scholarly journals Evolutionary History of the Global Emergence of the Escherichia coli Epidemic Clone ST131

mBio ◽  
2016 ◽  
Vol 7 (2) ◽  
Author(s):  
Nicole Stoesser ◽  
Anna E. Sheppard ◽  
Louise Pankhurst ◽  
Nicola De Maio ◽  
Catrin E. Moore ◽  
...  

ABSTRACT Escherichia coli sequence type 131 (ST131) has emerged globally as the most predominant extraintestinal pathogenic lineage within this clinically important species, and its association with fluoroquinolone and extended-spectrum cephalosporin resistance impacts significantly on treatment. The evolutionary histories of this lineage, and of important antimicrobial resistance elements within it, remain unclearly defined. This study of the largest worldwide collection ( n = 215) of sequenced ST131 E. coli isolates to date demonstrates that the clonal expansion of two previously recognized antimicrobial-resistant clades, C1/ H 30R and C2/ H 30Rx, started around 25 years ago, consistent with the widespread introduction of fluoroquinolones and extended-spectrum cephalosporins in clinical medicine. These two clades appear to have emerged in the United States, with the expansion of the C2/ H 30Rx clade driven by the acquisition of a bla CTX-M-15 -containing IncFII-like plasmid that has subsequently undergone extensive rearrangement. Several other evolutionary processes influencing the trajectory of this drug-resistant lineage are described, including sporadic acquisitions of CTX-M resistance plasmids and chromosomal integration of bla CTX-M within subclusters followed by vertical evolution. These processes are also occurring for another family of CTX-M gene variants more recently observed among ST131, the bla CTX-M-14/14-like group. The complexity of the evolutionary history of ST131 has important implications for antimicrobial resistance surveillance, epidemiological analysis, and control of emerging clinical lineages of E. coli . These data also highlight the global imperative to reduce specific antibiotic selection pressures and demonstrate the important and varied roles played by plasmids and other mobile genetic elements in the perpetuation of antimicrobial resistance within lineages. IMPORTANCE Escherichia coli , perennially a major bacterial pathogen, is becoming increasingly difficult to manage due to emerging resistance to all preferred antimicrobials. Resistance is concentrated within specific E. coli lineages, such as sequence type 131 (ST131). Clarification of the genetic basis for clonally associated resistance is key to devising intervention strategies. We used high-resolution genomic analysis of a large global collection of ST131 isolates to define the evolutionary history of extended-spectrum beta-lactamase production in ST131. We documented diverse contributory genetic processes, including stable chromosomal integrations of resistance genes, persistence and evolution of mobile resistance elements within sublineages, and sporadic acquisition of different resistance elements. Both global distribution and regional segregation were evident. The diversity of resistance element acquisition and propagation within ST131 indicates a need for control and surveillance strategies that target both bacterial strains and mobile genetic elements.

2015 ◽  
Author(s):  
Nicole Stoesser ◽  
Anna Sheppard ◽  
Louise Pankhurst ◽  
Nicola de Maio ◽  
Catrin E Moore ◽  
...  

ABSTRACT Background Escherichia coli sequence type 131 (ST131) has emerged globally as the most predominant lineage within this clinically important species, and its association with fluoroquinolone and extended-spectrum cephalosporin resistance impacts significantly on treatment. The evolutionary histories of this lineage, and of important antimicrobial resistance elements within it, remain unclearly defined. Results This study of the largest worldwide collection (n = 215) of sequenced ST131 E. coli isolates to date demonstrates that clonal expansion of two previously recognized antimicrobial-resistant clades, C1/H30R and C2/H30Rx, started around 25 years ago, consistent with the widespread introduction of fluoroquinolones and extended-spectrum cephalosporins in clinical medicine. These two clades appear to have emerged in the United States, with the expansion of the C2/H30Rx clade driven by the acquisition of a blaCTX-M-15-containing IncFII-like plasmid that has subsequently undergone extensive rearrangement. Several other evolutionary processes influencing the trajectory of this drug-resistant lineage are described, including sporadic acquisitions of CTX-M resistance plasmids, and chromosomal integration of blaCTX-M within sub-clusters followed by vertical evolution. These processes are also occurring for another family of CTX-M gene variants more recently observed amongst ST131, the blaCTX-M-14/14-like group. Conclusions The complexity of the evolutionary history of ST131 has important implications for antimicrobial resistance surveillance, epidemiological analysis, and control of emerging clinical lineages of E. coli. These data also highlight the global imperative to reduce specific antibiotic selection pressures, and demonstrate the important and varied roles played by plasmids and other mobile genetic elements in the perpetuation of antimicrobial resistance within lineages.


