Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain

Research in Microbiology

Volumn 156, Issue 7, 2005, Pages 793-806

  Mora, Azucena ^a   Blanco, Jesús E ^a   Blanco, Miguel ^a   Alonso, M Pilar ^b   Dhabi, Ghizlane ^a   Echeita, Aurora ^c   González, Enrique A ^a   Bernárdez, M Isabel ^a   Blanco, Jorge ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b Unidade de Microbioloxia   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Antimicrobial resistance; Escherichia coli; Shiga toxin; Spain; Verotoxin

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; COTRIMOXAZOLE; KANAMYCIN; NEOMYCIN; PIPERACILLIN; SHIGA TOXIN; STREPTOMYCIN; SULFAFURAZOLE; TETRACYCLINE DERIVATIVE; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM ISOLATE; CATTLE; ESCHERICHIA COLI; FOOD CONTAMINATION; GENE FUNCTION; HEMOLYTIC UREMIC SYNDROME; HUMAN; MEAT; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; SHEEP; SPAIN;

ADHESINS, BACTERIAL; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGE TYPING; CATTLE; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; FOOD MICROBIOLOGY; HUMANS; MICROBIAL SENSITIVITY TESTS; SEROTYPING; SHEEP; SHIGA TOXINS; SHIGA-LIKE TOXIN I; SPAIN; VIRULENCE FACTORS;

ANIMALIA; BOS TAURUS; BOVINAE; ESCHERICHIA COLI; ESCHERICHIA COLI O157-H7; OVIS; OVIS ARIES;

EID: 24144436935     PISSN: 09232508     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resmic.2005.03.006     Document Type: Article

References (66)

