Integrating multiple genomic technologies to investigate an outbreak of carbapenemase-producing Enterobacter hormaechei.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
24 01 2020
Historique:
received: 20 04 2019
accepted: 02 12 2019
entrez: 26 1 2020
pubmed: 26 1 2020
medline: 14 4 2020
Statut: epublish

Résumé

Carbapenem-resistant Enterobacteriaceae (CRE) represent an urgent threat to human health. Here we report the application of several complementary whole-genome sequencing (WGS) technologies to characterise a hospital outbreak of bla

Identifiants

pubmed: 31980604
doi: 10.1038/s41467-019-14139-5
pii: 10.1038/s41467-019-14139-5
pmc: PMC6981164
doi:

Substances chimiques

Bacterial Proteins 0
beta-Lactamases EC 3.5.2.6
carbapenemase EC 3.5.2.6

Types de publication

Case Reports Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

466

Références

Paterson, D. L. & Bonomo, R. A. Extended-spectrum beta-lactamases: a clinical update. Clin. Microbiol. Rev. 18, 657–686 (2005).
pubmed: 16223952 pmcid: 1265908 doi: 10.1128/CMR.18.4.657-686.2005
Gupta, N., Limbago, B. M., Patel, J. B. & Kallen, A. J. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin. Infect. Dis. 53, 60–67 (2011).
pubmed: 21653305 doi: 10.1093/cid/cir202 pmcid: 21653305
Sader, H. S., Biedenbach, D. J. & Jones, R. N. Global patterns of susceptibility for 21 commonly utilized antimicrobial agents tested against 48,440 Enterobacteriaceae in the SENTRY Antimicrobial Surveillance Program (1997-2001). Diagn. Microbiol. Infect. Dis. 47, 361–364 (2003).
pubmed: 12967751 doi: 10.1016/S0732-8893(03)00052-X pmcid: 12967751
World Health Organisation. Antimicrobial Resistance Global Report on Surveillance (WHO, Geneva, 2014).
Akova, M., Daikos, G. L., Tzouvelekis, L. & Carmeli, Y. Interventional strategies and current clinical experience with carbapenemase-producing Gram-negative bacteria. Clin. Microbiol. Infect. 18, 439–448 (2012).
pubmed: 22507111 doi: 10.1111/j.1469-0691.2012.03823.x pmcid: 22507111
Li, Y. Y. et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis. 16, 161–168 (2016).
doi: 10.1016/S1473-3099(15)00424-7
Nordmann, P. & Poirel, L. The difficult-to-control spread of carbapenemase producers among Enterobacteriaceae worldwide. Clin. Microbiol. Infect. 20, 821–830 (2014).
pubmed: 24930781 doi: 10.1111/1469-0691.12719 pmcid: 24930781
Magiorakos, A. P. et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268–281 (2012).
pubmed: 21793988 doi: 10.1111/j.1469-0691.2011.03570.x pmcid: 21793988
Turnidge, J., Gottlieb, T. & Bell, J. Enterobacteriaceae Sepsis Outcome Programme (EnSOP): 2013 Antimicrobial Susceptibility Report. http://agargroup.org.au/wp-content/uploads/2017/08/AGAR-EnSOP13-Web-Report-FINAL-2.pdf (2014).
Partridge, S. R. et al. Emergence of bla
pubmed: 25465526 doi: 10.1016/j.ijantimicag.2014.10.006 pmcid: 25465526
Wailan, A. M. et al. Genomic characteristics of NDM-producing Enterobacteriaceae isolates in Australia and their bla
pubmed: 26482302 pmcid: 4704237 doi: 10.1128/AAC.01243-15
Chang, L. W. et al. Managing a nosocomial outbreak of carbapenem-resistant Klebsiella pneumoniae: an early Australian hospital experience. Intern. Med. J. 45, 1037–1043 (2015).
pubmed: 26178306 doi: 10.1111/imj.12863 pmcid: 26178306
Sidjabat, H. E. et al. Dominance of IMP-4-producing Enterobacter cloacae among carbapenemase-producing Enterobacteriaceae in Australia. Antimicrob. Agents Chemother. 59, 4059–4066 (2015).
pubmed: 25918153 pmcid: 4468659 doi: 10.1128/AAC.04378-14
