Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-23T01:35:57.180Z Has data issue: false hasContentIssue false
  • English
  • Français

Splanchnic metabolism of volatile fatty acids in the dairy cow

Published online by Cambridge University Press:  09 March 2007

N. B. Kristensen
N. B. Kristensen*
Affiliation:
Danish Institute of Agricultural Sciences, Department of Animal Nutrition and Physiology, DK-8830 Tjele, Denmark
*
†E-mail: [email protected]
Get access

Abstract

Volatile fatty acids (VFA) are quantitatively important substrates for dairy cows and other ruminants. It has been a central dogma in the nutritional physiology of ruminants that the ruminal epithelium metabolizes a large fraction of VFA during theirabsorption and consequently a relatively small fraction of VFA is available for peripheral tissues including the mammary gland. New data on splanchnic metabolism of VFA indicate that the ruminal epithelium metabolizes none or small amounts of acetate and propionate absorbed from the rumen. However, the ruminal epithelium has a large fractional uptake of butyrate and valerate during their absorption from the rumen. The liver takes up proportionately 0·9 or more of the absorbed propionate, however multiple factors are involved in regulation of hepatic metabolism and propionate does not determine glucose availability to the cow per se. In light of the quantitative importance of VFA to the dairy cow it is important that future research attempts to bridge the gap between the biology of food degradation/digestion in the gastro-intestinal tract and availability of specific nutrients to the cow which impact intermediary metabolism and nutrient utilizationin productive tissues.

