Advertisement

American Journal of Cancer

, Volume 4, Issue 1, pp 49–64 | Cite as

The Role of Human Papillomaviruses in Cancer

Evidence to Date
  • Andrea R. Spence
  • Eduardo L. Franco
  • Alex Ferenczy
Review Article

Abstract

The human papillomavirus (HPV) has been implicated in the development of an estimated 10% of cancers worldwide. Both epidemiologic and molecular evidence have conclusively demonstrated that oncogenic HPV is the central causal agent of cervical cancer and of a substantial proportion of many other anogenital neoplasms. In fact, it is believed that HPV is the necessary cause of cervical cancer, which has implications for the prevention, screening, and treatment of this disease, especially for its precursor lesions.

This has led to the possibility of using HPV DNA testing in screening and as a method of triaging abnormal Papanicolaou (Pap) tests. Research into the development of vaccines is also currently very active. HPV has been implicated in the genesis of several other cancers, such as oral and non-melanoma skin malignancies. However, research is yet to provide a consistent body of unequivocal evidence for a causal role that could lead to public health policy.

Keywords

Cervical Cancer Anal Cancer Invasive Cervical Cancer Penile Cancer Long Control Region 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Research by the authors on human papillomaviruses and cancers has been funded in part by grants from the Canadian Institutes of Health Research (CIHR) and National Cancer Institute of Canada, and by the US National Institutes of Health. Alex Ferenczy and Eduardo L. Franco have conducted research that used commercially available human papillomavirus tests. Eduardo Franco is a recipient of a Distinguished Scientist Award from the CIHR and of a National Scholar Award from the Fonds de la Recherche en santé du Québec.

