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. Author manuscript; available in PMC: 2021 Dec 15.
Published in final edited form as: J Acquir Immune Defic Syndr. 2020 Dec 15;85(5):606–611. doi: 10.1097/QAI.0000000000002498

Time to repeat viral load testing among unsuppressed adolescents and young adults living with HIV in Kenya

MUGO Cyrus 1,4, WILSON Katherine 3, ONYANGO Alvin 9, NJUGUNA N Irene 1, MBURU W Caren 9, RICHARDSON Barbra 3,5, OYIENGO Laura 10, INWANI Irene 2, JOHN-STEWART Grace 3,4,6,7, WAMALWA Dalton 9, KOHLER Pamela 3,8
PMCID: PMC8559766  NIHMSID: NIHMS1750257  PMID: 32897936

Abstract

Background

Repeat HIV viral load (VL) testing is required after unsuppressed VL to confirm treatment failure. We assessed proportion of adolescents and young adults living with HIV (AYALHIV) in Kenya with a confirmatory VL test and time to repeat testing.

Design

A retrospective analysis of longitudinal data abstracted from Kenya’s national viral load database.

Methods

Viral load data for AYALHIV who were 10–24 years old between April 2017- May 2019 were abstracted from 117 HIV care clinics. Records were eligible if at least one VL test was done ≥6 months after antiretroviral treatment (ART) initiation. The proportion of unsuppressed AYALHIV (≥1000 copies/ml) and time in months between first unsuppressed VL and repeat VL was determined.

Results

We abstracted 40,928 VL records for 23,969 AYALHIV, of whom 17,092 (71%) were eligible for this analysis. Of these, 12,122 (71%) were female, median age 19 years (IQR: 13–23) and median ART duration 38 months (IQR: 16–76). Among eligible AYALHIV, 4,010 (23%) had an unsuppressed VL at first eligible measurement. Only 316 (8%) of the unsuppressed AYALHIV had a repeat VL within 3 months and 1,176 (29%) within 6 months. Among 2,311 virally unsuppressed AYALHIV with a repeat VL, median time between the first and the repeat VL was 6 months (IQR: 4–8), with 1,330 (58%) having confirmed treatment failure.

Conclusions

One-quarter of AYALHIV on ART had unsuppressed VL, with less than a third receiving a repeat VL within 6 months. Strategies to improve VL testing practices are needed to improve AYALHIV’s outcomes.

Keywords: Adolescents, HIV, viral load, antiretroviral treatment, Kenya, sub-Saharan Africa

Introduction

Over 90% of adolescents and young adults living with HIV (AYALHIV) are in sub-Saharan Africa (SSA).1 The burden of HIV among AYALHIV has increased due to high incidence of new infections,1 and more perinatally infected children entering adolescence due to improved access to antiretroviral therapy (ART).2,3 Compared to adults, adolescents have poorer viral suppression,4 likely due to poor retention in care and challenges with ART adherence.4–6

Viral load (VL) testing is the cornerstone of monitoring HIV treatment.7 The WHO HIV treatment guidelines, adopted in Kenya in 2016, recommended all HIV infected persons initiated on ART should have VL testing at 6 and 12 months after ART initiation.7,8 Viral suppression is defined as VL <1000 copies/ml after 6 months of ART.9 After 12 months, clients who are virally suppressed can receive annual VL measurements.7,8 For AYALHIV, the updated 2018 Kenya HIV treatment guidelines recommended routine VL testing every 6 months.10 The WHO and local guidelines7,10 do not recommend routine viral load measurements at ART initiation or baseline HIV genotyping, unlike guidelines in high-income countries.11

If unsuppressed, enhanced adherence counseling is recommended, and after 1–3 months, a repeat VL is done to rule out treatment failure.7,8,12,13 A diagnosis of virological treatment failure (two consecutive unsuppressed VL with adherence support) is required to make treatment failure-related ART regimen changes.7 Prompt use of VL data enables clinicians to make informed decisions about treatment including adherence support and regimen changes. Barriers that result in delay or failure to utilize VL information for the care of AYALHIV include missed clinic appointments and loss to follow-up,4,14 provider shortages15 or inadequate training on actions to take after a VL result.16 This study aimed to assess the proportion and characteristics of AYALHIV with unsuppressed VL who received a repeat VL and time until a repeat test.

Methods

Study design

This retrospective analysis of electronic VL records for AYALHIV ages 10–24 years was conducted in 113 public and 4 faith-based HIV care clinics, across 28 of 47 counties in Kenya participating in two clinical trials. The trials assessed the impact of health provider training on adolescent retention in care and clinical outcomes (NCT02928900),17 and implementation of a transition package to support adolescent transition to adult care (NCT03574129).18

Ethical considerations

The two trials and abstraction of VL records were approved by Kenyatta National Hospital Ethics and Research Committee, and the University of Washington Institutional Review Board, National AIDS and STI Control Programme (NASCOP), County governments and health facilities.

