A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings

This study aimed to compare antimicrobial resistance (AMR) in extended-spectrum cephalosporin-resistant and generic <i>Escherichia coli</i> from a One Health continuum of the beef production system in Alberta, Canada. A total of 705 extended-spectrum cephalosporin-resistant <i>E. c...

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Main Authors: Emelia H. Adator, Claudia Narvaez-Bravo, Rahat Zaheer, Shaun R. Cook, Lisa Tymensen, Sherry J. Hannon, Calvin W. Booker, Deirdre Church, Ron R. Read, Tim A. McAllister
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/8/6/885
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record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Emelia H. Adator
Claudia Narvaez-Bravo
Rahat Zaheer
Shaun R. Cook
Lisa Tymensen
Sherry J. Hannon
Calvin W. Booker
Deirdre Church
Ron R. Read
Tim A. McAllister
spellingShingle Emelia H. Adator
Claudia Narvaez-Bravo
Rahat Zaheer
Shaun R. Cook
Lisa Tymensen
Sherry J. Hannon
Calvin W. Booker
Deirdre Church
Ron R. Read
Tim A. McAllister
A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
Microorganisms
antimicrobial resistance
extended-spectrum beta-lactamase (ESBL)
one health
beef
sewage
author_facet Emelia H. Adator
Claudia Narvaez-Bravo
Rahat Zaheer
Shaun R. Cook
Lisa Tymensen
Sherry J. Hannon
Calvin W. Booker
Deirdre Church
Ron R. Read
Tim A. McAllister
author_sort Emelia H. Adator
title A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
title_short A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
title_full A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
title_fullStr A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
title_full_unstemmed A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical Settings
title_sort one health comparative assessment of antimicrobial resistance in generic and extended-spectrum cephalosporin-resistant <i>escherichia coli</i> from beef production, sewage and clinical settings
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2020-06-01
description This study aimed to compare antimicrobial resistance (AMR) in extended-spectrum cephalosporin-resistant and generic <i>Escherichia coli</i> from a One Health continuum of the beef production system in Alberta, Canada. A total of 705 extended-spectrum cephalosporin-resistant <i>E. coli</i> (ESC<sup>r</sup>) were obtained from: cattle feces (CFeces, <i>n</i> = 382), catch basins (CBasins, <i>n</i> = 137), surrounding streams (SStreams, <i>n</i> = 59), beef processing plants (BProcessing, <i>n</i> = 4), municipal sewage (MSewage; <i>n</i> = 98) and human clinical specimens (CHumans, <i>n</i> = 25). Generic isolates (663) included: CFeces (<i>n</i> = 142), CBasins (<i>n</i> = 185), SStreams (<i>n</i> = 81), BProcessing (<i>n</i> = 159) and MSewage (<i>n</i> = 96). All isolates were screened for antimicrobial susceptibility to 9 antimicrobials and two clavulanic acid combinations. In ESC<sup>r</sup><i>,</i> oxytetracycline (87.7%), ampicillin (84.4%) and streptomycin (73.8%) resistance phenotypes were the most common, with source influencing AMR prevalence (<i>p</i> < 0.001). In generic <i>E. coli,</i> oxytetracycline (51.1%), streptomycin (22.6%), ampicillin (22.5%) and sulfisoxazole (14.3%) resistance were most common. Overall, 88.8% of ESC<sup>r</sup>, and 26.7% of generic isolates exhibited multi-drug resistance (MDR). MDR in ESC<sup>r</sup> was high from all sources: CFeces (97.1%), MSewage (96.9%), CHumans (96%), BProcessing (100%), CBasins (70.5%) and SStreams (61.4%). MDR in generic <i>E. coli</i> was lower with CFeces (45.1%), CBasins (34.6%), SStreams (23.5%), MSewage (13.6%) and BProcessing (10.7%). ESBL phenotypes were confirmed in 24.7% (<i>n</i> = 174) ESC<sup>r</sup> and 0.6% of generic <i>E. coli</i>. Prevalence of <i>bla</i> genes in ESC<sup>r</sup> were <i>bla</i><sub>CTXM</sub> (30.1%), <i>bla</i><sub>CTXM-1</sub> (21.6%), <i>bla</i><sub>TEM</sub> (20%), <i>bla</i><sub>CTXM-9</sub> (7.9%), <i>bla</i><sub>OXA</sub> (3.0%), <i>bla</i><sub>CTXM-2</sub> (6.4%), <i>bla</i><sub>SHV</sub> (1.4%) and AmpC β-lactamase <i>bla</i><sub>CMY</sub> (81.3%). The lower AMR in ESC<sup>r</sup> from SStreams and BProcessing and higher AMR in CHumans and CFeces likely reflects antimicrobial use in these environments. Although MDR levels were higher in ESC<sup>r</sup> as compared to generic <i>E. coli</i>, AMR to the same antimicrobials ranked high in both ESC<sup>r</sup> and generic <i>E. coli</i> sub-populations. This suggests that both sub-populations reflect similar AMR trends and are equally useful for AMR surveillance. Considering that MDR ESC<sup>r</sup> MSewage isolates were obtained without enrichment, while those from CFeces were obtained with enrichment, MSewage may serve as a hot spot for MDR emergence and dissemination.
