Growth performance, duodenal morphology and the caecal microbial population in female broiler chickens fed glycine-fortified low protein diets under heat stress conditions

References

• Akinde, D. O. 2014a. “Amino Acid Efficiency with Dietary Glycine Supplementation: Part 2.” World’s Poultry Science Journal 70: 575–584. doi:10.1017/S0043933914000622.
   Web of Science ®Google Scholar
• Akinde, D. O. 2014b. “Amino Acid Efficiency with Dietary Glycine Supplementation: Part 1.” World’s Poultry Science Journal 70: 461–474. doi:10.1017/S004393391400052X.
   Web of Science ®Google Scholar
• Altan, Ö., A. Pabuçcuoğlu, A. Altan, S. Konyalioğlu, and H. Bayraktar. 2003. “Effect of Heat Stress on Oxidative Stress, Lipid Peroxidation and Some Stress Parameters in Broilers.” British Poultry Science 44: 545–550. doi:10.1080/00071660310001618334.
   PubMed Web of Science ®Google Scholar
• AOAC. 1990. Official Methods of Analysis. 15th ed. Arlington,VA: AOAC.
   Google Scholar
• Awad, E. A., M. Fadlullah, I. Zulkifli, A. F. Soleimani, and T. C. Loh. 2014b. “Amino Acids Fortification of Low-Protein Diet for Broilers under Tropical Climate: Ideal Essential Amino Acids Profile.” Italian Journal of Animal Science 13: 270–274. doi:10.4081/ijas.2014.3166.
   Web of Science ®Google Scholar
• Awad, E. A., I. Zulkifli, A. F. Soleimani, and A. Aljuobori. 2017. “Effects of Feeding Male and Female Broiler Chickens on Low-Protein Diets Fortified with Different Dietary Glycine Levels under the Hot and Humid Tropical Climate.” Italian Journal of Animal Science 16: 453–461. doi:10.1080/1828051X.2017.1291288.
   Web of Science ®Google Scholar
• Awad, E. A., I. Zulkifli, A. F. Soleimani, and T. C. Loh. 2014a. “Amino Acids Fortification of Low-Protein Diet for Broilers under Tropical Climate. 2. Nonessential Amino Acids and Increasing Essential Amino Acids.” Italian Journal of Animal Science 13: 631–636. doi:10.4081/ijas.2014.3297.
   Web of Science ®Google Scholar
• Awad, E. A., I. Zulkifli, A. F. Soleimani, and T. C. Loh. 2015. “Individual Non-Essential Amino Acids Fortification of a Low-Protein Diet for Broilers under the Hot and Humid Tropical Climate.” Poultry Science 94: 2772–2777. doi:10.3382/ps/pev258.
   PubMed Web of Science ®Google Scholar
• Baker, D. H. 1997. Ideal Amino Acid Profiles for Swine and Poultry and Their Applications in Feed Formulation. Biokyowa Technical Review Cape Girardeau, MO, Biokyowa 9:15–19.
   Google Scholar
• Baker, D. H. 2003. “Ideal Amino Acid Patterns for Broiler Chicks.” In Amino Acids in Animal Nutrition, Ed J. F. D’Mello, 223–235. Wallinford, UK,: CAB International.
   Google Scholar
• Baker, D. H. 2009. “Advances in Protein–Amino Acid Nutrition of Poultry.” Amino Acids 37: 29–41. doi:10.1007/s00726-008-0198-3.
   PubMed Web of Science ®Google Scholar
• Balnave, D. 2004. “Challenges of Accurately Defining the Nutrient Requirements of Heat-Stressed Poultry.” Poultry Science 83: 5–14. doi:10.1093/ps/83.1.5.
   PubMed Web of Science ®Google Scholar
• Bonnet, S., P. A. Geraert, M. Lessire, B. Carre, and S. Guillaumin. 1997. “Effect of High Ambient Temperature on Feed Digestibility in Broilers.” Poultry Science 76: 857–863. doi:10.1093/ps/76.6.857.
   PubMed Web of Science ®Google Scholar
• Bregendahl, K., J. L. Sell, and D. R. Zimmerman. 2002. “Effect of Low-Protein Diets on Growth Performance and Body Composition of Broiler Chicks.” Poultry Science 81: 1156–1167. doi:10.1093/ps/81.8.1156.
