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Lack of Awareness of Human Immunodeficiency Virus (HIV) Infection: Problems and Solutions With Self-reported HIV Serostatus of Men Who Have Sex With Men

Lack of Awareness of Human Immunodeficiency Virus (HIV) Infection: Problems and Solutions With... MA JO R A R T IC LE Lack of Awareness of Human Immunodeficiency Virus (HIV) Infection: Problems and Solutions With Self-reported HIV Serostatus of Men Who Have Sex With Men 1 1,2 1 1 1 3 Travis H. Sanchez, Colleen F. Kelley, Eli Rosenberg, Nicole Luisi, Brandon O’Hara, Rodriques Lambert, 1 1,2 4 5 6 1 1 Raphael Coleman, Paula Frew, Laura F. Salazar, Sijia Tao, William Clarke, Carlos del Rio, and Patrick S. Sullivan 1 2 Rollins School of Public Health, Emory University and Emory Center for AIDS Research, Division of Infectious Disease, Department of Medicine, Emory 3 4 University School of Medicine, HIV/AIDS Epidemiology, Georgia Department of Public Health, School of Public Health, Georgia State University, and 5 6 Laboratory of Biochemical Pharmacology, Emory University, Atlanta, Georgia; and School of Medicine, Johns Hopkins University, Baltimore, Maryland Background. Lack of human immunodeficiency virus (HIV) infection awareness may be a driver of racial dispar- ities in HIV infection among men who have sex with men (MSM). Lack of awareness is typically measured by comparing HIV test result to self-reported HIV status. This measure may be subject to reporting bias and alternatives are needed. Methods. The InvolveMENt study examined HIV disparities between black and white MSM from Atlanta. Among HIV-positive participants who did not report knowing they were positive, we examined other measures of awareness: HIV viral load (VL) <1000 copies/mL (low VL), antiretroviral (ARV) drugs in blood, and previous HIV case surveillance report. Results. Using self-report only, 32% (62 of 192) of black and 16% (7 of 45) of white MSM were not aware of their HIV infection (P = .03). Using self-report and low VL, 25% (48 of 192) black and 16% (7 of 45) white MSM lacked awareness (P = .18). Using self-report and ARVs, 26% (50 of 192) black and 16% (7 of 45) white MSM lacked awareness (P = .14). Using self-report and surveillance report, 15% (28 of 192) black and 13% (6 of 45) white MSM lacked aware- ness (P =.83). Conclusions. Self-report only may overestimate true lack of awareness of HIV status for black MSM. If, as our data suggest, black MSM are not less likely to be aware of their HIV infection than are white MSM, then this factor is not a substantial driver of HIV disparity. Future HIV research that depends on accurate measurement of HIV status awareness should consider including additional laboratory and case surveillance data. Keywords. HIV; MSM; survey; testing. Over the past decade, men who have sex with men incidence has increased [1]. More recently, increases (MSM) have been the only group in the United States in incidence have been concentrated among young in which human immunodeficiency virus (HIV) MSM of color [2]. Black MSM have over twice the prev- alence of HIV than white men, [3, 4] and data from the HIV Prevention Trials Network study number 061 sug- gest that black MSM experience an HIV incidence rate Received 23 May 2014; accepted 08 August 2014. over 5 times that of white MSM [5]. The reasons for Correspondence: Travis H. Sanchez, DVM, MPH, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, GA 30322 (travis.sanchez@emory. these racial disparities in HIV infection among MSM edu). are unclear, but differences in individual-level risk be- Open Forum Infectious Diseases haviors likely do not account for the observed dispari- © The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Societyof America. This is an Open Access article distributed under the terms ties [4, 6]. This same pattern of disparity exists among of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http:// black MSM in Atlanta, the city with the 8th highest creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work rate of new HIV diagnoses and 4th highest number of is not altered or transformed in any way, and that the work is properly cited. For new HIV diagnoses among MSM in the country in 2011 commercial re-use, please contact journals.permissions@oup.com. DOI: 10.1093/ofid/ofu084 [7]. Men who have sex with men comprise the largest Lack of Awareness of HIV Infection Among MSM OFID 1 � � group living with HIV in Atlanta, and black MSM are dis- participants were informed that they would be screened for proportionately affected, constituting approximately 60% of HIV infection, but the criteria for which participants would HIV-infected MSM, whereas black persons represent only ap- be offered enrollment in the prospective component of the proximately 30% of the overall Atlanta population [8]. study were not specifically discussed. Differences in awareness of HIV infection between black and All InvolveMENt study participants were tested for HIV white MSM are hypothesized to contribute to this disparity [6]. using a rapid test with confirmation by enzyme-linked immu- Overall, approximately 20% of persons infected with HIV in the nosorbent assay and Western blot analysis. Before results of United States are thought to be unaware of their infection; how- HIV testing were returned, participants completed a detailed ever, they account for an estimated 49% of transmission events computer-assisted self-interview. All HIV-positive men had [9]. Awareness of HIV infection results in a reduction in high- HIV VL testing (COBAS AmpliPrep/COBAS TaqMan HIV-1 risk sexual behavior [10], and it is the first critical step in the test kit version 2.0; Roche Molecular Systems, Inc.), and these continuum of HIV care, which ideally results in receipt of anti- results were returned to participants. Participants who had a retroviral (ARV) therapy, achievement of an undetectable HIV negative HIV rapid test at baseline were offered enrollment in viral load (VL), and reduction in HIV transmissions [11–13]. the follow-up study. If a participant subsequently tested HIV National surveillance data show that black MSM have high lev- positive at the 3-month visit, we conducted VL testing on the els (59%) of lack of awareness of HIV infection compared with stored specimen from the baseline visit. Those who had detect- white MSM (26%) [14]. able VL (but who were nonreactive on the HIV rapid test) were HIV surveillance projects and research studies use a similar considered to have acute HIV infection at the time of their base- set of testing history questions to define self-reported lack of line visit. The InvolveMENt study staff (eg, counselors, phlebot- awareness of infection that is detected through study-delivered omists, interviewers) were diverse in regards to race, ethnicity, testing. However, there are new reports that the validity of this age, and gender. The InvolveMENt study was reviewed and ap- self-reported measure may be questionable for some groups of proved by the institutional review board of Emory University. MSM [5, 15, 16]. It remains unknown whether the validity of these measures may differ by participant race and whether via- Measures ble solutions to improve the measure may be available to HIV