References

  1. 1.
    Zur Hausen H. Papillomavirus infections: a major cause of human cancers. In: ei]Livingston DM, editors. Biochimica et Biophysica Acta: reviews on cancer 1996 Oct. Germany: Elsevier Science BV, 1996: F55–78Google Scholar
  2. 2.
    Bosch FX, Lorincz A, Munoz N, et al. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55(4): 244–65PubMedCrossRefGoogle Scholar
  3. 3.
    The current status of development of prophylactic vaccines against human papillomavirus infection. Report of a technical meeting; 1999 Feb 16–18; Geneva. Geneva: Department of Vaccines and Other Biologicals, 1999 MayGoogle Scholar
  4. 4.
    Doll R, Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981; 66(6): 1191–308PubMedGoogle Scholar
  5. 5.
    Pisani P, Parkin DM, Munoz N, et al. Cancer and infection: estimates of the attributable fraction in 1990. Cancer Epidemiol Biomarkers Prev 1997; 6: 387–40PubMedGoogle Scholar
  6. 6.
    zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000; 92(9): 690–8PubMedCrossRefGoogle Scholar
  7. 7.
    de Villiers EM, Fauquet C, Broker TR, et al. Minireview: classification of papillomaviruses. Virology 2004; 324: 17–27PubMedCrossRefGoogle Scholar
  8. 8.
    Munger K. The role of human papillomaviruses in human cancers. Front Biosci 2002; 7: d641–9PubMedCrossRefGoogle Scholar
  9. 9.
    IARC Working Group. Human Papillomaviruses, IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 64. Lyon: International Agency for Research on Cancer, 1995Google Scholar
  10. 10.
    Bosch FX, Manos MM, Munoz N, et al. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J Natl Cancer Inst 1995; 87(11): 796–802PubMedCrossRefGoogle Scholar
  11. 11.
    Bauer HM, Hildesheim A, Schiffman MH, et al. Determinants of genital human papillomavirus infection in low-risk women in Portland, Oregon. Sex Transm Dis 1993; 20: 274–8PubMedCrossRefGoogle Scholar
  12. 12.
    Walboomers JMM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189(1): 12–9PubMedCrossRefGoogle Scholar
  13. 13.
    Park TW, Fujiwara H, Wright TC. Molecular biology of cervical cancer and its precursors. Cancer 1995; 76(10 Suppl.): 1902–13PubMedCrossRefGoogle Scholar
  14. 14.
    Southern SA, Herrington CS. Disruption of cell cycle control by human papillomaviruses with special reference to cervical carcinoma. Int J Gynecol Cancer 2000; 10(4): 263–74PubMedCrossRefGoogle Scholar
  15. 15.
    Cullen AP, Reid R, Camption M, Lorincz AT. Analysis of the physical state of different human papillomavirus DNAs in intraepithelial and invasive cervical neoplasm. J Virol 1991; 65(2): 606–12PubMedGoogle Scholar
  16. 16.
    Pirami L, Giache V, Becciolini A. Analysis of HPV 16, 18,31, and 35 DNA in preinvasive and invasive lesions of the uterine cervix 1997. J Clin Pathol 1997; 50(7): 600–4PubMedCrossRefGoogle Scholar
  17. 17.
    Zur Hausen H. Intracellular surveillance of persisting viral infections. Lancet 1986; II: 489–91CrossRefGoogle Scholar
  18. 18.
    Evans AS, Mueller NE. Viruses and cancer: causal associations. Ann Epidemiol 1990; 1: 71–92PubMedCrossRefGoogle Scholar
  19. 19.
    Fredricks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev 1996; 9: 18–33Google Scholar
  20. 20.
    Hill AB. The environment and disease: association or causation? Proc R Soc Med 1965; 58: 295–300PubMedGoogle Scholar
  21. 21.
    Ferlay J, Bray F, Pisani P, et al. GLOBOCAN 2000: cancer incidence, mortality, and prevalence worldwide, Version 1.0. IARC CancerBase No. 5. Lyon: IARC Press, 2001Google Scholar
  22. 22.
    Muir C, Waterhouse J, Powell J, et al. editors. Cancer incidence in five continents. Vol. V. IARC Scientific Publication No. 88. Lyon: International Agency for Research on Cancer, 1987Google Scholar
  23. 23.
    Harris RW, Brinton LA, Cowdell RH, et al. Characteristics of women with dysplasia or carcinoma in situ of the cervix uteri. Br J Cancer 1980; 42: 359–69PubMedCrossRefGoogle Scholar
  24. 24.
    Brock KE, MacLennan R, Brinton LA, et al. Smoking and infectious agents and risk of in situ cervical cancer in Sydney, Australia. Cancer Res 1989; 49: 4925–8PubMedGoogle Scholar
  25. 25.
    Cuzick J, Singer A, DeSatola BL, et al. Case-control study of risk factors for cervical intraepithelial neoplasia in young women. Eur J Cancer 1990; 26: 684–90PubMedCrossRefGoogle Scholar
  26. 26.
    Parazzini F, Lavecchia C, Negri E, et al. Risk factors for cervical intraepithelial neoplasia. Cancer 1992; 69(9): 2276–82PubMedCrossRefGoogle Scholar
  27. 27.
    Munoz N, Bosch FX, Desanjose S, et al. Risk factors for cervical intraepithelial neoplasia grade-3 carcinoma in situ in Spain and Colombia. Cancer Epidemiol Biomarkers Prev 1993; 2: 423–31PubMedGoogle Scholar
  28. 28.
    DeVet HCW, Sturmans F. Risk factors for cervical dysplasia: implications for prevention. Public Health 1994; 108: 241–9CrossRefGoogle Scholar
  29. 29.
