JAIDS Journal of Acquired Immune Deficiency Syndromes:
“What Took You So Long?” The Impact of PEPFAR on the Expansion of HIV Testing and Counseling Services in Africa
Marum, Elizabeth MSW, PhD*; Taegtmeyer, Miriam BM, BCh, MRCP, PhD†; Parekh, Bharat PhD*; Mugo, Nelly MBChB, MMed, MPH‡; Lembariti, Salama RN§; Phiri, Mannasseh BSc, MBChB‖; Moore, Jan PhD*; Cheng, Alison S. MPH¶
*Division of Global HIV and AIDS, Center for Global Health, Centers for Disease Control and Prevention, Department of Health and Human Services, Lusaka, Zambia
†Clinical Research Group, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
‡Department of Obstetrics and Gynecology, Kenyatta National Hospital, Nairobi, Kenya
§Tanzania AIDS Prevention Project, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania
‖Society for Family Health, Lusaka, Zambia
¶United States Agency for International Development, Washington, DC.
Correspondence to: Elizabeth Marum, Centers for Disease Control and Prevention, Lusaka, Zambia (e-mail:firstname.lastname@example.org).
Various authors have professional relationships with PEPFAR (either as employees of PEPFAR-supported US Government Agencies or as grantees/contractors) as outlined in the Copyright Transfer Agreement Forms.
The authors have no other funding or conflicts of interest to disclose.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the US government, the World Health Organization, the US Agency for International Development, the US Centers for Disease Control and Prevention, or the Office of the Global AIDS Coordination, US Department of State.
Abstract: HIV testing and counseling services in Africa began in the early 1990s, with limited availability and coverage. Fears of stigma and discrimination, complex laboratory systems, and lack of available care and treatment services hampered expansion. Use of rapid point-of-care tests, introduction of services to prevent mother-to-child transmission, and increasing provision of antiretroviral drugs were key events in the late 1990s and early 2000s that facilitated the expansion of HIV testing and counseling services. Innovations in service delivery included providing HIV testing in both clinical and community sites, including mobile and home testing. Promotional campaigns were conducted in many countries, and evolutions in policies and guidance facilitated expansion and uptake. Support from President's Emergency Plan for AIDS Relief and national governments, other donors, and the Global Fund for AIDS, Tuberculosis, and Malaria contributed to significant increases in the numbers of persons tested in many countries. Quality of both testing and counseling, limited number of health care workers, uptake by couples, and effectiveness of linkages and referral systems remain challenges. Expansion of antiretroviral treatment, especially in light of the evidence that treatment contributes to prevention of transmission, will require greater yet strategic coverage of testing services, especially in clinical settings and in combination with other high-impact HIV prevention strategies. Continued support from President's Emergency Plan for AIDS Relief, governments, and other donors is required for the expansion of testing needed to achieve international targets for the scale-up of treatment and universal access to knowledge of HIV status.
The first voluntary and anonymous HIV testing program in Africa was established in 1990 in Kampala, Uganda, with considerable advance publicity. The first day of operations, only one man requested services, and after pretest counseling, declined testing. Despite such a tentative start, millions of persons globally have now received HIV testing and counseling (HTC) services. Community attitudes to HTC have also changed dramatically, prompting a Kenyan village chief to say to one of the authors during the early years of President's Emergency Plan for AIDS Relief (PEPFAR): What took you so long to come here to serve my people? In this article, we will describe the history of HIV testing and the processes that facilitated the rapid PEPFAR-supported expansion of HTC, including the evolution of policies and innovative service delivery models, costs, and future challenges.
HISTORY OF HIV TESTING
Due to fears of stigma and discrimination, the primary model adopted in Africa in the early 1990s was based on “alternative testing sites” established in the 1980s in the United States, where persons who avoided health care settings could be tested anonymously. The first Ugandan program was located in a business building, and “clients” were not asked their names or charged a fee.1 Similar voluntary counseling and testing (VCT) services were established in a number of countries including Zimbabwe, Zambia, Malawi, Kenya, and Tanzania.2 However, the fear of adverse outcomes, lack of perceived benefit in the absence of treatment, and waiting periods of a week or more for results hindered expansion.
