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Published in: BMC Infectious Diseases 1/2020

01-12-2020 | HIV Drug | Research article

The role of drug resistance in poor viral suppression in rural South Africa: findings from a population-based study

Authors: Sheri A. Lippman, Alyssa C. Mooney, Adrian Puren, Gillian Hunt, Jessica S. Grignon, Lisa M. Prach, Hailey J. Gilmore, Hong-Ha M. Truong, Scott Barnhart, Teri Liegler

Published in: BMC Infectious Diseases | Issue 1/2020

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Abstract

Background

Understanding factors driving virological failure, including the contribution of HIV drug resistance mutations (DRM), is critical to ensuring HIV treatment remains effective. We examine the contribution of drug resistance mutations for low viral suppression in HIV-positive participants in a population-based sero-prevalence survey in rural South Africa.

Methods

We conducted HIV drug resistance genotyping and ART analyte testing on dried blood spots (DBS) from HIV-positive adults participating in a 2014 survey in North West Province. Among those with virologic failure (> 5000 copies/mL), we describe frequency of DRM to protease inhibitors (PI), nucleoside reverse transcriptase inhibitors (NRTI), and non-nucleoside reverse transcriptase inhibitors (NNRTI), report association of resistance with antiretroviral therapy (ART) status, and assess resistance to first and second line therapy. Analyses are weighted to account for sampling design.

Results

Overall 170 DBS samples were assayed for viral load and ART analytes; 78.4% of men and 50.0% of women had evidence of virologic failure and were assessed for drug resistance, with successful sequencing of 76/107 samples. We found ≥1 DRM in 22% of participants; 47% were from samples with detectable analyte (efavirenz, nevirapine or lopinavir). Of those with DRM and detectable analyte, 60% showed high–level resistance and reduced predicted virologic response to ≥1 NRTI/NNRTI typically used in first and second-line regimens.

