Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T14:01:09.435Z Has data issue: false hasContentIssue false

Impact of heat stress and nutritional interventions on poultry production

Published online by Cambridge University Press:  17 October 2018

S.P. HE
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
M.A. AROWOLO
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
R.F. MEDRANO
Affiliation:
College of Veterinary Science and Medicine, Central Luzon State University, Science City of Munoz, Nueva Ecija, Philippines
S. LI
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
Q.F. YU
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
J.Y. CHEN
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
J.H. HE*
Affiliation:
College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
*
Corresponding author: jianhuahy@hunau.net
Get access

Abstract

High ambient temperatures affect animal production and welfare in tropical and sub-tropical regions of the world. Feed intake, growth rate, mortality, egg production, hatchability and other production traits related to the economic success of the poultry industry are adversely affected by severe heat stress. In general, heat stress induces the activity of the neuroendocrine system, resulting in activation of the hypothalamic-pituitary-adrenal (HPA) axis, and elevated corticosterone (CORT) concentrations, which affects metabolism and immune responses. These include negative regulation of metabolic hormones, antibody production and heterophil to lymphocyte (H/L) ratio. Heat stress increases mitochondrial activity, causing reactive species overproduction which disrupts the antioxidant balance, leading to oxidative stress damage of membranes, protein and DNA. Heat stress stimulates the central nervous system (CNS), which significantly reduces daily gain, feed intake and FCR in poultry. Consequently, from an animal husbandry perspective, intervention strategies to relieve heat stress conditions have been the focus of many published studies. This review describes the effect of high temperature on production, behavioural, biochemical and immune responses, including oxidative damage that occur during heat stress in poultry, in broilers and laying hens. Moreover, nutritional interventions to alleviate the negative consequence of heat stress is discussed.

Type
Review
Copyright
Copyright © World's Poultry Science Association 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ABD EL-HACK, M.E., MAHROSE, K., ASKAR, A.A., ALAGAWANY, M., ARIF, M., SAEED, M., ABBASI, F., SOOMRO, R.N., SIYAL, F.A. and CHAUDHRY, M.T. (2017) Single and Combined Impacts of Vitamin A and Selenium in Diet on Productive Performance, Egg Quality, and Some Blood Parameters of Laying Hens During Hot Season. Biological Trace Element Research 177: 169-179.Google Scholar
ABDELQADER, A.M., ABUAJAMIEH, M., HAMMAD, H.M. and AL-FATAFTAH, A.A. (2017) Effects of dietary butyrate supplementation on intestinal integrity of heat-stressed cockerels. Journal of Animal Physiology and Animal Nutrition (Berl) 101: 1115-1121.Google Scholar
AGARWAL, A. and PRABAKARAN, S.A. (2005) Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian Journal of Experiment Biology 43: 963-974.Google Scholar
AKBARIAN, A., MICHIELS, J., DEGROOTE, J., MAJDEDDIN, M., GOLIAN, A. and DESMET, S. (2016) Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. Journal of Animal Science and Biotechnology 7: 37-50.Google Scholar
AKHAVAN-SALAMAT, H. and GHASEMI, H.A. (2016) Alleviation of chronic heat stress in broilers by dietary supplementation of betaine and turmeric rhizome powder: dynamics of performance, leukocyte profile, humoral immunity, and antioxidant status. Tropical Animal Health and Production 48: 181-188.Google Scholar
ALHENAKY, A., ABDELQADER, A., ABUAJAMIEH, M. and AL-FATAFTAH, A.R. (2017) The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. Journal of Thermal Biology 70: 9-14.Google Scholar
ALTAN, O., PABUCCUOGLU, A., ALTAN, A., KONYALIOGLU, S. and BAYRAKTAR, H. (2003) Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. British Poultry Science 44: 545-550.Google Scholar
