Epidemiology and Social
Human papillomavirus types among women infected with HIV: a meta-analysis
Clifford, Gary Ma; Gonçalves, Maria Alice Ga,b; Franceschi, Silviaa; for the HPV and HIV Study Group
From the aInternational Agency for Research on Cancer, Lyon, France
bDivision of Clinical Immunology, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.
*See the Appendix for study members.
Received 8 May, 2005
Accepted 7 July, 2006
Correspondence to G.M. Clifford, International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon cedex 08, France. E-mail: firstname.lastname@example.org.
Background: HIV-positive women have a high prevalence of human papillomavirus (HPV) infection and are infected with a broader range of HPV types than HIV-negative women. It is not known to what extent these different types are associated with high-grade squamous intraepithelial lesions (HSIL) and cancer.
Methods: Meta-analysis of HPV type-specific prevalence among HIV-positive women, stratified by geographical region and by cervical cytology: normal, atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesions (ASCUS/LSIL) or HSIL.
Results: In 20 studies, 5578 HIV-positive women were identified, largely from North America but also Africa, Asia, Europe and South/Central America. For 3230 with no cytological abnormalities, prevalence was 36.3% for any HPV and 11.9% for multiple HPV types. The six most common high-risk HPV types were 16 (4.5%), 58 (3.6%), 18 (3.1%), 52 (2.8%), 31 (2.0%) and 33 (2.0%). HPV16 was also the most common type in 2053 HIV-positive women with ASCUS/LSIL and 295 with HSIL. Those with HSIL were significantly less likely to be infected with HPV16 (odds ratio, 0.6; 95% confidence interval, 0.4–0.7) than the general female population with HSIL. In contrast, HIV-positive women with HSIL were significantly more likely to be infected with HPV types 11, 18, 33, 51, 52, 53, 58 and 61, and with multiple HPV types.
Conclusions: The proportion of HIV-positive women with HPV16 rose with increasing severity of cervical lesions. Nevertheless, HPV16 remained underrepresented in HIV-positive women with HSIL, who showed a higher proportion of other HPV types and multiple types compared with the general female population with HSIL.
The most important known determinant of human papillomavirus (HPV) persistence and progression to cancer is viral type, notably the presence of HPV16 [1–3]. Immune suppression by HIV infection also appears to worsen the outcome of HPV infection . Women infected with HIV are at significantly increased risk for invasive cervical cancer [5–8], which cannot be explained purely by a higher incidence of HPV infection among these women. Indeed, HPV infections are more likely to persist in HIV-positive women than in HIV-negative women [9–11], and this persistence contributes to a higher prevalence of HPV infection among HIV-positive women [12–15], and a higher-risk for low-grade (L) and high-grade (H) squamous intraepithelial lesions (SIL) [16–18].
There is evidence to suggest that HIV-positive women without cytological abnormalities may be infected with a broader range of HPV types than HIV-negative women [4,13,19–22]. Furthermore, HPV prevalence among HIV-positive women increases with lowering immune status [13,23], with HPV16 being notably more weakly associated with immune status than other HPV types . However, it remains unclear to what extent HPV types that rarely progress to severe lesions in immunocompetent women can cause HSIL and invasive cancer among HIV-positive women. This question is particularly relevant with regard to cervical cancer prevention in this high-risk population, given that the approaches of HPV-based screening, as well as prophylactic HPV vaccines [24,25], are HPV type specific.
This study aimed to collate all the published information on HPV type distribution among HIV-positive women, according to the severity of cervical lesions. It also provides a comparison of HPV type distribution in HIV-positive women with HSIL with previously published data on HSIL from the general female population .
Medline was used to search for articles published from January 1989 to June 2005, by means of the MeSH terms: ‘human immunodeficiency virus’, ‘human papillomavirus’, ‘cervical intraepithelial neoplasia’, ‘cervical neoplasia’, ‘squamous intraepithelial lesions’, ‘human’ and ‘female’ in combination with keywords ‘polymerase chain reaction’ or ‘PCR’. Selected studies had to include at least 20 HIV-positive women who had both cervical cytology and HPV test results. Moreover, HPV detection had to have been by one of four validated PCR primer sets, or refinements of them (MY09/11 , PGMY09/11 , GP5+/6+  or SPF10 ) and report type-specific HPV prevalence for at least HPV16 and HPV18.