    Kjellberg L, Wang Z, Wiklund F, et al. Sexual behaviour and papillomavirus exposure in cervical intraepithelial neoplasia: a population-based case-control study. J Gen Virol 1999; 80 (Pt 2): 391–8PubMedGoogle Scholar
  30. 30.
    Bosch FX, Munoz N. The viral etiology of cervical cancer. Virus Res 2002; 89(2): 183–90PubMedCrossRefGoogle Scholar
  31. 31.
    Munoz 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): 518–27PubMedCrossRefGoogle Scholar
  32. 32.
    Kuper HE, Tzonou A, Kaklamani E, et al. Hepatitis B and C viruses in the etiology of hepatocellular carcinoma; a study in Greece using third-generation assays. Cancer Causes Control 2000; 11: 171–5PubMedCrossRefGoogle Scholar
  33. 33.
    IARC Working Group. Tobacco smoking, IARC monographs on the evaluation of carcinogenic risk of chemicals to humans. Vol. 38. Lyon: International Agency for Research on Cancer, 1986Google Scholar
  34. 34.
    Lorincz AT, Castle PE, Sherman ME, et al. Viral load of human papillomavirus and risk of CIN3 or cervical cancer. Lancet 2002; 360(9328): 228–9PubMedCrossRefGoogle Scholar
  35. 35.
    van Duin M, Snijders PJ, Schrijnemakers HF, et al. Human papillomavirus 16 load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int J Cancer 2002; 98(4): 590–5PubMedCrossRefGoogle Scholar
  36. 36.
    Schlecht NF, Trevisan A, Duarte-Franco E, et al. Viral load as a predictor of the risk of cervical intraepithelial neoplasia. Int J Cancer 2003; 103(4): 519–24PubMedCrossRefGoogle Scholar
  37. 37.
    van den Brule AJC, Walboomers JMM, Dumaine M, et al. Difference in prevalence of human papillomavirus genotypes in cytomorphologically normal cervical smears is associated with a history of cervical intraepithelial neoplasia. Int J Cancer 1991; 48: 404–8CrossRefGoogle Scholar
  38. 38.
    Koutsky LA, Holmes KK, Critchlow CW, et al. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med 1992; 327: 1272–8PubMedCrossRefGoogle Scholar
  39. 39.
    Levine AJ, Harper J, Hilborne L, et al. HPV DNA and the risk of squamous intraepithelial lesions of the uterine cervix in young women. Am J Clin Pathol 1993; 100: 6–11PubMedGoogle Scholar
  40. 40.
    Bosch FX, Munoz N, Desanjose S, et al. Human papillomavirus and cervical intraepithelial neoplasia grade-3 carcinoma in situ: a case-control study in Spain and Colombia. Cancer Epidemiol Biomarkers Prev 1993; 2: 415–22PubMedGoogle Scholar
  41. 41.
    Coker AL, Jenkins GR, Busnardo MS, et al. Human papillomaviruses and cervical neoplasia in South-Carolina. Cancer Epidemiol Biomarkers Prev 1993; 2: 207–12PubMedGoogle Scholar
  42. 42.
    Becker TM, Wheeler CM, Mcgough NS, et al. Sexually transmitted diseases and other risk factors for cervical dysplasia among Southwestern Hispanic and non-Hispanic White women. JAMA 1994; 271: 1181–8PubMedCrossRefGoogle Scholar
  43. 43.
    Brisson J, Morin C, Fortier M, et al. Risk factors for cervical intraepithelial neoplasia: differences between low- and high-grade lesions. Am J Epidemiol 1994; 140: 700–10PubMedGoogle Scholar
  44. 44.
    Liaw KL, Hsing AW, Chen CJ, et al. Human papillomavirus and cervical neoplasia: a case-control study in Taiwan. Int J Cancer 1995; 62(5): 565–71PubMedCrossRefGoogle Scholar
  45. 45.
    Olsen AO, Gjoen K, Sauer T, et al. Human papillomavirus and cervical intraepithelial neoplasia grade II-III: a population-based case-control study. Int J Cancer 1995; 61: 312–5PubMedCrossRefGoogle Scholar
  46. 46.
    Sasagawa T, Dong YZ, Saijoh K, et al. Human papillomavirus infection and risk determinants for squamous intraepithelial lesion and cervical cancer in Japan. Jpn J Cancer Res 1997; 88: 376–84PubMedCrossRefGoogle Scholar
  47. 47.
    Liaw KL, Glass AG, Manos MM, et al. Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst 1999; 91: 954–60PubMedCrossRefGoogle Scholar
  48. 48.
    MacLehose RF, Harpster A, Lanier AP, et al. Risk factors for cervical intraepithelial neoplasm in Alaska Native women: a pilot study. Alaska Med 1999; 41(4): 76–85PubMedGoogle Scholar
  49. 49.
    Herrero R, Hildesheim A, Bratti C, et al. Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst 2000; 92(6): 464–74PubMedCrossRefGoogle Scholar
  50. 50.
    Schiff M, Becker TM, Masuk M, et al. Risk factors for cervical intraepithelial neoplasia in southwestern American Indian women. Am J Epidemiol 2000; 152(8): 716–26PubMedCrossRefGoogle Scholar
  51. 51.
    Franco EL, Rohan TE. Cancer precursors: epidemiology, detection, and prevention. New York: Springer-Verlag, 2002Google Scholar
  52. 52.
    Franco EL, Rohan TE, Villa LL. Epidemiologic evidence and human papillomavirus infection as a necessary cause of cervical cancer. J Natl Cancer Inst 1999; 91(6): 506–11PubMedCrossRefGoogle Scholar
  53. 53.
    Schlecht NF, Kulaga S, Robitaille J, et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001; 286(24): 3106–14PubMedCrossRefGoogle Scholar
  54. 54.