Leung, G. H., Gray, T. J., Cheong, E. Y., Haertsch, P. & Gottlieb, T. Persistence of related bla-IMP-4 metallo-beta-lactamase producing Enterobacteriaceae from clinical and environmental specimens within a burns unit in Australia—a six-year retrospective study. Antimicrob. Resist. Infect. Control 2, 35 (2013).
pubmed: 24345195 pmcid: 3878348 doi: 10.1186/2047-2994-2-35
Peleg, A. Y., Franklin, C., Bell, J. M. & Spelman, D. W. Dissemination of the metallo-beta-lactamase gene bla
pubmed: 16267725 doi: 10.1086/497831 pmcid: 16267725
Herbert, S. et al. Large outbreak of infection and colonization with gram-negative pathogens carrying the metallo-beta-lactamase gene bla
pubmed: 17230397 doi: 10.1086/508841 pmcid: 17230397
Koser, C. U. et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N. Engl. J. Med. 366, 2267–2275 (2012).
pubmed: 22693998 pmcid: 3715836 doi: 10.1056/NEJMoa1109910
Reuter, S. et al. A pilot study of rapid whole-genome sequencing for the investigation of a Legionella outbreak. BMJ Open, https://doi.org/10.1136/bmjopen-2012-002175 (2013).
pubmed: 23306006 pmcid: 3553392 doi: 10.1136/bmjopen-2012-002175
Quick, J. et al. Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella. Genome Biol. 16, 114 (2015).
pubmed: 26025440 pmcid: 4702336 doi: 10.1186/s13059-015-0677-2
Conlan, S. et al. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci. Transl. Med. 6, 254ra126 (2014).
pubmed: 25232178 pmcid: 4203314 doi: 10.1126/scitranslmed.3009845
Mathers, A. J. et al. Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae at a single institution: insights into endemicity from whole-genome sequencing. Antimicrob. Agents Chemother. 59, 1656–1663 (2015).
pubmed: 25561339 pmcid: 4325807 doi: 10.1128/AAC.04292-14
European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters version 6.0, http://www.eucast.org (2016).
European Committee on Antimicrobial Susceptibility Testing. EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance, http://www.eucast.org/resistance_mechanisms/ (2012).
Sidjabat, H. E., Heney, C., George, N. M., Nimmo, G. R. & Paterson, D. L. Interspecies transfer of bla
pubmed: 25056334 pmcid: 4187761 doi: 10.1128/JCM.01491-14
Kanamori, H. et al. Next-generation sequencing and comparative analysis of sequential outbreaks caused by multidrug-resistant Acinetobacter baumannii at a large academic burn center. Antimicrob. Agents Chemother. 60, 1249–1257 (2015).
pubmed: 26643351 doi: 10.1128/AAC.02014-15 pmcid: 26643351
Stoesser, N. et al. Dynamics of MDR Enterobacter cloacae outbreaks in a neonatal unit in Nepal: insights using wider sampling frames and next-generation sequencing. J. Antimicrob. Chemother. 70, 1008–1015 (2015).
pubmed: 25558071 pmcid: 4356206 doi: 10.1093/jac/dku521
Howden, B. P. et al. Genomic insights to control the emergence of vancomycin-resistant enterococci. MBio, https://doi.org/10.1128/mBio.00412-13 (2013).
Miller, R. R., Montoya, V., Gardy, J. L., Patrick, D. M. & Tang, P. Metagenomics for pathogen detection in public health. Genome Med. 5, 81 (2013).
pubmed: 24050114 pmcid: 3978900 doi: 10.1186/gm485
Forbes, J. D., Knox, N. C., Peterson, C. L. & Reimer, A. R. Highlighting clinical metagenomics for enhanced diagnostic decision-making: a step towards wider implementation. Comput. Struct. Biotechnol. J. 16, 108–120 (2018).
pubmed: 30026887 pmcid: 6050174 doi: 10.1016/j.csbj.2018.02.006
Friedman, N. D. et al. Prevalence of Clostridium difficile colonization among healthcare workers. BMC Infect. Dis. 13, 459 (2013).
pubmed: 24090343 pmcid: 3850636 doi: 10.1186/1471-2334-13-459
Dulon, M., Peters, C., Schablon, A. & Nienhaus, A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect. Dis. 14, 363 (2014).