Three major developments between 1998 and 2004 led to a sea change in HTC. First, the use of simple point-of-care rapid tests meant that same day results could be provided, not only in health facilities but also in community settings and in remote areas, with lay health workers conducting the tests.3 Second, the implementation of simplified antiretroviral (ARV) regimens to prevent mother-to-child transmission (PMTCT) in the late 1990s required a shift from the constraints of an “opt-in” or “client-initiated” approach to an opt-out provider-initiated approach, which resulted in significant increases in the numbers of women being tested. Third, the expansion of access to antiretroviral therapy (ART) meant health workers were motivated to offer HTC as they had treatment options to offer. In its first year, PEPFAR supported approximately 2 million testing sessions in 15 “focus countries” (13 countries in Africa; Guyana, and Vietnam).1 In fiscal year 2011, this had risen to over 40 million testing sessions (Figure 1). Over 125,000 counselors and health care workers were trained to provide HTC services between 2004 and 2010. Innovative models of service delivery rapidly expanded in health facilities and community settings.
EVOLUTION OF POLICY, GUIDANCE, AND PRACTICE
By 2004, guidelines in most countries emphasized anonymous client-initiated testing and a few included guidance for high-risk populations or testing as part of routine health care.5 Testing algorithms often required laboratory technicians, and in several countries, only nurses could provide counseling. The introduction of PEPFAR, and the World Health Organization's plan for 3 million people to be on treatment by 2005, known as the “3 by 5” plan,6 quickly led to the development of new national policies, and support from PEPFAR, other bilateral donors, and the Global Fund to Fight AIDS, Tuberculosis, and Malaria, and national governments financed the expansion of services. Testing in clinical settings became a standard of care. In 2007, WHO released international guidance, which acknowledged missed opportunities to diagnose HIV in clinical settings and articulated standards for provider-initiated testing and counseling.7 Of the 15 original PEPFAR focus countries, 12 currently have official provider-initiated testing and counseling policies.8,9 Other key policies and guidelines have been released to address special or vulnerable populations, including children, refugees, displaced persons, and others.10–14
In addition, many national HTC guidelines were modified to allow task shifting to lay counselors to conduct both counseling and rapid testing and to incorporate new approaches including mobile, outreach, and door-to-door testing.15 This shift was essential to the rapid scale-up of HTC in the face of chronic human resource shortages in the health sector.
New PEPFAR guidance for prevention of sexually transmitted HIV also clarifies the essential role of testing in combination prevention packages.16 This guidance identifies HTC as a prerequisite to high-impact synergistic prevention interventions including PMTCT, voluntary medical male circumcision, services for those at high risk, and access to treatment.
INNOVATIONS IN SERVICE DELIVERY
PEPFAR support has encouraged innovations in testing service delivery, based on successful pilot programs and research findings. These have included new models of outreach and an increasing emphasis on couple testing.
