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Maintenance threonine requirement and efficiency of its use for accretion of whole-body threonine and protein in Atlantic salmon (Salmo salar L.) fry

Published online by Cambridge University Press:  08 March 2007

Rollin Xavier*
Affiliation:
Laboratoire de Pisciculture M. Huet, Université catholique de Louvain, Route de Blocry, 2, B-1348 Louvain-la-NeuveBelgium
Jean-Baptiste Wauters
Affiliation:
Laboratoire de Pisciculture M. Huet, Université catholique de Louvain, Route de Blocry, 2, B-1348 Louvain-la-NeuveBelgium
Noélie Bodin
Affiliation:
Laboratoire de Pisciculture M. Huet, Université catholique de Louvain, Route de Blocry, 2, B-1348 Louvain-la-NeuveBelgium
Yvan Larondelle
Affiliation:
Unité de Biochimie de la Nutrition, Université catholique de Louvain, Croix du Sud, 2/8, 1348 Louvain-la-Neuve, Belgium
Wilfried Ooghe
Affiliation:
Laboratorium voor Bromatologie, Universiteit Gent, Harelbekestraat 72, 9000 Gent, Belgium
Bernard Wathelet
Affiliation:
Unité de Chimie Biologique Industrielle, Faculté universitaire des sciences agronomiques, Passage des Déportés, 2, B-5030 Gembloux, Belgium
Tarik Abboudi
Affiliation:
Laboratoire de Pisciculture M. Huet, Université catholique de Louvain, Route de Blocry, 2, B-1348 Louvain-la-NeuveBelgium
*
*Corresponding author: fax +32 10 474991, email rollin@efor.ucl.ac.be
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Abstract

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Eighteen groups of seventy Atlantic salmon (Salmo salar L.) fry (initial mean body weight 0·8 (sd 0·01) g) were fed on semi-purified diets containing graded levels of l-threonine (Thr) in 15 litres aquaria at a temperature of 14·5±1°C. Doses of Thr represented 1, 31, 41, 51, 62, 72, 83 and 93% of its ideal level for optimumprotein deposition. Indispensable amino acids other than Thr were included in the same proportion (on a g/16g N basis) as in the Atlantic salmon fry whole-body carcass. Following 36d of feeding and a 36h fast, fry were killed for whole-body protein and amino acid analysis. Weight gain (r2 0·98), protein accretion (r2 0·97), and Thr accretion (r2 0·97) were linear (P<0·01) functions of Thr intake. Slope of the Thr accretion regression line showed that the efficiency of Thr utilisation above maintenance was 76%. At zero Thr intake, fry lost 5·4mg Thr/kg body weight0·75 per d. The Thr maintenance requirement was 7·2mg/kg body weight0·75 per d and the Thr requirement for growth was 66mg for 1g protein deposition. Increasing doses of Thr resulted in increased (P<0·05) concentrations of histidine and lysine, and decreased concentrations of isoleucine in whole-body protein. The maintenance need for Thr represented 13·4% of the total need for Thr. The data suggest that efficiency of Thr utilisation above maintenance is constant at all levels of Thr intake between 1 and 93% of the level required for optimum protein deposition.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Adeola, ODietary lysine and threonine utilization by young pigs: efficiency for carcass growth. Can J Anim Sci 1995 75 445452CrossRefGoogle Scholar
Akiyama, T, Arai, SMurai, TThreonine, histidine and lysine requirement of chum salmon fry. Bul Jap Soc Sci Fish. 1985 51 635639CrossRefGoogle Scholar
Allen, GL, Johnson, RJ, Stone, DAJ & Frances, J Estimating digestible protein and lysine requirements of silver perch. In Fish Meal Replacement in Aquaculture Feed for Silver Perch Allen, GLRowlands, SJAustralia Report 120–03 Fisheries Research and Development Corporation Deakin 1998 199214Google Scholar
Association of Official Analytical Chemists Official Methods of Analysis 16th ed Arlington, VAAOAC 1995Google Scholar