Conclusions

DRM and predicted reduced susceptibility to first and second-line regimens were common among adults with ART exposure in a rural South African population-based sample. Results underscore the importance of ongoing virologic monitoring, regimen optimization and adherence counseling to optimize durable virologic suppression.
Literature
2.
go back to reference UNAIDS. Global AIDS Update 2016. Geneva: Joint United Nations Programme on HIV/AIDS; 2016. UNAIDS. Global AIDS Update 2016. Geneva: Joint United Nations Programme on HIV/AIDS; 2016.
3.
go back to reference Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, Hakim JG, Kumwenda J, Grinsztejn B, Pilotto JH, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365(6):493–505.CrossRef Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, Hakim JG, Kumwenda J, Grinsztejn B, Pilotto JH, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365(6):493–505.CrossRef
4.
go back to reference Granich RM, Gilks CF, Dye C, De Cock KM, Williams BG. Universal voluntary HIV testing with immediate antiretroviral therapy as a strategy for elimination of HIV transmission: a mathematical model. Lancet. 2009;373(9657):48–57.CrossRef Granich RM, Gilks CF, Dye C, De Cock KM, Williams BG. Universal voluntary HIV testing with immediate antiretroviral therapy as a strategy for elimination of HIV transmission: a mathematical model. Lancet. 2009;373(9657):48–57.CrossRef
5.
go back to reference Bartlett JA, Fath MJ, Demasi R, Hermes A, Quinn J, Mondou E, Rousseau F. An updated systematic overview of triple combination therapy in antiretroviral-naive HIV-infected adults. AIDS. 2006;20(16):2051–64.CrossRef Bartlett JA, Fath MJ, Demasi R, Hermes A, Quinn J, Mondou E, Rousseau F. An updated systematic overview of triple combination therapy in antiretroviral-naive HIV-infected adults. AIDS. 2006;20(16):2051–64.CrossRef
6.
go back to reference Bor J, Herbst AJ, Newell ML, Barnighausen T. Increases in adult life expectancy in rural South Africa: valuing the scale-up of HIV treatment. Science. 2013;339(6122):961–5.CrossRef Bor J, Herbst AJ, Newell ML, Barnighausen T. Increases in adult life expectancy in rural South Africa: valuing the scale-up of HIV treatment. Science. 2013;339(6122):961–5.CrossRef
7.
go back to reference Bangsberg DR, Hecht FM, Charlebois ED, Zolopa AR, Holodniy M, Sheiner L, Bamberger JD, Chesney MA, Moss A. Adherence to protease inhibitors, HIV-1 viral load, and development of drug resistance in an indigent population. AIDS. 2000;14(4):357–66.CrossRef Bangsberg DR, Hecht FM, Charlebois ED, Zolopa AR, Holodniy M, Sheiner L, Bamberger JD, Chesney MA, Moss A. Adherence to protease inhibitors, HIV-1 viral load, and development of drug resistance in an indigent population. AIDS. 2000;14(4):357–66.CrossRef
8.
go back to reference Hogg RS, Heath K, Bangsberg D, Yip B, Press N, O'Shaughnessy MV, Montaner JS. Intermittent use of triple-combination therapy is predictive of mortality at baseline and after 1 year of follow-up. AIDS. 2002;16(7):1051–8.CrossRef Hogg RS, Heath K, Bangsberg D, Yip B, Press N, O'Shaughnessy MV, Montaner JS. Intermittent use of triple-combination therapy is predictive of mortality at baseline and after 1 year of follow-up. AIDS. 2002;16(7):1051–8.CrossRef
9.
go back to reference Paterson DL, Swindells S, Mohr J, Brester M, Vergis EN, Squier C, Wagener MM, Singh N. Adherence to protease inhibitor therapy and outcomes in patients with HIV infection. Ann Intern Med. 2000;133(1):21–30.CrossRef Paterson DL, Swindells S, Mohr J, Brester M, Vergis EN, Squier C, Wagener MM, Singh N. Adherence to protease inhibitor therapy and outcomes in patients with HIV infection. Ann Intern Med. 2000;133(1):21–30.CrossRef
