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Effects of dietary tryptophan supplementation on body temperature, hormone, and cytokine levels in broilers exposed to acute heat stress

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Abstract

The present study was conducted to investigate the effects of tryptophan (Trp) supplementation on rectal temperature, hormone, and cytokine levels in broilers subjected to acute heat stress. A total of 300 18-day-old female Arbor Acres broilers were randomly allocated to five dietary treatment groups with six replicates per treatment group and ten birds per replicate. Broilers were fed a basal diet and in the thermoneutral conditions (TN, 23 ± 1 °C) was considered as the TN group. Broilers were fed a basal diet and exposed to acute heat stress (HS, 34 ± 1 °C) was regarded as the HS group, and other broilers exposed to acute heat stress (34 ± 1°C) were fed a basal diet supplemented with 0.09%, 0.18%, and 0.27% Trp. Results indicated that acute heat stress increased the rectal temperature (P < 0.05), enhanced the concentrations of corticosterone (CORT), dopamine (DA), adrenaline (Adr), adrenocorticotropic hormone (ACTH), and corticotropin-releasing hormone (CRH) in serum (P < 0.05), and elevated the levels of serum tryptophan hydroxylase (TPH)1, tryptophan 2, 3-dioxygenase (TDO), indoleamine 2, 3-dioxygenase (IDO), and kynurenic acid (P < 0.05), compared with the TN group. Meanwhile, acute heat stress increased the levels of serum Trp, hypothalamic Trp, 5-hydroxytryptophan (5-HT), and interleukin-22 (P < 0.05) relative to the TN group. However, compared with the heat stress group, Trp supplementation decreased the rectal temperature of heat-stressed broilers and dietary 0.09% Trp supplementation decreased the levels of serum CRH and TDO (P < 0.05), increased the levels of serum Trp and IL-22 (P < 0.05) in heat-stressed broilers. In addition, dietary supplemented with 0.18% Trp reduced the levels of serum DA, Adr, noradrenaline (NA), CRH, TDO, IDO, kynurenic acid, IL-1β, and hypothalamic 5-HIAA/5-HT (P < 0.05), increased the levels of serum Trp, 5-HT, and IL-22, and upregulated the concentrations of hypothalamic Trp and 5-HT in heat-stressed broilers (P < 0.05). Moreover, dietary 0.27% Trp supplementation decreased the levels of serum DA, CRH, TDO, and hypothalamic 5-HIAA/5-HT (P < 0.05), and upregulated the levels of serum Trp, 5-HT, IL-22, hypothalamic Trp and 5-HT in heat-stressed broilers (P < 0.05). Taken together, dietary 0.18% Trp supplementation may be the optimal level for broilers reared under acute heat stress.

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References

  • Alhassan, U.B., Zulkifli, I., Goh, Y.M., Elmutaz, A.A., Abdoreza, S.F. 2018. Gut microbiota and transportation stress response affected by tryptophan supplementation in broiler chickens. Italian Journal of Animal Science. 17(1),107-113.

    Article  Google Scholar 

  • Bai, M., Liu, H., Xu, K., Oso, A. O., Wu, X., Liu, G., Tossou, M. C., Al-Dhabi, N. A., Duraipandiyan, V., Xi, Q., Yin, Y. 2017. A review of the immunomodulatory role of dietary tryptophan in livestock and poultry. Amino Acids, 49(1), 67-74.

    Article  CAS  PubMed  Google Scholar 

  • Behnsen, J., Jellbauer, S., Wong, C.P., Edwards, R.A., George, M.D., Ouyang, W., Raffatellu, M. 2014. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity. 40, 262-273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biefer, H. R. C., Vasudevan, A., Elkhal, A. 2017. Aspects of Tryptophan and Nicotinamide Adenine Dinucleotide in Immunity: A New Twist in an Old Tale. International Journal of Tryptophan Research. 10, 1178646917713491.

