Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T02:09:55.114Z Has data issue: false hasContentIssue false
  • English
  • Français

Inflammatory responses to three modes of intense exercise in Standardbred mares – a pilot study

Published online by Cambridge University Press:  01 November 2008

E D Lamprecht ,
C A Bagnell  and
C A Williams
E D Lamprecht*
Affiliation:
Department of Animal Sciences, Rutgers, The State University of New Jersey, 84 Lipman Drive, Bartlett Hall, New Brunswick, NJ, USA
C A Bagnell
Affiliation:
Department of Animal Sciences, Rutgers, The State University of New Jersey, 84 Lipman Drive, Bartlett Hall, New Brunswick, NJ, USA
C A Williams
Affiliation:
Department of Animal Sciences, Rutgers, The State University of New Jersey, 84 Lipman Drive, Bartlett Hall, New Brunswick, NJ, USA
*
*Corresponding author: lamprecht@aesop.rutgers.edu
Get access

Abstract

The objective of this study was to compare exercise-induced inflammatory responses in horses undergoing three different treadmill exercise tests. Mares completed a graded exercise test (GXT), an interval exercise test (IET) and a repeated sprint exercise test (RSET). Blood and synovial fluid samples were taken 24 h before (PRE) exercise, 20–30 min, 2 and 24 h following exercise (REC). Blood was analysed for total protein, haematocrit and total nitrite concentration. Pro-inflammatory and anti-inflammatory cytokine transcripts were measured in whole blood using quantitative real-time polymerase chain reaction. Synovial fluid was analysed for total nitrite. Mares spent more time at greater than 90% of their maximum heart rate during the RSET than they did for either the GXT or IET. There was an effect of exercise test (P < 0.0001) and exercise test by sample interaction (P = 0.010) for plasma total nitrite. Pro-inflammatory cytokine transcripts and plasma total protein were elevated (P < 0.05) after exercise and there was a higher (P < 0.0001) nitrite concentration in tibiotarsal joints compared with radiocarpal joints. As hypothesised, the higher-intensity exercise test (RSET) resulted in greater nitric oxide responses as well as markers of exercise intensity compared with less intense exercise tests (IET, GXT).

Keywords

cytokinesequineexerciseinflammationnitric oxidesynovial fluid
Type
Research Paper
Information
Comparative Exercise Physiology , Volume 5 , Issue 3-4 , November 2008 , pp. 115 - 125
Copyright
Copyright © Cambridge University Press 2009

