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JAIDS Journal of Acquired Immune Deficiency Syndromes:
doi: 10.1097/QAI.0b013e3182170fd3
Implementation and Operational Research: Epidemiology and Prevention

HIV Diagnosis, Linkage to HIV Care, and HIV Risk Behaviors Among Newly Diagnosed HIV-Positive Female Sex Workers in Kigali, Rwanda

Braunstein, Sarah L PhD, MPH*; Umulisa, Marie-Michèle BA†; Veldhuijzen, Nienke J MD, MPH‡; Kestelyn, Evelyne MSc†; Ingabire, Chantal M MA†; Nyinawabega, Jeanine BA†; van de Wijgert, Janneke H H M PhD, MPH†‡; Nash, Denis PhD, MPH*

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Author Information

From the *Mailman School of Public Health, Columbia University, New York, NY; †Projet Ubuzima, Kigali, Rwanda; and ‡Department of Internal Medicine, Academic Medical Center of the University of Amsterdam and Amsterdam Institute for Global Health and Development, Amsterdam, The Netherlands. Sarah Braunstein is now with the New York City Department of Health and Mental Hygiene, New York, NY. Denis Nash is now with CUNY School of Public Health at Hunter College, New York, NY.

Received for publication November 11, 2010; accepted February 18, 2011.

Supported by Funding provided by the European and Developing Countries Clinical Trials Partnership (EDCTP) through a project entitled: “Preparing for Phase III vaginal microbicide trials in Rwanda and Kenya: preparedness studies, capacity building, and strengthening of medical referral systems.”

The authors have no conflicts of interest to disclose.

Correspondence to: Sarah L. Braunstein, PhD, MPH, New York City Department of Health and Mental Hygiene, Gotham Center 42-09 28th Street Queens, 22nd Floor, New York, NY 11101-4132. (e-mail: braunstein.sarah@gmail.com).

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Abstract

Objective: To evaluate linkage-to-care, sexual behavior change, and psychosocial experiences among newly HIV-diagnosed female sex workers (FSWs) in Rwanda.

Methods: FSWs (n = 800) with unknown serostatus were screened for HIV during 2007/2008. Women testing HIV positive (n = 192) were referred to care and asked to return for interviews and laboratory testing 12-36 months postdiagnosis. One hundred fourty-one women (73%) returned for the postdiagnosis visit.

Results: Median CD4 count at diagnosis was 460 cells per microliter [interquartile range (IQR): 308-628], with 32% eligible for antiretroviral therapy (ART) per national CD4 criteria (median CD4: 235, IQR: 152-303). Postdiagnosis, 92% of women reported having disclosed their HIV status to a friend or relative, 85% reported having enrolled in HIV care (median 30 days after diagnosis, IQR: 7-360), including 89% among ART-eligible women. Among ART-eligible women in care, 87% had initiated ART, with a median follow-up CD4 count of 354 cells per microliter (IQR: 213-456). Women who did not initiate ART experienced a 6-month CD4 count change of −14 cells per microliter (IQR: −41 to 13). Three-quarters of women reported reduced sexual risk behavior postdiagnosis, with only 64% continuing to identify as FSWs. However, 53% reported past month condom use only “sometimes.”

Conclusions: Timely linkage to care and ART uptake were high in this group of Rwandan FSWs. However, risky sexual behaviors remained common after enrollment in care. HIV-positive FSWs are an important and receptive group for targeted efforts to increase HIV diagnosis and linkage to care/treatment. Once in care, intensified and sustained HIV prevention education is necessary.

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INTRODUCTION

The benefits of early entry into medical care and timely initiation of antiretroviral therapy (ART) for newly HIV-diagnosed individuals are widely recognized, including reduced mortality, lower incidence of opportunistic infections, and reductions in risk behavior.1-3 HIV care and treatment programs have proliferated in sub-Saharan Africa in recent years, with ART coverage now estimated at 44% (41%-48%) of those in need.4 However, ART access remains variable across countries,5 and challenges in linking and retaining newly HIV-diagnosed individuals in care in resource-limited settings are well known.6-9

Rwanda is a small central African country with a 2010 population of approximately 11.0 million,10 and an estimated national adult HIV prevalence in 2005 of 3%.11 HIV prevalence is higher in urban areas (7.3%), including the capital city of Kigali (8.0%), than in rural areas (2.2%) and among women as compared with men.11 Although the general population adult HIV prevalence in Rwanda is relatively low compared with other sub-Saharan African countries, certain population subgroups experience high HIV burden, including female sex workers (FSWs). Population-based estimates of HIV prevalence among FSWs in Rwanda are sparse; however, data from HIV testing facilities suggest prevalence rates among sex workers of 16%-19%.12

