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HIV Drug Resistance in a Cohort of HIV-Infected MSM in the United States

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HIV Drug Resistance in a Cohort of HIV-Infected MSM in the United States HIV drug resistance in a cohort of HIV-infected MSM in the United States Jessica M. Fogela, Mariya V. Sivaya, Vanessa Cummingsa, Ethan A. Wilsonb, Stephen Hartc, Theresa Gambled, Oliver Laeyendeckere,f, Reinaldo E. Fernandezf, Carlos Del Riog, D. Scott Bateyh, Kenneth H. Mayeri,j, Jason E. Farleyk, Laura McKinstryb, James P. Hughesl, Robert H. Remienm, Chris Beyrern and Susan H. Eshlemana 12/16/2019 on BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3K8IvHCABgh/JBbI4K3ZsIj3/NC/+bQxLNOd90PvZp0g= by https://journals.lww.com/aidsonline from Downloaded Downloaded Objective: To analyze HIV drug resistance among MSM recruited for participation in from https://journals.lww.com/aidsonline the HPTN 078 study, which evaluated methods for achieving and maintaining viral suppression in HIV-infected MSM. Methods: Individuals were recruited at four study sites in the United States (Atlanta, Georgia; Baltimore, Maryland; Birmingham, Alabama; and Boston, Massachusetts; 2016–2017). HIV genotyping was performed using samples collected at study screen- ing or enrollment. HIV drug resistance was evaluated using the Stanford v8.7 algorithm. by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3K8IvHCABgh/JBbI4K3ZsIj3/NC/+bQxLNOd90PvZp0g= A multiassay algorithm was used to identify individuals with recent HIV infection. Clustering of HIV sequences was evaluated using phylogenetic methods. Results: High-level HIV drug resistance was detected in 44 (31%) of 142 individuals (Atlanta: 21%, Baltimore: 29%, Birmingham: 53%, Boston: 26%); 12% had multiclass resistance, 16% had resistance to tenofovir or emtricitabine, and 8% had resistance to integrase strand transfer inhibitors (INSTIs); 3% had intermediate-level resistance to second-generation INSTIs. In a multivariate model, self-report of ever having been on antiretroviral therapy (ART) was associated with resistance (P ¼ 0.005). One of six recently infected individuals had drug resistance. Phylogenetic analysis identified five clusters of study sequences; two clusters had shared resistance mutations. Conclusion: High prevalence of drug resistance was observed among MSM. Some had multiclass resistance, resistance to drugs used for preexposure prophylaxis (PrEP), and INSTI resistance. These findings highlight the need for improved HIV care in this high- risk population, identification of alternative regimens for PrEP, and inclusion of integrase resistance testing when selecting ART regimens for MSM in the United States. Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved. AIDS 2020, 34:91–101 Keywords: HIV drug resistance, HPTN 078, MSM, phylogenetic analysis, United States on 12/16/2019 aDepartment of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland, bFred Hutchinson Cancer Research Center, Seattle, Washington, cFrontier Science Foundation, Amherst, New York, dFHI 360, Durham, North Carolina, eNIAID, National Institutes of Health, fDepartment of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, gEmory University Rollins School of Public Health and School of Medicine, Atlanta, Georgia, hDepartment of Social Work, University of Alabama at Birmingham, Birmingham, Alabama, iDepartment of Medicine, Harvard Medical School, jFenway Institute, Boston, Massachusetts, kJohns Hopkins University School of Nursing, Baltimore, Maryland, lDepartment of Biostatistics, University of Washington, Seattle, Washington, mHIV Center for Clinical and Behavioral Studies, NY State Psychiatric Institute and Columbia University, New York, New York, and nDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA. Correspondence to Susan H. Eshleman, MD, PhD, Department of Pathology, The Johns Hopkins Medical Institutions, Ross Building, Room 646, 720 Rutland Avenue, Baltimore, MD 21205, USA. Tel: +1 410 614 4734; fax: +1 410 502 9244; e-mail: [email protected] Received: 19 March 2019; revised: 4 September 2019; accepted: 15 September 2019. DOI:10.1097/QAD.0000000000002394 ISSN 0269-9370 Copyright Q 2019 Wolters Kluwer Health, Inc. All rights reserved. 