ATTIA, Y.A., ABD, E.A., ABEDALLA, A.A., BERIKA, M.A., AL-HARTHI, M.A., KUCUK, O., SAHIN, K. and ABOU-SHEHEMA, B.M. (2016) Laying performance, digestibility and plasma hormones in laying hens exposed to chronic heat stress as affected by betaine, vitamin C, and/or vitamin E supplementation. Springer Plus 5: 1619-1630.Google Scholar
ATTIA, Y.A., HASSAN, R.A. and QOTA, E.M. (2009) Recovery from adverse effects of heat stress on slow-growing chicks in the tropics 1: Effect of ascorbic acid and different levels of betaine. Tropic Animal Health and Production 41: 807-818.Google Scholar
AZAD, M.A., KIKUSATO, M., MAEKAWA, T., SHIRAKAWA, H. and TOYOMIZU, M. (2010) Metabolic characteristics and oxidative damage to skeletal muscle in broiler chickens exposed to chronic heat stress. Comparative Biochemistry and Physiology A-molecular & Integrative Physiology 155: 401-406.Google Scholar
AZAD, M.A., KIKUSATO, M., ZULKIFLI, I. and TOYOMIZU, M. (2013) Electrolysed reduced water decreases reactive oxygen species-induced oxidative damage to skeletal muscle and improves performance in broiler chickens exposed to medium-term chronic heat stress. British Poultry Science 54: 503-509.Google Scholar
BARTLETT, J.R. and SMITH, M.O. (2003) Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poultry Science 82: 1580-1588.Google Scholar
BELHADJ SLIMEN, I., NAJAR, T., GHRAM, A., DABBEBI, H., BEN MRAD, M. and ABDRABBAH, M. (2014) Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. International Journal of Hyperthermia 30: 513-523.Google Scholar
BELHADJ, S.I., NAJAR, T., GHRAM, A. and ABDRRABBA, M. (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. Journal of Animal Physiology and Animal Nutrition (Berl) 100: 401-412.Google Scholar
BOGIN, E., AVIDAR, Y., PECH-WAFFENSCHMIDT, V., DORON, Y., ISRAELI, B.A. and KEVKHAYEV, E. (1996) The relationship between heat stress, survivability and blood composition of the domestic chicken. European Journal of Clinical Chemistry and Clinical Biochemistry 34: 463-469.Google Scholar
CAIN, D.W. and CIDLOWSKI, J.A. (2017) Immune regulation by glucocorticoids. Nature Reviews Immunology 17: 233-247.Google Scholar
CALDER, W.A. and SCHMIDT-NIELSEN, K. (1968) Panting and blood carbon dioxide in birds. The American Journal of Physiology 215: 477-482.Google Scholar
CALEFI, A.S., DE SIQUEIRA, A., NAMAZU, L.B., COSTOLA-DE-SOUZA, C., HONDA, B.B., FERREIRA, A.J., QUINTEIRO-FILHO, W.M., DA, S.F.J. and PALERMO-NETO, J. (2016) 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.Google Scholar
CAO, Y., LI, Y.S., LI, Z.J., WANG, F. and LI, C.M. (2015) Dietary zinc may attenuate heat-induced testicular oxidative stress in mice via up-regulation of Cu-Zn SOD. Genetics and Molecular Research 14: 16616-16626.Google Scholar
CHAND, N., NAZ, S., KHAN, A., KHAN, S. and KHAN, R.U. (2014) Performance traits and immune response of broiler chicks treated with zinc and ascorbic acid supplementation during cyclic heat stress. International Journal of Biometeorology 58: 2153-2157.Google Scholar
CHARLES, D.A. and WALKER, A.W. (2002) Poultry Environment Problems: a Guide to Solutions. The Veterinary Journal 166: 284.Google Scholar
DAVIES, K.J. (1995) Oxidative stress: the paradox of aerobic life. Biochemical Society Symposium 61: 1-31.Google Scholar
DROGE, W. (2002) Free radicals in the physiological control of cell function. Physiological Reviews 82: 47-95.Google Scholar
DELEZIE, E., SWENNEN, Q., BUYSE, J. and DECUYPERE, E. (2007) The effect of feed withdrawal and crating density in transit on metabolism and meat quality of broilers at slaughter weight. Poultry Science 86: 1414-1423.Google Scholar
EBEID, T.A. (2012) Vitamin E and organic selenium enhances the antioxidative status and quality of chicken semen under high ambient temperature. British Poultry Science 53: 708-714.Google Scholar
EBEID, T.A., SUZUKI, T. and SUGIYAMA, T. (2012) High ambient temperature influences eggshell quality and calbindin-D28k localisation of eggshell gland and all intestinal segments of laying hens. Poultry Science 91: 2282-2287.Google Scholar
