Increase in transmitted resistance to non-nucleoside reverse transcriptase inhibitors among newly diagnosed HIV-1 infections in Europe

Frentz, Dineke; Van de Vijver, David AMC; Abecasis, Ana B; Albert, Jan; Hamouda, Osamah; Jorgensen, Louise B; Kucherer, Claudia; Struck, Daniel; Schmit, Jean-Claude; Vercauteren, Jurgen; Balotta, Claudia; Beshkov, Danail; Camacho, Ricardo; Clotet, Bonaventura; Coughlan, Suzie; Griskevicius, Algirdas; Grossman, Zehava; Horban, Andrzej; Kolupajeva, Tatjana; Korn, Klaus; Kostrikis, Leondios G; Liitsola, Kirsi; Linka, Marek; Nielsen, Klaus; Otelea, Dan; Paraskevis, Dimitrios; Paredes, Roger; Poljak, Mario; Puchhammer-Stöckl, Elisabeth; Sönnerborg, Anders; Stanekova, Danika; Stanojevic, Maja; Van Wijngaerden, Eric; Wensing, Annemarie MJ; Boucher, Charles AB; Asjo, Birgitta

doi:10.1186/1471-2334-14-407

Article (Scientific journals)

Increase in transmitted resistance to non-nucleoside reverse transcriptase inhibitors among newly diagnosed HIV-1 infections in Europe

Frentz, Dineke; Van de Vijver, David AMC; Abecasis, Ana B et al.

2014 • In BMC Infectious Diseases, 14 (407), p. 1-12

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/259959

DOI
10.1186/1471-2334-14-407

PubMed
25047543

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Frentz et al. BMC Infectious Diseases 2014.pdf

Publisher postprint (685.34 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Europe; HIV-1; Resistance; Transmission

Abstract :

[en] Background : One out of ten newly diagnosed patients in Europe was infected with a virus carrying a drug resistant mutation. We analysed the patterns over time for transmitted drug resistance mutations (TDRM) using data from the European Spread program. Methods: Clinical, epidemiological and virological data from 4317 patients newly diagnosed with HIV-1 infection between 2002 and 2007 were analysed. Patients were enrolled using a pre-defined sampling strategy. Results: The overall prevalence of TDRM in this period was 8.9% (95% CI: 8.1-9.8). Interestingly, significant changes over time in TDRM caused by the different drug classes were found. Whereas nucleoside resistance mutations remained constant at 5%, a significant decline in protease inhibitors resistance mutations was observed, from 3.9% in 2002 to 1.6% in 2007 (p = 0.001). In contrast, resistance to non-nucleoside reverse transcriptase inhibitors (NNRTIs) doubled from 2.0% in 2002 to 4.1% in 2007 (p = 0.004) with 58% of viral strains carrying a K103N mutation. Phylogenetic analysis showed that these temporal changes could not be explained by large clusters of TDRM. Conclusion: During the years 2002 to 2007 transmitted resistance to NNRTI has doubled to 4% in Europe. The frequent use of NNRTI in first-line regimens and the clinical impact of NNRTI mutations warrants continuedmonitoring.

Disciplines :

Immunology & infectious disease

Author, co-author :

Frentz, Dineke; Erasmus Medical Center, Rotterdam, the Netherlands

Van de Vijver, David AMC; Erasmus Medical Center, Rotterdam, the Netherlands

Abecasis, Ana B; Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal

Albert, Jan; Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden ; Department of Clinical Microbiology, Karolinska University Hospital, Stockholm, Sweden

Hamouda, Osamah; Robert Koch Institute, Berlin, Germany

Jorgensen, Louise B; Statens Serum Institute, Copenhagen, Denmark

Kucherer, Claudia; Robert Koch Institute, Berlin, Germany

Struck, Daniel; Laboratory of Retrovirology, CRP-Santé, Luxembourg, Luxembourg

Schmit, Jean-Claude; Laboratory of Retrovirology, CRP-Santé, Luxembourg, Luxembourg ; Centre Hospitalier de Luxembourg, Luxembourg, Luxembourg

