Exploring the knowledge and perceptions of viral load testing and low-level viremia among health-care workers in Uganda: A qualitative study

Since the 2013 World Health Organization (WHO) recommendation of using viral load (VL) testing as the preferred method of monitoring people living with human immunodeficiency virus (PLHIV) on antiretroviral therapy (ART) [1], Uganda has made several strides in the scale-up of VL testing from about 16,411 VL samples (2% of PLHIV on ART) in 2014 to 1,442,373 VL samples (95% of PLHIV on ART) in 2022 [2]. Despite this progress, full scale-up and coverage of VL testing has been hindered by several challenges including unawareness about VL testing among HIV health-care workers [3, 4]. Furthermore, the previous use of a threshold of 1,000 copies/ml to determine VL non-suppression prior to this study resulted into accumulation of many PLHIV with a VL of at least 50 copies/ml but less than 1,000 copies/ml, which is referred to as low-level viremia (LLV).

An estimated 1.4 million people were living with HIV in Uganda, of which 1.2 million were accessing ART by 2022 [5]. As per the WHO recommendation, VL testing is used to monitor the efficacy of ART among PLHIV [6] and also recommended in Uganda [7]. HIV VL is the number of HIV viral RNA copies per milliliter of blood, and the test is used to determine the efficacy of ART. A VL of 1,000 copies/ml or higher is crucial in early detection of either poor drug adherence or virologic treatment failure [8]. A decreased VL is associated with better clinical outcomes and slowed disease progression [9] and is also associated with reduced HIV incidence at community level [9, 10]. VL non-suppression can be due to various risk factors including sociodemographic and psychological factors, comorbidities, poor absorption of ARVs, poor adherence to ART, and drug toxicity among others [11, 12, 13, 14]. PLHIV on ART with non-suppressed VL have an increased risk of fastened progression to acquired immune deficiency syndrome (AIDS) and have poor clinical outcomes [14, 15].

The use of 1,000 copies/ml as a threshold for viral non-suppression has previously resulted into increased PLHIV with LLV [16]. Previous studies have associated LLV with HIV drug resistance and increased risks of HIV transmission and virologic failure [17, 18, 19, 20, 21, 22, 23, 24, 25]. This is why the U.S. Centers for Disease Control and Prevention (CDC) and the International Association of Providers of AIDS Care (IAPAC) recommend using a threshold of 200 copies/ml for VL non-suppression [26, 27], against the WHO recommendation of a threshold of 1,000 copies/ml for viral non-suppression. Furthermore, LLV has been shown to be an emerging concern in Sub-Sahara Africa [28].

Health-care workers are the springboard of all HIV care at health facilities, including VL testing and management of LLV among PLHIV. However, their ability and willingness to provide these services is heavily influenced by their knowledge and perceptions [29]. Lack of knowledge on how to diagnose and manage common disease conditions, HIV inclusive is often associated with ineffective, suboptimal, and dangerous health-care practices, which can lead to delayed interventions and poor treatment outcomes [30]. Despite this, to date, there is no study that has explored knowledge and perceptions of VL testing and LLV, among health-care workers in Uganda. Therefore, in the efforts to scale up VL testing and institute interventions to manage LLV, this study aims to explore the knowledge and perceptions of VL testing and LLV among health-care workers in Uganda. This will contribute toward Uganda’s efforts to achieve the global targets of ending the HIV epidemic by 2030.

An exploratory qualitative study was conducted with a purposively selected sample of 15 health-care workers who work in 8 high-volume HIV clinics, with more than 1,000 active PLHIV, from the Central, Eastern, Northern, and Western geographical regions of Uganda. From each geographical region, 1 rural and 1 urban health facility providing VL services (to include participants with both rural and urban exposures) and having high numbers of PLHIV with LLV (compared to the other health facilities) was selected. The consolidated criteria for reporting qualitative research (COREQ) have been used to report these study findings [31].

