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Acute phase proteins: a review of their function, behaviour and measurement in chickens

Published online by Cambridge University Press:  27 February 2014

E.L. O'REILLY  and
P.D. ECKERSALL
E.L. O'REILLY*
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Bearsden Road, Glasgow, G61 1QH, United Kingdom
P.D. ECKERSALL
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Bearsden Road, Glasgow, G61 1QH, United Kingdom
*
Corresponding author: e.o'[email protected]
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Abstract

This review brings together and consolidates the large amount of research on acute phase proteins (APPs) that has been undertaken in chickens. Acute phase proteins are secreted from the liver as a result of inflammation or infection that can be measured in plasma. They have been well-characterised in other farm animal species and have been measured in a wide variety of poultry research areas. The acceleration in chicken APP research is in response to increased interest in ways the immune responses of the chicken can be measured and compared during infection or environmental or nutritional changes. All APPs that have been identified and characterised in chickens are described in the following review and their responses during infection discussed. The APPs are tabulated with basal values and classification to provide a comparative and useful reference. The ways APPs can be measured in chickens and the assays available are also described. This review will detail the functions of the positive APPs in chickens and their behaviour during an APR.

Keywords

chickenacute phase proteinbiomarkerinfection
Type
Review Article
Information
World's Poultry Science Journal , Volume 70 , Issue 1 , March 2014 , pp. 27 - 44
Copyright
Copyright © World's Poultry Science Association 2014 

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References

ABERNETHY, T. and AVERY, O. (1941) The occurrence during acute infections of a protein not normally present in the blood. The Journal of Experimental Medicine 73: 173-182.CrossRefGoogle Scholar
ADLER, K.L., PENG, P.H., PENG, R.K. and KLASING, K.C. (2001) The Kinetics of Hemopexin and α1-Acid Glycoprotein Levels Induced by Injection of Inflammatory Agents in Chickens Inflammatory Agents in Chickens. Avian Diseases 45: 289-296.Google Scholar
AGUILERA, O., QUIROS, L.M. and FIERRO, J.F. (2003) Transferrins selectively cause ion efflux through bacterial and artificial membranes. FEBS Letters 548: 5-10.Google Scholar
ALASONYALILAR, A., SEVIMLI, A., MISIRLIOGLU, D. and UGUZ, C. (2006) Chronic amyloid arthropathy and increased serum amyloid levels in brown layers. The Bulletin of the Veterinary Institute in Pulawy 50: 557-560.Google Scholar
AMRANI, D.L., MAUZY-MELITZ, D. and MOSESSON, M.W. (1986) Effect of hepatocyte-stimulating factor and glucocorticoids on plasma fibronectin levels. The Biochemical Journal 238: 365-371.CrossRefGoogle ScholarPubMed
ASCENZI, P., BOCEDI, A., VISCA, P., ALTRUDA, F., TOLOSANO, E., BERINGHELLI, T. and FASANO, M. (2005) Hemoglobin and heme scavenging. IUBMB life 57: 749-759.CrossRefGoogle ScholarPubMed
BARNES, D.M., SONG, Z., KLASING, K.C. and BOTTJE, W. (2002) Protein metabolism during an acute phase response in chickens. Amino acids 22: 15-26.Google Scholar
BUTLER, E.J., CURTIS, M.J., HARRY, E.G. and DEB, J.R. (1972) Effects of Escherichia coli endotoxins on plasma para-phenylenediamine oxidase (caeruloplasmin) activity in the domestic fowl. Journal of Comparative Pathology 82: 299-306.Google Scholar