Baker, DHPartitioning of nutrient for growth and other metabolic functions: efficiency and priority considerations. Poultry Sci 1991 70 17971805CrossRefGoogle ScholarPubMed
Baker, DHIdeal amino acid patterns for broiler chicks. In Amino Acid in Animal Nutrition 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003 223235Google Scholar
Baker, DH, Becker, DE, Norton, HW, Jensen, AHHarmon, BGQuantitative evaluation of the threonine, isoleucine, valine and phenylalanine needs of adult swine for maintenance. J Nutr 1966 88 391396CrossRefGoogle ScholarPubMed
Baker, DH, Fernandez, R, Parsons, CM, Edwards, HM IIIEmmert, JLWebel, DMMaintenance requirement for valine and effi-ciency of its use above maintenance for accretion of whole-body valine and protein in young chicks. J Nutr 1996 126 18441851Google Scholar
Ballévre, O, Cadenhead, A, Calder, AG, Rees, WD, Lobley, GE, Fuller, MF & Garlick, PJ1990) Quantitative partition of threonine oxidation in pigs: effect of dietary threonine. Am J Physiol 1990 259 E483E491Google ScholarPubMed
Batterham, ESIleal digestibilities of amino acids in feedstuffs. In Amino Acids in Farm Animal Nutrition D'Mello, JPFWallingford, OxonCAB International 1994 113131Google Scholar
Batterham, ES, Anderson, LM, Baigent, DR & White, EUtilization of ideal digestible amino acids by growing pigs:effect of dietary lysine concentration on efficiency of lysine retention. Br J Nutr 1990 64 8194CrossRefGoogle Scholar
Bikker, P PhD Thesis, Protein and lipid accretion in body components of growing pigs. Wageningen Agricultural University 1994Google Scholar
Bird, MI & Nunn, PBMetabolic homeostasis of L-threonine in the normally-fed rat. Importance of liver threonine dehydrogenase activity. Biochem J 1983 214 687694CrossRefGoogle ScholarPubMed
Boren, RS & Gatlin, DM IIIDietary threonine requirement of juvenile red drum (Sciaenops ocellatus). J World Aquac Soc 1995 26 279283CrossRefGoogle Scholar
Borlongan, IGQuantitative arginine and threonine requirements of milkfish (Chanos chanos) juveniles. Aquaculture 1991 93 312322CrossRefGoogle Scholar
Burns, RA & Millner, JAThreonine, tryptophan and histidine requirements of immature beagle dogs. J Nutr 1982 112 447452CrossRefGoogle ScholarPubMed
Campbell, RG, Taverner, MR & Curic, DMEffect of feeding level and dietary protein content on the growth, body composition and rate of protein deposition in pigs growing from 45 to 90 kg. Anim Prod 1984 38 233240Google Scholar
Campbell, RG, Taverner, MR & Curic, DMThe influence of feeding level on the protein requirement of pigs between 20 and 45 kg live weight Anim Prod 1985 40 489496Google Scholar
Chung, TK & Baker, DHEfficiency of dietary methionine utilization by young pigs. J Nutr 1992 122 18621869CrossRefGoogle ScholarPubMed
Cieslak, DG & Benevenga, NJThe effect of amino acid excess on utilization by the rat of the limiting amino acids lysine and threonine at equalized food intakes. J Nutr 1984 114 18781883CrossRefGoogle ScholarPubMed
Conceição, LE, Rønnestad, I & Tonheim, SKMetabolic budgets for lysine and glutamate in unfed herring (Clupea harengus)larvae. Aquaculture 2002 201 161175Google Scholar
Cowey, CBAmino acid requirements of fish: a critical appraisal of present values. Aquaculture 1994 124 111CrossRefGoogle Scholar
Cowey, CBProtein and amino acid requirements: a critique of methods. J Appl Ichthyol 1995 11 199204CrossRefGoogle Scholar
Cowey, CB & Luquet, PPhysiological basis of protein requirements of fishes. Critical analysis of allowances.In Protein Metabolism and Nutrition Arnal, M, Pion, R and Bonin, DParisINRA 1 1983 364384Google Scholar
Dabrowski, K & Guderley, HIntermediary metabolism.In Fish Nutrition, 3rd ed. Halver, JE & Hardy,, RWSan Diego, CAAcademic Press 2002 310367Google Scholar
