Open Forum Infectious Diseases

MAJOR ARTICLE

Human Immunodeficiency Virus Viral Load Monitoring

and Rate of Virologic Suppression Among Patients
Receiving Antiretroviral Therapy in Democratic Republic
of the Congo, 2013–2020
Nadine Mayasi Ngongo,1 Erick Kamangu Ntambwe,2 Hippolyte Situakibanza Nani-Tuma,1 Marcel Mbula Mambimbi,1 Madone Mandina Ndona,1
Murielle Longokolo Mashi,1 Ben Bepouka Izizag,1 Tuna Lukiana,1 Jérôme Odio Ossam,1 Donatien Mangala Sonzi,1 Nathalie Maes,3 Michel Moutschen,4,5

Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023

Majdouline El Moussaoui,4 and Gilles Darcis4,
1
Department of Internal Medicine, Infectious and Tropical Diseases, University Hospital of Kinshasa, Kinshasa, Democratic Republic of the Congo, 2Department of Molecular Biology of Basic
Sciences, University of Kinshasa, Kinshasa, Democratic Republic of the Congo, 3Biostatistics and Research Method Center (B-STAT), University Hospital of Liège, Liège, Belgium, 4Department of
Internal Medicine and Infectious Diseases, Liège University Hospital, Liège, Belgium, and 5AIDS Reference Laboratory, University of Liège, Liège, Belgium

Background. Antiretroviral therapy (ART) expansion and viral load as a treatment monitoring approach have increased the
demand for viral load testing. Many hurdles affect the coverage, quality, and use of viral load results. Estimates of viral load
monitoring and viral suppression rates are needed to assess the performance of ART programs and improve human
immunodeficiency virus (HIV) management outcomes.
Methods.. People with HIV (PWH) viral load monitoring data were routinely collected in 84 health facilities in Kinshasa,
Democratic Republic of the Congo (DRC), between 2013 and 2020. The number of PWH under ART, the number of participants
with at least 1 viral load test result, the rate of viral suppression (defined as ≤1000 HIV ribonucleic acid copies per mL), and the
mean turnaround time from sample collection to release of viral load test results were collected together with clinical data.
Results. A total of 14 057 PWH were included in the analysis. People with HIV were mainly enrolled after the “test and treat”
implementation. The patients were followed for a median period of 27 months. The proportion of PWH with at least 1 available
viral load largely increased in recent years. The delay from sample collection to release of viral load test results decreased
overtime, from 35 days in 2018 to 16 days in 2020. Pregnancy and advanced HIV disease were associated with a lower chance of
viral suppression.
Conclusions.. There has been considerable success in increasing viral load access for all PWH under therapy in DRC.
Nevertheless, viral load testing should be intensified with a particular effort to be made in groups at higher risk of viral failure.
Keywords. ART; monitoring; testing; viral load; virologic suppression.

The availability of antiretroviral therapy (ART) has dramati­ after the scaling up of ART coverage as well as a positive impact
cally improved the prognosis of human immunodeficiency vi­ on HIV incidence in the population with earlier initiation of
rus (HIV) infection. It has also improved the quality and life ART [2, 3].
expectancy of people with HIV (PWH) [1]. Antiretroviral ther­ To improve access to ART and follow the World Health
apy uptake is rapidly expanding in low- and middle-income Organization (WHO) recommendations, the Democratic
countries (LMICS), notably in sub-Saharan Africa (SSA). Republic of Congo (DRC) has adopted the “test and treat”
Numerous studies suggested an improvement in health, eco­ (T&T) strategy since November 2016 [4, 5]. In addition, to im­
nomic productivity, and a change in the epidemic trajectory prove treatment monitoring in LMICs, the WHO has recom­
mended viral load (VL) testing as the preferred strategy for
Received 28 February 2023; editorial decision 26 April 2023; accepted 02 May 2023; pub­ monitoring the effectiveness of ART, leading to progressive
lished online 3 May 2023 phasing out of baseline CD4 T-cell count testing [6, 7].
Correspondence: Gilles Darcis, MD, PhD, Avenue de l’hôpital 1, 4000 Liège, Belgium
([email protected]); Nadine Mayasi Ngongo, MD, PhD, Avenue de l’hôpital 1, 4000 Liège, Indeed, VL monitoring allows early detection of treatment fail­
Belgium (nadiamayas02@gmail). ure, before immunologic decline. One target of UNAIDS to end
Open Forum Infectious Diseases® the HIV/acquired immune deficiency syndrome (AIDS) epi­
© The Author(s) 2023. Published by Oxford University Press on behalf of Infectious Diseases
Society of America. This is an Open Access article distributed under the terms of the demic by 2030 is to achieve undetectable VL in 95% of all per­
Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons. sons receiving ART. Viral suppression (VS) is not only
org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of
the work, in any medium, provided the original work is not altered or transformed in any associated with a decrease in HIV disease progression but
way, and that the work is properly cited. For commercial re-use, please contact journals.permis­ also with the prevention of HIV transmission. Viral load mea­
[email protected]
https://doi.org/10.1093/ofid/ofad242
surement thus became a critical instrument to assess the impact