ELNAGAR, S.A., SCHEIDELER, S.E. and BECK, M.M. (2010) Reproductive hormones, hepatic deiodinase messenger ribonucleic acid, and vasoactive intestinal polypeptide-immunoreactive cells in hypothalamus in the heat stress-induced or chemically induced hypothyroid laying hen. Poultry Science 89: 2001-2009.Google Scholar
ESTEVEZ, I. (2007) Density allowances for broilers: where to set the limits? Poultry Science 86: 1265-1272.Google Scholar
FRAISSE, F. and COCKREM, J.F. (2006) Corticosterone and fear behaviour in white and brown caged laying hens. British Poultry Science 47: 110-119.Google Scholar
GERAERT, P.A., PADILHA, J.C. and GUILLAUMIN, S. (1996) Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: biological and endocrinological variables. British Journal of Nutrition 75: 205-216.Google Scholar
GHAZI, S., HABIBIAN, M., MOEINI, M.M. and ABDOLMOHAMMADI, A.R. (2012) Effects of different levels of organic and inorganic chromium on growth performance and immunocompetence of broilers under heat stress. Biological Trace Element Research 146: 309-317.Google Scholar
GITOEE, A., SADEGHI, G. and KARIMI, A. (2018) Combination effects of organic and inorganic chromium on production performance, reproductive response, immune status, and maternal antibody transmission in breeder quails under heat stress. Biological Trace Element Research 184: 508-516.Google Scholar
GOUS, R.M. and MORRIS, T.R. (2005) Nutritional interventions in alleviating the effects of high temperatures in broiler production. World's Poultry Science Journal 61: 463-466.Google Scholar
GREEN, D.R. and KROEMER, G. (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629.Google Scholar
GRIFFITHS, H.R. (2000) Antioxidants and protein oxidation. Free Radical Research 33 Supplement: 47-58.Google Scholar
HABIBIAN, M., GHAZI, S. and MOEINI, M.M. (2013) Lack of effect of dietary chromium supplementation on growth performance and serum insulin, glucose, and lipoprotein levels in broilers reared under heat stress condition. Biological Trace Element Research 153: 205-211.Google Scholar
HABIBIAN, M., GHAZI, S., MOEINI, M.M. and ABDOLMOHAMMADI, A. (2014) Effects of dietary selenium and vitamin E on immune response and biological blood parameters of broilers reared under thermoneutral or heat stress conditions. International Journal of Biometeorology 58: 741-752.Google Scholar
HABIBIAN, M., SADEGHI, G., GHAZI, S. and MOEINI, M.M. (2015) Selenium as a feed supplement for heat-stressed poultry: a review. Biological Trace Element Research 165: 183-193.Google Scholar
HALLIWELL, B. and WHITEMAN, M. (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? British Journal Pharmacology 142: 231-255.Google Scholar
HASHIZAWA, Y., KUBOTA, M., KADOWAKI, M. and FUJIMURA, S. (2013) Effect of dietary vitamin E on broiler meat qualities, color, water-holding capacity and shear force value, under heat stress conditions. Animal Science Journal 84: 732-736.Google Scholar
HEIDARISAFAR, Z., SADEGHI, G., KARIMI, A. and AZIZI, O. (2016) Apple peel waste as a natural antioxidant for heat-stressed broiler chickens. Tropical Animal Health and Production 48: 831-835.Google Scholar
HELED, Y., FLEISCHMANN, C. and EPSTEIN, Y. (2013) Cytokines and their role in hyperthermia and heat stroke. Journal of Basic and Clinical Physiology and Pharmacology 24: 85-96.Google Scholar
HICKMAN-MILLER, H.D. and HILDEBRAND, W.H. (2004) The immune response under stress: the role of HSP-derived peptides. Trends in Immunology 25: 427-433.Google Scholar
HOSSEINI-VASHAN, S.J., GOLIAN, A. and YAGHOBFAR, A. (2016) Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers fed diets supplemented with tomato pomace. International Journal of Biometeorology 60: 1183-1192.Google Scholar
HUNG, S.W., TU, C.Y. and WANG, W.S. (2007) In vivo effects of adding singular or combined anti-oxidative vitamins and/or minerals to diets on the immune system of tilapia (Oreochromis hybrids) peripheral blood monocyte-derived, anterior kidney-derived, and spleen-derived macrophages. Veterinary Immunology and Immunopathology 115: 87-99.Google Scholar
