JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Social Science
Undiagnosed HIV Infection and Couple HIV Discordance Among Household Members of HIV-Infected People Receiving Antiretroviral Therapy in Uganda
Were, Willy A. MBChB, MPH*; Mermin, Jonathan H. MD MPH*; Wamai, Nafuna MBChB MPH*; Awor, Anna C. MSc*; Bechange, Stevens BSc*; Moss, Susan MPH*; Solberg, Peter MD†; Downing, Robert G. PhD*; Coutinho, Alex MBChB, MSc‡; Bunnell, Rebecca E. PhD Med*
From the *CDC-Uganda, Global AIDS Program, National Center for HIV, STD and TB Prevention, Centers for Disease Control and Prevention, Entebbe, Uganda; †University of California, San Francisco; and ‡The AIDS Support Organization, Kampala, Uganda.
Received for publication December 12, 2005; accepted April 17, 2006.
Funding/Support: The US Department of Health and Human Services/Centers for Disease Control and Prevention provided intramural funds to support the study, and staff were involved in the study design, data collection, analysis, and writing the manuscript.
Author contributions: Willy A. Were was the main author of the paper. Peter Solberg, Jonathan Mermin, and Rebecca Bunnell, the principal investigators, wrote the protocol, supervised the study, guided data analysis, and had full access to all the data and take responsibility for the integrity of the data and accuracy of data analysis. Stevens Bechange and Susan Moss supervised data entry and cleaning and, with Ann Awor, analyzed data and conducted statistical analyses. Robert Downing supervised and conducted laboratory testing. Willy Were and Nafuna Wamai supervised the study. Rebecca Bunnell provided guidance to study staff on behavioral aspects of the study and assisted in interpreting results. Alex Coutinho helped design and conduct the study, and ensured the protocol was applicable to The AIDS Support Organization.
Conflict of interest statement: None of the authors had any conflicts of interest.
Reprints: Willy A. Were, MBChB, MPH, CDC-Uganda, Uganda Virus Research Institute, P.O. Box 49, Entebbe, Uganda (e-mail: firstname.lastname@example.org).
Introduction: Systematic efforts to identify HIV-infected members and HIV-discordant couples in households of individuals taking antiretroviral therapy (ART) could theoretically reduce HIV transmission and improve ART adherence.
Methods: We enrolled HIV-infected clients of an AIDS support organization in a randomized evaluation of different ART monitoring regimens that offered home-based ART care to them and their clinically eligible household members. At baseline, counselors visited participants' homes and offered voluntary counseling and testing (VCT) to all household members. We assessed uptake, HIV prevalence, HIV discordance, and rate of ART eligibility.
Results: Of the 2373 household members, 2348 (99%) accepted VCT. HIV prevalence among household members was 7.5% and varied by age with 9.5% among children aged 0 to 5 years, 2.9% among persons aged 6 to 24 years, and 37.1% among adults aged 25 to 44 years. Of the household members with HIV, 74% had never been previously tested, and 39% of these were clinically eligible for ART. Of the 120 spouses of ART patients that were tested for HIV, 52 (43%) were HIV negative, and of these, 99% had not been previously tested.
Conclusions: Provision of home-based VCT to household members of people initiating ART was well accepted and resulted in the detection of a large number of previously undiagnosed HIV infections and HIV-discordant relationships.
Both HIV/AIDS care and antiretroviral therapy (ART) are rapidly expanding in Africa and other resource-limited settings.1 Most care and treatment programs are clinic-based and utilize an individual approach to HIV care and treatment. However, the burden of HIV infection in households of people living with HIV may be high.2-4 In addition, HIV discordance is common within couples in Africa, ranging from 3% to 20% in the general population5-7 and 30% to 51% within couples in which one partner seeks HIV care services.2,8 However, knowledge of partner's HIV status is extremely low.9 Systematic efforts to identify HIV-infected members and HIV-discordant couples in households of individuals taking ART could theoretically reduce HIV transmission and drug sharing pressures, improve ART adherence, and prolong survival for people with previously unrecognized HIV infection.