Keywords

dairy cowslivermetabolismruminal epitheliumvolatile fatty acids
Type
Research Article
Information
Animal Science , Volume 80 , Issue 1 , February 2005 , pp. 3 - 10
Copyright
Copyright © British Society of Animal Science 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ash, R. and Baird, G. D. 1973. Activation of volatile fatty acids in bovine liver and rumen epithelium. Evidence for control by autoregulation. Biochemical Journal 136: 311–319.CrossRefGoogle ScholarPubMed
Bell, A. W. 1980. Lipid metabolism in liver and selected tissues and in the whole body of ruminant animals. Progress in Lipid Research 18: 117–164.CrossRefGoogle Scholar
Benson, J. A., Reynolds, C. K., Aikman, P. C., Lupoli, B. and Beever, D. E. 2002. Effects of abomasal vegetable oil infusion on splanchnic nutrient metabolism in lactating dairy cows. Journal of Dairy Science 85: 1804–1814.CrossRefGoogle ScholarPubMed
Bergman, E. N. 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70: 567–589.CrossRefGoogle ScholarPubMed
Bergman, E. N. and Wolff, J. E. 1971. Metabolism of volatile fatty acids by liver and portal-drained viscera in sheep. American Journal of Physiology 221: 586–592.CrossRefGoogle ScholarPubMed
Berthelot, V., Pierzynowski, S. G., Sauvant, D. and Kristensen, N. B. 2002. Hepatic metabolism of propionate and methylmalonate in growing lambs. Livestock Production Science 74: 33–43.CrossRefGoogle Scholar
Casse, E. A., Rulquin, H. and Huntington, G. B. 1994. Effect of mesenteric vein infusion of propionate on splanchnic metabolism in primiparous Holstein cows. Journal of Dairy Science 77: 3296–3303.CrossRefGoogle ScholarPubMed
Danfær, A. 1994. Nutrient metabolism and utilization in the liver. Livestock Production Science 39: 115–127.CrossRefGoogle Scholar
Danfær, A., Tetens, V. and Agergaard, N. 1995. Review and an experimental study on the physiological and quantitative aspects of gluconeogenesis in lactating ruminants. Comparative Biochemistry and Physiology 111B: 201–210.CrossRefGoogle Scholar
Emmanuel, B. 1974. On the origin of rumen protozoan fatty acids. Biochimica et Biophysica Acta 337: 404–413.CrossRefGoogle ScholarPubMed
Emmanuel, B., Milligan, L. P. and Turner, B. V. 1974. The metabolism of acetate by rumen microorganisms. Canadian Journal of Microbiology 20: 183–185.CrossRefGoogle Scholar
Exton, J. H. 1972. Gluconeogenesis. Metabolism 21: 945–990.CrossRefGoogle ScholarPubMed
Gray, F. V., Pilgrim, A. F., Rodda, H. J. and Weller, R. A. 1952. Fermentation in the rumen of the sheep. IV. The nature and origin of the volatile fatty acids in the rumen of the sheep. Journal of Experimental Biology 29: 57–65.CrossRefGoogle Scholar
Gross, K. L., Harmon, D. L. and Avery, T. B. 1990. Portal-drained visceral flux of nutrients in lambs fed alfalfa or maintained by total intragastric infusion. Journal of Animal Science 68: 214–221.CrossRefGoogle ScholarPubMed
Harmon, D. L., Gross, K. L., Krehbiel, C. R., Kreikemeier, K. K., Bauer, M. L. and Britton, R. A. 1991. Influence of dietary forage and energy intake on metabolism and acyl-coA synthetase activity in bovine ruminal epithelial tissue. Journal of Animal Science 69: 4117–4127.CrossRefGoogle ScholarPubMed
Hird, F. J. R., Jackson, R. B. and Weidemann, M. J. 1966. Transport and metabolism of fatty acids by isolated rumen epithelium. Biochemical Journal 98: 394–400.CrossRefGoogle ScholarPubMed
Huntington, G. B. 1990. Energy metabolism in the digestive tract and liver of cattle: influence of physiological state and nutrition. Reproduction, Nutrition, Development 30: 35–47.CrossRefGoogle ScholarPubMed
Huntington, G. B., Reynolds, C. K. and Stroud, B. H. 1989. Techniques for measuring blood flow in splanchnic tissues of cattle. Journal of Dairy Science 72: 1583–1595.CrossRefGoogle ScholarPubMed
Jenkins, T. C. 1993. Lipid metabolism in the rumen. Journal of Dairy Science 76: 3851–3863.CrossRefGoogle ScholarPubMed
Jesse, B. W., Solomon, R. K. and Baldwin VI, R. L. 1992. Palmitate metabolism by isolated sheep rumen epithelial cells. Journal of Animal Science 70: 2235–2242.CrossRefGoogle ScholarPubMed
Krebs, H. A. 1969. The role of equilibria in the regulation of metabolism. Current Topics in Cellular Regulation 1: 45–55.CrossRefGoogle Scholar
