Rapid whole-genome sequencing of mycobacterium tuberculosis isolates directly from clinical samples

Journal of Clinical Microbiology

Volumn 53, Issue 7, 2015, Pages 2230-2237

  Brown, Amanda C ^a,i   Bryant, Josephine M ^b   Einer Jensen, Katja ^c   Holdstock, Jolyon ^a   Houniet, Darren T ^a   Chan, Jacqueline Z M ^a   Depledge, Daniel P ^b   Nikolayevskyy, Vladyslav ^d   Broda, Agnieszka ^d   Stone, Madeline J ^e   Christiansen, Mette T ^b   Williams, Rachel ^b   McAndrew, Michael B ^a   Tutill, Helena ^b   Brown, Julianne ^b   Melzer, Mark ^f   Rosmarin, Caryn ^f   McHugh, Timothy D ^g   Shorten, Robert J ^g,h   Drobniewski, Francis ^d   Speight, Graham ^a   Breuer, Judith ^b   more..

^a OXFORD GENE TECHNOLOGY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Qiagen AAR   (Denmark)

^d HPA National Mycobacterium Reference Laboratory   (United Kingdom)

^e WEXHAM PARK HOSPITAL   (United Kingdom)

^f BARTS HEALTH NHS TRUST   (United Kingdom)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h MANCHESTER ROYAL INFIRMARY   (United Kingdom)

ⁱ Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMINOSALICYLIC ACID; ANTOFLOXACIN; BACTERIAL DNA; CAPREOMYCIN; ETHAMBUTOL; ETHIONAMIDE; ISONIAZID; KANAMYCIN; PROTIONAMIDE; PYRAZINAMIDE; RIFAMPICIN; STREPTOMYCIN;

ACCURACY; ALLELE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL MUTATION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CONTROLLED STUDY; DRUG RESISTANT TUBERCULOSIS; ENRICHMENT CULTURE; GENE SEQUENCE; GENOTYPE; HUMAN; LITHUANIA; LUNG TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPUTUM ANALYSIS; SPUTUM SMEAR; UNITED KINGDOM; WHOLE GENOME SEQUENCING; DNA SEQUENCE; DRUG EFFECTS; GENETICS; GENOTYPING TECHNIQUE; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PROCEDURES; SPECIMEN HANDLING; SPUTUM; TIME FACTOR; TUBERCULOSIS, PULMONARY;

MYCOBACTERIUM TUBERCULOSIS;

BACTERIOLOGICAL TECHNIQUES; DRUG RESISTANCE, BACTERIAL; GENOTYPING TECHNIQUES; HUMANS; LITHUANIA; MYCOBACTERIUM TUBERCULOSIS; SEQUENCE ANALYSIS, DNA; SPECIMEN HANDLING; SPUTUM; TIME FACTORS; TUBERCULOSIS, PULMONARY; UNITED KINGDOM;

EID: 84932650992     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00486-15     Document Type: Article

References (34)