In the late 1990s, programs in Uganda began offering home testing to family members of patients enrolled in care, which proved to be well accepted and effective in identifying undiagnosed children and adults.17 Door-to-door home testing was soon targeting entire communities,18 and PEPFAR has since supported the expansion of door-to-door and home testing in 10 high-prevalence countries. PEPFAR along with other donors and national governments have also supported mass HTC campaigns: in Malawi in 2007, 186,631 persons were tested in a 1-week campaign (with 75% being “new testers”); the Ethiopia Millennium AIDS Campaign 2006 resulted in 705,619 testing sessions in 3 months (with a yield of 5.3% HIV+, approximately double the national prevalence),19 and Lesotho sponsored an intensive door-to-door campaign between 2006 and 2007, testing an estimated 320,000 persons.20 Programs in a range of settings were established targeting high-risk clients including sex workers, injection drug users, prisoners, refugees, transport workers, men who have sex with men, the deaf,21 and others. Because these clients are often marginalized, programs typically offer anonymous testing, out-of-hour services, and mobile venues. Tanzania has introduced mobile vans that offer HTC for high-risk groups in Dar es Salaam. In 2010, of those identified as high risk who accessed HIV testing, 9.4% of males and 41% of females were HIV positive, highlighting the importance of this approach.22
In response to the evidence-base on the effectiveness of couple counseling23–26 and the importance of transmission within couples, PEPFAR has supported expansion of couple testing, which provides an opportunity for mutual disclosure and focused prevention counseling. Demographic and Health Survey (DHS) data and observational studies show that among individuals known to be HIV-1 infected, 50% of their partners are not infected or are “discordant.”17,26–28 A study by the Rakai project in Uganda in 2000 demonstrated that with no interventions, annual incidence rates of 11.8% were observed in discordant couples.29 More recent studies on ART for prevention also demonstrate high rates of transmission within discordant couples.30–32 For example, the recent HIV Prevention Trials Network 052 study found an incidence rate linked to the initially infected partner of 1.7 per 100 person-years in the delayed-therapy arm.33
Barriers to couple testing include misconceptions about HIV discordance, fear of abandonment, blame, stigma- and-gender based violence, and the lack of personnel trained in couple counseling, which is more complex than individual counseling. Uptake remains low, although home testing and programs to serve pregnant women have proved effective to some degree although the desire to conceive is a barrier to condom use, and this is compounded by reports of increased risk for HIV transmission and acquisition during pregnancy.34,35
INNOVATIONS IN PROMOTION OF HTC
In almost all countries receiving PEPFAR support, there has been social marketing of HTC, including mass media advertising and subsidized or free services. Studies have shown that such promotion can increase utilization of testing and may also increase health workers' interest in providing the service.36 A PEPFAR-supported campaign in 2010 in non–research-related settings in Zambia included mass media promotion, community outreach through village chiefs and other local leaders, and provision of couple HTC. Central to the campaign were 3 real couples telling how knowing their HIV status as a couple strengthened their relationships and helped them prepare for the future. In 2009, before the campaign, only 5% of persons served tested with a sexual partner. During the campaign in 2010, this increased to 14% and continued increasing to approximately 20% of persons tested in 2011.37 Figure 2 provides an example of the promotion of couple testing in Zambia.
INNOVATION IN TESTING: FROM LABORATORY TO POINT OF CARE
HIV rapid tests are simple to perform, with 2 or more tests providing confirmed results in 30 minutes or less in a serial or a parallel algorithm. Serial testing occurs when a first screening test is performed, and if positive, a second different confirmatory test is done. Parallel testing occurs when 2 different tests are performed simultaneously. Rapid tests became available in the late 1990s, but the number of tests being performed was modest, and there were only 10–15 kits on the market. PEPFAR support increased demand, and currently, there are over 50 rapid tests on the market. Starting in 2006, PEPFAR implemented a centralized validation process for test kits with a diverse and standardized set of specimens collected globally, requiring test kits to have a minimum sensitivity ≥99% and specificity ≥98%. Quality control testing has recently resulted in identification of problematic test kits and the disqualification of certain test kits from PEPFAR- and WHO-approved lists.38
Quality-assured rapid testing has facilitated the movement from laboratory-based testing to other settings, and most studies find that with good training, performance of nonlaboratory workers is similar to laboratory staff.39 Numerous quality assurance and quality control measures are in place, often with PEPFAR support,40,41 and WHO has published guidance on quality assurance and retesting.42,43
PEPFAR support for HTC services has also resulted in strengthening of reference laboratories in many countries,41,44 which now provide national guidance, monitor new test kit lots and testing practices, develop training curricula, and certify personnel. It has also had the effect of enabling laboratory networks to support other point-of-care tests including tests for pregnancy, malaria, and tuberculosis. There was a significant improvement in inventory management and procurement process after coordination with the PEPFAR-supported Supply Chain Management Services.