The following key variables were extracted and cross-checked by two investigators (M.A.G. and G.M.C.): cervical cytology results [normal, atypical squamous cells of undetermined significance (ASCUS)/LSIL, or HSIL]; presence/absence of histological confirmation; PCR primers used to detect HPV; and overall and type-specific prevalence of HPV infection. For cohort studies, only baseline data were considered. Each study was classified according to one of five broad geographical regions: Africa, Europe, North America, South/Central America, and Asia. Most publications did not present HPV prevalence among HIV-positive women in the required format (i.e., broken down by HPV type and cytological diagnosis), so data requests were made to authors. In the course of contacting authors, additional data became available for three studies expanded since their original publication [31–33]. Detailed information on all included studies [10,13–14,17–23,31–40] are available on-line at www.aidsonline.com.
Type-specific HPV prevalence data stratified by cervical cytology was not available for two eligible studies, from Canada  and Malawi , respectively; these, therefore, could not be included.
Estimation of type-specific prevalence
Type-specific prevalence is presented (a) for 13 high-risk HPV types included in the Hybrid Capture 2® screening test , namely 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59 and 68; (b) for HPV6 and HPV11, the two low-risk wart-related types included in the licensed quadrivalent HPV16/18/6/11 vaccine ; and (c) for the next five most common low-risk HPV types, as identified by this review.
All studies provided information on HPV16 and HPV18. For other types, prevalence was estimated only among those studies testing for the HPV type in question; therefore, sample size varied across the different analyses but was always based on at least 100 cases. Of the types reported in analyses, all were considered to be satisfactorily amplified by PCR primers MY09/11, PGMY09/11 and SPF10, and all except HPV53 to be satisfactorily amplified by GP5+/6+ . Type-specific prevalence included either single or multiple infections, since many of the included studies did not publish the type-specific breakdown for multiple infections.
Because of the scarcity of data, 14 HIV-positive women with invasive cervical cancer were not included [14,17,18,23,34]. Six HIV-positive women with invasive cervical cancer were positive for HPV16, one for HPV16/35, one for HPV33/45, one for HPV11/73/84, two for HPV18, one for HPV52 and two were apparently HPV negative.
Type-specific HPV prevalence is expressed as a crude proportion with corresponding 95% confidence intervals (CI) calculated assuming a normal distribution.
Among HIV-positive women without cervical abnormalities, type-specific HPV prevalence was compared across the five regions (Africa, Asia, Europe, North America, South/Central America) among HPV-positive women only, by the use of χ2 tests with four degrees of freedom.
Type-specific HPV prevalence in HSIL was compared between the HIV-positive women and the general female population  by the use of odds ratios (OR), adjusted for geographical region, by unconditional logistic regression.
A total of 5578 HIV-positive women from 20 studies were included in these analyses (Table 1). HIV-positive women came predominantly from North America (58.2%) but also from countries in Europe (15.2%), Africa (13.9%), South/Central America (7.8%) and Asia (4.8%). Detailed HPV type-specific data on each of the 20 included studies are presented stratified by cytological results in Appendices A (no cytological abnormalities), B (ASCUS/LSIL) and C (HSIL).
The overall prevalence of HPV infection among HIV-positive women was 36.3% for those without cytological abnormalities, and increased to 69.4% for those with ASCUS/LSIL and 84.1% for those with HSIL. The prevalence of infection in HIV-positive women with multiple HPV types was 11.9% for those without cytological abnormalities (32.8% of all HPV positive), and increased to 34.7% for those with ASCUS/LSIL (50.0% of all HPV positive) and 41.1% for those with HSIL (48.9% of all HPV positive).