   PubMed Web of Science ®Google Scholar
• Burkholder, K., K. Thompson, M. Einstein, T. Applegate, and J. Patterson. 2008. “Influence of Stressors on Normal Intestinal Microbiota, Intestinal Morphology, and Susceptibility to Salmonella Enteritidis Colonization in Broilers.” Poultry Science 87: 1734–1741. doi:10.3382/ps.2008-00107.
   PubMed Web of Science ®Google Scholar
• Buyse, J., E. Decuypere, L. Berghman, E. R. Kuhn, and F. Vandesande. 1992. “Effect of Dietary Protein Content on Episodic Growth Hormone Secretion and on Heat Production of Male Broiler Chickens.” British Poultry Science 33: 1101–1109. doi:10.1080/00071669208417552.
   PubMed Web of Science ®Google Scholar
• Campos, D., M. Macari, M. Fernadez-Alarcon, W. Nogueira, F. De Souza, F. Hada, R. Lunedo, and J. Denadai. 2016. “Performance and Carbon Turnover in Fast-And Slow-Growing Broilers Submitted to Cyclic Heat Stress and Fed on High-Protein Diets.” British Poultry Science 57: 84–92. doi:10.1080/00071668.2015.1115467.
   PubMed Web of Science ®Google Scholar
• Cant, J. P., B. W. Mcbride, and W. J. Croom. 1996. “The Regulation of Intestinal Metabolism and Its Impact on Whole Animal Energetics.” Journal of Animal Science 74: 2541–2553. doi:10.2527/1996.74102541x.
   PubMed Web of Science ®Google Scholar
• Carew, L., K. Evarts, and F. Alster. 1997. “Growth and Plasma Thyroid Hormone Concentrations of Chicks Fed Diets Deficient in Essential Amino Acids.” Poultry Science 76: 1398–1404. doi:10.1093/ps/76.10.1398.
   PubMed Web of Science ®Google Scholar
• Cheng, T. K., M. L. Hamre, and C. N. Coon. 1997. “Responses of Broilers to Dietary Protein Levels and Amino Acid Supplementation to Low Protein Diets at Various Environmental Temperatures.” Journal of Applied Poultry Research 6: 18–33. doi:10.1093/japr/6.1.18.
   Web of Science ®Google Scholar
• Cheng, T. K., M. L. Hamre, and C. N. Coon. 1999. “Effect of Constant and Cyclic Environmental Temperatures, Dietary Protein, and Amino Acid Levels on Broiler Performance.” The Journal of Applied Poultry Research 8: 426–439. doi:10.1093/japr/8.4.426.
   Web of Science ®Google Scholar
• Coon, C., A. Sowers, and J. Couch. 1975. “Effect of Various Concentrations of Protein in Chick Diet upon the Metabolic Enzymes of Glycine and Serine.” Poultry Science 54: 1461–1467. doi:10.3382/ps.0541461.
   PubMed Web of Science ®Google Scholar
• Corzo, A., C. A. Fritts, M. T. Kidd, and B. J. Kerr. 2005. “Response of Broiler Chicks to Essential and Non-Essential Amino Acid Supplementation of Low Crude Protein Diets.” Animal Feed Science and Technology 118: 319–327. doi:10.1016/j.anifeedsci.2004.11.007.
   Web of Science ®Google Scholar
• Corzo, A., M. T. Kidd, D. J. Burnham, and B. J. Kerr. 2004. “Dietary Glycine Needs of Broiler Chicks.” Poultry Science 83: 1382–1384. doi:10.1093/ps/83.8.1382.
   PubMed Web of Science ®Google Scholar
• Dean, D. W., T. D. Bidner, and L. L. Southern. 2006. “Glycine Supplementation to Low Protein, Amino Acid-Supplemented Diets Supports Optimal Performance of Broiler Chicks.” Poultry Science 85: 288–296. doi:10.1093/ps/85.2.288.
   PubMed Web of Science ®Google Scholar
• Durant, J. A., D. E. Corrier, J. A. Byrd, L. H. Stanker, and S. C. Ricke. 1999. “Feed Deprivation Affects Crop Environment and Modulates Salmonella Enteritidis Colonization and Invasion of Leghorn Hens.” Applied and Environmental Microbiology 65: 1919–1923.
   PubMed Web of Science ®Google Scholar
• Dziewanowska, K., A. R. Carson, J. M. Patti, C. F. Deobald, K. W. Bayles, and G. A. Bohach. 2000. “Staphylococcal Fibronectin Binding Protein Interacts with Heat Shock Protein 60 and Integrins: Role in Internalization by Epithelial Cells.” Infection and Immunity 68: 6321–6328. doi:10.1128/IAI.68.11.6321-6328.2000.