Vercauteren, Jurgen; Rega Institute, Katholieke Universiteit Leuven, Leuven, Belgium

More authors (26 more)

Other collaborator :

VAIRA, Dolorès ; Centre Hospitalier Universitaire de Liège - CHU > Unilab > Unité de laboratoire - LRS Biomol

Language :

English

Title :

Increase in transmitted resistance to non-nucleoside reverse transcriptase inhibitors among newly diagnosed HIV-1 infections in Europe

Publication date :

21 July 2014

Journal title :

BMC Infectious Diseases

eISSN :

1471-2334

Publisher :

BioMed Central, United Kingdom

Volume :

Issue :

407

Pages :

1-12

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 May 2021

Statistics

Number of views

75 (1 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Palella FJ, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, Aschman DJ, Holmberg SD. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998, 338(13):853-860.
Vercauteren J, Wensing AM, van de Vijver DA, Albert J, Balotta C, Hamouda O, Kucherer C, Struck D, Schmit JC, Asjo B, Bruckova M, Camacho RJ, Clotet B, Coughlan S, Grossman Z, Horban A, Korn K, Kostrikis L.G., Nielsen C, Paraskevis D, Poljak M, Puchhammer-Stockl E, Riva C, Ruiz L, Salminen M, Schuurman R, Sonnerborg A, Stanekova D, Stanojevic M, Vandamme AM, et al. Transmission of drug-resistant HIV-1 is stabilizing in Europe. J Infect Dis 2009, 200(10):1503-1508.
Bannister WP, Cozzi-Lepri A, Clotet B, Mocroft A, Kjaer J, Reiss P, von Wyl V, Lazzarin A, Katlama C, Phillips AN, Ruiz L, Lundgren JD, Euro S. Transmitted drug resistant HIV-1 and association with virologic and CD4 cell count response to combination antiretroviral therapy in the EuroSIDA study. J Acquir Immune Defic Syndr 2008, 48(3):324-333.
Booth CL, Garcia-Diaz AM, Youle MS, Johnson MA, Phillips A, Geretti AM. Prevalence and predictors of antiretroviral drug resistance in newly diagnosed HIV-1 infection. J Antimicrob Chemother 2007, 59(3):517-524.
Yerly S, von Wyl V, Ledergerber B, Boni J, Schupbach J, Burgisser P, Klimkait T, Rickenbach M, Kaiser L, Gunthard HF, Perrin L. Transmission of HIV-1 drug resistance in Switzerland: a 10-year molecular epidemiology survey. AIDS 2007, 21(16):2223-2229.
Wheeler WH, Ziebell RA, Zabina H, Pieniazek D, Prejean J, Bodnar UR, Mahle KC, Heneine W, Johnson JA, Hall HI, Variant A, Resistant HIVSG. Prevalence of transmitted drug resistance associated mutations and HIV-1 subtypes in new HIV-1 diagnoses, U.S.-2006. AIDS 2010, 24(8):1203-1212.
Hurt CB, McCoy SI, Kuruc J, Nelson JA, Kerkau M, Fiscus S, McGee K, Sebastian J, Leone P, Pilcher C, Hicks C, Eron J. Transmitted antiretroviral drug resistance among acute and recent HIV infections in North Carolina from 1998 to 2007. Antivir Ther 2009, 14(5):673-678.
Wittkop L, Gunthard HF, de Wolf F, Dunn D, Cozzi-Lepri A, de Luca A, Kucherer C, Obel N, von Wyl V, Masquelier B, Stephan C, Torti C, Antinori A, Garcia F, Judd A, Porter K, Thiebaut R, Castro H, van Sighem AI, Colin C, Kjaer J, Lundgren JD, Paredes R, Pozniak A, Clotet B, Phillips A, Pillay D, Chene G, EuroCoord C. Effect of transmitted drug resistance on virological and immunological response to initial combination antiretroviral therapy for HIV (EuroCoord-CHAIN joint project): a European multicohort study. Lancet Infect Dis 2011, 11(5):363-371.
