First Indian report on genome-wide comparison of multidrug-resistant Escherichia coli from blood stream infections

Naveen Kumar Devanga Ragupathi; Balaji Veeraraghavan; Dhiviya Prabaa Muthuirulandi Sethuvel; Shalini Anandan; Karthick Vasudevan; Ayyan Raj Neeravi; Jones Lionel Kumar Daniel; Sowmya Sathyendra; Ramya Iyadurai; Ankur Mutreja

doi:10.1371/journal.pone.0220428

Abstract

Background

Multidrug-resistant (MDR) E. coli with extended-spectrum β-lactamases (ESBLs) is becoming endemic in health care settings around the world. Baseline data on virulence and antimicrobial resistance (AMR) of specific lineages of E. coli circulating in developing countries like India is currently lacking.

Methods

Whole-genome sequencing was performed for 60 MDR E. coli isolates. The analysis was performed at single nucleotide polymorphism (SNP) level resolution to identify the presence of their virulence and AMR genes.

Results

Genome comparison revealed the presence of ST-131 global MDR and ST410 as emerging-MDR clades of E. coli in India. AMR gene profile for cephalosporin and carbapenem resistance differed between the clades. Genotypes bla_CTX-M-15 and bla_NDM-5 were common among cephalosporinases and carbapenemases, respectively. For aminoglycoside resistance, rmtB was positive for 31.7% of the isolates, of which 95% were co-harboring carbapenemases. In addition, the FimH types and virulence gene profile positively correlated with the SNP based phylogeny, and also revealed the evolution of MDR clones among the study population with temporal accumulation of SNPs. The predominant clone was ST167 (bla_NDM lineage) followed by ST405 (global clone ST131 equivalent) and ST410 (fast spreading high risk clone).

Conclusions

This is the first report on the whole genome analysis of MDR E. coli lineages circulating in India. Data from this study will provide public health agencies with baseline information on AMR and virulent genes in pathogenic E. coli in the region.

Citation: Devanga Ragupathi NK, Veeraraghavan B, Muthuirulandi Sethuvel DP, Anandan S, Vasudevan K, Neeravi AR, et al. (2020) First Indian report on genome-wide comparison of multidrug-resistant Escherichia coli from blood stream infections. PLoS ONE 15(2): e0220428. https://doi.org/10.1371/journal.pone.0220428

Editor: Grzegorz Woźniakowski, Panstwowy Instytut Weterynaryjny - Panstwowy Instytut Badawczy w Pulawach, POLAND

Received: July 20, 2019; Accepted: February 7, 2020; Published: February 26, 2020

Copyright: © 2020 Devanga Ragupathi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The author(s) received no specific funding for this research work. DRNK is funded by the Global Challenges Research Fellowship, The University of Sheffield, UK. AM is funded by the Department of Biotechnology in India and by the National Institute for Health Research [Cambridge Biomedical Research Centre at the Cambridge University Hospitals NHS Foundation Trust] in the UK. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Escherichia coli is the leading cause of bloodstream infections (BSIs) [1] and other common infections including urinary tract infections (UTIs). As an important commensal component of the biosphere, E. coli colonizes the lower gut of animals and humans and gets released in the environment.

Virulence of E. coli is driven by multiple factors including adhesins, toxins, siderophores, lipopolysaccharide (LPS), capsule, and invasins [2]. It has recently been reported that a large proportion of multi-drug resistant (MDR) E. coli carried by people is food acquired, especially from farm animals [3]. Although most of the MDR E. coli are reported to be community acquired, recently MDR E. coli, which produce extended-spectrum β-lactamases (ESBLs) have been found to be endemic in health care settings [4,5].

Among MDR E. coli, AMR caused by ESBL is mainly due to the bla_CTX-M family, particularly bla_CTX-M-15 and _-14, compared to the less frequently observed bla_SHV and bla_OXA families [6–8]. As per the literature, carbapenem resistance in E. coli is mostly mediated by bla_OXA-48 [9], bla_NDM and bla_VIM genes [10]. Also, increasingly, resistance is being reported for fluoroquinolones and third- and fourth-generation cephalosporins and ST-131 predominates globally among such MDR E. coli strains [11].

This current study was aimed at identifying the predominant virulent and AMR genes in MDR E. coli circulating in India. Core genome phylogeny was constructed using high quality SNP profiles to analyse the genome wide factors associated with these genes in E. coli isolates analyzed or sequenced.

Materials and methods

Isolates and identification

A total of 99257 specimens were received at the Department of Clinical Microbiology, Christian Medical College, Vellore, India for routine screening from BSI during the year 2006 to 2016. Isolation and identification of the organism were carried out using a standard protocol as reported earlier [12]. Of the 1100 samples found culture positive for E. coli, 10% were resistant to carbapenems, of which 60 MDR isolates were selected for further characterization.

Antimicrobial susceptibility testing (AST)

Disc diffusion.

AST testing was carried out using the Kirby-Bauer disk diffusion method. The antimicrobial agents tested were Amikacin (30 μg), netilmicin (30 μg), gentamycin (10 μg), chloramphenicol (30 μg), ciprofloxacin (5 μg), cefotaxime (30 μg), cefoxitin (30 μg), ceftazidime (30 μg), cefpodoxime (10 μg), piperacilllin-tazobactam (100/10 μg), cefoperazone-sulbactam (75/30), imipenem (10 μg) and meropenem (10 μg), tigecycline (15 μg) and tetracycline (30 μg) according to guidelines suggested by Clinical and Laboratory Standards Institute (CLSI) M100-S27, 2017. Quality control strains (K. pneumoniae ATCC 700603, P. aeruginosa ATCC 27853 and E. coli ATCC 25922) were used in all batches, as per the CLSI recommendation.

Minimum Inhibitory Concentration (MIC) for colistin.

Colistin MICs for the studied isolates were determined by broth microdilution and interpreted using CLSI 2017 breakpoint recommendations. mcr-1 positive E. coli with the expected range 4–8 μg/ml, E. coli ATCC 25922 (0.25–2 μg/ml) and P. aeruginosa ATCC 27853 (0.5–4 μg/ml) were used as quality and technical control (QC and TC) strains for colistin MIC determination.

Next generation sequencing and genome assembly

Genomic DNA was extracted using a QIAamp DNA Mini Kit (QIAGEN, Hilden, Germany). Whole genome sequencing (WGS) was performed using an Ion Torrent^™ Personal Genome Machine^™ (PGM) sequencer (Life Technologies, Carlsbad, CA) with 400-bp read chemistry according to the manufacturer’s instructions. Data were assembled with reference E. coli strain (NC000913) using Assembler SPAdes v.5.0.0.0 embedded in Torrent Suite Server v.5.0.3.