An emphasis on achieving targets has been both a strength and a problem for PEPFAR, as the emphasis on numbers of persons tested has not always been matched with an emphasis on quality. Reports from program evaluations repeatedly make reference to HTC workers abbreviating both testing and counseling protocols,45–47 and some persons performing rapid testing in field sites are poorly trained and supervised.48 Data on the effectiveness of HTC on enrollment in prevention and care are scant. Although quality standards exist for the testing elements of HTC services, adherence to these standards varies across and within countries. Counseling services are more difficult to standardize, and it is likely that this is associated with huge variations in the length and content of posttest counseling, although data are limited. Another threat to quality has been that manufacturing and distribution systems at the international, national, and local level have not always kept pace with demand, and stock-outs of rapid test kits have occurred in many PEPFAR-supported countries.
To provide a framework for addressing some of these gaps, PEPFAR in 2010 supported the WHO to develop a practical handbook that uses the quality assurance cycle (plan, define, monitor, improve, and evaluate) and has identified 10 key “building blocks” required to achieve the goal of quality testing and counseling services.49 Based on traditional quality improvement methodologies,50 it is hoped this handbook will assist countries and programs to improve services through a quality improvement approach.
COST OF HIV TESTING SERVICES SUPPORTED BY PEPFAR
To date, PEPFAR has spent more than $1.2 billion on HTC programming (Figure 3). The costs of HTC programs have varied across PEPFAR countries, from $8 to $20 per client in an analysis done by PEPFAR staff in 2006. These crude costing estimates include test kits, provider time, training, salaries, promotional services, and facility costs; costs to the individual or couple have rarely been quantified. In the first 8 years of PEPFAR, the proportion of annual country-level PEPFAR budgets devoted to HTC has ranged from 6% to 10%.8
A few studies have also examined cost-effectiveness. A study in Uganda found that overall the costs of HTC per person tested were quite low across models, with door-to-door home-based HTC being the least expensive at $8.29 per person tested and stand-alone VCT the most expensive at $19.26 per person. The cost per HIV-positive individual identified, however, varied widely by approach, with hospital-based HTC being the least expensive and home-based HTC being the most costly per positive individual identified.51 A study in Kenya comparing mobile and stand-alone HTC services found that the cost per person tested was low in the mobile services but higher per HIV-positive person identified.52 A study in Kenya analyzed cost-effectiveness in terms of PMTCT outcomes and found that both individual and couple HTC were cost-effective models for reducing infant HIV infections.53 In general, costs per person served are lowered when more people access HTC, indicating the need to promote HTC and ensure effective referral to care and treatment. Current global demands for treatment scale-up will require HTC programs to be more efficient.
POPULATION LEVEL COVERAGE
In its first 8 years, PEPFAR supported over 140 million testing sessions (Figure 1). In addition, by the end of 2010, the Global Fund had financed services that supported over 150 million sessions, often in partnership with PEPFAR programs (with potential overlap between PEPFAR and Global Fund reporting).54 However, because of repeat testing, the actual number of individuals who know their status as a result of PEPFAR support is likely to be lower than this. An alternate proxy measure of the impact of PEPFAR, the Global Fund, and national government support to increase the coverage of testing services is documented through the DHS. An analysis of DHS data from the 7 PEPFAR focus countries that conducted 2 DHS surveys in the time between 2003 and 201055 provides indirect evidence of the impact of PEPFAR support to HTC (Table 1). These data show a dramatic increase in the percentage of the population reporting testing in the last 12 months. In most countries, coverage at least doubled; in some, such as Kenya and Tanzania, coverage increased by 3 or 4 times. It is notable that the coverage for women increased more than for men, presumed to be due to PMTCT programs.