Dabrowski, K, Lee, KJ & Rinchard, JThe smallest vertebrate, telesot fish, can utilize synthetic dipeptide-based diets. J Nutr 2003 133 42254229CrossRefGoogle Scholar
Denton, JD & Yousef, MKBody composition and organ weights of rainbow trout, Salmo gairdneri. J Fish Biol 1976 8 489499CrossRefGoogle Scholar
D'Mello, JPFA comparison of two empirical methods of determining amino acid requirements. World Poult Sci J 1982 38 114119CrossRefGoogle Scholar
D'Mello, JPFAmino acid requirements of the turkey poult. In Proceedings of the 4th European Symposium on Poultry Nutrition Larbier, MTours, FranceWorld's Poultry Science Association 1983 6673Google Scholar
D'Mello, JPFResponses of growing poultry to amino acids.In Amino Acids in Farm Animal Nutrition, D'Mello, JPFWallingford, UKCAB International 1994a 205243Google Scholar
D'Mello, JPFAmino acid imbalances, antagonisms and toxicities. In Amino Acids in Farm Animal Nutrition, D'Mello,, JPFWallingford, UKCAB International 1994b 6397Google Scholar
D'Mello, JPFResponses of growing poultry to amino acids.In Amino Acids in Animal Nutrition, 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003a 223263Google Scholar
D'Mello, JPFAdverse effects of amino acids. In Amino Acids in Animal Nutrition, 2nd ed D'Mello, JPFWallingford, UKCAB International 2003b 125142Google Scholar
D'Mello, JPFAmino acids as multifunctional molecules. In Amino Acids in Animal Nutrition, 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003c 114Google Scholar
Draper, NR & Smith, HApplied Regression Analysis 2nd ed. New YorkJohn Wiley and Sons 1981Google Scholar
Dunkin, AC, Black, JL & James, KJNitrogen balance in relation to energy intake in entire male pigs weighing 75 kg. Br J Nutr 1986 55 201207CrossRefGoogle ScholarPubMed
Durbin, T & Watson, GSTesting for serial correlation in least square regression II. Biometrica 1951 38 159178CrossRefGoogle ScholarPubMed
Edwards, HM III, Baker, DH, Fernandez, SR & Parsons, CMMaintenance threonine requirement and efficiency of its use for accretion of whole-body threonine and protein in young chicks. Br J Nutr 1997 78 111119CrossRefGoogle ScholarPubMed
Edwards, HM IIIFernandez, SR &Baker, DHMaintenance lysine requirement and efficiency of using for accretion of whole-body lysine and protein in young chicks. Poultry Sci 1999 78 14121417CrossRefGoogle ScholarPubMed
Elliott, JMTolerance and resistance to thermal stress in juvenile Atlantic salmon, Salmo salar. Freshwat Biol 1991 25 6170CrossRefGoogle Scholar
Encarnação, P, de Lange, C, Rodehutscord, M, Hoehler, D, Bureau, W & Bureau, DPDiet digestible energy content affects lysine utilization, but not dietary lysine requirements of rainbow trout (Oncorhynchus mykiss) for maximum growth. Aquaculture 2004 235 569586CrossRefGoogle Scholar
Espe, MStudies on the utilization of pre-digested fish proteins in Atlantic salmon (Salmo salar). PhD Thesis Institute of Nutrition, Directorate of Fisheries and University of Bergen 1993Google Scholar
Espe, M, Haaland, H & Njaa, LRSubstitution of fish silage protein and a free amino acid mixture for fish meal protein in a chicken diet. J Sci Food Agric 1992 58 315320CrossRefGoogle Scholar
Fisher, C, Morris, TR & Jennings, RCA model for the description and prediction of the response of laying hens to amino acid intake. Br Poult Sci 1973 14 469484CrossRefGoogle Scholar
Fournier, V, Gouillou-Coustans, MF, Métailler, R, Vachot, CGuedes, MJ, Tulli, F, Oliva-Teles, A, Tibaldi, E & Kaushik, SJProtein and arginine requirements for maintenance and nitrogen gain in four teleosts. Br J Nutr 2002 87 459469CrossRefGoogle ScholarPubMed
