Well-known and new variants of pathogenic Escherichia coli as a consequence of the plastic genome
Katarzyna Baldy-Chudzik 1 , Ewa Bok 1 , Justyna Mazurek 1Abstract
E. coli is a diverse bacterial species encompassing commensal as well as intestinal and extraintestinal pathogenic strains. The ability to adapt to so many different niches in the host organism is determined by the extreme genomic plasticity of E. coli. The genetic diversity is due to a complex phylogenetic structure in which besides the well-known main groups A, B1, B2 and D, four new groups, C, E, F and Clad I, have been characterized recently. The mobile gene pool exchanged by horizontal gene transfer (HGT) is another important driving force in the evolution of E. coli. Pathogenicity of strains is conditioned by a specific repertoire of virulence factors located on the mobile genetic elements and transmitted by HGT. The environment changing constantly stimulates the formation of new virulence gene combinations that generate the formation, not observed so far, of new pathogenic clones of higher capacity for virulence and greater expansiveness. The presence of very similar virulence plasmids carrying conserved combinations of the virulence genes (CVP) among extraintestinal pathogenic strains in humans and birds has been observed. It indicates a real possibility of occurrence of common virulence factors. The increase in drug resistance among pathogenic E. coli is also reflected in the prevalence of highly expansive clones exhibiting both high virulence and resistance. The presented data indicate that further studies are required to determine the interdependencies of resistance and virulence at the genetic level to help improve our management of the infectious diseases caused by these bacteria.
References
- 1. Ahmed S.A., Awosika J., Baldwin C., Bishop-Lilly K.A., Biswas B.,Broomall S., Chain P.S., Chertkov O., Chokoshvili O., Coyne S., DavenportK., Detter J.C., Dorman W., Erkkila T.H., Folster J.P. i wsp.: Genomiccomparison of Escherichia coli O104:H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including Shigatoxin encoding phage stx2. PLoS One, 2012; 7: e48228
Google Scholar - 2. Amaya E., Reyes D., Vilchez S., Paniagua M., Möllby R., Nord C.E.,Weintraub A.: Antibiotic resistance patterns of intestinal Escherichia coliisolates from Nicaraguan children. J. Med. Microbiol., 2011; 60: 216-222
Google Scholar - 3. Barnich N., Carvalho F.A., Glasser A.L., Darcha C., Jantscheff P.,Allez M., Peeters H., Bommelaer G., Desreumaux P., Colombel J.F.,Darfeuille-Michaud A.: CEACAM6 acts as a receptor for adherent-invasiveE. coli, supporting ileal mucosa colonization in Crohn disease.J. Clin. Invest., 2007; 117: 1566-1574
Google Scholar - 4. Baudry-Simner P.J., Singh A., Karlowsky J.A., Hoban D. J., ZhanelG.G., the Canadian Antimicrobial Resistance Alliance.: Mechanismsof reduced susceptibility to ciprofloxacin in Escherichia coli isolatesfrom Canadian hospitals. Can. J. Infect. Dis. Med. Microbiol., 2012;23: e60-e71 5 Bielaszewska M., Mellmann A., Zhang W., Köck R., Fruth A., BauwensA., Peters G., Karch H.: Characterisation of the Escherichia colistrain associated with an outbreak of haemolytic uraemic syndromein Germany, 2011: a microbiological study. Lancet Infect. Dis.,2011; 11: 671-676
Google Scholar - 5. years of age with acute diarrhea in Tehran children’s hospitals. J.Infect., 2009; 58: 21-27
Google Scholar - 6. Blanco J., Mora A., Mamani R., López C., Blanco M., Dahbi G., HerreraA., Blanco J.E., Alonso M.P., García-Garrote F., Chaves F., OrellanaM.Á., Martínez-Martínez L., Calvo J., Prats G. i wsp.: Nationalsurvey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal group O25b:H4-B2-ST131, O15:H1–D-ST393 and CGA-D-ST69 with high virulence gene content in Spain.J. Antimicrob. Chemoter., 2011; 66: 2011-2021
Google Scholar - 7. Blanco M., Blanco J.E., Alonso M.P., Mora A., Balsalobre C., MuñoaF., Juárez A., Blanco J.: Detection of pap, sfa and afa adhesion-encodingoperons in uropathogenic Escherichia coli strains: relationshipwith expression of adhesins and production of toxins. Res. Microbiol.,1997; 148: 745-755