Type-specific HPV prevalence among 3230 HIV-positive women without cytological abnormalities is shown in Fig. 1, overall and by region. HPV prevalence was 56.6% in Africa, 31.1% in Asia, 32.4% in Europe, 31.4% in North America and 57.3% in South/Central America. HPV16 was the most commonly identified type, present in 4.5% of all HIV-positive women without cytological abnormalities (12.4% of all HPV positive). The next most common high-risk types among women without cytological abnormalities were, in decreasing order of prevalence, types 58 (3.6%), 18 (3.1%), 52 (2.8%), 31 (2.0%) and 33 (2.0%). The most common low-risk type was HPV53 (4.4%). A total of 26 individual types were each found in more than 1.0% of all HIV-positive women without cytological abnormalities (data not shown).
The relative distribution of HPV types appeared to vary by geographical region (Fig. 1). The strongest differences by region were seen for HPV31 (P < 0.001) and HPV35 (P < 0.001), which were particularly high in Africa; for HPV39 (P < 0.001), which was particularly high in Asia; and for HPV68 (P = 0.004), which was particularly high in South/Central America.
Type-specific HPV prevalence among 2053 HIV-positive women with ASCUS/LSIL and 295 with HSIL is shown in Fig. 2. HPV16 was nearly three times more prevalent in those with HSIL (31.9%) than in those with ASCUS/LSIL (12.0%) (P < 0.001). HPV types 18, 31 and 33 were also significantly more prevalent in those with HSIL than in those with ASCUS/LSIL (P = 0.012, P = 0.032 and P < 0.001, respectively). HPV6 was significantly less prevalent in those with HSIL than in those with ASCUS/LSIL (P = 0.050). For all other HPV types, prevalence in HSIL was not significantly different to that in ASCUS/LSIL.
HPV type-specific prevalence among those with HSIL was compared between HIV-positive women and the general female population, as published in a previous meta-analysis  (Table 2). Prevalence of any HPV was similar for HSIL in HIV-positive women (84.1%) and in the general female population (84.2%), but HIV-positive women with HSIL were much more likely to be infected with multiple HPV types (41.4%) than their counterparts from the general female population (6.7%) (OR, 9.3; 95% CI, 6.9–12.4). HSIL among HIV-positive women was significantly less likely to harbour HPV16 than HSIL in the general female population (OR, 0.6; 95% CI, 0.4–0.7). HPV35 also appeared slightly under-represented in HSIL in HIV-positive women, but the difference was not significant. In contrast, HSIL in HIV-positive women was approximately 50% more likely to harbour HPV types 18 and 33, approximately two-fold more likely to harbour HPV types 51, 52 and 58, and over three-fold more likely to harbour HPV types 11, 53 and 61, which were rarely detected (< 2.5%) in HSIL from the general female population.
This meta-analysis is the first, to our knowledge, to assess type-specific HPV prevalence in a large number of HIV-positive women from four continents by severity of cytological abnormalities, and to allow a comparison with that in the general female population. Our findings showed that the proportion of HPV prevalence attributable to HPV16 is lower in HIV-positive women, including those with HSIL, than in the general female population.
More than one-third of all HIV-positive women without cytological abnormalities were infected with HPV. HPV prevalence was higher in HIV-positive women from Africa and South/Central America than in those from Europe and North America, paralleling differences seen in the general female population from the corresponding regions .
HPV type spectrum among HIV-positive women without cytological abnormalities was confirmed to be broad, with 26 individual types found in more than 1% of HIV-positive women, many of which were present as multiple infections. Among HIV-positive women, HPV16 did not predominate over other HPV types to the same extent as seen in the general female population [45–47].
Among HIV-positive women, regardless of whether women with normal cytology or women with ASCUS/LSIL were taken as the comparison group, women with HSIL had increased HPV prevalence and HPV16 and HPV18 became increasingly dominant over other types, as seen in the general female population [46,48]. Nevertheless, even among women with HSIL, evidence remained of a shift towards HPV types other than HPV16 in HIV-positive women. A comparison with the HPV type distribution from similarly generated data from the general female population with HSIL  showed that HIV-positive women with HSIL were significantly less likely to be infected with HPV16 and concurrently more likely to be infected with high-risk HPV types other than HPV16 (i.e., HPV18, 51, 52 and 58). Furthermore, the low-risk HPV types, 11, 53 and 61, were detected much more frequently in HIV-positive women with HSIL than in the general female population with HSIL. This suggests that these types, which have little potential to cause neoplastic changes in women without an HIV infection , may induce HSIL in immunosuppressed women.