10.
go back to reference Wood E, Montaner JS, Yip B, Tyndall MW, Schechter MT, O'Shaughnessy MV, Hogg RS. Adherence and plasma HIV RNA responses to highly active antiretroviral therapy among HIV-1 infected injection drug users. CMAJ. 2003;169(7):656–61.PubMedPubMedCentral Wood E, Montaner JS, Yip B, Tyndall MW, Schechter MT, O'Shaughnessy MV, Hogg RS. Adherence and plasma HIV RNA responses to highly active antiretroviral therapy among HIV-1 infected injection drug users. CMAJ. 2003;169(7):656–61.PubMedPubMedCentral
11.
go back to reference Boender TS, Hoenderboom BM, Sigaloff KC, Hamers RL, Wellington M, Shamu T, Siwale M, Labib Maksimos EE, Nankya I, Kityo CM, et al. Pretreatment HIV drug resistance increases regimen switches in sub-Saharan Africa. Clin Infect Dis. 2015;61(11):1749–58.PubMed Boender TS, Hoenderboom BM, Sigaloff KC, Hamers RL, Wellington M, Shamu T, Siwale M, Labib Maksimos EE, Nankya I, Kityo CM, et al. Pretreatment HIV drug resistance increases regimen switches in sub-Saharan Africa. Clin Infect Dis. 2015;61(11):1749–58.PubMed
12.
go back to reference Boender TS, Sigaloff KC, McMahon JH, Kiertiburanakul S, Jordan MR, Barcarolo J, Ford N, Rinke de Wit TF, Bertagnolio S. Long-term Virological outcomes of first-line antiretroviral therapy for HIV-1 in low- and middle-income countries: a systematic review and meta-analysis. Clin Infect Dis. 2015;61(9):1453–61.CrossRef Boender TS, Sigaloff KC, McMahon JH, Kiertiburanakul S, Jordan MR, Barcarolo J, Ford N, Rinke de Wit TF, Bertagnolio S. Long-term Virological outcomes of first-line antiretroviral therapy for HIV-1 in low- and middle-income countries: a systematic review and meta-analysis. Clin Infect Dis. 2015;61(9):1453–61.CrossRef
13.
go back to reference Kharsany ABM, Cawood C, Khanyile D, Lewis L, Grobler A, Puren A, Govender K, George G, Beckett S, Samsunder N, et al. Community-based HIV prevalence in KwaZulu-Natal, South Africa: results of a cross-sectional household survey. Lancet HIV. 2018;5(8):e427–37.CrossRef Kharsany ABM, Cawood C, Khanyile D, Lewis L, Grobler A, Puren A, Govender K, George G, Beckett S, Samsunder N, et al. Community-based HIV prevalence in KwaZulu-Natal, South Africa: results of a cross-sectional household survey. Lancet HIV. 2018;5(8):e427–37.CrossRef
15.
go back to reference Rossouw TM, Nieuwoudt M, Manasa J, Malherbe G, Lessells RJ, Pillay S, Danaviah S, Mahasha P, van Dyk G, de Oliveira T. HIV drug resistance levels in adults failing first-line antiretroviral therapy in an urban and a rural setting in South Africa. HIV Med. 2017;18(2):104–14.CrossRef Rossouw TM, Nieuwoudt M, Manasa J, Malherbe G, Lessells RJ, Pillay S, Danaviah S, Mahasha P, van Dyk G, de Oliveira T. HIV drug resistance levels in adults failing first-line antiretroviral therapy in an urban and a rural setting in South Africa. HIV Med. 2017;18(2):104–14.CrossRef
16.
go back to reference Petersen M, Balzer L, Kwarsiima D, Sang N, Chamie G, Ayieko J, Kabami J, Owaraganise A, Liegler T, Mwangwa F, et al. Association of Implementation of a universal testing and treatment intervention with HIV diagnosis, receipt of antiretroviral therapy, and viral suppression in East Africa. Jama. 2017;317(21):2196–206.CrossRef Petersen M, Balzer L, Kwarsiima D, Sang N, Chamie G, Ayieko J, Kabami J, Owaraganise A, Liegler T, Mwangwa F, et al. Association of Implementation of a universal testing and treatment intervention with HIV diagnosis, receipt of antiretroviral therapy, and viral suppression in East Africa. Jama. 2017;317(21):2196–206.CrossRef
17.
