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REVIEW

Nutritional implications of feeding reduced-protein diets to meat chickens

M. Hilliar https://orcid.org/0000-0001-7292-0007 A B and R. A. Swick A
+ Author Affiliations
- Author Affiliations

A School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

B Corresponding author. Email: matthilliar@gmail.com

Animal Production Science 59(11) 2069-2081 https://doi.org/10.1071/AN19221
Submitted: 18 April 2019  Accepted: 12 June 2019   Published: 13 September 2019

Abstract

Global interest has emerged for the implementation of reduced-protein diets for meat chickens. The necessity of their development stems from environmental impacts and health and welfare concerns surrounding current meat-chicken production. Reduced crude-protein diets are possible with the increasing affordability of supplemental crystalline amino acids. Supplementing broiler feed with methionine, lysine and threonine is common practice in industry and has enabled a reduction of dietary crude protein to the levels currently used. However, further reduction of dietary protein often results in poor performance. Several nutritional options have been investigated with a focus on crystalline essential and non-essential amino acids such as glycine. However, reducing the crude protein of meat-chicken diets does change the ingredient and nutrient profile aside from the amino acid composition. Alterations in non-protein nitrogen concentrations, dietary electrolyte balance, minerals, fibre and carbohydrates, methyl-donors and polyphenols must be considered in formulations to ensure successful implementation of reduced-protein diets. The ability to maintain performance with reduced-protein diets may benefit sustainability and longevity of the meat-chicken industry.

Additional keywords: amino acids, broiler, crude protein, nitrogen, nutrition, sustainability.


References

Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. The Journal of Biological Chemistry 262, 5592–5595.

Alhotan RA, Pesti GM (2016) Quantitative estimates of the optimal balance between digestible lysine and the true protein contents of broiler feeds. British Poultry Science 57, 538–550.
Quantitative estimates of the optimal balance between digestible lysine and the true protein contents of broiler feeds.Crossref | GoogleScholarGoogle Scholar | 27098889PubMed |

Alleman F, Leclercq B (1997) Effect of dietary protein and environmental temperature on growth performance and water consumption of male broiler chickens. British Poultry Science 38, 607–610.
Effect of dietary protein and environmental temperature on growth performance and water consumption of male broiler chickens.Crossref | GoogleScholarGoogle Scholar | 9511009PubMed |

Alltech (2018) ‘2019 global feed survey.’ Available at https://www.alltech.com/feed-survey [Verified 10 March 2019]

Angel CR, Saylor W, Vierira SL, Ward N (2011) Effects of a monocomponent protease on performance and protein utilization in 7- to 22-day-old broiler chickens. Poultry Science 90, 2281–2286.
Effects of a monocomponent protease on performance and protein utilization in 7- to 22-day-old broiler chickens.Crossref | GoogleScholarGoogle Scholar | 21934011PubMed |

Anwar MN, Morel PCH, Ravindran V, Ravindran G, Cowieson AJ (2016) Measurement of true ileal calcium digestibility in meat and bone meal for broiler chickens using the direct method. Poultry Science 95, 70–76.
Measurement of true ileal calcium digestibility in meat and bone meal for broiler chickens using the direct method.Crossref | GoogleScholarGoogle Scholar | 26546671PubMed |

Apajalahti J, Vienola K (2016) Interaction between chicken intestinal microbiota and protein digestion. Animal Feed Science and Technology 221, 323–330.
Interaction between chicken intestinal microbiota and protein digestion.Crossref | GoogleScholarGoogle Scholar |

Apajalahti J, Kettunen A, Graham H (2004) Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World’s Poultry Science Journal 60, 223–232.
Characteristics of the gastrointestinal microbial communities, with special reference to the chicken.Crossref | GoogleScholarGoogle Scholar |

Armour JC, Perera RLC, Buchan WC, Grant G (1998) Protease inhibitors and lectins in soya beans and effects of aqueous heat-treatment. Journal of the Science of Food and Agriculture 78, 225–231.
Protease inhibitors and lectins in soya beans and effects of aqueous heat-treatment.Crossref | GoogleScholarGoogle Scholar |

Austic R (1976) Nutritional and metabolic interrelationships of arginine, glutamic acid and proline in the chicken. Federation Proceedings 35, 1914–1916.

