Low abundance drug resistance variants in transmitted HIV drug resistance surveillance specimens identified using tagged pooled pyrosequencing

Journal of Virological Methods

Volumn 187, Issue 2, 2013, Pages 314-320

  Ji, Hezhao ^a   Liang, Ben ^b   Li, Yang ^a   Van Domselaar, Gary ^b   Graham, Morag ^a   Tyler, Shaun ^a   Merks, Harriet ^a   Sandstrom, Paul ^a   Brooks, James ^a  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

HIV 1; Sanger sequencing; Surveillance; Tagged pooled pyrosequencing; Transmitted drug resistance

Indexed keywords

POL PROTEIN;

ACCURACY; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENOTYPING TECHNIQUE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERMETHOD COMPARISON; MAJOR CLINICAL STUDY; MOLECULAR PHYLOGENY; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PRIORITY JOURNAL; PYROSEQUENCING; QUANTITATIVE ANALYSIS; RELIABILITY; SEQUENCE ANALYSIS; STRUCTURAL GENE; SYSTEMATIC ERROR; VIRAL GENETICS; VIRUS IDENTIFICATION;

DRUG RESISTANCE, VIRAL; GENOTYPE; HIV; HIV INFECTIONS; HUMANS; MUTATION, MISSENSE; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SERUM;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84872687694     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2012.10.018     Document Type: Article

References (40)