go back to reference Iwuji CC, Orne-Gliemann J, Larmarange J, Balestre E, Thiebaut R, Tanser F, Okesola N, Makowa T, Dreyer J, Herbst K, et al. Universal test and treat and the HIV epidemic in rural South Africa: a phase 4, open-label, community cluster randomised trial. Lancet HIV. 2018;5(3):e116–25.CrossRef Iwuji CC, Orne-Gliemann J, Larmarange J, Balestre E, Thiebaut R, Tanser F, Okesola N, Makowa T, Dreyer J, Herbst K, et al. Universal test and treat and the HIV epidemic in rural South Africa: a phase 4, open-label, community cluster randomised trial. Lancet HIV. 2018;5(3):e116–25.CrossRef
19.
go back to reference Boender TS, Kityo CM, Boerma RS, Hamers RL, Ondoa P, Wellington M, Siwale M, Nankya I, Kaudha E, Akanmu AS, et al. Accumulation of HIV-1 drug resistance after continued virological failure on first-line ART in adults and children in sub-Saharan Africa. J Antimicrob Chemother. 2016;71(10):2918–27.CrossRef Boender TS, Kityo CM, Boerma RS, Hamers RL, Ondoa P, Wellington M, Siwale M, Nankya I, Kaudha E, Akanmu AS, et al. Accumulation of HIV-1 drug resistance after continued virological failure on first-line ART in adults and children in sub-Saharan Africa. J Antimicrob Chemother. 2016;71(10):2918–27.CrossRef
20.
go back to reference Steegen K, Carmona S, Bronze M, Papathanasopoulos MA, van Zyl G, Goedhals D, MacLeod W, Sanne I, Stevens WS. Moderate levels of pre-treatment HIV-1 antiretroviral drug resistance detected in the first South African National Survey. PLoS One. 2016;11(12):e0166305.CrossRef Steegen K, Carmona S, Bronze M, Papathanasopoulos MA, van Zyl G, Goedhals D, MacLeod W, Sanne I, Stevens WS. Moderate levels of pre-treatment HIV-1 antiretroviral drug resistance detected in the first South African National Survey. PLoS One. 2016;11(12):e0166305.CrossRef
21.
go back to reference Hunt GM, Dokubo EK, Takuva S, de Oliveira T, Ledwaba J, Dube N, Moodley P, Sabatier J, Deyde V, Morris L, et al. Rates of virological suppression and drug resistance in adult HIV-1-positive patients attending primary healthcare facilities in KwaZulu-Natal, South Africa. J Antimicrob Chemother. 2017;72(11):3141–8.CrossRef Hunt GM, Dokubo EK, Takuva S, de Oliveira T, Ledwaba J, Dube N, Moodley P, Sabatier J, Deyde V, Morris L, et al. Rates of virological suppression and drug resistance in adult HIV-1-positive patients attending primary healthcare facilities in KwaZulu-Natal, South Africa. J Antimicrob Chemother. 2017;72(11):3141–8.CrossRef
22.
go back to reference Gupta RK, Gregson J, Parkin N, Haile-Selassie H, Tanuri A, Andrade Forero L, Kaleebu P, Watera C, Aghokeng A, Mutenda N, et al. HIV-1 drug resistance before initiation or re-initiation of first-line antiretroviral therapy in low-income and middle-income countries: a systematic review and meta-regression analysis. Lancet Infect Dis. 2018;18(3):346–55.CrossRef Gupta RK, Gregson J, Parkin N, Haile-Selassie H, Tanuri A, Andrade Forero L, Kaleebu P, Watera C, Aghokeng A, Mutenda N, et al. HIV-1 drug resistance before initiation or re-initiation of first-line antiretroviral therapy in low-income and middle-income countries: a systematic review and meta-regression analysis. Lancet Infect Dis. 2018;18(3):346–55.CrossRef
23.
go back to reference Manasa J, Danaviah S, Lessells R, Elshareef M, Tanser F, Wilkinson E, Pillay S, Mthiyane H, Mwambi H, Pillay D, et al. Increasing HIV-1 drug resistance between 2010 and 2012 in adults participating in population-based HIV surveillance in rural KwaZulu-Natal, South Africa. AIDS Res Hum Retroviruses. 2016;32(8):763–9.CrossRef Manasa J, Danaviah S, Lessells R, Elshareef M, Tanser F, Wilkinson E, Pillay S, Mthiyane H, Mwambi H, Pillay D, et al. Increasing HIV-1 drug resistance between 2010 and 2012 in adults participating in population-based HIV surveillance in rural KwaZulu-Natal, South Africa. AIDS Res Hum Retroviruses. 2016;32(8):763–9.CrossRef
