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RESEARCH ARTICLE

Serological diversity, molecular characterisation and antimicrobial sensitivity of avian pathogenic Escherichia coli (APEC) isolates from broiler chickens in Kashmir, India

S. N. Magray A F , S. A. Wani B , Z. A. Kashoo B , M. A. Bhat C , S. Adil D , S. Farooq B , M. A. Rather A , Z. A. Kabli A , M. T. Banday D and Y. Nishikawa E
+ Author Affiliations
- Author Affiliations

A Disease Investigation Laboratory for Sheep and Goat, Department of Sheep Husbandry, Government of Jammu and Kashmir, Nowshera, Srinagar, 190011, India.

B Bacteriology Laboratory, Division of Veterinary Microbiology and Immunology, Faculty of Veterinary Sciences and Animal Husbandry, SKUAST-Kashmir, Shuhama, Srinagar, 190006, India.

C Division of Veterinary Microbiology and Immunology, Faculty of Veterinary Sciences and Animal Husbandry, R.S. Pora, SKUAST-Jammu, 181102, India.

D Division of Livestock Production and Management, Faculty of Veterinary Sciences and Animal Husbandry, SKUAST-Kashmir, Shuhama, Srinagar, 190006, India.

E Department of Food and Human Health Sciences, Graduate School of Human Life Science, Osaka City University, Osaka 558-8585, Japan.

F Corresponding author. Email: snmagraymicrobiol@gmail.com

Animal Production Science 59(2) 338-346 https://doi.org/10.1071/AN17065
Submitted: 4 February 2017  Accepted: 29 October 2017   Published: 8 January 2018

Abstract

The present study has determined the serological diversity, virulence-gene profile and in vitro antibiogram of avian pathogenic Escherichia coli (APEC) isolates from broiler chickens in India suspected to have died of colibacillosis. The virulence-gene profile of APEC was compared with that of the Escherichia coli isolates from faeces of apparently healthy chickens, called avian faecal E. coli (AFEC). In total, 90 representative isolates of APEC and 63 isolates of AFEC were investigated in the present study. The APEC were typed into 19 serogroups, while some isolates were rough and could not be typed. Most prevalent serogroup was O2 (24.44%). Among the eight virulence genes studied, the prevalence of seven genes (iss, iucD, tsh, cva/cvi, irp2, papC and vat) was significantly higher in APEC than in AFEC isolates. However, there was no significant difference between APEC and AFEC isolates for possession of astA gene. The most frequent gene detected among the two groups of organisms was iss, which was present in 98.88% and 44.44% of APEC and AFEC isolates respectively. The in vitro antibiogram showed that the majority (96.6%) of APEC isolates were resistant to tetracycline, while 82.2% were resistant to cephalexin, 78.8% to cotrimoxazole, 68.8% to streptomycin and 63.3% to ampicillin. However, most of them (84.45%) were sensitive to gentamicin. Thus, it is concluded that APEC from the broiler chickens carried putative virulence genes that attributed to their pathogenicity. Furthermore, the majority of APEC isolates were found to be multi-drug resistant, which, in addition to leading treatment failures in poultry, poses a public health threat.

Additional keywords: antibiogram, PCR, virulence genes.


References

Altekruse SF, Elvinger F, DebRoy C, Pierson FW, Eifert JD, Sriranganathan N (2002) Pathogenic and fecal Escherichia coli strains from turkeys in a commercial operation. Avian Diseases 46, 562–569.
Pathogenic and fecal Escherichia coli strains from turkeys in a commercial operation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38votFGmsg%3D%3D&md5=1bcd2c07f923c2f488b629847827e976CAS |

Amabile de Campos T, Lago JC, Nakazato G, Stehling EG, Brocchi M, Pestana de Castro AF, da Silveira WD (2008) Occurrence of virulence-related sequences and phylogenetic analysis of commensal and pathogenic avian Escherichia coli strains (APEC). Pesquisa Veterinaria Brasileira 28, 533–540.

Anand SK, Sharma F, Joshi CG, Purohit JH (2006) Molecular characterization of Escherichia coli using PCR–single strand conformation polymorphism analysis of 16S rRNA gene. Indian Journal of Poultry Science 41, 1–5.