pubmed: 24996225 pmcid: 4094410 doi: 10.1186/1471-2334-14-363
Lubbert, C. et al. Long-term carriage of Klebsiella pneumoniae carbapenemase-2-producing K pneumoniae after a large single-center outbreak in Germany. Am. J. Infect. Control 42, 376–380 (2014).
pubmed: 24679563 doi: 10.1016/j.ajic.2013.12.001 pmcid: 24679563
Quiroga, M. P. et al. Complex class 1 integrons with diverse variable regions, including aac(6′)-Ib-cr, and a novel allele, qnrB10, associated with ISCR1 in clinical enterobacterial isolates from Argentina. Antimicrob. Agents Chemother. 51, 4466–4470 (2007).
pubmed: 17938184 pmcid: 2167984 doi: 10.1128/AAC.00726-07
Wang, M. et al. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob. Agents Chemother. 47, 2242–2248 (2003).
pubmed: 12821475 pmcid: 161834 doi: 10.1128/AAC.47.7.2242-2248.2003
Ho, P.-L. et al. pIMP-PH114 carrying bla
pubmed: 24121549 doi: 10.1007/s00284-013-0471-x pmcid: 24121549
Roy Chowdhury, P. et al. Dissemination of multiple drug resistance genes by class 1 integrons in Klebsiella pneumoniae isolates from four countries: a comparative study. Antimicrob. Agents Chemother. 55, 3140–3149 (2011).
pubmed: 21518841 pmcid: 3122386 doi: 10.1128/AAC.01529-10
Abraham, S. et al. Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Sci. Rep. 6, 35527 (2016).
pubmed: 27767038 pmcid: 5073282 doi: 10.1038/srep35527
Morrill, H. J., Pogue, J. M., Kaye, K. S. & LaPlante, K. L. Treatment options for carbapenem-resistant Enterobacteriaceae infections. Open Forum Infect. Dis. 2, ofv050 (2015).
pubmed: 26125030 pmcid: 4462593 doi: 10.1093/ofid/ofv050
Tumbarello, M. et al. Predictors of mortality in bloodstream infections caused by Klebsiella pneumoniae carbapenemase-producing K. pneumoniae: importance of combination therapy. Clin. Infect. Dis. 55, 943–950 (2012).
pubmed: 22752516 doi: 10.1093/cid/cis588 pmcid: 22752516
Daikos, G. L. et al. Carbapenemase-producing Klebsiella pneumoniae bloodstream infections: lowering mortality by antibiotic combination schemes and the role of carbapenems. Antimicrob. Agents Chemother. 58, 2322–2328 (2014).
pubmed: 24514083 pmcid: 4023796 doi: 10.1128/AAC.02166-13
Carter, I. in PCR for Clinical Microbiology: An Australian and International Perspective (eds Schuller, M. et al.) 423−427 (Springer Netherlands, 2010).
Victorian-Bioinformatics-Consortium. Nesoni, https://github.com/Victorian-Bioinformatics-Consortium/nesoni (2014).
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
pubmed: 22506599 pmcid: 3342519 doi: 10.1089/cmb.2012.0021
Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).
pubmed: 23422339 pmcid: 3624806 doi: 10.1093/bioinformatics/btt086
Ondov, B. D. et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 17, 132 (2016).
pubmed: 27323842 pmcid: 4915045 doi: 10.1186/s13059-016-0997-x
Jain, C., Rodriguez, R. L., Phillippy, A. M., Konstantinidis, K. T. & Aluru, S. High throughput ANI analysis of 90 K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9, 5114 (2018).
pubmed: 30504855 pmcid: 6269478 doi: 10.1038/s41467-018-07641-9
David, M., Dzamba, M., Lister, D., Ilie, L. & Brudno, M. SHRiMP2: sensitive yet practical short read mapping. Bioinformatics 27, 1011–1012 (2011).
pubmed: 21278192 doi: 10.1093/bioinformatics/btr046 pmcid: 21278192
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623 pmcid: 3998144 doi: 10.1093/bioinformatics/btu033
Treangen, T. J., Ondov, B. D., Koren, S. & Phillippy, A. M. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 15, 1–15 (2014).
doi: 10.1186/s13059-014-0524-x