Baker DH (2009) Advances in protein–amino acid nutrition of poultry. Amino Acids 37, 29–41.
Advances in protein–amino acid nutrition of poultry.Crossref | GoogleScholarGoogle Scholar | 19009229PubMed |

Baker DH, Han Y (1994) Ideal amino acid profile for chicks during the first three weeks posthatching. Poultry Science 73, 1441–1447.
Ideal amino acid profile for chicks during the first three weeks posthatching.Crossref | GoogleScholarGoogle Scholar | 7800646PubMed |

Baker DH, Sugahara M, Scott HM (1968) The glycine-serine interrelationship in chick nutrition. Poultry Science 47, 1376–1377.
The glycine-serine interrelationship in chick nutrition.Crossref | GoogleScholarGoogle Scholar | 5725369PubMed |

Ball RO, Urschel KL, Pencharz PB (2007) Nutritional consequences of interspecies differences in arginine and lysine metabolism. The Journal of Nutrition 137, 1626S–1641S.
Nutritional consequences of interspecies differences in arginine and lysine metabolism.Crossref | GoogleScholarGoogle Scholar | 17513439PubMed |

Bao YM, Choct M (2010) Dietary NSP nutrition and intestinal immune system for broiler chickens. World’s Poultry Science Journal 66, 511–518.
Dietary NSP nutrition and intestinal immune system for broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Barnes S, Kirk M, Coward L (1994) Isoflavones and their conjugates in soy foods: extraction conditions and analysis by HPLC–mass spectrometry. Journal of Agricultural and Food Chemistry 42, 2466–2474.
Isoflavones and their conjugates in soy foods: extraction conditions and analysis by HPLC–mass spectrometry.Crossref | GoogleScholarGoogle Scholar |

Batterham ES, Darnell RE, Herbert LS, Major EJ (1986) Effect of pressure and temperature on the availability of lysine in meat and bone meal as determined by slope-ratio assays with growing pigs, rats and chicks and by chemical techniques. British Journal of Nutrition 55, 441–453.
Effect of pressure and temperature on the availability of lysine in meat and bone meal as determined by slope-ratio assays with growing pigs, rats and chicks and by chemical techniques.Crossref | GoogleScholarGoogle Scholar | 3118935PubMed |

Bedford MR (2018) The evolution and application of enzymes in the animal feed industry: the role of data interpretation. British Poultry Science 59, 486–493.
The evolution and application of enzymes in the animal feed industry: the role of data interpretation.Crossref | GoogleScholarGoogle Scholar | 29877713PubMed |

Belloir P, Meda B, Lambert W, Corrent E, Juin H, Lessire M, Tesseraud S (2017) Reducing the CP content in broiler feeds: impact on animal performance, meat quality and nitrogen utilization. Animal 11, 1881–1889.
Reducing the CP content in broiler feeds: impact on animal performance, meat quality and nitrogen utilization.Crossref | GoogleScholarGoogle Scholar | 28462773PubMed |

Bradbury EJ, Edwards L, Avery B, Nash D (2018) A review of the application of polyphenols in poultry. In ‘Australian poultry science symposium’, 4–7 February 2018, Sydney, NSW, Australia.

Bregendahl K, Sell JL, Zimmerman DR (2002) Effect of low protein diet on performance and body composition of broiler chicks. Poultry Science 81, 1156–1167.
Effect of low protein diet on performance and body composition of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 12211308PubMed |

Briggs J, Maier DE, Watkins B, Behnke K (1999) Effect of ingredients and processing parameters on pellet quality. Poultry Science 78, 1464–1471.
Effect of ingredients and processing parameters on pellet quality.Crossref | GoogleScholarGoogle Scholar | 10536797PubMed |

Burgdorfer B (2009) ‘US chicken feet are being booted out of China.’ (Reuters, Thomson Reuters: Chicago, IL)

Casteel SN, Maguire RO, Israel DW, Crozier CR, Brake J (2011) Broiler breeder manure phosphorus forms are affected by diet, location, and period of accumulation. Poultry Science 90, 2689–2696.
Broiler breeder manure phosphorus forms are affected by diet, location, and period of accumulation.Crossref | GoogleScholarGoogle Scholar | 22080005PubMed |

Choct M (2006) Enzymes for the feed industry: past, present and future. World’s Poultry Science Journal 62, 5–16.
Enzymes for the feed industry: past, present and future.Crossref | GoogleScholarGoogle Scholar |

Choct M, Annison G (1990) Anti‐nutritive activity of wheat pentosans in broiler diets. British Poultry Science 31, 811–821.
Anti‐nutritive activity of wheat pentosans in broiler diets.Crossref | GoogleScholarGoogle Scholar | 2097035PubMed |

Choct M, Annison G (1992) Anti‐nutritive effect of wheat pentosans in broiler chickens: roles of viscosity and gut microflora. British Poultry Science 33, 821–834.
Anti‐nutritive effect of wheat pentosans in broiler chickens: roles of viscosity and gut microflora.Crossref | GoogleScholarGoogle Scholar | 1393677PubMed |

Choct M, Dersjant-Li Y, McLeish J, Peisker M (2010) Soy oligosaccharides and soluble non-starch polysaccharides: a review of digestion, nutritive and anti-nutritive effects in pigs and poultry. Asian-Australasian Journal of Animal Sciences 23, 1386–1398.
Soy oligosaccharides and soluble non-starch polysaccharides: a review of digestion, nutritive and anti-nutritive effects in pigs and poultry.Crossref | GoogleScholarGoogle Scholar |

Chrystal PV, Selle PH, Moss AF, Yin D, Khoddami A, Naranjo VD, Liu SY (2019) The impact of dietary electrolyte balance on male broiler performance offered reduced crude protein diets. In ‘Australian poultry science symposium’, 17–20 February 2019, Sydney, NSW, Australia.