Barnes HJ, Gross WB (1997) Colibacillosis. In ‘Diseases of poultry’. 10th edn. (Eds BW Calnek, HJ Barnes, CW Beard, LR McDougald, YM Saif) pp. 131–141. (Iowa State University Press: Ames, IA)

Bass L, Liebert CA, Lee M, Summers AO (1999) Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrobial Agents and Chemotherapy 43, 2925–2929.

Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardised single disc method. American Journal of Clinical Pathology 45, 493–496.

Blanco JE, Blanco M, Mora A, Blanco J (1997) Production of toxins (enterotoxins, verortoxins, and necrotoxins) and colicins by Escherichia coli strains isolated from septicemic and healthy chickens: relationship with in vivo pathogenicity. Journal of Clinical Microbiology 35, 2953–2957.

Buchanan RE, Gibbon NE (1994) ‘Burgeye’s manual of determinative bacteriology.’ 9th edn. (Williams and Wilkins: Baltimore, MD)

Christensen JP, Chadfield MS, Bojesen AM, Bisgaard M (2003) Investigations on the clonality of E. coli infections in industrial poultry production. In ‘Proceedings of the XIII congress of the World Veterinary Poultry Association’, Denver, Colorado, USA. 83.

Circella E, Pennelli D, Tagliabue S, Ceruti R, Giovanardi D, Camarda A (2009) Virulence-associated genes in avian pathogenic Escherichia coli of turkey. Italian Journal of Animal Science 8, 775–779.
Virulence-associated genes in avian pathogenic Escherichia coli of turkey.Crossref | GoogleScholarGoogle Scholar |

Delicato ER, de Brito BG, Gaziri LCJ, Vidotto MC (2003) Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis. Veterinary Microbiology 94, 97–103.
Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFGns7g%3D&md5=9b8e2f3baeef8e75665f72966929f701CAS |

Dho-Moulin M, Fairbrother M (1999) Avian pathogenic Escherichia coli. Veterinary Research 30, 299–316.

Dominick MA, Jensen AE (1984) Colonization and persistence of Escherichia coli in axenic and monxenic turkeys. American Journal of Veterinary Research 45, 2331–2335.

Dozois CM, Fairbrother JM, Harel J, Bosse M (1992) Pap- and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infection and Immunity 60, 2648–2656.

Dozois CM, Dho-Moulin M, Bree A, Fairbrother JM, Desautels C, Curtiss R (2000) Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the tsh genetic region. Infection and Immunity 68, 4145–4154.
Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the tsh genetic region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlyntL0%3D&md5=762cce3bcf147ba36deb189d7e6ebd98CAS |

Dziva F, Stevens MP (2008) Colibacillosis in poultry: unraveling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts. Avian Pathology 37, 355–366.
Colibacillosis in poultry: unraveling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosFahtLY%3D&md5=be063bc71ce4e33b7e521dfe4658011bCAS |

Dziva F, Hauser H, Connor TR, van Diemen PM, Prescott G, Langridge GC, Eckert S, Chaudhuri RR, Ewers C, Mellata M, Mukhopadhyay S, Curtiss R, Dougan G, Wieler LH, Thomson NR, Pickard DJ, Stevens MP (2013) Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms. Infection and Immunity 81, 838–849.
Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1Smsb0%3D&md5=8bfc69e0c030d3f0b5a451b6f1f07551CAS |

Ewers C, Janssen T (2005) Rapid detection of virulence associated genes in avian pathogenic Escherichia coli (APEC) by multiplex polymerase chain reaction. Avian Diseases 49, 269–273.
Rapid detection of virulence associated genes in avian pathogenic Escherichia coli (APEC) by multiplex polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar |

Ewers C, Antao EM, Diehl I, Philipp HC, Wieler LH (2009) Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Applied and Environmental Microbiology 75, 184–192.
Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktlejtb0%3D&md5=00c5471ef6984c8fe08ebabd2ee5ccbcCAS |

Ewers C, Janssen T, Kiessling S, Philipp HC, Wieler LH (2004) Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry. Veterinary Microbiology 104, 91–101.
Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVKgsLg%3D&md5=0daeecf34ecbfd5443cf6d3687a0af23CAS |

