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Published in: Infectious Agents and Cancer 1/2016

Open Access 01-12-2016 | Research Article

Variability of high risk HPV genotypes among HIV infected women in Mwanza, Tanzania- the need for evaluation of current vaccine effectiveness in developing countries

Authors: Fridolin Mujuni, Mariam M. Mirambo, Peter Rambau, Korn Klaus, Muller Andreas, Dismas Matovelo, Mtebe Majigo, Christa Kasang, Stephen E. Mshana

Published in: Infectious Agents and Cancer | Issue 1/2016

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Abstract

Background

High risk (HR) human papilloma Virus (HPV) genotypes have been associated with cervical cancer. In Tanzania there is a limited data on the epidemiology of HPV and genotypes distribution among HIV infected women. Here we document varieties of HPV genotypes associated with cervical squamous intraepithelial lesions (SIL) among HIV- infected women at Bugando Medical Centre, Mwanza-Tanzania.

Methods

A cross sectional hospital based study involving HIV infected women was conducted between August and October, 2014. Exfoliated cells from ectocervix and endocervix were collected using cytobrush. HPV genotypes were detected using polymerase chain reaction (PCR) followed by sequencing using specific primers targeting broad range of HPV types. Cytology was done to establish squamous intraepithelial lesions. Log binomial regression analysis was done to establish risk ratios (RR) associated with HPV infection using STATA version 11.

Results

A total of 255 HIV infected women with mean age 39.2 ± 9.1 years were enrolled in the study. HPV DNA was detected in 138/255 (54.1 %, 95 % CI: 47-60) of HIV infected women. Twenty six genotypes were detected in various combinations; of these 17(65.3 %) were of HR genotypes. HR genotypes were detected in 124(48.6 %) of HIV infected women. Common HR genotypes detected were HPV-52(26), HPV-58(21), HPV-35(20) and HPV-16(14). The risk of being HPV positive was significantly higher among women with CD4 counts <100 (RR: 1.20, 95 % CI: 1.05-1.35, P = 0.006) and women with SIL (RR: 1.37, 95 % CI: 1.11-1.68, P = 0.005)

