Emergence of NDM-producing Klebsiella pneumoniae and Escherichia coli in Spain: Phylogeny, resistome, virulence and plasmids encoding blaNDM-like genes as determined by WGS

Journal of Antimicrobial Chemotherapy

Volumn 74, Issue 12, 2019, Pages 3489-3496

  Pérez Vázquez, María ^a,b   Sola Campoy, Pedro J ^a   Ortega, Adriana ^a,b   Bautista, Verónica ^a,b   Monzón, Sara ^b   Ruiz Carrascoso, Guillermo ^b,c   Mingorance, Jesus ^b,c   González Barberá, Eva M ^d   Gimeno, Concepción ^e   Aracil, Belén ^a,b   Sáez, David ^a,b   Lara, Noelia ^a,b   Fernández, Sara ^a,b   González López, Juan José ^b,f   Campos, José ^a,b   Kingsley, Robert A ^g,h   Dougan, Gordon ^g   Oteo Iglesias, Jesús ^a,b  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^d HOSPITAL UNIVERSITARIO LA FE   (Spain)

^e HOSPITAL GENERAL UNIVERSITARIO DE VALENCIA   (Spain)

^f HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^h INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE NDM; HYDROLASE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BETA LACTAMASE; BETA-LACTAMASE NDM-1;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTOME; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; CLONE; EPIDEMIC; ESCHERICHIA COLI; GENE LIBRARY; KLEBSIELLA PNEUMONIAE; MOBILE GENETIC ELEMENT; NONHUMAN; PHYLOGENY; PLASMID; POPULATION STRUCTURE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SPAIN; WHOLE GENOME SEQUENCING; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; CLASSIFICATION; ENTEROBACTERIACEAE INFECTION; ENZYMOLOGY; GENETICS; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; MULTILOCUS SEQUENCE TYPING; VIRULENCE;

ANTI-BACTERIAL AGENTS; BACTERIAL TYPING TECHNIQUES; BETA-LACTAMASES; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROBACTERIACEAE INFECTIONS; ESCHERICHIA COLI; GENOME, BACTERIAL; HUMANS; KLEBSIELLA PNEUMONIAE; MICROBIAL SENSITIVITY TESTS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; PLASMIDS; POLYMORPHISM, SINGLE NUCLEOTIDE; SPAIN; VIRULENCE; WHOLE GENOME SEQUENCING;

EID: 85075093285     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkz366     Document Type: Article

References (50)

