Characterization of Virulent Factors of Sorbitol-Negative  Escherichia coli Isolated from Quail

Khusnan Khusnan; Wahyu Prihtiyantoro

doi:10.22146/ijvs.v1i1.44793

Characterization of Virulent Factors of Sorbitol-Negative Escherichia coli Isolated from Quail

https://doi.org/10.22146/ijvs.v1i1.44793

Khusnan Khusnan^(1*), Wahyu Prihtiyantoro⁽²⁾

(1) Akademi Peternakan Brahmaputra, Yogyakarta
(2) Akademi Peternakan Brahmaputra Yogyakarta
(*) Corresponding Author

Abstract

Colibacillosis pada bangsa unggas merupakan penyakit yang disebabkan Avian Pathogen Escherichia coli (APEC) yang dapat menimbulkan kerugian ekonomi yang besar pada industri perunggasan. Isolates APEC pada penelitian ini dilakukan karakterisasi hemolisin, emaglutinin serta deteksi empat gen virulen yang penting yaitu gen increased serum survival (iss), antigen kapsul (kps), temperature sensitive haemagglutinin (tsh) dan enterohemolysin (hly). Pada penelitian ini dari 21 isolat Escherichia coli asal burung puyuh, secara fenotipik semua isolat negatif pada uji Sorbitol MacConkey, 38,1% isolat bersifat hemolitik, 52,4% memiliki hemaglutinin. Secara genotipik diketahui sebanyak 61,9% isolat memiliki gen iss, gen kps 9,5%, gen hly 9,5%, dan 4,8% isolat memiliki gen tsh. Isolat-isolat tersebut merupakan strain patogen dan berpotensi sebagai penyebab zoonosis.

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References

Abd El Tawab, A.A., Ammar, A.M., El-Hofy, F.I., Hakeem, M.A. and Galil, N.M.A. (2016). Molecular screening of virulence genes in avian pathogenic Escherichia coli. Benha Vet. Med. J. 30(1): 137‐149.

Abrar, M. (2009) Role of Escherichia coli haemaglutinin in adhesion process. J. Ked. Hewan. 3(1): 194-198.

Al-Arfaj, A.A., Ali, M.S., Hessain, A.M., Zakri, A.M., Dawoud, T.M., Al-Maary, K.S. and Moussa, I.M. (2016). Phenotypic and genotypic analysis of pathogenic Escherichia coli virulence genes recovered from Riyadh, Saudi Arabia. Saudi J. of Biological Sci., 23: 713-717.

AL-Saiedi, R.L.R. and Al-Mayah, A.A.S. (2014) Pathogenicity testing of several APEC isolates obtained from naturally infected broiler birds reared in Basrah. Int. J. of Poul. Sci., 13(7): 374-378.

Arslan, S. and Ozdemir, F. (2013) Investigation of Escherichia coli O157 in Turkish homemade white cheese. IUFS. J. Biol., 72(1): 45-51.

Badouei, M.A., Blackall, P.J., Koochakzadeh, A., Nazarpak, H.H. and Sepehri, M.A. (2015) Prevalence and clonal distribution of avian Escherichia coli isolates harboring increased serum survival (iss) gene. J. Appl. Poult. Res., 00: 1-7.

Barbieri, N.L., de Oliveira, A.L., Tejkowski, T.M., Pavanelo, D.B., Rocha, D.A., Matter, L.B., Callegari-Jacques, S.M., de Brito, B.G. and Horn, F. (2013). Genotypes and pathogenicity of cellulitis isolates reveal traits that modulate APEC virulence. PLoS ONE, 8(8). doi.org/10.1371/journal.pone.0072322.

Beutin, L., Montenegro, M.A., Orskov, I., Orskov, F., Prada, J., Zimmermann, S. and Stephan, R. (1989). Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J. Clin. Microbiol. 27(11): 2559-2564.

Bottero, M.T., Dalmasso, A., Soglia, D., Rosati, S., Decastelli, L. and Civera. T. (2004) Development of a multiplex PCR assay for the identification of pathogenic genes of Escherichia coli in milk and milk products. Mol. Cell. Probes., 18(4): 283-288.

Catana, N. and Herman, V. (2010). Epidemiological studies on some E. coli strains in broiler Chickens. Vet. Med. 67(2): 74-76.

Coote, J.G. (1996). The RTX toxins of gramnegative bacterial pathogens: modulators of the host immune system. Rev. In Med. Microbiol., 7: 53-62.