Programme SPREAD. Transmission of drug-resistant HIV-1 in Europe remains limited to single classes. AIDS 2008, 22(5):625-635.
Countries in the WHO European Region. [http://www.who.int/about/regions/euro/en/index.html].
Bennett DE, Camacho RJ, Otelea D, Kuritzkes DR, Fleury H, Kiuchi M, Heneine W, Kantor R, Jordan MR, Schapiro JM, Vandamme AM, Sandstrom P, Boucher CA, van de Vijver D, Rhee SY, Liu TF, Pillay D, Shafer RW. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS ONE 2009, 4(3):e4724.
Frentz D, Wensing AM, Albert J, Paraskevis D, Abecasis AB, Hamouda O, Jorgensen LB, Kucherer C, Struck D, Schmit JC, Asjo B, Balotta C, Beshkov D, Camacho RJ, Clotet B, Coughlan S, De Wit S, Griskevicius A, Grossman Z, Horban A, Kolupajeva T, Korn K, Kostrikis L.G., Liitsola K, Linka M, Nielsen C, Otelea D, Paredes R, Poljak M, Puchhammer-Stockl E, et al. Limited cross-border infections in patients newly diagnosed with HIV in Europe. Retrovirology 2013, 10:36.
de Oliveira T, Deforche K, Cassol S, Salminen M, Paraskevis D, Seebregts C, Snoeck J, van Rensburg EJ, Wensing AM, van de Vijver DA, Boucher CA, Camacho R, Vandamme AM. An automated genotyping system for analysis of HIV-1 and other microbial sequences. Bioinformatics 2005, 21(19):3797-3800.
Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14(9):817-818.
Hillis DM, Bull JJ. An emperical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 1993, 42(2):182-192.
Gifford RJ, de Oliveira T, Rambaut A, Pybus OG, Dunn D, Vandamme AM, Kellam P, Pillay D, Resistance UKCGoHD Phylogenetic surveillance of viral genetic diversity and the evolving molecular epidemiology of human immunodeficiency virus type 1. J Virol 2007, 81(23):13050-13056. Resistance UKCGoHD.
Yeni PG, Hammer SM, Carpenter CC, Cooper DA, Fischl MA, Gatell JM, Gazzard BG, Hirsch MS, Jacobsen DM, Katzenstein DA, Montaner JS, Richman DD, Saag MS, Schechter M, Schooley RT, Thompson MA, Vella S, Volberding PA. Antiretroviral treatment for adult HIV infection in 2002: updated recommendations of the International AIDS Society-USA Panel. JAMA 2002, 288(2):222-235.
Yeni PG, Hammer SM, Hirsch MS, Saag MS, Schechter M, Carpenter CC, Fischl MA, Gatell JM, Gazzard BG, Jacobsen DM, Katzenstein DA, Montaner JS, Richman DD, Schooley RT, Thompson MA, Vella S, Volberding PA. Treatment for adult HIV infection: 2004 recommendations of the International AIDS Society-USA panel. JAMA 2004, 292(2):251-265.
Hammer SM, Saag MS, Schechter M, Montaner JS, Schooley RT, Jacobsen DM, Thompson MA, Carpenter CC, Fischl MA, Gazzard BG, Gatell JM, Hirsch MS, Katzenstein DA, Richman DD, Vella S, Yeni PG, Volberding PA, International AS-USAp Treatment for adult HIV infection: 2006 recommendations of the International AIDS Society-USA panel. JAMA 2006, 296(7):827-843. International AS-USAp.