Fasenko GM, Christopher EEOD, McMullen LM (2009) Spraying hatching eggs with electrolyzed oxidizing water reduces eggshell microbial load without compromising broiler production parameters. Poultry Science 88, 1121–1127.
Spraying hatching eggs with electrolyzed oxidizing water reduces eggshell microbial load without compromising broiler production parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFOnsrg%3D&md5=876fcbe120faf3164894142ee7239c5fCAS |

Franck SM, Bosworth BT, Moon HW (1998) Multiplex PCR for enterotoxigenic, attaching and effacing and Shiga toxin-producing Escherichia coli strains from calves. Journal of Clinical Microbiology 36, 1795–1797.

Germon P, Chen YH, He L, Blanco JE, Bree A, Schouler C, Huang SH, Moulin-Schouleur M (2005) ibeA, a virulence factor of avian pathogenic Escherichia coli. Microbiology 151, 1179–1186.
ibeA, a virulence factor of avian pathogenic Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslWqtbw%3D&md5=8a970583d66406b4e391782e2b1998e5CAS |

Ghanbarpour R, Sami M, Salehi M, Ouromiei M (2011) Phylogenetic background and virulence genes of Escherichia coli isolates from colisepticemic and healthy broiler chickens in Iran. Tropical Animal Health and Production 43, 153–157.
Phylogenetic background and virulence genes of Escherichia coli isolates from colisepticemic and healthy broiler chickens in Iran.Crossref | GoogleScholarGoogle Scholar |

Ghosh RC, Hirpurkar SD, Suryawanshi PR (2006) Concurrent colibacillosis and infectious bursal disease in broiler chicks. The Indian Veterinary Journal 83, 1019–1020.

Gilson L, Mahanty HK, Kolter R (1987) Four plasmid genes are required for colicin V synthesis, export, and immunity. Journal of Bacteriology 169, 2466–2470.
Four plasmid genes are required for colicin V synthesis, export, and immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlCjtrY%3D&md5=37d8bfcb0a0f34f288e5e2f03897388aCAS |

Gyles CL (2008) Antimicrobial resistance in selected bacteria from poultry. Animal Health Research Reviews 9, 149–158.
Antimicrobial resistance in selected bacteria from poultry.Crossref | GoogleScholarGoogle Scholar |

Gyles CL, Prescott JF, Songer G, Thoen CO (2010) Escherichia coli. In ‘Pathogenesis of bacterial infection in animals’. (Eds CL Gyles, JM Fairbrother) pp. 267–298. (Wiley: Ames, IA)

Johnson TJ, Siek KE, Johnson SJ, Nolan LK (2006a) DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. Journal of Bacteriology 188, 745–758.
DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1OhtQ%3D%3D&md5=e55b8522cb4e13eae314a3b8c4acbc24CAS |

Johnson TJ, Johnson SJ, Nolan LK (2006b) Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. Journal of Bacteriology 188, 5975–5983.
Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVehtbk%3D&md5=2d36e516df4cb81d39dd1a749cfeb009CAS |

Kariyawasam S, Johnson TJ, DebRoy C, Nolan LK (2006) Occurrence of pathogenicity island IAPEC-01 genes among Escherichia coli implicated in avian colibacillosis. Avian Diseases 50, 405–410.
Occurrence of pathogenicity island IAPEC-01 genes among Escherichia coli implicated in avian colibacillosis.Crossref | GoogleScholarGoogle Scholar |

Kawano M, Kazuhiko Y, Osawa R (2006) Genotypic analysis of Escherichia coli isolated from chicken with colibacillosis and apparently healthy chicken in Japan. Microbiology and Immunology 50, 961–966.
Genotypic analysis of Escherichia coli isolated from chicken with colibacillosis and apparently healthy chicken in Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFCqur4%3D&md5=8f3a75733b8bc38b2211ef886feab357CAS |

Kim TE, Jeong YW, Cho SH, Kim SJ, Kwon HJ (2007) Chronological study of antibiotic resistances and their relevant genes in Korean avian pathogenic Escherichia coli isolates. Journal of Clinical Microbiology 45, 3309–3315.
Chronological study of antibiotic resistances and their relevant genes in Korean avian pathogenic Escherichia coli isolates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12rurfN&md5=b7a6904863421470895fa6de82423430CAS |

