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HIV-1 Drug Resistance Mutations: Potential Applications for Point-of-Care Genotypic Resistance TestingRunning Title: HIV-1 Drug Resistance MutationsAUTHORSSoo-Yon Rhee1#, Michael R. Jordan2, Elliot Raizes3, Arlene Chua4,5, Neil Parkin6, Rami Kantor7, Gert U. Van Zyl8,9, Irene Mukui10, Mina C. Hosseinipour11, Lisa M. Frenkel12, Nicaise Ndembi13, Raph L. Hamers14, Tobias F. Rinke de Wit14, Carole L. Wallis15, Ravindra K. Gupta16, Joseph Fokam17,18, Clement Zeh19, Jonathan M. Schapiro20, Sergio Carmona21,22, David Katzenstein1, Michele Tang1, Avelin F. Aghokeng23, Tulio De Oliveira24, Annemarie M.J. Wensing25, Joel E. Gallant26, Mark A. Wainberg27, Douglas D. Richman28, 29, Joseph E. Fitzgibbon30, Marco Schito31, Silvia Bertagnolio32, Chunfu Yang3, and Robert W. Shafer1. #Corresponding author: Soo-Yon Rhee, Division of Infectious Diseases, Lane Building, L-134, Stanford University Medical Center, 300 Pasteur Drive, Stanford, CA, 94305; Tel: (650) 736-0911; Fax: (650) 723-3474; Email: syrhee@stanford.eduAFFILIATIONS1Department of Medicine, Stanford University, Stanford, CA, USA; 2Tufts University School of Medicine, Boston, MA, USA; 3Division of Global HIV/AIDS, Centers for Disease Control and Prevention, GA, USA; 4Medecins Sans Frontieres, Access Campaign, Geneva, Switzerland;5Institute of Infectious Diseases and Epidemiology, Tan Tock Seng Hospital, Singapore;6Data First Consulting, Belmont, CA, USA;7Alpert Medical School, Brown University, Providence, RI, USA;8National Health Laboratory Service, Tygerberg, Coastal Branch, South Africa;9Division of Medical Virology, Stellenbosch University, Parow, South Africa;10National AIDS and Sexually Transmitted Infection (STI) Control Programme, Ministry of Health, Nairobi, Kenya;11UNC Project, Lilongwe, Malawi;12University of Washington and Seattle Children’s Research Institute, Seattle, WA, USA;13Institute of Human Virology, Abuja, Nigeria; 14Amsterdam Institute for Global Health and Development (AIGHD), Department of Global Health, Academic Medical Center of the University of Amsterdam, Amsterdam, Netherlands;15Lancet Laboratories and BARC-SA, Johannesburg, South Africa;16Department of Infection, University College London, London, UK;17Chantal BIYA International Reference Centre for Research on HIV/AIDS Prevention and Management, Yaoundé, Cameroon;18Faculty of Medicine and Biomedical Sciences (FMBS) of the University of Yaounde 1, Yaounde, Cameroon;19Division of HIV/AIDS Prevention, CDC, Atlanta, Georgia, USA;20National Hemophilia Center, Tel Hashomer, Israel;21Department of Haematology and Molecular Medicine, University of Witwatersrand, Johannesburg, South Africa;22National Health Laboratory Services, Johannesburg, South Africa;23Virology Laboratory CREMER-IMPM Yaoundé, Cameroon; 24Africa Centre for Health and Population Studies, School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa;25Virology, Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, the Netherlands;26Southwest CARE Center, Santa Fe, NM, USA;27McGill University AIDS Centre, Jewish General Hospital, Montreal, Quebec, Canada;28University of California San Diego, La Jolla, CA, USA;29Veterans Affairs San Diego Healthcare System, San Diego, CA, USA;30Drug Development and Clinical Sciences Branch, Division of AIDS, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA;31HJF-DAIDS, A Division of The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, USA;32WHO, Geneva, Switzerland; INTRODUCTION ……………………………………………………………………………………. 6Anitretroviral Therapy-Na?ve Patients Starting Therapy …………………………………………. 7Patients with VF on an Initial NRTI/NNRTI-Containing Regimen ………………………………. 7Patients with Detectable Viremia on a 1st- or 2nd-Line PI-Containing Regimen …………………. 7HIV-1 DRM Classification …………………………………………………………………… 8Polymorphism Frequency ……………………………………………………………………………. 9 Treatment Prevalence ……………………………………………………………………………….... 9Primacy ……………..………………………………………………………………………………… 10In Vitro Susceptibility………………………………………………………………………………… 10Clinical or Virological Response to ARV Therapy ……………………………….………………... 11DRM Prevalence in Different Clinical Scenarios ……………………………… 12Before Starting Initial ARV Therapy ……………………………………………………………….. 12VF on a 1st-Line NRTI/NNRTI-Containing Regimen ……………….……………………………... 13Persistently Detectable Viremia on a 1st- or 2nd-Line PI-Containing Regimen …………………… 14Proposed DRMs for POC Testing …………………………………………………………. 15Tier 1 RTI DRMs: K103N, V106M, Y181C, G190A (NNRTIs); K65R, M184V (NRTIs) ……….. 15Tier 2 RTI DRMs: Y188L, G190S (NNRTIs); L74V/I, Q151M, M184I, T215Y/F (NRTIs) …….. 16Tier 1 PI DRMs: I47A, L76V, V82A, I84V …………………………………………………………. 16Uncertain Issues and Future Directions ……………………………………………. 17Published Datasets ……………………………………………………………………………………..17Use of a POC Assay to Detect a Limited Number of DRMs ……………………………………….. 17Evolution of ART Strategies …………………………………………………………………………. 18Executive Summary…………………………………………………………………………… 19SummaryThe increasing prevalence of acquired and transmitted HIV-1 drug resistance is an obstacle to successful antiretroviral therapy (ART) in the low- and middle-income countries (LMICs) hardest hit by the HIV-1 pandemic. Genotypic drug resistance testing could facilitate the choice of initial ART in areas with rising transmitted drug resistance (TDR) and enable care-providers to determine which patients with virological failure (VF) on a 1st- or 2nd-line ART regimen require a change in treatment. An inexpensive near point-of-care (POC) genotypic resistance test would be useful in settings where the resources, capacity, and infrastructure to perform standard genotypic drug resistance testing are limited. Such a test would be particularly useful in conjunction with the POC HIV-1 viral load tests that are currently being introduced. A POC genotypic resistance test is likely to involve the use of allele-specific point mutation assays for detecting drug-resistance mutations (DRMs). This document proposes a set of DRMs for POC genotypic resistance testing in LMIC settings and outlines how such an assay could be used to optimize ART. Considering the technical challenges associated with the inclusion of each additional DRM in a point-mutation assay, we organized DRMs into a core group of essential tier 1 DRMs and additional tiers of incremental clinical usefulness. INTRODUCTIONThe global scale-up of antiretroviral therapy (ART) has dramatically reduced HIV-1-associated mortality, mother-to-child HIV-1 transmission, and adult HIV-1 incidence PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DaGk8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxSZWNO

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ADDIN EN.CITE.DATA (1-4). These public health accomplishments are the result of the widespread administration of standardized 1st-line regimens containing two NRTIs plus an NNRTI, followed by a LPV/r-based regimen in those patients who subsequently develop virological failure (VF) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Ib2xtZXM8L0F1dGhvcj48WWVhcj4yMDEwPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (5, 6). However, the margin of long-term ART success is compromised by the development of acquired drug resistance (ADR) and transmitted drug resistance (TDR) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5ISVYvQUlEUyBQcm9ncmFtbWUgV29ybGQgSGVhbHRoIE9y

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ADDIN EN.CITE.DATA (7, 8). Between 10% and 30% of patients receiving a 1st-line NRTI/NNRTI-containing treatment regimen will develop VF at some point during their treatment PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CYXJ0aDwvQXV0aG9yPjxZZWFyPjIwMTA8L1llYXI+PFJl

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ADDIN EN.CITE.DATA (9-11); the majority of these patients are expected to have NRTI- and/or NNRTI-resistant viruses PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5ISVYvQUlEUyBQcm9ncmFtbWUgV29ybGQgSGVhbHRoIE9y

