Detection of minority resistance during early HIV-1 infection: Natural variation and spurious detection rather than transmission and evolution of multiple viral variants

Journal of Virology

Volumn 85, Issue 16, 2011, Pages 8359-8367

  Gianella, Sara ^a   Delport, Wayne ^a   Pacold, Mary E ^a   Young, Jason A ^a   Choi, Jun Yong ^c   Little, Susan J ^a   Richman, Douglas D ^a,b   Kosakovsky Pond, Sergei L ^a   Smith, Davey M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABACAVIR PLUS AMPRENAVIR PLUS LAMIVUDINE PLUS RITONAVIR PLUS STAVUDINE; ABACAVIR PLUS EFAVIRENZ PLUS LAMIVUDINE; ABACAVIR PLUS FOSAMPRENAVIR PLUS LAMIVUDINE PLUS RETONAVIR; ABACAVIR PLUS LAMIVUDINE PLUS LOPINAVIR PLUS RITONAVIR PLUS ZIDOVUDINE; ANTIRETROVIRUS AGENT; ATAZANAVIR PLUS LAMIVUDINE PLUS RITONAVIR PLUS STAVUDINE; EFAVIRENZ PLUS EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; EFAVIRENZ PLUS LAMIVUDINE PLUS STAVUDINE PLUS TENOFOVIR; EFAVIRENZ PLUS LAMIVUDINE PLUS ZIDOVUDINE; EMTRICITABINE PLUS RITONAVIR PLUS TENOFOVIR PLUS ZIDOVUDINE; INDINAVIR PLUS LAMIVUDINE PLUS ZIDOVUDINE; LAMIVUDINE PLUS NELFINAVIR PLUS ZIDOVUDINE; LAMIVUDINE PLUS RITONAVIR PLUS SAQUINAVIR PLUS ZIDOVUDINE; LAMIVUDINE PLUS RITONAVIR PLUS TENOFOVIR PLUS ZIDOVUDINE; UNCLASSIFIED DRUG;

ACESSORY MUTATION; ADULT; ANALYTICAL ERROR; ANTIVIRAL RESISTANCE; ANTIVIRAL THERAPY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG RESISTANT MUTATION; DRUG TREATMENT FAILURE; ENVELOPE GENE; FEMALE; GENE MUTATION; GENETIC VARIABILITY; GROUP SPECIFIC ANTIGEN GENE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MALE; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STRUCTURAL GENE; ULTRADEEP SEQUENCING; VIRUS GENE; VIRUS TRANSMISSION;

ADULT; ANTI-HIV AGENTS; BASE SEQUENCE; DRUG RESISTANCE, VIRAL; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENES, ENV; GENES, GAG; GENES, POL; GENETIC VARIATION; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; TREATMENT OUTCOME;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79960717109     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02582-10     Document Type: Article

References (77)

