Experimental acute rumen acidosis in sheep: Consequences on clinical, rumen, and gastrointestinal permeability conditions and blood chemistry

Journal of Animal Science

Volumn 92, Issue 9, 2014, Pages 3966-3977

  Minuti, A ^a   Ahmed, S ^a,b   Trevisi, E ^a   Piccioli Cappelli, F ^a   Bertoni, G ^a   Jahan, N ^a   Bani, P ^a  

^a UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

^b BANGLADESH LIVESTOCK RESEARCH INSTITUTE   (Bangladesh)

Author keywords

Acute ruminal acidosis; Gastrointestinal permeability; Lactulose test; Sheep

Indexed keywords

3 HYDROXYBUTYRIC ACID; CERULOPLASMIN; GLUCOSE BLOOD LEVEL; LACTIC ACID; LACTIC ACID DERIVATIVE; LACTULOSE;

ACIDOSIS; ANIMAL; BLOOD; CHEMICALLY INDUCED; CLINICAL TRIAL; CROSSOVER PROCEDURE; DOMESTIC SHEEP; DRUG EFFECTS; GASTROINTESTINAL DISEASE; GLUCOSE BLOOD LEVEL; METABOLISM; METABOLOMICS; PERMEABILITY; PROCEDURES; RUMINANT STOMACH; SHEEP; SHEEP DISEASE; VETERINARY;

3-HYDROXYBUTYRIC ACID; ACIDOSIS; ANIMALS; BLOOD GLUCOSE; CERULOPLASMIN; CROSS-OVER STUDIES; GASTROINTESTINAL DISEASES; LACTATES; LACTIC ACID; LACTULOSE; METABOLOMICS; PERMEABILITY; RUMEN; SHEEP; SHEEP DISEASES; SHEEP, DOMESTIC;

EID: 84907646077     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2014-7594     Document Type: Article

References (76)

