Effect of dietary arginine to lysine ratios on productive performance,meat quality,plasma and muscle metabolomics profile in fast-growing broiler chickens
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摘要
Background: Due to the important functions of arginine in poultry,it should be questioned whether the currently adopted dietary Arg:Lys ratios are sufficient to meet the modern broiler requirement in arginine.The present study aimed,therefore,to evaluate the effects of the dietary supplementation of L-arginine in a commercial broiler diet on productive performance,breast meat quality attributes,incidence and severity of breast muscle myopathies and foot pad dermatitis(FPD),and plasma and muscle metabolomics profile in fast-growing broilers.Results: A total of 1,170 1-day-old Ross 308 male chicks was divided into two experimental groups of 9 replicates each fed either a commercial basal diet(CON,digestible Arg:Lys ratio of 1.05,1.05,1.06 and 1.07 in each feeding phase,respectively) or the same basal diet supplemented on-top with crystalline L-arginine(ARG,digestible Arg:Lys ratio of 1.15,1.15,1.16 and 1.17,respectively).Productive parameters were determined at the end of each feeding phase(12,22,33,43 d).At slaughter(43 d),incidence and severity of FPD and breast myopathies were assessed,while plasma and breast muscle samples were collected and analyzed by proton nuclear magnetic resonancespectroscopy.The dietary supplementation of arginine significantly reduced cumulative feed conversion ratio compared to the control diet at 12 d(1.352 vs.1.401,P < 0.05),22 d(1.398 vs.1.420; P < 0.01) and 33 d(1.494 vs.1.524; P < 0.05),and also tended to improve it in the overall period of trial(1.646 vs.1.675; P = 0.09).Body weight was significantly increased in ARG compared to CON group at 33 d(1,884 vs.1,829 g; P < 0.05).No significant effect was observed on meat quality attributes,breast myopathies and FPD occurrence.ARG birds showed significantly higher plasma concentration of arginine and leucine,and lower of acetoacetate,glutamate,adenosine and proline.Arginine and acetate concentrations were higher,whereas acetone and inosine levels were lower in the breast of ARG birds(P < 0.05).Conclusions: Taken together,these data showed that increased digestible Arg:Lys ratio had positive effects on feed efficiency in broiler chickens probably via modulation of metabolites that play key roles in energy and protein metabolism.
Background: Due to the important functions of arginine in poultry,it should be questioned whether the currently adopted dietary Arg:Lys ratios are sufficient to meet the modern broiler requirement in arginine.The present study aimed,therefore,to evaluate the effects of the dietary supplementation of L-arginine in a commercial broiler diet on productive performance,breast meat quality attributes,incidence and severity of breast muscle myopathies and foot pad dermatitis(FPD),and plasma and muscle metabolomics profile in fast-growing broilers.Results: A total of 1,170 1-day-old Ross 308 male chicks was divided into two experimental groups of 9 replicates each fed either a commercial basal diet(CON,digestible Arg:Lys ratio of 1.05,1.05,1.06 and 1.07 in each feeding phase,respectively) or the same basal diet supplemented on-top with crystalline L-arginine(ARG,digestible Arg:Lys ratio of 1.15,1.15,1.16 and 1.17,respectively).Productive parameters were determined at the end of each feeding phase(12,22,33,43 d).At slaughter(43 d),incidence and severity of FPD and breast myopathies were assessed,while plasma and breast muscle samples were collected and analyzed by proton nuclear magnetic resonancespectroscopy.The dietary supplementation of arginine significantly reduced cumulative feed conversion ratio compared to the control diet at 12 d(1.352 vs.1.401,P < 0.05),22 d(1.398 vs.1.420; P < 0.01) and 33 d(1.494 vs.1.524; P < 0.05),and also tended to improve it in the overall period of trial(1.646 vs.1.675; P = 0.09).Body weight was significantly increased in ARG compared to CON group at 33 d(1,884 vs.1,829 g; P < 0.05).No significant effect was observed on meat quality attributes,breast myopathies and FPD occurrence.ARG birds showed significantly higher plasma concentration of arginine and leucine,and lower of acetoacetate,glutamate,adenosine and proline.Arginine and acetate concentrations were higher,whereas acetone and inosine levels were lower in the breast of ARG birds(P < 0.05).Conclusions: Taken together,these data showed that increased digestible Arg:Lys ratio had positive effects on feed efficiency in broiler chickens probably via modulation of metabolites that play key roles in energy and protein metabolism.
