Transmitted HIV drug resistance in treatment-naive Romanian patients

Journal of Medical Virology

Volumn 85, Issue 7, 2013, Pages 1139-1147

  Temereanca, Aura ^a,b   Ene, Luminita ^c   Mehta, Sanjay ^d   Manolescu, Loredana ^a,b   Duiculescu, Dan ^c   Ruta, Simona ^a,b  

^a CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b STEFAN S NICOLAU INSTITUTE OF VIROLOGY   (Romania)

^c VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HIV 1; Romania; Subtype F; Transmitted drug resistance

Indexed keywords

ANTIRETROVIRUS AGENT; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ADOLESCENT; ADULT; ARTICLE; CHILD; DRUG RESISTANCE; DRUG USE; ENZYME IMMUNOASSAY; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; MALE; PHYLOGENY; ROMANIA; SCHOOL CHILD; TRANSMITTED HUMAN IMMUNODEFICIENCY VIRUS DRUG RESISTANCE; VIRUS TRANSMISSION;

HIV-1; ROMANIA; SUBTYPE F; TRANSMITTED DRUG RESISTANCE;

ADOLESCENT; ADULT; CHILD; CLUSTER ANALYSIS; DRUG RESISTANCE, VIRAL; FEMALE; GENOTYPE; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; MUTATION, MISSENSE; PHYLOGENY; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PREVALENCE; RNA, VIRAL; ROMANIA; SEQUENCE ANALYSIS, DNA; YOUNG ADULT;

EID: 84878224363     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23572     Document Type: Article

References (56)