1. Ahmed, S., A. Minuti, and P. Bani. 2013. In vitro rumen fermentation characteristics of some naturally occurring and synthetic sugars. Ital. J. Anim. Sci. 12:359-365.
2. Al Jassim, R. A. M., G. L. R. Gordon, and J. B. Rowe. 2003. The effect of basal diet on lactate-producing bacteria and the susceptibility of sheep to lactic acidosis. Anim. Sci. 77:459-469.
3. Ametaj, B. N., B. J. Bradford, G. Bobe, R. A. Nafikov, Y. Lu, J. W. Young, and D. C. Beitz. 2005. Strong relationships between mediators of the acute phase response and fatty liver in dairy cows. Can. J. Anim. Sci. 85:165-175.
4. Andersen, P. H., M. Hesselholt, and N. Jarløv. 1994. Endotoxin and arachidonic acid metabolites in portal, hepatic and arterial blood of cattle with acute ruminal acidosis. Acta Vet. Scand. 35:223-234.
5. Bertoni, G., F. Piccioli-Cappelli, L. Calamari, and E. Trevisi. 1989. Digestive upsets of ruminants: Possible role of endotoxins and/ or histamine. In: Proc. 7th Int. Conf. on Production diseases in farm animals, Ithaca, NY. p. 370-373.
6. Bertoni, G., and E. Trevisi. 2013. Use of the liver activity index and other metabolic variables in the assessment of metabolic health in dairy herds. Vet. Clin. North Am. Food Anim. Pract. 29:413-431.
7. Bionaz, M., E. Trevisi, L. Calamari, F. Librandi, A. Ferrari, and G. Bertoni. 2007. Plasma paraoxonase, health, inflammatory conditions, and liver function in transition dairy cows. J. Dairy Sci. 90:1740-1750.
8. Bjarnason, I., A. MacPherson, and D. Hollander. 1995. Intestinal permeability: An overview. Gastroenterology 108:1566-1581.
9. Bouchard, L., S. Blais, C. Desrosiers, X. Zhao, and P. Lacasse. 1999. Nitric oxide production during endotoxin-induced mastitis in the cow. J. Dairy Sci. 82:2574-2581.
10. Carlson, G. P. 1997. Fluid, electrolyte, and acid-base balance. In: J. J. Kaneko, J. W. Harvey, and M. L. Bruss, editors, Clinical biochemistry of domestic animals. Academic Press, San Diego, CA.
11. Connor, H., H. F. Woods, and J. G. Ledingham. 1983. Comparison of the kinetics and utilisation of D(-)-and L(+)-sodium lactate in normal man. Ann. Nutr. Metab. 27:481-487.
12. Danscher, M., M. B. Thoefner, P. M. H. Heegaard, C. T. Ekstrøm, and S. Jacobsen. 2011. Acute phase protein response during acute ruminal acidosis in cattle. Livest. Sci. 135:62-69.
13. Davis, C. D. 2003. Low dietary copper increases fecal free radical production, fecal water alkaline phosphatase activity and cytotoxicity in healthy men. J. Nutr. 133:522-527.
14. Dunlop, R. H. 1972. Pathogenesis of ruminant lactic acidosis. Adv. Vet. Sci. Comp. Med. 16:259-302.
15. Emmanuel, D. G. V., S. M. Dunn, and B. N. Ametaj. 2008. Feeding high proportions of barley grain stimulates an inflammatory response in dairy cows. J. Dairy Sci. 91:606-614.
16. Ewaschuk, J. B., J. M. Naylor, R. Palmer, S. J. Whiting, and G. A. Zello. 2004. D-lactate production and excretion in diarrheic calves. J. Vet. Intern. Med. 18:744-747.
17. Farhadi, A., A. Keshavarzian, E. W. Holmes, J. Fields, L. Zhang, and A. Banan. 2003. Gas chromatographic method for detection of urinary sucralose: Application to the assessment of intestinal permeability. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 784:145-154.
18. Ferré, N., J. Camps, E. Prats, E. Vilella, A. Paul, L. Figuera, and J. Joven. 2002. Serum paraoxonase activity: A new additional test for the improved evaluation of chronic liver damage. Clin. Chem. 48:261-268.
19. Garry, F. B. 2002. Indigestion in ruminants. In: B. P. Smith, editor, Large animal internal medicine. Mosby Inc., St. Louis, MO, Baltimore, MD. p. 722-747.
