Penile cancer: Epidemiology, pathogenesis and prevention

World Journal of Urology

Volumn 27, Issue 2, 2009, Pages 141-150

  Bleeker, M C G ^a   Heideman, D A M ^a   Snijders, P J F ^a   Horenblas, S ^b   Dillner, J ^c   Meijer, C J L M ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Erythroplasia of Queyrat; Flat penile lesions; Genital Bowen's disease; Human papillomavirus; Lichen sclerosis; Molecular pathogenesis; Penile cancer; Penile intraepithelial neoplasia; Prevention

Indexed keywords

CLASSIFICATION; HUMAN; MALE; PENIS TUMOR; REVIEW;

HUMANS; MALE; PENILE NEOPLASMS;

EID: 63649084378     PISSN: 07244983     EISSN: 14338726     Source Type: Journal    
DOI: 10.1007/s00345-008-0302-z     Document Type: Review

References (99)

1. Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR (2007) Incidence trends in primary malignant penile cancer. Urol Oncol 25(5):361-367
2. Pukkala E, Weiderpass E (2002) Socio-economic differences in incidence rates of cancers of the male genital organs in Finland, 1971-1995. Int J Cancer 102(6):643-648
3. Rubin MA, Kleter B, Zhou M, Ayala G, Cubilla AL, Quint WG, Pirog EC (2001) Detection and typing of human papillomavirus DNA in penile carcinoma: Evidence for multiple independent pathways of penile carcinogenesis. Am J Pathol 159(4):1211-1218
4. Wabinga HR, Parkin DM, Wabwire-Mangen F, Nambooze S (2000) Trends in cancer incidence in Kyadondo County, Uganda, 1960-1997. Br J Cancer 82(9):1585-1592
5. Parkin DM, Muir CS (1992) Cancer incidence in five continents. Comparability and quality of data. IARC Sci Publ (120):45-173.
6. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ (2007) Cancer statistics, 2007. CA Cancer J Clin 57(1):43-66
7. Maden C, Sherman KJ, Beckmann AM, Hislop TG, Teh CZ, Ashley RL, Daling JR (1993) History of circumcision, medical conditions, and sexual activity and risk of penile cancer (see comments). J Natl Cancer Inst 85(1):19-24
8. Moses S, Bailey RC, Ronald AR (1998) male circumcision: Assessment of health benefits and risks. Sex Transm Infect 74(5):368-373
9. Schoen EJ, Oehrli M, Colby C, Machin G (2000) The highly protective effect of newborn circumcision against invasive penile cancer. Pediatrics 105(3):E36
10. Dillner J, von Krogh G, Horenblas S, Meijer CJLM (2000) Etiology of squamous cell carcinoma of the penis. Scand J Urol Nephrol 34:189-193
11. Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, Carter JJ, Porter PL, Porter PL, Galloway DA, McDougall JK, Krieger JN (2005) Penile cancer: Importance of circumcision, human papillomavirus and smoking in in situ and invasive disease. Int J Cancer 116(4):606-616
12. Gross G, Pfister H (2004) Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immunol (Berl) 193(1):35-44
13. Reddy DG, Baruah IK (1963) Carcinogenic action of human smegma. Arch Pathol 75:414-420
14. Misra S, Chaturvedi A, Misra NC (2004) Penile carcinoma: A challenge for the developing world. Lancet Oncol 5(4):240-247
15. McCance DJ, Kalache A, Ashdown K, Andrade L, Menezes F, Smith P, Doll R (1986) Human papillomavirus types 16 and 18 in carcinomas of the penis from Brazil. Int J Cancer 37(1):55-59
16. Heideman DA, Waterboer T, Pawlita M, Delis-van Diemen P, Nindl I, Leijte JA, Bonfrer JM, Horenblas S, Meijer CJ, Snijders PJ (2007) Human papillomavirus-16. Is the predominant type etiologically involved in penile squamous cell carcinoma. J Clin Oncol 25(29):4550-4556
17. Gregoire L, Cubilla AL, Reuter VE, Haas GP, Lancaster WD (1995) Preferential association of human papillomavirus with high-grade histologic variants of penile-invasive squamous cell carcinoma. J Natl Cancer Inst 87(22):1705-1709
