JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Prevention
Accuracy of Definitions for Linkage to Care in Persons Living With HIV
Keller, Sara C. MD, MPH*,†; Yehia, Baligh R. MD, MPP, MSHP†; Eberhart, Michael G. MPH‡; Brady, Kathleen A. MD‡
*Center for Healthcare Improvement and Patient Safety and
†Division of Infectious Diseases, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA; and
‡City of Philadelphia Department of Public Health, AIDS Activities Coordinating Office, Philadelphia, PA.
Correspondence to: Sara C. Keller, MD, MPH, Center for Healthcare Improvement and Patient Safety and Division of Infectious Diseases, Perelman School of Medicine, University of Pennsylvania, 230 N 21st Street, Unit 907, Philadelphia, PA 19103 (e-mail: email@example.com).
Supported by an unrestricted grant from the Agency for Healthcare Research and Quality, Grant (GIM) 400-4239-4-555854-XXXX-2446-2192 (S.C.K.).
Portions of these data were presented at ID Week 2012, 2012, San Diego, CA.
S.C.K. was supported by an unrestricted grant from the Agency for Healthcare Research and Quality (AHRQ), Grant (GIM) 400-4239-4-555854-XXXX-2446-2192. B.R.Y. was supported by the National Institutes of Health/Institute of Mental Health (K23-MH-097647-01A1). K.A.B. was supported by a Health Resources and Services Administration Ryan White Grant (H89HA0013) and by a Centers for Disease Control and Prevention grant for FOA PS08-802 (5U62PS001044-04). M.G.E. has no conflicts of interest to disclose.
S.C.K. designed the study, acquired the data, performed statistical analyses, performed the data analysis and interpretation, drafted the manuscript, and provided critical revision of the manuscript for important intellectual content. M.G.E. performed statistical analyses, provided administrative support, acquired data, and provided critical revision of the manuscript for important intellectual content. B.R.Y. performed data interpretation and provided critical revision of the manuscript for important intellectual content. K.A.B. assisted in study design, performed data interpretation and provided critical revision of the manuscript for important intellectual content.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.jaids.com).
Received January 21, 2013
Accepted April 10, 2013
Objective: To compare the accuracy of linkage to care metrics for patients diagnosed with HIV using retention in care and virological suppression as the gold standards of effective linkage.
Design: A retrospective cohort study of patients aged 18 years and older with newly diagnosed HIV infection in the City of Philadelphia, 2007–2008.
Methods: Times from diagnosis to clinic visits or laboratory testing were used as linkage measures. Outcome variables included being retained in care and achieving virological suppression, 366–730 days after diagnosis. Positive predictive value (PPV), negative predictive value (NPV), and area under the curve (AUC) for each linkage measure and retention, and virological suppression outcomes are described.
Results: Of the 1781 patients in the study, 503 (28.2%) were retained in care in the Ryan White system and 418 (23.5%) achieved virological suppression 366–730 days after diagnosis. The linkage measure with the highest PPV for retention was having 2 clinic visits within 365 days of diagnosis, separated by 90 days (74.2%). Having a clinic visit between 21 and 365 days after diagnosis had both the highest NPV for retention (94.5%) and the highest adjusted AUC for retention (0.872). Having 2 tests within 365 days of diagnosis, separated by 90 days, had the highest adjusted AUC for virological suppression (0.780).
Conclusions: Linkage measures associated with clinic visits had higher PPV and NPV for retention, whereas linkage measures associated with laboratory testing had higher PPV and NPV for retention. Linkage measures should be chosen based on the outcome of interest.