Fuller, MFAmino acid requirements for maintenance, body protein accretion and reproduction.In Amino Acids in Farm Animal Nutrition D'Mello, JPFWallingford, OxonCAB International 1994 155184Google Scholar
Fuller, MF & Garthwaite, PThe form of response of body protein accretion to dietary amino acid supply. J Nutr 1993 123 957963CrossRefGoogle ScholarPubMed
Fuller, MF, McWilliam, R, Wang, TC & Giles, LRThe optimum dietary amino acid pattern for growing pigs. 2. Requirements for maintenance and for tissue protein accretion. Br J Nutr 1989 62 255267CrossRefGoogle ScholarPubMed
Fyhn, HJFirst feeding of marine fish larvae: are free amino acids the source of energy? Aquaculture 1989 80 111120CrossRefGoogle Scholar
Gahl, M, Finke, MD, Crenshaw, TD & Benevenga, NJUse of a four parameter logistic equation to evaluate the response of growing rats to ten levels of each indispensable amino acid. J Nutr 1991 121 17201729CrossRefGoogle ScholarPubMed
Gahl, M, Finke, MD, Crenshaw, TD & Benevenga, NJEfficiency of lysine or threonine retention in growing rats fed diets limiting in either lysine or threonine. J Nutr 1996 126 30903099CrossRefGoogle ScholarPubMed
Gous, RM An improved method for measuring the response of broiler chickens to increasing dietary concentrations of an amino acid. In Proceedings of the 6th European Poultry Conference HamburgWorld's Poultry Science Association 1980 III 3239Google Scholar
Gustafson, JM, Dodds, SJ, Rudquist, J, Kelley, J, Ayers, S & Mercer, LPFood intake and weight gain responses to graded amino acid deficiencies in rats. Nutr Rep Int 1984 30 10191025Google Scholar
Hara, TJ, Macdonald, S, Evans, RE, Marui, T & Arai, SMorpholine, bile acids and skin mucus as possible chemical cues in salmonid homing: electrophysiological re-evaluation.In Mechanisms of Migration in Fishes (McCleave, JD, Arnold, GP, Dodson, JJ and Neill, WHNew YorkPlenum 1984 363378Google Scholar
Hauler, RC & Carter, CGReevaluation of the quantitative dietary lysine requirements of fish. Rev Fish Sci 2001a 9 133163CrossRefGoogle Scholar
Hauler, RC & Carter, CGLysine deposition responds linearly to marginal lysine intake in Atlantic salmon (Salmo salar L.) parr. Aquac Res 2001b 32 suppl. 1. 147156CrossRefGoogle Scholar
Heger, J & Frydrych, ZEfficiency of utilisation of essential amino acids in growing rats at different levels on intake. Br JNutr 1985 54 499508Google ScholarPubMed
Hendricks, WHCanine and feline amino acid requirements forndifferent physiological functions.In Amino acids in Animal Nutrition, 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003 411426Google Scholar
Hendricks, WH, Moughan, PJ & Tarttelin, MFGut endogenous nitrogen and amino acid excretions in adult domestic cats using a protein-free diet or an enzymatically hydrolyzed casein-based diet. J Nutr 1996 126 955962CrossRefGoogle Scholar
Houlihan, DF, Carter, CG & McCarty, IDProtein synthesis in fish. In Biochemistry and Molecular Biology of Fishes. Metabolic Biochemistry Hochachka, PW and Mommsen, TPAmsterdamElsevier 1995 191220Google Scholar
Keembiyehetty, CN & Gatlin, DM IIIDietary threonine requirement of juvenile hybrid striped bass (Morone chrysops ♀ x M. saxatilis ♂). Aquaculture Nutrition 1997 3 217221CrossRefGoogle Scholar
Kidd, MT, Kerr, BJ & Anthony, NBDietary interaction between lysine and threonine in broilers. Poultry Sci 1997 76 608614CrossRefGoogle ScholarPubMed
Mambrini, MBesoins en acides aminés des poissons: détermination des besoins en acides amines soufrés pour l'entretien et l'accrétion protéique (Amino acid requirements in fish: determination of sulfur amino acids requirements for maintenance and for protein accretion).In Journées Nutrition des Poissons INRAIFREMER 21–22.02.96 Saint-Pée sur NivelleINRA, Unité mixte INRA-IFREMER de Nutrition des Poissons 1996 1720Google Scholar
