Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T13:51:16.912Z Has data issue: false hasContentIssue false
  • English
  • Français

Exercise stress, intestinal permeability and gastric ulceration in racing Alaskan sled dogs

Published online by Cambridge University Press:  09 March 2007

Christopher M Royer ,
Michael Willard ,
Katherine Williamson ,
Jörg M Steiner ,
David A Williams  and
Michael David
Christopher M Royer
Affiliation:
Department of Physiological Sciences, College of Veterinary Medicine, Oklahoma State University, 264 McElroy Hall, Stillwater, OK 74 078, USA
Michael Willard
Affiliation:
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Texas A&M University, College Station, TX, USA
Katherine Williamson
Affiliation:
Department of Physiological Sciences, College of Veterinary Medicine, Oklahoma State University, 264 McElroy Hall, Stillwater, OK 74 078, USA
Jörg M Steiner
Affiliation:
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Texas A&M University, College Station, TX, USA
David A Williams
Affiliation:
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Texas A&M University, College Station, TX, USA
Michael David*
Affiliation:
Department of Physiological Sciences, College of Veterinary Medicine, Oklahoma State University, 264 McElroy Hall, Stillwater, OK 74 078, USA
*
*Corresponding author: msdavis@cvm.okstate.edu
Get access

Abstract

Sustained strenuous exercise has been shown to produce gastrointestinal disease in athletic species, but the causative factors remain unknown. Since exercise results in oxidative stress and hypercortisolaemia, we tested the hypothesis that oxidative and physiological stress cause gastrointestinal disease in racing Alaskan sled dogs. Dogs from three racing teams were examined before (pre) and immediately after (post) completing a 1770-km sled dog race in approximately 11 days. Serum cortisol and isoprostane concentrations were compared with markers of gastrointestinal barrier integrity and endoscopic evidence of gastric ulceration. Gastric barrier integrity was assessed by measuring the urinary recovery of sucrose and intestinal barrier integrity was assessed using the urinary recovery ratio of lactulose to rhamnose (L/R), administered together by orogastric gavage. Exercise produced a significant increase in median serum cortisol (pre: 1040, 717–2946 pg ml−1 (range); post: 8072, 2228–29 571 pg ml−1; P<0.0001) and L/R recovery ratio (pre: 0.110, 0.060–0.270; post: 0.165, 0.080–0.240; P=0.009) but not isoprostane (pre: 1007, 656–2305 pg ml−1; post: 1164, 23–4710 pg ml−1; P=0.194) concentration. The increased serum cortisol concentration was not correlated with a change in L/R recovery ratio or urine sucrose concentration. Dogs with abnormal gastric endoscopy results (61% of finishers) had higher serum cortisol concentrations than dogs with normal endoscopy results (P=0.0007). We have demonstrated concurrent hypercortisolaemia and gastrointestinal barrier dysfunction with no correlation of the two. Thus, our data do not provide support for the hypothesis that increased serum cortisol concentration causes exercise-induced gastrointestinal disease.

Keywords

gastric ulcerintestinal permeabilityexercisecortisol
Type
Research Paper
Information
Equine and Comparative Exercise Physiology , Volume 2 , Issue 1 , February 2005 , pp. 53 - 59
Copyright
Copyright © Cambridge University Press 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

