Invited review: Use of butyrate to promote gastrointestinal tract development in calves

Journal of Dairy Science

Volumn 101, Issue 6, 2018, Pages 4785-4800

  Gorka P ^a   Kowalski, Z M ^a   Zabielski, R ^b   Guilloteau, P ^c  

^a UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^c INSERM   (France)

Author keywords

feed additive; maturation; rumen; small intestine

Indexed keywords

BUTYRIC ACID;

ANALYSIS; ANIMAL; ANIMAL FOOD; BOVINE; DIET; DIETARY SUPPLEMENT; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; VETERINARY MEDICINE;

ANIMAL FEED; ANIMALS; BUTYRIC ACID; CATTLE; DIET; DIETARY SUPPLEMENTS; GASTROINTESTINAL TRACT;

EID: 85042851784     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2017-14086     Document Type: Article

References (102)

1. Anderson, K.L., Nagaraja, T.G., Morrill, J.L., Ruminal metabolic development in calves weaned conventionally or early. J. Dairy Sci. 70 (1987), 1000–1005 10.3168/jds.S0022-0302(87)80105-4 3597925.
2. Andoh, A., Bamba, T., Sasaki, M., Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions. J. Parenter. Enteral. Nutr. 23 (1999), S70–S73 10.1177/014860719902300518 10483900.
3. Araujo, G., Terré, M., Mereu, A., Ipharraguerre, I.R., Bach, A., Effects of supplementing a milk replacer with sodium butyrate or tributyrin on performance and metabolism of Holstein calves. Anim. Prod. Sci. 56 (2015), 1834–1841 10.1071/AN14930.
4. Ash, R., Baird, G.D., Activation of volatile fatty acids in bovine liver and rumen epithelium. Biochem. J. 136 (1973), 311–319 10.1042/bj1360311 4359516.
5. Bailey, C.B., Growth of digestive organs and their contents in Holstein steers: Relation to body weight and diet. Can. J. Anim. Sci. 66 (1986), 653–661 10.4141/cjas86-072.
6. Baldwin, R.L. VI, McLeod, K.R., Klotz, J.L., Heitmann, R.N., Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. J. Dairy Sci. 87 (2004), E55–E65 10.3168/jds.S0022-0302(04)70061-2.
7. Bergman, E.N., Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70 (1990), 567–590 2181501.
8. Biernat, M., Zabielski, R., Sysa, P., Sosak-Świderska, B., Le Huërou-Luron, I., Guilloteau, P., Small intestinal and pancreatic microstructures are modified by an intraduodenal CCK-A receptor antagonist administration in neonatal calves. Regul. Pept. 85 (1999), 77–85 10.1016/S0167-0115(99)00079-8 10651060.
9. Bull, L.S., Bush, L.J., Friend, J.D., Harris, B. Jr., Jones, E.W., Incidence of ruminal parakeratosis in calves fed different rations and its relation to volatile fatty acid absorption. J. Dairy Sci. 48 (1965), 1459–1466 5864521.
10. Burakowska, K., Przybyło, M., Penner, G.B., Górka, P., Evaluating the effect of protein source and micro-encapsulated sodium butyrate in starter mixtures on gastrointestinal tract development of dairy calves. J. Dairy Sci., 100(Suppl. 2), 2017, 347 (Abstr.).
11. Burrin, D.G., Stoll, B., Guan, X., Glucagon-like peptide 2 function in domestic animals. Domest. Anim. Endocrinol. 24 (2003), 103–122 10.1016/S0739-7240(02)00210-2 12586312.
12. Canani, R.B., Di Costanzo, M., Leone, L., Pedata, M., Meli, R., Calignano, A., Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 17 (2011), 1519–1528 10.3748/wjg.v17.i12.1519 21472114.
13. Cavini, S., Iraira, S., Siurana, A., Foskolos, A., Ferret, A., Calsamiglia, S., Effect of sodium butyrate administered in the concentrate on rumen development and productive performance of lambs in intensive production system during the suckling and the fattening periods. Small Rumin. Res. 123 (2015), 212–217 10.1016/j.smallrumres.2014.11.009.