Background: Due to the important functions of arginine in poultry,it should be questioned whether the currently adopted dietary Arg:Lys ratios are sufficient to meet the modern broiler requirement in arginine.The present study aimed,therefore,to evaluate the effects of the dietary supplementation of L-arginine in a commercial broiler diet on productive performance,breast meat quality attributes,incidence and severity of breast muscle myopathies and foot pad dermatitis(FPD),and plasma and muscle metabolomics profile in fast-growing broilers.Results: A total of 1,170 1-day-old Ross 308 male chicks was divided into two experimental groups of 9 replicates each fed either a commercial basal diet(CON,digestible Arg:Lys ratio of 1.05,1.05,1.06 and 1.07 in each feeding phase,respectively) or the same basal diet supplemented on-top with crystalline L-arginine(ARG,digestible Arg:Lys ratio of 1.15,1.15,1.16 and 1.17,respectively).Productive parameters were determined at the end of each feeding phase(12,22,33,43 d).At slaughter(43 d),incidence and severity of FPD and breast myopathies were assessed,while plasma and breast muscle samples were collected and analyzed by proton nuclear magnetic resonancespectroscopy.The dietary supplementation of arginine significantly reduced cumulative feed conversion ratio compared to the control diet at 12 d(1.352 vs.1.401,P < 0.05),22 d(1.398 vs.1.420; P < 0.01) and 33 d(1.494 vs.1.524; P < 0.05),and also tended to improve it in the overall period of trial(1.646 vs.1.675; P = 0.09).Body weight was significantly increased in ARG compared to CON group at 33 d(1,884 vs.1,829 g; P < 0.05).No significant effect was observed on meat quality attributes,breast myopathies and FPD occurrence.ARG birds showed significantly higher plasma concentration of arginine and leucine,and lower of acetoacetate,glutamate,adenosine and proline.Arginine and acetate concentrations were higher,whereas acetone and inosine levels were lower in the breast of ARG birds(P < 0.05).Conclusions: Taken together,these data showed that increased digestible Arg:Lys ratio had positive effects on feed efficiency in broiler chickens probably via modulation of metabolites that play key roles in energy and protein metabolism.
引文
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3.National Research Council.Nutrient Requirements of Poultry.9th Revised Edition.National Academies Press;Washington DC;1994.
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6.Cobb-Vantress.Cobb 500 broiler performance and nutrition supplement.2018.https://cobbstorage.blob.core.windows.net/guides/5a171aa0-6994-11e8-9f14-bdc382f8d47e.Accessed 7 June 2018.
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8.Fernandes JIM,Murakami AE.Arginine metabolism in uricotelic species.Acta Sci Anim Sci.2010;32:357-66.
9.Khajali F,Wideman RF.Dietary arginine:metabolic,environmental,immunological and physiological interrelationships.Worlds Poult Sci J.2010;66:751-66.
10.Fouad AM,El-Senousey HK,Yang XJ,Yao JH.Role of dietary L-arginine in poultry production.Int J Poult Sci.2012;11:718-29.
11.Tamir H,Ratner S.Enzymes of arginine metabolism in chicks.Arch Biochem Biophys.1963;102:249-58.
12.Balnave D,Brake J.Re-evaluation of the classical dietary arginine:lysine interaction for modern poultry diets:a review.Worlds Poult Sci J.2002;58:275-89.
13.Baker DH.Ideal amino acid profiles for swine and poultry and their applications in feed formulation.BioKyowa Tech Rev.1997;9:1-24.
14.Wu G.Dietary requirements of synthesizable amino acids by animals:a paradigm shift in protein nutrition.J Anim Sci Biotechnol.2014;5:34.
15.Mutryn MF,Brannick EM,Fu W,Lee WR,Abasht B.Characterization of a novel chicken muscle disorder through differential gene expression and pathway analysis using RNA-sequencing.BMC Genomics.2015;16(399).https://doi.org/10.1186/s12864-015-1623-0.