2012 ◽  
Vol 56 (5) ◽  
pp. 2364-2370 ◽  
Author(s):  
James R. Johnson ◽  
Carl Urban ◽  
Scott J. Weissman ◽  
James H. Jorgensen ◽  
James S. Lewis ◽  
...  

ABSTRACTEscherichia colisequence type ST131 (from phylogenetic group B2), often carrying the extended-spectrum-β-lactamase (ESBL) geneblaCTX-M-15, is an emerging globally disseminated pathogen that has received comparatively little attention in the United States. Accordingly, a convenience sample of 351 ESBL-producingE. coliisolates from 15 U.S. centers (collected in 2000 to 2009) underwent PCR-based phylotyping and detection of ST131 andblaCTX-M-15. A total of 200 isolates, comprising 4 groups of 50 isolates each that were (i)blaCTX-M-15negative non-ST131, (ii)blaCTX-M-15positive non-ST131, (iii)blaCTX-M-15negative ST131, or (iv)blaCTX-M-15positive ST131, also underwent virulence genotyping, antimicrobial susceptibility testing, and pulsed-field gel electrophoresis (PFGE). Overall, 201 (57%) isolates exhibitedblaCTX-M-15, whereas 165 (47%) were ST131. ST131 accounted for 56% ofblaCTX-M-15-positive- versus 35% ofblaCTX-M-15-negative isolates (P< 0.001). Whereas ST131 accounted for 94% of the 175 total group B2 isolates, non-ST131 isolates were phylogenetically distributed byblaCTX-M-15status, with groups A (blaCTX-M-15-positive isolates) and D (blaCTX-M-15-negative isolates) predominating. BothblaCTX-M-15and ST131 occurred at all participating centers, were recovered from children and adults, increased significantly in prevalence post-2003, and were associated with molecularly inferred virulence. Compared with non-ST131 isolates, ST131 isolates had higher virulence scores, distinctive virulence profiles, and more-homogeneous PFGE profiles.blaCTX-M-15was associated with extensive antimicrobial resistance and ST131 with fluoroquinolone resistance. Thus,E. coliST131 andblaCTX-M-15are emergent, widely distributed, and predominant among ESBL-positiveE. colistrains in the United States, among children and adults alike. Enhanced virulence and antimicrobial resistance have likely promoted the epidemiological success of these emerging public health threats.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Pimlapas Leekitcharoenphon ◽  
Markus Hans Kristofer Johansson ◽  
Patrick Munk ◽  
Burkhard Malorny ◽  
Magdalena Skarżyńska ◽  
...  

AbstractThe emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.


mBio ◽  
2013 ◽  
Vol 4 (6) ◽  
Author(s):  
Lance B. Price ◽  
James R. Johnson ◽  
Maliha Aziz ◽  
Connie Clabots ◽  
Brian Johnston ◽  
...  

