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Published in: BMC Cancer 1/2009

Open Access 01-12-2009 | Research article

Human papillomavirus prevalence, viral load and pre-cancerous lesions of the cervix in women initiating highly active antiretroviral therapy in South Africa: a cross-sectional study

Authors: Jennifer R Moodley, Deborah Constant, Margaret Hoffman, Anna Salimo, Bruce Allan, Ed Rybicki, Inga Hitzeroth, Anna-Lise Williamson

Published in: BMC Cancer | Issue 1/2009

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Abstract

Background

Cervical cancer and infection with human immunodeficiency virus (HIV) are both important public health problems in South Africa (SA). The aim of this study was to determine the prevalence of cervical squamous intraepithelial lesions (SILs), high-risk human papillomavirus (HR-HPV), HPV viral load and HPV genotypes in HIV positive women initiating anti-retroviral (ARV) therapy.

Methods

A cross-sectional survey was conducted at an anti-retroviral (ARV) treatment clinic in Cape Town, SA in 2007. Cervical specimens were taken for cytological analysis and HPV testing. The Digene Hybrid Capture 2 (HC2) test was used to detect HR-HPV. Relative light units (RLU) were used as a measure of HPV viral load. HPV types were determined using the Roche Linear Array HPV Genotyping test. Crude associations with abnormal cytology were tested and multiple logistic regression was used to determine independent risk factors for abnormal cytology.

Results

The median age of the 109 participants was 31 years, the median CD4 count was 125/mm3, 66.3% had an abnormal Pap smear, the HR-HPV prevalence was 78.9% (Digene), the median HPV viral load was 181.1 RLU (HC2 positive samples only) and 78.4% had multiple genotypes. Among women with abnormal smears the most prevalent HR-HPV types were HPV types 16, 58 and 51, all with a prevalence of 28.5%. On univariate analysis HR-HPV, multiple HPV types and HPV viral load were significantly associated with the presence of low and high-grade SILs (LSIL/HSIL). The multivariate logistic regression showed that HPV viral load was associated with an increased odds of LSIL/HSIL, odds ratio of 10.7 (95% CI 2.0 – 57.7) for those that were HC2 positive and had a viral load of ≤ 181.1 RLU (the median HPV viral load), and 33.8 (95% CI 6.4 – 178.9) for those that were HC2 positive with a HPV viral load > 181.1 RLU.

