In 2008, an estimated 1.9 million deaths were attributable to HIV/AIDS in sub-Saharan Africa.1 HIV-infected individuals from this region usually present for care late and thus commence antiretroviral therapy (ART) with advanced immunodeficiency, thereby increasing their risk for HIV-related mortality.2–7 An earlier HIV diagnosis followed by timely initiation of HIV care can help maximize health benefits. HIV testing remains the entry point to a continuum of HIV medical care and social support.1 Over the past few years, the number of HIV testing sites has been scaled up significantly.1 However, increasing testing is of little use without strategies to direct newly diagnosed HIV-positive (HIV+) patients to appropriate packages of HIV care. In South Africa, HIV+ adults with baseline CD4 counts ≤200 cells per microliter or in World Health Organization's (WHO) clinical stage IV are considered ART eligible, whereas those above these thresholds are required to remain in pre-ART care until eligible.
There is a dearth of published literature on retention in ART programs, yet a few studies have examined linkage to HIV care. Nonetheless, recent studies have shown that linkage to care from traditional HIV testing points at stationary facilities is often inadequate and varies across sites.8–13 Factors known to enhance enrollment to care at these sites include use of referral forms, transportation allowances, and community escorts.12 The main predictors of nonlinkage to HIV and ART care from these facilities include unemployment;8 user fees;8 distance of clinic;10,12 transport costs;12 lack of education;14 history of tuberculosis (TB) treatment;10 referral by health care providers10; and being male,11 a young adult,11 or a patient with TB.11 Noteworthy is that failure to access care is prominent among those with lower CD4 counts8 and individuals self-referred for testing.11 Successful interventions resulting in earlier diagnosis of HIV must also be accompanied by strategies that enhance linkage into HIV care to improve health outcomes.
Mobile HIV testing services have been shown to facilitate testing of individuals earlier in their stage of HIV infection and to be more accessible to hard-to-reach and high-risk populations.15–19 Moreover, streamlined HIV counseling and testing (HCT) procedures offered by mobile services allow for a high number of individuals to be screened.15–19 Evidence indicates that in comparison to stationary testing facilities, mobile testing units are cost effective in diagnosing new cases of HIV.19 However, ongoing HIV care may not be sustainable from mobile units, therefore requiring patients to be referred to stationary facilities for the necessary follow-up care. Furthermore, it is possible that linkage to facility-based care from these units is inadequate because of their mobile nature.12
To date, no study has assessed the extent to which people diagnosed with HIV in mobile testing units link to HIV medical care at public health care facilities. Understanding the associated challenges of linkage to HIV care from mobile units is important if this mobile approach is to be considered for the expansion of HCT. The aim of this study was to assess the proportion and characteristics of individuals who accessed HIV care after testing HIV+ in a mobile testing unit. We investigated whether disease progression (as defined by CD4 count) influenced access to care, and we described the barriers of linkage to care.
Individuals diagnosed with HIV (for the first time) at the mobile unit during a 16-month period were identified retrospectively through mobile unit records. Those who received their laboratory CD4 count result were prospectively followed up to assess linkage to HIV care.
Setting and Population
A nurse-run and counselor-supported mobile testing unit, as described elsewhere,15 provided free HCT services to underserved communities within the Cape Metropolitan Region, Western Cape, South Africa.
Client-initiated HCT was offered in combination with free screening for other chronic conditions (ie, hypertension, diabetes, and obesity) and TB to a predominantly black Xhosa-speaking African population. HCT was performed according to the Provincial Government guidelines.20 Individuals who consented to rapid HIV testing and tested positive were subsequently clinically staged and underwent laboratory CD4 count testing.
After the completion of testing, individuals received a referral letter to take to a health care provider to facilitate their access to HIV care. Nurses detailed all conditions that the individual was referred for in this letter (ie, HIV/ART care, concomitant medical problems, and/or screening for other conditions). When CD4 counts became available (usually within 72 hours), patients were contacted telephonically and received their results. If contact numbers were unavailable, home visits were done or a letter was sent to the patient, requesting the individual to contact the counselor for their result. Once contact was established, the CD4 count result was received and implications discussed. All HIV+ patients were encouraged to attend clinics either for HIV care or to start ART if eligible according to the South African National Guidelines21 and other non–HIV-related health services if necessary. The aforementioned procedures were followed for all HIV+ patients.
Records of all those who were newly diagnosed with HIV between August 2008 and December 2009 were accessed and retrospectively reviewed to identify an eligible cohort (Fig. 1). Only those who were newly diagnosed with HIV (≥18 years of age) on the mobile unit within the Cape Metropolitan region and had a laboratory CD4 count done were eligible for follow-up. The majority of newly diagnosed HIV+ individuals diagnosed on this mobile unit have CD4 counts >350 cells per microliter.15 Due to a higher proportion of patients in this stratum, a stratified random sample was drawn. We sampled 100% of individuals with laboratory CD4 counts ≤350 cells per microliter and 30% of individuals with laboratory CD4 counts >350 cells per microliter.