The national VL program was started in 2014, and this is housed and coordinated at the Department of National Health Laboratory and Diagnostic Services (NHLDS/CPHL) in Kampala. The VL samples are transported from across the country to NHLDS/CPHL where they are tested by the national VL reference testing laboratory. The VL samples are transported through the hub sample transport system [32]. The VL data are managed through a comprehensive Laboratory Information Management System, hosted by a data center at NHLDS/CPHL, and the VL results are returned electronically through the electronic results download module [2]. The first VL test is done for PLHIV who have been on ART for 6 months, and then another VL test is done at 12 months. PLHIV with a VL result above 200 copies/ml and 400 copies/ml for plasma and dried blood spot samples, respectively, are now offered intensive adherence counseling (IAC) for 3 months, and a repeat VL test is repeated after 3 months. If PLHIV with a VL of 1,000 copies/ml or more does not attain viral suppression after IAC, a switch committee is convened, and the patient is switched to another ART line [7].

At the health facilities, the files of PLHIV due for VL testing are flagged with a sticker and sorted out on the day when they are due for testing. When the PLHIV come for the drug refill, they are reviewed by the Clinician, informed that they are due for VL testing and then sent to the laboratory for VL sample collection. A sample is then collected and transported to NHLDS/CPHL for testing, and the results turnaround time is about 2 weeks. The client is given their drugs, and they will receive their VL results at the next visit.

Health-care workers providing HIV care at the HIV clinic were selected by stratified purposive sampling based on age, sex, region, and cadre to create study variability [33]. These involved clinicians, nurses, laboratory staff, and counselors with different levels of experience. Each was invited to participate in the study by the research assistant and taken through an informed consent process. Two participants chose not to participate in the study because they had other conflicting priorities.

Key informant interviews (KIIs) were conducted with health-care workers in a safe place of their choice to collect information about their knowledge and perceptions of VL testing and LLV. A semi-structured interview guide was used, after piloting it with 2 PLHIV at 2 HIV clinics and reviewed for appropriateness by the study team. Several questions in the interview guide were restructured to make them more understandable, following the piloting of the guide. The guide included questions exploring the knowledge and perceptions of health-care workers regarding VL testing and LLV, the importance of these concepts in the management of HIV, and any challenges or barriers they may have encountered in VL testing and management of LLV. Interviews were conducted in English, by an experienced team of qualitative researchers, and each interview lasted approximately 30–45 min. Each interview was conducted in a quiet private room by 2 members of the study team, 1 interviewing and the other taking notes. The research team had daily reviews of the interviews conducted, and the data collection process was stopped when we reached saturation. Originally, we had planned to conduct a minimum of 16 KIIs but reached saturation at 15 KIIs and hence ended the data collection process [34].

Audio files were transcribed verbatim and checked for accuracy. Transcripts were imported in ATLAS.ti 6 for coding and we used thematic analysis to analyze the data [35]. Three analysts read through the transcripts to generate the initial codes. A meeting was then convened to review these codes and agree on the codebook that was applied to the rest of the data. We then identified the patterns and themes related to the perceptions and knowledge of VL testing and LLV among the participants, using a mixture of both inductive and deductive approaches.

The study acquired ethical approval from Makerere University School of Public Health Research and Ethics Committee (approval number is SPH-2021-144) and clearance from the Uganda National Council for Science and Technology (approval number is HS2008ES). We obtained informed consent from all the study participants prior to being interviewed.

The characteristics of the study participants are shown in Table 1. Figure 1 shows the major themes identified.

All the participants had a good understanding of VL testing, which matched its biomedical definition. Despite being of different cadres, all the participants described a VL test as the number of HIV viral copies in the blood of a PLHIV, and they indicated that a VL test is done to show the efficacy of ART.

They confidently used different biomedical terms to describe the different VL results, whereby a suppressed VL referred to results below 1,000 copies/ml and a result of 1,000 copies/ml or more was a non-suppressed VL. They associated a suppressed VL to both good treatment adherence and efficacy of ART while a non-suppressed VL was associated with either poor adherence or drug resistance.

The health-care workers were knowledgeable about the eligibility of PLHIV for VL testing, and they described with ease the different time intervals when a VL test is done. For example, they noted that a PLHIV who has been on ART for 6 months or more is the only 1 who is eligible for VL testing. They also highlighted that a VL test is repeated at 12 months, and then once every year for suppressed PLHIV. They however emphasized that a repeat VL is offered to non-suppressed PLHIV after 3 IAC sessions.

