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A role for arthropods as vectors of multidrug-resistant Enterobacterales in surgical site infections from South Asia

Abstract

Understanding how multidrug-resistant Enterobacterales (MDRE) are transmitted in low- and middle-income countries (LMICs) is critical for implementing robust policies to curb the increasing burden of antimicrobial resistance (AMR). Here, we analysed samples from surgical site infections (SSIs), hospital surfaces (HSs) and arthropods (summer and winter 2016) to investigate the incidence and transmission of MDRE in a public hospital in Pakistan. We investigated Enterobacterales containing resistance genes (blaCTX-M-15, blaNDM and blaOXA-48-like) for identification, antimicrobial susceptibility testing and whole-genome sequencing. Genotypes, phylogenetic relationships and transmission events for isolates from different sources were investigated using single-nucleotide polymorphism (SNP) analysis with a cut-off of ≤20 SNPs. Escherichia coli (14.3%), Klebsiella pneumoniae (10.9%) and Enterobacter cloacae (16.3%) were the main MDRE species isolated. The carbapenemase gene blaNDM was most commonly detected, with 15.5%, 15.1% and 13.3% of samples positive in SSIs, HSs and arthropods, respectively. SNP (≤20) and spatiotemporal analysis revealed linkages in bacteria between SSIs, HSs and arthropods supporting the One Health approach to underpin infection control policies across LMICs and control AMR.

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Fig. 1: Study flowchart.
Fig. 2: The distribution of resistance genes among HSs and species of arthropods represented as rose graphs.
Fig. 3: Antibiotic resistance profiles among different sources.
Fig. 4: E. coli phylogenetic and transmission analysis.
Fig. 5: E. cloacae phylogenetic and transmission analysis.

Data availability

Sequences reads have been submitted to the European Nucleotide Archive (ENA) under the project number PRJEB40861. A list of individual accession numbers is provided in Supplementary Data 2. The following databases were used: NCBI (https://github.com/tseemann/abricate/tree/master/db/ncbi); Resfinder v.4.0 (https://cge.cbs.dtu.dk/services/ResFinder/); Plasmidfinder v.2.0 (https://cge.cbs.dtu.dk/services/PlasmidFinder/); MLST v.2.0.4 (https://cge.cbs.dtu.dk/services/MLST/), with MLST allele and profile data from https://pubmlst.org; Serotype finder (https://bitbucket.org/genomicepidemiology/serotypefinder/src/master). Source data are provided with this paper.

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Acknowledgements

We acknowledge the staff at the Specialist Antimicrobial Chemotherapy Unit (SACU) for technical assistance for MALDI–TOF identification of isolates; the staff at Liofilchem (Roseto) for providing materials and consumables for the study; and the staff at the Wales Gene Park and ARCCA for providing support and infrastructure to perform bioinformatics analysis. We thank the team of curators of the databases at EnteroBase (https://enterobase.warwick.ac.uk/) and the Institute Pasteur MLST (https://bigsdb.pasteur.fr/) for curating the MLST datasets; and all of the staff at KTH, Peshawar, for their help with this study. This study was funded by Ser Cymru Life Science Research Network Wales.

Author information

Affiliations

Authors

Contributions

B.H. and T.R.W. designed and guided the study and analysis. M.I. and Asadullah Khan provided the epidemiological and clinical dataset and collected the samples in this study. B.H., K.S. and T.R.W. wrote the manuscript. B.H., G.-I.S., L.C., M.M.E.-B., G.L. and Afifah Khan performed microbiology culture and sample processing in Cardiff University. B.H., K.S. and E.P. performed WGS experiments. K.S. and B.H. performed bioinformatics analysis, following guidance from J.P. W.J.W. and B.H. performed statistical analysis.

Corresponding author

Correspondence to Brekhna Hassan.

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The authors declare no competing interests.

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Peer review information Nature Microbiology thanks Samuel Kariuki and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Prevalence of resistance genes from different sources and seasons.