EXPANSION OF TESTING IN LIGHT OF TREATMENT SCALE-UP AND TREATMENT AS PREVENTION
Recent scientific findings have provided strong evidence that treating the HIV-infected partner dramatically reduces transmission to the negative partner.33 These studies have followed stable discordant couples, and the need to expand couple HTC is now clear, not only for cohabiting couples but also to all persons in a sexual relationship. Couple testing should be offered not just only to couples who request this service but also to the partners of all patients enrolled in prevention, care, and treatment programs, including programs for pregnant women. Despite the benefits of serving sexually active couples together, the additional costs in training and time needed for counselors and health workers to conduct couple testing have to date impeded efforts to scale-up this intervention. At least 2 countries (Rwanda and Zambia) have already modified treatment guidelines to include early ART for persons in documented discordant relationships, and increasing public knowledge of the prevention benefits of treatment is likely to generate demand for HTC, both for couples and individuals. A status-blind approach in HIV prevention services is not adequate, and behavioral approaches to sexual prevention should be based on knowledge of one's own HIV status and should also support mutual disclosure with all sexual partners. Expansion of testing services will need additional resources; the decline in PEPFAR resources devoted to testing as seen in Figure 3 suggests that non-PEPFAR resources, including the Global Fund, other donors, and national governments, will be needed to support significant expansion.
REFLECTIONS FOR THE FUTURE
The mandate to double PEPFAR-supported ARV treatment from 3 to 6 million people will also require expansion of HTC, although methods to calculate the necessary HTC targets to reach PEPFAR ARV goals remain debated. HTC programs will need to be strategic and focused, including targeting sexual partners and family members of persons enrolled in care and treatment and most at-risk populations.
The challenge to already overburdened health care systems will be considerable, and there are fears that an overemphasis on HIV testing will divert the time and attention of health care workers from primary health care services. These concerns often relate to the time spent in training and the additional time required to serve patients, and more examination is needed to determine the optimum amount of training, health education, and counseling. Although most health planners and AIDS advocates believe that HIV testing should remain voluntary, the irony is that counseling remains mandatory for those receiving testing. In the words of a counselor in South Africa in 2009, “Some don't want counseling but we make them.” WHO and other normative bodies continue to require posttest counseling for all persons, despite inadequate evidence that posttest counseling results in risk reduction for those testing negative, many of whom assume, perhaps correctly, that they are not at risk. The emphasis on posttest counseling for all persons may have diluted attention from effective referral to care and treatment for all those testing positive, and in the future, early enrollment in care should be a key quality indicator in all settings. Alternate methods need assessment to ensure appropriate health education, effective referrals, and retention in care.
As rapid HIV testing kits become as easy to perform as home pregnancy tests, there will be continued interest in self-testing, although accuracy of self-testing results is not yet well documented. In addition, there are concerns that vulnerable women may be coerced into testing by their sexual partners and that persons testing positive will not have appropriate posttest counseling, referral, and supportive care. There have been several pilots of self-testing,56 and self-testing devices have been marketed in South Africa. In January 2012, the Ministry of Health in Zambia approved self-testing and it can be anticipated that more countries will adopt self-testing policies. The detection of acute or early infection, which plays an important role in HIV transmission but cannot be reliably detected by current rapid antibody tests, is another future challenge as newer rapid test kits become available.
