Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-30T20:06:06.276Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of l-leucine in ovo feeding on thermotolerance, growth and amino acid metabolism under heat stress in broilers

Published online by Cambridge University Press:  16 March 2020

G. Han ,
Y. Ouchi ,
T. Hirota ,
S. Haraguchi ,
T. Miyazaki ,
T. Arakawa ,
N. Masuhara ,
W. Mizunoya ,
R. Tatsumi  and
K. Tashiro
...Show all authors
G. Han
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
Y. Ouchi
Affiliation:
Department of Bioresource Science, Graduate School of Biosphere Science, Hiroshima University, 1-3-2 Kagamiyama, Higashi-Hiroshima739-8528, Japan
T. Hirota
Affiliation:
Department of Bioresource Science, Graduate School of Biosphere Science, Hiroshima University, 1-3-2 Kagamiyama, Higashi-Hiroshima739-8528, Japan
S. Haraguchi
Affiliation:
Department of Biochemistry, Showa University School of Medicine, 1-5-8 Hatanodai, Tokyo142-8555, Japan
T. Miyazaki
Affiliation:
Department of Biochemistry, Showa University School of Medicine, 1-5-8 Hatanodai, Tokyo142-8555, Japan
T. Arakawa
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
N. Masuhara
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
W. Mizunoya
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
R. Tatsumi
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
K. Tashiro
Affiliation:
Department of Bioscience and Biotechnology, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
T. Bungo
Affiliation:
Department of Bioresource Science, Graduate School of Biosphere Science, Hiroshima University, 1-3-2 Kagamiyama, Higashi-Hiroshima739-8528, Japan
M. Furuse
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
V. S. Chowdhury*
Affiliation:
Department of Bioresource Sciences, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan Division for Experimental Natural Science, Faculty of Arts and Science, Kyushu University, 744 Motooka, Fukuoka819-0395, Japan
*
†E-mail: [email protected]
Get access

Abstract

Recently, we found that in ovo feeding of l-leucine (l-Leu) afforded thermotolerance, stimulated lipid metabolism and modified amino acid metabolism in male broiler chicks. However, the effects of in ovo feeding of l-Leu on thermoregulation and growth performance until marketing age of broilers are still unknown. In this study, we investigated the effects of in ovo feeding of l-Leu on body weight (BW) gain under control thermoneutral temperature or chronic heat stress. We measured changes of body temperature and food intake, organ weight, as well as amino acid metabolism and plasma metabolites under acute and chronic heat stress in broilers. A total of 168 fertilized Chunky broiler eggs were randomly divided into 2 treatment groups in experiments. The eggs were in ovo fed with l-Leu (34.5 µmol/500 µl per egg) or sterile water (500 µl/egg) during incubation. After hatching, male broilers were selected and assigned seven to nine replicates (one bird/replicate) in each group for heat challenge experiments. Broilers (29- or 30-day-old) were exposed to acute heat stress (30 ± 1°C) for 120 min or a chronic heat cyclic and continued heat stress (over 30 ± 1°C; ages, 15 to 44 days). In ovo feeding of l-Leu caused a significant suppression of enhanced body temperature without affecting food intake, plasma triacylglycerol, non-esterified fatty acids, ketone bodies, glucose, lactic acid or thyroid hormones under acute heat stress. Daily body temperature was significantly increased by l-Leu in ovo feeding under chronic heat stress. Interestingly, in ovo feeding of l-Leu caused a significantly higher daily BW gain compared with that of the control group under chronic heat stress. Moreover, some essential amino acids, including Leu and isoleucine, were significantly increased in the liver and decreased in the plasma by l-Leu in ovo feeding under acute heat stress. These results suggested that l-Leu in ovo feeding afforded thermotolerance to broilers under acute heat stress mainly through changing amino acid metabolism until marketing age.