    Cox JT. Epidemiology of cervical intraepithelial neoplasia: the role of human papillomavirus. Clin Obstet Gynaecol 1995; 9: 1–37Google Scholar
  55. 55.
    Ley C, Bauer HM, Reingold A, al.Determinants of genital human papillomavirus infection in young women. J Natl Cancer Inst 1991; 83: 997–1003PubMedCrossRefGoogle Scholar
  56. 56.
    Melkert PW, Hopman E, van den Brule AJ, al. Prevalence of HPV in cytomorphologically normal cervical smears, as determined by the polymerase chain reaction, is age-dependent. Int J Cancer 1993; 53: 919–23PubMedCrossRefGoogle Scholar
  57. 57.
    Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998; 338: 423–8PubMedCrossRefGoogle Scholar
  58. 58.
    Franco EL, Villa LL, Sobrinho JP, et al. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis 1999; 180: 1415–23PubMedCrossRefGoogle Scholar
  59. 59.
    Thomas KK, Hughes JP, Kuypers JM, et al. Concurrent and sequential acquisition of different genital human papillomavirus types. J Infect Dis 2000; 182(4): 1097–102PubMedCrossRefGoogle Scholar
  60. 60.
    Liaw KL, Hildesheim A, Burk RD, et al. A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis 2001; 183(1): 8–15PubMedCrossRefGoogle Scholar
  61. 61.
    Brinton LA, Hamman RF, Huggins GR, et al. Sexual and reproductive risk factors for invasive squamous cell cervical cancer. J Natl Cancer Inst 1987; 79: 23–30PubMedGoogle Scholar
  62. 62.
    Brinton LA, Reeves WC, Brenes MM, et al. Parity as a risk factor for cervical cancer. Am J Epidemiol 1989; 130: 486–96PubMedGoogle Scholar
  63. 63.
    Bayo S, Bosch FX, de Sanjose S, et al. Risk factors of invasive cervical cancer in Mali. Int J Epidemiol 2002; 31(1): 202–9PubMedCrossRefGoogle Scholar
  64. 64.
    Ferrera A, Velema JP, Figueroa M, et al. Co-factors related to the causal relationship between human papillomavirus and invasive cervical cancer in Honduras. Int J Epidemiol 2000; 29(5): 817–25PubMedCrossRefGoogle Scholar
  65. 65.
    Thomas DB, Ray RM, Koetsawang A, et al. Human papillomaviruses and cervical cancer in Bangkok: I. Risk factors for invasive cervical carcinomas with human papillomavirus types 16 and 18 DNA. Am J Epidemiol 2001; 153(8): 723–31PubMedCrossRefGoogle Scholar
  66. 66.
    Schneider A, Hotz M, Gissmann L. Increased prevalence of human papillomaviruses in the lower genital tract of pregnant women. Int J Cancer 1987; 40: 198–201PubMedCrossRefGoogle Scholar
  67. 67.
    Pater MM, Mittal R, Pater A. Role of steroid hormones in potentiating transformation of cervical cells by human papillomaviruses. Trends Microbiol 1994; 2(7): 229–34PubMedCrossRefGoogle Scholar
  68. 68.
    Schiffman MH, Brinton LA, Devesa SS, et al. Cervical cancer. In: ed]Schottenfeld D, Fraumeni Jr JF, editors. Cancer epidemiology and prevention. New York: Oxford University Press, 1996Google Scholar
  69. 69.
    Becker TM, Wheeler CM, McGough NS, et al. Contraceptive and reproductive risks for cervical dysplasia in southwestern Hispanic and non-Hispanic white women. Int J Epidemiol 1994; 23(5): 913–22PubMedCrossRefGoogle Scholar
  70. 70.
    Molina R, Thomas DB, Dabancens A, et al. Oral contraceptives and cervical carcinoma in situ in Chile. Cancer Res 1988; 48: 1011–5PubMedGoogle Scholar
  71. 71.
    Brinton LA. Epidemiology of cervical cancer: overview. In: ed]Munoz N, Bosch FX, Shah KV, et al., editors. The epidemiology of human papillomavirus and cervical cancer. Lyon: WHO-IARC, 1992: 3–23Google Scholar
  72. 72.
    Winkelstein W. Smoking and cervical cancer: current status. A review. Am J Epidemiol 1990; 131: 945–57Google Scholar
  73. 73.
    Schiffman MH, Haley NJ, Felton JS, et al. Biochemical epidemiology of cervical neoplasia: measuring cigarette smoke constituents in the cervix. Cancer Res 1987; 47: 3886–8PubMedGoogle Scholar
  74. 74.
    Waggoner SE, Wang X. Effect of nicotine on proliferation of normal, malignant, and human papillomavirus-transformed human cervical cells. Gynecol Oncol 1994; 55(1): 91–5PubMedCrossRefGoogle Scholar
  75. 75.
    Potischman N, Brinton LA. Nutrition and cervical neoplasia. Cancer Causes Control 1996; 7(1): 113–26PubMedCrossRefGoogle Scholar
  76. 76.
    Giuliano AR. The role of nutrients in the prevention of cervical dysplasia and cancer. Nutrition 2000; 16(7-8): 570–3PubMedCrossRefGoogle Scholar
  77. 77.
    Ries LG, Eisner MP, Kosary CL, et al. SEER cancer statistics review, 1973–1997. Bethesda (MD): National Cancer Institute, 2000Google Scholar
  78. 78.
    Melbye M, Rabkin C, Frisch M, et al. Changing patterns of anal cancer incidence in the United States, 1940–1989. Am J Epidemiol 1994; 139(8): 773–80Google Scholar
  79. 79.
    Daling JR, Weiss NS, Hishop G, et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317: 973–7PubMedCrossRefGoogle Scholar
  80. 80.
    Melbye M, Cote TR, Kessler L, et al. High incidence of anal cancer among AIDS patients: The AIDS/Cancer Working Group. Lancet 1994; 343(8898): 636–9PubMedCrossRefGoogle Scholar
  81. 81.