1. Abrahams, M. R., et al. 2009. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-Poisson distribution of transmitted variants. J. Virol. 83:3556-3567.
2. Aghokeng, A. F., et al. 2010. Frequency of antiretroviral resistance mutations among ART-naive HIV-1-infected populations in rural areas from Cameroon, 2010. Antivir. Ther. 15(Suppl. 2):A151.
3. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19:716-723.
4. Anisimova, M., and C. Kosiol. 2009. Investigating protein-coding sequence evolution with probabilistic codon substitution models. Mol. Biol. Evol. 26:255-271.
5. Bacheler, L., et al. 2001. Genotypic correlates of phenotypic resistance to efavirenz in virus isolates from patients failing nonnucleoside reverse transcriptase inhibitor therapy. J. Virol. 75:4999-5008.
6. Balzarini, J., H. Pelemans, R. Esnouf, and E. De Clercq. 1998. A novel mutation (F227L) arises in the reverse transcriptase of human immunodeficiency virus type 1 on dose-escalating treatment of HIV type 1-infected cell cultures with the nonnucleoside reverse transcriptase inhibitor thiocarboxanilide UC-781. AIDS Res. Hum. Retroviruses 14:255-260.
7. Bar, K. J., et al. 2010. Wide variation in the multiplicity of HIV-1 infection among injection drug users. J. Virol. 84:6241-6247.
8. Butler, D. M., M. E. Pacold, P. S. Jordan, D. D. Richman, and D. M. Smith. 2009. The efficiency of single genome amplification and sequencing is improved by quantitation and use of a bioinformatics tool. J. Virol. Methods 162:280-283.
9. Coffin, J. M. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
10. Cummings, S. M., M. McMullan, D. A. Joyce, and C. van Oosterhout. 2010. Solutions for PCR, cloning and sequencing errors in population genetic analysis. Conserv. Genet. 11:1095-1097.
11. Delaugerre, C., et al. 2001. Prevalence and conditions of selection of E44D/A and V118I human immunodeficiency virus type 1 reverse transcriptase mutations in clinical practice. Antimicrob. Agents Chemother. 45:946-948.
12. Delport, W., A. F. Poon, S. D. Frost, and S. L. Kosakovsky Pond. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455-2457.
13. Delport, W., K. Scheffler, and C. Seoighe. 2009. Models of coding sequence evolution. Brief. Bioinform. 10:97-109.
14. Diakite, M., et al. 2010. High prevalence of transmitted drug resistance in HIV-1-infected antiretroviral-naive patients from Conakry, Guinea-Conakry. Antivir. Ther. 15(Suppl. 2):A149.
15. Ellis, G. M., L. C. Page, B. E. Burman, S. Buskin, and L. M. Frenkel. 2009. Increased detection of HIV-1 drug resistance at time of diagnosis by testing viral DNA with a sensitive assay. J. Acquir. Immune Defic. Syndr. 51:283-289.
16. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186-194.
17. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
18. Fiebig, E. W., et al. 2003. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 17:1871-1879.
19. Fischer, W., et al. 2010. Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 5:e12303.
20. X2 from contingency tables, and the calculation of P. J. R. Stat. Soc. 85:87-94.
21. Geretti, A. M., et al. 2009. Low-frequency K103N strengthens the impact of transmitted drug resistance on virologic responses to first-line efavirenz or nevirapine-based highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 52:569-573.
22. Gianella, S., and D. D. Richman. 2010. Minority variants of drug-resistant HIV. J. Infect. Dis. 202:657-666.
23. Gonzales, M. J., et al. 2003. Extended spectrum of HIV-1 reverse transcriptase mutations in patients receiving multiple nucleoside analog inhibitors. AIDS 17:791-799.
24. Goodman, D. D., et al. 2011. Low level of the K103N HIV-1 above a threshold is associated with virological failure in treatment-naive individuals undergoing efavirenz-containing therapy. AIDS 25:325-333.
25. Haaland, R. E., et al. 2009. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 5:e1000274.
26. Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
27. Hecht, F. M., et al. 2006. A multicenter observational study of the potential benefits of initiating combination antiretroviral therapy during acute HIV infection. J. Infect. Dis. 194:725-733.