1Gil, SMYazaki, E and Evans, DF (1998). Aetiology of running-related gastrointestinal dysfunction. How far is the finishing line? Sports Medicine 26: 365–378.CrossRefGoogle Scholar
2Pals, KL, Chang, RT, Ryan, AJ and Gisolfi, CV (1997). Effect of running intensity on intestinal permeability. Journal of Applied Physiology 82: 571–576.CrossRefGoogle ScholarPubMed
3Moses, FM (1990). The effect of exercise on the gastrointestinal tract. Sports Medicine 9: 159–172.CrossRefGoogle ScholarPubMed
4Michel, H, Larrey, D and Blanc, P (1994). Hepato-digestive disorders in athletic practice. Presse Medicale 23: 479–484.Google ScholarPubMed
5Choi, SC, Choi, SJ, Kim, JA, Kim, TH, Nah, YH, Yazaki, E et al. (2001). The role of gastrointestinal endoscopy in long-distance runners with gastrointestinal symptoms. European Journal of Gastroenterology & Hepatology 13: 1089–1094.CrossRefGoogle ScholarPubMed
6Baskin, CR, Hinchcliff, KW, Disilvestro, RA, Reinhart, GA, Hayek, MG, Chew, BP et al. (2000). Effects of dietary antioxidant supplementation on oxidative damage and resistance to oxidative damage during prolonged exercise in sled dogs. American Journal of Veterinary Research 61: 886–891.CrossRefGoogle ScholarPubMed
7Hinchcliff, KW, Reinhart, GA, DiSilvestro, R, Reynolds, AJ, Blostein-Fujii, A and Swenson, RA (2000). Oxidant stress in sled dogs subjected to repetitive endurance exercise. American Journal of Veterinary Research 61: 512–517.CrossRefGoogle ScholarPubMed
8Mastaloudis, A, Leonard, SW and Traber, MG (2001). Oxidative stress in athletes during extreme endurance exercise. Free Radical Biology & Medicine 31: 911–922.CrossRefGoogle ScholarPubMed
9Williams, CA, Kronfeldt, DS, Hess, TM, Saker, KE, Waldron, JN, Crandell, KM et al. (2004). Antioxidant supplementation and subsequent oxidative stress of horses during an 80-km endurance race. Journal of Animal Science 82: 588–594.CrossRefGoogle ScholarPubMed
10Child, RB, Wilkinson, DM, Fallowfield, JL, and Donnelly, AE (1998). Elevated serum antioxidant capacity and plasma malondialdehyde concentration in response to a simulated half-marathon run. Medicine and Science in Sports and Exercise 30: 1603–1607.CrossRefGoogle ScholarPubMed
11Luger, A, Deuster, PA, Kyle, SB, Gallucci, WT, Montgomery, LC, Gold, PW et al. (1987). Acute hypothalamic-pituitary-adrenal responses to the stress of treadmill exercise. Physiologic adaptations to physical training. New England Journal of Medicine 316: 1309–1315.CrossRefGoogle Scholar
12Snow, DH and Rose, RJ (1981). Hormonal changes associated with long distance exercise. Equine Veterinary Journal 13: 195–197.CrossRefGoogle ScholarPubMed
13Dybdal, NO, Gribble, D, Madigan, JE, and Stabenfelt, GH (1980). Alterations in plasma corticosteroids, insulin and selected metabolites in horses used in endurance rides. Equine Veterinary Journal 12: 137–140.CrossRefGoogle ScholarPubMed
14Rose, RJ, Hodgson, DR, Sampson, D, and Chan, W (1983). Changes in plasma biochemistry in horses competing in a 160 km endurance ride. Australian Veterinary Journal 60: 101–105.CrossRefGoogle Scholar
15Brzezinska, Z, Nazar, K and Kozlowski, S (1980). Effect of prolonged exhausting exercise on the adrenal cortex response to ACTH. Acta Physiologica Polonica 31: 567–569.Google ScholarPubMed
16Hammel, EP, Kronfeld, DS, Ganjam, VK and Dunlap, HL Jr (1977). Metabolic responses to exhaustive exercise in racing sled dogs fed diets containing medium, low, or zero carbohydrate. American Journal of Clinical Nutrition 30: 409–418.CrossRefGoogle ScholarPubMed
17Spitz, JC, Ghandi, S, Taveras, M, Aoys, E and Alverdy, JC (1996). Characteristics of the intestinal epithelial barrier during dietary manipulation and glucocorticoid stress. Critical Care Medicine 24: 635–641.CrossRefGoogle ScholarPubMed
18Martinez-Augustin, O, Sanchez de Medina, F Jr and Sanchez de Medina, M (2000). Effect of psychogenic stress on gastrointestinal function. Journal of Physiology and Biochemistry 56: 259–274.CrossRefGoogle ScholarPubMed
19Meddings, JB and Swain, MG (2000). Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat. Gastroenterology 119: 1019–1028.CrossRefGoogle ScholarPubMed
20Rohrer, CR, Hill, RC, Fischer, A, Fox, LE, Schaer, M, Ginn, PE et al. (1999). Gastric hemorrhage in dogs given high doses of methylprednisolone sodium succinate. American Journal of Veterinary Research. 60: 977–981.CrossRefGoogle ScholarPubMed
21Darmon, N, Pelissier, MA, Heyman, M, Albrecht, R, and Desjeux, JF (1993). Oxidative stress may contribute to the intestinal dysfunction of weanling rats fed a low protein diet. Journal of Nutrition 123: 1068–1075.Google Scholar