We used several approaches to classify HIV infection awareness. researchers. For this study, we hypothesized that the combina- The first method (“self-reported”)defined awareness of infec- tion of traditional survey, laboratory, and public health surveil- tion using a set of questions about their experiences ever getting lance data could improve the measurement of awareness of HIV tested, the most recent testing experiences, and their most re- infection among black and white MSM participants of a cent test result. In addition, during the posttest result discus- research study in Atlanta, Georgia. sion, any participant who disclosed prior knowledge of their HIV status to the study counselor was classified as “self-reported aware,” even if they did not report having a previous HIV-positive METHODS test in their survey. InvolveMENt Study Among those who were classified as not aware of their HIV The InvolveMENt study was a prospective cohort study de- infection by self-report, we also explored 2 laboratory measures signed to examine factors that may contribute to disparities in and a public health surveillance measure of awareness. One lab- HIV and sexually transmitted infection between black and oratory measure was low VL (<1000 copies/mL or undetectable) white MSM in Atlanta. MSM aged 18–39 years were recruited, on the baseline blood specimen. The other laboratory measure regardless of HIV status, primarily using time-space venue sam- was detectable ARV drugs using either of 2 nonmutually exclu- pling, with a sampling frame built upon that used for the Atlan- sive algorithms. First, for those MSM classified as not aware of ta site for the second MSM cycle of the National HIV their HIV infection by self-report and who also had a low VL, we Behavioral Surveillance System (NHBS-MSM) [17, 18]. Face- conducted a limited quantification ARV panel that included book was also included as a virtual venue. The InvolveMENt commonly prescribed nucleoside/nucleotide reverse-transcrip- study methods have been previously reported but are briefly tase inhibitors ([NRTIs] abacavir, emtricitabine, lamivudine, te- described here [19]. Eligible participants were self-identified nofovir, and zidovudine) [20]. This limited quantification ARV black and white MSM who reported sex with another man panel was the first we explored and was not done on all specimens in the previous 3 months, who were not in a mutually monog- because of the potential expense involved. Second, for all MSM amous relationship, could complete survey instruments in classified as not aware by self-report, we used mass spectrome- English, lived in the Atlanta metropolitan area, were not en- try to test an expanded ARV panel that included NRTIs (emtri- rolled in another HIV prevention study, who did not identify citabine, lamivudine, tenofovir, and zidovudine), nonnucleotide as Hispanic/Latino, and had no plans to relocate in the subse- reverse-transcriptase inhibitors (efavirenz and nevirapine), and quent 2 years. During the baseline visit consent process, protease inhibitors (atazanavir, darunavir, fosamprenavir, 2 OFID Sanchez et al � � indinavir, lopinavir, nelfinavir, ritonavir, saquinavir, and tipra- Table 1. Characteristics of MSM Classified as Lacking Awareness of Their HIV Infection, InvolveMENt Study, 2010–2012 navir) [16]. The results of the ARV testing were not returned to participants. Black MSM White For the public health surveillance measure of awareness, we (N = 62) MSM used evidence of a preexisting HIV case surveillance report at (N =7) the Georgia Department of Public Health. We submitted to No. (%) No. (%) the state health department a line-listing of black and white par- HIV Testing History Questions ticipants considered not aware of their status by self-report. The Never Tested 14 (23) 1 (14) health department reported back on the total number of per- Ever Tested, Last Result sons from the list who were already in the HIV case surveillance Negative 39 (63) 6 (86) system and whose first HIV diagnosis in the system had oc- Indeterminate 3 (5) 0 (0) curred at least 21 days before our diagnosis. This timeframe Didn’t Get It 6 (10) 0 (0) was selected to ensure that persons who were previously diag- HIV Viral Load <1000 copies/mL 14 (23) 0 (0) nosed more recently would have had at least some opportunity Any Antiretroviral Drug Detected 12 (19) 0 (0) to receive their previous test result. To protect confidentiality of Mass Spectrometry 12 (19) 0 (0) case surveillance data, the health department did not return a NRTI Quantification 7 (11) 0 (0) list of persons with previous diagnoses to the study’s research- Previously Reported to HIV Case 34 (55) 1 (14) Surveillance ers, but it only provided us with aggregate numbers. The health department also reported the mean number of days between the Abbreviations: HIV, human immunodeficiency virus; MSM, men who have sex with men; NRTI, nucleoside/tide reverse-transcriptase inhibitor. first HIV diagnosis in the system and our diagnosis. NRTI blood levels only performed among those with HIV viral load <1000 Participants who enrolled through February 2012 and were copies/mL. not aware of their HIV infection by self-report were also invited Average time between previous report and InvolveMENt report = 1590 days. to participate in an in-depth interview. A staff interviewer con- ducted one-on-one discussions with participants at a follow-up visit to the study office (ie, the qualitative interviews happened (prevalence ratio = 3.3; 95% confidence interval = 2.5, 4.4) [19]. after the visit in which they tested HIV-positive). The interview- There were 5 black MSM and 1 white MSM who were considered er used a semistructured qualitative interview method with a set to have acute HIV infection at the time of their baseline visit and of open-ended question domains with follow-up probes. The were excluded from further analysis. purpose of the interviews was to generate more detailed infor- Among black MSM with HIV infection at baseline, 69 were mation about previous HIV testing experiences and diagnoses, classified as not aware on survey responses alone, and 7 dis- general themes regarding disclosure of HIV status, and rephras- closed knowledge of their status during posttest counseling. ing activities to better understand comprehension of the HIV Among white MSM with HIV infection at baseline, 8 were clas- testing questions. Participants were not specifically asked sified as not aware by survey responses alone, and 1 disclosed about possible discrepancies between self-reported awareness knowledge of his status during posttest counseling. The measure and laboratory testing. of self-reported lack of awareness of HIV status was 32% (62 of 192) among black MSM and 16% (7 of 45) among white MSM. Analyses Most participants (65%, 45 of 69) who disclosed not being We compared lack of awareness of HIV infection between black aware of their infection had been previously HIV tested and re- and white MSM using χ tests for the different measures: self- ported that their most recent test result was negative (Table 1). report alone, self-report plus low VL, self-report plus detectable Fourteen participants (14 black MSM and 0 white MSM) ARV, and self-report plus previous HIV case