Persons living with HIV (PLWH) must fulfill several steps along the care continuum to achieve optimal clinical outcomes (Fig. 1 ).2–4 Individuals should be screened for HIV; however, 20% of PLWH in the United States are unaware of their diagnosis.5 Linkage to care is then necessary, but only 77% of individuals link to care.1–3,6 Patients must remain in care; yet, 50%–75% of those linked to care meet the US Health Resources and Services Administration (HRSA) retention criteria of ≥2 visits separated by 90 days in a year.1,2,7–10 Finally, PLWH need to receive and adhere to antiretroviral therapy (ART). Navigating all these steps is often unsuccessful11: only 28% of those with HIV achieve virological suppression.12
Linkage to care is a critical step in this process.13–15 However, no consistent definition of linkage to care exists. Previous studies have defined linkage to care as attending ≥1 clinic visit for HIV care within 1–6 months of diagnosis16–35 or ≥2 visits within 6–12 months of diagnosis.36–38 Other researchers have used laboratory monitoring data—CD4 T-cell counts and HIV-1 RNA levels—to investigate linkage to care, defining linkage as the occurrence of laboratory testing within 1–6 months of diagnosis,39–41 ≥21 days after diagnosis,42 or within 12 months of diagnosis.43 In addition, governmental agencies and professional organizations differ in how they measure linkage. The US National HIV/AIDS Strategy defines linkage as laboratory testing within 90 days of diagnosis,44 whereas the Emergency Department National HIV Testing Consortium defines linkage as a clinic visit within 30 days of diagnosis.27
Linkage rates have similarly varied among single-clinic or multisite cohort studies, from 38% to 100%, depending on the linkage criteria used.45,46 Few studies have been community based. A King County, Washington, study examined the timing of linkage to HIV care countywide47 but did not specifically address the predictive ability of linkage metrics. A recent study looked at the predictive ability of 2 linkage criteria (having either 1 or 2 laboratory tests within a year of diagnosis) for retention in care but did not evaluate other linkage definitions.43
To effectively monitor and improve linkage to care, a better understanding of the predictive accuracy of linkage to care measures for retention and virological suppression is necessary. To determine the diagnostic accuracy of linkage measures to predict retention in HIV care and HIV virological suppression, we compared clinic visit and laboratory testing based linkage measures using a city-wide cohort.
Data Sources and Study Population
The enhanced HIV/AIDS reporting system (eHARS)48 and the Ryan White CAREWare dataset (CAREWare) were combined. Philadelphia has used eHARS, a Centers for Disease Control and Prevention database to which all new HIV diagnoses are reported, for mandated name-based case reporting since 2009. Local mandates require reporting of CD4 T-cell counts <350 cells/mL and HIV-1 RNA levels to the Department of Public Health (DPH), which are electronically imported into eHARS.48 Thus, eHARS contains records of all PLWH who were diagnosed with HIV in Philadelphia or who had CD4 T-cell counts <350 cells/mL or HIV-1 RNA levels drawn in Philadelphia.
Patients in the eHARS dataset were matched with records in CAREWare. The eHARS and CAREWare records are routinely matched for surveillance via unique identification numbers contained in both datasets. All eligible patients (100%) identified in CAREWare were successfully matched to the eHARS database. CAREWare is free HIV care monitoring software developed by HRSA for use by Ryan White Program (RWP) grantees and providers. Among its functions, it produces Ryan White HIV/AIDS Program Services Reports to meet HRSA reporting requirements. Patient-level data in CAREWare includes demographic, laboratory, pharmacy, and health service utilization information for all patients seen at Philadelphia RWP-funded clinics, collected to evaluate site-specific and system-wide performance data. Clinics perform chart reviews to abstract patient-level information. After undergoing quality control and verification, data are submitted to the DPH AIDS Activities Coordinating Office, where they are combined across clinics to produce a uniform database. Chart reviews and site visits verify the accuracy and completeness of the data. The majority of Philadelphia HIV clinics are RWP funded, covering 71% of patients in care in Philadelphia (unpublished data, City of Philadelphia DPH). Therefore, all patients in all Philadelphia HIV clinics who receive RWP funding are in the CAREWare dataset. We performed retrospective analyses on PLWH linked to and retained in care at Philadelphia RWP-funded clinics.
The study population included all patients aged 18 years or older who were newly diagnosed with HIV in 2007 and 2008. All patients were residents of Philadelphia at the time of diagnosis. The study was approved by the Institutional Review Boards of the University of Pennsylvania Perelman School of Medicine and the City of Philadelphia DPH.
