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Low-protein diets affect ileal amino acid digestibility and gene expression of digestive enzymes in growing and finishing pigs

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Abstract

The objective of this study was to evaluate effects of dietary crude protein (CP) intake on ileal amino acid digestibilities and expression of genes for digestive enzymes in growing and finishing pigs. In Experiment 1, 18 growing pigs (average initial BW = 36.5 kg) were assigned randomly into one of three treatments (n = 6/treatment group) representing normal (18 % CP), low (15 % CP), and very low (12 % CP) protein intake. In Experiment 2, 18 finishing pigs (average initial BW = 62.3 kg) were allotted randomly into one of three treatments (n = 6/treatment group), representing normal (16 % CP), low (13 % CP) and very low (10 % CP) protein intake. In both experiments, diets with low and very low CP were supplemented with crystalline amino acids to achieve equal content of standardized ileal digestible Lys, Met, Thr, and Trp, and were provided to pigs ad libitum. Daily feed intake, BW, and feed/gain ratios were determined. At the end of each experiment, all pigs were slaughtered to collect pancreas, small-intestine samples, and terminal ileal chymes. Samples were used for determining expression of genes for digestive enzymes and ileal amino acid digestibilities. Growing pigs fed the 12 % CP and 15 % CP diets had lower final body weight (P < 0.01) and ADG (P < 0.0001) when compared with pigs fed the 18 % dietary CP diet. Growing pigs fed with the 12 % CP diet showed higher digestibilities for CP (P < 0.05), DM (P < 0.05), Lys (P < 0.0001), Met (P < 0.01), Cys (P < 0.01), Thr (P < 0.01), Trp (P < 0.05), Val (P < 0.05), Phe (P < 0.05), Ala (P < 0.05), Cys (P < 0.01), and Gly (P < 0.05) than those fed the 18 % CP diet. Finishing pigs fed the 16 % CP diet had a higher (P < 0.01) final body weight than those fed the 10 % CP diet. mRNA levels for digestive enzymes (trypsinogen, chymotrypsin B, and dipeptidases-II and III) differed among the three groups of pigs (P < 0.05), and no difference was noted in the genes expression between control group and lower CP group. These results indicated that a reduction of dietary CP by a six-percentage value limited the growth performance of growing–finishing pigs and that a low-protein diet supplemented with deficient amino acids could reduce the excretion of nitrogen into the environment without affecting weight gain.

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Abbreviations

AA:

Amino acids

BW:

Body weight

CP:

Crude protein

DE:

Digestible energy

References

  • Abbasi MA, Mahdavi AH, Samie AH, Jahanian R (2014) Effects of different levels of dietary crude protein and threonine on performance, humoral immune responses and intestinal morphology of broiler chicks. Braz J Poultry Sci 16:35–44

    Google Scholar 

  • Agyekum AK, Woyengo TA, Slominski BA, Yin YL, Nyachoti CM (2014) Effects of formulating growing pig diet with increasing levels of wheat-corn distillers dried grains with solubles on digestible nutrient basis on growth performance and nutrient digestibility. J Anim Physiol Anim Nutr 98:651–658

    Article  CAS  Google Scholar 

  • Assaad H, Zhou L, Carroll RJ, Wu G (2014) Rapid publication-ready MS-Word tables for one-way ANOVA. SpringerPlus 3:474

    Article  PubMed  PubMed Central  Google Scholar 

  • Awad EA, Fadlullah M, Zulkifli I, Farjam AS, Chwen LT (2014) Amino acids fortification of low-protein diet for broilers under tropical climate: ideal essential amino acids profile. Italian J Anim Sci 13

  • Bartelt J, Jadamus A, Wiese F, Swiech E, Buraczewska L, Simon O (2002) Apparent precaecal digestibility of nutrients and level of endogenous nitrogen in digesta of the small intestine of growing pigs as affected by various digesta viscosities. Arch Anim Nutr 56:93–107

    CAS  Google Scholar 

  • Cahu C, Ronnestad I, Grangier V, Infante JLZ (2004) Expression and activities of pancreatic enzymes in developing sea bass larvae (Dicentrarchus labrax) in relation to intact and hydrolyzed dietary protein; involvement of cholecystokinin. Aquaculture 238:295–308

    Article  CAS  Google Scholar 

  • Dai ZL, Wu ZL, Jia SC, Wu G (2014) Analysis of amino acid composition in proteins of animal tissues and foods as pre-column o-phthaldialdehyde derivatives by HPLC with fluorescence detection. J Chromatogr B 964:116–127