BUYSE, J., SWENNEN, Q., NIEWOLD, T.A., KLASING, K.C., JANSSENS, G.P.J., BAUMGARTNER, M. and GODDEERIS, B. (2007) Dietary L-carnitine supplementation enhances the lipopolysaccharide-induced acute phase protein response in broiler chickens. Veterinary Immunology and Immunopathology 118: 154-159.Google Scholar
CECILIANI, F. and POCACQUA, V. (2007) The acute phase protein 1-acid glycoprotein: a model for altered glycosylation during diseases. Current Protein and Peptide Science 8: 91-108.CrossRefGoogle Scholar
CERON, J.J., ECKERSALL, P.D. and MARTÝNEZ-SUBIELA, S. (2005) Acute phase proteins in dogs and cats: current knowledge and future perspectives. Veterinary Clinical Pathology 34: 85-99.CrossRefGoogle ScholarPubMed
CHAMANZA, R., TOUSSAINT, M.J.M., VAN EDEREN, A.M., VAN VEEN, L., HULSKAMP-KOCH, C. and FABRI, T.H.F. (1999a) Serum amyloid a and transferrin in chicken. A preliminary investigation of using acute-phase variables to assess diseases in chickens. Veterinary Quarterly 21: 37-41.Google Scholar
CHAMANZA, R., VAN VEEN, L., TIVAPASI, M.T. and TOUSSAINT, M.J.M. (1999b) Acute phase proteins in the domestic fowl. World's Poultry Science Journal 55: 61-71.CrossRefGoogle Scholar
CRAY, C., ZAIAS, J. and ALTMAN, N.H. (2009) Acute phase response in animals: a review. Comparative Medicine 59: 517-526.Google Scholar
DAVALOS, D. and AKASSOGLOU, K. (2012) Fibrinogen as a key regulator of inflammation in disease. Seminars in Immunopathology 34: 43-62.Google Scholar
DISILVESTRO, R.A. and HARRIS, E.D. (1985) Purification and partial characterization of ceruloplasmin from chicken serum. Archives of Biochemistry and Biophysics 241: 438-446.Google Scholar
DURAIRAJ, V., OKIMOTO, R., RASAPUTRA, K., CLARK, F.D. and RATH, N.C. (2009) Histopathology and serum clinical chemistry evaluation of broilers with femoral head separation disorder. Avian Diseases 53: 21-25.CrossRefGoogle ScholarPubMed
ECKERSALL, P.D., DUTHIE, S., SAFI, S., MOFFATT, D., HORADAGODA, N.U., DOYLE, S., PARTON, R., BENNETT, D. and FITZPATRICK, J.L. (1999) An Automated Biochemical Assay for Haptoglobin: Prevention of Interference from Albumin. Comparative Haemotology International 9: 117-124.Google Scholar
ECKERSALL, P.D. and BELL, R. (2010) Acute phase proteins: Biomarkers of infection and inflammation in veterinary medicine. The Veterinary journal 185: 23-27.CrossRefGoogle ScholarPubMed
ERIKSEN, N., MEEK, R.L. and BENDITT, E.P. (1993) The SAA lipoprotein family, in: MACKIEWICZ, A., KUSHNER, I. & BAUMANN, H. (Eds) Acute Phase Proteins: Molecular biology, Biochemistry and Clinical Applications, pp. 93-106 (CRC Press, Boca Raton, Florida).Google Scholar
FLORIS, G., MEDDA, R., PADIGLIA, A. and MUSCI, G. (2000) The physiopathological significance of ceruloplasmin. Biochemical Pharmacology 60: 1735-1741.CrossRefGoogle ScholarPubMed
GARCIA, K.O., BERCHIERI-JUNIOR, A., SANTANA, A.M., FREITAS-NETO, O.C. and FAGLIARI, J.J. (2009) Experimental infection of commercial layers using a Salmonella enterica serovar Gallinarum strain: Leukogram and serum acute-phase protein concentrations. Brazillian Journal of Poultry Science 11: 263-270.Google Scholar
