Evaluation of the timing of the Escherichia coli co-infection on pathogenecity of H9N2 avian influenza virus in broiler chickens

Document Type : Full paper (Original article)

Authors

1 Avian Diseases Research Center, School of Veterinary Medicine, Shiraz University, Shiraz, Iran; Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

2 Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

3 Graduated from School of Veterinary Medicine, Shiraz University, Shiraz, Iran

4 Graduated from School of Veterinary Medicine, Shiraz University, Shiraz, Iran; Department of Pathobiology, School of Veterinary Medicine, Lorestan University, Khorramabad, Iran

Abstract

Bacterial co-infections can probably influence the pathogenicity of H9N2 low pathogenic avian influenza virus (AIV). This study aimed to evaluate the effect of exposure time to Escherichia coli (O:2) on the pathogenicity of H9N2 AIV in broiler chickens. Three hundred and sixty broiler chickens were randomly allocated to six equal groups. At the age of 26 days, all chicks except groups 5 and 6 were inoculated intra-nasally with H9N2 virus. At the same time, the birds in groups 1 and 5 were infected with E. coli via spray route. Birds in groups 3 and 2 were infected with E. coli three days prior to and three days post AI challenge, respectively. Mortality rates, clinical signs, gross and microscopic lesions, excretion and duration of virus shedding in faecal and tracheal samples and seroconversion to H9N2 virus were assessed in the challenged groups. The highest mortality rate was observed in chickens inoculated with H9N2 followed by E. coli. The most severe clinical signs, gross lesions, mortality rate and virus detection were observed at day 6 post challenge (PC) in birds of group 2, while the duration of virus shedding was longer in group 3 (E. coli followed by H9N2) than other groups. In conclusion, E. coli infection prior to, after or concurrently with H9N2 virus infection could exacerbate the adverse effects of the virus. Our results indicate that E. coli and H9N2 together can mutually exacerbate the condition of either disease in broiler chicks as compared to single infected birds.