    Article  CAS  Google Scholar 

  • Dourmad JY, Jondreville C (2007) Impact of nutrition on nitrogen, phosphorus, Cu and Zn in pig manure, and on emissions of ammonia and odours. Livest Sci 112:192–198

    Article  Google Scholar 

  • Galassi G, Colombini S, Malagutti L, Crovetto GM, Rapetti L (2010) Effects of high fibre and low protein diets on performance, digestibility, nitrogen excretion and ammonia emission in the heavy pig. Anim Feed Sci Tech 161:140–148

    Article  CAS  Google Scholar 

  • Gallo L, Monta GD, Carraro L, Cecchinato A, Carnier P, Schiavon S (2014) Growth performance of heavy pigs fed restrictively diets with decreasing crude protein and indispensable amino acids content. Livest Sci 161:130–138

    Article  Google Scholar 

  • Gomez-Requeni P, Bedolla-Cazares F, Montecchia C, Zorrilla J, Villian M, Toledo-Cuevas EM, Canosa F (2013) Effects of increasing the dietary lipid levels on the growth performance, body composition and digestive enzyme activities of the teleost pejerrey (Odontesthes bonariensis). Aquaculture 416:15–22

    Article  Google Scholar 

  • Guzman-Pino SA, Sola-Oriol D, Figueroa J, Perez JF (2014) Influence of the protein status of piglets on their ability to select and prefer protein sources. Physiol Behav 129:43–49

    Article  PubMed  CAS  Google Scholar 

  • Hansen MJ, Norgaard JV, Adamsen APS, Poulsen HD (2014) Effect of reduced crude protein on ammonia, methane, and chemical odorants emitted from pig houses. Livest Sci 169:118–124

    Article  Google Scholar 

  • He LQ, Yang HS, Li TJ, Fang J, Zhou XH, Yin YL, Wu L, Nyachoti MN, Wu G (2013) Effects of dietary l-lysine intake on the intestinal mucosa and expression of CAT genes in weaned piglets. Amino Acids 45:383–391

    Article  PubMed  CAS  Google Scholar 

  • Hernandez F, Martinez S, Lopez C, Megias MD, Lopez M, Madrid J (2011) Effect of dietary crude protein levels in a commercial range, on the nitrogen balance, ammonia emission and pollutant characteristics of slurry in fattening pigs. Animal 5:1290–1298

    Article  PubMed  CAS  Google Scholar 

  • Hinson RB, Schinckel AP, Radcliffe JS, Allee GL, Sutton AL, Richert BT (2009) Effect of feeding reduced crude protein and phosphorus diets on weaning-finishing pig growth performance, carcass characteristics, and bone characteristics. J Anim Sci 87:1502–1517

    Article  PubMed  CAS  Google Scholar 

  • Hou YQ, Wang L, Yi D, Ding BY, Yang ZG, Li J, Chen X, Qiu YS, Wu G (2013) N-Acetylcysteine reduces inflammation in the small intestine by regulating redox, EGF and TLR4 signaling. Amino Acids 45:513–522

    Article  PubMed  CAS  Google Scholar 

  • Hou YQ, Yin YL, Wu G (2015) Dietary essentiality of “nutritionally nonessential amino acids” for animals and humans. Exp Biol Med. doi:10.1177/1535370215587913

    Google Scholar 

  • Hu HB et al (2015) Effects of dietary xylan on growth performance, digestive enzyme activity and intestinal morphology of juvenile turbot (Scophthalmus maximus L.) Isr J Aquacult Bamid 67:1–10

  • Infante JLZ, Cahu CL (2007) Dietary modulation of some digestive enzymes and Metabolic processes in developing marine fish: applications to diet formulation. Aquaculture 268:98–105

    Article  Google Scholar 

  • Jobgen WS, Fried SK, Fu WJ, Meininger CJ, Wu G (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17:571–588

    Article  PubMed  CAS  Google Scholar 

  • Kaji I, Akiba Y, Kaunitz JD (2013) DIGESTIVE PHYSIOLOGY OF THE PIG SYMPOSIUM: involvement of gut chemosensing in the regulation of mucosal barrier function and defense mechanisms. J Anim Sci 91:1957–1962

    Article  PubMed  CAS  Google Scholar 

  • Kerr BJ, Southern LL, Bidner TD, Friesen KG, Easter RA (2003a) Influence of dietary protein level, amino acid supplementation, and dietary energy levels on growing-finishing pig performance and carcass composition. J Anim Sci 81:3075–3087