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ADDIN EN.CITE.DATA (7, 11-13). As the number of patients with ADR has increased so has the proportion of newly infected patients with TDR PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5GcmVudHo8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (7, 14, 15, 17, 18). In upper-income countries, genotypic HIV-1 drug resistance testing is used to guide the selection of initial ART and subsequent treatments in patients with VF. However, the resources and capacity to perform standard genotypic resistance testing in the low- and middle-income countries (LMICs) for individual patient management are limited or concentrated in a few central laboratories. A point-of-care (POC) genotypic resistance test would avoid the logistical challenges and delays associated with centralized genotypic resistance testing. Assuming a clinic has the ability to act upon a genotypic resistance test result, such testing may strengthen the provider and patient relationship and support efforts to maximize retention on ART. Even in the context of a public health approach to ART, where few standardized regimens are available, a reliable and inexpensive POC genotypic resistance test would enable HIV-1 care providers to make informed treatment decisions for three categories of patients: (1) ART-na?ve patients starting therapy; (2) patients with VF on an initial NRTI/NNRTI-containing regimen; and (3) patients with persistently detectable viremia on a 1st- or 2nd-line PI-containing regimen. ART-Na?ve Patients Starting TherapyShould population -levels of TDR continue to increase, the inability to predict which patients will respond to an initial NRTI/NNRTI-containing regimen would undermine confidence in the treatability of HIV-1 in LMICs and weaken the HIV care continuum. In regions where surveillance indicates elevated levels of drug resistance in patients beginning ART, pre-therapy POC genotypic resistance testing would identify those patients who should receive standard 1st-line therapy and those who should instead receive a boosted PI-containing regimen. Genotypic resistance testing would likely be particularly useful in the management of the increasing proportion of patients presenting for care for whom the past ART history is uncertain and to ensure that HIV-infected pregnant women with drug-resistant viruses receive the optimal regimen to prevent mother-to-child transmission.Patients with VF on an Initial NRTI/NNRTI-Containing RegimenCoupling genotypic resistance testing with viral load testing would make it possible to determine which patients with VF also have ADR. As the number of patients undergoing POC viral load monitoring increases PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NdXJ0YWdoPC9BdXRob3I+PFllYXI+MjAxNDwvWWVhcj48

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ADDIN EN.CITE.DATA (19, 20), POC genotypic resistance tests will help HIV care providers determine which patients require further adherence support and which patients should switch regimens PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Cb25uZXI8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (15, 21, 22). Patients with Detectable Viremia on a 1st- or 2nd-Line PI-Containing RegimenPIs are the main component of 2nd-line therapy in LMICs. PIs are also recommended as 1st-line therapy in women previously treated with single-dose NVP to prevent mother-to-child transmission and in infants less than three years regardless of their perinatal NVP exposure status PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Mb2NrbWFuPC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48

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ADDIN EN.CITE.DATA (23-27). The absence of genotypic resistance in patients with detectable viremia on a PI-containing regimen is an indication for adherence counseling rather than a treatment change. The presence of genotypic PI resistance in patients with persistently detectable viremia could prompt consideration of a 3rd-line regimen in those regions in which this is an option. HIV-1 DRM ClassificationThe NRTIs, NNRTIs, and PIs are the ARV classes used in most LMICs. Although the integrase inhibitors (INIs) are highly effective, safe, and well tolerated, they have been used primarily in upper-income countries. Should INIs become affordable, they will also play a pivotal role in ART in LMICs ADDIN EN.CITE <EndNote><Cite><Author>Barnhart</Author><Year>2015</Year><RecNum>254</RecNum><DisplayText>(28)</DisplayText><record><rec-number>254</rec-number><foreign-keys><key app="EN" db-id="5v9ezzr5pfz5r7etddmvvf2vwteta9ee9wa9" timestamp="1424377040">254</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Barnhart, M.</author><author>Shelton, J.D.</author></authors></contributors><titles><title>ARVs: The next generation. Going boldly together to new frontiers of HIV treatment</title><secondary-title>Global Health Science and Practice</secondary-title></titles><volume>;(28). All NRTI and NNRTI drug-resistance mutations (DRMs) are in the RT gene but there is practically no cross-resistance between these two drug classes.A DRM can be characterized according to the following five criteria: (1) Polymorphism frequency: its prevalence in virus isolates from ART-na?ve patients in regions with low-levels of TDR; (2) Treatment prevalence: Its prevalence in virus isolates from patients receiving ART. (3) Primacy: its relative prevalence in the presence or absence of other DRMs; (4) In vitro phenotype: its contribution to reduced in vitro susceptibility either alone or in combination with other DRMs; (5) Association with VF: its association with a reduced virological response to an ARV in a new treatment regimen. The Stanford HIV Drug Resistance Database (HIVDB) has an online genotypic resistance interpretation program to help clinicians and laboratories interpret HIV-1 genotypic resistance tests (). The program accepts submitted RT, protease and/or integrase sequences and returns a list of penalty scores for each DRM in the sequence and an estimate of reduced susceptibility for each ARV obtained by adding the penalty scores for each DRM. The DRM penalty scores () are based upon the five criteria described in the previous paragraph and upon the consensus about the clinical significance of a DRM as reflected by experts such as the IAS-USA Drug Resistance Mutations Group PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XZW5zaW5nPC9BdXRob3I+PFllYXI+MjAxNDwvWWVhcj48

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ADDIN EN.CITE.DATA (29). A penalty score of 15 to 29 predicts low-level resistance; a score of 30 to 59 predicts intermediate resistance; and a score of 60 or above predicts high-level resistance. In this document, NRTI and PI DRMs with a score of 30 or more and NNRTI DRMs with a score of 60 or more are referred to as major DRMs. A lower score cut-off is used for the NRTIs and PIs because high-level NRTI and PI resistance usually results from the accumulation of multiple DRMs associated with low-level and intermediate resistance rather than from a single DRM associated with high-level resistance. Tables 1, 2 and 3 contain the HIVDB DRM penalty scores and summarize the polymorphism frequency, treatment prevalence, primacy, and in vitro phenotype of the NRTI, NNRTI and PI DRMs. Polymorphism FrequencyMost DRMs are nonpolymorphic in that they do not occur in the absence of selective drug pressure. Some DRMs, however, are polymorphic and may occur naturally in ARV-na?ve patients. Nonpolymorphic DRMs may reduce susceptibility either alone or in combination with other DRMs; polymorphic DRMs are usually accessory. The fourth column of Tables 1, 2 and 3 indicates the polymorphism rates of the NRTI, NNRTI and PI DRMs. Nonpolymorphic DRMs used for TDR surveillance (surveillance DRMs; SDRMs) are indicated by a check in the SDRM column PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CZW5uZXR0PC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48

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ADDIN EN.CITE.DATA (30). Treatment PrevalenceThe development of a mutation during ARV therapy is Darwinian evidence that the mutation is associated with resistance to the ARV that selected the mutation. Assays that include a sufficient number of common nonpolymorphic DRMs will be specific and sensitive for detecting TDR and ADR. The fifth column of Tables 1, 2 and 3 indicates the prevalence of NRTI, NNRTI and PI DRMs in pooled sequences from NRTI-, NNRTI- and PI-experienced patients in HIVDB.PI DRMs develop much less often in patients receiving a potent ritonavir-boosted PI-containing regimen such as LPV/r, ATV/r, and DRV/r than do NRTI and NNRTI DRMs in patients receiving NRTI/NNRTI-containing regimens PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MbGlicmU8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (31-36). The reduced risk of resistance associated with boosted PIs is likely due to the narrow drug concentration range in which PI levels are both low enough to allow virus replication and high enough to exert selective drug pressure PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Sb3NlbmJsb29tPC9BdXRob3I+PFllYXI+MjAxMjwvWWVh

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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Sb3NlbmJsb29tPC9BdXRob3I+PFllYXI+MjAxMjwvWWVh

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ADDIN EN.CITE.DATA (37). Indeed, most patients without PI DRMs who experience VF while on an initial PI-containing regimen achieve virologic suppression with improved adherence PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5aaGVuZzwvQXV0aG9yPjxZZWFyPjIwMTQ8L1llYXI+PFJl

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ADDIN EN.CITE.DATA (39, 40). Several DRMs preferentially occur in certain HIV-1 subtypes. The NNRTI DRM V106M occurs more often in subtype C viruses from patients treated with NVP or EFV because V106M requires a single base-pair change in subtype C viruses – GTG (V) => ATG (M) – but a two base-pair change in all other subtypes – GTA (V) => ATG (M) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CcmVubmVyPC9BdXRob3I+PFllYXI+MjAwMzwvWWVhcj48