Keywords

amino acidsin ovo administrationthermal challengemeat productionchickens
Type
Research Article
Information
animal , Volume 14 , Issue 8 , August 2020 , pp. 1701 - 1709
Copyright
© The Animal Consortium 2020

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.)

Footnotes

a

Present address: Department of Animal Nutrition and Food Science, College of Animal Science and Technology, Nanjing Agricultural University, No. 1 Weigang, Nanjing 210095, China.

b

Present address: Department of Veterinary Medicine, Azabu University, 1-17-71 Fuchinobe, Kanagawa 252-5201, Japan.

References

Abu-Dieyeh, ZHM 2006. Effect of chronic heat stress and long-term feed restriction on broiler performance. International Journal of Poultry Science 5, 185–190.Google Scholar
Al wakeel, RA, Shukry, M, Azeez, AA, Mahmoud, S and Saad, MF 2017. Alleviation by gamma amino butyric acid supplementation of chronic heat stress-induced degenerative changes in jejunum in commercial broiler chickens. Stress 6, 562–572.CrossRefGoogle Scholar
Azad, MAK, 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 Part A: Molecular & Integrative Physiology 155, 401–406.CrossRefGoogle ScholarPubMed
Boogers, I, Plugge, W, Stokkermans, YQ and Duchateau, AL 2008. Ultra-performance liquid chromatographic analysis of amino acids in protein hydrolysates using an automated pre-column derivatisation method. Journal of Chromatography A 1189, 406–409.CrossRefGoogle ScholarPubMed
Chowdhury, VS, Han, G, Bahry, MA, Tran, PV, Do, PH, Yang, H and Furuse, M 2017 l-Citrulline acts as potential hypothermic agent to afford thermotolerance in chicks. Journal of Thermal Biology 69, 163–170.CrossRefGoogle ScholarPubMed
Chowdhury, VS, Shigemura, A, Erwan, E, Ito, K, Bahry, MA, Phuong, TV and Furuse, M 2015. Oral administration of l-citrulline, but not l-arginine or l-ornithine, acts as a hypothermic agent in chicks. Journal of Poultry Science 52, 331–335.CrossRefGoogle Scholar
Chowdhury, VS, Tomonaga, S, Ikegami, T, Erwan, E, Ito, K, Cockrem, JF and Furuse, M 2014. Oxidative damage and brain concentrations of free amino acid in chicks exposed to high ambient temperature. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 169, 70–76.CrossRefGoogle ScholarPubMed
Corzo, A, Moran, ET and Hoehler, D 2003. Lysine needs of summer-reared male broilers from six to eight weeks of age. Poultry Science 82, 1602–1607.CrossRefGoogle ScholarPubMed
Duan, Y, Li, F, Liu, H, Li, Y, Liu, Y, Kong, X, Zhang, Y, Deng, D, Tang, Y, Feng, Z, Wu, G and Yin, Y 2015. Nutritional and regulatory roles of leucine in muscle growth and fat reduction. Frontiers in Bioscience, Landmark 20, 796–813.Google ScholarPubMed
Furuse, M 2015. Screening of central functions of amino acids and their metabolites for sedative and hypnotic effects using chick models. European Journal of Pharmacology 762, 382–393.CrossRefGoogle ScholarPubMed
Gonzalez-Esquerra, R and Leeson, S 2005. Effects of acute versus chronic heat stress on broiler response to dietary protein. Poultry Science 84, 1562–1569.CrossRefGoogle ScholarPubMed
Han, Y and Baker, DH 1993. Effects of sex, heat stress, body weight, and genetic strain on the dietary lysine requirement of broiler chicks. Poultry Science 72, 701–708.CrossRefGoogle ScholarPubMed