Hammer SM, Eron JJ, Reiss P, Schooley RT, Thompson MA, Walmsley S, Cahn P, Fischl MA, Gatell JM, Hirsch MS, Jacobsen DM, Montaner JS, Richman DD, Yeni PG, Volberding PA, International AS-USA Antiretroviral treatment of adult HIV infection: 2008 recommendations of the International AIDS Society-USA panel. JAMA 2008, 300(5):555-570. International AS-USA.
Cane P, Chrystie I, Dunn D, Evans B, Geretti AM, Green H, Phillips A, Pillay D, Porter K, Pozniak A, Sabin C, Smit E, Weber J, Zuckerman M, Resistance UKGoTHD Time trends in primary resistance to HIV drugs in the United Kingdom: multicentre observational study. BMJ 2005, 331(7529):1368. Resistance UKGoTHD.
Vercauteren J, Derdelinckx I, Sasse A, Bogaert M, Ceunen H, De Roo A, De Wit S, Deforche K, Echahidi F, Fransen K, Goffard JC, Goubau P, Goudeseune E, Yombi JC, Lacor P, Liesnard C, Moutschen M, Pierard D, Rens R, Schrooten Y, Vaira D, den HA V, der GB V, van Ranst M, van Wijngaerden E, Vandercam B, Vekemans M, Verhofstede C, Clumeck N, Vandamme AM, et al. Prevalence and epidemiology of HIV type 1 drug resistance among newly diagnosed therapy-naive patients in Belgium from 2003 to 2006. AIDS ResHumRetroviruses 2008, 24(3):355-362.
Bracciale L, Colafigli M, Zazzi M, Corsi P, Meraviglia P, Micheli V, Maserati R, Gianotti N, Penco G, Setti M, Di Giambenedetto S, Butini L, Vivarelli A, Trezzi M, De Luca A. Prevalence of transmitted HIV-1 drug resistance in HIV-1-infected patients in Italy: evolution over 12 years and predictors. J Antimicrob Chemother 2009, 64(3):607-615.
Bartmeyer B, Kuecherer C, Houareau C, Werning J, Keeren K, Somogyi S, Kollan C, Jessen H, Dupke S, Hamouda O, German HIVSSG. Prevalence of transmitted drug resistance and impact of transmitted resistance on treatment success in the German HIV-1 seroconverter cohort. PLoS ONE 2010, 5(10):e12718.
Karlsson A, Bjorkman P, Bratt G, Ekvall H, Gisslen M, Sonnerborg A, Mild M, Albert J. Low prevalence of transmitted drug resistance in patients newly diagnosed with HIV-1 infection in Sweden 2003-2010. PLoS ONE 2012, 7(3):e33484.
U. K. Collaborative Group on HIV Drug Resistance Time trends in drug resistant HIV-1 infections in the United Kingdom up to 2009: multicentre observational study. BMJ 2012, 345:e5253. U. K. Collaborative Group on HIV Drug Resistance.
Jain V, Liegler T, Vittinghoff E, Hartogensis W, Bacchetti P, Poole L, Loeb L, Pilcher CD, Grant RM, Deeks SG, Hecht FM. Transmitted drug resistance in persons with acute/early HIV-1 in San Francisco, 2002-2009. PLoS ONE 2010, 5(12):e15510.
Lockman S, Hughes MD, McIntyre J, Zheng Y, Chipato T, Conradie F, Sawe F, Asmelash A, Hosseinipour MC, Mohapi L, Stringer E, Mngqibisa R, Siika A, Atwine D, Hakim J, Shaffer D, Kanyama C, Wools-Kaloustian K, Salata RA, Hogg E, Alston-Smith B, Walawander A, Purcelle-Smith E, Eshleman S, Rooney J, Rahim S, Mellors JW, Schooley RT, Currier JS, Team OAS Antiretroviral therapies in women after single-dose nevirapine exposure. N Engl J Med 2010, 363(16):1499-1509. Team OAS.