Follow-up for Assessment of Linkage to HIV Care
Eligible individuals who had previously received their CD4 count result were telephoned or interviewed in person between April and June 2010, to obtain informed consent (Fig. 2). At least 3 telephonic attempts were made to track the participant, and if no contact number was available, a home visit was conducted. A questionnaire was subsequently administered to those consenting to participate. Clinical and socio-demographic data were collected by mobile unit record reviews and interviews.
Verification of Self-reported Linkage to HIV Care
A retrospective clinic folder review was conducted at respective public health care facilities on participants who reported that they were linked to medical care, once additional consent was acquired for this process (Fig. 2).
Informed consent (written or verbal) was obtained from participants. Data collection and analysis were approved by the University of Cape Town's Research Ethics Committee and the Provincial Government of the Western Cape's Research Ethics Committee.
Laboratory CD4 Count Result Received
A newly diagnosed HIV+ individual who was tested at the mobile unit and was subsequently successfully contacted (telephonically or by home visit) and received his/her laboratory CD4 count test result.
Linked to Care
A newly diagnosed HIV+ individual who accessed HIV care at a public health care facility at least once after testing on the mobile unit.
Presence of TB Symptoms
A newly diagnosed HIV+ patient who had one or more TB symptoms (ie, cough or fever for >2 weeks, weight loss of >1.5 kg in the last month, drenching night sweats, loss of appetite, and blood-stained sputum).
Disclosure of HIV Status
A newly diagnosed HIV+ patient who had disclosed his/her status to at least one other.
Data were double entered into EpiData Entry (Version 3.1), and analysis was carried out using STATA (Version 11.0; Stata Corporation LP, College Station, TX). Data were first explored via cross-tabulations and χ2 tests. Total proportions were calculated taking sampling weights into account. Baseline characteristics of the stratified random sample (N = 192) were used to identify correlates of receiving a laboratory CD4 count result through a binomial regression. Variables that had 10% significance in the bivariate analysis were included in the multivariate model. In addition, clinical and socio-demographic variables of all participants (n = 77) were examined to ascertain those that best predicted linkage to care through a binomial regression, using bivariate analysis only. All variables in the regression analysis were controlled for laboratory CD4 count strata.
A total of 6738 records of individuals accessing the mobile service (51.2% female) between August 2008 and December 2009 were available (Fig. 1). The overall prevalence of those newly diagnosed with HIV was 6.9% (463 of 6738). Only 376 (81.2%) of these newly diagnosed HIV+ individuals met the study's inclusion criteria. A stratified random sample (N = 192) was then drawn from this cohort (N = 376): 36 of 36 individuals with CD4 counts ≤200 cells per microliter, 80 of 80 individuals with CD4 counts between 201 and 350 cells per microliter, and 30% of individuals with CD4 counts >350 cells per microliter (76 of 260) were sampled.
Baseline Characteristics of Individuals in the Stratified Random Sample
Of the 192 newly diagnosed HIV+ individuals sampled, majority was women (60.5%) and the mean age was 34.8 years (Table 1). In total, 60.2% had tested for HIV previously. The mean CD4 count was 488.6 cells per microliter, majority (60.4%) was WHO clinical stage I, and the mean body mass index was 26.7 kg/m2. Furthermore, TB symptoms occurred in 20.7% of individuals, and only 18.2% of individuals could not provide a contact telephone number.
Predictors for Receiving a Laboratory CD4 Count Result
A total of 73% of individuals received their CD4 count (Table 1). Receipt of a CD4 count result was 0.82 times less likely for individuals with CD4 counts >350 cells per microliter compared to individuals with CD4 counts ≤350 cells per microliter [95% confidence interval (CI): 0.69 to 0.98] (Table 2). Being a woman, having access to a cell phone, and having lower CD4 counts were factors that increased the likelihood of receiving CD4 count results in the bivariate analysis. Results were similar in the multivariate analysis: individuals with a CD4 count >350 cells per microliter were 0.85 times less likely to receive their CD4 count result (95% CI: 0.73 to 0.99). Availability of a cell phone made a successful contact twice as likely.
Baseline Characteristics of Individuals Lost to Follow-up
Of the 145 individuals eligible for follow-up, 56 (42.4%) were untraceable, despite previously having been successfully contacted and received their CD4 count result (Fig. 1). This included 13 with CD4 counts <200 cells per microliter (46.4%), 20 with CD4 counts in the mid range (32.3%), and 23 with CD4 counts >350 cells per microliter (51.1%). The majority were women (52.9%) with a mean age of 34.2 years, mean body mass index of 26.5 kg/m2, mean CD4 count of 458.3 cells per microliter, and in WHO clinical stage I. Moreover, TB symptoms were prevalent in 16% and most (95.1%) had access to a cell phone.
