Peran Hemaglutinin dan Hemolisin pada Escherichia coli Sorbitol-negatif Isolat Burung Puyuh pada Proses Infeksi Secara in Vitro

Khusnan Khusnan(1*), Wahyu Prihtiyantoro(2), Dwi Kusmanto(3)

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




Escherichia coli sorbitol-negative in quails cause economic loss due to the death, growth rate inhibition, decreased egg production, and increased medical treatment. Escherichia coli sorbitol-negative has many virulence factors, including hemagglutinin and hemolysin. The aim of this study is to determine the role of hemagglutinin and hemolysin in the infection process of Escherichia coli sorbitol-negative in vitro. This study was performed using 23 isolates of Escherichia coli sorbitol-negative from quails, 52.2% (12 of 23 isolates) had hemagglutinin, while 34.8% (8 out of 23 isolates) had hemolysin. Isolates with hemagglutinin were more attached to human buccal epithelial cells than isolates without hemagglutinin (P <0.05). Isolates with hemolysin were less phagocyted by macrophages compared to isolates which without hemolysin (P <0.05). Escherichia coli sorbitol-negative isolates from quails that have hemagglutinin and hemolysin are pathogenic isolates that possess the potential to cause colibasilosis and transmission between quails and other birds.



hemagglutinin; hemolisin; Escherichia coli; Sorbitol-negative; Quail

Full Text:



Abrar, M., Wibawan, I.W.T., Priosoeryanto, B.P., Soedarwanto, M. and Pasaribu, F.H. (2013). Role of Staphylococcus aureus Haemaglutinin in Adhesion Process on Udder Epithelial Cells. Jurnal Kedokteran Hewan, 7(1): 43-46.

Aderem, A. and Ulevitch, R.J. (2000). Toll-like receptors in the induction of the innate immune response. Nature, 406: 782-787.

Allan, B.J., van den Hurk, J.V. and Potter, A.A. (1993). Characterization of Escherichia coli isolated from cases of avian colibacillosis. Can. J. of Vet. Res., 57: 146-151.

Al-Saiedi, R.I.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. Poul. Sci., 13: 374-378

Ambika, M., Murthy, V., Minh-Duy, P., Peters, K.M., Nhu, N.T., Welch, R.A., Ulett, G.C., Schembri, M.A. and Sweet, M.J. (2018). Regulation of hemolysin in uropathogenic Escherichia coli fine-tunes killing of human macrophages. Virulence. (9)1: 967-980.

August 14, 2008, pp: 18-29.

August 14, 2008, pp: 18-29.

August 14, 2008, pp: 18-29.

Banu A, Kabbin J, Anand M. 2011. Extraintestinal infections due to Escherichia coli. An emerging issue. Journal of Clinical and Diagnostic Researsh 5: 486-490.

Bashar T, Rahman M, Rabbi FA, Noor R, Rahman MM. 2011. Enterotoxin Profiling and Antibiogram of Escherichia coli Isolated from Poultry Feces in Dhaka District of Bangladesh. Stamford Journal of Microbiology 1(1): 51-57.

Bohach, G., and Snyder, I. (1985). Chemical and immunological analysis of the complex structure of Escherichia coli alphahemolysin. J. Bacteriol., 164: 1071-1080.

da Rocha, A.C.G.P., da Silva, A.B., de Brito, B.G., de Souza, H.L., Pontes, A.P., Cristine, C.M., do Nascimento, V.P. and Salle, C.T.P. (2002). Virulence Factors of Avian Pathogenic Escherichia coli Isolated from Broilers from the South of Brazil. Av. Dis., 46(3): 749-752.

Dho-Moulin, M. and Fairbrother, J.M. (1999). Avian pathogenic Escherichia coli (APEC). Vet. Res., 30: 299-316.

Dobrindt, U. and Hacker, J. (2008). Targeting virulence traits: potential strategies to combat extraintestinal pathogenic E. coli infections. Curr. Opinion in Microbiol, 11: 409-413.

Edwards, R.A,, Schifferli, D.M. and Maloy, S.R. (2000). A role for Salmonella fimbriae in intraperitoneal infections. Procc. of the National Academy of Sci., 97: 1258-1262.