Inouye, M. et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 6, 90 (2014).
pubmed: 25422674 pmcid: 4237778 doi: 10.1186/s13073-014-0090-6
Miyoshi-Akiyama, T., Hayakawa, K., Ohmagari, N., Shimojima, M. & Kirikae, T. Multilocus sequence typing (MLST) for characterization of Enterobacter cloacae. PLoS ONE 8, e66358 (2013).
pubmed: 23776664 pmcid: 3679064 doi: 10.1371/journal.pone.0066358
Compain, F. et al. Targeting relaxase genes for classification of the predominant plasmids in Enterobacteriaceae. Int. J. Med. Microbiol. 304, 236–242 (2014).
pubmed: 24342269 doi: 10.1016/j.ijmm.2013.09.009 pmcid: 24342269
Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644 (2012).
pubmed: 22782487 pmcid: 3468078 doi: 10.1093/jac/dks261
Gupta, S. K. et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob. Agents Chemother. 58, 212–220 (2014).
pubmed: 24145532 pmcid: 3910750 doi: 10.1128/AAC.01310-13
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows−Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
Alikhan, N. F., Petty, N. K., Ben Zakour, N. L. & Beatson, S. A. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom. 12, 402 (2011).
doi: 10.1186/1471-2164-12-402
Carver, T. J. et al. ACT: the Artemis Comparison Tool. Bioinformatics 21, 3422–3423 (2005).
pubmed: 15976072 doi: 10.1093/bioinformatics/bti553 pmcid: 15976072
Zhou, Y., Liang, Y., Lynch, K. H., Dennis, J. J. & Wishart, D. S. PHAST: a fast phage search tool. Nucleic Acids Res. 39, W347–W352 (2011).
pubmed: 21672955 pmcid: 3125810 doi: 10.1093/nar/gkr485
Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).
pubmed: 24580807 pmcid: 4053813 doi: 10.1186/gb-2014-15-3-r46

Auteurs

Leah W Roberts (LW)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia.

Patrick N A Harris (PNA)

UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia. p.harris@uq.edu.au.
Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia. p.harris@uq.edu.au.

Brian M Forde (BM)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia.

Nouri L Ben Zakour (NL)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia.

Elizabeth Catchpoole (E)

Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia.

Mitchell Stanton-Cook (M)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.

Minh-Duy Phan (MD)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.

Hanna E Sidjabat (HE)

Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia.

Haakon Bergh (H)

Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia.

Claire Heney (C)

Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia.

Jayde A Gawthorne (JA)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.

Jeffrey Lipman (J)

UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia.
Burns Trauma and Critical Care Research Centre, The University of Queensland, Brisbane, QLD, Australia.

Anthony Allworth (A)

Infectious Disease Unit, Royal Brisbane & Women's Hospital, Brisbane, QLD, Australia.

Kok-Gan Chan (KG)

Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia.
International Genome Centre, Jiangsu University, Zhenjiang, China.

Teik Min Chong (TM)

Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia.

Wai-Fong Yin (WF)

Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia.

Mark A Schembri (MA)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.

David L Paterson (DL)

Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia.

Scott A Beatson (SA)

School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.
Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.
Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.

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