Skip to main content
Download PDF

Association between differentiated HIV care delivery model and low-level viremia among people living with HIV in Rwanda

AIDS Research and Therapy volume 21, Article number: 79 (2024) Cite this article

Abstract

Background

Low-level viremia (LLV) (HIV-RNA 51–999 copies/mL) is associated with increased risk of non viral load suppression (HIV-RNA ≥ 1000 copies/mL). We assessed the association between differentiated service delivery model (DSDM) and LLV among people living with HIV (PLHIV) in Rwanda.

Methods

We conducted a retrospective cohort analysis using routinely collected data of adults living with HIV from 28-healthcare facilities in Rwanda before and after the introduction of DSDM. Under DSDM, PLHIV initiated treatment within seven days of HIV diagnosis and medication pick-up up to six months for those with sustained viral load suppression suppression. Proportions of LLV at 6,12 and 18 months were quantified. Multivariable log binomial regression models were used to assess the effect of DSDM on LLV. To handle missing data, multiple imputations was performed.

Results

Of 976 people living with HIV, 645(66.0%) were female and 463(47.4%) initiated treatment during DSDM. The median age was 37 (interquartile range: 32–43) years. LLV was 7.4%, 6.6% and 5.4%, at 6,12 and 18 months, respectively. Compared to those who initiated treatment before DSDM, starting treatment during DSDM increased six-month LLV [adjusted risk ratio (aRR) = 2.8: 95%CI (1.15–6.91)] but not at 12 [aRR = 2.3: 95%CI (0.93–5.75)] and 18 months [aRR = 0.3: 95%CI (0.09–1.20)]. Using imputed datasets, the association between DSDM and LLV persisted.

Conclusions

DSDM was associated with increased risk of LLV at 6-months. possibly due to the minimal amount of time PLHIV had in pondering and accepting the HIV diagnosis. Continued support is needed among people receiving early antiretroviral therapy initiation to prevent development of LLV.

Introduction

Access to antiretroviral therapy (ART) for people living with HIV has reduced morbidity and mortality associated with HIV and opportunistic infections, globally [1]. ART has turned HIV into a manageable chronic illness with a significant improvement in quality of life for people living with HIV [2, 3]. The success of ART are notable in HIV programs with improved retention in care, ART adherence and viral load suppression [4, 5].

For monitoring clinical outcomes of people living with HIV receiving ART, the World Health Organization (WHO) recommends categorization of people living with HIV based on viral load. Those with a viral load of < 1,000 copies/mL are regarded as virally suppressed and those with a viral load of ≥ 1,000 copies/mL as not suppressed [6]. People living with HIV with two or more consecutive viral loads of ≥ 1,000 copies/mL, often regarded as treatment failures, likely harbor resistance mutations and have higher risk of transmitting HIV to uninfected partners [7, 8]. Although people living with HIV with a viral load of < 1,000 copies/mL have lower likelihood of transmitting infection compared to those with a viral load of ≥ 1,000 copies/mL, evidence has shown that, compared to those with a viral load of ≤ 50 copies/mL, those with low-level viremia (LLV; VL: 51–999 copies/mL) have a higher risk of becoming non-virally suppressed [9,10,11] and developing resistance mutations [12, 13]. This evidence prompted debates on whether the threshold of viral load suppression needs to be revised [14].

Since 2016, WHO has recommended a differentiated service delivery model (DSDM) with different components to tailor client needs [15]. By the beginning of 2017, all health care facilities were implementing DSDM in Rwanda. Under DSDM, people living with HIV were categorized as stable or unstable based on duration on and ART and virologic monitoring. Stable clients living with HIV (on ART for ≥ 18 months and two consecutive suppressed viral loads) have the option to have a longer prescription filled of up to six months and assigned to peer educators who provides moral and psychological support and promote adherence to treatment and retention within a specified catchment area. Unstable clients receive monthly prescriptions from the health facility, were not assigned to peer educators, but benefited from monthly adherence and counseling from healthcare providers on each drug pick-up appointment. A systematic review of 37 DSDM reported higher estimates of retention for HIV programs that did not report comparison groups; however, for those that did, retention was shown to be comparable between people living with HIV who were under DSDM and those who were not under DSDM [16]. Another component of DSDM is early initiation of ART following HIV diagnosis without an extended counselling period compared to initiation of ART based on CD4 count which was characterized with an extended period of counselling. Although early initiation of ART has been associated with reduced time to viral load suppression [17] and overall viral load suppression [18, 19], it has also been associated with loss to follow up (LTFU) [20]. It has been argued that absence of extended periods of counselling may partly explain LTFU among people living with HIV who initiate ART immediately following HIV diagnosis. Prior data has shown that some newly diagnosed people living with HIV are highly overwhelmed and traumatized by the HIV diagnosis making adherence to ART in the first few months of HIV diagnosis challenging [21].