1. Bártolo I, Rocha C, Bartolomeu J, Gama A, Fonseca M, Mendes A, Cristina F, Thamm S, Epalanga M, Silva PC, Taveira N. 2009. Antiretroviral drug resistance surveillance among treatment-naive human immunodeficiency virus type 1-infected individuals in Angola: Evidence for low level of transmitted drug resistance. Antimicrob Agents Chemother 53:3156-3158.
2. Bennett DE, Myatt M, Bertagnolio S, Sutherland D, Gilks CF. 2008. Recommendations for surveillance of transmitted HIV drug resistance in countries scaling up antiretroviral treatment. Antivir Ther 13:25-36.
3. 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. 2009. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS ONE 4:e4724.
4. Cernescu C, Tardei G, Necula A, Ruta SM, Pau CP. 1994. The serologic significance of F viral genotype for human immunodeficiency virus type 1 epidemic. J Infect Dis 170:1043-1044.
5. Chaix ML, Descamps D, Wirden M, Bocket L, Delaugerre C, Tamalet C, Schneider V, Izopet J, Masquelier B, Rouzioux C, Meyer L, Costagliola D, ANRS AC11 Resistance Group, Cohort PRIMO ANRS CO6, FHDH ANRS CO4 Study Groups. 2009. Stable frequency of HIV-1 transmitted drug resistance in patients at the time of primary infection over 1996-2006 in France. AIDS 23:717-724.
6. Chilton D, Harrison L, Green H, Lattimore S, Delpech V, Pillay D. 2008. Trends in transmitted HIV drug resistance among non-B subtypes in the UK. J Int AIDS Soc 11:O2.
7. Chitu V, Diaconu CC, Veliceasa D, Ruta S, Grancea C, Tardei G, Cernescu CE. 1999. Dynamics of the HIV-1 variability in adults from Bucharest, 1992-1998. Rom J Virol 45:43-51.
8. Clemente JC, Hemrajani R, Blum LE, Goodenow MM, Dunn BM. 2003. Secondary mutations M36I and A71V in the human immunodeficiency virus type 1 protease can provide an advantage for the emergence of the primary mutation D30N. Biochemistry 42:15029-15035.
9. de Felipe B, Pérez-Romero P, Abad-Fernández M, Fernandez-Cuenca F, Martinez-Fernandez FJ, Trastoy M, Mata Rdel C, López-Cortés LF, Leal M, Viciana P, Vallejo A. 2011. Prevalence and resistance mutations of non-B HIV-1 subtypes among immigrants in Southern Spain along the decade 2000-2010. Virol J 8:416.
10. DeGruttola V, Dix L, D'Aquila R, Holder D, Phillips A, Ait-Khaled M, Baxter J, Clevenbergh P, Hammer S, Harrigan R, Katzenstein D, Lanier R, Miller M, Para M, Yerly S, Zolopa A, Murray J, Patick A, Miller V, Castillo S, Pedneault L, Mellors J. 2000. The relation between baseline HIV drug resistance and response to antiretroviral therapy: Re-analysis of retrospective and prospective studies using a standardized data analysis plan. Antivir Ther 5:41-48.
11. Dumans AT, Barreto CC, Santos AF, Arruda M, Sousa TM, Machado ES, Sabino EC, Brindeiro RM, Tanuri A, Duarte AJ, Soares MA. 2009. Distinct resistance mutation and polymorphism acquisition in HIV-1 protease of subtypes B and F1 from children and adult patients under virological failure. Infect Genet Evol 9:62-70.
12. Franzetti M, Lai A, Roberto Simonetti F, Bozzi G, De Luca A, Micheli V, Meraviglia P, Corsi P, Bagnarelli P, Almi P, Zoncada A, Balotta C. 2012. High burden of transmitted HIV-1 drug resistance in Italian patients carrying F1 subtype. J Antimicrob Chemother 67:1250-1253.
13. Grant RM, Hecht FM, Warmerdam M, Liu L, Liegler T, Petropoulos CJ, Hellmann NS, Chesney M, Busch MP, Kahn JO. 2002. Time trends in primary HIV-1 drug resistance among recently infected persons. JAMA 288:181-188.
14. Guimarães ML, Vicente AC, Otsuki K, da Silva RF, Francisco M, da Silva FG, Serrano D, Morgado MG, Bello G. 2009. Close phylogenetic relationship between Angolan and Romanian HIV-1 subtype F1 isolates. Retrovirology 6:39.