Predictor and Outcome Measures
We examined 2 sets of linkage to care measures based on the length of time between the individual's HIV/AIDS diagnosis date and first (1) HIV clinic visit or (2) laboratory monitoring test. Clinic visits were defined based on HRSA criteria: a visit to an outpatient provider with prescribing privileges (not including nurses, pharmacists, social workers, or other support services providers) in an HIV care setting.10 All linkage measures investigated were used or adapted from previous studies (Fig. 1).16–44,49 Linkage measures included having a clinic visit within 30,26 60, 90,28–32 180,33,34 and 365 days after diagnosis49; a clinic visit between 21 and 60 days, 21 and 90 days, 21 and 180 days, and 21 and 365 days after diagnosis42; 2 clinic visits within 90, 180,33 and 365 days after diagnosis49; and 2 clinic visits ≥90 days apart within 180 and 365 days after diagnosis.37 As an example, a patient diagnosed on July 1, 2007, who had a clinic visit 10 days after diagnosis would be considered to have had a clinic visit within 30, 60, 90, 180, and 365 days after diagnosis.
Laboratory tests were considered to be CD4 T-cell levels and HIV-1 RNA levels. Two laboratory tests performed on the same day were considered as 1 test, and the test date refers to the date that the laboratory test was drawn. Laboratory tests were acquired from both eHARS and CAREWare. Laboratory-based linkage measures included having tests within 30, 60, 90,40 180, and 365 days after diagnosis43; between 21 and 60 days, 21 and 90 days, 21 and 180 days, and 21 and 365 days after diagnosis42; 2 tests within 90, 180, and 365 days after diagnosis43; and 2 tests 90 days apart within 180 and 365 days after diagnosis.36
Outcome variables used as reference standards included retention in care and virological suppression, as the preferred outcome of linkage to care may differ depending on the organization (eg, health department, clinic, community-based organization). For each patient, the linkage period of the study was defined as the day of diagnosis to 365 days after diagnosis, and the retention and virological suppression period of the study was defined as 366–730 days after diagnosis. The length of follow-up was censored at 730 days after diagnosis in all patients. Retention measurement started 366 days after diagnosis to distinguish linkage from retention in care and was defined as ≥2 clinic visits for HIV care ≥90 days apart between 366 and 730 days after diagnosis.10 Virological suppression was defined as a viral load <200 copies per milliliter, as the last viral load sent between 366 and 730 days after diagnosis.
Demographic variables are defined according to the Centers for Disease Control and Prevention criteria.48 Gender was defined as sex at birth. Race/ethnicity was categorized as white, black, Hispanic, or other. Exposure risk was grouped into heterosexual, men who had sex with men, injection drug use (IDU), and other/unknown. If a patient had both IDU and heterosexual exposures, or exposures of both IDU and men who had sex with men, they were coded as having both risk factors.48 AIDS at the time of HIV diagnosis was based on having a CD4 T-cell count <200 cells per microliter or an AIDS-defining condition.48 Place of birth was dichotomized as in the United States vs. outside of the United States, including Puerto Rico.48 Death within 730 days of diagnosis was identified by monthly evaluation of all death records that include HIV or AIDS on the death certificate and annual matching of eHARS records with the Social Security Death Index. CD4 T-lymphocyte count was categorized as <200, 200–350, 351–500, and >500 cells per milliliter.
Univariate statistics described the dataset. Multivariate logistic regression models without repeated measures were used to assess relationships between the linkage measures and the outcomes. Models were adjusted for age (continuous), gender, race/ethnicity, HIV risk factor, and AIDS at the time of HIV diagnosis. We did not include CD4 T-lymphocyte counts given the degree of colinearity with AIDS at the time of HIV diagnosis. Adjusted odds ratios with 95% confidence intervals (CIs) are presented. Relationships were considered statistically significant at α < 0.05.