surveillance re- who were classified as not aware by self-report had a low VL. port. Findings were considered significant if P < .05. Statistical The limited panel of ARV testing was completed for 13 of analyses were performed using OpenEpi (www.OpenEpi.com, them; 7 of whom had at least 1 NRTI detected. The expanded version 2013/04/06). ARV panel was completed for 60 of 69 MSM (53 of 62 black MSM and 7 of 7 white MSM); 12 of whom (all black MSM) had ARV detected. Thirteen participants had both types of ARV RESULTS testing; 7 of whom had ARV detected on both tests, 4 had no Enrollment occurred from July 2010 through December 2012, re- ARV detected on either test, and 2 had ARV on mass spectrom- sulting in a total of 454 black MSM and 349 white MSM being etry that was not detected on the quantitative NRTI test (Table 2 enrolled and contributing to this analysis. The prevalence of HIV shows detected ARV results). Two participants with high VL infection at the baseline visit among black MSM was 43% (197 (14 755 and 16 802 copies/mL) had detectable ARV, and both of 454), compared with 13% (46 of 349) among white MSM had only zidovudine detected. Lack of Awareness of HIV Infection Among MSM OFID 3 � � Figure 1. Lack of awareness of human immunodeficiency virus (HIV) se- rostatus among black and white men who have sex with men (MSM) in the InvolveMENt study, 2010–2012, using 3 approaches to defining lack of awareness. χ P values provided. There were 35 participants (34 black MSM and 1 white MSM) who were classified as not aware on self-report and had a previous HIV diagnosis reported to the health department. The mean time between the first HIV diagnosis reported to the health department and the InvolveMENt study baseline visit was ∼4.4 years. Based on self-report only, black MSM were significantly less likely to be aware of their HIV infection than were white MSM (Figure 1). Based on self-report combined with any of the other criteria, the proportions of black MSM not aware of their infec- tion were not significantly higher than the proportions of white MSM not aware. Based on self-report and previous report to the health department, the proportions of black MSM and white MSM not aware of their infection was essentially the same (15% and 13%, respectively). Of the 55 participants who did not self-report awareness and were invited to the in-depth interviews, 15 took part (13 black MSM and 2 white MSM). Twelve participants confirmed accu- racy of their survey responses in regards to not being previou- sly aware of their HIV infection, 2 of whom had detectable ARV. Three participants identified inaccuracies in their original survey responses: 1 reported that his most recent test was HIV- negative, but his survey response was “indeterminate”;1reported that his most recent test was HIV-positive, but his survey response was “didn’t get result of most recent test”; and 1 was aware of his previous HIV diagnosis but had been retested and had not gotten the result of that most recent test. There were no issues noted in the comprehension of the HIV testing history questions. DISCUSSION Up to one half of our study participants who were not con- sidered to be aware of their positive HIV status based on 4 OFID Sanchez et al � � Table 2. Antiretroviral Drugs Detected Among Men Who Have Sex with Men Classified as Lacking Awareness of Their HIV Infection Based on Self-disclosure, InvolveMENt Study, 2010–2012 ARV detected HIV Viral Load NRTI Quantification Mass Spectrometry Participant ID (Copies/mL) ARV Detected ARV Detected ABC FPV ATV DRV FTC EFV IDV 3TC LPV NFV NVP RTV SQV TDF TPV ZDV 021 Undetectable Yes Yes x x x 031 162 Yes Yes x x 051 16802 Not Performed Yes x 081 14755 Not Performed Yes x 151 28 Yes Yes x x 171 Undetectable Yes Yes x x x 241 70 Yes Yes x x x 271 743 No Yes x x x x 451 Undetectable Yes Yes x x 521 181 Not Performed Yes x 591 Undetectable No Yes x 621 62 Yes Yes x x x Abbreviations: ABC, abacavir; ARV, antiretroviral; ATV, atazanavir; DRV, darunavir; EFV, efavirenz; FPV, amprenavir; FTC, emtricitabine; IDV, indinavir; LPV, lopinavir; NFV, nelfinavir; NRTI, nucleoside/nucleotide reverse- transcriptase inhibitor; NVP, nevirapine; RTV, ritonavir; SQV, saquinavir; TDF, tenofovir; TPV, tipranavir; ZDV, zidovudine; 3TC, lamivudine. discordance between self-report and testing results may have that almost two-thirds of black MSM have had an HIV test in actually been aware of their HIV infection. During qualitative the past year [25], but the average time between first case sur- interviewing with a subset of participants, we found some veillance report and our study’s diagnosis was more than 4 inconsistencies between survey responses and detailed ques- years. Even if ourparticipantsdid notget theresultofthat tions about HIV testing history, but there was no evidence of first reported diagnosis, the typical frequency of HIV testing systematic misinterpretation of testing questions or response among MSM makes it unlikely that they would have gone this options. When we used any of the alternative methods of defin- length of time without another HIV test for which they got their ing awareness, the difference in awareness between black and test result. white MSM was no longer significant. It should also be noted that several participants confirmed Our study’s sample size did not allow us to calculate sensitiv- their survey responses during the in-depth interviews, although ity and specificity of the laboratory measures of awareness, but results of ARV testing indicated that they were taking ARVs and this framework may be useful to consider here. The specificity therefore likely aware of their HIV status at the time of enroll- of ARV testing is likely very high as a measure of awareness of ment. These participants were also aware that researchers al- HIV status because there are probably few situations in which ready knew of their status through the study-delivered testing. someone not aware of their status would have detectable ARV; We did not have the results of all of the ARV testing at the one such possibility is use of HIV pre-exposure prophylaxis time of these interviews, and participants were not specifically (PrEP) [21]. The Centers for Disease Control and Prevention asked about possible discrepancies between the different mea- guidance on PrEP use among MSM was released in the middle sures of awareness. Regardless, these interviews still underscore of our study, and although we added questions about current that some part of the research process is creating an environ- PrEP use in follow-up surveys, most participants were not ment in which black MSM do not feel inclined to disclose asked this question in their baseline survey. The sensitivity of knowledge of their HIV status to researchers. This may be ARV detection as a measure of awareness is more questionable due to HIV-related stigma or distrust in HIV research, both and likely dependent on many factors, especially being engaged of which have been reported among black MSM [26–28]. in care and being adherent to an ARV regimen. The specificity The significant racial differences in self-reported awareness of of low VL as a measure of awareness is also likely high because, HIV infection in our study is similar to