Google Scholar - 8. Bonacorsi S., Bingen E.: Molecular epidemiology of Escherichiacoli causing neonatal meningitis. Int. J. Med. Microbiol.,2005; 295:373-381
Google Scholar - 9. Bonnet R.: Growing group of extended-spectrum β-lactamases:the CTX-M enzymes. Antimicrob. Agents Chemother., 2004; 48: 1-14
Google Scholar - 10. Branger C., Zamfir O., Geoffroy S., Laurans G., Arlet G., ThienH.V., Gouriou S., Picard B., Denamur E.: Genetic background of Escherichiacoli and extended-spectrum β-lactamase type. Emerg. Infect.Dis., 2005; 11: 54-61
Google Scholar - 11. Brisse S., Diancourt L., Laouénan C., Vigan M., Caro V., Arlet G.,Drieux L., Leflon-Guibout V., Mentré F., Jarlier V., Nicolas-ChanoineM.H., and the Coli β Study Group.: Phylogenetic distribution of CTX–M- and non-extended-spectrum-β-lactamase-producing Escherichiacoli isolates: group B2 isolates, except clone ST131, rarely produceCTX-M enzymes. J. Clin. Microbiol., 2012; 50: 2974-2981
Google Scholar - 12. Bryce J., Boschi-Pinto C., Shibuya K., Black R.E., the WHO ChildHealth Epidemiology Reference Group: WHO estimates of the causesof death in children. Lancet 2005; 365: 1147-1152
Google Scholar - 13. Brzuszkiewicz E., Thürmer A., Schuldes J., Leimbach A., LiesegangH., Meyer F.D., Boelter J., Petersen H., Gottschalk G., Daniel R.:Genome sequence analyses of two isolates from the recent Escherichiacoli outbreak in Germany reveal the emergence of a new pathotype:entero-aggregative haemorrhagic Escherichia coli (EAHEC). Arch. Microbiol.,2011; 193: 883-891
Google Scholar - 14. Bush K.: Extended-spectrum β-lactamases in North America,1987-2006. Clin. Microbiol. Infect., 2008; 14, Suppl. 1: 134-143
Google Scholar - 15. Carattoli A.: Resistance plasmid families in Enterobacteriaceae.Antimicrob. Agents Chemother., 2009; 53: 2227-2238
Google Scholar - 16. Cerquetti M., Giufrè M., García-Fernández A., Accogli M., FortiniD., Luzzi I., Carattoli A.: Ciprofloxacin resistant, CTX-M-15-producingEscherichia coli ST131 clone in extraintestinal infections in Italy. Clin.Microbiol. Infect., 2010; 16: 1555-1558
Google Scholar - 17. Chaudhuri R.R., Henderson, I.R.: The evolution of the Escherichiacoli phylogeny. Infect. Genet. Evol., 2012; 12: 214-226
Google Scholar - 18. Clermont O., Bonacorsi S., Bingen E.: Rapid and simple determinationof the Escherichia coli phylogenetic group. Appl. Environ.Microbiol., 2000; 66: 4555-4558
Google Scholar - 19. Clermont O., Christenson J.K., Denamur E., Gordon D.M.: TheClermont Escherichia coli phylo-typing method revisited: improvementof specificity and detection of new phylo-groups. Environ.Microbiol. Rep., 2013; 5: 58-65
Google Scholar - 20. Clermont O., Lavollay M., Vimont S., Deschamps C., Forestier C.,Branger C., Denamur E., Arlet G.: The CTX-M-15-producing Escherichiacoli diffusing clone belongs to a highly virulent B2 phylogeneticsubgroup. J. Antimicrob. Chemother., 2008; 61: 1024-1028
Google Scholar - 21. Clermont O., Olier M., Hoede C., Diancourt L., Brisse S., KeroudeanM., Glodt J., Picard B., Oswald E., Denamur E.: Animal and humanpathogenic Escherichia coli strains share common genetic backgrounds.Infect. Genet. Evol., 2011; 11: 654-662
Google Scholar - 22. Coelho A., Mora A., Mamani R., López C., González-López J.J.,Larrosa M.N., Quintero-Zarate J.N., Dahbi G., Herrera A., Blanco J.E.,Blanco M., Alonso M.P., Prats G., Blanco J.: Spread of Escherichia coliO25b:H4-B2-ST131 producing CTX-M-15 and SHV-12 with high virulencegene content in Barcelona (Spain). J. Antimicrob. Chemother.,2011; 66: 517-526
Google Scholar - 23. Czaja C., Stamm E., Stapleton A., Roberts P., Hawn T., ScholesD., Samadpour M., Hultgren S.J., Hooton T.M.: Prospective cohortstudy of microbial and inflammatory events immediately precedingEscherichia coli recurrent urinary tract infection in women. J. Infect.Dis., 2009; 200: 528-536