In a study in rural Uganda, we offered home-based HIV voluntary counseling and testing (VCT) to household members of people initiating ART. We assessed acceptance of home-based VCT, HIV prevalence, the proportion of household members with unrecognized HIV infection, the proportion of ART-eligible household members, and the proportion of HIV discordant couples.
Between May 2003 and December 2004, we enrolled HIV-infected adults aged 18 years and older (index participants) in the Home-Based AIDS Care project, a randomized evaluation of different ART monitoring regimens for persons receiving home-based ART care. Participants were recruited from The AIDS Support Organization, a nongovernmental organization in Tororo and Busia Districts, Uganda. After written informed consent was provided by the participants, a venous blood sample was collected for confirmation of HIV infection and CD4 cell count enumeration, and a physical examination and medical history were conducted for clinical staging. If found eligible for ART, the index participants provided written informed consent for study staff to visit their homes to request for the consent of their household members for VCT. A household was defined as persons who shared food cooked at a common hearth and slept in the same house or cluster of houses for at least 5 days in a week for the preceding 3 months. Consenting household members provided a finger stick sample of blood on filter paper for HIV testing. Results were returned after 2 weeks to individuals or couples at home or at the study clinic, depending on participants' preference. All participants could request for follow-up counseling and support, including counselor-assisted disclosure if desired.
For participants aged 10 to 17 years, VCT counseling included both the child and parent or legal guardian; consent was required from the parent or guardian, and assent was required from the child. For children aged 0 to 9 years, only the parent or legal guardian provided consent. Neither consent for HIV testing nor receiving test results was required for household members to receive free clinical care that was part of the study. The VCT was voluntary and confidential. We collected standardized information about testing history and, for first-time testers, previous barriers to testing. HIV-infected household members were offered cotrimoxazole prophylaxis (unless medically contraindicated), sexual risk reduction counseling for adults, and access to care at the study clinic; those found to be eligible by CD4 of 250 cells/μL or less or symptomatic AIDS were offered standard ART, most often consisting of lamivudine, stavudine, and either nevirapine or efavirenz.
Counselors encouraged couples to receive results together and, where HIV discordance was recognized, offered enhanced couple counseling, focusing on understanding discordance, making personalized couple risk reduction plans, and coping with challenges and social pressures around childbearing.
Plasma was screened for HIV infection using 2 enzyme-linked immunoassays (EIA) in parallel (Recombigen HIV-1/HIV-2; Trinity Biotech, Dublin, Ireland and Murex HIV 120; Abbot Diagnostics, Chicago, IL). Specimens negative on both EIA screening tests were considered negative; specimens positive on both assays were considered positive. Specimens with discordant results were retested by Western Blot (LAV Blot; Biorad, Richmond, CA). HIV testing of dried blood spots consisted of a screening EIA (Virinostika HIV; BioMerieux, Durham, NC) and a confirmation of reactive specimens by Western Blot. HIV-reactive specimens from children younger than 24 months were tested for HIV using the Roche Cobas r1.5 (Roche, Rariton, NJ) assay.
Although all household members were offered the opportunity to have an HIV test, only household members who had not received home-based VCT in a previous study10 were included in this analysis. Index participants were categorized as married if they were legally married or cohabiting with a partner at the time of enrollment in the study. If they had never married or cohabited or had divorced or were widowed, they were classified as unmarried. Children were categorized in the age groups of 0 to 5, 6 to 10, and 11 to 17 years. Data were double-entered in Epi-Info 2000 (CDC, Atlanta, GA) and analyzed using SAS version 9.1 (SAS Institute, Cary, NC). Frequency distributions were used to compute the proportion of clients who accepted testing, HIV prevalence, and the proportion eligible for ART.
The study was approved by the Science and Ethics Committee of the Uganda Virus Research Institute, the Uganda National Council of Science and Technology, the Institutional Review Boards of the Centers for Disease Control and Prevention, and the University of California, San Francisco.
