Prediction of staphylococcus aureus antimicrobial resistance by whole-genome sequencing

Journal of Clinical Microbiology

Volumn 52, Issue 4, 2014, Pages 1182-1191

  Gordon, N C ^a   Price, J R ^b   Cole, K ^b   Everitt, R ^c   Morgan, M ^a   Finney, J ^a   Kearns, A M ^d   Pichon, B ^d   Young, B ^a   Wilson, D J ^a   Llewelyn, M J ^b   Paul, J ^b   Peto, T E A ^a   Crook, D W ^a   Walker, A S ^a   Golubchik, T ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b ROYAL SUSSEX COUNTY HOSPITAL   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

^d PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; CLINDAMYCIN; ERYTHROMYCIN; FUSIDIC ACID; GENTAMICIN; METICILLIN; PENICILLIN DERIVATIVE; PSEUDOMONIC ACID; RIFAMPICIN; TETRACYCLINE; TRIMETHOPRIM; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENOME; BACTERIUM ISOLATE; BROTH DILUTION; CHROMOSOME MUTATION; CONTROLLED STUDY; ERROR; GENE SEQUENCE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; STAPHYLOCOCCUS AUREUS; WHOLE GENOME SEQUENCING; BIOLOGY; COMPARATIVE STUDY; DNA SEQUENCE; DRUG EFFECTS; EVALUATION STUDY; GENETICS; HUMAN; PROCEDURES;

ANTI-BACTERIAL AGENTS; COMPUTATIONAL BIOLOGY; DRUG RESISTANCE, BACTERIAL; GENOME, BACTERIAL; HUMANS; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCUS AUREUS;

EID: 84897134429     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03117-13     Document Type: Article

References (35)