IKEDA, M., RHEE, M. and CHIN, W.W. (1994) Thyroid hormone receptor monomer, homodimer, and heterodimer (with retinoid-X receptor) contact different nucleotide sequences in thyroid hormone response elements. Endocrinology 135: 1628-1638.Google Scholar
IMIK, H., ATASEVER, M.A., URCAR, S., OZLU, H., GUMUS, R. and ATASEVER, M. (2012b) Meat quality of heat stress exposed broilers and effect of protein and vitamin E. British Poultry Science 53: 689-698.Google Scholar
IMIK, H., OZLU, H., GUMUS, R., ATASEVER, M.A., URCAR, S. and ATASEVER, M. (2012a) Effects of ascorbic acid and alpha-lipoic acid on performance and meat quality of broilers subjected to heat stress. British Poultry Science 53: 800-808.Google Scholar
JAHANIAN, R. and RASOULI, E. (2015) Dietary chromium methionine supplementation could alleviate immunosuppressive effects of heat stress in broiler chicks. Journal of Animal Science 93: 3355-3363.Google Scholar
KAMEL, N.N., AHMED, A., MEHAISEN, G., MASHALY, M.M. and ABASS, A.O. (2017) Depression of leukocyte protein synthesis, immune function and growth performance induced by high environmental temperature in broiler chickens. International Journal of Biometeorology 61: 1637-1645.Google Scholar
KANANI, P.B., DANESHYAR, M., ALIAKBARLU, J. and HAMIAN, F. (2017) Effect of dietary turmeric and cinnamon powders on meat quality and lipid peroxidation of broiler chicken under heat stress condition. Veterinary Research Forum 8: 163-169.Google Scholar
KAUL, G. and THIPPESWAMY, H. (2011) Role of heat shock proteins in diseases and their therapeutic potential. Indian Journal of Microbiology 51: 124-131.Google Scholar
KAUR, H. and HALLIWELL, B. (1994) Evidence for nitric oxide-mediated oxidative damage in chronic inflammation. Nitrotyrosine in serum and synovial fluid from rheumatoid patients. FEBS Letters 350: 9-12.Google Scholar
KAWAI, T. and AKIRA, S. (2009) The roles of TLRs, RLRs and NLRs in pathogen recognition. International Immunology 21: 317-337.Google Scholar
KHAJAVI, M., RAHIMI, S., HASSAN, Z.M., KAMALI, M.A. and MOUSAVI, T. (2003) Effect of feed restriction early in life on humoral and cellular immunity of two commercial broiler strains under heat stress conditions. British Poultry Science 44: 490-497.Google Scholar
KHAN, R.U., NAZ, S., NIKOUSEFAT, Z. and TUFARELLI, V. (2011) Effect of vitamin E in heat-stressed poultry. World's Poultry Science Journal 67: 469-487.Google Scholar
KHAN, R.U., LAUDADIO, V. and TUFARELLI, V. (2012) Semen traits and seminal plasma biochemical parameters in white leghorn layer breeders. Reproduction in Domestic Animals 47: 190-195.Google Scholar
KIECOLT-GLASER, J.K., LOVING, T.J., STOWELL, J.R., MALARKEY, W.B., LEMESHOW, S., DICKINSON, S.L. and GLASER, R. (2005) Hostile marital interactions, proinflammatory cytokine production, and wound healing. Archives of General Psychiatry 62: 1377-1384.Google Scholar
KIKUSATO, M. and TOYOMIZU, M. (2013) Crucial role of membrane potential in heat stress-induced overproduction of reactive oxygen species in avian skeletal muscle mitochondria. PLoS One 8: e64412.Google Scholar
KIKUSATO, M., RAMSEY, J.J., AMO, T. and TOYOMIZU, M. (2010) Application of modular kinetic analysis to mitochondrial oxidative phosphorylation in skeletal muscle of birds exposed to acute heat stress. FEBS Letters 584: 3143-3148.Google Scholar
KIKUSATO, M., YOSHIDA, H., FURUKAWA, K. and TOYOMIZU, M. (2015) Effect of heat stress-induced production of mitochondrial reactive oxygen species on NADPH oxidase and heme oxygenase-1 mRNA levels in avian muscle cells. Journal of Thermal Biology 52: 8-13.Google Scholar
LARA, L. and ROSTAGNO, M. (2013) Impact of Heat Stress on Poultry Production. Animals 3: 356-369.Google Scholar
LEE, Y.J., CHO, H.N., JEOUNG, D.I., SOH, J.W., CHO, C.K., BAE, S., CHUNG, H.Y., LEE, S.J. and LEE, Y.S. (2004) HSP25 overexpression attenuates oxidative stress-induced apoptosis: roles of ERK1/2 signaling and manganese superoxide dismutase. Free Radical Biology and Medicine 36: 429-444.Google Scholar