Cunha, M.P.V., de Oliveira, M.C.V., Moreno, A.M., de Oliveira, M.G.X., da Silva, K.C. and Knöbl, T. (2014) Virulence profiles, phylogenetic background, and antibiotic resistance of Escherichia coli isolated from Turkeys with airsacculitis. Scientiﬁc World Journal. Article ID 289024, 8 pages http://dx.doi.org/10.1155/2014/289024

de Campos, T.A., Stehling, E.G., Ferreira, A., de Castro, A.F.P., Brocchi, M. and da Silveira, W.D. (2005) Adhesion properties, fimbrial expression and PCR detection of adhesin-related genes of avian Escherichia coli strains. Vet. Microbiol., 106(3-4): 275-285.

Delicato, E.R., de Brito, B.G., Konopatzki, A.P., Gaziri, L.C.J. and Vidotto, M.C. (2002). Occurrence of temperature-sensitive hemagglutinin among avian Escherichia coli. Avian Dis., 46: 713-716.

Dissanayake, D.R., Octavia, S. and Lan, R. (2014). Population structure and virulence contentof avian pathogenic Escherichia coli isolated from outbreaks in Sri Lanka. Vet. Microbiol. (31)168: 403-412.

Dozois, C.M., Dho-Moulin, M., Bree, A., Fairbrother, J.M., Desautels, C., Curtiss, III. R. (2000). Relationship between the tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the tsh genetic region. Infect. Immun., 68: 4145-4154.

Drugdova, Z. and Kmet, V. (2013) Prevalence of β-lactam and fluoroquinolone resistance, and virulence factors in Escherichia coli isolated from chickens in Slovakia. Biologia 68(1): 11-17.

Dziva, F. and Stevens, M.P. (2008). Colibacillosis in poultry: unravelling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts. Avian Pathol., 37(4): 355-366.

Dziva, F., Hauser, H., Connor, T.R., van Diemen, P.M., Prescott, G. and Langridge, G.C. (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. Infect. Immun., 81: 838-849.

Edwards, J.S. and Palsson, B.O. (2000). The Escherichia coli MG1655 in silico metabolic genotype: its definition, characteristics, and capabilities. Proc. Natl. Acad. Sci., 97: 5528-5533.

El-Demerdash, M.Z., Hanan, M.F.A. and Asmaa, E.A. (2013). Studies on mortalities in baby quail chicks. Proc. of the 6 th Animal Wealth Research Conf. in the Middle East & North Africa. Hurghada information center- 27-30 September (2013): 63-76.

Ewers, C., Janben, T., Kiebling, S., Philip, H.C. and Wieler, L.H. (2004). Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry. Vet. Microbiol., 104: 91-101.

Fakruddin, M.D., Reaz, M.M., Abhijit, C. and Khanjada, S.M. (2013). A preliminary study on virulence factors and antimicrobial resistance in extra-intestinal pathogenic E. coli (ExPEC) in Bangladesh. Ind. J. Med. Res., 137:988-990.

Fodor, I., Catana, N. and Herman, V. (2010). Epidemiological studies on some E. coli strains in broiler chickens.Vet. Med., 67(2): 74-76.

Foley, S.L., Horne, S.M., Giddings, C.W., Robinson, M. and Nolan, L.K. (2000). Iss from a virulent avian Escherichia coli. Avian Dis. 44: 185-191.

Gao, Q., Wang, W., Xu, H., Xu, Y., Ling, J., Zhang, D., Gao, S. and Liu, X. (2012). Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol. 12: 143.

Ghunaim, H., Abdu-Madi, M.A. and Kariyawasam. S. (2014). Advances in vaccination against avian pathogenic Escherichia coli respiratory disease: potencials and limitations. Vet. Microbiol. 172: 13-22.

Grover, P.S., Bareja, R., Narang, V.K. and Jaryal, S.C. (2013) Incidence of fimbriated strains amongst haemolytic Escherichia coli. J. of Den. and Med. Sci., 4(3): 69-72.

Hamad, M.A., Al-Aalim, A.M., Al-Dabbagh, S.Y.A. and Ali, H.H. (2012). Detection of organ bacterial load in quails. Iraqi J. of Vet. Sci., 26(2): 47-51.

Hamza, I. Abdelazeem, E., Algammal, M., Nasef, S.A., Elfeil, W.K. and Mansour, G.H. (2016). Genetic variation among avian pathogenic E. coli strains isolated from broiler chickens. Asian J. of An. and Vet. Advances., 11: 350-356.

