HIV-1 drug resistance in people on dolutegravir-based antiretroviral therapy: a collaborative cohort analysis

The widespread use of the integrase strand transfer inhibitor (INSTI) dolutegravir in first-line and second-line antiretroviral therapy (ART) might facilitate emerging resistance. The DTG RESIST study combined data from HIV cohorts to examine patterns of drug resistance mutations (DRMs) and identify...

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Vydáno v:	The lancet HIV Ročník 10; číslo 11; s. e733
Hlavní autoři:	Loosli, Tom, Hossmann, Stefanie, Ingle, Suzanne M, Okhai, Hajra, Kusejko, Katharina, Mouton, Johannes, Bellecave, Pantxika, van Sighem, Ard, Stecher, Melanie, d'Arminio Monforte, Antonella, Gill, M John, Sabin, Caroline A, Maartens, Gary, Günthard, Huldrych F, Sterne, Jonathan A C, Lessells, Richard, Egger, Matthias, Kouyos, Roger D
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	Netherlands 01.11.2023
Témata:	Cohort Studies Drug Resistance, Viral - genetics Heterocyclic Compounds, 3-Ring - pharmacology Heterocyclic Compounds, 3-Ring - therapeutic use HIV Infections - drug therapy HIV Integrase Inhibitors - pharmacology HIV Integrase Inhibitors - therapeutic use HIV Seropositivity - drug therapy HIV-1 - genetics Humans Lamivudine - therapeutic use Reverse Transcriptase Inhibitors - therapeutic use
ISSN:	2352-3018, 2352-3018
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Abstract	The widespread use of the integrase strand transfer inhibitor (INSTI) dolutegravir in first-line and second-line antiretroviral therapy (ART) might facilitate emerging resistance. The DTG RESIST study combined data from HIV cohorts to examine patterns of drug resistance mutations (DRMs) and identify risk factors for dolutegravir resistance. We included cohorts with INSTI resistance data from two collaborations (ART Cohort Collaboration, International epidemiology Databases to Evaluate AIDS in Southern Africa), and the UK Collaborative HIV Cohort. Eight cohorts from Canada, France, Germany, Italy, the Netherlands, Switzerland, South Africa, and the UK contributed data on individuals who were viraemic on dolutegravir-based ART and underwent genotypic resistance testing. Individuals with unknown dolutegravir initiation date were excluded. Resistance levels were categorised using the Stanford algorithm. We identified risk factors for resistance using mixed-effects ordinal logistic regression models. We included 599 people with genotypic resistance testing on dolutegravir-based ART between May 22, 2013, and Dec 20, 2021. Most had HIV-1 subtype B (n=351, 59%), a third had been exposed to first-generation INSTIs (n=193, 32%), 70 (12%) were on dolutegravir dual therapy, and 18 (3%) were on dolutegravir monotherapy. INSTI DRMs were detected in 86 (14%) individuals; 20 (3%) had more than one mutation. Most (n=563, 94%) were susceptible to dolutegravir, seven (1%) had potential low, six (1%) low, 17 (3%) intermediate, and six (1%) high-level dolutegravir resistance. The risk of dolutegravir resistance was higher on dolutegravir monotherapy (adjusted odds ratio [aOR] 34·1, 95% CI 9·93-117) and dolutegravir plus lamivudine dual therapy (aOR 9·21, 2·20-38·6) compared with combination ART, and in the presence of potential low or low (aOR 5·23, 1·32-20·7) or intermediate or high-level (aOR 13·4, 4·55-39·7) nucleoside reverse transcriptase inhibitor (NRTI) resistance. Among people with viraemia on dolutegravir-based ART, INSTI DRMs and dolutegravir resistance were rare. NRTI resistance substantially increased the risk of dolutegravir resistance, which is of concern, notably in resource-limited settings. Monitoring is important to prevent resistance at the individual and population level and ensure the long-term sustainability of ART. US National Institutes of Health, Swiss National Science Foundation.
