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Evidence of synergistic relationships between HIV and Human Papillomavirus (HPV): systematic reviews and meta‐analyses of longitudinal studies of HPV acquisition and clearance by HIV status, and of HIV acquisition by HPV status

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Looker, Katharine J, Rönn, Minttu M, Brock, Patrick M, Brisson, Marc, Drolet, Melanie, Mayaud, Philippe, Boily, Marie‐Claude·2018·Journal of the International AIDS Society
DOI 10.1002/jia2.25110PMC PMC5989783
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Abstract

Introduction: Observational studies suggest HIV and human papillomavirus (HPV) infections may have multiple interactions. We reviewed the strength of the evidence for the influence of HIV on HPV acquisition and clearance, and the influence of HPV on HIV acquisition. Methods: We performed meta‐analytic systematic reviews of longitudinal studies of HPV incidence and clearance rate by HIV status (review 1) and of HIV incidence by HPV status (review 2). We pooled relative risk (RR) estimates across studies using random‐effect models. I2 statistics and subgroup analyses were used to quantify heterogeneity across estimates and explore the influence of participant and study characteristics including study quality. Publication bias was examined quantitatively with funnel plots and subgroup analysis, as well as qualitatively. Results and Discussion: In review 1, 37 publications (25 independent studies) were included in the meta‐analysis. HPV incidence (pooled RR = 1.55, 95% CI: 1.29 to 1.88; heterosexual males: pooled RR = 1.95, 95% CI: 1.62, 2.34; females: pooled RR = 1.63, 95% CI: 1.26 to 2.11; men who have sex with men: pooled RR = 1.36, 95% CI: 1.01 to 1.82) and high‐risk HPV incidence (pooled RR = 2.20, 95% CI: 1.90 to 2.54) was approximately doubled among people living with HIV (PLHIV) whereas HPV clearance rate (pooled RR = 0.53, 95% CI: 0.42 to 0.67) was approximately halved. In review 2, 14 publications (11 independent studies) were included in the meta‐analysis. HIV incidence was almost doubled (pooled RR = 1.91, 95% CI 1.38 to 2.65) in the presence of prevalent HPV infection. There was more evidence of publication bias in review 2, and somewhat greater risk of confounding in studies included in review 1. There was some evidence that adjustment for key confounders strengthened the associations for review 2. Misclassification bias by HIV/HPV exposure status could also have biased estimates toward the null. Conclusions: These results provide evidence for synergistic HIV and HPV interactions of clinical and public health relevance. HPV vaccination may directly benefit PLHIV, and help control both HPV and HIV at the population level in high prevalence settings. Our estimates of association are useful for mathematical modelling. Although observational studies can never perfectly control for residual confounding, the evidence presented here lends further support for the presence of biological interactions between HIV and HPV that have a strong plausibility.

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  1. [2]Stanley MA, Sterling JC. Host responses to infection with human papillomavirus. Curr Probl Dermatol. 2014; 45: 58– 74. 24643178
  2. [7]Williamson AL. The interaction between human immunodeficiency virus and Human Papillomaviruses in heterosexuals in Africa. J Clin Med. 2015; 4(4): 579– 92. 26239348 PMC4470157
  3. [8]1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recommendations and reports: Morbidity and mortality weekly report Recommendations and reports/Centers for Disease Control. 1992;41(RR‐17):1‐19. 1361652
  4. [9]Bower M, Mazhar D, Stebbing J. Should cervical cancer be an acquired immunodeficiency syndrome‐defining cancer? J Clin Oncol. 2006; 24(16): 2417– 9. 16735700
  5. [10]Larke N, Thomas SL, Dos Santos Silva, I, Weiss, HA. Male circumcision and human papillomavirus infection in men: a systematic review and meta‐analysis. J Infect Dis. 2011; 204(9): 1375– 90. 21965090