28. Hertogs, K., et al. 2000. A novel human immunodeficiency virus type 1 reverse transcriptase mutational pattern confers phenotypic lamivudine resistance in the absence of mutation 184V. Antimicrob. Agents Chemother. 44:568-573.
29. Huse, S. M., J. A. Huber, H. G. Morrison, M. L. Sogin, and D. M. Welch. 2007. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 8:R143.
30. Jakobsen, M. R., et al. 2010. Transmission of HIV-1 drug-resistant variants: prevalence and effect on treatment outcome. Clin. Infect. Dis. 50:566-573.
31. Johnson, J. A., et al. 2007. Simple PCR assays improve the sensitivity of HIV-1 subtype B drug resistance testing and allow linking of resistance mutations. PLoS One 2:e638.
32. Johnson, J. A., et al. 2008. Minority HIV-1 drug resistance mutations are present in antiretroviral treatment-naive populations and associate with reduced treatment efficacy. PLoS Med. 5:e158.
33. Keele, B. F., et al. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557.
34. Kosakovsky Pond, S. L., and S. D. Frost. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22:1208-1222.
35. Kosakovsky Pond, S. L., et al. 2009. An evolutionary model-based algorithm for accurate phylogenetic breakpoint mapping and subtype prediction in HIV-1. PLoS Comput. Biol. 5:e1000581.
36. Kuritzkes, D. R., et al. 2008. Preexisting resistance to nonnucleoside reversetranscriptase inhibitors predicts virologic failure of an efavirenz-based regimen in treatment-naive HIV-1-infected subjects. J. Infect. Dis. 197:867-870.
37. Lataillade, M., et al. 2010. Prevalence and clinical significance of HIV drug resistance mutations by ultra-deep sequencing in antiretroviral-naive subjects in the CASTLE study. PLoS One 5:e10952.
38. Lee, H. Y., et al. 2009. Modeling sequence evolution in acute HIV-1 infection. J. Theor. Biol. 261:341-360.
39. Li, H., et al. 2010. High multiplicity infection by HIV-1 in men who have sex with men. PLoS Pathog. 6:e1000890.
40. Li, J. Z., et al. 2011. Low-frequency HIV-1 drug resistance mutations and risk of NNRTI-based antiretroviral treatment failure: a systematic review and pooled analysis. JAMA 305:1327-1335.
41. Liao, L., et al. 2010. The prevalence of transmitted antiretroviral drug resistance in treatment-naive HIV-infected individuals in China. J. Acquir. Immune Defic. Syndr. 53(Suppl. 1):S10-S4.
42. Little, S. J., et al. 2008. Persistence of transmitted drug resistance among subjects with primary human immunodeficiency virus infection. J. Virol. 82:5510-5518.
43. Little, S. J., et al. 2002. Antiretroviral-drug resistance among patients recently infected with HIV. N. Engl. J. Med. 347:385-394.
44. Margulies, M., et al. 2005. Genome sequencing in microfabricated highdensity picolitre reactors. Nature 437:376-380.
45. Metzner, K. J., et al. 2003. Emergence of minor populations of human immunodeficiency virus type 1 carrying the M184V and L90M mutations in subjects undergoing structured treatment interruptions. J. Infect. Dis. 188: 1433-1443.
46. Metzner, K. J., et al. 2009. Minority quasispecies of drug-resistant HIV-1 that lead to early therapy failure in treatment-naive and -adherent patients. Clin. Infect. Dis. 48:239-247.
47. Metzner, K. J., et al. 2010. Efficient suppression of minority quasispecies of drug-resistant viruses present at primary HIV-1 infection by RTV-boostered protease inhibitor containing ART. J. Infect. Dis. 201:1063-1071.
48. Metzner, K. J., et al. 2005. Detection of minor populations of drug-resistant HIV-1 in acute seroconverters. AIDS 19:1819-1825.
49. Montes, B., and M. Segondy. 2002. Prevalence of the mutational pattern E44D/A and/or V118I in the reverse transcriptase (RT) gene of HIV-1 in relation to treatment with nucleoside analogue RT inhibitors. J. Med. Virol. 66:299-303.
50. Nijhuis, M., S. Deeks, and C. Boucher. 2001. Implications of antiretroviral resistance on viral fitness. Curr. Opin. Infect. Dis. 14:23-28.
51. Nzeyimana, S. D., et al. 2010. Monitoring of HIV-1 drug resistance and associated programmatic factors in patients initiating antiretroviral therapy at two ART sites in Bujumbura, Burundi. Antivir. Ther. 15(Suppl. 2):A153.
52. Pacold, M., et al. 2010. Comparison of methods to detect HIV dual infection. AIDS Res. Hum. Retroviruses 26:1291-1298.
53. Palmer, S., et al. 2006. Selection and persistence of non-nucleoside reverse transcriptase inhibitor-resistant HIV-1 in patients starting and stopping nonnucleoside therapy. AIDS 20:701-710.