Genome annotation

The assembled sequence was annotated using PATRIC, the bacterial bioinformatics database and analysis resource (http://www.patricbrc.org), and NCBI Prokaryotic Genomes Automatic Annotation Pipeline (PGAAP, http://www.ncbi.nlm.nih.gov/genomes/static/Pipeline.html). Downstream analysis was performed using the CGE server (http://www.cbs.dtu.dk/services) and PATRIC. The resistance gene profile was analysed using ResFinder 2.1 from the CGE server (https://cge.cbs.dtu.dk//services/ResFinder/). The sequences were also screened for antimicrobial resistance genes in the Antibiotic Resistance Genes Database (ARDB) and Comprehensive Antibiotic Resistance Database (CARD) through PATRIC. Virulence genes from the genomes were identified using VirulenceFinder 2.0 (https://cge.cbs.dtu.dk/services/VirulenceFinder/). Serotype of the isolates were identified using SerotypeFinder 1.1 (https://cge.cbs.dtu.dk/services/SerotypeFinder/).

Genome based MLST analysis

Sequence types (STs) were analysed using multi-locus sequence typing (MLST) 1.8 tool (https://cge.cbs.dtu.dk//services/MLST/). To visualize the possible evolutionary relationships between isolates, STs of the study isolates and the globally reported strains were computed using PHYLOViZ software v2.0 based on goeBURST algorithm. The study used Warwick database for all sequence based MLST analysis of E. coli.

Genome comparison analyses

Gview, interactive genome viewer was used to compare the annotated E. coli genome arrangements with the reference E. coli K12 genome (NC_000913) [13]. Core genome analysis was performed using Roary: the Pan Genome Pipeline v3.11.2 from Sanger Institute [14]. The phylogenetic tree was constructed using the core SNPs using FastTree v2.1.10. To evaluate the effect of recombination regions on the E. coli genomes, SNIPPY was performed to retrieve core SNPs, that was followed by Genealogies Unbiased By recomBinations In Nucleotide Sequences (Gubbins) algorithm [15]. The tree was constructed with midpoint rooting. Further, the tree file was visualised and analysed in iTOL v4 (https://itol.embl.de/). A dendrogram representing core vs pan genes was constructed using hierarchical cluster analysis with hclust method in R.

This Whole Genome Shotgun project has been deposited at GenBank under the accession numbers as mentioned in S1 Table. The version described in this manuscript is version 1.

Ethical clearance

The study was approved by the Institutional Review Board and Ethical committee, Christian Medical College, Vellore, India (IRB No.: 9540 dt 22-07-2015). All the samples were fully anonymized before processing and since our study only utilised isolates received from routine blood cultures, we did not require informed written consent from the patients.

Results

Antimicrobial susceptibility

All 60 E. coli isolates were resistant to carbapenems, quinolones, cephalosporins and beta-lactamase inhibitors (S1 Table). Whereas all the isolates were susceptible to colistin except B7532 and B9021, which exhibited an MIC of 32 μg/ml.

Whole genome sequence analysis

Phylogeny of MDR E. coli.

MLSTFinder revealed the different sequence types of the isolates. The study isolates belonged to 6 clonal complexes with 14 different sequence types. Few of the sequence types were observed to share same founder types revealing the evolution of these strains. CC10 and CC 405 were the two major CCs observed with ST-167, ST-410 and ST-405 as the common STs. Interestingly, nine isolates belonging to CC/ST-131 were identified, of which, all were of H-30 clade, except the isolate BA9313 (H-24).

E. coli genome comparison.

Whole genome composition of 60 MDR E. coli was compared with the E. coli K-12 reference genome which shows the region of differences between these genomes (S1 Fig). A total of 2,518,792 SNPs were identified in all the analyzed genomes. On minimum, 5957 and maximum, 74713 SNPs were identified in the study MDR E. coli genomes when compared to the reference genome.

Core vs pan genome

Comparison between the core and pan genomes of 60 MDR E. coli isolates revealed 2258 core genes across all 60 isolates among the 17944 total gene clusters. This includes 600 soft core genes in 57 to 59 isolates, 3984 shell genes in 9 to 57 isolates and 11102 genes in less than 9 isolates (Fig 1).

Download:

Fig 1. Pan genome vs core genome comparison depicting number of pan genes and conserved genes (A), Distribution of core genes, soft core genes and pan genes among the 60 MDR E. coli isolates from BSI (B).

https://doi.org/10.1371/journal.pone.0220428.g001

Serotype prediction.

Serotypes were established from the whole genome data and O102:H6 was the most common serotype (18.75%), followed by O89:H9 (15.6%), O8:H9 (12.5%), O89:H5 (9.4%) and other serotypes (S1 Table).

Genetic virulence factors of MDR E. coli.

Three common virulence gene profiles were observed among the isolates as follows, i) iss, capU, gad, ii) ipfA, and iii) eilA, gad, air. The FimH virulence typing revealed the types 5, 24, 27, 28, 30, 35, 54, 191 and 54-like in comparison to the fimH database.

Comparison of virulence and clonal traits.

The virulence gene profiles of the 60 isolates were compared to the FimH virulence types, MLST sequence type and SNP phylogeny. The isolates clustered in two distinct groups including ST-131(H-30 clade), based on the virulence genes identified (Fig 2). The sequence types were found to be tightly linked to the groups of virulence gene profile and FimH types.

Download:

Fig 2. SNP phylogeny based comparison of genetic virulence traits observed in MDR E. coli strains.

Sequence types, virulence gene profile, O and H antigens and Fim-H types are shown next to the tree.

https://doi.org/10.1371/journal.pone.0220428.g002

Antimicrobial resistance genetic determinants.

ResFinder revealed the presence of multiple AMR genes in each of the MDR E. coli (Fig 3). Aminoglycoside and beta lactam resistance genes were the most dominant. The most common aminoglycoside resistance genes were aadA5 and aac(6’)lb-cr, followed by aadA2 and rmtB, while bla_CTX-M-15 followed by bla_NDM-5, bla_OXA-1 and bla_TEM-1B were most prevalent among beta lactamases. Most of the isolates also harboured mphA, catB4, sul1, tetB, dfrA17 and dfrA12. Interestingly, two isolates, B7532 and B9021 carried mcr-1.1, which is responsible for plasmid-mediated colistin resistance. The two isolates also showed phenotypic resistance to colistin with high MIC (>32 μg/ml). In addition, the phenotypic resistance for other antimicrobials exhibited significant correlation (>80%) with the presence of respective AMR genes.

Download:

Fig 3. Antimicrobial resistance genes observed in MDR E. coli compared to the SNP based phylogeny.

Depicting prevalence of bla_NDM-5 among carbapenemases and bla_CTX-M-15 among cephalosporinases.

https://doi.org/10.1371/journal.pone.0220428.g003

Discussion

The increasing use of third-generation β-lactams and β-lactam inhibitors was accompanied with increases in prevalence of the MDR phenotype among E. coli. The susceptibility profiles noted in invasive E. coli isolates of our study were similar to the previously (2014–2016) reported susceptibility to cefoxitin 53%, ceftazidime 33%, cefotaxime 26%, ceftriaxone 25%, cefepime 29%, piperacillin tazobactam 66%, imipenem and meropenem 89%, aztreonam 36%, ciprofloxacin 19%, levofloxavin 23%, and amikacin 91% [16]. Among these, about 64% of E. coli were found to be ESBL producers.