Google Scholar - 24. Danzeisen J.L., Wannemuehler Y., Nolan L.K., Johnson T.J.: Comparisonof multilocus sequence analysis and virulence genotypingof Escherichia coli from live birds, retail poultry meat, and humanextraintestinal infection. Avian Dis., 2013; 57: 104-108
Google Scholar - 25. Darfeuille-Michaud A., Boudeau J., Bulois P., Neut C., Glasser A.L.,Barnich N., Bringer M.A., Swidsinski A., Beaugerie L., Colombel J.F.:High prevalence of adherent-invasive Escherichia coli associated withileal mucosa in Crohn’s disease. Gastroenterology, 2004; 127: 412-421
Google Scholar - 26. Dhanji H., Doumith M., Rooney P.J., O’Leary M.C., Loughrey A.C.,Hope R., Woodford N., Livermore D.M.: Molecular epidemiology offluoroquinolone-resistant ST131 Escherichia coli producing CTX-Mextended – spectrum β-lactamases in nursing home in Belfast, UK.J. Antimicrob. Chemoter., 2011; 66: 297-303
Google Scholar - 27. Djie-Maletz A., Reither K., Danour S., Anyidoho L., Saad E., DanikuuF., Ziniel P., Weitzel T., Wagner J., Bienzle U., Stark K., Seidu–Korkor A., Mockenhaupt F.P., Ignatius R.: High rate of resistanceto locally used antibiotics among enteric bacteria from childrenin Northern Ghana. J. Antimicrob. Chemother., 2008; 61: 1315-1318
Google Scholar - 28. Dobrindt U.: (Patho-)Genomics of Escherichia coli. Int. J. Med.Microbiol., 2005; 295: 357-371
Google Scholar - 29. Donnenberg, M.S., Whittam T.S.: Pathogenesis and evolution ofvirulence in enteropathogenic and enterohemorrhagic Escherichiacoli. J. Clin. Invest., 2001; 107: 539-548
Google Scholar - 30. Dutta S., Guin S., Ghosh S., Pazhani G.P., Rajendran K., BhattacharyaM.K., Takeda Y., Nair G.B., Ramamurthy T.: Trends in the prevalenceof diarrheagenic Escherichia coli among hospitalized diarrhealpatients in Kolkata, India. PLoS One, 2013; 8: e56068
Google Scholar - 31. Elliott S.J., Sperandio V., Girón J.A., Shin S., Mellies J.L., WainwrightL., Hutcheson S.W., McDaniel T.K., Kaper J.B.: The locus of enterocyteeffacement (LEE)-encoded regulator controls expression of both LEEandnon-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagicEscherichia coli. Infect. Immun., 2000; 68: 6115-6126
Google Scholar - 32. Escobar-Paramo P., Clermont O., Blanc-Potard A.B., Bui H., LeBouguenec C., Denamur E.: A specific genetic background is requiredfor acquisition and expression of virulence factors in Escherichia coli.Mol. Biol. Evol., 2004; 21: 1085-1094
Google Scholar - 33. Escobar-Paramo P., Giudicelli C., Parsot C., Denamur E.: Theevolutionary history of Shigella and enteroinvasive Escherichia colirevised. J. Mol. Evol., 2003; 57: 140-148
Google Scholar - 34. Ewers C., Li G., Wilking H., Kiessling S., Alt K., Antáo E.M., LaturnusC., Diehl I., Glodde S., Homeier T., Böhnke U., Steinrück H.,Philipp H.C., Wieler L.H.: Avian pathogenic, uropathogenic, and newbornmeningitis-causing Escherichia coli: how closely related arethey? Int. J. Med. Microbiol., 2007; 297: 163-176
Google Scholar - 35. Farfan M.J., Torres A.G.: Molecular mechanisms that mediatecolonization of Shiga toxin-producing Escherichia coli strains. Infect.Immun., 2012; 80: 903-913
Google Scholar - 36. França F.L., Wells T.J., Browning D.F., Nogueira R.T., Sarges F.S.,Pereira A.C., Cunningham A.F., Lucheze K., Rosa A.C., Henderson I.R.,das Graças de Luna M.: Genotypic and phenotypic characterisationof enteroaggregative Escherichia coli from Children in Rio de Janeiro,Brazil. PLoS One, 2013; 8: e69971
Google Scholar - 37. Garza-Ramos U., Barrios H., Hernandez-Vargas M.J., Rojas-MorenoT., Reyna-Flores F., Tinoco P., Othon V., Poirel L., Nordmann P.,Cattoir V., Ruiz-Palacios G., Fernandez J.L., Santamaria R.I., BustosP., Castro N., Silva-Sanchez J.: Transfer of quinolone resistance geneqnrA1 to Escherichia coli through a 50 kb conjugative plasmid resultingfrom the splitting of a 300 kb plasmid. J. Antimicrob. Chemother.,2012; 67: 1627-1634
Google Scholar - 38. Gibreel T.M., Dodgson A.R., Cheesbrough J., Fox A.J., Bolton F.J.,Upton M.: Population structure, virulence potential and antibioticsusceptibility of uropathogenic Escherichia coli from Northwest England.J. Antimicrob. Chemother., 2012; 67: 346-356