    Frisch M, Melbye M, Moller H. Trends in incidence of anal cancer in Denmark. BMJ 1993; 306: 419–22PubMedCrossRefGoogle Scholar
  82. 82.
    Goldman S, Glimelius B, Nilsson B, et al. Incidence of anal epidermoid carcinoma in Sweden 1970–1984. Acta Chir Scand 1989; 155: 191–7PubMedGoogle Scholar
  83. 83.
    Binkley GE, Derrick WA. The association of squamous cancer with anal manifestations of lymphogranuloma venereum. Am J Dig Dis 1945; 12: 46–7CrossRefGoogle Scholar
  84. 84.
    Melbye M, Sprogel P. Aetiological parallel between anal cancer and cervical cancer. Lancet 1991; 338: 657–9PubMedCrossRefGoogle Scholar
  85. 85.
    Rabkin CS, Biggar RJ, Melbye M, et al. Second primary cancers following anal and cervical carcinoma: evidence of shared etiologic factors. Am J Epidemiol 1992; 136: 54–8PubMedGoogle Scholar
  86. 86.
    Holly EA, Whittemore AS, Aston DA, et al. Anal cancer incidence: genital warts, anal fissure or fistula, hemorrhoids, and smoking. J Natl Cancer Inst 1989; 81: 1726–31PubMedCrossRefGoogle Scholar
  87. 87.
    Poletti PA, Halfon A, Marti MC. Papillomavirus and anal carcinoma. Int J Colorectal Dis 1998; 13(2): 108–11PubMedCrossRefGoogle Scholar
  88. 88.
    Frisch M, Glimelius B, van den Brule AJ, et al. Sexually transmitted infection as a cause of anal cancer. N Engl J Med 1997; 337(19): 1350–8PubMedCrossRefGoogle Scholar
  89. 89.
    Palefsky JM, Holly EA, Gonzales J, et al. Detection of human papillomavirus DNA in anal intraepithelial neoplasia and anal cancer. Cancer Res 1991; 51(3): 1014–9PubMedGoogle Scholar
  90. 90.
    Critchlow CW, Surawicz CM, Holmes KK, et al. Prospective study of high grade anal squamous intraepithelial neoplasia in a cohort of homosexual men: influence of HIV infection, immunosuppression and human papillomavirus infection. AIDS 1995; 9(11): 1255–62PubMedCrossRefGoogle Scholar
  91. 91.
    Palefsky JM. Anal squamous intraepithelial lesions in human immunodeficiency virus-positive men and women. Semin Oncol 2000; 27(4): 471–9PubMedGoogle Scholar
  92. 92.
    Cabrera A, Tsukuda Y, Pickren JW, et al. Development of lower genital carcinomas in patients with anal carcinoma: a more than casual relationship. Cancer 1966; 19: 470–80PubMedCrossRefGoogle Scholar
  93. 93.
    Stern BD, Kaplan L. Multicentric foci of carcinomas arising in structure of cloacal origin. Am J Obstet Gynecol 1969; 104: 255–66PubMedGoogle Scholar
  94. 94.
    Tilston P. Anal human papillomavirus and anal cancer. J Clin Pathol 1997; 50(8): 625–34PubMedCrossRefGoogle Scholar
  95. 95.
    Palefsky JM. Human papillomavirus infection and anogenital neoplasia in human immunodeficiency virus-positive men and women. J Natl Cancer Inst Monogr 1998; (23): 15–20Google Scholar
  96. 96.
    Parkin DM, Muir CS, Whelan SL, et al. editors. Cancer incidence in five continents. IARC Scientific Publications No. 120. Vol. 6. Lyon: International Agency for Research on Cancer, 1992Google Scholar
  97. 97.
    Malek RS, Goellner JR, Smith TF, et al. Human papillomavirus infection and intraepithelial, in situ, and invasive carcinoma of penis. Urology 1993; 42(2): 159–70PubMedCrossRefGoogle Scholar
  98. 98.
    Rubin MA, Kleter B, Zhou M, et al. Detection and typing of human papillomavirus DNA in penile carcinoma: evidence for multiple independent pathways of penile carcinogenesis. Am J Pathol 2001; 159(4): 1211–8PubMedCrossRefGoogle Scholar
  99. 99.
    Maden C, Sherman KJ, Beckmann AM, et al. History of circumcision, medical conditions, and sexual activity and risk of penile cancer. J Natl Cancer Inst 1993; 85(1): 19–24PubMedCrossRefGoogle Scholar
  100. 100.
    Hellberg D, Valentin J, Eklundm T, et al. Penile cancer: is there an epidemiological role for smoking and sexual behaviour? BMJ 1987; 295: 1306–8PubMedCrossRefGoogle Scholar
  101. 101.
    Schoen EJ. The status of circumcision of newborns. N Engl J Med 1990; 322(18): 1308–12PubMedCrossRefGoogle Scholar
  102. 102.
    Graham S, Priore R, Graham M, et al. Genital cancer in wives of penile cancer patients. Cancer 1979; 44(5): 1870–4PubMedCrossRefGoogle Scholar
  103. 103.
    Barrasso R, DeBrux J, Croissant O, et al. High prevalence of papillomavirus-associated penile intraepithelial neoplasia in sexual partners of women with cervical intraepithelial neoplasia. N Engl J Med 1987; 317: 916–23PubMedCrossRefGoogle Scholar
  104. 104.
    Franco EL, Campos-Filho N, Villa LL, et al. Correlation patterns of cancer relative frequencies with some socioeconomic and demographic indicators in Brazil: an ecologic study. Int J Cancer 1988; 41: 24–9PubMedCrossRefGoogle Scholar
  105. 105.
    Bosch FX, Cardis E. Cancer incidence correlations: genital, urinary and some tobacco-related cancers. Int J Cancer 1990; 46: 178–84PubMedCrossRefGoogle Scholar
  106. 106.
    Castellsagué X, Bosch FX, Munox N et al. Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med 2002; 346(15): 1105–1112PubMedCrossRefGoogle Scholar
  107. 107.
