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Host immune responses and vaccination against avian pathogenic Escherichia coli - RETRACTED

Published online by Cambridge University Press:  13 December 2016

T. AZEEM ,
S.A. ABID ,
W. AHMAD ,
A. ASLAM ,
M.L. SOHAIL ,
S. JALEEL  and
S. UMAR
T. AZEEM
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences, Lahore, Pakistan
S.A. ABID*
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences, Lahore, Pakistan
W. AHMAD
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences, Lahore, Pakistan
A. ASLAM
Affiliation:
Department of Pathology, University of Veterinary & Animal Sciences, Lahore, Pakistan
M.L. SOHAIL
Affiliation:
Department of Clinical Medicine and Surgery, University of Veterinary and Animal Sciences, Lahore, Pakistan
S. JALEEL
Affiliation:
Department of Pathobiology, College of Veterinary and Animal Sciences, Jhang, Pakistan
S. UMAR
Affiliation:
Department of Pathobiology, PMAS Arid Agriculture University, Rawalpindi, Pakistan National Veterinary School of Toulouse, France
*
Corresponding author: [email protected]
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Abstract

Avian pathogenic Escherichia coli (APEC) is one of the most economically damaging diseases affecting the poultry industry. This group of extra-intestinal E. coli causes a variety of clinical conditions including air-sacculitis and cellulitis. The economic impact of APEC is mainly due to mortality, slower growth rates and carcass downgrading. In commercial broiler operations, APEC infections are controlled indirectly by vaccination against other respiratory diseases and minimising stress conditions, and directly by administration of antimicrobial agents to suppress symptoms in infected flocks. Several studies have demonstrated that the most common virulence factors studied in APEC are rarely present in the same isolate, showing that APEC strains constitute a heterogeneous group. Different isolates may harbour different associations of virulence factors, each able to induce colibacillosis. Despite its economical relevance, the pathogenesis of colibacillosis is poorly understood. The O antigen, a component of the surface lipopolysaccharide, has been identified as a promising vaccine target. With the availability of a novel bioconjugation technology it is expected that multivalent O antigen conjugate vaccines can be produced on an industrial scale. Despite the potential for developing an efficacious vaccine to combat this economically important poultry disease, several obstacles hinder such efforts. These include cost, vaccine delivery method and timing of vaccination. The present discusses current knowledge on APEC virulence, host response to infection and various attempts to develop an effective vaccine

Keywords

avian pathogenic E.colivirulencevaccinevaccinationchicken
Type
Reviews
Information
World's Poultry Science Journal , Volume 73 , Issue 1 , March 2017 , pp. 29 - 44
Copyright
Copyright © World's Poultry Science Association 2016 

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References

ANTÃO, E.-M., WIELER, L.H. and EWERS, C. (2009) Adhesive threads of extraintestinal pathogenic Escherichia coli. Gut pathogens 1: 1-20.Google Scholar
ARP, L. (1980) Consequences of active or passive immunisation of turkeys against Escherichia coli O78. Avian Diseases 24: 808-815.Google Scholar
