Next-generation sequencing to help monitor patients infected with HIV: Ready for clinical use?

Current Infectious Disease Reports

Volumn 16, Issue 4, 2014, Pages

  Gibson, Richard M ^a   Schmotzer, Christine L ^a,b   Quiñones Mateu, Miguel E ^a,b,c  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Coreceptor tropism; Drug resistance; Human immunodeficiency virus (HIV); Minority variants; Next generation sequencing (NGS)

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; ANTIRETROVIRUS AGENT;

ANTIVIRAL SUSCEPTIBILITY; ANTIVIRAL THERAPY; ASSAY; CLINICAL LABORATORY; DEEP SEQUENCING; GENE SEQUENCE; GENOTYPE; GENOTYPING TECHNIQUE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MICROBIAL DIVERSITY; NEXT GENERATION SEQUENCING; PATHOGENESIS; PATIENT MONITORING; PHENOTYPE; REVIEW; VIRAL TROPISM; VIRUS GENE;

EID: 84894483303     PISSN: 15233847     EISSN: 15343146     Source Type: Journal    
DOI: 10.1007/s11908-014-0401-5     Document Type: Review

References (107)

1. Marx JL. Drug-resistant strains of AIDS virus found. Science. 1989;243:1551-2.
2. MacArthur RD. Understanding HIV, phenotypic resistance testing: usefulness in managing treatment-experienced patients. AIDS Rev. 2009;11:223-30.
3. Zolopa AR. The evolution of HIV treatment guidelines: current state-of-the-art of ART. Antiviral Res. 2010;85:241-4.
4. Rose JD, Rhea AM, Weber J, Quinones-Mateu ME. Current tests to evaluate HIV-1 coreceptor tropism. Curr Opin HIV AIDS. 2009;4:136-42.
5. Dunn DT, Coughlin K, Cane PA. Genotypic resistance testing in routine clinical care. Curr Opin HIVAIDS. 2011;6:251-7.
6. Grant PM, Zolopa AR. The use of resistance testing in the management of HIV-1-infected patients. Curr Opin HIV AIDS. 2009;4:474-80.
7. Cunningham S, Ank B, Lewis D, Lu W, Wantman M, Dileanis JA, et al. Performance of the applied biosystems ViroSeq human immunodeficiency virus type 1 (HIV-1) genotyping system for sequence-based analysis of HIV-1 in pediatric plasma samples. J Clin Microbiol. 2001;39:1254-7. (Pubitemid 32275416)
8. Grant RM, Kuritzkes DR, Johnson VA, Mellors JW, Sullivan JL, Swanstrom R, et al. Accuracy of the TRUGENE HIV-1 genotyping kit. J Clin Microbiol. 2003;41:1586-93. (Pubitemid 36428108)
9. Paar C, Palmetshofer C, Flieger K, Geit M, Kaiser R, Stekel H, et al. Genotypic antiretroviral resistance testing for human immunodeficiency virus type 1 integrase inhibitors by use of the TruGene sequencing system. J Clin Microbiol. 2008;46:4087-90.
10. Obermeier M, Symons J, Wensing AM. HIV population genotypic tropism testing and its clinical significance. Curr Opin HIV AIDS. 2012;7:470-7.
11. Poveda E, Alcami J, Paredes R, Cordoba J, Gutierrez F, Llibre JM, et al. Genotypic determination of HIV tropism - clinical and methodological recommendations to guide the therapeutic use of CCR5 antagonists. AIDS Rev. 2010;12:135-48.
12. Larder BA, Kohli A, Kellam P, Kemp SD, Kronick M, Henfrey RD. Quantitative detection of HIV-1 drug resistance mutations by automated DNA sequencing. Nature. 1993;365:671-3.
13. Church JD, Jones D, Flys T, Hoover D, Marlowe N, Chen S, et al. Sensitivity of the ViroSeq HIV-1 genotyping system for detection of the K103N resistance mutation in HIV-1 subtypes A, C, and D. J Mol Diagn: JMD. 2006;8:430-2. quiz 527.