that reported by NHBS- although it is possible that a person may have a low VL but not MSM [29]. The HIV testing history questions used in our study be aware of his HIV status (eg, an “HIV controller”), this situa- were the same as those used in the first cycle of NHBS-MSM, tion is probably uncommon. Although there are no population- but more recent versions of the NHBS-MSM survey include level studies of VL in treatment-naive persons, there was an 8% an additional question about ever having had an HIV diagnosis. prevalence of VL <1000 copies/mL in reportedly treatment- There was no significant change in self-reported awareness of naive participants in a large combined study of multiple pro- HIV status between the first and second versions of the NHBS- spective research cohorts of patients infected with HIV [22]. MSM survey [30]; therefore, it is also unlikely that the addition of The prevalence of HIV controllers (>10 years of infection dura- the more sensitive “ever positive” question would have substan- tion and 90% of VL <500 copies/mL) was estimated to be 0.22% tially altered our findings. In addition, only 1 participant of the in 1 large cohort study of persons infected with HIV in France in-depth interviews reported awareness of his status based on [23]. Our findings suggest that the sensitivity of a low VL as a ever having a positive HIV test result. measure of awareness may be high because we found that all but Human immunodeficiency virus case surveillance data esti- 2 participants with detectable ARV had low VL. Future studies mates that 19.4% of MSM living with HIV infection in the Unit- with larger samples of HIV-positive persons should explore fur- ed States have not yet been diagnosed [31]. Although these ther the sensitivity and specificity of these 2 measures separately surveillance estimates should not be interpreted to be equivalent and in combination. to lack of awareness of HIV status, the wide discrepancy be- Matching findings from research studies to HIV case surveil- tween the most recent NHBS-MSM estimate (34%) and the sur- lance reports may also be a viable means of estimating lack of veillance-based estimate are problematic for public health [32]. awareness of HIV infection. Verification of whether a previous Our study gives a potential explanation for this discrepancy: positive HIV test result was returned to a patient is not part of that self-report alone may overestimate lack of awareness the surveillance case report. Men may have had a previous pos- among black MSM because of misclassification. itive HIV test but not actually received the results of the test and There is evidence from other research that underreporting of therefore may not have been aware of their status, although awareness to researchers is occurring. A recently published study there are factors that argue against this. Another study found from enrollment of black MSM in a community-randomized that 90% of MSM get the results of their HIV test and did HIV prevention trial in 5 cities (including Atlanta) determined not find any significant racial difference in getting results that among 155 HIV-positive black MSM who said that they [24]. Previous behavioral surveillance data have also reported were not aware of their HIV status, 54% had a VL of <1000 Lack of Awareness of HIV Infection Among MSM OFID 5 � � copies/mL and 78% of those had detectable ARVs [5, 16]. These larger studies that apply multiple measures of determining results are substantially higher than those we observed in our awareness of status and that include qualitative interviews to Atlanta cohort of black and white MSM. That other study specif- specifically explore situations in which there is a discrepancy ically recruited and enrolled black MSM who believed themselves in these measures. Until a potential gold standard for awareness to be HIV-negative, which may have produced the discrepancy of HIV status can be determined from these larger studies, fu- between our findings. Underreporting of awareness by HIV- ture HIV research that relies on the accuracy of this indicator positive black MSM may also not be isolated to just the research should consider using multiple ways to measure it. environment. Other studies have reported that from one third to one half of HIV-positive black MSM do not disclose their seros- Acknowledgments tatus to sexual partners [32, 33]. Author contributions. T. H. S. and N. L. conducted the quantitative The current paradigm for racial disparity in HIV infection analyses. R. C. collected the qualitative data, and T. H. S. and R. C. conduct- dictates that the higher rates of HIV acquisition among black ed the qualitative analyses. R. L. conducted the surveillance case match. S. T. MSM are due in part to (1) an increased likelihood for black MSM and W. C. conducted the ARV testing, and C. F. K. conducted analysis and wrote these sections of the paper. E. R. and B. O. created the data structure to have black male sex partners; (2) a higher rate of HIV preva- and verified analyses.P.F., L. F. S.,C. d.R., andP.S.S. designedthe lence among black MSM; and (3) a lower awareness of HIV status study. P. S. S. led the study. All authors contributed to the drafting of the among HIV-positive black MSM [4, 6]. This third pillar of the manuscript and read and approved the final version. Financial support. This work supported by the National Institute of paradigm is based on a premise that black MSM are less likely Mental Health (grant R01MH085600); Minority Health and Health Dispar- to be aware of their HIV status than are white MSM and are ities (grant RC1MD004370); Eunice Kennedy Shriver National Institute for therefore less able act on this knowledge to protect their suscep- Child Health and Human Development (grant R01HD067111); National tible sexual partners from exposure to HIV. At a minimum, the Institutes of Health (grant P30AI050409)-the Emory Center for AIDS Re- search; and the National Center for Advancing Translational Sciences (grant magnitude of disparity in lack of awareness of HIV status for UL1TR000454). black MSM may be overstated with the use of only self-reported data. If, as our data suggest, black MSM are equally aware of their References HIV status compared with white MSM, then the field would need to reconsider this paradigm and the HIV prevention programs 1. Hall HI, Song R, Rhodes P, et al. Estimation of HIV incidence in the United States. JAMA 2008; 300:520–9. upon which it is built. 2. Prejean J, Song R, Hernandez A, et al. Estimated HIV incidence in the Several limitations should be noted for this analysis. Our United States, 2006-2009. PloS One 2011; 6:e17502. study involved incentivized research and had relatively small 3. Purcell DW, Johnson CH, Lansky A, et al. 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Lack of Awareness of HIV Infection Among MSM OFID 7 � � http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Open Forum Infectious Diseases Oxford University Press

Lack of Awareness of Human Immunodeficiency Virus (HIV) Infection: Problems and Solutions With Self-reported HIV Serostatus of Men Who Have Sex With Men

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© The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America.
