The implications of whole-genome sequencing in the control of tuberculosis

Therapeutic Advances in Infectious Disease

Volumn 3, Issue 2, 2015, Pages 47-62

  Lee, Robyn S ^a   Behr, Marcel A ^b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

clinical microbiology; diagnostics; drug resistance; Mycobacterium tuberculosis; whole genome sequencing

Indexed keywords

AMIKACIN; AMINOGLYCOSIDE; CAPREOMYCIN; ETHAMBUTOL; ETHIONAMIDE; ISONIAZID; KANAMYCIN; LEVOFLOXACIN; MOXIFLOXACIN; PYRAZINAMIDE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; DRUG SENSITIVITY; GENE MUTATION; HUMAN; META ANALYSIS (TOPIC); MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEQUENCE ANALYSIS; TUBERCULOSIS; WHOLE GENOME SEQUENCING;

EID: 85016095250     PISSN: 20499361     EISSN: 2049937X     Source Type: Journal    
DOI: 10.1177/2049936115624630     Document Type: Review

References (87)

1. S.AltschulW.GishW.MillerE.MyersD.Lipman (1990) Basic local alignment search tool. J Mol Biol215: 403–410.
2. G.AlvarezD.Van DykM.DesjardinsA.YasseenIIIS.AaronD.Cameron (2015) The feasibility, accuracy, and impact of Xpert MTB/RIF testing in a remote aboriginal community in Canada. Chest148: 767–773.
3. M.BehrS.WarrenH.SalamonP.HopewellA.Ponce de LeonC.Daley (1999) Transmission of Mycobacterium tuberculosis from patients smear-negative for acid-fast bacilli. Lancet353: 444–449.
4. C.BoehmeP.NabetaD.HillemannM.NicolS.ShenaiF.Krapp (2010) Rapid molecular detection of tuberculosis and rifampin resistance. N Engl J Med363: 1005–1015.
5. A.BrownJ.BryantK.Einer-JensenJ.HoldstockD.HounietJ.Chan (2015) Rapid whole-genome sequencing of Mycobacterium tuberculosis isolates directly from clinical samples. J Clin Microbiol53: 2230–2237.
6. J.BryantA.SchurchH.van DeutekomS.HarrisJ.de BeerV.de Jager (2013) Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis13: 110.
7. E.CarpentierB.DrouillardM.DaillouxD.MoinardE.ValleeB.Dutilh (1995) Diagnosis of tuberculosis by Amplicor Mycobacterium-Tuberculosis Test - a multicenter study. J Clin Microbiol33: 3106–3110.
8. N.CasaliV.NikolayevskyyY.BalabanovaS.HarrisO.IgnatyevaI.Kontsevaya (2014) Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat Genet46: 279–286.
9. Centers for Disease Control and Prevention (CDC) (2009) Updated guidelines for the use of Nucleic Acid Amplification Tests in the diagnosis of tuberculosis. MMWR Morb Mortal Wkly Rep58: 7–10.
10. S.ChengZ.CuiY.LiZ.Hu (2014) Diagnostic accuracy of a molecular drug susceptibility testing method for the antituberculosis drug ethambutol: a systematic review and meta-analysis. J Clin Microbiol52: 2913–2924.
11. V.ChihotaA.GrantK.FieldingB.NdibongoA.van ZylD.Muirhead (2010) Liquid versus solid culture for tuberculosis: performance and cost in a resource-constrained setting. Int J Tuberc Lung Dis14: 1024–1031.
12. Clinical and Laboratory Standards Institute. (2014) Nucleic acid sequencing methods in diagnostic laboratory medicine; Approved guideline - second edition. CLSI document MM09-A2. Clinical and Laboratory Standards Institute: Wayne, PA
13. S.ColeR.BroschJ.ParkhillT.GarnierC.ChurcherD.Harris (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature393: 537–544.
14. F.CollR.McNerneyM.PrestonJ.Afonso Guerra-AssuncaoA.WarryG.Hill-Cawthorne (2015) Rapid determination of anti-tuberculosis drug resistance from whole-genome sequences. Genome Med7: 51.