Conclusion

Women initiating ARVs have a high prevalence of abnormal Pap smears and HR-HPV. Our results underscore the need for locally relevant, rigorous screening protocols for the increasing numbers of women accessing ARV therapy so that the benefits of ARVs are not partially offset by an excess risk in cervical cancer.
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Literature
1.
go back to reference Mqoqi N, Kellet P, Madhoo J, Sitas F: Cancer in South Africa, 1996–1997. National Cancer Registry of South Africa. 2003, National Health Laboratory Service, Johannesburg Mqoqi N, Kellet P, Madhoo J, Sitas F: Cancer in South Africa, 1996–1997. National Cancer Registry of South Africa. 2003, National Health Laboratory Service, Johannesburg
2.
go back to reference Department of Health of South Africa: The national HIV and syphilis prevalence survey South Africa, 2007. Annual report National Department of Health, Pretoria. 2008 Department of Health of South Africa: The national HIV and syphilis prevalence survey South Africa, 2007. Annual report National Department of Health, Pretoria. 2008
3.
go back to reference Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, Wright TC: Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA. 2000, 283: 1031-1037. 10.1001/jama.283.8.1031.CrossRefPubMed Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, Wright TC: Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA. 2000, 283: 1031-1037. 10.1001/jama.283.8.1031.CrossRefPubMed
4.
go back to reference Wright TC, Ellerbrock TV, Chiasson MA, Sun XW, Van Devanter N, the New York Cervical Disease Study: Cervical intraepithelial neoplasia in women infected with human immunodeficiency virus: prevalence, risk factors and the validity of Papaniculou smears. Obst Gynecol. 1994, 84: 591-597. Wright TC, Ellerbrock TV, Chiasson MA, Sun XW, Van Devanter N, the New York Cervical Disease Study: Cervical intraepithelial neoplasia in women infected with human immunodeficiency virus: prevalence, risk factors and the validity of Papaniculou smears. Obst Gynecol. 1994, 84: 591-597.
5.
go back to reference Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, Young M, Melnick S, Miotti P, Burk R: 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. 10.1093/jnci/91.3.226.CrossRefPubMed Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, Young M, Melnick S, Miotti P, Burk R: 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. 10.1093/jnci/91.3.226.CrossRefPubMed
6.
go back to reference Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC: Human papillomavirus infection in women infected with human immunodeficiency virus. N Engl J Med. 1997, 337: 1343-1349. 10.1067/mob.2002.123607.CrossRefPubMed Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC: Human papillomavirus infection in women infected with human immunodeficiency virus. N Engl J Med. 1997, 337: 1343-1349. 10.1067/mob.2002.123607.CrossRefPubMed
7.
go back to reference Tate DR, Anderson RJ: Recrudescence of cervical dysplasia among women who are infected with the human immunodeficiency virus: a case control analysis. Am J Obstet Gynecol. 2002, 186: 880-882. 10.1097/01.lgt.0000245038.06977.a7.CrossRefPubMed Tate DR, Anderson RJ: Recrudescence of cervical dysplasia among women who are infected with the human immunodeficiency virus: a case control analysis. Am J Obstet Gynecol. 2002, 186: 880-882. 10.1097/01.lgt.0000245038.06977.a7.CrossRefPubMed
8.
go back to reference Massad LS, Fazzari MJ, Anastos K, Klein RS, Minkoff H, Jamieson DJ, Duerr A, Celentano D, Gange S, Cu-Uvin S, Young M, Watts DH, Levine AM, Schuman P, Harris TG, Strickler HD: Outcomes after treatment of cervical intraepithelial neoplasia among women with HIV. J Low Genit Tract Dis. 2007, 1 (2): 90-97. 10.1097/01.lgt.0000245038.06977.a7.CrossRef Massad LS, Fazzari MJ, Anastos K, Klein RS, Minkoff H, Jamieson DJ, Duerr A, Celentano D, Gange S, Cu-Uvin S, Young M, Watts DH, Levine AM, Schuman P, Harris TG, Strickler HD: Outcomes after treatment of cervical intraepithelial neoplasia among women with HIV. J Low Genit Tract Dis. 2007, 1 (2): 90-97. 10.1097/01.lgt.0000245038.06977.a7.CrossRef