Viral Load Monitoring in DRC • OFID • 1

of HIV treatment efforts, and it is now the primary methodol­ DRC and is already widely used in Kinshasa [9]. The imple­
ogy for monitoring response to ART [7, 8]. Most country mentation of Tier.Net is ongoing in other provinces of DRC.
guidelines called for VL testing at 6 and 12 months after ART All patients on ART included in the study are systematically re­
initiation and then annually. corded at each clinical visit in a standardized clinical file and
Both ART expansion and VL testing as a treatment monitor­ then in electronic registers. Tier.net data are regularly validated
ing approach have increased demand for VL testing. However, against patient records. Viral load results were retrieved from
many hurdles have been identified affecting the coverage, qual­ the electronic VL database.
ity, and use of results. These comprise correct sampling proce­ Variables recorded at ART initiation included age, gender,
dures, transporting samples to laboratories, guaranteeing tests weight, height, body mass index, WHO stage, CD4 T cells,
are timely performed, and allowing rapid access to test results. the size of the health facility (categorized as small, medium,
Estimates of VL monitoring and VS rates are needed to as­ and large and, respectively, for <100, 100–500, and >500
sess the performance of ART programs and improve HIV man­ PWH under follow up), ART regimen, delay to ART initiation

Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023

agement outcomes. We performed the first multicentric (time between HIV diagnosis and ART initiation, categorized
longitudinal study assessing the impact of the “test and treat” as <7 and ≥7 days), the notion of advanced HIV disease
strategy on VL monitoring and viral suppression rate in a (AHD) (defined as CD4 T cells <200 cells/mm3 and/or WHO
very large population of PWH in Kinshasa, DRC. clinical stage 3 or 4), prophylaxis with cotrimoxazole and isoni­
azid, and type of care providers.
METHODS
Viral load suppression was defined as all viral load results ≥5
months from ARV initiation indicating viral suppression
Study Design, Framework, and Periods (<1000 copies/mL). First-year viral load suppression was de­
This is a historical cohort analysis using PWH monitoring data fined as all viral load results between 5 and 13 months from
routinely collected in 84 health facilities in Kinshasa, mainly ARV initiation indicating viral suppression (<1000 copies/mL).
health centers that constitute the peripheral and operational
level of the health system in the DRC, between January 1, Statistical Analyses
2013 and December 31, 2020. The duration of the study was di­ Continuous variables are presented using mean and standard de­
vided into 2 periods—from 1 January 1, 2013 to October 31, viation (SD) or median with interquartile ranges (IQRs) as appro­
2016 and after November 1, 2016 to December 31, 2020—cor­ priate. Qualitative variables are described using frequency tables
responding to the periods before and after the implementation (numbers and percentages). Comparison of patients for the 2
of the T&T strategy. studied periods, before and after T&T implementation, used χ2,
analysis of variance, or Kruskal-Wallis tests, as appropriate.
Participants and Viral Load Testing Logistic regression models were used to evaluate the impact
All PWH over the age of 15 years who initiated first-line ART of each prognostic factor on VS. Variables with a P value lower
during the study period were included. Antiretroviral therapy than .1 in the single logistic models were included in the mul­
should have been initiated between January 1, 2013 and tiple model.
December 31, 2019. Data were collected until December 31, The results were considered significant at the 5% level
2020. Participants with a follow up shorter than 5 months (P < .05). Missing data have not been replaced and calculations
were excluded. The Congolese national HIV program offers have always been made on the maximum number of data avail­
free ART using WHO-preferred antiretroviral regimens as able. Data analysis was performed using SAS (version 9.4 for
well as VL monitoring [6]. Virologic monitoring should consist Windows). R packages (version 3.6.1) were used for the figures.
of VL measurements at 6 and 12 months after ART initiation
and annual measurements thereafter. Virologic failure is de­ Ethics Approval and Patient Consent Statement
fined as viral load above 1000 copies/mL based on 2 consecutive The design of the work has been approved by local ethical com­
viral load measurements in a 3-month interval, with adherence mittees and it conforms to standards currently applied in DRC.
support after the first viral load test, after at least 6 months of Approval was granted by the Scientific Committee and the
starting a new ART regimen [6]. Research Ethics Committee of the School of Public Health of
the Faculty of Medicine of the University of Kinshasa in the
Data Sources and Data Collection DRC (ESP/CE/005/2019). Patient data were extracted anony­
The study population’s demographic, clinical, and laboratory mously, and confidentiality was respected. All methods were
data were extracted from the Tier.Net electronic database. carried out in accordance with relevant guidelines and regula­
Tier.Net is an electronic system with modules to capture tions. Informed consent was not required, according to the
patient-level data on HIV counseling, testing, pre-ART, and Ethics Committee recommendations, because this study does
ART services. The use of this tool is recommended in the not include factors necessitating patient consent.