The health-care workers described VL testing as an important monitoring tool, which enables them to assess the efficacy of ART and how well the patient adheres to the prescribed drugs, which triggers them to take the next course of management action if the patient is not achieving the desired treatment outcomes of viral suppression.

VL testing was perceived as an important indicator of HIV drug resistance, and this is a key guide of switching PLHIV from one ART line to another.

The participants further described VL testing as a vital tool for monitoring and evaluation of the quality of HIV care that they offer to PLHIV in their respective health facilities. They linked this to UNAIDS “95 95 95” goals where VL is one of the targets and indicated that they track the percentage of suppressed and non-suppressed PLHIV routinely. They indicated that they were motivated by having high numbers of suppressed PLHIV.

The participants described several best practices, which they were undertaking to improve VL services in their respective facilities. The most common best practice described was sending frequent reminders to PLHIV due for VL testing. The participants indicated that a list of PLHIV due for VL testing is prepared in advance, and these PLHIV are either sent text message reminders or called by phone. For those who fail to turn up for their VL appointments, the health-care workers call them, encouraging them to come for their appointments.

The use of linkage facilitators and the village health teams to track PLHIV in the communities, who are due for VL testing but have missed their appointments was described as a key strategy to improve VL testing and other HIV care services.

Another key strategy highlighted in improving VL testing was the use of continuous quality improvement (CQI) projects. Participants described that several CQI projects are undertaken to improve different thematic areas of the VL testing cascade.

The participants reported that stickers are put on the files of PLHIV who are due for VL testing, and this enables such PLHIV to be easily identified for VL testing. Furthermore, they indicated that they sort out files of PLHIV due for VL testing earlier before the actual day when the VL is supposed to be done.

The use of the web-based VL dashboard to receive VL results and download them remotely in health facilities was reported as a key strategy that had improved VL testing. The dashboard is fundamental in reducing VL results turnaround time and ensuring that the PLHIV get their results in time, after being tested and uploaded at the national VL testing reference laboratory at NHLDS/CPHL.

Regular counseling, sensitization, and education of PLHIV about VL testing were also described as an important strategy that has improved VL testing. The participants indicated that through regular counseling and education, PLHIV understand and appreciate the use of VL testing, and this motivates them to come back for the testing on the given appointment dates. Creating good health worker–patient relationship through understanding the PLHIV, showing empathy and creating bonds with them was also reported as being useful in improving HIV care, VL testing inclusive.

The participants described the different challenges affecting VL testing in 3 main categories, including personal, health system, and community challenges, as shown in Figure 2.

The main personal challenge highlighted was lack of transport to move to the facilities for VL testing and other HIV services. This was worsened by long distances between homes and the health facilities, and the high rates of poverty.

The health-care workers reported that some PLHIV have conflicting priorities like work that affect their ability to go for VL testing. Nondisclosure of the HIV status by most PLHIV was also discussed as a key personal challenge, which interferes with the ability to seek HIV services including VL testing.

Furthermore, loss of hope among PLHIV and risky behaviors such as taking excessive alcohol and having multiple sexual partners were reported to be negatively affecting VL testing. PLHIV with suppressed VL were said to be indulging in such risky behaviors because they have a suppressed VL, which they interpret as safe. Hence, this leads them to engage in various risky behaviors, which increases their risks of non-suppression.

The participants reported that some PLHIV have very low literacy rates and cannot follow proper medical advice. Poor attitudes of some PLHIV in following medical advice was also described as a key challenge to VL testing, as it affects the uptake of the service.

Among the health system challenges, the participants indicated that there were few health-care workers as compared to the number of PLHIV, and these were overwhelmed with loads of work, resulting into long waiting times for PLHIV at the health facilities. This challenge was also coupled with poor attitudes and low motivation of the health-care workers.

There was a protracted VL results turnaround time, creating delays in patient management. Some VL results would completely not return, hence the need to bleed the PLHIV again. The VL web-based dashboard was also reported to be offline and inaccessible at times, hence patient results could not be downloaded quickly.