22Liaudet, L, Szabo, A, Soriano, FG, Zingarelli, B, Szabo, C and Salzman, AL (2000). Poly(ADP-ribose) synthetase mediates intestinal mucosal barrier dysfunction after mesenteric ischemia. Shock 14: 134–141.CrossRefGoogle ScholarPubMed
23Moore, K and Roberts, LJ (1998). Measurement of lipid peroxidation. Free Radical Research 28: 659–671.CrossRefGoogle ScholarPubMed
24Davis, MS, Willard, M, Nelson, S, Mandsager, RE, McKiernan, BC, Mansell, JK et al. (2003). Prevalence of gastric lesions in racing Alaskan sled dogs. Journal of Veterinary Internal Medicine 17: 311–314.CrossRefGoogle ScholarPubMed
25Davis, MS, Willard, M, Nelson, S, McCullough, S, Mandsager, RE, Roberts, JE et al. (2003). Efficacy of omeprazole for the prevention of exercise-induced gastritis in racing Alaskan sled dogs. Journal of Veterinary Internal Medicine 17: 163–166.Google ScholarPubMed
26Steiner, JM, Williams, DA and Moeller, EM (2000). Development and validation of a method for simultaneous separation and quantification of 5 different sugars in canine urine. Canadian Journal Veterinary Research 64: 164–170.Google ScholarPubMed
27Gursoy, E, Cardounel, A, Hu, Y and Kalimi, M (2001). Biological effects of long-term caloric restriction: adaptation with simultaneous administration of caloric stress plus repeated immobilization stress in rats. Experimental Biology and Medicine 226: 97–102.CrossRefGoogle ScholarPubMed
28Hinchcliff, KW, Reinhart, GA, Burr, JR, Schreier, CJ and Swenson, RA (1997). Metabolizable energy intake and sustained energy expenditure of Alaskan sled dogs during heavy exertion in the cold. American Journal of Veterinary Research 58: 1457–1462.CrossRefGoogle ScholarPubMed
29Hinchcliff, KW, Olson, J, Crusberg, C, Kenyon, J, Long, R, Royle, W et al. (1993). Serum biochemical changes in dogs competing in a long-distance sled race. Journal of the American Veterinary Medical Association 202: 401–405.CrossRefGoogle Scholar
30Quaroni, A, Tian, JQ, Goke, M and Podolsky, DK (1999). Glucocorticoids have pleiotropic effects on small intestinal crypt cells. American Journal of Physiology 277: G1027–G1040.Google ScholarPubMed
31Bjarnason, I, MacPherson, A and Hollander, D (1995). Intestinal permeability: an overview Gastroenterology 108: 1566–1581.CrossRefGoogle ScholarPubMed
32Kang, YM, Bielefeldt, K and Gebhart, GF (2004). Sensitization of mechanosensitive gastric vagal afferent fibers in the rat by thermal and chemical stimuli and gastric ulcers. Journal of Neurophysiology 91: 1981–1989.CrossRefGoogle ScholarPubMed
33Hosoi, T, Okuma, Y and Nomura, Y (2000). Electrical stimulation of afferent vagus nerve induces IL-1β expression in the brain and activates HPA axis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 279: R141–R147.CrossRefGoogle ScholarPubMed
34Vatistas, NJ, Sifferman, RL, Holste, J, Cox, JL, Pinalto, G and Schultz, KT (1999). Induction and maintenance of gastric ulceration in horses in simulated race training. Equine Veterinary Journal Supplement 29: 40–44.CrossRefGoogle Scholar
35Filaretova, L, Maltcev, N, Bogdanov, A and Levkovich, Y (1999). Role of gastric microcirculation in the gastroprotection by glucocorticoids released during water-restraint stress in rats. Chinese Journal of Physiology 42: 145–152.Google ScholarPubMed
36Filaretova, LP, Filaretov, AA and Makara, GB (1998). Corticosterone increase inhibits stress-induced gastric erosions in rats. American Journal of Physiology 274: G1024–G1030.Google ScholarPubMed
37Mastaloudis, A, Morrow, JD, Hopkins, DW, Devaraj, S and Traber, MG (2004). Antioxidant supplementation prevents exercise-induced lipid peroxidation, but not inflammation, in ultramarathon runners. Free Radical Biology & Medicine 36: 1329–1341.CrossRefGoogle Scholar
38Radak, Z, Ogonovszky, H, Dubecz, J, Pavlik, G, Sasvari, M, Pucsok, J et al. (2003). Super-marathon race increases serum and urinary nitrotyrosine and carbonyl levels. European Journal of Clinical Investigation 33: 726–730.CrossRefGoogle ScholarPubMed
39White, A, Estrada, M, Walker, K, Wisnia, P, Filgueira, G, Valdes, F et al. (2001). Role of exercise and ascorbate on plasma antioxidant capacity in thoroughbred race horses. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 128: 99–104.CrossRefGoogle ScholarPubMed
40Basu, S (1998). Metabolism of 8-iso-prostaglandin F2α. FEBS Letters 428: 32–36.CrossRefGoogle Scholar
41Salmon, JA, Mullane, KM, Dusting, GJ, Moncada, S and Vane, JR (1979). Elimination of prostacyclin (PGI2) and 6-oxo-PGF1α in anaesthetized dogs. Journal of Pharmacy and Pharmacology 31: 529–532.CrossRefGoogle Scholar
42Morrow, JD, Harris, TM and Roberts, LJ (1990). Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Analytical Biochemistry 184: 1–10.CrossRefGoogle ScholarPubMed