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Effects of intraruminal propionate supplementation on nitrogen utilisation by the portal-drained viscera, the liver and the hindlimb in lambs fed frozen rye grass

Published online by Cambridge University Press:  09 March 2007

Isabelle C. Savary-Auzeloux ,
Linda Majdoub ,
Nathalie LeFloc'h  and
Isabelle Ortigues-Marty
Isabelle C. Savary-Auzeloux*
Affiliation:
Unité de Recherche sur les Herbivores, Equipe Nutriments et Métabolismes, INRA Clermont Ferrand-Theix, 63122 St Genès Champanelle, France
Linda Majdoub
Affiliation:
Unité de Recherche sur les Herbivores, Equipe Nutriments et Métabolismes, INRA Clermont Ferrand-Theix, 63122 St Genès Champanelle, France
Nathalie LeFloc'h
Affiliation:
Unité Mixte de Recherche sur le Veau et le Porc, INRA-ENSAR St Gilles, 35590 St Gilles, France
Isabelle Ortigues-Marty
Affiliation:
Unité de Recherche sur les Herbivores, Equipe Nutriments et Métabolismes, INRA Clermont Ferrand-Theix, 63122 St Genès Champanelle, France
*
*Corresponding author: Dr Isabelle Savary-Auzeloux, fax +33 4 73 62 46 39, email [email protected]
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Abstract

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The influence of propionate supplementation on the splanchnic metabolism of amino acids (AA) and other N compounds (urea-N and NH3-N) and the supply of AA and NH3-N to the hindlimb was investigated in growing lambs. Six rumen-cannulated and multicatheterised lambs (32·2kg) were fed frozen rye grass at 690kJ metabolisable energy intake/d per kg average metabolic body weight. They were infused intraruminally with a salt solution (control) or with propionate solutions at 0·23mol/l (P1) or 0·41mol/l (P2) infused at a maximal rate of 1·68 (sd 0·057) ml/min according to a repeated Latin square design. The propionate infusion did not increase the net portal appearance of total AA (TAA)-N but increased that of some branched-chain AA (valine and to a lesser extent isoleucine). Simultaneously, the propionate treatment (especially P2) induced an increased TAA utilisation by the liver. This was due mainly to an increased (+79%; P<0·07) utilisation of the essential AA and particularly the branched-chain AA. A stimulation of protein synthesis in the liver is hypothesised since (1) propionate stimulated insulin secretion and (2) utilisation of non-essential AA were less influenced by the propionate treatment in the liver (except for alanine), suggesting that the AA utilised by the liver were directed towards protein synthesis rather than towards oxidation or urea synthesis. At the splanchnic level, the propionate treatment did not have any effect on the TAA, non-essential AA and essential AA, except for a net splanchnic release that was decreased for leucine (P<0·02) and methionine (P<0·01) and increased for threonine (P<0·05). The propionate treatment did not have any effect on the hindlimb uptake of AA (essential and non-essential). As a consequence, even though the propionate treatment induced some major alterations in the splanchnic metabolism of AA, there were no changes in the net AA balance in the hindlimb (and hence probably on muscle growth). The role of the splanchnic tissues in the regulation of the AA supply to the peripheral tissues (such as muscle) therefore appears to be prominent in the regulation of muscle growth. Whether the peripheral tissues regulate their own supply by interacting with the splanchnic tissues (and especially the liver) or the liver is the only regulator of the AA supply to the muscle remains in doubt.