The degree of integration of HIV testing services into primary health care remains debated. Stand-alone programs such as traditional VCT were highly effective in the early days of PEPFAR but may not be sustainable in the future. There is the strong global push to integrate HTC into a comprehensive combination of HIV prevention, care, and treatment services and a more integrated approach to point-of-care testing for a range of pregnancy-related illnesses in antenatal care settings, and further implementation science and evaluation on combination HIV prevention approaches will provide important insights on the impact of this approach.57
In conclusion, PEPFAR support for HTC has been a catalyst for massive expansion in service delivery and significant increases in the proportion of the population who know their HIV status globally. Current shortages of health care workers necessitate the involvement of nonhealth worker counselors to provide HTC services. Technological advances in the ease of rapid testing will facilitate increases in community, home, and self-testing. HTC is the foundation for all other HIV services, and all HIV prevention programs should include the promotion and provision of testing. Expansion of HTC will continue to stress the complex chain including manufacturing, distribution, training, quality assurance, retention in care, and public trust. Despite these challenges, the substantial expansion of HTC in the first 8 years of PEPFAR demonstrates that with adequate financial, technical, and political support, it will be possible to achieve the goal of universal access to knowledge of HIV status.
The authors recognize the considerable assistance of Olivia Tulloch and Christine Veronika Kramer with editing and references. E. Marum, M. Taegtmeyer, and A. S. Cheng wrote and edited the article. S. Lembariti, N. Mugo, M. Phiri, and J. Moore wrote some portions of the article and assisted with editing. A. S. Cheng compiled the data from the PEPFAR headquarters database. We also recognize and appreciate the efforts over many years of counselors and health care workers in numerous countries who have provided HTC to millions of people. Finally, we recognize the courage and commitment of millions of individuals and couples who have learned their HIV status through HTC services.
1. Alwano-Edyegu MG, Marum E. Knowledge Is Power: Voluntary Counseling and Testing in Uganda. Geneva: UNAIDS Best Practices Collection;1999.
2. Marum E, Campbell C, Msowoya K, et al.. Voluntary counseling and testing. In: Essex M, Mboup S, Kanki P, eds. AIDS in Africa. New York: Springer-Verlag;2002.
3. Downing RG, Otten RA, Marum E, et al.. Optimizing the delivery of HIV counseling and testing: the Uganda experience using rapid antibody test algorithms. J Acquire Immune Defic Syndr Hum Retrovirol. 1998;18:384–388.
5. Kenya Ministry of Health. National Guidelines for Voluntary Counseling and Testing. Nairobi, Kenya: Kenya Ministry of Health; 2001.
6. WHO, UNAIDS. Treating 3 Million by 2005. Making it Happen. The WHO Strategy. WHO, UNAIDS; 2003.
7. WHO, UNAIDS. Guidance on Provider-Initiated HIV Testing and Counselling in Health Facilities. Geneva, Switzerland: WHO, UNAIDS; 2007.
8. PEPFAR. HIV Testing and Counseling Technical Working Group. Internal Records. PEPFAR. Available at: http://www.pepfar.gov/.
Accessed January 18, 2012.
9. Hensen B, Baggaley R, Wong VJ, et al.. Universal voluntary HIV testing in antenatal care settings: a review of the contribution of provider-initiated testing & counselling. Trop Med Int Health. 2011;17:59–70.
10. UNHRC. Policy Statement on HIV Testing and Counseling in Health Facilities for Refugees, Internally Displaced Persons and Other Persons of Concern. New York: UNHRC; 2009.
11. WHO, UNICEF. Policy Requirements for HIV Testing and Counseling of Infants and Young Children in Health Facilities. WHO, UNICEF; 2010.
12. WHO. Guidelines on HIV Disclosure Counselling for Children up to 12 Years of Age. Geneva: WHO; 2011.
13. UNICEF, WHO, FHI. HIV counselling resource package for the Asia-Pacific. Geneva: UNICEF, WHO, FHI; 2009.
14. WHO Europe. Scaling up HIV Testing and Counseling in the WHO European Region as an Essential Component of Efforts to Achieve Universal Access to HIV Prevention, Treatment, Care and Support. Policy Framework. Geneva: WHO Europe; 2010.
15. Taegtmeyer M, Martineau T, Namwebya JH, et al.. A qualitative exploration of the human resource policy implications of voluntary counselling and testing scale-up in Kenya: applying a model for policy analysis. BMC Public Health. 2011;11:812.