1. Metzker ML. 2010. Sequencing technologies - the next generation. Nat. Rev. Genet. 11:31-46. http://dx.doi.org/10.1038/nrg2626.
2. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW. 2012. Transforming clinical microbiology with bacterial genome sequencing. Nat. Rev. Genet. 13:601-612. http://dx.doi.org/10.1038/nrg3226.
3. Zankari E, Hasman H, Kaas RS, Seyfarth AM, Agerso Y, Lund O, Larsen MV, Aarestrup FM. 2013. Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J. Antimicrob. Chemother. 68:771-777. http://dx.doi.org/10.1093/jac/ dks496.
4. Stoesser N, Batty EM, Eyre DW, Morgan M, Wyllie DH, Del Ojo Elias C, Johnson JR, Walker AS, Peto TE, Crook DW. 2013. Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J. Antimicrob. Chemother. 68:2234-2244. http://dx.doi.org/10.1093/jac/dkt180.
5. Eyre DW, Golubchik T, Gordon NC, Bowden R, Piazza P, Batty EM, Ip CLC, Wilson DJ, Didelot X, O'Connor L, Lay R, Buck D, Kearns AM, Shaw A, Paul J, Wilcox MH, Donnelly PJ, Peto TEA, Walker AS, Crook DW. 2012. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2:e001124. http://dx.doi.org/10. 1136/bmjopen-2012-001124.
6. Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21:936-939. http://dx.doi.org/10.1101/gr.111120.110.
7. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. U. S. A. 101:9786-9791. http://dx.doi.org/10. 1073/pnas.0402521101. (Pubitemid 38869314)
8. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829. http://dx.doi.org/10. 1101/gr.074492.107. (Pubitemid 351645072)
9. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. http://dx.doi.org/10.1186/1471-2105-10-421.
10. Price J, Baker G, Heath I, Walker-Bone K, Cubbon M, Curtis S, Enright MC, Lindsay J, Paul J, Llewelyn M. 2010. Clinical and microbiological determinants of outcome in Staphylococcus aureus bacteraemia. Int. J. Microbiol. 2010:654858.
11. Gosden PE, Andrews JM, Bowker KE, Holt HA, MacGowan AP, Reeves DS, Sunderland J, Wise R. 1998. Comparison of the modified Stokes' method of susceptibility testing with results obtained using MIC methods and British Society of Antimicrobial Chemotherapy breakpoints. J. Antimicrob. Chemother. 42: 161-169. http://dx.doi.org/10.1093/jac/42.2.161. (Pubitemid 28393584)
12. Young BC, Golubchik T, Batty EM, Fung R, Larner-Svensson H, Votintseva AA, Miller RR, Godwin H, Knox K, Everitt RG, Iqbal Z, Rimmer AJ, Cule M, Ip CL, Didelot X, Harding RM, Donnelly P, Peto TE, Crook DW, Bowden R, Wilson DJ. 2012. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc. Natl. Acad. Sci. U. S. A. 109:4550-4555. http://dx.doi.org/ 10.1073/pnas.1113219109.
13. Howe RA, Andrews JM, BSAC Working Party on Susceptibility Testing. 2012. BSAC standardized disc susceptibility testing method (version 11). J. Antimicrob. Chemother. 67:2783-2784. http://dx.doi.org/10.1093/jac/dks391.
14. Yilmaz G, Aydin K, Iskender S, Caylan R, Koksal I. 2007. Detection and prevalence of inducible clindamycin resistance in staphylococci. J. Med. Microbiol. 56:342-345. http://dx.doi.org/10.1099/jmm.0.46761-0. (Pubitemid 46363978)
15. Pitkala A, Salmikivi L, Bredbacka P, Myllyniemi AL, Koskinen MT. 2007. Comparison of tests for detection of beta-lactamase-producing staphylococci. J. Clin. Microbiol. 45:2031-2033. http://dx.doi.org/10.1128/JCM.00621-07. (Pubitemid 46933954)
16. Kolbert CP, Connolly JE, Lee MJ, Persing DH. 1995. Detection of the staphylococcal mecA gene by chemiluminescent DNA hybridization. J. Clin. Microbiol. 33:2179-2182.
17. Blanc DS, Petignat C, Moreillon P, Entenza JM, Eisenring M, Kleiber H, Wenger A, Troillet N, Blanc C, Francioli P. 1999. Unusual spread of a penicillin-susceptible methicillin-resistant Staphylococcus aureus clone in a geographic area of low incidence. Clin. Infect. Dis. 29:1512-1518. http://dx.doi.org/10.1086/313522. (Pubitemid 30022750)
18. Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA. 2011. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect. Dis. 11:595-603. http://dx.doi.org/10.1016/ S1473-3099(11)70126-8.
19. Tanaka M, Wang T, Onodera Y, Uchida Y, Sato K. 2000. Mechanism of quinolone resistance in Staphylococcus aureus. J. Infect. Chemother. 6:131-139. http://dx.doi.org/10.1007/s101560070010.