Keywords

PropionateSplanchnic tissuesHindlimbAmino acidsNet flux
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 5 , November 2003 , pp. 939 - 952
Copyright
Copyright © The Nutrition Society 2003

References

Abdul-Razzaq, HA & Bickerstaffe, R (1989) The influence of rumen volatile fatty acids on protein metabolism in growing lambs. Br j Nutr 62, 297–310.CrossRefGoogle ScholarPubMed
Ahlman, B, Charlton, M, Fu, A, Berg, CO'Brien, P & Nair, KS (2001) Insulin's effect on synthesis rates of liver proteins. Diabetes 50, 947–954.CrossRefGoogle ScholarPubMed
Backwell, FRC, Hipolito-Reis, M, Wilson, D, Bruce, LA, Buchan, V & MacRae, JC (1997) Quantification of circulating peptides and assessment of peptide uptake across the gastrointestinal tract of sheep. J Anim Sci 75, 3315–3322.CrossRefGoogle ScholarPubMed
Balcells, J, Seal, CJ & Parker, DS (1995) Effect of intravenous glucose infusion on metabolism of portal-drained viscera in sheep fed a cereal/straw-based diet. J Anim Sci 73, 2146–2155.CrossRefGoogle ScholarPubMed
Baldwin, RL (1999) The proliferative actions of insulin, insulin-like growth factor-I, epidermal growth factor, butyrate and propionate on ruminal epithelial cells in vitro. Small Rumin Res 32, 261–268.CrossRefGoogle Scholar
Barle, H, Nyberg, B & Essen, P et al. (1997) The synthesis rates of total liver protein and plasma albumin determined simultaneously in vivo in humans. Hepatology 25, 154–158.Google 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, Dobson, e, editors]. Englewood Cliffs, NJ: Prentice Hall.Google Scholar
Bergmeyer, HU (1985) Ammonia determination. In Methods of Enzymatic Analysis, vol.8, p. 454 [Bergmeyer, HU, Bergmeyer, j and Grassl, M, editors]. London: Academic PressGoogle Scholar
Berthelot, M (1859) Violet d'aniline (Aniline violet). Répertoire de Chimie Appliquée 1, 284Google Scholar
Biolo, G, Tessari, P, Inchiostro, Set al. (1992) Leucine and phenylalanine kinetics during mixed meal ingestion: a multiple tracer approach. Am J Physiol 262, E455–E463.Google ScholarPubMed
Bruckental, I, Huntington, GB, Baer, CK & Erdman, RA (1997) The effect of abomasal infusion of casein and recombinant somatotropin hormone injection on nitrogen balance and amino acid fluxes in portal-drained viscera and net hepatic and total splanchnic blood in Holstein steers. J Anim Sci 75, 1119–1129.CrossRefGoogle ScholarPubMed
Cappelli, FP, Seal, CJ & Parker, DS (1997) Glucose and [13C]leucine metabolism by the portal-drained viscera of sheep fed on dried grass with acute intravenous and intraduodenal infusions of glucose. Br J Nutr 78, 931–946.CrossRefGoogle ScholarPubMed
Casse, EA, Rulquin, H & Huntington, GB (1994) Effect of mesenteric vein infusion of propionate on splanchnic metabolism in primiparous holstein cows. J Dairy Sci 77, 3296–3303.CrossRefGoogle ScholarPubMed
Chiku, K, Mochida, M, Yamamoto, M & Natori, Y (1993) Amino acids suppress intracellular protein degradation in rat liver during parenteral nutrition. J Nutr 123, 1771–1776.CrossRefGoogle ScholarPubMed
Connell, A, Calder, AG, Anderson, SE & Lobley, GE (1997) Hepatic protein synthesis in the sheep: effect of intake as monitored by use of stable-isotope-labelled glycine, leucine and phenylalanine. Br J Nutr 77, 255–271.CrossRefGoogle ScholarPubMed
De Feo, P, Gaisano, MG & Haymond, MW (1991) Differential effects of insulin deficiency on albumin and fibrinogen synthesis in humans. J Clin Invest 88, 833–840.CrossRefGoogle ScholarPubMed