16.Boerboom G,van Kempen T,Navarro-Villa A,Pérez-Bonilla A.Unraveling the cause of white striping in broilers using metabolomics.Poult Sci.2018.https://doi.org/10.3382/ps/pey266.
17.Bodle BC,Alvarado C,Shirley RB,Mercier Y,Lee JT.Evaluation of different dietary alterations in their ability to mitigate the incidence and severity of woody breast and white striping in commercial male broilers.Poult Sci.2018.https://doi.org/10.3382/ps/pey166.
18.Baeza E,Jégou M,Gondret F,Lalande-Martin J,Tea I,Le Bihan-Duval E,et al.Pertinent plasma indicators of the ability of chickens to synthesize and store lipids.J Anim Sci.2015;93:107-16.
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25.Kuttappan VA,Lee Y,Erf GF,Meullenet JF,Owens CM.Consumer acceptance of visual appearance of broiler breast meat with varying degrees of white striping.Poult Sci.2012;91:1240-7.
26.Sihvo HK,Immonen K,Puolanne E.Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers.Vet Pathol.2014;51:619-23.
27.Sirri F,Maiorano G,Tavaniello S,Chen J,Petracci M,Meluzzi A.Effect of different levels of dietary zinc,manganese,and copper from organic or inorganic sources on performance,bacterial chondronecrosis,intramuscular collagen characteristics,and occurrence of meat quality defects of broiler chickens.Poult Sci.2016;95:1813-24.
28.Jeacocke RE.Continuous measurement of the pH of beef muscle in intact beef carcasses.J Food Tech.1977;12:375-86.
29.Sirri F,Petracci M,Zampiga M,Meluzzi A.Effect of EU electrical stunning conditions on breast meat quality of broiler chickens.Poult Sci.2017;96:3000-4
30.Commission Internationale de l’Eclairage.Recommendations on uniform color spaces,color differences,equations.Psychometric color terms.1978;15:Suppl 2.CEI,Paris,France.
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32.Ventrella D,Laghi L,Barone F,Elmi A,Romagnoli N,Bacci ML.Age-related 1H NMR characterization of cerebrospinal fluid in newborn and young healthy piglets.PLoS One.2016;11:e0157623.
33.Barbara G,Scaioli E,Barbaro MR,Biagi E,Laghi L,Cremon C,et al.Gut microbiota,metabolome and immune signatures in patients with uncomplicated diverticular disease.Gut.2016.https://doi.org/10.1136/gutjnl-2016-312377.
34.Kneen MA,Annegarn HJ.Algorithm for fitting xRF,SEM and PIxE x-ray spectra backgrounds.Nucl Instrum Methods Phys Res B.1996;109:209-13.
35.Liland KH,Alm?y T,Mevik BH.Optimal choice of baseline correction for multivariate calibration of spectra.Appl Spectrosc.2010;64:1007-16.
36.Dieterle F,Ross A,Schlotterbeck G,Senn H.Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures.Application in 1H NMR metabonomics.Anal Chem.2006;78:4281-90.
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40.Hubert M,Rousseeuw PJ,Vanden Branden K.ROBPCA:a new approach to robust principal component analysis.Technometrics.2005;47:64-79.
41.Corzo A,Kidd MT.Arginine needs of the chick and growing broiler.Int JPoult Sci.2003;2:379-82.
42.Jahanian R,Khalifeh-Gholi M.Marginal deficiencies of dietary arginine and methionine could suppress growth performance and immunological responses in broiler chickens.J Anim Physiol Anim Nutr.2018;102:e11-20.
43.Ebrahimi M,Zare Shahneh A,Shivazad M,Ansari Pirsaraei Z,Tebianian M,Ruiz-Feria CA,et al.The effect of feeding excess arginine on lipogenic gene expression and growth performance in broilers.Br Poult Sci.2014;55:81-8.
44.Laika M,Jahanian R.Increase in dietary arginine level could ameliorate detrimental impacts of coccidial infection in broiler chickens.Livest Sci.2017;195:38-44.
45.Xu YQ,Guo YW,Shi BL,Yan SM,Guo XY.Dietary arginine supplementation enhances the growth performance and immune status of broiler chickens.Livest Sci.2018;209:8-13.
46.Fouad AM,El-Senousey HK,Yang XJ,Yao JH.Dietary L-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens.Animal.2013;7:1239-45.