1. Temkin E, Adler A, Lerner A et al. Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management. Ann N Y Acad Sci 2014; 1323: 22-42.
2. Kumarasamy KK, Toleman MA, Walsh TR et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 2010; 10: 597-602.
3. Johnson AP, Woodford N. Global spread of antibiotic resistance: the example of New Delhi metallo-b-lactamase (NDM)-mediated carbapenem resistance.JMedMicrobiol 2013; 62: 499-513.
4. Barberino MG, Cruvinel SA, Faria C et al. Isolation of blaNDM-producing Enterobacteriaceae in a public hospital in Salvador, Bahia, Brazil. Braz J Infect Dis 2018; 22: 47-50.
5. Pitart C, Sole M, Roca I et al. Molecular characterization of blaNDM-5 carried on an IncFII plasmid in an Escherichia coli isolate from a nontraveler patient in Spain. Antimicrob Agents Chemother 2015; 59: 659-62.
6. Wilson ME, Chen LH. NDM-1 and the role of travel in its dissemination. Curr Infect Dis Rep 2012; 14: 213-26.
7. Partridge SR, Iredell JR. Genetic contexts of blaNDM-1. Antimicrob Agents Chemother 2012; 56: 6065-7.
8. Sugawara Y, Akeda Y, Sakamoto N et al. Genetic characterization of blaNDM-harboring plasmids in carbapenem-resistant Escherichia coli from Myanmar. PLoS One 2017; 12: e0184720.
9. Oteo J, Domingo GD, Fernandez-Romero S et al. Abdominal abscess due to NDM-1-producing Klebsiella pneumoniae in Spain. J Med Microbiol 2012; 61: 864-7.
10. Oteo J, Ortega A, Bartolome R et al. Prospective multicenter study of carbapenemase-producing Enterobacteriaceae from 83 hospitals in Spain reveals high in vitro susceptibility to colistin and meropenem. Antimicrob Agents Chemother 2015; 59: 3406-12.
11. Oteo J, Saez D, Bautista V et al. Carbapenemase-producing Enterobacteriaceae in Spain in 2012. Antimicrob Agents Chemother 2013; 57: 6344-7.
12. Hernandez-Garcia M, Perez-Viso B, Carmen Turrientes M et al. Characterization of carbapenemase-producing Enterobacteriaceae from colonized patients in a university hospital in Madrid, Spain, during the RGNOSIS project depicts increased clonal diversity over time with maintenance of high-risk clones. J Antimicrob Chemother 2018; 73: 3039-43.
13. Dortet L, Brechard L, Cuzon G et al. Strategy for rapid detection of carbapenemase-producing Enterobacteriaceae. Antimicrob Agents Chemother 2014; 58: 2441-5.
14. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing-Twenty-Seventh Edition: M100. CLSI, Wayne, PA, USA, 2017.
15. Bankevich A, Nurk S, Antipov D et al. SPAdes: a newgenome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19: 455-77.
16. BoetzerM, Henkel CV, Jansen HJ et al. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27: 578-9.
17. Nadalin F, Vezzi F, Policriti A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics 2012; 13 Suppl 14: S8.
18. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30: 2068-9.
19. WuKM, Li LH, Yan JJ et al. Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol 2009; 191: 4492-501.
20. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 2009; 25: 1754-60.
21. Perez-Vazquez M, Oteo J, Garcia-Cobos S et al. Phylogeny, resistome and mobile genetic elements of emergent OXA-48 and OXA-245 Klebsiella pneumoniae clones circulating in Spain. J Antimicrob Chemother 2016; 71: 887-96.
22. Riley M, Abe T, Arnaud MB et al. Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res 2006; 34: 1-9.
23. Chin CS, Alexander DH, Marks P et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10: 563-9.
24. Mathers AJ, Stoesser N, Sheppard AE et al. Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae at a single institution: insights into endemicity from whole-genome sequencing. Antimicrob Agents Chemother 2015; 59: 1656-63.
25. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixedmodels. Bioinformatics 2006; 22: 2688-90.
26. Holt KE, Baker S, Weill FX et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 2012; 44: 1056-9.
27. Bialek-Davenet S, Criscuolo A, Ailloud F et al. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 2014; 20: 1812-20.
28. Zhou X, Garcia-Cobos S, Ruijs G et al. Epidemiology of extended-spectrum b-lactamase-producing E. coli and vancomycin-resistant enterococci in the Northern Dutch-German cross-border region. FrontMicrobiol 2017; 8: 1914.