In 2007, an estimated 150,000 Rwandans aged 15 years and older were living with HIV or AIDS.13 Beginning in 2003, HIV-related medical care services, including ART, were rapidly expanded in Rwanda.14,15 Current ART coverage rates in Rwanda are among the highest in the region, with an estimated 71% of 68,000 in need receiving ART.13 Fees for health care services are covered under a national health insurance program, and ART is provided free of charge by the Rwandan government. National guidelines dictate that all persons with CD4 <350 cells per microliter, and anyone with WHO Stage IV HIV disease, should be initiated on ART.15

Documentation of the experiences of newly HIV-diagnosed individuals in Rwanda in accessing HIV-related care and treatment is extremely limited. Information is particularly limited for most-at-risk-populations such as FSWs, for whom structural and psychosocial barriers are likely more common. Here, we report on the postdiagnosis experiences, including care and treatment, of newly HIV-diagnosed FSWs in Kigali, Rwanda.

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METHODS

Projet Ubuzima, a nongovernmental organization for medical research based in Kigali, Rwanda, conducted an HIV incidence study among FSWs during 2007/2008 in preparation for HIV prevention trials. As an add-on study to the main study, women who tested HIV positive during screening were invited to return to the clinic at least 1 year after HIV diagnosis for evaluation of linkage to care, initiation of treatment, experiences with stigma and disclosure, and attitudes and beliefs about ART (postdiagnosis visit).

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Study Design and Recruitment

For the main study, 800 FSWs of unknown HIV status 18 years and older were recruited via community meetings in 3 Kigali districts, after approval from local authorities. Study objectives, including the goal of estimating HIV incidence among FSWs to inform future prevention trials, were described in detail to potential participants. After prescreening at recruitment sites, potentially eligible women were invited to the clinic for eligibility assessment. Eligible women were aged ≥18, had engaged in transactional sex in the past month, had either unknown HIV serostatus or had a last test that was negative, and were willing and able to provide written informed consent.

Women who tested HIV positive in the baseline survey were further counseled, informed, and referred for HIV-related care and treatment. At least 1 year after the baseline survey, HIV-positive women were recontacted and asked to attend a one-time postdiagnosis visit to evaluate rates of linkage to HIV care and treatment and other experiences since diagnosis. As the postdiagnosis assessment was an amendment to the study protocol, women were not aware at baseline that they would be asked to attend a follow-up study visit. Recruitment was led by Projet Ubuzima outreach staff in collaboration with a network of community mobilizers with strong relationships with local community members.

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Study Procedures

Study procedures took place at the Projet Ubuzima clinic. All participants provided written informed consent (separately for the baseline survey and postdiagnosis visits). At baseline, women underwent face-to-face interviewing for information on demographics, medical and reproductive history, including HIV testing history, partnership status, and sexual behavior. In addition to HIV testing, blood specimens were tested for CD4 count and pregnancy. Women were given pregnancy test results and an appointment card to return to the clinic for CD4 results.

Study procedures at the postdiagnosis visit were similar to the baseline survey, with face-to-face interviewing and laboratory testing. The structured questionnaire at this visit, however, included additional questions related to linkage to HIV care (including barriers), ART initiation, and stigma and social support. As previously, women were advised to return to the clinic for CD4 results.

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Referrals for Care and Follow-Up

Women who tested HIV positive in the baseline survey received posttest counseling from study staff and were advised to return within 2 weeks for CD4 results. They were then referred to a health center for care and evaluation for treatment eligibility per Rwanda's national guidelines.15 Women were referred to a health center near their neighborhood of residence or in some cases to a more distant health center if they expressed concern about potential unintentional HIV disclosure to community members. Additional counseling and psychosocial support services were available at referral health centers. HIV-infected pregnant women were referred to health centers providing prevention of mother-to-child transmission.

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Laboratory Testing

HIV testing followed a slightly modified national testing protocol: First Response Rapid Test (Premier Medical Corporation, India); if positive, confirmation by Uni-Gold HIV Rapid Test (Trinity Biotech Plc, Bray, Ireland); and Capillus HIV-1/HIV-2 Rapid Test (Trinity Biotech Plc, Ireland) as tie-breaker if needed. HIV rapid test-positive specimens were confirmed by Murex HIV Ag/Ab Combination ELISA test (Murex Biotech Limited, Dartford, UK), and tested by CD4 cytometry. Blood specimens were also tested by the Fortress hCG serum pregnancy test (Fortress Diagnostics, Antrim, UK).