Data abstraction and cleaning

All VL records for AYALHIV ages 10–24 years in the period between April 1, 2017 and May 31, 2019 were abstracted from the national VL database. Variables abstracted included: the unique personal identification number (UPN), county, facility code, gender, age, ART initiation date, ART regimen, dates of sample collection and testing, date of entry of result in the database (dispatch), and the VL result.

Data analysis

Eligible AYALHIV records had documentation of ≥1 VL test in the dataset ≥6 months after ART initiation date. Further, the earliest eligible VL record in the dataset should have been performed ≥6 months before the administrative censoring date, May 31, 2019. This ensured that each AYALHIV included in the analysis had at least 6 months of follow up time after their first eligible VL to receive a second VL test, if indicated. We defined the first eligible viral load as the earliest viral load for each participant after April 1, 2017 that fit the above criteria.

Demographics and treatment at first eligible VL were summarized. To estimate mode of HIV acquisition, AYALHIV ages ≤12 years at first eligible VL or at ART initiation were classified as having perinatally acquired HIV with the rest as behaviorally acquired HIV.19 We calculated the proportion of AYALHIV with an unsuppressed first eligible VL (≥1000 copies/ml) and the proportion that received a subsequent VL test within 3 and 6 months, and 12 months among those with ≥12 months of follow up time. We compared the median time (months) from first VL test to repeat test for AYALHIV with a suppressed result and an unsuppressed result using the Wilcoxon signed-rank test,. Additionally, we calculated the proportion with documented regimen changes following two consecutive unsuppressed VL results.

We used log-binomial regression clustered by facility to obtain prevalence ratios (PR) and 95% confidence intervals (CI) to compare characteristics of unsuppressed AYALHIV with and without repeat VL testing. Variables considered in univariable analysis included age group (10–14, 15–19 and 19–24), gender, region categorized by HIV prevalence (low-medium [<5%], high [5–11%] and hyper-endemic [>11%]),19,20 facility level (health center/dispensary and County/sub-County), population served by facility (rural or urban), years on ART (≤1 year, >1 year-<5 years and ≥5 years), mode of HIV acquisition (behavioral or perinatal), and ART regimen. Regimens were categorized into non-nucleoside reverse transcriptase inhibitor (NNRTI-based), protease inhibitor (PI-based), dolutegravir (DTG-based), and non-standard regimen (two nucleoside reverse transcriptase inhibitors [NRTI] plus one NNRTI). Variables with p-values ≤0.1 in the univariable analysis were included in the multivariable model. Analyses used R Studio (Version 1.1.456, 2009–2018) and Stata (StataCorp, College Station TX).

Results

We abstracted 40,928 VL records for 23,969 AYALHIV, of whom 17,092 (71%) were eligible for this analysis. Of those, 12,122 (71%) were female, median age 19 years (IQR: 13–23) and on ART for a median 38 months (IQR: 16–76) (Table 1). The median time from sample collection to dispatch of results was 15 days (IQR: 10–21).

Table 1:

Characteristics of adolescents and young adults with repeat viral load testing ≤6 months after an unsuppressed viral load