    Google Scholar 

  • Breda, C., Sathyasaikumar, K.V., Sograte, I.S., Notarangelo, F.M., Estranero, J.G., Moore, G.G., Green, E.W., Kyriacou, C.P., Schwarcz, R., Giorgini, F. 2016. Tryptophan-2,3-dioxygenase (TDO) inhibition ameliorates neurodegeneration by modulation of kynurenine pathway metabolites. Proceedings of the National Academy of Sciences of the United States of America. 113, 5435-5440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calefi, A.S., Fonseca, J., Nunes, C., Lima, A., Quinteiro-Filho, W.M., Florio, J.C., Zager, A., Ferreira, A., Palermo-Neto, J. 2019. Heat Stress Modulates Brain Monoamines and Their Metabolites Production in Broiler Chickens Co-Infected with Clostridium perfringens Type A and Eimeria spp. Veterinary Sciences. 6(1),4.

    Article  PubMed Central  Google Scholar 

  • Castro-Portuguez, R., Sutphin, G.L. 2020. Kynurenine pathway, NAD (+) synthesis, and mitochondrial function: Targeting tryptophan metabolism to promote longevity and healthspan. Experimental Gerontology. 132, 110841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, X.Y., Wei, P.P., Xu, S.Y., Geng, Z.Y., Jiang, R.S. 2013. Rectal temperature as an indicator for heat tolerance in chickens. Animal Science Journal. 84, 737-739.

    Article  PubMed  Google Scholar 

  • Chrousos, G. P. 1995. The hypothalamic–pituitary–adrenal axis and immune-mediated inflammation. New England Journal of Medicine, 332(20), 1351-1363.

    Article  CAS  PubMed  Google Scholar 

  • Dinan, T.G., 1996. Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function. Life Sciences. 58, 1683-1694.

    Article  CAS  PubMed  Google Scholar 

  • Fuertig, R., Azzinnari, D., Bergamini, G., Cathomas, F., Sigrist, H., Seifritz, E., Vavassori, S., Luippold, A., Hengerer, B., Ceci, A., Pryce, C.R. 2016. Mouse chronic social stress increases blood and brain kynurenine pathway activity and fear behaviour: Both effects are reversed by inhibition of indoleamine 2,3-dioxygenase. Brain Behavior and Immunity. 54, 59-72.

    Article  CAS  PubMed  Google Scholar 

  • Gao, J., Xu, K., Liu, H., Liu, G., Bai, M., Peng, C., Li, T., Yin, Y. 2018. Impact of the Gut Microbiota on Intestinal Immunity Mediated by Tryptophan Metabolism. Frontiers in cellular and infection microbiology. 8, 13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez-Rivas, P.A., Chauhan, S.S., Ha, M., Fegan, N., Dunshea, F.R., Warner, R.D. 2020. Effects of heat stress on animal physiology, metabolism, and meat quality: A review. Meat Science. 162, 108025.

    Article  CAS  PubMed  Google Scholar 

  • He, X., Lu, Z., Ma, B., Zhang, L., Li, J., Jiang, Y., Zhou, G., Gao, F. 2019. Chronic heat stress alters hypothalamus integrity, the serum indexes and attenuates expressions of hypothalamic appetite genes in broilers. Journal of thermal biology, 81, 110-117.

    Article  CAS  PubMed  Google Scholar 

  • Hierden, Y.M., Koolhaas, J.M., Korte, S.M. 2004. Chronic increase of dietary l-tryptophan decreases gentle feather pecking behaviour. Applied Animal Behaviour Science. 89, 71-84.

    Article  Google Scholar 

  • Hoglund, E., Overli, O., Winberg, S. 2019. Tryptophan Metabolic Pathways and Brain Serotonergic Activity: A Comparative Review. Frontiers in endocrinology. 10, 158.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kadim, I. T., Mahgoub, O., Al-Kindi, A., Al-Marzooqi, W., Al-Saqri, N. M. 2006. Effects of transportation at high ambient temperatures on physiological responses, carcass and meat quality characteristics of three breeds of Omani goats. Meat Science. 73,626-634.

    Article  CAS  PubMed  Google Scholar 

  • Kang, D., Shim, K. 2021. Early heat exposure effect on the heat shock proteins in broilers under acute heat stress. Poultry science, 100(3), 100964.

