Virologic failure in HIV-positive adolescents with perfect adherence in Uganda: a cross-sectional study

Julian Natukunda, Peter Kirabira, Ken Ing Cherng Ong, Akira Shibanuma, Masamine Jimba, Julian Natukunda, Peter Kirabira, Ken Ing Cherng Ong, Akira Shibanuma, Masamine Jimba

Abstract

Background: Adolescents living with human immunodeficiency virus (HIV) die owing to acquired immune deficiency syndrome (AIDS)-related causes more than adults. Although viral suppression protects people living with HIV from AIDS-related illnesses, little is known about viral outcomes of adolescents in sub-Saharan Africa where the biggest burden of deaths is experienced. This study aimed to identify the factors associated with viral load suppression among HIV-positive adolescents (10-19 years) receiving antiretroviral therapy (ART) in Uganda.

Methods: We conducted a cross-sectional study among school-going, HIV-positive adolescents on ART from August to September 2016. We recruited 238 adolescents who underwent ART at a public health facility and had at least one viral load result recorded in their medical records since 2015. We collected the data of patients' demographics and treatment- and clinic-related factors using existing medical records and questionnaire-guided face-to-face interviews. For outcome variables, we defined viral suppression as < 1000 copies/mL. We used multivariate logistic regression to determine factors associated with viral suppression.

Results: We analyzed the data of 200 adolescents meeting the inclusion criteria. Viral suppression was high among adolescents with good adherence > 95% (adjusted odds ratio [AOR] 2.73, 95% confidence interval [95% CI, 1.09 to 6.82). However, 71% of all adolescents who did not achieve viral suppression were also sufficiently adherent (adherence > 95%). Regardless of adherence status, other risk factors for viral suppression at the multivariate level included having a history of treatment failure (AOR 0.26, 95% CI, 0.09 to 0.77), religion (being Anglican [AOR 0.19, 95% CI, 0.06 to 0.62] or Muslim [AOR 0.17, 95% CI, 0.05 to 0.55]), and having been prayed for (AOR 0.38, 95% CI, 0.15 to 0.96).

Conclusion: More than 70% of adolescents who experienced virologic failure were sufficiently adherent (adherence > 95). Adolescents who had unsuppressed viral loads in their initial viral load were more likely to experience virologic failure upon a repeat viral load regardless of their adherence level or change of regimen. The study also shows that strong religious beliefs exist among adolescents. Healthcare provider training in psychological counseling, regular and strict monitoring of adolescent outcomes should be prioritized to facilitate early identification and management of drug resistance through timely switching of treatment regimens to more robust combinations.

Keywords: Adherence; Adolescents; Antiretroviral therapy; Human immunodeficiency virus (HIV); Viral suppression; Virologic failure.

Conflict of interest statement

We obtained a waiver from the International Health Sciences University’s Degree Research and Ethics Committee. The reason for the waiver was that the study had no potential to cause harm whether physical or psychological to the participants. The decision was based on the National Guidelines for Research involving humans as research participants developed by the Uganda National Council for Science and Technology. We also obtained permission from the hospital administration to conduct the study.All participants (adolescents or caretakers) involved in the study gave their consent to use the information collected for publication purposes.The authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