Sensitivities, specificities, negative predictive values (NPVs), and positive predictive values (PPVs) were calculated for relationships between all linkage measures and outcome measures. Sensitivity for retention in care (and virological suppression) was defined as the proportion of those meeting the retention in care criteria (or virological suppression criteria) that were linked to care. Similarly, specificity for retention in care (and virological suppression) was defined as the proportion of those not retained in care (or not virologically suppressed) who were not linked to care. PPV was defined as the proportion of those meeting linkage criteria who were retained in care (or virologically suppressed). NPV was defined as the proportion of those not meeting linkage criteria who were not retained in care (or not virologically suppressed). Receiver operating characteristic curves were created and area under the curve (AUC) were calculated to determine the ability of each metric to predict retention in care and virological suppression. AUCs were adjusted for age, gender, race/ethnicity, exposure risk, and AIDS at the time of diagnosis.
We performed 4 subanalyses and sensitivity analyses: (1) to account for mortality, (2) to account for moving outside the city, (3) to determine the effect of clinic visits not captured in our dataset, and (4) to determine the effect of undetectable HIV viral loads not captured in our dataset. Because people who died or emigrated out of the city during the study period may not have had the opportunity to fulfill linkage, retention in care, and virological suppression criteria, we conducted subanalyses (including sensitivities, specificities, PPVs, and NPVs) on only those individuals with complete follow-up to examine if excluding those who died or emigrated out of the city changed the point estimates, respectively. Next, sensitivity analyses addressing the 29% of PLWH in Philadelphia seen outside of RWP-funded clinics were performed, assuming that all these individuals were linked to care. Finally, to account for the possibility of incomplete laboratory reporting, sensitivity analyses conducted based on the conservative estimate that 15% of the PLWH (ie, 50% of those not in care at RWP-funded clinics) had missing undetectable viral load measurements. Laboratory tests from 2 sources (eHARS and CAREWare) were available for 71% of the patients. As such, sensitivity analyses assumed that half of those not in the CAREWare were at risk of having missing undetectable HIV-1 RNA levels. SAS Version 10.0 was used for all analyses (SAS Institute Inc., Cary, NC).
Our cohort included 1781 patients. Most patients were male (70.1%) and black (63.3%) and had a heterosexual risk exposure (61.0%). Approximately one third had AIDS at HIV diagnosis (34.5%) (Table 1). Linkage rates for clinic-based measures were applicable for RWP-funded clinics only and ranged from 17.5% for having 2 visits in 180 days separated by 90 days to 39.5% for having any visit within 365 days of diagnosis. For laboratory-based measures, linkage rates ranged from 34.0% for having 2 tests 90 days apart within 365 days to 81.6% for having 1 test in 365 days (Table 2). Data and diagrams representing progression through the HIV care cascade for each linkage metric are presented (see Figures S1–S28, Supplemental Digital Content, http://links.lww.com/QAI/A425).50 Progression through the HIV care cascade, stratified by sociodemographic characteristics, is also shown (see Table S2, Supplemental Digital Content, http://links.lww.com/QAI/A425).
Between 366 and 730 days after diagnosis, 780 patients (43.8%) successfully attended ≥1 clinic visit, and 503 patients (28.2%) met the HRSA retention measure (2 clinic visits ≥90 days apart in 1 year). Similarly, 366–730 days after diagnosis, 23.5% (N = 419) had virological suppression. In total, 1108 patients (62.2%) were neither retained in care nor had virological suppression 366–730 days after diagnosis.
Using retention in care as the outcome of appropriate linkage, the measure with the highest PPV for retention was attending 2 clinic visits ≥90 days apart within 365 days of diagnosis (74.2%; 95% CI: 70.8% to 78.0%). The linkage measure with the lowest PPV for retention was laboratory monitoring within 30 days (32.0%; 95% CI: 29.1% to 34.9%). PLWH who did not have a clinic visit between 21 and 365 days after diagnosis had the highest NPV for retention in care (94.5%; 95% CI: 0.928 to 0.962), whereas the absence of laboratory monitoring within 30 days of diagnosis had the lowest NPV for retention (77.0%; 95% CI: 74.0% to 80.0%). The measure with the highest AUC for retention in care was attending a clinic visit between 21 and 365 days after diagnosis (Table 3).