Conclusion

Significant proportion of HIV infected women with low CD4 counts have various grades of cervical SIL associated with varieties of uncommon HR genotypes. There is a need to evaluate the effectiveness of the current vaccine in preventing cervical cancer in developing countries where HIV is endemic.
Literature
1.
go back to reference Cox JT. Epidemiology and natural history of HPV. J Fam Pract. 2006;21:3–9. Cox JT. Epidemiology and natural history of HPV. J Fam Pract. 2006;21:3–9.
2.
go back to reference WHO: ICO HPV Information Centre. WHO/ICO information Centre on Human Papilloma Virus (HPV) and cervical Cancer centre. 2010. WHO: ICO HPV Information Centre. WHO/ICO information Centre on Human Papilloma Virus (HPV) and cervical Cancer centre. 2010.
3.
go back to reference Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74–108.CrossRefPubMed Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74–108.CrossRefPubMed
4.
go back to reference Castellsague X, de Sanjose S, Aguado T: HPV and Cervical Cancer in The World, 2007 Report. WHO/ICO Information Centre on HPV and Cervical Cancer (HPV Information Centre). Geneva: WHO; Barcelona: ICO. In.; 2010 Castellsague X, de Sanjose S, Aguado T: HPV and Cervical Cancer in The World, 2007 Report. WHO/ICO Information Centre on HPV and Cervical Cancer (HPV Information Centre). Geneva: WHO; Barcelona: ICO. In.; 2010
5.
go back to reference Clifford GM, Goncalves MAG, Franceschi S, HPV, group Hs. Human papillomavirus types among women infected with HIV: a meta-analysis. Aids. 2006;20(18):2337–44.CrossRefPubMed Clifford GM, Goncalves MAG, Franceschi S, HPV, group Hs. Human papillomavirus types among women infected with HIV: a meta-analysis. Aids. 2006;20(18):2337–44.CrossRefPubMed
6.
go back to reference Konopnicki D, Manigart Y, Gilles C, Barlow P, De Marchin J, Feoli F, Larsimont D, Delforge M, De Wit S, Clumeck N: High-risk human papillomavirus infection in HIV-positive African women living in Europe. Journal of the International AIDS Society 2013, 16(1). Konopnicki D, Manigart Y, Gilles C, Barlow P, De Marchin J, Feoli F, Larsimont D, Delforge M, De Wit S, Clumeck N: High-risk human papillomavirus infection in HIV-positive African women living in Europe. Journal of the International AIDS Society 2013, 16(1).
7.
go back to reference Sahasrabuddhe V, Mwanahamuntu MH, Vermund S, Huh W, Lyon M, Stringer J, Parham G. Prevalence and distribution of HPV genotypes among HIV-infected women in Zambia. Br J Cancer. 2007;96(9):1480–3.PubMedPubMedCentral Sahasrabuddhe V, Mwanahamuntu MH, Vermund S, Huh W, Lyon M, Stringer J, Parham G. Prevalence and distribution of HPV genotypes among HIV-infected women in Zambia. Br J Cancer. 2007;96(9):1480–3.PubMedPubMedCentral
8.
go back to reference Heard I, Tassie J-M, Schmitz V, Mandelbrot L, Kazatchkine MD, Orth G. Increased risk of cervical disease among human immunodeficiency virus–infected women with severe immunosuppression and high human papillomavirus load. Obstet Gynecol. 2000;96(3):403–9.PubMed Heard I, Tassie J-M, Schmitz V, Mandelbrot L, Kazatchkine MD, Orth G. Increased risk of cervical disease among human immunodeficiency virus–infected women with severe immunosuppression and high human papillomavirus load. Obstet Gynecol. 2000;96(3):403–9.PubMed
9.
go back to reference De Vuyst H, Mugo N, Chung M, McKenzie K, Nyongesa-Malava E, Tenet V, Njoroge J, Sakr S, Meijer CM, Snijders P. Prevalence and determinants of human papillomavirus infection and cervical lesions in HIV-positive women in Kenya. Br J Cancer. 2012;107(9):1624–30.CrossRefPubMedPubMedCentral De Vuyst H, Mugo N, Chung M, McKenzie K, Nyongesa-Malava E, Tenet V, Njoroge J, Sakr S, Meijer CM, Snijders P. Prevalence and determinants of human papillomavirus infection and cervical lesions in HIV-positive women in Kenya. Br J Cancer. 2012;107(9):1624–30.CrossRefPubMedPubMedCentral
10.
