Metabolism of glycerol in pigs fed diets containing mixed crude glycerin and β-adrenergic agonist
A. B. F. Pinto A , L. de P. Naves B D , I. G. Lima A , C. A. P. Garbossa C , S. R. Silva
+ Author Affiliations
- Author Affiliations
A Departamento de Medicina Veterinária, Universidade Federal de Lavras, Lavras, Minas Gerais, Caixa Postal 3037, CEP 37200000, Brazil.
B Departamento de Zootecnia, Universidade Federal de Lavras, Lavras, Minas Gerais, Caixa Postal 3037, CEP 37200000, Brazil.
C Departamento de Nutrição e Produção Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Pirassununga, São Paulo, CEP 13635900, Brazil.
D Corresponding author. Email: luciananaves@ufla.br
Animal Production Science 59(9) 1631-1639 https://doi.org/10.1071/AN18210
Submitted: 24 March 2018 Accepted: 3 January 2019 Published: 8 February 2019
Abstract
The optimised use of mixed crude glycerin (MCG) and ractopamine hydrochloride (RH) in diets for finishing pigs requires a better understanding of glycerol metabolism. Therefore, the present study evaluated the performance, blood parameters, metabolite concentrations in the Longissimus lumborum muscle and the activity of enzymes in the liver, subcutaneous adipose tissue and kidney of pigs fed diets containing MCG and/or RH. According to the initial weight, 64 barrows were distributed in a 4 × 2 factorial design, corresponding to four concentrations of MCG (0, 100, 150, and 200 g/kg) in diets containing 0 or 10 mg/kg of RH. There was no MCG × RH interaction for any of the evaluated parameters (P > 0.05). Moreover, there was no isolated effect of dietary MCG or RH on the weight gain and the blood concentrations of glucose, insulin, triacylglycerols, total cholesterol, total protein, albumin, creatinine, cortisol and lactate (P > 0.05). There was a higher rate of phosphorylation of glycerol in the liver, stimulation of lipogenesis in adipose tissue and a likely increase in the utilisation of glycerol by muscle fibres in response to an increased concentration of circulating glycerol from the diet (P < 0.05). In contrast, when the diet contained up to 200 g/kg MCG and 10 mg/kg RH, there were indications of a lower utilisation of glycerol for the synthesis of triacylglycerols in muscle, liver and adipose tissue, in addition to increased oxidation of amino acids in the liver followed by improved feed conversion of pigs (P < 0.05).
Additional keywords: animal metabolism, glucose-6-phosphate dehydrogenase, glutamate dehydrogenase, glycerol kinase, glycerol-3-phosphate dehydrogenase, malic enzyme.
References
Adeola O, Ball RO, Young LG (1992) Porcine skeletal muscle myofibrillar protein synthesis is stimulated by ractopamine. The Journal of Nutrition 122, 488–495.| Porcine skeletal muscle myofibrillar protein synthesis is stimulated by ractopamine.Crossref | GoogleScholarGoogle Scholar | 1347314PubMed |
Araújo TS, Porto LCJ, Mario EG, Pereira LJ, Ferreira MSS, Zangeronimo MG, Napimoga MH, Botion LM, Sousa RV (2014) Ractopamine effect on lipid metabolism and GLUT4 amount of finishing pigs. Turkish Journal of Veterinary and Animal Sciences 38, 54–62.
| Ractopamine effect on lipid metabolism and GLUT4 amount of finishing pigs.Crossref | GoogleScholarGoogle Scholar |
Athayde NB, Dalla Costa OA, Roça RO, Guidoni AL, Ludtke CB, Oba E, Takahira RK, Lima GJMM (2013) Stress susceptibility in pigs supplemented with ractopamine. Journal of Animal Science 91, 4180–4187.