20. Gennari, F. J. 1998. Hypokalemia. N. Engl. J. Med. 339:451-458.
21. Giesecke, D., and P. von Wallenberg. 1985. Metabolism of D(-)lactic acid in rats given high intragastral doses. Comp. Biochem. Physiol. B 82:255-258.
22. Gilliam, M. B., M. P. Sherman, J. M. Griscavage, and L. J. Ignarro. 1993. A spectrophotometric assay for nitrate using NADPH oxidation by Aspergillus nitrate reductase. Anal. Biochem. 212:359-365.
23. Goad, D. W., C. L. Goad, and T. G. Nagaraja. 1998. Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers. J. Anim. Sci. 76:234-241.
24. Gozho, G. N., D. O. Krause, and J. C. Plaizier. 2006. Rumen lipopolysaccharide and inflammation during grain adaptation and subacute ruminal acidosis in steers. J. Dairy Sci. 89:4404-4413.
25. Gozho, G. N., D. O. Krause, and J. C. Plaizier. 2007. Ruminal lipopolysaccharide concentration and inflammatory response during grain-induced subacute ruminal acidosis in dairy cows. J. Dairy Sci. 90:856-866.
26. Harmon, D. L., R. A. Britton, and R. L. Prior. 1984. In vitro rates of oxidation and gluconeogenesis from L(+)- and D(-)lactate in bovine tissues. Comp. Biochem. Physiol. B 77:365-368.
27. Harmon, D. L., R. A. Britton, R. L. Prior, and R. A. Stock. 1985. Net portal absorption of lactate and volatile fatty acids in steers experiencing glucose-induced acidosis or fed a 70% concentrate diet ad libitum. J. Anim. Sci. 60:560-569.
28. Huber, T. L. 1976. Physiological effects of acidosis on feedlot cattle. J. Anim. Sci. 43:902-909.
29. Irwin, L. N., G. E. Mitchell, R. E. Tucker, and G. T. Schelling. 1979. Histamine, tyramine, tryptamine and electrolytes during glucose induced lactic acidosis. J. Anim. Sci. 48:367-374.
30. Ismail, M., A. Mahmound, M. Nasr, and Y. Badr. 2010. Clinical and laboratory studies on experimentally induced acute ruminal lactic acidosis in male goats. Alex. J. Vet. Sci. 31:53-62.
31. Jacobsen, S., P. H. Andersen, T. Toelboell, and P. M. H. Heegaard. 2004. Dose dependency and individual variability of the lipopolysaccharide- induced bovine acute phase protein response. J. Dairy Sci. 87:3330-3339.
32. Kezar, W. W., and D. C. Church. 1979. Ruminal changes during the onset and recovery of induced lactic acidosis in sheep. J. Anim. Sci. 49:1161-1167.
33. Khafipour, E., D. O. Krause, and J. C. Plaizier. 2009a. A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. J. Dairy Sci. 92:1060-1070.
34. Khafipour, E., D. O. Krause, and J. C. Plaizier. 2009b. Alfalfa pelletinduced subacute ruminal acidosis in dairy cows increases bacterial endotoxin in the rumen without causing inflammation. J. Dairy Sci. 92:1712-1724.
35. Kleen, J. L., G. A. Hooijer, J. Rehage, and J. P. T. M. Noordhuizen. 2003. Subacute ruminal acidosis (SARA): A review. J. Vet. Med. A Physiol. Pathol. Clin. Med. 50:406-414.
36. Lapré, J. A., H. T. De Vries, and R. Van der Meer. 1993. Cytotoxicity of fecal water is dependent on the type of dietary fat and is reduced by supplemental calcium phosphate in rats. J. Nutr. 123:578-585.
37. Lehmann, F. G., H. Hufnagel, and H. Lorenz-Meyer. 1981. Fecal intestinal alkaline phosphatase: A parameter for toxic damage of the small intestinal mucosa. Digestion 21:156-162.
38. Lettat, A., P. Nozière, M. Silberberg, D. P. Morgavi, C. Berger, and C. Martin. 2010. Experimental feed induction of ruminal lactic, propionic, or butyric acidosis in sheep. J. Anim. Sci. 88:3041-3046.
39. Littell, R., G. Milliken, W. Stroup, R. Wolfinger, and O. Schabenberger. 2006. SAS for Mixed Models. 2nd ed. SAS Institute Inc., Cary, NC.
