Mills, Caroline W. MPH; Sabharwal, Charulata J. MD, MPH; Udeagu, Chi-Chi MPH; Bocour, Angelica MPH; Bodach, Sara MPH; Shepard, Colin MD; Begier, Elizabeth M. MD, MPH
In 2008, 3809 persons in New York City (NYC) were newly diagnosed with human immunodeficiency virus (HIV), of whom 24.6% were concurrently diagnosed with acquired immunodeficiency syndrome (AIDS) (within 31 days of HIV diagnosis).1 About a quarter of new diagnoses of HIV in the past several years in NYC have been concurrent diagnoses.1 In the United States, late diagnosis of HIV represents a substantial proportion of new diagnoses.2–4 Without treatment, the mean time between HIV diagnosis and development of AIDS is 10 years,5 indicating that a concurrent diagnosis usually represents years of missed opportunities when infected persons could have initiated treatment and lowered their chances of HIV-related mortality.6,7 Late diagnosis also increases risk of transmission to others because knowledge of one's HIV-positive status reduces risk behavior on average by 50%.8–10
Medical and billing record studies have demonstrated that a majority of persons diagnosed with HIV have medical encounters before their diagnosis but are not tested,11–13 supporting the Centers for Disease Control and Prevention (CDC) recommendation for opt-out routine HIV screening for all patients aged 13 to 64 years.14 Prior studies have examined patient-level barriers to testing among HIV negative or status unknown persons.15–21 However, very few studies have explored the barriers for individuals concurrently diagnosed with HIV and AIDS (“late testers”), and these studies are limited by small sample size.22,23 We undertook this survey to describe reasons for delayed HIV testing and missed opportunities for testing among individuals concurrently diagnosed with HIV and AIDS in NYC.
Study Sample and Data Collection
Concurrently diagnosed persons were identified from patients participating in the NYC Department of Health and Mental Hygiene's (NYC DOHMH) HIV partner notification (PN) program, which provides PN and linkage to care services, between January 1, 2008 to December 31, 2008.24 As part of this program, NYC DOHMH staff members were outstationed to 8 hospitals in 3 NYC neighborhoods most affected by the HIV epidemic (South Bronx, Central Brooklyn, and Harlem) and NYC's main jail complex (Rikers Island).
Concurrent diagnosis was defined as an AIDS-defining CD4 count (<200 cells/mL or CD4% <14) within 90 days of first HIV diagnosis; 90 days duration was considered rather than 31 days, the NYC standard,6 for a larger participant pool. The presence of AIDS-defining opportunistic illnesses was not assessed for eligibility because available data on these illnesses were unreliable.
We conducted a retrospective review and the questionnaire was administered from November 26, 2008 to July 31, 2009. Three bilingual public health workers were trained to conduct the interviews. Questionnaires were in English and translated during the interview as needed for 19 Spanish and 6 Haitian-Creole speaking patients. Interviews were conducted via telephone, except in a small number of cases (n = 11) where the calls were unsuccessful and the interviewer went to the patient's home or HIV medical appointment to conduct the interview in person. Patient confidentiality was maintained in compliance with standards set by NYC DOHMH.
We used demographic data, including age, gender, race/ethnicity, number of sex partners in year before diagnosis, and HIV risk factor information collected during the initial NYC DOHMH PN investigation for all patients. Patients living in a zip code where at least one-fifth of the population lived below the federal poverty level per US Census 2000 were categorized as living in a poverty neighborhood.6
The survey focused on assessing HIV testing history, health care utilization, and testing barriers. To assess testing history, interviewees were asked if they had ever tested negative for HIV and if they had ever not received HIV test results. For previous testers, we asked the number of times they had tested for HIV in the year before their first positive test.
To assess health care utilization, interviewees were asked if they had a primary care provider (PCP) during the year before their diagnosis and if they had health insurance during the whole year, part of the year, or none of the year before their diagnosis. Health insurance was explained as including Medicaid. A PCP was defined as a clinic or doctor seen on a regular basis for routine health care. The interviewer read a list of types of health care facilities (e.g., emergency rooms, private doctors, community health clinics) and asked the interviewees the number of times they visited that facility type, and whether they were offered and accepted an HIV test.
To assess testing barriers, interviewees who reported having no HIV test in the year before diagnosis were first asked to give one or more reasons for not testing during that past year. The interviewer transcribed the responses, which were coded to a list of 23 potential barriers to testing or “other” if the reason did not fit an existing choice. This list of barriers was adapted from an instrument developed for the Never in Care study conducted by the CDC and NYC DOHMH.25 Next, the interviewer read the 23 potential testing barriers and asked the interviewee if each was part of the reason why the participant did not get tested during the year before diagnosis; after the interviewer read each item, the interviewee was asked to answer “Yes,” “No,” or “Not Sure.”