  6. [11]Kelly H, Weiss HA, Benavente Y, de Sanjose S, Mayaud P; ART and HPV Review Group. Association of antiretroviral therapy with high‐risk human papillomavirus, cervical intraepithelial neoplasia, and invasive cervical cancer in women living with HIV: a systematic review and meta‐analysis. Lancet HIV. 2018; 5(1): e45– 58. 29107561 PMC5757426
  7. [12]Houlihan CF, Larke NL, Watson‐Jones D, Smith‐McCune KK, Shiboski S, Gravitt PE, et al. Human papillomavirus infection and increased risk of HIV acquisition. A systematic review and meta‐analysis. AIDS. 2012; 26(17): 2211– 22. 22874522 PMC3831022
  8. [13]Lissouba P, Van de Perre P, Auvert B. Association of genital human papillomavirus infection with HIV acquisition: a systematic review and meta‐analysis. Sex Transm Infect. 2013; 89(5): 350– 6. 23761216 PMC3717604
  9. [14]Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta‐analysis of observational studies in epidemiology: a proposal for reporting. Meta‐analysis of observational studies in epidemiology (MOOSE) group. JAMA 2000; 283(15): 2008– 12. 10789670
  10. [15]Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta‐analyses: the PRISMA statement. PLoS Med. 2009; 6(7): e1000097. 19621072 PMC2707599
  11. [16]Boily MC, Baggaley RF, Wang L, Masse B, White RG, Hayes RJ, et al. Heterosexual risk of HIV‐1 infection per sexual act: systematic review and meta‐analysis of observational studies. Lancet Infect Dis. 2009; 9(2): 118– 29. 19179227 PMC4467783
  12. [17]Critchlow CW, Hawes SE, Kuypers JM, Goldbaum GM, Holmes KK, Surawicz CM, et al. Effect of HIV infection on the natural history of anal human papillomavirus infection. AIDS. 1998; 12(10): 1177– 84. 9677167
  13. [18]Breese PL, Judson FN, Penley KA, Douglas JM Jr. Anal human papillomavirus infection among homosexual and bisexual men: prevalence of type‐specific infection and association with human immunodeficiency virus. Sex Transm Dis. 1995; 22(1): 7– 14. 7709329
  14. [19]Dev D, Lo Y, Ho GY, Burk RD, Klein RS. Incidence of and risk factors for genital human papillomavirus infection in women drug users. J Acquir Immune Defic Syndr. 2006; 41(4): 527– 9. 16652064
  15. [20]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(1): 37– 45. 15195241
  16. [21]Aho J, Hankins C, Tremblay C, Forest P, Pourreaux K, Rouah F, et al. Genomic polymorphism of human papillomavirus type 52 predisposes toward persistent infection in sexually active women. J Infect Dis. 2004; 190(1): 46– 52. 15195242
  17. [22]Gagnon S, Hankins C, Tremblay C, Forest P, Pourreaux K, Coutlee F. Viral polymorphism in human papillomavirus types 33 and 35 and persistent and transient infection in the genital tract of women. J Infect Dis. 2004; 190(9): 1575– 85. 15478061
  18. [23]Fontaine J, Hankins C, Money D, Rachlis A, Pourreaux K, Ferenczy A, et al. Human papillomavirus type 16 (HPV‐16) viral load and persistence of HPV‐16 infection in women infected or at risk for HIV. J Clin Virol. 2008; 43(3): 307– 12. 18786854
  19. [24]Phelan DF, Gange SJ, Ahdieh‐Grant L, Mehta SH, Kirk GD, Shah K, et al. Determinants of newly detected human papillomavirus infection in HIV‐infected and HIV‐uninfected injection drug using women. Sex Transm Dis. 2009; 36(3): 149– 56. 19174735 PMC2888629
  20. [25]Ahdieh L, Munoz A, Vlahov D, Trimble CL, Timpson LA, Shah K. Cervical neoplasia and repeated positivity of human papillomavirus infection in human immunodeficiency virus‐seropositive and ‐seronegative women. Am J Epidemiol. 2000; 151(12): 1148– 57. 10905527
  21. [26]Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS, 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. 15840880
  22. [27]Watts DH, Fazzari M, Minkoff H, Hillier SL, Sha B, Glesby M, 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. 15747249