14. Chester-Jones, H., Moreland, S., Ziegler, D., Raeth-Knight, M., van Eys, J., Pre- and postweaning performance and health of dairy calves when sodium butyrate is fed in milk replacer and/or calf starter during the summer months. J. Dairy Sci., 95(Suppl. 2), 2012, 113.
15. Chilliard, Y., Martin, C., Rouel, J., Doreau, M., Milk fatty acids in dairy cows fed whole crude linseed, extruded linseed, or linseed oil, and their relationship with methane output. J. Dairy Sci. 92 (2009), 5199–5211 10.3168/jds.2009-2375 19762838.
16. Claus, R., Günthner, D., Letzgb, H., Effects of feeding fat-coated butyrate on mucosal morphology and function in the small intestine of the pig. J. Anim. Physiol. Anim. Nutr. (Berl.) 91 (2007), 312–318 10.1111/j.1439-0396.2006.00655.x 17615002.
17. Connor, E.E., Baldwin, R.L. IV, Li, C.J., Li, R.W., Chung, H., Gene expression in bovine rumen epithelium during weaning identifies molecular regulators of rumen development and growth. Funct. Integr. Genomics 13 (2013), 133–142 10.1007/s10142-012-0308-x 23314861.
18. Davarmanesh, A.R., Fathi Nasri, M.H., Kalantari Firouzabad, A.R., Montazer-Torbati, M.B., Effect of Ca-butyrate and oleobiotec (a flavouring agent) supplemented starter on the performance of Holstein calves. J. Agric. Sci. 153 (2015), 1506–1513 10.1017/S0021859615000726.
19. Dengler, F., Rackwitz, R., Benesch, F., Pfannkuche, H., Gäbel, G., Both butyrate incubation and hypoxia upregulate genes involved in the ruminal transport of SCFA and their metabolites. J. Anim. Physiol. Anim. Nutr. (Berl.) 99 (2015), 379–390 10.1111/jpn.12201 24804847.
20. Dieho, K., Dijkstra, J., Schonewille, J.T., Bannink, A., Changes in ruminal volatile fatty acid production and absorption rate during the dry period and early lactation as affected by rate of increase of concentrate allowance. J. Dairy Sci. 99 (2016), 5370–5384 10.3168/jds.2015-10819 27157578.
21. Doreau, M., Chilliard, Y., Digestion and metabolism of dietary fat in farm animals. Br. J. Nutr. 78:Suppl. 1 (1997), S15–S35 10.1079/BJN19970132 9292772.
22. Drackley, J.K., Calf nutrition from birth to breeding. Vet. Clin. North Am. Food Anim. Pract. 24 (2008), 55–86 10.1016/j.cvfa.2008.01.001 18299032.
23. Drucker, D.J., Gut adaptation and the glucagon-like peptides. Gut 50 (2002), 428–435 10.1136/gut.50.3.428 11839727.
24. Fernández-Rubio, C., Ordonez, C., Abad-González, J., Garcia-Gallego, A., Pilar Honrubia, M., Jose Mallo, J., Balana-Fouce, R., Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection. Poult. Sci. 88 (2009), 943–948 10.3382/ps.2008-00484 19359681.
25. Ferreira, L.S., Bittar, C.M., Performance and plasma metabolites of dairy calves fed starter containing sodium butyrate, calcium propionate or sodium monensin. Animal 5 (2011), 239–245 10.1017/S1751731110001965 22440769.
26. Flaga, J., Górka, P., Kowalski, Z.M., Kaczor, U., Pietrzak, P., Zabielski, R., Insulin-like growth factors 1 and 2 (IGF-1 and IGF-2) mRNA levels in relation to the gastrointestinal tract (GIT) development in newborn calves. Pol. J. Vet. Sci. 14 (2011), 605–613 10.2478/v10181-011-0090-z 22439332.