Basic descriptive statistics were calculated for all survey questions. Demographic information and risk behaviors of interviewed patients were compared to patients who declined interview, using χ2 statistics for categorical variables and t tests for continuous variables. Health care utilization and testing history were assessed overall and by gender, using χ2 statistics. To evaluate barriers to testing, we restricted our analysis to interviewees who reported no HIV test in the year before diagnosis to eliminate persons who rapidly progressed to AIDS and were not necessarily late testers. Characteristics of interviewees citing not being at risk as a barrier to testing were calculated for the whole cohort and by gender. Statistical analyses were performed using SAS 9.1 software (SAS Institute, Cary, NC).
A total of 236 patients met our eligibility criteria. Among those eligible, 63 could not be located. Of the 173 who were located, 139 patients agreed to participate in the survey. Of the remaining 34 patients who were located, 3 were medically unable to respond, 1 was found to be imprisoned outside of NYC, 5 had died, and 25 declined to participate. Participation rate was 85% (139/(173–9); Fig. 1).
Demographic Characteristics and Risk Behaviors
Table 1 summarizes demographics for those interviewed and those who declined. Sixty-five percent of interviewed persons were men, with a mean age of 41 (range, 18–68 years). One-third of interviewed patients (33%) identified as Hispanic, 64% as non-Hispanic black, and 3% as non-Hispanic white. Patients who declined interviews had demographic characteristics that were similar to interviewed patients.
Thirty-nine percent of male interviewed patients were men who have sex with men (MSM) and 24% of all interviewees reported having sex with an HIV-infected partner. Ever exchanging money or drugs for sex was reported by 14% (n = 20) of those interviewed, as was receiving an STD diagnosis in the year before HIV/AIDS diagnosis. Only 6 patients who received an STD diagnosis reported being offered an HIV test. Of interviewed patients, 12% reported 3 or more sex partners in the year before diagnosis. Individual risk behaviors were largely similar among those who declined the interview. The exception was that none who declined reported an STD diagnosis in the year before HIV/AIDS diagnosis (P = 0.05). Overall, 65% of interviewed patients and 44% of patients who declined had at least one of these reported risk behaviors (P = 0.05). Characteristics of patients interviewed and those unable to be located did not significantly differ.
Health Care Utilization in Year Before Diagnosis
Of interviewed patients, 40% reported having a PCP and 50% reported having health insurance during all or part of the year before concurrent HIV/AIDS diagnosis (Table 2). Seventy percent reported having at least 1 health care visit, and the median number of health care visits during the year was 1 (range, 0–39). Thirty-five percent reported visiting an emergency department and close to one-third (32%) reported visiting a private doctor.
HIV Testing History
Less than half (44%) of interviewees reported having ever tested HIV negative, and 1% reported testing and not receiving their results. In the year before diagnosis, only 20% reported being offered an HIV test and, of these, 13 (18%) reported accepting a test and testing negative. Two interviewees reported being offered the test at more than one visit, and 1 reported accepting and testing negative 4 times during the year. Having health insurance for all or part of the year was not found to make individuals more or less likely to report being offered a test, as 20% of insured respondents and 20% of uninsured respondents were offered a test (P = 0.97). When restricted to those reporting a health care visit in the past year (n = 97), 35% of uninsured respondents reported having been offered a test in contrast to 23% of insured respondents (P = 0.21).
HIV Testing Barriers
The 121 respondents who did not self-report testing negative in the year before diagnosis were allowed to give multiple reasons to the open-ended question about why they did not test for HIV in the prior year, though most (75%) gave only one reason. The majority (64%) responded with a reason that fell into the category “I did not believe I was at risk”; 13% stated that they were afraid to learn they had HIV. Eight percent responded with each of the following reasons: “I was not sick/I always felt fine,” “No one offered me a test,” and “I did not know my physical illnesses were signs of HIV.”
From the list of 23 potential testing barriers, the majority (69%) responded yes to “You did not believe you were at risk.” Half of the participants also responded yes to “You thought your behaviors kept you safe from getting HIV.” The next most attributed reasons were “No one offered you an HIV test” (42%) and “You didn't know your physical illnesses were possible signs of HIV” (41%). The remaining reasons were answered affirmatively 23% of the time or less (Table 3). No significant differences in affirmative responses were detected by gender.
There were no statistically significant differences between the demographic and risk profiles of those who did not test because they did not believe they were at risk and those who did not report this barrier.
In order to identify barriers to HIV testing, we interviewed over 100 patients diagnosed with HIV so late in their infection that they had already progressed to AIDS. This is the first large-scale survey asking persons with delayed HIV diagnosis why they did not seek testing sooner. The most frequently cited reason for not testing earlier was not perceiving oneself to be at risk for HIV. This was found not only when interviewees were asked to volunteer their primary reason for not having had an HIV test, but also when prompted with a list of potential barriers to testing. Actual reported risk behaviors did not vary by perception of risk, and a majority of the survey population had well-known, previously identified risk behaviors for HIV. These findings indicate a disagreement between acknowledging a risk behavior and perceiving oneself to be at risk for HIV.
