus prevalence in invasive penile cancer and association with clinical outcome. J Urol. 193:526–531. 2015.PubMed/NCBI View Article : Google Scholar | |
Lopes A, Bezerra ALR, Pinto CAL, Serrano SV, de Mello CA and Villa LL: p53 as a new prognostic factor for lymph node metastasis in penile carcinoma: Analysis of 82 patients treated with amputation and bilateral lymphadenectomy. J Urol. 168:81–86. 2002.PubMed/NCBI | |
Gross G and Pfister H: Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immunol (Berl). 193:35–44. 2004.PubMed/NCBI View Article : Google Scholar | |
Agarwal G, Gupta S and Spiess PE: Novel targeted therapies for the treatment of penile cancer. Expert Opin Drug Discov. 9:959–968. 2014.PubMed/NCBI View Article : Google Scholar | |
Flaherty A, Kim T, Giuliano A, Magliocco A, Hakky TS, Pagliaro LC and Spiess PE: Implications for human papillomavirus in penile cancer. Urol Oncol. 32:53.e1–8. 2014.PubMed/NCBI View Article : Google Scholar | |
Snijders PJ, Cromme FV, van den Brule AJ, Schrijnemakers HF, Snow GB, Meijer CJ and Walboomers JM: Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer. 51:845–850. 1992.PubMed/NCBI View Article : Google Scholar | |
Wilczynski SP, Lin BT, Xie Y and Paz IB: Detection of human papillomavirus DNA and oncoprotein overexpression are associated with distinct morphological patterns of tonsillar squamous cell carcinoma. Am J Pathol. 152:145–156. 1998.PubMed/NCBI | |
Ferreux E, Lont AP, Horenblas S, Gallee MP, Raaphorst FM, von Knebel Doeberitz M, Meijer CJ and Snijders PJ: Evidence for at least three alternative mechanisms targeting the p16INK4A/cyclin D/Rb pathway in penile carcinoma, one of which is mediated by high-risk human papillomavirus. J Pathol. 201:109–118. 2003.PubMed/NCBI View Article : Google Scholar | |
Cubilla AL, Lloveras B, Alejo M, Clavero O, Chaux A, Kasamatsu E, Monfulleda N, Tous S, Alemany L, Klaustermeier J, et al: Value of p16(INK)4(a) in the pathology of invasive penile squamous cell carcinomas: A report of 202 cases. Am J Surg Pathol. 35:253–261. 2011.PubMed/NCBI View Article : Google Scholar | |
Beder Ribeiro CM, Ferrer I, Santos de Farias AB, Fonseca DD, Morais Silva IH, Monteiro Gueiros LA, Carvalho AT, Porter SR and Leao JC: Oral and genital HPV genotypic concordance between sexual partners. Clin Oral Investig. 18:261–268. 2014.PubMed/NCBI View Article : Google Scholar | |
Deshmukh AA, Tanner RJ, Luetke MC, Hong YR, Sonawane Deshmukh K and Mainous AG III: Prevalence and risk of penile human papillomavirus infection: Evidence from the national health and nutrition examination survey 2013-2014. Clin Infect Dis. 64:1360–1366. 2017.PubMed/NCBI View Article : Google Scholar | |
Anic GM, Lee JH, Villa LL, Lazcano-Ponce E, Gage C, José C Silva R, Baggio ML, Quiterio M, Salmerón J, Papenfuss MR, et al: Risk factors for incident condyloma in a multinational cohort of men: The HIM study. J Infect Dis. 205:789–793. 2012.PubMed/NCBI View Article : Google Scholar | |
Vardas E, Giuliano AR, Goldstone S, Palefsky JM, Moreira ED Jr, Penny ME, Aranda C, Jessen H, Moi H, Ferris DG, et al: External genital human papillomavirus prevalence and associated factors among heterosexual men on 5 continents. J Infect Dis. 203:58–65. 2011.PubMed/NCBI View Article : Google Scholar | |
Winer RL, Hughes JP, Feng Q, O'Reilly S, Kiviat NB, Holmes KK and Koutsky LA: Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med. 354:2645–2654. 2006.PubMed/NCBI View Article : Google Scholar | |
Zhu YP, Jia ZW, Dai B, Ye DW, Kong YY, Chang K and Wang Y: Relationship between circumcision and human papillomavirus infection: A systematic review and meta-analysis. Asian J Androl. 19:125–131. 2017.PubMed/NCBI View Article : Google Scholar | |
