Identification and genotyping of human papillomavirus in a Spanish cohort of penile squamous cell carcinomas: Correlation with pathologic subtypes, p16INK4a expression, and prognosis

Journal of the American Academy of Dermatology

Volumn 68, Issue 1, 2013, Pages 73-82

  Ferrándiz Pulido, Carla ^a,b   Masferrer, Emili ^c,d   De Torres, Ines ^a   Lloveras, Belen ^d,e   Hernandez Losa, Javier ^a   Mojal, Sergio ^d   Salvador, Carlos ^a   Morote, Juan ^a   Ramon Y Cajal, Santiago ^a   Pujol, Ramon M ^d   Garcia Patos, Vicente ^a,b   Toll, Agustin ^b,d  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^e CATALAN INSTITUTE OF ONCOLOGY   (Spain)

Author keywords

human papillomavirus; p16INK4a; penile intraepithelial neoplasia; penis; squamous cell carcinoma; survival

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A;

ADULT; AGED; ARTICLE; CANCER INVASION; CANCER PROGNOSIS; COHORT ANALYSIS; ENZYME IMMUNOASSAY; GENE OVEREXPRESSION; GENOTYPE; HISTOLOGY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HYBRIDIZATION; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; NONHUMAN; PENILE INTRAEPITHELIAL NEOPLASIA; PENILE SQUAMOUS CELL CARCINOMA; PENIS CANCER; PENIS CARCINOMA; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SQUAMOUS CELL CARCINOMA; VIRUS DETECTION; WART VIRUS;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA IN SITU; CARCINOMA, SQUAMOUS CELL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; GENOTYPE; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PENILE NEOPLASMS; PREVALENCE; PROGNOSIS; RETROSPECTIVE STUDIES; SPAIN;

EID: 84870894590     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2012.05.029     Document Type: Article

References (49)

