In 2006, the Centers for Disease Control and Prevention recommended routine screening for HIV infection in patients aged 13–64 years in all health care settings where the prevalence of HIV infection is >0.1%.1 HIV-infected persons who do not know their status often present to medical settings and fail to be diagnosed, leading to late detection, higher morbidity, and prolonged transmission risk.2–4 Hospitals and their satellite clinics, therefore, are ideal settings to scale up HIV testing, especially because access to on-site HIV specialists has been shown to improve linkage to care for newly diagnosed and out-of-care HIV-infected patients.5
Historically, a significant barrier to expanding HIV testing in the medical center setting has been the use of testing technologies with long turnaround time, for example, enzyme immunoassay (EIA) testing. EIA testing, conducted in “batches” several times a week, is not well suited to settings with rapid patient turnover, as it may delay appropriate clinical management and has been associated with high failure-to-notify rates.6,7
Rapid HIV testing has the potential to increase testing in medical settings.8 Indeed, rapid HIV testing has been implemented successfully in medical settings such as labor and delivery, the emergency department (ED), and the inpatient wards.9–13 To date, however, the use of rapid HIV testing in medical settings has been limited to specific hospital departments. In addition, these initiatives have generally relied on point-of-care technology requiring ancillary staff, curtailing the ability to provide round-the-clock testing for large numbers of patients. As yet, a system for the effective application of rapid HIV testing across all care settings of a hospital and its satellite clinics has not been demonstrated.
An additional point regarding the adoption of rapid HIV testing is that the optimal testing technology for identifying HIV infection in medical settings has not been determined, especially because acute HIV infection may be relatively common in certain clinical venues, such as the urgent care clinic.14,15 Persons with acute HIV infection are highly infectious and may unknowingly transmit HIV infection if they remain unaware of their status.16–18 Fourth-generation immunoassays that can detect both HIV antibody and p24 antigen are a potentially appealing option. In addition, these assays can be run on automated platforms (as opposed to manual third-generation EIAs).19 However, few data exist on the prevalence of acute HIV infection across all inpatient and outpatient medical settings to justify a universal shift to this more sensitive testing format.
We therefore sought to investigate the potential contribution of acute HIV infection to hospital-wide HIV diagnosis. We drew upon a unique testing system developed at San Francisco General Hospital (SFGH) to execute this project. Key features of this testing system were laboratory-based, round-the-clock, rapid HIV testing on venipuncture specimens from all medical center care settings closely integrated with the services of an HIV clinic–based linkage-to-care team. Building on this system, we developed and implemented a program to screen rapid test–negative specimens for HIV RNA and link acutely HIV-infected individuals to care. Thus, the primary objective of this study was to describe the prevalence of all HIV cases, new HIV diagnoses, and acute HIV infections across medical center sites. Secondary objectives were to (1) determine the increase in HIV case detection conferred by screening for acute HIV infection, (2) calculate rapid test performance characteristics against a “gold standard” of pooled HIV RNA screening, and (3) ascertain disclosure and linkage-to-care outcomes.
We conducted a 6-month cross-sectional study of medical center rapid HIV testing with an algorithm that included pooled HIV RNA testing for acute HIV infection. The implementation of pooled HIV RNA testing and all evaluation procedures were approved by the University of California, San Francisco, Committee on Human Research.
Population, Sites, and Consent Procedures
The study included all patients undergoing HIV antibody testing via the SFGH Clinical Laboratory between November 1, 2008, and April 30, 2009, a period during which there were department-specific initiatives to increase HIV testing in the ED and the adult urgent care clinic. SFGH is a 300-bed acute care public hospital and a major provider for the estimated 150,000 people in San Francisco who have public insurance or are uninsured. HIV testing sites included medical/surgical specialty clinics located on the hospital campus, 18 community health centers, the ED, and all inpatient wards. In accordance with California state law, clinicians obtained verbal consent before rapid HIV testing, which was offered in an opt-in fashion. Several sites using the hospital laboratory for HIV testing were excluded from the pooled HIV RNA protocol because of (1) preference for individually managing patients at risk for acute HIV infection (occupational health, labor and delivery, the nursery), (2) a high number of individuals with known HIV infection (an on-site HIV primary care clinic, an off-site HIV skilled nursing facility), or (3) special administrative requirements (the outpatient jail, research studies).