LIN, H., DECUYPERE, E. and BUYSE, J. (2006a) Acute heat stress induces oxidative stress in broiler chickens. Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology 144: 11-17.Google Scholar
LIN, H., JIAO, H.C., BUYSE, J. and DECUYPERE, E. (2006b) Strategies for preventing heat stress in poultry. World's Poultry Science Journal 62: 71-86.Google Scholar
LIN, H., WANG, L.F., SONG, J.L., XIE, Y.M. and YANG, Q.M. (2002) Effect of dietary supplemental levels of vitamin A on the egg production and immune responses of heat-stressed laying hens. Poultry Science 81: 458-465.Google Scholar
LIU, L.L., HE, J.H., XIE, H.B., YANG, Y.S., LI, J.C. and ZOU, Y. (2014) Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poultry Science 93: 54-62.Google Scholar
LIU, L., FU, C., YAN, M., XIE, H., LI, S., YU, Q., HE, S. and HE, J. (2016) Resveratrol modulates intestinal morphology and HSP70/90, NF-kappaB and EGF expression in the jejunal mucosa of black-boned chickens on exposure to circular heat stress. Food Function 7: 1329-1338.Google Scholar
LU, K.C., WANG, J.Y., LIN, S.H., CHU, P. and LIN, Y.F. (2004) Role of circulating cytokines and chemokines in exertional heatstroke. Critical Care Medicine 32: 399-403.Google Scholar
LU, Q., WEN, J. and ZHANG, H. (2007) Effect of chronic heat exposure on fat deposition and meat quality in two genetic types of chicken. Poultry Science 86: 1059-1064.Google Scholar
MACK, L.A., FELVER-GANT, J.N., DENNIS, R.L. and CHENG, H.W. (2013) Genetic variations alter production and behavioral responses following heat stress in 2 strains of laying hens. Poultry Science 92: 285-294.Google Scholar
MAHMOUD, K.Z. and EDENS, F.W. (2005) Influence of organic selenium on hsp70 response of heat-stressed and enteropathogenic Escherichia coli-challenged broiler chickens (Gallus gallus). Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 141: 69-75.Google Scholar
MAHMOUD, K.Z., EDENS, F.W., EISEN, E.J. and HAVENSTEIN, G.B. (2004) Ascorbic acid decreases heat shock protein 70 and plasma corticosterone response in broilers (Gallus gallus domesticus) subjected to cyclic heat stress. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 137: 35-42.Google Scholar
MAHMOUD, U.T., ABDEL-RAHMAN, M.A.M., DARWISH, M.H.A., APPLEGATE, T.J. and CHENG, H. (2015) Behavioral changes and feathering score in heat stressed broiler chickens fed diets containing different levels of propolis. Applied Animal Behaviour Science 166: 98-105.Google Scholar
MARSDEN, A. and MORRIS, T.R. (1987) Quantitative review of the effects of environmental temperature on food intake, egg output and energy balance in laying pullets. British Poultry Science. 28:693-704.Google Scholar
MIGNON-GRASTEAU, S., MORERI, U., NARCY, A., ROUSSEAU, X., RODENBURG, T.B., TIXIER-BOICHARD, M. and ZERJAL, T. (2015) Robustness to chronic heat stress in laying hens: a meta-analysis. Poultry Science 94: 586-600.Google Scholar
MIOVA, B., DIMITROVSKA, M., DINEVSKA-KJOVKAROVSKA, S., ESPLUGUES, J.V. and APOSTOLOVA, N. (2016) The Heat Stress Response and Diabetes: More Room for Mitochondrial Implication. Current Pharmaceutical Design 22: 2619-2639.Google Scholar
MUJAHID, A., SATO, K., AKIBA, Y. and TOYOMIZU, M. (2006) Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. Poultry Science 85: 1259-1265.Google Scholar
MUJAHID, A., YOSHIKI, Y., AKIBA, Y. and TOYOMIZU, M. (2005) Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poultry Science 84: 307-314.Google Scholar
MURALIDHARAN, S. and MANDREKAR, P. (2013) Cellular stress response and innate immune signaling: integrating pathways in host defense and inflammation. Journal of Leukocyte Biology 94: 1167-1184.Google Scholar
NARINÇ, D., ERDOĞAN, S., TAHTABIÇEN, E. and AKSOY, T. (2016) Effects of thermal manipulations during embryogenesis of broiler chickens on developmental stability, hatchability and chick quality. Animal 10: 1328-1335.Google Scholar
NIU, Z.Y., LIU, F.Z., YAN, Q.L. and LI, W.C. (2009) Effects of different levels of vitamin E on growth performance and immune responses of broilers under heat stress. Poultry Science 88: 2101-2107.Google Scholar