14. Halvas EK, Aldrovandi GM, Balfe P, Beck IA, Boltz VF, Coffin JM, et al. Blinded, multicenter comparison of methods to detect a drug-resistant mutant of human immunodeficiency virus type 1 at low frequency. J Clin Microbiol. 2006;44:2612-4. (Pubitemid 44092442)
15. Leitner T, Halapi E, Scarlatti G, Rossi P, Albert J, Fenyo EM, et al. Analysis of heterogeneous viral populations by direct DNA sequencing. Biotechniques. 1993;15:120-7. (Pubitemid 23202530)
16. Swenson LC, Daumer M, Paredes R. Next-generation sequencing to assess HIV tropism. Curr Opin HIVAIDS. 2012;7:478-85.
17. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, et al. Insights into hominid evolution from the gorilla genome sequence. Nature. 2012;483:169-75.
18. Howden BP, McEvoy CR, Allen DL, Chua K, Gao W, Harrison PF, et al. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog. 2011;7:e1002359.
19. Quan PL, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM, Anthony SJ, et al. Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A. 2013;110:8194-9.
20. • Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, et al. Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol. 2012. An excellent study comparing 454's GS jr., Illumina's MiSeq, and Ion Torrent's PGM.
21. Liu L, Li Y, Li S, Hu N, He Y, Pong R, et al. Comparison of nextgeneration sequencing systems. J Biomed Biotechnol. 2012;2012:251364.
22. Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, et al. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genom. 2012;13:341.
23. Wong LJ. Challenges of bringing next generation sequencing technologies to clinical molecular diagnostic laboratories. Neurother: J Am Soc Exp Neurother. 2013;10:262-72.
24. Gullapalli RR, Lyons-Weiler M, Petrosko P, Dhir R, Becich MJ, LaFramboise WA. Clinical integration of next-generation sequencing technology. Clin Lab Med. 2012;32:585-99.
25. • Avidor B, Girshengorn S, Matus N, Talio H, Achsanov S, Zeldis I, et al. Evaluation of a benchtop HIV ultradeep pyrosequencing drug resistance assay in the clinical laboratory. J Clin Microbiol. 2013;51:880-6. Description of an HIV-1 genotyping assay based on the 454 GS Jr. platform.
26. Chang MW, Oliveira G, Yuan J, Okulicz JF, Levy S, Torbett BE. Rapid deep sequencing of patient-derived HIV with ion semiconductor technology. J Virol Methods. 2013;189:232-4.
27. Dudley DM, Chin EN, Bimber BN, Sanabani SS, Tarosso LF, Costa PR, et al. Low-cost ultra-wide genotyping using Roche/454 pyrosequencing for surveillance of HIV drug resistance. PloS One. 2012;7:e36494.
28. Messiaen P, Verhofstede C, Vandenbroucke I, Dinakis S, Van Eygen V, Thys K, et al. Ultra-deep sequencing of HIV-1 reverse transcriptase before start of an NNRTI-based regimen in treatment-naive patients. Virology. 2012;426:7-11.
29. Armenia D, Vandenbroucke I, Fabeni L, Van Marck H, Cento V, D'Arrigo R, et al. Study of genotypic and phenotypic HIV-1 dynamics of integrase mutations during raltegravir treatment: a refined analysis by ultra-deep 454 pyrosequencing. J Infect Dis. 2012;205:557-67.
30. Mukherjee R, Jensen ST, Male F, Bittinger K, Hodinka RL, Miller MD, et al. Switching between raltegravir resistance pathways analyzed by deep sequencing. AIDS. 1951-1959;2011:25.
31. Simen BB, Simons JF, Hullsiek KH, Novak RM, Macarthur RD, Baxter JD, et al. Low-abundance drug-resistant viral variants in chronically-HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J Infect Dis. 2009;199:693-701.