18. Parkin DM, Bray F (2006) Vaccine. Chapter 2: The burden of HPV-related cancers. Suppl 3:S11-S25.
19. Bjorge T, Dillner J, Anttila T, Engeland A, Hakulinen T, Jellum E, Lehtinen M, Luostarinen T, Paavonen J, Pukkala E, Sapp M, Schiller J, Youngman L, Thoresen S (1997) Prospective seroepidemiological study of role of human papillomavirus in non-cervical anogenital cancers. BMJ 315(7109):646-649
20. Carter JJ, Madeleine MM, Shera K, Schwartz SM, Cushing-Haugen KL, Wipf GC, Porter P, Daling JR, McDougall JK, Galloway DA (2001) Human papillomavirus 16 and 18 l1 serology compared across anogenital cancer sites. Cancer Res 61(5):1934-1940
21. van Doornum GJ, Korse CM, Buning-Kager JC, Bonfrer JM, Horenblas S, Taal BG, Dillner J (2003) Reactivity to human papillomavirus type 16 l1 virus-like particles in sera from patients with genital cancer and patients with carcinomas at five different extragenital sites. Br J Cancer 88(7):1095-1100
22. Newton R, Bousarghin L, Ziegler J, Casabonne D, Beral V, Mbidde E, Carpenter L, Parkin DM, Wabinga H, Mbulaiteye S, Jaffe H, Touze A, Coursaget P (2004) Human papillomaviruses and cancer in Uganda. Eur J Cancer Prev 13(2):113-118
23. Dorfman S, Cavazza M, Cardozo J (2006) Penile cancer associated with so-called low-risk human papilloma virus. Report of five cases from rural Venezuela. Trop Doct 36(4):232-233
24. Senba M, Kumatori A, Fujita S, Jutavijittum P, Yousukh A, Moriuchi T, Nakamura T, Toriyama K (2006) The prevalence of human papillomavirus genotypes in penile cancers from Northern Thailand. J Med Virol 78(10):1341-1346
25. Wieland U, Jurk S, Weissenborn S, Krieg T, Pfister H, Ritzkowsky A (2000) Erythroplasia of queyrat: Coinfection with cutaneous carcinogenic human papillomavirus type 8 and genital papillomaviruses in a carcinoma in situ. J Invest Dermatol 115(3):396-401
26. Hellberg D, Valentin J, Eklund T, Nilsson S (1987) Penile cancer: Is there an epidemiological role for smoking and sexual behaviour? Br Med J (Clin Res Ed) 295(6609):1306-1308
27. Harish K, Ravi R (1995) The role of tobacco in penile carcinoma. Br J Urol 75(3):375-377
28. Cubilla AL, Velazquez EF, Young RH (2004) Epithelial lesions associated with invasive penile squamous cell carcinoma: A pathologic study of 288 cases. Int J Surg Pathol 12(4):351-364
29. Cubilla AL, Reuter VE, Gregoire L, Ayala G, Ocampos S, Lancaster WD, Fair W (1998) Basaloid squamous cell carcinoma: A distinctive human papilloma virus- related penile neoplasm: A report of 20 cases. Am J Surg Pathol 22(6):755-761
30. Cubilla AL, Velazques EF, Reuter VE, Oliva E, Mihm MC Jr, Young RH (2000) Warty (condylomatous) squamous cell carcinoma of the penis: A report of 11 cases and proposed classification of 'verruciform' penile tumors. Am J Surg Pathol 24(4):505-512
31. van Geel AN, den Bakker MA, Kirkels W, Horenblas S, Kroon BB, de Wilt JH, Eggermont AM, Mooi WJ, van der Aa MN (2007) Prognosis of primary mucosal penile melanoma: A series of 19 Dutch patients and 47 patients from the literature. Urology 70(1):143-147
32. Fetsch JF, Davis CJ Jr, Miettinen M, Sesterhenn IA (2004) Leiomyosarcoma of the penis: A clinicopathologic study of 14 cases with review of the literature and discussion of the differential diagnosis. Am J Surg Pathol 28(1):115-125
33. Cubilla AL, Velazquez EF, Young RH (2004) Pseudohyperplastic squamous cell carcinoma of the penis associated with lichen sclerosus. An extremely well-differentiated, nonverruciform neoplasm that preferentially affects the foreskin and is frequently misdiagnosed: A report of 10 cases of a distinctive clinicopathologic entity. Am J Surg Pathol 28(7):895-900