24.
go back to reference Lippman SA, Shade SB, El Ayadi AM, Gilvydis JM, Grignon JS, Liegler T, Morris J, Naidoo E, Prach LM, Puren A, et al. Attrition and opportunities along the HIV care continuum: findings from a population-based sample, north West Province, South Africa. J Acquir Immune Defic Syndr. 2016;73(1):91–9.CrossRef Lippman SA, Shade SB, El Ayadi AM, Gilvydis JM, Grignon JS, Liegler T, Morris J, Naidoo E, Prach LM, Puren A, et al. Attrition and opportunities along the HIV care continuum: findings from a population-based sample, north West Province, South Africa. J Acquir Immune Defic Syndr. 2016;73(1):91–9.CrossRef
25.
go back to reference Shisana O, Rehle T, Simbayi LC, Zuma K, Jooste S, Zungu N, Labadarios D, Onoya D, et al. South African national HIV prevalence, incidence and behaviour survey, 2012. Cape Town: HSRC Press; 2014. Shisana O, Rehle T, Simbayi LC, Zuma K, Jooste S, Zungu N, Labadarios D, Onoya D, et al. South African national HIV prevalence, incidence and behaviour survey, 2012. Cape Town: HSRC Press; 2014.
26.
go back to reference National Department of Health. The National Antenatal Sentinel HIV and Syphilis Prevalence Survey, South Africa, 2015. Pretoria; 2017. National Department of Health. The National Antenatal Sentinel HIV and Syphilis Prevalence Survey, South Africa, 2015. Pretoria; 2017.
28.
go back to reference Prach LM, Puren A, Lippman SA, Carmona S, Stephenson S, Cutler E, Barnhart S, Liegler T. Design and implementation of an external quality assessment program for HIV viral load measurements using dried blood spots. J Clin Microbiol. 2015;53(3):964–6.CrossRef Prach LM, Puren A, Lippman SA, Carmona S, Stephenson S, Cutler E, Barnhart S, Liegler T. Design and implementation of an external quality assessment program for HIV viral load measurements using dried blood spots. J Clin Microbiol. 2015;53(3):964–6.CrossRef
29.
go back to reference Parkin NT. Measurement of HIV-1 viral load for drug resistance surveillance using dried blood spots: literature review and modeling of contribution of DNA and RNA. AIDS Rev. 2014;16(3):160–71.PubMed Parkin NT. Measurement of HIV-1 viral load for drug resistance surveillance using dried blood spots: literature review and modeling of contribution of DNA and RNA. AIDS Rev. 2014;16(3):160–71.PubMed
30.
go back to reference Zhou Z, Wagar N, DeVos JR, Rottinghaus E, Diallo K, Nguyen DB, Bassey O, Ugbena R, Wadonda-Kabondo N, McConnell MS, et al. Optimization of a low cost and broadly sensitive genotyping assay for HIV-1 drug resistance surveillance and monitoring in resource-limited settings. PLoS One. 2011;6(11):e28184.CrossRef Zhou Z, Wagar N, DeVos JR, Rottinghaus E, Diallo K, Nguyen DB, Bassey O, Ugbena R, Wadonda-Kabondo N, McConnell MS, et al. Optimization of a low cost and broadly sensitive genotyping assay for HIV-1 drug resistance surveillance and monitoring in resource-limited settings. PLoS One. 2011;6(11):e28184.CrossRef
31.
go back to reference Rhee SY, Fessel WJ, Zolopa AR, Hurley L, Liu T, Taylor J, Nguyen DP, Slome S, Klein D, Horberg M, et al. HIV-1 protease and reverse-transcriptase mutations: correlations with antiretroviral therapy in subtype B isolates and implications for drug-resistance surveillance. J Infect Dis. 2005;192(3):456–65.CrossRef Rhee SY, Fessel WJ, Zolopa AR, Hurley L, Liu T, Taylor J, Nguyen DP, Slome S, Klein D, Horberg M, et al. HIV-1 protease and reverse-transcriptase mutations: correlations with antiretroviral therapy in subtype B isolates and implications for drug-resistance surveillance. J Infect Dis. 2005;192(3):456–65.CrossRef