Han, G, Yang, H, Bahry, MA, Tran, PV, Do, PH, Ikeda, H, Furuse, M and Chowdhury, VS 2017. l-Leucine acts as a potential agent in reducing body temperature at hatching and affords thermotolerance in broiler chicks. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 204, 48–56.CrossRefGoogle ScholarPubMed
Han, G, Yang, H, Bungo, T, Ikeda, H, Wang, Y, Nguyen, LTT, Eltahan, EM, Furuse, M and Chowdhury, VS 2018. In ovo l-leucine administration stimulates lipid metabolisms in heat-exposed male, but not female, chicks to afford thermotolerance. Journal of Thermal Biology 71, 74–82.CrossRefGoogle Scholar
Han, G, Yang, H, Wang, Y, Haraguchi, S, Miyazaki, T, Bungo, T, Tashiro, K, Furuse, M and Chowdhury, VS 2019b. l-Leucine increases the daily body temperature and affords thermotolerance in broiler chicks. Asian-Australasian Journal of Animal Sciences 32, 842–848.CrossRefGoogle ScholarPubMed
Han, G, Yang, H, Wang, Y, Zhang, R, Tashiro, K, Bungo, T, Furuse, M and Chowdhury, VS 2019a. Effects of in ovo feeding of l-leucine on amino acids metabolism and heat-shock protein-70, and -90 mRNA expression in heat-exposed chicks. Poultry Science 98, 1243–1253.CrossRefGoogle ScholarPubMed
Hargis, PS and Van Elswyk, ME 1993. Manipulating the fatty acid composition of poultry meat and eggs for the health-conscious consumer. Worlds Poultry Science Journal 49, 251–264.CrossRefGoogle Scholar
He, S, Li, S, Arowolo, MA, Yu, Q, Chen, F, Hu, R and He, J 2019. Effect of resveratrol on growth performance, rectal temperature and serum parameters of yellow-feather broilers under heat stress. Animal Science Journal 90, 401–411.CrossRefGoogle ScholarPubMed
Hubbard, AH, Zhang, X, Jastrebski, S, Singh, A and Schmidt, C 2019. Understanding the liver under heat stress with statistical learning: an integrated metabolomics and transcriptomics computational approach. BMC Genomics 20, 502.CrossRefGoogle ScholarPubMed
Ito, K, Erwan, E, Nagasawa, M, Furuse, M and Chowdhury, VS 2014. Changes in free amino acid concentrations in the blood, brain and muscle of heat-exposed chicks. British Poultry Science 55, 644–652.CrossRefGoogle ScholarPubMed
Kita, K, Ito, K, Sugahara, M, Kobayashi, M, Makino, R, Takahashi, N, Nakahara, H, Takahashi, K and Nishimukai, M 2015. Effects of in ovo administration of branched-chain amino acids on embryo growth and hatching time of chickens. Journal of Poultry Science 52, 34–36.CrossRefGoogle Scholar
Kobayashi, K and Pillai, KS 2013. A handbook of applied statistics in pharmacology. CRC Press, Boca Raton, FL, USA.Google Scholar
Lara, JL and Rostagno, MH 2013. Impact of heat stress on poultry production. Animals 3, 356–369.CrossRefGoogle ScholarPubMed
Lin, H, Jiao, H, Buyse, J and Decuypere, E 2006. Strategies for preventing heat stress in poultry. Worlds Poultry Science Journal 62, 71–86.CrossRefGoogle Scholar
Longley, M 2010. Management review for the 308 broilers. Presented at the 91th Technical Seminar, Japan Chunky Association, 7–8 April 2010, Sendai, Japan.Google Scholar
Loyau, T, Bedrani, L, Berri, C, Métayer-Coustard, S, Praud, C, Coustham, V, Mignon-Grasteau, S, Duclos, MJ, Tesseraud, S, Rideau, N, Henequet-Antier, C, Everaert, N, Yahav, S and Collin, A 2015. Cyclic variations in incubation conditions induce adaptive responses to later heat exposure in chickens: a review. Animal 9, 76–85.CrossRefGoogle ScholarPubMed