34. Bezerra AL, Lopes A, Santiago GH, Ribeiro KC, Latorre MR, Villa LL (2001) Human papillomavirus as a prognostic factor in carcinoma of the penis: Analysis of 82 patients treated with amputation and bilateral lymphadenectomy. Cancer 91(12):2315-23211
35. Ferreux E, Lont AP, Horenblas S, Gallee MPW, Raaphorst FM, Doeberitz MV, Meijer CJLM, Snijders PJF (2003) Evidence for at least three alternative mechanisms targeting the P16(INK4A)/Cyclin D/Rb Pathway in penile carcinoma, one of which is mediated by high-risk human papillomavirus. J Pathol 201(1):109-118
36. Canavan TP, Cohen D (2002) Vulvar cancer. Am Fam Physician 66(7):1269-1274
37. Lont AP, Kroon BK, Horenblas S, Gallee MP, Berkhof J, Meijer CJ, Snijders PJ (2006) Presence of high-risk human papillomavirus DNA in penile carcinoma predicts favorable outcome in survival. Int J Cancer 119(5):1078-1081
38. Barrasso R, de Brux J, Croissant O, Orth G (1987) High prevalence of papillomavirus-associated penile intraepithelial neoplasia in sexual partners of women with cervical intraepithelial neoplasia. N Engl J Med 317(15):916-923
39. Porter WM, Francis N, Hawkins D, Dinneen M, Bunker CB (2002) Penile intraepithelial neoplasia: Clinical spectrum and treatment of 35 cases. Br J Dermatol 147(6):1159-1165
40. Hahn A, Loning T, Hoos A, Henke P (1988) Immunohistochemistry (S 100, KL 1) and human papillomavirus DNA hybridization on morbus bowen and bowenoid papulosis. Virchows Arch A Pathol Anat Histopathol 413(2):113-122
41. Ikenberg H, Gissmann L, Gross G, Grussendorf-Conen EI, zur Hausen H (1983) Human papillomavirus type-16-related DNA in genital Bowen's disease and in bowenoid papulosis. Int J Cancer 32(5):563-565
42. Kaye V, Zhang G, Dehner LP, Fraley EE (1990) Carcinoma in situ of penis. Is distinction between erythroplasia of queyrat and Bowen's disease relevant? Urology 36(6):479-482
43. von Krogh G, Horenblas SN (2000) Diagnosis and clinical presentation of premalignant lesions of the penis. Scand J Urol Nephrol 34:201-214
44. Obalek S, Jablonska S, Beaudenon S, Walczak L, Orth G (1986) Bowenoid papulosis of the Male and Female Genitalia: Risk of Cervical Neoplasia. J Am Acad Dermatol 14(3):433-444
45. Ammin BA, Tamboli P, Cubilla AL (2003) Penis and Scrotum. In: Weidner N, Cote RJ, Suster S, Weiss LM (eds) Modern surgical pathology. Elsevier Science, Philadelphia, pp 1197-1214
46. Barrasso R (1997) Latent and subclinical HPV external anogenital infection. Clin Dermatol 15(3):349-353
47. Hippelainen M, Yliskoski M, Saarikoski S, Syrjanen S, Syrjanen K (1991) Genital human papillomavirus lesions of the male sexual partners: The diagnostic accuracy of peniscopy (see comments). Genitourin Med 67(4):291-296
48. Bleeker MC, Hogewoning CJ, van den Brule AJ, Voorhorst FJ, Van Andel RE, Risse EK, Starink TM, Meijer CJ (2002) Penile lesions and human papillomavirus in male sexual partners of women with cervical intraepithelial neoplasia. J Am Acad Dermatol 47(3):351-357
49. Bleeker MC, Snijders PF, Voorhorst FJ, Meijer CJ (2006) Flat penile lesions: The infectious "Invisible" link in the transmission of human papillomavirus. Int J Cancer 119(11):2505-2512
50. Kataoka A, Claesson U, Hansson BG, Eriksson M, Lindh E (1991) Human papillomavirus infection of the male diagnosed by Southern-blot hybridization and polymerase chain reaction: Comparison between urethra samples and penile biopsy samples. J Med Virol 33(3):159-164
51. Hippelainen M, Syrjanen S, Hippelainen M, Koskela H, Pulkkinen J, Saarikoski S, Syrjanen K (1993) Prevalence and risk factors of genital human papillomavirus (HPV) infections in healthy males: A study on Finnish Conscripts. Sex Transm Dis 20(6):321-328