Google Scholar - 39. Goffaux F., China B., Mainil J.: Organisation and in vitro expressionof esp genes of the LEE (locus of enterocyte effacement) of bovineenteropathogenic and enterohemorrhagic Escherichia coli. Vet.Microbiol., 2001; 83: 275-286
Google Scholar - 40. Gordon D.M., Clermont O., Tolley H., Denamur E.: AssigningEscherichia coli strains to phylogenetic groups: multi-locus sequencetyping versus the PCR triplex method. Environ Microbiol., 2008;10: 2484-2496
Google Scholar - 41. Gordon D.M., Stern S.E., Collignon P.J.: Influence of the age andsex of human hosts on the distribution of Escherichia coli ECOR groupsand virulence traits. Microbiology, 2005; 151: 15-23
Google Scholar - 42. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W.,Gascuel O.: New algorithms and methods to estimate maximum–likelihood phylogenies: assessing the performance of PhyML 3.0.Syst. Biol., 2010; 59: 307-321
Google Scholar - 43. Gupta S.K., Keck J., Ram P.K., Crump J.A., Miller M.A., Mintz E.D.:Analysis of data gaps pertaining to enterotoxigenic Escherichia coliinfections in low and medium human development index countries,1984-2005. Epidemiol. Infect., 2008; 136: 721-738
Google Scholar - 44. Harris A.M., Chowdhury F., Begum Y.A., Khan A.I., Faruque A.S.,Svennerholm A.M., Harris J.B., Ryan E.T., Cravioto A., CalderwoodS.B., Qadri F.: Shifting prevalence of major diarrheal pathogens inpatients seeking hospital care during floods in 1998, 2004, and 2007in Dhaka, Bangladesh. Am. J. Trop. Med. Hyg., 2008; 79: 708-714
Google Scholar - 45. Hauser E., Mellmann A., Semmler T., Stoeber H., Wieler L.H., KarchH., Kuebler N., Fruth A., Harmsen D., Weniger T., Tietze E., Schmidt H.:Phylogenetic and molecular analysis of food-borne Shiga toxin-producingEscherichia coli. Appl. Environ. Microbiol., 2013; 79: 2731-2740
Google Scholar - 46. Herzer P.J., Inouye S., Inouye M., Whittam T.S.: Phylogeneticdistribution of branched RNA-linked multicopy single-strandedDNA among natural isolates of Escherichia coli. J. Bacteriol., 1990;172: 6175-6181
Google Scholar - 47. Huang D.B., Mohanty A., DuPont H.L., Okhuysen P.C., ChiangT.: A review of an emerging enteric pathogen: enteroaggregativeEscherichia coli. J. Med. Microbiol., 2006; 55: 1303-1311
Google Scholar - 48. Jadhav S., Hussain A., Devi S., Kumar A., Parveen S.: Virulencecharacteristics and genetic affinities of multiple drug resistanturopathogenic Escherichia coli from a semi urban locality in India.PLoS One, 2011; 6: e18063
Google Scholar - 49. Jafari F., Garcia-Gil L.J., Salmanzadeh-Ahrabi S., Shokrzadeh L.,Aslani M.M., Pourhoseingholi M.A., Derakhshan F., Zali M.R.: Diagnosisand prevalence of enteropathogenic bacteria in children less than
Google Scholar - 50. Jakobsen L., Garneau P., Kurbasic A., Bruant G., Stegger M., HarelJ., Jensen K.S., Brousseau R., Hammerum A.M., Frimodt-Møller N.:Microarray-based detection of extended virulence and antimicrobialresistance gene profiles in phylogroup B2 Escherichia coli of human,meat and animal origin. J. Med. Microbiol., 2011; 60: 1502-1511
Google Scholar - 51. Jaureguy F., Landraud L., Passet V., Diancour, L., Frapy E., GuigonG., Carbonnelle E., Lortholary O., Clermont O., Denamur E., Picard B.,Nassif X., Brisse S.: Phylogenetic and genomic diversity of humanbacteremic Escherichia coli strains. BMC Genomics, 2008; 9: 560-566
Google Scholar - 52. Johnson J.R., Johnston B., Clabots C., Kuskowski M.A., CastanheiraM.: Escherichia coli sequence type ST131 as the major cause ofserious multidrug-resistant E. coli infections in the United States(2007). Clin. Infect. Dis., 2010; 51: 286-294
Google Scholar - 53. Johnson J.R., Owens K.L., Clabots C.R., Weissman S.J., CannonS.B.: Phylogenetic relationships among clonal groups of extraintestinalpathogenic Escherichia coli as assessed by multi-locus sequenceanalysis. Microbes Infect., 2006; 8: 1702-1713