    1. Joint United Nations Programme on HIV/AIDS (UNAIDS) Ending AIDS; Progress towards 90-90-90 targets. Geneva: UNAIDS; 2017.
    1. World Health Organization . A global research for adolescents living with HIV. Geneva: WHO; 2017.
    1. UNICEF. Analysis of UNAIDS 2016 estimates.
    1. Bulage L, Ssewanyana I, Nankabirwa V, Nsubuga F, Kihembo C, Pande G, et al. Factors associated with virological non-suppression among HIV-positive patients on antiretroviral therapy in Uganda August 2014–July 2015. BMC Infect Dis. 2017;17:326. doi: 10.1186/s12879-017-2428-3.
    1. Boerma RS, Boender TS, Bussink AP, Calis JC, Bertagnolio S, Rinke de Wit TR, et al. Sub-optimal viral suppression rates among HIV-infected children in low-and middle- income countries: a meta-analysis. Clin Infect Dis. 2016; 10.1093/cid/ciw645.
    1. World Health Organization . Prevent HIV, test and treat all. Geneva: World Health Organization; 2016.
    1. Galea JT, Wong M, Muñoz M, Valle E, Leon SR, Perez DD, et al. Barriers and facilitators to antiretroviral therapy adherence among Peruvian adolescents living with HIV: a qualitative study. PLoS One. 2018;13:e0192791. doi: 10.1371/journal.pone.0192791.
    1. Shubber Z, Mills EJ, Nachega JB, Vreeman R, Freitas M, Bock P, et al. Patient-reported barriers to adherence to antiretroviral therapy: a systematic review and meta-analysis. PLoS Med. 2016;13:e1002183. doi: 10.1371/journal.pmed.1002183.
    1. Okawa S, Kabaghe SM, Mwiya M, Kikuchi K, Jimba M, Kankasa C, et al. Psychological well-being and adherence to antiretroviral therapy among adolescents living with HIV in Zambia. AIDS Care. 2018;30:634–642. doi: 10.1080/09540121.2018.1425364.
    1. McKinney O, Modeste NN, Lee JW, Gleason PC, Maynard-Tucker G. Determinants of antiretroviral therapy adherence among women in Southern Malawi: Healthcare providers’ perspectives. AIDS Res Treat. 2014; 10.1155/2014/489370.
    1. Bereznicki LR, Peterson GM, Bimirew MA, Kassie DM. Barriers and facilitators of adherence to antiretroviral drug therapy and retention in care among adult HIV-positive patients: a qualitative study from Ethiopia. PLoS One. 2014;9:e97353. doi: 10.1371/journal.pone.0097353.
    1. Zanoni BC, Sibaya T, Cairns C, Lammert S, Haberer JE. Higher retention and viral suppression with adolescent-focused HIV clinic in South Africa. PLoS One. 2017;12:e0190260. doi: 10.1371/journal.pone.0190260.
    1. Ferrand RA, Simms V, Dauya E, Bandason T, Mchugh G, Mujuru H, et al. The effect of community-based support for caregivers on the risk of virological failure in children and adolescents with HIV in Harare, Zimbabwe (ZENITH): an open-label, randomized controlled trial. Lancet Child Adolesc Health. 2017;1:175–183. doi: 10.1016/S2352-4642(17)30051-2.
    1. Joint United Nations Programme on HIV/AIDS (UNAIDS) The Gap report: beginning of the end of the AIDS epidemic. Geneva: UNAIDS; 2014.
    1. Ministry of health . Uganda HIV/AIDS country progress report July 2016-June 20. Reaching men, girls and young women to reduce new HIV infections. 2017.
    1. Kamya M, Mayanja-kizza H, Kambugu A, Bakeera-kitaka S, Semitala F, Mwebaze-songa P, et al. Predictors of long-term viral failure among Ugandan children and adults treated with antiretroviral therapy. J Acquir Immune Defic Syndr. 2007;46:187–193. doi: 10.1097/QAI.0b013e31814278c0.
    1. Duarte HA, Harris DR, Tassiopolous K, Leister E, Fabiana S, Ferreira FF, et al. Relationship between viral load and behavioral measures of adherence to antiretroviral therapy in children living with human immunodeficiency virus in Latin America. Braz J Infect Dis. 2015;19:263–271. doi: 10.1016/j.bjid.2015.01.004.
    1. Glass TR, Rotger M, Telenti A, Decosterd L, Csajka C, Bucher HC, et al. Determinants of sustained viral suppression in HIV-infected patients with self-reported poor adherence to antiretroviral therapy. PLoS One. 2012;7:e29186. doi: 10.1371/journal.pone.0029186.