52. Chu QD, Vezeridis MP, Libbey NP, Wanebo HJ (1994) Giant condyloma acuminatum (Buschke-Lowenstein tumor) of the anorectal and perianal regions. analysis of 42 cases. Dis Colon Rectum 37(9):950-957
53. Trombetta LJ, Place RJ (2001) Giant condyloma acuminatum of the anorectum: Trends in epidemiologyRand management: report of a case and review of the literature. Dis Colon Rectum 44(12):1878-1886
54. Grussendorf-Conen EI (1997) Anogenital premalignant and malignant Tumors (including Buschke-Lowenstein tumors). Clin Dermatol 15(3):377-388
55. Powell JJ, Wojnarowska F (1999) Lichen sclerosus. Lancet 353(9166):1777-1783
56. Meffert JJ, Davis BM, Grimwood RE (1995) Lichen sclerosus. J Am Acad Dermatol 32(3):393-416
57. Velazquez EF, Cubilla AL (2003) Lichen sclerosus in 68 patients with squamous cell carcinoma of the penis: Frequent atypias and correlation with special carcinoma variants suggests a precancerous role. Am J Surg Pathol 27(11):1448-1453
58. Carli P, Cattaneo A, De Magnis A, Biggeri A, Taddei G, Giannotti B (1995) Squamous cell carcinoma arising in vulval lichen sclerosus: A longitudinal cohort study. Eur J Cancer Prev 4(6):491-495
59. Perceau G, Derancourt C, Clavel C, Durlach A, Pluot M, Lardennois B, Bernard P (2003) Lichen sclerosus is frequently present in penile squamous cell carcinomas but is not always associated with oncogenic human papillomavirus. Br J Dermatol 148(5):934-938
60. Powell J, Robson A, Cranston D, Wojnarowska F, Turner R (2001) High incidence of lichen sclerosus in patients with squamous cell carcinoma of the penis. Br J Dermatol 145(1):85-89
61. Nasca MR, Innocenzi D, Micali G (1999) Penile cancer among patients with genital lichen sclerosus. J Am Acad Dermatol 41(6):911-914
62. Nasca MR, Innocenzi D, Micali G (2006) Association of penile lichen sclerosus and oncogenic human papillomavirus infection. Int J Dermatol 45(6):681-683
63. Snijders PJ, Steenbergen RD, Heideman DA, Meijer CJ (2006) HPV-mediated cervical carcinogenesis: Concepts and clinical implications. J Pathol 208(2):152-164
64. zur Hausen H (2002) Papillomaviruses and cancer: From basic studies to clinical application. Nat Rev Cancer 2(5):342-350
65. Scheffner M, Romanczuk H, Munger K, Huibregtse JM, Mietz JA, Howley PM (1994) Functions of human papillomavirus proteins. Curr Top Microbiol Immunol 186:83-99
66. Steenbergen RD, Kramer D, Meijer CJ, Walboomers JM, Trott DA, Cuthbert AP, Newbold RF, Overkamp WJ, Zdzienicka MZ, Snijders PJ (2001) Telomerase suppression by chromosome 6 in a human papillomavirus type 16-immortalized keratinocyte cell line and in a cervical cancer cell line. J Natl Cancer Inst 93(11):865-872
67. Franceschi S, Castellsague X, Dal Maso L, Smith JS, Plummer M, Ngelangel C, Chichareon S, Eluf-Neto J, Shah KV, Snijders PJ, Meijer CJ, Bosch FX, Munoz N (2002) Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 86(5):705-711
68. Bleeker MC, Hogewoning CJ, Berkhof J, Voorhorst FJ, Hesselink AT, van Diemen PM, van den Brule AJ, Snijders PJ, Meijer CJ (2005) Concordance of specific human papillomavirus types in sex partners is more prevalent than would be expected by chance and is associated with increased viral loads. Clin Infect Dis 41(5):612-620
69. Martins AC, Faria SM, Cologna AJ, Suaid HJ, Tucci S Jr (2002) Immunoexpression of P53 protein and proliferating cell nuclear antigen in penile carcinoma. J Urol 167(1):89-92
70. Scinicariello F, Rady P, Hannigan E, Dinh TV, Tyring SK (1992) Human papillomavirus type 16 found in primary transitional cell carcinoma of the bartholin's gland and in a lymph node metastasis. Gynecol Oncol 47(2):263-266