NYBLOM, H., BERGGREN, U., BALLDIN, J. and OLSSON, R. (2004) High AST/ALT ratio may indicate advanced alcoholic liver disease rather than heavy drinking. Alcohol and Alcoholism 39: 336-339.Google Scholar
ORHAN, C., AKDEMIR, F., SAHIN, N., TUZCU, M., KOMOROWSKI, J.R., HAYIRLI, A. and SAHIN, K. (2012) Chromium histidinate protects against heat stress by modulating the expression of hepatic nuclear transcription factors in quail. British Poultry Science 53: 828-835.Google Scholar
PADGETT, D.A. and GLASER, R. (2003) How stress influences the immune response. Trends in Immunology 24: 444-448.Google Scholar
PAMOK, S., AENGWANICH, W. and KOMUTRIN, T. (2009) Adaptation to oxidative stress and impact of chronic oxidative stress on immunity in heat-stressed broilers. Journal of Thermal Biology 34: 353-357.Google Scholar
PANDA, A.K., RAMARAO, S.V., RAJU, M.V. and CHATTERJEE, R.N. (2008) Effect of dietary supplementation with vitamins E and C on production performance, immune responses and antioxidant status of White Leghorn layers under tropical summer conditions. British Poultry Science 49: 592-599.Google Scholar
PAYNE, C.G. (1966) Practical Aspects of Environmental Temperature for Laying Hens. World's Poultry Science Journal e22: 126-139.Google Scholar
PERAI, A.H., KERMANSHAHI, H., NASSIRI, M.H. and ZARBAN, A. (2014) Effects of supplemental vitamin C and chromium on metabolic and hormonal responses, antioxidant status, and tonic immobility reactions of transported broiler chickens. Biological Trace Element Research 157: 224-233.Google Scholar
QUINTEIRO-FILHO, W.M., CALEFI, A.S., CRUZ, D., ALOIA, T., ZAGER, A., ASTOLFI-FERREIRA, C.S., PIANTINO, F.J., SHARIF, S. and PALERMO-NETO, J. (2017) Heat stress decreases expression of the cytokines, avian beta-defensins 4 and 6 and Toll-like receptor 2 in broiler chickens infected with Salmonella Enteritidis. Veterinary Immunology and Immunopathology 186: 19-28.Google Scholar
QUINTEIRO-FILHO, W.M., GOMES, A.V., PINHEIRO, M.L., RIBEIRO, A., FERRAZ-DE-PAULA, V., ASTOLFI-FERREIRA, C. S., FERREIRA, A.J. 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.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.Google Scholar
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 hypothalamic-pituitary-adrenal axis activation. Journal of Animal Science 90: 1986-1994.Google Scholar
RAFIEE, F., MAZHARI, M., GHOREISHI, M. and ESMAEILIPOUR, O. (2016) Effect of lemon verbena powder and vitamin C on performance and immunity of heat-stressed broilers. Journal of Animal Physiology and Animal Nutrition (Berl) 100: 807-812.Google Scholar
RAGHEBIAN, M., SADEGHI, A.A. and AMINAFSHAR, M. (2016) Energy sources and levels influenced on performance parameters, thyroid hormones, and HSP70 gene expression of broiler chickens under heat stress. Tropical Animal Health and Production 48: 1697-1702.Google Scholar
RAO, S.V., PRAKASH, B., RAJU, M.V., PANDA, A.K., KUMARI, R.K. and REDDY, E.P. (2016) Effect of Supplementing Organic Forms of Zinc, Selenium and Chromium on Performance, Anti-Oxidant and Immune Responses in Broiler Chicken Reared in Tropical Summer. Biological Trace Element Research 172: 511-520.Google Scholar
RAO, S.V., RAJU, M.V., PANDA, A.K., POONAM, N.S., MURTHY, O.K. and SUNDER, G.S. (2012) Effect of dietary supplementation of organic chromium on performance, carcass traits, oxidative parameters, and immune responses in commercial broiler chickens. Biological Trace Element Research 147: 135-141.Google Scholar
REHMAN, Z.U., CHAND, N. and KHAN, R.U. (2017) The effect of vitamin E, L-carnitine, and ginger on production traits, immune response, and antioxidant status in two broiler strains exposed to chronic heat stress. Environmental Science and Pollution Research International 24: 26851-26857.Google Scholar
RENAUDEAU, D., COLLIN, A., YAHAV, S., DE BASILIO, V., GOURDINE, J.L. and COLLIER, R.J. (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6: 707-728.Google Scholar
RICHTER, C., PARK, J.W. and AMES, B.N. (1988) Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proceedings of The National Academy of Sciences of The United States of America 85: 6465-6467.Google Scholar