32. Liu J, Miller MD, Danovich RM, Vandergrift N, Cai F, Hicks CB, et al. Analysis of low-frequency mutations associated with drug resistance to raltegravir before antiretroviral treatment. Antimicrob Agents Chemother. 2011;55:1114-9.
33. ShaoW, Boltz VF, Spindler JE, Kearney MF, Maldarelli F, Mellors JW, et al. Analysis of 454 sequencing error rate, error sources, and artifact recombination for detection of Low-frequency drug resistance mutations in HIV-1 DNA. Retrovirology. 2013;10:18.
34. •• Gibson RM, Meyer AM, Winner D, Archer J, Feyertag F, Robertson DL, et al. Characterization and validation of a deep sequencing-based HIV-1 genotypic and coreceptor tropism assay to simultaneously monitor susceptibility to maturation, protease, reverse transcriptase, and integrase inhibitors, and CCR5 antagonists. Antivir Ther. 2013;18:A43. Original description of the first all-inclusive HIV-1 genotyping and coreceptor tropism assay based on deep sequencing.
35. Swenson LC, Mo T, Dong WW, Zhong X, Woods CK, Thielen A, et al. Deep V3 sequencing for HIV type 1 tropism in treatmentnaive patients: a reanalysis of the MERIT trial of maraviroc. Clin Infect Dis: Off Publ Infect Dis Soc Am. 2011;53:732-42.
36. • Swenson LC, Mo T, Dong WW, Zhong X, Woods CK, Jensen MA, et al. Deep sequencing to infer HIV-1 co-receptor usage: application to three clinical trials of maraviroc in treatment-experienced patients. J Infect Dis. 2011;203:237-45. Excellent study describing the use of an deep sequencing-based HIV-1 coreceptor tropism test in the clinical setting.
37. Saliou A, Delobel P, Dubois M, Nicot F, Raymond S, Calvez V, et al. Concordance between two phenotypic assays and ultradeep pyrosequencing for determining HIV-1 tropism. Antimicrob Agents Chemother. 2011;55:2831-6.
38. Kagan RM, Johnson EP, Siaw MF, Van Baelen B, Ogden R, Platt JL, et al. Comparison of genotypic and phenotypic HIV Type 1 tropism assay: results from the screening samples of cenicriviroc study 202, a randomized phase II trial in treatment-naive subjects. AIDS Res Hum Retrovir. 2013;29.
39. • Kagan RM, Johnson EP, Siaw M, Biswas P, Chapman DS, Su Z, et al. A genotypic test for HIV-1 tropism combining Sanger sequencing with ultradeep sequencing predicts virologic response in treatment-experienced patients. PloS One. 2012;7:e46334. Description of a commercial HIV-1 coreceptor tropism assay based on deep sequencing.
40. • Archer J, Weber J, Henry K, Winner D, Gibson R, Lee L, et al. Use of Four Next-Generation Sequencing Platforms to Determine HIV-1 Coreceptor Tropism. PloS One. 2012;7:e49602. First study comparing all fourdeep sequencing technologies (454, Illumina, Ion Torrent, and Pacific Biosciences) to quantify HIV-1 coreceptor tropism.
41. Swenson LC, Moores A, Low AJ, Thielen A, Dong W, Woods C, et al. Improved detection of CXCR4-using HIV by V3 genotyping: application of population-based and "deep" sequencing to plasma RNA and proviral DNA. J Acquir Immune Defic Syndr. 2010;54:506-10.
42. Archer J, Braverman MS, Taillon BE, Desany B, James I, Harrigan PR, et al. Detection of low-frequency pretherapy chemokine (CXCmotif) receptor 4 (CXCR4)-using HIV-1 with ultradeep pyrosequencing. AIDS. 2009;23:1209-18.
43. Vandenbroucke I, Van Marck H, Mostmans W, Van Eygen V, Rondelez E, Thys K, et al. HIV-1 V3 envelope deep sequencing for clinical plasma specimens failing in phenotypic tropism assays. AIDS Res Ther. 2010;7:4.