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

1Higgins, A and Lees, P (1984). The acute inflammatory process, arachidonic acid metabolism and the mode of action of anti-inflammatory drugs – a review. Equine Veterinary Journal 16: 163–175.CrossRefGoogle Scholar
2Han, J and Ulevitch, R (2005). Limiting inflammatory responses during activation of innate immunity – a review. Nature Immunology 6: 1198–1205.CrossRefGoogle Scholar
3Cannon, J and Kluger, M (1983). Endogenous pyrogen activity in human plasma after exercise. Science 220: 617–619.Google Scholar
4Moldoveanu, A, Shephard, R and Shek, P (2001). The cytokine response to physical activity and training (Review). Sports Medicine 31: 115–144.CrossRefGoogle Scholar
5Brenner, I, Natale, V, Vasiliou, P, Moldoveanu, A, Shek, P and Shephard, R (1999). Impact of three different types of exercise on components of the inflammatory response. European Journal of Applied Physiology 80: 452–460.CrossRefGoogle ScholarPubMed
6Shek, P, Sabiston, B, Buguet, A and Radomski, M (1995). Strenuous exercise and immunological changes: a multiple-time-point analysis of leukocyte subsets, CD4/CD8 ratio, immunoglobulin production and NK cell response. International Journal of Sports Medicine 15: 466–474.CrossRefGoogle Scholar
7Cannon, J (2000). Inflammatory cytokines in nonpathological states. News in Physiological Sciences 15: 298–303.Google ScholarPubMed
8Moncada, S and Higgs, A (1993). The l-arginine–nitric oxide pathway. New England Journal of Medicine 329: 2002–2012.Google ScholarPubMed
9Sureda, A, Tauler, P, Aguilo, A, Fuentespina, E, Cordova, A, Tur, J and Pons, A (2006). Blood cell NO synthesis in response to exercise. Nitric Oxide 15: 5–12.Google Scholar
10Bird, J, Wells, T, Platt, D and Bayliss, M (1997). IL-1 beta induces the degradation of equine articular cartilage by a mechanism that is not mediated by nitric oxide. Biochemical and Biophysical Research Communications 238: 81–85.CrossRefGoogle Scholar
11Kim, D, Taylor, H, Moore, R, Paulsen, D and Cho, D (2003). Articular chondrocyte apoptosis in equine osteoarthritis. The Veterinary Journal 166: 52–57.Google Scholar
12Murrell, G, Jang, D and Williams, R (1995). Nitric oxide activates metalloprotease enzymes in articular cartilage. Biochemical and Biophysical Research Communications 206: 15–21.Google Scholar
13Farrell, A, Blake, D, Parlmer, R and Moncada, S (1992). Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Annals of the Rheumatic Diseases 51: 1219–1222.Google Scholar
14Johnston, S and Fox, S (1997). Mechanisms of action of anti-inflammatory medication used for the treatment of osteoarthritis. Journal of the American Veterinary Medical Association 210: 1486–1492.CrossRefGoogle ScholarPubMed
15Dimock, A, Siciliano, P and McIlwraith, C (2000). Evidence supporting an increased presence of reactive oxygen species in the diseased equine joint. Equine Veterinary Journal 32: 439–443.CrossRefGoogle ScholarPubMed
16Van den Boom, R, van de lest, C, Bull, S, Brama, P, van Weeren, P and Barneveld, A (2005). Influence of repeated arthrocentesis and exercise on synovial fluid concentrations of nitric oxide, prostaglandin E2 and glycosaminoglycans in healthy equine joints. Equine Veterinary Journal 37: 250–256.CrossRefGoogle ScholarPubMed
17Auer, D, Ng, J, Hrdlicka, J and Seawright, A (1989). The elimination of injected superoxide dismutase from synovial fluid of the horse. Australian Veterinary Journal 66: 117–119.Google Scholar
18Henneke, D, Potter, G, Kreider, J and Yeates, B (1983). Relationship between condition score, physical measurement, and body fat percentage in mares. Equine Veterinary Journal 15: 371–372.CrossRefGoogle ScholarPubMed
19Westervelt, R, Stouffer, H, Hintz, H and Schryver, H (1976). Estimating fatness in horses and ponies. Journal of Animal Science 43: 781–785.Google Scholar
20McKeever, KH and Malinowski, K (1997). Exercise capacity in young and old mares. American Journal of Veterinary Research 58: 1468–1472.CrossRefGoogle Scholar
21Williams, C and Carlucci, S (2006). Oral vitamin E supplementation and oxidative stress, vitamin and antioxidant status in intensely exercising horses. Equine Veterinary Journal Supplement 36: 617–621.CrossRefGoogle Scholar
22Graham-Thiers, P, Kronfeld, D, Kline, K, Sklan, D and Harris, P (2003). Dietary protein and fat effects on protein status in Arabian horses during interval training and repeated sprints. Journal of Equine Veterinary Science 23: 554–559.Google Scholar
23Wilson, J, Kronfeld, D, Gay, L, Williams, J, Wilson, T and Lindinger, M (1998). Sarcoplasmic reticulum responses to repeated sprints are affected by conditioning of horses. Journal of Animal Science 76: 3065–3071.CrossRefGoogle ScholarPubMed
24Vick, M, Adams, A, Murphy, B, Sessions, D, Horohov, D, Cook, R, Shelton, B and Fitzgerald, B (2007). Relationships among inflammatory cytokines, obesity, and insulin sensitivity in the horse. Journal of Animal Science 85: 1144–1155.CrossRefGoogle ScholarPubMed