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Ethical Review and Approvals

The study was approved by the National Ethics Committee and National AIDS Control Commission in Rwanda and Columbia University Medical Center's Institutional Review Board in the United States. Participants received compensation for transport fees and time spent at the clinic (approximately 7 USD per visit).

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Data Sources and Statistical Analysis
Data Sources

The primary data source for this analysis was quantitative questionnaire data from face-to-face interviews and laboratory data at the baseline and postdiagnosis visits among FSWs who attended both. Enrollment in care was determined by self-report and was defined as seeking follow-up medical care after HIV diagnosis at a health center providing HIV care and treatment. Reasons for nonenrollment were collected by open-ended question. Interviews included structured questions related to degree of stigma or negative reactions experienced within participants' communities, and whether and to whom patients had disclosed their HIV status after diagnosis.

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Statistical Analysis

Descriptive statistics were used to summarize participants' demographic and behavioral characteristics. Categorical variables were expressed as percentages and continuous data as medians and interquartile ranges (IQR). χ2 tests were used for categorical variables, and t tests for continuous variables. Analyses were performed in SAS, version 9.1.3 (SAS Institute, Inc, Cary, NC).

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RESULTS

Recruitment and Study Sample

Between October 2006 and August 2007, 1287 women attended 31 recruitment sessions for the main study; 1238 women were prescreened; and 1122 women were potentially eligible and invited to the clinic (116 were excluded because of age <18 years, known positive HIV serostatus, or not engaging in pastmonth transactional sex). The first 800 eligible women were enrolled.

During the baseline survey, 192 women tested HIV-1 positive for an HIV prevalence of 24.0% (95% confidence interval: 21.0 to 27.0). In total, 141 of these HIV-positive women attended the postdiagnosis visit, a median of 623 days (range: 432-861) after baseline.

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Baseline Sociodemographics

Median age among this sample of newly HIV-diagnosed FSWs (n = 141) was 27 years (range: 18-45), and 23% of women had no formal education (Table 1). Overall, 94% of FSWs reported currently using a contraceptive method, with 72% reporting condom use during their most recent sex act. FSWs had had a median of 2 pregnancies during their lifetimes, and 22% were currently breastfeeding. Finally, 50% of women had never been tested for HIV before the survey.

Table 1
Table 1
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Table 1
Table 1
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HIV Care and Treatment
Linkage to HIV Care After HIV Diagnosis

All women were referred for HIV-related care and evaluation for treatment eligibility after diagnosis in the baseline survey. At the postdiagnosis visit, 85% of women (120 of 141) reported they had enrolled in HIV-related medical care, a median of 30 days (range: 1-840; IQR: 7-360) after diagnosis. Among women in care, 53% (64 of 120) enrolled within 1 month after diagnosis, and 69% (83 of 120) within 6 months. Most women (88%, 105 of 120) enrolled in care at a public health center or hospital. The most commonly cited reasons for not enrolling in care were perceived good health (n = 7) or a high CD4 count at diagnosis along with the belief that care was unnecessary (n = 4).

There were several differences in baseline characteristics between women who did and did not enroll in care after diagnosis. For example, out-of-care women were more likely to be breastfeeding (P = 0.01), have a known HIV-infected sex partner (P = 0.04), and report condom use at last sex act (P = 0.04) than women who linked with care. There were no differences by age, baseline CD4 count, number of years in sex work, history of HIV testing, or sexually transmitted infection treatment.

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CD4 Count at Diagnosis and Postdiagnosis

CD4 count testing was conducted at the baseline and postdiagnosis visits (Table 2). For the entire sample, median CD4 counts at baseline and postdiagnosis were 460 cells per microliter (IQR: 308-628 cells/μL) and 472 cells per microliter (IQR: 355-640), respectively (P = 0.12). Among women who initiated ART, median CD4 count was 309 cells per microliter (IQR: 214-442) at baseline and 441 cells per microliter (IQR: 309-612) postdiagnosis (ie, after ART initiation).

Table 2
Table 2
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At HIV diagnosis, 11% (16 of 140) of women met the CD4 <200 cells per microliter criterion for a concurrent AIDS diagnosis.16 Furthermore, 32% of women (44 of 140) were eligible for ART at diagnosis based on CD4 <350 cells per microliter, with a median CD4 count at diagnosis in this group of 235 cells per microliter (IQR: 152-303). Eighty-nine percent of ART-eligible women (39 of 44) enrolled in HIV care, and 87% of these women (34 of 39) reported initiating ART at the postdiagnosis visit, with a median CD4 count at that visit of 354 cells per microliter (IQR: 213-456). All 5 ART-eligible women who were in care but had not initiated ART cited a medical provider deeming them ineligible.