Rapid Antibody Testing Protocol
The hospital clinical laboratory used the Uni-Gold Recombigen HIV Test (Trinity Biotech, Bray, Ireland) to conduct rapid HIV antibody testing on serum or plasma specimens during every shift, 7 days a week. A negative rapid antibody test was reported as rapid HIV antibody “negative,” and if an additional BD Vacutainer (BD, Franklin Lakes, NJ) plasma preparation tube (PPT) was also collected according to protocol, it was sent to the San Francisco Department of Public Health (SFDPH) Laboratory on the next business day to be placed in the queue for twice weekly pooled HIV RNA testing (Fig. 1). Rapid test results were available in the electronic medical record (EMR) within 2 hours after specimen receipt. A positive rapid HIV antibody result was reported as “preliminary positive.” Rapid test preliminary positive specimens underwent EIA testing with a third-generation test (Genetic Systems HIV-1/HIV-2 Plus O EIA; Bio-Rad, Redmond, WA) Mondays, Wednesdays, and Fridays, and were confirmed with immunoflorescence (IFA) testing (Fluorognost HIV-1 IFA; Sanochemia Pharmazeutika, Vienna, Austria). If the EIA and IFA were both negative, then a final HIV antibody test was reported as “negative.” If the EIA and IFA were both positive, then a final HIV antibody test was reported as “positive.” If the EIA was positive and the IFA was negative or indeterminate, the rapid test specimen was sent to the SFDPH Laboratory for Western blot testing; in addition, if a PPT specimen was available, it was sent to the SFDPH Laboratory for individual HIV RNA testing.
Pooled HIV RNA Testing Protocol
Given the use of pooled HIV RNA testing in public health practice,20–24 the institutional review board and hospital administration did not require separate consent or additional orders for pooled HIV RNA testing. Clinical staff were educated via administrative meetings on the need to draw additional specimen for pooled HIV RNA testing but were not systematically encouraged to target patients with symptoms consistent with acute HIV infection. Sites received monthly reports detailing the proportion of specimens screened for acute HIV infection.
The SFDPH Laboratory assembled aliquots from rapid antibody–negative patients into pooled samples at a 10:1 ratio. Pooled HIV RNA testing was performed twice a week using a qualitative HIV RNA assay (APTIMA HIV-1 RNA; Gen-Probe Inc, San Diego, CA) with a lower limit of detection of 30 copies per milliliter, theoretically permitting detection of individual specimens with 300 copies per milliliter in a master pool with a 1:10 dilution. Positive pools were deconstructed and each individual specimen underwent qualitative HIV RNA testing. Individual HIV RNA–positive specimens were then quantified (Abbott RealTime HIV-1 Assay; Abbott Laboratories, Des Plaines, IL) before being reported as “HIV-1 RNA detected” in the SFGH EMR. EIA-positive/IFA-negative or indeterminate specimens also underwent qualitative HIV RNA testing with subsequent quantification if positive. Negative pools were reported in the EMR as “HIV-1 RNA not detected” within 2–6 days, whereas HIV RNA–positive results were available within 4–8 days of rapid antibody testing.
Procedures for Disclosure and Linkage to Care
The hospital clinical laboratory paged all preliminary positive HIV rapid test results to a linkage-to-care team based in an on-site HIV primary care clinic in real time during business hours (8 AM to 5 PM) and on the next business day for results reported on evenings and weekends. Patients on the hospital campus were eligible for linkage-to-care team services (Fig. 2). For both admitted and nonadmitted patients, the linkage-to-care team, which consisted of a nurse, nurse practitioner, and social work associate, worked with the ordering clinician to ensure disclosure. Ordering clinicians were encouraged to disclose with linkage team support, but linkage team members also disclosed results directly, especially if the ordering clinician was not available. For patients still on-site, the linkage team met with the patient to provide counseling and an appointment for confirmatory results. For outpatients with preliminary positive results reported on nights or weekends, the linkage-to-care team contacted ordering clinicians and patients within 1 business day to ensure disclosure and a follow-up appointment. With regard to pooled HIV RNA results, the SFDPH Laboratory notified the ordering clinician, the linkage-to-care team, and the SFDPH HIV notification and partner services unit when specimens were confirmed RNA-positive.25 For patients with prior HIV diagnoses, the linkage-to-care team ascertained care status through review of EMR appointment data and direct patient query.