A previous study in Rwanda found that frequent clinic appointments to pick up drugs is difficult because of transportation costs, long waiting times and stigma; therefore, adoption of DSDM was thought to minimize these structural barriers [22]. Since 2017, Rwanda has adopted DSDM with reportable success in the number of people living with HIV who initiate ART immediately following HIV diagnosis without affecting retention [23]. Despite this success, it is not known whether DSDM may have an impact on LLV, which is a known risk factor non-viral load suppression, development of drug resistance and treatment failure. In this analysis, we aimed to evaluate the incidence of LLV at 6, 12 and 18 months of follow-up among people living with HIV receiving treatment from twenty-eight healthcare facilities in Rwanda before and after the introduction of DSDM.

Methods

Study design and population

This was a retrospective cohort study that used routinely collected data of people living with HIV from twenty-eight healthcare facilities in Rwanda. Rwanda’s healthcare delivery system is categorized as primary, secondary, and tertiary. Primary healthcare facilities are comprised of Health Post/Dispensaries, and Health Centers, secondary health facilities are District Hospitals while tertiary health facilties are comprised of National Referral and Univeristy Teaching Hospitals. Administratively, all twenty-eight healthcare facilities belong to the same primary health level of care. A validated chart abstraction tool (for adults) used by the AIDS Relief Project to evaluate patient-level outcomes [24] was adapted and used to collect patient demographics and clinical information, including viral load, CD4 count, compliance to appointments and adherence to ART. The data consisted of two cohorts of adult (≥ 18 years or older) people living with HIV who initiated ART from these facilities and were followed for 24 months. The first cohort (n = 514) consisted of adults living with HIV who initiated treatment between January and April 2014 (prior to the rollout of DSDM) and the second cohort (n = 463) involved people living with HIV who initiated treatment between January and April 2017 (after the rollout of DSDM). Under DSDM PLHIV initiated ART regardless of their CD4 count within seven days of HIV diagnosis, without an extended counseling period. In addition, upon attaining sustained viral load suppression (two consecutive viral load suppressions), PLHIV had opportunity for up to six month drug refills.

Definition of variables

The main outcome of interest was LLV defined per WHO guidelines as people living with HIV with viral load of 51–999 copies/mL. People living with HIV who had viral load of ≤ 50 copies/mL were considered fully suppressed. The main predictor variable was DSDM categorized to people living with HIV who initiated ART before and after the rollout of DSDM. Other variables evaluated included age (18–24, 25–34, 35–44, 45–54, ≥ 55), sex (male, female), disclosure of HIV status (disclosed, did not disclose), baseline WHO staging (I, II, III and IV). HIV disclosure was defined as sharing one’s HIV diagnosis to a partner, peer educator, friend or any family member). Self-reported adherence was measured based on the 30-day recall. Facilities assessed adherence in the past 30-days based on the prescription given during the past clinic vist. It was calculated as the proportion of pills taken out of the number prescribed within 30 days and categorized as optimal if adherence was ≥ 90% or suboptimal if adherence was < 90%. Baseline CD4 cell count was measured during the first clinic visit following HIV diagnosis. Those with CD4 count < 200 cells/mm3 were considered to have advanced HIV disease and those with CD4 count ≥ 200 cells/mm3 were considered not to have advanced HIV disease. Six-, 12- and 18-month viral load data was categorized as ≤ 50, 51–999 and ≥ 1000 copies/mL. Participants with a viral load of < 1,000copies/mL were considered virally suppressed.

Statistical analysis

Frequencies and proportions of categorical variables and median and interquartile range (IQR) for continuous variables were presented. We compared categorical participant characteristics by the status of DSDM using the Chi-square or Fisher’s exact tests where appropriate. Independent t-tests were used to compare continuous variables. For the association between DSDM and LLV, all participants with viral load > 1,000 copies/mL were excluded from the analysis. To assess the effect of DSDM on LLV, log binomial regression models were used to compute risk ratios (RRs) and 95% confidence intervals (CIs). First, bivariate log binomial regression models were fit. Then, all variables that were significantly associated with LLV on bivariate analysis along with factors that had a p-value of < 0.20 were included in the final multivariable models. The study participants were clustered within healthcare facilities; the latter were considered as clusters and random effects models were used to account for clustering in both bivariate and multivariable analysis. Complete case analysis was conducted initially. To account for missing data in the covariates, we conducted five multiple imputations assuming a missing at random mechanism. DSDM, age, sex, education, disclosure of HIV status, adherence, and baseline CD4 count were included in the imputation model as predictors. Each imputed dataset was analyzed using log binomial regression models, and the final estimates were pooled according to Rubin’s Rules [25]. Imputed data results were compared to those obtained under compete case analysis. All associations were presented as RR, adjusted odds ratio (aRR) and 95% CIs. Statistical analyses were conducted using SAS version 9.4 (SAS Institute Inc., Cary, NC).

Ethical consideration

The Rwanda National Ethics Committee approved this study. IRB # 00001497 of IORG0001100.

Results

A total of 976 people living with HIV were included in this analysis of whom, 462 (47.3%) initiated treatment after the rollout of DSDM (Table 1). The median age was 37 (IQR, 32–43) years. Nearly two-thirds, 645 (67.0%), were female, 429 (44.0%) did not have formal education and 587 (60. 1%) disclosed their HIV status. Three quarters of the participants, 739 (75.7%), were classified to have WHO stage one at baseline, 160 (16.4%) presented with advanced HIV disease and 618 (63.3%) self-reported adherence of ≥ 90%. LLV at 6, 12 and 18 months were 52 (7.3%), 44 (6.5%) and 22 (5.4%), respectively. Viral load suppression at 6, 12 and 18 months was 91.9%, 92.7% and 95.8%, respectively. Stratified analysis of participant characteristics by the model of care showed that, there was heterogeneity in the distribution of age, level of education and six monthx viral load results between the two groups. All other characteristics were comparable.

Table 1 Participant characteristics
Full size table
Table 2 Factors associated with low-level viremia at 6, 12 and 18 months among people living with HIV in Rwanda: Bivariate analysis
Full size table

Factors associated with LLV, complete case analysis and multiple imputation

Tables 2 and 3, respectively, present bivariate and multivariable factors associated with LLV under complete case analysis and after multiple imputation of missing covariate data. Overall, the effect sizes were similar in terms of magnitude and direction; however, the effect sizes under complete case analysis were characterized by wider 95% CIs due to missing data for certain covariates.

Table 3 Factors associated with low-level viremia at 6, 12 and 18 months among people living with HIV in Rwanda: multivariable analysis
Full size table

For the bivariate complete case analysis, compared to participants who initiated ART before the introduction of DSDM, those who initiated after the introduction of DSDM had statistically significant higher risk of having LLV at 6 months [RR = 2.8; 95% CI(1.15–6.91)] but not at 12 [RR = 2.3; 95%CI (0.93–5.75)] or 18 months [RR = 0.3; 95%CI (0.09–1.20)] (Table 2). Men had higher risk of having LLV at 6 months [OR = 1.8; 95% CI (1.06–2.95)]. Similar results were noted in the multivariable analysis under complete case analysis.

In the bivariate analysis using imputed datasets, the risk of having LLV at 6 months among participants who initiated treatment under DSDM was twice that of participants who initiated ART before DSDM. In the multivariable analysis, compared to participants who initiated ART before the introduction of DSDM, those who initiated after the introduction of DSDM had statistically significant higher risk of having LLV at 6 months [aRR = 2.1; 95% CI(1.11–4.12)] but not at 12 [aRR = 1.5; 95% CI(0.77–3.03)] or 18 months [aRR = 0.4; 95% CI(0.14–1.06)] (Table 3). Participants who self-reported adherence of ≥ 90% at 6 months had 60% lower risk of having LLV compared to those who self-reported adherence of < 90%.

Discussion

In this cohort of PLHIV receiving ART in Rwanda, LLV was 7.3%, 6.5% and 5.4% at 6, 12 and 18 months, respectively. Prevalence of LLV from this study is similar to the ones reported from other neighboring east African countries, 8% in Uganda [26] and 9% in Tanzania [27]. Those who initiated ART during DSDM had higher risk of having LLV at 6 months compared to those who initiated prior to the introduction of DSDM. Initiation of ART during DSDM was not associated with risk of having LLV at 12 and 18 months of follow-up. The risk of having LLV was consistently higher among men than women at 6 and 18 months of follow-up.

It is a well-established fact that adherence to ART is key to achieving viral load suppression, and counselling on the importance of taking medication as prescribed is critical to achieving desirable benefits of HIV treatment. Historically, people living with HIV initiated ART based on CD4 count [28]. During these periods of serial CD4 count assessments, people received counselling about HIV for an extended period to prepare to initiate lifelong treatment. These moments benefited people living with HIV in understanding and accepting their illness, which in turn reduced internalized perceived stigma and improved medication adherence [21, 29]. Although early ART initiation as recommended under DSDM reduces time to viral load suppression, absence of extended periods of counselling may explain higher risk of having LLV among people living with HIV who initiated treatment during DSDM compared to the period prior to the introduction of DSDM. HIV programs should consider continuing with extended periods of counselling, particularly during the first 3–6 months of ART initiation, educating people living with HIV on the importance of treatment and adherence.

We found that men had higher risk of having LLV at 6 and 18 months of follow-up compared to women. This finding is inconsistent with others who did not show differences in the risk of having LLV and gender [30, 31]. Although men are more likely to be affected by HIV stigma and, hence, low levels of drug adherence compared to women [32, 33], the prevalence of optimal adherence in this study for men and women was comparable, with 71% and 72% of men and women, respectively, having optimal adherence. Further data triangulation revealed that 50% of men and 45% of women initiated treatment after the introduction of DSDM. As previously described, those who initiated ART after the introduction of DSDM had higher risk of developing LLV; therefore, the association between gender and LLV could partly be explained by time of ART initiation in addition to gender. Studies have found low baseline CD4 count to be associated with higher risk of LLV [30, 34, 35]; however, we did not find a statistically significant difference in this association. The lack of association could be due to missing values with 16% of our study participants missing baseline CD4 count.

Limitations of this analysis include missing data on some of the important covariates, such as baseline CD4 count. For example, among clients who initiated treatment before DSDM who had viral load results at 6-months, 95% and 59% had viral load results at 12 and 18 months compared to 90% and 55% for those who initiated treatment after DSDM. The missingness of data could be differential between the two groups. Despite the presence of missing data, our results from complete case analysis and imputed datasets consistently showed that initiation of ART during DSDM of care was associated with increased risk of developing LLV at 6 months. Understanding the deficiencies of self-reported adherence and we did not consistently show the association between optimal adherence and LLV.

Conclusion

Although viral load suppression was high in this cohort, DSDM was associated with increased risk of LLV at 6 month of follow up, possibly due to the minimal amount of time people living with HIV had in pondering and accepting the HIV diagnosis as well as the lack of knowledge on the importance of adherence, which was usually reiterated multiple times during extended periods of counselling. A patient-centered interventional approach is needed for newly diagnosed people living with HIV who have difficulties adhering to their treatment to achieve the 95-95-95 goals and reach the target of ending the HIV epidemic. In this era of immediate ART initiation following HIV diagnosis, continued support is paramount to prevent development of LLV which is known to negatively impact virologic suppression. We thefore further recommend counseling sessions that used to be provided prior to the introduction of DSDM to simultaneously be continued as clients initiate treatment. Furthermore, monthly intensive check in to understand any barriers of treatment adherence during the first 6 months of ART initiations will be critical. Barrier analysis has shown to improve retention in care among people living with HIV [36].

Data availability

Access to study data is limited to study team members as per human research ethics committee approval.

References

  1. UNAIDS. UNAIDS global aids update. The path that ends aids 2023 [https://thepath.unaids.org/wp-content/themes/unaids2023/assets/files/2023_report.pdf

  2. Lifson AR, Grund B, Gardner EM, Kaplan R, Denning E, Engen N, et al. Improved quality of life with immediate versus deferred initiation of antiretroviral therapy in early asymptomatic HIV infection. Aids. 2017;31(7):953–63.

    Article  PubMed  Google Scholar 

  3. Berner K, Louw QA. Factors affecting quality of life in adults with HIV: a local cross-sectional study. S Afr J Physiother. 2023;79(1):1921.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Franke MF, Kaigamba F, Socci AR, Hakizamungu M, Patel A, Bagiruwigize E, et al. Improved retention associated with community-based accompaniment for antiretroviral therapy delivery in rural Rwanda. Clin Infect Dis. 2013;56(9):1319–26.

    Article  CAS  PubMed  Google Scholar 

  5. Memiah P, Tlale J, Shimabale M, Nzyoka S, Komba P, Sebeza J, et al. Continuous quality improvement (CQI) institutionalization to reach 95:95:95 HIV targets: a multicountry experience from the Global South. BMC Health Serv Res. 2021;21(1):711.

    Article  PubMed  PubMed Central  Google Scholar 

  6. WHO Guidelines Approved by the Guidelines Review Committee. Consolidated guidelines on HIV prevention, testing, treatment, service delivery and monitoring: recommendations for a public health approach. Geneva: World Health Organization © World Health Organization 2021.; 2021.

  7. Musengimana G, Tuyishime E, Kiromera A, Malamba SS, Mulindabigwi A, Habimana MR, et al. Acquired HIV drug resistance among adults living with HIV receiving first-line antiretroviral therapy in Rwanda: a cross-sectional nationally representative survey. Antivir Ther. 2022;27(3):13596535221102690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Mesele M, Asmare G, Ambaw G, Asmamaw M, Abdu M, Chekol E et al. Correlates of ART attrition among adults under antiretroviral therapy in Southern Ethiopia, retrospective cohort study. AIDS Care. 2023:1–8.

  9. Aoko A, Pals S, Ngugi T, Katiku E, Joseph R, Basiye F, et al. Retrospective longitudinal analysis of low-level viremia among HIV-1 infected adults on antiretroviral therapy in Kenya. EClinicalMedicine. 2023;63:102166.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hermans LE, Moorhouse M, Carmona S, Grobbee DE, Hofstra LM, Richman DD, et al. Effect of HIV-1 low-level viraemia during antiretroviral therapy on treatment outcomes in WHO-guided South African treatment programmes: a multicentre cohort study. Lancet Infect Dis. 2018;18(2):188–97.

    Article  PubMed  Google Scholar 

  11. Nzivo MM, Waruhiu CN, Kang’ethe JM, Budambula NLM. HIV virologic failure among patients with persistent low-level viremia in Nairobi, Kenya: it is time to review the > 1000 virologic failure threshold. Biomed Res Int. 2023;2023:8961372.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Taiwo B, Gallien S, Aga E, Ribaudo H, Haubrich R, Kuritzkes DR, et al. Antiretroviral drug resistance in HIV-1-infected patients experiencing persistent low-level viremia during first-line therapy. J Infect Dis. 2011;204(4):515–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ryscavage P, Kelly S, Li JZ, Harrigan PR, Taiwo B. Significance and clinical management of persistent low-level viremia and very-low-level viremia in HIV-1-infected patients. Antimicrob Agents Chemother. 2014;58(7):3585–98.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Esber A, Polyak C, Kiweewa F, Maswai J, Owuoth J, Maganga L, et al. Persistent low-level viremia predicts subsequent virologic failure: is it time to change the third 90? Clin Infect Dis. 2019;69(5):805–12.

    Article  PubMed  Google Scholar 

  15. World Health Organization. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection: recommendations for a public health approach. World Health Organization; 2016.

  16. Long L, Kuchukhidze S, Pascoe S, Nichols BE, Fox MP, Cele R, et al. Retention in care and viral suppression in differentiated service delivery models for HIV treatment delivery in sub-saharan Africa: a rapid systematic review. J Int AIDS Soc. 2020;23(11):e25640.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Pilcher CD, Ospina-Norvell C, Dasgupta A, Jones D, Hartogensis W, Torres S, et al. The effect of same-day observed initiation of antiretroviral therapy on HIV viral load and treatment outcomes in a US public health setting. J Acquir Immune Defic Syndr. 2017;74(1):44–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Koenig SP, Dorvil N, Dévieux JG, Hedt-Gauthier BL, Riviere C, Faustin M, et al. Same-day HIV testing with initiation of antiretroviral therapy versus standard care for persons living with HIV: a randomized unblinded trial. PLoS Med. 2017;14(7):e1002357.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Labhardt ND, Ringera I, Lejone TI, Klimkait T, Muhairwe J, Amstutz A, et al. Effect of offering same-day ART vs usual health facility referral during home-based HIV testing on linkage to care and viral suppression among adults with HIV in Lesotho: the CASCADE randomized clinical trial. JAMA. 2018;319(11):1103–12.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bakari HM, Alo O, Mbwana MS, Salim SM, Ludeman E, Lascko T et al. Same-day ART initiation, loss to follow-up and viral load suppression among people living with HIV in low-and middle-income countries: systematic review and meta-analysis.

  21. Ross J, Ingabire C, Umwiza F, Gasana J, Munyaneza A, Murenzi G, et al. How early is too early? Challenges in ART initiation and engaging in HIV care under treat all in Rwanda-A qualitative study. PLoS ONE. 2021;16(5):e0251645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ingabire C, Umwiza F, Gasana J. It’sa big problem to take that pill before you feel ready: ART initiation challenges under treat all in rwanda. oral presentation, international conference on AIDS and STDs in Africa. Kigali, Rwanda. 2019.

  23. Ross J, Sinayobye JD, Yotebieng M, Hoover DR, Shi Q, Ribakare M, et al. Early outcomes after implementation of treat all in Rwanda: an interrupted time series study. J Int AIDS Soc. 2019;22(4):e25279.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Riedel DJ, Stafford KA, Memiah P, Coker M, Baribwira C, Sebeza J, et al. Patient-level outcomes and virologic suppression rates in HIV-infected patients receiving antiretroviral therapy in Rwanda. Int J STD AIDS. 2018;29(9):861–72.

    Article  PubMed  Google Scholar 

  25. Liublinska V, Rubin DB. Sensitivity analysis for a partially missing binary outcome in a two-arm randomized clinical trial. Stat Med. 2014;33(24):4170–85.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nanyeenya N, Chang LW, Kiwanuka N, Nasuuna E, Nakanjako D, Nakigozi G, et al. The association between low-level viraemia and subsequent viral non-suppression among people living with HIV/AIDS on antiretroviral therapy in Uganda. PLoS ONE. 2023;18(1):e0279479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mnzava D, Okuma J, Ndege R, Kimera N, Ntamatungiro A, Nyuri A, et al. Decentralization of viral load testing to improve HIV care and treatment cascade in rural Tanzania: observational study from the Kilombero and Ulanga antiretroviral cohort. BMC Infect Dis. 2023;23(1):222.

    Article  PubMed  PubMed Central  Google Scholar 

  28. WHO. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection. recommendations for a public health approach 2013 [https://iris.who.int/bitstream/handle/10665/85321/9789241505727_eng.pdf?sequence=1

  29. Katz IT, Ryu AE, Onuegbu AG, Psaros C, Weiser SD, Bangsberg DR, et al. Impact of HIV-related stigma on treatment adherence: systematic review and meta-synthesis. J Int AIDS Soc. 2013;16(3 Suppl 2):18640.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ortíz DW, Roberts-Sano O, Marroquin HE, Larson L, Franco KB, Spec A, et al. Factors associated with viremia in people living with HIV on antiretroviral therapy in Guatemala. AIDS Res Ther. 2021;18(1):79.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Hsu JY, Sun HY, Hsieh TW, Chang SY, Chuang YC, Huang YS, et al. Incidence of low-level viremia and its impact on virologic failure among people living with HIV-1 who switched to elvitegravir-based antiretroviral therapy. J Glob Antimicrob Resist. 2022;29:7–16.

    Article  CAS  PubMed  Google Scholar 

  32. Shamos S, Hartwig KA, Zindela N. Men’s and women’s experiences with HIV and stigma in Swaziland. Qual Health Res. 2009;19(12):1678–89.

    Article  PubMed  Google Scholar 

  33. Yebei VN, Fortenberry J, Ayuku DO. Felt stigma among people living with HIV/AIDS in rural and urban Kenya. Afr Health Sci. 2008;8(2).

  34. Bai R, Lv S, Hua W, Su B, Wang S, Shao Y, et al. Factors associated with human immunodeficiency virus-1 low-level viremia and its impact on virological and immunological outcomes: a retrospective cohort study in Beijing, China. HIV Med. 2022;23(Suppl 1):72–83.

    Article  CAS  PubMed  Google Scholar 

  35. Brattgård H, Björkman P, Nowak P, Treutiger CJ, Gisslén M, Elvstam O. Factors associated with low-level viraemia in people with HIV starting antiretroviral therapy: a Swedish observational study. PLoS ONE. 2022;17(5):e0268540.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Violet Makokha HOR, Caroline Ngeno E, Amadi D, Wandina A, Ndaga R, Onkware E, Owino E, Katiku. Paul Musingila, Emily Koech. Structured support through a return to care package to reduce lost to follow-up among patients on antiretroviral therapy in rural western Kenya. AIDS. 2020:6–10, July 2020.

Download references

Acknowledgements

We would like to acknowledge the support from health facilities as well as the data collectors.

Funding

None declared.

Author information

Authors and Affiliations

  1. College of Medicine and Health Sciences, School of Public Health, University of Rwanda, Street Name: KG 11 Ave Gasabo Kigali, P.O. Box 3286, Kigali, Rwanda

    Jackson Sebeza

  2. Primary Health Care Institute, Iringa, Tanzania

    Jackson Sebeza & Mariam. S. Mbwana

  3. Institute of Human Virology, University of Maryland School of Medicine, Baltimore, USA

    Habib. O. Ramadhani & Taylor Lascko

  4. District Hospital, Tanga, Tanzania

    Zuhura M. Ally

  5. Graduate school, University of Maryland, Baltimore, USA

    Peter Memiah

  6. Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda

    Simeon Tuyishime & Galican Rwibasira

Authors
  1. Jackson Sebeza
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Mariam. S. Mbwana
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Habib. O. Ramadhani
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Zuhura M. Ally
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Taylor Lascko
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Peter Memiah
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Simeon Tuyishime
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Galican Rwibasira
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

J.S. formulated the research question, provided general oversight of this work, authored the first draft of the manuscript. H.O.R., conducted data analysis, interpreted results. M.S.M. and Z.A. M. oversaw data collection process, interpreted results, reviewed several versions of the manuscripts. T.L., P.M. and S.T., contributed to the interpretation of results, cross checked primary data analysis and reviewed several versions of the manuscripts. G.R. contributed to study design, assisted in the interpretation of results, and provided general oversight of this work. All authors reviewed this manuscript.

Corresponding author

Correspondence to Jackson Sebeza.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sebeza, J., Mbwana, M.S., Ramadhani, H.O. et al. Association between differentiated HIV care delivery model and low-level viremia among people living with HIV in Rwanda. AIDS Res Ther 21, 79 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12981-024-00650-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12981-024-00650-3

Keywords

AIDS Research and Therapy

ISSN: 1742-6405

Contact us