The majority of interviewees accessed medical care in the year before diagnosis but few reported being offered an HIV test, suggesting that lack of routine HIV testing in medical settings rather than lack of access to care was behind these delays in HIV diagnoses. Most interviewees who had been offered a test accepted it (64%), which suggests that implementation of routine testing in medical settings should be met with some immediate success. For the approximately one-third of patients who reported declining a prior offer of an HIV test, their reasons for refusal are worthy of additional exploration. The NYC DOHMH continues to fund targeted testing programs to outreach to high-risk populations in nonclinical settings, which may reach some of those that decline routine testing. Further, as HIV testing becomes more routine and thus a normative behavior, it is likely that many of those who would have previously declined testing will be willing to accept it. In June 2008, NYC launched the The Bronx Knows HIV Testing Initiative, the city's largest attempt at municipal scale-up of routine HIV screening to date. The goal of The Bronx Knows is to ensure that every resident of the Bronx aged 13 to 64 years knows his or her HIV status, and if he or she has never been tested for HIV, to get screened. This community-wide push for implementation has been resoundingly successful, as reflected in the 400,000 HIV tests performed in the Bronx as part of the initiative, and a statistically significant increase (P < 0.01) over the last 3 years in the proportion of Bronx adults aged 18 to 64 years reporting having ever had an HIV test (Bureau of Epidemiology Services, New York City Department of Health and Mental Hygiene: New York City Community Health Survey 2007–2009. May 2010).
Our findings that a lack of perception of risk was the greatest patient-level barrier to testing are consistent with other studies of persons at high risk for HIV but not necessarily already infected.15,21–23,26–28 Further, our findings also corroborate studies suggesting no association between high-risk behaviors and an individual's perceived risk factors and testing for HIV among undiagnosed persons with established HIV risk factors.18,20,29
CDC guidelines have moved away from using risk behaviors to determine who in the general population should be tested for HIV,14 and our results support these guidelines. This survey found that most of the interviewees accessed medical care and that a majority lacked perception of their own risk even as they acknowledged their risk behaviors. The most comprehensive way to ensure testing in this population would be to offer testing to all patients who present for medical care. Further, as these interviewees do not view themselves as being at risk for HIV infection, this population is unlikely to seek testing at community HIV testing centers, leaving regular medical care as the primary avenue for outreach. This survey was conducted in 2008, and suggests incomplete adoption of 2006 CDC guidelines recommending routine HIV testing of adults in clinical settings.14 Even those who reported an STD diagnosis in the year before their HIV/AIDS diagnosis infrequently reported being offered an HIV test (30% of such respondents). In New York State in 2010, the longstanding legislation mandating separate written consent for every HIV test conducted was amended to accommodate a streamlined consent procedure in clinical settings.30 Once implemented, this law should facilitate routine testing in New York State.31–33
Thirteen percent of the interviewees reported testing negative in the year before their HIV/AIDS diagnosis. We were not authorized to verify the negative test results of patients; we excluded these individuals from barriers to testing analysis. Although it is possible that they were reporting socially desirable responses,34 or rapidly progressed to AIDS (within 5 years of infection),35 several interviewees indicated that they assumed HIV testing was included in routine blood work. One interviewee stated that in his life he had tested “50 or 60 times and it was always negative.” A study of testing beliefs among high-risk heterosexuals found that approximately one-fifth of respondents believed that HIV testing was a routine procedure in medical care.36 Similarly, many members of an inner-city focus group in another study believed that they had been tested for HIV at some point without their consent.37 These findings suggest some of the surveyed patients believed that they were HIV negative because no doctor has ever told them otherwise.
There were several limitations of this survey. First, we were unable to locate 27% of eligible patients; however, demographics and risk behaviors of this group were similar to those interviewed. Although only 15% of eligible patients contacted declined to participate, this group was less likely to have an identified risk behavior than were participants. It is possible that eligible participants who declined would have offered different reasons for not having testing sooner. Second, we relied on self-reported data for health care utilization and testing history, which are subject to reporting errors.38,39 Studies have found substantial under-reporting of health services use.40,41 If such under-reporting occurred in our survey, even more concurrently diagnosed participants were accessing medical care before their HIV diagnosis.
Finally, our HIV PN program operates in a large city, within selected underserved neighborhoods with a high prevalence of HIV. As a result, findings from this survey may not be representative of all HIV-infected populations. However, demographics and risk profiles of this survey population was comparable to the larger population of concurrently diagnosed persons in NYC.6,42
Our results show that many individuals with concurrent HIV/AIDS diagnoses had accessed medical care before their diagnosis and that the lack of perception of risk is a major barrier to testing. Routine offer of HIV testing by providers would likely prevent late diagnosis by testing those who believe they are not at risk and would not otherwise seek testing.
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