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. 2022 Aug 9;88(15):e0083722.
doi: 10.1128/aem.00837-22. Epub 2022 Jul 12.

Extended Spectrum β-Lactamase Activity and Cephalosporin Resistance in Escherichia coli from U.S. Mid-Atlantic Surface and Reclaimed Water

Sultana Solaiman  1 , Eric Handy  2 , Taylor Brinks  1 , Kasey Goon  1 , Chris Bollinger  1 , Amy R Sapkota  3 , Manan Sharma  2 , Shirley A Micallef  1   4
Affiliations

Extended Spectrum β-Lactamase Activity and Cephalosporin Resistance in Escherichia coli from U.S. Mid-Atlantic Surface and Reclaimed Water

Sultana Solaiman et al. Appl Environ Microbiol. .

Abstract

Phylogenetic distribution and extended spectrum β-lactamase (ESBL) activity of Escherichia coli recovered from surface and reclaimed water in the mid-Atlantic U.S. were evaluated. Among 488 isolates, phylogroups B1 and A were the most and least prevalent, respectively. Water type, but not season, affected phylogroup distribution. The likelihood of detecting group A isolates was higher in reclaimed than pond (P < 0.01), freshwater river (P < 0.01) or brackish river (P < 0.05) water. Homogeneity in group distribution was lowest in pond water, where group B1 comprised 50% of isolates. Only 16 (3.3%) isolates exhibited phenotypic resistance to one or more cephalosporins tested and only four had ESBL activity, representing groups B1, B2 isolates, and D. Phylogroup was a factor in antimicrobial resistance (P < 0.05), with group A (8.7%) and D (1.6%) exhibiting the highest and lowest rates. Resistance to cefoxitin was the most prevalent. Multi- versus single drug resistance was affected by phylogroup (P < 0.05) and more likely in groups D and B1 than A which carried resistance to cefoxitin only. The most detected β-lactam resistance genes were blaCMY-2 and blaTEM. Water type was a factor for blaCTX-M gene detection (P < 0.05). Phenotypic resistance to cefotaxime, ceftriaxone, cefuroxime and ceftazidime, and genetic determinants for ESBL-mediated resistance were found predominantly in B2 and D isolates from rivers and reclaimed water. Overall, ESBL activity and cephalosporin resistance in reclaimed and surface water isolates were low. Integrating data on ESBL activity and β-lactam resistance among E. coli populations can inform decisions on safety of irrigation water sources and One Health. IMPORTANCE Extended spectrum β-lactamase (ESBL) producing bacteria, that are resistant to a broad range of antimicrobial agents, are spreading in the environment but data remain scarce. ESBL-producing Escherichia coli infections in the community are on the rise. This work was conducted to assess presence of ESBL-producing E. coli in water that could be used for irrigation of fresh produce. The study provides the most extensive evaluation of ESBL-producing E. coli in surface and reclaimed water in the mid-Atlantic United States. The prevalence of ESBL producers was low and phenotypic resistance to cephalosporins (types of β-lactam antibiotics) was affected by season but not water type. Data on antimicrobial resistance among E. coli populations in water can inform decisions on safety of irrigation water sources and One Health.

Keywords: ESBL-producing Escherichia coli; antimicrobial resistance genes; cephalosporin resistance; irrigation water; reclaimed wastewater for irrigation; β-lactam resistance.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIG 1
FIG 1
Distribution of different phylogenetic groups of E. coli by (A) surface and reclaimed water sources and (B) season. The mosaic plots display the % frequency in four water types: five non-tidal freshwater rivers (NF), one tidal brackish river water (TB), two on-farm ponds (PW), and three reclaimed water (RW) sites.
FIG 2
FIG 2
Cephalosporin resistance (% frequency) among 16 E. coli isolates by phylogroup. For each antibiotic, n denotes number of isolates resistant to that antibiotic.
FIG 3
FIG 3
Multiple correspondence analysis (MCA) plot showing the relationships between phylogenetic groups of E. coli (number of isolates = 16), their phenotypic resistance traits and carriage of β-lactam antibiotic resistance genes, and season of collection and water source. Presence or absence (+/−) of each gene, blaTEM, blaSHV, blaCTX-M, blaCMY-1, blaCMY-2, blaOXA-1, blaOXA-2 were denoted as tem, shv, ctxM, cmy1, cmy2, oxa1 and oxa2, respectively.
FIG 4
FIG 4
Hierarchical cluster analysis (HCA; group average method using simple matching coefficient) of resistant E. coli isolates based on profiles of phenotypic resistance to ceftazidime, ceftriaxone, cefotaxime, cefuroxime and cefoxitin, and genotypic resistance based on detection of genes blaTEM, blaSHV, blaCTX-M, blaCMY-1, blaCMY-2, blaOXA-1 and blaOXA-2, by phylogenetic group (A, B1, B2 and D), water type (non-tidal freshwater rivers [NF], tidal brackish river [TB]; on-farm ponds [PW] and reclaimed water [RW]), and season of collection.
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