Hassan, H.K. and Bakeet, A.A.M. (2014). Characterization of Escherichia coli strains isolated from infected pigeons in assiut province. Assiut Vet. Med. J., 60(142): 29-33.

Herlax, V., Henning, M.F., Bernasconi, A.M., Goni, F.M. and Bakas, L. (2010). The lytic mechanism of Escherichia coli α-hemolysin associated to outer membrane vesicles. Natural Sci. 2: 484-492.

Huja, S., Oren, Y., Trost, E., Brzuszkiewicz, E., Biran D., Blom J., Goesmann, A., Gottschalk, G., Hacker, J., Ron, E.Z. and Dobrindt, U. (2015). Genomic avenue to avian colisepticemia. MBio. 6: 1-13.

Jamshidi, A., Razmyar, J. and Fallah, N. (2016). Detection of eaeA, hlyA, stx1 and stx2 genes in pathogenic Escherichia coli isolated from broilers affected with colibacillosis. IJVM. 10 (2): 97-103.

Johnson, J.R., Kuskowski, M.A., Gajewski, A., Soto, S., Horcajada, J.P., de Anta, J.M.T. and Vila, J. (2005). Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J. Infect. Dis., 191: 46-50.

Johnson, R.J. (1991) Virulence factors in E. coli urinary tract infection. Clin. Microbiol. Rev., 4: 80-128.

Johnson, T.J. and Nolan, L.K. (2009) Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol and Molecular Biol Rev. 73(4):750-774.

Johnson, T.J., Giddings, C.W., Horne, S.M., Gibbs, P.S., Wooley, R.E., Skyberg, J., Olah, P., Kercher, R., Sherwood, J.S., Foley, S.L. and Nolan, L.K. (2002). Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate. Avian Dis., 46: 342-352.

Karimi, V., Salehi, Z.T., Sadegh, M. and Jaafarnejad, S. (2011). The relation of water contamination and colibacillosis occurrence in poultry farms in Qom province of Iran. Iran J. of Vet. Res., 12(2):133-138.

Kausar, Y., Chunchanur, S.K., Nadagir, S.D., Halesh, L.H. and Chandrasekhar, M.R. (2009) Virulence factors, serotypes and antimicrobial suspectibility pattern of Escherichia coli in urinary tract infections. Al Ameen J. Med. Sci., 2(1): 47-51.

Kim, J.Y., Kim, S., Kwon, N., Bae, W.K., Lim, J.Y. and Koo, H.C. (2005) Isolation and identification of Escherichia coli O157:H7 using different detection methods and molecular determination by multiplex PCR and RAPDJ. Vet. Sci., 6: 7-19.

Knobl, T, Saidenberg, A.B.S., Moreno, A.M.M., Gomes, T.A.T., Vieira, M.A.M., Leite, D.S., Blanco, J.E. and Ferreira, A.J.P. (2011) Serogroups and virulence genes of Escherichia coli isolated from psittacine birds. Pesq. Vet. Bras. 31(10):916-921.

Knobl, T., Tania, A.T.G., Midolli, M.A.V., Bottinoa, J.A. and Ferreira, A.J.P. (2004) Detection of pap, sfa, afa and fim adhesin-encoding operons in avian pathogenic Escherichia coli. Intern. J. Applied Res. Vet. Med., 2: 135-141.

Koochakzadeh, A., Salehi Z., Fasaei, T.N. and Badouei, B.A. (2014) Detection of verotoxin (Shiga-like toxin)-producing and eae harboring Escherichia coli in some wild captive and domestic equidae and canidae. Archives of Razi Institute., 69(2): 157-163.

Kostakioti, M. and Stathopoulos, C. (2004). Functional analysis of the Tsh autotransporter from an avian pathogenic Escherichia coli strain. Infect Imunn., 72:5548-5554.

Kukanur, S., Meundi, M.M., Bajaj, A. and Kotigadde, S. (2015). Co-Relation between virulence factors and antibiotic resistance of E. coli, with special reference to uropathogenic E. coli. J. of Dent. and Med. Sci., 14(3):15-21.

Kunert-Filho, H.C., Carvalho, D., Grassotti, T.T., Soares, B.D., Rossato, J.M., Cunha, A,C., Brito, K.C.T., Cavalli, L.S. and. Brito, B.G. (2015) Avian pathogenic Escherichia coli methods for improved diagnosis. World's Poult. Sci. J., 71: 249-258.

