Bone mineralisation status of broilers fed reduced-protein diets supplemented with l-arginine, guanidinoacetic acid and l-citrulline
Hiep Thi Dao
A B , Amy F. Moss A , Emma J. Bradbury C and Robert A. Swick A *
+ Author Affiliations
- Author Affiliations
A School of Environmental and Rural Science, Faculty of Science, Agriculture, Business and Law, University of New England, Armidale, NSW 2351, Australia.
B Faculty of Animal Science, Vietnam National University of Agriculture, Trau Quy Town, Gia Lam District, Hanoi 100000, Vietnam.
C Ridley AgriProducts, Melbourne, Vic. 3000, Australia.
Animal Production Science 62(6) 539-553 https://doi.org/10.1071/AN21539
Submitted: 14 October 2021 Accepted: 25 December 2021 Published: 17 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Mineralisation of the bone matrix is a pivotal factor affecting bone strength in broilers. Reduced bone strength might cause fracture during catching and transportation to slaughterhouses, leading to economic loss.
Aims: This study was conducted to investigate the effects of l-arginine (Arg), guanidinoacetic acid (GAA), and l-citrulline (Cit) supplementation to Arg-deficient reduced-protein diets on bone mineral composition and mineral digestibility of broiler chickens.
Methods: Day-old Ross 308 males were allocated to one of eight dietary treatments with six replicates of 16 birds per treatment. The treatments were standard protein (SP), reduced protein deficient in Arg (RP), and RP with two levels of either Arg (0.238% and 0.476%), GAA (0.309% and 0.618%) or Cit (0.238% and 0.476%). The difference in crude protein content between RP and SP was five percentage points.
Key results: Birds fed the RP diet had higher ileal digestibility of P, Na, Mg, S, Al, Fe, Cu and Zn than did those fed the SP on Day 23 (P < 0.01). Supplementation of both Arg, GAA and Cit to the RP reduced Mg digestibility on Day 23 (P < 0.001). The tibia and femur Ca and P concentrations were not different among the dietary treatments on either Day 23 or Day 35 (P > 0.05). Birds fed the RP had lower tibia and femur B concentrations and higher tibia and femur Zn concentrations on Day 23 and Day 35 and higher tibia and femur Mn concentrations on Day 35 than did those fed the SP (P < 0.01). Supplementation of Arg at the high level and Cit at both levels to the RP increased tibia S concentration on Day 23 (P < 0.001). Supplementation of Arg, Cit and GAA to the RP decreased femur Zn concentration on Day 35 (P < 0.001). Supplementation of GAA at the high level decreased concentrations of the tibia and femur B and Fe on Day 23, but increased tibia and femur Mn concentrations on Day 23 and Day 35 (P < 0.01).
Conclusions: The findings indicated an increased mineral digestibility but relatively similar bone mineral concentrations in broilers fed the RP diets when compared with the SP diets.
Implications: The results of the current study may provide useful information on the bird bone mineralisation and help expand the adoption of reduced-protein diets in the poultry industry.
Keywords: arginine, chicken, citrulline, femur, guanidinoacetic acid, low protein, mineral digestibility, tibia.
References
Ao T, Pierce JL, Power R, Pescatore AJ, Cantor AH, Dawson KA, Ford MJ (2009) Effects of feeding different forms of zinc and copper on the performance and tissue mineral content of chicks. Poultry Science 88, 2171–2175.| Effects of feeding different forms of zinc and copper on the performance and tissue mineral content of chicks.Crossref | GoogleScholarGoogle Scholar | 19762872PubMed |
Aviagen (2014a) ‘Ross 308 broiler management handbook.’ (Ross Breeders Limited: Newbridge, Midlothian, Scotland)
Aviagen (2014b) ‘Ross 308 broiler nutrition specification.’ (Ross Breeders Limited: Newbridge, Midlothian, Scotland)
Aviagen (2019) ‘Ross 308 broiler nutrition specification.’ (Ross Breeders Limited: Newbridge, Midlothian, Scotland)
Berta E, Andrásofszky E, Bersényi A, Glávits R, Gáspárdy A, Fekete SG (2004) Effect of inorganic and organic manganese supplementation on the performance and tissue manganese content of broiler chicks. Acta Veterinaria Hungarica 52, 199–209.