| Stress susceptibility in pigs supplemented with ractopamine.Crossref | GoogleScholarGoogle Scholar | 23825348PubMed |
Bernardino VMP, Rodrigues PB, Naves L de P, Rosa PV, Zangeronimo MG, Gomide EM, Saldanha MM, Alvarenga RR (2014) Content of plasmatic glycerol and activity of hepatic glycerol kinase in broiler chickens fed diets containing different sources and concentrations of glycerine. Journal of Animal Physiology and Animal Nutrition 98, 328–337.
| Content of plasmatic glycerol and activity of hepatic glycerol kinase in broiler chickens fed diets containing different sources and concentrations of glycerine.Crossref | GoogleScholarGoogle Scholar |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Braun JP, Lefebvre HP (2008) Kidney function and damage. In ‘Clinical biochemistry of domestic animals’. (Eds JJ Kaneko, JW Harvey, ML Bruss) pp. 485–528. (Elsevier: London)
Carr SN, Hamilton DN, Miller KD, Schroeder AL, Fernández-Dueñas D, Killefer J, Ellis M, McKeith FK (2009) The effect of ractopamine hydrochloride (Paylean®) on lean carcass yields and pork quality characteristics of heavy pigs fed normal and amino acid fortified diets. Meat Science 81, 533–539.
| The effect of ractopamine hydrochloride (Paylean®) on lean carcass yields and pork quality characteristics of heavy pigs fed normal and amino acid fortified diets.Crossref | GoogleScholarGoogle Scholar | 20416594PubMed |
Carvalho PLO, Moreira I, Scapinello C, Piano LM, Gallego AG, Moresco G (2013) Crude glycerine in growing and finishing pigs feeding. Semina. Ciências Agrárias 34, 1399–1410.
| Crude glycerine in growing and finishing pigs feeding.Crossref | GoogleScholarGoogle Scholar |
Corominas J, Ramayo-Caldas Y, Puig-Oliveras A, Estellé J, Castelló A, Alves E, Pena RN, Ballester M, Folch JM (2013) Analysis of porcine adipose tissue transcriptome reveals differences in de novo fatty acid synthesis in pigs with divergent muscle fatty acid composition. BMC Genomics 14, 843
| Analysis of porcine adipose tissue transcriptome reveals differences in de novo fatty acid synthesis in pigs with divergent muscle fatty acid composition.Crossref | GoogleScholarGoogle Scholar | 24289474PubMed |
Costa DV, Paulino RR, Okamura D, Oliveira MM, Rosa PV (2015) Growth and energy metabolism of ile tilapia juveniles fed glycerol. Pesquisa Agropecuária Brasileira 50, 347–354.
Costa-Lima BR, Suman SP, Li S, Beach CM, Silva TJ, Silveira ET, Bohrer BM, Boler DD (2015) Dietary ractopamine influences sarcoplasmic proteome profile of pork Longissimus thoracis. Meat Science 103, 7–12.
| Dietary ractopamine influences sarcoplasmic proteome profile of pork Longissimus thoracis.Crossref | GoogleScholarGoogle Scholar | 25576742PubMed |
Faria PB, Cantarelli VS, Fialho ET, Pinto AMBG, Faria JH, Rocha MFM, Guerreiro MC, Bressan MC (2015) Lipid profile and cholesterol of pork with the use of glycerin in feeding. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 67, 535–546.
| Lipid profile and cholesterol of pork with the use of glycerin in feeding.Crossref | GoogleScholarGoogle Scholar |
Ferreira MSS, Garbossa CAP, Oberlender G, Pereira LJ, Zangeronimo MG, Sousa RV, Cantarelli VS (2013) Effect of ractopamine on lipid metabolism in vivo: a systematic review. Brazilian Archives of Biology and Technology 56, 35–43.
| Effect of ractopamine on lipid metabolism in vivo: a systematic review.Crossref | GoogleScholarGoogle Scholar |
Gomide APC, Brustolini PC, Ferreira AS, Paulino PVR, Lima AL, Scottá BA, Rodrigues VV, Câmara LRA, Moita AMS, Oliveira Júnior GM, Ferreira RC, Formigoni AS (2012) Substitution of corn for crude glycerin in diets for finishing pigs. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 64, 1309–1316.