16. PEPFAR. Guidance for the Prevention of Sexually Transmitted HIV Infections. Washington, DC: PEPFAR; 2011.
17. Were WA, Mermin JH, Wamai N, et al.. Undiagnosed HIV infection and couple HIV discordance among household members of HIV-infected people receiving antiretroviral therapy in Uganda. J Acquire Immune Defic Syndr. 2006;43:91–95.
18. Tumwesigye E, Wana G, Kasasa S, et al.. High uptake of home-based, district-wide, HIV counseling and testing in Uganda. AIDS Patient Care STDS. 2010;24:735–741.
19. Abt Associates. VCT Events: Country Case Studies: Malawi, Ethiopia & Brazil. Washington, DC: PEPFAR, WHO and UNAIDS; 2008.
20. WHO. Towards Universal Access: Scaling up Priority HIV/AIDS interventions in the Health Sector. Progress Report. Geneva, Switzerland: WHO; 2008.
21. Taegtmeyer M, Hightower A, Opiyo W, et al.. A peer-led HIV counselling and testing programme for the deaf in Kenya. Disabil Rehabil. 2009;31:508–514.
22. Muhimbili University Teaching Hospital Annual Report to CDC Tanzania. Dar es Salaam, Tanzania: 2011.
23. Allen S, Karita E, Chomba E, et al.. Promotion of couples' voluntary counselling and testing for HIV through influential networks in two African capital cities. BMC Public Health. 2007;7:349.
24. Allen S, Tice J, Van de Perre P, et al.. Effect of serotesting with counselling on condom use and seroconversion among HIV discordant couples in Africa. BMJ. 1992;304:1605–1609.
25. Allen S, Meinzen-Derr J, Kautzman M, et al.. Sexual behavior of HIV discordant couples after HIV counseling and testing. AIDS. 2003;17:733–740.
26. Bunnell R, Opio A, Musinguzi J, et al.. HIV transmission risk behavior among HIV-infected adults in Uganda: results of a nationally representative survey. AIDS. 2008;22:617–624.
27. Lingappa JR, Lambdin B, Bukusi EA, et al.. Regional differences in prevalence of HIV-1 discordance in Africa and enrollment of HIV-1 discordant couples into an HIV-1 prevention trial. PLoS One. 2008;3:e1411.
28. Kaiser R, Bunnell R, Hightower A, et al.. Factors associated with HIV infection in married or cohabitating couples in Kenya: results from a nationally representative study. PLoS One. 2011;6:e17842.
29. Quinn TC, Wawer MJ, Sewankambo N, et al.. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med. 2000;342:921–929.
30. Donnell D, Baeten J, Kiarie J, et al.. Heterosexual HIV-1 transmission after initiation of antiretroviral therapy: a prospective cohort analysis. Lancet. 2010;12:2092–2098.
31. Reynolds S, Makumbi F, Nakigozi G, et al.. HIV-1 transmission among HIV-1 discordant couples before and after the introduction of antiretroviral therapy. AIDS. 2011;25:473–477.
32. Bunnell R, Ekwaru JP, Solberg P, et al.. Changes in sexual behavior and risk of HIV transmission after antiretroviral therapy and prevention interventions in rural Uganda. AIDS. 2006;20:85–92.
33. Cohen MS, Chen YQ, McCauley M, et al.. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365:493–505.
34. Mugo NR, Heffron R, Donnell D, et al.. Increased risk of HIV-1 transmission in pregnancy: a prospective study among African HIV-1-serodiscordant couples. AIDS. 2011;25:1887–1895.
35. Moodley D, Esterhuizen TM, Pather T, et al.. High HIV incidence during pregnancy: compelling reason for repeat HIV testing. AIDS. 2009;23:1255–1259.
36. Marum E, Morgan G, Hightower A, et al.. Using mass media campaigns to promote voluntary counseling and HIV-testing services in Kenya. AIDS. 2008;22:2019–2024.