Google Scholar - 54. Johnson J.R., Stell A.L.: Extended virulence genotypes of Escherichiacoli strains from patients with urosepsis in relation to phylogenyand host compromise. J. Infect. Dis., 2000; 181: 261-272
Google Scholar - 55. Johnson T.J., Jordan D., Kariyawasam S., Stell A.L., Bell N.P., WannemuehlerY.M., Alarcon C.F., Li G., Tivendale K.A., Logue C.M., NolanL.K.: Sequence analysis and characterization of a transferablehybrid plasmid encoding multidrug resistance and enabling zoonoticpotential for extraintestinal Escherichia coli. Infect. Immun.,2010; 78: 1931-1942
Google Scholar - 56. Johnson T.J., Kariyawasam S.,Wannemuehler Y., MangiameleP., Johnson S.J., Doetkott C., Skyberg J.A., Lynne A.M., Johnson J.R.,Nolan L.K.: The genome sequence of avian pathogenic Escherichia colistrain O1: K1: H7 shares strong similarities with human extraintestinalpathogenic E. coli genomes. J. Bacteriol., 2007; 189: 3228-3236
Google Scholar - 57. Johnson T.J., Lang K.S.: IncA/C plasmids: an emerging threatto human and animal health? Mob. Gen. Elements, 2012; 2: 55-58
Google Scholar - 58. Johnson T.J., Logue C.M., Johnson J.R., Kuskowski M.A., SherwoodJ.S., Barnes H.J., DebRoy C., Wannemuehler Y.M., Obata-Yasuoka M.,Spanjaard L., Nolan L.K.: Associations between multidrug resistance,plasmid content, and virulence potential among extraintestinal pathogenicand commensal Escherichia coli from humans and poultry.Foodborne Pathog. Dis., 2012; 9: 37-46
Google Scholar - 59. Johnson T.J., Nolan L.K.: Pathogenomics of the virulence plasmidsof Escherichia coli. Microbiol. Mol. Biol. Rev., 2009; 73: 750-774
Google Scholar - 60. Johnson T.J., Wannemuehler Y.M., Johnson S.J., Stell A.L., DoetkottC., Johnson J.R., Kim K.S., Spanjaard L., Nolan L.K.: Comparisonof extraintestinal pathogenic Escherichia coli strains from humanand avian sources reveals a mixed subset representing potentialzoonotic pathogens. Appl. Environ. Microbiol., 2008; 74: 7043-7050
Google Scholar - 61. Johnson T.J., Wannemuehler Y.M., Nolan L.K.: Evolution of the issgene in Escherichia coli. Appl. Environ. Microbiol., 2008; 74: 2360-2369
Google Scholar - 62. Kahali S., Sarkar B., Rajendran K., Khanam J., Yamasaki S.H.,Nandy R.K., Bhattacharya S.K., Ramamurthy T.: Virulence characteristicsand molecular epidemiology of enteroaggregative Escherichiacoli isolates from hospitalized diarrheal patients in Kolkata, India. J.Clin. Microbiol., 2004; 42: 4111-4120
Google Scholar - 63. Kaper J.B., Nataro J.P., Mobley H.L.: Pathogenic Escherichia coli.Nat. Rev. Microbiol., 2004; 2: 123-140
Google Scholar - 64. Karch H., Friedrich A.W., Gerber A., Zimmerhackl L.B., SchmidtM.A., Bielaszewska M.: New aspects in the pathogenesis of enteropathichemolytic uremic syndrome. Semin. Thromb. Hemost.,2006; 32: 105-112
Google Scholar - 65. Karisik E., Ellington M.J., Pike R., Warren R.E., Livermore D.M.,Woodford N.: Molecular characterization of plasmids encoding CTX–M-15 β-lactamases from Escherichia coli strains in the United Kingdom.J. Antimicrob. Chemother., 2006; 58: 665-668
Google Scholar - 66. Khoshvaght H., Haghi F., Zeighami H.: Extended spectrum betalactamaseproducing enteroaggregative Escherichia coli from youngchildren in Iran. Gastroenterol. Hepatol. Bed Bench., 2014; 7: 131-136
Google Scholar - 67. Kiranmayi C.B., Krishnaiah N.E. Mallika E.N.: Escherichia coliO157:H7 – an emerging pathogen in foods of animal origin. Vet.World, 2010; 3: 382-389
Google Scholar - 68. Kotlowski R., Bernstein C.N., Sepehri S., Krause D.O.: High prevalenceof Escherichia coli belonging to the B2+D phylogenetic groupin inflammatory bowel disease. Gut, 2007; 56: 669-675
Google Scholar - 69. Köhler C.D., Dobrindt U.: What defines extraintestinal pathogenicEscherichia coli? Int. J. Med. Microbiol., 2011; 301: 642-647
Google Scholar - 70. Lawrence J.G., Retchless A.C.: The interplay of homologous recombinationand horizontal gene transfer in bacterial speciation.Meth. Mol. Biol., 2009; 532: 29-53