1. K.A. Bettelheim, M.A. Hornitzky, S.P. Djordjevic, and A. Kuzevski Antibiotic resistance among verocytotoxigenic Escherichia coli (STEC) and non-STEC isolated from domestic animals and humans J. Med. Microbiol. 52 2003 155 162
2. L. Beutin, S. Zimmermann, and K. Gleier Human infections with Shiga toxin-producing Escherichia coli other than serogroup O157 in Germany Emerg. Infect. Dis. 4 1998 635 639
3. L. Beutin, S. Kaulfuss, T. Cheasty, B. Brandenburg, S. Zimmermann, K. Gleier, G.A. Willshaw, and H.R. Smith Characteristics and association with disease of two major subclones of Shiga toxin (verocytotoxin)-producing strains of Escherichia coli (STEC) O157 that are present among isolates from patients in Germany Diag. Microbiol. Infect. Dis. 44 2002 337 346
4. L. Beutin, G. Krause, S. Zimmermann, S. Kaulfuss, and K. Gleier Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period J. Clin. Microbiol. 42 2004 1099 1108
5. J. Blanco, M. Blanco, J.E. Blanco, M.P. Alonso, J.I. Garabal, and E.A. González Escherichia coli Enterotoxigénicos, Necrotoxigé nicos y Verotoxigénicos de Origen Humano y Bovino: Patogénesis, Epidemiología y Diagnóstico Microbiológico 1993 Servicio de Publicaciones de la Diputación Provincial de Lugo Spain pp. 212-222
6. J. Blanco, M. Blanco, J.E. Blanco, A. Mora, M.P. Alonso, E.A. González, and M.I. Bernárdez Epidemiology of verocytotoxigenic Escherichia coli (VTEC) in ruminants G. Duffy P. Garvey D. McDowell Verocytotoxigenic Escherichia coli 2001 Food and Nutrition Press Inc. Trumbull, USA 113 148
7. J. Blanco, M. Blanco, J.E. Blanco, A. Mora, E.A. González, M.I. Bernárdez, M.P. Alonso, A. Coira, A. Rodríguez, J. Rey, J.M. Alonso, and M.A. Usera Verotoxin-producing Escherichia coli in Spain: Prevalence, serotypes, and virulence genes of O157:H7 and non-O157 STEC in ruminants, raw beef products, and humans Exp. Biol. Med. 228 2003 345 351
8. J.E. Blanco, M. Blanco, A. Mora, and J. Blanco Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain J. Clin. Microbiol. 35 1997 2184 2185
9. J.E. Blanco, M. Blanco, M.P. Alonso, A. Mora, G. Dahbi, M.A. Coira, and J. Blanco Serotypes, virulence genes and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: Prevalence in Lugo (Spain) from 1992 through 1999 J. Clin. Microbiol. 42 2004 311 319
10. M. Blanco, J. Blanco, J.E. Blanco, E.A. González, J.I. Garabal, A. Cantalapiedra, and A. Goicoa Resistencia a antibióticos en Escherichia coli de origen bovino Med. Vet. 10 1993 154 162
11. M. Blanco, J. Blanco, J.E. Blanco, and J. Ramos Enterotoxigenic, verotoxigenic, and necrotoxigenic Escherichia coli isolated from cattle in Spain Am. J. Vet. Res. 54 1993 1446 1451
12. M. Blanco, J.E. Blanco, J. Blanco, E.A. González, A. Mora, C. Prado, L. Fernández, M. Rio, J. Ramos, and M.P. Alonso Prevalence and characteristics of Escherichia coli serotype O157:H7 and other verotoxin-producing E. coli in healthy cattle Epidemiol. Infect. 117 1996 251 257
13. M. Blanco, J.E. Blanco, J. Blanco, A. Mora, C. Prado, M.P. Alonso, M. Mouriño, C. Madrid, C. Balsalobre, and A. Juárez Distribution and characterization of fecal verotoxin-producing Escherichia coli (VTEC) isolated from healthy cattle Vet. Microbiol. 54 1997 309 319
14. M. Blanco, J.E. Blanco, A. Mora, J. Rey, J.M. Alonso, M. Hermoso, J. Hermoso, M.P. Alonso, G. Dhabi, E.A. González, M.I. Bernárdez, and J. Blanco Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain J. Clin. Microbiol. 41 2003 1351 1365
15. M. Blanco, J.E. Blanco, A. Mora, G. Dahbi, M.P. Alonso, E.A. González, M.I. Bernárdez, and J. Blanco Serotypes, virulence genes and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from cattle in Spain: Identification of a new intimin variant gene (eae-ε) J. Clin. Microbiol. 42 2004 645 651