topic antimicrobial resistance
extended-spectrum beta-lactamase (ESBL)
one health
beef
sewage
url https://www.mdpi.com/2076-2607/8/6/885
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spelling doaj-06c33d81f12241db9e0f36769522cc5f2020-11-25T03:09:59ZengMDPI AGMicroorganisms2076-26072020-06-01888588510.3390/microorganisms8060885A One Health Comparative Assessment of Antimicrobial Resistance in Generic and Extended-Spectrum Cephalosporin-Resistant <i>Escherichia coli</i> from Beef Production, Sewage and Clinical SettingsEmelia H. Adator0Claudia Narvaez-Bravo1Rahat Zaheer2Shaun R. Cook3Lisa Tymensen4Sherry J. Hannon5Calvin W. Booker6Deirdre Church7Ron R. Read8Tim A. McAllister9Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, CanadaDepartment of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, CanadaLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB T1J 4B1, CanadaIrrigation and Farm Water Branch, Alberta Agriculture and Forestry, Lethbridge, AB T1J 4V6, CanadaIrrigation and Farm Water Branch, Alberta Agriculture and Forestry, Lethbridge, AB T1J 4V6, CanadaHealth Management Services Ltd, Okotoks, AB T1S 2A2, CanadaHealth Management Services Ltd, Okotoks, AB T1S 2A2, CanadaDepartment of Pathology & Laboratory Medicine and Medicine, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, CanadaDepartment of Pathology & Laboratory Medicine and Medicine, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, CanadaDepartment of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, CanadaThis study aimed to compare antimicrobial resistance (AMR) in extended-spectrum cephalosporin-resistant and generic <i>Escherichia coli</i> from a One Health continuum of the beef production system in Alberta, Canada. A total of 705 extended-spectrum cephalosporin-resistant <i>E. coli</i> (ESC<sup>r</sup>) were obtained from: cattle feces (CFeces, <i>n</i> = 382), catch basins (CBasins, <i>n</i> = 137), surrounding streams (SStreams, <i>n</i> = 59), beef processing plants (BProcessing, <i>n</i> = 4), municipal sewage (MSewage; <i>n</i> = 98) and human clinical specimens (CHumans, <i>n</i> = 25). Generic isolates (663) included: CFeces (<i>n</i> = 142), CBasins (<i>n</i> = 185), SStreams (<i>n</i> = 81), BProcessing (<i>n</i> = 159) and MSewage (<i>n</i> = 96). All isolates were screened for antimicrobial susceptibility to 9 antimicrobials and two clavulanic acid combinations. In ESC<sup>r</sup><i>,</i> oxytetracycline (87.7%), ampicillin (84.4%) and streptomycin (73.8%) resistance phenotypes were the most common, with source influencing AMR prevalence (<i>p</i> < 0.001). In generic <i>E. coli,</i> oxytetracycline (51.1%), streptomycin (22.6%), ampicillin (22.5%) and sulfisoxazole (14.3%) resistance were most common. Overall, 88.8% of ESC<sup>r</sup>, and 26.7% of generic isolates exhibited multi-drug resistance (MDR). MDR in ESC<sup>r</sup> was high from all sources: CFeces (97.1%), MSewage (96.9%), CHumans (96%), BProcessing (100%), CBasins (70.5%) and SStreams (61.4%). MDR in generic <i>E. coli</i> was lower with CFeces (45.1%), CBasins (34.6%), SStreams (23.5%), MSewage (13.6%) and BProcessing (10.7%). ESBL phenotypes were confirmed in 24.7% (<i>n</i> = 174) ESC<sup>r</sup> and 0.6% of generic <i>E. coli</i>. Prevalence of <i>bla</i> genes in ESC<sup>r</sup> were <i>bla</i><sub>CTXM</sub> (30.1%), <i>bla</i><sub>CTXM-1</sub> (21.6%), <i>bla</i><sub>TEM</sub> (20%), <i>bla</i><sub>CTXM-9</sub> (7.9%), <i>bla</i><sub>OXA</sub> (3.0%), <i>bla</i><sub>CTXM-2</sub> (6.4%), <i>bla</i><sub>SHV</sub> (1.4%) and AmpC β-lactamase <i>bla</i><sub>CMY</sub> (81.3%). The lower AMR in ESC<sup>r</sup> from SStreams and BProcessing and higher AMR in CHumans and CFeces likely reflects antimicrobial use in these environments. Although MDR levels were higher in ESC<sup>r</sup> as compared to generic <i>E. coli</i>, AMR to the same antimicrobials ranked high in both ESC<sup>r</sup> and generic <i>E. coli</i> sub-populations. This suggests that both sub-populations reflect similar AMR trends and are equally useful for AMR surveillance. Considering that MDR ESC<sup>r</sup> MSewage isolates were obtained without enrichment, while those from CFeces were obtained with enrichment, MSewage may serve as a hot spot for MDR emergence and dissemination.https://www.mdpi.com/2076-2607/8/6/885antimicrobial resistanceextended-spectrum beta-lactamase (ESBL)one healthbeefsewage