In total, irrespective of ART eligibility at HIV diagnosis, 57 women reported initiating ART at the postdiagnosis visit. This group experienced an overall mean change in CD4 cell count from baseline to the postdiagnosis visit of 139 cells per microliter (IQR: 34-261). The average rate of change was 43 CD4 cells per microliter per 6 months on ART (IQR: 11-73). Among ART-naive women (n = 82) during this same period, overall mean change in CD4 cell count was −52 cells per microliter (IQR: −148 to 57), with a rate of change of −14 cells per microliter per 6 months (IQR: −41 to 13).

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Self-Reported Adherence to ART Medication

Among women who enrolled in care since diagnosis, nearly half (48%, 57 of 120) reported initiating ART (Table 3). One-third (19 of 57) reported ever having missed taking pills since initiating ART, and 14% (8 of 57) had missed pills in the past 3 days. The most common reasons for nonadherence were as follows: forgetting (47%); not having food to take with medication (32%); and interruptions because of imprisonment or hospitalization (21%). More than one-third of women (35%) could not identify which regimen/medications they were taking.

Table 3
Table 3
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Table 3
Table 3
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Attitudes Toward ART

Eighty-two percent of women who initiated ART felt their health had improved since starting treatment. In structured interviews, women who had enrolled in care generally displayed positive attitudes toward ART, as well as good knowledge of its purpose and benefits (Table 3). Nearly all women understood that ART improves survival and general health of HIV-infected persons, and few felt that side effects were a reason not to take ART or questioned its efficacy. However, 51% of women believed that HIV/AIDS was no longer a serious illness given availability of treatment. Furthermore, ART-naive women were more likely than women taking ART women to believe that individuals taking ART should hide their treatment status (24% vs. 12%, P = 0.09), and women taking ART women were more likely than ART-naive women to believe that ART can cure HIV (18% vs. 5%, P = 0.03).

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Psychosocial Experiences After Diagnosis
Disclosure of HIV Status and HIV-Related Stigma

At the postdiagnosis visit, 92% (130 of 141) of women reported that they had disclosed their new positive HIV status. Among women who disclosed, most told a family member (65%), friend (59%), or spouse/partner (39%). Almost two-thirds (63%) of women who disclosed to their spouse/partner said the partner had subsequently sought HIV testing. In structured interviews, 16% of women reported experiencing “some” or “a lot” of stigma since HIV diagnosis.

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Changes in Sexual Behavior After Diagnosis

Three-quarters (75%) of women reported or evidenced some change in sexual activity related to engagement in sex work, number of sex partners, and condom use, with nearly all reporting reduced risk behaviors. For example, 36% of women reported no longer self-identifying as sex workers at the postdiagnosis visit. Furthermore, among women still identifying as sex workers, the median number of clients per week was 3 (IQR: 2-5) at the postdiagnosis visit compared with 10 (IQR: 5-18) among all FSWs at baseline. However, 53% of these women reported using condoms only “sometimes” during the past 30 days.

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DISCUSSION

The majority of newly HIV-diagnosed FSWs in our study had enrolled in HIV-related medical care within 2 years after HIV diagnosis, and most did so within 6 months. Among those who had not enrolled in care, there seemed to be a belief that current immune health or lack of symptoms precluded the need for HIV-related care. About half of women in care reported taking ART at follow-up, including over three-quarters of women who were ART eligible based on CD4 testing at diagnosis. Our rates of linkage-to-care (77% by 1 year, 85% overall) and ART initiation among eligible individuals (77%) were substantially higher than those documented in a cohort of outpatients in Durban, South Africa, in which 39% of ART-eligible individuals initiated treatment within 12 months of diagnosis.7 Our linkage rate was, however, comparable with the rate found in a randomized trial in Uganda of the impact of inpatient HIV testing on rates of linkage to HIV care, where 73.6% of patients diagnosed with HIV in the outpatient setting (control arm) were linked with HIV care within 6 months of testing.17 Our rate was also more or less comparable to a third study of Cape Town area residents diagnosed with HIV between 2004 and 2009, which found a linkage-to-care rate of 62.6% within 6 months of diagnosis.18 Differences in evaluation settings (research clinic, outpatient, community), study design (randomized trial vs. observational), follow-up time, approaches to confirmation of ART initiation (medical chart review vs. self-report), and high rates of pre-ART initiation death in the Durban and Uganda studies might explain the disparate rates. However, our results nonetheless underscore the potential for timely care and treatment in this important most-at-risk-population.