On genotypic characterization of MDR E. coli isolates, the increasing frequency of antimicrobial resistance in clinical E. coli isolates was found to be associated with bla_CTX-M, bla_NDM, and mcr genes. In our study, multiple AMR genes for beta lactams, carbapenems, fluoroquinolones, tetracycline, aminoglycosides and colistin were identified. The presence of genotypic AMR genes correlated well with phenotypic expression for beta lactams, carbapenems, fluoroquinolones and tetracycline. Plasmids IncFII majorly carried AMR genes bla_CTX-M-15, bla_NDM-5, aadA2, rmtB, sul1, drfA12, erm(B) and tetA, while IncFI plasmids carried mostly aadA5, sul2, dfrA17, mph(A) and tetB genes. Results from plasmid analysis of the study isolates were previously published elsewhere [17].

The MDR E. coli isolates phylogenetically grouped into four major clades: ST167, ST410, ST405 and ST131. Variant bla_NDM-5, responsible for carbapenem resistance was common in comparison to other bla_NDM variants. The bla_NDM positive isolates belonging to ST410 and ST405 harboured only the bla_NDM-5 variant, whereas ST167 and ST131 isolates had bla_NDM-4 and bla_NDM-1 respectively, in addition to bla_NDM-5. Interestingly only two isolates out of 60 MDR E. coli had bla_NDM-1, while it is still common among other species of MDR clinical pathogens in India [18]. From Hong Kong, a previous report identified bla_NDM-1 as common among E. coli though the sample size was lesser [19], whereas in central China, bla_NDM-1 and bla_NDM-5 occurrence in E. coli has been reported in equal numbers [20].

Globally, bla_OXA-48 type were the most commonly reported carbapenemases among E. coli [21], followed by bla_NDM [22], bla_IMP [23] and bla_KPC [24]. Studies have reported occurrence of bla_OXA-48 from as low as 3% to 22% [25, 9]. In contrast, a previous report from India on carbapenem-resistant clinical E. coli isolates from 2013 and 2015 has shown that bla_NDM was common among carbapenemases in E. coli (70%), followed by bla_OXA-48 (24%) and bla_VIM (17%). Co-occurences of bla_NDM along with bla_OXA (5%) and bla_VIM (17%) have also been reported [26]. Similar results were seen in our study and the combinations observed were only bla_NDM+bla_OXA-1. Though, bla_OXA-181 was rare in combination with bla_NDM (n = 1). These observations confirm that bla_NDM is prevalent among E. coli followed by bla_OXA in India, which is otherwise the most prevalent elsewhere.

There has been a global concern on aminoglycoside resistance in Gram-negatives. Acquired 16S-RMTases are known to confer extremely high level of aminoglycoside resistance, due to which key aminoglycosides including gentamicin, tobramycin, and amikacin are ineffective against carbapenem resistant strains [27]. Accordingly, plazomicin, a new aminoglycoside agent identified to combat against carbapenem-resistant Enterobacteriaceae, was found inactive if the isolates co-produced 16S-RMTases [28]. In this study, ~ 95% of the RMTase positive E. coli co-harboured carbapenemases, which worryingly contributes to the already high burden of carbapenem resistance. Similar to our study, Taylor et al. [29] and Poirel et al. [30] have reported 83.1% and 45.4% co-occurrence of carbapenemases in 16S RMTase producing Enterobacteriaceae, respectively.

Our study shows that, for cephalosporin resistance, the isolates from ST131 and ST405 clades carried bla_CTX-M-15 in 100% and 92% of their respective clades, whereas ST167 and ST410 isolates carried 18% and 43% bla_CMY genes in addition to 63% and 100% bla_CTX-M-15. However, 54.34% bla_CTX-M was reported previously in ESBL positive isolates from India [31]. Among the study isolates, ST167 carried significantly (P<0.05) lesser bla_CTX-M-15 in comparison to other clades. Similarly, ST167 and ST410 carried bla_CMY in addition for cephalosporin resistance which was not seen in ST131 and ST405. Recently, plasmid-mediated colistin resistance is being increasingly reported in E. coli [32–34]. This study also observed two isolates (B7532, B9021) with mcr-1.1 expressing high MIC of >32 μg/ml to colistin and both the isolates, from the same time period and ward, were closely related with same sequence type (ST624). After this observation made in 2007 strains, there have been no reports of mcr.

The antimicrobial susceptibility of E. coli has been shown to vary geographically [35]. Among the different clonal groups observed elsewhere, E. coli ST131 was previously reported to be most commonly associated with community acquired infection [36–37], which recently were highly associated with healthcare settings. Also, ST131 was reported earlier as the predominant lineage carrying bla_CTX-M-15 and other ESBLs. Most of the MDR E. coli carrying bla_CTX-M-15 from different countries in Europe and North America were homogenously grouped into the E. coli O25:H4-ST131 [6,36–37]. In our study, 87% of the isolates carried bla_CTX-M-15, among various STs, with only nine isolates of ST131. Among the observed STs in this study, bla_CTX-M-15 was previously reported for its association with ST617, ST405 and ST131 [37].

Though ST131 clones were predominantly reported worldwide, the STs observed in our study were striking for clustering in distinct phylogenetic lineages. ST167 was previously reported for its ability to carry bla_NDM genes in China [38–40]. ST405 has been known as another global clonal group similar to ST131 [41] and has been reported to carry bla_NDM genes in hospital settings [42], in addition to blaKPC-2 [43]. ST405 was reported as a lineage, carrying fluoroquinolone resistance in Japan [41]. Recently, ST410 was reported as a possible international high risk clone with B2/H24R, B3/H24Rx, and B4/H24RxC AMR clades. B3/H24Rx was reported to be evolved by acquisition of the bla_CTX-M-15 and an IncFII plasmid. B4/H24RxC emerged by acquiring IncX3 plasmid with bla_OXA-181 known for carbapenem resistance, which further acquired bla_NDM-5, on a conserved IncFII plasmid [44]. In this study, all ST410 isolates (n = 7) harboured bla_CTX-M-15 gene, while only B25762, BV643, B12243 and B32605 had IncFII plasmids and bla_NDM-5 (B3/H24RxC). B12243, in addition harboured IncX3 with bla_OXA-181 (B4/H24RxC), while BA22372 and BA9615 had only bla_OXA-181 in IncX3 plasmid (B4/H24RxC).

Virulence genes observed among the E. coli isolates varied according to the different clades observed. The comparison of the virulence gene type with SNP based phylogeny revealed the acquisition and deletion of virulence genes. Genes iss, capU and gad were observed in ST167 clade. ST131 possessed iha, sat, cnfl and senB, in addition to iss and gad. ST131 strains in our study have lost the capU genes. Further, ST405 clade also lost iss and gained eilA and air genes with FimH type 29. Few isolates of ST405 retained iha and sat genes belonging to FimH 27 type within ST405. ST410 (FimH 24) that predominantly had ipfA gene, on the contrary, lost all other genes, except gad gene in two isolates. Overall, gad gene served as backbone for ST167, ST131 and ST405 clades, while ipfA was consistent in ST410. Ours is the first study that compares the evolution of virulence pattern with phylogeny, which explains the emergence of a stable clinical virulent phenotype.