32.
go back to reference Department of Health, Republic of South Africa. National Consolidated Guidelines for the Prevention of Mother-to-Child Transmission of HIV (PMTCT) and the Management of HIV in Children, Adolescents and Adults. Pretoria: Department of Health, Republic of South Africa; 2014. Department of Health, Republic of South Africa. National Consolidated Guidelines for the Prevention of Mother-to-Child Transmission of HIV (PMTCT) and the Management of HIV in Children, Adolescents and Adults. Pretoria: Department of Health, Republic of South Africa; 2014.
33.
go back to reference Levy PS, Lemeshow SA. Sampling of populations: methods and applications., 4th edn. Hoboken: Wiley; 2008.CrossRef Levy PS, Lemeshow SA. Sampling of populations: methods and applications., 4th edn. Hoboken: Wiley; 2008.CrossRef
34.
go back to reference Bertagnolio S, Parkin NT, Jordan M, Brooks J, Garcia-Lerma JG. Dried blood spots for HIV-1 drug resistance and viral load testing: a review of current knowledge and WHO efforts for global HIV drug resistance surveillance. AIDS Rev. 2010;12(4):195–208.PubMed Bertagnolio S, Parkin NT, Jordan M, Brooks J, Garcia-Lerma JG. Dried blood spots for HIV-1 drug resistance and viral load testing: a review of current knowledge and WHO efforts for global HIV drug resistance surveillance. AIDS Rev. 2010;12(4):195–208.PubMed
35.
go back to reference Mooney AC, Campbell CK, Ratlhagana MJ, Grignon JS, Mazibuko S, Agnew E, Gilmore H, Barnhart S, Puren A, Shade SB, et al. Beyond social desirability Bias: investigating inconsistencies in self-reported HIV testing and treatment behaviors among HIV-positive adults in north West Province, South Africa. AIDS Behav. 2018;22(7):2368–79.CrossRef Mooney AC, Campbell CK, Ratlhagana MJ, Grignon JS, Mazibuko S, Agnew E, Gilmore H, Barnhart S, Puren A, Shade SB, et al. Beyond social desirability Bias: investigating inconsistencies in self-reported HIV testing and treatment behaviors among HIV-positive adults in north West Province, South Africa. AIDS Behav. 2018;22(7):2368–79.CrossRef
36.
go back to reference Inzaule SC, Ondoa P, Peter T, Mugyenyi PN, Stevens WS, de Wit TFR, Hamers RL. Affordable HIV drug-resistance testing for monitoring of antiretroviral therapy in sub-Saharan Africa. Lancet Infect Dis. 2016;16(11):e267–75.CrossRef Inzaule SC, Ondoa P, Peter T, Mugyenyi PN, Stevens WS, de Wit TFR, Hamers RL. Affordable HIV drug-resistance testing for monitoring of antiretroviral therapy in sub-Saharan Africa. Lancet Infect Dis. 2016;16(11):e267–75.CrossRef
37.
go back to reference Venter WDF, Moorhouse M, Sokhela S, Fairlie L, Mashabane N, Masenya M, Serenata C, Akpomiemie G, Qavi A, Chandiwana N, et al. Dolutegravir plus two different Prodrugs of Tenofovir to treat HIV. N Engl J Med. 2019;381(9):803–15. Venter WDF, Moorhouse M, Sokhela S, Fairlie L, Mashabane N, Masenya M, Serenata C, Akpomiemie G, Qavi A, Chandiwana N, et al. Dolutegravir plus two different Prodrugs of Tenofovir to treat HIV. N Engl J Med. 2019;381(9):803–15.
38.
go back to reference Department of Health, Republic of South Africa. 2019 ART Clinical Guidelines for the Management of HIV in Adults, Pregnancy, Adolescents, Children, Infants and Neonates. Pretoria: Department of Health, Republic of South Africa; 2019. Department of Health, Republic of South Africa. 2019 ART Clinical Guidelines for the Management of HIV in Adults, Pregnancy, Adolescents, Children, Infants and Neonates. Pretoria: Department of Health, Republic of South Africa; 2019.