Demigné, C, Yacoub, C, Morand, C & Rémésy, C (1991) Interactions between propionate and amino acid metabolism in isolated sheep hepatocytes. Br J Nutr 65, 301–317.CrossRefGoogle ScholarPubMed
DeVisser, 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. J Dairy Sci 80, 1666–1673.CrossRefGoogle Scholar
Eskeland, B, Pfander, WH & Preston, RL (1973) Utilisation of volatile fatty acids and glucose for protein deposition in lambs. Br J Nutr 29, 347–355.CrossRefGoogle ScholarPubMed
Eskeland, B, Pfander, WH & Preston, RL (1974) Intravenous energy infusion in lambs: effects on nitrogen retention, plasma free amino acids and plasma urea nitrogen. Br J Nutr 31, 201–211.CrossRefGoogle ScholarPubMed
Ferrel, CL, Freetly, HC, Goetsch, AL & Kreikemeier, KK (2001) The effect of dietary nitrogen and protein on feed intake, nutrient digestibility and nitrogen flux across the portal-drained viscera and liver of sheep consuming high-concentrate diets ad libitum. J Anim Sci 79, 1322–1328.CrossRefGoogle Scholar
Garwacki, S, Wiechetek, M, Karlik, W, Souffrant, WB & Krawielitzki, K (1990) Effect of propionate on the utilization of nitrogen from 15 NH 4 Cl for urea synthesis in hepatocytes isolated from sheep liver. Int J Biochem 22, 1185–1188.CrossRefGoogle Scholar
Gate, JJ, Parker, DS & Lobley, GE (1999) The metabolic fate of the amino-N group of glutamine in the tissues of the gastrointestinal tract in 24 h-fasted sheep. Br J Nutr 81, 297–306.CrossRefGoogle Scholar
Grizard, J, Dardevet, D & Papet, I (1995) Nutrient regulation of skeletal muscle protein metabolism in animals. The involvement of hormones and substrates. Nutr Res Rev 8, 67–91.CrossRefGoogle ScholarPubMed
Harmon, DL (1992) Impact of nutrition on pancreatic exocrine and endocrine secretion in ruminants: a review. J Anim Sci 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. J Anim Sci 65, 1610–1616.CrossRefGoogle ScholarPubMed
Hovell, FD & Greenhalgh, JFD (1978) The utilization of diets containing acetate, propionate or butyrate salts by growing lambs. Br J Nutr 40, 171–183.CrossRefGoogle ScholarPubMed
Hristov, AN (1998) Nitrogen fractions and in sacco dry matter and crude protein degradability of fresh and frozen alfalfa. Anim Feed Sci Technol 71, 351–355.CrossRefGoogle Scholar
Huhtanen, PJ, Blauwiekel, R & Saastamoinen, I (1998) Effects of intraruminal infusions of propionate and butyrate with two different protein supplements on milk production and blood metabolites in dairy cows receiving grass silage-based diet. J Sci Food Agric 77, 213–222.3.0.CO;2-6>CrossRefGoogle Scholar
Huntington, GB, Varga, GA, Glenn, BP & Waldo, DR (1988) Net absorption and oxygen consumption by Holstein steers fed alfalfa or orchardgrass silage at two equalized intakes. J Anim Sci 66, 1292–1302.CrossRefGoogle ScholarPubMed
Huntington, GB, Zetina, EJ, Whitt, JM & Potts, W (1996) Effects of dietary concentrate level on nutrient absorption, liver metabolism, and urea kinetics of beef steers fed isonitrogenous and isoenergetic diets. J Anim Sci 74, 908–916.CrossRefGoogle ScholarPubMed
Institut National de Recherches Agronomiques (1978) Alimentation des Ruminants (The Feeding of Ruminants) [Jarrige, R, editor]. Versailles, France: INRA PublicationsGoogle Scholar
Journet, M, Huntington, G & Peyraud, JL (1995) Le bilan des produits terminaux de la digestion (The assessment of the terminal products of digestion). In Nutrition des Ruminants Domestiques, Ingestion et Digestion, pp. 26–71 [Jarrige, R, Ruckebush, Y, Demarquilly, C, Farce, MH, Journet, M, editors]. Paris, France: INRA.Google Scholar