2 • OFID • Ngongo et al
RESULTS T&T implementation, the proportion of patients with at least
Participants’ Characteristics
1 available VL (68.6% vs 58.3%, P < .0001) (Supplementary
Data from 14 057 patients infected with HIV out of the 17 023 Table S1) and with a VL within the year of ART initiation
PWH who started ART between 2013 and end of 2019 regis­ (55.6% vs 4.4%, P < .0001) (Figure 2) was higher in recent years.
tered in the databases met the inclusion criteria (Figure 1). Despite a drastic increase in the number of VL tests per­
Table 1 describes the general characteristics of PWH at ART formed during recent years, the delay from sample collection
initiation. The patients were mostly women (67.2%). The mean to return of viral load test results decreased overtime, from
age was 40.0 ± 11.4 years. The median CD4 T-cell count was 35 days in 2018 to 16 days in 2020 (Figure 3 and
254 (IQR, 141–400) cells/mm³ with 68.3% of participants Supplementary Table 2).
with CD4 T-cell count below 350 cells/mm³ and 31.4% with
WHO clinical stage at 3 or 4. At ART initiation, 68.3% of reg­ Rate of Viral Suppression
imens contained efavirenz (EFV) and 17.2% contained dolute­ The overall rate of VS was 82.3% at the threshold of VL less

Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023

gravir (DTG). Eighty-four percent of PWH started ART within than 1000 copies/mL (Supplementary Table S3). Considering
1 week after diagnosis of HIV infection. Eighty-seven percent the first available VL only, 87.2% of the participants were virally
of participants had cotrimoxazole prophylaxis (CPT). suppressed at the threshold <1000 copies/mL. Considering
People with HIV were mainly enrolled during the T&T peri­ both the total available VL tests and the VL tests performed
od (72.9%). Compared to the period before this strategy, there within 1 year after ART initiation, viral suppression did not sig­
were significantly (P < .0001) fewer adolescents (2% vs 2.6%), nificantly differ before or after T&T implementation (Figure 4)
fewer women, pregnant or not (65.7% vs 71.4%), and less and remained above 80%.
AHD (25.1% vs 53.9%). Patients were more likely to start When the VL was greater than 1000 copies/mL, 72.5% of
ART within 7 days (94.6% vs 51.3%) and to receive ART con­ PWH had control of the VL after a median delay of 116 days
taining DTG (23.5%) as well as CPT (90.8% vs 76.7%) (Table 1). (IQR, 26–193) and 23.1% maintained a VL greater than 1000
copies/mL, defining virologic failure according to the WHO
Viral Load Testing
definition [6] (Supplementary Table 3). The percentage of
The patients were followed for a median period of 27 months PWH with a second VL test performed in the case of unsup­
(IQR, 17–44). Only 65.8% of PWH had at least 1 available VL pressed VL was higher after the T&T implementation (76%
test. The percentage of participants having a VL test within 1 vs 62.4%, P < .0001) (Supplementary Table 3). Among those
year after ART initiation increased overtime (Supplementary with a second VL performed, the rate of viral suppression
Table S1). When comparing the periods before and after the was higher after the T&T implantation (Supplementary
Table 3). In other words, a reduced percentage of participants
met the definition of virologic failure after the T&T
implementation.

