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Intraruminal propionate supplementation modifies hindlimb energy metabolism without changing the splanchnic release of glucose in growing lambs

Published online by Cambridge University Press:  09 March 2007

Linda Majdoub ,
Michel Vermorel  and
Isabelle Ortigues-Marty
Linda Majdoub
Affiliation:
Unité de Recherches sur les Herbivores, INRA Theix, 63122 Saint Genès Champanelle, France
Michel Vermorel
Affiliation:
Unité de Recherches sur les Herbivores, INRA Theix, 63122 Saint Genès Champanelle, France
Isabelle Ortigues-Marty*
Affiliation:
Unité de Recherches sur les Herbivores, INRA Theix, 63122 Saint Genès Champanelle, France
*
*Corresponding Author: Dr Isabelle Ortigues-Marty, fax +33 4 73 62 46 39, email ortigues@clermont.inra.fr
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Abstract

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The influence of propionate supplementation on the splanchnic metabolism of energy-yielding nutrients and the supply of glucose to the hindlimb was investigated in growing lambs. Six rumen-cannulated and multicatheterized lambs (32·2 kg), fed frozen rye grass at 690 kJ metabolizable energy intak/ per kg body weight0·75, were infused intraruminally with a salt solution (control) or with propionate solutions at 0·55 mo/ (P1) or 0·98 mo/ (P2) according to a replicated Latin square design. In the rumen fluid, supplementation decreased the acetate:propionate molar ratio from 2·36:1 to 1·37:1, without modifying the ruminal concentrations of acetate and NH4. As a result, the portal appearance of propionate increased by 51 and 72 % with P1 and P2, respectively, and that of L-LACTATE DOUBLED. ACROSS THE Liver, net extraction of propionate increased by 47 and 67 % with P1 and P2, respectively. However, the net hepatic production of glucose remained unchanged, probably as the result of a substantial rise in insulin secretion and its hepatic extraction. Overall, the net splanchnic release of acetate, glucose and butyrate was not modified while that of L-lactate increased. Despite this, the net uptake of acetate, glucose, l-lactate and non-esterified fatty acids by the hindlimb increased. Propionate probably enhanced the storage of energy-yielding nutrients in the hindlimb, despite their unchanged release by the splanchnic tissues and the unmodified insulinaemia. Regulatory mechanisms are not clear.

Keywords

PropionateSplanchnic tissuesHindlimbInsulin
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 1 , January 2003 , pp. 39 - 50
Copyright
Copyright © The Nutrition Society 2003

References

Armentano, E (1992) Ruminant hepatic metabolism of volatile fatty acids, lactate and pyruvate. Journal of Nutrition 122, 838–842.CrossRefGoogle ScholarPubMed
Baird, GD, Lomax, MA, Symonds, HW & Shaw, SR (1980) Net hepatic and splanchnic metabolism of lactate, pyruvate and propionate in dairy cows in vivo in relation to lactation and nutrient supply. Biochemical Journal 186, 47–57.CrossRefGoogle ScholarPubMed
Barnes, RJ, Comline, RS & Dobson, A (1986) The control of splanchnic blood flow. In Control of Digestion and Metabolism in Ruminants, pp. 41–59 [Milligan, LP, Grovum, WL and Dobson, A, editors]. Englewood Cliffs, NJ: Prentice Hall.Google Scholar
Bergman, EN (1990) Energy contribution of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–587.CrossRefGoogle ScholarPubMed