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MA JO R A R T IC LE Lack of Awareness of Human Immunodeficiency Virus (HIV) Infection: Problems and Solutions With Self-reported HIV Serostatus of Men Who Have Sex With Men 1 1,2 1 1 1 3 Travis H. Sanchez, Colleen F. Kelley, Eli Rosenberg, Nicole Luisi, Brandon O’Hara, Rodriques Lambert, 1 1,2 4 5 6 1 1 Raphael Coleman, Paula Frew, Laura F. Salazar, Sijia Tao, William Clarke, Carlos del Rio, and Patrick S. Sullivan 1 2 Rollins School of Public Health, Emory University and Emory Center for AIDS Research, Division of Infectious Disease, Department of Medicine, Emory 3 4 University School of Medicine, HIV/AIDS Epidemiology, Georgia Department of Public Health, School of Public Health, Georgia State University, and 5 6 Laboratory of Biochemical Pharmacology, Emory University, Atlanta, Georgia; and School of Medicine, Johns Hopkins University, Baltimore, Maryland Background. Lack of human immunodeficiency virus (HIV) infection awareness may be a driver of racial dispar- ities in HIV infection among men who have sex with men (MSM). Lack of awareness is typically measured by comparing HIV test result to self-reported HIV status. This measure may be subject to reporting bias and alternatives are needed. Methods. The InvolveMENt study examined HIV disparities between black and white MSM from Atlanta. Among HIV-positive participants who did not report knowing they were positive, we examined other measures of awareness: HIV viral load (VL) <1000 copies/mL (low VL), antiretroviral (ARV) drugs in blood, and previous HIV case surveillance report. Results. Using self-report only, 32% (62 of 192) of black and 16% (7 of 45) of white MSM were not aware of their HIV infection (P = .03). Using self-report and low VL, 25% (48 of 192) black and 16% (7 of 45) white MSM lacked awareness (P = .18). Using self-report and ARVs, 26% (50 of 192) black and 16% (7 of 45) white MSM lacked awareness (P = .14). Using self-report and surveillance report, 15% (28 of 192) black and 13% (6 of 45) white MSM lacked aware- ness (P =.83). Conclusions. Self-report only may overestimate true lack of awareness of HIV status for black MSM. If, as our data suggest, black MSM are not less likely to be aware of their HIV infection than are white MSM, then this factor is not a substantial driver of HIV disparity. Future HIV research that depends on accurate measurement of HIV status awareness should consider including additional laboratory and case surveillance data. Keywords. HIV; MSM; survey; testing. Over the past decade, men who have sex with men incidence has increased [1]. More recently, increases (MSM) have been the only group in the United States in incidence have been concentrated among young in which human immunodeficiency virus (HIV) MSM of color [2]. Black MSM have over twice the prev- alence of HIV than white men, [3, 4] and data from the HIV Prevention Trials Network study number 061 sug- gest that black MSM experience an HIV incidence rate Received 23 May 2014; accepted 08 August 2014. over 5 times that of white MSM [5]. The reasons for Correspondence: Travis H. Sanchez, DVM, MPH, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, GA 30322 (travis.sanchez@emory. these racial disparities in HIV infection among MSM edu). are unclear, but differences in individual-level risk be- Open Forum Infectious Diseases haviors likely do not account for the observed dispari- © The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Societyof America. This is an Open Access article distributed under the terms ties [4, 6]. This same pattern of disparity exists among of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http:// black MSM in Atlanta, the city with the 8th highest creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work rate of new HIV diagnoses and 4th highest number of is not altered or transformed in any way, and that the work is properly cited. For new HIV diagnoses among MSM in the country in 2011 commercial re-use, please contact journals.permissions@oup.com. DOI: 10.1093/ofid/ofu084 [7]. Men who have sex with men comprise the largest Lack of Awareness of HIV Infection Among MSM OFID 1 � � group living with HIV in Atlanta, and black MSM are dis- participants were informed that they would be screened for proportionately affected, constituting approximately 60% of HIV infection, but the criteria for which participants would HIV-infected MSM, whereas black persons represent only ap- be offered enrollment in the prospective component of the proximately 30% of the overall Atlanta population [8]. study were not specifically discussed. Differences in awareness of HIV infection between black and All InvolveMENt study participants were tested for HIV white MSM are hypothesized to contribute to this disparity [6]. using a rapid test with confirmation by enzyme-linked immu- Overall, approximately 20% of persons infected with HIV in the nosorbent assay and Western blot analysis. Before results of United States are thought to be unaware of their infection; how- HIV testing were returned, participants completed a detailed ever, they account for an estimated 49% of transmission events computer-assisted self-interview. All HIV-positive men had [9]. Awareness of HIV infection results in a reduction in high- HIV VL testing (COBAS AmpliPrep/COBAS TaqMan HIV-1 risk sexual behavior [10], and it is the first critical step in the test kit version 2.0; Roche Molecular Systems, Inc.), and these continuum of HIV care, which ideally results in receipt of anti- results were returned to participants. Participants who had a retroviral (ARV) therapy, achievement of an undetectable HIV negative HIV rapid test at baseline were offered enrollment in viral load (VL), and reduction in HIV transmissions [11–13]. the follow-up study. If a participant subsequently tested HIV National surveillance data show that black MSM have high lev- positive at the 3-month visit, we conducted VL testing on the els (59%) of lack of awareness of HIV infection compared with stored specimen from the baseline visit. Those who had detect- white MSM (26%) [14]. able VL (but who were nonreactive on the HIV rapid test) were HIV surveillance projects and research studies use a similar considered to have acute HIV infection at the time of their base- set of testing history questions to define self-reported lack of line visit. The InvolveMENt study staff (eg, counselors, phlebot- awareness of infection that is detected through study-delivered omists, interviewers) were diverse in regards to race, ethnicity, testing. However, there are new reports that the validity of this age, and gender. The InvolveMENt study was reviewed and ap- self-reported measure may be questionable for some groups of proved by the institutional review board of Emory University. MSM [5, 15, 16]. It remains unknown whether the validity of these measures may differ by participant race and whether via- Measures ble solutions to improve the measure may be available to HIV We used several approaches to classify HIV infection awareness. researchers. For this study, we hypothesized that