Skip to main content
Log in

Virulence genotyping of Escherichia coli isolates from avian cellulitis in relation to phylogeny

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Coliform cellulitis in broilers is caused by certain avian pathogenic Escherichia coli strains. Sixty-four E. coli samples were isolated in a slaughterhouse from broiler carcasses with cellulitis. The isolates were examined for the presence of selected virulence genes and phylogenetic determination by PCR assays. E. coli isolates belonged to A (51.56%), B1 (18.75%) and D (29.68%) phylogenetic groups. All of the isolates were positive for at least two virulence genes. The three most prevalent genes were csgA (92.18%), fimH (85.93%) and iucD (76.56%). F17 fimbrial family (f17A), P (papC) and S (sfa) fimbriae encoding genes were detected in one, nine and two isolates, respectively. The highest and the lowest number of virulence genes were found in D and A phylogenetic groups, respectively. Several combination of the virulence genes were detected; csgA, fimH, iucD was the most prevalent pattern. None of the isolates harboured the afa E-VIII, afaI B-C, eaeA, hly, stx1 and stx virulence genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amabile de Campos T, Stehling EG, Ferreira A et al (2005) Adhesion properties, fimbrial expression and PCR detection of adhesin-related genes of avian Escherichia coli strains. Vet Microbiol 106:275–285. doi:10.1016/j.vetmic.2004.12.025

    Article  CAS  PubMed  Google Scholar 

  • Bertin Y, Martin C, Oswald E, Girardeau JP et al (1996) Rapid and specific detection of F17-related pilin and adhesin genes in diarrheic and septicemic Escherichia coli strains by multiplex PCR. J Clin Microbiol 34:2921–2928

    CAS  PubMed  Google Scholar 

  • China B, Pirson V, Mainil J (1996) Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes. Appl Environ Microbiol 62:3462–3465

    CAS  PubMed  Google Scholar 

  • Chouikha I, Bree A, Moulin-Schouleur M et al (2008) Differential expression of iutA and ibeA in the early stages of infection by extra-intestinal pathogenic E. coli. Microbes Infect 10:432–438. doi:10.1016/j.micinf.2008.01.002

    Article  CAS  PubMed  Google Scholar 

  • Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558. doi:10.1128/AEM.66.10.4555-4558.2000

    Article  CAS  PubMed  Google Scholar 

  • de Brito BG, Gaziri LC, Vidotto MC (2003) Virulence factors and clonal relationships among Escherichia coli strains isolated from broiler chickens with cellulitis. Infect Immun 71:4175–4177. doi:10.1128/IAI.71.7.4175-4177.2003

    Article  PubMed  Google Scholar 

  • Delicato ER, de Brito BG, Gaziri LC et al (2003) Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis. Vet Microbiol 94:97–103

    CAS  PubMed  Google Scholar 

  • Derakhshanfar A, Ghanbarpour R (2002) A study on avian cellulitis in broiler chickens. Veterinarski Arhive 72:277–284

    Google Scholar 

  • Dissanayake DR, Wijewardana TG, Gunawardena GA et al (2008) Distribution of lipopolysaccharide core types among avian pathogenic Escherichia coli in relation to the major phylogenetic groups. Vet Microbiol 132:355–363. doi:10.1016/j.vetmic.2008.05.024

    Article  CAS  PubMed  Google Scholar 

  • Dozois CM, Fairbrother JM, Harel J et al (1992) pap- and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infect Immun 60:2648–2656

    CAS  PubMed  Google Scholar 

  • Escobar-Paramo P, Le Menac’h A, Le Gall T et al (2006) Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ Microbiol 8:1975–1984. doi:10.1111/j.1462-2920.2006.01077.x

    Article  CAS  PubMed  Google Scholar 

  • Ewers C, Li G, Wilking H et al (2007) Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297:163–176. doi:10.1016/j.ijmm.2007.01.003

    Article  CAS  PubMed  Google Scholar 

  • Ghanbarpour R, Derakhshanfar A, Pourbakhsh A (2003) Determination of P (F11) and F1 fimbriae of Escherichia coli isolated from avian cellulitis. Veterinarski Arhive 73:227–236

    Google Scholar 

  • Gomis SM, Gomis AI, Horadagoda NU et al (2000) Studies on cellulitis and other disease syndromes caused by Escherichia coli in broilers in Sri Lanka. Trop Anim Health Prod 32:341–351. doi:10.1023/A:1005293400605

    Article  CAS  PubMed  Google Scholar 

  • Gomis SM, Riddell C, Potter AA et al (2001) Phenotypic and genotypic characterization of virulence factors of Escherichia coli isolated from broiler chickens with simultaneous occurrence of cellulitis and other colibacillosis lesions. Can J Vet Res 65:1–6

