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Neuroimmunomodulation and heat stress in poultry

Published online by Cambridge University Press:  03 July 2017

A.S. CALEFI Open the ORCID record for A.S. CALEFI [Opens in a new window] ,
W.M. QUINTEIRO-FILHO ,
A.J.P. FERREIRA  and
J. PALERMO-NETO
A.S. CALEFI*
Affiliation:
Neuroimmunomodulation Research Group, Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo, 05508-270, São Paulo/SP, Brazil
W.M. QUINTEIRO-FILHO
Affiliation:
Neuroimmunomodulation Research Group, Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo, 05508-270, São Paulo/SP, Brazil
A.J.P. FERREIRA
Affiliation:
Neuroimmunomodulation Research Group, Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo, 05508-270, São Paulo/SP, Brazil
J. PALERMO-NETO
Affiliation:
Neuroimmunomodulation Research Group, Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo, 05508-270, São Paulo/SP, Brazil
*
Corresponding author: atilio@usp.br
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Abstract

The intensification of poultry production has favoured the occurrence of stressful conditions such as infections, decreased feed intake, reduced feed conversion and carcass condemnation are some of the consequences of stress in birds. This stress is a consequence of the neuroendocrine-immune interplay. Neuroimmunomodulation is the scientific study of the bidirectional relation of the immune and nervous systems, i.e., physiological effects in response to exposure of animals to stressful conditions. Stress is responsible for activating the hypothalamic-pituitary-adrenal axis, which results in the production and release of corticosterone and catecholamines. Furthermore, recent studies have shown that the brain-gut-microbiota axis is responsible for the maturation and maintenance of the balance of the immune and nervous systems, which ensures improvement in the productive system. This review presents and discusses information concerning neuroimmunomodulation in birds with an emphasis on the involvement of heat stress.

Keywords

neuroimmunomodulationstressheatpsychoneuroimmunomodulation
Type
Reviews
Information
World's Poultry Science Journal , Volume 73 , Issue 3 , September 2017 , pp. 493 - 504
Copyright
Copyright © World's Poultry Science Association 2017 

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References

ADER, R. (2000) On the Development of Psychoneuroimmunology. European Journal of Pharmacology 405: 167-176.CrossRefGoogle ScholarPubMed
ADER, R., COHEN, N. and FELTEN, D. (1995) Psychoneuroimmunology: Interactions between the Nervous System and the Immune System. The Lancet 345: 99-103.Google Scholar
BAARENDSE, P.J.J., DEBONNE, M., DECUYPERE, E., KEMP, B. and VAN DEN BRAND, H. (2007) Ontogeny of avian thermoregulation from a neural point of view. World's Poultry Science Journal 63: 267-276.Google Scholar
BANFIELD, M.J., TEN DOESCHATE, R.A.H.M. and FORBES, J. M. (1998) Effect of Whole Wheat and Heat Stress on a Coccidial Infection in Broiler Chickens. British Poultry Science 39: 25-26.Google Scholar
BÉDÉCARRATS, G.Y., BAXTER, M. and SPARLING, B. (2016) An updated model to describe the neuroendocrine control of reproduction in chickens. General and Comparative Endocrinology 227: 58-63.CrossRefGoogle ScholarPubMed
BERCZI, I. (1998) The Stress Concept and Neuroimmunoregulation in Modern Biology. Annals of the New York Academy of Sciences 851: 3-12.Google Scholar