  23. [28]Viscidi RP, Ahdieh‐Grant L, Schneider MF, Clayman B, Massad LS, Anastos KM, et al. Serum immunoglobulin a response to human papillomavirus type 16 virus‐like particles in human immunodeficiency virus (HIV)‐positive and high‐risk HIV‐negative women. J Infect Dis. 2003; 188(12): 1834– 44. 14673762
  24. [29]Silverberg MJ, Ahdieh L, Munoz A, Anastos K, Burk RD, Cu‐Uvin S, 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. 12172526
  25. [30]D'Souza G, Fakhry C, Sugar EA, Seaberg EC, Weber K, Minkoff HL, et al. Six‐month natural history of oral versus cervical human papillomavirus infection. Int J Cancer. 2007; 121(1): 143– 50. 17354235
  26. [31]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(6): 682– 90. 11517428
  27. [32]Koshiol JE, Schroeder JC, Jamieson DJ, Marshall SW, Duerr A, Heilig CM, et al. Time to clearance of human papillomavirus infection by type and human immunodeficiency virus serostatus. Int J Cancer. 2006; 119(7): 1623– 9. 16646070
  28. [33]Viscidi RP, Snyder B, Cu‐Uvin S, Hogan JW, Clayman B, Klein RS, et al. Human papillomavirus capsid antibody response to natural infection and risk of subsequent HPV infection in HIV‐positive and HIV‐negative women. Cancer Epidemiol Biomark Prev. 2005; 14(1): 283– 8. 15668510
  29. [34]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(19): 1343– 9. 9358128
  30. [35]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(5): 982– 6. 9609571
  31. [36]Silva RJ, Casseb J, Andreoli MA, Villa LL. Persistence and clearance of HPV from the penis of men infected and non‐infected with HIV. J Med Virol. 2011; 83(1): 127– 31. 21108349
  32. [37]van der Snoek EM, Niesters HG, van Doornum GJ, Mulder PG, Osterhaus AD, van der Meijden WI. Acquisition and clearance of perianal human papillomavirus infection in relation to HIV‐positivity in men who have sex with men in the Netherlands. Acta dermato‐venereologica. 2005; 85(5): 437– 43. 16159738
  33. [38]Tornesello ML, Duraturo ML, Giorgi‐Rossi P, Sansone M, Piccoli R, Buonaguro L, et al. Human papillomavirus (HPV) genotypes and HPV16 variants in human immunodeficiency virus‐positive Italian women. J General Virol. 2008; 89(Pt 6): 1380– 9. 18474553
  34. [39]Branca M, Garbuglia AR, Benedetto A, Cappiello T, Leoncini L, Migliore G, et al. Factors predicting the persistence of genital human papillomavirus infections and PAP smear abnormality in HIV‐positive and HIV‐negative women during prospective follow‐up. Int J STD AIDS. 2003; 14(6): 417– 25. 12816671
  35. [40]Mbulawa ZZ, Marais DJ, Johnson LF, Coetzee D, Williamson AL. Impact of human immunodeficiency virus on the natural history of human papillomavirus genital infection in South African men and women. J Infect Dis. 2012; 206(1): 15– 27. 22517913
  36. [41]Banura C, Sandin S, Van Doorn LJ, Quint W, Kleter B, Wabwire‐Mangen F, et al. Type‐specific incidence, clearance and predictors of cervical human papillomavirus infections (HPV) among young women: a prospective study in Uganda. Infect Agents Cancer. 2010; 5(1): 7. 20380709 PMC2873244
  37. [42]Banura C, Franceschi S, van Doorn LJ, Arslan A, Kleter B, Wabwire‐Mangen F, et al. Prevalence, incidence and clearance of human papillomavirus infection among young primiparous pregnant women in Kampala, Uganda. Int J Cancer. 2008; 123(9): 2180– 7. 18711697
  38. [43]Nowak RG, Gravitt PE, Morrison CS, Gange SJ, Kwok C, Oliver AE, et al. Increases in human papillomavirus detection during early HIV infection among women in Zimbabwe. J Infect Dis. 2011; 203(8): 1182– 91. 21451006 PMC3068021
  39. [44]Safaeian M, Kiddugavu M, Gravitt PE, Gange SJ, Ssekasanvu J, Murokora D, et al. Determinants of incidence and clearance of high‐risk human papillomavirus infections in rural Rakai, Uganda. Cancer Epidemiol Biomark Prev. 2008; 17(6): 1300– 7. PMC3158656 18559545
  40. [45]Rowhani‐Rahbar A, Hawes SE, Sow PS, Toure P, Feng Q, Dem A, et al. The impact of HIV status and type on the clearance of human papillomavirus infection among Senegalese women. J Infect Dis. 2007; 196(6): 887– 94. 17703420
  41. [46]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(3): 714– 7. 8627037