Google Scholar - 71. Leimbach A., Hacker J., Dobrindt U.: E. coli as an all-rounder:the thin line between commensalism and pathogenicity. Curr. Top.Microbiol. Immunol., 2013; 358: 3-32
Google Scholar - 72. Lemaître C., Mahjoub-Messai F., Dupont D., Caro V., DiancourtL., Bingen E., Bidet P., Bonacorsi S.: A conserved virulence plasmidicregion contributes to the virulence of the multiresistant Escherichiacoli meningitis strain S286 belonging to phylogenetic group C. PLoSOne, 2013; 8: e74423
Google Scholar - 73. Levine M.M.: Escherichia coli that cause diarrhea: enterotoxigenic,enteropathogenic, enteroinvasive, enterohemorrhagic, andenteroadherent. J. Infect. Dis., 1987; 155: 377-389
Google Scholar - 74. Lloyd A.L., Henderson T.A., Vigil P.D., Mobley H.L.: Genomicislands of uropathogenic Escherichia coli contribute to virulence. J.Bacteriol., 2009; 191: 3469-3481
Google Scholar - 75. Martínez-Martínez L., Eliecer C.M., Rodriguez-Martinez M.J.,Calvo J., Pascual A.: Plasmid-mediated quinolone resistance. ExpertRev. Anti. Infect. Ther., 2008; 6: 685-711
Google Scholar - 76. Martinez-Medina M., Aldeguer X., Lopez-Siles M., González–Huix F., López-Oliu C., Dahbi G., Blanco J.E., Blanco J., Garcia-GilL.J., Darfeuille-Michaud A.: Molecular diversity of Escherichia coliin the human gut: new ecological evidence supporting the role ofadherent-invasive E. coli (AIEC) in Crohn’s disease. Inflamm. BowelDis., 2009; 15: 872-882
Google Scholar - 77. Martinez-Medina M., Mora A., Blanco M., López C., Alonso M.P.,Bonacors S.I., Nicolas-Chanoine M.H., Darfeuille-Michaud A., Garcia–Gil J., Blanco J.: Similarity and divergence among adherent-invasiveEscherichia coli and extraintestinal pathogenic E. coli strains. J. Clin.Microbiol., 2009; 47: 3968-3979
Google Scholar - 78. Mokady D., Gophna U., Ron E.Z.: Virulence factors of septicemicEscherichia coli strains. Int. J. Med. Microbiol., 2005; 295: 455-462
Google Scholar - 79. Momtaz H., Dehkordi F.S., Hosseini M.J., Sarshar M., Heidari M.:Serogroups, virulence genes and antibiotic resistance in Shiga toxin–producing Escherichia coli isolated from diarrheic and non-diarrheicpediatric patients in Iran. Gut Pathog., 2013; 5: 39-49
Google Scholar - 80. Mora A., Herrera A., Mamani R., López C., Alonso M.P., Blanco J.E.,Blanco M., Dahbi G.I., García-Garrote F., Pita J.M., Coira A., BernárdezM.I., Blanco J.: Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, includingCTX-M-9-producing strains, and comparison with clinical humanisolates. Appl. Environ. Microbiol., 2010; 76: 6991-6997
Google Scholar - 81. Muniesa M., Hammerl J.A., Hertwig S., Appel B., Brüssow H.:Shiga toxin-producing Escherichia coli O104:H4: a new challenge formicrobiology. Appl. Environ. Microbiol., 2012; 78: 4065-4073
Google Scholar - 82. Müller D., Hagedorn P., Brast S., Heusipp G., Bielaszewska M., FriedrichA.W., Karch H., Schmidt M.A.: Rapid identification and differentiationof clinical isolates of enteropathogenic Escherichia coli (EPEC),atypical EPEC, and shiga toxin-producing Escherichia coli by a one-stepmultiplex PCR method. J. Clin. Microbiol., 2006; 44: 2626-2629
Google Scholar - 83. Naseer U., Haldorsen B., Tofteland S., Hegstad K., Scheutz F., SimonsenG.S., Sundsfjord A., Norwegian ESBL Study Group: Molecularcharacterization of CTX-M-15-producing clinical isolates of Escherichiacoli reveals the spread of multidrug-resistant ST131 (O25:H4)and ST964 (O102:H6) strains in Norway. APMIS, 2009; 117: 526-536
Google Scholar - 84. Nguyen T.V., Le P.V., Le C.H., Weintraub A.: Antibiotic resistancein diarrheagenic Escherichia coli and Shigella strains isolated fromchildren in Hanoi, Vietnam. Antimicrob. Agents Chemother., 2005;49: 816-819
Google Scholar - 85. Nicolas-Chanoine M.H., Blanco J., Leflon-Guibout V., Demarty R.,Alonso M.P., Canica M.M., Park Y.J., Lavigne J.P., Pitout J., Johnson J.R.:Intercontinental emergence of Escherichia coli clone O25:H4-ST131producing CTX-M-15. J. Antimicrob. Chemother., 2008; 61: 273-281