29. Gastmeier P, Schwab F, Bärwolff S et al. Correlation between the genetic diversity of nosocomial pathogens and their survival time in intensive care units.JHospInfect 2006; 62: 181-6.
30. Inouye M, Dashnow H, Raven LA et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6: 90.
31. Gupta SK, Padmanabhan BR, Diene SM et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58: 212-20.
32. Wyres KL, Wick RR, Gorrie C et al. Identification of Klebsiella capsule synthesis loci from whole genome data. Microb Genom 2016; 2: e000102.
33. Seara N, Oteo J, Carrillo R et al. Interhospital spread of NDM-7-producing Klebsiella pneumoniae belonging to ST437 in Spain. Int J Antimicrob Agents 2015; 46: 169-73.
34. Albiger B, Glasner C, Struelens MJ et al. Carbapenemase-producing Enterobacteriaceae in Europe: assessment by national experts from 38 countries, May 2015. Euro Surveill 2015; 20: pii=30062.
35. Stoesser N, Sheppard AE, Peirano G et al. Genomic epidemiology of global Klebsiella pneumoniae carbapenemase (KPC)-producing Escherichia coli. Sci Rep 2017; 7: 5917.
36. Barrado L, Perez-Vazquez M, Del Pozo JL et al. Clonal transmission of NDM-5-producing Escherichia coli belonging to high-risk sequence type ST405. Int J Antimicrob Agents 2018; 52: 123-4.
37. Yu F, Lv J, Niu S et al. Multiplex PCR analysis for rapid detection of Klebsiella pneumoniae carbapenem-resistant (ST258, 11) and hypervirulent (ST23, 65, 86, 375) strains. JClinMicrobiol 2018; 56: e00731-18.
38. Chen L, Chavda KD, Findlay J et al. Multiplex PCR for identification of two capsular types in epidemic KPC-producing Klebsiella pneumoniae sequence type 258 strains. Antimicrob Agents Chemother 2014; 58: 4196-9.
39. Lam MMC, Wick RR, Wyres KL et al. Genetic diversity, mobilisation and spread of the yersiniabactin-encodingmobile element ICEKp in Klebsiella pneumoniae populations. Microb Genom 2018; 4: doi:10.1099/mgen. 0.000196.
40. YanQ, ZhouM, ZouMet al. Hypervirulent Klebsiella pneumoniae induced ventilator-associated pneumonia in mechanically ventilated patients in China. Eur J Clin Microbiol Infect Dis 2016; 35: 387-96.
41. Oteo J, Perez-Vazquez M, Bautista V et al. The spread of KPC-producing Enterobacteriaceae in Spain: WGS analysis of the emerging high-risk clones of Klebsiella pneumoniae ST11/KPC-2, ST101/KPC-2 and ST512/KPC-3. J Antimicrob Chemother 2016; 71: 3392-9.
42. KhongWX, Marimuthu K, Teo J et al. Tracking inter-institutional spread of NDM and identification of a novel NDM-positive plasmid, pSg1-NDM, using next-generation sequencing approaches. J Antimicrob Chemother 2016; 71: 3081-9.
43. Campos JC, da Silva MJ, dos Santos PR et al. Characterizationof Tn3000, a transposon responsible for blaNDM-1 dissemination among Enterobacteriaceae in Brazil, Nepal, Morocco, and India. Antimicrob Agents Chemother 2015; 59: 7387-95.
44. Espedido BA, Dimitrijovski B, van Hal SJ et al. The use ofwhole-genome sequencing formolecular epidemiology and antimicrobial surveillance: identifying the role of IncX3 plasmids and the spread of blaNDM-4-like genes in the Enterobacteriaceae. JClinPathol 2015; 68: 835-8.
45. Chen YT, Lin AC, Siu LK et al. Sequence of closely related plasmids encoding blaNDM-1 in two unrelated Klebsiella pneumoniae isolates in Singapore. PLoS One 2012; 7: e48737.
46. Mataseje LF, Boyd DA, Lefebvre B et al. Complete sequences of a novel blaNDM-1-harbouring plasmid from Providencia rettgeri and an FII-type plasmid from Klebsiella pneumoniae identified in Canada. J Antimicrob Chemother 2014; 69: 637-42.
47. Giufre M, Errico G, Accogli M et al. Emergence of NDM-5-producing Escherichia coli sequence type 167 clone in Italy. Int J Antimicrob Agents 2018; 52: 76-81.
48. Ho PL, Li Z, LoWUet al. Identification and characterization of a novel incompatibility group X3 plasmid carrying blaNDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China. EmergMicrobes Infect 2012; 1: e39.
49. Nordmann P, Poirel L, Walsh TR et al. The emerging NDM carbapenemases. TrendsMicrobiol 2011; 19: 588-95.
50. Paskova V, Medvecky M, Skalova A et al. Characterization of NDMencoding plasmids fromEnterobacteriaceae recovered from Czech hospitals. FrontMicrobiol 2018; 9: 1549.