BICEGO, K.C., BARROS, R.C. and BRANCO, L.G. (2007) Physiology of temperature regulation: comparative aspects. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 147: 616-639.Google Scholar
BROWN-BORG, H.M. and EDENS, F.W. (1992) In Vivo Neurotoxin Administration Alters Immune Responses in Chickens (Gallus Domesticus). Comparative Biochemistry and Physiology C. 1: 177-183.CrossRefGoogle ScholarPubMed
CALEFI, A.S., HONDA, B.T.B., COSTOLA-DE-SOUZA, C., DE SIQUEIRA, A., NAMAZU, L.B., QUINTEIRO-FILHO, W.M., FONSECA, J.G.S., ALOIA, T.P.A. and PALERMO-NETO, J. (2014) Effects of long-term heat stress in an experimental model of avian necrotic enteritis. Poultry Science 93: 1344-1353.Google Scholar
CALEFI, A.S., FONSECA, J.G.S., COHN, D.W.H., HONDA, B.T.B., COSTOLA-DE-SOUZA, C., TSUGIYAMA, L.E., QUINTEIRO-FILHO, W.M., FERREIRA, A.J.P. and PALERMO-NETO, J. (2016a) Gut-Brain Axis Interactions during Heat Stress and Avian Necrotic Enteritis. Poultry Science 95: 1005-1014.Google Scholar
CALEFI, A.S., QUINTEIRO-FILHO, W.M., FUKUSHIMA, A.R., CRUZ, D.S.G., SIQUEIRA, A., SALVAGNI, F.A., NAMAZU, L.B., MASSOCO, C.S.G., PIANTINO-FERREIRA, A.J. and PALERMO NETO, J. (2016b) Dexamethasone Regulates Macrophage and CD4+CD25+ Cell Numbers in the Chicken Spleen. Brazilian Journal of Poultry Science 18: 93-100.Google Scholar
CALEFI, A.S., SIQUEIRA, A., NAMAZU, L.B., COSTOLA-DE-SOUZA, C., HONDA, B.B.T., FERREIRA, A.J.P., QUINTEIRO-FILHO, W.M., DA SILVA FONSECA, J.G. and PALERMO-NETO, J. (2016c) Effects of heat stress on the formation of splenic germinal centres and immunoglobulins in broilers infected by Clostridium perfringens type A. Veterinary Immunology and Immunopathology 171: 38-46.CrossRefGoogle ScholarPubMed
CHANDRATILLEKE, D., HÀLA, K. and MARSH, J.A. (1996) Effects of in Vivo Thyroid Hormone Treatment on the Expression of Interleukin-2 Receptors on Avian Splenocytes. International Journal of Immunopharmacology 3: 203-210.CrossRefGoogle Scholar
CHEN, P., CHRISTINE, V.H., DANIEL, L. and CHIEN, L. (2012) Central Urocortin 3 and Type 2 Corticotropin-Releasing Factor Receptor in the Regulation of Energy Homeostasis: Critical Involvement of the Ventromedial Hypothalamus. Frontiers in Endocrinology 3: 180.Google Scholar
CIRIACO, E., RICCI, A., BRONZETTI, E., MAMMOLA, C.L., GERMANA, G. and VEGA, J.A. (1995) Age-Related Changes of the Noradrenergic and Acetylcholinesterase Reactive Nerve Fibres Innervating the Pigeon Bursa of Fabricius. Annals of Anatomy 177: 237-242.Google Scholar
CORDIER, A. (1969) Innervation of the Bursa of Fabricius during Embryobenesis and Adult Life. L'innervation de La Bourse de Fabricius Durant L'embryogenèse et La Vie Adulte 73: 38-47.Google Scholar
COSTA-PINTO, F.A. and PALERMO-NETO, J. (2010) Neuroimmune Interactions in Stress. Neuroimmunomodulation 17: 196-199.CrossRefGoogle ScholarPubMed
DAWKINS, M.S., CHRISTL, A.D. and TRACEY, A.J. (2004) Chicken Welfare Is Influenced More by Housing Conditions than by Stocking Density. Nature 427: 342-344.Google Scholar
DENNO, K.M., MCCORKLE, F.M. and TAYLOR, R.L. (Jr) (1994) Catecholamines Modulate Chicken Immunoglobulin M and Immunoglobulin G Plaque-Forming Cells. Poultry Science 73: 1858-1866.Google Scholar
DEVICHE, P. and CORTEZ, L. (2005) Androgen Control of Immunocompetence in the Male House Finch, Carpodacus Mexicanus Müller. Journal of Experimental Biology 208: 1287-1295.Google Scholar