Bergmeyer, HU, Bernt, E, Schmidt, F & Stork, H (1974) Determination with Hexokinase and Glucose-6-Phosphate dehydrogenase. In Methods of Enzymatic Analysis, pp. 1196–1200 [Bergmayer, HU, editor]. London: Academic Press.Google Scholar
Berthelot, V, Bas, P, Schmidely, P & Duvaux-Ponter, C (2001) Effect of dietary propionate on intake patterns and fatty acid composition of adipose tissues in lambs. Small Ruminant Research 40, 29–36.CrossRefGoogle ScholarPubMed
Berthelot, V, Pierzynowski, SG, Sauvant, D & Kristensen, NB (2002) Hepatic metabolism of propionate and methylmalonate in growing lambs. Livestock Production Science 74, 33–43.CrossRefGoogle Scholar
Brockman, RP (1985) Role of insulin in regulating hepatic gluconeogenesis in sheep. Canadian Journal of Physiology and Pharmacology 63, 1460–1464.CrossRefGoogle ScholarPubMed
Brockman, RP (1993) Glucose and short-chain fatty acid metabolism. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 249–265 [Forbes, JM, editor]. Cambridge: CAB International.Google Scholar
Brockman, RP & Larveld, B (1986) Hormonal regulation of metabolism in ruminants: a review. Livestock Production Science 14, 313–334.CrossRefGoogle Scholar
Casse, EA, Rulquin, H & Huntington, GB (1994) Effect of mesenteric vein infusion of propionate on splanchnic metabolism in primiparous Holstein cows. Journal of Dairy Science 77, 3296–3303.CrossRefGoogle ScholarPubMed
Demigné, C, Yacoub, C, Morand, C & Rémésy, C (1991) Interactions between propionate and amino acid metabolism in isolated sheep hepatocytes. British Journal of Nutrition 65, 301–317.CrossRefGoogle ScholarPubMed
De Visser, H, Valk, H, Klop, A, Van Der Meulen, J, Bakker, JGM & Huntington, GB (1997) Nutrient fluxes in splanchnic tissue of dairy cows: Influence of grass quality. Journal of Dairy Science 80, 1666–1673.CrossRefGoogle ScholarPubMed
Donkin, SS, Bertics, SJ & Armentano, LE (1997) Chronic and transitional regulation of gluconeogenesis and glyconeogenesis by insulin and glucagon in neonatal calf hepatocytes. Journal of Animal Science 75, 3082–3087.CrossRefGoogle ScholarPubMed
Drackley, JK, Overton, TR & Douglas, GN (2001) Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during the periparturient period. Journal of Dairy Science 84, Suppl., E100–E112.CrossRefGoogle Scholar
Eisemann, JH, Catherman, DR & Huntington, GB (1994) Comparison of insulin infusion sites on metabolite net flux and insulin kinetics in growing euglycemic beef steers. Journal of Animal Science 72, 990–997.CrossRefGoogle ScholarPubMed
Eisemann, JH & Huntington, GB (1994) Metabolite flux across portal-drained viscera, liver and hindquarters of hyperinsulinemic, euglycemic beef steers. Journal of Animal Science 72, 2919–2929.CrossRefGoogle ScholarPubMed
Geay, Y, Bauchart, D, Hocquette, JF & Culioli, J (2001) Effect of nutritional factors on biochemical, structural and metabolic characteristics of muscles in ruminants, consequences on dietetic value and sensorial qualities of meat. Reproduction Nutrition Development 41, 1–26.CrossRefGoogle ScholarPubMed
Girard, C, Majdoub, L & Ortigues-Marty, I (2001) Effects of propionate supply on plasma vit B12 in growing lambs. Journal of Animal Science 79, Suppl., 78.Google Scholar
Gross, KL, Harmon, DL, Minton, JE & Avery, TB (1990) Effects of isoenergetic infusions of propionate and glucose on portal-drained visceral nutrient flux and concentrations of hormones in lambs maintained by total intragastric infusion. Journal of Animal Science 68, 2566–2574.CrossRefGoogle ScholarPubMed
