Human Papillomavirus in the HIV-Infected Host: Epidemiology and Pathogenesis in the Antiretroviral Era

Current HIV/AIDS Reports

Volumn 12, Issue 1, 2015, Pages 6-15

  Brickman, Cristina ^a   Palefsky, Joel M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anal cancer; Anal squamous intraepithelial lesions; Antiretroviral therapy; Cervical cancer; Cervical squamous intraepithelial lesions; Human immunodeficiency virus; Human papillomavirus

Indexed keywords

ANTIRETROVIRUS AGENT;

ANUS CANCER; CANCER GROWTH; CANCER SCREENING; DISEASE CLASSIFICATION; DISEASE COURSE; EPITHELIUM CELL; GENE EXPRESSION; HISTORY; HOST; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; LONGEVITY; ONCOGENE; PAPILLOMAVIRUS INFECTION; PATHOGENESIS; PREVALENCE; REVIEW; SCREENING; SQUAMOUS INTRAEPITHELIAL LESION OF THE CERVIX; TIGHT JUNCTION; TUMOR INVASION; UPREGULATION; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; VIRUS PATHOGENESIS; WART VIRUS; ANUS NEOPLASMS; CARCINOMA IN SITU; FEMALE; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS; MALE; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PATHOGENICITY; UTERINE CERVICAL NEOPLASMS; VIROLOGY;

ANTI-RETROVIRAL AGENTS; ANUS NEOPLASMS; CARCINOMA IN SITU; FEMALE; HIV; HIV INFECTIONS; HUMANS; MALE; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; UTERINE CERVICAL NEOPLASMS;

EID: 84925502028     PISSN: 15483568     EISSN: 15483576     Source Type: Journal    
DOI: 10.1007/s11904-014-0254-4     Document Type: Review

References (97)