ABSTRACT The Escherichia coli sequence type 131 (ST131) clone is notorious for extraintestinal infections, fluoroquinolone resistance, and extended-spectrum beta-lactamase (ESBL) production, attributable to a CTX-M-15-encoding mobile element. Here, we applied pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing to reconstruct the evolutionary history of the ST131 clone. PFGE-based cluster analyses suggested that both fluoroquinolone resistance and ESBL production had been acquired by multiple ST131 sublineages through independent genetic events. In contrast, the more robust whole-genome-sequence-based phylogenomic analysis revealed that fluoroquinolone resistance was confined almost entirely to a single, rapidly expanding ST131 subclone, designated H30-R. Strikingly, 91% of the CTX-M-15-producing isolates also belonged to a single, well-defined clade nested within H30-R, which was named H30-Rx due to its more extensive resistance. Despite its tight clonal relationship with H30Rx, the CTX-M-15 mobile element was inserted variably in plasmid and chromosomal locations within the H30-Rx genome. Screening of a large collection of recent clinical E. coli isolates both confirmed the global clonal expansion of H30-Rx and revealed its disproportionate association with sepsis (relative risk, 7.5; P < 0.001). Together, these results suggest that the high prevalence of CTX-M-15 production among ST131 isolates is due primarily to the expansion of a single, highly virulent subclone, H30-Rx. IMPORTANCE We applied an advanced genomic approach to study the recent evolutionary history of one of the most important Escherichia coli strains in circulation today. This strain, called sequence type 131 (ST131), causes multidrug-resistant bladder, kidney, and bloodstream infections around the world. The rising prevalence of antibiotic resistance in E. coli is making these infections more difficult to treat and is leading to increased mortality. Past studies suggested that many different ST131 strains gained resistance to extended-spectrum cephalosporins independently. In contrast, our research indicates that most extended-spectrum-cephalosporin-resistant ST131 strains belong to a single highly pathogenic subclone, called H30-Rx. The clonal nature of H30-Rx may provide opportunities for vaccine or transmission prevention-based control strategies, which could gain importance as H30-Rx and other extraintestinal pathogenic E. coli subclones become resistant to our best antibiotics.


2017 ◽  
Vol 4 (2) ◽  
Author(s):  
James R. Johnson ◽  
Stephen Porter ◽  
Paul Thuras ◽  
Mariana Castanheira

Abstract Background Extraintestinal Escherichia coli infections are increasingly challenging due to emerging antimicrobial resistance, including resistance to extended-spectrum beta-lactams and fluoroquinolones. Sequence type 131 (ST131) is a leading contributor. Methods Three hundred sixty E. coli clinical isolates from across the United States (2011–2012), selected randomly from the SENTRY collection within 3 resistance categories (extended-spectrum cephalosporin [ECS]–reduced susceptibility [RS]; fluoroquinolone-resistant, ESC-susceptible; and fluoroquinolone-susceptible, ESC-susceptible) were typed for phylogroup, sequence type complex (STc), subsets thereof, virulence genotype, O type, and beta-lactamase genes. Molecular results were compared with susceptibility profile, specimen type, age, and sex. Results Phylogroup B2 accounted for most isolates, especially fluoroquinolone-resistant isolates (83%). Group B2–derived ST131 and its H30 subclone (divided between H30Rx and H30R1) predominated, especially among ESC-RS and fluoroquinolone-resistant isolates. In contrast, among fluoroquinolone-susceptible isolates, group B2–derived STc73 and STc95 predominated. Within each resistance category, ST131 isolates exhibited more extensive resistance and/or virulence profiles than non-ST131 isolates. ST131-H30 was distributed broadly by geographical region, age, and specimen type and exhibited distinctive beta-lactamase genes. Back-calculations indicated that within the source population ST131 accounted for 26.4% of isolates overall (vs 17% in 2007), including 19.8% ST131-H30, 13.2% ST131-H30R1, and 6.6% each ST131-H30Rx and non-H30 ST131. Conclusions ST131-H30, with its ESC resistance-associated H30Rx subset, caused most antimicrobial-resistant E. coli infections across the United States in 2011–2012 and, since 2007, increased in relative prevalence by &gt;50%. Focused attention to this strain could help combat the current E. coli resistance epidemic.