Gutmann, I & Wahlefeld, AW (1974) L-(+)-Lactate determination with lactate dehydrogenase and NAD. In Methods of Enzymatic Analysis, pp. 1464–1468 [Bergmayer, HU, editor]. London: Academic Press.Google Scholar
Harmon, DL (1986) Influence of dietary energy intake and substrate addition on the in vitro metabolism of glucose and glutamine in rumen epithelial tissue. Comparative Biochemistry and Physiology 3, 643–647.Google Scholar
Harmon, DL (1992) Impact of nutrition on pancreatic exocrine and endocrine secretion in ruminants: a review. Journal of Animal Science 70, 1290–1301.CrossRefGoogle ScholarPubMed
Harmon, DL & Avery, TB (1987) Effects of dietary monensin and sodium propionate on net nutrient flux in steers fed a high-concentrate diet. Journal of Animal Science 65, 1610–1616.CrossRefGoogle ScholarPubMed
Harmon, DL, Gross, KL & Avery, TB (1989) Influence of ionophore addition to a high-concentrate diet on net nutrient flux in steers. Nutrition Reports International 40, 1127–1135.Google Scholar
Harris, PM, Skene, PA, Bauchan, V, Milne, E, Calder, AG, Anderson, SE, Connell, A & Lobley, GE (1992) Effect of intake on hind-limb and whole-body protein metabolism in young growing sheep: chronic studies based on arterio-venous techniques. British Journal of Nutrition 68, 389–407.CrossRefGoogle ScholarPubMed
Hocquette, JF, Ortigues-Marty, I, Pethick, D, Herpin, P & Fernandez, X (1998) Nutritional and hormonal regulation of energy metabolism in skeletal muscles of meat-producing animals. Livestock Production Science 56, 115–143.CrossRefGoogle Scholar
Hristov, AN (1998) Nitrogen fractions and in sacco dry matter and crude protein degradability of fresh and frozen alfalfa. Animal Feed Science Technology 71, 351–355.CrossRefGoogle Scholar
Institut National de Recherches Agronomiques (1978) Tableaux de la valeur nutritive des aliments (Tables of nutritive values of foods). In Alimentation des Ruminants, pp. 519–555 [Publications, INRA, editor]. Versailles: INRA.Google Scholar
Isserty, A & Ortigues, I (1994) Methods of analysis relating to blood flow measurement of the viscera and aorta in sheep. Reproduction Nutrition Development 34, 399–413.CrossRefGoogle ScholarPubMed
Jouany, JP (1982) Volatile fatty acids and alcohol determination in digestive contents, silage juices, bacterial cultures and anaerobic fermentor contents. Sciences des Aliments 2, 131–144.Google Scholar
Journet, M, Huntington, G & Peyraud, JL (1995) Le bilan des produits terminaux de la digestion (Quantification of digestion end-products). In Nutrition des Ruminants Domestiques, Ingestion et Digestion, pp. 671–720 [Jarrige, R, Ruckebusch, Y, Demarquilly, C, Farce, MH and Journet, M, editors]. Paris: INRA.Google Scholar
Katz, ML & Bergman, EN (1969) A method for simultaneous cannulation of the major splanchnic blood vessels of the sheep. American Journal of Veterinary Research 30, 655–660.Google ScholarPubMed
Kaufman, CF & Bergman, EN (1971) Renal glucose, free fatty acid, and ketone body metabolism in the unanesthetized sheep. American Journal of Physiology 221, 967–972.CrossRefGoogle ScholarPubMed
Kaufman, CF & Bergman, EN (1974) Renal ketone body metabolism and gluconeogenesis in normal and hypoglycemic sheep. American Journal of Physiology 226, 827–832.CrossRefGoogle ScholarPubMed
Kristensen, NB, Gabel, G, Pierzynowski, SG & Danfaer, A (2000a) Portal recovery of short-chain fatty acids infused into the temporarily-isolated and washed reticulo-rumen of sheep. British Journal of Nutrition 84, 477–482.CrossRefGoogle ScholarPubMed