go back to reference Firnhaber C, Zungu K, Levin S, Michelow P, Montaner LJ, McPhail P, Williamson A, Allan BR, Van der Horst C, Rinas A. Diverse and high prevalence of human papillomavirus associated with a significant high rate of cervical dysplasia in human immunodeficiency virus–infected women in Johannesburg, South Africa. Acta Cytol. 2009;53(1):10–7.CrossRefPubMedPubMedCentral Firnhaber C, Zungu K, Levin S, Michelow P, Montaner LJ, McPhail P, Williamson A, Allan BR, Van der Horst C, Rinas A. Diverse and high prevalence of human papillomavirus associated with a significant high rate of cervical dysplasia in human immunodeficiency virus–infected women in Johannesburg, South Africa. Acta Cytol. 2009;53(1):10–7.CrossRefPubMedPubMedCentral
11.
go back to reference MacLeod IJ, O'Donnell B, Moyo S, Lockman S, Shapiro RL, Kayembe M, van Widenfelt E, Makhema J, Essex M, Wester C. Prevalence of human papillomavirus genotypes and associated cervical squamous intraepithelial lesions in HIV‐infected women in Botswana. J Med Virol. 2011;83(10):1689–95.CrossRefPubMedPubMedCentral MacLeod IJ, O'Donnell B, Moyo S, Lockman S, Shapiro RL, Kayembe M, van Widenfelt E, Makhema J, Essex M, Wester C. Prevalence of human papillomavirus genotypes and associated cervical squamous intraepithelial lesions in HIV‐infected women in Botswana. J Med Virol. 2011;83(10):1689–95.CrossRefPubMedPubMedCentral
12.
go back to reference Dartell M, Rasch V, Kahesa C, Mwaiselage J, Ngoma T, Junge J, Gernow A, Ejlersen SF, Munk C, Iftner T. Human papillomavirus prevalence and type distribution in 3603 HIV-positive and HIV-negative women in the general population of Tanzania: the PROTECT study. Sex Transm Dis. 2012;39(3):201–8.CrossRefPubMed Dartell M, Rasch V, Kahesa C, Mwaiselage J, Ngoma T, Junge J, Gernow A, Ejlersen SF, Munk C, Iftner T. Human papillomavirus prevalence and type distribution in 3603 HIV-positive and HIV-negative women in the general population of Tanzania: the PROTECT study. Sex Transm Dis. 2012;39(3):201–8.CrossRefPubMed
13.
go back to reference Assoumou SZ, Mbiguino AN, Mabika BM, Ogoula SN, El Mzibri M, Khattabi A, Ennaji MM. Human papillomavirus genotypes distribution among Gabonese women with normal cytology and cervical abnormalities. Infectious Agents Cancer. 2016;11(1):1–8.CrossRef Assoumou SZ, Mbiguino AN, Mabika BM, Ogoula SN, El Mzibri M, Khattabi A, Ennaji MM. Human papillomavirus genotypes distribution among Gabonese women with normal cytology and cervical abnormalities. Infectious Agents Cancer. 2016;11(1):1–8.CrossRef
14.
go back to reference Moore RA, Ogilvie G, Fornika D, Moravan V, Brisson M, Amirabbasi-Beik M, Kollar A, Burgess T, Hsu R, Towers L, et al. Prevalence and type distribution of human papillomavirus in 5,000 British Columbia women--implications for vaccination. Cancer Causes Control. 2009;20(8):1387–96.CrossRefPubMedPubMedCentral Moore RA, Ogilvie G, Fornika D, Moravan V, Brisson M, Amirabbasi-Beik M, Kollar A, Burgess T, Hsu R, Towers L, et al. Prevalence and type distribution of human papillomavirus in 5,000 British Columbia women--implications for vaccination. Cancer Causes Control. 2009;20(8):1387–96.CrossRefPubMedPubMedCentral
15.
go back to reference Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348(6):518–27.CrossRefPubMed Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348(6):518–27.CrossRefPubMed
16.
go back to reference Organization WH. WHO position on HPV vaccines. Vaccine. 2009;27(52):7236–7.CrossRef Organization WH. WHO position on HPV vaccines. Vaccine. 2009;27(52):7236–7.CrossRef
17.
go back to reference Luque AE, Hitti J, Mwachari C, Lane C, Messing S, Cohn SE, Adler D, Rose R, Coombs R. Prevalence of human papillomavirus genotypes in HIV-1-infected women in Seattle, USA and Nairobi, Kenya: results from the Women's HIV Interdisciplinary Network (WHIN). Int J Infect Dis. 2010;14(9):e810–4.CrossRefPubMedPubMedCentral Luque AE, Hitti J, Mwachari C, Lane C, Messing S, Cohn SE, Adler D, Rose R, Coombs R. Prevalence of human papillomavirus genotypes in HIV-1-infected women in Seattle, USA and Nairobi, Kenya: results from the Women's HIV Interdisciplinary Network (WHIN). Int J Infect Dis. 2010;14(9):e810–4.CrossRefPubMedPubMedCentral