Emody, L., Kerenyi, M. and Nagy, G. (2003). Virulence factors of uropathogenic Escherichia coli. Int. J. Antimicrobiol Agents, 22: 529-533.

Evans, D.J., Evans, D.G., Hohne, C., Noble. MA., Haldane, E.V., Lior, H. and Young L.S. (1981). Hemolysin and K antigens in relation to serotype and hemagglutination type of Escherichia coli isolated from extraintestinal infections. J. Clin. Microbiol, 13:171-178.

Fakruddin, M., Mazumdar, R., Chowdhury, A. and Mannan, K. (2013). A preliminary study on virulence factors and antimicrobial resistance in extra-intestinal pathogenic Escherichia coli (ExPEC) in Bangladesh. Ind. J. Med. Res., 137: 988-990.

Fatima, N., Agrawal, M., Shukla, I. and Khan, P.A. (2012). Characterization of uropathogenic E. coli in relation to virulence factors. Scientific Reports 1:342. doi:10.4172/ scientificreports. 342.

Fodor, I., Catana, N. and Herman, V. (2010). Epidemiological Studies on some E. coli Strains in Broiler Chickens.UASVM. Vet. Med., 67(2): 74-76.

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

Goosney, D.L., Celli, J., Kenny, B. and Finlay, B.B. (1999). Enteropathogenic Escherichia coli Inhibits Phagocytosis. Infect. and Immunity, 67(2): 490-495.

Grover, P.S., Bareja, R., Jaryal, S.C. and Narang, V.K. (2013). Characterization of Haemolytic Escherichia coli. Int. J. of Sci. and Res. Pub., 3(2): 1-6.

Hamad, M., Al-Aalim, A., Al-Dabbagh, S. and Ali, H. (2012). Detection of organ bacterial load in quails. Proc. 6th Scient. Conf., College of Vet. Med. University of Mosul, Iraq, 23-24 May 2012, 26: 47-51.

Herlax, V., Henning, M.F., Bernascon, A.M., Goni, F.M. and Bakas, L. (2010). Health The lytic mechanism of Escherichia coli α-hemolysin associated to outer membrane vesicles Lytic action mechanism of OMVs-associated HlyA. Nat. Sci., 2: 484-492

Hogan, J.S., Todhunter, D.A., Smith, K.L, and Schoenberger, P.S. (1990). Hemagglutination and Hemolysis by Escherichia coli Isolated from Bovine Intramammary Infections. J. Daily Sci., 73: 3126-313.

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). Gen. avenue to avian. colisepticemia. MBio., 6:1-13

Italia, J.T., Rovira, H.G., Masangkay, J.S., Yoshikawa, Y., Talia, M.T., Rovira, J. Masangkay, S., Yoshikawa, Y., Perez, M.T.M., Reyes, A.W.B. and Baticados, W.N. (2012). Conventional isolation and polymerase chain reaction for detection of Escherichia coli O157:H7 from intestines of philippine bats. Veterinarski Arhiv, 82: 283-294.

Jabur, Z.A., Fakhry, S.S., Hassan, M.A. and Kadhem, B.Q. (2016). Detection of Escherichia coli O157:H7 in Food. World J. of Exp. Biosci, 4: 83-86.

Johnson, J.R. (1991). Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol, Rev., 4(1): 80-128.

Kaira, S.S. and Pai, C. (2018). Study of uropathogenic Escherichia coli with special reference to its virulence factors. Int. J. of Comm. Med. and Publ. Health, 5(1): 177-181.

Kalule, J.B., Keddy, K.H., Mark, P. and Nicol, M.P. (2018). Characterisation of STEC and other diarrheic E. coli isolated on CHROMagar™STEC at a tertiary referral hospital Cape Town. BMC Microbiol, 18: 1195-1197.

Kenneth A, 2008. Scaled quail management in Trans-Pecos

Kenneth A, 2008. Scaled quail management in Trans-Pecos

Kenneth A, 2008. Scaled quail management in Trans-Pecos

Kenneth, A. (2008). Scaled quail management in Trans-Pecos Texas. Proc Wildlife Conference, Alpine, Texas, August 14, 2008, 18-19.