DOKLADNY, K.L, POPE, L.M. and THOMAS, Y.M. (2006) Physiologically Relevant Increase in Temperature Causes an Increase in Intestinal Epithelial Tight Junction Permeability. American Journal of Physiology. Gastrointestinal and Liver Physiology 290: G204-212.CrossRefGoogle ScholarPubMed
DUFFY, D.L., BENTLEY, G.E., DRAZEN, D.L. and BALL, G.F.B. (2000) Effects of Testosterone on Cell-Mediated and Humoral Immunity in Non-Breeding Adult European Starlings. Behavioral Ecology 11: 654-662.Google Scholar
EL-FAR, A.A., MASHALY, M.M. and KAMAR, G.A. (1994) Bursectomy and in Vitro Response of Adrenal Gland to Adrenocorticotropic Hormone and Testis to Human Chorionic Gonadotropin in Immature Male Chickens. Poultry Science 73: 113-117.Google Scholar
ETCHES, R.J., JOHN, T.M. and GIBBINS, A.M.V. (2008) Behavioural, Physiological, Neuroendocrine and Molecular Responses to Heat Stress. Poultry Production in Hot Climates, pp. 31-66.Google Scholar
FOWLES, J.R., FAIRBROTHER, A., FIX, M., SCHILLER, S. and KERKVLIET, N.I. (1993) Glucocorticoid Effects on Natural and Humoral Immunity in Mallards. Developmental and Comparative Immunology 17: 165-177.Google Scholar
FRANCHINI, A. and OTTAVIANI, E. (1999) Immunoreactive POMC-Derived Peptides and Cytokines in the Chicken Thymus and Bursa of Fabricius Microenvironments: Age-Related Changes. Journal of Neuroendocrinology 9: 685-692.Google Scholar
GARRIGA, C., HUNTER, R.R., AMAT, C., PLANAS, J.M., MITCHELL, M.A. and MORETO, M. (2006) Heat Stress Increases Apical Glucose Transport in the Chicken Jejunum. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 290: R195-201.CrossRefGoogle ScholarPubMed
GEHAD, A.E., LILLEHOJ, H.S., HENDRICKS III, G.L. and MASHALY, M.M. (2002) Initiation of Humoral Immunity. I. The Role of Cytokines and Hormones in the Initiation of Humoral Immunity Using T-Independent and T-Dependent Antigens. Developmental and Comparative Immunology 26: 751-759.Google Scholar
GILLIES, G.E., LINTON, E.A. and LOWRY, P.J. (1982) Corticotropin Releasing Activity of the New CRF Is Potentiated Several Times by Vasopressin. Nature 299: 355-357.CrossRefGoogle ScholarPubMed
GLASER, R. and KIECOLT-GLASER, J.K. (2005) Stress-Induced Immune Dysfunction: Implications for Health. Nature Review in Immunology 5: 243-251.Google Scholar
GLEESON, M. and BRACKENBURY, J.H. (1984) Effects of Body Temperature on Ventilation, Blood Gases and Acid-Base Balance in Exercising Fowl. Quarterly Journal of Experimental Physiology 69: 61-72.Google Scholar
GLICK, B. (1984) Interrelation of the Avian Immune and Neuroendocrine Systems. Journal of Experimental Zoology 3: 671-682.Google Scholar
GLICK, B. (1991) Historical Perspective: The Bursa of Fabricius and Its Influence on B-Cell Development, Past and Present. Veterinary Immunology and Immunopathology 30: 3-12.CrossRefGoogle ScholarPubMed
GOMES, A.V.S., QUINTEIRO-FILHO, W.M., RIBEIRO, A., FERRAZ-DE-PAULA, V., PINHEIRO, M.L., BASKEVILLE, E., AKAMINE, A.T., ASTOLFI-FERREIRA, C.S., FERREIRA, A.J.P. and PALERMO-NETO, J. (2014) Overcrowding Stress Decreases Macrophage Activity and Increases Salmonella Enteritidis Invasion in Broiler Chickens. Avian Pathology 43: 82-90.Google Scholar