1. Stanley M, Lowy DR, Frazer I. Chapter 12: prophylactic HPV vaccines: underlying mechanisms. Vaccine. 2006;24 Suppl 3:S3/106–13.
2. Schiffman M et al. Human papillomavirus and cervical cancer. Lancet. 2007;370(9590):890–907.
3. Centers for Disease, C. and Prevention. Human papillomavirus-associated cancers—United States, 2004–2008. MMWR Morb Mortal Wkly Rep. 2012;61:258–61.
4. Chaturvedi AK et al. Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst. 2009;101(16):1120–30.
5. Frisch M, Biggar RJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst. 2000;92(18):1500–10.
6. Patel P et al. Incidence of types of cancer among HIV-infected persons compared with the general population in the United States, 1992–2003. Ann Intern Med. 2008;148(10):728–36.
7. High KP et al. HIV and aging: state of knowledge and areas of critical need for research. A report to the NIH Office of AIDS Research by the HIV and Aging Working Group. J Acquir Immune Defic Syndr. 2012;60 Suppl 1:S1–18.
8. Smith JS et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007;121(3):621–32.
9. Ferlay J, et al. GLOBOCAN 2012 v1.0, Cancer incidence and mortality worldwide: IARC CancerBase No.11 [Internet]. 2012; Available from: http://globocan.iarc.fr, accessed on 11/28/2014.
10. Howlader N, et al. SEER Cancer Statistics Review, 1975–2011, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2011/, based on November 2013 SEER data submission, posted to the SEER web site, April 2014. 2014; Available from: http://seer.cancer.gov/csr/1975_2011/.
11. International Collaboration of Epidemiological Studies of Cervical, C. Comparison of risk factors for invasive squamous cell carcinoma and adenocarcinoma of the cervix: collaborative reanalysis of individual data on 8,097 women with squamous cell carcinoma and 1,374 women with adenocarcinoma from 12 epidemiological studies. Int J Cancer. 2007;120(4):885–91.
12. Castro KG et al. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recomm Rep. 1992;41(RR-17):1–19.
13. Bower M, Mazhar D, Stebbing J. Should cervical cancer be an acquired immunodeficiency syndrome-defining cancer? J Clin Oncol. 2006;24(16):2417–9.
14. Clifford GM et al. Cancer risk in the Swiss HIV Cohort Study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy. J Natl Cancer Inst. 2005;97(6):425–32.
15. Hleyhel M et al. Risk of AIDS-defining cancers among HIV-1-infected patients in France between 1992 and 2009: results from the FHDH-ANRS CO4 cohort. Clin Infect Dis. 2013;57(11):1638–47. Data from large French HIV cohort that summarizes the most recent incidence trends of AIDS-defining malignancies.
16. Mbulaiteye SM et al. Spectrum of cancers among HIV-infected persons in Africa: the Uganda AIDS-Cancer Registry Match Study. Int J Cancer. 2006;118(4):985–90.
17. Tanon A et al. The spectrum of cancers in West Africa: associations with human immunodeficiency virus. PLoS One. 2012;7(10):e48108.
18. Sasco AJ et al. The challenge of AIDS-related malignancies in sub-Saharan Africa. PLoS One. 2010;5(1):e8621.
19. Dhir AA et al. Spectrum of HIV/AIDS related cancers in India. Cancer Causes Control. 2008;19(2):147–53.
20. Guiguet M et al. Effect of immunodeficiency, HIV viral load, and antiretroviral therapy on the risk of individual malignancies (FHDH-ANRS CO4): a prospective cohort study. Lancet Oncol. 2009;10(12):1152–9.
21. Biggar RJ et al. AIDS-related cancer and severity of immunosuppression in persons with AIDS. J Natl Cancer Inst. 2007;99(12):962–72.
22. Franceschi S et al. Changing patterns of cancer incidence in the early- and late-HAART periods: the Swiss HIV Cohort Study. Br J Cancer. 2010;103(3):416–22.
23. Shiels MS et al. Cancer burden in the HIV-infected population in the United States. J Natl Cancer Inst. 2011;103(9):753–62.
24. Hoots BE et al. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer. 2009;124(10):2375–83.
25. Steinau M et al. Human papillomavirus prevalence in invasive anal cancers in the United States before vaccine introduction. J Low Genit Tract Dis. 2013;17(4):397–403. Used SEER registry to identify and perform HPV testing on anal cancer specimens. 90% of anal cancers are associated with HPV-infection, primarily HPV-16.
26. Darragh T, et al. The anal canal and perianus: HPV-related disease, in modern colposcopy: textbook and atlas E.J. Mayeaux and J. Thomas Cox, Editors. 2012, Lippincott, Williams, & Wilkins: Baltimore.
