Prevalence of diarrheagenic Escherichia coli virulence genes in the feces of slaughtered cattle, chickens, and pigs in Burkina Faso

MicrobiologyOpen

Volumn 1, Issue 3, 2012, Pages 276-284

  Kagambèga, Assèta ^a,b   Martikainen, Outi ^a   Siitonen, Anja ^a   Traoré, Alfred S ^b   Barro, Nicolas ^b   Haukka, Kaisa ^a,c  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITÉ DE OUAGADOUGOU   (Burkina Faso)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Cattle; Chickens; Diarrheagenic Escherichia coli; Multiplex PCR; Pigs; Virulence genes

Indexed keywords

AGGR GENE; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; BFPB GENE; BURKINA FASO; CARCASS; CATTLE; CHICKEN; CONTROLLED STUDY; EAEA GENE; ELT GENE; ENT GENE; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENTEROINVASIVE ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCV GENE; ESTLA GENE; ESTLB GENE; FECES ANALYSIS; GENE IDENTIFICATION; HLY GENE; INVE GENE; IPAH GENE; NONHUMAN; PIC GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; STX1 GENE; STX2 GENE; SWINE; VIRULENCE GENE;

ANIMALIA; BACTERIA (MICROORGANISMS); BOS; ESCHERICHIA COLI; GALLUS GALLUS; SUIDAE;

EID: 84881549264     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.30     Document Type: Article

References (64)