FimH, that had been reported as a major candidate for the development of a vaccine against pathogenic E. coli [45] is responsible for producing mannose-sensitive bacterial adhesion [45]. Though high nucleotide conservation of >98% was observed in fimH alleles, minor sequence differences have been reported to correlate with differential binding and adhesion phenotypes [46]. Fim-H types in our study correlated well with the STs.

Our study shows that with a SNPs based phylogeny, higher discrimination between the clinical MDR E. coli isolates is apparent. Therefore, more such studies with integrated approach to analysing pathogenic E. coli in India are required to fully understand and follow the dynamic virulence and AMR landscape of this rapidly evolving group of pathogens.

Conclusions

To the best of our knowledge, this is the first report on SNP phylogeny in comparison with AMR and virulence traits in E. coli in India. The study revealed the prevalence of bla_NDM-5 among the clades ST131, ST405 and ST410 clades. bla_CTX-M-15 was responsible for cephalosporin resistance in ST131 and ST405 clades whereas, ST167 and ST410 carried both bla_CTX-M-15 and bla_CMY genes. For aminoglycoside resistance, rmtB was positive for 31.7% of the isolates, of which 30% were co-harbouring carbapenemases. The FimH types and virulence gene profile positively correlated with the SNP based phylogeny. However the predominant ST131 epidemic clone was smaller in our study population while ST167 and ST405 clones with multiple AMR genes were predominant. Further larger studies are needed to rule out any possible bias. Isolates with iss, capU and gad virulence genes were the major type. Moreover, SNP based phylogeny revealed evolution of the MDR clones among the study population, which suggests that continuous WGS level molecular surveillance would be necessary to keep track of the spread of MDR clones in India.

Supporting information

S1 Table. Serotype and antimicrobial resistance profiles of MDR E. coli from blood stream infections (n = 60).

https://doi.org/10.1371/journal.pone.0220428.s001

(DOCX)

S1 Fig. Circular genome plot comparing 60 MDR E. coli thereby showing differences in genome composition in comparison to the reference genome NC000913 E. coli.

https://doi.org/10.1371/journal.pone.0220428.s002

(TIF)

Acknowledgments

The authors thank the Christian Medical College, Vellore, India for providing basic infrastructure required for this study.