15. Gunthard HF, Wong JK, Ignacio CC, Havlir DV, Richman DD. 1998. Comparative performance of high-density oligonucleotide sequencing and dideoxynucleotide sequencing of HIV type 1 pol from clinical samples. AIDS Res Hum Retroviruses 14:869-876.
16. Halvas EK, Aldrovandi GM, Balfe P, Beck IA, Boltz VF, Coffin JM, Frenkel LM, Hazelwood JD, Johnson VA, Kearney M, Kovacs A, Kuritzkes DR, Metzner KJ, Nissley DV, Nowicki M, Palmer S, Ziermann R, Zhao RY, Jennings CL, Bremer J, Brambilla D, Mellors JW. 2006. Blinded, multicenter comparison of methods to detect a drug-resistant mutant of human immunodeficiency virus type 1 at low frequency. J Clin Microbiol 44:2612-2614.
17. Hamers RL, Wallis CL, Kityo C, Siwale M, Mandaliya K, Conradie F, Botes ME, Wellington M, Osibogun A, Sigaloff KC, Nankya I, Schuurman R, Wit FW, Stevens WS, van Vugt M, de Wit TF, PharmAccess African Studies to Evaluate Resistance (PASER). 2011. HIV-1 drug resistance in antiretroviral-naive individuals in sub-Saharan Africa after rollout of antiretroviral therapy: A multicentre observational study. Lancet Infect Dis 11:750-759.
18. Hamers RL, Schuurman R, Sigaloff KC, Wallis CL, Kityo C, Siwale M, Mandaliya K, Ive P, Botes ME, Wellington M, Osibogun A, Wit FW, van Vugt M, Stevens WS, de Wit TF, PharmAccess African Studies to Evaluate Resistance (PASER) Investigators. 2012. Effect of pretreatment HIV-1 drug resistance on immunological, virological, and drug-resistance outcomes of first-line antiretroviral treatment in sub-Saharan Africa: A multicentre cohort study. Lancet Infect Dis 12:307-317.
19. Harrison L, Castro H, Cane P, Pillay D, Booth C, Phillips A, Geretti AM, Dunn D, UK Collaborative Group on HIV Drug Resistance, UK Collaborative HIV Cohort Study (UK CHIC). 2010. The effect of transmitted HIV-1 drug resistance on pre-therapy viral load. AIDS 24:1917-1922.
20. Hirsch MS, Günthard HF, Schapiro JM, Brun-Vézinet F, Clotet B, Hammer SM, Johnson VA, Kuritzkes DR, Mellors JW, Pillay D, Yeni PG, Jacobsen DM, Richman DD. 2008. Antiretroviral drug resistance testing in adult HIV-1 infection: 2008 recommendations of an International AIDS Society-USA panel. Clin Infect Dis 47:266-285.
21. Hudson RR, Boos DD, Kaplan NL. 1992. A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138-151.
22. Iversen A, Shafer R, Wehrly K, Winters MA, Mullins JI, Chesebro B, Meriganet TC. 1996. Multidrug-resistant HIV-1 strains resulting from combination antiretroviral therapy. J Virol 70:1086-1090.
23. Johnson VA, Brun-Vezinet F, Clotet B, Gunthard HF, Kuritzkes DR, Pillay D, Schapiro JM, Richman DD. 2007. Update of the drug resistance mutations in HIV-1: 2007. Top HIV Med 15:119-125.
24. Johnson VA, Brun-Vezinet F, Clotet B, Gunthard HF, Kuritzkes DR, Pillay D, Schapiro JM, Richman DD. 2008. Update of the drug resistance mutations in HIV-1. Top HIV Med 16:138-145.
25. Joint United Nations Programme on HIV/AIDS (UNAIDS). 2004. The Changing HIV/AIDS Epidemic in Europe and Central Asia. WHO Library, Geneva, available online at http://data.unaids.org/Publications/IRC-pub06/jc1038-changingepidemic_en.pdf, accessed on September 15, 2012.
26. Kuritzkes DR, Lalama CM, Ribaudo HJ, Marcial M, Meyer WA III, Shikuma C, Johnson VA, Fiscus SA, D'Aquila RT, Schackman BR, Acosta EP, Gulick RM. 2008. Preexisting resistance to nonnucleoside reverse-transcriptase inhibitors predicts virologic failure of an efavirenz-based regimen in treatment-naive HIV-1-infected subjects. J Infect Dis 197:867-870.
27. Lanier E, Ait-Khaled M, Scott J, Stone C, Melby T, Sturge G, St Clair M, Steel H, Hetherington S, Pearce G, Spreen W, Lafon S. 2004. Antiviral efficacy of abacavir in antiretroviral therapy experienced adults harboring HIV-1 with specific patterns of resistance to NRTI. Antivir Ther 9:37-45.