Characteristic Overall (N=17,092) n (%) VL ≥ 1000 copies/ml (N=4,010) * n (%) Repeat VL ≤6 months (N=1,176) * n (%) Univariable PR 95% CI, p value Multivariable PR 95% CI, p value
Gender
 Male 4953 (29) 1562 (32) 445 (28) Reference
 Female 12122 (71) 2447 (20) 731 (30) 1.03 (0.92–1.17), 0.580
Age categories (years)
 10–14 5267 (31) 1629 (31) 502 (31) Reference
 15–19 3641 (21) 1109 (30) 311 (28) 0.89 (0.77–1.02), 0.103
 20–24 8184 (48) 1272 (16) 363 (29) 0.92 (0.80–1.05), 0.218
^ HIV prevalence of County of residence
 Low-medium 8140 (48) 2246 (28) 633 (28) Reference Reference
 High 2742 (16) 572 (21) 171 (30) 1.02 (0.80–1.31), 0.852 1.02 (0.80–1.31), 0.865
 Hyper-endemic 6210 (36) 1192 (19) 372 (31) 1.20 (0.98–1.47), 0.081 1.20 (0.98–1.47), 0.078
Facility level
 Health center/dispensary 7260 (42) 1550 (21) 443 (29) Reference
 County/sub-County hospital 9832 (58) 2460 (25) 733 (30) 1.10 (0.92–1.32), 0.284
Population served by facility
 Rural 13577 (79) 3322 (25) 967 (29) Reference
 Urban 3515 (21) 688 (20) 209 (30) 0.96 (0.76–1.21), 0.706
ART experience
 ≤1 year 3245 (19) 507 (16) 160 (32) Reference
 >1-<5 years 8001 (47) 1701 (21) 483 (28) 0.91 (0.76–1.08), 0.280
 ≥ 5 years 5846 (34) 1802 (31) 533 (30) 0.94 (0.79–1.13), 0.503
Mode of HIV acquisition
 Behavioral 9810 (57) 1639 (17) 461 (28) Reference
 Perinatal 7282 (43) 2371 (33) 715 (30) 1.07 (0.95–1.21), 0.236
Regimen at first VL
 NNRTI based 14128 (82) 3181 (23) 945 (30) Reference Reference
 PI based 2601 (15) 744 (29) 198 (27) 0.91 (0.78–1.07), 0.255 0.91 (0.78–1.06), 0.242
 DTG based 89 (1) 24 (27) 5 (21) 0.71 (0.29–1.72), 0.442 0.71 (0.29–1.73), 0.455
 Non-standard 262 (2) 59 (23) 27 (46) 1.51 (1.03–2.23), 0.037 1.52 (1.03–2.24), 0.036
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*

Row percentage (across variable category); NNRTI – non-nucleoside reverse transcriptase inhibitor;

^

Global Wald test p value = 0.209; PI – protease inhibitor; DTG - dolutegravir

Non-standard – Two nucleoside reverse transcriptase inhibitors (NRTI) and one NNRTI; Bolded: Association significant or trends towards significance

Among 17,092 AYALHIV, 4,010 (23%) had an unsuppressed VL at first eligible measurement. Of these, only 316 (8%) had a repeat VL within 3 months and 1,176 (29%) within 6 months. Among the 3,184 unsuppressed AYALHIV with ≥12 months of follow up time, 2,051 (64%) had a second viral load within 12 months (Figure 1). The median time between the first unsuppressed VL and subsequent VL was 6 months (IQR: 4–8). In contrast, among the 6,587/13,082 (50%) with a suppressed first VL and a second viral load, the median time between the two tests was 9 months (IQR: 6–12), p<0.001.

Figure 1: Analysis flowchart showing proportion of adolescents and young adults unsuppressed and with repeat HIV viral load measurements.

Figure 1:

Open in a new tab

AYALHIV – Adolescents and young adults living with HIV

ART – Antiretroviral treatment

ID – Identification number

In multivariable analysis, AYALHIV who were virally unsuppressed on a non-standard regimen, were 52% more likely to have a repeat VL when compared to those on an NNRTI (aPR: 1.52 [1.03–2.24], p=0.036). There was a non-significant trend towards higher likelihood of having a repeat VL within 6 months for unsuppressed AYALHIV from hyper-endemic regions compared to those from low-medium prevalence regions (aPR: 1.20 [0.98–1.47], p=0.078), global Wald test, p=0.209. (Table 1). No significant associations were found with age categories, gender, facility level, population served by facility, ART experience and mode of HIV acquisition.

Of the 2,311/4,010 (58%) unsuppressed AYALHIV with a subsequent VL, 1,330 (58%) had two consecutive unsuppressed VLs. Of those, 729 (55%) had a third VL record, a median 6 months (IQR: 4–8) after the second unsuppressed VL, and information on ART regimen. Only 238/729 (33%) had documentation of a change of regimen after confirmation of treatment failure.

Discussion

In this analysis using Kenya’s HIV program VL data, one quarter of AYALHIV on ART had viral non-suppression and needed a second test to determine treatment failure. Close to two-thirds of unsuppressed AYALHIV had a subsequent VL within a year, though only 8% had the repeat VL test within the recommended 3 months. Slightly over half of unsuppressed AYALHIV had a confirmation of treatment failure though only a third had a subsequent change of ART regimen. Virally unsuppressed AYALHIV from high prevalence regions and those on non-standard ART regimens were more likely to receive repeat VL tests.