Using virological suppression as the outcome of appropriate linkage, the measure with the highest NPV for virological suppression was lacking laboratory testing within 365 days of diagnosis (98.2%; 95% CI: 96.1% to 99.3%) and the measure with the lowest NPV was the absence of a clinic visit within 30 days of diagnosis (87.0%; 95% CI: 85.0% to 89.0%). The measure with the lowest PPV for virological suppression was having 2 tests in 180 days separated by 90 days (41.0%; 95% CI: 37.0% to 45.0%), whereas having 2 visits in 180 days separated by 90 days had the highest PPV for virological suppression (49.0%; 95% CI: 43.0% to 55.0%). Patients completing 2 laboratory tests separated by 90 days in 365 days had the highest AUC for virological suppression (Table 4).
Sensitivity analyses were performed to account for care received outside of RWP-funded clinics. Linkage measures associated with the highest and lowest odds of retention in care, sensitivities, specificities, NPVs, and PPVs did not change. Sensitivity analyses were also performed to account for the possibility of unreported undetectable viral loads. NPVs and PPVs did not differ greatly. When sensitivity analyses were performed assuming that both laboratory monitoring–based measures and the outcome measure of virological suppression were underestimated, PPV changed a little but NPV decreased to as little as 11% for having any laboratory test sent within 365 days (see Tables S3–S6, Supplemental Digital Content, http://links.lww.com/QAI/A425).
Additional analyses were performed to determine the effect of mortality on estimates. Point analyses of those alive at 730 days after diagnosis did not differ by 10% of their baseline. We also performed subanalyses examining only those patients who did not move out of Philadelphia during the study. Point analyses did not differ by 10% of their baseline.
This is one of the first studies comparing multiple laboratory- and clinic-based measures of linkage to care. Clinic-based linkage measures, in particular completing ≥1 clinic visits between 21 and 365 days after diagnosis, best predict retention in care. However, completing 2 laboratory tests separated by 90 days within 365 days of diagnosis best predicts virological suppression. These data suggest that both clinic- and laboratory-based linkage measures have value. Selection of a linkage measure should be tailored to the outcome of interest.
Government agencies and professional organizations vary in criteria used to define linkage to care. The Emergency Department National HIV Testing Consortium metric is a clinic visit within 30 days of diagnosis.27 In our study, only 62.3% of patients meeting this measure were retained in care, and only 40.5% achieved virological suppression. The US National HIV/AIDS Strategy recommends linking 85% of persons to care within 90 days of diagnosis, using a laboratory-based measure.47 Although 72.0% of patients met this measure, only 32.5% were retained, and 27.7% achieved virological suppression. Using the linkage metric most predictive of retention in care, 38.2% of patients completed a clinic visit between 21 and 365 days after diagnosis, with 65.0% of patients meeting this measure retained in care. Alternatively, using the linkage metric most predictive of virological suppression, 56.3% of patients had 2 laboratory tests 90 days apart within 365 days of diagnosis, and 38.0% of them achieved virological suppression. Our data suggest that agencies and organizations should consider which linkage metrics best meet their outcomes of interest when recommending linkage criteria.
Laboratory-based linkage measures had lower predictive abilities for retention in care than clinic-based measures. Within 365 days of diagnosis, 81.6% of the population had a laboratory test, whereas only 39.5% had a clinic visit within the Ryan White system within 365 days of diagnosis. Clinic visits were underreported to a greater extent than laboratory testing because we used the HRSA definition for HIV clinic visits10 (which excludes pharmacy, nursing, social work, and other visits to providers without prescribing privileges) and because we were unable to detect visits to non–RWP-funded clinics. Furthermore, laboratory testing may occur outside of the primary HIV care setting, including in non-HIV clinics, inpatient hospitals, and emergency departments. Our data differ from recent studies suggesting the use of laboratory testing as a proxy for clinic visits.51 Although using laboratory tests as a proxy for clinic visits may be helpful in clinic cohort–based studies,51 our data suggest that laboratory tests may not be as predictive of clinic visits in all settings, such as surveillance.