27. Brewster DH, Bhatti LA. Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975–2002. Br J Cancer. 2006;95(1):87–90.
28. Robinson D, Coupland V, Moller H. An analysis of temporal and generational trends in the incidence of anal and other HPV-related cancers in Southeast England. Br J Cancer. 2009;100(3):527–31.
29. Nielsen A, Munk C, Kjaer SK. Trends in incidence of anal cancer and high-grade anal intraepithelial neoplasia in Denmark, 1978–2008. Int J Cancer. 2012;130(5):1168–73.
30. Jin F et al. Trends in anal cancer in Australia, 1982–2005. Vaccine. 2011;29(12):2322–7.
31. van der Zee RP et al. The increasing incidence of anal cancer: can it be explained by trends in risk groups? Neth J Med. 2013;71(8):401–11.
32. Daling JR et al. Correlates of homosexual behavior and the incidence of anal cancer. JAMA. 1982;247(14):1988–90.
33. Daling JR et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med. 1987;317(16):973–7.
34. Frisch M et al. Sexually transmitted infection as a cause of anal cancer. N Engl J Med. 1997;337(19):1350–8.
35. Saleem AM et al. Risk of anal cancer in a cohort with human papillomavirus-related gynecologic neoplasm. Obstet Gynecol. 2011;117(3):643–9.
36. Piketty C et al. Incidence of HIV-related anal cancer remains increased despite long-term combined antiretroviral treatment: results from the French hospital database on HIV. J Clin Oncol. 2012;30(35):4360–6. Data from large French HIV cohort that summarizes recent incidence trends for anal cancer in HIV-infected patients.
37. Silverberg MJ et al. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis. 2012;54(7):1026–34. Recent incidence rates of anal cancer among HIV-infected patients in the US.
38. Silverberg MJ et al. HIV infection, immunodeficiency, viral replication, and the risk of cancer. Cancer Epidemiol Biomarkers Prev. 2011;20(12):2551–9.
39. Crum-Cianflone NF et al. Anal cancers among HIV-infected persons: HAART is not slowing rising incidence. AIDS. 2010;24(4):535–43.
40. Shiels MS et al. Impact of the HIV epidemic on the incidence rates of anal cancer in the United States. J Natl Cancer Inst. 2012;104(20):1591–8.
41. Prevention, C.f.D.C.a. HIV surveillance report, 2011. 2013 November 28 2013]; Available from: http://www.cdc.gov/hiv/topics/surveillance/resources/reports/.
42. Bertisch B et al. Risk factors for anal cancer in persons infected with HIV: a nested case-control study in the Swiss HIV Cohort Study. Am J Epidemiol. 2013;178(6):877–84.
43. Chiao EY et al. The impact of HIV viral control on the incidence of HIV-associated anal cancer. J Acquir Immune Defic Syndr. 2013;63(5):631–8.
44. Weaver BA. Epidemiology and natural history of genital human papillomavirus infection. J Am Osteopath Assoc. 2006;106(3 Suppl 1):S2–8.
45. Dunne EF et al. Prevalence of HPV infection among females in the United States. JAMA. 2007;297(8):813–9.
46. Chin-Hong PV et al. Age-Specific prevalence of anal human papillomavirus infection in HIV-negative sexually active men who have sex with men: the EXPLORE study. J Infect Dis. 2004;190(12):2070–6.
47. Hernandez BY et al. Anal human papillomavirus infection in women and its relationship with cervical infection. Cancer Epidemiol Biomarkers Prev. 2005;14(11 Pt 1):2550–6.
48. Silverberg MJ et al. The impact of HIV infection and immunodeficiency on human papillomavirus type 6 or 11 infection and on genital warts. Sex Transm Dis. 2002;29(8):427–35.
49. Massad LS et al. Prevalence and predictors of squamous cell abnormalities in Papanicolaou smears from women infected with HIV-1. Women's Interagency HIV Study Group. J Acquir Immune Defic Syndr. 1999;21(1):33–41.
50. Palefsky JM et al. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst. 1999;91(3):226–36.
51. Jamieson DJ et al. Characterization of genital human papillomavirus infection in women who have or who are at risk of having HIV infection. Am J Obstet Gynecol. 2002;186(1):21–7.
52. Watts DH et al. Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis. 2005;191(7):1129–39.
53. de Pokomandy A et al. Prevalence, clearance, and incidence of anal human papillomavirus infection in HIV-infected men: the HIPVIRG cohort study. J Infect Dis. 2009;199(7):965–73.