18.
go back to reference Tanzania Commission for AIDS ZAC, National Bureau of Statistics , Office of the Chief Government Statistician, Inter-national I: Tanzania HIV/AIDS and Malaria Indicator Survey 2007–08. In.: TACAIDS, ZAC, NBS, OCGS, and Macro International Inc Dar es Salaam, Tanzania; 2008. Tanzania Commission for AIDS ZAC, National Bureau of Statistics , Office of the Chief Government Statistician, Inter-national I: Tanzania HIV/AIDS and Malaria Indicator Survey 2007–08. In.: TACAIDS, ZAC, NBS, OCGS, and Macro International Inc Dar es Salaam, Tanzania; 2008.
19.
go back to reference Apgar BS, Zoschnick L, Wright Jr TC. The 2001 Bethesda System terminology. Am Fam Physician. 2003;68(10):1992–8.PubMed Apgar BS, Zoschnick L, Wright Jr TC. The 2001 Bethesda System terminology. Am Fam Physician. 2003;68(10):1992–8.PubMed
20.
go back to reference Petry K, Menton S, Menton M, van Loenen-Frosch F, de Carvalho GH, Holz B, Schopp B, Garbrecht-Buettner S, Davies P, Boehmer G. Inclusion of HPV testing in routine cervical cancer screening for women above 29 years in Germany: results for 8466 patients. Br J Cancer. 2003;88(10):1570–7.CrossRefPubMedPubMedCentral Petry K, Menton S, Menton M, van Loenen-Frosch F, de Carvalho GH, Holz B, Schopp B, Garbrecht-Buettner S, Davies P, Boehmer G. Inclusion of HPV testing in routine cervical cancer screening for women above 29 years in Germany: results for 8466 patients. Br J Cancer. 2003;88(10):1570–7.CrossRefPubMedPubMedCentral
21.
go back to reference Markowitz LE, Dunne E, Saraiya M, Lawson H, Chesson H, Unger E. Quadrivalent human papillomavirus vaccine. Morb Mortal Wkly Rep. 2007;56(RR-2):1–24. Markowitz LE, Dunne E, Saraiya M, Lawson H, Chesson H, Unger E. Quadrivalent human papillomavirus vaccine. Morb Mortal Wkly Rep. 2007;56(RR-2):1–24.
22.
go back to reference Didelot-Rousseau M-N, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Van de Perre P, Mayaud P, Segondy M. Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-1 infection in Burkina Faso. Br J Cancer. 2006;95(3):355–62.CrossRefPubMedPubMedCentral Didelot-Rousseau M-N, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Van de Perre P, Mayaud P, Segondy M. Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-1 infection in Burkina Faso. Br J Cancer. 2006;95(3):355–62.CrossRefPubMedPubMedCentral
23.
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 Dis. 2006;194(4):428–34.CrossRefPubMed 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 Dis. 2006;194(4):428–34.CrossRefPubMed
24.
go back to reference Levi JE, Kleter B, Quint WG, Fink MC, Canto CL, Matsubara R, Linhares I, Segurado A, Vanderborght B, Neto JE. 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(9):3341–5.CrossRefPubMedPubMedCentral Levi JE, Kleter B, Quint WG, Fink MC, Canto CL, Matsubara R, Linhares I, Segurado A, Vanderborght B, Neto JE. 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(9):3341–5.CrossRefPubMedPubMedCentral
25.
go back to reference Strickler HD, Palefsky JM, Shah KV, Anastos K, Klein RS, Minkoff H, Duerr A, Massad LS, Celentano DD, Hall C. Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst. 2003;95(14):1062–71.CrossRefPubMed Strickler HD, Palefsky JM, Shah KV, Anastos K, Klein RS, Minkoff H, Duerr A, Massad LS, Celentano DD, Hall C. Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst. 2003;95(14):1062–71.CrossRefPubMed
26.
go back to reference Castellsagué X, Klaustermeier J, Carrilho C, Albero G, Sacarlal J, Quint W, Kleter B, Lloveras B, Ismail MR, de Sanjosé S. Vaccine‐related HPV genotypes in women with and without cervical cancer in Mozambique: Burden and potential for prevention. Int J Cancer. 2008;122(8):1901–4.CrossRefPubMed Castellsagué X, Klaustermeier J, Carrilho C, Albero G, Sacarlal J, Quint W, Kleter B, Lloveras B, Ismail MR, de Sanjosé S. Vaccine‐related HPV genotypes in women with and without cervical cancer in Mozambique: Burden and potential for prevention. Int J Cancer. 2008;122(8):1901–4.CrossRefPubMed