Kwon, S.G., Cha, S.Y., Choi, E.J., Kim, B., Song, H.J. and Jang, H.K. (2008) Epidemiological prevalence of avian pathogenic Escherichia coli differentiated by multiplex PCR from commercial chickens and hatchery in Korea. J. Bacteriol. Virul. 38: 179-188.

Lefebvre, B., Gattuso, M., Moisan, H., Malouin, F. and Diarra, M.S. (2009). Genotype comparison of sorbitol-negative Escherichia coli isolates from healthy broiler chickens from different commercial farms. Poult. Sci., 88: 1474-1484.

Lutwyche, P., Rupps, T.R., Cavanagh, J., Warren, R.A.J. and Brooks, D.E. (1994). Cloning, sequencing, and viscometric adhesion analysis of heat-resistant Agglutinin, an integral membrane hemagglutinin from Escherichia coli 09:H1O:K99. Infect. and Immunity., 78(3): 5020-5026.

Lynne, A.M., Skyberg, J.A., Logue C.M. and Nolan L.K. (2007). Detection of iss and Bor on the surface of Escherichia coli. J. of App. Microbiol., 102: 660-666

Maheswari, U.B., Palvai, S., Anuradha P.R. and Kammili, N. (2013). Hemagglutination and biofilm formation as virulence markers of uropathogenic E. coli in acute urinary tract infections and urolithiasis. Ind. J. Urol., 29: 277-281.

Maturana, V.G., de Pace, F., Carlos, C., Pires M., de Campos, A.T, Nakazato, G., Stheling E.G., Logue, C.M., Nolan, L.K., da Silveira, W.D. (2011). Subpathotypes of avian pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence Traits. Open Microbiol J., 55: 55-64.

Mbanga, J. And Nyararai, Y.O. (2015). Virulence gene profiles of avian pathogenic Escherichia coli isolated from chickens with colibacillosis in Bulawayo, Zimbabwe, Onderstepoort J. of Vet. Res. 82(1), Art. #850, 8 pages. http:// dx.doi.org/10.4102/ojvr. v82i1.850.

McNamee, P.T., McCullagh, J.J., Thorp, B.H., Ball, H.J., Graham, D., McCullough, S.J., McConaghy, D. and Smyth, J.A. (1998). Study of leg weakness in two commercial broiler flocks. Vet. Rec., 143: 131-135.

Mellata, M., Dho-Moulin, M., Dozois, C.M., Curtiss III, R., Brown, P.K., Arne, P., Bree, A., Desautels, C. and Fairbrother, J.M. (2003). Role of virulence factor in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect. Immun., 71: 536-540.

Mitchell, N.M., Johnson, J.R., Johnston, B., Curtiss, R. and Mellata, M. (2015). Zoonotic potential of Escherichia coli isolates from retail chicken meat products and eggs. Appl Environ Microbiol., 81: 1177-1187.

Mittal E., Kumar S., Rahman A., Krishnasastry M. V. (2014). Modulation of phagolysosome maturation by bacterial tlyA gene product. J. Biosci., 39: 821-834.

Mohamed, M.A., Shehata, M.A. and Rafeek, E. (2014). Virulence genes content and antimicrobial resistance in Escherichia coli from broiler chickens. Vet. Med. Int. Article ID 195189, 6 pages http://dx.doi.org/10.1155/2014/195189.

Monroy, M.A., Knöbl, T., Bottino, J.A., Ferreira, C.S. and Ferreira, A.J.P. (2005). Virulence Characteristics of Escherichia coli isolates obtained from broilers breeders with salpingitis. Comp. Immunol. Microbiol. Infect. Dis., 28: 1-15.

Moon, B.M., Won, G.Y., Choi, Y.Y., Jin, J.K., Oh, I.G., Park, J.H., Eo, S.K. and Lee, J.H. (2006). Isolation and characteristics of avian pathogenic Escherichia coli from birds associated with colibacillosis. Proceedings of AZWMP 2006 Chulalongkorn Uni. Fac. of Vet. Sc., Bangkok, Thailand, 26-29 Oct 2006.

Morales, C., Lee, M.D., Hofacre, C. and Maurer, J.J. (2004). Detection of a novel virulence gene and a Salmonella virulence homologue among Escherichia coli isolated from broiler chickens. Foodborne Pathol. Dis., 1(3): 160-165.