    PubMed  CAS  Google Scholar 

  • Kerr BJ, Yen JT, Nienaber JA, Easter RA (2003b) Influences of dietary protein level, amino acid supplementation and environmental temperature on performance, body composition, organ weights and total heat production of growing pigs. J Anim Sci 81:1998–2007

    PubMed  CAS  Google Scholar 

  • Kim BG, Petersen GI, Hinson RB, Allee GL, Stein HH (2009) Amino acid digestibility and energy concentration in a novel source of high-protein distillers dried grains and their effects on growth performance of pigs. J Anim Sci 87:4013–4021

    Article  PubMed  CAS  Google Scholar 

  • Kim JC, Heo JM, Mullan BP, Pluske JR (2011) Efficacy of a reduced protein diet on clinical expression of post-weaning diarrhoea and life-time performance after experimental challenge with an enterotoxigenic strain of Escherichia coli. Anim Feed Sci Tech 170:222–230

    Article  CAS  Google Scholar 

  • Kulthe AA, Pawar VD, Kotecha PM, Chavan UD, Bansode VV (2014) Development of high protein and low calorie cookies. J Food Sci Tech Mys 51:153–157

    Article  CAS  Google Scholar 

  • Mills PA, Rotter RG, Marquardt RR (1989) Modification of the glucosamine method for the quantification of fungal contamination. Can J Anim Sci 69:1105–1106

    Article  Google Scholar 

  • National Research Council (2012) Nutrient Requirements of Swine: Eleventh Revised Edition. The National Academies Press, Washington, DC

  • Navarro-Guillen C, Moyano FJ, Yufera M (2015) Diel food intake and digestive enzyme production patterns in Solea senegalensis larvae. Aquaculture 435:33–42

    Article  CAS  Google Scholar 

  • Noblet J, Le Bellego L, Van Milgen J, Dubois S (2001) Effects of reduced dietary protein level and fat addition on heat production and nitrogen and energy balance in growing pigs. Anim Res 50:227–238

    Article  Google Scholar 

  • Orlando UAD, de Oliveira RFM, Donzele JL, Silva FCD, Generoso RAR, de Siqueira JC (2007) Dietary crude protein levels and amino acid supplementation for gilts from 30 to 60 kg maintained in a high environmental temperature. Rev Bras Zootecn 36:1573–1578

    Article  Google Scholar 

  • Perez-Jimenez A, Cardenete G, Morales AE, Garcia-Alcazar A, Abellan E, Hidalgo MC (2009) Digestive enzymatic profile of Dentex dentex and response to different dietary formulations. Comp Biochem Phys A 154:157–164

    Article  Google Scholar 

  • Portejoie S, Dourmad JY, Martinez J, Lebreton Y (2004) Effect of lowering dietary crude protein on nitrogen excretion, manure composition and ammonia emission from fattening pigs. Livest Prod Sci 91:45–55

    Article  Google Scholar 

  • Rezaei R, Wang WW, Wu ZL, Dai ZL, Wang JJ, Wu G (2013a) Biochemical and physiological bases for utilization of dietary amino acids by young pigs. J Anim Sci Biotechnol 4:7

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rezaei R, Knabe DA, Tekwe CD, Dahanayaka S, Ficken MD, Fielder SE, Eide SJ, Lovering SL, Wu G (2013b) Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids 44:911–923

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Gonzalez H, Hernandez-Llamas A, Garcia-Ulloa M, Racotta IS, Montoya-Mejia M, Villarreal H (2014) Effect of protein and lipid levels in diets for female red claw crayfish Cherax quadricarinatus on quality of offspring (juvenile), with emphasis on growth performance, biochemical composition and stress resistance to low oxygen, high ammonia and salinity. Aquacult Nutr 20:557–565

    Article  CAS  Google Scholar 

  • Ruusunen M, Partanen K, Poso R, Puolanne E (2007) The effect of dietary protein supply on carcass composition, size of organs, muscle properties and meat quality of pigs. Livest Sci 107:170–181

    Article  Google Scholar 

  • Sharma VC, Mahesh MS, Mohini M, Datt C, Nampoothiri VM (2014) Nutrient utilisation and methane emissions in Sahiwal calves differing in residual feed intake. Arch Anim Nutr 68:345–357