39.
go back to reference Inzaule SC, Hamers RL, Doherty M, Shafer RW, Bertagnolio S, Rinke de Wit TF. Curbing the rise of HIV drug resistance in low-income and middle-income countries: the role of dolutegravir-containing regimens. Lancet Infect Dis. 2019;19(7):e246–52.CrossRef Inzaule SC, Hamers RL, Doherty M, Shafer RW, Bertagnolio S, Rinke de Wit TF. Curbing the rise of HIV drug resistance in low-income and middle-income countries: the role of dolutegravir-containing regimens. Lancet Infect Dis. 2019;19(7):e246–52.CrossRef
40.
go back to reference Lehman DA, Baeten JM, McCoy CO, Weis JF, Peterson D, Mbara G, Donnell D, Thomas KK, Hendrix CW, Marzinke MA, et al. Risk of drug resistance among persons acquiring HIV within a randomized clinical trial of single- or dual-agent preexposure prophylaxis. J Infect Dis. 2015;211(8):1211–8.PubMedPubMedCentral Lehman DA, Baeten JM, McCoy CO, Weis JF, Peterson D, Mbara G, Donnell D, Thomas KK, Hendrix CW, Marzinke MA, et al. Risk of drug resistance among persons acquiring HIV within a randomized clinical trial of single- or dual-agent preexposure prophylaxis. J Infect Dis. 2015;211(8):1211–8.PubMedPubMedCentral
41.
go back to reference Liegler T, Abdel-Mohsen M, Bentley LG, Atchison R, Schmidt T, Javier J, Mehrotra M, Eden C, Glidden DV, McMahan V, et al. HIV-1 drug resistance in the iPrEx preexposure prophylaxis trial. J Infect Dis. 2014;210(8):1217–27.CrossRef Liegler T, Abdel-Mohsen M, Bentley LG, Atchison R, Schmidt T, Javier J, Mehrotra M, Eden C, Glidden DV, McMahan V, et al. HIV-1 drug resistance in the iPrEx preexposure prophylaxis trial. J Infect Dis. 2014;210(8):1217–27.CrossRef
42.
go back to reference Margot NA, Waters JM, Miller MD. In vitro human immunodeficiency virus type 1 resistance selections with combinations of tenofovir and emtricitabine or abacavir and lamivudine. Antimicrob Agents Chemother. 2006;50(12):4087–95.CrossRef Margot NA, Waters JM, Miller MD. In vitro human immunodeficiency virus type 1 resistance selections with combinations of tenofovir and emtricitabine or abacavir and lamivudine. Antimicrob Agents Chemother. 2006;50(12):4087–95.CrossRef
43.
go back to reference Zhang G, DeVos J, Medina-Moreno S, Wagar N, Diallo K, Beard RS, Zheng DP, Mwachari C, Riwa C, Jullu B, et al. Utilization of dried blood spot specimens can expedite nationwide surveillance of HIV drug resistance in resource-limited settings. PLoS One. 2018;13(9):e0203296.CrossRef Zhang G, DeVos J, Medina-Moreno S, Wagar N, Diallo K, Beard RS, Zheng DP, Mwachari C, Riwa C, Jullu B, et al. Utilization of dried blood spot specimens can expedite nationwide surveillance of HIV drug resistance in resource-limited settings. PLoS One. 2018;13(9):e0203296.CrossRef
45.
go back to reference Tanser F, Barnighausen T, Grapsa E, Zaidi J, Newell ML. High coverage of ART associated with decline in risk of HIV acquisition in rural KwaZulu-Natal, South Africa. Science. 2013;339(6122):966–71.CrossRef Tanser F, Barnighausen T, Grapsa E, Zaidi J, Newell ML. High coverage of ART associated with decline in risk of HIV acquisition in rural KwaZulu-Natal, South Africa. Science. 2013;339(6122):966–71.CrossRef
Metadata
Title
The role of drug resistance in poor viral suppression in rural South Africa: findings from a population-based study
Authors
Sheri A. Lippman
Alyssa C. Mooney
Adrian Puren
Gillian Hunt
Jessica S. Grignon
Lisa M. Prach
Hailey J. Gilmore
Hong-Ha M. Truong
Scott Barnhart
Teri Liegler
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-020-4933-z

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