RIMOLDI, S., LASAGNA, E., SARTI, F.M., MARELLI, S.P., COZZI, M.C., BERNARDINI, G. and TEROVA, G. (2015) Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions. Meta Gene 6: 17-25.Google Scholar
SAFDARI-ROSTAMABAD, M., HOSSEINI-VASHAN, S.J., PERAI, A.H. and SARIR, H. (2017) Nanoselenium supplementation of heat-stressed broilers: effects on performance, carcass characteristics, blood metabolites, immune response, antioxidant status, and jejunal morphology. Biological Trace Element Research 178: 105-116.Google Scholar
SAHIN, K., ORHAN, C., TUZCU, M., ALI, S., SAHIN, N. and HAYIRLI, A. (2010) Epigallocatechin-3-gallate prevents lipid peroxidation and enhances antioxidant defense system via modulating hepatic nuclear transcription factors in heat-stressed quails. Poultry Science 89: 2251-2258.Google Scholar
SAHIN, N., ONDERCI, M., BALCI, T.A., CIKIM, G., SAHIN, K. and KUCUK, O. (2007) The effect of soy isoflavones on egg quality and bone mineralisation during the late laying period of quail. British Poultry Science 48: 363-369.Google Scholar
SCHMIDT, K.L., FURLONGER, A.A., LAPIERRE, J.M., MACDOUGALL-SHACKLETON, E.A. and MACDOUGALL-SHACKLETON, S.A. (2012) Regulation of the HPA axis is related to song complexity and measures of phenotypic quality in song sparrows. Hormones and Behavior 61: 652-659.Google Scholar
SINGH, H., SODHI, S. and KAUR, R. (2006) Effects of dietary supplements of selenium, vitamin E or combinations of the two on antibody responses of broilers. British Poultry Science 47: 714-719.Google Scholar
SONG, Z., CHENG, K., ZHANG, L. and WANG, T. (2017) Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat-stressed broilers. Journal of Thermal Biology 69: 184-190.Google Scholar
SONG, Z., LIU, L., SHEIKHAHMADI, A., JIAO, H. and LIN, H. (2012) Effect of heat exposure on gene expression of feed intake regulatory peptides in laying hens. Journal of Biomedicine and Biotechnology 2012: 1-8.Google Scholar
STAR, L., DECUYPERE, E., PARMENTIER, H.K. and KEMP, B. (2008) Effect of single or combined climatic and hygienic stress in four layer lines: 2. Endocrine and oxidative stress responses. Poultry Science 87: 1031-1038.Google Scholar
STARKIE, R.L., HARGREAVES, M., ROLLAND, J. and FEBBRAIO, M.A. (2005) Heat stress, cytokines, and the immune response to exercise. Brain Behavior and Immunity 19: 404-412.Google Scholar
STEINMANN, M., MOOSMANN, N., SCHIMMEL, M., GERHARDUS, C. and BAUER, G. (2004) Differential role of extra- and intracellular superoxide anions for nitric oxide-mediated apoptosis induction. In Vivo 18: 293-309.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-E77.Google Scholar
SYAFWAN, S., KWAKKEL, R.P. and VERSTEGEN, M.W.A. (2011) Heat stress and feeding strategies in meat-type chickens. World's Poultry Science Journal 67: 653-674.Google Scholar
TAN, G.Y., YANG, L., FU, Y.Q., FENG, J.H. and ZHANG, M.H. (2010) Effects of different acute high ambient temperatures on function of hepatic mitochondrial respiration, antioxidative enzymes, and oxidative injury in broiler chickens. Poultry Science 89: 115-122.Google Scholar
TANG, J. and CHEN, Z. (2016) The protective effect of gamma-aminobutyric acid on the development of immune function in chickens under heat stress. Journal of Animal Physiology and Animal Nutrition (Berl) 100: 768-777.Google Scholar
TANKSON, J.D., VIZZIER-THAXTON, Y., THAXTON, J.P., MAY, J.D. and CAMERON, J.A. (2001) Stress and nutritional quality of broilers. Poultry Science 80: 1384-1389.Google Scholar
TORKI, M., ZANGENEH, S. and HABIBIAN, M. (2014) Performance, egg quality traits, and serum metabolite concentrations of laying hens affected by dietary supplemental chromium picolinate and vitamin C under a heat-stress condition. Biological Trace Element Research 157: 120-129.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: e138975.Google Scholar
VINCENT, J.B. (2000) The biochemistry of chromium. Journal of Nutrition 130: 715-718.Google Scholar
WAN, X., JIANG, L., ZHONG, H., LU, Y., ZHANG, L. and WANG, T. (2017a) Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress. Animal Science Journal 88: 1239-1246.Google Scholar