| Effect of inorganic and organic manganese supplementation on the performance and tissue manganese content of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 15168751PubMed |
Bhasker TV, Gowda NKS, Mondal S, Krishnamoorthy P, Pal DT, Mor A, Bhat SK, Pattanaik AK (2016) Boron influences immune and antioxidant responses by modulating hepatic superoxide dismutase activity under calcium deficit abiotic stress in Wistar rats. Journal of Trace Elements in Medicine and Biology 36, 73–79.
| Boron influences immune and antioxidant responses by modulating hepatic superoxide dismutase activity under calcium deficit abiotic stress in Wistar rats.Crossref | GoogleScholarGoogle Scholar | 27259355PubMed |
Boivin G, Meunier PJ (2002) The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcified Tissue International 70, 503–511.
| The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography.Crossref | GoogleScholarGoogle Scholar | 12019458PubMed |
Bradshaw RH, Kirkden RD, Broom DM (2002) A review of the aetiology and pathology of leg weakness in broilers in relation to welfare. Avian and Poultry Biology Reviews 13, 45–103.
| A review of the aetiology and pathology of leg weakness in broilers in relation to welfare.Crossref | GoogleScholarGoogle Scholar |
Bruno LDG, Luquetti BC, Furlan RL, Macari M (2007) Influence of early qualitative feed restriction and environmental temperature on long bone development of broiler chickens. Journal of Thermal Biology 32, 349–354.
| Influence of early qualitative feed restriction and environmental temperature on long bone development of broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Buijs S, Van Poucke E, Van Dongen S, Lens L, Baert J, Tuyttens FAM (2012) The influence of stocking density on broiler chicken bone quality and fluctuating asymmetry. Poultry Science 91, 1759–1767.
| The influence of stocking density on broiler chicken bone quality and fluctuating asymmetry.Crossref | GoogleScholarGoogle Scholar | 22802165PubMed |
Capps SG, Bottcher RW, Abrams CF, Scheideler SE (1997) Proximal tibiotarsal cancellous bone mechanical properties in broilers. Transactions of the ASAE 40, 1469–1473.
| Proximal tibiotarsal cancellous bone mechanical properties in broilers.Crossref | GoogleScholarGoogle Scholar |
Castro FLS, Su S, Choi H, Koo E, Kim WK (2019a) l-Arginine supplementation enhances growth performance, lean muscle, and bone density but not fat in broiler chickens. Poultry Science 98, 1716–1722.
| l-Arginine supplementation enhances growth performance, lean muscle, and bone density but not fat in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 30452708PubMed |
Castro FLS, Kim HY, Hong YG, Kim WK (2019b) The effect of total sulfur amino acid levels on growth performance, egg quality, and bone metabolism in laying hens subjected to high environmental temperature. Poultry Science 98, 4982–4993.
| The effect of total sulfur amino acid levels on growth performance, egg quality, and bone metabolism in laying hens subjected to high environmental temperature.Crossref | GoogleScholarGoogle Scholar | 31152669PubMed |
Corzo A, Moran ET, Hoehler D (2003) Arginine need of heavy broiler males: applying the ideal protein concept. Poultry Science 82, 402–407.
| Arginine need of heavy broiler males: applying the ideal protein concept.Crossref | GoogleScholarGoogle Scholar | 12705400PubMed |
Cowieson AJ, Ravindran V (2008) Effect of exogenous enzymes in maize-based diets varying in nutrient density for young broilers: growth performance and digestibility of energy, minerals and amino acids. British Poultry Science 49, 37–44.