Keywords


Alexander, DJ (2002). Report on avian influenza in the eastern hemisphere during 1997-2002. Avian Dis., 47: 792-797.
Azizpour, A; Goudarzi, H; Banani, M; Nouri, A; Momayez, M; Hablolvarid, MH; Abdoshah, M and Bijanzade, P (2013). Evaluation of clinical signs, gross lesions and antibody response in experimental of individual and co-infection of H9N2 avian influenza and Ornithbacterium rhinotracheale in SPF chickens. Eur. J. Exp. Biol., 3: 503-507.
Bano, S; Naeem, K and Malik, SA (2003). Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. Avian Dis., 47: 817-822.
Barbour, EK; Mastori, FA; Abdel Nour, AM; Shaib, HA; Jaber, LS; Yaghi, RH; Sabra, A; Sleiman, FT; Sawaya, RK; Niedzwieck, A; Tayeb, IT; Kassaify, ZG; Rath, M; Harakeh, S and Barbour, KE (2009). Standardization of a new model of H9N2/E.coli challenge in broilers in the Lebanon. Vet. Ital., 45: 317-322.
Dobrindt, U (2005). (Patho-) Genomics of Escherichia coli. Int. J. Med. Microbiol., 295: 357-371.
Ganapathy, K; Salamat, MH; Lee, CC and Johara, MY (2000). Concurrent occurrence of salmonellosis, coli-bacillosis and histomoniasis in a broiler flock fed with antibiotic-free commercial feed. Avian Pathol., 29: 639-642.
Gharaibeh, S (2008). Pathogenicity of an avian influenza virus serotype H9N2 in chickens. Avian Dis., 52: 106-110.
Ginns, CA; Browning, GF; Benham, ML and Whithear, KG (1998). Development and application of an aerosol challenge method for reproduction of avian colibacillosis. Avian Pathol., 27: 505-511.
Goudarzi, H; Azizpour, A; Banani, M; Nouri, A; Charkhkar, S; Momayez, R; Hablolvarid, MH; Bijanzad, P; Mirzaei, GHR; Eshratabadi, F and Mahmoodzadeh, M (2014). Study on clinical signs and gross lesions due to individually and concurrent experimental infection of H9N2 avian influenza and Ornithobacterium rhinotracheale in SPF chickens. J. Comp. Pathol., 10: 1077-1086.
Haghighat-Jahromi, M; Asasi, K; Nili, H; Dadras, H and Shooshtari, AH (2008). Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. Arch. Virol., 153: 651-655.
Jiang, X; Zhang, M; Ding, Y; Yao, I; Chen, H; Zhu, D and Muramata, M (1998). Escherichia coli prlc gene encodes a trypsin-like proteinase regulating the cell cycle. J. Biochem., 124: 980-985.
Karimi-Madab, M; Ansari-Lari, M; Asasi, K and Nili, H (2010). Risk factors for detection of bronchial cast, most frequently seen in endemic H9N2 avian influenza infection in poultry flocks in Iran. Prev. Vet. Med., 95: 275-280.
Kato, M; Irisawa, T; Ohtani, M and Muramatu, M (1992). Purification and characterization of proteinase in a trypsin-like proteinase, in Escherichia coli. Eur. J. Biochem., 210: 1007-1014.
Kishida, N; Eto, M; Sunaga, Y and Kida, H (2004). Enhancement of pathogenicity of H9N2 influenza A virus isolated from chicken in China by co-infection with Staphylococcus aureus and Haemophilus paragallinarum. Int. Congr. Ser., 1263: 481-485.
Lee, MS; Chang, PC; Shien, JH; Cheng, MC and Sheih, HK (2001). Identification and subtyping of avian influenza viruses by reverse transcription-PCR. J. Virol. Methods. 97: 13-22.
Lee, B; Robinson, KM; McHugh, KJ; Scheller, EV; Mandalapu, S; Chen, C; Di, YP; Clay, ME; Enelow, RI; Dubin, PJ and Alcorn, JF (2015). Influenza-induced type I interferon suppressed the immunity in mice. Am. J. Physiol. Lung. Cell. Mol. Physiol., 309: 158-167.
Mészáros, J and Stipkovits, L (1967a). Spread of Escherichia coli infection in poultry flocks infected with Mycoplasma gallisepticum. Acta Vet. Acad. Sci. Hung., 17: 161-167.
Mészáros, J and Stipkovits, L (1967b). Study of the development of Escherichia coli bacteremia in artificially infected chickens. Acta Vet. Acad. Sci. Hung., 17: 169-177.
Nakamura, K; Imada, Y and Maeda, M (1986). Lympho-cytic depletion of bursa of fibricius and thymus in chickens inoculated with Escherichia coli. Vet. Pathol., 23: 712-717.
Nili, H and Asasi, K (2003). Avian influenza (H9N2) outbreak in Iran. Avian Dis., 47: 828-831.
Pan, Q; Liu, A; Zhang, F; Ling, Y; Ou, C; Hou, N and He, C (2012). Co-infection of broiler with Ornithobacterium rhinotracheale and H9N2 avian influenza virus. BMC. Vet. Res., 8: 104-110.
Pedersen, JC (2008). Hemagglutination-inhibition test for avian influenza virus subtype identification and the detection and quantitation of serum antibodies to the avian influenza virus. Methods Mol. Biol., 436: 53-66.
Reed, LJ and Muench, H (1938). A simple method for estimating fifty percent endpoints. Am. J. Hyg., 27: 493-497.
Seifi, S; Asasi, K and Mohammadi, A (2012). An
experimental study on broiler chicken co-infected with the specimens containing avian influenza (H9 subtype) and infectious bronchitis (4/91 strain) viruses. Iran. J. Vet. Res., 13: 138-142.
Śmietanka, K; Minta, Z; Świętoń, E; Olszewska, M; Jóźwiak, M; Domańska-Blicharz, K; Wyrostek, K; Tomczyk, G and Pikuła, A (2014). Avian influenza H9N2 subtype in Poland – characterization of the isolates and evidence of concomitant infections. Avian Pathol., 43: 427-436.
Stipkovits, L; Glavits, R; Palfi, V; Beres, A; Egyed, L; Denes, B; Somogyi, M and Szathmary, S (2012). Pathologic lesions caused by coinfection of Mycoplasma gallisepticum and H3N8 low pathogenic avian influenza virus in chickens. Vet. Pathol., 49: 273-283.
Tajmanesh, S; Toroghi, R; Momayez, R and Pourbakhsh, SA (2006). Establishment of RT-PCR for detection of avian influenza virus (H9N2) in field cases compared to virus isolation method. Arch. Razi. Inst., 97: 111-116.
Tavakkoli, H; Asasi, K and Mohammadi, A (2009). Evidence that infectious bronchitis vaccine increases H9N2 avian influenza virus replication in broiler chicks. Online J. Vet. Res., 13: 37-47.
Umar, S; Younus, M; Rehmanb, MU; Aslam, A; Abdullah Shah, MA; Munir, MT; Hussain, S; Iqbald, F; Fiazd, M and Ullahe, S (2015). Role of aflatoxin toxicity on transmissibility and pathogenicity of H9N2 avian influenza virus in turkeys. Avian Pathol., 44: 305-310.
Vasfi-Marandi, M; Pazani, J; Ashrafi, H; Marjanmehr, SH and Ghods, F (2007). Evaluation of the pathogenicity of A/chicken/Iran/ZMT-173/99 (H9N2) strain of avian influenza virus in serologically Mycoplasma gallisepticum positive and negative broiler chickens. Iranian J. of Virol., 1: 20-27.