Data Collection and Analyses
We obtained test data and demographics on all individuals undergoing HIV testing from the EMR and laboratory databases. For individuals with confirmed HIV infection, we assessed testing history, HIV care status, and linkage to care, defined as attendance at 1 outpatient HIV-related visit at any time, using the EMR, linkage-to-care team logs, and laboratory/public health databases. As outlined previously, patients with EIA/IFA-positive results were considered to have confirmed HIV infection. Acute HIV infection was defined as being (1) EIA-negative/HIV RNA–positive, (2) EIA-positive/IFA-negative/HIV RNA–positive, or (3) EIA-positive/IFA-indeterminate/HIV RNA–positive. We report data on the total number of tests processed by the hospital laboratory and the number of tests from sites eligible for pooled HIV RNA testing, along with test outcomes and the proportion of HIV diagnoses considered to be new (previously unknown). The increase in HIV case detection attributable to pooled HIV RNA testing was calculated using only those samples with adequate specimen available for further testing. Rates of disclosure and linkage to care were calculated considering HIV-infected inpatients and outpatients who were tested on the hospital campus and thus eligible for linkage team services. Descriptive statistics were calculated using Stata SE/10 (Stata Corp, College Station, TX). Test performance characteristics were calculated using an open-source software program (OpenEpi, version 2.3.1; Emory University Rollins School of Public Health, Atlanta, GA).
Prevalence of HIV Infection Among Hospital System Testers
Between November 1, 2008, and April 30, 2009, there were 9938 specimens rapid tested for HIV antibody by the hospital clinical laboratory (Table 1), of which 8550 specimens were from patients seen at sites participating in pooled HIV RNA testing (5809 specimens from the hospital campus and 2741 specimens from 18 off-site community clinics). These 8550 specimens were drawn from 7927 unique patients. Approximately 76,811 unique patients were seen at testing sites during the study period; thus, ∼10% of patients were tested for HIV. Patients had a median age of 40 years (interquartile range: 28–52 years), were evenly divided between men and women, and were 61.8% racial/ethnic minority (Table 2). As detailed in Table 1, there were 137 cases of HIV infection [prevalence 1.7%, 95% confidence interval (CI): 1.5% to 2.0%] from sites participating in pooled HIV RNA testing (134 confirmed HIV infections, 2 acute infections with inconclusive antibody results, and 1 antibody-negative acute infection). Of these 137 cases, there were 46 (33.6%) new diagnoses of HIV infection, for a prevalence of newly diagnosed HIV infection = 0.58% (95% CI: 0.43% to 0.77%) and a prevalence of acute HIV infection = 0.05% (95% CI: 0.01% to 0.14%; as calculated by dividing the acute cases by the number of unique individuals undergoing pooling). The median CD4 cell count for newly diagnosed patients was 331 cells per microliter (interquartile range: 260–517 cells per microliter). Half of the cases of new HIV infection were from the ED or adult urgent care clinic. Indeed, the 3 cases of acute HIV infection were from the ED, the adult urgent care clinic, and a “drop-in” visit at a community health center. All were Latino men who identified their HIV risk factor as having sex with men. When considering just the yield of new and acute cases from the ED and adult urgent care clinic, estimates doubled to 1.2% (95% CI: 0.8% to 1.9%) and 0.1% (95% CI: 0.01% to 0.4%), respectively.