    Article  PubMed  CAS  Google Scholar 

  • Koopmans, S. J., Ruis, M., Dekker, R., Diepen, H. V., Korte, M., Mroz, Z. 2005. Surplus dietary tryptophan reduces plasma cortisol and noradrenaline concentrations and enhances recovery after social stress in pigs. Physiology & Behavior, 85(4), 469-478.

    Article  CAS  Google Scholar 

  • Koopmans, S.J., Guzik, A.C., van der Meulen, J., Dekker, R., Kogut, J., Kerr, B.J., Southern, L.L. 2006. Effects of supplemental L-tryptophan on serotonin, cortisol, intestinal integrity, and behavior in weanling piglets. Journal of Animal Science. 84, 963-971.

    Article  CAS  PubMed  Google Scholar 

  • Lee, J.S., Cella, M., McDonald, K.G., Garlanda, C., Kennedy, G.D., Nukaya, M., Mantovani, A., Kopan, R., Bradfield, C.A., Newberry, R.D., Colonna, M. 2011. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nature Immunology. 13, 144-151.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee, J., Sung, Y. K., & Kong, C. 2020. Ideal ratios of standardized ileal digestible methionine, threonine, and tryptophan relative to lysine for male broilers at the age of 1 to 10 days. Animal Feed Science and Technology, 262, 114427.

    Article  CAS  Google Scholar 

  • Li, Q., Wan, G., Peng, C., Xu, L., Yu, Y., Li, L., Li, G. 2020. Effect of probiotic supplementation on growth performance, intestinal morphology, barrier integrity, and inflammatory response in broilers subjected to cyclic heat stress. Animal Science Journal. 91, e13433.

    Article  CAS  PubMed  Google Scholar 

  • Lin, H., Decuypere, E., Buyse, J. 2006. Acute heat stress induces oxidative stress in broiler chickens. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 144(1), 11-17.

    Article  CAS  Google Scholar 

  • Liu, Y., Yuan, J.M., Zhang, L.S., Zhang, Y.R., Cai, S.M., Yu, J.H., Xia, Z.F. 2015. Effects of tryptophan supplementation on growth performance, antioxidative activity, and meat quality of ducks under high stocking density. Poultry Science. 94, 1894-1901.

    Article  CAS  PubMed  Google Scholar 

  • Luo, Y., Yang, M., Guo, M., Zhong, X., Hu, Y. 2019. Huang Qin Hua Shi decoction for high-temperature- and high-humidity-induced cognitive-behavioral disorder in rats is associated with deactivation of the hypothalamic-pituitary-adrenal axis. The Journal of International Medical Research. 2019, 47, 5752-5766.

    Article  CAS  Google Scholar 

  • Ma, N., He, T., Johnston, L. J., Ma, X. 2020. Host–microbiome interactions: the aryl hydrocarbon receptor as a critical node in tryptophan metabolites to brain signaling. Gut Microbes, 11(5), 1203-1219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madoka, S., Etsuko, K., Ken, I.Y. 2018. Effects of intravenous tryptophan infusion on thermoregulation in steers exposed to acute heat stress. Animal Science Journal. 89(5), 777-783.

    Article  CAS  Google Scholar 

  • Monson, M. S., Van Goor, A. G., Persia, M. E., Rothschild, M. F., Schmidt, C. J., Lamont, S. J. 2019. Genetic lines respond uniquely within the chicken thymic transcriptome to acute heat stress and low dose lipopolysaccharide. Scientific reports, 9(1), 1-12.

    Article  CAS  Google Scholar 

  • Mujahid, A., Pumford, N. R., Bottje, W., Nakagawa, K., Miyazawa, T., Akiba, Y., Toyomizu, M. 2007. Mitochondrial oxidative damage in chicken skeletal muscle induced by acute heat stress. The Journal of Poultry Science, 44(4), 439-445.