Characteristics of Study Participants
Seventy-seven newly diagnosed HIV+ individuals who received their CD4 count result participated (Table 3). Most of these individuals completed primary school (84.8%). Unemployment was more prevalent in individuals with CD4 counts ≤200 cells per microliter (76.9%) compared to individuals with CD4 counts >350 cells per microliter. Of the 69.3% who disclosed their HIV status, only a small proportion (10.9%) felt stigmatized after disclosing. The majority of participants (73.8%) rated their health status as “strong.”
Linkage to HIV Care
Overall, 52.5% (49) accessed HIV medical care (Table 3). There was an inverse relationship between CD4 count result and linkage to care: all of those with CD4 counts ≤200 cells per microliter linked to care; however, 66.7% and 36.4% of those with CD4 counts between 201 and 350 and >350 cells per microliter, respectively, linked to care. Among those who accessed care, the majority (71.0%) stated that the mobile unit's referral letter facilitated their linkage to care at a public health care facility. The overall mean time from diagnosis to accessing HIV care was 2.2 months. Those with CD4 counts ≤200 cells per microliter took on average less than a month (3 weeks) to access care, whereas those with CD4 counts >350 cells per microliter took a mean time of 3 months. Of those with CD4 counts ≤200 cells per microliter, 69.2% started ART within 2 months of diagnosis and the remaining 30.8% were within the ART screening process.
Verification of Self-reported Linkage to HIV Care
Among the 49 who linked to care, 43 (88%) provided additional consent to access their clinic folders at respective public health care facilities. Eight (19%) of these folders were untraceable. A validation of the 35 (81.4%) clinic folders, which were traced, showed that the sensitivity of self-reported linkage to care was excellent (100%).
Predictors of Accessing HIV Medical Care
Those contactable patients with CD4 counts >350 cells per microliter were 0.49 times less likely to link to care compared to individuals with CD4 counts ≤350 cells per microliter (95% CI: 0.27 to 0.87) (Table 4). In the bivariate analysis, individuals who had TB symptoms and who had disclosed their HIV status were more likely to link to care, whereas those employed were less likely.
Barriers of Linking to HIV Care
The most common stated barrier (41.4%) to linking to care was the inability to access public health care facilities during working hours, and many participants reported that they could not get time off work (Table 3). Other barriers included fear of toxicity and side effects of ART (12.6%) and stigma and fear of disclosure (8.8%).
Losses can occur at critical phases in the cascade from HIV testing to care. This study highlights the challenges of contacting newly diagnosed HIV+ individuals accessing a mobile testing service to inform them of their CD4 count result and the poor linkage to HIV care among those with higher CD4 counts. However, results also indicate that linkage to care among those eligible for ART from this mobile unit is higher than that reported in studies examining linkage from stationary facilities.
Approximately 27% of newly diagnosed HIV+ individuals who underwent CD4 count testing at the mobile unit did not receive this test result. Failure to receive a baseline CD4 count could result in delays in entering into HIV care. Our findings indicate that a CD4 count result of ≤350 cells per microliter, availability of a cell phone, and being female increased one's likelihood for receiving a CD4 count result. Other recently conducted studies in South Africa have shown poor return for CD4 count results particularly in patients with higher CD4 counts.9,10 In our study, the CD4 count variable was adjusted for in the model as it is conceivable that due to the urgency for ART-eligible patients to link to care, personnel may have placed more emphasis on following up this stratum of patients with their result, despite protocol; additionally, these patients may have felt unwell at the time of diagnosis and therefore might have actively facilitated the receipt of their result. Overall, these data underscore the difficulties faced in following up clients after blood is drawn for laboratory CD4 testing and the value of point-of-care CD4 count testing in mobile units and in stationary facilities to attenuate the high attrition occurring between HIV diagnoses and receiving a CD4 count result.
All individuals diagnosed HIV+ on this mobile are given a referral letter to actively seek care. In our study, linkage to care among the ART-eligible patients who could be traced was 100%, albeit a small sample size. This finding was unexpectedly higher than studies assessing linkage to care in stationary facilities as these found a 30%–80% linkage among ART-eligible individuals.8–13
We showed that there was a delay from time of diagnosis to initiation of ART, in that 30.8% of these individuals were still waiting to commence ART after 2 months post diagnosis. This period of ART initiation delay is consistent with findings from South Africa (3–6 months),8–11 Mozambique (3 months),13 and Malawi (22 days after screening).14 This indicates the need for further interventions, if recommendations of shortening treatment readiness programs and prioritizing those with advance disease are met.8 In contrast, we found that linkage to care among those with higher CD4 counts was poor as more than 60% of those with CD4 counts >350 cells per microliter failed to access care. This is similar to the findings from 2 South African studies conducted in stationary services;9,11 however, there is a paucity of studies assessing linkage to care among ART-ineligible patients. More data and possibly better interventions in this category are required as test and treat strategies are contemplated for reduced population HIV transmission.