27. Flaga, J., Górka, P., Zabielski, R., Kowalski, Z.M., Differences in monocarboxylic acid transporter type 1 expression in rumen epithelium of newborn calves due to age and milk or milk replacer feeding. J. Anim. Physiol. Anim. Nutr. (Berl.) 99 (2015), 521–530 10.1111/jpn.12218 24980113.
28. Foote, A.P., Zarek, C.M., Kuehn, L.A., Cunningham, H.C., Cammack, K.M., Freetly, H.C., Lindholm-Perry, A.K., Effect of abomasal butyrate infusion on gene expression in the duodenum of lambs. J. Anim. Sci. 95 (2017), 1191–1196 10.2527/jas.2016.1022 28380531.
29. Frieten, D., Gerbert, C., Koch, C., Dusel, G., Eder, K., Kanitz, E., Weitzel, J.M., Hammon, H.M., Ad libitum milk replacer feeding, but not butyrate supplementation, affects growth performance as well as metabolic and endocrine traits in Holstein calves. J. Dairy Sci. 100 (2017), 6648–6661 10.3168/jds.2017-12722 28601458.
30. Galfi, P., Bokori, J., Feeding trial in pigs with a diet containing sodium n-butyrate. Acta Vet. Hung. 38 (1990), 3–17 2100936.
31. Gerbert, C., Frieten, D., Koch, C., Dusel, G., Eder, K., Zitnan, R., Hammon, H., Organ and epithelial growth in the gastrointestinal tract of Holstein calves fed milk replacer ad libitum and supplemented with butyrate. Proc. Nutr. Physiol., 26, 2017, 24.
32. Gherardi, S., Black, J., Effect of palatability on voluntary feed intake by sheep. I. Identification of chemicals that alter the palatability of a forage. Aust. J. Agric. Res. 42 (1991), 571–584 10.1071/AR9910571.
33. Górka, P., Kowalski, Z.M., Pietrzak, P., Kotunia, A., Jagusiak, W., Holst, J.J., Guilloteau, R., Zabielski, R., Effect of method of delivery of sodium butyrate on rumen development in newborn calves. J. Dairy Sci. 94 (2011), 5578–5588 10.3168/jds.2011-4166 22032381.
34. Górka, P., Kowalski, Z.M., Pietrzak, P., Kotunia, A., Jagusiak, W., Zabielski, R., Is rumen development in newborn calves affected by different liquid feeds and small intestine development?. J. Dairy Sci. 94 (2011), 3002–3013 10.3168/jds.2010-3499 21605770.
35. Górka, P., Pietrzak, P., Kotunia, A., Zabielski, R., Kowalski, Z.M., Effect of method of delivery of sodium butyrate on maturation of the small intestine. J. Dairy Sci. 97 (2014), 1026–1035 10.3168/jds.2013-7251 24342681.
36. Górka, P., Śliwiński, B., Flaga, J., Wieczorek, J., Godlewski, M.M., Wierzchoś, E., Zabielski, R., Kowalski, Z.M., Effect of butyrate infusion into the rumen on butyrate flow to the duodenum, selected gene expression in the duodenum epithelium, and nutrient digestion in sheep. J. Anim. Sci. 95 (2017), 2144–2155 10.2527/jas.2016.1218 28726987.
37. Górka, P., Śliwiński, B., Miltko, R., Flaga, J., Barć, J., Godlewski, M.M., Zabielski, R., Kowalski, Z.M., Effect of supplemental sodium butyrate on the activity of carbohydrate-digesting enzymes in the reticulo-ruminal digesta and brush border enzymes in sheep. J. Anim. Sci., 95(Suppl. 4), 2017, 314.
38. Guilloteau, P., Martin, L., Eeckhaut, V., Ducatelle, R., Zabielski, R., Van Immerseel, F., From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr. Res. Rev. 23 (2010), 366–384 10.1017/S0954422410000247 20937167.