Performance of Rapid HIV Testing Versus Rapid Testing Plus HIV RNA Testing
Pooled HIV RNA testing was performed on 6704 (78.4%) specimens from HIV rapid test–negative patients. Compliance with specimen submission, defined as submission of both a rapid test specimen and the PPT necessary for pooled RNA testing, increased from 54.4% in the first month of the observation period to 87.0% in the last month. The number of monthly rapid HIV tests from the hospital campus rose from 632 during the first month of the study to 1101 during the last month of the study. Although the rapid test plus HIV RNA testing algorithm identified 3 cases that met our study definition of acute HIV infection, only 1 of these was rapid test–negative/HIV RNA–positive (1 was rapid test–positive/EIA-positive/IFA-negative/HIV RNA–positive and 1 was rapid test–positive/EIA-positive/IFA-indeterminate/HIV RNA–positive). All had quantitative viral loads >500,000 copies per milliliter and subsequent complete seroconversion (Fig. 1). The single rapid test–negative/HIV RNA–positive specimen was also negative on a third-generation EIA test. Using the number of confirmed cases sent with a PPT tube (and hence eligible for pooled HIV RNA screening had these specimens been rapid test–negative) as the denominator, these 3 cases represented 3.5% of all HIV cases and 10.3% of new HIV cases. However, because 2 of the 3 acute HIV cases would have been detected (though not confirmed) by the rapid test alone, the addition of pooled HIV RNA screening identified only 1 case that would have been completely missed, representing 1.2% of all cases and 3.5% of new cases.
The performance of the Uni-Gold rapid HIV test was assessed using EIA/IFA/HIV RNA testing as the gold standard. The sensitivity of the rapid test was 98.9% (95% CI: 93.8% to 99.8%) and the specificity 99.9% (95% CI: 99.7% to 99.9%). The positive predictive value was 90.5% (95% CI: 82.0% to 94.9%) and the negative predictive value 100% (95% CI: 99.9% to 100%).
Disclosure and Linkage-to-Care Outcomes
There were 98 patients with a preliminary positive rapid HIV test result diagnosed on the hospital campus and thus eligible for linkage-to-care team services (Table 1). Of these patients, 12 had a false-positive rapid HIV test result and 1 was an infant with maternal antibodies and a negative quantitative HIV viral load, whereas 54 rapid test results were in patients who proved to have confirmed, previously diagnosed HIV infection (Fig. 3). Of the 31 patients who were rapid test–positive and subsequently confirmed as new HIV diagnoses, 9 admitted patients and 18 of 22 outpatients received their test results during the same clinical encounter. Of the remaining 4 outpatients, 3 patients were disclosed to 5–9 days later and 1 learned his diagnosis after re-presenting to the ED for care. The 1 patient with rapid test–negative/HIV RNA–positive acute HIV infection received his final test results 1 week after testing negative on the rapid test. This patient was already in care with a community physician with HIV expertise. All newly diagnosed patients who lived in the county and did not have insurance incompatible with the SFGH clinic system were confirmed as linked to care. Time to linkage was calculated as time from diagnosis to first outpatient HIV visit except for those patients admitted after diagnosis, in which case time to linkage was time from hospital discharge to first outpatient HIV visit. The median time to linkage to care was 3.5 days (interquartile range: 2–8.5 days; range: 0–70 days). Of those with prior HIV diagnoses, the majority (74%) were in care. Of the 12 patients who were not in care, 11 were relinked to care. Thus, the overall proportion of patients linked to care was 97.5% (95% CI: 86.8% to 99.9%).
We leveraged the novel features of a hospital laboratory–based rapid testing system to add pooled HIV RNA testing for a period of 6 months. We found that screening for acute HIV infection in rapid test–negative patients from an urban medical center contributed only minimally (1.2%) to the total number of HIV cases identified. Perhaps more importantly, we found that by using round-the-clock rapid testing, the hospital laboratory was able to provide preliminary results that had both high positive and negative predictive values within 2 hours of specimen receipt. Use of an HIV clinic–based linkage-to-care team resulted in very high rates of linkage to care. These results support round-the-clock, laboratory-based rapid testing as a successful approach to medical center HIV testing. In addition, this testing system has the potential to sustain efforts to expand HIV testing, as it provides these round-the-clock and rapid results without requiring dedicated staff to conduct point-of-care testing.