We offered VCT to 2373 household members of 730 index clients. The median age of household members was 12 years (interquartile range, 7-17 years), and 52% were female. Overall, 2348 (99%) accepted VCT; 99% of them were tested in their home. HIV prevalence was 7.5% among all household members and varied by age. Among children aged 0 to 5 years, 9.5% were infected; among persons aged 6 to 24 years, 2.9% were infected. Among adults aged 25 to 44 years, 37.1% were infected (Table 1). HIV prevalence among people living in households did not vary by sex of the index participants (Table 2). Among children whose mothers had died or were HIV positive, HIV prevalence was 17.7% for those aged 0 to 5 years, 5.2% for those aged6 to 10 years, and 1.7% for those aged 11 to 17 years (Table 3). Of the 238 whose mothers were HIV negative, only 1 child was HIV infected. Overall, 95% of the household members had never been previously tested for HIV. Only 1 of the 1575 children aged 14 years and younger had been previously tested. Previous barriers to testing among 657 (85%) of the 773 household members older than 15 years who had never been tested included no perceived risk of infection (52%), distance from testing sites (8%), and fear of knowing one's HIV status (17%). Less than 1% listed lack of access to antiretroviral (ARV) care as a barrier to HIV testing.
Of the 176 (7.5%) household members diagnosed with HIV infection, 130 (74%) had never been previously tested for HIV. None of the 76 children with HIV infection had been previously tested. All household members who tested HIV positive and all 52 HIV-infected household members (30%) who were clinically eligible for ART-initiated treatment received cotrimoxazole prophylaxis. Of the 397 spouses living in the households, 268 (68%) had never been tested for HIV. Of the 120 spouses of patients on ART tested, 52 (43%) were HIV negative (Table 2), and of these, 99% had not been previously tested.
Ninety-nine percent of the household members of people with HIV taking ART accepted VCT, and almost all were tested in their homes. The prevalence of previously undiagnosed HIV infection was high, particularly among adults and young children. Over 70% of HIV infections among household members were diagnosed for the first time through home-based provision of HIV counseling and testing. HIV discordance within couples was high: 43% of spouses of HIV-infected index participants were HIV negative.
HIV prevalence among adults aged 15 to 44 years within households of HIV-infected patients was more than 3 times that found in a recent national HIV prevalence survey in Uganda,11 highlighting the importance of targeting family members of HIV-infected people for VCT even in a country with high prevalence of HIV in the general population. Theoretically, VCT can be provided within clinics or at home, although uptake seems to be much higher during home visits. For example, experience in facility-based Prevention of Mother-to-Child Transmission programs has shown that only between 3% and 15% of the partners received testing.12 Two general population studies in Uganda showed 2- to 4-fold increases in receipt of HIV test results when provided to participants in their homes rather than through a nearby clinic.13-16 The high rate of acceptance of VCT among family members of people with HIV in the present study does not seem to be caused by the availability of ART. Uptake of VCT was more than 97% in a previous study of more than 3000 household members of people with HIV in which no ART was offered to participants in the same area.13
In Uganda, like elsewhere in sub-Saharan Africa, most HIV care programs include mainly adult clients. Yet, approximately 2.5 million children in Africa have HIV,17 and without effective care, almost half will die before their third birthday.18 In this study, because of a household approach to HIV testing, we identified many children with HIV infection-half of whom needed and were provided ART at the time of testing. Only 1 of the 238 children whose mothers were HIV negative had HIV, but 6% of the children with HIV-infected or deceased mothers were infected with HIV. Prevalence was very high, nearly 18%, among those aged younger than 5 years but was also high for older children of HIV-infected and deceased mothers. It would likely be most cost-effective to limit child VCT to all children whose mothers died or who are HIV infected.
The implementation of home-based VCT is operationally feasible in rural Uganda. At the time of enrollment in this study, we conducted laboratory testing in the study laboratory and made a return visit to homes for results counseling. However, at The AIDS Support Organization centers and several community-based programs, trained lay providers are now conducting rapid finger stick testing in client homes, and this is supported by the new Ugandan Ministry of Health counseling and testing guidelines.19 Over 200,000 individuals in various communities of Uganda have received VCT in their homes. Dried blood spots are routinely collected for quality control using a parallel EIA testing algorithm (Virinostika Uniform II plus 0 and Murex HIV 120). Cost-utility analyses will be important to help compare the potential benefits of a home-based approach, including coverage, disclosure, and couples counseling with more traditional facility-based and referral approaches.