    CAS  PubMed  Google Scholar 

  • Gyles CL, Prescott JF, Songer JG et al (2004) Pathogenesis of bacterial infections in animals, Thirdth edn. Blackwell, London

    Google Scholar 

  • Higgins J, Hohn C, Hornor S et al (2007) Genotyping of Escherichia coli from environmental and animal samples. J Microbiol Methods 70:227–235. doi:10.1016/j.mimet.2007.04.009

    Article  CAS  PubMed  Google Scholar 

  • Ishii S, Meyer KP, Sadowsky MJ (2007) Relationship between phylogenetic groups, genotypic clusters, and virulence gene profiles of Escherichia coli strains from diverse human and animal sources. Appl Environ Microbiol 73:5703–5710. doi:10.1128/AEM.00275-07

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey JS, Nolan LK, Tonooka KH et al (2002) Virulence factors of Escherichia coli from cellulitis or colisepticemia lesions in chickens. Avian Dis 46:48–52. doi:10.1637/0005-2086(2002) 046[0048:VFOECF]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey JS, Singer RS, O’Connor R et al (2004) Prevalence of pathogenic Escherichia coli in the broiler house environment. Avian Dis 48:189–195. doi:10.1637/7043

    Article  CAS  PubMed  Google Scholar 

  • Johnson JR, Stell AL (2000) Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272. doi:10.1086/315217

    Article  CAS  PubMed  Google Scholar 

  • Johnson LC, Bilgili SF, Hoerr FJET et al (2001) The effects of early exposure of cellulitis-associated Escherichia coli in 1-day-old broiler chickens. Avian Pathol 30:175–178. doi:10.1080/03079450125145

    Article  CAS  PubMed  Google Scholar 

  • Johnson TJ, Johnson SJ, Nolan LK (2006) Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. J Bacteriol 188:5975–5983. doi:10.1128/JB.00204-06

    Article  CAS  PubMed  Google Scholar 

  • Kariyawasam S, Scaccianoce JA, Nolan LK (2007) Common and specific genomic sequences of avian and human extraintestinal pathogenic Escherichia coli as determined by genomic subtractive hybridization. BMC Microbiol 7:81. doi:10.1186/1471.2180.7.81

    Article  PubMed  Google Scholar 

  • Kawano M, Yaguchi K, Osawa R (2006) Genotypic analyses of Escherichia coli isolated from chickens with colibacillosis and apparently healthy chickens in Japan. Microbiol Immunol 50:961–966

    CAS  PubMed  Google Scholar 

  • La Ragione RM, Woodward MJ (2002) Virulence factors of Escherichia coli serotypes associated with avian colisepticaemia. Res Vet Sci 73:27–35. doi:10.1016/S0034-5288(02)00075-9

    Article  PubMed  Google Scholar 

  • La Ragione RM, McLaren IM, Foster G et al (2002) Phenotypic and genotypic characterization of avian Escherichia coli O86:K61 isolates possessing a gamma-like intimin. Appl Environ Microbiol 68:4932–4942. doi:10.1128/AEM.68.10.4932-4942.2002

    Article  PubMed  Google Scholar 

  • Leclerc B, Fairbrother JM, Boulianne M et al (2003) Evaluation of the adhesive capacity of Escherichia coli isolates associated with avian cellulitis. Avian Dis 47:21–31. doi:10.1637/0005-2086(2003) 047[0021:EOTACO]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Lymberopoulos MH, Houle S, Daigle F et al (2006) Characterization of Stg fimbriae from an avian pathogenic Escherichia coli O78:K80 strain and assessment of their contribution to colonization of the chicken respiratory tract. J Bacteriol 188:6449–6459. doi:10.1128/JB.00453-06

    Article  CAS  PubMed  Google Scholar 

  • McPeake SJ, Smyth JA, Ball HJ (2005) Characterisation of avian pathogenic Escherichia coli (APEC) associated with colisepticaemia compared to faecal isolates from healthy birds. Vet Microbiol 110:245–253. doi:10.1016/j.vetmic.2005.08.001

    Article  CAS  PubMed  Google Scholar 

  • Mokady D, Gophna U, Ron EZ (2005) Virulence factors of septicemic Escherichia coli strains. Int J Med Microbiol 295:455–462. doi:10.1016/j.ijmm.2005.07.007

    Article  CAS  PubMed  Google Scholar 

  • Moulin-Schouleur M, Reperant M, Laurent S et al (2007) Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45:3366–3376. doi:10.1128/JCM.00037-07

    Article  CAS  PubMed  Google Scholar 

  • Ngeleka M, Kwaga JK, White DG et al (1996) Escherichia coli cellulitis in broiler chickens: clonal relationships among strains and analysis of virulence-associated factors of isolates from diseased birds. Infect Immun 64:3118–3126