BARNS, H., NOLAN, L. and VAILLANCOURT, J. (2008) Colibacillosis, in: SAIF, Y.M., FADLEY, A.M., GLISSON, J.R., MCDOUGALD, L.R., NOLAN, L.K. & SWAYNE, D.E. (Eds) Diseases of Poultry, pp. 691-737 (Blackwell Publishing, USA).Google Scholar
BERTRAND, N., HOULE, S., LEBIHAN, G., POIRIER, É., DOZOIS, C.M. and HAREL, J. (2010) Increased pho regulon activation correlates with decreased virulence of an avian pathogenic Escherichia coli O78 strain. Infection and immunity 78: 5324-5331.Google Scholar
CAZA, M., LÉPINE, F., MILOT, S. and DOZOIS, C. M. (2008) Specific roles of the irobcden genes in virulence of an avian pathogenic Escherichia coli O78 strain and in production of salmochelins. Infection and Immunity 76: 3539-3549.Google Scholar
CHOUIKHA, I., GERMON, P., BRÉE, A., GILOT, P., MOULIN-SCHOULEUR, M. and SCHOULER, C. (2006) A selc-associated genomic island of the extraintestinal avian pathogenic escherichia coli strain ben2908 is involved in carbohydrate uptake and virulence. Journal of Bacteriology 188: 977-987.Google Scholar
CVMP (2012) Committee for medicinal products for veterinary use assessment report for poulvace. Coli (emea/v/c/002007) Journal, (European Medicines Agency, London).Google Scholar
DE PAIVA, J.B., LEITE, J.L., DA SILVA, L.P.M., ROJAS, T.C.G., DE PACE, F., CONCEIÇÃO, R.A., SPERANDIO, V. and DA SILVEIRA, W.D. (2015) Influence of the major nitrite transporter nirc on the virulence of a swollen head syndrome avian pathogenic E. coli (apec) strain. Veterinary Microbiology 175: 123-131.Google Scholar
DEB, J. and HARRY, E. (1978) Laboratory trials with inactivated vaccines against Escherichia coli (O2: K1) infection in fowls. Research in Veterinary Science 24: 308-313.Google Scholar
DHO-MOULIN, M. and FAIRBROTHER, J.M. (1999) Avian pathogenic Escherichia coli (apec). Veterinary Research 30: 299-316.Google Scholar
DOZOIS, C.M., DHO-MOULIN, M., BRÉE, A., FAIRBROTHER, J. M., DESAUTELS, C. and CURTISS, R. (2000) Relationship between the tsh autotransporter and pathogenicity of avian Escherichia coli and localisation and analysis of the tsh genetic region. Infection and Immunity 68: 4145-4154.Google Scholar
DZIVA, F., HAUSER, H., CONNOR, T.R., VAN DIEMEN, P.M., PRESCOTT, G., LANGRIDGE, G.C., ECKERT, S., CHAUDHURI, R.R., EWERS, C. and MELLATA, M. (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.Google Scholar
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 Pathology 37: 355-366.Google Scholar
EMERY, D.A., STRAUB, D.E., HUISINGA, R. and CARLSON, B.A. (2000) Active immunisation using a siderophore receptor protein. Publication. U.S. Patent (6,027,736). U.S.A.Google Scholar
EWERS, C., ANTÃO, E.-M., DIEHL, I., PHILIPP, H.-C. and WIELER, L.H. (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.Google Scholar
EWERS, C., JANßEN, T., KIEßLING, S., PHILIPP, H.-C. and WIELER, L.H. (2004) Molecular epidemiology of avian pathogenic Escherichia coli (apec) isolated from colisepticemia in poultry. Veterinary Microbiology 104: 91-101.Google Scholar
FELDMAN, M.F., WACKER, M., HERNANDEZ, M., HITCHEN, P.G., MAROLDA, C.L., KOWARIK, M., MORRIS, H.R., DELL, A., VALVANO, M.A. and AEBI, M. (2005) Engineering n-linked protein glycosylation with diverse o antigen lipopolysaccharide structures in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 102: 3016-3021.Google Scholar
FILHO, T.F., FÁVARO, C. (Jr), INGBERMAN, M., BEIRÃO, B.C., INOUE, A., GOMES, L. and CARON, L.F. (2013) Effect of spray Escherichia coli vaccine on the immunity of poultry. Avian Diseases 57: 671-676.Google Scholar