1. Andersson A.F., Lindberg M., Jakobsson H., Backhed F., Nyren P., Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 2008, 3:e2836.
2. Bartlett J.A., DeMasi R., Quinn J., Moxham C., Rousseau F. Overview of the effectiveness of triple combination therapy in antiretroviral-naive HIV-1 infected adults. AIDS 2001, 15:1369-1377.
3. Beck I.A., Mahalanabis M., Pepper G., Wright A., Hamilton S., Langston E., Frenkel L.M. Rapid and sensitive oligonucleotide ligation assay for detection of mutations in human immunodeficiency virus type 1 associated with high-level resistance to protease inhibitors. J. Clin. Microbiol. 2002, 40:1413-1419.
4. Bennett D.E. The requirement for surveillance of HIV drug resistance within antiretroviral rollout in the developing world. Curr. Opin. Infect. Dis. 2006, 19:607-614.
5. Bennett D.E., Bertagnolio S., Sutherland D., Gilks C.F. The World Health Organization's global strategy for prevention and assessment of HIV drug resistance. Antivir. Ther. 2008, 13(Suppl. 2):1-13.
6. Bennett D.E., Camacho R.J., Otelea D., Kuritzkes D.R., Fleury H., Kiuchi M., Heneine W., Kantor R., Jordan M.R., Schapiro J.M., Vandamme A.M., Sandstrom P., Boucher C.A., van d.V., Rhee S.Y., Liu T.F., Pillay D., Shafer R.W. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS ONE 2009, 4:e4724.
7. Bennett D.E., Myatt M., Bertagnolio S., Sutherland D., Gilks C.F. Recommendations for surveillance of transmitted HIV drug resistance in countries scaling up antiretroviral treatment. Antivir. Ther. 2008, 13(Suppl. 2):25-36.
8. Boltz V.F., Zheng Y., Lockman S., Hong F., Halvas E.K., McIntyre J., Currier J.S., Chibowa M.C., Kanyama C., Nair A., Owino-Ong'or W., Hughes M., Coffin J.M., Mellors J.W. Role of low-frequency HIV-1 variants in failure of nevirapine-containing antiviral therapy in women previously exposed to single-dose nevirapine. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9202-9207.
9. Booth C.L., Geretti A.M. Prevalence and determinants of transmitted antiretroviral drug resistance in HIV-1 infection. J. Antimicrob. Chemother. 2007, 59:1047-1056.
10. Burger D.M., van d.V., Koopmans P.P. Highly active antiretroviral therapy for HIV infection: lessons for the future. Neth. J. Med. 2004, 62:407-408.
11. De L.A., Cozzi-Lepri A., Perno C.F., Balotta C., Di G.S., Poggio A., Pagano G., Tositti G., Piscopo R., Del F.A., Chiodo F., Magnani G., d'Arminio M.A. Variability in the interpretation of transmitted genotypic HIV-1 drug resistance and prediction of virological outcomes of the initial HAART by distinct systems. Antivir. Ther. 2004, 9:743-752.
12. Demeter L.M., D'Aquila R., Weislow O., Lorenzo E., Erice A., Fitzgibbon J., Shafer R., Richman D., Howard T.M., Zhao Y., Fisher E., Huang D., Mayers D., Sylvester S., Arens M., Sannerud K., Rasheed S., Johnson V., Kuritzkes D., Reichelderfer P., Japour A. Interlaboratory concordance of DNA sequence analysis to detect reverse transcriptase mutations in HIV-1 proviral DNA. ACTG Sequencing Working Group. AIDS Clinical Trials Group. J. Virol. Methods. 1998, 75:93-104.
13. Dudley D.M., Chin E.N., Bimber B.N., Sanabani S.S., Tarosso L.F., Costa P.R., Sauer M.M., Kallas E.G., 'Connor D.H. Low-cost ultra-wide genotyping using Roche/454 pyrosequencing for surveillance of HIV drug resistance. PLoS ONE 2012, 7:e36494.
14. Gianella S., Richman D.D. Minority variants of drug-resistant HIV. J. Infect. Dis. 2010, 202:657-666.
15. Halvas E.K., Wiegand A., Boltz V.F., Kearney M., Nissley D., Wantman M., Hammer S.M., Palmer S., Vaida F., Coffin J.M., Mellors J.W. Low frequency nonnucleoside reverse-transcriptase inhibitor-resistant variants contribute to failure of efavirenz-containing regimens in treatment-experienced patients. J. Infect. Dis. 2010, 201:672-680.
16. Hoffmann C., Minkah N., Leipzig J., Wang G., Arens M.Q., Tebas P., Bushman F.D. DNA bar coding and pyrosequencing to identify rare HIV drug resistance mutations. Nucleic Acids Res. 2007, 35:e91.
17. Ji H., Li Y., Graham M., Liang B.B., Pilon R., Tyson S., Peters G., Tyler S., Merks H., Bertagnolio S., Soto-Ramirez L., Sandstrom P., Brooks J. Next-generation sequencing of dried blood spot specimens: a novel approach to HIV drug-resistance surveillance. Antivir. Ther. 2011, 16:871-878.
18. Ji H., Masse N., Tyler S., Liang B., Li Y., Merks H., Graham M., Sandstrom P., Brooks J. HIV drug resistance surveillance using pooled pyrosequencing. PLoS ONE 2010, 5:e9263.
19. Johnson J.A., Li J.F., Wei X., Lipscomb J., Bennett D., Brant A., Cong M.E., Spira T., Shafer R.W., Heneine W. Simple PCR assays improve the sensitivity of HIV-1 subtype B drug resistance testing and allow linking of resistance mutations. PLoS ONE 2007, 2:e638.
20. Johnson J.A., Li J.F., Wei X., Lipscomb J., Irlbeck D., Craig C., Smith A., Bennett D.E., Monsour M., Sandstrom P., Lanier E.R., Heneine W. Minority HIV-1 drug resistance mutations are present in antiretroviral treatment-naive populations and associate with reduced treatment efficacy. PLoS Med. 2008, 5:e158.