40. Liu, H., W. Li, X. Wang, J. Li, and W. Yu. 2008. Early gut mucosal dysfunction in patients with acute pancreatitis. Pancreas 36:192-196.
41. Meddings, J. B., J. Jarand, S. J. Urbanski, J. Hardin, and D. G. Gall. 1999. Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am. J. Physiol. 276:G951-G957.
42. Melichar, B., J. Dvorák, R. Hyspler, and Z. Zadák. 2005. Intestinal permeability in the assessment of intestinal toxicity of cytotoxic agents. Chemotherapy 51:336-338.
43. Metzler-Zebeli, B. U., S. Schmitz-Esser, F. Klevenhusen, L. Podstatzky- Lichtenstein, M. Wagner, and Q. Zebeli. 2013. Grain-rich diets differently alter ruminal and colonic abundance of microbial populations and lipopolysaccharide in goats. Anaerobe 20:65-73.
44. Minuti, A., S. Ahmed, E. Trevisi, F. Piccioli-Cappelli, G. Bertoni, and P. Bani. 2013. Assessment of gastrointestinal permeability by lactulose test in sheep after repeated indomethacin treatment. J. Anim. Sci. 91:5646-5653.
45. Mohamed Nour, M., M. Abusamra, and B. E. Hago. 1998. Experimentally induced lactic acidosis in Nubian goats: Clinical, biochemical and pathological investigations. Small Rumin. Res. 31:7-17.
46. Muir, L. A., E. L. Rickes, P. F. Duquette, and G. E. Smith. 1980. Control of wheat-induced lactic acidosis in sheep by thiopeptin and related antibiotics. J. Anim. Sci. 50:547-553.
47. Nagaraja, T. G., E. E. Bartley, L. R. Fina, and H. D. Anthony. 1978. Relationship of rumen gram-negative bacteria and free endotoxin to lactic acidosis in cattle. J. Anim. Sci. 47:1329-1337.
48. Nagaraja, T. G., and G. W. Miller. 1989. Rumen microbial changes in ionophore antibiotic-treated steers with experimentally induced acidosis. Asian-Australas. J. Anim. Sci. 2:465-468.
49. Nagaraja, T. G., and E. C. Titgemeyer. 2007. Ruminal acidosis in beef cattle: The current microbiological and nutritional outlook. J. Dairy Sci. 90(Suppl. 1):E17-E38.
50. Nagaraja, T. G., and G. Towne. 1990. Ciliated protozoa in relation to ruminal acidosis and lactic acid metabolism. In: S. Hoshino, R. Onodera, H. Minato, and H. Itabashi, editors, The Rumen Ecosystem: The Microbial Metabolism and Its Regulation, Springer-Verlag, New York, NY. p. 187-194.
51. Naylor, J. M., and D. S. Kronfeld. 1986. Relationships between metabolic changes and clinical signs in pregnant sheep given endotoxin. Can. J. Vet. Res. 50:402-409.
52. Nikolov, Y. 1998. Clinical experimental studies on acute rumen acidosis in buffaloes (Bubalus bubalis L.). V. Influence on several blood and rumen biochemical parameters. Vet. Arh. 68:205-212.
53. Nikolov, Y. 2003. Clinical experimental studies on acute rumen acidosis in sheep with a pre-existing chronic lead and organophosphorus compound intoxication. I. Clinical and haematological changes. Trakia J. Sci. 1:61-66.
54. Nocek, J. E. 1997. Bovine acidosis: Implications on laminitis. J. Dairy Sci. 80:1005-1028.
55. Odongo, N. E., S. L. Greenwood, M. M. Or-Rashid, D. Radford, O. Alzahal, A. K. Shoveller, M. I. Lindinger, J. C. Matthews, and B. W. McBride. 2009. Effects of nutritionally induced metabolic acidosis with or without glutamine infusion on acid-base balance, plasma amino acids, and plasma nonesterified fatty acids in sheep. J. Anim. Sci. 87:1077-1084.
56. Patra, R. C., S. B. Lal, and D. Swarup. 1996. Biochemical profile of rumen liquor, blood and urine in experimental acidosis in sheep. Small Rumin. Res. 19:177-180.
57. Plaizier, J. C., E. Khafipour, S. Li, G. N. Gozho, and D. O. Krause. 2012. Subacute ruminal acidosis (SARA), endotoxins and health consequences. Anim. Feed Sci. Technol. 172:9-21.