39. Guilloteau, P., Savary, G., Jaguelin-Peyrault, Y., Rome, V., Le Normand, L., Zabielski, R., Dietary sodium butyrate supplementation increases digestibility and pancreatic secretion in young milk-fed calves. J. Dairy Sci. 93 (2010), 5842–5850 10.3168/jds.2009-2751 21094757.
40. Guilloteau, P., Zabielski, R., Blum, J.W., Gastrointestinal tract and digestion in the young ruminant: Ontogenesis, adaptations, consequences and manipulations. J. Physiol. Pharmacol. 60:Suppl. 3 (2009), 37–46 19996480.
41. Guilloteau, P., Zabielski, R., David, J.C., Blum, J.W., Morisset, J.A., Biernat, M., Woliński, J., Laubitz, D., Hamon, Y., Sodium-butyrate as a growth promoter in milk replacer formula for young calves. J. Dairy Sci. 92 (2009), 1038–1049 10.3168/jds.2008-1213 19233797.
42. Harmon, D.L., Influence of dietary energy-intake and substrate addition on the in vitro metabolism of glucose and glutamine in rumen epithelial tissue. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 85 (1986), 643–647 10.1016/0305-0491(86)90062-3 3791964.
43. Harmon, D.L., Gross, K.L., Krehbiel, R.C., Kreikemeier, K.K., Bauer, M.L., Britton, R.A., Influence of dietary forage and energy intake on metabolism and acyl-CoA synthetase activity in bovine ruminal epithelial tissue. J. Anim. Sci. 69 (1991), 4117–4127 10.2527/1991.69104117x 1778826.
44. Heinrichs, J., Rumen development in the dairy calf. Adv. Dairy Technol. 17 (2005), 179–187.
45. Herrick, K.J., Hippen, A.R., Kalscheur, K.F., Schingoethe, D.J., Casper, D.P., Moreland, S.C., van Eys, J.E., Single-dose infusion of sodium butyrate, but not lactose, increases plasma beta-hydroxybutyrate and insulin in lactating dairy cows. J. Dairy Sci. 100 (2017), 757–768 10.3168/jds.2016-11634 27837980.
46. Hill, T.M., Aldrich, J.M., Schlotterbeck, R.L., Bateman, H.G. II, Amino acids, fatty acids, and fat sources for calf milk replacers. Prof. Anim. Sci. 23 (2007), 401–408 10.15232/S1080-7446(15)30995-5.
47. Hill, T.M., Aldrich, J.M., Schlotterbeck, R.L., Bateman, H.G. II, Effects of changing the fat and fatty acid composition of milk replacers fed to neonatal calves. Prof. Anim. Sci. 23 (2007), 135–143 10.15232/S1080-7446(15)30953-0.
48. Hill, T.M., Bateman, H.G. II, Aldrich, J.M., Schlotterbeck, R.L., Effect of milk replacer program on digestion of nutrients in dairy calves. J. Dairy Sci. 93 (2010), 1105–1115 10.3168/jds.2009-2458 20172232.
49. Hill, T.M., Bateman, H.G. II, Aldrich, J.M., Schlotterbeck, R.L., Effect of various fatty acids on dairy calf performance. Prof. Anim. Sci. 27 (2011), 167–175 10.15232/S1080-7446(15)30470-8.
50. Hill, T.M., Quigley, J.D., Suarez-Mena, F.X., Bateman, H.G. II, Schlotterbeck, R.L., Effect of milk replacer feeding rate and functional fatty acids on dairy calf performance and digestion of nutrients. J. Dairy Sci. 99 (2016), 6352–6361 10.3168/jds.2015-10812 27289150.
51. Hill, T.M., VandeHaar, M.J., Sordillo, L.M., Catherman, D.R., Bateman, H.G. II, Schlotterbeck, R.L., Fatty acid intake alters growth and immunity in milk-fed calves. J. Dairy Sci. 94 (2011), 3936–3948 10.3168/jds.2010-3935 21787930.