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ADDIN EN.CITE.DATA (44), and subtype A viruses from the former Soviet Union (AFSU) preferentially develop the NNRTI DRM G190S ADDIN EN.CITE <EndNote><Cite><Author>Kolomeets</Author><Year>2014</Year><RecNum>265</RecNum><DisplayText>(45)</DisplayText><record><rec-number>265</rec-number><foreign-keys><key app="EN" db-id="5v9ezzr5pfz5r7etddmvvf2vwteta9ee9wa9" timestamp="1425425306">265</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Kolomeets, A. N.</author><author>Varghese, V.</author><author>Lemey, P.</author><author>Bobkova, M. R.</author><author>Shafer, R. W.</author></authors></contributors><auth-address>aOmsk Research Institute of Natural Focal Infections; Siberian Federal District Center For AIDS Prevention and Fight; Omsk, Russia bDivision of Infectious Diseases, Stanford University, Stanford, California, USA cDepartment of Microbiology and Immunology, REGA Institute KU Leuven, University of Leuven, Leuven, Belgium dIvanovsky Research Institute of Virology, Russian Ministry of Health, Moscow, Russia.</auth-address><titles><title>A uniquely prevalent nonnucleoside reverse transcriptase inhibitor resistance mutation in Russian subtype A HIV-1 viruses</title><secondary-title>AIDS</secondary-title><alt-title>Aids</alt-title></titles><periodical><full-title>AIDS</full-title><abbr-1>AIDS</abbr-1><abbr-2>AIDS</abbr-2></periodical><alt-periodical><full-title>AIDS</full-title><abbr-1>AIDS</abbr-1><abbr-2>AIDS</abbr-2></alt-periodical><pages>F1-8</pages><volume>28</volume><number>17</number><dates><year>2014</year><pub-dates><date>Nov 13</date></pub-dates></dates><isbn>1473-5571 (Electronic)&#xD;0269-9370 (Linking)</isbn><accession-num>25259833</accession-num><urls><related-urls><url>;(45). By a different mechanism, subtype C viruses are predisposed to develop the NRTI DRM K65R ADDIN EN.CITE <EndNote><Cite><Author>Coutsinos</Author><Year>2009</Year><RecNum>151</RecNum><DisplayText>(46)</DisplayText><record><rec-number>151</rec-number><foreign-keys><key app="EN" db-id="5v9ezzr5pfz5r7etddmvvf2vwteta9ee9wa9" timestamp="1399329869">151</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Coutsinos, D.</author><author>Invernizzi, C. F.</author><author>Xu, H.</author><author>Moisi, D.</author><author>Oliveira, M.</author><author>Brenner, B. G.</author><author>Wainberg, M. A.</author></authors></contributors><auth-address>McGill University AIDS Center, McGill University, Lady Davis Institute for Medical Research, Sir Mortimer B. Davis Jewish General Hospital, Montreal, Canada.</auth-address><titles><title>Template usage is responsible for the preferential acquisition of the K65R reverse transcriptase mutation in subtype C variants of human immunodeficiency virus type 1</title><secondary-title>J Virol</secondary-title><alt-title>Journal of virology</alt-title></titles><periodical><full-title>Journal of Virology</full-title><abbr-1>J. Virol.</abbr-1><abbr-2>J Virol</abbr-2></periodical><alt-periodical><full-title>Journal of Virology</full-title><abbr-1>J. Virol.</abbr-1><abbr-2>J Virol</abbr-2></alt-periodical><pages>2029-33</pages><volume>83</volume><number>4</number><keywords><keyword>Amino Acid Substitution/genetics</keyword><keyword>DNA, Viral/*biosynthesis</keyword><keyword>HIV Reverse Transcriptase/*genetics/*metabolism</keyword><keyword>HIV-1/*genetics</keyword><keyword>Humans</keyword><keyword>*Mutation, Missense</keyword><keyword>*Templates, Genetic</keyword></keywords><dates><year>2009</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>1098-5514 (Electronic)&#xD;0022-538X (Linking)</isbn><accession-num>19073730</accession-num><urls><related-urls><url>;(46). PrimacyHIV-1 strains from patients with VF often contain more than one DRM associated with resistance to an ARV they are receiving. Usually, the first or primary DRM reduces ARV susceptibility and subsequent DRMs either reduce susceptibility or compensate for reduced fitness associated with the primary DRM ADDIN EN.CITE <EndNote><Cite><Author>Rhee</Author><Year>2007</Year><RecNum>102</RecNum><DisplayText>(47)</DisplayText><record><rec-number>102</rec-number><foreign-keys><key app="EN" db-id="5v9ezzr5pfz5r7etddmvvf2vwteta9ee9wa9" timestamp="1393973921">102</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rhee, S. Y.</author><author>Liu, T. F.</author><author>Holmes, S. P.</author><author>Shafer, R. W.</author></authors></contributors><auth-address>Division of Infectious Diseases, Department of Medicine, Stanford University, Stanford, California, United States of America.</auth-address><titles><title>HIV-1 subtype B protease and reverse transcriptase amino acid covariation</title><secondary-title>PLoS Comput Biol</secondary-title><alt-title>PLoS computational biology</alt-title></titles><periodical><full-title>PLoS Computational Biology</full-title><abbr-1>PLoS Comput. Biol.</abbr-1><abbr-2>PLoS Comput Biol</abbr-2></periodical><alt-periodical><full-title>PLoS Computational Biology</full-title><abbr-1>PLoS Comput. Biol.</abbr-1><abbr-2>PLoS Comput Biol</abbr-2></alt-periodical><pages>e87</pages><volume>3</volume><number>5</number><edition>2007/05/16</edition><keywords><keyword>Amino Acid Substitution</keyword><keyword>Chromosome Mapping/*methods</keyword><keyword>Genetic Variation/genetics</keyword><keyword>HIV Protease/*chemistry/*genetics</keyword><keyword>HIV Reverse Transcriptase/*chemistry/*genetics</keyword><keyword>HIV-1/*enzymology/*genetics</keyword><keyword>Linkage Disequilibrium/genetics</keyword></keywords><dates><year>2007</year><pub-dates><date>May</date></pub-dates></dates><isbn>1553-7358 (Electronic)&#xD;1553-734X (Linking)</isbn><accession-num>17500586</accession-num><work-type>Research Support, N.I.H., Extramural</work-type><urls><related-urls><url>;(47). The order in which DRMs develop depends on the ART regimen. For example, M184V causes high-level lamivudine (3TC)- and emtricitabine (FTC) resistance and develops rapidly in patients with VF while receiving one of these NRTIs. K65R, L74V and T215Y are primary DRMs associated with reduced susceptibility to ARVs other than 3TC or FTC. These DRMs usually follow M184V because 3TC and FTC are essential components of most NRTI-containing regimens. The sixth column of Tables 1, 2 and 3 indicates the prevalence with which each DRM occurs in the absence of other major DRMs.In Vitro SusceptibilityThe clinical significance of reductions in in vitro susceptibility often varies among ARVs belonging to the same or different ARV classes. For example, the dynamic susceptibility range between wild type and the most NRTI-resistant viruses can be as low as 5-fold for tenofovir (TDF) and abacavir (ABC) but above 200-fold for zidovudine (AZT), 3TC and FTC PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XaGl0Y29tYjwvQXV0aG9yPjxZZWFyPjIwMDM8L1llYXI+

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PjwvRW5kTm90ZT5=

ADDIN EN.CITE.DATA (48-50). Similar but less pronounced dynamic susceptibility range differences exist in the NNRTI, PI and INI classes PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5SaGVlPC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (51-53). The difference in ARV susceptibility between a wild type laboratory clone and one containing a DRM yields an unbiased assessment of that DRM’s phenotypic effect. However, the number of DRMs studied with the same susceptibility assay is limited. The contribution of a DRM to reduced ARV susceptibility can also be studied in clinical isolates using regression analyses in which the presence or absence of a DRM is an explanatory variable and the fold reduction in susceptibility is the outcome variable. The regression coefficients obtained from these models indicate the relative contribution of a DRM to reduced ARV susceptibility while attempting to control for the other DRMs in a virus sequence. Columns 7 to 10 in Tables 1, 2 and 3 indicate the estimated fold reduction in susceptibility to the NRTIs 3TC, ABC, AZT and TDF; the NNRTIs nevirapine (NVP), efavirenz (EFV), etravirine (ETR) and rilpivirine (RPV); and the PIs ATV, darunavir (DRV) and LPV. For the same virus, FTC susceptibility levels are highly similar to 3TC susceptibility levels. The estimates in these tables were derived using regression models similar to those recently described PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5SaGVlPC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (49, 51, 52). The dataset used in these regression models can be downloaded from . Clinical or Virological Response to ARV TherapyIn some regions, genotypic resistance tests are routinely performed prior to treatment to guide initial ARV therapy choices. This makes it difficult to examine the effect of a pre-existing DRM on the response to an initial ARV regimen. To do so, it is necessary to rely on the few studies in which HIV-1 was sequenced from cryopreserved blood samples obtained prior to the initiation of therapy from patients for whom genotypic resistance testing was not used to guide initial treatment decisions PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5LdXJpdHprZXM8L0F1dGhvcj48WWVhcj4yMDA4PC9ZZWFy