16. C.A. Bopp, K.D. Greene, F.P. Downes, E.G. Sowers, J.G. Wells, and I.K. Wachsmuth Unusual verotoxin-producing Escherichia coli associated with hemorrhagic colitis J. Clin. Microbiol. 25 1987 1486 1489
17. D. Cid, S. Piriz, J.A. Ruiz Santa-Quiteria, J. Valle, S. Vadillo, and R. de la Fuente In vitro susceptibility of Escherichia coli strains isolated from diarrheic lambs and goat kids to 14 antimicrobial agents J. Vet. Pharmacol. Therap. 19 1996 397 401
18. P.M. Desmarchelier, S.S. Bilge, N. Fegan, L. Mills, J.C. Vary Jr., and P.I. Tarr A PCR specific for Escherichia coli O157 based on the rfb locus encoding O157 lipopolysaccharide J. Clin. Microbiol. 36 1998 1801 1804
19. M. Eklund, F. Scheutz, and A. Siitonen Clinical isolates of non-O157 Shiga toxin-producing Escherichia coli: Serotypes, virulence characteristics, and molecular profiles of strains of the same serotype J. Clin. Microbiol. 39 2001 2829 2834
20. C. Farina, A. Goglio, G. Conedera, F. Minelli, and A. Caprioli Antimicrobial susceptibility of Escherichia coli O157 and other enterohemorrhagic Escherichia coli isolated in Italy Eur. J. Clin. Microbiol. Infect. Dis. 15 1996 351 353
21. H. Fukushima, T. Hashizume, Y. Morita, J. Tanaka, K. Azuma, Y. Mizumoto, M. Kaneno, M. Matsuura, K. Konma, and T. Kitani Clinical experiences in Sakai City Hospital during the massive outbreak of enterohemorrhagic Escherichia coli O157 infections in Sakai City, 1996 Pediatr. Int. 41 1999 213 217
22. J.C. Galland, D.R. Hyatt, S.S. Crupper, and D.W. Acheson Prevalence, antibiotic susceptibility, and diversity of Escherichia coli O157:H7 isolates from a longitudinal study of beef cattle feedlots Appl. Environ. Microbiol. 67 2001 1619 1627
23. V.P. Gannon, S. D'Souza, T. Graham, R.K. King, K. Rahn, and S. Read Use of the flagellar H7 gene as a target in multiplex PCR assays and improved specificity in identification of enterohemorrhagic Escherichia coli strains J. Clin. Microbiol. 35 1997 656 662
24. E.A. González, and J. Blanco Serotypes and antibiotic resistance of verotoxigenic (STEC) and necrotizing (NTEC) Escherichia coli strains isolated from calves with diarrhea FEMS Microbiol. Lett. 60 1989 31 36
25. P.M. Griffin, and R.V. Tauxe The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic-uremic syndrome Epidemiol. Rev. 13 1991 60 98
26. P.M. Griffin Escherichia coli O157:H7 and other enterohemorrhagic Escherichia coli M.J. Blaser P.D. Smith J.I. Ravdin H.B. Greenberg R.L. Grerrant Infections of Gastrointestinal Tract 1995 Raven Press New York 739 761
27. P.A.M. Guinée, W.H. Jansen, T. Wadström, and R. Sellwood Escherichia coli associated with neonatal diarrhea in piglets and calves Curr. Top. Vet. Anim. Sci. 13 1981 126 162
28. N. Hiruta, T. Murase, and N. Okamura An outbreak of diarrhea due to multiple antimicrobial-resistant Shiga toxin-producing Escherichia coli O26:H11 in a nursery Epidemiol. Infect. 127 2001 221 227
29. T. Horii, S. Barua, T. Kimura, S. Kasugai, K. Sato, K. Shibayama, S. Ichiyama, and M. Ohta Heterogeneity of phenotypic and genotypic traits including organic-acid resistance in Escherichia coli O157 isolates Microbiol. Immunol. 42 1998 871 874
30. K. Ikeda, O. Ida, K. Kimoto, T. Takatorige, N. Nakanishi, and K. Tatara Effect of early fosfomycin treatment on prevention of hemolytic-uremic syndrome accompanying Escherichia coli O157:H7 infection Clin. Nephrol. 52 1999 357 362
31. K. Izumikawa, Y. Hirakata, T. Yamaguchi, R. Yoshida, M. Nakano, J. Matsuda, C. Mochida, S. Maesaki, K. Tomono, Y. Yamada, T. Tashiro, S. Kohno, and S. Kamihira Analysis of genetic relationships and antimicrobial susceptibility of verotoxin-producing Escherichia coli strains isolated in Nagasaki prefecture, Japan in 1996 Microbiol. Immunol. 42 1998 677 681