Saibishkumar EP, Crook J and Sweet J: Neonatal circumcision and invasive squamous cell carcinoma of the penis: A report of 3 cases and a review of the literature. Can Urol Assoc J. 2:39–42. 2008.PubMed/NCBI View Article : Google Scholar | |
Albero G, Castellsagué X, Lin H-Y, Fulp W, Villa LL, Lazcano-Ponce E, Papenfuss M, Abrahamsen M, Salmerón J, Quiterio M, et al: Male circumcision and the incidence and clearance of genital human papillomavirus (HPV) infection in men: The HPV Infection in men (HIM) cohort study. BMC Infect Dis. 14(75)2014.PubMed/NCBI View Article : Google Scholar | |
Weaver BA, Feng Q, Holmes KK, Kiviat N, Lee SK, Meyer C, Stern M and Koutsky LA: Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis. 189:677–685. 2004.PubMed/NCBI View Article : Google Scholar | |
Boda D, Neagu M, Constantin C, Voinescu RN, Caruntu C, Zurac S, Spandidos DA, Drakoulis N, Tsoukalas D and Tsatsakis AM: HPV strain distribution in patients with genital warts in a female population sample. Oncol Lett. 12:1779–1782. 2016.PubMed/NCBI View Article : Google Scholar | |
Auvert B, Sobngwi-Tambekou J, Cutler E, Nieuwoudt M, Lissouba P, Puren A and Taljaard D: Effect of male circumcision on the prevalence of high-risk human papillomavirus in young men: Results of a randomized controlled trial conducted in Orange Farm, South Africa. J Infect Dis. 199:14–19. 2009.PubMed/NCBI View Article : Google Scholar | |
Tobian AAR, Serwadda D, Quinn TC, Kigozi G, Gravitt PE, Laeyendecker O, Charvat B, Ssempijja V, Riedesel M, Oliver AE, et al: Male circumcision for the prevention of HSV-2 and HPV infections and syphilis. N Engl J Med. 360:1298–1309. 2009.PubMed/NCBI View Article : Google Scholar | |
Giuliano AR, Viscidi R, Torres BN, Ingles DJ, Sudenga SL, Villa LL, Baggio ML, Abrahamsen M, Quiterio M, Salmeron J, et al: Seroconversion following anal and genital HPV infection in men: The HIM Study. Papillomavirus Res. 1:109–115. 2015.PubMed/NCBI View Article : Google Scholar | |
Lu B, Viscidi RP, Wu Y, Lee JH, Nyitray AG, Villa LL, Lazcano-Ponce E, da Silva RJ, Baggio ML, Quiterio M, et al: Prevalent serum antibody is not a marker of immune protection against acquisition of oncogenic HPV16 in men. Cancer Res. 72:676–685. 2012.PubMed/NCBI View Article : Google Scholar | |
Hillman RJ, Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Vardas E, Aranda C, Jessen H, Ferris DG, Coutlee F, et al: Immunogenicity of the quadrivalent human papillomavirus (type 6/11/16/18) vaccine in males 16 to 26 years old. Clin Vaccine Immunol. 19:261–267. 2012.PubMed/NCBI View Article : Google Scholar | |
Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Penny ME, Aranda C, Vardas E, Moi H, Jessen H, Hillman R, et al: Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. N Engl J Med. 364:401–411. 2011.PubMed/NCBI View Article : Google Scholar | |
Ghita MA, Caruntu C, Rosca AE, Kaleshi H, Caruntu A, Moraru L, Docea AO, Zurac S, Boda D, Neagu M, et al: Reflectance confocal microscopy and dermoscopy for in vivo, non-invasive skin imaging of superficial basal cell carcinoma. Oncol Lett. 11:3019–3024. 2016.PubMed/NCBI View Article : Google Scholar | |
Diaconeasa A, Boda D, Solovan C, Enescu DM, Vîlcea AM and Zurac S: Histopathologic features of Spitzoid lesions in different age groups. Rom J Morphol Embryol. 54:51–62. 2013.PubMed/NCBI | |
Căruntu C, Boda D, Guţu DE and Căruntu A: In vivo reflectance confocal microscopy of basal cell carcinoma with cystic degeneration. Rom J Morphol Embryol. 55:1437–1441. 2014.PubMed/NCBI | |
Lupu M, Caruntu A, Caruntu C, Boda D, Moraru L, Voiculescu V and Bastian A: Non-invasive imaging of actinic cheilitis and squamous cell carcinoma of the lip. Mol Clin Oncol. 8:640–646. 2018.PubMed/NCBI View Article : Google Scholar | |