| Effect of exogenous enzymes in maize-based diets varying in nutrient density for young broilers: growth performance and digestibility of energy, minerals and amino acids.Crossref | GoogleScholarGoogle Scholar | 18210288PubMed |
Cowieson AJ, Perez-Maldonado R, Kumar A, Toghyani M (2020) Possible role of available phosphorus in potentiating the use of low-protein diets for broiler chicken production. Poultry Science 99, 6954–6963.
| Possible role of available phosphorus in potentiating the use of low-protein diets for broiler chicken production.Crossref | GoogleScholarGoogle Scholar | 33248611PubMed |
Dao HT, Sharma NK, Bradbury EJ, Swick RA (2021) Response of meat chickens to different sources of arginine in low-protein diets. Journal of Animal Physiology and Animal Nutrition 105, 731–746.
| Response of meat chickens to different sources of arginine in low-protein diets.Crossref | GoogleScholarGoogle Scholar | 33410556PubMed |
David LS, Abdollahi MR, Bedford MR, Ravindran V (2020) Effect of age and dietary crude protein content on the apparent ileal calcium digestibility of limestone in broiler chickens. Animal Feed Science and Technology 263, 114468
| Effect of age and dietary crude protein content on the apparent ileal calcium digestibility of limestone in broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Davis CD, Ney DM, Greger JL (1990) Manganese, iron and lipid interactions in rats. The Journal of Nutrition 120, 507–513.
| Manganese, iron and lipid interactions in rats.Crossref | GoogleScholarGoogle Scholar | 2341915PubMed |
Davis CD, Wolf TL, Greger JL (1992) Varying levels of manganese and iron affect absorption and gut endogenous losses of manganese by rats. The Journal of Nutrition 122, 1300–1308.
| Varying levels of manganese and iron affect absorption and gut endogenous losses of manganese by rats.Crossref | GoogleScholarGoogle Scholar | 1588448PubMed |
DeGroot AA, Braun U, Dilger RN (2018) Efficacy of guanidinoacetic acid on growth and muscle energy metabolism in broiler chicks receiving arginine-deficient diets. Poultry Science 97, 890–900.
| Efficacy of guanidinoacetic acid on growth and muscle energy metabolism in broiler chicks receiving arginine-deficient diets.Crossref | GoogleScholarGoogle Scholar | 29294127PubMed |
Dilger RN, Bryant-Angeloni K, Payne RL, Lemme A, Parsons CM (2013) Dietary guanidino acetic acid is an efficacious replacement for arginine for young chicks. Poultry Science 92, 171–177.
| Dietary guanidino acetic acid is an efficacious replacement for arginine for young chicks.Crossref | GoogleScholarGoogle Scholar | 23243244PubMed |
Dilworth BC, Day EJ (1965) Effect of varying dietary calcium: phosphorus ratios on tibia and femur composition of the chick. Poultry Science 44, 1474–1479.
| Effect of varying dietary calcium: phosphorus ratios on tibia and femur composition of the chick.Crossref | GoogleScholarGoogle Scholar | 5863775PubMed |
Fernandes JIM, Murakami AE, de Souza LMG, Ospina-Rojas IC, Rossi RM (2014) Effect of arginine supplementation of broiler breeder hens on progeny performance. Canadian Journal of Animal Science 94, 313–321.
| Effect of arginine supplementation of broiler breeder hens on progeny performance.Crossref | GoogleScholarGoogle Scholar |
Heaney RP, Layman DK (2008) Amount and type of protein influences bone health. The American Journal of Clinical Nutrition 87, 1567S–1570S.
| Amount and type of protein influences bone health.Crossref | GoogleScholarGoogle Scholar | 18469289PubMed |
Hilliar M, Huyen N, Girish CK, Barekatain R, Wu S, Swick RA (2019) Supplementing glycine, serine, and threonine in low protein diets for meat type chickens. Poultry Science 98, 6857–6865.