Mambrini, M & Kaushik, SJPartial replacement of dietary protein nitrogen with dispensable amino acids in diets of Nile tilapia Oreochromis niloticus. Comp Biochem Physiol 109A 1994 469477CrossRefGoogle Scholar
Mambrini, MKaushik, SJEffect of temperature on sulfur amino acid requirements for maintenance and growth of juvenile rainbow trout.In Protein Metabolism and Nutrition Nunes, AF, Portugal, AV, Costa, JP and Ribeiro, JROeiras, PortugaINIA 1995 117122Google Scholar
Mambrini, M & Seudre, LSulfur amino acid requirements for maintenance and growth of juvenile rainbow trout. Reprod Nutr Dév 1995 35 603604CrossRefGoogle Scholar
Mercer, LPThe quantitative nutrient-response relationship. J Nutr 1982 112 560566CrossRefGoogle ScholarPubMed
Morris, TR, Al-Azzawi, K, Gous, RM & Jackson, GLEffects of protein concentration on responses to dietary lysine by chicks. Br Poult Sci 1987 33 185195CrossRefGoogle Scholar
National Research Council Nutrients Requirements of Fish. Washington, DCNational Academy Press 1993Google Scholar
Nose, Summary report on the requirement of essential amino acids for carp. In Proceedings of the World Symposium on Finfish Nutrition and Finfish Technology Halver, JE, Tiews, JEBerlinHeenemann 1979 145156Google Scholar
Ooghe, WOn the influence of hydrogen peroxide on the amino acid composition of foodstuffs. In Proceedings of the Second European Conference on Food Chemistry, Euro Food Chem II RomeThe Federation of European Chemical Societies, Working Party on Food Chemistry and the Italian Society for Food Science 1983 315321Google Scholar
Pack, M, Hoehler, D & Lemme, AEconomic assessment of amino acid responses in growing poultry. In Amino Acids in Farm Animal Nutrition, 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003 459483Google Scholar
Perry, SF & Laurent, PEnvironmental effects of fish gill structure and function. In Fish Ecophysiology Rankin, JC and Jensen, FBLondonChapman & Hall 1993 231264Google Scholar
Ravi, J & Devaraj, KVQuantitative essential amino acid requirements for growth of catla, Catla catla (Hamilton). Aquaculture 1991 96 281291CrossRefGoogle Scholar
Rodehutscord, M, Becker, A, Pack, M & Pfeffer, EResponse of rainbow trout (Oncorhynchus mykiss) to supplements of individual essential amino acids in a semipurified diet, including an estimate of the maintenance requirement for essential amino acids. J Nutr 1997 127 11661175CrossRefGoogle Scholar
Rodehutscord, M, Borchert, F, Gregus, ZPack, M & Pfeffer, EAvailability and utilization of free lysine in rainbow trout (Oncorhynchus mykiss). I. Effect of dietary crude protein level. Aquaculture 2002 187 163176CrossRefGoogle Scholar
Rodehutscord, M, Jacobs, S, Pack, M & Pfeffer, EResponse of rainbow trout (Oncorhynchus mykiss) growing from 50 to 150 g to supplements of DL-methionine in a semipurified diet containing low or high levels of cystine. J Nutr 1995b 125 970975Google ScholarPubMed
Rodehutscord, M & Pack, MEstimates of essential amino acid requirements from dose-response studies with rainbow trout and broiler chicken: effect of mathematical model. Arch Anim Nutr 1999 52 223244Google ScholarPubMed
Rollin, XEtude critique des besoins en acides aminés indispensables de l'alevin de saumon atlantique (Salmo salar L.) (Critical study of the indispensable amino acids requirements in Atlantic salmon (Salmo salar L.) fry).PhD Thesis, Université catholiquede Louvain 1999Google Scholar
Rollin, X, Mambrini, M, Abboudi, T, Larondelle, Y & Kaushik, SThe optimum dietary indispensable amino acid pattern for growing Atlantic salmon (Salmo salar) fry. Br J Nutr 2003a 90 865876CrossRefGoogle Scholar