Google Scholar - 86. Nishikawa Y., Zhou Z., Hase A., Ogasawara J., Kitase T., Abe N.,Nakamura H., Wada T., Ishii E., Haruki K.: Diarrheagenic Escherichiacoli isolated from stools of sporadic cases of diarrheal illness in OsakaCity, Japan between 1997 and 2000: prevalence of enteroaggregativeE. coli heat-stable enterotoxin 1 gene-possessing E. coli. Jpn. J. Infect.Dis., 2002; 55: 183-190
Google Scholar - 87. Novais Â., Viana D., Baquero F., Martínez-Botas J., Cantón R.,Coque T.M.: Contribution of IncFII and broad-host IncA/C and IncNplasmids to the local expansion and diversification of phylogroupB2 Escherichia coli ST131 clones carrying blaCTX-M-15 and qnrS1 genes.Antimicrob. Agents Chemother., 2012; 56: 2763-2766
Google Scholar - 88. Ochoa T.J., Ecker L., Barletta F., Mispireta M.L., Gil A.I., ContrerasC., Molina M., Amemiya I., Verastegui H., Hall E.R., Cleary T.G., LanataC.F.: Age-related susceptibility to infection with diarrheagenicEscherichia coli among infants from Periurban areas in Lima, Peru.Clin. Infect. Dis., 2009; 49: 1694-1702
Google Scholar - 89. Paton A.W., Paton J.C.: Direct detection and characterization ofShiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae,ehxA, and saa. J. Clin. Microbiol., 2002; 40: 271-274
Google Scholar - 90. Paton A.W., Srimanote P., Woodrow M.C., Paton J.C.: Characterizationof Saa, a novel autoagglutinating adhesin produced by locus ofenterocyte effacement-negative Shiga-toxigenic Escherichia coli strainsthat are virulent for humans. Infect. Immun., 2001; 69: 6999-7009
Google Scholar - 91. Peirano G., Pitout J.D.: Molecular epidemiology of Escherichia coliproducing CTX-M β-lactamases: the worldwide emergence of cloneST131 O25:H4. Int. J. Antimicrob. Agents, 2010; 35: 316-321
Google Scholar - 92. Pitout J.D., Laupland K.B., Church D.L., Menard M.L., JohnsonJ.R.: Virulence factors of Escherichia coli isolates that produce CTX–M-type extended-spectrum β-lactamases. Antimicrob. Agents Chemother.,2005; 49: 4667-4670
Google Scholar - 93. Prats G., Mirelis B., Llovet T., Munoz C., Miró E., Navarro F.: Antibioticresistance trends in enteropathogenic bacteria isolated in1985-1987 and 1995-1998 in Barcelona. Antimicrob. Agents Chemother.,2000; 44: 1140-1145
Google Scholar - 94. Qadri F., Das S.K., Faruque A.S., Fuchs G.J., Albert M.J., Sack R.B.,Svennerholm A.M.: Prevalence of toxin types and colonization factorsin enterotoxigenic Escherichia coli isolated during a 2-year period fromdiarrheal patients in Bangladesh. J. Clin. Microbiol., 2000; 38: 27-31
Google Scholar - 95. Rodas C., Mamani R., Blanco J., Blanco J.E., Wiklund G., SvennerholmA.M., Sjöling Å., Iniguez V.: Enterotoxins, colonization factors,serotypes and antimicrobial resistance of enterotoxigenic Escherichiacoli (ETEC) strains isolated from hospitalized children with diarrheain Bolivia. Braz. J. Infect. Dis., 2011; 15: 132-137
Google Scholar - 96. Rogers B.A., Sidjabat H.E., Paterson D.L.: Escherichia coli O25b–ST131: a pandemic, multiresistant, community associated strain. J.Antimicrob. Chemother., 2011; 66: 1-14
Google Scholar - 97. Russo T.A., Johnson J.R.: Proposal for a new inclusive designationfor extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J.Infect. Dis., 2000; 181: 1753-1754
Google Scholar - 98. Scaletsky I.C., Souza T.B., Aranda K.R., Okeke I.N.: Genetic elementsassociated with antimicrobial resistance in enteropathogenicEscherichia coli (EPEC) from Brazil. BMC Microbiol., 2010; 10: 25-33
Google Scholar - 99. Sepehri S., Kotlowski R., Bernstein C.N., Krause D.O.: Phylogeneticanalysis of inflammatory bowel disease associated Escherichia coli and thefimH virulence determinant. Inflamm. Bowel Dis., 2009; 15: 1737-1745
Google Scholar - 100. Servin A.L.: Pathogenesis of Afa/Dr diffusely adhering Escherichiacoli. Clin. Microbiol. Rev., 2005; 18: 264-292
Google Scholar - 101. Silva-Sánchez J., Cruz-Trujillo E., Barrios H., Reyna-Flores F.,Sánchez-Pérez A., Bacterial Resistance Consortium, Garza-Ramos U.:Characterization of plasmid-mediated quinolone resistance (PMQR)genes in extended-spectrum β-lactamase-producing Enterobacteriaceaepediatric clinical isolates in Mexico. PLoS One, 2013; 8: e77968