52. Huhtanen, P., Miettinen, H., Ylinen, M., Effect of increasing ruminal butyrate on milk yield and blood constituents in dairy cows fed a grass silage-based diet. J. Dairy Sci. 76 (1993), 1114–1124 10.3168/jds.S0022-0302(93)77440-8 8486840.
53. Kaczmarek, S.A., Barri, A., Hejdysz, M., Rutkowski, A., Effect of different doses of coated butyric acid on growth performance and energy utilization in broilers. Poult. Sci. 95 (2016), 851–859 10.3382/ps/pev382 26740137.
54. Kato, S., Sato, K., Chida, H., Roh, S.G., Ohwada, S., Sato, S., Guilloteau, P., Katoh, K., Effects of Na-butyrate supplementation in milk formula on plasma concentrations of GH and insulin, and on rumen papilla development in calves. J. Endocrinol. 211 (2011), 241–248 10.1530/JOE-11-0299 21911440.
55. Kendall, P.E., McLeay, L.M., Excitatory effects of volatile fatty acids on the in vitro motility of the rumen of sheep. Res. Vet. Sci. 61 (1996), 1–6 10.1016/S0034-5288(96)90101-0 8819185.
56. Khan, M.A., Bach, A., Weary, D.M., von Keyserlingk, M.A.G., Invited review: Transitioning from milk to solid feed in dairy heifers. J. Dairy Sci. 99 (2016), 885–902 10.3168/jds.2015-9975 26709160.
57. Klein, R.D., Kincaid, R.L., Hodgson, A.S., Harrison, J.H., Hillers, J.K., Cronrath, J.D., Dietary fiber and early weaning on growth and rumen development of calves. J. Dairy Sci. 70 (1987), 2095–2104 10.3168/jds.S0022-0302(87)80259-X 2824583.
58. Konturek, S.J., Zabielski, R., Konturek, J.W., Czarnecki, J., Neuroendocrinology of the pancreas; role of brain–gut axis in pancreatic secretion. Eur. J. Pharmacol. 481 (2003), 1–14 10.1016/j.ejphar.2003.08.042 14637169.
59. Kotunia, A., Woliński, J., Laubitz, D., Jurkowska, M., Romé, V., Guilloteau, P., Zabielski, R., Effect of sodium butyrate on the small intestine development in neonatal piglets feed by artificial sow. J. Physiol. Pharmacol. 55:Suppl. 2 (2004), 59–68 15608361.
60. Kowalski, Z.M., Górka, P., Flaga, J., Barteczko, A., Burakowska, K., Oprządek, J., Zabielski, R., Effect of microencapsulated sodium butyrate in the close-up diet on performance of dairy cows in the early lactation period. J. Dairy Sci. 98 (2015), 3284–3291 10.3168/jds.2014-8688 25726104.
61. Kristensen, N.B., Harmon, D.L., Effect of increasing ruminal butyrate absorption on splanchnic metabolism of volatile fatty acids absorbed from the washed reticulorumen of steers. J. Anim. Sci. 82 (2004), 3549–3559 10.2527/2004.82123549x 15537776.
62. Kristensen, N.B., Harmon, D.L., Splanchnic metabolism of volatile fatty acids absorbed from the washed reticulorumen of steers. J. Anim. Sci. 82 (2004), 2033–2042 10.2527/2004.8272033x 15309950.
63. Kristensen, N.B., Pierzynowski, S.G., Danfaer, A., Net portal appearance of volatile fatty acids in sheep intraruminally infused with mixtures of acetate, propionate, isobutyrate, butyrate, and valerate. J. Anim. Sci. 78 (2000), 1372–1379 10.2527/2000.7851372x 10834594.
64. Kristensen, N.B., Pierzynowski, S.G., Danfaer, A., Portal-drained visceral metabolism of 3-hydroxybutyrate in sheep. J. Anim. Sci. 78 (2000), 2223–2228 10.2527/2000.7882223x 10947112.