21. Larder B.A., Kellam P., Kemp S.D. Zidovudine resistance predicted by direct detection of mutations in DNA from HIV-infected lymphocytes. AIDS 1991, 5:137-144.
22. Margulies M., Egholm M., Altman W.E., Attiya S., Bader J.S., Bemben L.A., Berka J., Braverman M.S., Chen Y.J., Chen Z., Dewell S.B., Du L., Fierro J.M., Gomes X.V., Godwin B.C., He W., Helgesen S., Ho C.H., Irzyk G.P., Jando S.C., Alenquer M.L., Jarvie T.P., Jirage K.B., Kim J.B., Knight J.R., Lanza J.R., Leamon J.H., Lefkowitz S.M., Lei M., Li J., Lohman K.L., Lu H., Makhijani V.B., McDade K.E., McKenna M.P., Myers E.W., Nickerson E., Nobile J.R., Plant R., Puc B.P., Ronan M.T., Roth G.T., Sarkis G.J., Simons J.F., Simpson J.W., Srinivasan M., Tartaro K.R., Tomasz A., Vogt K.A., Volkmer G.A., Wang S.H., Wang Y., Weiner M.P., Yu P., Begley R.F., Rothberg J.M. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380.
23. Metzner K.J., Bonhoeffer S., Fischer M., Karanicolas R., Allers K., Joos B., Weber R., Hirschel B., Kostrikis L.G., Gunthard H.F. 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. 2003, 188:1433-1443.
24. Metzner K.J., Giulieri S.G., Knoepfel S.A., Rauch P., Burgisser P., Yerly S., Gunthard H.F., Cavassini M. Minority quasispecies of drug-resistant HIV-1 that lead to early therapy failure in treatment-naive and -adherent patients. Clin. Infect. Dis. 2009, 48:239-247.
25. Metzner K.J., Rauch P., Walter H., Boesecke C., Zollner B., Jessen H., Schewe K., Fenske S., Gellermann H., Stellbrink H.J. Detection of minor populations of drug-resistant HIV-1 in acute seroconverters. AIDS 2005, 19:1819-1825.
26. Oette M., Kaiser R., Daumer M., Petch R., Fatkenheuer G., Carls H., Rockstroh J.K., Schmaloer D., Stechel J., Feldt T., Pfister H., Haussinger D. Primary HIV drug resistance and efficacy of first-line antiretroviral therapy guided by resistance testing. J. Acquir. Immune Defic. Syndr. 2006, 41:573-581.
27. Palella F.J., Delaney K.M., Moorman A.C., Loveless M.O., Fuhrer J., Satten G.A., Aschman D.J., Holmberg S.D. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl. J. Med. 1998, 338:853-860.
28. Paredes R., Lalama C.M., Ribaudo H.J., Schackman B.R., Shikuma C., Giguel F., Meyer W.A., Johnson V.A., Fiscus S.A., D'Aquila R.T., Gulick R.M., Kuritzkes D.R. Pre-existing minority drug-resistant HIV-1 variants, adherence, and risk of antiretroviral treatment failure. J. Infect. Dis. 2010, 201:662-671.
29. Rozera G., Abbate I., Bruselles A., Vlassi C., D'Offizi G., Narciso P., Chillemi G., Prosperi M., Ippolito G., Capobianchi M.R. Massively parallel pyrosequencing highlights minority variants in the HIV-1 env quasispecies deriving from lymphomonocyte sub-populations. Retrovirology 2009, 6:15. Public Health Agency of Canada. HIV-1 Strain and Primary Drug Resistance in Canada: Surveillance Report to March 31, 2005. Public Health Agency of Canada. 2006. Surveillance and Risk Assessment Division; Center for Infectious Disease Prevention and Control; Public Health Agency of Canada.
30. Schuurman R., Demeter L., Reichelderfer P., Tijnagel J., de G.T., Boucher C. Worldwide evaluation of DNA sequencing approaches for identification of drug resistance mutations in the human immunodeficiency virus type 1 reverse transcriptase. J. Clin. Microbiol. 1999, 37:2291-2296.
31. Shendure J., Ji H. Next-generation DNA sequencing. Nat. Biotechnol. 2008, 26:1135-1145.
32. Simen B.B., Simons J.F., Hullsiek K.H., Novak R.M., Macarthur R.D., Baxter J.D., Huang C., Lubeski C., Turenchalk G.S., Braverman M.S., Desany B., Rothberg J.M., Egholm M., Kozal M.J. 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.
33. Sequencing Technical Bulletin No. 005-2009. Using Multiplex Identifier (MID) Adaptors for the GS FLX Titanium Chemistry-Extended MID Set. 2009.
34. Sequencing Technical Bulletin No. 013-2009. Amplicon Fusion Primer Design Guidelines for GS FLX Titanium Series Lib-A Chemistry. 2009.
35. UNAIDS. AIDS epidemic update-December 2009. 2010.
36. van d.V., Boucher C.A. The risk of HIV drug resistance following implementation of pre-exposure prophylaxis. Curr. Opin. Infect. Dis. 2010, 23:621-627.
37. Van L.K., De L.A., Antinori A., Cingolani A., Perna C.F., Vandamme A.M. A genotypic drug resistance interpretation algorithm that significantly predicts therapy response in HIV-1-infected patients. Antivir. Ther. 2002, 7:123-129.
38. Walensky R.P., Paltiel A.D., Losina E., Mercincavage L.M., Schackman B.R., Sax P.E., Weinstein M.C., Freedberg K.A. The survival benefits of AIDS treatment in the United States. J. Infect. Dis. 2006, 194:11-19.
39. Wang C., Mitsuya Y., Gharizadeh B., Ronaghi M., Shafer R.W. Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res. 2007, 17:1195-1201.
40. Zhang H., DiBaise J.K., Zuccolo A., Kudrna D., Braidotti M., Yu Y., Parameswaran P., Crowell M.D., Wing R., Rittmann B.E., Krajmalnik-Brown R. Human gut microbiota in obesity and after gastric bypass. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2365-2370.