| Substitution of corn for crude glycerin in diets for finishing pigs.Crossref | GoogleScholarGoogle Scholar |
Gunawan AM, Richert BT, Schinckel AP, Grant AL, Gerrard DE (2007) Ractopamine induces differential gene expression in porcine skeletal muscle. Journal of Animal Science 85, 2115–2124.
| Ractopamine induces differential gene expression in porcine skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 17468428PubMed |
Hansen CF, Hernandez A, Mullan BP, Moore K, Trezona-Murray M, King RH, Pluske JR (2009) A chemical analysis of samples of crude glycerol from the production of biodiesel in Australia and the effects of feeding crude glycerol to growing–finishing pigs on performance, plasma metabolites and meat quality at slaughter. Animal Production Science 49, 154–161.
| A chemical analysis of samples of crude glycerol from the production of biodiesel in Australia and the effects of feeding crude glycerol to growing–finishing pigs on performance, plasma metabolites and meat quality at slaughter.Crossref | GoogleScholarGoogle Scholar |
Huang QC, Xu ZR, Han XY, Li WF (2008) Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mRNA expression in finishing pigs. Animal Feed Science and Technology 140, 365–375.
| Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mRNA expression in finishing pigs.Crossref | GoogleScholarGoogle Scholar |
Inoue M, Wakayama Y, Kojima H, Shibuya S, Jimi T, Hara H, Iijima S, Masaki H, Oniki H, Matsuzaki Y (2009) Aquaporin 9 expression and its localization in normal skeletal myofiber. Journal of Molecular Histology 40, 165–170.
| Aquaporin 9 expression and its localization in normal skeletal myofiber.Crossref | GoogleScholarGoogle Scholar | 19629726PubMed |
Jocken JW, Roepstorff C, Goossens GH, van der Baan P, an Baak M, Saris WH, Kiens B, Blaak EE (2008) Hormone-sensitive lipase serine phosphorylation and glycerol exchange across skeletal muscle in lean and obese subjects: effect of β-adrenergic stimulation. Diabetes 57, 1834–1841.
| Hormone-sensitive lipase serine phosphorylation and glycerol exchange across skeletal muscle in lean and obese subjects: effect of β-adrenergic stimulation.Crossref | GoogleScholarGoogle Scholar | 18398140PubMed |
Kaneko JJ, Harvey JW, Bruss ML (2008) Appendix VII. In ‘Clinical biochemistry of domestic animals’. (Eds JJ Kaneko, JW Harvey, ML Bruss) pp. 882–888. (Elsevier: London, UK)
Kihara F, Itoh K, Iwasaka M, Niimi T, Yamashita O, Yaginuma T (2009) Glycerol kinase activity and glycerol kinase-3 gene are up-regulated by acclimation to 5°C in diapause eggs of the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 39, 763–769.
| Glycerol kinase activity and glycerol kinase-3 gene are up-regulated by acclimation to 5°C in diapause eggs of the silkworm, Bombyx mori.Crossref | GoogleScholarGoogle Scholar | 19748584PubMed |
Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N, Nishida M, Nishizawa H, Matsuda M, Takahashi M, Hotta K, Nakamura T, Yamashita S, Tochino Y, Matsuzawa Y (2000) Aquaporin adipose, a putative glycerol channel in adipocytes. The Journal of Biological Chemistry 275, 20896–20902.
| Aquaporin adipose, a putative glycerol channel in adipocytes.Crossref | GoogleScholarGoogle Scholar | 10777495PubMed |
Klem TB, Bleken E, Morberg H, Thoresen SI, Framstad T (2010) Hematologic and biochemical reference intervals for Norwegian crossbreed grower pigs. Veterinary Clinical Pathology 39, 221–226.