65. Krokowicz, L., Kaczmarek, B.F., Krokowicz, P., Stojcev, Z., Mackiewicz, J., Walkowiak, J., Drews, M., Banasiewicz, T., Sodium butyrate and short chain fatty acids in prevention of travellers' diarrhoea: A randomized prospective study. Travel Med. Infect. Dis. 12 (2014), 183–188 10.1016/j.tmaid.2013.08.008 24063909.
66. Le Gall, M., Gallois, M., Seve, B., Louveau, I., Holst, J.J., Oswald, I.P., Lallès, J.P., Guilloteau, P., Comparative effect of orally administered sodium butyrate before or after weaning on growth and several indices of gastrointestinal biology of piglets. Br. J. Nutr. 102 (2009), 1285–1296 10.1017/S0007114509990213 19480733.
67. Lesmeister, K.E., Heinrichs, A.J., Effects of adding extra molasses to a texturized calf starter on rumen development, growth characteristics, and blood parameters in neonatal dairy calves. J. Dairy Sci. 88 (2005), 411–418 10.3168/jds.S0022-0302(05)72702-8 15591407.
68. Li, R.W., Wu, S.T., Baldwin, R.L., Li, W.Z., Li, C.J., Perturbation dynamics of the rumen microbiota in response to exogenous butyrate. PLoS One, 7, 2012, e29392 10.1371/journal.pone.0029392 22253719.
69. Li, S., Khafipour, E., Krause, D.O., Kroeker, A., Rodriguez-Lecompte, J.C., Gozho, G.N., Plaizier, J.C., Effects of subacute ruminal acidosis challenges on fermentation and endotoxins in the rumen and hindgut of dairy cows. J. Dairy Sci. 95 (2012), 294–303 10.3168/jds.2011-4447 22192209.
70. Malhi, M., Gui, H., Yao, L., Aschenbach, J.R., Gäbel, G., Shen, Z., Increased papillae growth and enhanced short-chain fatty acid absroption in the rumen of goats are associated with transient increases in cyclin D1 expression after ruminal butyrate infusion. J. Dairy Sci. 96 (2013), 7603–7616 10.3168/jds.2013-6700 24119813.
71. Mallo, J.J., Balfagón, A., Gracia, M.I., Honrubia, P., Puyalto, M., Evaluation of different protections of butyric acid aiming for release in the last part of the gastrointestinal tract of piglets. J. Anim. Sci. 90:Suppl. 4 (2012), 227–229 10.2527/jas.53959 23365338.
72. Manzanilla, E.G., Nofrarias, M., Anguita, M., Castillo, M., Perez, J.F., Martin-Orue, S.M., Kamel, C., Gasa, J., Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. J. Anim. Sci. 84 (2006), 2743–2751 10.2527/jas.2005-509 16971576.
73. Mazzoni, M., Le Gall, M., De Filippi, S., Minieri, L., Trevisi, P., Woliński, J., Lalatta-Costerbosa, G., Lallés, J.P., Guilloteau, P., Bosi, P., Supplemental sodium butyrate stimulates different gastric cells in weaned pigs. J. Nutr. 138 (2008), 1426–1431 18641186.
74. McGavin, M.D., Morrill, J.L., Scanning electron microscopy of ruminal papillae in calves fed various amounts and forms of roughage. Am. J. Vet. Res. 37 (1976), 497–508 1275333.
75. Mentschel, J., Leiser, R., Mülling, C., Pfarrer, C., Claus, R., Butyric acid stimulates rumen mucosa development in the calf mainly by a reduction of apoptosis. Arch. Anim. Nutr. 55 (2001), 85–102 10.1080/17450390109386185 12068484.
76. Moquet, P.C.A., Onrust, L., van Immerseel, F., Ducatelle, R., Hendriks, W.H., Kwakkel, R.P., Importance of release location on the mode of action of butyrate derivatives in the avian gastrointestinal tract. Worlds Poult. Sci. J. 72 (2016), 61–80 10.1017/s004393391500269x.