Müller, E.E. and Ehlers, M.M. (2005). Biolog identiﬁcation of non-sorbitol fermenting bacteria. Water SA., 31: 247-251.

Musa, H.H., He, S.F., Wu, S.L., Zhu, C.H., Liu, Z.H., Zhang, Z.N., Raj, V.S., Gu, R.X. and Zhu, G.Q. (2009). Genetic engineering of avian pathogenic E. coli to study the functions of FimH adhesion. Indian J Exp Biol., 47: 916-920.

Nakazato, G., Compos, A.E.G., Brocchi, S.M. and da Silveira, W.D. (2009). Virulence factor of avian pathogenic Escherichia coli (APEC). Pesq. Vet. Bras., 29: 479-486.

Naveen, R. and Mathai, E. (2005). Some virulence characteristics of uropathogenic Escherichia coli indifferent patient groups, Ind. J. of Med. Res., 122:143-147.

Oh, Y., Kang, M.S., Kim, J.M., An, B.K., Song, E.A., Kim, J.Y., Shin, E.G., Kim, M.J., Kwon, J.H. and Kwon, Y.K. (2011). Characterization of Escherichia coli isolates from laying hens with colibacillosis on 2 commercial egg-producing farms in Korea. J. Poultry Sci., 90:1948-1954.

Olsen, R.H., Chadfield, M.S., Christensen, J.P., Scheutz, F., Christensen, H. and Bisgaard, M. (2011). Clonality and virulence traits of Escherichia coli associated with haemorrhagic septicaemia in turkeys. Avian Pathol., 40(6): 587-595.

Paixao, A.C., Ferreira, A.C., Fevereiro, M., Fontes, M., Martins, L., Themudo, P., Albuquerque, T. and Correa de Sa, M.I. (2016). Detection of virulence-associated genes in pathogenic and commensal avian Escherichia coli isolates. Poult Sci., 95(7): 1646-1652.

Park, S.H., Ryu, S. and Kang, D.H. (2010) Improved selective and differential medium for isolation of Escherichia coli O157:H7. J. of Clin. Microbiol., 49(1): 405-408.

Pfaff-McDonough, S.J., Horne, S.M., Giddings, C.W., Jebert, J.O., Doetkott, C., Smith, M.H. and Nolan, L.K. (2000). Complement resistancerelated traits among Escherichia coli isolates from apparently healthy birds and birds with colibacillosis. Avian Dis., 44: 23-33.

Pourbakhsh, S.A., Dho-Moulin, M., Bree, A., Desautels, C., Martineau-Doize, B. and Fairbrother, J.B. (1997). Localization of the in vivo expression of P and F1 fimbriae in chickens experimentally inoculated with pathogenic Escherichia coli. Microb. Pathog., 22: 231-341.

Provence, D.L. and Curtiss, R. (1994). Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli Strain. Infect. and Immun., 62: 1369-1380.

Radwan, I.A.E.H., Salam, H.S.H., Abd-Alwanis, S.A.E. and Al-Sayed, M.A.Y. (2014). Frequency of some virulence associated genes among multidrug-resistant Escherichia coli isolated from septicemic broiler chicken. Int. J. of Adv. Res., 2(12): 867-874.

Raji, M.A., Adekeye, J.O, Kwaga, J.K.P. and Bale, J.O.O. (2003). In vitro and in vivo pathogenicity studies of Escherichia coli isolated from poultry in Nigeria. Israel J. of Vet. Med., 58(1): 21-28.

Raksha, R., Srinivasa, H. and Macaden, R.S. (2003). Occurrence and characterization of uropathogenic Escherichia coli in urinary tract infections. Indian J Med Microbiol., 21:102-107.

Ramirez, R.M., Almanza, Y., Garcia, S. and Heredia, N. (2009). Adherence and invasion of avian pathogenic Escherichia coli to avian tracheal epithelial cells. World. J. Microbiol. Biotechnol. 25:1019-1023.

Reingold, J., Starr, J. Maurer, M.D. and Lee M.D. (1999). Identification of a new Escherichia coli the haemolysin homolog in avian E. coli Vet. Microbiol., 66: 125-134.

Rocha, A.C.G.P., Rocha, S.L.S., Lima-Rosa, C.A.V., Souza, G.F., Moraes, H.L.S., Salle, C.F.O., Moraes, L.B. and Salle, C.T.P. (2008). Genes associated with pathogenicity of avian Escherichia coli (APEC) isolated from respiratory cases of poultry. Pesq. Vet. Bras., 28(3): 183-186.