Lu JR, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology 69, 6816–6824.
Diversity and succession of the intestinal bacterial community of the maturing broiler chicken.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVyktbs%3D&md5=47fbc4eedca6e6953a86bfab580d450fCAS |

Maurer JJ, Brown TP, Steffens WL, Thayer SG (1998) The occurrence of ambient temperature-regulated adhesions curli and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Diseases 42, 106–118.
The occurrence of ambient temperature-regulated adhesions curli and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7psVarsw%3D%3D&md5=588fd5f18086ecdc22584ea3350f7e41CAS |

McPeake SJW, Smyth JA, Ball HJ (2005) Characterization of avian pathogenic Escherichia coli (APEC) associated with colisepticaemia compared to faecal isolates from healthy birds. Veterinary Microbiology 110, 245–253.
Characterization of avian pathogenic Escherichia coli (APEC) associated with colisepticaemia compared to faecal isolates from healthy birds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MrhsVejug%3D%3D&md5=afc0a677983c3fd34cb1476146da8f43CAS |

Moniri R, Dastehgoli K (2007) Antimicrobial resistance among Escherichia coli strains isolated from healthy and septicemic chickens. Pakistan Journal of Biological Sciences 10, 2984–2987.
Antimicrobial resistance among Escherichia coli strains isolated from healthy and septicemic chickens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FjslOgsA%3D%3D&md5=a68e7552ede947aae6dda61ee40ad410CAS |

Morris JG, Potter M (1997) Emergence of new pathogens as a function of changes in host susceptibility. Emerging Infectious Diseases 3, 435–441.
Emergence of new pathogens as a function of changes in host susceptibility.Crossref | GoogleScholarGoogle Scholar |

Nagaraja KV, Emery DA, Jordan KA, Sivanandan V, Newman JA, Pomeroy BS (1984) Effect of ammonia on the quantitative clearance of Escherichia-coli from lungs, air sacs, and livers of turkeys aerosol vaccinated against Escherichia coli. American Journal of Veterinary Research 45, 392–395.

Ngeleka M, Brereton L, Brown G, Fairbrother JM (2002) Pathotypes of avian Escherichia coli as related to tsh-, pap-, pil-, and iuc-DNA sequences, and antibiotic sensitivity of isolates from internal tissues and the cloacae of broilers. Avian Diseases 46, 143–152.
Pathotypes of avian Escherichia coli as related to tsh-, pap-, pil-, and iuc-DNA sequences, and antibiotic sensitivity of isolates from internal tissues and the cloacae of broilers.Crossref | GoogleScholarGoogle Scholar |

Petersen A, Christensen JP, Kuhnert P, Bisgaard M, Olsen JE (2006) Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation. Veterinary Microbiology 116, 120–128.
Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsFyntLk%3D&md5=a41f8eabb4eabd32a3d187dfd4d7f57dCAS |

Raji M, Adekeye J, Kwaga J, Bale J, Henton M (2007) Serovars and biochemical characterization of Escherichia coli isolated from colibacillosis cases and dead-in-shell embryos in poultry in Zaria-Nigeria. Veterinarski Arhiv 77, 495–505.

Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK (2005) Characterizing the APEC pathotype. Veterinary Research 36, 241–256.
Characterizing the APEC pathotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVOrs74%3D&md5=29e925fc47d6902cd51f83d6d9547547CAS |

Saha T, Guha C, Biswas U, Chakraborty D, Chakaborty GC, Sadhukhan TK (2007) Escherichia coli isolates from respiratory disease of broiler birds. The Indian Veterinary Journal 84, 915–917.

Salehi TZ, Bonab SF (2006) Antibiotics susceptibility pattern of Escherichia coli strains isolated from chickens with colisepticemia in Tabriz Province Iran. International Journal of Poultry Science 5, 677–684.
Antibiotics susceptibility pattern of Escherichia coli strains isolated from chickens with colisepticemia in Tabriz Province Iran.Crossref | GoogleScholarGoogle Scholar |

Sharda R, Ruban W, Thiyageeswaran M (2010) Isolation, characterization and antibiotic resistance pattern of Escherichia coli isolated from poultry. American Eurasian Journal of Scientific Research 5, 18–22.