Rollin, X, Peng, J, Pham, D, Ackman, RG & Larondelle, YThe effects of dietary lipid and strain difference on polyunsaturated fatty acid composition and conversion in anadromous and landlocked salmon (Salmo salar L.) parr. Comp Biochem Physiol 2003b 134B 349366CrossRefGoogle Scholar
Rønnestad, I, Conceição, LEAragão, C & Dinis, MTFree amino acids are absorbed faster and assimilated more effi-ciently than protein in postlarval Senegal sole. J Nutr 2000 130 28092812CrossRefGoogle Scholar
Rønnestad, I, Conceição, LE, Aragão, C & Dinis, MTAssimilation and catabolism of dispensable and indispensable free amino acids in post-larval Senegal sole (Solea senegalensis Comp Biochem Physiol 2001a 130C 461466Google Scholar
Rønnestad, I, Rojas-García, CR, Tonheim, SKConceição, LE (2001b) In vivo studies of digestion and nutrient assimilation in marine fish larvae. Aquaculture 201 161175CrossRefGoogle Scholar
Rust, MBQuantitative aspects of nutrient assimilation in six species of fish larvae. PhD Thesis SeattleUniversity of Washington, School of Fisheries 1995Google Scholar
Rust, MB, Hardy, RW & Stickney, RRA new method for forcefeeding larval fish. Aquaculture 1993 116 341352CrossRefGoogle Scholar
Said, AKHegsted, DMResponse of adult rats to low dietary levels of essential amino acids. J Nutr 1970 100 13631375CrossRefGoogle ScholarPubMed
Saldana, CI, Knabe, DA, Owen, KQ, Burgoon, KG & Gregg, EJ (1994) Digestible threonine requirements of starter and finisher pigs. J Anim Sci 72 144150CrossRefGoogle ScholarPubMed
Shearer, KThe use of factorial modeling to determine the dietary requirements for essential elements in fishes. Aquaculture 1995 133 5772CrossRefGoogle Scholar
Sokal, RR & Rohlf, FJBiometry: the Principles and Practice of Statistics in Biological Research. 3rd ed. New York, NYFreeman and Company 1995Google Scholar
Tacon, AGJ & Cowey, CBProtein and amino acid requirements.In Fish Energetics: New Perspectives Tytler, P and Calow, PBaltimore, MD:The Johns Hopkins University Press 1985 155183Google Scholar
Tibaldi, E & Tulli, FDietary threonine requirement of juvenile European sea bass (Dicentrarchus labrax. Aquaculture 1999 175 155166CrossRefGoogle Scholar
Titchenal, CA, Rogers, QR, Indrieri, RJ & Morris, JGThreonine imbalance, deficiency and neurologic dysfunction in the kitten. J Nutr 1980 110 24442459CrossRefGoogle ScholarPubMed
Weatherley, AH & Gill, HSRelative growth of tissues at different somatic growth rates in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 1983 22 4360CrossRefGoogle Scholar
Webel, DM, Fernandez, SR, Parson, CM & Baker, DHThreonine requirement of broiler chickens during the period 3 to 6 and 6 to 8 weeks posthatching. Poultry Sci 1996 75 12531257CrossRefGoogle ScholarPubMed
Wilson, RPAmino acids and proteins. In Fish Nutrition, 3rd ed., Halver, JESan Diego, CAAcademic Press 2002 143179Google Scholar
Wilson, RPAmino acid requirements of finfish and crustaceans. In Amino Acids in Animal Nutrition, 2nd ed., D'Mello, JPFWallingford, UKCAB International 2003 427447Google Scholar
Wilson, RP, Allen, OW, Robinson, EH & Poe, WETryptophan and threonine requirements of fingerling channel catfish J Nutr 1978 108 15951599CrossRefGoogle ScholarPubMed
Wilson, RP, Poe, WE & Robinson, EHApparent and true availability of amino acids from common feed ingredients for channel catfish. J Nutr 1981 111 923929CrossRefGoogle ScholarPubMed
Yokogoshi, H & Yoshida, ASome factors affecting the nitrogen sparing action of methionine and threonine in rats fed a proteinbfree diet. J Nutr 1976 106 4857CrossRefGoogle ScholarPubMed
Yoshida, A & Moritoki, KNitrogen sparing action of methionine and threonine in rats receiving a protein free diet. Nutr Rep Int 1974 9 159168Google Scholar