FLÉCHARD, M., CORTES, M.A., RÉPÉRANT, M. and GERMON, P. (2012) New role for the ibea gene in H2O2 stress resistance of Escherichia coli. Journal ofBacteriology 194: 4550-4560.Google Scholar
FROMMER, A., FREIDLIN, P., BOCK, R.R., LEITNER, G., CHAFFER, M. and HELLER, E. (1994) Experimental vaccination of young chickens with a live, non-pathogenic strain of Escherichia coli. Avian Pathology 23: 425-433.Google Scholar
GAO, Q., JIA, X., WANG, X., XIONG, L., GAO, S. and LIU, X. (2015a) The avian pathogenic Escherichia coli O2 strain e058 carrying the defined aerobactin-defective iucd or iucdiuta mutation is less virulent in the chicken. Infection, Genetics and Evolution 30: 267-277.Google Scholar
GAO, Q., WANG, X., 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 Microbiology 12: 1.Google Scholar
GAO, Q., YE, Z., WANG, X., MU, X., GAO, S. and LIU, X. (2015b) Rsta is required for the virulence of an avian pathogenic Escherichia coli O2 strain e058. Infection, Genetics and Evolution 29: 180-188.Google Scholar
GROSS, W. (1957) Pathological changes of an escherichia coli infection in chickens and turkeys. American Journal of Veterinary Research 18: 724-730.Google Scholar
GUABIRABA, R. and SCHOULER, C. (2015) Avian colibacillosis: Still many black holes. FEMS Microbiology Letters 362: fnv118. doi: 10.1093/femsle/fnv118.Google Scholar
GHUNAIM, H., ABU-MADI, M.A. and KARIYAWASAM, S. (2014) Advances in vaccination against avian pathogenic Escherichia coli respiratory disease: Potentials and limitations Veterinary Microbiology 172: 13-22.Google Scholar
HERREN, C.D., MITRA, A., PALANIYANDI, S.K., COLEMAN, A., ELANKUMARAN, S. and MUKHOPADHYAY, S. (2006) The bara-uvry two-component system regulates virulence in avian pathogenic Escherichia coli O78: K80: H9. Infection and Immunity 74: 4900-4909.Google Scholar
HORN, F., CORRÊA, A.M.R., BARBIERI, N.L., GLODDE, S., WEYRAUCH, K.D., KASPERS, B., DRIEMEIER, D., EWERS, C. and WIELER, L.H. (2012) Infections with avian pathogenic and faecal Escherichia coli strains display similar lung histopathology and macrophage apoptosis. PloS One 7: e41031.Google Scholar
HORNE, S.M., PFAFF-MCDONOUGH, S.J., GIDDINGS, C.W. and NOLAN, L.K. (2000) Cloning and sequencing of the iss gene from a virulent avian Escherichia coli. Avian Diseases 44: 179-184.Google Scholar
IDESES, D., GOPHNA, U., PAITAN, Y., CHAUDHURI, R.R., PALLEN, M.J. and RON, E.Z. (2005) A degenerate type iii secretion system from septicemic Escherichia coli contributes to pathogenesis. Journal of Bacteriology 187: 8164-8171.Google Scholar
JANSEN, C.A., VAN DE HAAR, P.M., VAN HAARLEM, D., VAN KOOTEN, P., DE WIT, S., VAN EDEN, W., VIERTLBÖCK, B.C., GÖBEL, T.W. and VERVELDE, L. (2010) Identification of new populations of chicken natural killer (nk) cells. Developmental & Comparative Immunology 34: 759-767.Google Scholar
KARIYAWASAM, S. and NOLAN, L.K. (2009) Pap mutant of avian pathogenic Escherichia coli O1, an O1: K1: H7 strain, is attenuated in vivo. Avian Diseases 53: 255-260.Google Scholar
KARIYAWASAM, S., WILKIE, B. and GYLES, C. (2004a) Construction, characterisation, and evaluation of the vaccine potential of three genetically defined mutants of avian pathogenic Escherichia coli. Avian Diseases 48: 287-299.Google Scholar
KARIYAWASAM, S., WILKIE, B. and GYLES, C. (2004b) Resistance of broiler chickens to Escherichia coli respiratory tract infection induced by passively transferred egg-yolk antibodies. Veterinary Microbiology 98: 273-284.Google Scholar