32. J.H. Jorgensen, J.D. Turnidge, and J.A. Washington Antibacterial susceptibility tests: Dilution and disk diffusion methods P.R. Murray E.J. Baron M.A. Pfaller F.C. Tenover R.H. Yolken Manual of Clinical Microbiology seventh ed. 1999 American Society for Microbiology Washington 1526 1543
33. J.B. Kaper, S. Elliott, V. Sperandio, N.T. Perna, G.F. Mayhew, and F.R. Blattner Attaching and effacing intestinal histopathology and the locus of enterocyte effacement J.B. Kaper A.D. O'Brien Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains 1998 American Society for Microbiology Washington 163 182
34. M.A. Karmali Infection by verocytotoxin-producing Escherichia coli Clin. Microbiol. Rev. 2 1989 5 38
35. A.R. Khachatryan, D.D. Hancock, T.E. Besser, and D.R. Call Role of calf-adapted Escherichia coli in maintenance of antimicrobial drug resistance in dairy calves Appl. Environ. Microbiol. 70 2004 752 757
36. R. Khakria, D. Duck, and H. Lior Extended phage-typing scheme for Escherichia coli O157:H7 Epidemiol. Infect. 105 1990 511 520
37. A. Khan, S.C. Das, T. Ramamurthy, A. Sikdar, J. Khanam, S. Yamasaki, Y. Takeda, and G. Balakrish Nair Antibiotic ressistance, virulence gene, and molecular profiles of Shiga toxin-producing Escherichia coli isolates from diverse sources in Calcutta, India J. Clin. Microbiol. 40 2002 2009 2015
38. H.H. Kim, M. Samadpour, L. Grimm, C.R. Clausen, T.E. Besser, M. Baylor, J.M. Kobayashi, M.A. Neill, F.D. Schoenknecht, and P.I. Tarr Characteristics of antibiotic-resistant Escherichia coli O157:H7 in Washington state, 1984-1991 J. Infect. Dis. 70 1994 1606 1609
39. H. Kobayashi, J. Shimada, M. Nakazawa, T. Morozumi, T. Pohjanvirta, S. Pelkonen, and K. Yamamoto Prevalence and characteristics of Shiga toxin-producing Escherichia coli from healthy cattle in Japan Appl. Environ. Microbiol. 67 2001 484 489
40. H. Maidhof, B. Guerra, S. Abbas, H.M. Elsheikha, T.S. Whittam, and L. Beutin A multiresistant clone of Shiga toxin-producing Escherichia coli O118:H16 is spread in cattle and humans over different European countries Appl. Environ. Microbiol. 68 2002 5834 5842
41. J. Meng, S. Zhao, M. Doyle, and S.W. Joseph Antibiotic resistance of Escherichia coli O157:H7 and O157:NM isolated from animals, food, and humans J. Food Prot. 1 1998 1511 1514
42. A. Mora, M. Blanco, J.E. Blanco, M.P. Alonso, G. Dhabi, F. Thompson-Carter, M.A. Usera, R. Bartolomé, G. Prats, and J. Blanco Phage types and genotypes of human and animal Shiga toxin-producing Escherichia coli O157:H7 in Spain. Identification of two predominating phage types (PT2 and PT8) J. Clin. Microbiol. 42 2004 4007 4015
43. National Committee for Clinical Laboratory Standards, Performance Standards for Antimicrobial Disk Susceptibility Tests, seventh ed., Approved Standard M2-A7. Committee for Clinical Laboratory Standards, Wayne, PA, 2000
44. C.H. Pai, R. Gordon, H.V. Sims, and L.E. Bryan Sporadic cases of hemorrhagic colitis associated with Escherichia coli O157:H7 Ann. Intern. Med. 101 1984 738 742
45. J.C. Paton, and A.W. Paton Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections Clin. Microbiol. Rev. 11 1998 450 479
46. A.F. Pestana de Castro, B. Guerra, L. Leomil, L. Aidar-Ugrinovitch, and L. Beutin Multidrug-resitant Shiga toxin-producing Escherichia coli O118:H16 in Latin America Emerg. Infect. Dis. 9 2003 1027 1028
47. S. Ratnam, S.B. March, R. Ahmed, G.S. Bezanson, and S. Kasatiya Characterization of Escherichia coli serotype O157:H7 J. Clin. Microbiol. 26 1988 2006 2012
48. R.S. Remis, K.L. MacDonald, L.W. Riley, N.D. Puhr, J.G. Welss, B.R. Davis, P.A. Bleice, and M.L. Cohen Sporadic cases of hemorrhagic colitis associated with Escherichia coli O157:H7 Ann. Intern. Med. 101 1984 624 626