Pingen M, Nijhuis M, de Bruijn JA, Boucher CA, Wensing AM. Evolutionary pathways of transmitted drug-resistant HIV-1. J Antimicrob Chemother 2011, 66(7):1467-1480.
UK Collaborative Group on HIV Drug Resistance; UK Collaborative HIV Cohort Study; UK Register of HIV Seroconverters Evidence of a decline in transmitted HIV-1 drug resistance in the United Kingdom. AIDS 2007, 21(8):1035-1039. UK Collaborative Group on HIV Drug Resistance; UK Collaborative HIV Cohort Study; UK Register of HIV Seroconverters.
Bezemer D, van Sighem A, Lukashov VV, van der Hoek L, Back N, Schuurman R, Boucher CA, Claas EC, Boerlijst MC, Coutinho RA, de Wolf F, Cohort A. Transmission networks of HIV-1 among men having sex with men in the Netherlands. AIDS 2010, 24(2):271-282.
Turner D, Amit S, Chalom S, Penn O, Pupko T, Katchman E, Matus N, Tellio H, Katzir M, Avidor B. Emergence of an HIV-1 cluster harbouring the major protease L90M mutation among treatment-naive patients in Tel Aviv, Israel. HIV Med 2012, 13(4):202-206.
Carpenter CC, Cooper DA, Fischl MA, Gatell JM, Gazzard BG, Hammer SM, Hirsch MS, Jacobsen DM, Katzenstein DA, Montaner JS, Richman DD, Saag MS, Schechter M, Schooley RT, Thompson MA, Vella S, Yeni PG, Volberding PA. Antiretroviral therapy in adults: updated recommendations of the International AIDS Society-USA panel. JAMA 2000, 283(3):381-390.
Staszewski S, Morales-Ramirez J, Tashima KT, Rachlis A, Skiest D, Stanford J, Stryker R, Johnson P, Labriola DF, Farina D, Manion DJ, Ruiz NM. Efavirenz plus zidovudine and lamivudine, efavirenz plus indinavir, and indinavir plus zidovudine and lamivudine in the treatment of HIV-1 infection in adults. Study 006 team. N Engl J Med 1999, 341(25):1865-1873.
Riddler SA, Haubrich R, DiRienzo AG, Peeples L, Powderly WG, Klingman KL, Garren KW, George T, Rooney JF, Brizz B, Lalloo UG, Murphy RL, Swindells S, Havlir D, Mellors JW. Class-sparing regimens for initial treatment of HIV-1 infection. N Engl J Med 2008, 358(20):2095-2106.
Parienti JJ, Bangsberg DR, Verdon R, Gardner EM. Better adherence with once-daily antiretroviral regimens: a meta-analysis. Clin Infect Dis 2009, 48(4):484-488.
Smit M, Smit C, Geerlings S, Gras L, Brinkman K, Hallett TB, de Wolf F, Athena Observational C Changes in first-line cART regimens and short-term clinical outcome between 1996 and 2010 in The Netherlands. PLoS ONE 2013, 8(9):e76071. Athena Observational C.
van de Vijver DA, Wensing AM, Angarano G, Asjo B, Balotta C, Boeri E, Camacho R, Chaix ML, Costagliola D, De Luca A, Derdelinckx I, Grossman Z, Hamouda O, Hatzakis A, Hemmer R, Hoepelman A, Horban A, Korn K, Kucherer C, Leitner T, Loveday C, MacRae E, Maljkovic I, de Mendoza C, Meyer L, Nielsen C, Op de Coul EL, Ormaasen V, Paraskevis D, Perrin L, et al. The calculated genetic barrier for antiretroviral drug resistance substitutions is largely similar for different HIV-1 subtypes. J Acquir Immune Defic Syndr 2006, 41(3):352-360.
Gallant JE, DeJesus E, Arribas JR, Pozniak AL, Gazzard B, Campo RE, Lu B, McColl D, Chuck S, Enejosa J, Toole JJ, Cheng AK, Study G. Tenofovir DF, emtricitabine, and efavirenz vs. zidovudine, lamivudine, and efavirenz for HIV. N Engl J Med 2006, 354(3):251-260.