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dGU+AG==

ADDIN EN.CITE.DATA (54-59). These studies suggest that pre-therapy DRMs pose a higher risk to the success of 1st-line NRTI/NNRTI-containing regimens than to boosted PI-containing regimens. This conclusion is supported by additional studies in which ARV therapy was selected on the basis of standard genotypic resistance testing but was followed by assays for low-abundant variants not detectable by standard dideoxy-terminator Sanger sequencing PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Db292YWRpYTwvQXV0aG9yPjxZZWFyPjIwMDk8L1llYXI+

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ZD48L0NpdGU+PC9FbmROb3RlPn==

ADDIN EN.CITE.DATA (69)-containing regimen; NNRTI DRMs on the response to an etravirine (ETR)-containing regimen PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5WaW5nZXJob2V0czwvQXV0aG9yPjxZZWFyPjIwMTA8L1ll

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ZE5vdGU+AG==

ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5WaW5nZXJob2V0czwvQXV0aG9yPjxZZWFyPjIwMTA8L1ll

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ZE5vdGU+AG==

ADDIN EN.CITE.DATA (70); and INI DRMs on the response to a dolutegravir (DTG)-containing regimen PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Fcm9uPC9BdXRob3I+PFllYXI+MjAxMzwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (7, 14, 15). Table 4 shows the absolute and cumulative prevalence of the major NRTI and NNRTI DRMs in RT sequences from a recently published individual patient-level meta-analysis of more than 50,000 ARV-na?ve patients in 287 published studies PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5SaGVlPC9BdXRob3I+PFllYXI+MjAxNTwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (16). In the NRTI class, M184V was the most common transmitted major DRM, accounting for more than 50% of viruses with one or more major DRMs regardless of region or subtype. M184I, K65R, L74V/I, Y115F and the TAMs K70R and T215Y/F were the next most common transmitted major NRTI DRMs. The TAMs M41L, D67N/E/G and K219Q/E/N/R and the T215 revertant mutations were the most common non-major transmitted NRTI DRMs. K103N, Y181C and G190A were the three most common NNRTI DRMs in all regions and subtypes, occurring in more than 80% of viruses with a major NNRTI DRM. V106M was the fourth most common NNRTI DRM in subtype C viruses. V106A, Y188L and G190S accounted for most of the remaining transmitted major NNRTI DRMs. A98G and K101E were the most common non-major transmitted NNRTI DRMs.VF on a 1st-Line NRTI/NNRTI-Containing RegimenTo identify sensitive and specific indicators of ADR in patients with VF on a 1st-line NRTI/NNRTI regimen, we analyzed published RT sequences from 4,926 patients with VF while receiving the most commonly used 1st-line therapy regimens in LMICs. Table S1 summarizes the number of patients according to 1st-line regimen and HIV-1 subtype. Fifty-five percent, 27%, 16% and 2% received a d4T-, AZT-, TDF- or ABC-containing regimen, respectively. Fifty-four percent received EFV and 46% received NVP. The most common subtypes were C (46%), circulating recombinant form (CRF) 01_AE (15%), B (11%), A (8%), G (8%) and CRF02_AG (7%). Seventy-three percent of patients had one or more major NRTI DRMs and one or more major NNRTI DRMs. Nine percent had a major NNRTI DRM but no major NRTI DRM; 2% percent had a major NRTI DRM but no major NNRTI DRM; and 16% had no major NRTI or NNRTI DRM. Table 5 shows that in viruses with one or more major NRTI DRM the most common were M184V (91%) and M184I (4.3%), K65R (11%), and the TAMs K70R (14%), T215Y (10%) and T215F (8.6%). About one-half of the viruses with K65R did not have M184V, making K65R the second largest contributor to the cumulative proportion of viruses with a major NRTI DRM. K65R also occurred in 48% of 467 patients with VF on a 1st-line TDF-containing regimen (Table S2). The TAMs nearly always occurred in combination with M184V and contributed less to the cumulative proportion of viruses with a major NRTI DRM than did K65R. In patients with VF on a 3TC- or FTC-containing regimen, M184I often emerges before M184V. However, M184V outcompetes M184I within several weeks in most patients PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5LZXVsZW48L0F1dGhvcj48WWVhcj4xOTk2PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (73, 74). The spectrum of DRMs in 712 children was similar to adults with the exception that L74V/I occurred more often in children because a higher proportion of children received an ABC-containing regimen (Tables S3 and S4). Indeed, among both adults and children receiving ABC, L74V/I were the second most common major NRTI DRMs after M184V PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5WYW4gWnlsPC9BdXRob3I+PFllYXI+MjAxMzwvWWVhcj48

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ADDIN EN.CITE.DATA (34, 75), although L74V/I rarely occurred in the absence of M184V.Table 5 shows that the most common NNRTI DRMs in viruses from the 3,899 patients with one or more major NNRTI DRMs were K103N (49%), Y181C (26%), G190A (20%) and V106M (17%). One or more of these four DRMs occurred in 89% of viruses with a major NNRTI DRM. V106M was the second-most common NNRTI DRM in subtype C viruses, occurring in 33% of patients with a major NNRTI DRM. The six next-most common NNRTI DRMs – V106A, Y181I/V, Y188L, and G190S/E – accounted for an additional 10% of viruses with one or more major NNRTI DRM. Persistently Detectable Viremia on a 1st- or 2nd-Line PI-Containing RegimenTable 6 shows the most common major LPV-associated DRMs in published protease sequences from 1,214 previously PI-na?ve patients with VF on an LPV/r-containing regimen. Of these 1,214 patients, 203 (17%) had viruses with predicted intermediate or high-level LPV resistance. The most common major PI DRMs were V82A, I76V, I84V and L47A. One or more of these four DRMs occurred in 88% of viruses with intermediate or high-level LPV/r resistance. The next two most common major LPV DRMs – I50V and V82F – accounted for an additional 4% of viruses with predicted intermediate or high-level LPV resistance. The remaining 8% of viruses with predicted intermediate or high-level LPV resistance had a combination of two or more PI DRMs with lower mutation scores, including V32I, M46I, I54M/L/V, I47V, V82S/T/M and L90M. The most common subtypes of these 203 viruses were C (49%), CRF01_AE (14%), CRF01_AG (12%), B (8%), G (7%) and A (5%). Overall 170 (84%) of the 203 LPV-resistant viruses had predicted intermediate or high-level cross-resistance to ATV/r; 36 (18%) had predicted intermediate or high-level cross-resistance to DRV/r. Few protease sequences are available from PI-na?ve patients with VF on ATV/r- or DRV/r-containing regimens. Published reports of aggregated data indicate that I50L and N88S are the main DRMs developing in PI-na?ve patients with VF on an ATV- or ATV/r-containing regimen PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NYWxhbjwvQXV0aG9yPjxZZWFyPjIwMTA8L1llYXI+PFJl

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ADDIN EN.CITE.DATA (32, 76, 77). These DRMs do not confer cross-resistance to LPV or DRV PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5SaGVlPC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (51). In fact, I50L is associated with increased susceptibility to LPV, DRV and other PIs PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XZWluaGVpbWVyPC9BdXRob3I+PFllYXI+MjAwNTwvWWVh