Klemm, P. and Schembri, M.A. (2000). Bacterial adhesins: function and structure. Int. J. Med. Microbiol, 290: 27-35.

Knobl, T., Gomes, T.A.T., Vieira, M.A.M., Ferreira, F., Bottino, J.A. and Ferreira, A.J.P. (2006) Some adhesins of avian pathogenic Escherichia coli (APEC) isolated from septicemic poultry in Brazil. Braz. J. Microbiol, 37(3): 379-384.

Kukanur, S., Meundi, 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., Cavalli, L.S. and Brito, B.G. (2015). Avian pathogenic Escherichia coli-methods for improved diagnosis. World Poult. Sci J., doi: 10.1017/S0043933915000264

Kurl, D.N., Haataja, S. and Finne, J. (1989). Hemagglutination activities of group B, C, D and G streptococci: Demonstration of novel sugar-specific cell-binding activities in Streptococcus suis. Infect. Immun. 57(2): 384-389.

Laura, C., Rodney, R. and Welch, A. (2016). Hemolysin of uropathogenic Escherichia coli: A cloak or a dagger?, Biochimica et Biophysica ACTA. 538-545.

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. of Urol., 29: 277-281.

Mittal, S., Sharma, M. and Chaudhary, U. (2014). Study of Virulence Factors of Uropathogenic Escherichia coli and Its Antibiotic Susceptibility Pattern. Irian J. Pathol. and Microbiol, 57(1): 61-64.

Moon, G.S., Pyun, Y.R. and Kim, W.J. (2006). Expression and purification of a fusion-typed pediocin PA-1 in Escherichia coli and recovery of biologically active pediocin PA-1. Int. J. of Food Microbiol, 108(1): 136-140.

Moulin-Schouleur, M., Reperant, M., Laurent, S., Bree, A., Mignon-Grasteau, S., Germon, P., Rasschaert, D. and Schouler, C. (2007). Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J. Clin. Microbiol, 45(10): 3366-3376.

Neter, E., Bertram, L.F., Zak, D.A. and Arbesman, C.E. (1952). Studies on hemagglutination and hemolysis by Escherichia coli antisera. J. of Exp. Med., 96(1):1-15.

Nowicki, B., Truong, L., Moulds, J. and Hull. R. (1988). Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. Am. J. of Pathol, 133: 1-4.

Osman, K.M., Hessain, A.M., Abo-shama, U.H., Girh, Z.M., Kabli, S.A., Hemeg, H.A. and Moussa, I.M. (2018). An alternative approach for evaluating the phenotypic virulence factors of pathogenic Escherichia coli. Saudi J. of Biolog. Sci., 25: 195-197.

Prihtiyantoro W dan Khusnan. (2016). Karakterisasi fenotip dan genotip faktor-faktor virulensi Escherichia coli dari kasus kolibasilosis burung puyuh. Laporan Penelitian Dasar. Kopertis Wilayah V Yogyakarta, Kementerian Pendidikan dan Kebudayaan.

Radwan, I.E.H., Sayed, H.S., Soad, A.A.A. and Marwa, A.Y.A. (2014). Frequency of some virulence associated genes among multidrug-resistant Escherichia coli isolated form septicemic broiler chickens. Int. J. of Adv. Res., 2(12): 867-874.

Rodriguez-Siek, K.E., Giddings, C.W., Doetkott, C., Johnson, T.J. 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, characterization, and antimicrobial drug resistance pattern of Escherichia coli isolated from Japanese quail and their environment. J. of Appl. Poult. Res., 15: 442-446.

Salasia, S.I.O. and Laemler C. (1994). Occurrence of haemagglutinating adhesin among virulent and avirulent isolates of Streptococcus suis. Med. Sci. Res., 22: 763-764.

Salasia, S.I.O. 1994. Untersuhungen zu mutmalichen Pathogenistäts faktoren von Streptococcus suis. Veterinary Medicine Disertasi. Justus-Liebig-Universität-Gieen.

Salehi, M. and Ghanbarpour, R. (2010). Characterization of Escherichia coli Isolates from Commercial Layer Hens with Salpingitis. Am. J. of Anim. and Vet. Sci., 5 (3): 208-214.