    Levi JE, Rahal P, Sarkis AS, et al. Human papillomavirus DNA and p53 status in penile carcinomas. Int J Cancer 1998; 76(6): 779–83PubMedCrossRefGoogle Scholar
  108. 108.
    Gregoire L, Cubilla AL, Reuter VE, et al. Preferential association of human papillomavirus with high-grade histologie variants of penile-invasive squamous cell carcinoma. J Natl Cancer Inst 1995; 87: 1705–9PubMedCrossRefGoogle Scholar
  109. 109.
    Picconi MA, Eijan AM, Distefano AL, et al. Human papillomavirus (HPV) DNA in penile carcinomas in Argentina: analysis of primary tumors and lymph nodes. J Med Virol 2000; 61(1): 65–9PubMedCrossRefGoogle Scholar
  110. 110.
    Daling JR, Madeleine MM, Schwartz SM, et al. A population-based study of squamous cell vaginal cancer: HPV and cofactors. Gynecol Oncol 2002; 84(2): 263–70PubMedCrossRefGoogle Scholar
  111. 111.
    Merino MJ. Vaginal cancer: the role of infectious and environmental factors. Am J Obstet Gynecol 1991; 165(4): 1255–62PubMedGoogle Scholar
  112. 112.
    Hildesheim A, Han CL, Brinton LA, et al. Sexually transmitted agents and risk of carcinoma of the vagina. Int J Gynecol Cancer 1997; 7: 251–5CrossRefGoogle Scholar
  113. 113.
    Choo YC, Anderson DG. Neoplasms of the vagina following cervical carcinoma. Gynecol Oncol 1982; 14: 125–32PubMedCrossRefGoogle Scholar
  114. 114.
    Ikenberg H, Runge M, Goppinger A, et al. A. Human papillomavirus DNA in invasive carcinoma of the vagina. Obstet Gynecol 1990; 76: 432–8PubMedGoogle Scholar
  115. 115.
    Brinton LA, Nasca PC, Mailin K, et al. Case-control study of in situ and invasive carcinoma of the vagina. Gynecol Oncol 1990; 38: 49–54PubMedCrossRefGoogle Scholar
  116. 116.
    Herman J, Homesley H, Dignan M. Is hysterectomy a risk factor for vaginal cancer? JAMA 1986; 256: 601–3PubMedCrossRefGoogle Scholar
  117. 117.
    Olaitan A, Murdoch J. Clinical management of vulval cancer. Rev Gynaecological Pract 2002; 2: 16–22CrossRefGoogle Scholar
  118. 118.
    Al-Ghamdi A, Freedman D, Miller D, et al. Vulvar squamous cell carcinoma in young women: a clinicopathologic study of 21 cases. Gynecol Oncol 2002; 84(1): 94–101PubMedCrossRefGoogle Scholar
  119. 119.
    Crum CP. Carcinoma of the vulva: epidemiology and pathogenesis. Obstet Gynecol 1992; 79(3): 448–54PubMedCrossRefGoogle Scholar
  120. 120.
    Bloss JD, Liao S Y, Wilczynski SP, et al. Clinical and histologic features of vulvar carcinomas analyzed for human papillomavirus status: evidence that squamous cell carcinoma of the vulva has more than one etiology. Hum Pathol 1991; 22(7): 711–8PubMedCrossRefGoogle Scholar
  121. 121.
    Franceschi S, Talamini R, Barra S, et al. Smoking and drinking in relation to cancers of the oral cavity, pharynx, larynx, and esophagus in Northern Italy. Cancer Res 1990; 50: 6502–7PubMedGoogle Scholar
  122. 122.
    Scully C. Oral squamous cell carcinoma; from a hypothesis about a virus, to concern about possible sexual transmission. Oral Oncol 2002; 38(3): 227–34PubMedCrossRefGoogle Scholar
  123. 123.
    Wong DTW, Munger K. Association of human papillomaviruses with a subgroup of head and neck squamous cell carcinomas. J Natl Cancer Inst 2000; 92(9): 675–7PubMedCrossRefGoogle Scholar
  124. 124.
    Hemminki K, Jiang Y, Dong C. Second primary cancers after anogenital, skin, oral, esophageal and rectal cancers: etiological links? Int J Cancer 2001; 93(2): 294–8PubMedCrossRefGoogle Scholar
  125. 125.
    Steinberg BM, Auborn KJ. Papillomaviruses in head and neck disease: pathophysiology and possible regulation. J Cell Biochem Suppl 1993; 17F: 155–64PubMedCrossRefGoogle Scholar
  126. 126.
    Schwartz SM, Daling JR, Doody DR, et al. Oral cancer risk in relation to sexual history and evidence of human papillomavirus infection. J Natl Cancer Inst 1998; 90: 1626–36PubMedCrossRefGoogle Scholar
  127. 127.
    Smith EM, Hoffman HT, Summersgill KS, et al. Human papillomavirus and risk of oral cancer. Laryngoscope 1998; 108(7): 1098–103PubMedCrossRefGoogle Scholar
  128. 128.
    Summersgill KF, Smith EM, Kirchner HL, et al. p53 polymorphism, human papillomavirus infection in the oral cavity, and oral cancer. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000; 90(3): 334–9PubMedCrossRefGoogle Scholar
  129. 129.
    Maden C, Beckmann AM, Thomas DB, et al. Human papillomaviruses, herpes simplex viruses, and the risk of oral cancer in men. Am J Epidemiol 1992; 135: 1093–102PubMedGoogle Scholar
  130. 130.
    Herrero R, Munoz N, Franceschi S, et al. International case-control study of HPV and cancer of the oral cavity and pharynx. 18th International Papillomavirus Conference; 2003 Jul 23–28; Barcelona: 184Google Scholar
  131. 131.
    Miller CS, Johnstone BM. Human papillomavirus as a risk factor for oral squamous cell carcinoma: a meta-analysis, 1982–1997. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001; 91(6): 622–35PubMedCrossRefGoogle Scholar
  132. 132.