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ADDIN EN.CITE.DATA (78).Proposed DRMs for POC TestingRTI DRMs can be used to identify TDR in ART-na?ve patients starting ART, and ADR in patients receiving a 1st-line NRTI/NNRTI-containing regimen. PI DRMs can be used to identify acquired PI resistance in patients receiving a 1st- or 2nd-line PI-containing regimen. The proposed RTI DRMs should be particularly sensitive at detecting ADR on a 1st-line NRTI/NNRT-containing regimen because a false-negative test result in such patients could delay an appropriate treatment change. In contrast, failure to detect TDR would result in a patient receiving the standard-of-care, though possibly suboptimal, 1st-line regimen. For both RT and protease, different mutations at the same amino acid position (e.g., M184V and M184I) are treated as separate DRMs despite the fact that some POC assays may be able to detect more than one DRM at the same position.Tier 1 RTI DRMs: K103N, V106M, Y181C and G190A (NNRTIs); K65R and M184V (NRTIs)Proposed tier 1 DRMs include the four NNRTI and two NRTI DRMs with the highest cumulative sensitivity for detecting ADR on a 1st-line NRTI/NNRTI-containing regimen (Table 7). This set of six DRMs was 99% sensitive for detecting ADR on a 1st-line NRTI/NNRTI regimen and 82% sensitive for detecting TDR in ART-na?ve patients. No significant differences in sensitivity were observed for the subset of LMIC patients with ADR or TDR, the subset of children with ADR on a 1st-line NRTI/NNRTI-containing regimen, or the subset of adult patients with ADR on a 1st-line TDF-containing regimen. In an ART-na?ve patient, the presence of each of the tier 1 DRMs except K65R may be considered an indication for starting an initial PI-containing regimen or closer virological monitoring based on cost-effectiveness or country policy. The presence of K65R would be an indication for using an AZT/3TC nucleoside backbone.In patients with VF on a 1st-line NRTI/NNRTI-containing regimen, the presence of a Tier 1 DRM indicates that the regimen has reduced antiviral activity. Although the presence of a DRM in patients with VF on a 1st-line NRTI/NNRTI regimen does not preclude a virological response to continued therapy with improved adherence PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Ib2ZmbWFubjwvQXV0aG9yPjxZZWFyPjIwMDk8L1llYXI+

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ADDIN EN.CITE.DATA (79-81), continued therapy is expected to result in a higher rate of immunological and clinical deterioration than would occur if the patient is switched to a 2nd-line PI-based therapy.Tier 2 RTI DRMs: Y188L and G190S (NNRTIs); L74V/I, Q151M, M184I, and T215Y/F (NRTIs) Y188L and G190S were the most common major non-tier 1 NNRTI DRMs associated with ADR on a 1st-line NRTI/NNRTI-containing regimen and among the most common non-tier 1 NNRTI DRMs associated with TDR. L74V/I, Q151M, M184I, and T215Y/F were among the most common major non-tier 1 DRMs associated with ADR on a 1st-line NRTI/NNRTI-containing regimen and pared to an assay that just detected tier 1 RTI DRMs, an assay that detected both tier 1 and 2 RTI DRMs would have increased the sensitivity for detecting a major NRTI or NNRTI DRMs from 82% to 91% in patients with TDR. Such an assay would also have increased sensitivity for detecting both a major NRTI and a major NNRTI-associated DRM from 85% to 95% in the 3,475 patients with dual-class ADR on a 1st-line NRTI/NNRTI-containing regimen. However, an assay with tier 1 and 2 RTI DRMs would only marginally increase the sensitivity for detecting at least one major NRTI or NNRTI DRM in patients with ADR on a 1st-line NRTI/NNRTI-containing regimen from 98% to 99%. Additional NNRTI DRMs that may eventually have a role in a POC genotypic test include L100I, K101P, Y181I/V and G190E – DRMs associated with high-level ETR and RPV resistance PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5WaW5nZXJob2V0czwvQXV0aG9yPjxZZWFyPjIwMTA8L1ll

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ADDIN EN.CITE.DATA (29, 52, 70). Additional NRTI DRMs that may eventually have a role in a POC genotypic resistance test include K65N, K70E/G and Y115 – DRMs associated with reductions in ABC and TDF susceptibility PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Sb3NzPC9BdXRob3I+PFllYXI+MjAwNjwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (34, 49, 82-84).Tier 1 PI DRMs: I47A, L76V, V82A and I84VPatients with VF on an LPV/r-containing regimen who have one or more of these DRMs have evidence for reduced LPV susceptibility. The sensitivity of a POC assay for detecting intermediate or high-level LPV resistance could be increased from 88% to 98%, if it also included the DRMs M46I and I54V. A test with these six mutations would require additional interpretation because, when they occur alone, M46I or I54V confer only low-level LPV resistance. The PI DRMs – I50L and N88S – are likely to be useful in regions where ATV/r is the most commonly used initial PI PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Nb2xsYW48L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (32, 76, 77). Uncertain Issues and Future DirectionsThere are several areas of uncertainty with the analyses and recommendations in this document including whether the analyzed datasets were sufficiently representative to identify the most common major DRMs associated with TDR and ADR, whether a POC assay for a limited number of DRMs can be a useful replacement for standard sequencing, and how changes in ARV-treatment strategies would influence the choice of POC DRMs. Published DatasetsThe sequences used to identify the most common major NRTI and NNRTI DRMs associated with TDR were obtained from a recently published meta-analysis of 287 studies including 151 studies from Sub-Saharan Africa and the LMICs of South/Southeast Asia PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5SaGVlPC9BdXRob3I+PFllYXI+MjAxNTwvWWVhcj48UmVj

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ADDIN EN.CITE.DATA (16). The predominance of four of the tier 1 DRMs in all regions and subtypes suggests that these DRMs are robust indicators of TDR. Of the 3,282 LMIC patients with ADR with a major NRTI or NNRTI DRM, only 291 (9%) were receiving a TDF-containing regimen. Additionally, most of the virus sequences in LMICs were from patients whose virus levels were not being monitored and who may therefore have had prolonged VF. As routine virus load monitoring is introduced in more regions, VF will likely be associated with fewer DRMs. Ongoing surveillance remains necessary to track the most common NRTI and NNRTI DRMs that will arise in the increasing number of patients receiving a TDF-containing 1st-line regimen and/or undergoing virological monitoring. Use of a POC Assay to Detect a Limited Number of DRMsAlthough many allele-specific point mutation assays for HIV-1 drug resistance have been developed for research purposes, only a few have been developed and studied for their reliability and applicability in routine patient management PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5aaGFuZzwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+PFJl

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ADDIN EN.CITE.DATA (87-91). One of the promises of POC HIV-1 drug resistance testing is that it is expected to be less expensive than standard genotypic resistance testing using DNA sequencing. However, developing a POC test will require surmounting technical and regulatory hurdles. Therefore, an economic analysis relevant to the costs of developing such an assay would need to consider its use over the range of potential clinical applications, including the selection of the most efficacious ART regimens for patients with TDR and for patients with 1st- and 2nd-line ADR. Evolution of ART StrategiesThe usefulness of a POC genotypic resistance test will depend on regional treatment options. The extent to which ATV/r will be used for 2nd-line therapy and the potential availability of DRV/r and the INIs are key areas of uncertainty. In contrast to LPV/r, ATV/r has not been studied for treating patients with VF on a 1st-line NRTI/NNRTI regimen. Although LPV/r and ATV/r-containing regimens are equally efficacious for initial ART PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Nb2xpbmE8L0F1dGhvcj48WWVhcj4yMDA4PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA (92, 93), ATV/r-containing regimens may be less efficacious for second-line therapy. ATV/r has a lower genetic barrier to resistance than LPV/r and ATV/r monotherapy has consistently been less effective than LPV/r for regimen simplification PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5LYXJsc3Ryb208L0F1dGhvcj48WWVhcj4yMDA3PC9ZZWFy

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Tm90ZT4A

ADDIN EN.CITE.DATA (94-96). These data suggest that ATV/r may be less effective than LPV/r in treating patients with NRTI resistance. Therefore, the extent of NRTI resistance following initial therapy will likely have greater implications for the use of ATV/r-containing than for LPV/r-containing 2nd-line regimens.However, if ATV/r-containing 2nd-line regimens prove effective, their use would have favorable implications for both POC testing and 3rd-line treatment. I50L and N88S are the most commonly occurring major DRMs in PI-na?ve patients receiving ATV/r. Identifying clinically relevant ATV resistance would therefore be simpler than identifying the more complex patterns of DRMs associated with LPV resistance. In addition, most patients with VF on a 2nd-line ATV/r-containing regimen are expected to have viruses that are fully susceptible to LPV and DRV making it possible to create a highly effective 3rd-line regimen using these PIs.Although the NNRTI rilpivirine (RPV) has recently been approved in upper-income countries for use in a fixed-dose combination with TDF and FTC, further studies would be necessary before it could be considered a standard first-line treatment option in LMICs. In particular, RPV is approved only for patients with plasma HIV-1 RNA levels below 100,000 copies/ml whose viruses do not have the RT mutation E138A – a mutation, which occurs in about 5% of viruses belonging to subtypes A and C PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TbHVpcy1DcmVtZXI8L0F1dGhvcj48WWVhcj4yMDE0PC9Z