    1. Williams PL, Storm D, Montepiedra G, Nichols S, Kammerer B, Sirois PA, et al. Predictors of adherence to antiretroviral medications in children and adolescents with HIV infection. J Pediatr. 2006;118:e1745–e1757. doi: 10.1542/peds.2006-0493.
    1. Ministry of Health, Uganda . Consolidated guidelines for prevention and treatment of HIV in Uganda. 2016.
    1. World Health Organization. Technical and operational considerations for implementing HIV viral load testing; Interim update. Geneva: WHO; 2014. .
    1. Nlend N, Esther A, Annie Nga M, Suzie Tetang N, Joseph F. Predictors of virologic failure on first-line antiretroviral therapy among children in a referral pediatric center in Cameroon. Pediatr Infect Dis J. 2017;362. 10.1097/INF.0000000000001672.
    1. Buma D, Bakari M, Fawzi W, Mugusi F. The influence of HIV-status disclosure on adherence, immunological and virological outcomes among HIV-infected patients started on antiretroviral therapy in Dar-es-Salaam, Tanzania. J HIV AIDS. 2015;1. doi. org/10.16966/2380-5536.111.
    1. Agwu AL, Fairlie L. Antiretroviral treatment, management challenges and outcomes in perinatally HIV-infected adolescents. Int AIDS Soc. 2013;16:18579. doi: 10.7448/IAS.16.1.18579.
    1. Sithole Z, Mbizvo E, Chonzi P, Mungati M, Juru TP, Shambira G, et al. Virological failure among adolescents on ART, Harare City, 2017- a case-control study. BMC Infect Dis. 2018;18:469. doi: 10.1186/s12879-018-3372-6.
    1. Nasuuna E, Kigozi J, Babirye L, Muganzi A, Sewankambo NK, Nakanjako D. Low HIV viral suppression rates following the intensive adherence counseling (IAC) program for children and adolescents with viral failure in public health facilities in Uganda. BMC Public Health. 2018:1048.ty 0 10.1186/s12889-018-5964-x.
    1. World Health Organization. HIV drug resistance report 2017. Geneva: WHO; 2017. .
    1. Geary RS, Gómez-Olivé FX, Kahn K, Tollman S, Norris SA. Barriers to and facilitators of the provision of a youth-friendly health services programme in rural South Africa. BMC Health Serv Res. 2014;14:259. doi: 10.1186/1472-6963-14-259.
    1. Pillay P, Ford N, Shubber Z, Ferrand RA. Outcomes for efavirenz versus nevirapine-containing regimens for treatment of HIV-1 infection: a systematic review and meta-analysis. PLoS One. 2013;8:e68995. doi: 10.1371/journal.pone.0068995.
    1. Bayu B, Tariku A, Bulti AB, Habitu YA, Derso T, Teshome DF. Determinants of virological failure among patients on highly active antiretroviral therapy in University of Gondar Referral Hospital, Northwest Ethiopia: a case–control study. J HIV AIDS. 2017;9:153–159. doi: 10.2147/HIV.S139516.
    1. Jobanputra K, Parker LA, Azih C, Okello V, Maphalala G, Kershberger B, et al. Factors associated with virological failure and suppression after enhanced adherence counselling, in children, adolescents and adults on antiretroviral therapy for HIV in Swaziland. PLoS One 2015;10:e0116144. 10.1371/journal.pone.0116144.
    1. Nachega JB, Marconi VC, van Zyl GU, Gardner EM, Preiser W, Hong SY, et al. HIV treatment adherence, drug resistance, virologic failure: evolving concepts. Infect Disord Drug Targets. 2011;11(2):167–174. doi: 10.2174/187152611795589663.
    1. Lowenthal ED, Ellenberg JH, Machine E, Sagdeo A, Boititswe S, Steenhoff AP, et al. Association between efavirenz-based compared with nevirapine-based antiretroviral regimens and virological failure in HIV-infected children. JAMA. 2013;309:1803–1809. doi: 10.1001/jama.2013.3710.
    1. Kyaw NT, Harries AD, Kumar AM, Oo MM, Kyaw KW, Win T, et al. High rate of virological failure and low rate of switching to second-line treatment among adolescents and adults living with HIV on first-line ART in Myanmar, 2005-2015. PLoS One. 2017;12(2):e0171780. doi: 10.1371/journal.pone.0171780.
    1. MacCarthy S, Saya U, Samba C, Birungi J, Okoboi S, Linnemayr S. “How am I going to live?”: exploring barriers to ART adherence among adolescents and young adults living with HIV in Uganda. BMC public health. 2018;18(1):1158. doi: 10.1186/s12889-018-6048-7.

Source: PubMed

3
Abonnere