AbstractList	The widespread use of the integrase strand transfer inhibitor (INSTI) dolutegravir in first-line and second-line antiretroviral therapy (ART) might facilitate emerging resistance. The DTG RESIST study combined data from HIV cohorts to examine patterns of drug resistance mutations (DRMs) and identify risk factors for dolutegravir resistance.BACKGROUNDThe widespread use of the integrase strand transfer inhibitor (INSTI) dolutegravir in first-line and second-line antiretroviral therapy (ART) might facilitate emerging resistance. The DTG RESIST study combined data from HIV cohorts to examine patterns of drug resistance mutations (DRMs) and identify risk factors for dolutegravir resistance.We included cohorts with INSTI resistance data from two collaborations (ART Cohort Collaboration, International epidemiology Databases to Evaluate AIDS in Southern Africa), and the UK Collaborative HIV Cohort. Eight cohorts from Canada, France, Germany, Italy, the Netherlands, Switzerland, South Africa, and the UK contributed data on individuals who were viraemic on dolutegravir-based ART and underwent genotypic resistance testing. Individuals with unknown dolutegravir initiation date were excluded. Resistance levels were categorised using the Stanford algorithm. We identified risk factors for resistance using mixed-effects ordinal logistic regression models.METHODSWe included cohorts with INSTI resistance data from two collaborations (ART Cohort Collaboration, International epidemiology Databases to Evaluate AIDS in Southern Africa), and the UK Collaborative HIV Cohort. Eight cohorts from Canada, France, Germany, Italy, the Netherlands, Switzerland, South Africa, and the UK contributed data on individuals who were viraemic on dolutegravir-based ART and underwent genotypic resistance testing. Individuals with unknown dolutegravir initiation date were excluded. Resistance levels were categorised using the Stanford algorithm. We identified risk factors for resistance using mixed-effects ordinal logistic regression models.We included 599 people with genotypic resistance testing on dolutegravir-based ART between May 22, 2013, and Dec 20, 2021. Most had HIV-1 subtype B (n=351, 59%), a third had been exposed to first-generation INSTIs (n=193, 32%), 70 (12%) were on dolutegravir dual therapy, and 18 (3%) were on dolutegravir monotherapy. INSTI DRMs were detected in 86 (14%) individuals; 20 (3%) had more than one mutation. Most (n=563, 94%) were susceptible to dolutegravir, seven (1%) had potential low, six (1%) low, 17 (3%) intermediate, and six (1%) high-level dolutegravir resistance. The risk of dolutegravir resistance was higher on dolutegravir monotherapy (adjusted odds ratio [aOR] 34·1, 95% CI 9·93-117) and dolutegravir plus lamivudine dual therapy (aOR 9·21, 2·20-38·6) compared with combination ART, and in the presence of potential low or low (aOR 5·23, 1·32-20·7) or intermediate or high-level (aOR 13·4, 4·55-39·7) nucleoside reverse transcriptase inhibitor (NRTI) resistance.FINDINGSWe included 599 people with genotypic resistance testing on dolutegravir-based ART between May 22, 2013, and Dec 20, 2021. Most had HIV-1 subtype B (n=351, 59%), a third had been exposed to first-generation INSTIs (n=193, 32%), 70 (12%) were on dolutegravir dual therapy, and 18 (3%) were on dolutegravir monotherapy. INSTI DRMs were detected in 86 (14%) individuals; 20 (3%) had more than one mutation. Most (n=563, 94%) were susceptible to dolutegravir, seven (1%) had potential low, six (1%) low, 17 (3%) intermediate, and six (1%) high-level dolutegravir resistance. The risk of dolutegravir resistance was higher on dolutegravir