    CAS  PubMed  Google Scholar 

  • Olkowski AA, Wojnarowicz C, Chirino-Trejo M et al (2005) The role of first line of defense mechanisms in the pathogenesis of cellulitis in broiler chickens: skin structural, physiological and cellular response factors. J Vet Med A Physiol Pathol Clin Med 52:517–524. doi:10.1111/j.1439-0442.2005.00768.x

    CAS  PubMed  Google Scholar 

  • Parreira VR, Gyles CL (2002) Shiga toxin genes in avian Escherichia coli. Vet Microbiol 87:341–352. doi:10.1016/S0378-1135(02)00084-6

    Article  CAS  PubMed  Google Scholar 

  • Rocha CGPA, Rocha LSS, Lima-Rosa AVC et al (2008) Genes associated with pathogenicity of avian Escherichia coli (APEC) isolated from respiratory cases of poultry. Pesqui Vet Bras 28:183–186

    Google Scholar 

  • Saif YM, Fadly AM, Glisson JR et al (2008) Diseases of poultry, 12th edn. Blackwell, London

    Google Scholar 

  • Singer RS, Jeffrey JS, Carpenter TE et al (2000) Persistence of cellulitis-associated Escherichia coli DNA fingerprints in successive broiler chicken flocks. Vet Microbiol 75:59–71. doi:10.1016/S0378-1135(00)00205-4

    Article  CAS  PubMed  Google Scholar 

  • Someya A, Otsuki K, Murase T (2007) Characterization of Escherichia coli strains obtained from layer chickens affected with colibacillosis in a commercial egg-producing farm. J Vet Med Sci 69:1009–1014. doi:10.1292/jvms.69.1009

    Article  CAS  PubMed  Google Scholar 

  • Stordeur P, Marlier D, Blanco J et al (2002) Examination of Escherichia coli from poultry for selected adhesin genes important in disease caused by mammalian pathogenic E. coli. Vet Microbiol 84:231–241. doi:10.1016/S0378-1135(01)00464-3

    Article  CAS  PubMed  Google Scholar 

  • Stordeur P, Bree A, Mainil J et al (2004) Pathogenicity of pap-negative avian Escherichia coli isolated from septicaemic lesions. Microbes Infect 6:637–645. doi:10.1016/j.micinf.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  • Van Bost S, Jacquemin E, Oswald E et al (2003) Multiplex PCRs for identification of necrotoxigenic Escherichia coli. J Clin Microbiol 41:4480–4482. doi:10.1128/JCM.41.9.4480-4482.2003

    Article  PubMed  Google Scholar 

  • Van Gerven N, De Greve H, Hernalsteens JP (2008) Presentation of the functional receptor-binding domain of the bacterial adhesin F17a-G on bacteriophage M13. Antonie Van Leeuwenhoek 93:219–226. doi:10.1007/s10482-007-9195-x

    Article  PubMed  Google Scholar 

  • Vandekerchove D, Vandemaele F, Adriaensen C et al (2005) Virulence-associated traits in avian Escherichia coli: comparison between isolates from colibacillosis-affected and clinically healthy layer flocks. Vet Microbiol 108:75–87. doi:10.1016/j.vetmic.2005.02.009

    Article  CAS  PubMed  Google Scholar 

  • Vidotto MC, Gaziri LC, Delicato ER (2004) Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis: correction. Vet Microbiol 102:95–96. doi:10.1016/j.vetmic.2004.06.00

    Article  CAS  PubMed  Google Scholar 

  • Wyborn NR, Clark A, Roberts RE et al (2004) Properties of haemolysin E (HlyE) from a pathogenic Escherichia coli avian isolate and studies of HlyE export. Microbiology 150:1495–1505. doi:10.1099/mic.0.26877-0

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto S, Terai A, Yuri K et al (1995) Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol Med Microbiol 12:85–90. doi:10.1111/j.1574-695X.1995.tb00179.x

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Maurer JJ, Hubert S et al (2005) Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Vet Microbiol 107:215–224. doi:10.1016/j.vetmic.2005.01.021

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant (No. 1386.10) from the Shahid Bahonar University of Kerman. The authors are thankful to the manager of the Eslam Kish industrial poultry slaughterhouse of Kerman for his cooperation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Reza Ghanbarpour.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ghanbarpour, R., Salehi, M. & Oswald, E. Virulence genotyping of Escherichia coli isolates from avian cellulitis in relation to phylogeny. Comp Clin Pathol 19, 147–153 (2010). https://doi.org/10.1007/s00580-009-0837-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-009-0837-4

Keywords

Navigation