HADDAD, E.E. and MASHALY, M.M. (1990) Effect of Thyrotropin-Releasing Hormone, Triiodothyronine, and Chicken Growth Hormone on Plasma Concentrations of Thyroxine, Triiodothyronine, Growth Hormone, and Growth of Lymphoid Organs and Leukocyte Populations in Immature Male Chickens. Poultry Science 69: 1094-1102.Google Scholar
HADDAD, E.E. and MASHALY, M.M. (1991) Chicken Growth Hormone, Triiodothyronine and Thyrotropin Releasing Hormone Modulation of the Levels of Chicken Natural Cell-Mediated Cytotoxicity. Developmental and Comparative Immunology 15: 65-71.Google Scholar
HECKERT, R.A., ESTEVEZ, I., RUSSEK-COHEN, E. and PETTIT-RILEY, R. (2002) Effects of Density and Perch Availability on the Immune Status of Broilers. Poultry Science 81: 451-457.CrossRefGoogle ScholarPubMed
HENDRICKS, G.L. and MASHALY, M.M. (1998) Effects of Corticotropin Releasing Factor on the Production of Adrenocorticotropic Hormone by Leukocyte Populations. British Poultry Science 39: 123-127.CrossRefGoogle ScholarPubMed
HENDRICKS III, G.L., SIEGEL, H.S. and MASHALY, M.M. (1991) Ovine Corticotropin-Releasing Factor Increases Endocrine and Immunologic Activity of Avian Leukocytes in Vitro. Proceedings of the Society for Experimental Biology and Medicine 196: 390-395.Google Scholar
HILLHOUSE, E.W. and GRAMMATOPOULOS, D.K. (2006) The Molecular Mechanisms Underlying the Regulation of the Biological Activity of Corticotropin-Releasing Hormone Receptors: Implications for Physiology and Pathophysiology. Endocrine Reviews 27: 260-286.CrossRefGoogle ScholarPubMed
HONDA, B.T.B., CALEFI, A.S., COSTOLA-DE-SOUZA, C., QUINTEIRO-FILHO, W.M., DA SILVA FONSECA, J.G., DE PAULA, V.F. and PALERMO-NETO, J. (2015) Effects of Heat Stress on Peripheral T and B Lymphocyte Profiles and IgG and IgM Serum Levels in Broiler Chickens Vaccinated for Newcastle Disease Virus. Poultry Science 94: 2375-2381.Google Scholar
HUMPHREY, T. (2006) Are Happy Chickens Safer Chickens? Poultry Welfare and Disease Susceptibility. British Poultry Science 47: 379-391.Google Scholar
JOHNSON, J.D., CAMPISI, J., SHARKEY, C.M., KENNEDY, S.L., NICKERSON, M., GREENWOOD, B.N. and FLESHNER, M. (2005) Catecholamines Mediate Stress-Induced Increases in Peripheral and Central Inflammatory Cytokines. Neuroscience 135: 1295-1307.Google Scholar
KAISER, P., WU, Z., ROTHWELL, L., FIFE, M., GIBSON, M., POH, T.Y., SHINI, A., BRYDEN, W. and SHINI, S. (2009) Prospects for Understanding Immune-Endocrine Interactions in the Chicken. General and Comparative Endocrinology 163: 83-91.CrossRefGoogle ScholarPubMed
KANG, Z., BÉDÉCARRATS, G.Y. and ZADWORNY, D. (2007) Expression patterns of the prolactin receptor gene in chicken lymphoid tissues during embryogenesis and posthatch period. Poultry Science 86: 2404-2412.CrossRefGoogle ScholarPubMed
KARROW, N.A. (2006) Activation of the hypothalamic-pituitary-adrenal axis and autonomic nervous system during inflammation and altered programming of the neuroendocrine-immune axis during fetal and neonatal development: Lessons learned from the model inflammagen, lipopolysaccharide. Brain, Behavior, and Immunity 20: 144-158.CrossRefGoogle ScholarPubMed
LAMBERT, G.P., GISOLFI, C.V., BERG, D.J., MOSELEY, P.L., OBERLEY, L.W. and KREGEL, K.C. (2002) Selected Contribution: Hyperthermia-Induced Intestinal Permeability and the Role of Oxidative and Nitrosative Stress. Journal of Applied Physiology 92: 1750-1761; discussion 1749.Google Scholar