monotherapy (adjusted odds ratio [aOR] 34·1, 95% CI 9·93-117) and dolutegravir plus lamivudine dual therapy (aOR 9·21, 2·20-38·6) compared with combination ART, and in the presence of potential low or low (aOR 5·23, 1·32-20·7) or intermediate or high-level (aOR 13·4, 4·55-39·7) nucleoside reverse transcriptase inhibitor (NRTI) resistance.Among people with viraemia on dolutegravir-based ART, INSTI DRMs and dolutegravir resistance were rare. NRTI resistance substantially increased the risk of dolutegravir resistance, which is of concern, notably in resource-limited settings. Monitoring is important to prevent resistance at the individual and population level and ensure the long-term sustainability of ART.INTERPRETATIONAmong people with viraemia on dolutegravir-based ART, INSTI DRMs and dolutegravir resistance were rare. NRTI resistance substantially increased the risk of dolutegravir resistance, which is of concern, notably in resource-limited settings. Monitoring is important to prevent resistance at the individual and population level and ensure the long-term sustainability of ART.US National Institutes of Health, Swiss National Science Foundation.FUNDINGUS National Institutes of Health, Swiss National Science Foundation. The widespread use of the integrase strand transfer inhibitor (INSTI) dolutegravir in first-line and second-line antiretroviral therapy (ART) might facilitate emerging resistance. The DTG RESIST study combined data from HIV cohorts to examine patterns of drug resistance mutations (DRMs) and identify risk factors for dolutegravir resistance. We included cohorts with INSTI resistance data from two collaborations (ART Cohort Collaboration, International epidemiology Databases to Evaluate AIDS in Southern Africa), and the UK Collaborative HIV Cohort. Eight cohorts from Canada, France, Germany, Italy, the Netherlands, Switzerland, South Africa, and the UK contributed data on individuals who were viraemic on dolutegravir-based ART and underwent genotypic resistance testing. Individuals with unknown dolutegravir initiation date were excluded. Resistance levels were categorised using the Stanford algorithm. We identified risk factors for resistance using mixed-effects ordinal logistic regression models. We included 599 people with genotypic resistance testing on dolutegravir-based ART between May 22, 2013, and Dec 20, 2021. Most had HIV-1 subtype B (n=351, 59%), a third had been exposed to first-generation INSTIs (n=193, 32%), 70 (12%) were on dolutegravir dual therapy, and 18 (3%) were on dolutegravir monotherapy. INSTI DRMs were detected in 86 (14%) individuals; 20 (3%) had more than one mutation. Most (n=563, 94%) were susceptible to dolutegravir, seven (1%) had potential low, six (1%) low, 17 (3%) intermediate, and six (1%) high-level dolutegravir resistance. The risk of dolutegravir resistance was higher on dolutegravir monotherapy (adjusted odds ratio [aOR] 34·1, 95% CI 9·93-117) and dolutegravir plus lamivudine dual therapy (aOR 9·21, 2·20-38·6) compared with combination ART, and in the presence of potential low or low (aOR 5·23, 1·32-20·7) or intermediate or high-level (aOR 13·4, 4·55-39·7) nucleoside reverse transcriptase inhibitor (NRTI) resistance. Among people with viraemia on dolutegravir-based ART, INSTI DRMs and dolutegravir resistance were rare. NRTI resistance substantially increased the risk of dolutegravir resistance, which is of concern, notably in resource-limited settings. Monitoring is important to prevent resistance at the individual and population level and ensure the long-term sustainability of ART. US National Institutes of Health, Swiss National Science Foundation.