Google Scholar - 102. Skippington E., Ragan M.A.: Phylogeny rather than ecology orlifestyle biases the construction of Escherichia coli–Shigella geneticexchange communities. Open Biol., 2012; 2: 102112
Google Scholar - 103. Spano L.C., Sadovsky A.D., Segui P.N., Saick K.W., Kitagawa S.M.,Pereira F.E., Fagundes-Neto U., Scaletsky I.C.: Age-specific prevalenceof diffusely adherent Escherichia coli in Brazilian children with acutediarrhea. J. Med. Microbiol., 2008; 57: 359-363
Google Scholar - 104. Steinsland H., Lacher D.W., Sommerfelt H., Whittam T.S.. Ancestrallineages of human enterotoxigenic Escherichia coli. J. Clin.Microbiol., 2010; 48: 2916-2924
Google Scholar - 105. Subashchandrabose S., Smith S.N., Spurbeck R.R., Kole M.M.,Mobley H.L.: Genome-wide detection of fitness genes in uropathogenicEscherichia coli during systemic infection. PLoS Pathog., 2013;9: e1003788
Google Scholar - 106. Tenaillon O., Skurnik D., Picard B., Denamur E.: The populationgenetics of commensal Escherichia coli. Nat. Rev. Microbiol.,2010; 8: 207-217
Google Scholar - 107. Touchon M., Hoede C., Tenaillon O., Barbe V., Baeriswyl S.,Bidet P., Bingen E., Bonacorsi S., Bouchier C., Bouvet O., Calteau A.,Chiapello H., Clermont O., Cruveiller S., Danchin A. i wsp.: Organisedgenome dynamics in the Escherichia coli species results in highlydiverse adaptive paths. PLoS Genet., 2009; 5: e1000344
Google Scholar - 108. Trabulsi L.R., Keller R., Tardelli Gomes T.A.: Typical and atypicalenteropathogenic Escherichia coli. Emerg. Infect. Dis., 2002; 8: 508-513
Google Scholar - 109. Usein C.R., Tatu-Chitoiu D., Ciontea S., Condei M., Damian M.:Escherichia coli pathotypes associated with diarrhea in Romanianchildren younger than 5 years of age. Jpn. J. Infect. Dis., 2009; 62:289-293
Google Scholar - 110. Van den Beld M.J., Reubsaet F.A.: Differentiation between Shigella,enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichiacoli. Eur. J. Clin. Microbiol. Infect. Dis., 2012; 31: 899-904
Google Scholar - 111. Vicente A.C., Teixeira L.F., Iniguez-Rojas L., Luna M.G., Silva L.,Andrade J.R., Guth B.E.: Outbreaks of cholera-like diarrhoea causedby enterotoxigenic Escherichia coli in the Brazilian Amazon Rainforest.Trans. R. Soc. Trop. Med. Hyg., 2005; 99: 669-674
Google Scholar - 112. Vila J., Vargas M., Ruiz J., Corachan M., Jimenez De Anta M.T.,Gascon J.: Quinolone resistance in enterotoxigenic Escherichia colicausing diarrhea in travelers to India in comparison with other geographicalareas. Antimicrob. Agents Chemother., 2000; 44: 1731-1733
Google Scholar - 113. Vilchez S., Reyes D., Paniagua M., Bucardo F., Möllby R., WeintraubA.: Prevalence of diarrhoeagenic Escherichia coli in childrenfrom León, Nicaragua. J. Med. Microbiol., 2009; 58: 630-637
Google Scholar - 114. Walk S.T., Alm E.W., Gordon D.M., Ram J.L., Toranzos G.A., TiedjeJ.M., Whittam T.S.: Cryptic lineages of the genus Escherichia. Appl.Environ. Microbiol., 2009; 75: 6534-6544
Google Scholar - 115. Whittam T.S., Ochman H., Selander R.K.: Multilocus geneticstructure in natural populations of Escherichia coli. Proc. Natl. Acad.Sci. USA, 1983; 80: 1751-1755
Google Scholar - 116. Wolf M.K.: Occurrence, distribution, and associations of O andH serogroups, colonization factor antigens, and toxins of enterotoxigenicEscherichia coli. Clin. Microbiol. Rev., 1997; 10: 569-584
Google Scholar - 117. Wong A.R., Pearson J.S., Bright M.D., Munera D., Robinson K.S.,Lee S.F., Frankel G., Hartland E.L.: Enteropathogenic and enterohaemorrhagicEscherichia coli: even more subversive elements. Mol.Microbiol., 2011; 80: 1420-1438
Google Scholar - 118. Ziebell K., Konczy P., Yong I., Frost S., Mascarenhas M., KropinskiA.M., Whittam T.S., Read S.C., Karmali M.A.: Applicability of phylogeneticmethods for characterizing the public health significanceof verocytotoxin-producing Escherichia coli strains. Appl. Environ.Microbiol., 2008; 74: 1671-1675
Google Scholar