This study demonstrated that there are several clinical locations, particularly those that provide drop-in care, that diagnose a large number and proportion of new HIV infections. Half of the new HIV infections in this study were identified in the ED and adult urgent care clinic, including 2 of the 3 acute infections. In these important sites of health care for vulnerable urban populations,2 scaling up testing to identify new and acute cases remains a challenge, as busy providers in these settings face numerous barriers to performing HIV testing.26 Screening for acute HIV infection by pooled HIV RNA testing requires too lengthy a turnaround time to guide clinical management in real time. However, the recent US Food and Drug Administration approval of 2 fourth-generation immunoassays offers the potential for both acute HIV screening and relatively fast (perhaps same-day) test turnaround.27 Indeed, a preliminary recommendation for new laboratory HIV testing guidelines advocates for screening with the most sensitive immunoassay available, that is, a fourth-generation test, followed by an antibody test that can distinguish between HIV-1 and HIV-2.28,29
However, several points bear mentioning. First, even same-day results may not be fast enough for locations such as the ED and urgent care clinic, where a cornerstone of HIV testing has been the availability of truly rapid results. Second, the fourth-generation tests currently available in the United States do not distinguish between acute and established HIV infection, making it necessary to investigate the discordance between a reactive fourth-generation test and a negative confirmatory test (such as a Western blot) with HIV RNA testing. In our study, 2 of 3 acute infections were positive, negative, or indeterminate for the rapid test by confirmatory IFA testing, and RNA-positive. These 2 cases highlight the importance of resolving discordant test results.
Although screening for acute HIV infection may be important in the ED and urgent care clinic, its impact in other medical settings will likely be less pronounced. In the inpatient setting—and even in many outpatient clinics—HIV testing is frequently used to confirm a patient’s HIV status, as prior test results may not be readily available and clinical management decisions need to be made. In our study, two thirds of patients testing HIV-positive were found to have previously tested HIV-positive. Reasons for this finding bear further investigation but may include the need to document HIV status, lack of immediate disclosure of HIV status, and denial of HIV status. Moreover, some previously diagnosed HIV-infected individuals had lapsed in care, and reporting positive rapid test results to the linkage team facilitated effective reengagement for these patients.
Indeed, the ability of the testing system to facilitate linkage team follow-up of positive HIV test results in real time and across a range of hospital settings is a unique feature that merits attention. As hospitals and acute care settings look for sustainable and cost-effective ways to scale up HIV testing, we believe elements of this testing system hold great promise, with or without screening for acute HIV infection.
There were several limitations to our analysis. This was a laboratory-based study designed to screen for acute HIV infection, rather than an effort to actively promote hospital-wide HIV case finding. Because not all medical center patients were tested for HIV, the true prevalence of acute and nonacute HIV infection is not known. Furthermore, because this was an observational study, we cannot evaluate the separate effects of rapid testing, pooled RNA screening, and the linkage-to-care team on patient outcomes. Finally, we do not formally assess labor requirements and cost, although we are able to document that this rapid testing system allowed the hospital campus to nearly double the monthly number of tests without need for additional laboratory staff while maintaining excellent diagnostic test performance.
Clinical laboratory-based rapid HIV testing with integrated linkage to care works well for many medical settings and has the potential to sustain HIV testing efforts. However, patients in certain clinical venues, such as the ED and the urgent care clinic, may benefit from being screened for acute HIV infection. Although pooled RNA testing can aid in the detection of acute HIV infection, its long turnaround time may limit its application in these settings. Fourth-generation immunoassays performed in a rapid fashion may be one option for these locations.
The authors thank the following individuals, without whom this project and its evaluation would not have been possible: Diane Jones, Clarissa Ospina-Norvell, and Alida Marrero-Calderon of the San Francisco General Hospital Positive Health Program for their dedication in linking HIV-infected patients to care; Sally Liska of the SFDPH Laboratory for technical guidance; and Fred Strauss of the San Francisco General Hospital for medical informatics support. For the data used in this study, the authors thank Margaret Wong of the San Francisco General Hospital Clinical Laboratory; Paul Norris and Ketty Mobed of the University of California, San Francisco, The Health Record Data Service program; and Kyle Bernstein and Robert Kohn of the SFDPH STD Prevention and Control Services. They thank Wendy Hartogensis of the San Francisco General Hospital HIV/AIDS Division for assembling the final data sets and Jane Drake of the University of California, San Francisco, Global Health Sciences for administrative support.
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Keywords:© 2013 Lippincott Williams & Wilkins, Inc.
HIV serodiagnosis; HIV rapid tests; acute HIV infection; HIV testing in medical settings