Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil

Extra-intestinal pathogenic Escherichia coli (ExPEC) represent an emerging pathogen, with pandemic strains increasingly involved in cases of urinary tract infections (UTIs), bacteremia, and meningitis. In addition to affecting humans, the avian pathotype of ExPEC, avian pathogenic E. coli (APEC), causes severe economic losses to the poultry industry. Several studies have revealed overlapping characteristics between APEC and human ExPEC, leading to the hypothesis of a zoonotic potential of poultry strains. However, the description of certain important pandemic clones, such as Sequence Type 73 (ST73), has not been reported in food sources. We characterized 27 temporally matched APEC strains from diverse poultry farms in Brazil belonging to the O6 serogroup because this serogroup is frequently described as a causal factor in UTI and septicemia in humans in Brazil and worldwide. The isolates were genotypically characterized by identifying ExPEC virulence factors, phylogenetically tested by phylogrouping and multilocus sequence type (MLST) analysis, and compared to determine their similarity employing the pulsed field gel electrophoresis (PFGE) technique. The strains harbored a large number of virulence determinants that are commonly described in uropathogenic E. coli (UPEC) and sepsis associated E. coli (SEPEC) strains and, to a lesser extent in neonatal meningitis associated E. coli (NMEC), such as pap (85%), sfa (100%), usp (100%), cnf1 (22%), kpsMTII (66%), hlyA (52%), and ibeA (4%). These isolates also yielded a low prevalence of some genes that are frequently described in APEC, such as iss (37%), tsh, ompT, and hlyF (8% each), and cvi/cva (0%). All strains were classified as part of the B2 phylogroup and sequence type 73 (ST73), with a cluster of 25 strains showing a clonal profile by PFGE. These results further suggest the zoonotic potential of some APEC clonal lineages and their possible role in the epidemiology of human ExPEC, in addition to providing the first description of the O6-B2-ST73 clonal group in poultry.

[1]  L. Riley,et al.  Escherichia coli sequence type 73 as a cause of community acquired urinary tract infection in men and women in Rio de Janeiro, Brazil. , 2017, Diagnostic microbiology and infectious disease.

[2]  M. Woodward,et al.  Comparative genomics of European avian pathogenic E. Coli (APEC) , 2016, BMC Genomics.

[3]  J. Wain,et al.  Population structure of Escherichia coli causing bacteraemia in the UK and Ireland between 2001 and 2010. , 2016, The Journal of antimicrobial chemotherapy.

[4]  R. Ecco,et al.  Diversity of Escherichia coli strains involved in vertebral osteomyelitis and arthritis in broilers in Brazil , 2016, BMC Veterinary Research.

[5]  N. Woodford,et al.  Trends in ExPEC serogroups in the UK and their significance , 2016, European Journal of Clinical Microbiology & Infectious Diseases.

[6]  A. Manges Escherichia coli and urinary tract infections: the role of poultry-meat. , 2016, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[7]  K. Paszkiewicz,et al.  Increase in bacteraemia cases in the East Midlands region of the UK due to MDR Escherichia coli ST73: high levels of genomic and plasmid diversity in causative isolates. , 2016, The Journal of antimicrobial chemotherapy.

[8]  R. Dolz,et al.  Diversity of Multi-Drug Resistant Avian Pathogenic Escherichia coli (APEC) Causing Outbreaks of Colibacillosis in Broilers during 2012 in Spain , 2015, PloS one.

[9]  Xiaoqiang Liu,et al.  Multilocus Sequence Typing and Virulence Profiles in Uropathogenic Escherichia coli Isolated from Cats in the United States , 2015, PloS one.

[10]  Jingwei Jiang,et al.  Comparative Genomic Analysis Shows That Avian Pathogenic Escherichia coli Isolate IMT5155 (O2:K1:H5; ST Complex 95, ST140) Shares Close Relationship with ST95 APEC O1:K1 and Human ExPEC O18:K1 Strains , 2014, PloS one.

[11]  C. Logue,et al.  Overlapped Sequence Types (STs) and Serogroups of Avian Pathogenic (APEC) and Human Extra-Intestinal Pathogenic (ExPEC) Escherichia coli Isolated in Brazil , 2014, PloS one.

[12]  T. Knöbl,et al.  Virulence Profiles, Phylogenetic Background, and Antibiotic Resistance of Escherichia coli Isolated from Turkeys with Airsacculitis , 2014, TheScientificWorldJournal.

[13]  L. Riley,et al.  Pandemic lineages of extraintestinal pathogenic Escherichia coli. , 2014, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[14]  M. Mellata,et al.  Human and avian extraintestinal pathogenic Escherichia coli: infections, zoonotic risks, and antibiotic resistance trends. , 2013, Foodborne pathogens and disease.