GEORGIEVA, T.M., KOINARSKI, V.N., URUMOVA, V.S., MARUTSOV, P.D., CHRISTOV, T.T., NIKOLOV, J., CHAPRAZOV, T., WALSHE, K., KAROV, R.S., GEORGIEV, I.P. and KOINARSKI, Z.V. (2010) Effects of Escherichia coli infection and Eimeria tenella invasion on blood concentrations of some positive acute phase proteins (haptoglobin (PIT 54), fibrinogen and ceruloplasmin). Revue de Medecine Veterinaire 161: 84-89.Google Scholar
GRIENINGER, G., LIANG, T.J., BEUVING, G., GOLDFARB, V., METCALFE, S.A. and MULLER-EBERHARD, U. (1986) Hemopexin is a developmentally regulated, acute-phase plasma protein in the chicken. The Journal of Biological Chemistry 261: 15719-15724.Google Scholar
GRUYS, E., TOUSSAINT, M.J.M., NIEWOLD, T.A. and KOOPMANS, S.J. (2005) Acute phase reaction and acute phase proteins. Journal of Zhejiang University. Science B 6: 1045-1056.Google Scholar
HALLQUIST, N.A. and KLASING, K.C. (1994) Serotransferrin, ovotransferrin and metallothionein levels during an immune response in chickens. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 108: 375-384.Google Scholar
HRUBEC, T., WHICHARD, J.M., LARSEN, C.T. and PIERSON, M.S. (2002) Plasma versus serum: specific differences in biochemical analyte values. Journal of Avian Medicine and Surgery 16: 101-105.Google Scholar
INOUE, M., SATOH, W. and MURAKAMI, H. (1997) Plasma alpha 1-acid glycoprotein in chickens infected with infectious bursal disease virus. Avian Diseases 41: 164-170.Google Scholar
IWASAKI, K., MORIMATSU, M., INANAMI, O., UCHIDA, E., SYUTO, B., KUWABARA, M. and NIIYAMA, M. (2001) Isolation, characterization, and cDNA cloning of chicken turpentine-induced protein, a new member of the scavenger receptor cysteine-rich (SRCR) family of proteins. The Journal of Biological Chemistry 276: 9400-9405.Google Scholar
JIANHUA, L., LICHENG, L., JIUSHAN, J. and HONGKUI, L. (2000) Effects of high temperature on plasma fibronectin levels and serum biochemical parameters in broilers. Chinese Journal of Veterinary Science 20: 591-593.Google Scholar
JUUL-MADSEN, H.R., MUNCH, M., HANDBERG, K.J., SØRENSEN, P., JOHNSON, A.A., NORUP, L.R. and JØRGENSEN, P.H. (2003) Serum levels of mannan-binding lectin in chickens prior to and during experimental infection with avian infectious bronchitis virus. Poultry Science 82: 235-241.CrossRefGoogle ScholarPubMed
JUUL-MADSEN, H.R., NORUP, L.R., HANDBERG, K.J. and JØRGENSEN, P.H. (2007) Mannan-binding lectin (MBL) serum concentration in relation to propagation of infectious bronchitis virus (IBV) in chickens. Viral Immunology 20: 562-570.CrossRefGoogle Scholar
KOH, T.S., PENG, R.K. and KLASING, K.C. (1996) Dietary copper level affects copper metabolism during lipopolysaccharide-induced immunological stress in chicks. Poultry Science 75: 867-872.Google Scholar
LABAT-ROBERT, J. (2012) Cell-Matrix interactions, the role of fibronectin and integrins. A survey Pathologie-Biologie 60: 15-19.CrossRefGoogle ScholarPubMed
LABAT-ROBERT, J. and ROBERT, L. (2012) Fifty years of structural glycoproteins. Pathologie-Biologie 60: 66-75.Google Scholar
LANDMAN, W., GRUYS, E. and DWARS, R. (1994) A syndrome associated with growth depression and amyloid arthropathy in layers: a preliminary report. Avian Pathology 23: 461-470.Google Scholar
LANDMAN, W.J.M. (1998) Amyloid Arthropathy. Ph. D. thesis, Utrecht University.Google Scholar
LAURSEN, S.B., HEDEMAND, J.E., NIELSEN, O.L., THIEL, S., KOCH, C. and JENSENIUS, J.C. (1998) Serum levels, ontogeny and heritability of chicken mannan-binding lectin (MBL). Immunology 94: 587-593.Google Scholar
LAURSEN, S.B. and NIELSEN, O.L. (2000) Mannan-binding lectin (MBL) in chickens: molecular and functional aspects. Developmental and Comparative Immunology 24: 85-101.Google Scholar