    Article  PubMed  CAS  Google Scholar 

  • Toledo JB, Furlan AC, Pozza PC, Carraro J, Moresco G, Ferreira SL, Gallego AG (2014) Reduction of the crude protein content of diets supplemented with essential amino acids for piglets weighing 15 to 30 kilograms. Rev Bras Zootecn 43:301–309

    Article  Google Scholar 

  • Wang YF, Zhang YZ, Feng ZM, Zhang YG, Li TJ, Huang RL (2012) Measurement of protein and amino acid digestibility for swine diet formulation. J Food Agric Environ 10:650–654

    CAS  Google Scholar 

  • Wang WW, Dai ZL, Wu ZL, Lin G, Jia SC, Hu SD, Dahanayaka S, Wu G (2014) Glycine is a nutritionally essential amino acid for maximal growth of milk-fed young pigs. Amino Acids 46:2037–2045

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Zhang C, Wu G, Sun YL, Wang B, He BB, Dai ZL, Wu ZL (2015a) Glutamine enhances tight-junction protein expression and modulates CRF signaling in the jejunum of weanling piglets. J Nutr 145:25–31

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Ji Y, Wu G, Sun KJ, Sun YL, Li W, Wang B, He BB, Zhang Q, Dai ZL, Wu ZL (2015b) L-Tryptophan activates mammalian target of rapamycin and enhances expression of tight junction proteins in intestinal porcine epithelial cells. J Nutr 145:1156–1162

    Article  PubMed  CAS  Google Scholar 

  • Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17

    Article  PubMed  Google Scholar 

  • Wu G (2013a) Amino Acids: Biochemistry and Nutrition. CRC Press, Boca Raton, Florida

    Book  Google Scholar 

  • Wu G (2013b) Functional amino acids in nutrition and health. Amino Acids 45:407–411

    Article  PubMed  CAS  Google Scholar 

  • Wu G (2014) Dietary requirements of synthesizable amino acids by animals: a paradigm shift in protein nutrition. J Anim Sci Biotechnol 5:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu G, Wu ZL, Dai ZL, Yang Y, Wang WW, Liu C, Wang B, Wang JJ, Yin YL (2013) Dietary requirements of “nutritionally nonessential amino acids” by animals and humans. Amino Acids 44:1107–1113

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Fanzo J, Miller DD, Pingali P, Post M, Steiner JL, Thalacker-Mercer AE (2014a) Production and supply of high-quality food protein for human consumption: sustainability, challenges and innovations. Ann NY Acad Sci 1321:1–19

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Cross HR (2014b) Land-based production of animal protein: impacts, efficiency, and sustainability. Ann NY Acad Sci 1328:18–28

    Article  PubMed  Google Scholar 

  • Wu G, Bazer FW, Dai ZL, Li DF, Wang JJ, Wu ZL (2014c) Amino acid nutrition in animals: Protein synthesis and beyond. Annu Rev Anim Biosci 2:387–417

    Article  PubMed  CAS  Google Scholar 

  • Xiccato G, Schiavon S, Gallo L, Bailoni L, Bittante G (2005) Nitrogen excretion in dairy cow, beef and veal cattle, pig, and rabbit farms in Northern Italy. Italian J Anim Sci 4:103–111

    Google Scholar 

  • Xu WJ, Pan LQ (2014) Dietary protein level and C/N ratio manipulation in zero-exchange culture of Litopenaeus vannamei: evaluation of inorganic nitrogen control, biofloc composition and shrimp performance. Aquac Res 45:1842–1851

    CAS  Google Scholar 

  • Zollitschstelzl J (1992) Effects of reduced protein-content on performance and N-excretion in pig fattening. Bodenkultur 43:353–362

    Google Scholar 

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Acknowledgments

This work was supported by National Basic Research Program of China (2013CB127301, 2013CB127306), National Scientific and Technology Support Project (2013BAD21B04), the Chinese Academy of Sciences through its Hundred Talent Program to Kan Yao, and Texas A&M AgriLife Research (H-8200).

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Correspondence to Tiejun Li, Kang Yao or Yulong Yin.

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The authors declare that they have no conflict of interest.

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L. He and L. Wu made equal contributions to this study, so they are joint first authors.

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He, L., Wu, L., Xu, Z. et al. Low-protein diets affect ileal amino acid digestibility and gene expression of digestive enzymes in growing and finishing pigs. Amino Acids 48, 21–30 (2016). https://doi.org/10.1007/s00726-015-2059-1

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  • DOI: https://doi.org/10.1007/s00726-015-2059-1

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