The proportion unsuppressed among these AYALHIV (23%) was comparable to results of other recent studies in Kenya.21–23 Studies from other SSA counties had mixed prevalence of non-suppression ranging from 18% to 56%.24–30 The low proportion of unsuppressed AYALHIV with repeat VL testing within guidelines in our study is also consistent with previous reports from Kenya23 and other SSA countries.31–35 In this study however, the period between sample collection to dispatch of results was a median of 15 days, which is lower than what was previously reported in Kenya (21 days)23 and other SSA countries (24–48 days)16,36

Although WHO guidelines recommend repeat VL testing within 3 months of an unsuppressed VL, and adherence support in the intervening period to confirm or exclude treatment failure,7 local guidelines in Kenya10 and other SSA countries13,37 require that good adherence is first established, and 1–3 months after, a repeat VL is offered. The guidelines10 recommend three or more enhanced adherence counseling (EAC) sessions, whose spacing is at the convenience of the health provider and the adolescent, and there is no suggested timing for re-testing if adherence issues are not resolved. Establishing good adherence is challenging and could be a barrier to repeat VL testing if it takes time to complete counseling. Providers need clear guidance to repeat testing if good adherence is not achieved within a certain period. It is possible that AYALHIV school and work schedules prevented timely clinic appointments and initiation of the required EAC.14,38 Previous studies have further demonstrated that re-suppression rates were higher in adults than adolescents and children after EAC.31,39 While EAC avoids unnecessary regimen changes, children and adolescents may require additional interventions to enhance adherence including cognitive behavioral therapy, supporter interventions, weekly short message service, and interventions targeting stigma and depressive illnesses, which have been shown to be more effective than basic or enhanced adherence counseling.40–42

Lack of repeat testing means that the diagnosis of treatment failure is not made, in which case treatments cannot be modified, and AYALHIV are left susceptible to opportunistic infections and mortality.43 Though non-significant, the trend towards a higher likelihood for AYALHIV from high HIV prevalence regions getting a timely repeat VL if unsuppressed, is a pattern also demonstrated in retention in care44 and viral suppression45, likely because health providers serving AYALHIV in high prevalence regions are more experienced with HIV procedures.19 We also found that the practice of offering repeat VL testing may be different based on the ART regimen AYALHIV are taking. Those on non-standard regimen8 were more likely to have a repeat VL when compared to those on NNRTI regimen, likely because they have failed standard regimen or developed side effects and are therefore followed more closely by health providers. In this study, over half of unsuppressed AYALHIV with a repeat VL had treatment failure, similar to previous studies in SSA.23,33 However, only one third had a subsequent change of regimen documented, exposing another potential gap in care. The under-utilization of VL results by providers in determining treatment regimens for AYALHIV has been demonstrated in other studies31. Training and mentoring of providers on recommended treatment modification algorithms could reduce the population of AYALHIV on ineffective treatment.46

Interventions to improve time to repeat testing for unsuppressed AYALHIV may target health providers, health systems, or caregivers and AYALHIV. Health provider behavior can be addressed through training on utilization of VL information in care of AYALHIV.47 Systems-level interventions may include adoption of point of care VL testing,48–50 community-level VL testing using dried blood spots,51 reminders in electronic records to request testing, and decongesting adolescent clinics through differentiated care models.52,53 Empowering AYALHIV and caregivers of younger adolescents to take charge of their own care and request their test results could also help testing demand.54

The strength of our study included a large sample size of AYALHIV with wide geographical representation. A limitation of the study was that we were not able to establish the number of AYALHIV on ART without a VL, whether unsuppressed AYALHIV had EAC and whether lack of repeat VL testing was due to AYALHIV loss to follow up, gaps in documentation, or gaps in service delivery at the facility. We did not have information on pregnancy status and co-infections like tuberculosis which may have influenced ART regimen changes.10

Conclusion

Delays in repeat VL testing may contribute to poor treatment outcomes among AYALHIV. Targeted interventions aimed at reducing turnaround time for confirmatory VL test, developing systems to ensure timely repeat tests, and educating AYALHIV and their caregivers to be their own care advocates could improve treatment outcomes.

Acknowledgements

We acknowledge the study participants, SPEED, ATTACH and facility staff. CM and AO performed data collection and CM led the primary data analysis and writing of this paper; KW, INN, CWM, BR, LO, II, GJS, DW, PK were involved in design and review of the paper. Funding was provided by National Institutes for Health (R01HD085807 and R01HD089850-01). Additional support was provided to CM and INN by Fogarty International Center (D43TW009783), the University of Washington Global Center for Integrated Health of Women, Adolescents and Children (Global WACh), and Center for Global Health Nursing.

Conflicts of interest and Sources of funding:

The authors have no conflicts of interest to declare. The study was funded under two grants by the National Institutes of Health (R01HD085807 and R01HD089850). Additional support was provided to CM and INN by Fogarty International Center (D43TW009783); the University of Washington (UW) Global Center for Integrated Health of Women, Adolescents and Children (Global WACh); and the UW Center for Global Health Nursing.

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