15. I.ComasJ.ChakravarttiP.SmallJ.GalaganS.NiemannK.Kremer (2010) Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat Genet42: 498–503.
16. A.DemersS.VerverA.BoulleR.WarrenP.van HeldenM.Behr (2012) High yield of culture-based diagnosis in a TB-endemic setting. BMC Infect Dis12: 218.
17. C.DenkingerS.SchumacherC.BoehmeN.DendukuriM.PaiK.Steingart (2014) Xpert MTB/RIF Assay for the diagnosis of extrapulmonary tuberculosis: a systematic review and meta-analysis. Eur Respir J44: 435–446.
18. E.DoughtyM.SergeantI.AdetifaM.AntonioM.Pallen (2014) Culture-independent detection and characterisation of Mycobacterium tuberculosis and M. Africanum in sputum samples using shotgun metagenomics on a benchtop sequencer. Peer J2(3): e585. DOI: 10.7717/peerj.585/supp-3.
19. F.DrobniewskiV.NikolayevskyyH.MaxeinerY.BalabanovaN.CasaliI.Kontsevaya (2013) Rapid diagnostics of tuberculosis and drug resistance in the industrialized world: clinical and public health benefits and barriers to implementation. BMC Med11: 190.
20. M.FadzilahK.Peng NgY.Fong Ngeow (2009) The manual MGIT system for the detection of M. tuberculosis in respiratory specimens: an experience in the University Malaya Medical Centre. Malay J Pathol31: 93–97.
21. M.FarhatB.ShapiroK.KieserR.SultanaK.JacobsonT.Victor (2013) Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat Genet45: 1183–1189.
22. S.FeuerriegelV.SchleusenerP.BeckertT.KohlP.MiottoD.Cirillo (2015) PhyResSE: a web tool delineating Mycobacterium tuberculosis antibiotic resistance and lineage from whole-genome sequencing data. J Clin Microbiol53: 1908–1914.
23. J.FlandroisG.LinaO.Dumitrescu (2014) MUBII-TB-DB: a database of mutations associated with antibiotic resistance in Mycobacterium tuberculosis. BMC Bioinform15: 107.
24. J.GardyJ.JohnstonS.Ho SuiV.CookL.ShahE.Brodkin (2011) Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med364: 730–739.
25. J.Guerra-AssuncaoA.CrampinR.Houben (2015) Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. Elife4: e05166.
26. S.HarrisM.TorokE.CartwrightM.QuailS.PeacockJ.Parkhill (2013) Read and assembly metrics inconsequential for clinical utility of whole-genome sequencing in mapping outbreaks. Nat Biotechnol31: 592–594.
27. Heather, J. and Chan, B. (2015) The sequence of sequencers: The history of sequencing DNA. Genomics DOI: 10.1016/j.ygeno.2015.11.003
28. D.HewlettD.HornC.Alfalla (1995) Drug-resistant tuberculosis: Inconsistent results of pyrazinamide susceptibility testing. JAMA273: 916–917.
29. D.HorneL.PintoM.ArentzS.LinE.DesmondL.Flores (2013) Diagnostic accuracy and reproducibility of WHO-endorsed phenotypic drug susceptibility testing methods for first-line and second-line antituberculosis drugs. J Clin Microbiol51: 393–401.
30. S.IchiyamaY.IinumaS.YamoriY.HasegawaK.SimokataN.Nakashima (1997) Mycobacterium growth indicator tube testing in conjunction with the AccuProbe or the AMPLICOR-PCR assay for detecting and identifying mycobacteria from sputum samples. J Clin Microbiol35: 2022–2025.
31. M.JainI.FiddesK.MigaH.OlsenB.PatenM.Akeson (2015) Improved data analysis for the MinION Nanopore sequencer. Nat Meth12: 351–356.
32. F.JamiesonJ.GuthrieA.NeemuchwalaO.LastovetskaR.MelanoC.Mehaffy (2014a) Profiling of rpoB mutations and MICs for rifampin and rifabutin in Mycobacterium tuberculosis. J Clin Microbiol52: 2157–2162.