Rodriguez-Siek, K.E., Giddings, C.W., Doetkott, C., Johnson, T.G. and Nolan. L.K. (2005). Characterizing the APEC pathotype. Vet. Res., 36: 241-256.

Roy, P., Purushothaman, V., Koteeswaran, A. and Dhillon, A.S. (2006). Isolation, Character-ization, and antimicrobial drug resistance pattern of Escherichia coli isolated from japanese quail and their environment. J. Appl. Poult. Res., 15: 442-446.

Samy A. Selim, Salwa F. Ahmed, Mohamed H. Abdel Aziz, Amira M. Zakaria, John D. Klena & Domenico Pangallo (2013). Prevalence and Characterization of Shiga-Toxin O157:H7 and Non-O157:H7 Enterohemorrhagic Escherichia coli isolated from different sources, Biotechnology & Biotechnological Equipment, 27(3): 3834-3842.

Schmidt, H., Zhang, W.L., Hemmrich, U., Jelacic, S., Brunder, W., Tarr, P.I., Dobrindt, U., Hacker, J. and Karch, H. (2001). Identification and characterization of a novel genomic island integrated at selC in locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infection and Immunity. 69: 6863-6873.

Shangkar, S.T.V., Sharma, A. and Grover, Y.P. (2010). Studies on different virulances factor of avian pathogenic Escherichia coli. Haryana Vet., 49: 45-47.

Sharada, R., Ruban, S.W. and Thiyageeswaran, M. (2010). Isolation, characterizationa and antibiotic resistance pattern of Escherichia coli isolated from poultry. Am-Eu. J. of Sci. Rec., 5(1):18-22.

Shtylla T., Kumbe, I., Cabeli, P. and Camarda, A. (2012). Virulence genes and biotype prevalence associated with avian Escherichia coli pathogenicity, in Albanian Poultry Farms. Macedonian J. of An. Sci., 2(3): 281-285.

Stathopoulos, C., Provence, D.L. and Curtiss III.R. (1999). Characterization of the avian pathogenic Escherichia coli hemagglutinin tsh, a member of the immunoglobulin a protease-type family of autotransporters. Infect. Immun., 67: 772-781.

Tivendale, K.A., Allen, J.L,, Ginns, C.A., Crabb, B.S. and Browning, G.F. (2004). Association of iss and iucA, but not tsh, with plas- mid-mediated virulence of avian pathogenic Escherichia coli. Infect Immun., 72: 6554-6560.

Vidotto, M.C., Miiller, E.E.A., de Freitas, B.J.C., Alfieri, B.A.A., Ivens B.G., Guimaraes, B. and Santosc, D.S. (1999). Virulence factors of avian Escherichia coli. Avian Dis., 34:531-538.

Yaguchi, K., Ogitani, T., Osawa, R., Kawano, M., Kokumai, N., Kaneshige, T., Noro, T., Masubuchi, K. and Shimizu, Y. (2007). Virulence factors of avian pathogenic Escherichia coli strains isolated from chickens with colisepticemia in Japan. Avian Dis., 51(3): 656-662.

Welch, R.A., Bauer, M.E., Kent, A.D., Leeds, J.A., Moayeri, M., Regassa, L.B. and Swenson, D.L. (1995). Battling against host phagocytes: thewherefore of the RTX family of toxins. Infect. Agents Dis., 4: 254-272.

Welch, R.A., Dellinger, E.P., Minshew, B. and Falkow, S. (1981). Haemolysin contributes to virulence of extra-intestinal E. coli infections. Nature. 294: 665-666.

Wibawan, I.W.T., Laemmler, C., Seleim, R.S. and Pasaribu, F.H. (1993). A haemagglutinating adhesin of group B streptococci isolated from cases of bovine mastitis mediates adherence to HeLa cells. J. Gen. Microbiol., 139: 2173-2175.

Zahid, A.A.H., AL-Mossawei, M.T.M. and Mahmood, A.B. (2016). In vitro and in vivo pathogenicity tests of local isolates apec from naturally infected broiler in Baghdad. Int. J. Adv. Res. Biol. Sci., 3(3): 89-100.

Zhao, S. Maurer, S.J., Hubert, S., De Villena, J.F., McDermott, P.F., Meng, J., Ayers, S., English, L. and Whit, D.G. (2005). Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Vet. Microbiol., 107: 215-224.

DOI: https://doi.org/10.22146/ijvs.v1i1.44793