    Article  CAS  Google Scholar 

  • Mund, M.D., Riaz, M., Mirza, M.A., Rahman, Z.U., Mahmood, T., Ahmad, F., Ammar, A. 2020. Effect of dietary tryptophan supplementation on growth performance, immune response and anti-oxidant status of broiler chickens from 7 to 21 days. Veterinary Medicine and Science. 6, 48-53.

    Article  CAS  PubMed  Google Scholar 

  • Mutibvu, T., Chimonyo, M., Halimani, T. 2017. Physiological responses of slow-growing chickens under diurnally cycling temperature in a hot environment. Brazilian Journal of Poultry Science. 19(4), 567-576.

    Article  Google Scholar 

  • Nawab, A., Ibtisham, F., Li, G., Kieser, B., Wu, J., Liu, W., Zhao, Y., Nawab, Y., Li, K., Xiao, M., 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.

    Article  PubMed  Google Scholar 

  • Platten, M., Nollen, E., Rohrig, U.F., Fallarino, F., Opitz, C.A. 2019. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nature Reviews Drug Discovery. 18, 379-401.

    Article  CAS  PubMed  Google Scholar 

  • Shakeri, M., Cottrell, J.J., Wilkinson, S., Le Hieu, H., Suleria, H.A.R., Warner, R.D., Dunshea, F.R. 2019. Growth performance and characterization of meat quality of broiler chickens supplemented with betaine and antioxidants under cyclic heat stress. Antioxidants (Basel, Switzerland). 8(9),336.

    CAS  PubMed Central  Google Scholar 

  • Shen, Y.B., Voilque, G., Odle, J., Kim, S.W. 2012a. Dietary L-tryptophan supplementation with reduced large neutral amino acids enhances feed efficiency and decreases stress hormone secretion in nursery pigs under social-mixing stress. Journal of Nutrition. 142, 1540-1546.

    Article  CAS  PubMed  Google Scholar 

  • Shen, Y.B., Voilque, G., Kim, J.D., Odle, J., Kim, S.W. 2012b. Effects of increasing tryptophan intake on growth and physiological changes in nursery pigs. Journal of Animal Science. 90, 2264-2275.

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui, S.H., Kang, D., Park, J., Khan, M., Shim, K. 2020. Chronic heat stress regulates the relation between heat shock protein and immunity in broiler small intestine. Scientific Reports. 10, 18872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sohail, M.U., Ijaz, A., Yousaf, M.S., Ashraf, K., Zaneb, H., Aleem, M., Rehman, H. 2010. Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poultry Science. 89, 1934-1938.

    Article  CAS  PubMed  Google Scholar 

  • Sohail, M. U., Hume, M. E., Byrd, J. A., Nisbet, D. J., Ijaz, A., Sohail, A., Shabbir, M. Z.; Rehman, H. 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poultry science, 91(9), 2235-2240.

    Article  CAS  PubMed  Google Scholar 

  • Sun, M., Ma, N., He, T., Johnston, L.J., Ma, X. 2020. Tryptophan (Trp) modulates gut homeostasis via aryl hydrocarbon receptor (AhR). Critical Reviews in Food Science & Nutrition. 60, 1760-1768.

    Article  CAS  Google Scholar 

  • Taherkhani, R., Shivazad, M., Zaghari, M., Zareshahne, A. 2005. Male and female broilers response to different ideal amino acid ratios during the second and third weeks post-hatch. International Journal of Poultry Science, 4(8), 563-567.

    Article  Google Scholar 

  • Taherkhani, R., Shivazad, M., Zaghari, M., & Shahneh, A. Z. 2008. Comparison of different ideal amino acid ratios in male and female broiler chickens of 21 to 42 days of age. The Journal of Poultry Science, 45(1), 15-19.

    Article  Google Scholar 

  • Vesco, A. P., Khatlab, A., Santana, T. P., Pozza, P. C., Soares, M. A. M., Brito, C. O., Barbosa, L. T., Gasparino, E. 2020. Heat stress effect on the intestinal epithelial function of broilers fed methionine supplementation. Livestock Science, 240, 104152.

    Article  Google Scholar 

  • Wilder, R. L. 1995. Neuroendocrine-immune system interactions and autoimmunity. Annual review of immunology, 13(1), 307-338.