2020 ◽  
Vol 83 (7) ◽  
pp. 1115-1124
Author(s):  
MIN-HYEOK CHA ◽  
JAE-GEE RYU ◽  
YOUNG-MIN CHI ◽  
GUN-JO WOO

ABSTRACT This study was conducted to characterize Escherichia coli strains and evaluate the spread of antimicrobial resistance among these strains from fresh produce and farm environments in Korea. We then conducted phenotypic and genetic studies on antimicrobial-resistant isolates. We determined the genetic epidemiological characteristics of isolates that produced extended-spectrum β-lactamase (ESBL) and confirmed plasmid transfer in isolates that carried blaCTX-M-type genes. E. coli strains were isolated from 8 samples of fresh produce and 152 samples from the farm environment collected from May 2014 to June 2016. Cephalosporin resistance was the most prevalent (61.8%) type of resistance among the isolates. Five ESBL-producing strains with high genetic homology with E. coli of human or livestock origin were identified. Lateral transfer of plasmids harboring blaCTX-M-type genes to transconjugants was successful. Two isolates from Chinese cabbage and from water samples collected from a nearby stream harbored the ISEcp1-blaCTX-M-55-orf477 operon and were confirmed as sequence type 1196 and the same type of plasmid replicon, suggesting that cross-contamination was highly likely. A high-risk clone of sequence type 69 (clonal complex 69) isolates was also recovered from the farm environment. This study provides genetic evidence that antimicrobial resistance factors in E. coli from farm environments originate in the clinic or in livestock, highlighting the fact that good agricultural practices in farming are important to inhibit the spread of antimicrobial resistance to bacteria on fresh produce. HIGHLIGHTS


2013 ◽  
Vol 57 (12) ◽  
pp. 6385-6388 ◽  
Author(s):  
Ritu Banerjee ◽  
Ari Robicsek ◽  
Michael A. Kuskowski ◽  
Stephen Porter ◽  
Brian D. Johnston ◽  
...  

ABSTRACTWe assessedEscherichia coliST131 and its H30 and H30-Rx subclones for virulence genes, antimicrobial resistance, and extended-spectrum beta-lactamase (ESBL) type. Although both subclones were associated with ESBL production, H30-Rx isolates had higher resistance scores and were associated specifically with CTX-M-15. Three virulence genes (iha,sat, andiutA) were more prevalent among H30 than non-H30 ST131 isolates. Thus, the H30 and H30-Rx subclones are more antimicrobial resistant and have virulence profiles that are distinct from those of non-H30 ST131 isolates.


2020 ◽  
Vol 8 (6) ◽  
pp. 885 ◽  
Author(s):  
Emelia H. Adator ◽  
Claudia Narvaez-Bravo ◽  
Rahat Zaheer ◽  
Shaun R. Cook ◽  
Lisa Tymensen ◽  
...  