| Hematologic and biochemical reference intervals for Norwegian crossbreed grower pigs.Crossref | GoogleScholarGoogle Scholar | 20051064PubMed |
Ladeira MM, Carvalho JRR, Chizzotti ML, Teixeira PD, Dias JCO, Gionbelli TR, Rodrigues AC, Oliveira DM (2016) Effect of increasing levels of glycerin on growth rate, carcass traits and liver gluconeogenesis in young bulls. Animal Feed Science and Technology 219, 241–248.
| Effect of increasing levels of glycerin on growth rate, carcass traits and liver gluconeogenesis in young bulls.Crossref | GoogleScholarGoogle Scholar |
Lee DP, Deonarine AS, Kienetz M, Zhu Q, Skrzypczak M, Chan M, Choy PC (2001) A novel pathway for lipid biosynthesis: the direct acylation of glycerol. Journal of Lipid Research 42, 1979–1986.
Li M, Li C, Allen A, Stanley CA, Smith TJ (2012) The structure and allosteric regulation of mammalian glutamate dehydrogenase. Archives of Biochemistry and Biophysics 519, 69–80.
| The structure and allosteric regulation of mammalian glutamate dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 22079166PubMed |
Li G, Fu Y, Han X, Li X, Li C (2016) Metabolomic investigation of porcine muscle and fatty tissue after Clenbuterol treatment using gas chromatography/mass spectrometry. Journal of Chromatography. A 1456, 242–248.
| Metabolomic investigation of porcine muscle and fatty tissue after Clenbuterol treatment using gas chromatography/mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 27320379PubMed |
Liu CY, Grant AL, Kim KH, Ji SQ, Hancock DL, Anderson DB, Mills SE (1994) Limitations of ractopamine to affect adipose tissue metabolism in swine. Journal of Animal Science 72, 62–67.
| Limitations of ractopamine to affect adipose tissue metabolism in swine.Crossref | GoogleScholarGoogle Scholar | 7908017PubMed |
Melo DS, Faria PB, Cantarelli VS, Rocha MFM, Pinto AMBG, Ramos EM (2014) Meat quality of swine with the use of glycerine in feeding. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 66, 583–592.
| Meat quality of swine with the use of glycerine in feeding.Crossref | GoogleScholarGoogle Scholar |
Mendoza SM, Boyd RD, Zier-Rush CE, Ferket PR, Haydon KD, van Heugten E (2017) Effect of natural betaine and ractopamine HCl on whole-body and carcass growth in pigs housed under high ambient temperatures. Journal of Animal Science 95, 3047–3056.
Montell E, Lerín C, Newgard CB, Gómez-Foix AM (2002) Effects of modulation of glycerol kinase expression on lipid and carbohydrate metabolism in human muscle cells. The Journal of Biological Chemistry 277, 2682–2686.
| Effects of modulation of glycerol kinase expression on lipid and carbohydrate metabolism in human muscle cells.Crossref | GoogleScholarGoogle Scholar | 11714702PubMed |
Newsholme EA, Taylor K (1969) Glycerol kinase activities in muscles from vertebrates and invertebrates. The Biochemical Journal 112, 465–474.
| Glycerol kinase activities in muscles from vertebrates and invertebrates.Crossref | GoogleScholarGoogle Scholar | 5801671PubMed |
Oliveira L, Madrid J, Ramis G, Martínez S, Orengo J, Villodre C, Valera L, López MJ, Palláres FL, Quereda JJ, Mendonça L, Hernández F (2014) Adding crude glycerin to nursery pig diet: effect on nutrient digestibility, metabolic status, intestinal morphology and intestinal cytokine expression. Livestock Science 167, 227–235.