1. Gandhi NR, Nunn P, Dheda K, Schaaf HS, Zignol M, van Soolingen D, Jensen P, Bayona J. 2010. Multidrug-resistant and extensively drug-resistant tuberculosis: a threat to global control of tuberculosis. Lancet 375:1830-1843. http://dx.doi.org/10.1016/S0140-6736(10)60410-2.
2. Weyer K, Mirzayev F, Migliori GB, Van Gemert W, D'Ambrosio L, Zignol M, Floyd K, Centis R, Cirillo DM, Tortoli E, Gilpin C, de Dieu Iragena J, Falzon D, Raviglione M. 2013. Rapid molecular TB diagnosis: evidence, policy making and global implementation of Xpert MTB/RIF. Eur Respir J 42:252-271. http://dx.doi.org/10.1183/09031936.00157212.
3. Drobniewski F, Nikolayevskyy V, Maxeiner H, Balabanova Y, Casali N, Kontsevaya I, Ignatyeva O. 2013. Rapid diagnostics of tuberculosis and drug resistance in the industrialized world: clinical and public health benefits and barriers to implementation. BMC Med 11:190. http://dx.doi.org/10.1186/1741-7015-11-190.
4. Casali N, Nikolayevskyy V, Balabanova Y, Harris SR, Ignatyeva O, Kontsevaya I, Corander J, Bryant J, Parkhill J, Nejentsev S, Horstmann RD, Brown T, Drobniewski F. 2014. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat Genet 46:279-286. http://dx.doi.org/10.1038/ng.2878.
5. Comas I, Homolka S, Niemann S, Gagneux S. 2009. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS One 4:e7815. http://dx.doi.org/10.1371/journal.pone.0007815.
6. Gardy JL, Johnston JC, Ho Sui SJ, Cook VJ, Shah L, Brodkin E, Rempel S, Moore R, Zhao Y, Holt R, Varhol R, Birol I, Lem M, Sharma MK, Elwood K, Jones SJ, Brinkman FS, Brunham RC, Tang P. 2011. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730-739. http://dx.doi.org/10.1056/NEJMoa1003176.
7. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE. 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13:137-146. http://dx.doi.org/10.1016/S1473-3099(12)70277-3.
8. Roetzer A, Diel R, Kohl TA, Ruckert C, Nubel U, Blom J, Wirth T, Jaenicke S, Schuback S, Rusch-Gerdes S, Supply P, Kalinowski J, Niemann S. 2013. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 10:e1001387. http://dx.doi.org/10.1371/journal.pmed.1001387.
9. Smit PW, Vasankari T, Aaltonen H, Haanperä M, Casali N, Marttila H, Marttila J, Ojanen P, Ruohola A, Ruutu P, Drobniewski F, Lyytikäinen O, Soini H. 2015. Enhanced tuberculosis outbreak investigation using whole genome sequencing and IGRA. Eur Respir J 45:276-279. http://dx.doi.org/10.1183/09031936.00125914.
10. Köser CU, Bryant JM, Becq J, Torok ME, Ellington MJ, Marti-Renom MA, Carmichael AJ, Parkhill J, Smith GP, Peacock SJ. 2013. Wholegenome sequencing for rapid susceptibility testing of M. tuberculosis. N Engl J Med 369:290-292. http://dx.doi.org/10.1056/NEJMc1215305.
11. Fadzilah MN, Ng KP, Ngeow YF. 2009. The manual MGIT system for the detection of M. tuberculosis in respiratory specimens: an experience in the University Malaya Medical Centre. Malays J Pathol 31:93-97.
12. Chihota VN, Grant AD, Fielding K, Ndibongo B, van Zyl A, Muirhead D, Churchyard GJ. 2010. Liquid vs. solid culture for tuberculosis: performance and cost in a resource-constrained setting. Int J Tuberc Lung Dis 14:1024-1031.
13. Warren RM, Victor TC, Streicher EM, Richardson M, Beyers N, Gey van Pittius NC, van Helden PD. 2004. Patients with active tuberculosis often have different strains in the same sputum specimen. Am J Respir Crit Care Med 169:610-614. http://dx.doi.org/10.1164/rccm.200305-714OC.
14. Krüüner A, Yates MD, Drobniewski FA. 2006. Evaluation of MGIT 960-based antimicrobial testing and determination of critical concentrations of first- and second-line antimicrobial drugs with drug-resistant clinical strains of Mycobacterium tuberculosis. J Clin Microbiol 44:811-818. http://dx.doi.org/10.1128/JCM.44.3.811-818.2006.
15. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J. 1997. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35: 907-914.
16. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, III, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544. http://dx.doi.org/10.1038/31159.
17. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK. 2012. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22:568-576. http://dx.doi.org/10.1101/gr.129684.111.
18. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
19. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
20. Bryant JM, Schurch AC, van Deutekom H, Harris SR, de Beer JL, de Jager V, Kremer K, van Hijum SA, Siezen RJ, Borgdorff M, Bentley SD, Parkhill J, van Soolingen D. 2013. Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis 13:110. http://dx.doi.org/10.1186/1471-2334-13-110.
21. Plinke C, Walter K, Aly S, Ehlers S, Niemann S. 2011. Mycobacterium tuberculosis embB codon 306 mutations confer moderately increased resistance to ethambutol in vitro and in vivo. Antimicrob Agents Chemother 55:2891-2896. http://dx.doi.org/10.1128/AAC.00007-10.
22. Sreevatsan S, Stockbauer KE, Pan X, Kreiswirth BN, Moghazeh SL, Jacobs WR, Jr, Telenti A, Musser JM. 1997. Ethambutol resistance in Mycobacterium tuberculosis: critical role of embB mutations. Antimicrob Agents Chemother 41:1677-1681.
23. Bakuła Z, Napiórkowska A, Bielecki J, Augustynowicz-Kopeć E, Zwolska Z, Jagielski T. 2013. Mutations in the embB gene and their association with ethambutol resistance in multidrug-resistant Mycobacterium tuberculosis clinical isolates from Poland. Biomed Res Int 2013:167954. http://dx.doi.org/10.1155/2013/167954.
24. Safi H, Fleischmann RD, Peterson SN, Jones MB, Jarrahi B, Alland D. 2010. Allelic exchange and mutant selection demonstrate that common clinical embCAB gene mutations only modestly increase resistance to ethambutol in Mycobacterium tuberculosis. Antimicrob Agents Chemother 54:103-108. http://dx.doi.org/10.1128/AAC.01288-09.
25. Hazbón MH, Brimacombe M, Bobadilla del Valle M, Cavatore M, Guerrero MI, Varma-Basil M, Billman-Jacobe H, Lavender C, Fyfe J, García-García L, León CI, Bose M, Chaves F, Murray M, Eisenach KD, Sifuentes-Osornio J, Cave MD, Ponce de León A, Alland D. 2006. Population genetics study of isoniazid resistance mutations and evolution of multidrug-resistant Mycobacterium tuberculosis. Antimicrob Agents Chemother 50:2640-2649. http://dx.doi.org/10.1128/AAC.00112-06.
26. Cavusoglu C, Karaca-Derici Y, Bilgic A. 2004. In-vitro activity of rifabutin against rifampicin-resistant Mycobacterium tuberculosis isolates with known rpoB mutations. Clin Microbiol Infect 10:662-665. http://dx.doi.org/10.1111/j.1469-0691.2004.00917.x.
27. Nelson MC, Morrison HG, Benjamino J, Grim SL, Graf J. 2014. Analysis, optimization and verification of Illumina-generated 16S rRNA gene amplicon surveys. PLoS One 9:e94249. http://dx.doi.org/10.1371/journal.pone.0094249.
28. Achtman M. 2008. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62:53-70. http://dx.doi.org/10.1146/annurev.micro.62.081307.162832.
29. Al-Moamary MS, Black W, Bessuille E, Elwood RK, Vedal S. 1999. The significance of the persistent presence of acid-fast bacilli in sputum smears in pulmonary tuberculosis. Chest 116:726-731. http://dx.doi.org/10.1378/chest.116.3.726.
30. Zhang X, Zhao B, Huang H, Zhu Y, Peng J, Dai G, Jiang G, Liu L, Zhao Y, Jin Q. 2013. Co-occurrence of amikacin-resistant and -susceptible Mycobacterium tuberculosis isolates in clinical samples from Beijing, China. J Antimicrob Chemother 68:1537-1542. http://dx.doi.org/10.1093/jac/dkt082.
31. Tolani MP, D'souza DT, Mistry NF. 2012. Drug resistance mutations and heteroresistance detected using the GenoType MTBDRplus assay and their implication for treatment outcomes in patients from Mumbai, India. BMC Infect Dis 12:9. http://dx.doi.org/10.1186/1471-2334-12-9.
32. Cullen MM, Sam NE, Kanduma EG, McHugh TD, Gillespie SH. 2006. Direct detection of heteroresistance in Mycobacterium tuberculosis using molecular techniques. J Med Microbiol 55:1157-1158. http://dx.doi.org/10.1099/jmm.0.46483-0.
33. Falagas ME, Makris GC, Dimopoulos G, Matthaiou DK. 2008. Heteroresistance: a concern of increasing clinical significance? Clin Microbiol Infect 14:101-104. http://dx.doi.org/10.1111/j.1469-0691.2007.01912.x.
34. Doughty EL, Sergeant MJ, Adetifa I, Antonio M, Pallen MJ. 2014. Culture-independent detection and characterisation of Mycobacterium tuberculosis and M. africanum in sputum samples using shotgun metagenomics on a benchtop sequencer. PeerJ 2:e585. http://dx.doi.org/10.7717/peerj.585.