37. Society for Family Health. Motivating Couples to Learn their HIV Status Together: Case Study, Zambia. Lusaka, Zambia: Society for Family Health; 2010.
39. Kenyon T, Alwano M, Jikijela C, et al.. The accuracy of HIV rapid testing as performed by counselors compared with lab technicians, Botswana Tebelopele VCT centers. Paper presented at: XII International Conference on AIDS and STDs in Africa; 2001; Ouagadougou, Burkina Faso.
40. Parekh BS, Anyanwu J, Patel H, et al.. Dried tube specimens: a simple and cost-effective method for preparation of HIV proficiency testing panels and quality control materials for use in resource-limited settings. J Virol Methods. 2010;163:295–300.
41. Parekh BS, Kalou MB, Alemnji G, et al.. Scaling up HIV rapid testing in developing countries: comprehensive approach for implementing quality assurance. Am J Clin Pathol. 2010;134:573–584.
42. WHO. A Handbook for Improving HIV Testing and Counselling Services—Field Test Version. Geneva, Switzerland: World Health Organization; 2010.
43. WHO. Delivering HIV Test Results and Messages for Re-Testing and Counselling in Adults. Geneva, Switzerland: World Health Organization; 2010.
44. Birx D, de Souza M, Nkengasong JN. Laboratory challenges in the scaling up of HIV, TB, and malaria programs: the interaction of health and laboratory systems, clinical research, and service delivery. Am J Clin Pathol. 2009;131:849–851.
45. Eng B, Cain K, Nong K, et al.. Using program evaluation to improve the performance of a TB-HIV project in Banteay Meanchey, Cambodia. Int J Tuberc Lung Dis. 2008;12(suppl 1):44–50.
46. Mashauri F, Siza HJ, Temu M, et al.. Assessment of quality assurance in HIV testing in health facilities in Lake Victoria zone, Tanzania. Tanzan Health Res Bull. 2007;9:110–114.
47. Youngleson M, Nkurunziza P, Jennings K, et al.. Improving a mother to child HIV transmission programme through health system redesign: quality improvement, protocol adjustment and resource addition. PLoS One. 2010;5:e13891.
48. Wolpaw B, Mathews C, Chopra M, et al.. The failure of routine rapid HIV testing: a case study of improving low sensitivity in the field. BMC Health Serv Res. 2010;22:10–73.
49. Doyle V, Taegtmeyer M. A Handbook for Improving HIV Testing and Counselling Services. Geneva, Switzerland: WHO; 2010.
50. Leatherman S, Ferris T, Berwick D, et al.. The role of quality improvement in strengthening health systems in developing countries. Int J Qual Health Care. 2010;22:237–243.
51. Menzies N, Abang B, Wanyenze R, et al.. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS. 2009;23:395–401.
52. Grabbe KL, Menzies N, Taegtmeyer M, et al.. Increasing access to HIV counseling and testing through mobile services in Kenya: strategies, utilization, and cost-effectiveness. J Acquir Immune Defic Syndr. 2010;54:317–323.
53. John FN, Farquhar C, Kiarie JN, et al.. Cost effectiveness of couple counselling to enhance infant HIV-1 prevention. Int J STD AIDS. 2008;19:406–409.
54. David AM, Mercado SP, Becker D, et al.. The prevention and control of HIV/AIDS, TB and Vector-borne diseases in informal settlements: challenges, opportunities and insights. J Urban Health. 2007;84(suppl):i65–i74.
56. Choko AT, Desmond N, Webb EL, et al.. The uptake and accuracy of oral kits for HIV self-testing in high HIV prevalence setting: a cross-sectional feasibility study in Blantyre, Malawi. PLoS Med. 2011;8:e1001102.
57. Padian N, Holmes C, et al.. Implementation science for the US President's Emergency Plan for AIDS Relief (PEPFAR). J Acquir Immune Defic Syndr. 2011;56:199–203.
PEPFAR; HIV; counseling; testing
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