| Adding crude glycerin to nursery pig diet: effect on nutrient digestibility, metabolic status, intestinal morphology and intestinal cytokine expression.Crossref | GoogleScholarGoogle Scholar |
Orengo J, Villodre C, Madrid J, Martínez S, López MJ, Megías MD, Valera L, Hernández F (2014) Effect of dietary crude glycerin on growth performance, nutrient digestibility and hormone levels of Iberian crossbred pigs from 50 to 100 kg body weight. Livestock Science 165, 95–99.
| Effect of dietary crude glycerin on growth performance, nutrient digestibility and hormone levels of Iberian crossbred pigs from 50 to 100 kg body weight.Crossref | GoogleScholarGoogle Scholar |
Papadomichelakis G, Zoidis E, Mountzouris KC, Lippas T, Fegeros K (2012) Glycerine kinase gene expression, nutrient digestibility and gut microbiota composition in post-weaned pigs fed diets with increasing crude glycerine levels. Animal Feed Science and Technology 177, 247–252.
| Glycerine kinase gene expression, nutrient digestibility and gut microbiota composition in post-weaned pigs fed diets with increasing crude glycerine levels.Crossref | GoogleScholarGoogle Scholar |
Pérez MP, Palacio J, Santolaria MP, Aceña MC, Chacón G, Gascón M, Calvo JH, Zaragoza P, Beltran JA, Garcıa-Belenguer S (2002) Effect of transport time on welfare and meat quality in pigs. Meat Science 61, 425–433.
| Effect of transport time on welfare and meat quality in pigs.Crossref | GoogleScholarGoogle Scholar | 22061073PubMed |
Perri AM, O’Sullivan TL, Harding JC, Wood RD, Friendship RM (2017) Hematology and biochemistry reference intervals for Ontario commercial nursing pigs close to the time of weaning. The Canadian Veterinary Journal. La Revue Veterinaire Canadienne 58, 371–376.
Puls CL, Trout WE, Ritter MJ, McKeith FK, Carr SN, Ellis M (2015) Impact of ractopamine hydrochloride on growth performance, carcass and pork quality characteristics and responses to handling and transport in finishing pigs. Journal of Animal Science 93, 1229–1238.
| Impact of ractopamine hydrochloride on growth performance, carcass and pork quality characteristics and responses to handling and transport in finishing pigs.Crossref | GoogleScholarGoogle Scholar | 26020899PubMed |
Ribeiro PAP, Costa LS, Pereira RT, Murgas LDS, Rosa PV (2013) Metabolic parameters of pacu fed different oil sources. Pesquisa Agropecuária Brasileira 48, 1035–1042.
| Metabolic parameters of pacu fed different oil sources.Crossref | GoogleScholarGoogle Scholar |
Rosdahl H, Hamrin K, Ungerstedt U, Henriksson J (1998) Metabolite levels in human skeletal muscle and adipose tissue studied with microdialysis at low perfusion flow. American Journal of Physiology. Endocrinology and Metabolism 274, E936–E945.
| Metabolite levels in human skeletal muscle and adipose tissue studied with microdialysis at low perfusion flow.Crossref | GoogleScholarGoogle Scholar |
Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RF, Lopes DC, Ferreira AS, Barreto SLT, Euclides RF (2011) ‘Brazilian tables for poultry and swine: composition of feedstuffs and nutritional requirements.’ (Federal University of Viçosa: Minas Gerais, Brazil)
Samra JS, Ravell CL, Giles SL, Arner P, Frayn KN (1996) Interstitial glycerol concentration in human skeletal muscle and adipose tissue is close to the concentration in blood. Clinical Science 90, 453–456.
| Interstitial glycerol concentration in human skeletal muscle and adipose tissue is close to the concentration in blood.Crossref | GoogleScholarGoogle Scholar | 8697714PubMed |
Sato T, Morita A, Mori N, Miura S (2014) The role of glycerol-3-phosphate dehydrogenase 1 in the progression of fatty liver after acute ethanol administration in mice. Biochemical and Biophysical Research Communications 444, 525–530.