91 Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved. 92 AIDS 2020, Vol 34 No 1 Introduction Methods In the United States, the current administration’s plan, Study cohort ‘Ending the HIV Epidemic: A Plan for America’, includes The HPTN 078 (NCT02663219) clinical trial was interventions such as early antiretroviral therapy (ART) to conducted in Atlanta, Georgia; Baltimore, Maryland; achieve viral suppression and preexposure prophylaxis Birmingham, Alabama; and Boston, Massachusetts. (PrEP) [1]. Goals of this program and other programs for Individuals aged 16 years or older were recruited using HIV treatment and prevention may be compromised by deep-chain RDS (DC-RDS) and direct recruitment. HIV drug resistance [2,3]. Acquired drug resistance can DC-RDS recruitment was conducted by identifying emerge in HIV-infected individuals with sub-optimal ‘seeds’ who referred members in their social and sexual adherence to ART, in individuals who become HIV- networks; this process was then repeated using referrals infected while taking PrEP [4,5], and in those taking from sequential waves of RDS. Direct recruitment was antiretroviral (ARV) drugs for other reasons. Individuals conducted from clinical/hospital referrals, support group can also be infected with drug-resistant HIV [transmitted referrals, alliances with testing programs, study advertise- drug resistance (TDR)]. Some studies have reported ment, and venue-based recruitment. HPTN 078 decreases in acquired drug resistance in high-income screened 1305 MSM for study participation; 902 were countries [6,7], which may reflect increased use of drugs HIV-infected, and 864 had a viral load result from the with high genetic barriers for resistance and increased use screening visit (median age of 46; 79% Black; 82% were of HIV genotyping and viral load monitoring to guide virally suppressed [22]). The study enrolled 144 MSM treatment. However, the frequency of acquired drug who were not virally suppressed (median age 39; 84% resistance remains high in many settings, and TDR has Black [23]). Transgender women were eligible for also increased in some settings [8–10]. participation in HPTN 078 but were not specifically recruited for the study. Approximately two-thirds of new HIV infections in the United States occur in MSM [11]. In 2015, only 62% of In this report, we analyzed samples from all HIV-infected MSM diagnosed with HIV were receiving care, and only individuals who were screened for HPTN 078 and 52% were virally suppressed [12]. Surveillance data have had viral loads at least 1000 copies/ml at study entry. shown that most HIV infections among MSM in the Enrolled individuals included those who were newly United States are linked to infections in other MSM [13], diagnosed, aware of their status but not in care, or in care and phylogenetic studies have found that active but not virally suppressed. Demographic and behavioral transmission clusters are more concentrated among data were collected at the screening visit. MSM than other risk groups [14]. Data on drug resistance among MSM in the United States are limited. Laboratory testing In a study of Black MSM in six cities in the United States HIV diagnostic testing, HIV viral load testing, and CD4þ [HIV Prevention Trials Network (HPTN) 061; enroll- cell count testing were performed at study sites. Other ment 2009–2010], 28% of 169 HIV-infected study testing described below was performed at the HPTN participants had drug resistance; 36% of those with Laboratory Center, Baltimore, Maryland, USA. HIV resistance had ARVdrugs detected, including many who genotyping was performed using the ViroSeq HIV-1 did not report being in care [15]. Resistance to integrase Genotyping System, v.2.0 and the ViroSeq HIV-1 strand transfer inhibitors (INSTIs) was not observed in Integrase Genotyping Kit, RUO (Abbott Molecular, that cohort [16]. Some studies have also reported higher Des Plaines, Illinois, USA) using samples collected at rates of TDR among MSM compared with other risk study entry (screening or enrollment). These methods are groups [8,17,18]. based on population sequencing and generate consensus sequences for HIV protease, HIV reverse transcriptase HPTN 078 evaluated an HIV prevention strategy focused (amino acids 1–335), and HIV integrase. HIV drug on achieving and maintaining viral suppression in HIV- resistance was assessed using the Resistance Calculator infected MSM in the United States (screening/enroll- Program (Frontier Science Foundation, Stanford v8.7 ment: 2016–2017). The study enrolled HIV-infected algorithm); cases were classified as being susceptible individuals who were not virally suppressed at study or having low-level, intermediate-level, or high-level sites in four US cities, including two study sites that resistance to drugs in the four drug-classes analyzed participated in HPTN 061. Many individuals were [protease inhibitors, nonnucleoside reverse transcriptase recruited using respondent-driven sampling (RDS), inhibitors (NNRTIs), nucleotide/nucleoside reverse which has been shown to help identify most-at-risk transcriptase inhibitors (NRTIs), and INSTIs]. This populations, including Black and Hispanic MSM and algorithm includes analysis of resistance to doravirine and MSM with lower socioeconomic status [19–21]. In this bictegravir, which were recently approved for HIV study, we analyzed HIV drug resistance and the treatment by the
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