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Digestion and nutrient net fluxes across the rumen, and the mesenteric- and portal-drained viscera in sheep fed with fresh forage twice daily: net balance and dynamic aspects

Published online by Cambridge University Press:  09 March 2007

Didier Rémond*
Affiliation:
Unité Nutrition et Métabolisme Protéique, Institut National de la Recherche Agronomique de Clermont-Ferrand, 63 122 St Genès-Champanelle, France
Laurence Bernard
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique de Clermont-Ferrand, 63 122 St Genès-Champanelle, France
Béatrice Chauveau
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique de Clermont-Ferrand, 63 122 St Genès-Champanelle, France
Pierre Nozière
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique de Clermont-Ferrand, 63 122 St Genès-Champanelle, France
Claude Poncet
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique de Clermont-Ferrand, 63 122 St Genès-Champanelle, France
*
*Corresponding Author: Dr Didier Rémond, fax +33 4 73 62 47 55, email dremond@clermont.inra.fr
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Abstract

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Digestion and portal net flux of nutrients were studied in sheep fed twice daily with fresh orchard-grass. Digestive flows were measured in six fistulated sheep using the double-marker technique. Three sheep were fitted with catheters and blood-flow probes, allowing nutrient net flux measurements across the portal-drained viscera (PDV), the mesenteric-drained viscera (MDV) and the rumen. Total tract apparent digestion of N was similar to portal net appearance of N, calculated as the sum of free amino acids (FAA), peptide amino acids (PAA), NH3, and urea net fluxes. PAA accounted for 25 % of non-protein amino acid net release across the PDV. With the exception of glycine and glutamate, the small intestine was the main contributor to this PAA net release. The essential amino acid (EAA) apparent disappearance between the duodenum and the ileum was lower than the net appearance of EAA (FAA + PAA) across the MDV. The value of PDV:MDV flux of free EAA was, on average, 78 %. The rumen accounted for 30 % of the net uptake of EAA by the PDV tissues not drained by the mesenteric vein. Rumen net release of acetate, propionate, butyrate, 3-hydroxybutyrate, and lactate accounted for 70, 55, 46, 77 and 52 %, respectively, of their portal net releases. Conversely, the small intestine was a net consumer of arterial acetate and 3-hydroxybutyrate. Dynamic study of nutrient net fluxes across the PDV showed that throughout a feeding cycle, the liver faced a constant flux of amino acids (AA), whereas volatile fatty acid and NH3 net fluxes varied in response to the meal. The present study specified, in forage-fed sheep, the partitioning of nutrient net fluxes across the PDV and the role of peptides in portal net release of AA.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

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. Journal of Animal Sciences 75 33153322.CrossRefGoogle ScholarPubMed
Balcells, J, Deal, CJ & Parker, DS (1995) Effect of intravenous glucose infusion on metabolism of the portal-drained viscera in sheep fed a cereal/straw-based diet. Journal of Animal Science 73 21462155.CrossRefGoogle ScholarPubMed
Barnes, RJ, Comline, RS & Dobson, A (1983) Changes in the blood flow to the digestive organs of the sheep induced by feeding. Quarterly Journal of Experimental Physiology 68 7788.CrossRefGoogle Scholar
Bergman, EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70 567590.CrossRefGoogle ScholarPubMed
Bernard, L, Backwell, CFR, Rémond, D, Wilson, D, Bruce, LA, Buchan, V & MacRae, JC (2002) Effect of the methodology on circulating peptides determination and consequences on net flux measurements across the gastrointestinal tract of sheep. Archives of Animal Nutrition 56 1321.Google ScholarPubMed
