Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry

Timothy J. Johnson, Catherine M. Logue, James R. Johnson, Michael A. Kuskowski, Julie S. Sherwood, H. John Barnes, Chitrita Debroy, Yvonne M. Wannemuehler, Mana Obata-Yasuoka, Lodewijk Spanjaard, Lisa K. Nolan

Research output: Contribution to journalArticle

56 Citations (Scopus)

Abstract

The emergence of plasmid-mediated multidrug resistance (MDR) among enteric bacteria presents a serious challenge to the treatment of bacterial infections in humans and animals. Recent studies suggest that avian Escherichia coli commonly possess the ability to resist multiple antimicrobial agents, and might serve as reservoirs of MDR for human extraintestinal pathogenic Escherichia coli (ExPEC) and commensal E. coli populations. We determined antimicrobial susceptibility profiles for 2202 human and avian E. coli isolates, then sought for associations among resistance profile, plasmid content, virulence factor profile, and phylogenetic group. Avian-source isolates harbored greater proportions of MDR than their human counterparts, and avian ExPEC had higher proportions of MDR than did avian commensal E. coli. MDR was significantly associated with possession of the IncA/C, IncP1-α, IncF, and IncI1 plasmid types. Overall, inferred virulence potential did not correlate with drug susceptibility phenotype. However, certain virulence genes were positively associated with MDR, including ireA, ibeA, fyuA, cvaC, iss, iutA, iha, and afa. According to the total dataset, isolates segregated significantly according to host species and clinical status, thus suggesting that avian and human ExPEC and commensal E. coli represent four distinct populations with limited overlap. These findings suggest that in extraintestinal E. coli, MDR is most commonly associated with plasmids, and that these plasmids are frequently found among avian-source E. coli from poultry production systems.

Original languageEnglish (US)
Pages (from-to)37-46
Number of pages10
JournalFoodborne pathogens and disease
Volume9
Issue number1
DOIs
StatePublished - Jan 1 2012

Fingerprint

multiple drug resistance
Multiple Drug Resistance
Poultry
Virulence
plasmids
poultry
Plasmids
virulence
Escherichia coli
anti-infective agents
Virulence Factors
Enterobacteriaceae
Anti-Infective Agents
Extraintestinal Pathogenic Escherichia coli
Bacterial Infections
Population
poultry production
bacterial infections
intestinal microorganisms
Phenotype

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Applied Microbiology and Biotechnology
  • Food Science
  • Animal Science and Zoology

Cite this

Johnson, Timothy J. ; Logue, Catherine M. ; Johnson, James R. ; Kuskowski, Michael A. ; Sherwood, Julie S. ; Barnes, H. John ; Debroy, Chitrita ; Wannemuehler, Yvonne M. ; Obata-Yasuoka, Mana ; Spanjaard, Lodewijk ; Nolan, Lisa K. / Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry. In: Foodborne pathogens and disease. 2012 ; Vol. 9, No. 1. pp. 37-46.
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abstract = "The emergence of plasmid-mediated multidrug resistance (MDR) among enteric bacteria presents a serious challenge to the treatment of bacterial infections in humans and animals. Recent studies suggest that avian Escherichia coli commonly possess the ability to resist multiple antimicrobial agents, and might serve as reservoirs of MDR for human extraintestinal pathogenic Escherichia coli (ExPEC) and commensal E. coli populations. We determined antimicrobial susceptibility profiles for 2202 human and avian E. coli isolates, then sought for associations among resistance profile, plasmid content, virulence factor profile, and phylogenetic group. Avian-source isolates harbored greater proportions of MDR than their human counterparts, and avian ExPEC had higher proportions of MDR than did avian commensal E. coli. MDR was significantly associated with possession of the IncA/C, IncP1-α, IncF, and IncI1 plasmid types. Overall, inferred virulence potential did not correlate with drug susceptibility phenotype. However, certain virulence genes were positively associated with MDR, including ireA, ibeA, fyuA, cvaC, iss, iutA, iha, and afa. According to the total dataset, isolates segregated significantly according to host species and clinical status, thus suggesting that avian and human ExPEC and commensal E. coli represent four distinct populations with limited overlap. These findings suggest that in extraintestinal E. coli, MDR is most commonly associated with plasmids, and that these plasmids are frequently found among avian-source E. coli from poultry production systems.",
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Johnson, TJ, Logue, CM, Johnson, JR, Kuskowski, MA, Sherwood, JS, Barnes, HJ, Debroy, C, Wannemuehler, YM, Obata-Yasuoka, M, Spanjaard, L & Nolan, LK 2012, 'Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry', Foodborne pathogens and disease, vol. 9, no. 1, pp. 37-46. https://doi.org/10.1089/fpd.2011.0961

Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry. / Johnson, Timothy J.; Logue, Catherine M.; Johnson, James R.; Kuskowski, Michael A.; Sherwood, Julie S.; Barnes, H. John; Debroy, Chitrita; Wannemuehler, Yvonne M.; Obata-Yasuoka, Mana; Spanjaard, Lodewijk; Nolan, Lisa K.

In: Foodborne pathogens and disease, Vol. 9, No. 1, 01.01.2012, p. 37-46.

Research output: Contribution to journalArticle

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T1 - Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry

AU - Johnson, Timothy J.

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AU - Johnson, James R.

AU - Kuskowski, Michael A.

AU - Sherwood, Julie S.

AU - Barnes, H. John

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AU - Wannemuehler, Yvonne M.

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AU - Spanjaard, Lodewijk

AU - Nolan, Lisa K.

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N2 - The emergence of plasmid-mediated multidrug resistance (MDR) among enteric bacteria presents a serious challenge to the treatment of bacterial infections in humans and animals. Recent studies suggest that avian Escherichia coli commonly possess the ability to resist multiple antimicrobial agents, and might serve as reservoirs of MDR for human extraintestinal pathogenic Escherichia coli (ExPEC) and commensal E. coli populations. We determined antimicrobial susceptibility profiles for 2202 human and avian E. coli isolates, then sought for associations among resistance profile, plasmid content, virulence factor profile, and phylogenetic group. Avian-source isolates harbored greater proportions of MDR than their human counterparts, and avian ExPEC had higher proportions of MDR than did avian commensal E. coli. MDR was significantly associated with possession of the IncA/C, IncP1-α, IncF, and IncI1 plasmid types. Overall, inferred virulence potential did not correlate with drug susceptibility phenotype. However, certain virulence genes were positively associated with MDR, including ireA, ibeA, fyuA, cvaC, iss, iutA, iha, and afa. According to the total dataset, isolates segregated significantly according to host species and clinical status, thus suggesting that avian and human ExPEC and commensal E. coli represent four distinct populations with limited overlap. These findings suggest that in extraintestinal E. coli, MDR is most commonly associated with plasmids, and that these plasmids are frequently found among avian-source E. coli from poultry production systems.

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