Bar chart representing occurrence of blaNDM, blaOXA-48-like and blaCTX-M-15 among collected samples in percentage from arthropods (AR), SSI (surgical site infections) and hospital surfaces (HS) a. collective resistance prevalence; b. winter; c. summer.

Source data

Extended Data Fig. 2 Antibiotic resistance profiles of arthropods.

Antibiotic resistance profiles of the blaNDM and blaOXA-48-like positive isolates (n = 177) among different species of arthropods. Antibiotics are denoted as TGC = tigecycline; FOS = Fosfomycin; CIP = ciprofloxacin; CN = gentamycin; F = nitrofurantoin; AMC = amoxicillin-clavulanic acid; CTX = cefotaxime; CAZ = ceftazidime; FEP = cefepime; IPM = imipenem; MEM = meropenem; ATM = aztreonam; CS = colistin.

Source data

Extended Data Fig. 3 E. coli WGS results.

Figure showing samples source, STs, phylogroups, virulence score, antibiotic resistance genes and plasmid types among E. coli isolated from SSI, HS and arthropods (AR) samples. Sample source is identified by labelled symbols followed by STs, phylogroups and virulence score in text. Presence of antibiotic resistance genes are shown in pink and plasmid Inc groups in blue coloured squares.

Source data

Extended Data Fig. 4 E. cloacae WGS results.

Figure showing samples source, STs, virulence score, antibiotic resistance genes and plasmid types among E. cloacae isolated from SSI, HS and arthropods (AR) samples. Sample source is identified by labelled symbols followed by STs and virulence score in text. Presence of antibiotic resistance genes are shown in pink and plasmid Inc groups in blue coloured squares.

Source data

Extended Data Fig. 5 K. pneumoniae WGS results.

Figure showing samples source, STs, capsular types, virulence score, antibiotic resistance genes and plasmid types among K. pneumoniae isolated from SSI, HS and arthropods (AR) samples. Sample source is identified by labelled symbols followed by STs, capsular types and virulence score in text. Presence of antibiotic resistance genes are shown in pink and plasmid Inc groups in blue coloured squares.

Source data

Extended Data Fig. 6 K. pneumoniae phylogenetic and transmission analysis.

Phylogenetic and transmission analysis of K. pneumoniae. a, The core phylogenetic tree between samples derived from this study, including the reference genomes extracted from the NCBI database. The sources are shown as coloured circles on branches (SSIs from this study and clinical sample from databases (pink); arthropods from this study and animals originating from databases (blue); HSs from this study and environmental samples from databases (green)). ST and geographical location are displayed as text on the outside. Isolates of this study are labelled in red font and clades of ≥3 isolates from this study are shown in different coloured ranges. Missing information is denoted by NA (not available). b, The network chart between samples of different origins with ≤20 SNPs is shown. Connections between samples are represented by different styles of lines corresponding to the number of SNPs (0–5 (solid lines), 6–10 (dashed lines) and 11–20 (dotted lines) SNPs). The background colour represents the origin of the isolates (SSIs (pink); HSs (green) and arthropods (blue (cockroach) and orange (flies)) and the shape represents the ward of isolation (female (round) and male (rectangle)). The presence of target resistance genes for each sample is shown by the outline colour (blaCTX-M-15 (green), blaCTX-M-15 and blaNDM (black), blaCTX-M-15 and blaOXA-48-like (pink), blaNDM (red) and blaOXA-48-like (blue)). The exact location of the surfaces or species of insect is shown as text within the network edges.

Source data

Extended Data Fig. 7 SNP threshold sensitivity.

The histogram represents the number of transmission links at each SNP-cutoff point (0-50) among samples between SSI, HS and arthropods (AR) from isolates of a. E. coli, b. E. cloacae and c. K. pneumoniae.

Source data

Extended Data Fig. 8 Network chart of E. coli grouped by seasons.