LARA, L.J. and ROSTAGNO, M.H. (2013) Impact of heat stress on poultry production. Animals 3: 356-369.CrossRefGoogle ScholarPubMed
LICINIO, J. and FROST, P. (2000) The Neuroimmune-Endocrine Axis: Pathophysiological Implications for the Central Nervous System Cytokines and Hypothalamus-Pituitary-Adrenal Hormone Dynamics. Brazilian Journal of Medical and Biological Research 33: 1141-1148.CrossRefGoogle ScholarPubMed
LUKAS, N.W., MCCORKLE, F.M. and TAYLOR, R.L. (Jr) (1987) Monoamines Suppress the Phytohemagglutinin Wattle Response in Chickens. Developmental and Comparative Immunology 11: 759-768.Google Scholar
MARKOWSKA, M., MAJEWSKI, P.M. and SKWARŁO-SOŃTA, K. (2017) Avian biological clock-Immune system relationship. Developmental & Comparative Immunology 66: 130-138.Google Scholar
MARSH, J.A., LAUTERIO, T.J. and SCANES, C.G. (1984) Effects of Triiodothyronine Treatments on Body and Organ Growth and the Development of Immune Function in Dwarf Chickens. Proceedings of the Society of Experimental Biology Medicine. 1: 82-91.Google Scholar
MARSH, J.A. and SCANES, C.G. (1994) Neuroendocrine-Immune Interactions. Poultry Science 73: 1049-1061.CrossRefGoogle ScholarPubMed
MASHALY, M.M., HENDRICKS III, G.L., KALAMA, M.A., GEHAD, A.E., ABBAS, A.O. and PATTERSON, P.H. (2004) Effect of Heat Stress on Production Parameters and Immune Responses of Commercial Laying Hens. Poultry Science 83: 889-894.Google Scholar
MASHALY, M.M., TROUT, J.M. and HENDRICKS III, G.L. (1993) The Endocrine Function of the Immune Cells in the Initiation of Humoral Immunity. Poultry Science 72: 1289-1293.Google Scholar
MASHALY, M.M., TROUT, J.M., HENDRICKS III, G., AL-DOKHI, L.M. and GEHAD, A. (1998) The Role of Neuroendocrine Immune Interactions in the Initiation of Humoral Immunity in Chickens. Domestic Animal Endocrinology 15: 409-422.CrossRefGoogle ScholarPubMed
MCCORKLE, F.M., TAYLOR, R.L., DENNO, K.M. and JABE, J.M. (1990) Monoamines Alter in Vitro Migration of Chicken Leukocytes. Developmental and Comparative Immunology 14: 85-93.CrossRefGoogle ScholarPubMed
MCCORKLE, F.M. and TAYLOR, R.L. (Jr) (1994) Continuous Administration of Dopamine Alters Cellular Immunity in Chickens. Comparative Biochemistry and Physiology - C Pharmacology Toxicology and Endocrinology 109: 289-293.Google Scholar
MENEZES, A.G., NÄÄS, I.A. and BARACHO, M.S. (2010) Identification of critical points of thermal environment in broiler production. Revista Brasileira de Ciência Avícola 12: 21-29.CrossRefGoogle Scholar
MOTOBU, M., EL-ABASY, M., NA, K.J., VAINIO, O., TOIVANEN, P. and HIROTA, Y. (2003) Effects of 6-Hydroxydopamine on the Development of the Immune System in Chickens. Journal of Veterinary Medical Science 65: 35-42.Google Scholar
MOURA, D.J., VERCELLINO, R.A., SANTOS, J.P.A. and VALE, M.M. (2015) Heat stress impact on weight gain in broiler chickens: a meta-analytical study of environmental factor that impact production losses. In ASABE 1st Climate Change Symposium: Adaptation and Mitigation Conference Proceedings (pp. 1-3). American Society of Agricultural and Biological Engineers.Google Scholar
NANCE, D.M. and SANDERS, V.M. (2007) Autonomic Innervation and Regulation of the Immune System (1987-2007). Brain Behaviour and Immunology 21: 736-745.Google Scholar
OLIVER, S.R., PHILLIPS, N., NOVOSAD, V.L., BAKOS, M.P., TALBERT, E.E. and CLANTON, T.L. (2012) Hyperthermia Induces Injury to the Intestinal Mucosa in the Mouse: Evidence for an Oxidative Stress Mechanism. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 302: R845-R853.Google Scholar