27.
go back to reference Joura EA, Giuliano AR, Iversen O-E, Bouchard C, Mao C, Mehlsen J, Moreira Jr ED, Ngan Y, Petersen LK, Lazcano-Ponce E. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med. 2015;372(8):711–23.CrossRefPubMed Joura EA, Giuliano AR, Iversen O-E, Bouchard C, Mao C, Mehlsen J, Moreira Jr ED, Ngan Y, Petersen LK, Lazcano-Ponce E. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med. 2015;372(8):711–23.CrossRefPubMed
28.
go back to reference Denny L, Adewole I, Anorlu R, Dreyer G, Moodley M, Smith T, Snyman L, Wiredu E, Molijn A, Quint W. Human papillomavirus prevalence and type distribution in invasive cervical cancer in sub‐Saharan Africa. Int J Cancer. 2014;134(6):1389–98.CrossRefPubMed Denny L, Adewole I, Anorlu R, Dreyer G, Moodley M, Smith T, Snyman L, Wiredu E, Molijn A, Quint W. Human papillomavirus prevalence and type distribution in invasive cervical cancer in sub‐Saharan Africa. Int J Cancer. 2014;134(6):1389–98.CrossRefPubMed
29.
go back to reference Schäfer A, Friedmann W, Mielke M, Schwartländer B, Koch MA. The increased frequency of cervical dysplasia-neoplasia in women infected with the human immunodeficiency virus is related to the degree of immunosuppression. Am J Obstet Gynecol. 1991;164(2):593–9.CrossRefPubMed Schäfer A, Friedmann W, Mielke M, Schwartländer B, Koch MA. The increased frequency of cervical dysplasia-neoplasia in women infected with the human immunodeficiency virus is related to the degree of immunosuppression. Am J Obstet Gynecol. 1991;164(2):593–9.CrossRefPubMed
30.
go back to reference Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA. 2001;286(24):3106–14.CrossRefPubMed Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA. 2001;286(24):3106–14.CrossRefPubMed
31.
go back to reference Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS. Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol. 2008;168(2):123–37.CrossRefPubMedPubMedCentral Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS. Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol. 2008;168(2):123–37.CrossRefPubMedPubMedCentral
32.
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(3):226–36.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(3):226–36.CrossRefPubMed
33.
go back to reference Dames DN, Blackman E, Butler R, Taioli E, Eckstein S, Devarajan K, Griffith-Bowe A, Gomez P, Ragin C, Consortium ACC. High-risk cervical human papillomavirus infections among human immunodeficiency virus-positive women in the Bahamas. PLoS One. 2014;9(1), e85429.CrossRefPubMedPubMedCentral Dames DN, Blackman E, Butler R, Taioli E, Eckstein S, Devarajan K, Griffith-Bowe A, Gomez P, Ragin C, Consortium ACC. High-risk cervical human papillomavirus infections among human immunodeficiency virus-positive women in the Bahamas. PLoS One. 2014;9(1), e85429.CrossRefPubMedPubMedCentral
34.
go back to reference Dames DN, Ragin C, Griffith-Bowe A, Gomez P, Butler R. The prevalence of cervical cytology abnormalities and human papillomavirus in women infected with the human immunodeficiency virus. Infect Agent Cancer. 2009;4 Suppl 1:S8.CrossRefPubMedPubMedCentral Dames DN, Ragin C, Griffith-Bowe A, Gomez P, Butler R. The prevalence of cervical cytology abnormalities and human papillomavirus in women infected with the human immunodeficiency virus. Infect Agent Cancer. 2009;4 Suppl 1:S8.CrossRefPubMedPubMedCentral
Metadata
Title
Variability of high risk HPV genotypes among HIV infected women in Mwanza, Tanzania- the need for evaluation of current vaccine effectiveness in developing countries
Authors
Fridolin Mujuni
Mariam M. Mirambo
Peter Rambau
Korn Klaus
Muller Andreas
Dismas Matovelo
Mtebe Majigo
Christa Kasang
Stephen E. Mshana
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Infectious Agents and Cancer / Issue 1/2016
Electronic ISSN: 1750-9378
DOI
https://doi.org/10.1186/s13027-016-0097-2

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