  42. [47]Blitz S, Baxter J, Raboud J, Walmsley S, Rachlis A, Smaill F, 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. 23624362
  43. [48]Mullins TL, Wilson CM, Rudy BJ, Sucharew H, Kahn JA. Incident anal human papillomavirus and human papillomavirus‐related sequelae in HIV‐infected versus HIV‐uninfected adolescents in the United States. Sex Transm Dis. 2013; 40(9): 715– 20. 23949587 PMC4313540
  44. [49]Strickler HD, Martinson J, Desai S, Xie X, Burk RD, Anastos K, et al. The relation of plasmacytoid dendritic cells (pDCs) and regulatory T‐cells (Tregs) with HPV persistence in HIV‐infected and HIV‐uninfected women. Viral Immunol. 2014; 27(1): 20– 5. 24494969 PMC3920755
  45. [50]Grabowski MK, Gray RH, Serwadda D, Kigozi G, Gravitt PE, Nalugoda F, et al. High‐risk human papillomavirus viral load and persistence among heterosexual HIV‐negative and HIV‐positive men. Sex Transm Infect. 2014; 90(4): 337– 43. 24482488 PMC4030299
  46. [51]Jalil EM, Bastos FI, Melli PP, Duarte G, Simoes RT, Yamamoto AY, et al. HPV clearance in postpartum period of HIV‐positive and negative women: a prospective follow‐up study. BMC Infect Dis. 2013; 13: 564. 24289532 PMC4219400
  47. [52]Phanuphak N, Teeratakulpisarn N, Pankam T, Kerr SJ, Barisri J, Deesua A, et al. Anal human papillomavirus infection among Thai men who have sex with men with and without HIV infection: prevalence, incidence, and persistence. J Acquir Immune Defic Syndr. 2013; 63(4): 472– 9. 23514956 PMC3700660
  48. [53]Phanuphak N, Teeratakulpisarn N, Triratanachat S, Keelawat S, Pankam T, Kerr SJ, et al. High prevalence and incidence of high‐grade anal intraepithelial neoplasia among young Thai men who have sex with men with and without HIV. AIDS. 2013; 27(11): 1753– 62. 23807271 PMC3706028
  49. [54]Tobian AA, Kigozi G, Gravitt PE, Xiao C, Serwadda D, Eaton KP, et al. Human papillomavirus incidence and clearance among HIV‐positive and HIV‐negative men in sub‐Saharan Africa. AIDS. 2012; 26(12): 1555– 65. 22441255 PMC3442933
  50. [55]Chin‐Hong PV, Husnik M, Cranston RD, Colfax G, Buchbinder S, Da Costa M, et al. Anal human papillomavirus infection is associated with HIV acquisition in men who have sex with men. AIDS. 2009; 23(9): 1135– 42. 19390418 PMC4577294
  51. [56]Auvert B, Lissouba P, Cutler E, Zarca K, Puren A, Taljaard D. Association of oncogenic and nononcogenic human papillomavirus with HIV incidence. J Acquir Immune Defic Syndr. 2010; 53(1): 111– 6. 19779357 PMC3203884
  52. [57]Smith JS, Moses S, Hudgens MG, Parker CB, Agot K, Maclean I, et al. Increased risk of HIV acquisition among Kenyan men with human papillomavirus infection. J Infect Dis. 2010; 201(11): 1677– 85. 20415595 PMC2873838
  53. [58]Veldhuijzen NJ, Vyankandondera J, van de Wijgert JH. HIV acquisition is associated with prior high‐risk human papillomavirus infection among high‐risk women in Rwanda. AIDS. 2010; 24(14): 2289– 92. 20613457
  54. [59]Smith‐McCune KK, Shiboski S, Chirenje MZ, Magure T, Tuveson J, Ma Y, et al. Type‐specific cervico‐vaginal human papillomavirus infection increases risk of HIV acquisition independent of other sexually transmitted infections. PLoS ONE. 2010; 5(4): e10094. 20386706 PMC2851652
  55. [60]Wang C, Wright TC, Denny L, Kuhn L. 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. 21216869 PMC3071227
  56. [61]Myer L, Denny L, Wright TC, Kuhn L. Prospective study of hormonal contraception and women's risk of HIV infection in South Africa. Int J Epidemiol. 2007; 36(1): 166– 74. 17175547
  57. [62]Low AJ, Clayton T, Konate I, Nagot N, Ouedraogo A, Huet C, et al. Genital warts and infection with human immunodeficiency virus in high‐risk women in Burkina Faso: a longitudinal study. BMC Infect Dis. 2011; 11: 20. 21251265 PMC3031229
  58. [63]Auvert B, Marais D, Lissouba P, Zarca K, Ramjee G, Williamson AL. High‐risk human papillomavirus is associated with HIV acquisition among South African female sex workers. Inf Dis Obstet Gynecol. 2011; 2011: 692012. PMC3143430 21804752