47.Corzo A,Moran ET Jr,Hoehler D.Arginine need of heavy broiler males:applying the ideal protein concept.Poult Sci.2003;82:402-7.
48.Kidd MT,Peebles ED,Whitmarsh SK,Yeatman JB,Wideman RF Jr.Growth and immunity of broiler chicks as affected by dietary arginine.Poult Sci.2001;80:1535-42.
49.Christensen K,Owens C,Kidd MT.The effect of added l-arginine on the severity of woody breast and white striping in male broilers.Poultry Science Association Annual Meeting Abstracts.Poult Sci.2015;94(E-Suppl 1):147.
50.Jiao P,Guo Y,Yang X,Long F.Effects of dietary arginine and methionine levels on broiler carcass traits and meat quality.J Anim Vet Adv.2010;9:1546-51.
51.Rueda E,Michelangeli C,Gonzalez-Mujica F.L-canavanine inhibits L-arginine uptake by broiler chicken intestinal brush border membrane vesicles.Br Poult Sci.2003;44:620-5.
52.Brake J,Balnave D.Essentiality of arginine in broilers during hot weather.St Louis:Proceedings of 12th Annual Biokyowa Amino Acid Council Meeting;1995
53.Escobar J,Frank JW,Suryawan A,Nguyen HV,Kimball SR,Jefferson LS,et al.Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation.Am JPhysiol Endocrinol Metab.2005;288:E914-21.
54.Wu LY,Fang YJ,Guo XY.Dietary L-arginine supplementation beneficially regulates body fat deposition of meat-type ducks.Br Poult Sci.2011;52:221-6.
55.Newsholme P,Lima MMR,Procopio J,Pithon-Curi TC,Bazotte RB,Curi R.Glutamine and glutamate as vital metabolites.Braz J Med Biol Res.2003;36:153-63.
56.Wu G,Bazer FW,Burghardt RC,Johnson GA,Kim SW,Knabe DA,et al.Proline and hydroxyproline metabolism:implications for animal and human nutrition.Amino Acids.2011;40:1053-63.
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2.Zuidhof MJ,Schneider BL,Carney VL,Korver DR,Robinson FE.Growth,efficiency,and yield of commercial broilers from 1957,1978,and 2005.Poult Sci.2014;93:2970-82.
3.National Research Council.Nutrient Requirements of Poultry.9th Revised Edition.National Academies Press;Washington DC;1994.
4.Dozier WA III,Kidd MT,Corzo A.Dietary amino acid responses of broiler chickens.J Appl Poult Res.2008;17:157-67.
5.Aviagen.Ross 308 broiler performance objectives.2014.http://eu.aviagen.com/assets/Tech_Center/Ross_Broiler/Ross-308-Broiler-Nutrition-Specs-plant-2014-EN.pdf.Accessed 7 June 2018.
6.Cobb-Vantress.Cobb 500 broiler performance and nutrition supplement.2018.https://cobbstorage.blob.core.windows.net/guides/5a171aa0-6994-11e8-9f14-bdc382f8d47e.Accessed 7 June 2018.
7.Kidd MT,Kerr BJ,Anthony NB.Dietary interactions between lysine and threonine in broilers.Poult Sci.1997;76:608-14.
8.Fernandes JIM,Murakami AE.Arginine metabolism in uricotelic species.Acta Sci Anim Sci.2010;32:357-66.
9.Khajali F,Wideman RF.Dietary arginine:metabolic,environmental,immunological and physiological interrelationships.Worlds Poult Sci J.2010;66:751-66.
10.Fouad AM,El-Senousey HK,Yang XJ,Yao JH.Role of dietary L-arginine in poultry production.Int J Poult Sci.2012;11:718-29.
11.Tamir H,Ratner S.Enzymes of arginine metabolism in chicks.Arch Biochem Biophys.1963;102:249-58.
12.Balnave D,Brake J.Re-evaluation of the classical dietary arginine:lysine interaction for modern poultry diets:a review.Worlds Poult Sci J.2002;58:275-89.
13.Baker DH.Ideal amino acid profiles for swine and poultry and their applications in feed formulation.BioKyowa Tech Rev.1997;9:1-24.