Katz, ML & Bergman, EN (1969) A method for simultaneous cannulation of the major splanchnic blood vessels of the sheep. Am J Vet Res 30, 655–660.Google ScholarPubMed
Kelly, JM, Park, H, Summers, M & Milligan, LP (1993) Interactions between protein and energy metabolism. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 341–362 [Forbes, JM and France, J, editors]. Cambridge, MA: CAB International.Google Scholar
Kim, H-S, Choung, JJ, Chamberlain, D & Lobley, GE (1999) Effect of propionate on ovine urea kinetics. In Proceedings of the VIIIth International Symposium on Protein Metabolism and Nutrition, p. 57 [Lobley, GE, White, A and MacRae, JC, editors]. Wageningen, The Netherlands Wageningen Press.Google Scholar
Koeln, LL, Schlagheck, TG & Webb, KE (1993) Amino acid flux across the gastrointestinal tract and liver of calves. J Dairy Sci 76, 2275–2285.CrossRefGoogle ScholarPubMed
Kristensen, NB, Pierzynowski, SG & Danfaer, A (2000) Net portal appearance of volatile fatty acids in sheep intraruminally infused with mixtures of acetate, propionate, isobutyrate, butyrate and valerate. J Anim Sci 78, 1372–1379.CrossRefGoogle ScholarPubMed
Lapierre, H, Bernier, JF & Dubreuil, P (2000) The effect of feed intake level on splanchnic metabolism in growing beef steers. J Anim Sci 78, 1084–1099.CrossRefGoogle ScholarPubMed
Lapierre, H, Blouin, JP, Lobley, GE, Reynolds, CK, Dubreuil, P & Bernier, JF (1997) Effect of protein degradability on protein splanchnic metabolism in dairy cows. Proc Nutr Soc 56 162A.Google Scholar
Lapierre, H & Lobley, GE (2001) Nitrogen recycling in the ruminant: a review. J Dairy Sci 84, E223–E236.CrossRefGoogle Scholar
Lien, KA, Sauer, WC & Fenton, M (1997) Mucin output in ileal digesta of pigs fed a protein free diet. Z Ernahrungswiss 36, 182–190.CrossRefGoogle ScholarPubMed
Lobley, GE (1994) Amino acid and protein metabolism in the whole body and individual tissues of ruminant. In Principles of Protein Nutrition of Ruminants, pp. 147–178 [Asplund, JM, editor]. London: CRC Press.Google Scholar
Lobley, GE, Connell, A, Revell, DK, Bequette, BJ, Brown, DS & Calder, AG, (1996b) Splanchnic-bed transfers of amino acids in sheep blood and plasma, as monitored through use of a multiple U- 13 C-labelled amino acid mixture. Br J Nutr 75, 217–235.CrossRefGoogle Scholar
Lobley, GE, Hoskin, SO & McNeil, CJ (2001) Glutamine in animal science and production. J Nutr 131, 2525S–2531S.CrossRefGoogle ScholarPubMed
Lobley, GE, Milano, GD & Van der Walt, JG (1999) The liver: integrator of nitrogen metabolism. IXth International Symposium on Ruminant Physiology, Pretoria, South Africa, pp. 149–168 [Cronje, PJ, editor]. Wallingford, Oxon CABIGoogle Scholar
Lobley, GE, Weijs, PJM, Connell, A, Calder, AG, Brown, DS & Milne, E (1996a) The fate of absorbed and exogenous ammonia as influenced by forage or forage-concentrate diets in growing sheep. Br J Nutr 76, 231–248.CrossRefGoogle ScholarPubMed
MacRae, JCCambell, DR & Eadie, J (1975) Changes in biochemical composition of herbage upon freezing and thawing. J Agric Sci Camb 84, 125–131.CrossRefGoogle Scholar