As would be expected, initiation of ART had immunological benefits, with clinically important gains in CD4 count among ART-positive women during the observation period. Similarly, robust responses in CD4 count after ART initiation have been documented in Rwanda and elsewhere.19,20 In contrast, CD4 counts generally declined among ART-naive women. Although we did not collect detailed information on clinical benefits associated with ART, the vast majority of ART-positive women reported health improvements. In general, women had very positive attitudes toward ART. However, reported treatment nonadherence was relatively common in this sample, although similar to levels reported by other studies in Rwanda21 and sub-Saharan Africa.22 The role of structural barriers to adherence (eg, poor access to food, imprisonment of FSWs despite legality of sex work in Rwanda) warrants urgent attention. Although rare, the finding that some women were misinformed about ART eligibility despite meeting CD4 criterion was disconcerting; provider training in national treatment guidelines is critical.

More than one-fifth of these newly HIV-diagnosed women were breastfeeding. Although we did not collect information on whether women attended ANC before delivery, ANC coverage is very high (94%) in Rwanda.11 If women did attend ANC during their pregancy, it is possible that their HIV infections were somehow missed by prevention of mother-to-child transmission. However, given the median 1 year between delivery and HIV screening in this study, it is also possible that women became HIV infected after delivery. Furthermore, nearly one-fifth of the women reported having sought sexually transmitted infection treatment in the 3 months before their HIV diagnosis in this study. This suggests another missed opportunity for HIV testing among this high-risk group.

Information about women's psychosocial experiences since diagnosis underscores the difficulties of receiving an HIV diagnosis in a setting such as Rwanda. Although nearly all women reported having disclosed their HIV status, and many reported emotional and other support as a result, a substantial proportion of women reported experiencing HIV-related stigma. Women's status as sex workers, especially if known within the community, may have increased the likelihood or intensity of stigma and interpersonal problems related to HIV disclosure.

The majority of these HIV-positive women reported reducing sexual risk behaviors after diagnosis, namely ceasing transactional sex. However, two-thirds of women continued to engage in sex work, and a substantial number reported ongoing unprotected sexual contact. There is a clear need for secondary prevention programs, including those focused on “prevention with positives,” among FSWs, including after enrollment in care.23-25

Importantly, this article is one of the first to document experiences with care and treatment among newly HIV-diagnosed FSWs in Rwanda. Furthermore, this analysis combined biologic data with data from structured interviews. Study limitations are also noted. First, sample size was determined by HIV prevalence in the main study and was relatively small. Second, selection bias is possible given that 51 (of 192) women who tested HIV positive at baseline did not return for the postdiagnosis visit within the specified timeframe and were not followed up any further. This group, who was informed of their diagnosis and posttest counseled at baseline, may have been less likely to have linked with care, which could result in overestimated linkage rates in this population. Third, linkage-to-care outcomes for individuals participating in research may not be representative of the referral or linkage patterns for HIV-infected individuals diagnosed as a result of routine medical care or testing initiatives in Kigali. Finally, data on enrollment in care and ART initiation were self-reported. The lack of confirmation of ART status by biologic testing may have resulted in inaccurate estimates of the true proportion of this sample in care or on treatment. However, changes in CD4 counts according to self-reported ART status were consistent with what would be expected. For example, our median 6-month CD4 decline of −14 cells per microliter was comparable to the median yearly CD4 decline of −21.5 cells per microliter reported for a cohort in Tanzania.26

In conclusion, given high rates of HIV infection and high-risk sexual behavior, timely postdiagnosis care and treatment are especially important for FSWs in Rwanda. Marginalization and stigma likely have a negative impact on FSWs' access to health care in general, and barriers may be particularly pronounced for HIV-infected FSWs. However, our study demonstrated that high rates of linkage to care and ART uptake within a short period after HIV diagnosis are possible in this population. Psychosocial support services and secondary prevention initiatives for HIV-infected FSWs in Rwanda, alongside primary prevention for at-risk FSWs, should be scaled up.

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ACKNOWLEDGMENTS

The authors acknowledge the following groups and individuals for their contributions to this study: study participants; Projet Ubuzima study team; Projet Ubuzima Governing Council, specifically Dr Anita Assimwe; Projet Ubuzima Community Advisory Group and community mobilizers; staff at the National Reference Laboratory in Kigali, including John Rusine, and Odette Mukabayire; staff at the Academic Medical Center-Center for Poverty-related and Communicable Diseases, specifically Robert Meester. Funding for the prospective cohort in the main study was provided by the International Partnership for Microbicides, Inc.

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© 2011 Lippincott Williams & Wilkins, Inc.

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