References

1. Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust. 2008;188:209–13. pmid:18279126
- View Article
- PubMed/NCBI
- Google Scholar
2. López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, et al. Identification of Virulence Factors Genes in Escherichia coli Isolates from Women with Urinary Tract Infection in Mexico. BioMed Research International, Volume 2014, Article ID 959206, 10 pages. http://dx.doi.org/10.1155/2014/959206
- View Article
- Google Scholar
3. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, et al. Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis. 2007;13:838–46. pmid:17553221
- View Article
- PubMed/NCBI
- Google Scholar
4. Mesa RJ, Blanc V, Blanch AR, Cortés P, González JJ, Lavilla S et al. Extended-spectrum β-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms, and sewage). J Antimicrob Chemother. 2006;58:211–5. pmid:16720567
- View Article
- PubMed/NCBI
- Google Scholar
5. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD. Community-onset extended-spectrum β-lactamase (ESBL)-producing Escherichia coli: importance of international travel. J Infect. 2008;57:441–448. pmid:18990451
- View Article
- PubMed/NCBI
- Google Scholar
6. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, Demarty R, Alonso MP, Canica MM. Intercontinental emergence of Escherichia coli clone O25:H4–ST131 producing CTX-M-15. J Antimicrob Chemother. 2008;61:273–81. pmid:18077311
- View Article
- PubMed/NCBI
- Google Scholar
7. Lau SH, Kaufmann ME, Livermore DM, Woodford N, Willshaw GA, Cheasty T. UK epidemic Escherichia coli strains A–E, with CTX-M-15 β-lactamase, all belong to the international O25:H4–ST131 clone. J Antimicrob Chemother. 2008;62:1241–4. pmid:18779256
- View Article
- PubMed/NCBI
- Google Scholar
8. Alhashash F, Weston V, Diggle M, McNally A. Multidrug-Resistant Escherichia coli Bacteremia. Emerg Infect Dis. 2013;19(10):1699–701. pmid:24050656
- View Article
- PubMed/NCBI
- Google Scholar
9. Candan ED, Aksöz N. Escherichia Coli: Characteristics of Carbapenem Resistance and Virulence Factors. Braz arch biol technol. 2017;60.
- View Article
- Google Scholar
10. Nagaraj S, Chandran SP, Shamanna P, Macaden R. Carbapenem resistance among Escherichia coli and Klebsiella pneumoniae in a tertiary care hospital in south India. Indian J Med Microbiol. 2012;30(1):93–5. pmid:22361769
- View Article
- PubMed/NCBI
- Google Scholar
11. Kanamori H, Parobek CM, Juliano JJ, Johnson JR, Johnston BD, Johnson TJ, Weber DJ, et al. Genomic Analysis of Multidrug-Resistant Escherichia coli from North Carolina Community Hospitals: Ongoing Circulation of CTX-M-Producing ST131-H30Rx and ST131-H30R1 Strains. Antimicrob Agents Chemother. 2017;61(8):pii: e00912–17. pmid:28584139
- View Article
- PubMed/NCBI
- Google Scholar
12. Abbott SL, Cheung WKW, Janda JM. The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol. 2003;41:2348–57. pmid:12791848
- View Article
- PubMed/NCBI
- Google Scholar
13. Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms. PLoS ONE 2014;9(8):e104984. pmid:25110940
- View Article
- PubMed/NCBI
- Google Scholar
14. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691–3. pmid:26198102
- View Article
- PubMed/NCBI
- Google Scholar
15. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2014; pmid:25414349
- View Article
- PubMed/NCBI
- Google Scholar
16. Veeraraghavan B, Jesudason MR, Prakasah JAJ, Anandan S, Sahni RD, Pragasam AK, et al. Antimicrobial susceptibility profiles of gram-negative bacteria causing infections collected across India during 2014–2016: Study for monitoring antimicrobial resistance trend report. Indian J Med Microbiol. 2018;36:32–6. pmid:29735823
- View Article
- PubMed/NCBI
- Google Scholar
17. Ragupathi NKD, Bakthavatchalam YD, Mathur P, Pragasam AK, Walia K, Ohri VC, et al. Plasmid profiles among some ESKAPE pathogens in a tertiary care centre in south India. Indian J Med Res. 2019;149(2):222–31. pmid:31219087
- View Article
- PubMed/NCBI
- Google Scholar
18. Veeraraghavan B, Shankar C, Karunasree S, Kumari S, Ravi R, Ralph R. Carbapenem resistant Klebsiella pneumoniae isolated from bloodstream infection: Indian experience. Pathog glob health. 2017;111(5):240–6. pmid:28670975
- View Article
- PubMed/NCBI
- Google Scholar
19. Ho PL, Cheung YY, Wang Y, Lo WU, Lai EL, Chow KH, et al. Characterization of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from a healthcare region in Hong Kong. Eur J Clin Microbiol Infect Dis. 2016;35(3):379–85. pmid:26740321
- View Article
- PubMed/NCBI
- Google Scholar
20. Liang WJ, Liu HY, Duan GC, Zhao YX, Chen SY, Yang HY, et al. Emergence and mechanism of carbapenem-resistant Escherichia coli in Henan, China, 2014. J Infect Public Health. 2018;11(3):347–51. pmid:29107607
- View Article
- PubMed/NCBI
- Google Scholar
21. Doi Y, Paterson DL. Carbapenemase-producing Enterobacteriaceae. Semin Respir Crit Care Med. 2015; 36(1):74–84). pmid:25643272
- View Article
- PubMed/NCBI
- Google Scholar
22. Mushtaq S, Irfan S, Sarma JB, Doumith M, Pike R, Pitout J et al. Phylogenetic diversity of Escherichia coli strains producing NDM-type carbapenemases. J Antimicrob Chemother. 2011;66:2002–5. pmid:21669947
- View Article
- PubMed/NCBI
- Google Scholar
23. Aktas Z, Satana D, Kayacan C, Ozbek B, Gurler N, Somer A et al. Carbapenem resistance in Turkey: Repeat report on OXA-48 in Klebsiella pneumoniae and first report on IMP-1 beta-lactamase in Escherichia coli. Afr J Microbiol Res. 2012;6:3874–8.
- View Article
- Google Scholar
24. Morris D, Boyle F, Ludden C, Condon I, Hale J, O’Connell N et al. Production of KPC-2 Carbapenemase by an Escherichia coli Clinical Isolate Belonging to the International ST131 Clone. Antimicrob Agents Chemother. 2011;55:4935–6. pmid:21768521
- View Article
- PubMed/NCBI
- Google Scholar
25. Budak S, Oncul O, Aktas Z, Acar A, Ozyurt M, Turhan V, et al. The determination of carbapenem resistance in Escherichia coli and Pneumoniae isolates related to nosocomial infections and the evaluation of risk factors. Southeast Asian J Trop Med Public Health. 2014;45(1):113–22. pmid:24964660
- View Article
- PubMed/NCBI
- Google Scholar
26. Sharma A, Bakthavatchalam YD, Gopi R, Anandan S, Verghese VP, Veeraraghavan B. Mechanisms of Carbapenem Resistance in K. pneumoniae and E. coli from Bloodstream Infections in India. J Infect Dis Ther. 2016;4:293.
- View Article
- Google Scholar
27. Doi Y, Wachino JI, Arakawa Y. Aminoglycoside Resistance: The Emergence of Acquired 16S Ribosomal RNA Methyltransferases. Infect Dis Clin North Am. 2016; 30(2): 523–37. pmid:27208771
- View Article
- PubMed/NCBI
- Google Scholar
28. Yu F, Wang L, Pan J, Yao D, Chen C, Zhu T, et al. Prevalence of 16S rRNA methylase genes in Klebsiella pneumoniae isolates from a Chinese teaching hospital: coexistence of rmtB and armA genes in the same isolate. Diagn Microbiol Infect Dis. 2009;64:57–63. pmid:19232867
- View Article
- PubMed/NCBI
- Google Scholar
29. Taylor E, Sriskandan S, Woodford N, Hopkins KL. High prevalence of 16S rRNA methyltransferases among carbapenemase-producing Enterobacteriaceae in the UK and Ireland. Int J Antimicrob Agents. 2018; 52(2):278–82. pmid:29596903
- View Article
- PubMed/NCBI
- Google Scholar
30. Poirel L, Goutines J, Aires-de-Sousa M, Nordmann P. High Rate of Association of 16S rRNA Methylases and Carbapenemases in Enterobacteriaceae Recovered from Hospitalized Children in Angola. Antimicrob Agents Chemother. 2018;62:e00021–18. pmid:29439957
- View Article
- PubMed/NCBI
- Google Scholar
31. Ravikant , Kumar P, Ranotkar S, Zutshi S, Lahkar M, Phukan C, et al. Prevalence and identification of extended spectrum β-lactamases (ESBL) in Escherichia coli isolated from a tertiary care hospital in North-East India. Ind J Exp Biol. 2016;54:108–114.
- View Article
- Google Scholar
32. Elnahriry SS, Khalifa HO, Soliman AM, Ahmed AM, Hussein AM, Shimamoto T, et al. Emergence of Plasmid-Mediated Colistin Resistance Gene mcr-1 in a Clinical Escherichia coli Isolate from Egypt. Antimicrob Agents Chemother. 2016;60 (5):3249–50. pmid:26953204
- View Article
- PubMed/NCBI
- Google Scholar
33. Ghafur A, Shankar C, GnanaSoundari P, Venkatesan M, Mani D, Thirunarayanan MA, et al. Detection of chromosomal and plasmid-mediated mechanisms of colistin resistance in Escherichia coli and Klebsiella pneumoniae from Indian food samples. J Glob Antimicrob Resist. 2019;16:48–52. pmid:30244040
- View Article
- PubMed/NCBI
- Google Scholar
34. Yang F, Shen C, Zheng X, Liu Y, El-Sayed Ahmed MAE, Zhao Z, et al. Plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli and Klebsiella pneumoniae isolated from market retail fruits in Guangzhou, China. Infect Drug Resist. 2019;12:385–9. pmid:30809099
- View Article
- PubMed/NCBI
- Google Scholar
35. Ikram R, Psutka R, Carter A, Priest P. An outbreak of multi-drug resistant Escherichia coli urinary tract infection in an elderly population: a case-control study of risk factors. BMC Infect Dis. 2015;15:224. pmid:26054866
- View Article
- PubMed/NCBI
- Google Scholar
36. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, Semmler T, et al. Emergence of human pandemic O25:H4‐ST131 CTX‐M‐15 extended‐spectrum‐β‐lactamase‐producing Escherichia coli among companion animals. J Antimicrob Chemother. 2010;65:651–60. pmid:20118165
- View Article
- PubMed/NCBI
- Google Scholar
37. Brolund A, Edquist PJ, Makitalo B, Olsson-Liljequist B, Soderblom T, Wisell KT, et al. Epidemiology of extended-spectrum b-lactamase-producing Escherichia coli in Sweden 2007–2011. Clin Microbiol Infect. 2014;20:O344–O352. pmid:24118431
- View Article
- PubMed/NCBI
- Google Scholar
38. Yang P, Xie Y, Feng P, Zong Z. blaNDM-5 Carried by an IncX3 Plasmid in Escherichia coli Sequence Type 167. Antimicrob Agents Chemother. 2014;58(12):7548–52. pmid:25246393
- View Article
- PubMed/NCBI
- Google Scholar
39. Feng Y, Yang P, Xie Y, Wang X, McNally A, Zong Z. Escherichia coli of sequence type 3835 carrying blaNDM-1, blaCTX-M-15, blaCMY-42 and blaSHV-12. Sci Rep. 2015;5:12275. pmid:26194736
- View Article
- PubMed/NCBI
- Google Scholar
40. Shen P, Yi M, Fu Y, Ruan Z, Du X, Yu Y, et al. Detection of an Escherichia coli Sequence Type 167 Strain with Two Tandem Copies of blaNDM-1 in the Chromosome. J Clin Microbiol. 2017;55:199–205. pmid:27807154
- View Article
- PubMed/NCBI
- Google Scholar
41. Matsumura Y, Yamamoto M, Nagao M, Ito Y, Takakura S, Ichiyama S, et al. Association of Fluoroquinolone Resistance, Virulence Genes, and IncF Plasmids with Extended-Spectrum-_-Lactamase-Producing Escherichia coli Sequence Type 131 (ST131) and ST405 Clonal Groups. Antimicrob Agents Chemother. 2013;57(10):4736–42. pmid:23856781
- View Article
- PubMed/NCBI
- Google Scholar
42. Zhang X, Feng Y, Zhou W, McNally A, Zong Z. Cryptic transmission of ST405 Escherichia coli carrying blaNDM-4 in hospital. Sci Rep. 2018;8:390. pmid:29321680
- View Article
- PubMed/NCBI
- Google Scholar
43. Cai JC, Zhang R, Hu YY, Zhou HW, Chen GX. Emergence of Escherichia coli Sequence Type 131 Isolates Producing KPC-2 Carbapenemase in China. Antimicrob Agents Chemother. 2014;58(2):1146–52. pmid:24323475
- View Article
- PubMed/NCBI
- Google Scholar
44. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, et al. Escherichia coli Sequence Type 410 Is Causing New International High-Risk Clones. mSphere. 2018;3(4):pii: e00337–18. pmid:30021879
- View Article
- PubMed/NCBI
- Google Scholar
45. Tchesnokova V, Aprikian P, Kisiela D, Gowey S, Korotkova N, Thomas W et al. Type 1 Fimbrial Adhesin FimH Elicits an Immune Response That Enhances Cell Adhesion of Escherichia coli. Infect. Immun. 2011;79(10):3895–3904. pmid:21768279
- View Article
- PubMed/NCBI
- Google Scholar
46. Bouckaert J, Mackenzie J, de Paz JL, Chipwaza B, Choudhury D, Zavialov A et al. The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol Microbiol. 2006;61(6):1556–1568. pmid:16930149
- View Article
- PubMed/NCBI
- Google Scholar