Cooper KK, Songer GJ, Uzal FA (2013) Diagnosing clostridial enteric disease in poultry. Journal of Veterinary Diagnostic Investigation 25, 314–327.
Diagnosing clostridial enteric disease in poultry.Crossref | GoogleScholarGoogle Scholar | 23572451PubMed |

Corzo A, Kidd MT, Burnham DJ, Kerr BJ (2004) Dietary glycine needs of broiler chicks. Poultry Science 83, 1382–1384.
Dietary glycine needs of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 15339014PubMed |

Corzo A, Fritts CA, Kidd MT, Kerr BJ (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.
Response of broiler chicks to essential and non-essential amino acid supplementation of low crude protein diets.Crossref | GoogleScholarGoogle Scholar |

Corzo A, Kidd MT, Dozier WA, Kerr BJ (2009) Dietary glycine and threonine interactive effects in broilers. Journal of Applied Poultry Research 18, 79–84.
Dietary glycine and threonine interactive effects in broilers.Crossref | GoogleScholarGoogle Scholar |

Cowieson AJ, Ruckebusch JP, Sorbara JOB, Wilson JW, Guggenbuhl P, Roos FF (2017a) A systematic view on the effect of phytase on ileal amino acid digestibility in broilers. Animal Feed Science and Technology 225, 182–194.
A systematic view on the effect of phytase on ileal amino acid digestibility in broilers.Crossref | GoogleScholarGoogle Scholar |

Cowieson AJ, Zaefarian F, Knap I, Ravindran V (2017b) Interactive effects of dietary protein concentration, a mono-component exogenous protease and ascorbic acid on broiler performance, nutritional status and gut health. Animal Production Science 57, 1058–1068.
Interactive effects of dietary protein concentration, a mono-component exogenous protease and ascorbic acid on broiler performance, nutritional status and gut health.Crossref | GoogleScholarGoogle Scholar |

D’Este M, Alvarado-Morales M, Angelidake I (2018) Amino acids production focusing on fermentation technologies: a review. Biotechnology Advances 36, 14–25.
Amino acids production focusing on fermentation technologies: a review.Crossref | GoogleScholarGoogle Scholar | 28888551PubMed |

Davis AJ, Austic RE (1997) Dietary protein and amino acid levels alter threonine dehydrogenase activity in hepatic mitochondria of Gallus domesticus. The Journal of Nutrition 127, 738–744.
Dietary protein and amino acid levels alter threonine dehydrogenase activity in hepatic mitochondria of Gallus domesticus.Crossref | GoogleScholarGoogle Scholar | 9164995PubMed |

Dean WF, Scott HM (1968) Ability of arginine to reverse the growth depression induced by supplementing a crystalline amino acid diet with excess lysine. Poultry Science 47, 341–342.
Ability of arginine to reverse the growth depression induced by supplementing a crystalline amino acid diet with excess lysine.Crossref | GoogleScholarGoogle Scholar | 5645315PubMed |

Dean D, Bidner TD, Southern LL (2006) Glycine supplementation to low crude protein, amino acid supplemented diets supports optimal performance of broiler chicks. Poultry Science 85, 288–296.
Glycine supplementation to low crude protein, amino acid supplemented diets supports optimal performance of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 16523629PubMed |

DeGroot AA, Braun U, Dilger RN (2019) Guanidinoacetic acid is efficacious in improving growth performance and muscle energy homeostasis in broiler chicks fed arginine-deficient or arginine-adequate diets. Poultry Science 98, 2896–2905.
Guanidinoacetic acid is efficacious in improving growth performance and muscle energy homeostasis in broiler chicks fed arginine-deficient or arginine-adequate diets.Crossref | GoogleScholarGoogle Scholar | 30850832PubMed |

Drew MD, Syed NA, Goldade BG, Laarveld B, Van Kessel AG (2004) Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens. Poultry Science 83, 414–420.
Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 15049494PubMed |

du Vigneaud V, Chandler JP, Moyer AW, Keppel DM (1939) The effect of choline on the ability of homocystine to replace methionine in the diet. The Journal of Biological Chemistry 131, 57–76.

Ducrot C, Paul M, Calavas D (2013) BSE risk and the use of meat and bone meal in the feed industry: perspectives in the context of relaxing control measures. Nature Sciences Sociétés 21, 3–12.
BSE risk and the use of meat and bone meal in the feed industry: perspectives in the context of relaxing control measures.Crossref | GoogleScholarGoogle Scholar |

Dumas MD, Polson SW, Ritter D, Ravel J, Gleb J, Morgan R, Wommack KE (2011) Impacts of poultry house environment on poultry litter bacterial community composition. PLoS One 6, e24785
Impacts of poultry house environment on poultry litter bacterial community composition.Crossref | GoogleScholarGoogle Scholar | 21949751PubMed |