Majdoub, L, Savary, I, Bayle, G, Grizard, J, Vermorel, M & Ortigues-Marty, I (1999) Répartition des nutriments azotés et des dépenses énergétiques entre le tube digestif, le foie et les muscles chez des agneaux recevant du ray-grass, stade pâturage (Distribution of nitrogenised nutrients and energy expenditure between the digestive tract, the liver and muscles in lambs receiving rye-grass, at the pasture stage). In Rencontres Recherches Ruminant 6th ed., pp. 119–122.Google Scholar
Majdoub, L, Vermorel, M & Ortigues-Marty, I (2003) Intraruminal propionate supplementation modifies hindlimb energy metabolism without changing the splanchnic release of glucose in growing lambs. Br J Nutr 89, 39–50.CrossRefGoogle ScholarPubMed
Meijer, AJ, Blommaart, EFC, Dubbelhuis, PF & Van Sluijters, DA (1999) Regulation of hepatic nitrogen metabolism. In Proceedings of the VIIIth International Symposium on Protein Metabolism and Nutrition, pp. 155–175 [Lobley, GE, White, A and MacRae, JC, editors]. Wageningen, The Netherlands: Wageningen Press.Google Scholar
Milano, GD, Holston-Moore, A & Lobley, GE (2000) Influence of hepatic ammonia removal on ureagenesis, amino acid utilization and energy metabolism in the ovine liver. Br J Nutr 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. Livest Prod Sci 56, 157–164.CrossRefGoogle Scholar
Mukkur, TK, Watson, DL, Saini, S & Lascelles, AK (1985) Purification and characterization of goblet-cell mucin of high Mr from the small intestine of sheep. Biochem J 229, 419–428.CrossRefGoogle ScholarPubMed
Mutsvangwa, T, Buchanan-Smith, JG & McBride, BW (1997) Effects of ruminally degradable nitrogen intake and in vitro addition of ammonia and propionate on the metabolic fate of L-[1-14C]alanine and L-[15N]lysine in isolated sheep hepatocytes. J Anim Sci 75, 1149–1159.CrossRefGoogle Scholar
Newsholme, EA & Carrie, AL (1994) Quantitative aspects of glucose and glutamine metabolism by intestinal cells. Gut 35, S13–S17.CrossRefGoogle ScholarPubMed
Norton, BW, Janes, AN & Armstrong, DG (1982) The effects of intraruminal infusions of sodium bicarbonate, ammonium chloride and sodium butyrate on urea metabolism in sheep. Br J Nutr 48, 265–274.CrossRefGoogle ScholarPubMed
Nozière, P, Martin, CRémond, D, Kristensen, NB, Bernard, R & Doreau, M (2000) Effect of composition of ruminally-infused short-chain fatty acids on net fluxes of nutrients across portal-drained viscera in underfed ewes. Br J Nutr 83, 521–531.CrossRefGoogle ScholarPubMed
Nozière, P, Rémond, D, Ferlay, A & Doreau, M (1998) Differences between blood and plasma concentrations of acetate, β-hydroxybutyrate, glucose, ammonia and urea: implications for measurement of portal net fluxes in ewes. Reprod Nutr Dev 38, 509–518.CrossRefGoogle ScholarPubMed
Obitsu, T, Bremner, D, Milne, E & Lobley, GE (2000) Effect of abomasal glucose infusion on alanine metabolism and urea production in sheep. Br J Nutr 84, 157–163.CrossRefGoogle ScholarPubMed
Ørskov, ER, Meehan, DE, MacLeod, NA & Kyle, DJ (1999) Effect of glucose supply on fasting nitrogen excretion and effect of level and type of volatile fatty acid infusion on response to protein infusion in cattle. Br J Nutr 81, 389–393.CrossRefGoogle ScholarPubMed
Ortigues, I & Doreau, M (1995) Responses of the splanchnic tissues of ruminants to changes in intake: absorption of digestion end products, tissue mass, metabolic activity and implications to whole animal energy metabolism. Ann Zootech 44, 321–346.CrossRefGoogle Scholar
Ortigues, I & Durand, D (1995) Adaptation of energy metabolism to undernutrition in ewes. Contribution of portal-drained viscera, liver and hindquarters. Br J Nutr 73, 209–226.CrossRefGoogle ScholarPubMed