14.Wu G.Dietary requirements of synthesizable amino acids by animals:a paradigm shift in protein nutrition.J Anim Sci Biotechnol.2014;5:34.
15.Mutryn MF,Brannick EM,Fu W,Lee WR,Abasht B.Characterization of a novel chicken muscle disorder through differential gene expression and pathway analysis using RNA-sequencing.BMC Genomics.2015;16(399).https://doi.org/10.1186/s12864-015-1623-0.
16.Boerboom G,van Kempen T,Navarro-Villa A,Pérez-Bonilla A.Unraveling the cause of white striping in broilers using metabolomics.Poult Sci.2018.https://doi.org/10.3382/ps/pey266.
17.Bodle BC,Alvarado C,Shirley RB,Mercier Y,Lee JT.Evaluation of different dietary alterations in their ability to mitigate the incidence and severity of woody breast and white striping in commercial male broilers.Poult Sci.2018.https://doi.org/10.3382/ps/pey166.
18.Baeza E,Jégou M,Gondret F,Lalande-Martin J,Tea I,Le Bihan-Duval E,et al.Pertinent plasma indicators of the ability of chickens to synthesize and store lipids.J Anim Sci.2015;93:107-16.
19.European Union.Council directive 2007/43/EC of 28 June 2007 laying down minimum rules for the protection of chickens kept for meat production.Off J.2007;L182:19-28.
20.European Union.Council directive 2010/63/EU of 22 September 2010 on the protection of animals used for scientific purposes.Off J.2010;L276:33-79.
21.European Union.Council regulation(EC)no 1099/2009 of 24 sept.2009 on the protection of animals at the time of killing.Off J.2009;L303:1-30.
22.Association of Official Analytical Chemists.Official methods of analysis.15th ed.Washington,DC:AOAC;1990.
23.Ajinomoto Heartland LLC.True amino acid digestibility values for poultry.Chicago:Ajinomoto Heartland LLC;2015.http://aaa.lysine.com/AATable/Ingredients.aspx
24.Ekstrand C,Algers B,Svedberg J.Rearing conditions and foot-pad dermatitis in Swedish broiler chickens.Prev Vet Med.1997;31:167-74.
25.Kuttappan VA,Lee Y,Erf GF,Meullenet JF,Owens CM.Consumer acceptance of visual appearance of broiler breast meat with varying degrees of white striping.Poult Sci.2012;91:1240-7.
26.Sihvo HK,Immonen K,Puolanne E.Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers.Vet Pathol.2014;51:619-23.
27.Sirri F,Maiorano G,Tavaniello S,Chen J,Petracci M,Meluzzi A.Effect of different levels of dietary zinc,manganese,and copper from organic or inorganic sources on performance,bacterial chondronecrosis,intramuscular collagen characteristics,and occurrence of meat quality defects of broiler chickens.Poult Sci.2016;95:1813-24.
28.Jeacocke RE.Continuous measurement of the pH of beef muscle in intact beef carcasses.J Food Tech.1977;12:375-86.
29.Sirri F,Petracci M,Zampiga M,Meluzzi A.Effect of EU electrical stunning conditions on breast meat quality of broiler chickens.Poult Sci.2017;96:3000-4
30.Commission Internationale de l’Eclairage.Recommendations on uniform color spaces,color differences,equations.Psychometric color terms.1978;15:Suppl 2.CEI,Paris,France.
31.Folch J,Lees M,Sloane Stanley GH.A simple method for the isolation and purification of total lipids from animal tissues.J Biol Chem.1957;226:497-509.
32.Ventrella D,Laghi L,Barone F,Elmi A,Romagnoli N,Bacci ML.Age-related 1H NMR characterization of cerebrospinal fluid in newborn and young healthy piglets.PLoS One.2016;11:e0157623.
33.Barbara G,Scaioli E,Barbaro MR,Biagi E,Laghi L,Cremon C,et al.Gut microbiota,metabolome and immune signatures in patients with uncomplicated diverticular disease.Gut.2016.https://doi.org/10.1136/gutjnl-2016-312377.
34.Kneen MA,Annegarn HJ.Algorithm for fitting xRF,SEM and PIxE x-ray spectra backgrounds.Nucl Instrum Methods Phys Res B.1996;109:209-13.