1. M.C. Bleeker, D.A. Heideman, P.J. Snijders, S. Horenblas, J. Dillner, and C.J. Meijer Penile cancer: epidemiology, pathogenesis and prevention World J Urol 27 2009 141 150
2. A.L. Cubilla The role of pathologic prognostic factors in squamous cell carcinoma of the penis World J Urol 27 2009 169 177
3. C. Renaud-Vilmer, B. Cavelier-Balloy, O. Verola, P. Morel, J.M. Servant, and F. Desgrandchamps Analysis of alterations adjacent to invasive squamous cell carcinoma of the penis and their relationship with associated carcinoma J Am Acad Dermatol 62 2010 284 290
4. A. Chaux, R. Pfannl, B. Lloveras, M. Alejo, O. Clavero, and C. Lezcano Distinctive association of p16INK4a overexpression with penile intraepithelial neoplasia depicting warty and/or basaloid features: a study of 141 cases evaluating a new nomenclature Am J Surg Pathol 34 2010 385 392
5. A. Chaux, E.F. Velazquez, A. Amin, A. Soskin, R. Pfannl, and I.M. Rodríguez Distribution and characterization of subtypes of penile intraepithelial neoplasia and their association with invasive carcinomas: a pathological study of 139 lesions in 121 patients Hum Pathol 43 2012 1020 1027
6. A. Pascual, M. Pariente, J.M. Godínez, R. Sánchez-Prieto, M. Atienzar, and M. Segura High prevalence of human papillomavirus 16 in penile carcinoma Histol Histopathol 22 2007 177 183
7. D. Guerrero, R. Guarch, A. Ojer, J.M. Casas, S. Ropero, and A. Mancha Hypermethylation of the thrombospondin-1 gene is associated with poor prognosis in penile squamous cell carcinoma BJU Int 102 2008 747 755
8. V. Gentile, P. Vicini, L. Giacomelli, M.R. Cardillo, A. Pierangeli, and A.M. Degener Detection of human papillomavirus DNA, p53 and ki67 expression in penile carcinomas Int J Immunopathol Pharmacol 19 2006 209 215
9. G. Perceau, C. Derancourt, C. Clavel, A. Durlach, M. Pluot, and B. Lardennois Lichen sclerosus is frequently present in penile squamous cell carcinomas but is not always associated with oncogenic human papillomavirus Br J Dermatol 148 2003 934 938
10. N. Muñoz, F.X. Bosch, S. de Sanjosé, R. Herrero, X. Castellsagué, and K.V. Shah Epidemiologic classification of human papillomavirus types associated with cervical cancer N Engl J Med 348 2003 518 527
11. O. Kayes, H.U. Ahmed, M. Arya, and S. Minhas Molecular and genetic pathways in penile cancer Lancet Oncol 8 2007 420 429
12. A.P. Lont, B.K. Kroon, S. Horenblas, M.P. Gallee, J. Berkhof, and C.J. Meijer Presence of high-risk human papillomavirus DNA in penile carcinoma predicts favorable outcome in survival Int J Cancer 119 2006 1078 1081
13. A.L. Bezerra, A. Lopes, G.H. Santiago, K.C. Ribeiro, M.R. Latorre, and L.L. Villa Human papillomavirus as a prognostic factor in carcinoma of the penis: analysis of 82 patients treated with amputation and bilateral lymphadenectomy Cancer 91 2001 2315 2321
14. E.E. Doxtader, and A.L. Katzenstein 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 43 2012 327 332
15. 4(a) in the pathology of invasive penile squamous cell carcinomas: a report of 202 cases Am J Surg Pathol 35 2011 253 261
16. E. Stankiewicz, D.M. Prowse, E. Ktori, J. Cuzick, L. Ambroisine, and X. Zhang The retinoblastoma protein/p16 INK4A pathway but not p53 is disrupted by human papillomavirus in penile squamous cell carcinoma Histopathology 58 2011 433 439
17. D.M. Prowse, E.N. Ktori, D. Chandrasekaran, A. Prapa, and S. Baithun Human papillomavirus-Associated increase in p16INK4A expression in penile lichen sclerosus and squamous cell carcinoma Br J Dermatol 158 2008 261 265
18. M. Poetsch, M. Hemmerich, C. Kakies, B. Kleist, E. Wolf, and F. vom Dorp Alterations in the tumor suppressor gene p16(INK4A) are associated with aggressive behavior of penile carcinomas Virchows Arch 458 2011 221 229
19. E. Ferreux, A.P. Lont, S. Horenblas, M.P. Gallee, F.M. Raaphorst, and M. von Knebel Doeberitz 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 2003 109 118
20. B. Kleter, L.J. Van Doorn, L. Schrauwen, A. Molijn, S. Sastrowijoto, and J. ter Schegget Development and clinical evaluation of a highly sensitive PCR-reverse hybridization line probe assay for detection and identification of anogenital human papillomavirus J Clin Microbiol 37 1999 2508 2517
21. C.B. Lajer, and C. von Buchwald The role of human papillomavirus in head and neck cancer APMIS 118 2010 510 519
22. S. Marur, G. D'Souza, W.H. Westra, and A.A. Forastiere HPV-Associated head and neck cancer: a virus-related cancer epidemic Lancet Oncol 11 2010 781 789
23. H.P. Van de Nieuwenhof, L.C. van Kempen, J.A. de Hullu, R.L. Bekkers, J. Bulten, and W.J. Melchers The etiologic role of HPV in vulvar squamous cell carcinoma fine tuned Cancer Epidemiol Biomarkers Prev 18 2009 2061 2067
24. I.A. Van der Avoort, H. Shirango, B.M. Hoevenaars, J.M. Grefte, J.A. de Hullu, and P.C. de Wilde Vulvar squamous cell carcinoma is a multifactorial disease following two separate and independent pathways Int J Gynecol Pathol 25 2006 22 29
25. C. Miralles-Guri, L. Bruni, A.L. Cubilla, X. Castellsagué, F.X. Bosch, and S. de Sanjosé Human papillomavirus prevalence and type distribution in penile carcinoma J Clin Pathol 62 2009 870 878