71. Leis PF, Stevens KR, Baer SC, Kadmon D, Goldberg LH, Wang XJ (1998) AC-RasHa mutation in the metastasis of a human papillomavirus (HPV)-18 positive penile squamous cell carcinoma suggests a cooperative effect between HPV-18 and C-RasHa activation in malignant progression. Cancer 83(1):122-129
72. Couturier J, Sastre-Garau X, Schneider-Maunoury S, Labib A, Orth G (1991) Integration of papillomavirus DNA near Myc genes in genital carcinomas and its consequences for proto-oncogene Expression. J Virol 65(8):4534-4538
73. Sastre-Garau X, Favre M, Couturier J, Orth G (2000) Distinct patterns of alteration of myc genes associated with integration of human papillomavirus type 16 or type 45 DNA in two genital tumours. J Gen Virol 81(Pt 8):1983-1993
74. Campos RS, Lopes A, Guimaraes GC, Carvalho AL, Soares FA (2006) E-Cadherin, MMP-2, and MMP-9 as prognostic markers in penile cancer: analysis of 125 patients. Urology 67(4):797-802
75. Golijanin D, Tan JY, Kazior A, Cohen EG, Russo P, Dalbagni G, Auborn KJ, Subbaramaiah K, Dannenberg AJ (2004) Cyclooxygenase-2 and microsomal prostaglandin E synthase-1 are overexpressed in squamous cell carcinoma of the penis. Clin Cancer Res 10(3):1024-1031
76. Kayes O, Ahmed HU, Arya M, Minhas S (2007) Molecular and genetic pathways in penile cancer. Lancet Oncol 8(5):420-429
77. Soufir N, Queille S, Liboutet M, Thibaudeau O, Bachelier F, Delestaing G, Balloy BC, Breuer J, Janin A, Dubertret L, Vilmer C, Basset-Seguin N (2007) Inactivation of the CDKN2A and the P53 tumour suppressor genes in external genital carcinomas and their precursors. Br J Dermatol 156(3):448-453
78. Castren K, Vahakangas K, Heikkinen E, Ranki A (1998) Absence of P53 mutations in benign and pre-malignant male genital lesions with over-expressed P53 protein. Int J Cancer 77(5):674-678
79. Pilotti S, Donghi R, D'Amato L, Giarola M, Longoni A, Della Torre G, De Palo G, Pierotti MA, Rilke F (1993) HPV detection and P53 alteration in squamous cell verrucous malignancies of the lower genital tract. Diagn Mol Pathol 2(4):248-256
80. Ranki A, Lassus J, Niemi KM (1995) Relation of P53 tumor suppressor protein expression to human papillomavirus (HPV) DNA and to cellular atypia in male genital warts and in premalignant lesions. Acta Derm Venereol 75(3):180-186
81. Castellsague X, Bosch FX, Munoz N, Meijer CJ, Shah KV, de Sanjose S, Eluf-Neto J, Ngelangel CA, Chichareon S, Smith JS, Herrero R, Moreno V, Franceschi S (2002) Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med 346(15):1105-1112
82. Vaccarella S, Lazcano-Ponce E, Castro-Garduno JA, Cruz-Valdez A, Diaz V, Schiavon R, Hernandez P, Kornegay JR, Hernandez-Avila M, Franceschi S (2006) Prevalence and determinants of human papillomavirus infection in men attending vasectomy clinics in Mexico. Int J Cancer 119(8):1934-1939
83. Levine RU, Crum CP, Herman E, Silvers D, Ferenczy A, Richart RM (1984) Cervical papillomavirus infection and intraepithelial neoplasia: A study of male sexual partners. Obstet Gynecol 64(1):16-20
84. Bleeker MC, Hogewoning CJ, Voorhorst FJ, van den Brule AJ, Berkhof J, Hesselink AT, Lettink M, Starink TM, Stoof TJ, Snijders PJ, Meijer CJ (2005) HPV-associated flat penile lesions in men of a non-STD hospital population: Less frequent and smaller in size than in male sexual partners of women with CIN. Int J Cancer 113(1):36-41
85. Schoen EJ, Colby CJ, To TT (2006) Cost analysis of neonatal circumcision in a large health maintenance organization. J Urol 175(3 Pt 1):1111-1115