the combina- The first method (“self-reported”)defined awareness of infec- tion of traditional survey, laboratory, and public health surveil- tion using a set of questions about their experiences ever getting lance data could improve the measurement of awareness of HIV tested, the most recent testing experiences, and their most re- infection among black and white MSM participants of a cent test result. In addition, during the posttest result discus- research study in Atlanta, Georgia. sion, any participant who disclosed prior knowledge of their HIV status to the study counselor was classified as “self-reported aware,” even if they did not report having a previous HIV-positive METHODS test in their survey. InvolveMENt Study Among those who were classified as not aware of their HIV The InvolveMENt study was a prospective cohort study de- infection by self-report, we also explored 2 laboratory measures signed to examine factors that may contribute to disparities in and a public health surveillance measure of awareness. One lab- HIV and sexually transmitted infection between black and oratory measure was low VL (<1000 copies/mL or undetectable) white MSM in Atlanta. MSM aged 18–39 years were recruited, on the baseline blood specimen. The other laboratory measure regardless of HIV status, primarily using time-space venue sam- was detectable ARV drugs using either of 2 nonmutually exclu- pling, with a sampling frame built upon that used for the Atlan- sive algorithms. First, for those MSM classified as not aware of ta site for the second MSM cycle of the National HIV their HIV infection by self-report and who also had a low VL, we Behavioral Surveillance System (NHBS-MSM) [17, 18]. Face- conducted a limited quantification ARV panel that included book was also included as a virtual venue. The InvolveMENt commonly prescribed nucleoside/nucleotide reverse-transcrip- study methods have been previously reported but are briefly tase inhibitors ([NRTIs] abacavir, emtricitabine, lamivudine, te- described here [19]. Eligible participants were self-identified nofovir, and zidovudine) [20]. This limited quantification ARV black and white MSM who reported sex with another man panel was the first we explored and was not done on all specimens in the previous 3 months, who were not in a mutually monog- because of the potential expense involved. Second, for all MSM amous relationship, could complete survey instruments in classified as not aware by self-report, we used mass spectrome- English, lived in the Atlanta metropolitan area, were not en- try to test an expanded ARV panel that included NRTIs (emtri- rolled in another HIV prevention study, who did not identify citabine, lamivudine, tenofovir, and zidovudine), nonnucleotide as Hispanic/Latino, and had no plans to relocate in the subse- reverse-transcriptase inhibitors (efavirenz and nevirapine), and quent 2 years. During the baseline visit consent process, protease inhibitors (atazanavir, darunavir, fosamprenavir, 2 OFID Sanchez et al � � indinavir, lopinavir, nelfinavir, ritonavir, saquinavir, and tipra- Table 1. Characteristics of MSM Classified as Lacking Awareness of Their HIV Infection, InvolveMENt Study, 2010–2012 navir) [16]. The results of the ARV testing were not returned to participants. Black MSM White For the public health surveillance measure of awareness, we (N = 62) MSM used evidence of a preexisting HIV case surveillance report at (N =7) the Georgia Department of Public Health. We submitted to No. (%) No. (%) the state health department a line-listing of black and white par- HIV Testing History Questions ticipants considered not aware of their status by self-report. The Never Tested 14 (23) 1 (14) health department reported back on the total number of per- Ever Tested, Last Result sons from the list who were already in the HIV case surveillance Negative 39 (63) 6 (86) system and whose first HIV diagnosis in the system had oc- Indeterminate 3 (5) 0 (0) curred at least 21 days before our diagnosis. This timeframe Didn’t Get It 6 (10) 0 (0) was selected to ensure that persons who were previously diag- HIV Viral Load <1000 copies/mL 14 (23) 0 (0) nosed more recently would have had at least some opportunity Any Antiretroviral Drug Detected 12 (19) 0 (0) to receive their previous test result. To protect confidentiality of Mass Spectrometry 12 (19) 0 (0) case surveillance data, the health department did not return a NRTI Quantification 7 (11) 0 (0) list of persons with previous diagnoses to the study’s research- Previously Reported to HIV Case 34 (55) 1 (14) Surveillance ers, but it only provided us with aggregate numbers. The health department also reported the mean number of days between the Abbreviations: HIV, human immunodeficiency virus; MSM, men who have sex with men; NRTI, nucleoside/tide reverse-transcriptase inhibitor. first HIV diagnosis in the system and our diagnosis. NRTI blood levels only performed among those with HIV viral load <1000 Participants who enrolled through February 2012 and were copies/mL. not aware of their HIV infection by self-report were also invited Average time between previous report and InvolveMENt report = 1590 days. to participate in an in-depth interview. A staff interviewer con- ducted one-on-one discussions with participants at a follow-up visit to the study office (ie, the qualitative interviews happened (prevalence ratio = 3.3; 95% confidence interval = 2.5, 4.4) [19]. after the visit in which they tested HIV-positive). The interview- There were 5 black MSM and 1 white MSM who were considered er used a semistructured qualitative interview method with a set to have acute HIV infection at the time of their baseline visit and of open-ended question domains with follow-up probes. The were excluded from further analysis. purpose of the interviews was to generate more detailed infor- Among black MSM with HIV infection at baseline, 69 were mation about previous HIV testing experiences and diagnoses, classified as not aware on survey responses alone, and 7 dis- general themes regarding disclosure of HIV status, and rephras- closed knowledge of their status during posttest counseling. ing activities to better understand comprehension of the HIV Among white MSM with HIV infection at baseline, 8 were clas- testing questions. Participants were not specifically asked sified as not aware by survey responses alone, and 1 disclosed about possible discrepancies between self-reported awareness knowledge of his status during posttest counseling. The measure and laboratory testing. of self-reported lack of awareness of HIV status was 32% (62 of 192) among black MSM and 16% (7 of 45) among white MSM. Analyses Most participants (65%, 45 of 69) who disclosed not being We compared lack of awareness of HIV infection between black aware of their infection had been previously HIV tested and re- and white MSM using χ tests for the different measures: self- ported that their most recent test result was negative (Table 1). report alone, self-report plus low VL, self-report plus detectable Fourteen participants (14 black MSM and 0 white MSM) ARV, and self-report plus