OTTINGER, M.A. and LAVOIE, E. (2007) Neuroendocrine and immune characteristics of aging in avian species. Cytogenetic and Genome Research 117: 352-357.Google Scholar
PIESTUN, Y., DRUYAN, S., BRAKE, J. and YAHAV, S. (2013) Thermal manipulations during broiler incubation alter performance of broilers to 70 days of age. Poultry Science 92: 1155-1163.Google Scholar
PINTEA, V., CONSTANTINESCU, G.M. and RADU, C. (1967) Vascular and Nervous Supply of Bursa of Fabricius in the Hen. Acta Veterinaria Academiae Scientiarum Hungaricae 17: 263-268.Google ScholarPubMed
POST, J., REBEL, J.M. and TER HUURNE, A.A. (2003) Physiological Effects of Elevated Plasma Corticosterone Concentrations in Broiler Chickens. An Alternative Means by Which to Assess the Physiological Effects of Stress. Poultry Science 82: 1313-1318.Google Scholar
QUINTEIRO-FILHO, W.M., RIBEIRO, A., FERRAZ-DE-PAULA, V., PINHEIRO, M.L., SAKAI, M., SA, L.R., FERREIRA, A.J. and PALERMO-NETO, J. (2010) Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poultry Science 89: 1905-1914.CrossRefGoogle ScholarPubMed
QUINTEIRO-FILHO, W.M., GOMES, A.V.S., PINHEIRO, M.L., RIBEIRO, A., FERRAZ-DE-PAULA, V., ASTOLFI-FERREIRA, C.S., FERREIRA, A.J.P. and PALERMO-NETO, J. (2012a) Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella enteritidis. Avian Pathology 41: 421-427.CrossRefGoogle ScholarPubMed
QUINTEIRO-FILHO, W.M., RODRIGUES, M.V, RIBEIRO, A., FERRAZ-DE-PAULA, V., PINHEIRO, M.L., SA, L.R., FERREIRA, A.J. and PALERMO-NETO, J. (2012b) Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute HPA axis activation . Journal of Animal Science 90: 1986-1994.Google Scholar
QUINTEIRO-FILHO, W.M., CALEFI, A.S., CRUZ, D.S.G., ALOIA, T.P.A., ZAGER, A., ASTOLFI-FERREIRA, C.S., FERREIRA, A.J.P. and PALERMO-NETO, J. (2017) Heat stress decreases expression of the cytokines, avian β-defensins 4 and 6 and Toll-like receptor 2 in broiler chickens infected with Salmonella Enteritidis. Veterinary Immunology and Immunopathology 186: 19-28.CrossRefGoogle ScholarPubMed
RICHARD, D., QIN, L. and TIMOFEEVA, E. (2002) The Corticotropin-Releasing Factor Family of Peptides and CRF Receptors: Their Roles in the Regulation of Energy Balance. European Journal of Pharmacology 440: 189-197.Google Scholar
ROZENBOIM, I., TAKO, E., GAL-GARBER, O., PROUDMAN, J.A. and UNI, Z. (2007) The Effect of Heat Stress on Ovarian Function of Laying Hens. Poultry Science 86: 1760-1765.CrossRefGoogle ScholarPubMed
RYU, S.T., PARK, B.S., BANG, H.T., KANG, H.K. and HWANGBO, J. (2016) Effects of anti-heat diet and inverse lighting on growth performance, immune organ, microorganism and short chain fatty acids of broiler chickens under heat stress. Journal of Environmental Biology 37: 185.Google Scholar
SEEBACHER, F. (2009) Responses to temperature variation: integration of thermoregulation and metabolism in vertebrates. Journal of Experimental Biology 212: 2885-2891.Google Scholar
SELYE, H. (1955) Stress and Disease. Science 122: 625-631.Google Scholar
SELYE, H. (1936) A Syndrome Produced by Diverse Nocuous Agents. Nature 138: 32.Google Scholar
SHINI, S., HUFF, G.R., SHINI, A. and KAISER, P. (2010) Understanding Stress-Induced Immunosuppression: Exploration of Cytokine and Chemokine Gene Profiles in Chicken Peripheral Leukocytes. Poultry Science 89: 841-851.Google Scholar