[15]  L. Price,et al.  Foodborne urinary tract infections: a new paradigm for antimicrobial-resistant foodborne illness , 2013, Front. Microbiol..

[16]  E. Denamur,et al.  The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. , 2013, Environmental microbiology reports.

[17]  Gemma C. Langridge,et al.  Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveals the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms , 2013 .

[18]  Paul D. Cotter,et al.  Nucleic acid-based approaches to investigate microbial-related cheese quality defects , 2012, Front. Microbio..

[19]  P. Garneau,et al.  Is Escherichia coli urinary tract infection a zoonosis? Proof of direct link with production animals and meat , 2012, European Journal of Clinical Microbiology & Infectious Diseases.

[20]  A. Manges,et al.  Food-borne origins of Escherichia coli causing extraintestinal infections. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[21]  J. Cheesbrough,et al.  Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England. , 2012, The Journal of antimicrobial chemotherapy.

[22]  J. Martínez,et al.  Natural Antibiotic Resistance and Contamination by Antibiotic Resistance Determinants: The Two Ages in the Evolution of Resistance to Antimicrobials , 2012, Front. Microbio..

[23]  J. Pitout Extraintestinal Pathogenic Escherichia coli: A Combination of Virulence with Antibiotic Resistance , 2012, Front. Microbio..

[24]  J. Harel,et al.  Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. , 2011, FEMS immunology and medical microbiology.

[25]  Karen Ejrnæs Bacterial characteristics of importance for recurrent urinary tract infections caused by Escherichia coli. , 2011, Danish medical bulletin.

[26]  J. Klena,et al.  CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. , 2011, Microbial drug resistance.

[27]  Y. Wannemuehler,et al.  Avian-Pathogenic Escherichia coli Strains Are Similar to Neonatal Meningitis E. coli Strains and Are Able To Cause Meningitis in the Rat Model of Human Disease , 2010, Infection and Immunity.

[28]  Richard J. Reid-Smith,et al.  Food Reservoir for Escherichia coli Causing Urinary Tract Infections , 2010, Emerging infectious diseases.

[29]  L. Riley,et al.  Clonal composition of Escherichia coli causing community-acquired urinary tract infections in the State of Rio de Janeiro, Brazil. , 2009, Microbial drug resistance.

[30]  J. Blanco,et al.  Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution , 2009, BMC Microbiology.

[31]  M. Kuskowski,et al.  Multiple-Host Sharing, Long-Term Persistence, and Virulence of Escherichia coli Clones from Human and Animal Household Members , 2008, Journal of Clinical Microbiology.

[32]  T. Johnson,et al.  Identification of Minimal Predictors of Avian Pathogenic Escherichia coli Virulence for Use as a Rapid Diagnostic Tool , 2008, Journal of Clinical Microbiology.

[33]  K. Kim,et al.  Comparison of Extraintestinal Pathogenic Escherichia coli Strains from Human and Avian Sources Reveals a Mixed Subset Representing Potential Zoonotic Pathogens , 2008, Applied and Environmental Microbiology.

[34]  F. Dziva,et al.  Colibacillosis in poultry: unravelling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts , 2008, Avian pathology : journal of the W.V.P.A.

[35]  M. Kuskowski,et al.  Virulence Genotypes and Phylogenetic Background of Escherichia coli Serogroup O6 Isolates from Humans, Dogs, and Cats , 2007, Journal of Clinical Microbiology.

[36]  L. Wieler,et al.  Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? , 2007, International journal of medical microbiology : IJMM.

[37]  G. Prats,et al.  Pathogenicity island markers in commensal and uropathogenic Escherichia coli isolates. , 2006, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[38]  B. Swaminathan,et al.  Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. , 2006, Foodborne pathogens and disease.

[39]  T. Johnson,et al.  Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. , 2005, Microbiology.

[40]  Yu-hua Chen,et al.  ibeA, a virulence factor of avian pathogenic Escherichia coli. , 2005, Microbiology.

[41]  A. Siitonen,et al.  Molecular epidemiology of 3 putative virulence genes for Escherichia coli urinary tract infection-usp, iha, and iroN(E. coli). , 2002, The Journal of infectious diseases.

[42]  J. Fairbrother,et al.  Avian pathogenic Escherichia coli (APEC). , 1999, Veterinary research.

[43]  J. R. Johnson,et al.  Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. , 2000, The Journal of infectious diseases.

[44]  R. Sellwood,et al.  Escherichia Coli Associated with Neonatal Diarrhoea in Piglets and Calves , 1981 .