| Supplementing glycine, serine, and threonine in low protein diets for meat type chickens.Crossref | GoogleScholarGoogle Scholar | 31433853PubMed |
Itoh H, Hatano T (1964) Comparison of calcium metabolism in various bones of growing chicks in varying states of vitamin D supplementation. Poultry Science 43, 70–76.
| Comparison of calcium metabolism in various bones of growing chicks in varying states of vitamin D supplementation.Crossref | GoogleScholarGoogle Scholar |
Jasek A, Latham RE, Mañón A, Llamas-Moya S, Adhikari R, Poureslami R, Lee JT (2018) Impact of a multicarbohydrase containing α-galactosidase and xylanase on ileal digestible energy, crude protein digestibility, and ileal amino acid digestibility in broiler chickens. Poultry Science 97, 3149–3155.
| Impact of a multicarbohydrase containing α-galactosidase and xylanase on ileal digestible energy, crude protein digestibility, and ileal amino acid digestibility in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 29897592PubMed |
Jin E, Hu Q, Ren M, Jin G, Liang L, Li S (2019) Effects of selenium yeast in combination with boron on muscle growth and muscle quality in broilers. Biological Trace Element Research 190, 472–483.
| Effects of selenium yeast in combination with boron on muscle growth and muscle quality in broilers.Crossref | GoogleScholarGoogle Scholar | 30392019PubMed |
Juanpere J, Pérez-Vendrell AM, Angulo E, Brufau J (2005) Assessment of potential interactions between phytase and glycosidase enzyme supplementation on nutrient digestibility in broilers. Poultry Science 84, 571–580.
| Assessment of potential interactions between phytase and glycosidase enzyme supplementation on nutrient digestibility in broilers.Crossref | GoogleScholarGoogle Scholar | 15844813PubMed |
Kidd MT, Ferket PR, Qureshi MA (1996) Zinc metabolism with special reference to its role in immunity. World’s Poultry Science Journal 52, 309–324.
| Zinc metabolism with special reference to its role in immunity.Crossref | GoogleScholarGoogle Scholar |
Küçükyilmaz K, Bozkurt M, Çınar M, Tüzün AE (2017) Evaluation of the boron and phytase, alone or in combination, in broiler diets. The Journal of Poultry Science 54, 26–33.
| Evaluation of the boron and phytase, alone or in combination, in broiler diets.Crossref | GoogleScholarGoogle Scholar | 32908405PubMed |
Kurtoğlu F, Kurtoğlu V, Celik I, Keçeci T, Nizamlioğlu M (2005) Effects of dietary boron supplementation on some biochemical parameters, peripheral blood lymphocytes, splenic plasma cells and bone characteristics of broiler chicks given diets with adequate or inadequate cholecalciferol (vitamin D3) content. British Poultry Science 46, 87–96.
| Effects of dietary boron supplementation on some biochemical parameters, peripheral blood lymphocytes, splenic plasma cells and bone characteristics of broiler chicks given diets with adequate or inadequate cholecalciferol (vitamin D3) content.Crossref | GoogleScholarGoogle Scholar | 15835257PubMed |
Leach MR, Lilburn MS (1992) Current knowledge on the etiology of tibial dyschondroplasia in the avian species. Poultry Science Review 4, 57–65.