LICHENG, L., JIANHUA, L., JIUSHAN, J., JIXUN, Z. and CHENG, H. (2000) Effect of ACTH and dexamethasone on plasma fibronectin levels and serum biochemical parameters in broilers. Journal of China Agricultural University 5: 106-110.Google Scholar
LYNAGH, G.R., COLLINS, R.A. and KAISER, P. (2000) Development and use of monoclonal antibodies to chicken fibronectin to show that the chicken hepatocellular carcinoma cell line, LMH, constitutively expresses fibronectin. Research in Veterinary Science 68: 147-152.Google Scholar
MARTÍNEZ-SUBIELA, S., TECLES, F. and CERON, J.J. (2007) Comparison of two automated spectrophotometric methods for ceruloplasmin measurement in pigs. Research in Veterinary Science 83: 12-19.CrossRefGoogle ScholarPubMed
MILLET, S., BENNETT, J., LEE, K.A., HAU, M. and KLASING, K.C. (2007) Quantifying and comparing constitutive immunity across avian species. Developmental and Comparative Immunology 31: 188-201.Google Scholar
MURATA, H., SHIMADA, N. and YOSHIOKA, M. (2004) Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal 168: 28-40.Google Scholar
NAKAMURA, K., MITARAI, Y. and YOSHIOKA, M. (1998) Serum levels of interleukin-6, alpha1-acid glycoprotein, and corticosterone in two-week-old chickens inoculated with Escherichia coli lipopolysaccharide. Poultry Science 77: 908-911.Google Scholar
NAKAMURA, K., IMAI, K. and TANIMURA, N. (1996) Comparison of the effects of infectious bronchitis and infectious laryngotracheitis on the chicken respiratory tract. Journal of Comparative Pathology 114: 11-21.Google Scholar
NAZIFI, S., TABANDE, M.R., HOSSEINIAN, S.A., ANSARI-LARI, M. and SAFARI, H. (2011) Evaluation of sialic acid and acute-phase proteins (haptoglobin and serum amyloids A) in healthy and avian infection bronchitis virus-infected chicks. Comparative Clinical Pathology 20: 69-73.Google Scholar
NAZIFI, S., DADRAS, H., HOSEINIAN, S.A., ANSARI-LARI, M. and MASOUDIAN, M. (2010) Measuring acute phase proteins (haptoglobin, ceruloplasmin, serum amyloid A, and fibrinogen) in healthy and infectious bursal disease virus-infected chicks. Comparative Clinical Pathology 19: 283-286.CrossRefGoogle Scholar
NIELSEN, O.L., SØRENSEN, P., HEDEMAND, J.E., LAURSEN, S.B. and JØRGENSEN, P.H. (1998a) Inflammatory response of different chicken lines and B haplotypes to infection with infectious bursal disease virus. Avian Pathology 27: 181-189.Google Scholar
NIELSEN, O.L., JØRGENSEN, P.H., HEDEMAND, J., JENSENIUS, J.C., KOCH, C. and LAURSEN, S.B. (1998b) Immunohistochemical investigation of the tissue distribution of mannan-binding lectin in non-infected and virus-infected chickens Immunology 94: 122-128.Google Scholar
NIELSEN, O.L., JENSENIUS, J.C., JØRGENSEN, P.H. and LAURSEN, S.B. (1999) Serum levels of chicken mannan-binding lectin (MBL) during virus infections; indication that chicken MBL is an acute phase reactant. Veterinary Immunology and Immunopathology 70: 309-316.Google Scholar
OVELGÖNNE, J.H., LANDMAN, W.J., GRUYS, E., GIELKENS, A.L. and PEETERS, B.P. (2001) Identical amyloid precursor proteins in two breeds of chickens which differ in susceptibility to develop amyloid arthropathy. Amyloid 8: 41-51.Google Scholar
PANKOV, R. and YAMADA, K.M. (2002) Fibronectin at a glance. Journal of Cell Science 115: 3861-3863.Google Scholar
PATTERSON, L.T. and MORA, E.C. (1964) Occurance of a substance analogous to C-reactive protein in the blood of the domestic fowl. Texas Reports on biology and medicine 22: 716-721.Google Scholar