Evonik Nutrition and Care GmbH (2015) ‘AMINODat® 5.0.’ Available at https://animal-nutrition.evonik.com/product/feed-additives/en/services/animal-nutrition/aminodat/ [Verified 10 April 2019]

Evonik Nutrition and Care GmbH (2017) ‘Evonik industries AG.’ Available at https://corporate.evonik.com/misc/micro/methionine/methionin_en.html [Verified 8 April 2019]

Fancher BI, Jensen LS (1989a) Influence on performance of three to six-week-old broilers of varying dietary protein contents with supplementation of essential amino acid requirements. Poultry Science 68, 113–123.
Influence on performance of three to six-week-old broilers of varying dietary protein contents with supplementation of essential amino acid requirements.Crossref | GoogleScholarGoogle Scholar | 2704667PubMed |

Fancher BI, Jensen LS (1989b) Male broiler performance during the starting and growing periods as affected by dietary protein, essential amino acids, and potassium levels. Poultry Science 68, 1385–1395.
Male broiler performance during the starting and growing periods as affected by dietary protein, essential amino acids, and potassium levels.Crossref | GoogleScholarGoogle Scholar | 2587474PubMed |

Fukushima D (2011) Soy proteins. In ‘Handbook of food proteins’. pp. 210–232. (Woodhead Publishing: Cambridge, UK)

Gregg K, Rogers GE (1986) Feather keratin: composition, structure and biogenesis. In ‘Biology of the integument. Vol. 2’. (Ed. J Bereiter-Hahn) pp. 667–690. (Springer Verlag: Berlin)

Hafkenscheid JCM, Hectors MPC (1975) An enzymic method for the determination of the glycine/taurine ratio of conjugated bile acids in bile. Clinica Chimica Acta 65, 67–74.
An enzymic method for the determination of the glycine/taurine ratio of conjugated bile acids in bile.Crossref | GoogleScholarGoogle Scholar |

Harms RH, Damron BL, Simpson CF (1977) Effect of wet litter and supplemental biotin and/or whey on the production of foot pad dermatitis in broilers. Poultry Science 56, 291–296.
Effect of wet litter and supplemental biotin and/or whey on the production of foot pad dermatitis in broilers.Crossref | GoogleScholarGoogle Scholar | 605009PubMed |

Harper AE, Miller RH, Block KP (1984) Branched-chain amino acid metabolism. Annual Review of Nutrition 4, 409–454.
Branched-chain amino acid metabolism.Crossref | GoogleScholarGoogle Scholar | 6380539PubMed |

He S, Zhao S, Dai S, Liu D, Bokhari SG (2015) Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress. Animal Science Journal 86, 897–903.
Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress.Crossref | GoogleScholarGoogle Scholar | 25780810PubMed |

Heger J, Pack M (1996) Effects of glycine + serine on starting broiler performance as influenced by dietary crude protein concentrations. Agribiological Research 49, 257–265.

Hernández F, Lopez M, Martinez S, Megias MD, Catala P, Madrid J (2012) Effect of low-protein diets and single sex on production performance, plasma metabolites, digestibility, and nitrogen excretion in 1- to 48-day-old broilers. Poultry Science 91, 683–692.
Effect of low-protein diets and single sex on production performance, plasma metabolites, digestibility, and nitrogen excretion in 1- to 48-day-old broilers.Crossref | GoogleScholarGoogle Scholar | 22334744PubMed |

Hilliar M, Ninh H, Morgan N, Hargreave G, Barekatain R, Wu S, Girish CK, Swick RA (2018) Investigating the effects of glycine and glycine equivalents on meat chicken performance under low protein diets. In ‘Australian poultry science symposium’, 4–7 February 2018, Sydney, NSW, Australia.

Hilliar M, Kheravii SK, Ninh H, Wu S, Girish CK, Swick RA (2019) Low protein diets downregulate hepatic enzymes responsible for nonessential amino acid synthesis in broilers. In ‘Australian poultry science symposium’, 17–20 February 2019, Sydney, NSW, Australia.

Hurwitz S, Cohen I, Bar A, Bornstein S (1973) Sodium and chloride requirements of the chick: relationship to acid-base balance. Poultry Science 52, 903–909.
Sodium and chloride requirements of the chick: relationship to acid-base balance.Crossref | GoogleScholarGoogle Scholar | 4754047PubMed |

Ireland PA, Dziedzic SZ, Kearsley MW (1986) Saponin content of soya and some commercial soya products by means of high-performance liquid chromatography of the sapogenins. Journal of the Science of Food and Agriculture 37, 694–698.
Saponin content of soya and some commercial soya products by means of high-performance liquid chromatography of the sapogenins.Crossref | GoogleScholarGoogle Scholar |

James EC, Wheeler RS (1949) Relation of dietary protein content to water intake, water elimination and amount of cloacal excreta produced by growing chickens. Poultry Science 28, 465–467.
Relation of dietary protein content to water intake, water elimination and amount of cloacal excreta produced by growing chickens.Crossref | GoogleScholarGoogle Scholar |