KARIYAWASAM, S., WILKIE, B., HUNTER, D. and GYLES, C. (2002) Systemic and mucosal antibody responses to selected cell surface antigens of avian pathogenic escherichia coli in experimentally infected chickens. Avian Diseases 46: 668-678.Google Scholar
KEESTRA, A.M., DE ZOETE, M.R., BOUWMAN, L.I. and VAN PUTTEN, J.P. (2010) Chicken tlr21 is an innate cpg DNA receptor distinct from mammalian tlr9. The Journal of Immunology 185: 460-467.Google Scholar
KOGUT, M.H., CHIANG, H.-I., SWAGGERTY, C.L., PEVZNER, I.Y. and ZHOU, H. (2015) Gene expression analysis of Toll-like receptor pathways in heterophils from genetic chicken lines that differ in their susceptibility to salmonella enteritidis. Fronteirs in Genetic 3: 1-10, doi: 10.3389/fgene.2012.00121Google Scholar
KOGUT, M.H., GENOVESE, K.J. and LOWRY, V.K. (2001) Differential activation of signal transduction pathways mediating phagocytosis, oxidative burst, and degranulation by chicken heterophils in response to stimulation with opsonised salmonella enteritidis. Inflammation 25: 7-15.Google Scholar
KOGUT, M.H., ROTHWELL, L. and KAISER, P. (2003) Differential regulation of cytokine gene expression by avian heterophils during receptor-mediated phagocytosis of opsonised and nonopsonised salmonella enteritidis. Journal of Interferon & Cytokine Research 23: 319-327.Google Scholar
KWAGA, J.K., ALLAN, B.J., VAN DER HURK, J.V., SEIDA, H. and POTTER, A.A. (1994) A carAB mutant of avian pathogenic Escherichia coli serogroup O2 is attenuated and effective as a live oral vaccine against colibacillosis in turkeys. Infection and Immunity 62: 3766-3772.Google Scholar
LA RAGIONE, R., COOLEY, W. and WOODWARD, M.J. (2000) The role of fimbriae and flagella in the adherence of avian strains of Escherichia coli O78: K80 to tissue culture cells and tracheal and gut explants. Journal of Medical Microbiology 49: 327-338.Google Scholar
LAMARCHE, M.G., DOZOIS, C.M., DAIGLE, F., CAZA, M., CURTISS, R., DUBREUIL, J.D. and HAREL, J. (2005) Inactivation of the pst system reduces the virulence of an avian pathogenic Escherichia coli O78 strain. Infection and Immunity 73: 4138-4145.Google Scholar
LANDMAN, W., BUTER, G., DIJKMAN, R. and VAN ECK, J. (2014) Molecular typing of avian pathogenic escherichia coli colonies originating from outbreaks of E. Coli peritonitis syndrome in chicken flocks. Avian Pathology 43: 345-356.Google Scholar
LANDMAN, W., HEUVELINK, A. and VAN ECK, J. (2013) Reproduction of the escherichia coli peritonitis syndrome in laying hens. AvianPathology 42: 157-162.Google Scholar
LI, G., EWERS, C., LATURNUS, C., DIEHL, I., ALT, K., DAI, J., ANTAO, E.-M., SCHNETZ, K. and WIELER, L.H. (2008) Characterisation of a yjjq mutant of avian pathogenic Escherichia coli (apec). Microbiology 154: 1082-1093.Google Scholar
LI, G., FENG, Y., KARIYAWASAM, S., TIVENDALE, K.A., WANNEMUEHLER, Y., ZHOU, F., LOGUE, C.M., MILLER, C.L. and NOLAN, L.K. (2010) Aata is a novel autotransporter and virulence factor of avian pathogenic Escherichia coli. Infection and Immunity 78: 898-906.Google Scholar
LOWENTHAL, J., BEAN, A. and KOGUT, M. (2013) What's so special about chicken immunology? Developmental and Comparative Immunology 41: 307-309Google Scholar
LYMBEROPOULOS, M.H., HOULE, S., DAIGLE, F., LÉVEILLÉ, S., BRÉE, A., MOULIN-SCHOULEUR, M., JOHNSON, J.R. and DOZOIS, C.M. (2006) Characterisation of stg fimbriae from an avian pathogenic Escherichia coli O78: K80 strain and assessment of their contribution to colonisation of the chicken respiratory tract. Journal of Bacteriology 188: 6449-6459.Google Scholar