   PubMed Web of Science ®Google Scholar
• Farouk, M. M., H. M. Al-Mazeedi, A. B. Sabow, A. E. D. Bekhit, K. D. Adeyemi, A. Q. Sazili, and A. Ghani. 2014. “Halal and Kosher Slaughter Methods and Meat Quality: A Review.” Meat Science 98: 505–519. doi:10.1016/j.meatsci.2014.05.021.
   PubMed Web of Science ®Google Scholar
• Ferguson, N. S., R. S. Gates, J. L. Taraba, A. H. Cantor, A. J. Pescatore, M. J. Ford, and D. J. Burnham. 1998. “The Effect of Dietary Crude Protein on Growth, Ammonia Concentration, and Litter Composition in Broilers.” Poultry Science 77: 1481–1487. doi:10.1093/ps/77.10.1481.
   PubMed Web of Science ®Google Scholar
• Ferket, P., E. Van Heugten, T. Van Kempen, and R. Angel. 2002. “Nutritional Strategies to Reduce Environmental Emissions from Nonruminants.” Journal of Animal Science 80: E168–E182. doi:10.2527/animalsci2002.80E-Suppl_2E168x.
   Google Scholar
• Jin, L., L. Reynolds, D. Redmer, J. Caton, and J. Crenshaw. 1994. “Effects of Dietary Fiber on Intestinal Growth, Cell Proliferation, and Morphology in Growing Pigs.” Journal of Animal Science 72: 2270–2278. doi:10.2527/1994.7292270x.
   PubMed Web of Science ®Google Scholar
• Laudadio, V., L. Passantino, A. Perillo, G. Lopresti, A. Passantino, R. Khan, and V. Tufarelli. 2012. “Productive Performance and Histological Features of Intestinal Mucosa of Broiler Chickens Fed Different Dietary Protein Levels.” Poultry Science 91: 265–270. doi:10.3382/ps.2011-01675.
   PubMed Web of Science ®Google Scholar
• Leeson, S. 1986. “Nutritional Considerations of Poultry during Heat Stress.” World’s Poultry Science Journal 42: 69–81. doi:10.1079/WPS19860007.
   Web of Science ®Google Scholar
• Lensing, M., J. Van Der Klis, L. Le Bellego, and M. Rovers (2007) The Threonine Requirement of Broiler Chickens during Subclinical Intestinal Infection. In World Poultry Science Association, Proceedings of the 16th European Symposium on Poultry Nutrition, Strasbourg, France, 26-30 August, 2007, pp. 343–346.
   Google Scholar
• Mack, L., J. Felver-Gant, R. Dennis, and H. W. Cheng. 2013. “Genetic Variations Alter Production and Behavioral Responses following Heat Stress in 2 Strains of Laying Hens.” Poultry Science 92: 285–294. doi:10.3382/ps.2012-02589.
   PubMed Web of Science ®Google Scholar
• Meddings, J. B., and M. Swain. 2000. “Environmental Stress–Induced Gastrointestinal Permeability Is Mediated by Endogenous Glucocorticoids in the Rat.” Gastroenterology 119: 1019–1028. doi:10.1053/gast.2000.18152.
   PubMed Web of Science ®Google Scholar
• Mohamed, E. A. A., O. H. A. Ali, E. E. Huwaida, and I. A. Yousif. 2012. “Effect of Season and Dietary Protein Level on Some Haematological Parameters and Blood Biochemical Compositions of Three Broiler Strains.” International Journal of Poultry Science 11: 787–793. doi:10.3923/ijps.2012.787.793.
   Google Scholar
• Moran, E. T. 2014. “Intestinal Events and Nutritional Dynamics Predispose Clostridium Perfringens Virulence in Broilers.” Poultry Science 93: 3028–3036. doi:10.3382/ps.2014-04313.
   PubMed Web of Science ®Google Scholar
• Mosca, F., C. Kuster, S. Stella, G. Farina, M. Madeddu, L. Zaniboni, and S. Cerolini. 2016. “Growth Performance, Carcass Characteristics and Meat Composition of Milanino Chickens Fed on Diets with Different Protein Concentrations.” British Poultry Science 57: 531–537. doi:10.1080/00071668.2016.1174768.