Previous studies have evaluated metrics for retention in care52,53 and predictors of virological suppression.54 However, few studies have examined how well the different linkage metrics predict retention in care or virological suppression. Among these, only 141 or 243 linkage metrics were compared. We present a more complete picture of linkage to care, retention in care, and virological suppression than previous clinic cohort–based studies.
Our study had limitations. First, generalizability was limited as we only studied patients in 1 US city. Also, linkage, retention, and virological suppression are lower than reported elsewhere.1,2,45,46,55–58 For example, a meta-analysis of 28 studies estimated that 77% of patients are linked to care, 51% are retained in care, and 35% achieve virological suppression.1,2 Linkage rates in our study ranged from 17.5% to 81.6%, 28.2% of patients were retained in care and 23.5% achieved virological suppression. Our inability to access clinic visit data on patients seen outside RWP-funded clinics would have underestimated linkage to and retention in care for the metrics that used these data. However, sensitivity analyses accounting for PLWH not attending RWP-funded clinics demonstrated that the linkage metrics most predictive for retention in care and virological suppression did not change. If laboratories were not reporting undetectable HIV-1 RNA levels, we also may have underestimated virological suppression. Sensitivity analyses accounting for this did not alter the results. We also performed sensitivity analyses to account for those who died or migrated out of the city. Although it is possible that PLWH in care may lack laboratory monitoring, this is rare (unpublished data, Philadelphia DPH). Similarly, it is unlikely that PLWH not in care would achieve virological suppression.
We focused on virological suppression and retention in care between 366 and 730 days after diagnosis to differentiate linkage to care from retention in care, as some researchers defined linkage to care within the first 365 days after diagnosis.38 Some patients may have dropped out of care before this time, potentially contributing to the lower retention rates seen in the study. In addition, we did not collect data on the timing of ART initiation, which has been associated with both improved retention in care and virological suppression.59,60 Low rates of ART initiation among PLWH in our cohort could further lower the proportion of patients not meeting retention in care and virological suppression targets.
Despite these adjustments, linkage and retention metrics were still lower than reported elsewhere.1,2,45,46,55–58 Our data came from a large city with many racial minorities and persons below the poverty line, which may be associated with lower rates of retention in care. Care provider characteristics may also differ from other cities. For example, providers, including non-HIV providers working in urgent care, emergency, inpatient, and primary care clinic settings, may be less likely to send laboratory tests than in other regions, lowering laboratory-based linkage rates. Further studies are needed to evaluate how linkage measures perform in other locals and settings.
Understanding the predictive ability of measures of linkage to care is necessary for improving the quality of HIV care and reducing HIV transmissions. Our data suggest that selection of the ideal linkage measure depends on the outcome of interest being evaluated. The clinic-based measure of completing a visit between 21 and 365 days after diagnosis best predicted retention in care and may be useful for testing centers focused on referring PLWH to care. Meanwhile, the laboratory-based measure of completing 2 laboratory tests separated by 90 days within 365 days of diagnosis best predicted virological suppression and may be a helpful definition for test-and-treat strategies aimed at reducing community viral load. Researchers studying retention and virological suppression in PLWH, testing agencies seeking to improve the quality of their work, and funding agencies deciding how to allocate resources should tailor linkage measures based on the outcome of interest.
The authors would like to acknowledge the staff of the City of Philadelphia Department of Public Health AIDS Activities Coordinating Office for their assistance in creating the Ryan White dataset, especially Jane Baker; Coleman Terrell; Mark Shpaner, MD; Marlene Matosky, MPH, RN; and Ethan Schofer.
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HIV; linkage to care; retention in care; virological suppression; HIV care cascade
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