  59. [64]Rositch AF, Mao L, Hudgens MG, Moses S, Agot K, Backes DM, et al. Risk of HIV acquisition among circumcised and uncircumcised young men with penile HPV infection. AIDS. 2013; 28(5): 745. PMC4074250 24149088
  60. [65]Tobian AA, Grabowski MK, Kigozi G, Redd AD, Eaton KP, Serwadda D, et al. Human papillomavirus clearance among males is associated with HIV acquisition and increased dendritic cell density in the foreskin. J Infect Dis. 2013; 207(11): 1713– 22. 23345339 PMC3636782
  61. [66]Averbach SH, Gravitt PE, Nowak RG, Celentano DD, Dunbar MS, Morrison CS, et al. The association between cervical human papillomavirus infection and HIV acquisition among women in Zimbabwe. AIDS. 2010; 24(7): 1035– 42. 20397287 PMC3831602
  62. [67]Adler D, Wallace M, Bennie T, Abar B, Sadeghi R, Meiring T, et al. High risk human papillomavirus persistence among HIV‐infected young women in South Africa. Int J Infect Dis. 2015; 33: 219– 21. 25697074 PMC4397173
  63. [68]Ceccato Junior BP, Guimaraes MD, Lopes AP, Nascimento LF, Novaes LM, Del Castillo DM, et al. Incidence of cervical human papillomavirus and cervical intraepithelial neoplasia in women with positive and negative HIV status. Rev Bras Ginecol Obstet. 2016; 38(5): 231– 8. 27123772 PMC10309363
  64. [69]Gallagher KE, Baisley K, Grosskurth H, Vallely A, Kapiga S, Vandepitte J, et al. The association between cervical Human Papillomavirus infection and subsequent HIV acquisition in Tanzanian and Ugandan Women: a nested case‐control study. J Infect Dis. 2016; 214(1): 87– 95. 26951818 PMC4907415
  65. [70]Mooij SH, van Santen DK, Geskus RB, van der Sande MA, Coutinho RA, Stolte IG, et al. The effect of HIV infection on anal and penile human papillomavirus incidence and clearance: a cohort study among MSM. AIDS. 2016; 30(1): 121– 32. 26474302
  66. [71]Malagon T, Lemieux‐Mellouki P, Laprise JF, Brisson M. Bias due to correlation between times‐at‐risk for infection in epidemiologic studies measuring biological interactions between sexually transmitted infections: a case study using Human Papillomavirus type interactions. Am J Epidemiol. 2016; 184(12): 873– 83. 27927619 PMC5161088
  67. [72]Liu G, Sharma M, Tan N, Barnabas R. HIV‐positive women have higher risk of HPV infection, precancerous lesions, and cervical cancer: a systematic review and meta‐analysis[Epub ahead of print]. AIDS 2018; 32: 795– 808. 29369827 PMC5854529
  68. [73]Denslow SA, Rositch AF, Firnhaber C, Ting J, Smith JS. Incidence and progression of cervical lesions in women with HIV: a systematic global review. Int J STD AIDS. 2014; 25(3): 163– 77. 24216030 PMC5524184
  69. [74]Tong WW, Jin F, McHugh LC, Maher T, Sinclair B, Grulich AE, et al. Progression to and spontaneous regression of high‐grade anal squamous intraepithelial lesions in HIV‐infected and uninfected men. AIDS. 2013; 27(14): 2233– 43. 24157904
  70. [75]Looker KJ, Elmes JAR, Gottlieb SL, Schiffer JT, Vickerman P, Turner KME, et al. Effect of HSV‐2 infection on subsequent HIV acqusition: an updated systematic review and meta‐analysis. Lancet Infect Dis. 2017; 17(12): 1303– 16. 28843576 PMC5700807
  71. [76]van Schalkwyk C, Moodley J, Welte A, Johnson L. Are associations between HIV and HPV transmission due to behavioural confounding factors or biological effects?. Paris, France: IAS; 2017. 30171173
  72. [77]Omori R, Nagelkerke N, Abu‐Raddad LJ. HIV and herpes simplex virus type 2 epidemiological synergy: misguided observational evidence? A modelling study [Epub ahead of print]. Sex Transm Infect 2017. 10.1136/sextrans‐2017‐053336 PMC6204970 29203577 · DOI
  73. [78]Lemieux‐Mellouki P, Drolet M, Brisson J, Franco EL, Boily M‐C, Baussano I, et al. Assortative mixing as a source of bias in epidemiological studies of sexually transmitted infections: the case of smoking and human papillomavirus. Epidemiol Infect. 2016; 144(7): 1490– 9. 26584685 PMC9150526