PATTERSON, L.T. and MORA, E.C. (1965) The C-reactive protein response and disease resistance in domestic fowl. Texas Reports on biology and medicine 23: 600-606.Google Scholar
PETERSEN, H.H., NIELSEN, J.P. and HEEDAARD, P.M.H. (2004) Application of acute phase protein measurements in veterinary clinical chemistry. Veterinary Research 35: 163-187.Google Scholar
RATH, N.C., ANTHONY, N.B., KANNAN, L., HUFF, W.E., HUFF, G.R., CHAPMAN, H.D., ERF, G.F. and WAKENELL, P. (2009) Serum ovotransferrin as a biomarker of inflammatory diseases in chickens. Poultry Science 88: 2069-2074.Google Scholar
RICHARDS, M.P. and AUGUSTINE, P.C. (1988) Serum and liver zinc, copper, and iron in chicks infected with Eimeria acervulina or Eimeria tenella. Biological Trace Element Research 17: 207-219.CrossRefGoogle ScholarPubMed
RÖCKEN, C. and SHAKESPEARE, A. (2002) Pathology, diagnosis and pathogenesis of AA amyloidosis. Virchows Archiv 440: 111-122.Google Scholar
SALAMANO, G., MELLIA, E., TARANTOLA, M., GENNERO, M.S., DOGLIONE, L. and SCHIAVONE, A. (2010) Acute phase proteins and heterophil:lymphocyte ratio in laying hens in different housing systems. The Veterinary Record 167: 749-751.Google Scholar
SCHOU, T.W., PERMIN, A., CHRISTENSEN, J.P., CU, H.P. and JUUL-MADSEN, H.R. (2010) Mannan-binding lectin (MBL) in two chicken breeds and the correlation with experimental Pasteurella multocida infection. Comparative Immunology, Microbiology and Infectious Diseases 33: 183-195.CrossRefGoogle ScholarPubMed
SEVIMLI, A., MISIRLIOĞLU, D., POLAT, U., YALÇIN, M., AKKOÇ, A. and UĞUZ, C. (2005) The effects of vitamin A, pentoxyfylline and methylprednisolone on experimentally induced amyloid arthropathy in brown layer chicks. Avian Pathology 34: 143-149.Google Scholar
SHAINKIN-KESTENBAUM, R., BERLYNE, G., ZIMLICHMAN, S., SORIN, H.R. NYSKA, M. and DANON, A. (1991) Acute phase protein, serum amyloid A, inhibits IL-1- and TNF-induced fever and hypothalamic PGE2 in mice. Scandinavian Journal of Immunology 34: 179-183.Google Scholar
SOHAIL, M.U., IJAZ, A., YOUSAF, M.S., ASHRAF, K., ZANEB, H., ALEEM, M. and REHMAN, H. (2010) Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poultry Science 89: 1934-1938.Google Scholar
SONG, Z., ZHU, L., ZHAO, T., JIAO, H. and LIN, H. (2009) Effect of copper on plasma ceruloplasmin and antioxidant ability in broiler chickens challenged by lipopolysaccharide. Asian-Australasian Journal of Animal Sciences 22: 1400-1406.Google Scholar
SUNDERMAN, F. and NOMOTO, S. (1970) Measurement of human serum ceruloplasminby its p-phenylenediamine oxidase activity. Clinical Chemistry 16: 903-910.Google Scholar
SYLTE, M.J. and SUAREZ, D.L. (2012) Vaccination and acute phase mediator production in chickens challenged with low pathogenic avian influenza virus; novel markers for vaccine efficacy? Vaccine 30: 3097-3105.CrossRefGoogle ScholarPubMed
TAKAHASHI, K., AKIBA, Y., IWATA, T. and KASAI, M. (2002) Dietary conjugated linoleic acids alleviate early inflammatory response caused by lipopolysaccharide injection in male broiler chicks. Animal Science Journal 73: 47-50.CrossRefGoogle Scholar
TAKAHASHI, K., KAJI, N., AKIBA, Y. and TAMURA, K. (1994) Plasma alpha 1-acid glycoprotein concentration in broilers: influence of age, sex and injection of Escherichia coli lipopolysaccharide. British Poultry Science 35: 427-432.CrossRefGoogle ScholarPubMed