33. F.JamiesonS.TeateroJ.L.GuthrieA.NeemuchwalaN.FittipaldiC.Mehaffy (2014b) Whole-genome sequencing of the Mycobacterium tuberculosis Manila sublineage results in less clustering and better resolution than Mycobacterial Interspersed Repetitive-Unit-Variable-Number Tandem-Repeat (MIRU-VNTR) typing and spoligotyping. J Clin Microbiol52: 3795–3798.
34. M.Kato-MaedaC.HoB.PassarelliN.BanaeiJ.GrinsdaleL.Flores (2013) Use of whole genome sequencing to determine the microevolution of Mycobacterium tuberculosis during an outbreak. PLoS One8(3): e58235.
35. C.KöserM.HoldenM.EllingtonE.CartwrightN.BrownA.Ogilvy-Stuart (2012) Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med366: 2267–2275.
36. J.KwongN.McCallumV.SintchenkoB.Howden (2015) Whole genome sequencing in clinical and public health microbiology. Pathology47: 199–210.
37. E.LanderM.Waterman (1988) Genomic mapping by fingerprinting random clones: a mathematical analysis. Genomics2: 231–239.
38. T.LaverJ.HarrisonP.O’NeillK.MooreA.FarbosK.Paszkiewicz (2015) Assessing the performance of the Oxford Nanopore technologies MinIon. Biomol Detect Quantif3: 1–8.
39. R.LeeN.RadomskiJ.ProulxJ.ManryF.McIntoshF.Desjardins (2015) Reemergence and amplification of tuberculosis in the Canadian arctic. J Infect Dis211: 1905–1914.
40. D.LingA.ZwerlingM.Pai (2008) GenoType MTBDR assays for the diagnosis of multidrug-resistant tuberculosis: a meta-analysis. Eur Respir J32: 1165–1174.
41. N.LomanC.ConstantinidouJ.ChanM.HalachevM.SergeantC.Penn (2012a) High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat Rev Microbiol10: 599–606.
42. N.LomanR.MisraT.DallmanC.ConstantinidouS.GharbiaJ.Wain (2012b) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol30: 434–439.
43. S.LongS.BeresR.OlsenJ.Musser (2014) Absence of patient-to-patient intrahospital transmission of Staphylococcus aureus as determined by whole-genome sequencing. mBio5(5): e01692–e1714.
44. L.Maynard-SmithN.LarkeJ.PetersS.Lawn (2014) Diagnostic accuracy of the Xpert MTB/RIF assay for extrapulmonary and pulmonary tuberculosis when testing non-respiratory samples: a systematic review. BMC Infect Dis14: 709.
45. G.MiglioriA.MatteelliD.CirilloM.Pai (2008) Diagnosis of multidrug-resistant tuberculosis and extensively drug-resistant tuberculosis: current standards and challenges. Can J Infect Dis Med Microbiol19: 169–172.
46. A.MikheyevM.Tin (2014) A first look at the Oxford Nanopore MinION Sequencer. Mol Ecol Resour14: 1097–1102.
47. B.Molina-MoyaA.LacomaC.PratJ.DiazA.DudnykL.Haba (2015) AID TB Resistance line probe assay for rapid detection of resistant Mycobacterium tuberculosis in clinical samples. J Infect70: 400–408.
48. M.MorganS.KalantriL.FloresM.Pai (2005) A commercial line probe assay for the rapid detection of rifampicin resistance in Mycobacterium tuberculosis: a systematic review and meta-analysis. BMC Infect Dis5(1): 62.
49. H.Nebenzahl-GuimaraesK.JacobsonM.FarhatM.Murray (2014) Systematic review of allelic exchange experiments aimed at identifying mutations that confer drug resistance in Mycobacterium tuberculosis. J Antimicrobial Chemother69: 331–342.
50. K.NoorL.ShephardI.Bastian (2015) Molecular diagnostics for tuberculosis. Pathology47: 250–256.