However, this interpretation is complicated by the fact that HIV-positive women with HSIL from this meta-analysis were also much more likely to be infected with multiple HPV types than women with HSIL from the general female population. Consequently, HPV types rarely seen in HSIL from the general female population may, in HIV-positive women, simply represent benign infections in the presence of another type. For example, among 185 HPV-positive women with HSIL from the subset of studies testing for all high-risk types and providing the type-specific breakdown of multiple infections [14,17,19–23,31,32,34–36], 14 of 18 with HPV53 infections (a low-risk type) were found to be coinfected with a high-risk HPV type. Sixteen of these 185 HPV-positive HSIL had no evidence of high-risk HPV type infection.
Importantly, an internal comparison of the prevalence of each HPV type in the most (CD4 cell count < 200 cells/μl) and least (≥ 500 cells/μl) immunocompromised HIV-positive women of the two large US cohort studies included in this meta-analysis  showed that the prevalence and incidence of HPV16 was more weakly associated with CD4 cell count than that of other HPV types. One possible interpretation of HPV16's relative independence from immune status is that, through its evolution, it has created better mechanisms to avoid even intact host immune surveillance relative to other HPV types .
Some limitations of our meta-analysis are worth bearing in mind. Unfortunately, given that the data were primarily sourced from published articles, no individual information was available on age, CD4 cell count, HIV viral load or antiretroviral treatment that would allow adjustment or stratification of type-specific HPV prevalence for these variables. Even the four well-validated HPV PCR primers accepted for inclusion in this meta-analysis do not amplify all individual types , most notably in multiple-type infections , with the same sensitivity. Such differences are a potential source of variation in the detection of types between studies, particularly for types other than HPV16 and HPV18, and for comparisons with data on HSIL from the general female population, which included an even greater variety of HPV detection techniques . Furthermore, the quality of cytological and histological testing may also vary from one study to another and HSIL is not a good surrogate of truly precancerous lesions (i.e., cervical intraepithelial neoplasia grade 3).
Most importantly, our meta-analysis reveals that there are substantial limitations in the information on HPV type distribution in HIV-positive women with severe cervical lesions. HSIL represented a relatively small fraction of study women and histological confirmation was seldom reported. Only 14 cases of invasive cervical cancer in HIV-positive women were identified in this study. This lack of information should be remedied by additional studies of HPV type-specific distribution among HIV-positive women with cervical intraepithelial neoplasia grade 3 and invasive cervical cancer.
Sponsorship: The work of the core IARC staff was funded by grants from OncoSuisse (ICP OCS – 01355-03-2003) and the Bill & Melinda Gates Foundation (grant 35537). Maria Alice G. Gonçalves was a visiting scientist at the International Agency for Research on Cancer, Lyon, France. Her time at IARC was supported by FAPESP (97/04490-8; 01/02908-2), CAPES (0313-04-1) and the Ministry of Health (Brazil-France Cooperation). The Women's Interagency Health Study is funded by the National Institute of Allergy and Infectious Diseases with supplemental funding from the National Cancer Institute, and the National Institute on Drug Abuse (grants UO1-AI-35004, UO1-AI-31834, UO1-AI-34994, UO1-AI-34989, UO1-AI-34993 and UO1-AI-42590). Funding is also provided by the National Institute of Child Health and Human Development (grant UO1-HD-32632) and the National Center for Research Resources (grants MO1-RR-00071, MO1-RR-00079, MO1-RR-00083). The HIV Epidemiology Research Study is supported by cooperative agreements U64/CCU106795, U64/CCU206798, U64/CCU306802 and U64/CCU506831, Centers for Disease Control and Prevention. The Reaching for Excellence in Adolescent Care and Health cohort is supported by NIH Grants U01-HD32830 from the National Institute of Child Health and Human Development with cofunding from the National Institutes of Drug Abuse, Allergy and Infectious Diseases, and Mental Health.
1. Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001; 286:3106–3114.
2. Castle PE, Schiffman M, Herrero R, Hildesheim A, Rodriguez AC, Bratti MC, et al. A prospective study of age trends in cervical human papillomavirus acquisition and persistence in Guanacaste, Costa Rica. J Infect Dis 2005; 191:1808–1816.
3. Schiffman M, Herrero R, Desalle R, Hildesheim A, Wacholder S, Rodriguez AC, et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337:76–84.
4. Palefsky JM, Holly EA. Chapter 6: Immunosuppression and co-infection with HIV. J Natl Cancer Inst Monogr 2003; 31:41–46.
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; 92:1500–1510.
6. Dal Maso L, Franceschi S, Polesel J, Braga C, Piselli P, Crocetti E, et al. Risk of cancer in persons with AIDS in Italy. Br J Cancer 2003; 89:94–100.
7. Clifford GM, Polesel J, Rickenbach M, Dal Maso L, Keiser O, Kofler A, et al. Cancer risk in the Swiss HIV Cohort Study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy. J Natl Cancer Inst 2005; 97:425–432.
8. Mbulaiteye SM, Katabira ET, Wabinga H, Parkin DM, Virgo P, Ochai R, et al. Spectrum of cancers among HIV-infected persons in Africa: The Uganda AIDS–Cancer Registry Match Study. Int J Cancer 2006; 118:985–990.
9. Minkoff H, Feldman J, DeHovitz J, Landesman S, Burk R. A longitudinal study of human papillomavirus carriage in human immunodeficiency virus-infected and human immunodeficiency virus-uninfected women. Am J Obstet Gynecol 1998; 178:982–986.
10. Moscicki AB, Ellenberg JH, Farhat S, Xu J. Persistence of human papillomavirus infection in HIV-infected and -uninfected adolescent girls: risk factors and differences, by phylogenetic type. J Infect Dis 2004; 190:37–45.
11. Ahdieh L, Klein RS, Burk R, Cu-Uvin S, Schuman P, Duerr A, et al. Prevalence, incidence, and type-specific persistence of human papillomavirus in human immunodeficiency virus (HIV)-positive and HIV-negative women. J Infect Dis 2001; 184:682–690.
12. Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC Jr. Human papillomavirus infection in women infected with the human immunodeficiency virus. N Engl J Med 1997; 337:1343–1349.
13. Chaturvedi AK, Dumestre J, Gaffga AM, Mire KM, Clark RA, Braly PS, et al. Prevalence of human papillomavirus genotypes in women from three clinical settings. J Med Virol 2005; 75:105–113.
14. de Vuyst H, Steyaert S, van Renterghem L, Claeys P, Muchiri L, Sitati S, et al. Distribution of human papillomavirus in a family planning population in Nairobi, Kenya. Sex Transm Dis 2003; 30:137–142.
15. Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, et al. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst 1999; 91:226–236.
16. Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, et al. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA 2000; 283:1031–1037.
17. La Ruche G, You B, Mensah-Ado I, Bergeron C, Montcho C, Ramon R, et al. Human papillomavirus and human immunodeficiency virus infections: relation with cervical dysplasia–neoplasia in African women. Int J Cancer 1998; 76:480–486.
18. Hawes SE, Critchlow CW, Faye Niang MA, Diouf MB, Diop A, Toure P, et al. Increased risk of high-grade cervical squamous intraepithelial lesions and invasive cervical cancer among African women with human immunodeficiency virus type 1 and 2 infections. J Infect Dis 2003; 188:555–563.
19. Cappiello G, Garbuglia AR, Salvi R, Rezza G, Giuliani M, Pezzotti P, et al. HIV infection increases the risk of squamous intra-epithelial lesions in women with HPV infection: an analysis of HPV genotypes. DIANAIDS Collaborative Study Group. Int J Cancer 1997; 72:982–986.
20. Goncalves MA, Massad E, Burattini MN, Villa LL. Relationship between human papillomavirus (HPV) genotyping and genital neoplasia in HIV-positive patients of Santos City, Sao Paulo, Brazil. Int J STD AIDS 1999; 10:803–807.