TAKAHASHI, K., MIYAKE, N. and OHTA, T. (1998) Changes in plasma alpha 1-acid glycoprotein concentration and selected immune response in broiler chickens injected with Escherichia coli lipopolysaccharide. British Poultry Science 39: 152-155.Google Scholar
TAKAHASHI, K., TAKAGI, K. and AKIBA, Y. (2009) Effects of dietary glycine supplementation and fish meal on inflammatory responses in broiler chicks. British Poultry Science 50: 479-486.Google Scholar
TAKAHASHI, K., YODOGAWA, S., AKIBA, Y. and TAMURA, K. (1995) Effect of dietary protein concentration on responses to Escherichia coli endotoxin in broiler chickens. British Journal of Nutrition 74: 173-182.Google Scholar
THRALL, M.A., BAKER, D.C., CAMPBELL, T.W., DENICOLA, D.B., FETTMAN, M.J. and LASSEN, E.D. (2004) Veterinary Hematology and Clinical Chemistry (John Wiley & Sons).Google Scholar
TOLOSANO, E., FAGOONEE, S., MORELLO, N., VINCHI, F. and FIORITO, V. (2010) Heme scavenging and the other facets of hemopexin. Antioxidants & Redox Signaling 12: 305-320.Google Scholar
TUYTTENS, F., HEYNDRICKX, M., DE BOECK, M., MOREELS, A., VAN NUFFEL, A., VAN POUCKE, E., VAN COILLIE, E., VAN DONGEN, S. and LENS, L. (2008) Broiler chicken health, welfare and fluctuating asymmetry in organic versus conventional production systems. Livestock Science 113: 123-132.Google Scholar
UHLAR, C.M. and WHITEHEAD, A.S. (1999) Serum amyloid A, the major vertebrate acute-phase reactant. European Journal of Biochemistry 265: 501-523.Google Scholar
UPRAGARIN, N. (2005) In vitro studies on the pathogenesis of AA amyloid arthropathy in chicken. Ph. D. thesis, Utrecht University.Google Scholar
UPRAGARIN, N., VAN ASTEN, A.J.A.M., TOOTEN, P.C.J., LANDMAN, W.J.M. and GRUYS, E. (2005) Serum amyloid A production by chicken fibroblast-like synoviocytes. Veterinary Immunology and Immunopathology 106: 39-51.Google Scholar
WICHER, K.B. and FRIES, E. (2010) Evolutionary aspects of hemoglobin scavengers. Antioxidants & Redox Signaling 12: 249-259.Google Scholar
WICHER, K.B. and FRIES, E. (2006) Haptoglobin, a hemoglobin-binding plasma protein, is present in bony fish and mammals but not in frog and chicken. Proceedings of the National Academy of Sciences of the United States of America 103: 4168-4173.Google Scholar
WIGLEY, P. and KAISER, P. (2003) Avian cytokines in health and disease. Revista Brasileira de Ciência Avícola 5: 1-14.Google Scholar
WILLIAMS, J. (1968) A comparison of glycopeptides from the ovotransferrin and serum transferrin of the hen. The Biochemical Journal 108: 57-67.CrossRefGoogle ScholarPubMed
XIE, H., RATH, N.C., HUFF, G.R., HUFF, W.E. and BALOG, J.M. (2000) Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poultry Science 79: 33-40.Google Scholar
XIE, H., HUFF, G.R., HUFF, W.E., BALOG, J.M., HOLT, P. and RATH, N.C. (2002a) Identification of ovotransferrin as an acute phase protein in chickens. Poultry Science 81: 112-20.Google Scholar
XIE, H., NEWBERRY, L., CLARK, F.D., HUFF, W.E., HUFF, G.R., BALOG, J.M. and RATH, N.C. (2002b) Changes in Serum Ovotransferrin Levels in Chickens with Experimentally Induced Inflammation and Diseases Changes in Serum Ovotransferrin Levels in Chickens with Experimentally Induced Inflammation and Diseases. Avian Diseases 46: 122-131.Google Scholar
XIE, H., HUFF, G.R., HUFF, W.E., BALOG, J.M. and RATH, N.C. (2002c) Effects of ovotransferrin on chicken macrophages and heterophil-granulocytes. Developmental & Comparative Immunology 26: 805-815.Google Scholar