Jiang Q, Waldroup PW, Fritts CA (2005) Improving the utilization of diets low in crude protein for broiler chicken 1. Evaluation of special amino acid supplementation to diets low in crude protein. International Journal of Poultry Science 4, 115–122.
Improving the utilization of diets low in crude protein for broiler chicken 1. Evaluation of special amino acid supplementation to diets low in crude protein.Crossref | GoogleScholarGoogle Scholar |

Jiang ZY, Jiang SQ, Lin YC, Xi PB, Yu DQ, Wu TX (2007) Effects of soybean isoflavone on growth performance, meat quality, and antioxidation in male broilers. Poultry Science 86, 1356–1362.
Effects of soybean isoflavone on growth performance, meat quality, and antioxidation in male broilers.Crossref | GoogleScholarGoogle Scholar | 17575182PubMed |

Jung B, Batal AB (2012) Effect of dietary nucleotide supplementation on performance and development of the gastrointestinal tract of broilers. British Poultry Science 53, 98–105.
Effect of dietary nucleotide supplementation on performance and development of the gastrointestinal tract of broilers.Crossref | GoogleScholarGoogle Scholar | 22404810PubMed |

Kamboh AA, Hang SQ, Bakhetgul M, Zhu W-Y (2013) Effects of genistein and hesperidin on biomarkers of heat stress in broilers under persistent summer stress. Poultry Science 92, 2411–2418.
Effects of genistein and hesperidin on biomarkers of heat stress in broilers under persistent summer stress.Crossref | GoogleScholarGoogle Scholar | 23960125PubMed |

Khajali F, Slominski BA (2012) Factors that affect the nutritive value of canola meal for poultry. Poultry Science 91, 2564–2575.
Factors that affect the nutritive value of canola meal for poultry.Crossref | GoogleScholarGoogle Scholar | 22991543PubMed |

Kheravii SK, Swick RA, Choct M, Wu S (2017) Dietary sugarcane bagasse and coarse particle size of corn are beneficial to performance and gizzard development in broilers fed normal and high sodium diets. Poultry Science 96, 4006–4016.
Dietary sugarcane bagasse and coarse particle size of corn are beneficial to performance and gizzard development in broilers fed normal and high sodium diets.Crossref | GoogleScholarGoogle Scholar | 29050432PubMed |

Khoddami A, Chrystal PV, Selle PH, Liu SY (2018) Dietary starch to lipid ratios influence growth performance, nutrient utilisation and carcass traits in broiler chickens offered diets with different energy densities. PLoS One 13, e0205272
Dietary starch to lipid ratios influence growth performance, nutrient utilisation and carcass traits in broiler chickens offered diets with different energy densities.Crossref | GoogleScholarGoogle Scholar | 30304011PubMed |

Kidd MT, Kerr BJ (1996) L-threonine for poultry: a review. Journal of Applied Poultry Research 5, 358–367.
L-threonine for poultry: a review.Crossref | GoogleScholarGoogle Scholar |

Knudsen KEB (2014) Fiber and nonstarch polysaccharide content and variation in common crops used in broiler diets. Poultry Science 93, 2380–2393.
Fiber and nonstarch polysaccharide content and variation in common crops used in broiler diets.Crossref | GoogleScholarGoogle Scholar |

Kriseldi R, Tillman PB, Jiang Z, Dozier WA (2017) Effects of glycine and glutamine supplementation to reduced crude protein diets on growth performance and carcass characteristics of male broilers during a 41-day production period. Journal of Applied Poultry Research 26, 558–572.

Kurzer MS, Xu X (1997) Dietary phytoestrogens. Annual Review of Nutrition 17, 353–381.
Dietary phytoestrogens.Crossref | GoogleScholarGoogle Scholar | 9240932PubMed |

Leach RM, Dam R, Zeigler TR, Norris LC (1959) The effect of protein and energy on the potassium requirement of the chick. The Journal of Nutrition 68, 89–100.
The effect of protein and energy on the potassium requirement of the chick.Crossref | GoogleScholarGoogle Scholar | 13655128PubMed |

Lilburn MS, Loeffler S (2015) Early intestinal growth and development in poultry. Poultry Science 94, 1569–1576.
Early intestinal growth and development in poultry.Crossref | GoogleScholarGoogle Scholar | 25910905PubMed |

Liu SY, Selle PH (2017) Starch and protein digestive dynamics in low-protein diets supplemented with crystalline amino acids. Animal Production Science 57, 2250–2256.
Starch and protein digestive dynamics in low-protein diets supplemented with crystalline amino acids.Crossref | GoogleScholarGoogle Scholar |

Mack S, Bercovici D, De Groote G, Leclercq B, Lippens M, Pack M, Schutte JB, Van Cauwenberghe S (1999) Ideal amino acid profile and dietary lysine specification for broiler chickens of 20 to 40 days of age. British Poultry Science 40, 257–265.
Ideal amino acid profile and dietary lysine specification for broiler chickens of 20 to 40 days of age.Crossref | GoogleScholarGoogle Scholar | 10465394PubMed |