21. Levi JE, Kleter B, Quint WG, Fink MC, Canto CL, Matsubara R, et al. High prevalence of human papillomavirus (HPV) infections and high frequency of multiple HPV genotypes in human immunodeficiency virus-infected women in Brazil. J Clin Microbiol 2002; 40:3341–3345.
22. Baay MF, Kjetland EF, Ndhlovu PD, Deschoolmeester V, Mduluza T, Gomo E, et al. Human papillomavirus in a rural community in Zimbabwe: the impact of HIV co-infection on HPV genotype distribution. J Med Virol 2004; 73:481–485.
23. Strickler HD, Palefsky JM, Shah KV, Anastos K, Klein RS, Minkoff H, et al. Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst 2003; 95:1062–1071.
24. Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, et al. 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 2005; 6:271–278.
25. Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, et al. 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 2004; 364:1757–1765.
26. Clifford GM, Smith JS, Aguado T, Franceschi S. Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer 2003; 89:101–105.
27. Bernard HU, Chan SY, Manos MM, Ong CK, Villa LL, Delius H, et al. Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis 1994; 170:1077–1085.
28. Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, et al. Improved amplification of genital human papillomaviruses. J Clin Microbiol 2000; 38:357–361.
29. Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, Snijders PJ. The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 1995; 76:1057–1062.
30. Kleter B, van Doorn LJ, Schrauwen L, Molijn A, Sastrowijoto S, ter Schegget J, et al. 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 1999; 37:2508–2517.
31. Del Mistro A, Bonaldi L, Bertorelle R, Minucci D, Franzetti M, Cattelan A, et al. Genital human papillomavirus types in immunocompetent and immunodepressed women in Northeast Italy: prevalence and cytomorphological correlations. J Low Genit Tract Dis 2001; 5:12–20.
32. de Sanjose S, Valls I, Paz CM, Lloveras B, Quintana MJ, Shah KV, et al. Human papillomavirus and human immunodeficiency virus infections as risk factors for cervix cancer in women prisoners. Med Clin (Barc) 2000; 115:81–84.
33. van Doornum GJ, van den Hoek JA, van Ameijden EJ, van Haastrecht HJ, Roos MT, Henquet CJ, et al. Cervical HPV infection among HIV-infected prostitutes addicted to hard drugs. J Med Virol 1993; 41:185–190.
34. Jamieson DJ, Duerr A, Burk R, Klein RS, Paramsothy P, Schuman P, 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; 186:21–27.
35. Bollen LJ, Chuachoowong R, Kilmarx PH, Mock PA, Culnane M, Skunodom N, et al. Human papillomavirus (HPV) detection among human immunodeficiency virus-infected pregnant Thai women: implications for future HPV immunization. Sex Transm Dis 2006; 33:259–264.
36. Lillo FB, Ferrari D, Veglia F, Origoni M, Grasso MA, Lodini S, 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; 184:547–551.
37. Mayaud P, Gill DK, Weiss HA, Uledi E, Kopwe L, Todd J, et al. The interrelation of HIV, cervical human papillomavirus, and neoplasia among antenatal clinic attenders in Tanzania. Sex Transm Infect 2001; 77:248–254.
38. Thomas DB, Qin Q, Kuypers J, Kiviat N, Ashley RL, Koetsawang A, et al. Human papillomaviruses and cervical cancer in Bangkok. II. Risk factors for in situ and invasive squamous cell cervical carcinomas. Am J Epidemiol 2001; 153:732–739.
39. Rezza G, Giuliani M, Serraino D, Branca M, Benedetto A, Garbuglia A, et al. Risk factors for cervical presence of human papillomavirus DNA among women at risk for HIV infection. DIANAIDS Collaborative Study Group. Epidemiol Infect 1998; 121:173–177.
40. Volkow P, Rubi S, Lizano M, Carrillo A, Vilar-Compte D, Garcia-Carranca A, et al. High prevalence of oncogenic human papillomavirus in the genital tract of women with human immunodeficiency virus. Gynecol Oncol 2001; 82:27–31.