Kristensen, NB, Pierzynowski, SG & Danfaer, A (2000b) Net portal appearance of volatile fatty acids in sheep intraruminally infused with mixtures of acetate, propionate, isobutyrate, butyrate, and valerate. Journal of Animal Science 78, 1372–1379.CrossRefGoogle ScholarPubMed
Lapierre, H, Bernier, JF, Dubreuil, P, Reynolds, CK, Farmer, C, Ouellet, DR & Lobley, GE (2000) The effect of feed intake level on splanchnic metabolism in growing beef steers. Journal of Animal Science 78, 1084–1099.CrossRefGoogle ScholarPubMed
McLean, JA (1986) The significance of carbon dioxide and methane measurements in the estimation of heat production in cattle. British Journal of Nutrition 55, 631–633.CrossRefGoogle ScholarPubMed
Milano, GD, Hotston-Moore, A & Lobley, GE (2000) Influence of hepatic ammonia removal on ureagenesis, amino acid utilization and energy metabolism in the ovine liver. British Journal of Nutrition 83, 307–315.CrossRefGoogle ScholarPubMed
Moloney, AP (1998) Growth and carcass composition in sheep offered isoenergetic rations which resulted in different concentrations of ruminal metabolites. Livestock Production Science 56, 157–164.CrossRefGoogle Scholar
Morand, C, Redon, C, Remesy, C & Demigné, C (1990) Non-hormonal and hormonal control of glycogen metabolism in isolated sheep liver cells. International Journal of Biochemistry 22, 873–881.CrossRefGoogle ScholarPubMed
Ndi Bualonji, BB & Godeau, JM (1993) La néoglucogenèse et les acides aminés chez les ruminants: revue (Gluconeogenesis and amino acids in ruminants: a review). Annales Médicales Vétérinaires 137, 537–554.Google Scholar
Ortigues, I, Durand, D & Lefaivre, J (1994) Use of para-amino hippuric acid to measure blood flows through portal-drained-viscera, liver and hindquarters in sheep. Journal of Agricultural Science, Cambridge 122, 299–308.CrossRefGoogle Scholar
Patil, AR, Goetsch, AL, Park, KK, Kouakou, B, Galloway, DL & Johnson, ZB (1996) Influence of grass source and legume level on net flux of nutrients across splanchnic tissues in sheep. Small Ruminant Research 22, 111–122.CrossRefGoogle Scholar
Pethick, DW (1993) Carbohydrate and lipid oxidation during exercise. Australian Journal of Agricultural Research 44, 431–441.CrossRefGoogle Scholar
Pethick, DW & Dunshea, FR (1997) The partitioning of fat in farm animals. Proceedings of the Nutrition Society of Australia 20, 3–13.Google Scholar
Prior, RL, Huntington, GB & Reynolds, PJ (1984) Role of insulin and glucose on metabolite uptake by the hind half of beef steers. Journal of Animal Science 58, 1446–1453.CrossRefGoogle ScholarPubMed
Prior, RL & Scott, RA (1980) Effects of intravenous infusions of glucose, lactate, propionate or acetate on the induction of lipogenesis in bovine adipose tissue. Journal of Nutrition 110, 2011–2019.CrossRefGoogle ScholarPubMed
Rémond, D, Ortigues, I & Jouany, JP (1995) Energy substrates for the rumen epithelium. Proceedings of the Nutrition Society 54, 95–105.CrossRefGoogle ScholarPubMed
Reynolds, CK, Harmon, DL, Prior, RL & Tyrrell, HF (1994) Effects of mesenteric vein L-alanine infusion on liver metabolism of organic acids by beef heifers fed diets differing in forage: concentrate ratio. Journal of Animal Science 72, 3196–3206.CrossRefGoogle ScholarPubMed
Reynolds, PJ, Huntington, GB & Reynolds, CK (1986) Determination of volatile fatty acids, lactate and B-hydroxybutyrate in blood by ion exchange cleanup and gas chromatography. Journal of Animal Science 63, 424 AbstrGoogle Scholar