54. Conley L et al. Factors associated with prevalent abnormal anal cytology in a large cohort of HIV-infected adults in the United States. J Infect Dis. 2010;202(10):1567–76.
55. Palefsky JM et al. Prevalence and risk factors for anal human papillomavirus infection in human immunodeficiency virus (HIV)-positive and high-risk HIV-negative women. J Infect Dis. 2001;183(3):383–91.
56. Piketty C et al. High prevalence of anal human papillomavirus infection and anal cancer precursors among HIV-infected persons in the absence of anal intercourse. Ann Intern Med. 2003;138(6):453–9.
57. Nyitray AG et al. Prevalence of and risk factors for anal human papillomavirus infection in men who have sex with women: a cross-national study. J Infect Dis. 2010;201(10):1498–508.
58. Strickler HD et al. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst. 2005;97(8):577–86. First study to show that newly detected HPV infection occurs in celibate women, suggesting the reactivation of previously latent HPV infection.
59. Lillo FB et al. Human papillomavirus infection and associated cervical disease in human immunodeficiency virus-infected women: effect of highly active antiretroviral therapy. J Infect Dis. 2001;184(5):547–51.
60. Del Mistro A et al. Antiretroviral therapy and the clinical evolution of human papillomavirus-associated genital lesions in HIV-positive women. Clin Infect Dis. 2004;38(5):737–42.
61. Palefsky JM et al. Effect of highly active antiretroviral therapy on the natural history of anal squamous intraepithelial lesions and anal human papillomavirus infection. J Acquir Immune Defic Syndr. 2001;28(5):422–8.
62. Konopnicki D et al. Sustained viral suppression and higher CD4+ T-cell count reduces the risk of persistent cervical high-risk human papillomavirus infection in HIV-positive women. J Infect Dis. 2013;207(11):1723–9. Large cohort study of HIV-infected women with extended follow-up time. Shows very limited effect of ART in decreasing the risk of persistent cervical hr-HPV infection.
63. Blitz S et al. Evaluation of HIV and highly active antiretroviral therapy on the natural history of human papillomavirus infection and cervical cytopathologic findings in HIV-positive and high-risk HIV-negative women. J Infect Dis. 2013;208(3):454–62. Additional recent large cohort of HIV-infected women with extended follow-up time. Shows limited effect of ART in promoting regression of SIL.
64. Minkoff H et al. Influence of adherent and effective antiretroviral therapy use on human papillomavirus infection and squamous intraepithelial lesions in human immunodeficiency virus-positive women. J Infect Dis. 2010;201(5):681–90.
65. van der Snoek EM et al. Use of highly active antiretroviral therapy is associated with lower prevalence of anal intraepithelial neoplastic lesions and lower prevalence of human papillomavirus in HIV-infected men who have sex with men. Sex Transm Dis. 2012;39(7):495–500.
66. The 1988 Bethesda System for reporting cervical/vaginal cytological diagnoses. National Cancer Institute Workshop. JAMA, 1989. 262(7): p. 931–4.
67. Darragh TM et al. The Lower Anogenital Squamous Terminology Standardization Project for HPV-associated lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. J Low Genit Tract Dis. 2012;16(3):205–42. Describes the Lower Anogenital Terminology Standardization (LAST) project and new proposed terminology to classify HPV lesion.
68. Wright TC, Kurman RJ, and Ferenczy A. Precancerous lesions of the cervix, in Blaustein’s pathology of the female genital tract, Kurman RJ, Editor. 2002, Springer-Verlag: New York City. p. 277.
69. Rodriguez AC et al. Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections. J Natl Cancer Inst. 2008;100(7):513–7.
70. Committee on Practice, B.-G. ACOG practice bulletin number 131: screening for cervical cancer. Obstet Gynecol. 2012;120(5):1222–38.
71. Duerr A et al. Human papillomavirus-associated cervical cytologic abnormalities among women with or at risk of infection with human immunodeficiency virus. Am J Obstet Gynecol. 2001;184(4):584–90.
72. Chirenje ZM et al. Association of cervical SIL and HIV-1 infection among Zimbabwean women in an HIV/STI prevention study. Int J STD AIDS. 2002;13(11):765–8.
73. Ellerbrock TV et al. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA. 2000;283(8):1031–7.