The network chart between samples collected in summer and winter with <20 SNPs. Connections between samples are represented by different styles of lines corresponding to the number of SNPs (⎼⎼⎼ = 0 – 5, – ∙ – ∙ – = 6 – 10 and ∙ ∙∙∙∙∙∙∙∙ = 11– 20 SNPs). Colours of the edge represent the origin of the isolates (SSI: pink; HS: green and arthropods: blue and orange [cockroach: blue; ant: yellow; spider: purple and fly: orange] and shape represent ward of isolation (round: female and rectangle: male). The presence of target resistance genes for each sample are shown by outline colour of the edges (green: blaCTX-M-15, black: blaCTX-M-15 and blaNDM, pink: blaCTX-M-15 and blaOXA-48-like, red: blaNDM, blue: blaOXA-48-like). The exact location of surfaces or species of insect is shown as text within the network edges.

Source data

Extended Data Fig. 9 Network chart of K. pneumoniae grouped by seasons.

The network chart between samples collected in summer and winter with <20 SNPs. Connections between samples are represented by different styles of lines corresponding to the number of SNPs (⎼⎼⎼ = 0 – 5, – ∙ – ∙ – = 6 – 10 and ∙ ∙∙∙∙∙∙∙∙ = 11– 20 SNPs). Colours of the edge represent the origin of the isolates (SSI: pink; HS: green and arthropods: blue and orange [cockroach: blue; ant: yellow; spider: purple and fly: orange] and shape represent ward of isolation (round: female and rectangle: male). The presence of target resistance genes for each sample are shown by outline colour of the edges (green: blaCTX-M-15, black: blaCTX-M-15 and blaNDM, pink: blaCTX-M-15 and blaOXA-48-like, red: blaNDM, blue: blaOXA-48-like). The exact location of surfaces or species of insect is shown as text within the network edges.

Source data

Extended Data Fig. 10 Network chart of E. cloacae grouped by seasons.

The network chart between samples collected in summer and winter with <20 SNPs. Connections between samples are represented by different styles of lines corresponding to the number of SNPs (⎼⎼⎼ = 0 – 5, – ∙ – ∙ – = 6 – 10 and ∙ ∙∙∙∙∙∙∙∙ = 11– 20 SNPs). Colours of the edge represent the origin of the isolates (SSI: pink; HS: green and arthropods: blue and orange [cockroach: blue; ant: yellow; spider: purple and fly: orange] and shape represent ward of isolation (round: female and rectangle: male). The presence of target resistance genes for each sample are shown by outline colour of the edges (green: blaCTX-M-15, black: blaCTX-M-15 and blaNDM, pink: blaCTX-M-15 and blaOXA-48-like, red: blaNDM, blue: blaOXA-48-like). The exact location of surfaces or species of insect is shown as text within the network edges.

Source data

Supplementary information

Supplementary Information

Supplementary Figures 1-9, Supplementary Tables 1-6

Reporting Summary

Supplementary Data

Anonymised patient data

Supplementary Data

Accession Codes

Source data

Source Data Fig. 2

PCR results

Source Data Fig. 3

Antibiograms results

Source Data Fig. 4

Whole genomic sequencing and SNP analysis output (E. coli)

Source Data Fig. 5

Whole genomic sequencing and SNP analysis output (Enterobacter)

Source Data Extended Data Fig. 1

PCR results

Source Data Extended Data Fig. 2

Antibiograms results

Source Data Extended Data Fig. 3

Whole genomic sequence output (E. coli)

Source Data Extended Data Fig. 4

Whole genomic sequence output (Enterobacter)

Source Data Extended Data Fig. 5

Whole genomic sequence output (Klebsiella)

Source Data Extended Data Fig. 6

Whole genomic sequencing and SNP analysis output (Klebsiella)

Source Data Extended Data Fig. 7

SNP analysis output

Source Data Extended Data Fig. 8

SNP analysis output (E. coli)

Source Data Extended Data Fig. 9

SNP analysis output (Klebsiella)

Source Data Extended Data Fig. 10

SNP analysis output (Enterobacter)

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Hassan, B., Ijaz, M., Khan, A. et al. A role for arthropods as vectors of multidrug-resistant Enterobacterales in surgical site infections from South Asia. Nat Microbiol 6, 1259–1270 (2021). https://doi.org/10.1038/s41564-021-00965-1

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