44. Archer J, Rambaut A, Taillon BE, Harrigan PR, Lewis M, Robertson DL. The evolutionary analysis of emerging low frequency HIV-1 CXCR4 using variants through time-an ultra-deep approach. PLoS Comput Biol. 2010;6:e1001022.
45. Raymond S, Saliou A, Nicot F, Delobel P, Dubois M, Cazabat M, et al. Frequency of CXCR4-using viruses in primary HIV-1 infections using ultra-deep pyrosequencing. AIDS. 2011;25:1668-70.
46. Abbate I, Vlassi C, Rozera G, Bruselles A, Bartolini B, Giombini E, et al. Detection of quasispecies variants predicted to use CXCR4 by ultra-deep pyrosequencing during early HIVinfection. AIDS. 2011;25:611-7.
47. Lee GQ, Harrigan PR, Dong W, Poon AF, Heera J, Demarest J, et al. Comparison of population and 454 "deep" sequence analysis for HIV type 1 tropism versus the original trofile assay in non-B subtypes. AIDS Res Hum Retrovir. 2013;29:979-84.
48. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, Wang C, et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science. 2011;333:1593-602.
49. Henn MR, Boutwell CL, Charlebois P, Lennon NJ, Power KA, Macalalad AR, et al. Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection. PLoS Pathog. 2012;8:e1002529.
50. Raymond S, Delobel P, Izopet J. Phenotyping methods for determining HIV tropism and applications in clinical settings. Curr Opin HIVAIDS. 2012;7:463-9.
51. Japour AJ, Mayers DL, Johnson VA, Kuritzkes DR, Beckett LA, Arduino JM, et al. Standardized peripheral blood mononuclear cell culture assay for determination of drug susceptibilities of clinical human immunodeficiency virus type 1 isolates. The RV-43 Study Group, the AIDS Clinical Trials Group Virology Committee Resistance Working Group. Antimicrob Agents Chemother. 1993;37:1095-101. (Pubitemid 23141326)
52. Hertogs K, de Bethune MP, Miller V, Ivens T, Schel P, Van Cauwenberge A, et al. A rapid method for simultaneous detection of phenotypic resistance to inhibitors of protease and reverse transcriptase in recombinant human immunodeficiency virus type 1 isolates from patients treated with antiretroviral drugs. Antimicrob Agents Chemother. 1998;42:269-76. (Pubitemid 28114430)
53. Kellam P, Larder BA. Recombinant virus assay: a rapid, phenotypic assay for assessment of drug susceptibility of human immunodeficiency virus type 1 isolates. Antimicrob Agents Chemother. 1994;38:23-30. (Pubitemid 24018152)
54. Petropoulos CJ, Parkin NT, Limoli KL, Lie YS, Wrin T, Huang W, et al. A novel phenotypic drug susceptibility assay for human immunodeficiency virus type 1. Antimicrob Agents Chemother. 2000;44:920-8. (Pubitemid 30165271)
55. Weber J, Vazquez AC, Winner D, Rose JD, Wylie D, Rhea AM, et al. Novel method for simultaneous quantification of phenotypic resistance to maturation, protease, reverse transcriptase, and integrase HIV inhibitors based on 3?Gag(p2/p7/p1/p6)/PR/RT/ INT-recombinant viruses: a useful tool in the multitarget era of antiretroviral therapy. Antimicrob Agents Chemother. 2011;55:3729-42.
56. Meyerhans A, Cheynler R, Albert J, Seth M, Kwok S, Sninsky J, et al. Temporal Fluctuations in HIV Quasispecies In Vivo Are Not Reflected by Sequential HIV Isolations. Cell. 1989;58:901-10. (Pubitemid 19227898)
57. Race E, Dam E, Obry V, Paulous S, Clavel F. Analysis of HIV cross-resistance to protease inhibitors using a rapid single-cycle recombinant virus assay for patients failing on combination therapies. AIDS. 1999;13:2061-8. (Pubitemid 29509582)