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ADDIN EN.CITE.DATA (97).It is difficult to predict how the introduction of INIs will influence the development of POC genotypic resistance testing strategies because such strategies depend on which INIs will be introduced and on whether they will be used for 1st-, 2nd- or 3rd-line therapy. However, if INIs will be used beyond the first line of therapy and in combination with NRTIs, it may become important to identify the NRTI DRMs most likely to increase the risk of VF on an NRTI/INI-containing regimen. Executive SummaryThe increasing prevalence of acquired and transmitted HIV-1 drug resistance is an obstacle to successful antiretroviral therapy (ART) in the low- and middle-income countries (LMICs) hardest hit by the HIV-1 pandemic. Genotypic drug resistance testing could facilitate the choice of initial ART in areas with rising transmitted drug resistance (TDR) and enable care-providers to determine which patients with virological failure (VF) on a 1st- or 2nd-line ART regimen require a change in treatment. An inexpensive near point-of-care (POC) genotypic resistance test would be useful in settings where the resources, capacity, and infrastructure to perform standard genotypic drug resistance testing are limited. Such a test would be particularly useful in conjunction with the POC HIV-1 viral load tests that are currently being introduced. A POC genotypic resistance test is likely to involve the use of allele-specific point mutation assays for detecting drug-resistance mutations (DRMs). The inclusion of a DRM in a POC assay should be based on its sensitivity and specificity for identifying drug-resistant HIV-1 strains and its relevance to the success of ART. This document proposes a set of DRMs for POC genotypic resistance testing in LMIC settings and outlines how such an assay could be used to optimize ART. Considering the technical challenges associated with the inclusion of each additional DRM in a point-mutation assay, we organized DRMs into a core group of essential tier 1 DRMs and additional tiers of incremental clinical usefulness. Nucleoside reverse transcriptase (RT) inhibitor (NRTI), nonnucleoside RT inhibitor (NNRTI), and protease inhibitor (PI)-associated DRMs were selected for inclusion based on their scores in the Stanford HIV Drug Resistance Database (HIVDB) genotypic resistance interpretation system and their prevalence in ART-na?ve patients with TDR and ART-experienced patients with ADR. To identify the most common transmitted DRMs, we analyzed HIV-1 RT sequences described in a recent meta-analysis of 287 studies with more than 50,000 adult ART-na?ve patients. To identify the most commonly acquired NRTI- and NNRTI-associated DRMs, we analyzed published HIV-1 RT sequences from nearly 5,000 adult and children with VF on a standard 1st-line NRTI/NNRTI-containing ART regimen. To identify the most common ritonavir-boosted lopinavir (LPV/r)-associated DRMs, we analyzed protease sequences from 1,214 previously PI-na?ve patients with VF on an LPV/r-containing regimen.One or more members of a set of six tier 1 RT DRMs – two major NRTI-associated DRMs (M184V and K65R) and four major NNRTI-associated DRMs (K103N, Y181C, G190A, and V106M) – were present in 82% of analyzed virus sequences from ART-na?ve patients with TDR and 98% of analyzed virus sequences from patients with ADR on a 1st-line NRTI/NNRTI-containing regimen. The detection of one or more of these six RT DRMs in an ART-na?ve patient or in a patient with VF on a 1st-line NRTI/NNRTI-containing regimen may be considered an indication for a PI-containing regimen or closer virological monitoring based on cost-effectiveness or country policy. The six tier 1 RT DRMs were also highly sensitive for detecting ADR in the subsets of children receiving a 1st-line NRTI/NNRTI regimen and adults receiving a 1st-line TDF-containing NRTI/NNRTI regimen.A set of Tier 2 RTI DRMs including the NNRTI DRMs Y188L and G190S and the NRTI DRMs L74V/I, Q151M, M184I, and T215F/Y increased the sensitivity for detecting TDR from 82% to 92% and for detecting dual class NRTI/NNRTI resistance in patients with VF on a 1st-line NRTI/NNRTI-containing regimen from 85% to 95%. However, considering the limited number of treatment options in many LMICs and the technical challenges associated with the inclusion of each additional DRM in a point mutation assay, the inclusion of the Tier 2 mutations in a POC assay is currently not a high priority. Our analysis indicated that a set of four PI DRMs – I47A, L76V, V82A, and I84V – was 88% sensitive for detecting intermediate and high-level LPV resistance in patients receiving a 1st- or 2nd-line LPV/r-containing regimen. In published studies, the PI DRMs I50L and N88S are likely to be the most sensitive DRMs for detecting intermediate and high-level ATV resistance in patients receiving a 1st- or 2nd-line ATV/r-containing regimen. The inclusion of PI DRMs in a POC genotypic resistance test is likely to be useful primarily in settings in which third-line ART regimens are available.Acknowledgment: RWS and SYR were supported in part by a grant from the Bill and Melinda Gates Foundation and from the NIH (AI068581). NP was supported by a grant from the Bill and Melinda Gates Foundation.Table 1. Prevalence of Nucleoside RT Inhibitor (NRTI) Drug-Resistance Mutations (DRMs) in Antiretroviral (ARV)-Na?ve and -Treated Patients and Their Estimated Contributions to Reduced NRTI SusceptibilityDRMHIVDBScoreaSDRMbPrevalence (%)c% Without Other Major DRMsdPhenotypic Fold ResistanceeARV-Na?ve(n=54,728)ARV-Treated(n=25,424)3TC(n=1361)ABC(n=1267)AZT(n=1373)TDF(n=1081)M184V60?0.25235>5030.30.5K65R60?0.04430530.82Q151M60?0391.7451.1M184I60?0.03228>501.70.30.6T215Y45?0.0228211.51.861.4T215F45?0.011071.51.781.6Y115F45?0.01211.4341.7T69i45?01335184K70R30?0.0718121.31.351.7L74V30?0.019611.50.30.6L74I30?0.02420.81.20.80.8D67d3000.090NANANANAM41L15?0.33021.11.121.5D67N15?0.042811.21.221.2L210W15?0.061921.21.441.6T215I15?0.03161.81.551.6T215S15?0.30.9130.80.80.30.7T215C15?0.090.8200.911.20.8T215D15?0.30.6451.30.80.30.6T215V15?0.010.641.111.71K70E15?0.020.6721.10.21K70G1500.441.41.20.31.1T69d1500.22NANANANAT215E15?0.10.23921.11.21.3K65N150.030.120NANANANAK219Q10?0.091121.110.91T69D10?0.03631.110.80.9K219E10?0.036210.90.40.8V75M10?0.03310.91.31.41.1K219N10?0.04331.21.11.1-1K219R10?0.07321.81.631.5D67G10?0.05251.11.121.2F116Y10?0.01201.1131.2F77L10?0.12210.941.4V75T10?0161.81.60.80.9D67E10?0.010.611.21.511.5K70T100.030.380.10.931.8K70N100.030.3611.31.61.4K70Q100.020.23NANANANAK65E100.030.122NANANANAA62V50.9430.91.01.21.2V75I50.04341.51.11.80.9aHIVDB Score: Highest penalty score according to the Stanford HIV Drug Resistance Database (HIVDB) genotypic resistance interpretation program (version 7.0) for lamivudine (3TC), abacavir (ABC), zidovudine (AZT), and tenofovir (TDF). Scores of 15 to 29, 30 to 59, and ≥60 indicate low, intermediate, and high-level resistance. Emtricitabine (FTC) and 3TC scores are identical. bSurveillance Drug Resistance Mutation (SDRM): In ARV-na?ve patients, these DRMs are indicators of transmitted drug resistance (TDR) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CZW5uZXR0PC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48

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ADDIN EN.CITE.DATA (30). cDRM prevalence in samples from patients with known ARV treatment history in HIVDB. The ARV-Na?ve category excludes viruses with ≥2 SDRMs considered to be consistent with TDR rather than natural variation. dProportion of patient samples having the DRM and no other major NRTI DRM (score ≥30) / all patient samples with the DRM. eEstimated contribution to fold-reduced susceptibility based on linear regression analysis of PhenoSense susceptibility test results PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5QZXRyb3BvdWxvczwvQXV0aG9yPjxZZWFyPjIwMDA8L1ll