   PubMed Web of Science ®Google Scholar
• Musharaf, N. A., and J. D. Latshaw. 1999. “Heat Increment as Affected by Protein and Amino Acid Nutrition.” World’s Poultry Science Journal 55: 233–240. doi:10.1079/WPS19990017.
   Web of Science ®Google Scholar
• NRC. 1994. Nutrient Requirements of Poultry. 9th revised edition ed. Washington, DC: National Academy Press.
   Google Scholar
• Ospina-Rojas, I. C., A. E. Murakami, C. R. A. Duarte, C. Eyng, C. A. L. Oliveira, and V. Janeiro. 2014. “Valine, Isoleucine, Arginine and Glycine Supplementation of Low-Protein Diets for Broiler Chickens during the Starter and Grower Phases.” British Poultry Science 55: 766–773. doi:10.1080/00071668.2014.970125.
   PubMed Web of Science ®Google Scholar
• Ospina-Rojas, I. C., A. E. Murakami, I. Moreira, K. P. Picoli, R. J. B. Rodrigueiro, and A. C. Furlan. 2013. “Dietary Glycine+ Serine Responses of Male Broilers Given Low-Protein Diets with Different Concentrations of Threonine.” British Poultry Science 54: 486–493. doi:10.1080/00071668.2013.794257.
   PubMed Web of Science ®Google Scholar
• Paulus, U., C. S. Potten, and M. Loeffler. 1992. “A Model of the Control of Cellular Regeneration in the Intestinal Crypt after Perturbation Based Solely on Local Stem Cell Regulation.” Cell Proliferation 25: 559–578. doi:10.1111/j.1365-2184.1992.tb01460.x.
   PubMed Web of Science ®Google Scholar
• Pearce, S. C., V. Mani, R. L. Boddicker, J. S. Johnson, T. E. Weber, J. W. Ross, R. P. Rhoads, L. H. Baumgard, and N. K. Gabler. 2013. “Heat Stress Reduces Intestinal Barrier Integrity and Favors Intestinal Glucose Transport in Growing Pigs.” PloS One 8: e70215. doi:10.1371/journal.pone.0070215.
   PubMed Web of Science ®Google Scholar
• Quinteiro-Filho, W., A. Ribeiro, V. Ferraz-De-Paula, M. Pinheiro, M. Sakai, L. Sá, A. Ferreira, and J. Palermo-Neto. 2010. “Heat Stress Impairs Performance Parameters, Induces Intestinal Injury, and Decreases Macrophage Activity in Broiler Chickens.” Poultry Science 89: 1905–1914. doi:10.3382/ps.2010-00812.
   PubMed Web of Science ®Google Scholar
• Rezaei, S., M. F. Jahromi, J. B. Liang, I. Zulkifli, A. S. Farjam, V. Laudadio, and V. Tufarelli. 2015. “Effect of Oligosaccharides Extract from Palm Kernel Expeller on Growth Performance, Gut Microbiota and Immune Response in Broiler Chickens.” Poultry Science 94: 2414–2420. doi:10.3382/ps/pev216.
   PubMed Web of Science ®Google Scholar
• Savory, C. J. 1986. “Influence of Ambient Temperature on Feeding Activity Parameters and Digestive Function in Domestic Fowls.” Physiology & Behavior 38: 353–357. doi:10.1016/0031-9384(86)90106-X.
   PubMed Web of Science ®Google Scholar
• Silva, J. E. 1995. “Thyroid Hormone Control of Thermogenesis and Energy Balance.” Thyroid 5: 481–492. doi:10.1089/thy.1995.5.481.
   PubMed Web of Science ®Google Scholar
• Sohail, M., M. Hume, J. Byrd, D. Nisbet, A. Ijaz, A. Sohail, M. Shabbir, and H. Rehman. 2012. “Effect of Supplementation of Prebiotic Mannan-Oligosaccharides and Probiotic Mixture on Growth Performance of Broilers Subjected to Chronic Heat Stress.” Poultry Science 91: 2235–2240. doi:10.3382/ps.2012-02182.
   PubMed Web of Science ®Google Scholar
• Soleimani, A. F., I. Zulkifli, M. Hair-Bejo, A. R. Omar, and A. R. Raha. 2012. “The Role of Heat Shock Protein 70 in Resistance to Salmonella Enteritidis in Broiler Chickens Subjected to Neonatal Feed Restriction and Thermal Stress.” Poultry Science 91: 340–345. doi:10.3382/ps.2011-01703.