58. Plaizier, J. C., D. O. Krause, G. N. Gozho, and B. W. McBride. 2008. Subacute ruminal acidosis in dairy cows: The physiological causes, incidence and consequences. Vet. J. 176:21-31.
59. Prior, R. L. 1983. Plasma clearance of L- and D-lactate in steers fed alfalfa hay or high concentrate diets. J. Anim. Sci. 57:1029-1036.
60. Saleem, F., B. N. Ametaj, S. Bouatra, R. Mandal, Q. Zebeli, S. M. Dunn, and D. S. Wishart. 2012. A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. J. Dairy Sci. 95:6606-6623.
61. Schietroma, M., B. Pessia, F. Carlei, E. M. Cecilia, and G. Amicucci. 2013. Intestinal permeability, systemic endotoxemia, and bacterial translocation after open or laparoscopic resection for colon cancer: A prospective randomized study. Int. J. Colorectal Dis. 28:1651-1660.
62. Schweigel, M., and H. Martens. 2000. Magnesium transport in the gastrointestinal tract. Front. Biosci. 5:D666-D677.
63. Skinner, J. G., R. A. Brown, and L. Roberts. 1991. Bovine haptoglobin response in clinically defined field conditions. Vet. Rec. 128:147-149.
64. Slyter, L. L. 1976. Influence of acidosis on rumen function. J. Anim. Sci. 43:910-929.
65. Slyter, L.L., and T. S. Rumsey. 1991. Effect of coliform bacteria, feed deprivation, and pH on ruminal D-lactic acid production by steer or continuous-culture microbial populations changed from forage to concentrates. J. Anim. Sci. 69:3055-3066.
66. Steele, M. A., O. AlZahal, S. E. Hook, J. Croom, and B. W. McBride. 2009. Ruminal acidosis and the rapid onset of ruminal parakeratosis in a mature dairy cow: A case report. Acta Vet. Scand. 51:39.
67. Sun, Y., R. A. Ahokas, S. K. Bhattacharya, I. C. Gerling, L. D. Carbone, and K. T. Weber. 2006. Oxidative stress in aldosteronism. Cardiovasc. Res. 71:300-309.
68. Sunderman, F. W., and S. Nomoto. 1970. Measurement of human serum ceruloplasmin by its p-phenylenediamine oxidase activity. Clin. Chem. 16:903-910.
69. Taché, S., G. Parnaud, E. Van Beek, and D. E. Corpet. 2006. Polyethylene glycol, unique among laxatives, suppresses aberrant crypt foci, by elimination of cells. Scand. J. Gastroenterol. 41:730-736.
70. Thomas, D. W., and D. H. Henton. 1985. The use of fecal alkaline phosphatase as an indicator of intestinal damage. Digestion 31:82-88.
71. Waldron, M. R., B. J. Nonnecke, T. Nishida, R. L. Horst, and T. R. Overton. 2003. Effect of lipopolysaccharide infusion on serum macromineral and vitamin D concentrations in dairy cows. J. Dairy Sci. 86:3440-3446.
72. Yue, C., B. Ma, Y. Zhao, Q. Li, and J. Li. 2012. Lipopolysaccharideinduced bacterial translocation is intestine site-specific and associates with intestinal mucosal inflammation. Inflammation 35:1880-1888.
73. Zebeli, Q., and B. N. Ametaj. 2009. Relationships between rumen lipopolysaccharide and mediators of inflammatory response with milk fat production and efficiency in dairy cows. J. Dairy Sci. 92:3800-3809.
74. Zebeli, Q., S. M. Dunn, and B. N. Ametaj. 2010. Strong associations among rumen endotoxin and acute phase proteins with plasma minerals in lactating cows fed graded amounts of concentrate. J. Anim. Sci. 88:1545-1553.
75. Zebeli, Q., S. Sivaraman, S. M. Dunn, and B. N. Ametaj. 2011. Intermittent parenteral administration of endotoxin triggers metabolic and immunological alterations typically associated with displaced abomasum and retained placenta in periparturient dairy cows. J. Dairy Sci. 94:4968-4983.
76. Zust, J., U. Pestevsek, and A. Vengust. 2000. Impact of lactic acid fermentation in the large intestine on acute lactic acidosis in cattle. Dtsch. Tierarztl. Wochenschr. 107:359-363.