54. Paredes, R., V. C. Marconi, T. B. Campbell, and D. R. Kuritzkes. 2007. Systematic evaluation of allele-specific real-time PCR for the detection of minor HIV-1 variants with pol and env resistance mutations. J. Virol. Methods 146:136-146.
55. Paredes, R., et al. 2010. Pre-existing minority drug-resistant HIV-1 variants, adherence, and risk of antiretroviral failure. J. Infect. Dis. 201:662-671.
56. Parkin, N. T., S. Gupta, C. Chappey, and C. J. Petropoulos. 2006. The K101P and K103R/V179D mutations in human immunodeficiency virus type 1 reverse transcriptase confer resistance to nonnucleoside reverse transcriptase inhibitors. Antimicrob. Agents Chemother. 50:351-354.
57. Pelemans, H., et al. 1997. Characteristics of the Pro225His mutation in human immunodeficiency virus type 1 (HIV-1) reverse transcriptase that appears under selective pressure of dose-escalating quinoxaline treatment of HIV-1. J. Virol. 71:8195-8203.
58. Peuchant, O., et al. 2008. Transmission of HIV-1 minority-resistant variants and response to first-line antiretroviral therapy. AIDS 22:1417-1423.
59. Pillay, D., et al. 2006. The impact of transmitted drug resistance on the natural history of HIV infection and response to first-line therapy. AIDS 20:21-28.
60. Pond, S. L., and S. D. Frost. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533.
61. Poon, A. F., et al. 2010. Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of HIV-1. Mol. Biol. Evol. 27:819-832.
62. Rhee, S. Y., et al. 2006. Genotypic predictors of human immunodeficiency virus type 1 drug resistance. Proc. Natl. Acad. Sci. U. S. A. 103:17355-17360.
63. Simen, B. B., et al. 2009. Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J. Infect. Dis. 199:693-701.
64. Simon, V., et al. 2002. Evolving patterns of HIV-1 resistance to antiretroviral agents in newly infected individuals. AIDS 16:1511-1519.
65. Toni, T. A., et al. 2009. Detection of human immunodeficiency virus (HIV) type 1 M184V and K103N minority variants in patients with primary HIV infection. Antimicrob. Agents Chemother. 53:1670-1672.
66. Van Laethem, K., et al. 2007. No response to first-line tenofovi lamivudine efavirenz despite optimization according to baseline resistance testing: impact of resistant minority variants on efficacy of low genetic barrier drugs. J. Clin. Virol. 39:43-47.
67. Varghese, V., et al. 2009. Minority variants associated with transmitted and acquired HIV-1 nonnucleoside reverse transcriptase inhibitor resistance: implications for the use of second-generation nonnucleoside reverse transcriptase inhibitors. J. Acquir. Immune Defic. Syndr. 52:309-315.
68. Varghese, V., et al. 2010. Nucleic acid template and the risk of a PCRinduced HIV-1 drug resistance mutation. PLoS One 5:e10992.
69. Vercauteren, J., et al. 2009. Transmission of drug-resistant HIV-1 is stabilizing in Europe. J. Infect. Dis. 200:1503-1508.
70. Vingerhoets, J., et al. 2005. TMC125 displays a high genetic barrier to the development of resistance: evidence from in vitro selection experiments. J. Virol. 79:12773-12782.
71. Violin, M., et al. 2004. Risk of failure in patients with 215 HIV-1 revertants starting their first thymidine analog-containing highly active antiretroviral therapy. AIDS 18:227-235.
72. Wang, C., Y. Mitsuya, B. Gharizadeh, M. Ronaghi, and R. W. Shafer. 2007. Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res. 17:1195-1201.
73. Wang, G. P., S. A. Sherrill-Mix, K. M. Chang, C. Quince, and F. D. Bushman. 2010. Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J. Virol. 84:6218-6228.
74. Yang, Z., W. S. Wong, and R. Nielsen. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107-1118.
75. Yap, S. H., et al. 2007. N348I in the connection domain of HIV-1 reverse transcriptase confers zidovudine and nevirapine resistance. PLoS Med. 4:e335.
76. Yerly, S., et al. 2007. Transmission of HIV-1 drug resistance in Switzerland: a 10-year molecular epidemiology survey. AIDS 21:2223-2229.
77. Zagordi, O., L. Geyrhofer, V. Roth, and N. Beerenwinkel. 2010. Deep sequencing of a genetically heterogeneous sample: local haplotype reconstruction and read error correction. J. Comput. Biol. 17:417-428.