9.
go back to reference Hawes SE, Critchlow CW, Niang MAF, Diouf MB, Diop A, Toure P, Kasse AA, Dembele B, Sow PS, Coll-Seck AM, Kuypers JM, Kiviat NB: Increased Risk of High-Grade Cervical Squamous Intraepithelial Lesions and Invasive Cervical Cancer among African Women with Immunodeficiency Virus Type 1 and 2 Infections. JID. 2003, 188: 555-563. 10.1086/376996.CrossRefPubMed Hawes SE, Critchlow CW, Niang MAF, Diouf MB, Diop A, Toure P, Kasse AA, Dembele B, Sow PS, Coll-Seck AM, Kuypers JM, Kiviat NB: Increased Risk of High-Grade Cervical Squamous Intraepithelial Lesions and Invasive Cervical Cancer among African Women with Immunodeficiency Virus Type 1 and 2 Infections. JID. 2003, 188: 555-563. 10.1086/376996.CrossRefPubMed
10.
go back to reference Schuman P, Ohmit SE, Klein RS, Duerr A, Cu-Uvin S, Jamieson DJ, Anderson J, Shah KV, for the Epidemiology Research Study (HERS) Group: Longitudinal Study of Cervical Squamous Intraepithelial Lesions in Human Immunodeficiency Virus (HIV)-Seropositive and At-Risk HIV-Seronegative Women. JID. 2003, 188: 128-136. 10.1086/520883.CrossRefPubMed Schuman P, Ohmit SE, Klein RS, Duerr A, Cu-Uvin S, Jamieson DJ, Anderson J, Shah KV, for the Epidemiology Research Study (HERS) Group: Longitudinal Study of Cervical Squamous Intraepithelial Lesions in Human Immunodeficiency Virus (HIV)-Seropositive and At-Risk HIV-Seronegative Women. JID. 2003, 188: 128-136. 10.1086/520883.CrossRefPubMed
11.
go back to reference Rowhani-Rahbar A, Hawes SE, Sow PS, Toure P, Feng Q, Dem A, Dembele B, Critchlow CW, N'Doye I, Kiviat NB: 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. 10.1086/520883.CrossRefPubMed Rowhani-Rahbar A, Hawes SE, Sow PS, Toure P, Feng Q, Dem A, Dembele B, Critchlow CW, N'Doye I, Kiviat NB: 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. 10.1086/520883.CrossRefPubMed
12.
go back to reference Moodley JR, Hoffman M, Carrara H, Allan BR, Cooper DD, Rosenberg L, Denny LE, Shapiro S, Williamson AL: HIV and pre-neoplastic and neoplastic lesions of the cervix in South Africa: a case-control study. BMC Cancer. 2006, 6: 135-10.1186/1471-2407-6-135.CrossRefPubMedPubMedCentral Moodley JR, Hoffman M, Carrara H, Allan BR, Cooper DD, Rosenberg L, Denny LE, Shapiro S, Williamson AL: HIV and pre-neoplastic and neoplastic lesions of the cervix in South Africa: a case-control study. BMC Cancer. 2006, 6: 135-10.1186/1471-2407-6-135.CrossRefPubMedPubMedCentral
13.
go back to reference Ledergerber B, Telenti A, Egger M: Risk of HIV related Kaposi's sarcoma and non-Hodgkin's lymphoma with potent antiretroviral therapy: a prospective cohort study. Swiss HIV Cohort Study. BMJ. 1999, 319: 23-24.CrossRefPubMedPubMedCentral Ledergerber B, Telenti A, Egger M: Risk of HIV related Kaposi's sarcoma and non-Hodgkin's lymphoma with potent antiretroviral therapy: a prospective cohort study. Swiss HIV Cohort Study. BMJ. 1999, 319: 23-24.CrossRefPubMedPubMedCentral
14.
go back to reference Jacobsen LP: Impact of potent antiretroviral therapy on the incidence of Kaposi's sarcoma and non-Hodgkin's lymphoma among HIV-infected individuals. J Acquir Immune Defic Syndr. 1999, 21: S34-S41. Jacobsen LP: Impact of potent antiretroviral therapy on the incidence of Kaposi's sarcoma and non-Hodgkin's lymphoma among HIV-infected individuals. J Acquir Immune Defic Syndr. 1999, 21: S34-S41.
15.
go back to reference Palefsky JM: Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy. Current opinion in Oncology. 2003, 15: 382-388. 10.1097/00001622-200309000-00007.CrossRefPubMed Palefsky JM: Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy. Current opinion in Oncology. 2003, 15: 382-388. 10.1097/00001622-200309000-00007.CrossRefPubMed
16.
go back to reference Heard I, Palefsky JM, Kazatchkine MD: The impact of HIV antiviral therapy on human papillomavirus (HPV) infections and HPV-related diseases. Antivir Ther. 2004, 9 (1): 13-22.PubMed Heard I, Palefsky JM, Kazatchkine MD: The impact of HIV antiviral therapy on human papillomavirus (HPV) infections and HPV-related diseases. Antivir Ther. 2004, 9 (1): 13-22.PubMed
17.