Lee DY, Johnson PE (1988) Factors affecting absorption and excretion of 54Mn in rats. The Journal of Nutrition 118, 1509–1516.
| Factors affecting absorption and excretion of 54Mn in rats.Crossref | GoogleScholarGoogle Scholar | 3210079PubMed |
Lewis PD, Danisman R, Gous RM (2009) Photoperiodic responses of broilers. III. Tibial breaking strength and ash content. British Poultry Science 50, 673–679.
| Photoperiodic responses of broilers. III. Tibial breaking strength and ash content.Crossref | GoogleScholarGoogle Scholar | 19946820PubMed |
McCarty KF, Mills MJ, Medlin DL, Friedmann TA (1994) Comment on ‘Growth and characterization of epitaxial cubic boron nitride films on silicon’. Physical Review B: Condensed Matter and Materials Physics 50, 8907
| Comment on ‘Growth and characterization of epitaxial cubic boron nitride films on silicon’.Crossref | GoogleScholarGoogle Scholar |
McCoy H, Kenney MA, Montgomery C, Irwin A, Williams L, Orrell R (1994) Relation of boron to the composition and mechanical properties of bone. Environmental Health Perspectives 102, 49–53.
| Relation of boron to the composition and mechanical properties of bone.Crossref | GoogleScholarGoogle Scholar | 7889880PubMed |
Moran ET, Todd MC (1994) Continuous submarginal phosphorus with broilers and the effect of preslaughter transportation: carcass defects, further-processing yields, and tibia-femur integrity. Poultry Science 73, 1448–1457.
| Continuous submarginal phosphorus with broilers and the effect of preslaughter transportation: carcass defects, further-processing yields, and tibia-femur integrity.Crossref | GoogleScholarGoogle Scholar | 7800647PubMed |
Morris SM (2016) Arginine metabolism revisited. The Journal of Nutrition 146, 2579S–2586S.
| Arginine metabolism revisited.Crossref | GoogleScholarGoogle Scholar | 27934648PubMed |
Moss A (2020) Database of the nutrient content of Australian feed ingredients. AgriFutures Australia, Publication No. 20-078, Wagga Wagga, NSW, Australia. Available at https://agrifutures.com.au/wp-content/uploads/2020/09/20-078.pdf. [Verified 17 February 2021]
Moss AF, Sydenham CJ, Khoddami A, Naranjo VD, Liu SY, Selle PH (2018) Dietary starch influences growth performance, nutrient utilisation and digestive dynamics of protein and amino acids in broiler chickens offered low-protein diets. Animal Feed Science and Technology 237, 55–67.
| Dietary starch influences growth performance, nutrient utilisation and digestive dynamics of protein and amino acids in broiler chickens offered low-protein diets.Crossref | GoogleScholarGoogle Scholar |
Mwangi S, Timmons J, Ao T, Paul M, Macalintal L, Pescatore A, Cantor A, Dawson KA (2019) Effect of manganese preconditioning and replacing inorganic manganese with organic manganese on performance of male broiler chicks. Poultry Science 98, 2105–2113.
| Effect of manganese preconditioning and replacing inorganic manganese with organic manganese on performance of male broiler chicks.Crossref | GoogleScholarGoogle Scholar | 30590788PubMed |
Naz S, Idris M, Khalique MA Naz S, Idris M, Khalique MA Naz S, Idris M, Khalique MA (2016) The activity and use of zinc in poultry diets. World’s Poultry Science Journal 72, 159–167.
| The activity and use of zinc in poultry diets.Crossref | GoogleScholarGoogle Scholar |
NHMRC (2013) ‘Australian code of practice for the care and use of animals for scientific purposes.’, 8th edn. (The National Health and Medical Research Council, Australia)
Olgun O, Bahtiyarca Y (2015) Effects of dietary cadmium and boron supplementation on performance, eggshell quality and mineral concentrations of bone in laying hens. Biological Trace Element Research 167, 56–62.
| Effects of dietary cadmium and boron supplementation on performance, eggshell quality and mineral concentrations of bone in laying hens.Crossref | GoogleScholarGoogle Scholar | 25749927PubMed |
Pradhan SK, Kumar B, Banakara KB, Patel VR, Pandya HR, Singh RR (2020) Effect of boron supplementation on the performance and metabolism of minerals in broiler chicken. Animal Nutrition and Feed Technology 20, 39–49.