   PubMed Web of Science ®Google Scholar
• Song, J., K. Xiao, Y. L. Ke, L. F. Jiao, C. H. Hu, Q. Y. Diao, B. Shi, and X. T. Zou. 2014. “Effect of a Probiotic Mixture on Intestinal Microflora, Morphology, and Barrier Integrity of Broilers Subjected to Heat Stress.” Poultry Science 93: 581–588. doi:10.3382/ps.2013-03455.
   PubMed Web of Science ®Google Scholar
• Thompson, K., and T. Applegate. 2006. “Feed Withdrawal Alters Small-Intestinal Morphology and Mucus of Broilers.” Poultry Science 85: 1535–1540. doi:10.1093/ps/85.9.1535.
   PubMed Web of Science ®Google Scholar
• Uni, Z. 1999. “Functional Development of the Small Intestine in Domestic Birds: Cellular and Molecular Aspects.” Poultry and Avian Biology Reviews 10: 167–179.
   Google Scholar
• Waldroup, P. W., Q. Jiang, and C. A. Fritts. 2005. “Effects of Glycine and Threonine Supplementation on Performance of Broiler Chicks Fed Diets Low in Crude Protein.” International Journal of Poultry Science 4: 250–257. doi:10.3923/ijps.2005.250.257.
   Google Scholar
• Wehkamp, J., J. Harder, K. Wehkamp, B. Wehkamp-Von Meissner, M. Schlee, C. Enders, U. Sonnenborn, S. Nuding, S. Bengmark, and K. Fellermann. 2004. “NF-κB-and AP-1-mediated Induction of Human Beta Defensin-2 in Intestinal Epithelial Cells by Escherichia Coli Nissle 1917: A Novel Effect of a Probiotic Bacterium.” Infection and Immunity 72: 5750–5758. doi:10.1128/IAI.72.10.5750-5758.2004.
   PubMed Web of Science ®Google Scholar
• Wolfenson, D., D. Sklan, Y. Graber, O. Kedar, I. Bengal, and S. Hurwitz. 1987. “Absorption of Protein, Fatty Acids and Minerals in Young Turkeys under Heat and Cold Stress.” British Poultry Science 28: 739–742. doi:10.1080/00071668708417010.
   PubMed Web of Science ®Google Scholar
• Yason, C. V., B. A. Summers, and K. A. Schat. 1987. “Pathogenesis of Rotavirus Infection in Various Age Groups of Chickens and Turkeys: Pathology.” American Journal of Veterinary Research 48: 927–938.
   PubMed Web of Science ®Google Scholar
• Zaghari, M., F. Zaefarian, and M. Shivazad. 2011. “Standardized Ileal Digestible Threonine Requirements and Its Effects on Performance and Gut Morphology of Broiler Chicks Fed Two Levels of Protein.” Journal of Agricultural Science and Technology 13: 541–552.
   Web of Science ®Google Scholar
• Zaman, Q. U., T. Mushtaq, H. Nawaz, M. A. Mirza, S. Mahmood, T. Ahmad, M. E. Babar, and M. M. H. Mushtaq. 2008. “Effect of Varying Dietary Energy and Protein on Broiler Performance in Hot Climate.” Animal Feed Science and Technology 146: 302–312. doi:10.1016/j.anifeedsci.2008.01.006.
   Web of Science ®Google Scholar
• Zhang, A. W., B. D. Lee, S. K. Lee, K. W. Lee, G. H. An, K. B. Song, and C. H. Lee. 2005. “Effects of Yeast (Saccharomyces Cerevisiae) Cell Components on Growth Performance, Meat Quality, and Ileal Mucosa Development of Broiler Chicks.” Poultry Science 84: 1015–1021. doi:10.1093/ps/84.7.1015.
   PubMed Web of Science ®Google Scholar
• Zhou, W., M. Fujita, and S. Yamamoto. 1999. “Effects of Ambient Temperatures on Blood Viscosity and Plasma Protein Concentration of Broiler Chickens (Gallus Domesticus).” Journal of Thermal Biology 24: 105–112. doi:10.1016/S0306-4565(98)00045-X.
   Web of Science ®Google Scholar
• Zuo, J., M. Xu, Y. A. Abdullahi, L. Ma, Z. Zhang, and D. Feng. 2015. “Constant Heat Stress Reduces Skeletal Muscle Protein Deposition in Broilers.” Journal of the Science of Food and Agriculture 95: 429–436. doi:10.1002/jsfa.2015.95.issue-2.
   PubMed Web of Science ®Google Scholar