Bernard, L, Chauveau, B & Rémond, D (2001) Effect of methodology on peptide amino acid concentrations in blood and plasma of sheep. Archives of Animal Nutrition 54 281296.Google ScholarPubMed
Berthiaume, R, Dubreuil, P, Stevenson, M, McBride, BW & Lapierre, H (2001) Intestinal disappearance and mesenteric and portal appearance of amino acids in dairy cows fed ruminally protected methionine. Journal of Dairy Science 84 194203.CrossRefGoogle ScholarPubMed
Caton, JS, Reynolds, CK, Bequett, BJ, Lupoli, B, Aikman, PC & Humphries, DJ (2001) Effect of abomasal casein or essential amino acids infusion on splanchnic leucine and phenylalanine metabolism in lactating dairy cows. Journal of Animal Science 79, Suppl. 1, 363.Google Scholar
Early, RJ, Thompson, JR, Christopherson, RJ & Sedgwich, GW (1987) Blood branched-chain amino and α-keto acid concentrations and net exchange across the portal-drained viscera and hindlimb of fed and fasted ruminants. Canadian Journal of Animal Science 67 10111020.CrossRefGoogle Scholar
Faichney, GJ (1980) The use of markers to measure digesta flow from the stomach of sheep fed once daily. Journal of Agricultural Science (Cambridge) 94 313318.CrossRefGoogle Scholar
Gabel, M & Poppe, S (1986) Untersuchungen zum protein und aminosäurenumsatz im verdauungstrakt bei wachenden jungbullen. 5. Fluss von Aminosäuren ins duodenum (Investigations into protein and amino acid conversion in the digestive tract with conscious young bulls. 5. Flow of amino acids in the duodenum). Archiv für Tierernahrung, Berlin 36 420454.Google Scholar
Gate, JJ, Parker, DS & Lobley, GE (1999) The metabolic fate of the amido-N group of glutamine in the tissues of the gastrointestinal tract in 24 h-fasted sheep. British Journal of Nutrition 81 297306.CrossRefGoogle ScholarPubMed
Hamza, AN (1976) The rate of secretion by sheep pancreas and the amino acid composition of the pancreatic juice. Nutrition Reports International 14 7987.Google Scholar
Han, XT, Nozière, P, Rémond, D, Chabrot, J & Doreau, M (2002) Respective effects of nutrient supply and dietary bulk on O2 uptake and nutrient net fluxes across rumen, mesenteric- and portal-drained viscera in ewes. Journal of Animal Science 80 13621375.CrossRefGoogle Scholar
Han, XT, Xue, B, Hu, LH & Du, JZ (2001) Effect of dietary protein degradability on net fluxes of free and peptide amino acids across the portal-drained viscera of steers. Journal of Agricultural Science, Cambridge 137 471481.CrossRefGoogle Scholar
Heitmann, RN & Bergman, EN (1978) Glutamine metabolism, interorgan transport, and glucogenicity in the sheep. American Journal of Physiology 234 E197E203.Google ScholarPubMed
Kennedy, PM & Milligan, LP (1980) Input of endogenous protein into the forestomachs of sheep. Canadian Journal of Animal Science 60 10291032.CrossRefGoogle Scholar
Koeln, LL, Schlagheck, TG & Webb, KE (1993) Amino acid flux across the gastrointestinal tract and liver of calves. Journal of Dairy Science 76 22752285.CrossRefGoogle ScholarPubMed
Kowalik, B, Kowalczyk, J, Pajak, JJ, Zebrowska, T & Dlugolecka, Z (2001). The influence of dietary starch level and type on the activity of pancreatic digestive enzymes in sheep. Journal of Animal Feed Science 10 5763.CrossRefGoogle Scholar
Kristensen, NB, Danfaer, A & Agergaard, N (1996) Diurnal patterns of ruminal concentrations and portal appearance rates of short-chain fatty acids in sheep fed a hay or a concentrate/straw diet in two meals daily. Acta Agriculturae Scandinavica 46A 227238.CrossRefGoogle Scholar
Kristensen, NB, Gabel, G, Pierzynowski, SG & Danfaer, A (2000 a) Portal recovery of short-chain fatty acids infused into the temporarily-isolated and washed reticulo-rumen of sheep. British Journal of Nutrition 84 477482.CrossRefGoogle ScholarPubMed