25Ainsworth, D, Appleton, J, Eicker, S, Luce, R, Flaminio, M and Antczak, F (2003). The effect of strenuous exercise on mRNA concentrations of interleukin-12, interferon-gamma and interleukin-4 in equine pulmonary and peripheral blood mononuclear cells. Veterinary. Immunology and Immunopathology 91: 61–71.Google Scholar
26Colahan, P, Kollias-Baker, C, Leutenegger, C and Jones, J (2002). Does training affect mRNA transcription for cytokine production in circulating leucocytes? Equine Veterinary Journal Supplement 34: 154–158.CrossRefGoogle Scholar
27Ostrowski, K, Rohde, T, Asp, S, Schjerling, P and Pedersen, B (1999). Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. Journal of Physiology 515: 287–291.Google Scholar
28Cross, A (1996). Novel approaches to the treatment of sepsis: lessons learned and future directions. Shock 6: 71–74.Google Scholar
29Rhind, S, Shek, P, Shinkai, S and Shephard, R (1996). Effects of moderate endurance exercise and training on in vitro lymphocyte proliferation, interleukin-2, production, and IL-2 receptor expression. European Journal of Applied Physiology 74: 348–360.CrossRefGoogle ScholarPubMed
30Peake, J, Suzuki, K, Hordern, M, Wilson, G, Nosaka, K and Coombes, J (2005). Plasma cytokine changes in relation to exercise intensity and muscle damage. European Journal of Applied Physiology 95: 514–521.Google Scholar
31Flynn, M, McFarlin, B and Markofski, M (2007). The anti-inflammatory actions of exercise training. American Journal of Lifestyle Medicine 1: 220–235.Google Scholar
32Moyna, N, Acker, G, Fulton, J, Weber, K, Goss, F, Roberson, R, Tollerud, D and Rabin, B (1996). Lymphocyte function and cytokine production during incremental exercise in active and sedentary males and females. International Journal of Sports Medicine 17: 585–591.CrossRefGoogle ScholarPubMed
33Pavlov, V and Tracey, K (2004). Review – neural regulators of innate immune responses and inflammation. Cellular and Molecular Life Sciences 61: 2322–2331.Google Scholar
34Gannon, G, Rhind, S, Suzuki, M, Shek, P and Shaphard, R (1997). Circulating levels of peripheral blood leucocytes and cytokines following competitive cycling. Canadian Journal of Applied Physiology 22: 133–147.CrossRefGoogle ScholarPubMed
35Niess, A, Passek Lorenz, I, Dickhuth, H, Northoff, H and Fehrenback, E (1999). Expression of the antioxidant stress protein heme oxygenase-I (HO-I) I human leukocytes. Acute and adaptational response to endurance exercise. Journal of Free Radicals and Biology in Medicine 26: 184–192.CrossRefGoogle Scholar
36Bruunsgaard, H, Galbo, H, Halkjaer-Kristensen, J, Johansen, T, MacLean, D and Pedersen, B (1997). Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. Journal of Physiology 499: 833–841.Google Scholar
37Northoff, H, Enkel, S and Weinstock, C (1995). Exercise, injury and immune function. Exercise Immunology Reviews 1: 1–25.Google Scholar
38Mucci, P, Durand, F, Lebel, B, Bousquet, J and Prefaut, C (2000). Interleukins 1-beta, -8, and histamine increases in highly trained, exercising athletes. Medicine and Science in Sports and Exercise 32: 1094–1100.CrossRefGoogle ScholarPubMed
39Suzuki, S, Nakaji, S, Yamada, M, Totsuka, M, Sato, K and Sugawara, K (2002). Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exercise Immunology Review 8: 6–48.Google Scholar
40Suzuki, K, Nakaji, S, Yamada, M, Liu, Q, Kurakake, S, Okamura, N, Kumae, T, Umeda, T and Sugawara, K (2003). Impact of a competitive marathon race on systemic cytokine and neutrophil responses. Medicine and Science in Sports and Exercise 35: 348–355.CrossRefGoogle ScholarPubMed
41Sprenger, H, Jacobs, C, Nain, M, Gressner, A, Prinz, H, Wesemann, W and Gemsa, D (1992). Enhanced release of cytokines, interleukin-2 receptors, and neopterin after long-distance running. Clinical Immunology and Immunopathology 63: 188–195.Google Scholar
42Petersen, A and Pedersen, B (2005). The anti-inflammatory effect of exercise. Journal of Applied Physiology 98: 1154–1162.Google Scholar
43Ostrowski, K, Hermann, C, Bangash, A, Schjerling, P, Nielsen, J and Pedersen, B (1998). A trauma-like elevation of plasma cytokines in humans in response to treadmill running. Journal of Physiology 513: 889–894.Google Scholar
44Pedersen, B (2000). Special feature for the Olympics: effects of exercise on the immune system: exercise and cytokines. Immunology and Cell Biology 78: 532–535.Google Scholar
45MacIntyre, D, Sorichter, S, Mair, J, Berg, A and McKenzie, D (2001). Markers of inflammation and myofibrillar proteins following eccentric exercise in humans. European Journal of Applied Physiology 84: 180–186.Google Scholar
46Haahr, P, Pedersen, B, Fomsgaard, A, Tvede, N, Diamant, M, Klarlund, K, Halkjaer-Kristensen, J and Bendtzen, K (1991). