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      Uptake, Accuracy, Safety, and Linkage into Care over Two Years of Promoting Annual Self-Testing for HIV in Blantyre, Malawi: A Community-Based Prospective Study

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          Abstract

          Background

          Home-based HIV testing and counselling (HTC) achieves high uptake, but is difficult and expensive to implement and sustain. We investigated a novel alternative based on HIV self-testing (HIVST). The aim was to evaluate the uptake of testing, accuracy, linkage into care, and health outcomes when highly convenient and flexible but supported access to HIVST kits was provided to a well-defined and closely monitored population.

          Methods and Findings

          Following enumeration of 14 neighbourhoods in urban Blantyre, Malawi, trained resident volunteer-counsellors offered oral HIVST kits (OraQuick ADVANCE Rapid HIV-1/2 Antibody Test) to adult (≥16 y old) residents ( n = 16,660) and reported community events, with all deaths investigated by verbal autopsy. Written and demonstrated instructions, pre- and post-test counselling, and facilitated HIV care assessment were provided, with a request to return kits and a self-completed questionnaire. Accuracy, residency, and a study-imposed requirement to limit HIVST to one test per year were monitored by home visits in a systematic quality assurance (QA) sample.

          Overall, 14,004 (crude uptake 83.8%, revised to 76.5% to account for population turnover) residents self-tested during months 1–12, with adolescents (16–19 y) most likely to test. 10,614/14,004 (75.8%) participants shared results with volunteer-counsellors. Of 1,257 (11.8%) HIV-positive participants, 26.0% were already on antiretroviral therapy, and 524 (linkage 56.3%) newly accessed care with a median CD4 count of 250 cells/μl (interquartile range 159–426). HIVST uptake in months 13–24 was more rapid (70.9% uptake by 6 mo), with fewer (7.3%, 95% CI 6.8%–7.8%) positive participants. Being “forced to test”, usually by a main partner, was reported by 2.9% (95% CI 2.6%–3.2%) of 10,017 questionnaire respondents in months 1–12, but satisfaction with HIVST (94.4%) remained high. No HIVST-related partner violence or suicides were reported. HIVST and repeat HTC results agreed in 1,639/1,649 systematically selected (1 in 20) QA participants (99.4%), giving a sensitivity of 93.6% (95% CI 88.2%–97.0%) and a specificity of 99.9% (95% CI 99.6%–100%). Key limitations included use of aggregate data to report uptake of HIVST and being unable to adjust for population turnover.

          Conclusions

          Community-based HIVST achieved high coverage in two successive years and was safe, accurate, and acceptable. Proactive HIVST strategies, supported and monitored by communities, could substantially complement existing approaches to providing early HIV diagnosis and periodic repeat testing to adolescents and adults in high-HIV settings.

          Abstract

          In a prospective study, Augustine Choko and colleagues assess uptake, accuracy, and outcomes of implementation of community-wide HIV self-testing delivered and supported by resident community volunteers in 14 neighborhoods of Blantyre, Malawi.

          Editors' Summary

          Background

          Every year, about 2.1 million people (70% of whom live in sub-Saharan Africa) are newly infected with HIV, the virus that causes AIDS, and 1.5 million people (again, mainly in sub-Saharan Africa) die as a result. HIV, which is usually transmitted through unprotected sex with an infected individual, gradually destroys CD4 lymphocytes and other immune system cells, leaving HIV-positive individuals susceptible to other serious infections and to unusual cancers. HIV is diagnosed by looking for antibodies to HIV in blood or saliva. After diagnosis, the progression of HIV infection is monitored by regularly counting the number of CD4 cells in the blood. Initiation of antiretroviral therapy—a combination of drugs that keeps HIV replication in check but that does not cure the infection—is recommended when an individual’s CD4 count falls below 500 cells/μl or when he or she develops an AIDS-defining condition.

          Why Was This Study Done?

          HIV-positive individuals need to know their status so that they can take steps to avoid transmitting the virus to other people (for example, by always using a condom during sexual intercourse) and so that they can begin treatment. Treatment helps to keep HIV-positive individuals healthy but also reduces their chances of transmitting the virus to their sexual partners. Unfortunately, many HIV-positive individuals are unaware of their status. The situation is particularly bad in sub-Saharan Africa, where, despite major investments in facility-based and community-based HIV testing and counseling (HTC) programs, only a quarter of adults have had a recent HIV test, and only half of the people living with HIV know they are HIV positive. Barriers to facility-based HTC include concern about lack of confidentiality and fears of stigmatization. Home-based HTC avoids some of these barriers and can achieve high uptake of testing, but doubts have been expressed about the sustainability of this approach to testing. Here, the researchers evaluate an alternative to home-based HTC—HIV self-testing (HIVST)—by undertaking a community-based prospective study of HIVST in Blantyre, Malawi. HIVST involves individuals performing and interpreting their own HIV test and has the potential to be widely implemented with minimal involvement of trained healthcare workers.

          What Did the Researchers Do and Find?

          Trained resident volunteer-counselors offered one oral HIVST kit (a kit that measures HIV in saliva) per year for a two-year period to 16,660 adult residents in 14 neighborhoods in urban Blantyre. All the participants received instructions on how to use the kits, pre- and post-counseling, and, for participants self-testing HIV positive, a referral card to attend an HIV care clinic. The residents also completed a questionnaire about their experience of HIVST. Three-quarters of the residents self-tested in the first and second year of the study. HIVST uptake was more rapid in the second year than in the first year and was high among men and adolescents, two hard-to-reach populations. Three-quarters of the residents who self-tested during the first year of the study shared their results with a volunteer-counselor. Of the 1,257 participants who discovered they were HIV positive during the first year of the study, more than half accessed HIV care. Importantly, 94.4% of the participants reported that they were happy with HIVST even though 2.9% reported being forced to take the test, usually by a main partner; no HIVST-related partner violence or suicides were reported by the study’s community surveillance system. Finally, HIVST and repeat HTC results agreed in 99.4% of participants selected as a quality assurance sample (one in 20 of the participants).

          What Do These Findings Mean?

          These findings show that, in urban neighborhoods in Malawi, coverage with community-based HIVST was high (particularly among adolescents and men) in two successive years and that HIVST was safe, accurate, and acceptable. Importantly, HIVST using a delivery model based on trained volunteers led to acceptable linkage into HIV care services, and the approach had a very low incidence of major social harms such as partner violence. Uncertainty about estimates of uptake and linkage to care and other aspects of the study design may limit the accuracy of these results. Nevertheless, these findings suggest that scaling up HIVST could complement existing strategies for providing early HIV diagnosis and periodic repeat testing and could thus have a sustained impact on the coverage of HIV testing and care in Africa and on the control of the HIV/AIDS epidemic.

          Additional Information

          This list of resources contains links that can be accessed when viewing the PDF on a device or via the online version of the article at http://dx.doi.org/10.1371/journal.pmed.1001873.

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          What is community? An evidence-based definition for participatory public health.

          E McLellan, Phyllis Strauss, Jeffrey L. Blanchard … (2001)
          Increased emphasis on community collaboration indicates the need for consensus regarding the definition of community within public health. This study examined whether members of diverse US communities described community in similar ways. To identify strategies to support community collaboration in HIV vaccine trials, qualitative interviews were conducted with 25 African Americans in Durham, NC; 26 gay men in San Francisco, Calif; 25 injection drug users in Philadelphia, Pa; and 42 HIV vaccine researchers across the United States. Verbatim responses to the question "What does the word community mean to you?" were analyzed. Cluster analysis was used to identify similarities in the way community was described. A common definition of community emerged as a group of people with diverse characteristics who are linked by social ties, share common perspectives, and engage in joint action in geographical locations or settings. The participants differed in the emphasis they placed on particular elements of the definition. Community was defined similarly but experienced differently by people with diverse backgrounds. These results parallel similar social science findings and confirm the viability of a common definition for participatory public health.
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            Prognosis of patients with HIV-1 infection starting antiretroviral therapy in sub-Saharan Africa: a collaborative analysis of scale-up programmes.

            Landon Myer, Olivia Keiser, Sam Phiri … (2010)
            Prognostic models have been developed for patients infected with HIV-1 who start combination antiretroviral therapy (ART) in high-income countries, but not for patients in sub-Saharan Africa. We developed two prognostic models to estimate the probability of death in patients starting ART in sub-Saharan Africa. We analysed data for adult patients who started ART in four scale-up programmes in Côte d'Ivoire, South Africa, and Malawi from 2004 to 2007. Patients lost to follow-up in the first year were excluded. We used Weibull survival models to construct two prognostic models: one with CD4 cell count, clinical stage, bodyweight, age, and sex (CD4 count model); and one that replaced CD4 cell count with total lymphocyte count and severity of anaemia (total lymphocyte and haemoglobin model), because CD4 cell count is not routinely measured in many African ART programmes. Death from all causes in the first year of ART was the primary outcome. 912 (8.2%) of 11 153 patients died in the first year of ART. 822 patients were lost to follow-up and not included in the main analysis; 10 331 patients were analysed. Mortality was strongly associated with high baseline CD4 cell count (>/=200 cells per muL vs /=60 kg vs <45 kg; 0.23, 0.18-0.30), and anaemia status (none vs severe: 0.27, 0.20-0.36). Other independent risk factors for mortality were low total lymphocyte count, advanced age, and male sex. Probability of death at 1 year ranged from 0.9% (95% CI 0.6-1.4) to 52.5% (43.8-61.7) with the CD4 model, and from 0.9% (0.5-1.4) to 59.6% (48.2-71.4) with the total lymphocyte and haemoglobin model. Both models accurately predict early mortality in patients starting ART in sub-Saharan Africa compared with observed data. Prognostic models should be used to counsel patients, plan health services, and predict outcomes for patients with HIV-1 infection in sub-Saharan Africa. US National Institute of Allergy And Infectious Diseases, Eunice Kennedy Shriver National Institute of Child Health and Human Development, and National Cancer Institute. Copyright 2010 Elsevier Ltd. All rights reserved.
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              Routine HIV Testing in Botswana: A Population-Based Study on Attitudes, Practices, and Human Rights Concerns

              Sheri D Weiser, Michele Heisler, Karen Leiter … (2006)
              Introduction There has been widespread concern about the slow uptake of voluntary counseling and testing (VCT) in many parts of sub-Saharan Africa [ 1, 2]. VCT is a cornerstone of cost-effective HIV prevention and linkage to expanding HIV treatment in low-resource settings [ 3, 4]. Some of the most significant barriers to HIV testing identified in sub-Saharan Africa include lack of access to VCT and to high quality clinical services, lack of access to antiretroviral (ARV) therapy, and HIV-related stigma [ 1, 5, 6]. With a seroprevalence of 37% of adults ages 15–49 [ 7, 8], Botswana established universal access to antiretroviral treatment (ART) beginning in 2002 for all patients with CD4 counts less than 200 or with an AIDS-defining illness [ 9– 11]. By January 2004, however, only 17,500 patients were enrolled in the Botswana National Treatment Program out of an estimated 110,000 eligible individuals [ 9]. Slow enrollment in HIV treatment was thought to be due in part to underutilization of HIV testing [ 9, 11, 12]; by mid-2003, only 70,000 tests in total had been performed in Botswana out of a population of 1.7 million [ 13]. HIV stigma was identified by government and press sources as one possible impediment to HIV testing and hence to the success of the new ART program, in that individuals may avoid testing and treatment facilities to avoid potential stigma and discrimination [ 8, 11, 13]. We previously reported that social stigma and fear of positive test results significantly delayed testing among a group of patients treated in the private sector in 2000 [ 14]. In an attempt to increase the uptake of HIV testing and ART, the Botswana government introduced the policy of routine HIV testing in early 2004, whereby nearly all patients would be tested as a routine part of medical visits unless they explicitly refused [ 13, 15]. While this approach to testing is provider-initiated, all patients should receive essential information about HIV testing and be informed of their right to refuse. In addition, there is typically greater emphasis on post-test compared with pre-test counseling [ 16]. Studies in resource-rich settings have shown that routine HIV testing can be cost-effective and life-saving, both by increasing the life expectancy of individuals with HIV and by reducing the annual HIV transmission rate [ 17– 21]. In June 2004, as part of a change in testing policy recommendations, UNAIDS and the World Health Organization recommended the routine offer of HIV testing by healthcare providers in a wide range of clinical encounters based in part on the Botswana experience [ 22, 23]. The goal of routine testing is to increase the proportion of individuals aware of their status, and thereby reduce “HIV exceptionalism,” lessen HIV-related stigma, and provide more people access to life-saving therapy [ 16, 24]. While provider-initiated approaches to testing are gaining popularity, there have been concerns that routine testing policies are potentially coercive, that counseling will no longer be practiced, that people may be dissuaded from visiting their doctors for fear of being tested, and that this policy may increase testing-related partner violence [ 15, 25– 27]. As routine testing is increasingly being recommended as an option in other countries [ 17, 18, 28– 30], it is important to improve our understanding of the consequences and specific human rights concerns associated with implementation of this policy in Botswana. We therefore assessed: 1) knowledge of and attitudes toward routine testing in Botswana with a focus on human rights concerns associated with this policy; 2) factors associated with whether respondents had heard of routine testing, and with positive attitudes toward this policy; and 3) the prevalence and correlates of HIV testing, barriers and facilitators to testing, and reported experiences with testing 11 months after the introduction of routine testing in Botswana. Methods In November and December 2004, we conducted a cross-sectional study using structured survey instruments among a probability sample of 1,268 adults selected from the five districts of Botswana with the highest number of HIV-infected individuals. These districts included Gaborone, Kweneng East, Francistown, Serowe/Palapye, and Tutume, and cover a population of 725,000 out of a total population of 1.7 million individuals in Botswana. We used a stratified two-stage probability sample design for the selection of the population-based sample with the assistance of the Central Statistics Office at the Ministry of Finance and Development Planning in Botswana. In the first stage of sampling, 89 enumeration areas were selected with probability proportional to measures of size, where measures of size are the number of households in the enumeration area as defined by the 2001 Population and Housing Census. At the second stage of sampling, households were systematically selected in each enumeration area by trained field researchers under the guidance of field supervisors. With a target sample of 1,200 households, and 15% over-sampling for an anticipated 85% response rate, 1,433 households were selected. Within each household, random number tables were used to select one adult member who met our inclusion criteria, and up to two repeat visits were made. Participants were excluded if they were older than 49 or younger than 18 years old, if they had cognitive disabilities, or if there was inadequate privacy to conduct the interviews. The 45- to 60-minute survey was conducted in either English or Setswana in a private setting, and written consent was obtained from all study participants. Our structured survey instrument and consent forms were pilot-tested among 20 individuals from Gaborone, and then translated into Setswana and back-translated into English. All study procedures were approved by the Human Subjects Committee at the University of California San Francisco (San Francisco, California, United States), as well as by the Botswana Ministry of Health Research and Development Committee. Measures Domains of inquiry for our 234-item survey ( Protocol S1) included demographics, HIV knowledge, experiences with HIV testing, barriers and facilitators to HIV testing, attitudes toward routine testing, HIV risk behaviors, HIV-related stigma, depression, beliefs about gender roles and gender discrimination, and measures of healthcare access and utilization. Based on an extensive literature review [ 2, 6, 31– 37] and discussions with key informants, we developed a conceptual model that guided the selection of variables for our multivariate model for correlates of testing, as shown in Figure 1. Relevant variables are explained below. Knowledge of and attitudes toward routine testing. Participants were asked whether they had heard of routine testing and were given a detailed explanation of this policy (see Table 1). Participants then indicated the extent to which they are in favor of routine testing and whether they think this policy affects HIV-related stigma, barriers to testing, violence against women related to testing, and uptake of ARVs. From questions assessing attitudes toward routine testing ( Table 1), we constructed an ordinal outcome of positive attitudes toward this policy. Participants were categorized as having zero to one, two, three, or four positive views toward routine testing. (See Tables 1 and 2 for specific items.) HIV testing. Participants were asked whether they had ever been tested for HIV (by either VCT or routine testing). If so, they were asked detailed questions about their experiences with pre-test and post-test counseling, confidentiality, facilitators to testing, and personal repercussions of testing. If not, they were asked a series of questions related to barriers to testing adapted from the CDC HIV Testing Instrument, version 9.00, and about their intention to be tested within the next six months. HIV status was not asked in order to maximize response rate and hence the generalizability of the population-based sample. HIV-related stigma. Respondents were asked seven questions representing potential stigmatizing attitudes adapted from the UNAIDS general population survey and the Department of Health Services AIDS module, which have been used successfully in previous studies in Botswana [ 38]. Anyone who reported a discriminatory attitude on any of four principal questions was registered as having stigmatizing attitudes per the UNAIDS scoring system. Since participants may not always openly endorse stigmatizing views toward people living with HIV and AIDS (PLWA) due to social desirability bias, as an additional measure of stigma, we also asked individuals to project the type of responses they would anticipate from others if they were to test positive for HIV and divulge their status to others. We converted this information to a nine-item index on “projected HIV stigma” with higher scores associated with a greater number of reported adverse social consequences associated with testing positive. This index had high internal reliability with a Cronbach alpha of 0.77. HIV knowledge. Participants were asked 15 questions about their knowledge of HIV transmission and prevention, based on questions modified from the UNAIDS General Population Survey and the Department of Health Services AIDS module. Using the UNAIDS knowledge indicator scoring system, individuals were scored as having HIV knowledge if they correctly identified the two most common modes of HIV prevention in Botswana. Depression. As depression is known to impede access to care and to worsen HIV outcomes in Western settings, we included depression in our analysis [ 39– 41]. Symptoms of depression were measured using the 15-item Hopkins Symptom Checklist for Depression [ 42] which has been validated previously in locations in Africa and elsewhere [ 43]. Analysis We used standard procedures for data entry and quality control. All data were analyzed with S TATA statistical software. Outcomes of interest included: a) having heard of routine testing; b) number of positive attitudes toward routine testing (categorized as an ordinal variable consisting of the following categories: zero to one, two, three, and four positive statements about routine testing); c) self-reported HIV testing (by either VCT or routine testing); d) having been tested under routine testing; and e) planning to test within the next six months (among people who had not tested). The following covariates were included in our analyses: 1) age (continuous); 2) sex; 3) income (≥population mean,
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                Author and article information

                Contributors
                David R. Bangsberg: Role: Academic Editor
                Journal
                Journal ID (nlm-ta): PLoS Med
                Journal ID (iso-abbrev): PLoS Med
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosmed
                Title: PLoS Medicine
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Print): 1549-1277
                ISSN (Electronic): 1549-1676
                Publication date (Electronic): 8 September 2015
                Publication date Collection: September 2015
                Volume: 12
                Issue: 9
                Electronic Location Identifier: e1001873
                Affiliations
                [1 ]Malawi–Liverpool–Wellcome Trust Clinical Research Programme, Blantyre, Malawi
                [2 ]Department of Public Health and Policy, University of Liverpool, Liverpool, United Kingdom
                [3 ]Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                [4 ]London School of Hygiene & Tropical Medicine, London, United Kingdom
                [5 ]HIV Unit, Ministry of Health, Lilongwe, Malawi
                [6 ]Division of Health Sciences, Warwick Medical School, Coventry, United Kingdom
                Massachusetts General Hospital, Harvard Medical School, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ELC. Performed the experiments: ATC RS AM. Analyzed the data: ATC EW. Contributed reagents/materials/analysis tools: ELC. Wrote the first draft of the manuscript: ATC HM. Contributed to the writing of the manuscript: ATC PM EW BW HF RS AM SM ND RH HM EC. Enrolled patients: RS. Agree with the manuscript’s results and conclusions: ATC PM EW BW HF RS AM SM ND RH HM EC. All authors have read, and confirm that they meet, ICMJE criteria for authorship.

                Article
                Publisher ID: PMEDICINE-D-15-00605
                DOI: 10.1371/journal.pmed.1001873
                PMC ID: 4562710
                PubMed ID: 26348035
                SO-VID: 9fae8833-9fa6-4374-8e7c-4c1317f8691e
                Copyright statement: Copyright @ 2015
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                Date received : 26 February 2015
                Date accepted : 31 July 2015
                Page count
                Figures: 5, Tables: 4, Pages: 21
                Funding
                The study was funded as part of a Wellcome Trust Senior Research Fellowship in Clinical Science (grant number: WT091769) awarded to ELC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Custom metadata
                Data Availability Data are publicly available at 10.17037/DATA.7 through London School of Hygiene & Tropical Medicine Data Compass http://datacompass.lshtm.ac.uk/.

                ScienceOpen disciplines: Medicine
                Data availability:
                ScienceOpen disciplines: Medicine

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