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

Leah W Roberts; Patrick N A Harris; Brian M Forde; Nouri L Ben Zakour; Elizabeth Catchpoole; Mitchell Stanton-Cook; Minh-Duy Phan; Hanna E Sidjabat; Haakon Bergh; Claire Heney; Jayde A Gawthorne; Jeffrey Lipman; Anthony Allworth; Kok-Gan Chan; Teik Min Chong; Wai-Fong Yin; Mark A Schembri; David L Paterson; Scott A Beatson

doi:10.1038/s41467-019-14139-5

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

Nat Commun. 2020 Jan 24;11(1):466. doi: 10.1038/s41467-019-14139-5.

Authors

Leah W Roberts^{1

2

3}, Patrick N A Harris^{4

5}, Brian M Forde^{1

2

3}, Nouri L Ben Zakour^{1

2

3}, Elizabeth Catchpoole⁶, Mitchell Stanton-Cook^{1

2}, Minh-Duy Phan^{1

2}, Hanna E Sidjabat^{2

7}, Haakon Bergh⁶, Claire Heney⁶, Jayde A Gawthorne^{1

2}, Jeffrey Lipman^{7

8}, Anthony Allworth⁹, Kok-Gan Chan^{10

11}, Teik Min Chong¹⁰, Wai-Fong Yin¹⁰, Mark A Schembri^{1

2}, David L Paterson^{2

7}, Scott A Beatson^{12

13

14}

Affiliations

¹ School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.
² Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
³ Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia.
⁴ UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia. p.harris@uq.edu.au.
⁵ Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia. p.harris@uq.edu.au.
⁶ Pathology Queensland, Central Microbiology, Brisbane, QLD, Australia.
⁷ UQ Centre for Clinical Research, The University of Queensland, Brisbane, QLD, Australia.
⁸ Burns Trauma and Critical Care Research Centre, The University of Queensland, Brisbane, QLD, Australia.
⁹ Infectious Disease Unit, Royal Brisbane & Women's Hospital, Brisbane, QLD, Australia.
¹⁰ Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia.
¹¹ International Genome Centre, Jiangsu University, Zhenjiang, China.
¹² School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.
¹³ Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.
¹⁴ Australian Centre for Ecogenomics, The University of Queensland, Brisbane, QLD, Australia. s.beatson@uq.edu.au.

Abstract

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_IMP-4 carbapenemase-producing E. hormaechei. Using Illumina sequencing, we determined that all outbreak strains were sequence type 90 (ST90) and near-identical. Comparison to publicly available data linked all outbreak isolates to a 2013 isolate from the same ward, suggesting an environmental source in the hospital. Using Pacific Biosciences sequencing, we resolved the complete context of the bla_IMP-4 gene on a large IncHI2 plasmid carried by all IMP-4-producing strains across different hospitals. Shotgun metagenomic sequencing of environmental samples also found evidence of ST90 E. hormaechei and the IncHI2 plasmid within the hospital plumbing. Finally, Oxford Nanopore sequencing rapidly resolved the true relationship of subsequent isolates to the initial outbreak. Overall, our strategic application of three WGS technologies provided an in-depth analysis of the outbreak.

Publication types

Case Reports

MeSH terms

Bacterial Proteins / biosynthesis*
Bacterial Proteins / genetics*
Burns / microbiology
Carbapenem-Resistant Enterobacteriaceae / enzymology*
Carbapenem-Resistant Enterobacteriaceae / genetics*
Carbapenem-Resistant Enterobacteriaceae / pathogenicity
Cross Infection / epidemiology
Cross Infection / microbiology
Disease Outbreaks*
Drug Resistance, Multiple, Bacterial / genetics
Enterobacter / enzymology*
Enterobacter / genetics*
Enterobacter / isolation & purification
Enterobacteriaceae Infections / epidemiology*
Enterobacteriaceae Infections / microbiology
Genome, Bacterial
Humans
Queensland / epidemiology
R Factors / genetics
Sanitary Engineering
Tertiary Care Centers
Whole Genome Sequencing / methods
beta-Lactam Resistance / genetics
beta-Lactamases / biosynthesis*
beta-Lactamases / genetics*

Substances

Bacterial Proteins
beta-Lactamases
carbapenemase

Supplementary concepts

Enterobacter hormaechei