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ADDIN EN.CITE.DATA (50) (). ‘NA’: fewer than three phenotypes with the DRM. Fold-resistance levels in bold (≥1.5 for ABC and 3TC, ≥2 for AZT, and ≥3 for 3TC) indicate a statistically and probable clinically significant increase above 1.0 compared with wildtype. Table 2. Prevalence of Non-Nucleoside RT Inhibitor (NNRTI) Drug-Resistance Mutations (DRMs) in Antiretroviral (ARV)-Na?ve and -Treated Patients and Their Estimated Contributions to Reduced NNRTI SusceptibilityDRMHIVDBScoreaSDRMbPrevalence (%)cWithout / With other Major DRMsdPhenotypic Fold ResistanceeARV-Na?ve(n=54,728)ARV-Treated(n=25,424)NVP(n=1694)EFV(n=1687)ETR(n=484)RPV(n=183)K103N60?1.0363724211.32Y181C60?0.1202916283G190A60?0.2151211110.91.3V106M60?0.0151518320.6NAL100I60?0.014131467Y188L60?0.04455>50>50310G190S60?0.0132635>500.9NAM230L60?0.02256745V106A60?0.01213>5070.4NAK103S60?0.04251171.51.7K101P60?015182522>50Y188C60?0.010.919>5035NANAY181I60?0.010.949>501.43024Y181V60?00.656>502>50NAG190E60?0.020.567>50>50>5027Y188H60?0.030.5759NANAG190Q6000.370>50>50NANAK101E30?0.284231.52A98G300.2613221.43P225H30?0.0242231.2NAF227L300.04351.422NAK238T300.0423321.4NAY318F300.124NANANANAE138K300.10.418-0.6121.6F227C3000.0413NANANANAN348I150.091417NANANANAV108I150.5952310.9E138A1533321.51.621.8K101H15013331.31E138Q150.03131.41NANAE138G150.30.71821.431.7V179F15?00.300.9330.4V179D1023183531.8aHIVDB Score: The highest mutation penalty score according to the Stanford HIV Drug Resistance Database (HIVDB) genotypic resistance interpretation program (version 7.0) for nevirapine (NVP), efavirenz (EFV), etravirine (ETR), and rilpivirine (RPV). Total scores of 15 to 29, 30 to 59, and ≥60 indicates low-level, intermediate, and high-level resistance. bSurveillance Drug Resistance Mutation (SDRM): When present in ARV-na?ve patients, these DRMs are considered specific indicators of transmitted drug resistance (TDR) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CZW5uZXR0PC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48

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ADDIN EN.CITE.DATA (50) (). ‘NA’: fewer than three phenotypes with the DRM. Fold-resistance levels in bold (≥2 for NVP, EFV, and NVP and ≥3 for ETR) indicate a statistically and probable clinically significant increase above 1.0 compared with wildtype. Table 3. Prevalence of Protease Inhibitor (PI) Drug-Resistance Mutations (DRMs) PI-Na?ve and -Treated Patients and Their Estimated Contributions to Reduced PI SusceptibilityDRMHIVDBScoreaSDRMbPrevalence (%)cWithout / With other Major DRMsdPhenotypic Fold ResistanceePI-Na?ve(n=60,537)PI-Treated(n=13,660)ATV(n=1100)DRV(n=590)LPV(n=1389)I84V60?0.02157433N88S60?0.0327070.91.1I47A60?00.580.9243I50L60?0.010.54860.40.3I84A60?00.25447NA6I84C60?00.2645NA1.9V82A30?0.0424271.50.83G48V30?04340.82L76V30?0.01490.424I50V30?0.022110.944V82F30?0222247G48M30?00.5021.11.8L90M25?0.3332331.21.9V82T25?031820.63V82S25?01254NA6V82M25?00.32211.20.9I54L20?0.0134231.9I54M20?033253I54V15?027131.44M46I15?0.32331.21.21.6V32I15?0.0152331.3I47V15?0.0350.60.91.34I54A15?010.512NA11I54T15?0.010.92969I54S15?00.7210211M46L10?0.31041.51.31.6G73S10?0.039321.21.5D30N10?0.026283-0.91.1L24I10?0.0263211.8F53L10?0.04611.71.11.3K20T100.15721.11.9G73T10?03121.61.5T74P100.042621.51.4G73C10?010.61.71.11.6N83D10?0.020.81230.91.3V82C10?00.641.31.33V82L10?0.020.33021.51.2L33F50.41321.221.8L10F50.21031.41.52L89V50.06441.231.4aHIVDB Score: The highest mutation penalty score according to the Stanford HIV Drug Resistance Database (HIVDB) genotypic resistance interpretation program (version 7.0) for atazanavir (ATV), darunavir (DRV), and lopinavir (LPV). Total scores of 15 to 29, 30 to 59, and ≥60 indicates low-level, intermediate, and high-level resistance. bSurveillance Drug Resistance Mutation (SDRM): When present in ARV-na?ve patients, these DRMs are considered specific indicators of transmitted drug resistance (TDR) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5CZW5uZXR0PC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48

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ADDIN EN.CITE.DATA (30). cPrevalence of DRM in samples from patients with known ARV treatment history in HIVDB. The ARV-Na?ve category excludes viruses containing ≥2 SDRMs as these were considered to be consistent with TDR rather than natural variation. dProportion of patient samples having the DRM and no other major NNRTI DRM (score ≥30) / all patient samples with the DRM. eEstimated contribution to fold-reduced susceptibility based on linear regression analysis of PhenoSense susceptibility test results PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5QZXRyb3BvdWxvczwvQXV0aG9yPjxZZWFyPjIwMDA8L1ll