Mahmoud AA, Natarajan SS, Bennett JO, Mawhinney TP, Wiebold WJ, Krishnan HB (2006) Effect of six decades of selective breeding on soybean protein composition and quality: a biochemical and molecular analysis. Journal of Agricultural and Food Chemistry 54, 3916–3922.
Effect of six decades of selective breeding on soybean protein composition and quality: a biochemical and molecular analysis.Crossref | GoogleScholarGoogle Scholar | 16719515PubMed |

Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L (2004) Polyphenols: food sources and bioavailability. The American Journal of Clinical Nutrition 79, 727–747.
Polyphenols: food sources and bioavailability.Crossref | GoogleScholarGoogle Scholar | 15113710PubMed |

Matrone G, Thomason EL, Bunn CR (1960) Requirement and utilization of iron by the baby pig. The Journal of Nutrition 72, 459–465.
Requirement and utilization of iron by the baby pig.Crossref | GoogleScholarGoogle Scholar | 13768190PubMed |

Meléndez-Hevia E, de Paz-Lugo P, Cornish-Bowden A, Cárdenas ML (2009) A weak link in metabolism: the metabolic capacity for glycine biosynthesis does not satisfy the need for collagen synthesis. Journal of Biosciences 34, 853–872.
A weak link in metabolism: the metabolic capacity for glycine biosynthesis does not satisfy the need for collagen synthesis.Crossref | GoogleScholarGoogle Scholar | 20093739PubMed |

Moran ET, Stilborn HL (1996) Effect of glutamic acid on broilers given submarginal crude protein with adequate essential amino acids using feeds high and low in potassium. Poultry Science 75, 120–129.
Effect of glutamic acid on broilers given submarginal crude protein with adequate essential amino acids using feeds high and low in potassium.Crossref | GoogleScholarGoogle Scholar | 8650101PubMed |

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 |

Murakami AE, Franco JRG, Martins EN, Oviedo Rondon EO, Sakamoto MI, Pereira MS (2003) Effect of electrolyte balance in low-protein diets on broiler performance and tibial dyschondroplasia incidence. Journal of Applied Poultry Research 12, 207–216.
Effect of electrolyte balance in low-protein diets on broiler performance and tibial dyschondroplasia incidence.Crossref | GoogleScholarGoogle Scholar |

Namroud NF, Shivazad M, Zaghari M (2008) Effects of fortifying low crude protein diet with crystalline amino acids on performance, blood ammonia level, and excreta characteristics of broiler chicks. Poultry Science 87, 2250–2258.
Effects of fortifying low crude protein diet with crystalline amino acids on performance, blood ammonia level, and excreta characteristics of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 18931175PubMed |

Namroud NF, Shivazad M, Zaghari M, Zare Shahneh A (2010) Impact of dietary crude protein and amino acids status on performance, thyroid function and fat deposition in chickens. South African Journal of Animal Science 40, 238–244.
Impact of dietary crude protein and amino acids status on performance, thyroid function and fat deposition in chickens.Crossref | GoogleScholarGoogle Scholar |

NRC (1994) ‘Nutrient requirements for poultry.’ (National Academies Press: Washington, DC)

Ospina-Rojas IC, Murakami AE, Eyng C, Nunes RV, Duarte CR, Vargas MD (2012) Commercially available amino acid supplementation of low-protein diets for broiler chickens with different ratios of digestible glycine + serine : lysine. Poultry Science 91, 3148–3155.
Commercially available amino acid supplementation of low-protein diets for broiler chickens with different ratios of digestible glycine + serine : lysine.Crossref | GoogleScholarGoogle Scholar | 23155025PubMed |

Ospina-Rojas IC, Murakami AE, Moreira I, Picoli KP, Rodrigueiro RJ, Furlan AC (2013) Dietary glycine + serine responses of male broilers given low-protein diets with different concentrations of threonine. British Poultry Science 54, 486–493.
Dietary glycine + serine responses of male broilers given low-protein diets with different concentrations of threonine.Crossref | GoogleScholarGoogle Scholar | 23742016PubMed |

Ospina-Rojas IC, Murakami AE, Duarte CR, Eyng C, Oliveira CA, Janeiro V (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.
Valine, isoleucine, arginine and glycine supplementation of low-protein diets for broiler chickens during the starter and grower phases.Crossref | GoogleScholarGoogle Scholar | 25269797PubMed |

Parsons CM, Edmonds MS, Baker DH (1984) Influence of dietary electrolyte balance, energy, and amino acid supplementation on the monensin response in chicks fed diets varying in protein content. Poultry Science 63, 2438–2443.
Influence of dietary electrolyte balance, energy, and amino acid supplementation on the monensin response in chicks fed diets varying in protein content.Crossref | GoogleScholarGoogle Scholar | 6531332PubMed |