Factors Associated With Virologic Suppression

Regarding factors associated with virologic suppression, preg­
nancy (adjusted odds ratio [aOR], 0.62; 95% confidence inter­
val [CI], .47–.81) (P = .0004) and AHD (aOR, 0.83; 95% CI,
.72–.97) (P = .017) were associated with a lower chance of VS
(Figure 5; Supplementary Table 4). In contrast, the probability
of VS was higher when ART was initiated by a nurse (aOR, 1.2;
95% CI, 1.04–1.4) (P = .012), when the initial regimen con­
tained DTG compared with EFV (aOR, 1.2; 95% CI, 1.01–
1.5) (P = .014), and when patients were under follow up in a
medium or large facility (aOR, 1.3; 95% CI, 1.04–1.5)
(P = .017). Age, gender, time to ART initiation, period of treat­
ment for PWH, and duration of follow up did not influence on
the probability of VS (Figure 5; Supplementary Table 4).

DISCUSSION

During last years, viral load testing became the favored moni­
Figure 1. Flowchart. ART, antiretroviral therapy. toring strategy for PWH [7]. Viral load testing enables early

Viral Load Monitoring in DRC • OFID • 3

Table 1. Description of PWH at ARV Treatment Initiation

ARV Initiated From Jan 2013 to ARV Initiated From Nov 2016 to
All (N = 14 057) Nov 2016 (N = 3800) Dec 2019 (N = 10 257)
Comparison
Characteristics N Nonmissing Results N Nonmissing Results N Nonmissing Results P Value

Gender, women 14 057 9448 (67.2) 3800 2712 (71.4) 10 257 6736 (65.7) <.0001
Pregnant women 9271 744 (8.0) 2577 343 (13.3) 6694 401 (6.0) <.0001
Age (years) 14 057 40.0 ± 11.4 3800 39.6 ± 11.0 10 257 40.2 ± 11.6 .0023
15–19 … 299 (2.1) … 97 (2.6) … 202 (2.0) …
20–24 … 1054 (7.5) … 258 (6.8) … 796 (7.8) …
25–49 … 9884 (70.3) … 2754 (72.5) … 7130 (69.5) …
≥ 50 … 2820 (20.1) … 691 (18.2) … 2129 (20.8) …
Height (cm) 276 164 ± 9 270 164 ± 9 6 165 ± 9 …
Weight (kg) 12 491 61.2 ± 11.1 3314 62.1 ± 12.1 9177 60.8 ± 10.7 <.0001

Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023

BMI (kg/m²) 268 22.6 ± 4.7 262 22.5 ± 4.7 6 23.2 ± 6.5 …
CD4 (cells/mm³) 2116 254 (141; 400) 1953 250 (138; 395) 163 290 (187; 480) …
<200 … 797 (37.7) … 752 (38.5) … 45 (27.6) …
200–350 … 647 (30.6) … 597 (30.6) … 50 (30.7) …
351–500 … 368 (17.4) … 339 (17.4) … 29 (17.8) …
>500 … 304 (14.4) … 265 (13.6) … 39 (23.9) …
WHO Stage 10 651 … 2796 … 7855 … <.0001
I … 4834 (45.4) … 804 (28.8) … 4030 (51.3) …
II … 2472 (23.2) … 611 (21.9) … 1861 (23.7) …
III … 3028 (28.4) … 1243 (44.5) … 1785 (22.7) …
IV … 317 (3.0) … 138 (4.9) … 179 (2.3) …
Advanced HIVa 11 094 3702 (33.4) 3186 1717 (53.9) 7908 1985 (25.1) <.0001
Initial ART 14 035 … 3785 … 10 250 … <.0001
TDF/3TC/DTG … 2411 (17.2) … 0 (.0) … 2411 (23.5) …
TDF/3TC/EFV … 9149 (65.2) … 1674 (44.2) … 7475 (72.9) …
TDF/3TC/NVP … 185 (1.3) … 89 (2.3) … 96 (0.9) …
TDF/3TC/LPVr … 29 (0.2) … 9 (0.2) … 20 (0.2) …
AZT/3TC/DTG … 1 (0.0) … 0 (0.0) … 1 (0.0) …
AZT/3TC/EFV … 433 (3.1) … 396 (10.5) … 37 (0.4) …
AZT/3TC/NVP … 1674 (11.9) … 1569 (41.4) … 105 (1.0) …
AZT/3TC/LPVr … 22 (0.2) … 7 (0.2) … 15 (0.1) …
Others … 131 (0.9) … 41 (1.1) … 90 (0.9) …
Days since HIV diagnosis 10 418 0 (0; 0) 2520 7 (0; 28) 7898 0 (0; 0) <.0001
≤7 days … 8761 (84.1) … 1292 (51.3) … 7469 (94.6) …
>7days … 1657 (15.9) … 1228 (48.7) … 429 (5.4) …
IPT 13 018 1833 (14.1) 3059 76 (2.5) 9959 1757 (17.6) <.0001
CPT 13 925 12 117 (87.0) 3701 2837 (76.7) 10 224 9280 (90.8) <.0001
Healthcare provider 14 001 … 3761 … 10 240 … .0051
Doctor … 3570 (25.5) … 1023 (27.2) … 2547 (24.9) …
Nurse … 10 431 (74.5) … 2738 (72.8) … 7693 (75.1) …
Care Center 14 057 … 3800 … 10 257 … <.0001
Small … 1837 (13.1) … 296 (10.4) … 1429 (14.0) …
Medium … 8846 (62.9) … 1978 (52.0) … 6868 (67.0) …
High … 3374 (24.0) … 1426 (37.5) … 1948 (19.0) …
Abbreviations: 3TC, lamivudine; ART, antiretroviral therapy; ARV, antiretroviral; AZT, zidovudine; BMI, body mass index; CPT, cotrimoxazole preventive therapy; Dec, December; DTG,
dolutegravir; EFV, efavirenz; HIV, human immunodeficiency virus; IPT, isoniazid preventive therapy; Jan, January; LPVr, ritonavir-boosted lopinavir; Nov, November; NVP, nevirapine;
PWH, people with HIV; TDF, tenofovir disoproxil fumarate; WHO, World Health Organization.
NOTE: Results are expressed as N (%), mean ± standard deviation, or median (interquartile range), and P values as χ2, analysis of variance, or Kruskal-Wallis, respectively.
a
Advanced HIV disease if CD4 <200 cells/mm³ and/or WHO stage III/IV.

detection of treatment failure. In addition, virologic suppres­ the HIV/AIDS epidemic by 2030 is that 95% of all individuals
sion is associated with reduced HIV transmission [10]. under ART reach viral suppression [11], highlighting the need
Consequently, testing all PWH for VL became a universal for global and sustained VL monitoring. In addition, the WHO
health priority. One key element of the UNAIDS goal to end now recommends immediate initiation of ART for all people