previous HIV case surveillance re- who were classified as not aware by self-report had a low VL. port. Findings were considered significant if P < .05. Statistical The limited panel of ARV testing was completed for 13 of analyses were performed using OpenEpi (www.OpenEpi.com, them; 7 of whom had at least 1 NRTI detected. The expanded version 2013/04/06). ARV panel was completed for 60 of 69 MSM (53 of 62 black MSM and 7 of 7 white MSM); 12 of whom (all black MSM) had ARV detected. Thirteen participants had both types of ARV RESULTS testing; 7 of whom had ARV detected on both tests, 4 had no Enrollment occurred from July 2010 through December 2012, re- ARV detected on either test, and 2 had ARV on mass spectrom- sulting in a total of 454 black MSM and 349 white MSM being etry that was not detected on the quantitative NRTI test (Table 2 enrolled and contributing to this analysis. The prevalence of HIV shows detected ARV results). Two participants with high VL infection at the baseline visit among black MSM was 43% (197 (14 755 and 16 802 copies/mL) had detectable ARV, and both of 454), compared with 13% (46 of 349) among white MSM had only zidovudine detected. Lack of Awareness of HIV Infection Among MSM OFID 3 � � Figure 1. Lack of awareness of human immunodeficiency virus (HIV) se- rostatus among black and white men who have sex with men (MSM) in the InvolveMENt study, 2010–2012, using 3 approaches to defining lack of awareness. χ P values provided. There were 35 participants (34 black MSM and 1 white MSM) who were classified as not aware on self-report and had a previous HIV diagnosis reported to the health department. The mean time between the first HIV diagnosis reported to the health department and the InvolveMENt study baseline visit was ∼4.4 years. Based on self-report only, black MSM were significantly less likely to be aware of their HIV infection than were white MSM (Figure 1). Based on self-report combined with any of the other criteria, the proportions of black MSM not aware of their infec- tion were not significantly higher than the proportions of white MSM not aware. Based on self-report and previous report to the health department, the proportions of black MSM and white MSM not aware of their infection was essentially the same (15% and 13%, respectively). Of the 55 participants who did not self-report awareness and were invited to the in-depth interviews, 15 took part (13 black MSM and 2 white MSM). Twelve participants confirmed accu- racy of their survey responses in regards to not being previou- sly aware of their HIV infection, 2 of whom had detectable ARV. Three participants identified inaccuracies in their original survey responses: 1 reported that his most recent test was HIV- negative, but his survey response was “indeterminate”;1reported that his most recent test was HIV-positive, but his survey response was “didn’t get result of most recent test”; and 1 was aware of his previous HIV diagnosis but had been retested and had not gotten the result of that most recent test. There were no issues noted in the comprehension of the HIV testing history questions. DISCUSSION Up to one half of our study participants who were not con- sidered to be aware of their positive HIV status based on 4 OFID Sanchez et al � � Table 2. Antiretroviral Drugs Detected Among Men Who Have Sex with Men Classified as Lacking Awareness of Their HIV Infection Based on Self-disclosure, InvolveMENt Study, 2010–2012 ARV detected HIV Viral Load NRTI Quantification Mass Spectrometry Participant ID (Copies/mL) ARV Detected ARV Detected ABC FPV ATV DRV FTC EFV IDV 3TC LPV NFV NVP RTV SQV TDF TPV ZDV 021 Undetectable Yes Yes x x x 031 162 Yes Yes x x 051 16802 Not Performed Yes x 081 14755 Not Performed Yes x 151 28 Yes Yes x x 171 Undetectable Yes Yes x x x 241 70 Yes Yes x x x 271 743 No Yes x x x x 451 Undetectable Yes Yes x x 521 181 Not Performed Yes x 591 Undetectable No Yes x 621 62 Yes Yes x x x Abbreviations: ABC, abacavir; ARV, antiretroviral; ATV, atazanavir; DRV, darunavir; EFV, efavirenz; FPV, amprenavir; FTC, emtricitabine; IDV, indinavir; LPV, lopinavir; NFV, nelfinavir; NRTI, nucleoside/nucleotide reverse- transcriptase inhibitor; NVP, nevirapine; RTV, ritonavir; SQV, saquinavir; TDF, tenofovir; TPV, tipranavir; ZDV, zidovudine; 3TC, lamivudine. discordance between self-report and testing results may have that almost two-thirds of black MSM have had an HIV test in actually been aware of their HIV infection. During qualitative the past year [25], but the average time between first case sur- interviewing with a subset of participants, we found some veillance report and our study’s diagnosis was more than 4 inconsistencies between survey responses and detailed ques- years. Even if ourparticipantsdid notget theresultofthat tions about HIV testing history, but there was no evidence of first reported diagnosis, the typical frequency of HIV testing systematic misinterpretation of testing questions or response among MSM makes it unlikely that they would have gone this options. When we used any of the alternative methods of defin- length of time without another HIV test for which they got their ing awareness, the difference in awareness between black and test result. white MSM was no longer significant. It should also be noted that several participants confirmed Our study’s sample size did not allow us to calculate sensitiv- their survey responses during the in-depth interviews, although ity and specificity of the laboratory measures of awareness, but results of ARV testing indicated that they were taking ARVs and this framework may be useful to consider here. The specificity therefore likely aware of their HIV status at the time of enroll- of ARV testing is likely very high as a measure of awareness of ment. These participants were also aware that researchers al- HIV status because there are probably few situations in which ready knew of their status through the study-delivered testing. someone not aware of their status would have detectable ARV; We did not have the results of all of the ARV testing at the one such possibility is use of HIV pre-exposure prophylaxis time of these interviews, and participants were not specifically (PrEP) [21]. The Centers for Disease Control and Prevention asked about possible discrepancies between the different mea- guidance on PrEP use among MSM was released in the middle sures of awareness. Regardless, these interviews still underscore of our study, and although we added questions about current that some part of the research process is creating an environ- PrEP use in follow-up surveys, most participants were not ment in which black MSM do not feel inclined to disclose asked this question in their baseline survey. The sensitivity of knowledge of their HIV status to researchers. This may be ARV detection as a measure of awareness is more questionable due to HIV-related stigma or distrust in HIV research, both and likely dependent on many factors, especially being engaged of which have been reported among black MSM [26–28]. in care and being adherent to an ARV regimen. The specificity The