This study aimed to compare antimicrobial resistance (AMR) in extended-spectrum cephalosporin-resistant and generic Escherichia coli from a One Health continuum of the beef production system in Alberta, Canada. A total of 705 extended-spectrum cephalosporin-resistant E. coli (ESCr) were obtained from: cattle feces (CFeces, n = 382), catch basins (CBasins, n = 137), surrounding streams (SStreams, n = 59), beef processing plants (BProcessing, n = 4), municipal sewage (MSewage; n = 98) and human clinical specimens (CHumans, n = 25). Generic isolates (663) included: CFeces (n = 142), CBasins (n = 185), SStreams (n = 81), BProcessing (n = 159) and MSewage (n = 96). All isolates were screened for antimicrobial susceptibility to 9 antimicrobials and two clavulanic acid combinations. In ESCr, oxytetracycline (87.7%), ampicillin (84.4%) and streptomycin (73.8%) resistance phenotypes were the most common, with source influencing AMR prevalence (p < 0.001). In generic E. coli, oxytetracycline (51.1%), streptomycin (22.6%), ampicillin (22.5%) and sulfisoxazole (14.3%) resistance were most common. Overall, 88.8% of ESCr, and 26.7% of generic isolates exhibited multi-drug resistance (MDR). MDR in ESCr 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 E. coli 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% (n = 174) ESCr and 0.6% of generic E. coli. Prevalence of bla genes in ESCr were blaCTXM (30.1%), blaCTXM-1 (21.6%), blaTEM (20%), blaCTXM-9 (7.9%), blaOXA (3.0%), blaCTXM-2 (6.4%), blaSHV (1.4%) and AmpC β-lactamase blaCMY (81.3%). The lower AMR in ESCr from SStreams and BProcessing and higher AMR in CHumans and CFeces likely reflects antimicrobial use in these environments. Although MDR levels were higher in ESCr as compared to generic E. coli, AMR to the same antimicrobials ranked high in both ESCr and generic E. coli sub-populations. This suggests that both sub-populations reflect similar AMR trends and are equally useful for AMR surveillance. Considering that MDR ESCr 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.


2021 ◽  
Vol 6 (2) ◽  
pp. 105
Author(s):  
Regina Ama Banu ◽  
Jorge Matheu Alvarez ◽  
Anthony J. Reid ◽  
Wendemagegn Enbiale ◽  
Appiah-Korang Labi ◽  
...  

Infections by Extended-Spectrum Beta-Lactamase producing Escherichia coli (ESBL-Ec) are on the increase in Ghana, but the level of environmental contamination with this organism, which may contribute to growing Antimicrobial Resistance (AMR), is unknown. Using the WHO OneHealth Tricycle Protocol, we investigated the contamination of E. coli (Ec) and ESBL-Ec in two rivers in Ghana (Odaw in Accra and Okurudu in Kasoa) that receive effluents from human and animal wastewater hotspots over a 12-month period. Concentrations of Ec, ESBL-Ec and percent ESBL-Ec/Ec were determined per 100 mL sample. Of 96 samples, 94 (98%) were positive for ESBL-Ec. concentrations per 100 mL (MCs100) of ESBL-Ec and %ESBL-Ec from both rivers were 4.2 × 104 (IQR, 3.1 × 103–2.3 × 105) and 2.79 (IQR, 0.96–6.03), respectively. MCs100 were significantly lower in upstream waters: 1.8 × 104 (IQR, 9.0 × 103–3.9 × 104) as compared to downstream waters: 1.9 × 106 (IQR, 3.7 × 105–5.4 × 106). Both human and animal wastewater effluents contributed to the increased contamination downstream. This study revealed high levels of ESBL-Ec in rivers flowing through two cities in Ghana. There is a need to manage the sources of contamination as they may contribute to the acquisition and spread of ESBL-Ec in humans and animals, thereby contributing to AMR.


2010 ◽  
Vol 54 (7) ◽  
pp. 3043-3046 ◽  
Author(s):  
Stephen P. Hawser ◽  
Samuel K. Bouchillon ◽  
Daryl J. Hoban ◽  
Robert E. Badal ◽  
Rafael Cantón ◽  
...  

ABSTRACT From 2002 to 2008, there was a significant increase in extended-spectrum beta-lactamase (ESBL)-positive Escherichia coli isolates in European intra-abdominal infections, from 4.3% in 2002 to 11.8% in 2008 (P < 0.001), but not for ESBL-positive Klebsiella pneumoniae isolates (16.4% to 17.9% [P > 0.05]). Hospital-associated isolates were more common than community-associated isolates, at 14.0% versus 6.5%, respectively, for E. coli (P < 0.001) and 20.9% versus 5.3%, respectively, for K. pneumoniae (P < 0.01). Carbapenems were consistently the most active drugs tested.


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