51. O.OcheretinaL.ShenV.EscuyerM.MabouG.Royal-MardiS.Collins (2015) Whole genome sequencing investigation of a tuberculosis outbreak in Port-Au-Prince, Haiti caused by a strain with a ‘Low-Level’ rpoB mutation L511P – insights into a mechanism of resistance escalation. PLoS One10(6): e0129207.
52. N.OlsonS.LundR.ColmanJ.FosterJ.SahlJ.Schupp (2015) Best practices for evaluating single nucleotide variant calling methods for microbial genomics. Front Genet6: 235.
53. S.PabingerA.DanderM.FischerR.SnajderM.SperkM.Efremova (2014) A survey of tools for variant analysis of next-generation genome sequencing data. Brief Bioinform15: 256–278.
54. M.ParkA.DavisN.SchlugerH.CohenW.Rom (1996) Outcome of MDR-TB patients, 1983–1993 - prolonged survival with appropriate therapy. Am J Respir Crit Care Med153: 317–324.
55. N.ParrishK.Carroll (2008) Importance of improved TB diagnostics in addressing the extensively drug-resistant TB crisis. Future Microbiol3: 405–413.
56. N.ParrishK.Carroll (2011) Role of the clinical mycobacteriology laboratory in diagnosis and management of tuberculosis in low-prevalence settings. J Clin Microbiol49: 772–776.
57. M.PerkinsJ.Cunningham (2007) Facing the crisis: improving the diagnosis of tuberculosis in the HIV era. J Infect Dis196(Suppl. 1): S15–S27.
58. J.PriceT.GolubchikK.ColeD.WilsonD.CrookG.Thwaites (2014) Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus in an intensive care unit. Clin Infect Dis58: 609–618.
59. Public Health Agency of Canada (2015) Tuberculosis: Drug resistance in Canada. 2013, Ottawa (Canada): Minister of Public Works and Government Services Canada.
60. J.QuickN.CumleyC.WearnM.NiebelC.ConstantinidouC.Thomas (2014) Seeking the source of Pseudomonas aeruginosa infections in a recently opened hospital: an observational study using whole-genome sequencing. BMJ Open4: e006278.
61. J.QuickP.AshtonS.CalusC.ChattS.GossainJ.Hawker (2015) Rapid draft sequencing and real-time Nanopore sequencing in a hospital outbreak of Salmonella. Genome Biol16: 114.
62. C.RitterK.LuckeF.SirgelR.WarrenP.van HeldenE.Bottger (2014) Evaluation of the AID TB Resistance line probe assay for rapid detection of genetic alterations associated with drug resistance in Mycobacterium tuberculosis strains. J Clin Microbiol52: 940–946.
63. A.RoetzerR.DielT.KohlC.RückertU.NübelJ.Blom (2013) Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med10(2): e1001387.
64. E.Sanchez-PadillaM.MerkerP.BeckertF.JochimsT.DiaminiP.Kahn (2015) Detection of drug-resistant tuberculosis by Xpert MTB/RIF in Swaziland. N Engl J Med372: 1181–1182.
65. A.SandgrenM.StrongP.MuthukrishnanB.WeinerG.ChurchM.Murray (2009) Tuberculosis drug resistance mutation database. PLoS Med6(2): e1000002.
66. A.SchurchK.KremerO.DavienaA.KiersM.BoereeR.Siezen (2010) High-resolution typing by integration of genome sequencing data in a large tuberculosis cluster. J Clin Microbiol48: 3403–3406.
67. N.SegataL.WaldronA.BallariniV.NarasimhanO.JoussonC.Huttenhower (2012) Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Meth9: 811–814.
68. D.SenGuptaL.CummingsD.HoogestraatS.Butler-WuJ.ShendureB.Cookson (2014) Whole-genome sequencing for high-resolution investigation of methicillin-resistant Staphylococcus aureus epidemiology and genome plasticity. J Clin Microbiol52: 2787–2796.