Jain V, Sucupira MC, Bacchetti P, Hartogensis W, Diaz RS, Kallas EG, Janini LM, Liegler T, Pilcher CD, Grant RM, Cortes R, Deeks SG, Hecht FM. Differential persistence of transmitted HIV-1 drug resistance mutation classes. J Infect Dis 2011, 203(8):1174-1181.
Kikaire B, Khoo S, Walker AS, Ssali F, Munderi P, Namale L, Reid A, Gibb DM, Mugyenyi P, Grosskurth H, Team DT. Nevirapine clearance from plasma in African adults stopping therapy: a pharmacokinetic substudy. AIDS 2007, 21(6):733-737.
Bartlett JA, Buda JJ, von Scheele B, Mauskopf JA, Davis EA, Elston R, King MS, Lanier ER. Minimizing resistance consequences after virologic failure on initial combination therapy: a systematic overview. J Acquir Immune Defic Syndr 2006, 41(3):323-331.
Gupta R, Hill A, Sawyer AW, Pillay D. Emergence of drug resistance in HIV type 1-infected patients after receipt of first-line highly active antiretroviral therapy: a systematic review of clinical trials. Clin Infect Dis 2008, 47(5):712-722.
Lima VD, Gill VS, Yip B, Hogg RS, Montaner JS, Harrigan PR. Increased resilience to the development of drug resistance with modern boosted protease inhibitor-based highly active antiretroviral therapy. J Infect Dis 2008, 198(1):51-58.
Elzi L, Erb S, Furrer H, Ledergerber B, Cavassini M, Hirschel B, Vernazza P, Bernasconi E, Weber R, Battegay M, for the Swiss HIVCS Choice of initial combination antiretroviral therapy in individuals with HIV infection: determinants and outcomes. Arch Intern Med 2012, 172(17):1313-1321. for the Swiss HIVCS.
Vo TT, Ledergerber B, Keiser O, Hirschel B, Furrer H, Battegay M, Cavassini M, Bernasconi E, Vernazza P, Weber R, Swiss HIVCS Durability and outcome of initial antiretroviral treatments received during 2000-2005 by patients in the Swiss HIV Cohort Study. J Infect Dis 2008, 197(12):1685-1694. Swiss HIVCS.
Schuurman R, Brambilla D, de Groot T, Huang D, Land S, Bremer J, Benders I, Boucher CA, Group EW. Underestimation of HIV type 1 drug resistance mutations: results from the ENVA-2 genotyping proficiency program. AIDS Res Hum Retroviruses 2002, 18(4):243-248.
Li JZ, Paredes R, Ribaudo HJ, Svarovskaia ES, Metzner KJ, Kozal MJ, Hullsiek KH, Balduin M, Jakobsen MR, Geretti AM, Thiebaut R, Ostergaard L, Masquelier B, Johnson JA, Miller MD, Kuritzkes DR. Low-frequency HIV-1 drug resistance mutations and risk of NNRTI-based antiretroviral treatment failure: a systematic review and pooled analysis. JAMA 2011, 305(13):1327-1335.
Wensing AM, van de Vijver DA, Angarano G, Asjo B, Balotta C, Boeri E, Camacho R, Chaix ML, Costagliola D, De Luca A, Derdelinckx I, Grossman Z, Hamouda O, Hatzakis A, Hemmer R, Hoepelman A, Horban A, Korn K, Kucherer C, Leitner T, Loveday C, MacRae E, Maljkovic I, de Mendoza C, Meyer L, Nielsen C, Op de Coul EL, Ormaasen V, Paraskevis D, Perrin L, et al. Prevalence of drug-resistant HIV-1 variants in untreated individuals in Europe: implications for clinical management. J Infect Dis 2005, 192(6):958-966.