It would be useful to evaluate this type of intervention in urban settings where acceptance may be different. Concern has been raised about possible negative social consequences that may occur with partner VCT,20,21 but in follow-up studies of the population in this study, we found substantial increases in positive social events such as strengthened relationships and community support and no increase in negative events during the 3 months after home-based VCT as compared with 3 months before enrollment.22 Our high acceptance rates were in the context of provision of ART and may not be applicable to other settings. However, similarly, acceptance rates have been demonstrated in this same population and several other home-based VCT programs in Uganda even before the availability of ART.10,13
Provision of VCT for family members of people in HIV care and treatment programs is an important intervention for both case finding and for prevention of HIV transmission. Providing couples with HIV testing and counseling decreases high-risk sexual behavior and HIV transmission,23,24 particularly among HIV-discordant couples.25-27 Many persons with HIV believe that their partners are already infected and therefore do not avoid high-risk practices; however, in our study, 43% of the spouses of HIV-infected married participants were HIV negative. Reduction of HIV transmission within HIV-discordant couples should also help control the spread of ARV-resistant virus from persons taking ARVs. Integration of family VCT as a routine part of HIV care and treatment programs will be necessary for public health efforts to control the HIV epidemic and support people with HIV to live longer and healthier lives.
We thank Tororo Hospital administrative and clinical staff; the volunteers, staff, and clients of The AIDS Support Organization; the US Embassy in Kampala; GAP headquarters; and staff of CDC-Uganda, including the informatics, clinical, laboratory, and administrative units of CDC-Tororo.
2. Kabatesi D, Ransom R, Lule JR, et al. HIV prevalence among household members of persons living with HIV in rural Uganda. XIV International Aids Conference; July 7, 2002; Barcelona, Spain. Abstract No.10BT5-1.
3. Zaba B, Whitworth J, Marston M, et al. HIV and mortality of mothers and children: evidence from cohort studies in Uganda, Tanzania, and Malawi. Epidemiology
4. De Cock KM, Mbori-Ngacha D, Marum E. Shadow on the continent: public health and HIV/AIDS in Africa in the 21st century. Lancet
5. McKenna SL, Muyinda GK, Roth D, et al. Rapid HIV testing and counseling for voluntary testing centers in Africa. AIDS
6. Carpenter LM, Kamali A, Ruberantwari A, et al. Rates of HIV-1 transmission within marriage in rural Uganda in relation to the HIV sero-status of the partners. AIDS
7. Lurie MN, Williams BG, Zuma K, et al. Who infects whom? HIV-1 concordance and discordance among migrant and non-migrant couples in South Africa. AIDS
8. N'Gbichi JM, de Cock KM, Batter V, et al. HIV status of female sex partners of men reactive to HIV-1, HIV-2 or both viruses in Abidjan, Cote d'Ivoire. AIDS
9. Moatti JP, Prudhomme J, Traore DC, et al. Access to antiretroviral treatment and sexual behaviours of HIV-infected patients aware of their serostatus in Cote d'Ivoire. AIDS
. 2003;17(3 (suppl)):S69-S77.
10. Mermin J, Lule J, Ekwaru JP, et al. Effect of cotrimoxazole prophylaxis on morbidity, mortality, CD4 cell count, and HIV viral load among persons with HIV in rural Uganda. Lancet
11. Ministry of Health (MOH) Kampala. Preliminary results of the Uganda HIV/AIDS sero-behavioural survey (UHSBS); May 2, 2005. Press Release. 2005.