1. Afset, J. E., E. Anderssen, G. Bruant, J. Harel, L. Wieler, and K. Bergh 2008. Phylogenetic backgrounds and virulence profiles of atypical enteropathogenic Escherichia coli strains from a case-control study using multilocus sequence typing and DNA microarray analysis. J. Clin. Microbiol. 46:2280-2290.
2. Akanbi, B. O., I. P. Mbah, and P. C. Kerry 2011. Prevalence of Escherichia coli O157:H7 on hides and faeces of ruminants at slaughter in two major abattoirs in Nigeria. Lett. Appl. Microbiol. 53:336-240.
3. Aktan, I., K. A. Sprigings, R. M. La Ragione, L. M. Faulkner, G. A. Paiba, and M. J. Woodward 2004. Characterization of attaching-effacing Escherichia coli isolated from animals at slaughter in England and Wales. Vet. Microbiol. 102:43-53.
4. Alonso, M. Z., N. L. Padola, A. E. Parma, and P. M. A. Lucchesi 2011. Enteropathogenic Escherichia coli contamination at different stages of the chicken slaughtering process. Poult. Sci. 90:2638-2641.
5. Antikainen, J., E. Tarkka, K. Haukka, A. Siitonen, M. Vaara, and J. Kirveskari 2009. New 16-plex PCR method for rapid detection of diarrheagenic Escherichia coli directly from stool samples. Eur. J. Clin. Microbiol. Infect. Dis. 28:899-908.
6. Baldini, M. M., J. B. Kaper, M. M. Levine, D. C. Candy, and H. W. Moon 1983. Plasmid-mediated adhesion in enteropathogenic Escherichia coli. J. Pediatr. Gastroenterol. Nutr. 2:534-538.
7. Blanco, C., P. Ritzenthaler, and M. Mata-Gilsinger 1982. Cloning and endonuclease restriction analysis of uidA and uidR genes in Escherichia coli K-12: determination of transcription direction for the uidA gene. J. Bacteriol. 149:587-594.
8. Blanco, J., M. Blanco, J. E. Blanco, A. Mora, E. Gonzales, M. I. Bernardez, et al. 2003. Verotoxin-producing Escherichia coli in Spain: prevalence, serotypes and virulence genes of O157:H7 and non-O157 VTEC in ruminants, raw beef products and humans. Exp. Biol. Med. 228:345-351.
9. Blanco, M., N. L. Padola, A. Krüger, M. E. Sanz, J. E. Blanco, E. A. González, et al. 2004. Virulence genes and intimin types of Shiga-toxin-producing Escherichia coli isolated from cattle and beef products in Argentina. Int. Microbiol. 7:269-276.
10. Bonardi, S., F. Brindani, G. Pizzin, L. Lucidi, M. D'Incau, E. Liebana, et al. 2003. Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin-producing Escherichia coli O157 in pigs at slaughter in Italy. Int. J. Food Microbiol. 15:101-110.
11. Bonkoungou, I. J., T. Lienemann, O. Martikainen, R. Dembelé, I. Sanou, A. S. Traoré, et al. In press. Diarrhoeagenic Escherichia coli detected by 16-plex PCR in children with and without diarrhoea in Burkina Faso. Clin. Microbiol. Infect. doi: 10.1111/j.1469-0691.2011.03675.x
12. Caprioli, A., S. Morabito, H. Brugère, and E. Oswald 2005. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet. Res. 36:289-311.
13. Cerna, J. F., J. P. Nataro, and T. Estrada-Garcia 2003. Multiplex PCR for detection of three plasmid-borne genes of enteroaggregative Escherichia coli strains. J. Clin. Microbiol. 41:2138-2140.
14. Clermont, O., M. Olier, C. Hoede, L. Diancourt, S. Brisse, M. Keroudean, et al. 2011. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect. Genet. Evol. 11:654-662.
15. Cookson, A. L., S. C. S. Taylor, J. Bennett, F. Thomson-Carter, and G. T. Attwood 2006. Serotypes and analysis of distribution of Shiga toxin-producing Escherichia coli from cattle and sheep in the lower North Island, New Zealand. N Z Vet. J. 54:78-84.
16. Cookson, A. L., M. Cao, J. Bennett, C. Nicol, F. Thomson-Carter, and G. T. Attwood 2010. Relationship between virulence gene profiles of atypical enteropathogenic Escherichia coli and Shiga toxin-producing E. coli isolates from cattle and sheep in New Zealand. Appl. Environ. Microbiol. 76:3744-3747.
17. Das, S. C., A. Khan, P. Panja, S. Datta, A. Sikdar, S. Yamasaki, et al. 2005. Dairy farm investigation on Shiga toxin-producing Escherichia coli (STEC) in Kolkata, India with emphasis on molecular characterization. Epidemiol. Infect. 133:617-626.
18. Dipineto, L., A. Santaniello, M. Fontanella, K. Lagos, A. Fioretti, and L. F. Menna 2006. Presence of Shiga toxin-producing Escherichia coli O157:H7 in living layer hens. Lett. Appl. Microbiol. 43:293-295.
19. Fagan, P. K., M. A. Hornitzky, K. A. Bettelheim, and S. P. Djordjevic 1999. Detection of Shiga-like toxin (stx1 and stx2), intimin (eaeA), and enterohemorrhagic Escherichia coli (EHEC) hemolysin (EHEC hlyA) genes in animal feces by multiplex PCR. Appl. Environ. Microbiol. 65:868-872.