77. Nazari, M., Karkoodi, K., Alizadeh, A., Performance and physiological responses of milk-fed calves to coated calcium butyrate supplementation. S. Afr. J. Anim. Sci. 42 (2012), 296–303 10.4314/sajas.v42i3.12.
78. Palmquist, D.L., Denise Beaulieu, A., Barbano, D.M., Feed and animal factors influencing milk fat composition. J. Dairy Sci. 76 (1993), 1753–1771 10.3168/jds.S0022-0302(93)77508-6 8326036.
79. Penner, G.B., Steele, M.A., Aschenbach, J.R., McBride, B.W., Ruminant Nutrition Symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J. Anim. Sci. 89 (2011), 1108–1119 10.2527/jas.2010-3378 20971890.
80. Piva, A., Pizzamiglio, V., Morlacchini, M., Tedeschi, M., Piva, G., Lipid microencapsulation allows slow release of organic acids and natural identical flavors along the swine intestine. J. Anim. Sci. 85 (2007), 486–493 10.2527/jas.2006-323 17040943.
81. Ploger, S., Stumpff, F., Penner, G.B., Schulzke, J.D., Gäbel, G., Martens, H., Shen, Z.M., Gunzel, D., Aschenbach, J.R., Microbial butyrate and its role for barrier function in the gastrointestinal tract. Fromm, M., Schulzke, J.D., (eds.) Ann. N. Y. Acad. Sci., Vol. 1258, 2012, Blackwell Science Publ, Oxford, UK, 52–59 10.1111/j.1749-6632.2012.06553.x.
82. Quigley, J.D. III, Smith, P., Heitmann, R.N., Changes in plasma volatile fatty acids in response to weaning and feed intake in young calves. J. Dairy Sci. 74 (1991), 258–263 10.3168/jds.S0022-0302(91)78168-X 2030171.
83. Rossi, F., Maurizio, M., Francesco, M., Giovanna, C., Gianfranco, P., Rumen degradation and intestinal digestibility of rumen protected amino acids: comparison between in situ and in vitro data. Anim. Feed Sci. Technol. 108 (2003), 223–229 10.1016/S0377-8401(03)00131-7.
84. Sakata, T., Tamate, H., Rumen epithelial cell proliferation accelerated by rapid increase in intaruiminal butyrate. J. Dairy Sci. 61 (1978), 1109–1113 10.3168/jds.S0022-0302(78)83694-7 721981.
85. Seegraber, F.J., Morrill, J.L., Effect of protein source in calf milk replacers on morphology and absorptive ability of small intestine. J. Dairy Sci. 69 (1986), 460–469 10.3168/jds.S0022-0302(86)80424-6 3700793.
86. Serbester, U., Cakmakci, C., Goncu, S., Gorgulu, M., Effect of feeding starter containing butyrate salt on pre- and post-weaning performance of early or normally weaned calves. Rev. Med. Vet. 165 (2014), 44–48.
87. Shen, Z., Kuhla, S., Zitnan, R., Seyfert, H.M., Schneider, F., Hagemeister, H., Chudy, A., Löhrke, B., Blum, J.W., Hammon, H., Voigt, J., Intraruminal infusion of n-butyric acid induces an increase of ruminal papillae size independent of IGF-1 system in castrated bulls. Arch. Anim. Nutr. 59 (2005), 213–225 10.1080/17450390500216894 16320810.
88. Shen, Z., Martens, H., Schweigel-Rontghen, M., Na transport across rumen epithelium of hay-fed sheep is acutely stimulated by the peptide IGF-1 in vitro. Exp. Physiol. 97 (2012), 497–505 10.1113/expphysiol.2011.061580 22227200.
89. Ślusarczyk, K., Strzetelski, J.A., Furgał-Dierżuk, I., The effect of sodium butyrate on calf growth and serum level of beta-hydroxybutyric acid. J. Anim. Feed Sci. 19 (2010), 348–357 10.22358/jafs/66298/2010.