Krehbiel, C. R., Harmon, D. L. and Schnieder, J. E. 1992. Effect of increasing ruminal butyrate on portal and hepatic nutrient flux in steers. Journal of Animal Science 70: 904–914.CrossRefGoogle ScholarPubMed
Kristensen, N. B. 2001. Rumen microbial sequestration of [2–13C]acetate in cattle. Journal of Animal Science 79: 2491–2498.CrossRefGoogle ScholarPubMed
Kristensen, N. B., Danfær, A., Røjen, B. A., Raun, B.-M. L., Weisbjerg, M. R. and Hvelplund, T. 2002. Metabolism of propionate and 1, 2-propanediol absorbed from the washed reticulorumen of lactating cows. Journal of Animal Science 80: 2168–2175.Google ScholarPubMed
Kristensen, N. B., Danfær, A., Tetens, V. and Agergaard, N. 1996. Portal recovery of intraruminally infused short-chain fatty acids in sheep. Acta Agriculturœ Scandinavica, SectionA 46: 26–38.CrossRefGoogle Scholar
Kristensen, N. B., Gäbel, G., Pierzynowski, S. G. and Danfœr, 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, N. B. and Harmon, D. L. 2004a. Effect of increasing ruminal butyrate absorption on splanchnic metabolism of volatile fatty acids absorbed from the washed reticulorumen of steers. Journal of Animal Science 82: 3549–3559.CrossRefGoogle ScholarPubMed
Kristensen, N. B. and Harmon, D. L. 2004b. Splanchnic metabolism of VFA absorbed from the washed reticulorumen of steers. Journal of Animal Science 82: 2033–2042.CrossRefGoogle ScholarPubMed
Kristensen, N. B., Pierzynowski, S. G. and Danfœr, 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
Kristensen, N. B., Pierzynowski, S. G. and Danfœr, A. 2000c. Portal-drained visceral metabolism of 3-hydroxybutyrate in sheep. Journal of Animal Science 78: 2223–2228.CrossRefGoogle ScholarPubMed
Lemosquet, S., Rigout, S., Bach, A., Rulquin, H. and Blum, J. W. 2004. Glucose metabolism in lactating cows in response to isoenergetic infusions of propionic acid or duodenal glucose. Journal of Dairy Science 87: 1767–1777.CrossRefGoogle ScholarPubMed
Leng, R. A. and Brett, D. J. 1966. Simultaneous measurements of the rates of production of acetic, propionic and butyric acids in the rumen of sheep on different diets and the correlation between production rates and concentrations of these acids in the rumen. British Journal of Nutrition 20: 541–552.CrossRefGoogle ScholarPubMed
Lomax, M. A. and Baird, G. D. 1983. Blood flow and nutrient exchange across the liver and gut of the dairy cow. British Journal of Nutrition 49: 481–496.CrossRefGoogle ScholarPubMed
Majdoub, L., Vermorel, M. and Ortiques-Marty, I. 2003.Google Scholar
Ørskov, E. R., MacLeod, N. A., Kay, R. N. B. and Gregory, P. C. 1984. Method and validation of intragastric nutrition. Canadian Journal of Animal Science 64: (suppl. ) 138–139.CrossRefGoogle Scholar
Oshio, S. and Tahata, I. 1984. Absorption of dissociated volatile fatty acids through the rumen wall of sheep. Canadian Journal of Animal Science 64: (suppl. ) 167–168.CrossRefGoogle Scholar
Pennington, R. J. 1952. The metabolism of short-chain fatty acids in the sheep. 1. Fatty acid utilization and ketone body production by rumen epithelium and other tissues. Biochemical Journal 51: 251–258.CrossRefGoogle Scholar
Prasad, K. N. and Sinha, P. 1976. Effect of sodium butyrate on mammalian cells in culture: a review. In Vitro 12: 125–132.CrossRefGoogle ScholarPubMed
Reynolds, C. K. 1995. Quantitative aspects of liver metabolism in ruminants. In Ruminant physiology: digestion, metabolism, growth and reproduction(ed. Engelhardt, W. V., Leonhard-Marek, S., Breves, G., and Giesecke, D.), pp. 351–371. Ferdinand Enke Verlag, Stuttgart.Google Scholar
Reynolds, C. K., Aikman, P. C., Lupoli, B., Humphries, D. J. and Beever, D. E. 2003. Splanchnic metabolism of dairy cows during the transition from late gestation through early lactation. Journal of Dairy Science 86: 1201–1217.CrossRefGoogle ScholarPubMed
Reynolds, C. K. and Huntington, G. B. 1988a. Partition of portaldrained visceral net flux in beef steers. 2. Net flux of volatile fatty acids, Z -b-hydroxybutyrate and b-lactate across stomach and poststomach tissues. British Journal of Nutrition 60: 553–562.CrossRefGoogle Scholar
Reynolds, C. K., Huntington, G. B., Tyrrell, H. F. and Reynolds, P. J. 1988a. Net metabolism of volatile fatty acids, Z -β-hydroxybutyrate, nonesterified fatty acids, and blood gasses by portal-drained viscera and liver of lactating Holstein cows. Journal of Dairy Science 71: 2395–2405.CrossRefGoogle Scholar