Kristensen, NB, Pierzynowski, SG & Danfaer, A (2000 b) Portal-drained visceral metabolism of 3-hydroxybutyrate in sheep. Journal of Animal Science 78 22232228.CrossRefGoogle ScholarPubMed
Lindsay, DB (1993) Metabolism of the portal drained viscera. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 267289 [Forbes, JM and France, J, editors]. Wallingford, Oxon: CAB International.Google Scholar
Lobley, G, Connell, A, Lomax, MA, Brown, DS, Milne, E, Calder, AG & Farningham, DAH (1995) Hepatic detoxification of ammonia in the ovine liver: possible consequences for amino acid catabolism. British Journal of Nutrition 73 667685.CrossRefGoogle ScholarPubMed
MacRae, JC, Bruce, LA, Brown, DS & Calder, G (1997 a) Amino acid use by the gastrointestinal tract of sheep given lucerne forage. American Journal of Physiology 273 G1200G1207.Google ScholarPubMed
MacRae, JC, Bruce, LA, Brown, DS, Farningham, DAH & Franklin, M (1997 b) Absorption of amino acids from the intestine and their net flux across the mesenteric- and portal-drained viscera in lambs. Journal of Animal Science 75 33073314.CrossRefGoogle ScholarPubMed
Milano, GD & Lobley, GE (2001) Liver nitrogen movements during short-term infusion of high levels of ammonia into the mesenteric vein of sheep. British Journal of Nutrition 86 507513.CrossRefGoogle ScholarPubMed
Neutze, SA, Oddy, VH & Gooden, JM (1994) A cranial mesenteric vein preparation for measurement of amino acid uptake by lambs. Journal of Agricultural Science, Cambridge 122 309314.CrossRefGoogle Scholar
Nozière, P, Martin, C, Rémond, D, Kristensen, NB, Bernard, R & Doreau, M (2000 a) Effect of composition of ruminally-infused short-chain fatty acids on net fluxes of nutrients across portal-drained viscera in underfed ewes. British Journal of Nutrition 83 521531.CrossRefGoogle ScholarPubMed
Nozière, P, Rémond, D, Bernard, L & Doreau, M (2000 b) Effect of underfeeding on metabolism of portal-drained viscera in ewes. British Journal of Nutrition 84 821828.CrossRefGoogle ScholarPubMed
Ortigues, I & Visseiche, AL (1995) Whole body fuel selection in ruminants: nutrient supply and utilization by major tissues. Proceedings of the Nutrition Society 54 235251.CrossRefGoogle ScholarPubMed
Piccioli Cappelli, F, 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. British Journal of Nutrition 78 931946.CrossRefGoogle Scholar
Prior, LR, Huntington, GB & Britton, RA (1981) Influence of diet on amino acid absorption in beef cattle and sheep. Journal of Nutrition 111 22122222.CrossRefGoogle ScholarPubMed
Reeds, PJ, Burrin, DG, Stoll, BB, Jahor, F, Wykes, L, Henty, J & Frazer, ME (1997) Enteral glutamate is the preferential source for mucosal glutathione synthesis in fed piglets. American Journal of Physiology 273 E408E415.Google ScholarPubMed
Rémond, D, Bernard, L & Poncet, C (2000 a) Amino acid flux in ruminal and gastric veins of sheep: effects of ruminal and omasal injections of free amino acids and carnosine. Journal of Animal Science 78 158166.CrossRefGoogle ScholarPubMed
Rémond, D, Bernard, L & Poncet, C (2000 b) Free and peptide amino acid net flux across the rumen and the mesenteric- and portal-drained viscera of sheep. Journal of Animal Science 78 19601972.CrossRefGoogle ScholarPubMed
Rémond, D, Chaise, JP, Delval, E & Poncet, C (1993 a) Net flux of metabolites across the ruminal wall of sheep fed twice a day with orchardgrass hay. Journal of Animal Science 71 25292538.CrossRefGoogle Scholar
Rémond, D, Chaise, JP, Delval, E & Poncet, C (1993 b) Net transfer of urea and ammonia across the ruminal wall of sheep. Journal of Animal Science 71 27852792.CrossRefGoogle ScholarPubMed