Reeds, PJ & Burrin, DG (2001) Glutamine and the bowel. J Nutr 131, 2505S–2508S.CrossRefGoogle Scholar
Reeds, PJ, Burrin, DG, Stoll, B & Jahoor, F (2000) Intestinal glutamate metabolism. J Nutr 130, 978S–982S.CrossRefGoogle ScholarPubMed
Reeds, PJ, Burrin, DG, Stoll, B & Van Goudoever, JB (1999) Consequences and regulation of gut metabolism. In Proceedings of the VIIIth International Symposium on Protein Metabolism and Nutrition, pp. 127–153 [Lobley, GE, White, A and MacRae, JC, editors]. Wageningen, The NetherlandsWageningen Press.Google Scholar
Rémond, D, Bernard, L & Poncet, C (2000a) Amino acid flux in ruminal and gastric veins and sheep, effects of ruminal and omasal injections of free amino acids and carnosine. J Anim Sci 78, 158–166.CrossRefGoogle ScholarPubMed
Rémond, D, Bernard, L & Poncet, C (2000b) Free and peptide amino acid net flux across the rumen and the mesenteric- and portal-drained viscera of sheep. J Anim Sci 78, 1960–1972.CrossRefGoogle ScholarPubMed
Rémond, D, Meschy, F & Boivin, R (1996) Metabolites, water and mineral exchanges across the rumen wall: mechanisms and regulation. Ann Zootech 45, 97–119.CrossRefGoogle Scholar
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. J Anim Sci 72, 3196–3206.CrossRefGoogle ScholarPubMed
Reynolds, CK, Tyrrell, HF & Reynolds, PJ (1991) Effect of diet forage-to-concentrate ratio and intake on energy metabolism in growing beef steers: net nutrient metabolism by visceral tissues. J Nutr 121, 1004–1015.CrossRefGoogle Scholar
Sakata, T & Tamate, H (1978) Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. J Dairy Sci 61, 1109–1113.CrossRefGoogle ScholarPubMed
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. J Anim Sci 72, 1325–1334.CrossRefGoogle ScholarPubMed
Seal, CJ & Parker, DS (1996) Effect of intraruminal propionic acid infusion on metabolism of mesenteric- and portal-drained viscera in growing steers fed a forage diet: II. Ammonia, urea, amino acids and peptides. J Anim Sci 74, 245–256.CrossRefGoogle ScholarPubMed
Seal, CJ, Parker, DS, Balcells, J & Mole, JL (1993) Nitrogen digestion in forage-fed sheep with and without intraruminal propionate infusion. J Agric Sci Camb 120, 107–114.CrossRefGoogle Scholar
Stewart, PM & Walser, M (1980) Failure of the normal ureagenic response to amino acids in organic acid-loaded rats. Proposed mechanism for the hyperammonemia of propionic and methylmalonic acidemia. J Clin Invest 66, 484–492.CrossRefGoogle ScholarPubMed
Storm, E, Ørskov, ER (1983) The nutritive value of rumen micro-organisms in ruminants. Br J Nutr 50, 463–470.CrossRefGoogle ScholarPubMed
Theurer, CB, Huntington, GB, Huber, JT, Swingle, RS & Moore, JA (2002) Net absorption and utilization of nitrogenous compounds across ruminal, intestinal, and hepatic tissues of growing beef steers fed dry-rolled or steam flaked sorghum grain. J Anim Sci 80, 525–532.CrossRefGoogle ScholarPubMed
Van der Walt, JG (1993) Nitrogen metabolism in ruminant liver. Aust J Agric Res 44, 381–403.CrossRefGoogle Scholar
Webb, KE Jr (1999) Tissue, cellular and molecular aspects of peptide absorption and utilization. IXth International Symposium on Ruminant Physiology, Pretoria, South Africa, pp. 117–130 [Cronje, PJ, editor]. Wallingford, Oxon: CABI.Google Scholar
Windmueller, HG (1982) Glutamine utilization by the small intestine. Adv Enzymol Relat Areas Mol Biol 53, 201–237.Google ScholarPubMed