significant racial differences in self-reported awareness of of low VL as a measure of awareness is also likely high because, HIV infection in our study is similar to that reported by NHBS- although it is possible that a person may have a low VL but not MSM [29]. The HIV testing history questions used in our study be aware of his HIV status (eg, an “HIV controller”), this situa- were the same as those used in the first cycle of NHBS-MSM, tion is probably uncommon. Although there are no population- but more recent versions of the NHBS-MSM survey include level studies of VL in treatment-naive persons, there was an 8% an additional question about ever having had an HIV diagnosis. prevalence of VL <1000 copies/mL in reportedly treatment- There was no significant change in self-reported awareness of naive participants in a large combined study of multiple pro- HIV status between the first and second versions of the NHBS- spective research cohorts of patients infected with HIV [22]. MSM survey [30]; therefore, it is also unlikely that the addition of The prevalence of HIV controllers (>10 years of infection dura- the more sensitive “ever positive” question would have substan- tion and 90% of VL <500 copies/mL) was estimated to be 0.22% tially altered our findings. In addition, only 1 participant of the in 1 large cohort study of persons infected with HIV in France in-depth interviews reported awareness of his status based on [23]. Our findings suggest that the sensitivity of a low VL as a ever having a positive HIV test result. measure of awareness may be high because we found that all but Human immunodeficiency virus case surveillance data esti- 2 participants with detectable ARV had low VL. Future studies mates that 19.4% of MSM living with HIV infection in the Unit- with larger samples of HIV-positive persons should explore fur- ed States have not yet been diagnosed [31]. Although these ther the sensitivity and specificity of these 2 measures separately surveillance estimates should not be interpreted to be equivalent and in combination. to lack of awareness of HIV status, the wide discrepancy be- Matching findings from research studies to HIV case surveil- tween the most recent NHBS-MSM estimate (34%) and the sur- lance reports may also be a viable means of estimating lack of veillance-based estimate are problematic for public health [32]. awareness of HIV infection. Verification of whether a previous Our study gives a potential explanation for this discrepancy: positive HIV test result was returned to a patient is not part of that self-report alone may overestimate lack of awareness the surveillance case report. Men may have had a previous pos- among black MSM because of misclassification. itive HIV test but not actually received the results of the test and There is evidence from other research that underreporting of therefore may not have been aware of their status, although awareness to researchers is occurring. A recently published study there are factors that argue against this. Another study found from enrollment of black MSM in a community-randomized that 90% of MSM get the results of their HIV test and did HIV prevention trial in 5 cities (including Atlanta) determined not find any significant racial difference in getting results that among 155 HIV-positive black MSM who said that they [24]. Previous behavioral surveillance data have also reported were not aware of their HIV status, 54% had a VL of <1000 Lack of Awareness of HIV Infection Among MSM OFID 5 � � copies/mL and 78% of those had detectable ARVs [5, 16]. These larger studies that apply multiple measures of determining results are substantially higher than those we observed in our awareness of status and that include qualitative interviews to Atlanta cohort of black and white MSM. That other study specif- specifically explore situations in which there is a discrepancy ically recruited and enrolled black MSM who believed themselves in these measures. Until a potential gold standard for awareness to be HIV-negative, which may have produced the discrepancy of HIV status can be determined from these larger studies, fu- between our findings. Underreporting of awareness by HIV- ture HIV research that relies on the accuracy of this indicator positive black MSM may also not be isolated to just the research should consider using multiple ways to measure it. environment. Other studies have reported that from one third to one half of HIV-positive black MSM do not disclose their seros- Acknowledgments tatus to sexual partners [32, 33]. Author contributions. T. H. S. and N. L. conducted the quantitative The current paradigm for racial disparity in HIV infection analyses. R. C. collected the qualitative data, and T. H. S. and R. C. conduct- dictates that the higher rates of HIV acquisition among black ed the qualitative analyses. R. L. conducted the surveillance case match. S. T. MSM are due in part to (1) an increased likelihood for black MSM and W. C. conducted the ARV testing, and C. F. K. conducted analysis and wrote these sections of the paper. E. R. and B. O. created the data structure to have black male sex partners; (2) a higher rate of HIV preva- and verified analyses.P.F., L. F. S.,C. d.R., andP.S.S. designedthe lence among black MSM; and (3) a lower awareness of HIV status study. P. S. S. led the study. All authors contributed to the drafting of the among HIV-positive black MSM [4, 6]. This third pillar of the manuscript and read and approved the final version. Financial support. This work supported by the National Institute of paradigm is based on a premise that black MSM are less likely Mental Health (grant R01MH085600); Minority Health and Health Dispar- to be aware of their HIV status than are white MSM and are ities (grant RC1MD004370); Eunice Kennedy Shriver National Institute for therefore less able act on this knowledge to protect their suscep- Child Health and Human Development (grant R01HD067111); National tible sexual partners from exposure to HIV. At a minimum, the Institutes of Health (grant P30AI050409)-the Emory Center for AIDS Re- search; and the National Center for Advancing Translational Sciences (grant magnitude of disparity in lack of awareness of HIV status for UL1TR000454). black MSM may be overstated with the use of only self-reported data. If, as our data suggest, black MSM are equally aware of their References HIV status compared with white MSM, then the field would need to reconsider this paradigm and the HIV prevention programs 1. Hall HI, Song R, Rhodes P, et al. Estimation of HIV incidence in the United States. JAMA 2008; 300:520–9. upon which it is built. 2. Prejean J, Song R, Hernandez A, et al. Estimated HIV incidence in the Several limitations should be noted for this analysis. Our United States, 2006-2009. PloS One 2011; 6:e17502. study involved incentivized research and had relatively small 3. Purcell DW, Johnson CH, Lansky A, et al. 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Journal

Open Forum Infectious Diseases – Oxford University Press

Published: Sep 1, 2014

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