26. D. Krustrup, H.L. Jensen, A.J. van den Brule, and M. Frisch Histological characteristics of human papilloma-virus-positive and -negative invasive and in situ squamous cell tumors of the penis Int J Exp Pathol 90 2009 182 189
27. D.A. Heideman, T. Waterboer, M. Pawlita, P. Delis-van Diemen, I. Nindl, and J.A. Leijte Human papillomavirus-16 is the predominant type etiologically involved in penile squamous cell carcinoma J Clin Oncol 25 2007 4550 4556
28. K.W. Chan, K.Y. Lam, A.C. Chan, P. Lau, and G. Srivastava Prevalence of human papillomavirus types 16 and 18 in penile carcinoma: a study of 41 cases using PCR J Clin Pathol 47 1994 823 826
29. G.M. Clifford, S. Gallus, R. Herrero, N. Muñoz, P.J. Snijders, S. Vaccarella Prevalence Surveys Study Group Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis Lancet 366 2005 991 998
30. M. Senba, A. Kumatori, S. Fujita, P. Jutavijittum, A. Yousukh, and T. Moriuchi The prevalence of human papillomavirus genotypes in penile cancers from northern Thailand J Med Virol 78 2006 1341 1346
31. M.A. Rubin, B. Kleter, M. Zhou, G. Ayala, A.L. Cubilla, and W.G. Quint Detection and typing of human papillomavirus DNA in penile carcinoma: evidence for multiple independent pathways of penile carcinogenesis Am J Pathol 159 2001 1211 1218
32. A.L. Bezerra, A. Lopes, G. Landman, G.N. Alencar, H. Torloni, and L.L. Villa Clinicopathologic features and human papillomavirus DNA prevalence of warty and squamous cell carcinoma of the penis Am J Surg Pathol 25 2001 673 678
33. A.L. Cubilla, B. Lloveras, M. Alejo, O. Clavero, A. Chaux, and E. Kasamatsu The basaloid cell is the best tissue marker for human papillomavirus in invasive penile squamous cell carcinoma: a study of 202 cases from Paraguay Am J Surg Pathol 34 2010 104 114
34. M.N. de Koning, W.G. Quint, and E.C. Pirog Prevalence of mucosal and cutaneous human papillomaviruses in different histologic subtypes of vulvar carcinoma Mod Pathol 21 2008 334 344
35. M. Frisch, C. Fenger, A.J. van den Brule, P. Sorensen, C.J. Meijer, and J.M. Walboomers Variants of squamous cell carcinoma of the anal canal and perianal skin and their relation to human papillomaviruses Cancer Res 59 1999 753 757
36. E.F. Velazquez, G. Ayala, H. Liu, A. Chaux, M. Zanotti, and J. Torres Histologic grade and perineural invasion are more important than tumor thickness as predictor of nodal metastasis in penile squamous cell carcinoma invading 5 to 10 mm Am J Surg Pathol 32 2008 974 979
37. J.P. Klussman, J.J. Mooren, M. Lehnen, S.M. Claessen, M. Stenner, and C.U. Huebbers Genetic signatures of HPV-related and unrelated oropharyngeal carcinoma and their prognostic implications Clin Cancer Res 15 2009 1779 1786
38. K. Lindel, K.T. Beer, J. Laissue, R.H. Greiner, and D.M. Aebersold Human papillomavirus positive squamous cell carcinoma of the oropharynx: a radiosensitive subgroup of head and neck carcinoma Cancer 92 2001 805 813
39. A.C. Nichols, W.C. Faquin, W.H. Westra, E.A. Mroz, S. Begum, and J.R. Clark HPV-16 infection predicts treatment outcome in oropharyngeal squamous cell carcinoma Otolaryngol Head Neck Surg 140 2009 228 234
40. A.R. Sedaghat, Z. Zhang, S. Begum, R. Palermo, S. Best, and K.M. Ulmer Prognostic significance of human papillomavirus in oropharyngeal squamous cell carcinomas Laryngoscope 119 2009 1542 1549
41. K.K. Ang, J. Harris, R. Wheeler, R. Weber, D.I. Rosenthal, and P.F. Nguyen-Tân Human papillomavirus and survival of patients with oropharyngeal cancer N Engl J Med 363 2010 24 35
42. C. Fakhry, W.H. Westra, S. Li, A. Cmelak, J.A. Ridge, and H. Pinto Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial J Natl Cancer Inst 100 2008 261 269
43. G.F. Huber, A. Albinger-Hegyi, A. Soltermann, M. Roessle, N. Graf, and S.K. Haerle Expression patterns of Bmi-1 and p16 significantly correlate with overall, disease-specific, and recurrence-free survival in oropharyngeal squamous cell carcinoma Cancer 117 2011 4659 4670
44. INK4a in nonmelanoma skin cancer Dermatol Surg 30 2004 409 414
45. M. Śnietura, M. Jaworska, W. Pigłowski, A. Goraj-Zajac, G. Woźniak, and D. Lange High-risk HPV DNA status and p16 (INK4a) expression as prognostic markers in patients with squamous cell cancer of oral cavity and oropharynx Pol J Pathol 61 2010 133 139
46. P. Schulz, A. Scholz, A. Rexin, P. Hauff, M. Schirner, and B. Wiedenmann Inducible re-expression of p16 in an orthotopic mouse model of pancreatic cancer inhibits lymphangiogenesis and lymphatic metastasis Br J Cancer 99 2008 110 117
47. M.R. Cupp, R.S. Malek, J.R. Goellner, T.F. Smith, and M.J. Espy The detection of human papillomavirus deoxyribonucleic acid in intraepithelial, in situ, verrucous and invasive carcinoma of the penis J Urol 154 1995 1024 1029
48. J.R. Daling, M.M. Madeleine, L.G. Johnson, S.M. Schwartz, K.A. Shera, and M.A. Wurscher Penile cancer: importance of circumcision, human papillomavirus and smoking in in situ and invasive disease Int J Cancer 116 2005 606 616
49. G. Gross, and H. Pfister Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts Med Microbiol Immunol 193 2004 35 44