35.Liland KH,Alm?y T,Mevik BH.Optimal choice of baseline correction for multivariate calibration of spectra.Appl Spectrosc.2010;64:1007-16.
36.Dieterle F,Ross A,Schlotterbeck G,Senn H.Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures.Application in 1H NMR metabonomics.Anal Chem.2006;78:4281-90.
37.Wishart DS,Tzur D,Knox C,Eisner R,Guo AC,Young N,et al.HMDB:the human metabolome database.Nucleic Acids Res.2007;35(suppl 1):D521-6.
38.SAS.SAS/STAT Guide for Personal Computers,Version 6.03 edition.Cary:SAS Institute Inc;1988.
39.Foschi C,Laghi L,D’Antuono A,Gaspari V,Zhu C,Dellarosa N,et al.Urine metabolome in women with chlamydia trachomatis infection.PLoS One.2018;13(3):e0194827.
40.Hubert M,Rousseeuw PJ,Vanden Branden K.ROBPCA:a new approach to robust principal component analysis.Technometrics.2005;47:64-79.
41.Corzo A,Kidd MT.Arginine needs of the chick and growing broiler.Int JPoult Sci.2003;2:379-82.
42.Jahanian R,Khalifeh-Gholi M.Marginal deficiencies of dietary arginine and methionine could suppress growth performance and immunological responses in broiler chickens.J Anim Physiol Anim Nutr.2018;102:e11-20.
43.Ebrahimi M,Zare Shahneh A,Shivazad M,Ansari Pirsaraei Z,Tebianian M,Ruiz-Feria CA,et al.The effect of feeding excess arginine on lipogenic gene expression and growth performance in broilers.Br Poult Sci.2014;55:81-8.
44.Laika M,Jahanian R.Increase in dietary arginine level could ameliorate detrimental impacts of coccidial infection in broiler chickens.Livest Sci.2017;195:38-44.
45.Xu YQ,Guo YW,Shi BL,Yan SM,Guo XY.Dietary arginine supplementation enhances the growth performance and immune status of broiler chickens.Livest Sci.2018;209:8-13.
46.Fouad AM,El-Senousey HK,Yang XJ,Yao JH.Dietary L-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens.Animal.2013;7:1239-45.
47.Corzo A,Moran ET Jr,Hoehler D.Arginine need of heavy broiler males:applying the ideal protein concept.Poult Sci.2003;82:402-7.
48.Kidd MT,Peebles ED,Whitmarsh SK,Yeatman JB,Wideman RF Jr.Growth and immunity of broiler chicks as affected by dietary arginine.Poult Sci.2001;80:1535-42.
49.Christensen K,Owens C,Kidd MT.The effect of added l-arginine on the severity of woody breast and white striping in male broilers.Poultry Science Association Annual Meeting Abstracts.Poult Sci.2015;94(E-Suppl 1):147.
50.Jiao P,Guo Y,Yang X,Long F.Effects of dietary arginine and methionine levels on broiler carcass traits and meat quality.J Anim Vet Adv.2010;9:1546-51.
51.Rueda E,Michelangeli C,Gonzalez-Mujica F.L-canavanine inhibits L-arginine uptake by broiler chicken intestinal brush border membrane vesicles.Br Poult Sci.2003;44:620-5.
52.Brake J,Balnave D.Essentiality of arginine in broilers during hot weather.St Louis:Proceedings of 12th Annual Biokyowa Amino Acid Council Meeting;1995
53.Escobar J,Frank JW,Suryawan A,Nguyen HV,Kimball SR,Jefferson LS,et al.Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation.Am JPhysiol Endocrinol Metab.2005;288:E914-21.
54.Wu LY,Fang YJ,Guo XY.Dietary L-arginine supplementation beneficially regulates body fat deposition of meat-type ducks.Br Poult Sci.2011;52:221-6.
55.Newsholme P,Lima MMR,Procopio J,Pithon-Curi TC,Bazotte RB,Curi R.Glutamine and glutamate as vital metabolites.Braz J Med Biol Res.2003;36:153-63.
56.Wu G,Bazer FW,Burghardt RC,Johnson GA,Kim SW,Knabe DA,et al.Proline and hydroxyproline metabolism:implications for animal and human nutrition.Amino Acids.2011;40:1053-63.
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