4 • OFID • Ngongo et al
 Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023
Figure 3. Evolution of time from sample collection to return of viral load (VL) test
results to referring care center (linear regression of year impact on log-transformed
time to return of results). ARV, antiretroviral.
Figure 2. Percentage of patients who had ≥1 viral load test within the year of
antiretroviral therapy initiation (≤13 months) before and after “test and treat” im­
plementation (before and after November 2016).
Regarding viral suppression, we observed an overall VS rate
of 82.3%. This is lower than the target of 95% of UNAIDS but
diagnosed with HIV, regardless of CD4 T-cell count [6]. similar than those reported in the majority of cohorts from
Expansions in ART eligibility criteria for PWH were followed LMICs [8, 13–16]. Considering the first VL performed after a
by substantial increases in rates of timely ART initiation, median delay of 12 months, this VS rate is higher (87.2%)
with much larger increases among those newly eligible under than the overall VS rate. This difference should raise the ques­
the expanded guidelines compared with those eligible under tion of the maintenance of VS in the long term. Adherence to
prior guidelines [12]. Both ART expansion and switch from ART seems to be a key issue because the majority of patients
CD4 T-cell counts to VL to monitor ART effectiveness should with a controlled VL after a first test above 1000 copies/mL
be accompanied by progress on the scale up of VL testing. achieved VS without any change in the therapeutic regimen.
In this study, we showed that there has been considerable suc­ Those patients do not meet the definition of virologic failure.
cess in increasing VL access for all PWH under therapy. Despite In our study, the risk of unsuppressed viremia (>1000 cop­
a huge increase in the number of PWH in Kinshasa under ART, ies/mL) was higher in pregnant women, in PWH with AHD,
we observed a dramatic improvement in access to VL, with and in patients treated with nevirapine-based or EFV-based
more than 50% benefiting from VL testing within 1 year after regimens compared with DTG-based regimens, confirming
ART initiation since 2016. This number rapidly increased to the results of several studies in SSA [17–21]. Careful follow
reach 66.9% in 2019. In the case of VL above 1000 copies/mL, up should be proposed to groups at higher risk of treatment
a subsequent VL test is required within 6 months to define viro­ failure and lower adherence to therapy to ensure the individual
logic failure. This control is also much more frequently per­ and population benefits of ART. It is interesting to note that
formed since 2016. The increase in the number of VL tests is PWH who initiated ART at a medium- or large-volume center
accompanied by a reduction in the delay from sample collection or by a nurse achieved viral suppression more often. It is reas­
to return of VL test results during recent years, reflecting the im­ suring that delegating the monitoring and treatment of PWH to
provement in the scale up of VL testing. Nevertheless, sustained nurses, initiated to expand access to care to a larger number of
engagement is required to hit UNAIDS targets. Efforts and pro­ PWH, can effectively support rapid ART scale up in the era of
gress accomplished until now remain insufficient to reach T&T in the DRC.
WHO guidelines related to virologic monitoring at 6 and 12 We showed that PWH with low viremia (51–999 copies/mL)
months after ART initiation and then annually. represent a significant proportion of our patients. Although the

Viral Load Monitoring in DRC • OFID • 5

 Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023
Figure 4. Percentage of participants with viral suppression (<1000 copies/mL). (A) Percentage of participants with viral suppression during the first year from antiretroviral
(ARV) initiation. (B) Percentage of participants with viral suppression (all available viral load results ≥5 months from antiretroviral therapy initiation).

which the cross-referencing of codes impeded the full recovery

of VL data. Finally, we were not able to assess adherence to
ART, which is described as the main cause of unsuppressed vi­
remia in several cohorts [25–27]. Nevertheless, our study has
some strengths. It covers a period after the implementation
of T&T with enough hindsight to assess its impact on virologic
suppression. The analyses relate to a large number of PWH fol­
lowed in numerous healthcare centers distributed in all the
health zones of the city of Kinshasa. The results of this study
reflect routine clinical practice under the programmatic condi­
tions of resource-limited settings.

Figure 5. Characteristics associated with the probability of viral suppression (<1000 CONCLUSIONS
copies/mL): multiple logistic regression. 3TC, lamivudine; AVR, antiretroviral; AZT, zido­
vudine; CI, confidence interval; DTG, dolutegravir; EFV, efavirenz; OR, odds ratio. We showed a successful increase in VL monitoring in the DRC
before and after the implementation and T&T strategy. This
goes together with a reduction in the delay from sample collec­
WHO guidelines do not recommend changing treatment in this tion to the VL results. Nevertheless, the scale up of VL testing
condition, some studies in resource-limited settings have de­ should be intensified because the percentage of PWH with
scribed low viremia as a predictor of subsequent virologic failure available VL tests remains insufficient. Unsuppressed viral
[22–24]. Those patients likely deserve closer monitoring. load is mostly due to poor adherence as the majority of the par­
Our results should be interpreted considering certain limita­ ticipants later achieved suppressed viral load without ART
tions. We used data collected in the routine management of pa­ modification. Pregnant women and PWH with AHD are at
tients, which may have several gaps. We used 2 databases for higher risk of viral failure and should be carefully followed.