LYNNE, A.M., FOLEY, S.L. and NOLAN, L.K. (2006) Immune response to recombinant Escherichia coli iss protein in poultry. Avian Diseases 50: 273-276.Google Scholar
LYNNE, A.M., KARIYAWASAM, S., WANNEMUEHLER, Y., JOHNSON, T.J., JOHNSON, S.J., SINHA, A.S., LYNNE, D.K., MOON, H.W., JORDAN, D.M. and LOGUE, C.M. (2012) Recombinant iss as a potential vaccine for avian colibacillosis. Avian Disease 56: 192-199.Google Scholar
MA, J., BAO, Y., SUN, M., DONG, W., PAN, Z., ZHANG, W., LU, C. and YAO, H. (2014) Two functional type vi secretion systems in avian pathogenic Escherichia coli are involved in different pathogenic pathways. Infection and immunity 82: 3867-3879.Google Scholar
MELAMED, D., LEITNER, G. and HELLER, E.D. (1991) A vaccine against avian colibacillosis based on ultrasonic inactivation of Escherichia coli. Avian Diseases 35: 17-22.Google Scholar
MELLATA, M., AMEISS, K., MO, H. and CURTISS, R. (2010) Characterisation of the contribution to virulence of three large plasmids of avian pathogenic Escherichia coli χ7122 (O78: K80: H9). Infection and Immunity 78: 1528-1541.Google Scholar
MELLATA, M., DHO-MOULIN, M., DOZOIS, C.M., CURTISS III, R., BROWN, P.K., ARNÉ, P., BRÉE, A., DESAUTELS, C. and FAIRBROTHER, J.M. (2003) Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infection and Immunity 71: 536-540.Google Scholar
MU, X., HUAN, H., XU, H., GAO, Q., XIONG, L., GAO, R., GAO, S. and LIU, X. (2013) The transfer-messenger rna-small protein b system plays a role in avian pathogenic Escherichia coli pathogenicity. Journal of Bacteriology 195: 5064-5071.Google Scholar
NIVAS, S. and POMEROY, B. (1985) Attenuation of pathogenic escherichia coli using acridine orange. Abstract. Proceedings of the Proc. Conference of Research Workers in Animal Disease, Chicago, IL.Google Scholar
NAVEH, M.W. and RON, E.Z. (1985) Vaccination against colisepticemia in chickens. In: 35th Western Poultry Disease Conference, Davis, CA,Google Scholar
NOLAN, L., HORNE, S., GIDDINGS, C., FOLEY, S., JOHNSON, T., LYNNE, A. and SKYBERG, J. (2003) Resistance to serum complement, iss, and virulence of avian escherichia coli. Veterinary Research Communications 27: 101-110.Google Scholar
PARREIRA, V. and GYLES, C. (2003) A novel pathogenicity island integrated adjacent to the thrw trna gene of avian pathogenic Escherichia coli encodes a vacuolating autotransporter toxin. Infection and Immunity 71: 5087-5096.Google Scholar
PEIGHAMBARI, S., HUNTER, D., SHEWEN, P. and GYLES, C. (2002) Safety, immunogenicity, and efficacy of two Escherichia coli cya crp mutants as vaccines for broilers. Avian Diseases 46: 287-297.Google Scholar
POOLMAN, J.T. and WACKER, M. (2015) Extra-intestinal pathogenic Escherichia coli (expec), a common human pathogen: Challenges for vaccine development and progress in the field. Journal of Infectious Diseases 213: 6-13.Google Scholar
RODRIGUEZ-SIEK, K.E., GIDDINGS, C.W., DOETKOTT, C., JOHNSON, T.J. and NOLAN, L.K. (2005) Characterizing the apec pathotype. Veterinary Research 36: 241-256.Google Scholar
ROLAND, K., CURTISS III, R. and SIZEMORE, D. (1999) Construction and evaluation of a cya crp Salmonella typhimurium strain expressing avian pathogenic escherichia coli o78 lps as a vaccine to prevent airsacculitis in chickens. Avian Diseases 43: 429-441.Google Scholar
ROY, C.R. and MOCARSKI, E.S. (2007) Pathogen subversion of cell-intrinsic innate immunity. Nature Immunology 8: 1179-1187.Google Scholar