Reynolds, P. J. and Huntington, G. B. 1988b. Net portal absorption of volatile fatty acids and b( + )-lactate by lactating Holstein cows. Journal of Dairy Science 71: 124–133.CrossRefGoogle Scholar
Savary-Auzeloux, I. C., Majdoub, L., LeFloc'h, N. and Ortigues-Marty, I. 2003. Effects of intraruminal propionate supplementation on nitrogen utilisation by the portal-drained viscera, the liver and the hindlimb in lambs fed frozen rye grass. British Journal of Nutrition 90: 939–952.CrossRefGoogle ScholarPubMed
Seal, C. J. and Parker, D. S. 2000. Influence of gastrointestinal metabolism on substrate supply to the liver. In Ruminant physiology: digestion, metabolism, growth and reproduction(ed. Cronjé, P. B.), pp. 131–148. CABI Publishing, Oxon.CrossRefGoogle Scholar
Sehested, J., Diernœs, L., Møller, P. D. and Skadhauge, E. 1999. Ruminal transport and metabolism of short-chain fatty acids (SCFA) in vitro: effect of SCFA chain length and pH. Comparative Biochemistry and Physiology, A 123: 359–368.CrossRefGoogle ScholarPubMed
Sievers, A. K., Kristensen, N. B., Laue, H.-J. and Wolffram, S. 2004. Development of an intraruminal device for data sampling and transmission. Journal of Animal and Feed Sciences 13: (suppl. 1) 207–210.CrossRefGoogle Scholar
Steinhour, W. D. and Bauman, D. E. 1988. Propionate metabolism: a new interpretation. In Aspects of digestive physiology in ruminants(ed. Dobson, A. and Dobson, M. J.), pp. 238–256. Comstock Publishing Associates, Ithaca, NY.Google Scholar
Stevens, C. E. 1970. Fatty acid tranport through the rumen epithelium. In Physiology of digestion and metabolism in the ruminant(ed. Phillipson, A. T.), pp. 101–112. Oriel Press, Newcastle upon Tyne, England.Google Scholar
Sutton, J. D. 1985. Digestion and absorption of energy substrates in the lactating cow. Journal of Dairy Science 68: 3376–3393.CrossRefGoogle Scholar
Sutton, J. D., Dhanoa, M. S., Morant, S. V., France, J., Napper, D. J. and Schuller, E. 2003. Rates of production of acetate,propionate, and butyrate in the rumen of lactating dairy cows given normal and low-roughage diets. Journal of Dairy Science 86: 3620–3633.CrossRefGoogle ScholarPubMed
Sutton, J. D. and Morant, S. V. 1978. Measurement of the rate of volatile fatty acid production in the rumen. In Ruminant digestion and feed evaluation(ed. Osburn, D. F., Beever, D. E. and Thomson, D. J.), pp. 7. 1–7. 11. Agricultural Research Council, London.Google Scholar
Topping, D. L. and Clifton, P. M. 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81: 1031–1064.CrossRefGoogle ScholarPubMed
Veenhuizen, J. J., Russell, R. W. and Young, J. W. 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
Visser de, H., Klop, A., van der Meulen, J. and van Vuuren, A. M. 1998. Influence of maturity of grass silage and flaked corn starch on the production and metabolism of volatile fatty acids in dairy cows. Journal of Dairy Science 81: 1028–1035.CrossRefGoogle Scholar
Webster, L. T. Jr, Gerowin, L. D. and Rakita, L. 1965. Puri.cation and characteristics of a butyryl coenzyme A synthetase from bovine heart mitochondria. Journal of Biological Chemistry 240: 29–33.CrossRefGoogle ScholarPubMed
Weekes, T. E. C. and Webster, A. J. F. 1975. Metabolism of propionate in the tissues of the sheep gut. British Journal of Nutrition 33: 425–438.CrossRefGoogle Scholar
Weigand, E., Young, J. W. and McGilliard, A. D. 1972. Extent of propionate metabolism during absorption from the bovine ruminoreticulum. Biochemical Journal 126: 201–209.CrossRefGoogle ScholarPubMed
Weigand, E., Young, J. W. and McGilliard, A. D. 1975. Volatile fatty acid metabolism by rumen mucosa from cattle fed hay or grain. Journal of Dairy Science 58: 1294–13001.CrossRefGoogle ScholarPubMed
Young, J. W., Thorp, S. L. and De Lumen, H. Z. 1969. Activity of selected gluconeogenic and lipogenic enzymes in bovine rumen mucosa, liver and adipose tissue. Biochemical Journal 114: 83–88.CrossRefGoogle ScholarPubMed
Zierler, K. L. 1961. Theory of the use of arteriovenous concentration differences for measuring metabolism in steady and non-steady states. Journal of Clinical Investigation 40: 2111–2125.CrossRefGoogle ScholarPubMed