6 • OFID • Ngongo et al
Supplementary Data Kinshasa, DRC, before and after the implementation of the ‘treat-all’. Strategy.
PLoS Global Public Health 2022; 2:e0000259.
Supplementary materials are available at Open Forum Infectious Diseases
10. Ghosn J, Taiwo B, Seedat S, Autran B, Katlama C. HIV. Lancet 2018; 392:685–97.
online. Consisting of data provided by the authors to benefit the reader, the
11. UNAIDS. Ambitious treatment targets: writing the final chapter of the AIDS ep­
posted materials are not copyedited and are the sole responsibility of the idemic: writing the final chapter of the AIDS epidemic. Geneva, 2014. Available
authors, so questions or comments should be addressed to the correspond­ at: https://www.unaids.org/sites/default/files/media_asset/JC2670_UNAIDS_
ing author. Treatment_Targets_en.pdf. Accessed June 13, 2023.
12. Tymejczyk O, Brazier E, Yiannoutsos C, et al. HIV Treatment eligibility expan­
Acknowledgments sion and timely antiretroviral treatment initiation following enrollment in HIV
care: a metaregression analysis of programmatic data from 22 countries. PLoS
We thank all participants and staff at the human immunodeficiency virus Med 2018; 15:e1002534.
care facilities included in these analyses. 13. Hermans LE, Carmona S, Nijhuis M, et al. Virological suppression and clinical
Author contributions. NMN, HSN-T, MMM, MMN, MLM, EKN, BB, management in response to viremia in South African HIV treatment program:
JOO, and GD contributed to conceptualization. NMN, HSN-T, MMM, a multicenter cohort study. PLoS Med 2020; 17:e1003037.
DMS, TL, and JOO contributed to data curation. NMN, BB, NM, and 14. Pillay T, Cornell M, Fox MP, et al. Recording of HIV viral loads and viral suppres­
GD contributed to formal analysis. NMN and EKN contributed to investi­ sion in South African patients receiving antiretroviral treatment: a multicentre co­
gations. NMN, NM, and GD contributed to methodology. HSN-T, MMM, hort study. Antivir Ther 2020; 25:257–66.
15. Haas AD, Radin E, Hakim AJ, et al. Prevalence of nonsuppressed viral load and

Downloaded from https://academic.oup.com/ofid/article/10/6/ofad242/7150390 by guest on 21 September 2023