20. FAO, Food and Agriculture Organization. 2005. Code of hygienic practice for meat. CAC/RCP 58-200. Codex Alimentarius, FAO, Rome.
21. Gyles, C. L. 2007. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 85:45-62.
22. Hale, T. L. 1991. Genetic basis of virulence in Shigella species. Microbiol. Rev. 55:206-224.
23. Harrington, S. M., E. G. Dudley, and J. P. Nataro 2006. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol. Lett. 254:12-18.
24. Henderson, I. R., J. Czeczulin, C. Eslava, F. Noriega, and J. P. Nataro 1999. Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect. Immun. 67:5587-5596.
25. Heuvelink, A. E., J. T. Zwartkruis-Nahuis, F. L. van den Biggelaar, W. J. van Leeuwen, and E. de Boer 1999. Isolation and characterization of verocytotoxin-producing Escherichia coli O157 from slaughter pigs and poultry. Int. J. Food Microbiol. 52:67-75.
26. Hsu, B. M., S. F. Wu, S. W. Huang, Y. J. Tseng, D. D. Ji, J. S. Chen, et al. 2010. Differentiation and identification of Shigella spp. and enteroinvasive Escherichia coli in environmental waters by a molecular method and biochemical test. Water Res. 44:949-955.
27. Huang, D. B., P. C. Okhuysen, Z. Jiang, and H. L. Dupont 2004. Enteroaggregative Escherichia coli: an emerging enteric pathogen. Am. J. Gastroenterol. 99:383-389.
28. Hussein, H. S. 2007. Prevalence and pathogenicity of shiga toxin-producing Escherichia coli in beef cattle and their products. J. Anim. Sci. 85:63-72.
29. Islam, M. A., A. S. Mondol, E. de Boer, R. R. Beumer, M. H. Zwietering, K. A. Talukder, et al. 2008. Prevalence and genetic characterization of Shiga toxin-producing Escherichia coli isolates from slaughtered animals in Bangladesh. Appl. Environ. Microbiol. 74:5414-5421.
30. Johnsen, G., Y. Wasteson, E. Heir, O. I. Berget, and H. Herikstad 2001. Escherichia coli O157:H7 in faeces from cattle, sheep and pigs in the southwest part of Norway during 1998 and 1999. Int. J. Food Microbiol. 65:193-200.
31. Kagambèga, A., K. Haukka, A. Siitonen, A. S. Traoré, and N. Barro 2011. Prevalence of Salmonella enterica and the hygienic indicator Escherichia coli in raw meat at markets in Ouagadougou, Burkina Faso. J. Food Prot. 74:1547-1551.
32. Kagambèga, A., O. Martikainen, T. Lienemann, A. Siitonen, A. S. Traoré, N. Barro, et al. 2012. Diarrheagenic Escherichia coli detected by 16-plex PCR in raw meat and beef intestines sold at local markets in Ouagadougou, Burkina Faso. Int. J. Food Microbiol. 153:154-158.
33. Kaper, J. B., J. P. Nataro, and H. L. Mobley 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-1240.
34. Kariuki, S., C. Gilks, J. Kimari, A. Obanda, J. Muyodi, P. Waiyaki, et al. 1999. Genotype analysis of Escherichia coli strains isolated from children and chickens living in close contact. Appl. Environ. Microbiol. 65:472-476.
35. Keskimäki, M., L. Mattila, H. Peltola, and A. Siitonen 2000. Prevalence of diarrheagenic Escherichia coli in Finns with or without diarrhea during a round-the-world trip. J. Clin. Microbiol. 38:4425-4429.
36. Kobayashi, H., J. Shimada, M. Nakazawa, T. Morozumi, T. Pohjanvirta, S. Pelkonen, et al. 2001. Prevalence and characteristics of Shiga toxin-producing Escherichia coli from healthy cattle in Japan. Appl. Environ. Microbiol. 67:484-489.
37. Kobayashi, H., T. Pohjanvirta, and S. Pelkonen 2002. Prevalence and characteristics of intimin and Shiga toxin-producing Escherichia coli from gulls, pigeons and broilers in Finland. J. Vet. Med. Sci. 64:1071-1073.
38. Krause, G., S. Zimmermann, and L. Beutin 2005. Investigation of domestic animals and pets as a reservoir for intimin- (eae) gene positive Escherichia coli types. Vet. Microbiol. 106:87-95.
39. Lan, R., M. A. Alles, K. Donohoe, M. B. Martinez, and P. R. Reeves 2004. Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infect. Immun. 72:5080-5088.
40. Lee, G. Y., H. I. Jang, I. G. Hwang, and M. S. Rhee 2009. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int. J. Food Microbiol. 134:196-200.
41. Madoroba, E., E. Van Driessche, H. De Greve, J. Mast, I. Ncube, J. Read, et al. 2009. Prevalence of enterotoxigenic Escherichia coli virulence genes from scouring piglets in Zimbabwe. Trop. Anim. Health Prod. 41:1539-1547.