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ADDIN EN.CITE.DATA (50) (). ‘NA’: fewer than three phenotypes with the DRM. Fold-resistance levels in bold (≥2 for ATV and ≥3 for LPV and DRV) indicate a statistically and probable clinically significant increase compared with wildtype.Table 4. Absolute and Cumulative Prevalence of Each Major Nucleoside (NRTI) and Nonnucleoside RT Inhibitor (NNRTI) Drug-Resistance Mutation (DRM) In Patients With Transmitted Drug Resistance and ≥1 Major NRTI or NNRTI DRM in a Meta-Analysis of 287 Studies Published Between 2000 and 2013LMICsa(n=24,173 individuals) Upper-income countriesa(n=24,898 individuals)Prevalence of Each Major NRTI DRMb(n=285 viruses with ≥1 major NRTI DRM)Prevalence of Each Major NRTI DRMb (n=782 viruses with ≥1 major NRTI DRM)DRMAbsolute %dCumulative %eDRMAbsolute % dCumulative % e184V63.563.5184V52.152.170R19.973.9215Y31.472.1184I7.580.170R24.487.565R6.685.165R5.391.2215Y19.590215F10.894.174I5.894.274V6.895.8115F2.997.1184I3.597.4215F10.899.2151M3.398.774V4.610074I4.899.8151M1.7100115F2.9100Prevalence of Each Major NNRTI DRMc(n=732 viruses with ≥1 major NNRTI DRM)Prevalence of Each Major NNRTI DRMc(n=1,089 viruses with ≥1 major NNRTI DRM)DRMAbsolute % dCumulative % eDRMAbsolute % dCumulative % e103N55.255.2103N6767181C23.775.5181C14.778190A16.486.1190A11.786.4188L3.189188L5.190.5103S4.390.8103S3.492.2106M292.2188H1.693.6190S1.893.7188C1.494.9190E1.495.1106A1.696100I1.896.3106M1.197106A197.1190S1.397.8188C1.298190E0.898.7230L298.8230L0.899.2181I0.699.4181I199.6188H0.699.8100I2.499.9181V0.6100101P1.1100101P0.6100181V0.1100aLMICs: Low- and Middle-Income Countries of Sub-Saharan Africa, South / Southeast Asia, and Latin America and Caribbean; Upper-Income Countries: Upper-Income Countries of North America, Europe, and Southeast Asia. bNRTI DRM with an HIVDB score ≥30. There were no insertions or deletions between codons 67 and 70. cNNRTI DRMs with an HIVDB score ≥60. dAbsolute %: number of individuals with DRM / number of individuals with a major DRM of the same drug class (NRTI or NNRTI). eCumulative %: number of individuals with one or more of the preceding DRMs in the list / number of individuals with a major DRM of the same drug class (NRTI or NNRTI).Table 5. Absolute and Cumulative Prevalence of Each Major Nucleoside (NRTI) and Nonnucleoside RT Inhibitor (NNRTI) Drug-Resistance Mutation (DRM) in 4,926 Patients with Virological Failure and Acquired Drug Resistance while Receiving a 1st-Line NRTI/NNRTI-Containing Regimena LMICsb(n=3,981 individuals) Upper-income countriesb(n=945 individuals)Prevalence of Each Major NRTI DRMc(n=3,110 viruses with ≥1 major NRTI DRM)Prevalence of Each Major NRTI DRMc(n=514 viruses with ≥1 major NRTI DRM)DRMAbsolute %eCumulative % fDRMAbsolute % eCumulative % f184V91.791.7184V87.487.465R9.896.765R16.794.2184I3.798.8184I897.9215Y11.199.3115F4.998.470R14.799.6215Y5.699215F9.499.870R8.999.4151M3.699.974I3.799.6115F399.9151M0.499.874I2.310074V5.410074V4.1100215F3.9100Prevalence of Each Major NNRTI DRMd(n=3,291 viruses with ≥1 major NNRTI DRM)Prevalence of Each Major NNRTI DRMd(n=608 viruses with ≥1 major NNRTI DRM)DRMAbsolute % eCumulative % fDRMAbsolute % eCumulative % f103N45.745.7103N63.863.8181C27.266.9181C19.178.3106M18.879.9190A13.583.6190A21.289.3190S6.688.3188L5.792.8188L5.392.3190S2.995106M4.694.6106A1.796.2190E1.696.2181V1.297.1106A297.5190E0.997.9188C1.898181I0.898.6188H1.398.5190Q0.699.1190Q0.598.8188C299.6230L399.2103S2.899.8181V0.599.5230L599.9181I0.599.8188H1.2100100I6.4100100I2.2100101P0.7100aRegimens include four AZT/d4T-containing regimens – AZT/d4T+3TC+EFV/NVP (n=4,020), four TDF-containing regimens – TDF+3TC/FTC+EFV/NVP (n=772), and two ABC-containing regimens – ABC+3TC+NVP/EFV (n=134).bLMICs: Low- and Middle-Income Countries of Sub-Saharan Africa, South / Southeast Asia, and Latin America and Caribbean; Upper-Income Countries: Upper-Income Countries of North America, Europe, and Southeast Asia. cNRTI DRM with an HIVDB score ≥30. There were no insertions or deletions between codons 67 and 70. dNNRTI DRMs with an HIVDB score ≥60. eAbsolute %: number of individuals with DRM / number of individuals with a major DRM of the same drug class (NRTI or NNRTI). fCumulative %: number of individuals with one or more of the preceding DRMs in the list / number of individuals with a major DRM of the same drug class (NRTI or NNRTI).Table 6. Absolute and Cumulative Prevalence of Major Lopinavir-Associated Mutations in 203 Lopinavir (LPV)-Resistant Viruses From 1,214 Previously PI-Na?ve Patients with Virological Failure on a Ritonavir-Boosted LPV (LPV/r)-Containing RegimenaDRMPrevalence of Major LPV/r DRMs(n=203 Viruses with Intermediate or High-Level LPV Resistance)Absolute %bCumulative %eV82A59.659.6L76V32.574.9I84V15.382.8I47A8.488.2V82F2.590.1I50V4.991.6Other d8.4100aResistance was defined as the presence of a cumulative HIVDB LPV mutation penalty score ≥30. bAbsolute %: number of individuals with DRM / number of individuals with a major LPV/r DRM. cCumulative %: number of individuals with one or more of the preceding major LPV/r DRMs in the list / number of individuals with a major LPV/r DRM. dOther included viruses having intermediate or high-level resistance arising from an accumulation of mutations with an HIVDB penalty score <30 including: M46I/I54V/V82S (n=4), I54V/V82M (n=3), I54V/L90M (n=1), V32I/M46I/I47V/I54M/L90M (n=1), I54V/V82T/L90M (n=1), M46I/I54V/V82T (n=1), I54V/V82T (n=1), I54V/V82S/V82T (n=1), L90M (n=1), M46I/L90M (n=1), M46I/I47V/I54V/V82S (n=1).Table 7. Cumulative Prevalence or Sensitivity of the Six Tier 1 RT Inhibitor (RTI) Drug-Resistance Mutations (DRMs) for Detecting Transmitted or Acquired Drug Resistance in Viruses from Patients with one or more Major NRTI or NNRTI DRMaRTI-DRMTDR1st-Line ADRAll Regions, All Subtypes?Total(n=1761)Total(n=3,996) Children (n=734)TDF(n=558)K103N5047.34947.3M184V65.691.394.879.2Y181C74.7959887.5G190A80.296.198.488.9V106M8197.698.993K65R81.998.599.397LMICs, All Subtypes?Total(n=573)Total(n=3,282)Children(n=725)TDF(n=291)K103N46.84549.440.5M184V62.79295.279Y181C76.195.697.987.6G190A81.796.798.389V106M82.998.498.995.9K65R83.99999.399All Regions, Subtype C?Total (n=157)Total(n=1,909)Children(n=473)TDF(n=242)K103N45.951.156.738.8M184V56.79296.275.6Y181C71.394.697.583.5G190A80.395.597.985.1V106M83.498.598.794.2K65R84.799.499.498.8aTDR and ADR were defined as having one or more major DRMs. Major NRTI-associated DRMs (HIVDB score ≥30) included K65R, D67 deletion, T69 insertion, K70R, L74V/I, Y115F, Q151M, M184I/V, and T215F/Y. Major NNRTI-associated DRMs (HIVDB score ≥60) included: L100I, K101P, K103N/S, V106A/M, Y181C/I/V, Y188L/H/C, G190A/S/E/Q, and M230L.Table S1. Summary of Sequences from Patients Receiving NRTI/NNRTI First-Line RegimensRegimenNo. PtsNo. RefsSubtype %ABC0102DGFOthersAZT/3TC/EFV6445314.821.932.68.76.53.69.91.20.8D4T/3TC/EFV1318442.1686.72.40.90.30.60.30.6TDF/3TC/EFV25116215.972.90.4404.40.40TDF/FTC/EFV34911639.320.98.65.2215.51.41.1ABC/3TC/EFV11395.313.375.202.703.500AZT/3TC/NVP6735417.88.92510.113.79.111.90.72.8D4T/3TC/NVP1385506.12.725.138.711.52.48.70.84TDF/3TC/NVP85122.411.845.93.518.82.415.300TDF/FTC/NVP8799.23116.16.983.425.300ABC/3TC/NVP2171933.34.84.81901900Total4926957.611.24614.97.42.77.70.71.8Abbreviations: AZT (zidovudine), 3TC (lamivudine), EFV (efavirenz), D4T (stavudine), TDF (tenofovir), FTC (emtricitabine), ABC (abacavir), NVP (nevirapine). Table S2. Absolute and Cumulative Percent of Each Major Nucleoside (NRTI) Drug-Resistance Mutation (DRM) in 467 Patients with Virological Failure and Acquired NRTI Drug Resistance while Receiving a 1st-Line TDF Containing Regimena DRMAbsolute %bCumulative %cM184V72.672.6K65R4893.4M184I13.798.7Y115F11.699.6Q151M0.999.8T215Y1.9100L74I6.2100L74V4.9100K70R4.7100T215F1.7100a NRTI DRM with an HIVDB score ≥30.bAbsolute. %: number of individuals with DRM / number of individuals with a major NRTI umulative. %: number of individuals with one or more of the preceding DRMs in the list / number of individuals with a major NRTI DRM .Table S3. Absolute and Cumulative Percent of Each Major Nucleoside (NRTI) Drug-Resistance Mutation (DRM) ? in 712 Children with Virological Failure and Acquired NRTI Drug Resistance while Receiving a 1st-Line NRTI/NNRTI RegimenaDRMAbsolute %b Cumulative %cM184V94.894.8K65R5.697.9M184I2.799.6K70R1099.9T215Y6.7100T215F8100L74V8100Y115F3.9100Q151M3.5100L74I2100aNRTI DRM with an HIVDB score ≥30.bAbsolute. %: number of individuals with DRM / number of individuals with a major NRTI umulative. %: number of individuals with one or more of the preceding DRMs in the list / number of individuals with a major NRTI DRM .Table S4. Absolute and Cumulative Percent of Each Major Nonnucleoside (NNRTI) Drug-Resistance Mutation (DRM) in 721 Children with Virological Failure and Acquired NNRTI Drug Resistance while Receiving a 1st-Line NRTI/NNRTI Regimena DRMAbsolute %b Cumulative %cK103N49.949.9V106M28.369.6Y181C21.584.9G190A17.690.8Y188L6.894.7G190S2.196.4G190Q1.297.6G190E198.5Y181V0.799M230L6.199.4V106A0.699.7L100I3.999.9Y188C2.2100K103S3.3100K101P2.5100Y188H1.1100aNNRTI DRM with an HIVDB score ≥60.bAbsolute. %: number of individuals with DRM / number of individuals with a major NNRTI umulative. %: number of individuals with one or more of the preceding DRMs in the list / number of individuals with a major NNRTI DRM .REFERENCES ADDIN EN.REFLIST 1.Chi BH, Bolton-Moore C, Holmes CB. 2013. Prevention of mother-to-child HIV transmission within the continuum of maternal, newborn, and child health services. 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