28. Little SJ, Holte S, Routy JP, Daar ES, Markowitz M, Collier AC, Koup RA, Mellors JW, Connick E, Conway B, Kilby M, Wang L, Whitcomb JM, Hellmann NS, Richman DD. 2002. Antiretroviral-drug resistance among patients recently infected with HIV. N Engl J Med 347:385-394.
29. Marcelin AG, Flandre P, Pavie J, Schmidely N, Wirden M, Lada O, Chiche D, Molina JM, Calvez V. 2005. Clinically relevant genotype interpretation of resistance to didanosine. Antimicrob Agents Chemother 49:1739-1744.
30. Martinez-Picado J, Savara AV, Sutton L, D'Aquila RT. 1999. Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1. J Virol 73:3744-3752.
31. Masharsky AE, Dukhovlinova EN, Verevochkin SV, Toussova OV, Skochilov RV, Anderson JA, Hoffman I, Cohen MS, Swanstrom R, Kozlov AP. 2010. A substantial transmission bottleneck among newly and recently HIV-1-infected injection drug users in St Petersburg, Russia. J Infect Dis 201:1697-1702.
32. Montes B, Vergne L, Peeters M, Reynes J, Delaporte E, Segondy M. 2004. Comparison of drug resistance mutations and their interpretation in patients infected with non-B HIV-1 variants and matched patients infected with HIV-1 subtype B. J Acquir Immune Defic Syndr 35:329-336.
33. Paraschiv S, Otelea D, Dinu M, Maxim D, Tinischi M. 2007. Polymorphisms and resistance mutations in the protease and reverse transcriptase genes of HIV-1 F subtype Romanian strains. Int J Infect Dis 11:123-128.
34. Paraschiv S, Otelea D, Batan I, Baicus C, Magiorkinis G, Paraskevis D. 2012. Molecular typing of the recently expanding subtype B HIV-1 epidemic in Romania: Evidence for local spread among MSMs in Bucharest area. Infect Genet Evol 12:1052-1057.
35. Paraskevis D, Nikolopoulos G, Tsiara C, Paraskeva D, Antoniadou A, Lazanas M, Gargalianos P, Psychogiou M, Malliori M, Kremastinou J, Hatzakis A. 2011. HIV-1 outbreak among injecting drug users in Greece, 2011: A preliminary report. Eur Surveill 16:19962.
36. Rhee S, Liu T, Ravela J, Gonzales M, Shafer R. 2004. Distribution of HIV-1 protease and reverse transcriptase mutation patterns in 4, 183 persons undergoing genotypic resistance testing. Antimicrob Agents Chemother 48:3122-3126.
37. Rhee S, Taylor J, Wadhera G, Ben-Hur A, Brutlag D, Shafer R. 2006. Genotypic predictors of HIV-1 drug resistance. Proc Natl Acad Sci USA 103:17355-17360.
38. Rozera G, Abbate I, Ciccozzi M, Presti AL, Bruselles A, Vlassi C, D'Offizi G, Narciso P, Giombini E, Bartolini B, Ippolito G, Capobianchi MR. 2012. Ultra-deep sequencing reveals hidden HIV-1 minority lineages and shifts of viral population between the main cellular reservoirs of the infection after therapy interruption. J Med Virol 84:839-844.
39. Schuurman R, Brambilla D, de Groot T, Huang D, Land S, Bremer J, Benders I, Boucher CA. 2002. Underestimation of HIV type 1 drug resistance mutations: Results from the ENVA-2 genotyping proficiency program. AIDS Res Hum Retroviruses 18:243-248.
40. Shafer RW, Schapiro JM. 2008. HIV-1 drug resistance mutations: An updated framework for the second decade of HAART. AIDS Rev 10:67-84.
41. Shirasaka T, Kavlick MF, Ueno T, Gao WY, Kojima E, Alcaide ML, Chokekijchai S, Roy BM, Arnold E, Yarchoan R. 1995. Emergence of human immunodeficiency virus type 1 variants with resistance to multiple dideoxynucleosides in patients receiving therapy with dideoxynucleosides. Proc Natl Acad Sci USA 92:2398-2402.
42. Slatkin M, Maddison WP. 1989. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 123:603-613.
43. Smith DM, May SJ, Tweeten S, Drumright L, Pacold ME, Kosakovsky Pond SL, Pesano RL, Lie YS, Richman DD, Frost SD, Woelk CH, Little SJ. 2009. A public health model for the molecular surveillance of HIV transmission in San Diego, California. AIDS 23:225-232.
