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Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Dietary leucine deficiency alters performance, body composition, intestine microbiota, and immune response of female Cobb broilers

Saeid Amirdahri A , Hossein Janmohammadi A , Akbar Taghizadeh A , Majid Olyayee https://orcid.org/0000-0002-8764-2895 A , Babak Hosseintabar-Ghasemabad A , Alireza Seidavi https://orcid.org/0000-0002-1903-2753 B and Radoslava Vlčková https://orcid.org/0000-0002-0977-8295 C *
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran.

B Department of Animal Science, Rasht Branch, Islamic Azad University, Rasht, Iran.

C Department of Biology and Physiology, University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, Košice 041 81, Slovak Republic.

* Correspondence to: radoslava.vlckova@uvlf.sk

Handling Editor: Reza Barekatain

Animal Production Science 63(17) 1750-1758 https://doi.org/10.1071/AN23100
Submitted: 15 March 2023  Accepted: 16 August 2023  Published: 26 September 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Leucine (Leu) is one of the branched-chain amino acids that is necessary for muscle protein synthesis. Basically, poultry feed ingredients contain abundant amounts of Leu. But little is known about dietary Leu deficiency in performance and health-attributing parameters of female broiler chickens, which may occur in crude protein-restricted diets.

Aims

This study evaluates the effect of Leu deficiency in diets on the growth performance, body composition, immunity, and caecum microbiota of female broilers.

Methods

Female broiler chicks (Cobb 500; 8 days old; n = 540) were randomly divided into six groups with six replicates (15 birds in each replicate) in a completely randomised design. The experimental diets included six concentrations of Leu (80%, 84%, 88%, 92%, 96%, and 100%) fed for 14 days. A basal Leu-deficient diet was formulated at the 80% recommended level, and the experimental diets were created by gradual replacing of crystalline L-glutamic acid with crystalline L-Leu. Average daily intake (ADI), average daily gain (ADG), feed efficiency (gain:feed), body composition, cutaneous basophil hypersensitivity (CBH) test to phytohaemagglutinin-P (PHA-P), antibody response to sheep red blood cell (SRBC) and caecum microbiota were investigated.

Key results

The birds receiving the lowest Leu application level had the lowest ADI (P < 0.05) and a 20% higher fat content (P < 0.01) than did the birds fed 96% Leu. The population of Escherichia coli and coliform bacteria count was increased (P < 0.001; by 36% and 10.3% compared with the birds fed 100% Leu in the diet respectively), and Lactobacillus (but not Enterococcus) count was decreased (P < 0.001; by 26.4% compared with the birds fed 100% Leu in the diet) with decreasing concentrations of dietary Leu. Average daily gain, feed efficiency, carcass dry matter, protein and ash percentages, and immunity were not affected markedly by dietary treatments with different Leu concentrations.

Conclusions

The Leu deficiency influenced the broiler performance, body composition, and caecum microbiota, but not the immune response.

Implications

This study points to the importance of Leu supplementation in the diet of broilers to improve their growth performance, fat content, and intestine health.

Keywords: branched-chain amino acid, broiler, fat content, immune system, intestine health, leucine, microbiota, performance.

References

Al-Mayah AAS (2006) Immune response of broiler chicks to DL-methionine supplementation at different ages. International Journal of Poultry Science 5(2), 169-172.
| Crossref | Google Scholar |

Amirdahri S, Janmohammadi H, Tagizadeh A, Soumeh EA, Oliayi M (2021) Leucine requirement of female cobb broilers from 8 to 14 days of age. Iranian Journal of Applied Animal Science 11(2), 391-398.
| Google Scholar |

Amirdahri S, Janmohammadi H, Taghizadeh A, Lambert W, Olyayee M, Assadi Soumeh E (2023) The optimum ratio of digestible leucine: lysine in wheat-based diets for female broiler chickens from 8–21 days of age. Journal of Applied Poultry Research 32, 100289.
| Crossref | Google Scholar |

Anthony JC, Anthony TG, Kimball SR, Jefferson LS (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. The Journal of Nutrition 131(3), 856S-860S.
| Crossref | Google Scholar | PubMed |

AOAC International (1995) ‘Official methods of analysis of AOAC international.’ 16th edn. (Association of Official Analytical Chemists: Washington, DC, USA)

Beaumont M, Blachier F (2020) Amino acids in intestinal physiology and health. In ‘Amino acids in nutrition and health, Vol. 1265’. Advances in Experimental Medicine and Biology. (Ed. G Wu) pp. 1–20. (Springer) doi:10.1007/978-3-030-45328-2_1. pubmed id:32761567

Bello AU, Idrus Z, Yong Meng G, Awad EA, Soleimani Farjam A (2018) Gut microbiota and transportation stress response affected by tryptophan supplementation in broiler chickens. Italian Journal of Animal Science 17(1), 107-113.
| Crossref | Google Scholar |

Calder PC (2006) Branched-chain amino acids and immunity. The Journal of Nutrition 136(1), 288S-293S.
| Crossref | Google Scholar |