go back to reference Denny L, Boa R, Williamson AL, Allan B, Hardie D, Stan R, Myer L: Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women. Obstet Gynecol. 2008, 111 (6): 1380-1387.CrossRefPubMed Denny L, Boa R, Williamson AL, Allan B, Hardie D, Stan R, Myer L: Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women. Obstet Gynecol. 2008, 111 (6): 1380-1387.CrossRefPubMed
18.
go back to reference Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T, Young N, Forum Group Members; Bethesda 2001 Workshop: The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002, 287 (16): 2114-2119. 10.1001/jama.287.16.2114.CrossRefPubMed Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T, Young N, Forum Group Members; Bethesda 2001 Workshop: The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002, 287 (16): 2114-2119. 10.1001/jama.287.16.2114.CrossRefPubMed
19.
go back to reference Massad LS, Riester KA, Anastos KM, Fruchter RG, Palefsky JM, Burk RD, Burns D, Greenblatt RM, Muderspach LI, Miotti P: 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. 10.1097/00002030-200008180-00013.CrossRefPubMed Massad LS, Riester KA, Anastos KM, Fruchter RG, Palefsky JM, Burk RD, Burns D, Greenblatt RM, Muderspach LI, Miotti P: 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. 10.1097/00002030-200008180-00013.CrossRefPubMed
20.
go back to reference Delmas MC, Larsen C, Van Benthem B, Hamers FF, Bergeron C, Poveda JD, Anzen B, Hoek van den A, Meier F, Pena JM, Savonius H, Sperandeo D, Suligoi B, Vernazza P, Brunet JB, De Vincenzi I, for the European Study Group on Natural History of HIV Infection in Women: Cervical squamous intraepithelial lesions in HIV infected women: prevalence, incidence and regression. AIDS. 2000, 14: 1775-1784. 10.1097/00002030-200008180-00013.CrossRefPubMed Delmas MC, Larsen C, Van Benthem B, Hamers FF, Bergeron C, Poveda JD, Anzen B, Hoek van den A, Meier F, Pena JM, Savonius H, Sperandeo D, Suligoi B, Vernazza P, Brunet JB, De Vincenzi I, for the European Study Group on Natural History of HIV Infection in Women: Cervical squamous intraepithelial lesions in HIV infected women: prevalence, incidence and regression. AIDS. 2000, 14: 1775-1784. 10.1097/00002030-200008180-00013.CrossRefPubMed
21.
go back to reference Ahdieh L, Muñoz 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): 1148-1157. 10.1016/j.ygyno.2006.06.015.CrossRefPubMed Ahdieh L, Muñoz 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): 1148-1157. 10.1016/j.ygyno.2006.06.015.CrossRefPubMed
22.
go back to reference Parham GP, Sahasrabuddhe VV, Mwanahamuntu MH, Shepherd BE, Hicks ML, Stringer EM, Vermund SH: Prevalence and predictors of squamous intraepithelial lesions of the cervix in HIV-infected women in Lusaka, Zambia. Gynecol Oncol. 2006, 103 (3): 1017-1022. 10.1016/j.ygyno.2006.06.015.CrossRefPubMedPubMedCentral Parham GP, Sahasrabuddhe VV, Mwanahamuntu MH, Shepherd BE, Hicks ML, Stringer EM, Vermund SH: Prevalence and predictors of squamous intraepithelial lesions of the cervix in HIV-infected women in Lusaka, Zambia. Gynecol Oncol. 2006, 103 (3): 1017-1022. 10.1016/j.ygyno.2006.06.015.CrossRefPubMedPubMedCentral
23.
go back to reference Anorlu RI, Igwilo CI, Akanmu AS, Banjo AA, Odunukwe NN, Okany CC, Abudu OO, Dim ST: Prevalence of abnormal cervical smears among patients with HIV in Lagos, Nigeria. West Afr J Med. 2007, 26 (2): 143-147.PubMed Anorlu RI, Igwilo CI, Akanmu AS, Banjo AA, Odunukwe NN, Okany CC, Abudu OO, Dim ST: Prevalence of abnormal cervical smears among patients with HIV in Lagos, Nigeria. West Afr J Med. 2007, 26 (2): 143-147.PubMed
24.
go back to reference Jamieson DJ, Duerr A, Burk R, Klein RS, Paramsothy P, Schuman P, Cu-Uvin S, Shah K, HIV Epidemiology Research Study (HERS) Group: Characterization of genital human papillomavirus infection in women. Am J Obstet Gynecol. 2002, 186 (1): 21-27. 10.1067/mob.2002.119776.CrossRefPubMed Jamieson DJ, Duerr A, Burk R, Klein RS, Paramsothy P, Schuman P, Cu-Uvin S, Shah K, HIV Epidemiology Research Study (HERS) Group: Characterization of genital human papillomavirus infection in women. Am J Obstet Gynecol. 2002, 186 (1): 21-27. 10.1067/mob.2002.119776.CrossRefPubMed
25.