[ref1] 1. Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust. 2008;188:209–13. pmid:18279126
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, et al. Identification of Virulence Factors Genes in Escherichia coli Isolates from Women with Urinary Tract Infection in Mexico. BioMed Research International, Volume 2014, Article ID 959206, 10 pages. http://dx.doi.org/10.1155/2014/959206
View Article
Google Scholar

[6] View Article

[7] Google Scholar

[ref3] 3. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, et al. Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis. 2007;13:838–46. pmid:17553221
View Article
PubMed/NCBI
Google Scholar

[9] View Article

[10] PubMed/NCBI

[11] Google Scholar

[ref4] 4. Mesa RJ, Blanc V, Blanch AR, Cortés P, González JJ, Lavilla S et al. Extended-spectrum β-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms, and sewage). J Antimicrob Chemother. 2006;58:211–5. pmid:16720567
View Article
PubMed/NCBI
Google Scholar

[13] View Article

[14] PubMed/NCBI

[15] Google Scholar

[ref5] 5. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD. Community-onset extended-spectrum β-lactamase (ESBL)-producing Escherichia coli: importance of international travel. J Infect. 2008;57:441–448. pmid:18990451
View Article
PubMed/NCBI
Google Scholar

[17] View Article

[18] PubMed/NCBI

[19] Google Scholar

[ref6] 6. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, Demarty R, Alonso MP, Canica MM. Intercontinental emergence of Escherichia coli clone O25:H4–ST131 producing CTX-M-15. J Antimicrob Chemother. 2008;61:273–81. pmid:18077311
View Article
PubMed/NCBI
Google Scholar

[21] View Article

[22] PubMed/NCBI

[23] Google Scholar

[ref7] 7. Lau SH, Kaufmann ME, Livermore DM, Woodford N, Willshaw GA, Cheasty T. UK epidemic Escherichia coli strains A–E, with CTX-M-15 β-lactamase, all belong to the international O25:H4–ST131 clone. J Antimicrob Chemother. 2008;62:1241–4. pmid:18779256
View Article
PubMed/NCBI
Google Scholar

[25] View Article

[26] PubMed/NCBI

[27] Google Scholar

[ref8] 8. Alhashash F, Weston V, Diggle M, McNally A. Multidrug-Resistant Escherichia coli Bacteremia. Emerg Infect Dis. 2013;19(10):1699–701. pmid:24050656
View Article
PubMed/NCBI
Google Scholar

[29] View Article

[30] PubMed/NCBI

[31] Google Scholar

[ref9] 9. Candan ED, Aksöz N. Escherichia Coli: Characteristics of Carbapenem Resistance and Virulence Factors. Braz arch biol technol. 2017;60.
View Article
Google Scholar

[33] View Article

[34] Google Scholar

[ref10] 10. Nagaraj S, Chandran SP, Shamanna P, Macaden R. Carbapenem resistance among Escherichia coli and Klebsiella pneumoniae in a tertiary care hospital in south India. Indian J Med Microbiol. 2012;30(1):93–5. pmid:22361769
View Article
PubMed/NCBI
Google Scholar

[36] View Article

[37] PubMed/NCBI

[38] Google Scholar

[ref11] 11. Kanamori H, Parobek CM, Juliano JJ, Johnson JR, Johnston BD, Johnson TJ, Weber DJ, et al. Genomic Analysis of Multidrug-Resistant Escherichia coli from North Carolina Community Hospitals: Ongoing Circulation of CTX-M-Producing ST131-H30Rx and ST131-H30R1 Strains. Antimicrob Agents Chemother. 2017;61(8):pii: e00912–17. pmid:28584139
View Article
PubMed/NCBI
Google Scholar

[40] View Article

[41] PubMed/NCBI

[42] Google Scholar

[ref12] 12. Abbott SL, Cheung WKW, Janda JM. The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol. 2003;41:2348–57. pmid:12791848
View Article
PubMed/NCBI
Google Scholar

[44] View Article

[45] PubMed/NCBI

[46] Google Scholar

[ref13] 13. Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms. PLoS ONE 2014;9(8):e104984. pmid:25110940
View Article
PubMed/NCBI
Google Scholar

[48] View Article

[49] PubMed/NCBI

[50] Google Scholar

[ref14] 14. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691–3. pmid:26198102
View Article
PubMed/NCBI
Google Scholar

[52] View Article

[53] PubMed/NCBI

[54] Google Scholar

[ref15] 15. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2014; pmid:25414349
View Article
PubMed/NCBI
Google Scholar