69. E.SnitkinA.ZelaznyP.ThomasF.StockNISC Comparative Sequencing Program GroupD.Henderson (2012) Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med4(148): 148ra116.
70. H.SohnA.AeroD.MenziesM.BehrK.SchwartzmanG.Alvarez (2014) Xpert MTB/RIF testing in a low tuberculosis incidence, high-resource setting: limitations in accuracy and clinical impact. Clin Infect Dis58: 970–976.
71. A.SteinerD.StuckiM.CoscollaS.BorellS.Gagneux (2014) KvarQ: targeted and direct variant calling from fastq reads of bacterial genomes. BMC Genom15: 881.
72. K.SteingartI.SchillerD.HorneM.PaiC.BoehmeN.Dendukuri (2014) Xpert® MTB/RIF assay for pulmonary tuberculosis and rifampicin resistance in adults (review). Cochrane Libr1: 1–168.
73. K.SteingartM.HenryV.NgP.HopewellA.RamsayJ.CunninghamR.Urbanczik (2006a) Fluorescence versus conventional sputum smear microscopy for tuberculosis: a systematic review. Lancet Infect Dis6: 570–581.
74. K.SteingartV.NgM.HenryP.HopewellA.RamsayJ.CunninghamR.Urbanczik (2006b) Sputum processing methods to improve the sensitivity of smear microscopy for tuberculosis: a systematic review. Lancet Infect Dis6: 664–674.
75. D.StuckiM.BallifT.BodmerM.CoscollaA.MaurerS.Droz (2015) Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis211: 1306–1316.
76. G.TheronJ.PeterM.RichardsonM.BarnardS.DoneganR.Warren (2014a) The diagnostic accuracy of the GenoType MTBDRsl assay for the detection of resistance to second-line anti-tuberculosis drugs (review). Cochrane Libr10: 1–123.
77. G.TheronL.ZijenahD.ChandaP.ClowesA.RachowM.Lesosky (2014b) Feasibility, accuracy, and clinical effect of point-of-care XpertMTB/RIF testing for tuberculosis in primary care settings in Africa: a multicentre, randomised, controlled trial. Lancet383: 424–435.
78. H.ThorvaldsdottirJ.RobinsonJ.Mesirov (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform14: 178–192.
79. M.TorokS.ReuterJ.BryantC.KoserS.StinchcombeB.Nazareth (2013) Rapid whole-genome sequencing for investigation of a suspected tuberculosis outbreak. J Clin Microbiol51: 611–614.
80. A.TraunerS.BorrellK.ReitherS.Gagneux (2014) Evolution of drug resistance in tuberculosis: recent progress and implications for diagnosis and therapy. Drugs74: 1063–1072.
81. P.VuorinenA.MiettinenR.VuentoO.Hallstrom (1995) Direct detection of Mycobacterium tuberculosis complex in respiratory specimens by Gen-Probe Amplified Mycobacterium tuberculosis Direct Test and Roche Amplicor Mycobacterium Tuberculosis Test. J Clin Microbiol33: 1856–1859.
82. T.WalkerC.IpR.HarrellJ.EvansG.KapataiM.Dedicoat (2013) Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis13: 137–146.
83. T.WalkerT.KohlS.OmarJ.HedgeC.Del Ojo EliasP.Bradley (2015) Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis15: 1193–1202.
84. A.WitneyK.GouldA.ArnoldD.ColemanR.DelgadoJ.Dhillon (2015) Clinical application of whole-genome sequencing to inform treatment for multidrug-resistant tuberculosis cases. J Clin Microbiol53: 1473–1483.
85. D.WoodS.Salzberg (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol15(3): R46.
86. World Health Organization (2015) Global Tuberculosis Report 2014, Geneva: World Health Organization.
87. N.ZetolaS.ShinK.TumediK.MoetiR.NcubeM.Nicol (2014) Mixed Mycobacterium tuberculosis complex infections and false-negative results for rifampin resistance by GeneXpert MTB/RIF are associated with poor clinical outcomes. J Clin Microbiol52: 2422–2429.