go back to reference Wu Y, Chen Y, Li L, Yu G, Zhang Y, He Y: Associations of high-risk HPV types and viral load with cervical cancer in China. J Clin Viro. 2006, 35 (3): 264-269. 10.1016/j.jcv.2005.07.011.CrossRef Wu Y, Chen Y, Li L, Yu G, Zhang Y, He Y: Associations of high-risk HPV types and viral load with cervical cancer in China. J Clin Viro. 2006, 35 (3): 264-269. 10.1016/j.jcv.2005.07.011.CrossRef
26.
go back to reference Sun CA, Lai HC, Chang CC, Neih S, Yu CP, Chu TY: The significance of human papillomavirus viral load in prediction of histologic severity and size of squamous intraepithelial lesions of uterine cervix. Gynecol Oncol. 2001, 83: 95-99. 10.1006/gyno.2001.6336.CrossRefPubMed Sun CA, Lai HC, Chang CC, Neih S, Yu CP, Chu TY: The significance of human papillomavirus viral load in prediction of histologic severity and size of squamous intraepithelial lesions of uterine cervix. Gynecol Oncol. 2001, 83: 95-99. 10.1006/gyno.2001.6336.CrossRefPubMed
27.
go back to reference Levi JE, Fernandes S, Tateno AF, Motta E, Lima LP, Eluf-Neto J, Pannuti CS: Presence of multiple human papillomavirus types in cervical samples from HIV-infected women. Gynecol Onco. 2004, 92 (1): 225-231. 10.1016/j.ygyno.2003.10.004.CrossRef Levi JE, Fernandes S, Tateno AF, Motta E, Lima LP, Eluf-Neto J, Pannuti CS: Presence of multiple human papillomavirus types in cervical samples from HIV-infected women. Gynecol Onco. 2004, 92 (1): 225-231. 10.1016/j.ygyno.2003.10.004.CrossRef
28.
go back to reference Pretet JL, Dalstein V, Monnier-Benoit S, Delpeut S, Mougin C: High risk HPV load estimated by Hybrid Capture II correlates with HPV16 load measured by real-time PCR in cervical smears of HPV16-infected women. J Clin Virol. 2004, 31: 140-147. 10.1016/j.jcv.2004.02.008.CrossRefPubMed Pretet JL, Dalstein V, Monnier-Benoit S, Delpeut S, Mougin C: High risk HPV load estimated by Hybrid Capture II correlates with HPV16 load measured by real-time PCR in cervical smears of HPV16-infected women. J Clin Virol. 2004, 31: 140-147. 10.1016/j.jcv.2004.02.008.CrossRefPubMed
29.
go back to reference Gravitt PE, Burk RD, Lorincz A, Herrero R, Hildesheim A, Sherman ME, Bratti MC, Rodriguez AC, Helzlsouer KJ, Schiffman M: A Comparison between Real-Time Polymerase Chain Reaction and Hybrid Capture 2 for Human Papillomavirus DNA Quantitation. Cancer Epidemiol Biomark Prev. 2003, 12: 477-484. Gravitt PE, Burk RD, Lorincz A, Herrero R, Hildesheim A, Sherman ME, Bratti MC, Rodriguez AC, Helzlsouer KJ, Schiffman M: A Comparison between Real-Time Polymerase Chain Reaction and Hybrid Capture 2 for Human Papillomavirus DNA Quantitation. Cancer Epidemiol Biomark Prev. 2003, 12: 477-484.
30.
go back to reference Clifford GM, Gonçalves MA, Franceschi S, HPV and HIV Study Group: Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS. 2006, 20 (18): 2337-2344. 10.1097/01.aids.0000253361.63578.14.CrossRefPubMed Clifford GM, Gonçalves MA, Franceschi S, HPV and HIV Study Group: Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS. 2006, 20 (18): 2337-2344. 10.1097/01.aids.0000253361.63578.14.CrossRefPubMed
31.
go back to reference Ho GY, Burk RD, Klein S, Kadish AS, Chan CJ, Palan P, Basu J, Farthing A, Masterson P, Mason WP, Vousden KH: Persistent genital human papillomavirusinfection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst. 1995, 87: 1365-1371. 10.1093/jnci/91.11.954.CrossRefPubMed Ho GY, Burk RD, Klein S, Kadish AS, Chan CJ, Palan P, Basu J, Farthing A, Masterson P, Mason WP, Vousden KH: Persistent genital human papillomavirusinfection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst. 1995, 87: 1365-1371. 10.1093/jnci/91.11.954.CrossRefPubMed
32.
go back to reference Liaw KL, Glass AG, Manos MM, Greer CE, Scott DR, Sherman M, Burk RD, Kurman RJ, Wacholder S, Rush BB, Cadell DM, Lawler P, Tabor D, Schiffman M: Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst. 1999, 91: 954-960. 10.1093/jnci/91.11.954.CrossRefPubMed Liaw KL, Glass AG, Manos MM, Greer CE, Scott DR, Sherman M, Burk RD, Kurman RJ, Wacholder S, Rush BB, Cadell DM, Lawler P, Tabor D, Schiffman M: Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst. 1999, 91: 954-960. 10.1093/jnci/91.11.954.CrossRefPubMed