86. Van Howe RS (1999) Does circumcision influence sexually transmitted diseases? A literature review. BJU Int 83(Suppl 1):52-62
87. Siegfried N, Muller M, Deeks J, Volmink J, Egger M, Low N, Walker S, Williamson P (2005) HIV and male circumcision - a systematic review with assessment of the quality of studies. Lancet Infect Dis 5(3):165-173
88. Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, Jenkins D, Schuind A, Costa Clemens SA, Dubin G (2006) Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: Follow-up from a randomised control trial. Lancet 367(9518):1247-1255
89. Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, Zahaf T, Innis B, Naud P, De Carvalho NS, Roteli-Martins CM, Teixeira J, Blatter MM, Korn AP, Quint W, Dubin G (2004) Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: A randomised controlled trial. Lancet 364(9447):1757-1765
90. Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, Wheeler CM, Koutsky LA, Malm C, Lehtinen M, Skjeldestad FE, Olsson SE, Steinwall M, Brown DR, Kurman RJ, Ronnett BM, Stoler MH, Ferenczy A, Harper DM, Tamms GM, Yu J, Lupinacci L, Railkar R, Taddeo FJ, Jansen KU, Esser MT, Sings HL, Saah AJ, Barr E (2005) Prophylactic Quadrivalent Human Papillomavirus (Types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: A randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 6(5):271-278
91. Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, Tang GW, Ferris DG, Steben M, Bryan J, Taddeo FJ, Railkar R, Esser MT, Sings HL, Nelson M, Boslego J, Sattler C, Barr E, Koutsky LA (2007) Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 356(19):1928-1943
92. Block SL, Nolan T, Sattler C, Barr E, Giacoletti KE, Marchant CD, Castellsague X, Rusche SA, Lukac S, Bryan JT, Cavanaugh PF Jr, Reisinger KS (2006) Comparison of the immunogenicity and reactogenicity of a prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in male and female adolescents and young adult women. Pediatrics 118(5):2135-2145
93. Garnett GP (2005) Role of herd immunity in determining the effect of vaccines against sexually transmitted disease. J Infect Dis 191(Suppl 1):S97-S106
94. Holmes KK, Levine R, Weaver M (2004) Effectiveness of condoms in preventing sexually transmitted infections. Bull World Health Organ 82(6):454-461
95. Vaccarella S, Franceschi S, Herrero R, Munoz N, Snijders PJ, Clifford GM, Smith JS, Lazcano-Ponce E, Sukvirach S, Shin HR, de Sanjose S, Molano M, Matos E, Ferreccio C, Anh PT, Thomas JO, Meijer CJ (2006) Sexual behavior, condom use, and human papillomavirus: Pooled analysis of the IARC human papillomavirus prevalence surveys. Cancer Epidemiol Biomarkers Prev 15(2):326-333
96. Nielson CM, Harris RB, Dunne EF, Abrahamsen M, Papenfuss MR, Flores R, Markowitz LE, Giuliano AR (2007) Risk factors for anogenital human papillomavirus infection in men. J Infect Dis 196(8):1137-1145
97. Winer RL, Hughes JP, Feng Q, O'Reilly S, Kiviat NB, Holmes KK, Koutsky LA (2006) Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med 354(25):2645-2654
98. Hogewoning CJ, Bleeker MC, van den Brule AJ, Voorhorst FJ, Snijders PJ, Berkhof J, Westenend PJ, Meijer CJ (2003) Condom use promotes regression of cervical intraepithelial neoplasia and clearance of human papillomavirus: A randomized clinical trial. Int J Cancer 107(5):811-816
99. Bleeker MC, Hogewoning CJ, Voorhorst FJ, van den Brule AJ, Snijders PJ, Starink TM, Berkhof J, Meijer CJ (2003) Condom use promotes regression of human papillomavirus-associated penile lesions in male sexual partners of women with cervical intraepithelial neoplasia. Int J Cancer 107(5):804-810