74. Palefsky JM et al. Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men. AIDS. 2005;19(13):1407–14.
75. Chin-Hong PV et al. Comparison of patient- and clinician-collected anal cytology samples to screen for human papillomavirus-associated anal intraepithelial neoplasia in men who have sex with men. Ann Intern Med. 2008;149(5):300–6.
76. Hessol NA et al. Anal intraepithelial neoplasia in a multisite study of HIV-infected and high-risk HIV-uninfected women. AIDS. 2009;23(1):59–70.
77. Kojic EM et al. Human papillomavirus infection and cytologic abnormalities of the anus and cervix among HIV-infected women in the study to understand the natural history of HIV/AIDS in the era of effective therapy (the SUN study). Sex Transm Dis. 2011;38(4):253–9.
78. Palefsky JM. Antiretroviral therapy and anal cancer: the good, the bad, and the unknown. Sex Transm Dis. 2012;39(7):501–3.
79. de Pokomandy A et al. HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect Dis. 2011;52(9):1174–81.
80. Gunthard HF et al. Antiretroviral treatment of adult HIV infection: 2014 recommendations of the International Antiviral Society-USA Panel. JAMA. 2014;312(4):410–25.
81. McCredie MR et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol. 2008;9(5):425–34. Describes New Zealand study that quantified risk of cervical HSIL progression in HIV-uninfected women.
82. Holowaty P et al. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst. 1999;91(3):252–8.
83. Machalek DA et al. Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol. 2012;13(5):487–500. Uses data from meta-analysis to estimate yearly risk of developing anal cancer among HIV-infected and HIV-uninfected MSM with HSIL.
84. Doorbar J. The papillomavirus life cycle. J Clin Virol. 2005;32 Suppl 1:S7–15.
85. Herfs M et al. Mucosal junctions: open doors to HPV and HIV infections? Trends Microbiol. 2011;19(3):114–20.
86. Zheng ZM, Baker CC. Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci. 2006;11:2286–302.
87. Selvakumar R et al. Regression of papillomas induced by cottontail rabbit papillomavirus is associated with infiltration of CD8+ cells and persistence of viral DNA after regression. J Virol. 1997;71(7):5540–8.
88. Maglennon GA, McIntosh P, Doorbar J. Persistence of viral DNA in the epithelial basal layer suggests a model for papillomavirus latency following immune regression. Virology. 2011;414(2):153–63.
89. Ojesina AI et al. Landscape of genomic alterations in cervical carcinomas. Nature. 2014;506(7488):371–5.
90. Barrow-Laing L, Chen W, Roman A. Low- and high-risk human papillomavirus E7 proteins regulate p130 differently. Virology. 2010;400(2):233–9.
91. Fang J, Zhang H, Jin S. Epigenetics and cervical cancer: from pathogenesis to therapy. Tumour Biol. 2014;35(6):5083–93.
92. Tugizov SM et al. HIV-associated disruption of mucosal epithelium facilitates paracellular penetration by human papillomavirus. Virology. 2013;446(1–2):378–88. In vitro study that shows how HIV-derived tat and gp120 disrupt epithelial tight-cell junctions which allow HPV pseudovirion infection of the basal cell l epithelium.
93. van der Burg SH, Palefsky JM. Human immunodeficiency virus and human papilloma virus—why HPV-induced lesions do not spontaneously resolve and why therapeutic vaccination can be successful. J Transl Med. 2009;7:108.
94. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 2008;1(1):23–30.
95. Nowak RG et al. Increases in human papillomavirus detection during early HIV infection among women in Zimbabwe. J Infect Dis. 2011;203(8):1182–91. Cohort study showing a rapid rise in cervical HPV infection soon after HIV infection. Argues that immune dysregulation associated with acute HIV leads to the reactivation of previously latent HPV.
96. Wang C et al. Rapid rise in detection of human papillomavirus (HPV) infection soon after incident HIV infection among South African women. J Infect Dis. 2011;203(4):479–86. Cohort study showing a rapid rise in cervical HPV infection soon after HIV infection. Argues that immune dysregulation associated with acute HIV leads to the reactivation of previously latent HPV.
97. Borges AH, Dubrow R, Silverberg MJ. Factors contributing to risk for cancer among HIV-infected individuals, and evidence that earlier combination antiretroviral therapy will alter this risk. Curr Opin HIV AIDS. 2014;9(1):34–40.