12. Farquhar C, Kiarie JN, Richardson BA, et al. Antenatal couple counseling increases uptake of interventions to prevent HIV-1 transmission. J Acquir Immune Defic Syndr
13. Were W, Mermin J, Bunnell R, et al. Home-based model for HIV voluntary counselling and testing. Lancet
14. Matovu JKB, Kigozi G, Nalugoda F, et al. The Rakai Project counselling programme experience. Trop Med Int Health
15. Wolff B, Nyanzi B, Katongole G, et al. Evaluation of a home-based voluntary counselling and testing intervention in rural Uganda. Health Policy and Planning
16. Mermin J, Lule J, Ekwaru JP, et al. Cotrimoxazole prophylaxis by HIV-infected persons in Uganda reduces morbidity and mortality among HIV-uninfected family members. AIDS
18. Spira R, Lepage P, Msellati P, et al. Natural history of human immunodeficiency virus type 1 infection in children: a five-year prospective study in Rwanda. Mother-to-Child HIV-1 Transmission Study Group. Pediatrics
19. Ministry of Health (MOH) Kampala. Uganda National Policy Guidelines for HIV Voluntary Counselling and Testing. 2005.
20. Van der SA, King R, Grinstead O, et al. Couple communication, sexual coercion and HIV risk reduction in Kigali, Rwanda. AIDS
21. Grinstead OA, Gregoricch SE, Choi K, et al. Positive and negative life events after counselling and testing; the voluntary HIV-1 Counselling and Testing Efficacy Study. AIDS
22. Apondi R. Home-based antiretroviral care in rural Uganda is associated with positive social outcomes. 4th Uganda National AIDS Conference; March 21-22, 2005; Kampala, Uganda. Abstract No.10BT5-1.
23. 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
24. The Voluntary HIV-1 Counseling and Testing Efficacy Study Group. Efficacy of voluntary HIV-1 counselling and testing in individual and couples in Kenya, Tanzania, and Trinidad: a randomised trial. Lancet
25. Kamenga M, Ryder RW, Jingu M, et al. Evidence of marked sexual behavior change associated with low HIV-1 seroconversion in 149 married couples with discordant HIV-1 serostatus: experience at an HIV couselling center in Zaire. AIDS
26. Allen S, Meinzen-Derr J, Kautzman M, et al. Sexual behavior of HIV discordant couples after HIV counseling and testing. AIDS
27. Allen S, Serufilira A, Bogaerts J, et al. Confidential HIV testing and condom promotion in Africa. Impact on HIV and gonorrhea rates. JAMA
This article has been cited 40 time(s).
Journal of the International AIDS SocietyInvolving fathers in prevention of mother to child transmission initiatives - what the evidence suggestsJournal of the International AIDS Society
Social Science & MedicineStrong effects of home-based voluntary HIV counselling and testing on acceptance and equity: A cluster randomised trial in ZambiaSocial Science & Medicine
Bmj OpenPromotion of couples' voluntary HIV counselling and testing in Lusaka, Zambia by influence network leaders and agentsBmj Open
Lancet Infectious Diseases
Combination implementation for HIV prevention: moving from clinical trial evidence to population-level effects
Lancet Infectious Diseases, 13(1):
Bmc Public HealthTrends in HIV counseling and testing uptake among married individuals in Rakai, UgandaBmc Public Health
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivUtilization of a basic care and prevention package by HIV-infected persons in UgandaAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
Bmc Public HealthVoluntary HIV counselling and testing among men in rural western Uganda: Implications for HIV preventionBmc Public Health
Plos OneReproductive Intentions and Outcomes among Women on Antiretroviral Therapy in Rural Uganda: A Prospective Cohort StudyPlos One
Tropical Medicine & International HealthProvider-initiated HIV testing for paediatric inpatients and their caretakers is feasible and acceptableTropical Medicine & International Health
Plos OneSexually Transmitted Infections among HIV-1-Discordant CouplesPlos One
New heterosexually transmitted HIV infections in married or cohabiting couples in urban Zambia and Rwanda: an analysis of survey and clinical data
Tropical Medicine & International HealthExpanding access to voluntary HIV counselling and testing in sub-Saharan Africa: alternative approaches for improving uptake, 2001-2007Tropical Medicine & International Health
Bmc Public HealthPromotion of couples' voluntary counselling and testing for HIV through influential networks in two African capital citiesBmc Public Health
International Journal of Tuberculosis and Lung Disease
A simple screening tool for active tuberculosis in HIV-infected adults receiving antiretroviral treatment in Uganda
International Journal of Tuberculosis and Lung Disease, 13(1):
Sahara J-Journal of Social Aspects of Hiv-AIDS
Provider-initiated HIV testing in health care settings: Should it include client-centered counselling?
