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.
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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).
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