41. Coutlee F, Hankins C, Lapointe N. Comparison between vaginal tampon and cervicovaginal lavage specimen collection for detection of human papillomavirus DNA by the polymerase chain reaction. The Canadian Women's HIV Study Group. J Med Virol 1997; 51:42–47.
42. Miotti PG, Dallabetta GA, Daniel RW, Canner JK, Chiphangwi JD, Liomba GN, et al. Cervical abnormalities, human papillomavirus, and human immunodeficiency virus infections in women in Malawi. J Infect Dis 1996; 173:714–717.
43. Terry G, Ho L, Londesborough P, Cuzick J, Mielzynska-Lohnas I, Lorincz A. Detection of high-risk HPV types by the hybrid capture 2 test. J Med Virol 2001; 65:155–162.
44. Iftner T, Villa LL. Chapter 12: Human papillomavirus technologies. J Natl Cancer Inst Monogr 2003; 31:80–88.
45. Clifford GM, Gallus S, Herrero R, Munoz N, Snijders PJ, Vaccarella S, et al. 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 2005; 366:991–998.
46. Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, et al. Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis 2005; 191:1796–1807.
47. Liaw KL, Glass AG, Manos MM, Greer CE, Scott DR, Sherman M, et al. Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst 1999; 91:954–960.
48. Franceschi S, Clifford GM. Re: A study of the impact of adding HPV types to cervical cancer screening and triage tests. J Natl Cancer Inst 2005; 97:938–939.
The HPV and HIV Study Group comprises Guy La Ruche (National AIDS Program, Abidjan, Côte d'Ivoire); Hugo de Vuyst (International Centre for Reproductive Health, Ghent University, Belgium); Stephen Hawes (University of Washington, Seattle, WA, USA); Philippe Mayaud, Helene Weiss (London School of Hygiene & Tropical Medicine, London, UK); Marc Baay, (University of Antwerp, Antwerp, Belgium); Eyrun Kjetland (Ullevaal University Hospital, Oslo, Norway); Liesbeth Bollen (Thailand MOPH-US CDC Collaboration, Nonthaburi, Thailand); David Thomas (Fred Hutchinson Cancer Research Center, Seattle, WA, USA); Diego Serraino (Centro di Riferimento Oncologico, Aviano, Italy); Maria Capobianchi, Pierluca Piselli, Stefania Zaniratti (Instituto Nazionale Malattie Infective L. Spallanzani, Rome, Italy); Annarosa Del Mistro (Instituto Oncologico Veneto, Padova, Italy); Flavia Lillo (San Raffaele Hospital, Milan, Italy); Silvia de Sanjosé (Institut Català d' Oncologia, Barcelona, Spain); Gerard van Doornum (Erasmus MC, Rotterdam, the Netherlands); Paula Schuman [HIV Epidemiology Research Study (HERS), Detroit, MI, USA]; David Celentano, Keerti Shah (HERS, Baltimore, MD, USA); Robert Klein (HERS, New York, USA); Susan Cu-Uvin (HERS, Providence, RI, USA); Denise Jamieson (Centers for Disease Control and Prevention, Atlanta, GA, USA); Anna-Barbara Moscicki (Reaching for Excellence in Adolescent Care and Health Cohort, University of California, San Francisco, CA, USA); Michael Hagensee (Louisiana State University Health Science Center, New Orleans, LA, USA); Howard Strickler, Robert Burk, Kathryn Anastos [Womens Interagency HIV Study (WIHS), New York City/Bronx, NY, USA); Howard Minkoff (WIHS, Brooklyn, NY, USA); Mary Young (WIHS, Washington, DC, USA); Ruth Greenblatt, Joel Palefsky (WIHS, Northern California, USA); Alexandra Levine (WIHS, Los Angeles County/Southern California, USA); Mardge Cohen (WIHS, Chicago, IL, USA); Stephen Gange (WIHS, Data Coordinating Center); José Eduardo Levi (Instituto de Medicina Tropical da Universidade de São Paulo, São Paulo, Brazil); Patricia Volkow (Mexican National Institute of Cancer, Mexico City, Mexico).
human papillomavirus; cervical cancer; HIV; epidemiology
© 2006 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.