Chalvon-Demersay T, Luise D, Le Floc’h N, Tesseraud S, Lambert W, Bosi P, Trevisi P, Beaumont M, Corrent E (2021) Functional amino acids in pigs and chickens: implication for gut health. Frontiers in Veterinary Science 8, 663727.
| Crossref | Google Scholar | PubMed |

Cook ME (1991) Nutrition and the immune response of the domestic fowl. Critical Reviews in Poultry Biology 3, 167-189.
| Google Scholar |

Corrier DE, DeLoach JR (1990) Evaluation of cell-mediated, cutaneous basophil hypersensitivity in young chickens by an interdigital skin test. Poultry Science 69(3), 403-408.
| Crossref | Google Scholar | PubMed |

Davila A-M, Blachier F, Gotteland M, Andriamihaja M, Benetti P-H, Sanz Y, Tomé D (2013) Re-print of ‘Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host’. Pharmacological Research 69(1), 114-126.
| Crossref | Google Scholar | PubMed |

Deng H, Zheng A, Liu G, Chang W, Zhang S, Cai H (2014) Activation of mammalian target of rapamycin signaling in skeletal muscle of neonatal chicks: effects of dietary leucine and age. Poultry Science 93(1), 114-121.
| Crossref | Google Scholar | PubMed |

Drummond MJ, Rasmussen BB (2008) Leucine-enriched nutrients and the regulation of mammalian target of rapamycin signalling and human skeletal muscle protein synthesis. Current Opinion in Clinical Nutrition and Metabolic Care 11(3), 222-226.
| Crossref | Google Scholar | PubMed |

Farran MT, Barbour EK, Ashkarian VM (2003) Effect of excess leucine in low protein diet on ketosis in 3-week-old male broiler chicks fed different levels of isoleucine and valine. Animal Feed Science and Technology 103(1–4), 171-176.
| Crossref | Google Scholar |

Franco SM, Tavernari FdC, Maia RC, Barros VRSM, Albino LFT, Rostagno HS, Lelis GR, Calderano AA, Dilger RN (2017) Estimation of optimal ratios of digestible phenylalanine + tyrosine, histidine, and leucine to digestible lysine for performance and breast yield in broilers. Poultry Science 96(4), 829-837.
| Crossref | Google Scholar | PubMed |

Hale LL, Pharr GT, Burgess SC, Corzo A, Kidd MT (2004) Isoleucine needs of thirty- to forty-day-old female chickens: immunity. Poultry Science 83(12), 1979-1985.
| Crossref | Google Scholar | PubMed |

Harris RA, Joshi M, Ho Jeoung N (2004) Mechanisms responsible for regulation of branched-chain amino acid catabolism. Biochemical and Biophysical Research Communications 313(2), 391-396.
| Crossref | Google Scholar | PubMed |

Hosseintabar B, Dadashbeiki M, Bouyeh M, Seidavi A (2014) Is the amount of L-carnitine and methionine-lysine affect on the microbial flora of broiler cecum. Journal of Pure and Applied Microbiology 8(1), 353-360.
| Google Scholar |

Hu C, Li F, Duan Y, Yin Y, Kong X (2019) Dietary supplementation with leucine or in combination with arginine decreases body fat weight and alters gut microbiota composition in finishing pigs. Frontiers in Microbiology 10, 1767.
| Crossref | Google Scholar | PubMed |

Kim WK, Singh AK, Wang J, Applegate T (2022) Functional role of branched chain amino acids in poultry: a review. Poultry Science 101, 101715.
| Crossref | Google Scholar |

Konashi S, Takahashi K, Akiba Y (2000) Effects of dietary essential amino acid deficiencies on immunological variables in broiler chickens. British Journal of Nutrition 83(4), 449-456.
| Google Scholar | PubMed |

Kratei HM, Shahir MH (2021) Response of broiler chicks to dietary L-leucine supplementation in the starter period. Brazilian Journal of Poultry Science 23(1), 1-8.
| Crossref | Google Scholar |

Kristensen L, Therkildsen M, Riis B, Sørensen MT, Oksbjerg N, Purslow PP, Ertbjerg P (2002) Dietary-induced changes of muscle growth rate in pigs: effects on in vivo and postmortem muscle proteolysis and meat quality. Journal of Animal Science 80(11), 2862-2871.
| Crossref | Google Scholar | PubMed |

Kumar S, Adhikari P, Oakley B, Kim WK (2019) Changes in cecum microbial community in response to total sulfur amino acid (TSAA: DL-methionine) in antibiotic-free and supplemented poultry birds. Poultry Science 98(11), 5809-5819.
| Crossref | Google Scholar | PubMed |

Li F, Yin Y, Tan B, Kong X, Wu G (2011) Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids 41(5), 1185-1193.
| Crossref | Google Scholar | PubMed |

Luise D, Bertocchi M, Bosi P, Correa F, Spinelli E, Trevisi P (2020) Contribution of L-Arginine supplementation during gestation on sow productive performance and on sow microbial faecal profile. Italian Journal of Animal Science 19(1), 330-340.
| Crossref | Google Scholar |