Occasional stock out of the different sample collection materials like syringes, gloves, and vacutainers among others was also reported to interrupt VL services. At times, there was also stock out of stationery, hence VL results could not be printed. Furthermore, many of the lower health facilities could not access the web-based dashboard to print their VL results and could only rely on other health facilities to receive their results.

HIV-related stigma was noted as the key community-related challenge affecting VL testing services. Due to stigma and discrimination associated with living with HIV in communities, many PLHIV feared to seek HIV care from facilities, including VL testing.

HIV stigma was also associated with many myths about HIV, and these created unnecessary fear about going for VL testing.

Participants emphasized that there was need to scale up the different best practices to strength and improve VL testing services like continuous sensitization and counseling, use of linkage facilitators, use of stickers, and CQI projects among others. Important to note was the need to reduce VL results turnaround time, which could be achieved through scaling up the use of the web-based VL dashboard and integrating the centralized VL testing with VL point-of-care testing.

Nearly all the participants could not define the term “low-level viremia” and this was new to them.

Those who struggled to define LLV interpreted it as having a suppressed VL, which is the aim of antiretroviral treatment.

When we described LLV as a range of viremia between 50 and 999 copies/ml among PLHIV on ART, many participants reported that this range of viremia was caused by sub-optimal drug adherence among PLHIV.

However, a few participants highlighted that this range could also be caused by drug resistance.

LLV was also reported to be more common in children and adolescents, as compared to the adult PLHIV.

The participants highlighted that LLV was also associated with risky behaviors like excessive consumption of alcohol, drug abuse, and having multiple partners among others. They explained that behaviors like alcohol consumption interfere with the ability to take drugs very well, hence leading to detectable viremia in blood.

Many participants had negative perceptions about LLV, and the main concern was that PLHIV with LLV had increased risks of becoming virally non-suppressed. Having detectable viremia in blood was also described to increase the risk of HIV transmission.

The participants explained that they were occasionally doing supplementary counseling to PLHIV with LLV to improve their drug adherence and manage the LLV. However, they reported that this counseling was informal and unstructured, being offered to PLHIV at will.

However, a few participants indicated that LLV was a suppressed state of viremia and hence did not worry about it at all. These participants said that LLV was not harmful to the PLHIV.

The knowledge and perceptions of health-care workers are a key determinant in provision of health-care services, including HIV VL testing and management of LLV [29]. This is why in this study, we set out to explore the knowledge and perceptions of VL testing and LLV among health-care workers in Uganda. Our findings indicated that the health-care workers at the different HIV clinics were proficient in VL testing. They described the eligibility for VL testing and also explained the different benefits of VL testing with ease. These findings could partly explain the progress achieved in scaling up of VL testing in Uganda since 2014 [2].

On contrary, the health-care workers could not define LLV, and they were not familiar with the term. However, most of them were aware that a VL range between 50 and 999 copies/ml was not desirable for PLHIV, since it had increased risks of viral non-suppression and HIV transmission, and this perception was in line with the various studies, which have associated LLV to virologic failure and HIV transmission [18, 19, 20]. The LLV range was perceived to be caused by sub-optimal drug adherence among PLHIV, and this finding is similar with another study which indicated that reduced drug adherence causes residual LLV [36]. LLV was also reported to be more common in children and adolescents, as compared to adults, and this could be explained by the sub-optimal drug adherence which is common among children and adolescents, as indicated in many recent studies [13, 36, 37, 38, 39, 40].

Participants indicated that interventions like supplementary counseling to manage PLHIV with LLV were very informal and unstructured, based on individual will of the health-care worker. This unfortunate finding was explained by the lack of guidance and national policy in the national HIV consolidated guidelines previously to emphasize that LLV was an emerging concern in Uganda, which needed to be adequately managed and addressed [41]. However, IAC has recently been instituted as an intervention to be offered to PLHIV with LLV in Uganda [7]. Furthermore, this was also caused by the sub-optimal understanding of LLV and its implications by the health-care workers, as indicated by the study findings.