    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): 1125–31PubMedCrossRefGoogle Scholar
  133. 133.
    Gillison ML, Koch WM, Capone RB, et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000; 92(9): 709–20PubMedCrossRefGoogle Scholar
  134. 134.
    Mineta H, Ogino T, Amano HM, et al. Human papillomavirus (HPV) type 16 and 18 detected in head and neck squamous cell carcinoma. Anticancer Res 1998; 18(6B): 4765–8PubMedGoogle Scholar
  135. 135.
    Pintos J, Franco EL, Black MJ, et al. Human papillomavirus and prognoses of patients with cancers of the upper aerodigestive tract. Cancer 1999; 85(9): 1903–9PubMedGoogle Scholar
  136. 136.
    Snijders PJF, Cromme FV, van den Brule AJC, et al. Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer 1992; 51: 845–50PubMedCrossRefGoogle Scholar
  137. 137.
    Vega LJP. Human papillomavirus infection and oral cancer: a case-control study [thesis]. Montreal (QC): McGill University, 2002Google Scholar
  138. 138.
    Matsha T, Erasmus R, Kafuko AB, et al. Human papillomavirus associated with oesophageal cancer. J Clin Pathol 2002; 55(8): 587–90PubMedCrossRefGoogle Scholar
  139. 139.
    Munoz N, Day NE. Esophagus. In: Schottenfeld D, Fraumeni JF Jr. editors. Cancer epidemiology and prevention. New York (NY): Oxford University Press, 1996: 681–706Google Scholar
  140. 140.
    Dillner J, Knekt P, Schiller JT, et al. Prospective seroepidemiological evidence that human papillomavirus type 16 infection is a risk factor for oesophageal squamous cell carcinoma. BMJ 1995; 311: 1346PubMedCrossRefGoogle Scholar
  141. 141.
    Han C, Qiao G, Hubbert NL, et al. Serologic association between human papillomavirus type 16 infection and esophageal cancer in Shaanxi Province, China. J Natl Cancer Inst 1996; 88(20): 1467–71PubMedCrossRefGoogle Scholar
  142. 142.
    Bjorge T, Hakulinen T, Engeland A, et al. A prospective, seroepidemiological study of the role of human papillomavirus in esophageal cancer in Norway. Cancer Res 1997; 57(18): 3989–92PubMedGoogle Scholar
  143. 143.
    Lagergren J, Wang Z, Bergstrom R, et al. Human papillomavirus infection and esophageal cancer: a nationwide seroepidemiologic case-control study in Sweden. J Natl Cancer Inst 1999; 91: 156–62PubMedCrossRefGoogle Scholar
  144. 144.
    Ko CB, Walton S, Keczkes K, et al. The emerging epidemic of skin cancer. Br J Dermatol 1994; 131: 455–64Google Scholar
  145. 145.
    Kiviat NB. Papillomaviruses in non-melanoma skin cancer: epidemiological aspects. Semin Cancer Biol 1999; 9(6): 397–403PubMedCrossRefGoogle Scholar
  146. 146.
    Orth G. Epidermodysplasia verruciformis: the Papovaviridae. Vol. 2. New York: Plenum Press, 1987: 199–243CrossRefGoogle Scholar
  147. 147.
    Birkeland SA, Storm HH. Risk for tumor and other disease transmission by transplantation: a population-based study of unrecognized malignancies and other diseases in organ donors. Transplantation 2002; 74(10): 1409–13PubMedCrossRefGoogle Scholar
  148. 148.
    Bouwes Bavinck JN. Epidemiological aspects of immunosuppression: role of exposure to sunlight and human papillomavirus on the development of skin cancer. Hum Exp Toxicol 1995; 14(1): 98PubMedCrossRefGoogle Scholar
  149. 149.
    Penn I. Skin disorders in organ transplant recipients: external anogenital lesions. Arch Dermatol 1997; 133(2): 221–3PubMedCrossRefGoogle Scholar
  150. 150.
    Ortho G. Epidermodysplasia verruciformis: a model for understanding the oncogenicity of human papillomaviruses. Ciba Found Symp 1984; 120: 157–74Google Scholar
  151. 151.
    De Villiers EM. Papillomavirus and HPV typing. Clin Dermatol 1997; 15: 199–206PubMedCrossRefGoogle Scholar
  152. 152.
    Koss LG. The Papanicolaou test for cervical cancer detection: a triumph and a tragedy. JAMA 1989; 261: 737–43PubMedCrossRefGoogle Scholar
  153. 153.
    Nanda K, McCrory DC, Myers ER, et al. Accuracy of the papanicolaou test in screening for and follow-up of cervical cytologie abnormalities: a systematic review. Ann Intern Med 2000; 132(10): 810–9PubMedGoogle Scholar
  154. 154.
    Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 2002; 52(6): 342–62PubMedCrossRefGoogle Scholar
  155. 155.
    Ferenczy A, Franco E. Persistent human papillomavirus infection and cervical neoplasia. Lancet Oncol 2002; 3(1): 11–6PubMedCrossRefGoogle Scholar
  156. 156.
    Wright Jr TC, Cox JT, Massad LS, et al. 2001 Consensus guidelines for the management of women with cervical cytological abnormalities. JAMA 2002; 287(16): 2120–9PubMedCrossRefGoogle Scholar
  157. 157.
    Montz FJ, Farber FL, Bristow RE, et al. Impact of increasing Papanicolaou test sensitivity and compliance: a modeled cost and outcomes analysis. Obstet Gynecol 2001; 97(5 Pt 1): 781–8PubMedCrossRefGoogle Scholar
  158. 158.
    Kulasingam SL, Hughes JP, Kiviat NB, et al. Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral. JAMA 2002; 288(14): 1749–57PubMedCrossRefGoogle Scholar