Maynard CW, Mullenix GJ, Maynard CJ, Lee JT, Rao SK, Butler LD, Hiltz JZ, Orlowski SK, Kidd MT (2022) Failure of excess leucine to impact live performance and carcass traits in male and female Cobb MV× 500 broilers during a 15- to 32-day grower period. Journal of Applied Poultry Research 31(2), 100242.
| Crossref | Google Scholar |

Nascimento GR, Murakami AE, Ospina-Rojas IC, Diaz-Vargas M, Picoli KP, Garcia RG (2016) Digestible valine requirements in low-protein diets for broilers chicks. Brazilian Journal of Poultry Science 18, 381-386.
| Crossref | Google Scholar |

National Research Council (1994) ‘Nutrient requirements of poultry.’ (National Academies Press)

Nguyen AD, Herzog H, Sainsbury A (2011) Neuropeptide Y and peptide YY: important regulators of energy metabolism. Current Opinion in Endocrinology, Diabetes and Obesity 18(1), 56-60.
| Crossref | Google Scholar | PubMed |

Omidi S, Ebrahimi M, Janmohammadi H, Moghaddam G, Rajabi Z, Hosseintabar-Ghasemabad B (2020) The impact of in ovo injection of L-arginine on hatchability, immune system and caecum microflora of broiler chickens. Journal of Animal Physiology and Animal Nutrition 104(1), 178-185.
| Crossref | Google Scholar | PubMed |

Ospina-Rojas IC, Murakami AE, Duarte CRA, Nascimento GR, Garcia ERM, Sakamoto MI, Nunes RV (2017) Leucine and valine supplementation of low-protein diets for broiler chickens from 21 to 42 days of age. Poultry Science 96(4), 914-922.
| Crossref | Google Scholar | PubMed |

Petro TM, Bhattacharjee JK (1981) Effect of dietary essential amino acid limitations upon the susceptibility to Salmonella typhimurium and the effect upon humoral and cellular immune responses in mice. Infection and Immunity 32(1), 251-259.
| Crossref | Google Scholar | PubMed |

Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RFd, Lopes DC, Ferreira AS, Barreto SLdT, Euclides RF (2011) ‘Tabelas brasileiras para aves e suínos. Composição de Alimentos e Exigências Nutricionais’. Universidade Federal de Viçosa – Departamento de Zootecnia 2, p. 186.

SAS Institute (2002) ‘SAS/STAT User’s Guide.’ Version 8, 6th edn. (SAS Institute: Cary, USA).

Soumeh EA, van Milgen J, Sloth NM, Corrent E, Poulsen HD, Nørgaard JV (2015) The optimum ratio of standardized ileal digestible leucine to lysine for 8 to 12 kg female pigs. Journal of Animal Science 93(5), 2218-2224.
| Crossref | Google Scholar | PubMed |

Spring S, Premathilake H, Bradway C, Shili C, DeSilva U, Carter S, Pezeshki A (2020) Effect of very low-protein diets supplemented with branched-chain amino acids on energy balance, plasma metabolomics and fecal microbiome of pigs. Scientific Reports 10(1), 15859.
| Crossref | Google Scholar | PubMed |

Stanley BG, Leibowitz SF (1984) Neuropeptide Y: stimulation of feeding and drinking by injection into the paraventricular nucleus. Life Sciences 35(26), 2635-2642.
| Crossref | Google Scholar | PubMed |

Suryawan A, Orellana RA, Fiorotto ML, Davis TA (2011) Triennial Growth Symposium: leucine acts as a nutrient signal to stimulate protein synthesis in neonatal pigs. Journal of Animal Science 89(7), 2004-2016.
| Crossref | Google Scholar | PubMed |

Thornton SA, Corzo A, Pharr GT, Dozier Iii WA, Miles DM, Kidd MT (2006) Valine requirements for immune and growth responses in broilers from 3 to 6 weeks of age. British Poultry Science 47(2), 190-199.
| Crossref | Google Scholar | PubMed |

Wang S, Khondowe P, Chen S, Yu J, Shu G, Zhu X, Wang L, Gao P, Xi Q, Zhang Y, Jiang Q (2012) Effects of “Bioactive” amino acids leucine, glutamate, arginine and tryptophan on feed intake and mRNA expression of relative neuropeptides in broiler chicks. Journal of Animal Science and Biotechnology 3(1), 27.
| Crossref | Google Scholar |

Zeitz JO, Käding S-C, Niewalda IR, Most E, Dorigam JCdP, Eder K (2019) The influence of dietary leucine above recommendations and fixed ratios to isoleucine and valine on muscle protein synthesis and degradation pathways in broilers. Poultry Science 98(12), 6772-6786.
| Crossref | Google Scholar | PubMed |

Zhang S, Zeng X, Ren M, Mao X, Qiao S (2017) Novel metabolic and physiological functions of branched chain amino acids: a review. Journal of Animal Science and Biotechnology 8(1), 10.
| Crossref | Google Scholar |