SABRI, M., CAZA, M., PROULX, J., LYMBEROPOULOS, M.H., BRÉE, A., MOULIN-SCHOULEUR, M., CURTISS, R. and DOZOIS, C.M. (2008) Contribution of the sitabcd, mnth, and feob metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain χ7122. Infection and Immunity 76: 601-611.Google Scholar
SADEYEN, J.-R., WU, Z., DAVIES, H., VAN DIEMEN, P.M., MILICIC, A., LA RAGIONE, R.M., KAISER, P., STEVENS, M.P. and DZIVA, F. (2015) Immune responses associated with homologous protection conferred by commercial vaccines for control of avian pathogenic Escherichia coli in turkeys. Veterinary Research 46: 1-5. DOI: 10.1186/s13567-014-0132-5.Google Scholar
SALEHI, T.Z., TABATABAEI, S., KARIMI, V., FASAEI, B.N., DERAKHSHANDEH, A. and JAHROMI, O.A.N. (2012) Assessment of immunity against avian colibacillosis induced by an aroa mutant containing increased serum survival gene in broilers. Brazilian Journal of Microbiology 43: 363-370.Google Scholar
SANDFORD, E.E., ORR, M., SHELBY, M., LI, X., ZHOU, H., JOHNSON, T.J., KARIYAWASAM, S., LIU, P., NOLAN, L.K. and LAMONT, S.J. (2012) Leukocyte transcriptome from chickens infected with avian pathogenic Escherichia coli identifies pathways associated with resistance. Results in Immunology 2: 44-53.Google Scholar
SPERLING, B., VIERTLBOECK, B.C. and GÖBEL, T.W. (2015) Chicken cd300a homolog is found on b lymphocytes, various leukocytes populations and binds to phospholipids. Developmental & Comparative Immunology 50: 121-128.Google Scholar
STACY, A.K., MITCHELL, N.M., MADDUX, J.T., MIGUEL, A., DURÁN, L., GIRÓN, J.A., CURTISS 3RD, R. and MELLATA, M. (2014) Evaluation of the prevalence and production of Escherichia coli common pilus among avian pathogenic E. coli and its role in virulence. PloS One 9: e86565.Google Scholar
STRAUB, C., NEULEN, M.-L., SPERLING, B., WINDAU, K., ZECHMANN, M., JANSEN, C.A., VIERTLBOECK, B.C. and GÖBEL, T.W. (2013) Chicken nk cell receptors. Developmental & Comparative Immunology 41: 324-333.Google Scholar
UMAR, S., SHAH, M.A.A. and MUNIR, M.T. (2015) Infectious bronchitis virus: Evolution and vaccination. World's Poultry Science Journal 72: 49-60.Google Scholar
UMAR, S., SUBHAN, S., AZAM, T., MUNIR, M.T. and SHAH, M.A.A. (2017a) Mycoplasmosis in poultry: update on diagnosis and preventive measures. World's Poultry Science Journal 73: xx-xx (accepted).Google Scholar
UMAR, S., MUNIR, M.T., AHSAN, U., RAZA, I., CHOWDHURY, M.R., AHMED, Z. and SHAH, M.A.A. (2017b) Immunosuppressive interactions of viral diseases in poultry. World's Poultry Science Journal 73: xx-xx (accepted).Google Scholar
UMAR, S., SABIR, H., AHMED, A. and SUBHAN, S. (2016) Avian metapneumovirus infection in poultry: an updated review. World's Poultry Science Journal 72 (4): 833-846.Google Scholar
VANDEMAELE, F., BLEYEN, N., ABUABOUD, O., VANDERMEER, E., JACOBS, A. and GODDEERIS, B.M. (2006) Immunisation with the biologically active lectin domain of papgii induces strong adhesion-inhibiting antibody responses but not protection against avian pathogenic Escherichia coli. Avian Pathology 35: 238-249.Google Scholar
WONG, G.K.-S., LIU, B., WANG, J., ZHANG, Y., YANG, X., ZHANG, Z., MENG, Q., ZHOU, J., LI, D. and ZHANG, J. (2004) A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432: 717-722.Google Scholar
ZHUANG, Q.-Y., WANG, S.-C., LI, J.-P., LIU, D., LIU, S., JIANG, W.-M. and CHEN, J.-M. (2014) A clinical survey of common avian infectious diseases in china. Avian Diseases 58: 297-302.Google Scholar