58. Paredes R, Clotet B. Clinical management of HIV-1 resistance. Antiviral Res. 2010;85:245-65.
59. Shafer RW. Rationale and uses of a public HIV drug-resistance database. J Infect Dis. 2006;194 Suppl 1:S51-58. (Pubitemid 44420873)
60. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, et al. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC- CKR-5. Nature. 1996;381:667-73. (Pubitemid 26197680)
61. Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science. 1996;272:872-7. (Pubitemid 26154590)
62. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996;381:661-6. (Pubitemid 26197679)
63. Dorr P, Westby M, Dobbs S, Griffin P, Irvine B, Macartney M, et al. Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob Agents Chemother. 2005;49:4721-32. (Pubitemid 41552605)
64. Poveda E, Briz V, Quinones-Mateu M, Soriano V. HIV tropism: diagnostic tools and implications for disease progression and treatment with entry inhibitors. AIDS. 2006;20:1359-67. (Pubitemid 43948242)
65. Weber J, Piontkivska H, Quinones-Mateu ME. HIV type 1 tropism and inhibitors of viral entry: clinical implications. AIDS Rev. 2006;8:60-77. (Pubitemid 44043555)
66. Trouplin V, Salvatori F, Cappello F, Obry V, Brelot A, Heveker N, et al. Determination of coreceptor usage of human immunodeficiency virus type 1 from patient plasma samples by using a recombinant phenotypic assay. J Virol. 2001;75:251-9.
67. Whitcomb JM, Huang W, Fransen S, Limoli K, Toma J, Wrin T, et al. Development and characterization of a novel single-cycle recombinantvirus assay to determine human immunodeficiency virus type 1 coreceptor tropism. Antimicrob Agents Chemother. 2007;51:566-75. (Pubitemid 46185274)
68. Raymond S, Delobel P, Mavigner M, Cazabat M, Souyris C, Encinas S, et al. Development and performance of a new recombinant virus phenotypic entry assay to determine HIV-1 coreceptor usage. J Clin Virol: Off Publ Pan Am Soc Clin Virol. 2010;47:126-30.
69. Holland AU, Munk C, Lucero GR, Nguyen LD, Landau NR. Alpha- complementation assay for HIV envelope glycoprotein-mediated fusion. Virology. 2004;319:343-52. (Pubitemid 38251274)
70. Grund S, Klein A, Adams O. Expression plasmids are only useful for the investigation of co-receptor tropism and fusion capacity of short HIV-1 envelope domains. J Virol Methods. 2010;166:106-9.
71. Weber J, Vazquez AC, Winner D, Gibson RM, Rhea AM, Rose JD, et al. Sensitive Cell-based Assay to Determine Human Immunodeficiency Virus Type 1 Coreceptor Tropism. J Clin Microbiol. 2013;51:1517-27.
72. Sing T, Low AJ, Beerenwinkel N, Sander O, Cheung PK, Domingues FS, et al. Predicting HIV coreceptor usage on the basis of genetic and clinical covariates. Antivir Ther. 2007;12:1097-106. (Pubitemid 350114990)
73. Jensen MA, Li FS, van't Wout AB, Nickle DC, Shriner D, He HX, et al. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J Virol. 2003;77:13376-88. (Pubitemid 37494331)
74. Cardozo T, Kimura T, Philpott S, Weiser B, Burger H, Zolla- Pazner S. Structural basis for coreceptor selectivity by the HIV type 1 V3 loop. AIDS Res Hum Retrovir. 2007;23:415-26. (Pubitemid 46608562)
75. Rosen O, Sharon M, Quadt-Akabayov SR, Anglister J. Molecular switch for alternative conformations of the HIV-1 V3 region: implications for phenotype conversion. Proc Natl Acad Sci U S A. 2006;103:13950-5. (Pubitemid 44452963)
76. Reeves JD, Coakley E, Petropoulos CJ, Whitcomb JM. An Enhanced-Sensitivity Trofile™ HIV Coreceptor Tropism Assay for Selecting Patients for Therapy with Entry Inhibitors Targeting CCR5: A Review of Analytical and Clinical Studies. J Viral Entry. 2009;3:94-102.