44. Tambuyzer L, Nijs S, Daems B, Picchio G, Vingerhoets J. 2011. Effect of mutations at position E138 in HIV-1 reverse transcriptase on phenotypic susceptibility and virologic response to etravirine. J Acquir Immune Defic Syndr 58:18-22.
45. UK Collaborative Group on HIV Drug Resistance, UK Collaborative HIV Cohort Study, UK Register of HIV Seroconverters. 2007. Evidence of a decline in transmitted HIV-1 drug resistance in the United Kingdom. AIDS 21:1035-1039.
46. Vandamme AM, Camacho RJ, Ceccherini-Silberstein F, De Luca A, Palmisano L, Paraskevis D, Paredes R, Poljak M, Schmit JC, Soriano V, Walter H, Sönnerborg A. 2011. European recommendations for the clinical use of HIV drug resistance testing: 2011 update. AIDS Rev 13:77-108.
47. Vercauteren J, Wensing AM, van de Vijver DA, Albert J, Balotta C, Hamouda O, Kücherer C, Struck D, Schmit JC, Åsjö B, Bruckova M, Camacho R, Clotet B, Coughlan S, Grossman Z, Horban A, Korn K, Kostrikis L, Nielsen C, Paraskevis D, Poljak M, Puchhammer-Stöckl E, Riva C, Ruiz L, Salminen M, Schuurman R, Sonnerborg A, Stanekova D, Stanojevic M, Vandamme AM, Boucher CA. 2009. Transmission of drug-resistant HIV-1 is stabilizing in Europe. J Infect Dis 200:1503-1508.
48. Vergne L, Stuyver L, Van Houtte M, Butel C, Delaporte E, Peeters M. 2006. Natural polymorphism in protease and reverse transcriptase genes and in vitro antiretroviral drug susceptibilities of non-B HIV-1 strains from treatment-naive patients. J Clin Virol 36:43-49.
49. Vermeiren H, Van Craenenbroeck E, Alen P, Bacheler L, Picchio G, Lecocq P. 2007. Prediction of HIV-1 drug susceptibility phenotype from the viral genotype using linear regression modeling. J Virol Methods 145:47-55.
50. Wensing AM, van de Vijver DA, Angarano G, Åsjö 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, Kücherer C, Leitner T, Loveday C, MacRae E, Maljkovic I, de Mendoza C, Meyer J, Nielsen C, Op de Coul EL, Ormaasen V, Paraskevis D, Perrin L, Puchhammer-Stöckl E, Ruiz L, Salminen M, Schmit JC, Schneider F, Schuurman R, Soriano V, Stanczak G, Stanojevic M, Vandamme AM, Van Laethem K, Violin M, Wilbe K, Yerly S, Zazzi M, Boucher CA. 2005. Prevalence of drug-resistant HIV-1 variants in untreated individuals in Europe: Implications for clinical management. J Infect Dis 192:958-966.
51. Wheeler WH, Ziebell RA, Zabina H, Pieniazek D, Prejean J, Bodnar UR, Mahle KC, Heneine W, Johnson JA, Hall HI, Variant, Atypical, and Resistant HIV Surveillance Group. 2010. Prevalence of transmitted drug resistance associated mutations and HIV-1 subtypes in new HIV-1 diagnoses, U.S.-2006. AIDS 24:1203-1212.
52. Whitcomb J, Parkin N, Chappey C, Hellmann N, Petropoulos CJ. 2003. Broad NRTI cross-resistance in HIV-1 clinical isolates. J Infect Dis 188:992-1000.
53. WHO HIV Drug Resistance Report. 2012. Transmitted HIV drug resistance in low- and middle-income countries. WHO Library, Geneva, available online at http://apps.who.int/iris/bitstream/10665/75183/1/9789241503938_eng.pdf, accessed on September 20, 2012.
54. Yahi N, Tamalet C, Tourres C, Tivoli N, Ariasi F, Volot F. 1999. Mutation patterns of reverse transcriptase and protease genes in human immunodeficiency virus type 1 infected patients undergoing combination therapy: Survey of 787 sequences. J Clin Microbiol 37:4099-4106.
55. Yebra G, de Mulder M, Pérez-Elías MJ, Pérez-Molina JA, Galán JC, Llenas-García J, Moreno S, Holguín A. 2011. Increase of transmitted drug resistance among HIV-infected sub-Saharan Africans residing in Spain in contrast to the native population. PLoS ONE 6:e26757.
56. Zetola NM, Pilcher CD. 2007. Diagnosis and management of acute HIV infection. Infect Dis Clin North Am 21:19-48.