Our results also illustrate that having a higher CD4 count, no TB symptoms, not disclosing an HIV+ status, and being employed increased one's risk for not linking to care. Patients who are physically well may not perceive the need to register for follow-up care, especially those in the higher CD4 count bracket as evidenced in this study. Hence, linkage to care at health care facilities maybe considerably higher than mobile services because patients presenting at these sites have advanced disease compared with those accessing mobile services.15 Those patients with lower CD4 counts and TB symptoms were possibly more motivated to link to care because of their weakened physical condition at the time of diagnosis or mobile unit staff may have put greater emphasis on the urgency to link to care based on their clinical results. Furthermore, unemployment was the highest among individuals with CD4 counts ≤200 cells per microliter; hence, these individuals may have had time during the day to access clinics.
The main barriers of linkage to HIV and ART care from stationary facilities have been well established; these include transportation costs,12 being male,11 and having a low CD4 count.8 This is the first study, to our knowledge, that has assessed barriers to linkage from a mobile unit. The fact that clinics are inaccessible outside working hours was identified as a major barrier to linkage to care from a mobile unit. The mobile unit, unlike state run facilities, does operate outside of traditional working hours and hence may have accessed clients who would not have tested due to difficulties with clinic operating hours. It is likely that those who access the mobile unit outside working hours and on weekends have difficulty in subsequently linking to care at a public health care facility. Thus, extending service hours to evenings and weekends at public clinics and establishing workplace programs through mobile units might improve linkage to care among the working population. In addition, more thought into the type of messaging delivered to those with higher baseline CD4 counts and the type of services offered while waiting for ART eligibility are warranted. This study would suggest that at least adequate advice and support on disclosure of an HIV+ status might improve linkage to HIV wellness programs.
Our findings are subject to several limitations. The small sample size limited the power to detect associations particularly in the group of individuals with CD4 counts ≤200 cells per microliter. Furthermore, a multivariate analysis for the assessment of predictors of linkage to care could not be conducted due to insufficient power. Notably, we were unable to track 42.4% of the eligible participants despite multiple follow-up attempts that might have resulted in a biased estimate. The strata with <200 and >350 CD4 cells per microliter had the greatest proportion of uncontactable patients. The challenges we encountered in following up HIV+ patients were exacerbated by the fact that this study was conducted 6–18 months after their HIV+ diagnosis and were similar to those highlighted in an earlier study conducted in South Africa. These include incorrect contact details, lost cell phones, disconnected cell phone numbers, and changes in physical address.8 It is likely that the proportion deceased in our study maybe underestimated as the high number of disconnected cell phone numbers is perhaps indicative of death particularly in the more advanced patients.8 We were unable to trace 19% of patient folders to validate clinic attendance as these were either misplaced at the clinic or participants provided us with incorrect clinic information. Recall and social desirability bias may have also influenced findings pertaining to disclosure, clinic visit, reasons for failing to link to care and self-assessment of one's current health, and the mobile unit.
Strengths of the study included that self-reported linkage to HIV care was verified through clinic folder reviews, and experienced HIV/AIDS counselors conducted follow-ups. Trained bilingual counselors were employed to minimize respondent bias, and no incentives were received for participation. The mobile HIV testing services and HIV care at public health care facilities that these individuals accessed were free of charge; therefore, our results could be generalized to a similar setting.
In conclusion, findings from this study indicate that linkage to care from a mobile testing unit is feasible. In the cascade from HIV testing to care, one area of attrition is the delivery of CD4 count results that can be remedied with the use of reliable point-of-care CD4 count testing. Linkage to HIV care was shown to be inversely related to CD4 count result. This will need to be addressed in the setting of test and treatment interventions. Of note, ART-eligible patients linked to care best, but this study also indicates delays in ART commencement among these patients, which could adversely affect outcomes. Other areas for intervention include improving health care access for employed HIV-infected individuals, and ensuring health staff emphasize the need to link to care despite feeling well and having a high CD4 count.
The authors would like to acknowledge all those who sacrificed their time to participate in this study. The authors are indebted to the dedicated study staff, Tutu Tester Project, and staff at Desmond Tutu HIV Foundation. The authors are also thankful to all public health care facilities within the Cape Metropolitan region that kindly assisted us with patient folder reviews.
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