WAN, X., ZHANG, J., HE, J., BAI, K., ZHANG, L. and WANG, T. (2017b) Dietary enzymatically treated Artemisia annua L. supplementation alleviates liver oxidative injury of broilers reared under high ambient temperature. International Journal of Biometeorology 61: 1629-1636.Google Scholar
WANG, W.C., YAN, F.F., HU, J.Y., AMEN, O.A. and CHENG, H.W. (2018) Supplementation of Bacillus subtilis based probiotic reduces heat stress-related behaviors and inflammatory response in broiler chickens. Journal of Animal Science 96: 1654-1666.Google Scholar
WILLIAMS, G.R. and BASSETT, J.H. (2011) Deiodinases: the balance of thyroid hormone: local control of thyroid hormone action: role of type 2 deiodinase. Journal of Endocrinology 209: 261-272.Google Scholar
WOOD, Z.A., POOLE, L.B. and KARPLUS, P.A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653.Google Scholar
XIE XIE, J., TANG, L., TANGLI LIN LU, Z.L., LIN, X., LIU, H.C., ODLE, J. and LUO, X. (2015) Effects of acute and chronic heat stress on plasma metabolites, hormones and oxidant status in restrictedly fed broiler breeders. Poultry Science 94: 1635-1644.Google Scholar
XU, D. and TIAN, Y. (2015) Selenium and Polysaccharides of Atractylodes macrocephala Koidz Play Different Roles in Improving the Immune Response Induced by Heat Stress in Chickens. Biological Trace Element Research 168: 235-241.Google Scholar
XU, D., LI, B., CAO, N., LI, W., TIAN, Y. and HUANG, Y. (2017) The protective effects of polysaccharide of Atractylodes macrocephala Koidz (PAMK) on the chicken spleen under heat stress via antagonizing apoptosis and restoring the immune function. Oncotarget 8: 70394-70405.Google Scholar
XU, D., LI, W., HUANG, Y., HE, J. and TIAN, Y. (2014) The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on immune response in chicken spleen under heat stress. Biological Trace Element Research 160: 232-237.Google Scholar
YAHAV, S., COLLIN, A., SHINDER, D. and PICARD, M. (2004) Thermal manipulations during broiler chick embryogenesis: effects of timing and temperature. Poult Sci 83: 1959-1963.Google Scholar
YANG, Y., SHARMA, R., SHARMA, A., AWASTHI, S. and AWASTHI, Y.C. (2003) Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling. Acta Biochimica Polonica 50: 319-336.Google Scholar
ZABOLI, G.R., RAHIMI, S., SHARIATMADARI, F., TORSHIZI, M.A., BAGHBANZADEH, A. and MEHRI, M. (2017) Thermal manipulation during Pre and Post-Hatch on thermotolerance of male broiler chickens exposed to chronic heat stress. Poultry Science 96: 478-485.Google Scholar
ZHANG, C., ZHAO, X., WANG, L., YANG, L., CHEN, X. and GENG, Z. (2017) Resveratrol beneficially affects meat quality of heat-stressed broilers which is associated with changes in muscle antioxidant status. Animal Science Journal 88: 1569-1574.Google Scholar
ZHANG, Z.Y., JIA, G.Q., ZUO, J.J., ZHANG, Y., LEI, J., REN, L. and FENG, D.Y. (2012) Effects of constant and cyclic heat stress on muscle metabolism and meat quality of broiler breast fillet and thigh meat. Poultry Science 91: 2931-2937.Google Scholar
ZHAO, Q.L., FUJIWARA, Y. and KONDO, T. (2006) Mechanism of cell death induction by nitroxide and hyperthermia. Free Radical Biology and Medicine 40: 1131-1143.Google Scholar
ZHU, W., JIANG, W. and WU, L.Y. (2014) Dietary L-arginine supplement alleviates hepatic heat stress and improves feed conversion ratio of Pekin ducks exposed to high environmental temperature. Journal of Animal Physiology and Animal Nutrition (Berl) 98: 1124-1131.Google Scholar
ZHU, Y.W., LI, W.X., LU, L., ZHANG, L.Y., JI, C., LIN, X., LIU, H.C., ODLE, J. and LUO, X.G. (2017) Impact of maternal heat stress in conjunction with dietary zinc supplementation on hatchability, embryonic development, and growth performance in offspring broilers. Poultry Science 96: 2351-2359.Google Scholar
ZUO, J., XU, M., ABDULLAHI, Y.A., MA, L., ZHANG, Z. and FENG, D. (2015) Constant heat stress reduces skeletal muscle protein deposition in broilers. Journal of The Science of Food and Agriculture 95: 429-436.Google Scholar