Ianoși SL, Batani A, Ilie MA, Tampa M, Georgescu SR, Zurac S, Boda D, Ianosi NG, Neagoe D, Calina D, et al: Non-invasive imaging techniques for the in vivo diagnosis of Bowen's disease: Three case reports. Oncol Lett. 17:4094–4101. 2019.PubMed/NCBI View Article : Google Scholar | |
Lupu M, Caruntu C, Popa MI, Voiculescu VM, Zurac S and Boda D: Vascular patterns in basal cell carcinoma: Dermoscopic, confocal and histopathological perspectives. Oncol Lett. 17:4112–4125. 2019.PubMed/NCBI View Article : Google Scholar | |
Cioplea M, Caruntu C, Zurac S, Bastian A, Sticlaru L, Cioroianu A, Boda D, Jugulete G, Nichita L and Popp C: Dendritic cell distribution in mycosis fungoides vs. inflammatory dermatosis and other T-cell skin lymphoma. Oncol Lett. 17:4055–4059. 2019.PubMed/NCBI View Article : Google Scholar | |
Ilie MA, Caruntu C, Lupu M, Lixandru D, Tampa M, Georgescu SR, Bastian A, Constantin C, Neagu M, Zurac SA, et al: Current and future applications of confocal laser scanning microscopy imaging in skin oncology. Oncol Lett. 17:4102–4111. 2019.PubMed/NCBI View Article : Google Scholar | |
Ianoși SL, Forsea AM, Lupu M, Ilie MA, Zurac S, Boda D, Ianosi G, Neagoe D, Tutunaru C, Popa CM, et al: Role of modern imaging techniques for the in vivo diagnosis of lichen planus. Exp Ther Med. 17:1052–1060. 2019.PubMed/NCBI View Article : Google Scholar | |
Harder T, Wichmann O, Klug SJ, van der Sande MA and Wiese-Posselt M: Efficacy, effectiveness and safety of vaccination against human papillomavirus in males: A systematic review. BMC Med. 16(110)2018.PubMed/NCBI View Article : Google Scholar | |
Socea LI, Visan DC, Barbuceanu SF, Apostol TV, Bratu OG and Socea B: The antioxidant activity of some acylhydrazones with dibenzo[a,d][7]annulene moiety. Rev Chim Buchar. 69:795–797. 2018. | |
Spinu D, Bratu O, Marcu D, Mischianu D, Huica R, Surcel M, Munteanu A, Socea B, Bodean O and Ursaciuc C: The use of ELISA and PCR in identifying correlations between viral infections and benign prostatic hypertrophy. Rev Chim Buchar. 69:645–649. 2018. | |
Radulescu A, Madan V, Aungurenci A, Bratu O, Farcas C, Dinu M and Mischianu D: Antibiotic resistant urinary tract infections in an urology ward. Rom J Mil Med. 118:20–22. 2015. | |
Spinu D, Bratu O, Marcu D, Niculae A, Geavlete B, Diaconu C and Mischianu D: HPV and bladder cancer - is there a connection? Mod Med. 24:1–4. 2017. | |
Spinu D, Mischianu D, Bratu O, Aungurenci A, Manache S and Ciuca A: HPV implications in benign prostatic impairments -a literature review. Mod Med. 21:298–303. 2014. | |
Spinu D, Bratu O, Popescu R, Marcu D, Radulescu A and Mischianu D: Clostridium difficile - an emerging plague. Rom J Mil Med. 118:12–15. 2015. | |
Markowitz LE, Dunne EF, Saraiya M, Chesson HW, Curtis CR, Gee J, Bocchini JA Jr and Unger ER: Centers for Disease Control and Prevention (CDC): Human papillomavirus vaccination: Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 63:1–30. 2014.PubMed/NCBI | |
Petrosky E, Bocchini JA Jr, Hariri S, Chesson H, Curtis CR, Saraiya M, Unger ER and Markowitz LE: Centers for Disease Control and Prevention (CDC): Use of 9-valent human papillomavirus (HPV) vaccine: Updated HPV vaccination recommendations of the advisory committee on immunization practices. MMWR Morb Mortal Wkly Rep. 64:300–304. 2015.PubMed/NCBI | |
Boda D, Docea AO, Calina D, Ilie MA, Caruntu C, Zurac S, Neagu M, Constantin C, Branisteanu DE, Voiculescu V, et al: Human papilloma virus: Apprehending the link with carcinogenesis and unveiling new research avenues (Review). Int J Oncol. 52:637–655. 2018.PubMed/NCBI View Article : Google Scholar |