| The role of glycerol-3-phosphate dehydrogenase 1 in the progression of fatty liver after acute ethanol administration in mice.Crossref | GoogleScholarGoogle Scholar | 24472537PubMed |
Seltzer WK, Angelini C, Dhariwal G, Ringel SP, McCabe ER (1989) Muscle glycerol kinase in Duchenne dystrophy and glycerol kinase deficiency. Muscle & Nerve 12, 307–313.
| Muscle glycerol kinase in Duchenne dystrophy and glycerol kinase deficiency.Crossref | GoogleScholarGoogle Scholar |
Shaw FD, Trout GR, McPhee CP (1995) Plasma and muscle cortisol measurements as indicators of meat quality and stress in pigs. Meat Science 39, 237–246.
| Plasma and muscle cortisol measurements as indicators of meat quality and stress in pigs.Crossref | GoogleScholarGoogle Scholar | 22059829PubMed |
Shelton JL, Matthews JO, Southern LL, Higbie AD, Bidner TD, Fernandez JM, Pontif JE (2004) Effect of nonwaxy and waxy sorghum on growth, carcass traits, and glucose and insulin kinetics of growing-finishing barrows and gilts. Journal of Animal Science 82, 1699–1706.
| Effect of nonwaxy and waxy sorghum on growth, carcass traits, and glucose and insulin kinetics of growing-finishing barrows and gilts.Crossref | GoogleScholarGoogle Scholar | 15216997PubMed |
Skowronski MT, Lebeck J, Rojek A, Praetorius J, Fuchtbauer EM, Frøkiær J, Nielsen S (2007) AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. American Journal of Physiology. Renal Physiology 292, F956–F965.
| AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism.Crossref | GoogleScholarGoogle Scholar | 17077387PubMed |
Sohara E, Uchida S, Sasaki S (2009) Function of aquaporin-7 in the kidney and the male reproductive system. In ‘Aquaporins. Handbook of experimental pharmacology’. (Ed. E Beitz) pp. 219–231. (Springer: Heidelberg, Germany)
Spina J, Bright HJ, Rosenbloom J (1970) Purification and properties of L-malic enzyme from Escherichia coli. Biochemistry 9, 3794–3801.
| Purification and properties of L-malic enzyme from Escherichia coli.Crossref | GoogleScholarGoogle Scholar |
United States Department of Agriculture – Foreing Agricultural Service (USDA–FAS) (2017) EU-28 biofuels annual report 2017. GAIN report NL7015. United States Department of Agriculture, Foreing Agricultural Service, Washington, DC.
Wakayama Y, Inoue M, Kojima H, Jimi T, Shibuya S, Hara H, Oniki H (2004) Expression and localization of aquaporin 7 in normal skeletal myofiber. Cell and Tissue Research 316, 123–129.
| Expression and localization of aquaporin 7 in normal skeletal myofiber.Crossref | GoogleScholarGoogle Scholar | 14986101PubMed |
Wang T, Yao W, He Q, Shao Y, Zheng R, Huang F (2018) L-leucine stimulates glutamate dehydrogenase activity and glutamate synthesis by regulating mTORC1/SIRT4 pathway in pig liver. Animal Nutrition Journal
| L-leucine stimulates glutamate dehydrogenase activity and glutamate synthesis by regulating mTORC1/SIRT4 pathway in pig liver.Crossref | GoogleScholarGoogle Scholar |
Watford M (2000) Functional glycerol kinase activity and the possibility of a major role for glyceroneogenesis in mammalian skeletal muscle. Nutrition Reviews 58, 145–148.
| Functional glycerol kinase activity and the possibility of a major role for glyceroneogenesis in mammalian skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 10860394PubMed |
Xue L-L, Chen H-H, Jiang J-G (2017) Implications of glycerol metabolism for lipid production. Progress in Lipid Research 68, 12–25.
| Implications of glycerol metabolism for lipid production.Crossref | GoogleScholarGoogle Scholar | 28778473PubMed |