49. Y. Sáenz, M. Zarazaga, L. Briñas, M. Lantero, F. Ruiz-Larrea, and C. Torres Antibiotic resistance in Escherichia coli isolates obtained from animals, foods and humans in Spain Int. J. Antimicrob. Agents 18 2001 353 358
50. H. Schmidt, J. von Maldeghem, M. Frosch, and H. Karch Antibiotic susceptibilities of verocytotoxin-producing Escherichia coli O157 and non-O157 strains isolated from patients and healthy subjects in Germany during 1996 J. Antimicrob. Chemother. 42 1998 548 550
51. C.M. Schroeder, J. Meng, S. Zhao, C. DebRoy, J. Torcolini, C. Zhao, P.F. McDermott, D.D. Wagner, R.D. Walker, and D.G. White Antimicrobial resistance of Escherichia coli O26, O103, O111, O128, and O145 from animals and humans Emerg. Infect. Dis. 8 2002 1409 1414
52. C.M. Schroeder, C. Zhao, C. DebRoy, J. Torcolini, S. Zhao, D.G. White, D.D. Wagner, P.F. McDermott, R.D. Walker, and J. Meng Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine, and food Appl. Environ. Microbiol. 68 2002 576 581
53. R. Stephan, and S. Schumacher Resistance patterns of non-O157 Shiga toxin-producing Escherichia coli (STEC) strains isolated from animals, food and asymptomatic human carriers in Switzerland Lett. Appl. Microbiol. 32 2001 114 117
54. P.I. Tarr, M.A. Neill, D.L. Christie, and D.E. Anderson Escherichia coli O157:H7 hemorrhagic colitis (letter) New Engl. J. Med. 318 1988 1697
55. T. Teshager, I.A. Herrero, M.C. Porrero, J. Garde, M.A. Moreno, and L. Domínguez Surveillance of antimicrobial resistance in Escherichia coli strains isolated from pigs at Spanish slaughterhouses Int. J. Antimicrob. Agents 15 2000 137 142
56. A. Thomas, T. Cheasty, J.A. Frost, H. Chart, H.R. Smith, and B. Rowe Verocytotoxin-producing Escherichia coli, particularly serogroup O157 associated with human infections in England and Wales: 1992-1994 Epidemiol. Infect. 117 1996 1 10
57. J. Walterspiel, S. Ashkenazi, A. Morrow, and T.G. Cleary Effect of subinhibitory concentrations of antibiotics on extracellular Shiga-like toxin 1 Infection. 20 1992 25 29
58. D.G. White, S. Zhao, P.F. McDermott, S. Ayers, S. Gaines, S. Friedman, D.D. Wagner, J. Meng, D. Needle, M. Davis, and C. DebRoy Characterization of antimicrobial resistance among Escherichia coli O111 isolates of animal and human origin Microb. Drug Resist. 8 2002 139 146
59. G.A. Willshaw, T. Cheasty, H.R. Smith, S.J. O'Brien, and G.K. Adak Verocytotoxin-producing Escherichia coli (VTEC) O157 and other VTEC from human infections in England and Wales: 1995-1998 J. Med. Microbiol. 50 2001 135 142
60. W. Witte Medical consequences of antibiotic use in agriculture Science 279 1998 996 997
61. C.S. Wong, S. Jelacic, R.L. Habeeb, S.L. Watkins, and P.I. Tarr The risk of hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections New Engl. J. Med. 342 2000 1930 1936
62. T. Yamamoto, and N. Wakisaka Status of emerging drug resistance in Shiga toxin-producing Escherichia coli in Japan during 1996: A minireview Nippon Rinsho. 56 1998 2718 2729
63. X. Zhang, A.D. McDaniel, L.E. Wolf, G.T. Keusch, M.K. Waldor, and D.W. Acheson Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice J. Infect. Dis. 181 2000 664 670
64. S. Zhao, D.G. White, B. Ge, S. Ayers, S. Friedman, L. English, D. Wagner, S. Gaines, and J. Meng Identification and characterization of integron-mediated antibiotic resistance among Shiga toxin-producing Escherichia coli isolates Appl. Environ. Microbiol. 67 2001 1558 1564
65. M. Braoudaki, A.C. Hilton, 5th Int. Symp. Shiga toxin (verocytotoxin)-producing Escherichia coli infections, Edinburgh, UK, abstract P99, p. 128, 2003
66. B. Jiggle, T. Cheasty, G. Willshaw, 5th Int. Symp. Shiga Toxin (Verocytotoxin)-Producing Escherichia coli Infections, Edinburgh, UK, abstract P241, p. 201, 2003