Loyau, T, Métayer-Coustard, S, Berri, C, Crochet, S, Cailleau-Audouin, E, Sannier, M, Chartrin, P, Praud, C, Hennequet-Antier, C, Rideau, N, Couroussé, N, Mignon-Grasteau, S, Everaert, N, Duclos, JM, Yahav, S, Tesseraud, S and Collin, A 2014. Thermal manipulation during embryogenesis has long-term effects on muscle and liver metabolism in fast-growing chickens. PLoS ONE 9, e105339.CrossRefGoogle ScholarPubMed
Lu, Z, He, X, Ma, B, Zhang, L, Li, J, Jiang, Y, Zhou, G and Gao, F 2017. Chronic heat stress impairs the quality of breast-muscle meat in broilers by affecting redox status and energy-substance metabolism. Journal of Agricultural and Food Chemistry 65, 11251–11258.CrossRefGoogle ScholarPubMed
Luo, S and Levine, RL 2009. Methionine in proteins defends against oxidative stress. Federation of American Societies for Experimental Biology Journal 23, 464–472.CrossRefGoogle ScholarPubMed
Maeda, E, Kimura, S, Yamada, M, Tashiro, M and Ohashi, T 2017. Enhanced gap junction intercellular communication inhibits catabolic and pro-inflammatory responses in tenocytes against heat stress. Journal of Cell Communication and Signaling 11, 369–380.CrossRefGoogle ScholarPubMed
Nawab, A, Ibtisham, F, Li, G, Kieser, B, Wu, J, Liu, W, Zhao, Y, Nawab, Y, Li, K, Xiao, M and An, L 2018. Heat stress in poultry production: mitigation strategies to overcome the future challenges facing the global poultry industry. Journal of Thermal Biology 78, 131–139.CrossRefGoogle ScholarPubMed
Roushdy, EM, Zaglool, AW and El-Tarabany, MS 2018. Effects of chronic thermal stress on growth performance, carcass traits, antioxidant indices and the expression of HSP70, growth hormone and superoxide dismutase genes in two broiler strains. Journal of Thermal Biology 74, 337–343.CrossRefGoogle ScholarPubMed
Suryawan, A and Davis, TA 2014. Regulation of protein degradation pathways by amino acids and insulin in skeletal muscle of neonatal pigs. Journal of Animal Science and Biotechnology 5, 8.CrossRefGoogle ScholarPubMed
Tran, PV, Chowdhury, VS and Furuse, M 2019. Central regulation of feeding behavior through neuropeptides and amino acids in neonatal chicks. Amino Acids 51, 1129–1152.CrossRefGoogle ScholarPubMed
Wen, H, Naito, K, Kinoshita, Y, Kobayashi, H, Honjoh, K, Tashiro, K and Miyamoto, T 2012. Changes in transcription during recovery from heat injury in Salmonella typhimurium and effects of BCAA on recovery. Amino Acids 42, 2059–2066.Google Scholar
Wu, G 2009. Amino acids: metabolism, functions, and nutrition. Amino Acids 37, 1–17.CrossRefGoogle ScholarPubMed
Xie, J, Tang, L, Lu, L, Zhang, L, Lin, X, Liu, HC, 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.CrossRefGoogle ScholarPubMed
Yahav, S 2015. Regulation of body temperature: strategies and mechanisms. In Sturkie’s avian physiology (ed. Scanes, CG), 6th edition, pp. 869–905. Academic Press, Milwaukee, WI, USA.CrossRefGoogle Scholar
Zaboli, G, Huang, X, Feng, X and Ahn, DU 2019. How can heat stress affect chicken meat quality? – a review. Poultry Science 98, 1551–1556.CrossRefGoogle ScholarPubMed
Zhang, Z, Jia, G, Zuo, J, Zhang, Y, Lei, J, Ren, L and Feng, D 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.CrossRefGoogle ScholarPubMed
Supplementary material: File

Han et al. supplementary material

Tables S1-S3

Download Han et al. supplementary material(File)
File 30.2 KB