Parsons CM, Zhang Y, Araba M (2000) Nutritional evaluation of soybean meals varying in oligosaccharide content. Poultry Science 79, 1127–1131.
Nutritional evaluation of soybean meals varying in oligosaccharide content.Crossref | GoogleScholarGoogle Scholar | 10947181PubMed |

Peng Y, Gubin J, Harper AE, Vavich MG, Kemmerer AR (1973) Food intake regulation: amino acid toxicity and changes in rat brain and plasma amino acids. The Journal of Nutrition 103, 608–617.
Food intake regulation: amino acid toxicity and changes in rat brain and plasma amino acids.Crossref | GoogleScholarGoogle Scholar | 4693672PubMed |

Pesti GM (2009) Impact of dietary amino acid and crude protein levels in broiler feeds on biological performance. Journal of Applied Poultry Research 18, 477–486.
Impact of dietary amino acid and crude protein levels in broiler feeds on biological performance.Crossref | GoogleScholarGoogle Scholar |

Platel K, Srinivasan K (2004) Digestive stimulant action of spices: a myth or reality? The Indian Journal of Medical Research 119, 167–179.

Powers W, Angel R (2008) A review of the capacity for nutritional strategies to address environmental challenges in poultry production. Poultry Science 87, 1929–1938.
A review of the capacity for nutritional strategies to address environmental challenges in poultry production.Crossref | GoogleScholarGoogle Scholar | 18809853PubMed |

Rasouli E, Jahanian R (2015) Improved performance and immunological responses as the result of dietary genistein supplementation of broiler chicks. Animal 9, 1473–1480.
Improved performance and immunological responses as the result of dietary genistein supplementation of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 25998982PubMed |

Reeds PJ, Burrin DG, Stoll B, Jahoor F, Wykes L, Henry J, Frazer ME (1997) Enteral glutamate is the preferential source for mucosal glutathione synthesis in fed piglets. American Journal of Physiology. Endocrinology and Metabolism 273, E408–E415.
Enteral glutamate is the preferential source for mucosal glutathione synthesis in fed piglets.Crossref | GoogleScholarGoogle Scholar |

Rehman ZU, Kamran J, El-Hack MEA, Alagawany M, Bhatti SA, Ahmad G, Saleem A, Ullah Z, Yameen RMK, Ding C (2018) Influence of low-protein and low-amino acid diets with different sources of protease on performance, carcasses and nitrogen retention of broiler chickens. Animal Production Science 58, 1625–1631.
Influence of low-protein and low-amino acid diets with different sources of protease on performance, carcasses and nitrogen retention of broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Schutte JB, Smink W, Pack M (1997) Requirement of young broiler chicks for glycine + serine. Archiv für Geflügelkunde 61, 43–47.

Selle PH, Chrystal PV, Moss AF, Yin D, Khoddami A, Naranjo VD, Liu SY (2019) The relevance of starch–protein digestive dynamics in crude protein-reduced broiler diets. In ‘Australian poultry science symposium. Vol. 30’, 17–20 February 2019, Sydney, NSW, Australia. pp. 37–40.

Shepherd EM, Fairchild BD (2010) Footpad dermatitis in poultry. Poultry Science 89, 2043–2051.
Footpad dermatitis in poultry.Crossref | GoogleScholarGoogle Scholar | 20852093PubMed |

Shoulders M, Raines R (2009) Collagen structure and stability. Annual Review of Biochemistry 78, 929–958.
Collagen structure and stability.Crossref | GoogleScholarGoogle Scholar | 19344236PubMed |

Si J, Burnham DJ, Waldroup PW (2004) Extent to which crude protein may be reduced in corn-soybean meal broiler diets through amino acid supplementation. International Journal of Poultry Science 3, 46–50.
Extent to which crude protein may be reduced in corn-soybean meal broiler diets through amino acid supplementation.Crossref | GoogleScholarGoogle Scholar |

Siegert W, Ahmadi H, Helmbrecht A, Rodehutscord M (2015a) A quantitative study of the interactive effects of glycine and serine with threonine and choline on growth performance in broilers. Poultry Science 94, 1557–1568.
A quantitative study of the interactive effects of glycine and serine with threonine and choline on growth performance in broilers.Crossref | GoogleScholarGoogle Scholar | 25908238PubMed |

Siegert W, Ahmadi H, Rodehutscord M (2015b) Meta-analysis of the influence of dietary glycine and serine, with consideration of methionine and cysteine, on growth and feed conversion of broilers. Poultry Science 94, 1853–1863.
Meta-analysis of the influence of dietary glycine and serine, with consideration of methionine and cysteine, on growth and feed conversion of broilers.Crossref | GoogleScholarGoogle Scholar | 26047669PubMed |

Smith RE, Scott HM (1965) Biological evaluation of fish meal proteins as sources of amino acids for the growing chick. Poultry Science 44, 394–400.
Biological evaluation of fish meal proteins as sources of amino acids for the growing chick.Crossref | GoogleScholarGoogle Scholar | 14340724PubMed |

Song Z, Deaciuc I, Zhou Z, Song M, Chen T, Hill D, McClain CJ (2007) Involvement of AMP-activated protein kinase in beneficial effects of betaine on high-sucrose diet-induced hepatic steatosis. American Journal of Physiology. Gastrointestinal and Liver Physiology 293, G894–G902.
Involvement of AMP-activated protein kinase in beneficial effects of betaine on high-sucrose diet-induced hepatic steatosis.Crossref | GoogleScholarGoogle Scholar | 17702954PubMed |

Sonne JC, Buchanan JM, Delluva AM (1948) Biological precursors of uric acid carbon. The Journal of Biological Chemistry 173, 81–98.