SHINI, S., KAISER, P., SHINI, A. and BRYDEN, W.L. (2008) Biological Response of Chickens (Gallus Gallus Domesticus) Induced by Corticosterone and a Bacterial Endotoxin. Comparative Biochemistry and Physiology PartB 149: 324-333.Google Scholar
SHINI, S., SHINI, A. and HUFF, G.R. (2009) Effects of Chronic and Repeated Corticosterone Administration in Rearing Chickens on Physiology, the Onset of Lay and Egg Production of Hens. Physiology and Behavior 98: 73-77.Google Scholar
SHINI, S. and KAISER, P. (2009) Effects of Stress, Mimicked by Administration of Corticosterone in Drinking Water, on the Expression of Chicken Cytokine and Chemokine Genes in Lymphocytes. Stress 12: 388-399.CrossRefGoogle ScholarPubMed
SKWARLO-SONTA, K. (1992) Prolactin as an Immunoregulatory Hormone in Mammals and Birds. Immunology Letters 33: 105-121.CrossRefGoogle ScholarPubMed
SOLEIMANI, A.F., ZULKIFLI, I., OMAR, A.R. and RAHA, A.R. (2011) Physiological Responses of 3 Chicken Breeds to Acute Heat Stress. Poultry Science 90: 1435-1440.Google Scholar
ST-PIERRE, N.R., COBANOV, B. and SCHNITKEY, G. (2003) Economic Losses from Heat Stress by US Livestock Industries. Journal of Dairy Science 86: E52-77.Google Scholar
STAR, L., NIEUWLAND, M.G., KEMP, B. and PARMENTIER, H.K. (2007) Effect of Single or Combined Climatic and Hygienic Stress on Natural and Specific Humoral Immune Competence in Four Layer Lines. Poultry Science 86: 1894-1903.CrossRefGoogle ScholarPubMed
TROUT, J.M. and MASHALY, M.M. (1994) The Effects of Adrenocorticotropic Hormone and Heat Stress on the Distribution of Lymphocyte Populations in Immature Male Chickens. Poultry Science 73: 1694-1698.Google Scholar
TROUT, J.M. and MASHALY, M.M. (1995) Effects of in Vitro Corticosterone on Chicken T- and B-Lymphocyte Proliferation. British Poultry Science 36: 813-820.Google Scholar
TSIOURIS, V., GEORGOPOULOU, I., BATZIOS, C., PAPPAIOANNOU, N., DUCATELLE, R. and FORTOMARIS, P. (2015a) High Stocking Density as a Predisposing Factor for Necrotic Enteritis in Broiler Chicks. Avian Pathology 44: 59-66.Google Scholar
TSIOURIS, V., GEORGOPOULOU, I., BATZIOS, C., PAPPAIOANNOU, N., DUCATELLE, R. and FORTOMARIS, P. (2015b) The Effect of Cold Stress on the Pathogenesis of Necrotic Enteritis in Broiler Chicks. Avian Pathology 44: 430-435.Google Scholar
VARASTEH, S., BRABER, S., AKBARI, P., GARSSEN, J. and FINK-GREMMELS, J. (2015) Differences in Susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PloS one 10: e0138975.Google Scholar
YAHAV, S. and BRAKE, J. (2014) Chick Embryogenesis: A Unique Platform to Study the Effects of Environmental Factors on Embryo Development. Journal of Stem Cells 9: 17.Google Scholar
ZENTEL, H.J., NOHR, D., ALBRECHT, R., JEURISSEN, S.H., VAINIO, O. and WEIHE, E. (1991) Peptidergic Innervation of the Bursa Fabricii: Interrelation with T-Lymphocyte Subsets. International Journal of Neuroscience 59: 177-188.CrossRefGoogle ScholarPubMed
ZENTEL, H.J. and WEIHE, E. (1991) The Neuro-B Cell Link of Peptidergic Innervation in the Bursa Fabricii. Brain, Behavior, and Immunity 5: 132-147.Google Scholar
ZIEGLER, D.R. and HERMAN, J.P. (2002) Neurocircuitry of Stress Integration: Anatomical Pathways Regulating the Hypothalamo-Pituitary-Adrenocortical Axis of the Rat. Integrative and Comparative Biology 42: 541-551.Google Scholar