Rémond, D, Nozière, P & Poncet, C (2002) Effect of time of starch supply to the rumen on the dynamics of urea and ammonia net flux across the rumen wall of sheep. Animal Research 51 313.CrossRefGoogle Scholar
Rémond, D, Ortigues, I, Isserty, A & Lefaivre, J (1998) Technical note: measuring portal blood flow in sheep using an ultrasonic transit time flow probe. Journal of Animal Science 76 27122716.CrossRefGoogle ScholarPubMed
Reynolds, CK, Bequette, BJ, Caton, JS, Humphries, DJ, Aikman, PC, Lupoli, B & Sutton, JD (2001) Effect of intake and lactation on absorption and metabolism of leucine and phenylalanine by splanchnic tissues of dairy cows. Journal of Animal Science 79, Suppl. 1, 362.Google Scholar
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. Journal of Animal Science 74 245256.CrossRefGoogle ScholarPubMed
Seal, CJ & Reynolds, CK (1993) Nutritional implications of gastrointestinal and liver metabolism in ruminants. Nutrition Research Reviews 6 185208.CrossRefGoogle ScholarPubMed
Souffrant, WB (1991) Endogenous nitrogen losses during digestion in pigs. In Proceedings of the Vth International Symposium on Digestive Physiology in Pigs, pp. 147166 [Verstegen, MWA, Huisman, J and Hartog, LA, editors]. Wageningen, The Netherlands: EAAP Publication, Pudoc.Google Scholar
Stoll, B, Burrin, DG, Henry, JF, Jahor, F & Reeds, PJ (1999) Dietary and systemic phenylalanine utilization for mucosal and hepatic constitutive protein synthesis in pigs. American Journal of Physiology 276 G49G57.Google ScholarPubMed
Stoll, B, Henry, JF, Reeds, PJ, Yu, H, Jahor, F & Burrin, DG (1998) Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. Journal of Nutrition 128 606614.CrossRefGoogle ScholarPubMed
Tagari, H & Bergman, EN (1978) Intestinal disappearance and portal blood appearance of amino acids in sheep. Journal of Nutrition 108 790803.CrossRefGoogle ScholarPubMed
Taschenov, KT, Varady, J, Boda, K & Fejes, J (1979) Role of bile and pancreatic juice in the secretion of endogenous nitrogen in the digestive tract of sheep. Archiv für Tierernahrung 29 477486.CrossRefGoogle Scholar
Van Bruchem, JV, Voigt, J, Lammers-Wienhoven, TSCW, Schonhusen, U, Ketelaars, JJM & Tamminga, S (1997) Secretion and reabsorption of endogenous protein along the small intestine of sheep: estimates derived from 15N dilution of plasma non-protein-N. British Journal of Nutrition 77 273286.CrossRefGoogle ScholarPubMed
Weigand, E, Young, JW & McGilliard, AD (1975) Volatile fatty acid metabolism by rumen mucosa from cattle fed hay or grain. Journal of Dairy Science 58 12941300.CrossRefGoogle ScholarPubMed
Weston, RH & Hogan, JP (1968) The digestion of pasture plants by sheep: 1. Ruminal production of volatile fatty acids by sheep offered diets of ryegrass and forage oats. Australian Journal of Agricultural Research 19 419432.CrossRefGoogle Scholar
Weatherburn, MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39 971973.CrossRefGoogle Scholar
Whitt, J, Huntington, G, Zetina, E, Casse, E, Taniguchi, K & Potts, W (1996) Plasma flow and net nutrient flux across gut and liver of cattle fed twice daily. Journal of Animal Science 74 24502461.CrossRefGoogle ScholarPubMed
Windmueller, HG & Spaeth, AE (1980) Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rat. Quantitative importance of glutamine, glutamate and aspartate. Journal of Biological Chemistry 255 107112.CrossRefGoogle ScholarPubMed
Wu, G (1998) Intestinal mucosal amino acid catabolism. Journal of Nutrition 128 12491252.CrossRefGoogle ScholarPubMed
Yu, F, Bruce, LA, Calder, AG, Milne, E, Coop, RL, Jackson, F, Horgan, GW & MacRae, JC (2000) Subclinical infection with the nematode Trichostrongylus colubriformis increases gastrointestinal tract leucine metabolism and reduces availability of leucine for other tissues. Journal of Animal Science 78 380390.CrossRefGoogle ScholarPubMed