  74. [79]Boily M‐C, Anderson RM. Human immunodeficiency virus transmission and the role of other sexually transmitted diseases. Measures of association and study design. Sex Transm Dis. 1996; 23(4): 312– 32. 8836026
  75. [81]Kang M, Cu‐Uvin S. Association of HIV viral load and CD4 cell count with human papillomavirus detection and clearance in HIV‐infected women initiating highly active antiretroviral therapy. HIV Med. 2012; 13(6): 372– 8. 22257000 PMC3500098
  76. [82]Konopnicki D, Manigart Y, Gilles C, Barlow P, de Marchin J, Feoli F, 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. 23463709
  77. [83]Guidry JT, Scott RS. The interaction between human papillomavirus and other viruses. Virus Res. 2017; 231: 139– 47. 27826043 PMC5325789
  78. [84]Massad LS, Xie X, D'Souza G, Darragh TM, Minkoff H, Wright R, et al. Incidence of cervical precancers among HIV‐seropositive women. Am J Obstet Gynecol. 2015; 212(5): 606e1– 8. 25499260 PMC4416973
  79. [85]De Vuyst H, Lillo F, Broutet N, Smith JS. HIV, human papillomavirus, and cervical neoplasia and cancer in the era of highly active antiretroviral therapy. Eur J Cancer Prev. 2008; 17(6): 545– 54. 18941376
  80. [86]Herfs M, Hubert P, Moutschen M, Delvenne P. Mucosal junctions: open doors to HPV and HIV infections? Trends Microbiol. 2011; 19(3): 114– 20. 21216598
  81. [87]Kojic EM, Kang M, Cespedes MS, Umbleja T, Godfrey C, Allen RT, et al. Immunogenicity and safety of the quadrivalent human papillomavirus vaccine in HIV‐1‐infected women. Clin Infect Dis. 2014; 59(1): 127– 35. 24723284 PMC4305143
  82. [90]Kojic EM, Rana AI, Cu‐Uvin S. Human papillomavirus vaccination in HIV‐infected women: need for increased coverage. Expert Rev Vaccines. 2016; 15(1): 105– 17. 26599305 PMC4825670

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Authors
Looker, K. J., Rönn, M. M., Brock, P. M., Brisson, M., Drolet, M., Mayaud, P., & Boily, M.
Affiliations
  • University of Bristol (GB)
  • Harvard University (US)
  • University of Glasgow (GB)
  • Centre de recherche du CHU de Québec-Université Laval (CA)
  • Centre de recherche du CHU de Québec‐Université Laval Axe santé des populations et pratiques optimales en santé Québec Canada
  • London School of Hygiene & Tropical Medicine (GB)
  • Imperial College London (GB)
Corresponding author
Looker, Katharine J
ORCID
Venue
Journal of the International AIDS Society
Publisher
Wiley
Published
2018-06
Volume
21
Issue
6
Pages
e25110-e25110
ISSN
1758-2652 (ISSN-L)
DOI
10.1002/jia2.25110
PMC
PMC5989783
OpenAlex
W2806229809
Cited by
185
References
1
Citations by year
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FWCI
1.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of the International AIDS Society (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by-sa)
  • Explore Bristol Research (acceptedVersion, cc-by)
  • LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
  • Bristol Research (University of Bristol) (submittedVersion, cc-by)
  • Spiral (Imperial College London) (submittedVersion, cc-by)
Funders
  • Seventh Framework Programme (242061)
  • Medical Research Council (PH01/14‐39)
  • National Institutes of Health (NIH UM1 AI068617)
  • Canadian Institutes of Health Research (FDN‐143283)
Topics
  • Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
  • Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
  • Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
Keywords
HIV, human papillomavirus, HPV acquisition, HPV clearance, HIV acquisition, synergistic interaction, people living with HIV, HPV incidence, high-risk HPV, HPV vaccination, men who have sex with men, heterosexual men, women, publication bias, confounding, misclassification bias, sexually transmitted infections, cervical cancer prevention, HIV prevention, STD prevention
MeSH terms
Female, Humans, Longitudinal Studies, Male, Pregnancy, Vaccination, HIV Infections, Incidence, Papillomavirus Infections, Papillomavirus Vaccines

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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