Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses

Previous research identified veterinary clinics as hotspots with respect to accumulation and spread of multidrug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (EC). Therefore, promoting the prudent use of antibiotics to decrease selective pressure in that particular clini...

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Main Authors: Anne Kauter, Lennard Epping, Fereshteh Ghazisaeedi, Antina Lübke-Becker, Silver A. Wolf, Dania Kannapin, Sabita D. Stoeckle, Torsten Semmler, Sebastian Günther, Heidrun Gehlen, Birgit Walther
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.671676/full
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author Anne Kauter
Lennard Epping
Fereshteh Ghazisaeedi
Antina Lübke-Becker
Silver A. Wolf
Dania Kannapin
Sabita D. Stoeckle
Torsten Semmler
Sebastian Günther
Heidrun Gehlen
Birgit Walther
author_facet Anne Kauter
Lennard Epping
Fereshteh Ghazisaeedi
Antina Lübke-Becker
Silver A. Wolf
Dania Kannapin
Sabita D. Stoeckle
Torsten Semmler
Sebastian Günther
Heidrun Gehlen
Birgit Walther
author_sort Anne Kauter
collection DOAJ
description Previous research identified veterinary clinics as hotspots with respect to accumulation and spread of multidrug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (EC). Therefore, promoting the prudent use of antibiotics to decrease selective pressure in that particular clinical environment is preferable to enhance biosecurity for animal patients and hospital staff. Accordingly, this study comparatively investigated the impact of two distinct perioperative antibiotic prophylaxis (PAP) regimens (short-term versus prolonged) on ESBL-EC carriage of horses subjected to colic surgery. While all horses received a combination of penicillin/gentamicin (P/G) as PAP, they were assigned to either the “single-shot group” (SSG) or the conventional “5-day group” (5DG). Fecal samples collected on arrival (t0), on the 3rd (t1) and on the 10th day after surgery (t2) were screened for ESBL-EC. All isolates were further investigated using whole genome sequences. In total, 81 of 98 horses met the inclusion criteria for this study. ESBL-EC identified in samples available at t0, t1 and t2 were 4.8% (SSG) and 9.7% (5DG), 37% (SSG) and 47.2% (5DG) as well as 55.6% (SSG) and 56.8% (5DG), respectively. Regardless of the P/G PAP regimen, horses were 9.12 times (95% CI 2.79–29.7) more likely to carry ESBL-EC at t1 compared to t0 (p < 0.001) and 15.64 times (95% CI 4.57–53.55) more likely to carry ESBL-EC at t2 compared to t0 (p < 0.001). ESBL-EC belonging to sequence type (ST) 10, ST86, ST641, and ST410 were the most prevalent lineages, with blaCTX–M–1 (60%) being the dominant ESBL gene. A close spatio-temporal relationship between isolates sharing a particular ST was revealed by genome analysis, strongly indicating local spread. Consequently, hospitalization itself has a strong impact on ESBL-EC isolation rates in horses, possibly masking differences between distinct PAP regimens. The results of this study reveal accumulation and spread of multi-drug resistant ESBL-EC among horses subjected to colic surgery with different P/G PAP regimens, challenging the local hygiene management system and work-place safety of veterinary staff. Moreover, the predominance of particular ESBL-EC lineages in clinics providing health care for horses needs further investigation.
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spelling doaj.art-e2015e2139594691b11667905755a5a62022-12-21T23:45:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-04-011210.3389/fmicb.2021.671676671676Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized HorsesAnne Kauter0Lennard Epping1Fereshteh Ghazisaeedi2Antina Lübke-Becker3Silver A. Wolf4Dania Kannapin5Sabita D. Stoeckle6Torsten Semmler7Sebastian Günther8Heidrun Gehlen9Birgit Walther10Advanced Light and Electron Microscopy (ZBS-4), Robert Koch Institute, Berlin, GermanyGenome Sequencing and Genomic Epidemiology (MF2), Robert Koch Institute, Berlin, GermanyCentre for Infection Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, GermanyCentre for Infection Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, GermanyGenome Sequencing and Genomic Epidemiology (MF2), Robert Koch Institute, Berlin, GermanyEquine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, GermanyEquine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, GermanyGenome Sequencing and Genomic Epidemiology (MF2), Robert Koch Institute, Berlin, GermanyInstitute of Pharmacy, Universität Greifswald, Greifswald, GermanyEquine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, GermanyAdvanced Light and Electron Microscopy (ZBS-4), Robert Koch Institute, Berlin, GermanyPrevious research identified veterinary clinics as hotspots with respect to accumulation and spread of multidrug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (EC). Therefore, promoting the prudent use of antibiotics to decrease selective pressure in that particular clinical environment is preferable to enhance biosecurity for animal patients and hospital staff. Accordingly, this study comparatively investigated the impact of two distinct perioperative antibiotic prophylaxis (PAP) regimens (short-term versus prolonged) on ESBL-EC carriage of horses subjected to colic surgery. While all horses received a combination of penicillin/gentamicin (P/G) as PAP, they were assigned to either the “single-shot group” (SSG) or the conventional “5-day group” (5DG). Fecal samples collected on arrival (t0), on the 3rd (t1) and on the 10th day after surgery (t2) were screened for ESBL-EC. All isolates were further investigated using whole genome sequences. In total, 81 of 98 horses met the inclusion criteria for this study. ESBL-EC identified in samples available at t0, t1 and t2 were 4.8% (SSG) and 9.7% (5DG), 37% (SSG) and 47.2% (5DG) as well as 55.6% (SSG) and 56.8% (5DG), respectively. Regardless of the P/G PAP regimen, horses were 9.12 times (95% CI 2.79–29.7) more likely to carry ESBL-EC at t1 compared to t0 (p < 0.001) and 15.64 times (95% CI 4.57–53.55) more likely to carry ESBL-EC at t2 compared to t0 (p < 0.001). ESBL-EC belonging to sequence type (ST) 10, ST86, ST641, and ST410 were the most prevalent lineages, with blaCTX–M–1 (60%) being the dominant ESBL gene. A close spatio-temporal relationship between isolates sharing a particular ST was revealed by genome analysis, strongly indicating local spread. Consequently, hospitalization itself has a strong impact on ESBL-EC isolation rates in horses, possibly masking differences between distinct PAP regimens. The results of this study reveal accumulation and spread of multi-drug resistant ESBL-EC among horses subjected to colic surgery with different P/G PAP regimens, challenging the local hygiene management system and work-place safety of veterinary staff. Moreover, the predominance of particular ESBL-EC lineages in clinics providing health care for horses needs further investigation.https://www.frontiersin.org/articles/10.3389/fmicb.2021.671676/fullhorseESBLEscherichia coliantibiotic resistancemultidrug resistantspread
spellingShingle Anne Kauter
Lennard Epping
Fereshteh Ghazisaeedi
Antina Lübke-Becker
Silver A. Wolf
Dania Kannapin
Sabita D. Stoeckle
Torsten Semmler
Sebastian Günther
Heidrun Gehlen
Birgit Walther
Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
Frontiers in Microbiology
horse
ESBL
Escherichia coli
antibiotic resistance
multidrug resistant
spread
title Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
title_full Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
title_fullStr Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
title_full_unstemmed Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
title_short Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses
title_sort frequency local dynamics and genomic characteristics of esbl producing escherichia coli isolated from specimens of hospitalized horses
topic horse
ESBL
Escherichia coli
antibiotic resistance
multidrug resistant
spread
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.671676/full
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