Author	Loosli, Tom Hossmann, Stefanie Okhai, Hajra d'Arminio Monforte, Antonella Maartens, Gary Egger, Matthias Mouton, Johannes van Sighem, Ard Günthard, Huldrych F Kouyos, Roger D Gill, M John Sterne, Jonathan A C Stecher, Melanie Kusejko, Katharina Ingle, Suzanne M Sabin, Caroline A Lessells, Richard Bellecave, Pantxika
Author_xml	– sequence: 1 givenname: Tom surname: Loosli fullname: Loosli, Tom organization: Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland; Institute of Medical Virology, University of Zurich, Zurich, Switzerland – sequence: 2 givenname: Stefanie surname: Hossmann fullname: Hossmann, Stefanie organization: Institute of Social and Preventive Medicine (ISPM), University of Bern, Bern, Switzerland – sequence: 3 givenname: Suzanne M surname: Ingle fullname: Ingle, Suzanne M organization: Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK – sequence: 4 givenname: Hajra surname: Okhai fullname: Okhai, Hajra organization: Institute for Global Health, University College London, London, UK – sequence: 5 givenname: Katharina surname: Kusejko fullname: Kusejko, Katharina organization: Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland; Institute of Medical Virology, University of Zurich, Zurich, Switzerland – sequence: 6 givenname: Johannes surname: Mouton fullname: Mouton, Johannes organization: Division of Clinical Pharmacology, Department of Medicine, University of Cape Town, Cape Town, South Africa – sequence: 7 givenname: Pantxika surname: Bellecave fullname: Bellecave, Pantxika organization: Virology Laboratory, University Hospital Bordeaux, Bordeaux, France – sequence: 8 givenname: Ard surname: van Sighem fullname: van Sighem, Ard organization: Stichting HIV Monitoring, Amsterdam, Netherlands – sequence: 9 givenname: Melanie surname: Stecher fullname: Stecher, Melanie organization: German Center for Infection Research (DZIF), Partner-Site Cologne-Bonn, Cologne, Germany; Department I of Internal Medicine, University Hospital Cologne, University of Cologne, Cologne, Germany – sequence: 10 givenname: Antonella surname: d'Arminio Monforte fullname: d'Arminio Monforte, Antonella organization: Italian Cohort Naive Antiretrovirals (ICONA), University of Milan, Milan, Italy – sequence: 11 givenname: M John surname: Gill fullname: Gill, M John organization: Southern Alberta Clinic, Calgary, AB, Canada; Department of Medicine, University of Calgary, Calgary, AB, Canada – sequence: 12 givenname: Caroline A surname: Sabin fullname: Sabin, Caroline A organization: Institute for Global Health, University College London, London, UK – sequence: 13 givenname: Gary surname: Maartens fullname: Maartens, Gary organization: Division of Clinical Pharmacology, Department of Medicine, University of Cape Town, Cape Town, South Africa – sequence: 14 givenname: Huldrych F surname: Günthard fullname: Günthard, Huldrych F organization: Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland; Institute of Medical Virology, University of Zurich, Zurich, Switzerland – sequence: 15 givenname: Jonathan A C surname: Sterne fullname: Sterne, Jonathan A C organization: Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK – sequence: 16 givenname: Richard surname: Lessells fullname: Lessells, Richard organization: KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), University of KwaZulu-Natal, Durban, South Africa; Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa – sequence: 17 givenname: Matthias surname: Egger fullname: Egger, Matthias email: matthias.egger@unibe.ch organization: Institute of Social and Preventive Medicine (ISPM), University of Bern, Bern, Switzerland; Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK; Centre for Infectious Disease Epidemiology and Research, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa. Electronic address: matthias.egger@unibe.ch – sequence: 18 givenname: Roger D surname: Kouyos fullname: Kouyos, Roger D organization: Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland; Institute of Medical Virology, University of Zurich, Zurich, Switzerland
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References	37066200 - medRxiv. 2023 Apr 05:2023.04.05.23288183. doi: 10.1101/2023.04.05.23288183 37832568 - Lancet HIV. 2023 Nov;10(11):e696-e698. doi: 10.1016/S2352-3018(23)00259-X
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SubjectTerms	Cohort Studies Drug Resistance, Viral - genetics Heterocyclic Compounds, 3-Ring - pharmacology Heterocyclic Compounds, 3-Ring - therapeutic use HIV Infections - drug therapy HIV Integrase Inhibitors - pharmacology HIV Integrase Inhibitors - therapeutic use HIV Seropositivity - drug therapy HIV-1 - genetics Humans Lamivudine - therapeutic use Reverse Transcriptase Inhibitors - therapeutic use
Title	HIV-1 drug resistance in people on dolutegravir-based antiretroviral therapy: a collaborative cohort analysis
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