90. Steele, M.A., Dionissopoulos, L., AlZahal, O., Doelman, J., McBride, B.W., Rumen epithelial adaptation to ruminal acidosis in lactating cattle involves the coordinated expression of insulin-like growth factor-binding proteins and a cholesterolgenic enzyme. J. Dairy Sci. 95 (2012), 318–327 10.3168/jds.2011-4465 22192211.
91. Storm, A.C., Hanigan, M.D., Kristensen, N.B., Effects of ruminal ammonia and butyrate concentrations on reticuloruminal epithelial blood flow and volatile fatty acid absorption kinetics under washed reticulorumen conditions in lactating dairy cows. J. Dairy Sci. 94 (2011), 3980–3994 10.3168/jds.2010-4091 21787934.
92. Vazquez-Anon, M., Heinrichs, A.J., Aldrich, J.M., Varga, G.A., Postweaning age effects on rumen fermentation end-products and digesta kinetics in calves weaned at 5 weeks of age. J. Dairy Sci. 76 (1993), 2742–2748 10.3168/jds.S0022-0302(93)77611-0 8227677.
93. Vinolo, M.A.R., Rodrigues, H.G., Festuccia, W.T., Crisma, A.R., Alves, V.S., Martins, A.R., Amaral, C.L., Fiamoncini, J., Hirabara, S.M., Sato, F.T., Fock, R.A., Malheiros, G., dos Santos, M.F., Curi, R., Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. Am. J. Physiol. Endocrinol. Metab. 303 (2012), E272–E282 10.1152/ajpendo.00053.2012 22621868.
94. Wanat, P., Górka, P., Kowalski, Z.M., Short communication: Effect of inclusion rate of microencapsulated sodium butyrate in starter mixture for dairy calves. J. Dairy Sci. 98 (2015), 2682–2686 10.3168/jds.2014-8482 25648817.
95. Weigand, E., Young, J.W., McGilliard, A.D., Extent of butyrate metabolism by bovine ruminoreticulum epithelium and relationship to absorption rate. J. Dairy Sci. 55 (1972), 589–597 10.3168/jds.S0022-0302(72)85541-3 5022825.
96. Wiese, B.I., Górka, P., Mutsvangwa, T., Okine, E., Penner, G.B., Short communication: Interrelationship between butyrate and glucose supply on butyrate and glucose oxidation by ruminal epithelial preparations. J. Dairy Sci. 96 (2013), 5914–5918 10.3168/jds.2013-6677 23810600.
97. Wilson, D.J., Mutsvangwa, T., Penner, G.B., Supplemental butyrate does not enhance the absorptive or barrier functions of the isolated ovine ruminal epithelia. J. Anim. Sci. 90 (2012), 3153–3161 10.2527/jas.2011-4315 22585785.
98. Wu, S.H.W., Papas, A., Rumen-stable delivery systems. Adv. Drug Deliv. Rev. 28 (1997), 323–334 10.1016/S0169-409X(97)00087-2 10837573.
99. Zabielski, R., Regulatory peptides in milk, food and in the gastrointestinal lumen of young animals and children. J. Anim. Feed Sci. 7 (1998), 65–78 10.22358/jafs/69956/1998.
100. Zabielski, R., Le Huërou-Luron, I., Guilloteau, P., Development of gastrointestinal and pancreatic functions in mammalians (mainly bovine and porcine species): Influence of age and ingested food. Reprod. Nutr. Dev. 39 (1999), 5–26 10.1051/rnd:19990101 10222497.
101. Zabielski, R., Morisset, J., Podgurniak, P., Romé, V., Biernat, M., Bernard, C., Chayvialle, J.A., Guilloteau, P., Bovine pancreatic secretion in the first week of life: Potential involvement of intestinal CCK receptors. Regul. Pept. 103 (2002), 93–104 10.1016/S0167-0115(01)00362-7 11786148.
102. Zabielski, R., Onaga, T., Mineo, H., Pierzynowski, S.G., Kato, S., Local versus peripheral blood administration of cholecystokinin-8 and secretin on pancreatic secretion in calves. Exp. Physiol. 79 (1994), 301–311 8074843.