Stevens L (1996) Avian nutrition. In ‘Avian biochemistry and molecular biology’. pp. 9–28. (Cambridge University Press: Cambridge, UK)

Sugahara M, Ariyoshi S (1967) The nonessentiality of glycine and the essentiality of L-proline in the chick nutrition. Agricultural and Biological Chemistry 31, 106–110.
The nonessentiality of glycine and the essentiality of L-proline in the chick nutrition.Crossref | GoogleScholarGoogle Scholar |

USDA (2019) ‘Production, supply and distribution.’ (United States Department of Agriculture, Foreign Agricultural Service: Washington, DC) Available at https://apps.fas.usda.gov/psdonline/app/index.html#/app/advQuery [Verified 29 March 2019]

van Harn J, Dijkslag MA, van Krimpen MM (2019) Effect of low protein diets supplemented with free amino acids on growth performance, slaughter yield, litter quality, and footpad lesions of male broilers. Poultry Science.
Effect of low protein diets supplemented with free amino acids on growth performance, slaughter yield, litter quality, and footpad lesions of male broilers.Crossref | GoogleScholarGoogle Scholar | 30995304PubMed |

Velíšek J, Cejpek K (2006) Biosynthesis of food constituents amino acids 2. The alanine-valine-leucine, serine-cysteine-glycine, and aromatic and heterocyclic amino acids groups: a review. Czech Journal of Food Sciences 24, 45–58.
Biosynthesis of food constituents amino acids 2. The alanine-valine-leucine, serine-cysteine-glycine, and aromatic and heterocyclic amino acids groups: a review.Crossref | GoogleScholarGoogle Scholar |

Vieira SL, Angel CR (2012) Optimizing broiler performance using different amino acid density diets: what are the limits? Journal of Applied Poultry Research 21, 149–155.
Optimizing broiler performance using different amino acid density diets: what are the limits?Crossref | GoogleScholarGoogle Scholar |

Wade B, Keyburn AL (2015) The true cost of necrotic enteritis. World Poultry 31, 16–17.

Waguespack AM, Powell S, Bidner TD, Southern LL (2009) The glycine plus serine requirement of broiler chicks fed low-crude protein, corn–soybean meal diets. Journal of Applied Poultry Research 18, 761–765.
The glycine plus serine requirement of broiler chicks fed low-crude protein, corn–soybean meal diets.Crossref | GoogleScholarGoogle Scholar |

Waldroup P, Jiang Q, Fritts CA (2005) Effects of glycine and threonine supplementation on performance of broiler chicks fed diets low in crude protein. International Journal of Poultry Science 5, 250–257.

Wang W, Wu Z, Dai Z, Yang Y, Wang J, Wu G (2013) Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids 45, 463–477.
Glycine metabolism in animals and humans: implications for nutrition and health.Crossref | GoogleScholarGoogle Scholar | 23615880PubMed |

Watford M, Lund P, Krebs HA (1979) Isolation and metabolic characteristics of rat and chicken enterocytes. The Biochemical Journal 178, 589–596.
Isolation and metabolic characteristics of rat and chicken enterocytes.Crossref | GoogleScholarGoogle Scholar | 454367PubMed |

Wu G (2013) ‘Amino acids: biochemistry and nutrition.’ (CRC Press: Boca Raton, FL)

Wu S, Rodgers N, Choct M (2010) Optimized necrotic enteritis model producing clinical and subclinical infection of Clostridium perfringens in broiler chickens. Avian Diseases 54, 1058–1065.
Optimized necrotic enteritis model producing clinical and subclinical infection of Clostridium perfringens in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 20945788PubMed |

Yanaka M, Okumura J-I (1982) Effects of dietary excess tyrosine and level of feed intake on nitrogen and energy utilization in chicks. Poultry Science 61, 2440–2446.
Effects of dietary excess tyrosine and level of feed intake on nitrogen and energy utilization in chicks.Crossref | GoogleScholarGoogle Scholar | 7163121PubMed |

Yi Z, Kornegay ET, Denbow DM (1996) Effect of microbial phytase on nitrogen and amino acid digestibility and nitrogen retention of turkey poults fed corn–soybean meal diets. Poultry Science 75, 979–990.
Effect of microbial phytase on nitrogen and amino acid digestibility and nitrogen retention of turkey poults fed corn–soybean meal diets.Crossref | GoogleScholarGoogle Scholar | 8829230PubMed |