| Effect of boron supplementation on the performance and metabolism of minerals in broiler chicken.Crossref | GoogleScholarGoogle Scholar |
Rath NC, Huff GR, Huff WE, Balog JM (2000) Factors regulating bone maturity and strength in poultry. Poultry Science 79, 1024–1032.
| Factors regulating bone maturity and strength in poultry.Crossref | GoogleScholarGoogle Scholar | 10901206PubMed |
Reichling TD, German RZ (2000) Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. The Journal of Nutrition 130, 2326–2332.
| Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size.Crossref | GoogleScholarGoogle Scholar | 10958831PubMed |
Rerkasem B, Jamjod S (2004) Boron deficiency in wheat: a review. Field Crops Research 89, 173–186.
| Boron deficiency in wheat: a review.Crossref | GoogleScholarGoogle Scholar |
Ringel J, Rademacher M, Elwert C (2013) Arginine sparing effect of guanidinoacetic acid in broilers. In ‘Proceedings of the 19th european symposium on poultry nutrition’. (World’s Poultry Science Association: Potsdam, Germany)
Rondanelli M, Faliva MA, Peroni G, Infantino V, Gasparri C, Iannello G, Perna S, Riva A, Petrangolini G, Tartara A (2020) Pivotal role of boron supplementation on bone health: a narrative review. Journal of Trace Elements in Medicine and Biology 62, 126577
| Pivotal role of boron supplementation on bone health: a narrative review.Crossref | GoogleScholarGoogle Scholar | 32540741PubMed |
Rossander-Hultén L, Brune M, Sandström B, Lönnerdal B, Hallberg L (1991) Competitive inhibition of iron absorption by manganese and zinc in humans. The American Journal of Clinical Nutrition 54, 152–156.
| Competitive inhibition of iron absorption by manganese and zinc in humans.Crossref | GoogleScholarGoogle Scholar | 2058577PubMed |
Sazzad HM, Bertechini AG, Nobre PTC (1994) Egg production, tissue deposition and mineral metabolism in two strains of commercial layers with various levels of manganese in diets. Animal Feed Science and Technology 46, 271–275.
| Egg production, tissue deposition and mineral metabolism in two strains of commercial layers with various levels of manganese in diets.Crossref | GoogleScholarGoogle Scholar |
Scott ML, Nesheim MC, Yang RJ (1982) Essential inorganic elements. In ‘Nutrition of the Chicken’. (Eds ML Scott, MC Nesheim, RJ Yang) pp. 277–382. (ML Scott and Associates: New York, NY, USA)
Shim MY, Karnuah AB, Mitchell AD, Anthony NB, Pesti GM, Aggrey SE (2012) The effects of growth rate on leg morphology and tibia breaking strength, mineral density, mineral content, and bone ash in broilers. Poultry Science 91, 1790–1795.
| The effects of growth rate on leg morphology and tibia breaking strength, mineral density, mineral content, and bone ash in broilers.Crossref | GoogleScholarGoogle Scholar | 22802169PubMed |
Short FJ, Gorton P, Wiseman J, Boorman KN (1996) Determination of titanium dioxide added as an inert marker in chicken digestibility studies. Animal Feed Science and Technology 59, 215–221.
| Determination of titanium dioxide added as an inert marker in chicken digestibility studies.Crossref | GoogleScholarGoogle Scholar |
Skinner JT, Beasley JN, Waldroup PW (1991) Effects of dietary amino acid levels on bone development in broiler chickens. Poultry Science 70, 941–946.
| Effects of dietary amino acid levels on bone development in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1876569PubMed |
Smith DP (1999) Know your quality. Broiler Industry 62, 22
Su CL, Austic RE (1999) The recycling of l-citrulline to l-arginine in a chicken macrophage cell line. Poultry Science 78, 353–355.