Snedecor GW, Cochran WG (1980) ‘Statistical methods.’ 7th edn. (Iowa State University Press: Ames, IA)

Tivendale KA, Allen JL, Ginns CA, Crabb BS, Browning GF (2004) Association of iss and iucA, but not tsh, with plasmid-mediated virulence of avian pathogenic Escherichia coli. Infection and Immunity 72, 6554–6560.
Association of iss and iucA, but not tsh, with plasmid-mediated virulence of avian pathogenic Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsFekt7s%3D&md5=051944eb621c2b17c019db7b30537d7aCAS |

van den Bogaard AE, London N, Driessen C, Stobberingh EE (2001) Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. The Journal of Antimicrobial Chemotherapy 47, 763–771.
Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksFCiurY%3D&md5=f538d366bee5d4b395faa3e75cfd23e7CAS |

Vandekerchove D, Vandemaele F, Adriaensen C, Zaleska M, Hernalsteens JP, Baets LD, Butaye P, Immerseel FV, Wattiau P, Laevens H, Mast J, Goddeeris B, Pasmans F (2005) Virulence-associated traits in avian Escherichia coli: comparison between isolates from colibacillosis-affected and clinically healthy layer flocks. Veterinary Microbiology 108, 75–87.
Virulence-associated traits in avian Escherichia coli: comparison between isolates from colibacillosis-affected and clinically healthy layer flocks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Wmtrs%3D&md5=d195ef34c214f9cd129925287a93a79eCAS |

Wang XM, Liao XP, Zhang WJ, Jiang HX, Sun J, Zhang MJ, He XF, Lao DX, Liu YH (2010) Prevalence of serogroups, virulence genotypes, antimicrobial resistance, and phylogenetic background of avian pathogenic Escherichia coli in south of China. Foodborne Pathogens and Disease 7, 1099–1106.
Prevalence of serogroups, virulence genotypes, antimicrobial resistance, and phylogenetic background of avian pathogenic Escherichia coli in south of China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSju77N&md5=d0a573fa3dbd991be8777455c3e9b9d8CAS |

Wani SA, Nabi A, Fayaz I, Ahmad I, Nishikawa Y, Qureshi K, Khan MA, Chowdhary J (2006) Investigation of diarrhoeic faecal samples for enterotoxigenic, Shiga toxin-producing and typical or atypical enteropathogenic Escherichia coli in Kashmir, India. FEMS Microbiology Letters 261, 238–244.

Wooley RE, Spears KR, Brown J, Nolan LK, Fletcher OJ (1992) Relationship of complement resistance and selected virulence factors in pathogenic avian Escherichia coli. Avian Diseases 36, 679–684.
Relationship of complement resistance and selected virulence factors in pathogenic avian Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2FjvVensA%3D%3D&md5=c61c48aabfb850779b4bda1df4249bf0CAS |

Yaguchi K, Ogitani T, Osawa R, Kawano M, Kokumai N, Kaneshige T, Noro T, Masubuchi K, Shimizu Y (2007) Virulence factors of avian pathogenic Escherichia coli strains isolated from chickens with colisepticemia in Japan. Avian Diseases 51, 656–662.
Virulence factors of avian pathogenic Escherichia coli strains isolated from chickens with colisepticemia in Japan.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snmslOisA%3D%3D&md5=79a517a8751acbfbb31534bc4d7838e3CAS |

Yamamoto T, Echeverria P (1996) Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infection and Immunity 64, 1441–1445.

Yang H, Chen S, White DG, Zhao S, McDermott P, Walker R, Meng J (2004) Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. Journal of Clinical Microbiology 42, 3483–3489.
Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1Ogtro%3D&md5=7401850f3e70f6e06fc866293a19d4a7CAS |

Zhao S, Hubert S, Maurer S (2005) Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Veterinary Microbiology 107, 215–224.
Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1KlsL4%3D&md5=b263d59cb80c1832a732e1a405c76492CAS |