Sahara J-Journal of Social Aspects of Hiv-AIDS, 6(3):
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivLong-term voluntary counseling and testing (VCT) uptake dynamics in a multicountry HIV workplace program in sub-Saharan AfricaAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
Tropical Medicine & International HealthUptake of HIV voluntary counselling and testing services in rural Tanzania: implications for effective HIV prevention and equitable access to treatmentTropical Medicine & International Health
Health Policy and Planning'What if they ask how I got it?' Dilemmas of disclosing parental HIV status and testing children for HIV in UgandaHealth Policy and Planning
Clinical Infectious DiseasesIntegrating HIV Screening into Routine Health Care in Resource-Limited SettingsClinical Infectious Diseases
International Journal of Std & AIDSNon-vertical HIV transmission to children in sub-Saharan AfricaInternational Journal of Std & AIDS
Bulletin of the World Health OrganizationAcceptability of routine HIV counselling and testing, and HIV seroprevalence in Ugandan hospitalsBulletin of the World Health Organization
AIDS and BehaviorComparing Couples' and Individual Voluntary Counseling and Testing for HIV at Antenatal Clinics in Tanzania: A Randomized TrialAIDS and Behavior
Current Hiv Research
HIV-1-discordant couples in sub-Saharan Africa: Explanations and implications for high rates of discordancy
Current Hiv Research, 5(4):
Universal HIV testing and counselling in Africa
Culture Health & SexualityPregnancy decisions among HIV-positive pregnant women in Mulago Hospital, UgandaCulture Health & Sexuality
Bmc Infectious DiseasesUptake of HIV testing and outcomes within a Community-based Therapeutic Care (CTC) programme to treat Severe Acute Malnutrition in Malawi: a descriptive studyBmc Infectious Diseases
LancetTuberculosis 8 Scale-up of services and research priorities for diagnosis, management, and control of tuberculosis: a call to actionLancet
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivPartners at risk: motivations, strategies, and challenges to HIV transmission risk reduction among HIV-infected men and women in UgandaAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
International Journal of Std & AIDSCouples at risk for HIV infection in Southern India: characteristics of HIV-infected patients in concordant and discordant heterosexual relationshipsInternational Journal of Std & AIDS
AIDS Patient Care and StdsInitial Outcomes of Provider-Initiated Routine HIV Testing and Counseling During Outpatient Care at a Rural Ugandan Hospital: Risky Sexual Behavior, Partner HIV Testing, Disclosure, and HIV Care SeekingAIDS Patient Care and Stds
Clinical Infectious DiseasesTreatment to Prevent Transmission of HIV-1Clinical Infectious Diseases
Plos MedicineUptake of Home-Based Voluntary HIV Testing in Sub-Saharan Africa: A Systematic Review and Meta-AnalysisPlos Medicine
AIDS Patient Care and StdsPregnant Women and Disclosure to Sexual Partners After Testing HIV-1-Seropositive During Antenatal CareAIDS Patient Care and Stds
Bmc Health Services ResearchPregnant women's experiences of routine counselling and testing for HIV in Eastern Uganda: a qualitative studyBmc Health Services Research
Plos MedicineTowards Universal Voluntary HIV Testing and Counselling: A Systematic Review and Meta-Analysis of Community-Based ApproachesPlos Medicine
JAIDS Journal of Acquired Immune Deficiency SyndromesEvolution of Couples' Voluntary Counseling and Testing for HIV in Lusaka, ZambiaJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesIncreasing Uptake of HIV Testing and Counseling Among the Poorest in Sub-Saharan Countries Through Home-Based Service ProvisionJAIDS Journal of Acquired Immune Deficiency Syndromes
Sexually Transmitted DiseasesSexual Transmission of HIV-1 Among Serodiscordant Couples in Porto Alegre, Southern BrazilSexually Transmitted Diseases
HIV; prevalence; family members; voluntary counseling and testing; antiretroviral therapy; Uganda
© 2006 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.