    Article  CAS  PubMed  Google Scholar 

  • Winberg, S., Nilsson, A., Hylland, P., Soderstom, V., Nilsson, G.E. 1997. Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neuroscience Letters. 230, 113-116.

    Article  CAS  PubMed  Google Scholar 

  • Yalcin, S., Özkan, S., Türkmut, L., Siegel, P. B. 2001. Responses to heat stress in commercial and local broiler stocks. 1. Performance traits. British Poultry Science, 42(2), 149-152.

    Article  CAS  PubMed  Google Scholar 

  • Yue, Y., Guo, Y., Yang, Y. 2017. Effects of dietary L-tryptophan supplementation on intestinal response to chronic unpredictable stress in broilers. Amino Acids. 49(7), 1227-1236.

    Article  CAS  PubMed  Google Scholar 

  • Zelante, T., Iannitti, R.G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R., D'Angelo, C., Massi-Benedetti, C., Fallarino, F., Carvalho, A., Puccetti, P., Romani, L. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 39, 372-385.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., Zhao, X., Wang, L., Yang, L., Chen, X., 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(10), 1569-1574.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J.F., Bai, K.W., Sa, W.P., Wang, A A, Zhang, L.L., Huang, H.K., Wang, T. 2018. Curcumin attenuates heat-stress-induced oxidant damage by simultaneous activation of GSH-related antioxidant enzymes and Nrf2-mediated phase II detoxifying enzyme systems in broiler chickens. Poultry Science. 97(4),1209-1212.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, H. T., Zhuang, Z. X., Chen, C. J., Liao, H. Y., Chen, H. L., Hsueh, H. C., Chen, C. F., Chen, S. E., Huang, S. Y. 2021. Effects of acute heat stress on protein expression and histone modification in the adrenal gland of male layer-type country chickens. Scientific reports, 11(1), 1-13.

    CAS  Google Scholar 

  • Abdel-Moneim, A. M. E., Shehata, A. M., Khidr, R. E., Paswan, V. K., Ibrahim, N. S., El-Ghoul, A. A., Aldhumri, S. A., Gabr, S. A., Mesalam, N. M., Elbazd, A. M., Elsayed, M. A., Wakwak, M. M., Ebeid, T. A. 2021. Nutritional manipulation to combat heat stress in poultry–A comprehensive review. Journal of Thermal Biology, 102915.

  • National Research Council, 1994. Nutrient Requirements of Poultry, 9th ed. National Academic Press. Washington, DC.

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Funding

This study was financially supported by the National Natural Science Foundation of China (31860651), Key Project of the Natural Science Foundation of Jiangxi Province (20181ACB20015), and the Postgraduate Innovation Foundation of Jiangxi Province (YC2020-B088).

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  1. Qiufen Li and Hua Zhou contributed equally to this work.

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  1. Jiangxi Province Key Laboratory of Animal Nutrition, College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang, 330045, China

    Qiufen Li, Hua Zhou, Jingxin Ouyang, Shuaipeng Guo, Jun Zheng & Guanhong Li

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All authors contributed to the study’s conception and design. Conceptualization, Guanhong Li; Data curation, Qiufen Li, Hua Zhou, and Jingxin Ouyang; Formal analysis, Qiufen Li; Funding acquisition, Guanhong Li and Qiufen Li; Investigation, Qiufen Li, Hua Zhou, Jingxin Ouyang, Shuaipeng Guo, and Jun Zheng; Methodology, Qiufen Li, Hua Zhou, Jingxin Ouyang, Shuaipeng Guo, and Jun Zheng; Supervision, Guanhong Li; Writing—original draft, Qiufen Li and Jingxin Ouyang; Writing—review & editing, Huan Zhou and Guanhong Li. All authors have read and approved the submitted version.

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Li, Q., Zhou, H., Ouyang, J. et al. Effects of dietary tryptophan supplementation on body temperature, hormone, and cytokine levels in broilers exposed to acute heat stress. Trop Anim Health Prod 54, 164 (2022). https://doi.org/10.1007/s11250-022-03161-3

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