| The recycling of l-citrulline to l-arginine in a chicken macrophage cell line.Crossref | GoogleScholarGoogle Scholar | 10090261PubMed |
Talaty PN, Katanbaf MN, Hester PY (2009) Life cycle changes in bone mineralization and bone size traits of commercial broilers. Poultry Science 88, 1070–1077.
| Life cycle changes in bone mineralization and bone size traits of commercial broilers.Crossref | GoogleScholarGoogle Scholar | 19359697PubMed |
Tamir H, Ratner S (1963) A study of ornithine, citrulline and arginine synthesis in growing chicks. Archives of Biochemistry and Biophysics 102, 259–269.
| A study of ornithine, citrulline and arginine synthesis in growing chicks.Crossref | GoogleScholarGoogle Scholar | 14061730PubMed |
Thomson ABR, Olatunbosun D, Valberg LS (1971) Interrelation of intestinal transport system for manganese and iron. The Journal of Laboratory and Clinical Medicine 78, 642–655.
| Interrelation of intestinal transport system for manganese and iron.Crossref | GoogleScholarGoogle Scholar |
Truong HH, Bold RM, Liu SY, Selle PH (2015) Standard phytase inclusion in maize-based broiler diets enhances digestibility coefficients of starch, amino acids and sodium in four small intestinal segments and digestive dynamics of starch and protein. Animal Feed Science and Technology 209, 240–248.
| Standard phytase inclusion in maize-based broiler diets enhances digestibility coefficients of starch, amino acids and sodium in four small intestinal segments and digestive dynamics of starch and protein.Crossref | GoogleScholarGoogle Scholar |
Waldenstedt L (2006) Nutritional factors of importance for optimal leg health in broilers: a review. Animal Feed Science and Technology 126, 291–307.
| Nutritional factors of importance for optimal leg health in broilers: a review.Crossref | GoogleScholarGoogle Scholar |
Wang W, Xiao K, Zheng X, Zhu D, Yang Z, Tang J, Sun P, Wang J, Peng K (2014) Effects of supplemental boron on growth performance and meat quality in african ostrich chicks. Journal of Agricultural and Food Chemistry 62, 11024–11029.
| Effects of supplemental boron on growth performance and meat quality in african ostrich chicks.Crossref | GoogleScholarGoogle Scholar | 25363572PubMed |
Wedekind KJ, Titgemeyer EC, Twardock AR, Baker DH (1991) Phosphorus, but not calcium, affects manganese absorption and turnover in chicks. The Journal of Nutrition 121, 1776–1786.
| Phosphorus, but not calcium, affects manganese absorption and turnover in chicks.Crossref | GoogleScholarGoogle Scholar | 1941186PubMed |
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37, 1–17.
| Amino acids: metabolism, functions, and nutrition.Crossref | GoogleScholarGoogle Scholar | 19301095PubMed |
Wu G, Morris SM (1998) Arginine metabolism: nitric oxide and beyond. Biochemical Journal 336, 1–17.
| Arginine metabolism: nitric oxide and beyond.Crossref | GoogleScholarGoogle Scholar |
Zanu HK, Kheravii SK, Morgan NK, Bedford MR, Swick RA (2020) Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. Serum calcium and phosphorus, and bone mineralization. Poultry Science 99, 3617–3627.
| Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. Serum calcium and phosphorus, and bone mineralization.Crossref | GoogleScholarGoogle Scholar | 32616258PubMed |
Zhu Z, Yan L, Hu S, An S, Lv Z, Wang Z, Wu Y, Zhu Y, Zhao M, Gu C, Zhang A (2019) Effects of the different levels of dietary trace elements from organic or inorganic sources on growth performance, carcass traits, meat quality, and faecal mineral excretion of broilers. Archives of Animal Nutrition 73, 324–337.
| Effects of the different levels of dietary trace elements from organic or inorganic sources on growth performance, carcass traits, meat quality, and faecal mineral excretion of broilers.Crossref | GoogleScholarGoogle Scholar | 31192701PubMed |