20. Kaatz GW, Seo SM. 1997. Mechanisms of fluoroquinolone resistance in genetically related strains of Staphylococcus aureus. Antimicrob. Agents Chemother. 41:2733-2737. (Pubitemid 27524749)
21. Qin X, Poon B, Kwong J, Niles D, Schmidt BZ, Rajagopal L, Gantt S. 2011. Two paediatric cases of skin and soft-tissue infections due to clindamycin-resistant Staphylococcus aureus carrying a plasmid-encoded vga(A) allelic variant for a putative efflux pump. Int. J. Antimicrob. Agents 38:81-83. http://dx.doi.org/10.1016/j.ijantimicag.2011.03.007.
22. Vidaillac C, Gardete S, Tewhey R, Sakoulas G, Kaatz GW, Rose WE, Tomasz A, Rybak MJ. 2013. Alternative mutational pathways to intermediate resistance to vancomycin in methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 208:67-74. http://dx.doi.org/10.1093/infdis/jit127.
23. McLaws FB, Larsen AR, Skov RL, Chopra I, O'Neill AJ. 2011. Distribution of fusidic acid resistance determinants in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 55:1173-1176. http://dx.doi.org/10.1128/ AAC.00817-10.
24. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. 2012. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67:2640-2644. http://dx.doi.org/10. 1093/jac/dks261.
25. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O'Brien JS, Pawlowski AC, Piddock LJ, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD. 2013. The Comprehensive Antibiotic Resistance Database. Antimicrob. Agents Chemother. 57:3348-3357. http://dx.doi.org/10.1128/AAC.00419-13.
26. Nonhoff C, Rottiers S, Struelens MJ. 2005. Evaluation of the Vitek 2 system for identification and antimicrobial susceptibility testing of Staphylococcus spp. Clin. Microbiol. Infect. 11:150-153. http://dx.doi.org/10. 1111/j.1469-0691.2004.01047.x. (Pubitemid 40253821)
27. Carroll KC, Borek AP, Burger C, Glanz B, Bhally H, Henciak S, Flayhart DC. 2006. Evaluation of the BD Phoenix automated microbiology system for identification and antimicrobial susceptibility testing of staphylococci and enterococci. J. Clin. Microbiol. 44:2072-2077. http://dx.doi.org/10.1128/JCM. 02636-05. (Pubitemid 43902155)
28. US Food and Drug Administration. 2003. Class II special controls guidance document: antimicrobial susceptibility test (AST) systems: guidance for industry and FDA. US Food and Drug Administration, Rockville, MD.
29. Olsen JE, Christensen H, Aarestrup FM. 2006. Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. J. Antimicrob. Chemother. 57:450-460. http://dx.doi.org/10.1093/jac/dki492. (Pubitemid 43240197)
30. Haveri M, Suominen S, Rantala L, Honkanen-Buzalski T, Pyorala S. 2005. Comparison of phenotypic and genotypic detection of penicillin G resistance of Staphylococcus aureus isolated from bovine intramammary infection. Vet. Microbiol. 106:97-102. http://dx.doi.org/10.1016/j.vetmic.2004.12.015. (Pubitemid 40298863)
31. Tasara T, Cernela N, Stephan R. 2013. Function impairing mutations in blaZ and blaR genes of penicillin susceptible Staphylococcus aureus strains isolated from bovine mastitis. Schweiz. Arch. Tierheilkd. 155:359-363. http://dx.doi.org/10.1024/0036-7281/a000471.
32. Golubchik T, Batty EM, Miller RR, Farr H, Young BC, Larner-Svensson H, Fung R, Godwin H, Knox K, Votintseva A, Everitt RG, Street T, Cule M, Ip CL, Didelot X, Peto TE, Harding RM, Wilson DJ, Crook DW, Bowden R. 2013. Within-host evolution of Staphylococcus aureus during asymptomatic carriage. PLoS One 8:e61319. http://dx.doi.org/10.1371/journal.pone.0061319.
33. Koser CU, Ellington MJ, Cartwright EJ, Gillespie SH, Brown NM, Farrington M, Holden MT, Dougan G, Bentley SD, Parkhill J, Peacock SJ. 2012. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 8:e1002824. http://dx.doi.org/10.1371/journal.ppat. 1002824.
34. Price JR, Golubchik T, Cole K, Wilson DJ, Crook DW, Thwaites GE, Bowden R, Walker AS, Peto TEA, Paul J, Llewelyn MJ. 9 January 2014. Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus on an intensive care unit. Clin. Infect. Dis. http://dx.doi.org/10.1093/cid/cit807.
35. Harris SR, Cartwright EJ, Torok ME, Holden MT, Brown NM, Ogilvy-Stuart AL, Ellington MJ, Quail MA, Bentley SD, Parkhill J, Peacock SJ. 2013. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect. Dis. 13:130-136. http://dx.doi.org/10.1016/S1473-3099(12)70268-2.