77. Metzker ML. Sequencing technologies - the next generation. Nat Rev Genet. 2010;11:31-46.
78. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, et al. Genome sequencing in microfabricated highdensity picolitre reactors. Nature. 2005;437:376-80. (Pubitemid 41613494)
79. Bennett S. Solexa Ltd. Pharmacogenomics. 2004;5:433-8. (Pubitemid 38923657)
80. Rothberg JM, Hinz W, Rearick TM, Schultz J, Mileski W, Davey M, et al. An integrated semiconductor device enabling non-optical genome sequencing. Nature. 2011;475:348-52.
81. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, et al. Real-time DNA sequencing from single polymerase molecules. Science. 2009;323:133-8.
82. Howorka S, Cheley S, Bayley H. Sequence-specific detection of individual DNA strands using engineered nanopores. Nat Biotechnol. 2001;19:636-9. (Pubitemid 32625433)
83. Quinones-Mateu ME, Albright JL, Mas A, Soriano V, Arts EJ. Analysis of pol gene heterogeneity, viral quasispecies, and drug resistance in individuals infected with group O strains of human immunodeficiency virus type 1. J Virol. 1998;72:9002-15. (Pubitemid 28471844)
84. Willerth SM, Pedro HA, Pachter L, Humeau LM, Arkin AP, Schaffer DV. Development of a low bias method for characterizing viral populations using next generation sequencing technology. PloS One. 2010;5:e13564.
85. Eriksson N, Pachter L, Mitsuya Y, Rhee SY, Wang C, Gharizadeh B, et al. Viral population estimation using pyrosequencing. PLoS Comput Biol. 2008;4:e1000074.
86. Poon AF, Swenson LC, Dong WW, Deng W, Kosakovsky Pond SL, Brumme ZL, et al. Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of HIV-1. Mol Biol Evol. 2010;27:819-32.
87. Redd AD, Quinn TC, Tobian AA. Frequency and implications of HIV superinfection. Lancet Infect Dis. 2013;13:622-8.
88. Fisher R, van Zyl GU, Travers SA, Kosakovsky Pond SL, Engelbrech S, Murrell B, et al. Deep sequencing reveals minor protease resistance mutations in patients failing a protease inhibitor regimen. J Virol. 2012;86:6231-7.
89. Wang C, Mitsuya Y, Gharizadeh B, Ronaghi M, Shafer RW. Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res. 2007;17:1195-201. (Pubitemid 47204863)
90. Stelzl E, Proll J, Bizon B, Niklas N, Danzer M, Hackl C, et al. Human immunodeficiency virus type 1 drug resistance testing: Evaluation of a new ultra-deep sequencing-based protocol and comparison with the TRUGENE HIV-1 Genotyping Kit. J Virol Methods. 2011;178:94-7.
91. Lataillade M, Chiarella J, Yang R, DeGrosky M, Uy J, Seekins D, et al. Virologic failures on initial boosted-PI regimen infrequently possess low-level variants with major PI resistance mutations by ultra-deep sequencing. PloS One. 2012;7:e30118.
92. Nicot F, Saliou A, Raymond S, Saune K, Dubois M, Massip P, et al. Minority variants associated with resistance to HIV-1 nonnucleoside reverse transcriptase inhibitors during primary infection. J Clin Virol: Off Publ Pan Am Soc Clin Virol. 2012;55:107-13.
93. D'Aquila RT, Geretti AM, Horton JH, Rouse E, Kheshti A, Raffanti S, et al. Tenofovir (TDF)-selected or abacavir (ABC)-selected low-frequency HIV type 1 subpopulations during failure with persistent viremia as detected by ultradeep pyrosequencing. AIDS Res Hum Retrovir. 2011;27:201-9.