[56] View Article

[57] PubMed/NCBI

[58] Google Scholar

[ref16] 16. Veeraraghavan B, Jesudason MR, Prakasah JAJ, Anandan S, Sahni RD, Pragasam AK, et al. Antimicrobial susceptibility profiles of gram-negative bacteria causing infections collected across India during 2014–2016: Study for monitoring antimicrobial resistance trend report. Indian J Med Microbiol. 2018;36:32–6. pmid:29735823
View Article
PubMed/NCBI
Google Scholar

[60] View Article

[61] PubMed/NCBI

[62] Google Scholar

[ref17] 17. Ragupathi NKD, Bakthavatchalam YD, Mathur P, Pragasam AK, Walia K, Ohri VC, et al. Plasmid profiles among some ESKAPE pathogens in a tertiary care centre in south India. Indian J Med Res. 2019;149(2):222–31. pmid:31219087
View Article
PubMed/NCBI
Google Scholar

[64] View Article

[65] PubMed/NCBI

[66] Google Scholar

[ref18] 18. Veeraraghavan B, Shankar C, Karunasree S, Kumari S, Ravi R, Ralph R. Carbapenem resistant Klebsiella pneumoniae isolated from bloodstream infection: Indian experience. Pathog glob health. 2017;111(5):240–6. pmid:28670975
View Article
PubMed/NCBI
Google Scholar

[68] View Article

[69] PubMed/NCBI

[70] Google Scholar

[ref19] 19. Ho PL, Cheung YY, Wang Y, Lo WU, Lai EL, Chow KH, et al. Characterization of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from a healthcare region in Hong Kong. Eur J Clin Microbiol Infect Dis. 2016;35(3):379–85. pmid:26740321
View Article
PubMed/NCBI
Google Scholar

[72] View Article

[73] PubMed/NCBI

[74] Google Scholar

[ref20] 20. Liang WJ, Liu HY, Duan GC, Zhao YX, Chen SY, Yang HY, et al. Emergence and mechanism of carbapenem-resistant Escherichia coli in Henan, China, 2014. J Infect Public Health. 2018;11(3):347–51. pmid:29107607
View Article
PubMed/NCBI
Google Scholar

[76] View Article

[77] PubMed/NCBI

[78] Google Scholar

[ref21] 21. Doi Y, Paterson DL. Carbapenemase-producing Enterobacteriaceae. Semin Respir Crit Care Med. 2015; 36(1):74–84). pmid:25643272
View Article
PubMed/NCBI
Google Scholar

[80] View Article

[81] PubMed/NCBI

[82] Google Scholar

[ref22] 22. Mushtaq S, Irfan S, Sarma JB, Doumith M, Pike R, Pitout J et al. Phylogenetic diversity of Escherichia coli strains producing NDM-type carbapenemases. J Antimicrob Chemother. 2011;66:2002–5. pmid:21669947
View Article
PubMed/NCBI
Google Scholar

[84] View Article

[85] PubMed/NCBI

[86] Google Scholar

[ref23] 23. Aktas Z, Satana D, Kayacan C, Ozbek B, Gurler N, Somer A et al. Carbapenem resistance in Turkey: Repeat report on OXA-48 in Klebsiella pneumoniae and first report on IMP-1 beta-lactamase in Escherichia coli. Afr J Microbiol Res. 2012;6:3874–8.
View Article
Google Scholar

[88] View Article

[89] Google Scholar

[ref24] 24. Morris D, Boyle F, Ludden C, Condon I, Hale J, O’Connell N et al. Production of KPC-2 Carbapenemase by an Escherichia coli Clinical Isolate Belonging to the International ST131 Clone. Antimicrob Agents Chemother. 2011;55:4935–6. pmid:21768521
View Article
PubMed/NCBI
Google Scholar

[91] View Article

[92] PubMed/NCBI

[93] Google Scholar

[ref25] 25. Budak S, Oncul O, Aktas Z, Acar A, Ozyurt M, Turhan V, et al. The determination of carbapenem resistance in Escherichia coli and Pneumoniae isolates related to nosocomial infections and the evaluation of risk factors. Southeast Asian J Trop Med Public Health. 2014;45(1):113–22. pmid:24964660
View Article
PubMed/NCBI
Google Scholar

[95] View Article

[96] PubMed/NCBI

[97] Google Scholar

[ref26] 26. Sharma A, Bakthavatchalam YD, Gopi R, Anandan S, Verghese VP, Veeraraghavan B. Mechanisms of Carbapenem Resistance in K. pneumoniae and E. coli from Bloodstream Infections in India. J Infect Dis Ther. 2016;4:293.
View Article
Google Scholar

[99] View Article

[100] Google Scholar

[ref27] 27. Doi Y, Wachino JI, Arakawa Y. Aminoglycoside Resistance: The Emergence of Acquired 16S Ribosomal RNA Methyltransferases. Infect Dis Clin North Am. 2016; 30(2): 523–37. pmid:27208771
View Article
PubMed/NCBI
Google Scholar

[102] View Article

[103] PubMed/NCBI

[104] Google Scholar

[ref28] 28. Yu F, Wang L, Pan J, Yao D, Chen C, Zhu T, et al. Prevalence of 16S rRNA methylase genes in Klebsiella pneumoniae isolates from a Chinese teaching hospital: coexistence of rmtB and armA genes in the same isolate. Diagn Microbiol Infect Dis. 2009;64:57–63. pmid:19232867
View Article
PubMed/NCBI
Google Scholar

[106] View Article

[107] PubMed/NCBI

[108] Google Scholar

[ref29] 29. Taylor E, Sriskandan S, Woodford N, Hopkins KL. High prevalence of 16S rRNA methyltransferases among carbapenemase-producing Enterobacteriaceae in the UK and Ireland. Int J Antimicrob Agents. 2018; 52(2):278–82. pmid:29596903
View Article
PubMed/NCBI
Google Scholar

[110] View Article

[111] PubMed/NCBI

[112] Google Scholar

[ref30] 30. Poirel L, Goutines J, Aires-de-Sousa M, Nordmann P. High Rate of Association of 16S rRNA Methylases and Carbapenemases in Enterobacteriaceae Recovered from Hospitalized Children in Angola. Antimicrob Agents Chemother. 2018;62:e00021–18. pmid:29439957
View Article
PubMed/NCBI
Google Scholar

[114] View Article

[115] PubMed/NCBI

[116] Google Scholar

[ref31] 31. Ravikant , Kumar P, Ranotkar S, Zutshi S, Lahkar M, Phukan C, et al. Prevalence and identification of extended spectrum β-lactamases (ESBL) in Escherichia coli isolated from a tertiary care hospital in North-East India. Ind J Exp Biol. 2016;54:108–114.
View Article
Google Scholar

[118] View Article

[119] Google Scholar

[ref32] 32. Elnahriry SS, Khalifa HO, Soliman AM, Ahmed AM, Hussein AM, Shimamoto T, et al. Emergence of Plasmid-Mediated Colistin Resistance Gene mcr-1 in a Clinical Escherichia coli Isolate from Egypt. Antimicrob Agents Chemother. 2016;60 (5):3249–50. pmid:26953204
View Article
PubMed/NCBI
Google Scholar