Our study identified different best practices in scaling up and improving VL testing. The use of linkage facilitators to follow-up PLHIV due for VL testing was reported to be critical for the service, and this has also been highlighted to be very useful in improving other HIV services [42, 43, 44, 45]. Previous studies have shown that continuous reminders are very useful in health care [46, 47], and likewise, our participants noted that sending continuous reminders to PLHIV due for VL testing was very important. The participants emphasized that continuous patient counseling and education was the change-idea in scaling up and improving VL services, and this is in line with recent research [48, 49]. The use of a web-based VL dashboard was also noted to be very key in ensuring early return of VL results; and a similar study in Ivory Coast also indicated similar results about using a VL dashboard [50].

The main personal challenge was lack of transport to go to the clinics for VL testing, and this was coupled with by long distances and poverty; and this is similar to other studies that have highlighted transport and poverty challenges in seeking HIV care [51, 52, 53]. Hence, there is need to decentralize ART services and VL testing to lower health facilities and to community level, so that PLHIV do not have to move long distances to do their VL testing.

Few health-care workers resulting into long waiting times for PLHIV at the clinics and delayed return of VL results were noted as the key health system challenges, and these have also been reported in several other studies [54, 55, 56]. To reduce this challenge, several strategies like task-shifting and advocacy with the government to increase the human resource at the different health centers providing HIV care are recommended, since these have been found to be effective in HIV care in other studies [56, 57, 58]. Among the community-related challenges, HIV-related stigma associated with nondisclosure and myths about HIV were described as the key challenges, just like in several other studies [51, 52]. Hence, there is still need to create massive community education and awareness to overcome the issue of stigma.

From our study, there is an urgent need to create massive and targeted health education and sensitization about LLV among health-care workers and institute interventions to either reduce the number of PLHIV with LLV or manage the LLV. Furthermore, there is need to complement VL centralized testing with point-of-care testing to reduce the VL results turnaround time. Continuous awareness and education of both health-care workers and PLHIV about VL testing are also still vital in improving VL services.

This study included a diverse range of health-care workers from various clinics across the different regions of Uganda. This study is not without limitations. The study involved interviewing different health-care workers at selected HIV clinics in Uganda, and hence, we relied on what we were informed by the participants. As a result, social desirability bias could have affected our results. However, we created rapport with the participants and also kept the questions simple, not biased, neutral and not threatening.

The findings of this study suggest that many health-care workers still lack sufficient knowledge and understanding about LLV. To effectively address LLV and help Uganda reach UNAIDS viral suppression targets, a range of interventions will be necessary, and these mainly may include health education and sensitization programs for health-care workers. In addition, it will be important to improve access to VL testing by implementing point-of-care testing. Finally, comprehensive community awareness and sensitization efforts will be necessary to reduce HIV stigma.

Special thanks to the project administration team of Makerere University Behavioral and Social Science Research (MakBSSR) project, including Prof. Moses Kamya, Prof. Anne R. Katahoire, Dr. Fred Semitala, Mrs. Namubiru Rhoda, Ms. Joanita Nangendo, and Mr. Sempala Moses, for the efforts devoted toward conduction of this study.

Research reported in this publication was supported by the Fogarty International Center, National Institute of Alcohol Abuse and Alcoholism, National Institute of Mental Health, of the National Institutes of Health under Award Number D43 TW011304. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

The authors declare that they have no competing interests.

NN, GN, GS, SPSK, NK, FM, and DN developed and conceptualized the study. NN, SPSK, CK, GS, EN, and SN organized the data collection process and also analyzed the data. NN, GN, and EN wrote the article draft, which was then reviewed by all the authors.

How to cite this article: Nanyeenya N, Nakigozi G, Siu G, Kiwanuka N, Makumbi F, Nasuuna E, Nabadda S, Kiyaga C, Kibira SPS, Nakanjako D. Exploring the knowledge and perceptions of viral load testing and low-level viremia among health-care workers in Uganda: A qualitative study. Adv Glob Health. 2024;3(1). https://doi.org/10.1525/agh.2024.2315085

Editor-in-Chief: Craig R. Cohen, University of California San Francisco, CA, USA

Senior Editor: Andres G. Lescano, Cayetano University, Peru

Section: Improving Health and Well-Being