Salit, I.E. and Gotschlich, E.C. (1977). Hemagglutination by purified type I Escherichia coli pili. J. Exp. Med., 146(5): 1169-1181.

Sekhar, M.S., Sharif, N.M. and Rao, T.S. (2017). Serotypes of sorbitol-positive shiga toxigenic Escherichia coli (SP-STEC) isolated from freshwater fish. Int. J. of Fish. and Aqua. Stud., 5(3): 503-505.

Shankar, T.V.S., Sharma, A. and Grover, Y. (2010). Studies on different virulence factors of avian pathogenic Escherichia coli. Haryana Veterinarian. 49: 45-47.

Sharma, S., Bhat, G.K. and Shenoy, S. (2007). Virulence factors and drug resistance in Escherichia coli isolated from extraintestinal infections. Ind. J. Med. Microbiol, 25: 369-373.

Stapp, J.R., Jelacic, S., Yoo-Lee, Y., Klein, E.J., Fischer, M., Clausen, C.R., Qin, X., Swerdlow, D.L. and Tarr, P.I. (2000). Comparison of Escherichia coli O157:H7 antigen setection in stool and broth cultures to that in sorbitol-MacConkey agar stool culture. J. of Clin. Microbiol, 38(9): 3404-3406.

Texas. Proc Trans-Pecos Wildlife Conference, Alpine, Texas,

Texas. Proc Trans-Pecos Wildlife Conference, Alpine, Texas,

Texas. Proc Trans-Pecos Wildlife Conference, Alpine, Texas,

Tivendale KA, Logue C.M., Kariyawasam, S., Jordan, D., Hussein, A., Li, G., Wannemuehler, Y. and Nolan, L.K. (2010). Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infection and Immunity. 78(8): 3412-3419.

Turblin V. 2009. E. coli in poultry production: Laboratory Diagnostic of Avian Pathogenic Strains (APEC). 26 September 2009. CEVA Animal Health Asia Pacific. Selangor, Malaysia.

van der Westhuizen, W.A. and Bragg, R.R. (2012). Multiplex polymerase chain reaction for screening avian pathogenic Escherichia coli for virulence genes. Av. Pathol, 41(1): 33-40.

Vidotto, M.C., Muller, E.E., Freitas, J.C., Alfieri, A.A., Guimaraes, I.G. and Santos, D.S. (1990). Virulence factors of avian Escherichia coli. Av. Dis., 34: 531-538.

Vidotto, M.C., Cacao, J.M., Goes, C.R. and Santos, D.S. (1991). Plasmid coding for aerobactin production and drug resistance is involved in virulence of Escherichia coli avian strains. Brazil J. Med. Biol. Res, 24(7): 677-685.

Welch, R.A., Dellinger, E.P., Minshew, B. and Falkow, S. (1981). Haemolysin contributes to virulence of extra-intestinal E. coli infections. Nature. 17: 665-667.

Welch, R.A. (1991) Pore-forming cytolysins of gram-negative bacteria. Mol. Microbiol, 5(3): 521-528.

Wibawan, I.W.T., Laemmler, C. and Pasaribu, F.H. (1993). A haemagglutinin adhesion of group B Streptococci isolate form cases of bovine mastitis mediated adherence to hella cell. J. Gen Microbiol, 139: 2173.

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. of Adv. Res., 3(3): 89-100.

Zhao, T., Doyle, M.P., Shere, J. and Garber L. (1995). Prevalence of enterohemorrhagic Escherichia coli O157:H7 in a survey of dairy herds. Appl. and Envir. Microbiol, 61: 1290-1293.


Article Metrics

Abstract views : 1045 | views : 1821


  • There are currently no refbacks.

Copyright (c) 2021 Jurnal Sain Veteriner

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Jurnal Sain Veteriner Indexed by


Copyright of JSV (Jurnal Sain Veteriner) ISSN 0126-0421 (print), ISSN 2407-3733 (online).

Fakultas Kedokteran Hewan, Universitas Gadjah Mada

Jl. Fauna No.2, Karangmalang, Yogyakarta

Phone: 0274-560862

Fax: 0274-560861


HP. 0895363078367

Jurnal Sain Veteriner is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.


web stats View My Stats