[121] View Article

[122] PubMed/NCBI

[123] Google Scholar

[ref33] 33. Ghafur A, Shankar C, GnanaSoundari P, Venkatesan M, Mani D, Thirunarayanan MA, et al. Detection of chromosomal and plasmid-mediated mechanisms of colistin resistance in Escherichia coli and Klebsiella pneumoniae from Indian food samples. J Glob Antimicrob Resist. 2019;16:48–52. pmid:30244040
View Article
PubMed/NCBI
Google Scholar

[125] View Article

[126] PubMed/NCBI

[127] Google Scholar

[ref34] 34. Yang F, Shen C, Zheng X, Liu Y, El-Sayed Ahmed MAE, Zhao Z, et al. Plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli and Klebsiella pneumoniae isolated from market retail fruits in Guangzhou, China. Infect Drug Resist. 2019;12:385–9. pmid:30809099
View Article
PubMed/NCBI
Google Scholar

[129] View Article

[130] PubMed/NCBI

[131] Google Scholar

[ref35] 35. Ikram R, Psutka R, Carter A, Priest P. An outbreak of multi-drug resistant Escherichia coli urinary tract infection in an elderly population: a case-control study of risk factors. BMC Infect Dis. 2015;15:224. pmid:26054866
View Article
PubMed/NCBI
Google Scholar

[133] View Article

[134] PubMed/NCBI

[135] Google Scholar

[ref36] 36. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, Semmler T, et al. Emergence of human pandemic O25:H4‐ST131 CTX‐M‐15 extended‐spectrum‐β‐lactamase‐producing Escherichia coli among companion animals. J Antimicrob Chemother. 2010;65:651–60. pmid:20118165
View Article
PubMed/NCBI
Google Scholar

[137] View Article

[138] PubMed/NCBI

[139] Google Scholar

[ref37] 37. Brolund A, Edquist PJ, Makitalo B, Olsson-Liljequist B, Soderblom T, Wisell KT, et al. Epidemiology of extended-spectrum b-lactamase-producing Escherichia coli in Sweden 2007–2011. Clin Microbiol Infect. 2014;20:O344–O352. pmid:24118431
View Article
PubMed/NCBI
Google Scholar

[141] View Article

[142] PubMed/NCBI

[143] Google Scholar

[ref38] 38. Yang P, Xie Y, Feng P, Zong Z. blaNDM-5 Carried by an IncX3 Plasmid in Escherichia coli Sequence Type 167. Antimicrob Agents Chemother. 2014;58(12):7548–52. pmid:25246393
View Article
PubMed/NCBI
Google Scholar

[145] View Article

[146] PubMed/NCBI

[147] Google Scholar

[ref39] 39. Feng Y, Yang P, Xie Y, Wang X, McNally A, Zong Z. Escherichia coli of sequence type 3835 carrying blaNDM-1, blaCTX-M-15, blaCMY-42 and blaSHV-12. Sci Rep. 2015;5:12275. pmid:26194736
View Article
PubMed/NCBI
Google Scholar

[149] View Article

[150] PubMed/NCBI

[151] Google Scholar

[ref40] 40. Shen P, Yi M, Fu Y, Ruan Z, Du X, Yu Y, et al. Detection of an Escherichia coli Sequence Type 167 Strain with Two Tandem Copies of blaNDM-1 in the Chromosome. J Clin Microbiol. 2017;55:199–205. pmid:27807154
View Article
PubMed/NCBI
Google Scholar

[153] View Article

[154] PubMed/NCBI

[155] Google Scholar

[ref41] 41. Matsumura Y, Yamamoto M, Nagao M, Ito Y, Takakura S, Ichiyama S, et al. Association of Fluoroquinolone Resistance, Virulence Genes, and IncF Plasmids with Extended-Spectrum-_-Lactamase-Producing Escherichia coli Sequence Type 131 (ST131) and ST405 Clonal Groups. Antimicrob Agents Chemother. 2013;57(10):4736–42. pmid:23856781
View Article
PubMed/NCBI
Google Scholar

[157] View Article

[158] PubMed/NCBI

[159] Google Scholar

[ref42] 42. Zhang X, Feng Y, Zhou W, McNally A, Zong Z. Cryptic transmission of ST405 Escherichia coli carrying blaNDM-4 in hospital. Sci Rep. 2018;8:390. pmid:29321680
View Article
PubMed/NCBI
Google Scholar

[161] View Article

[162] PubMed/NCBI

[163] Google Scholar

[ref43] 43. Cai JC, Zhang R, Hu YY, Zhou HW, Chen GX. Emergence of Escherichia coli Sequence Type 131 Isolates Producing KPC-2 Carbapenemase in China. Antimicrob Agents Chemother. 2014;58(2):1146–52. pmid:24323475
View Article
PubMed/NCBI
Google Scholar

[165] View Article

[166] PubMed/NCBI

[167] Google Scholar

[ref44] 44. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, et al. Escherichia coli Sequence Type 410 Is Causing New International High-Risk Clones. mSphere. 2018;3(4):pii: e00337–18. pmid:30021879
View Article
PubMed/NCBI
Google Scholar

[169] View Article

[170] PubMed/NCBI

[171] Google Scholar

[ref45] 45. Tchesnokova V, Aprikian P, Kisiela D, Gowey S, Korotkova N, Thomas W et al. Type 1 Fimbrial Adhesin FimH Elicits an Immune Response That Enhances Cell Adhesion of Escherichia coli. Infect. Immun. 2011;79(10):3895–3904. pmid:21768279
View Article
PubMed/NCBI
Google Scholar

[173] View Article

[174] PubMed/NCBI

[175] Google Scholar

[ref46] 46. Bouckaert J, Mackenzie J, de Paz JL, Chipwaza B, Choudhury D, Zavialov A et al. The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol Microbiol. 2006;61(6):1556–1568. pmid:16930149
View Article
PubMed/NCBI
Google Scholar

[177] View Article

[178] PubMed/NCBI

[179] Google Scholar

Figures

Abstract

Background

Methods

Results

Conclusions

Introduction

Materials and methods

Isolates and identification

Antimicrobial susceptibility testing (AST)

Disc diffusion.

Minimum Inhibitory Concentration (MIC) for colistin.

Next generation sequencing and genome assembly

Genome annotation

Genome based MLST analysis

Genome comparison analyses

Ethical clearance

Results

Antimicrobial susceptibility

Whole genome sequence analysis

Phylogeny of MDR E. coli.

E. coli genome comparison.

Core vs pan genome

Serotype prediction.

Genetic virulence factors of MDR E. coli.

Comparison of virulence and clonal traits.

Antimicrobial resistance genetic determinants.

Discussion

Conclusions

Supporting information

S1 Table. Serotype and antimicrobial resistance profiles of MDR E. coli from blood stream infections (n = 60).

S1 Fig. Circular genome plot comparing 60 MDR E. coli thereby showing differences in genome composition in comparison to the reference genome NC000913 E. coli.

Acknowledgments

References