  159. 159.
    Cuzick J, Szarewski A, Terry G, et al. Human papillomavirus testing in primary cervical screening. Lancet 1995; 345(8964): 1533–6PubMedCrossRefGoogle Scholar
  160. 160.
    Clavel C, Masure M, Bory JP, et al. Hybrid capture II-based human papillomavirus detection, a sensitive test to detect in routine high-grade cervical lesions: a preliminary study on 1518 women. Br J Cancer 1999; 80(9): 1306–11PubMedCrossRefGoogle Scholar
  161. 161.
    Cuzick J, Beverley E, Ho L, et al. HPV testing in primary screening of older women. Br J Cancer 1999; 81(3): 554–8PubMedCrossRefGoogle Scholar
  162. 162.
    Kuhn L, Denny L, Pollack A, et al. Human papillomavirus DNA testing for cervical cancer screening in low- resource settings. J Natl Cancer Inst 2000; 92(10): 818–25PubMedCrossRefGoogle Scholar
  163. 163.
    Ratnam S, Franco EL, Ferenczy A. Human papillomavirus testing for primary screening of cervical cancer precursors. Cancer Epidemiol Biomarkers Prev 2000; 9: 945–51PubMedGoogle Scholar
  164. 164.
    Schiffman M, Herrero R, Hildesheim A, et al. HPV DNA testing in cervical cancer screening: results from women in a high-risk province of Costa Rica. JAMA 2000; 283(1): 87–93PubMedCrossRefGoogle Scholar
  165. 165.
    Wright Jr TC, Denny L, Kuhn L, et al. HPV DNA testing of self-collected vaginal samples compared with cytologic screening to detect cervical cancer. JAMA 2000; 283(1): 81–6PubMedCrossRefGoogle Scholar
  166. 166.
    Schneider A, Hoyer H, Lotz B, et al. Screening for high-grade cervical intraepithelial neoplasia and cancer by testing for high-risk HPV, routine cytology or colposcopy. Int J Cancer 2000; 89: 529–34PubMedCrossRefGoogle Scholar
  167. 167.
    Belinson J, Qiao YL, Pretorius R, et al. Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia. Gynecol Oncol 2001; 83(2): 439–44PubMedCrossRefGoogle Scholar
  168. 168.
    Blumenthal PD, Gaffikin L, Chirenje ZM, et al. Adjunctive testing for cervical cancer in low resource settings with visual inspection, HPV, and the Pap smear. Int J Gynaecol Obstet 2001; 72(1): 47–53PubMedCrossRefGoogle Scholar
  169. 169.
    Clavel C, Masure M, Bory JP, et al. Human papillomavirus testing in primary screening for the detection of high-grade cervical lesions: a study of 7932 women. Br J Cancer 2001; 84(12): 1616–23PubMedCrossRefGoogle Scholar
  170. 170.
    Hillemanns P, Kimmig R, Huttemann U, et al. Screening for cervical neoplasia by self-assessment for human papillomavirus DNA. Lancet 1999; 354(9194):1970PubMedCrossRefGoogle Scholar
  171. 171.
    Sellors JW, Lorincz AT, Mahony JB, et al. Comparison of self-collected vaginal, vulvar and urine samples with physician-collected cervical samples for human papillomavirus testing to detect high-grade squamous intraepithelial lesions. CMAJ 2000; 163(5): 513–8PubMedGoogle Scholar
  172. 172.
    Solomon D, Schiffman M, Tarone R. Comparison of three management strategies for patients with atypical squamous cells of undetermined significance: baseline results from a randomized trial. J Natl Cancer Inst 2001; 93(4): 293–9PubMedCrossRefGoogle Scholar
  173. 173.
    Manos MM, Kinney WK, Hurley LB, et al. Identifying women with cervical neoplasia: using human papillomavirus DNA testing for equivocal papanicolaou results. JAMA 1999; 281(17): 1605–10PubMedCrossRefGoogle Scholar
  174. 174.
    The Atypical Squamous Cells of undetermined Significance/Low-Grade Squamous Intraepithelial Lesions Triage Study (ALTS) group. Human papillomavirus testing for triage of women with cytologic evidence of low-grade squamous intraepithelial lesions: baseline data form a randomized trial. J Natl Cancer Inst 2000; 92(5): 397–402CrossRefGoogle Scholar
  175. 175.
    Crum CP. The beginning of the end for cervical cancer? N Engl J Med 2002; 347(21): 1703–5PubMedCrossRefGoogle Scholar
  176. 176.
    Harro CD, Pang YY, Roden RB, et al. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J Natl Cancer Inst 2001; 93(4): 284–92PubMedCrossRefGoogle Scholar
  177. 177.
    Schiller JT, Lowy DR. Papillomavirus-like particle vaccines. J Natl Cancer Inst Monogr 2000; 28: 50–4CrossRefGoogle Scholar
  178. 178.
    Koutsky LA, Ault KA, Wheeler CM, et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002; 347(21): 1645–51PubMedCrossRefGoogle Scholar
  179. 179.
    Davidson EJ, Kitchener HC, Stern PL. The use of vaccines in the prevention and treatment of cervical cancer. Clin Oncol 2002; 14: 193–200CrossRefGoogle Scholar

Copyright information

© Adis Data Information BV 2005

Authors and Affiliations

  • Andrea R. Spence
    • 1
  • Eduardo L. Franco
    • 1
  • Alex Ferenczy
    • 2
    • 3
  1. 1.Departments of Oncology and EpidemiologyMcGill UniversityMontrealCanada
  2. 2.Department of PathologySir Mortimer B. Davis Jewish General Hospital and McGill UniversityMontrealCanada
  3. 3.Sir Mortimer B. Davis Jewish General HospitalMontrealCanada

Personalised recommendations