MLM, JOO, MM, and GD contributed to supervision. NM, BB, EKN, MM,
associated factors among HIV-positive adults receiving antiretroviral therapy in
and GD contributed to validation. NMN, MEM, and GD contributed to
eswatini, Lesotho, Malawi, Zambia and Zimbabwe (2015 to 2017): results from
writing the original draft. All authors contributed to writing, reviewing, population-based nationally representative surveys. J Int AIDS Soc 2020; 23:
and editing. e25631.
Financial support. GD is postdoctorate clinical master specialist for the 16. Fast-Track strategy to end the AIDS epidemic by 2030. Available at: https://www.
Fonds National de la Recherche Scientifique (FNRS) (Belgium). MEM is unaids.org/en/resources/campaigns/World-AIDS-Day-Report-2014. Accessed
medical doctor applicant to an MSc (medicine, infectious diseases) and a April 24, 2023.
PhD in medical sciences for the FNRS (Belgium). 17. Kerschberger B, Schomaker M, Ciglenecki I, et al. Programmatic outcomes and
Potential conflicts of interest. All authors: No reported conflicts of impact of rapid public sector antiretroviral therapy expansion in adults prior to
interest. introduction of the WHO treat-all approach in rural Eswatini. Trop Med Int
Health 2019; 24:701–14.
18. Hirasen K, Fox MP, Hendrickson CJ, Sineke T, Onoya D. HIV treatment out­
References comes among patients initiated on antiretroviral therapy pre and post-universal
1. Silveira MPT, Silveira CPT, Guttier MC, Page K, Moreira LB. Long-term immune test and treat guidelines in South Africa. Ther Clin Risk Manag 2020; 16:169–80.
and virological response in HIV-infected patients receiving antiretroviral therapy. 19. Wekesa P, McLigeyo A, Owuor K, Mwangi J, Nganga E, Masamaro K. Factors as­
J Clin Pharm Ther 2016; 41:689–94. sociated with 36-month loss to follow-up and mortality outcomes among
2. Petersen M, Balzer L, Kwarsiima D, et al. Association of implementation of a uni­ HIV-infected adults on antiretroviral therapy in central Kenya. BMC Public
versal testing and treatment intervention with HIV diagnosis, receipt of antiretro­ Health 2020; 20:328.
viral therapy, and viral suppression in East Africa. JAMA 2017; 317:2196–206. 20. Chammartin F, Zürcher K, Keiser O, et al. Outcomes of patients lost to follow-up
3. Molina JM, Grund B, Gordin F, et al. Which HIV-infected adults with high CD4 in African antiretroviral therapy programs: individual patient data meta-analysis.
T-cell counts benefit most from immediate initiation of antiretroviral therapy? A Clin Infect Dis 2018; 67:1643–52.
post-hoc subgroup analysis of the START trial. Lancet HIV 2018; 5:e172–80. 21. Yotebieng M, Mpody C, Ravelomanana NL, et al. HIV viral suppression among
4. REPUBLIQUE DEMOCRATIQUE DU CONGO MINISTERE DE LA SANTE pregnant and breastfeeding women in routine care in the Kinshasa province: a
PROGRAMME NATIONAL DE LUTTE CONTRE LE SIDA ET LES IST baseline evaluation of participants in CQI-PMTCT study. J Int AIDS Soc 2019;
« PNLS ». Guide de prise en charge intégrée du VIH en République 22:e25376.
démocratique du Congo. PNLS. RDC 2019. Available at: https://www. 22. Hermans LE, Moorhouse M, Carmona S, et al. Effect of HIV-1 low-level viraemia
prepwatch.org/wp-content/uploads/2022/03/DRC-National-PrEP-Guideliens-2019. during antiretroviral therapy on treatment outcomes in WHO-guided South
pdf. Accessed April 24, 2023. African treatment programmes: a multicentre cohort study. Lancet Infect Dis
5. Ngongo NM, Darcis G, Nanituna HS, et al. Longitudinal analysis of sociodemo­ 2018; 18:188–97.
graphic, clinical and therapeutic factors of HIV-infected individuals in Kinshasa 23. Zhang T, Ding H, An M, et al. Factors associated with high-risk low-level viremia
at antiretroviral therapy initiation during 2006-2017. PLoS One 2021; 16: leading to virologic failure: 16-year retrospective study of a Chinese antiretroviral
e0259073. therapy cohort. BMC Infect Dis 2020; 20:147.
6. World Health Organization. Consolidated guidelines on the use of antiretroviral 24. Joya C, Won SH, Schofield C, et al. Persistent low-level viremia while on antire­
drugs for treating and preventing HIV infection. Recommendations for a Public troviral therapy is an independent risk factor for virologic failure. Clin Infect Dis
Health Approach. 2013 revision. Geneva, WHO 2013. Available at: http://apps. 2019; 69:2145–52.
who.int/iris/bitstream/10665/85321/1/9789241505727_eng.pdf?ua=1. Accessed 25. Myer L, Redd AD, Mukonda E, et al. Antiretroviral adherence, elevated viral load,
April 24, 2023. and drug resistance mutations in human immunodeficiency virus-infected wom­
7. Ngongo NM, Nani-Tuma HS, Mambimbi MM, et al. Progressive phasing out of en initiating treatment in pregnancy: a nested case-control study. Clin Infect Dis
baseline CD4 + cell count testing for people living with HIV in Kinshasa, 2020; 70:501–8.
Democratic Republic of the Congo. AIDS 2021; 35:841–3. 26. Bezabhe WM, Chalmers L, Bereznicki LR, Peterson GM. Adherence to antiretro­
8. Lecher SL, Fonjungo P, Ellenberger D, et al. HIV viral load monitoring among pa­ viral therapy and virologic failure: a meta-analysis. Medicine (Baltimore) 2016; 95:
tients receiving antiretroviral therapy—eight sub-Saharan Africa countries, 2013– e3361.
2018. MMWR Morb Mortal Wkly Rep 2021; 70:775–8. 27. Altice F, Evuarherhe O, Shina S, Carter G, Beaubrun AC. Adherence to HIV treat­
9. Mayasi N, Situakibanza H, Mbula M, et al. Retention in care and predictors of at­ ment regimens: systematic literature review and meta-analysis. Patient Prefer
trition among HIV-infected patients who started antiretroviral therapy in Adherence 2019; 13:475–90.

Viral Load Monitoring in DRC • OFID • 7