42. Majalija, S., H. Segal, F. Ejobi, and B. G. Elisha 2008. Shiga toxin gene-containing Escherichia coli from cattle and diarrheic children in the pastoral systems of southwestern Uganda. J. Clin. Microbiol. 46:352-354.
43. Meng, J., M. P. Doyle, T. Zhao, and S. Zhao 2007. Enterohemorrhagic Escherichia coli. Pp. 249-269 in M. P. Doyle and L. R. Beuchat, eds. Food microbiology: fundamentals and frontiers. 3rd ed. American Society for Microbiology, Washington, DC.
44. Mersha, G., D. Asrat, B. M. Zewde, and M. Kyule 2010. Occurrence of Escherichia coli O157:H7 in faeces, skin and carcasses from sheep and goats in Ethiopia. Lett. Appl. Microbiol. 50:71-76.
45. Müller, D., L. Greune, G. Heusipp, H. Karch, A. Fruth, H. Tschäpe, et al. 2007. Identification of unconventional intestinal pathogenic Escherichia coli isolates expressing intermediate virulence factor profiles by using a novel single-step multiplex PCR. Appl. Environ. Microbiol. 73:3380-3390.
46. Nataro, J. P., and J. B. Kaper 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
47. Ojo, O. E., A. T. P. Ajuwape, E. B. Otesile, A. A. Owoade, M. A. Oyekunle, and A. I. Adetosoye 2010. Potentially zoonotic shiga toxin-producing Escherichia coli serogroups in the faeces and meat of food-producing animals in Ibadan, Nigeria. Int. J. Food Microbiol. 142:214-221.
48. Okeke, I. N. 2009. Diarrheagenic Escherichia coli in sub-Saharan Africa: status, uncertainties and necessities. J. Infect. Dev. Ctries. 3:817-842.
49. Paton, J. C., and A. W. Paton 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
50. Pradel, N., V. Livrelli, C. D. De Champs, J. B. Palcoux, A. Reynaud, F. Scheutz, et al. 2000. Prevalence and characterization of Shiga toxin-producing Escherichia coli isolated from cattle, food, and children during a one-year prospective study in France. J. Clin. Microbiol. 38:1023-1031.
51. Qadri, F., A. M. Svennerholm, A. S. G. Faruque, and R. B. Sack 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18:465-483.
52. Raji, M. A., U. M. Minga, and R. S. Machang'u 2006. Prevalence and characterization of verotoxigenic Escherichia coli 0157 isolated from local chickens in Morogoro, Tanzania. J. Anim. Vet. Adv. 5:952-958.
53. Rhoades, J. R., G. Duffy, and K. Koutsoumanis 2009. Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiol. 26:357-376.
54. Rogerie, F., A. Marecat, S. Gambade, F. Dupond, P. Beaubois, and M. Lange 2001. Characterization of Shiga toxin producing E. coli and O157 serotype E. coli isolated in France from healthy domestic cattle. Food Microbiol. 63:217-223.
55. Rwego, I. B., T. R. Gillespie, G. Isabirye-Basuta, and T. L. Goldberg 2008. High rates of Escherichia coli transmission between livestock and humans in rural Uganda. J. Clin. Microbiol. 46:3187-3191.
56. Schmidt, M. A. 2010. LEE ways: tales of EPEC, ATEC and EHEC. Cell. Microbiol. 12:1544-1552.
57. Schmidt, H., L. Beutin, and H. Karch 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63:1055-1061.
58. Schmidt, H., C. Geitz, I. T. Phillips, F. Mathias, and H. Karch 1999. Non-O157 pathogenic Shiga toxin producing Escherichia coli: Phenotypic and genetic profiling of virulence traits and evidence for clonality. J. Infect. Dis. 179:115-123.
59. Schouten, J. M., A. W. van de Giessen, K. Frankena, M. C. De Jong, and E. A. Graat 2005. Escherichia coli O157 prevalence in Dutch poultry, pig finishing and veal herds and risk factors in Dutch veal herds. Prev. Vet. Med. 70:1-15.
60. Sidjabat-Tambunan, H., and J. C. Bensink 1997. Verotoxin-producing Escherichia coli from the faeces of sheep, calves and pigs. Aust. Vet. J. 75:292-293.
61. da Silva, A. S., G. F. Valadares, M. P. Penatti, B. G. Brito, and D. da Silva Leite 2001. Escherichia coli strains from edema disease: O serogroups, and genes for Shiga toxin, enterotoxins, and F18 fimbriae. Vet. Microbiol. 6:227-233.
62. Strockbine, N. A., J. G. Wells, C. A. Bopp, and T. J. Barrett 1998. Overview of detection and subtyping methods. Pp. 331-356 in J. B. Kaper and A. D. O'Brien, eds. Escherichia coli O157:H7 and other Shiga toxin producing E. coli strains. American Society for Microbiology, Washington, DC.
63. Trabulsi, L. R., R. Keller, and T. A. Tardelli Gomes 2002. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8:508-513.
64. Uber, A. P., L. R. Trabulsi, K. Irino, L. Beutin, Å. C. R. Ghilardi, T. A. T. Gomes, et al. 2006. Enteroaggregative Escherichia coli from humans and animals differ in major phenotypical traits and virulence genes. FEMS Microbiol. Lett. 256:251-257.