33.
go back to reference Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, Alfaro ME, Sherman S, Wacholder S, Chen A, Rodriguez C, Burk RD: Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis. 2005, 191: 1796-1807. 10.1086/428850.CrossRefPubMed Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, Alfaro ME, Sherman S, Wacholder S, Chen A, Rodriguez C, Burk RD: Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis. 2005, 191: 1796-1807. 10.1086/428850.CrossRefPubMed
34.
go back to reference Clifford GM, Gallus S, Herrero R, Munoz N, Snijders PJ, Vaccarella S, Anh PT, Ferreccio C, Hieu NT, Matos E, Molano M, Rajkumar R, Ronco G, de Sanjosé S, Shin HR, Sukvirach S, Thomas JO, Tunsakul S, Meijer CJ, Franceschi S, IARC HPV Prevalence Surveys Study Group: 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. 10.1086/505876.CrossRefPubMed Clifford GM, Gallus S, Herrero R, Munoz N, Snijders PJ, Vaccarella S, Anh PT, Ferreccio C, Hieu NT, Matos E, Molano M, Rajkumar R, Ronco G, de Sanjosé S, Shin HR, Sukvirach S, Thomas JO, Tunsakul S, Meijer CJ, Franceschi S, IARC HPV Prevalence Surveys Study Group: 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. 10.1086/505876.CrossRefPubMed
35.
go back to reference Luque AE, Jabeen M, Messing S, Lane CA, Demeter LM, Rose RC, Reichman RC: Prevalence of human papillomavirus genotypes and related abnormalities of cervical cytological results among HIV-1-infected women in Rochester, New York. J Infect Di. 2006, 194 (4): 428-434. 10.1086/505876.CrossRef Luque AE, Jabeen M, Messing S, Lane CA, Demeter LM, Rose RC, Reichman RC: Prevalence of human papillomavirus genotypes and related abnormalities of cervical cytological results among HIV-1-infected women in Rochester, New York. J Infect Di. 2006, 194 (4): 428-434. 10.1086/505876.CrossRef
36.
go back to reference Sahasrabuddhe VV, Mwanahamuntu MH, Vermund SH, Huh WK, Lyon MD, Stringer JS, Parham GP: Prevalence and distribution of HPV genotypes among HIV-infected women in Zambia. Br J Cancer. 2007, 96 (9): 1480-1483.PubMedPubMedCentral Sahasrabuddhe VV, Mwanahamuntu MH, Vermund SH, Huh WK, Lyon MD, Stringer JS, Parham GP: Prevalence and distribution of HPV genotypes among HIV-infected women in Zambia. Br J Cancer. 2007, 96 (9): 1480-1483.PubMedPubMedCentral
37.
go back to reference Massad LS, Ahdieh L, Benning L, Minkoff H, Greenblatt RM, Watts H, Miotti P, Anastos K, Moxley M, Muderspach LI, Melnick S: Evolution of cervical abnormalities among women with HIV-1: Evidence from surveillance cytology in the Women's Interagency HIV Study. J Acquir Immun Defic Syndr. 2001, 27: 432-442.CrossRef Massad LS, Ahdieh L, Benning L, Minkoff H, Greenblatt RM, Watts H, Miotti P, Anastos K, Moxley M, Muderspach LI, Melnick S: Evolution of cervical abnormalities among women with HIV-1: Evidence from surveillance cytology in the Women's Interagency HIV Study. J Acquir Immun Defic Syndr. 2001, 27: 432-442.CrossRef
38.
go back to reference Fahey MT, Irwig L, Macaskill P: Meta-analysis of Pap test accuracy. Am J Epidemiol. 1995, 141 (7): 680-689.PubMed Fahey MT, Irwig L, Macaskill P: Meta-analysis of Pap test accuracy. Am J Epidemiol. 1995, 141 (7): 680-689.PubMed
39.
go back to reference Nanda K, McCrory DC, Myers ER, Bastian LA, Hasselblad V, Hickey JD, Matchar DB: Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med. 2000, 132 (10): 810-819.CrossRefPubMed Nanda K, McCrory DC, Myers ER, Bastian LA, Hasselblad V, Hickey JD, Matchar DB: Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med. 2000, 132 (10): 810-819.CrossRefPubMed
Metadata
Title
Human papillomavirus prevalence, viral load and pre-cancerous lesions of the cervix in women initiating highly active antiretroviral therapy in South Africa: a cross-sectional study
Authors
Jennifer R Moodley
Deborah Constant
Margaret Hoffman
Anna Salimo
Bruce Allan
Ed Rybicki
Inga Hitzeroth
Anna-Lise Williamson
Publication date
01-12-2009
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2009
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-9-275

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