94. Bellecave P, Recordon-Pinson P, Papuchon J, Vandenhende MA, Reigadas S, Tauzin B, et al. Detection of low-frequency HIV Type 1 reverse transcriptase drug resistance mutations by Ultradeep Sequencing in Naive HIV Type 1-Infected individuals. AIDS Res Hum Retrovir. 2013.
95. •• Li JZ, Kuritzkes DR. Clinical implications of HIV-1 minority variants. Clin Infect Dis: Off Publ Infect Dis Soc Am. 2013;56: 1667-74. Excellent article that analyses the potential use of deep sequencing HIV-1 assays in the clinical setting.
96. Li JZ, Paredes R, Ribaudo HJ, Svarovskaia ES, Metzner KJ, Kozal MJ, et al. Low-frequency HIV-1 drug resistance mutations and risk of NNRTI-based antiretroviral treatment failure: a systematic review and pooled analysis. JAMA: J Am Med Assoc. 2011;305:1327-35.
97. Stekler JD, Ellis GM, Carlsson J, Eilers B, Holte S, Maenza J, et al. Prevalence and impact of minority variant drug resistance mutations in primary HIV-1 infection. PloS One. 2011;6:e28952.
98. Li JZ, Paredes R, Ribaudo HJ, Kozal MJ, Svarovskaia ES, Johnson JA, et al. Impact of minority nonnucleoside reverse transcriptase inhibitor resistance mutations on resistance genotype after virologic failure. J Infect Dis. 2013;207:893-7.
99. Li JZ, Paredes R, Ribaudo HJ, Svarovskaia ES, Kozal MJ, Hullsiek KH, et al. Relationship between minority nonnucleoside reverse transcriptase inhibitor resistance mutations, adherence, and the risk of virologic failure. AIDS. 2012;26:185-92.
100. Codoner FM, Pou C, Thielen A, Garcia F, Delgado R, Dalmau D, et al. Added value of deep sequencing relative to population sequencing in heavily pre-treated HIV-1-infected subjects. PloS One. 2011;6:e19461.
101. Gonzalez S, Tully DC, Gondwe C, Wood C. Low-abundance resistant mutations in HIV-1 subtype C antiretroviral therapy-naive individuals as revealed by pyrosequencing. Curr HIV Res. 2013;11:43-9.
102. Bunnik EM, Swenson LC, Edo-Matas D, Huang W, Dong W, Frantzell A, et al. Detection of inferred CCR5- and CXCR4-using HIV-1 variants and evolutionary intermediates using ultra-deep pyrosequencing. PLoS Pathog. 2011;7:e1002106.
103. Rozera G, Abbate I, Bruselles A, Vlassi C, D'Offizi G, Narciso P, et al. Archived HIV-1 minority variants detected by ultra-deep pyrosequencing in provirus may be fully replication competent. AIDS. 2009;23:2541-3.
104. Gonzalez-Serna A, McGovern RA, Harrigan PR, Vidal F, Poon AF, Ferrando-Martinez S, et al. Correlation of the virological response to short-term maraviroc monotherapy with standard and deep-sequencing-based genotypic tropism prediction methods. Antimicrob Agents Chemother. 2012;56:1202-7.
105. Raymond S, Recordon-Pinson P, Saliou A, Delobel P, Nicot F, Descamps D, et al. Improved V3 genotyping with duplicate PCR amplification for determining HIV-1 tropism. J Antimicrob Chemother. 2011;66:1972-5.
106. Van HM, Picchio G, Van der Borght K, Pattery T, Lecocq P, Bacheler LT. A comparison of HIV-1 drug susceptibility as provided by conventional phenotyping and by a phenotype prediction tool based on viral genotype. J Med Virol. 2009;81:1702-9.
107. Gonzalez-Serna A, Leal M, Genebat M, Abad MA, Garcia-Perganeda A, Ferrando-Martinez S, et al. TROCAI (tropism coreceptor assay information): a new phenotypic tropism test and its correlation with Trofile enhanced sensitivity and genotypic approaches. J Clin Microbiol. 2010;48:4453-8.