Sano, H, Matsunobu, S, Abe, T & Terashima, Y (1992) Combined effects of diet and cold exposure on insulin responsiveness to glucose and tissue responsiveness to insulin in sheep. Journal of Animal Science 70, 3514–3520.CrossRefGoogle ScholarPubMed
Sano, H, Narahara, S, Kondo, T, Takahashi, A & Terashima, Y (1993) Insulin responsiveness to glucose and tissue responsiveness to insulin during lactation in dairy cows. Domestic Animal Endocrinology 10, 191–197.CrossRefGoogle ScholarPubMed
Sano, H & Teashima, Y (1998) The effect of supplemental propionate on insulin responsiveness to glucose and tissue responsiveness to insulin in relation to feeding in sheep. Reproduction Nutrition Development 38, 81–91.CrossRefGoogle ScholarPubMed
Scollan, ND & Jessop, NS (1995) Diet-induced variation in acetate metabolism of ovine perirenal adipose tissue in vitro. Journal of Agricultural Science, Cambridge 125, 429–436.CrossRefGoogle Scholar
Seal, CJ & Parker, DS (1994) Effect of intraruminal propionic acid infusion on metabolism of mesenteric and portal-drained viscera in growing steers fed a forage diet: I. Volatile fatty acids, glucose and lactate. Journal of Animal Science 72, 1325–1334.CrossRefGoogle ScholarPubMed
Seal, CJ, Parker, DS & Avery, DJ (1992) The effect of forage and forage-concentrate diets on rumen fermentation and metabolism of nutrients by the mesenteric and portal-drained viscera in growing steers. British Journal of Nutrition 67, 335–370.CrossRefGoogle ScholarPubMed
Seal, CJ & Reynolds, CK (1993) Nutritional implications of gastrointestinal and liver metabolism in ruminants. Nutrition Research Reviews 6, 185–208.CrossRefGoogle ScholarPubMed
Sharp, WM, Johnson, RR & Owens, FN (1982) Ruminal VFA production with steers fed whole or ground corn grain. Journal of Animal Science 55, 1505–1514.CrossRefGoogle ScholarPubMed
Smith, BS & Crouse, JD (1984) Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. Journal of Nutrition 114, 792–800.CrossRefGoogle ScholarPubMed
Sutton, JD, Hart, IC, Broster, WH, Elliott, RJ & Schuller, E (1986) Feeding frequency for lactating cows: effects on rumen fermentation and blood metabolites and hormones. British Journal of Nutrition 56, 181–192.CrossRefGoogle ScholarPubMed
Tucker, A (1967) Method for oxygen content and dissociation curves on microliter blood samples. Journal of Applied Physiology 23, 410–414.CrossRefGoogle ScholarPubMed
Van Eenaeme, C, Bienfait, JM, Lambot, O & Pondant, A (1969) Determination automatique de l'ammoniaque dans le liquide du rumen par la méthode de Berthelot adaptée à l'autoanalyseur (Automatic determination of ammonia in rumen liquid using the Berthelot method adapted for the autoanalyser). Annales Médicales et Vétérinaires 7, 419–425.Google Scholar
Veenhuizen, J, Russell, RW & Young, JW (1988) Kinetics of metabolism of glucose, propionate and CO2 in steers as affected by injecting phlorizin and feeding propionate. Journal of Nutrition 118, 1366–1375.CrossRefGoogle ScholarPubMed
Watford, M, Lane, SF & Douglas, EG (1987) The synthesis of glucose and ammonia by kidney tubules isolated from suckling and early-weaned lambs. Comparative Biochemistry and Physiology 86B 689–691.Google Scholar
Williamson, DH, Mellanby, J & Krebs, A (1962) Enzymatic Determination of D-(–)-3-Hydroxybutyric acid and acetoacetic acid in blood. Biochemistry Journal 82, 90–96.CrossRefGoogle Scholar
Xie, H & Lautt, WW (1996) Insulin resistance of skeletal muscle produced by hepatic parasympathetic interruption. American Journal of Physiology 270, E858–E863.Google ScholarPubMed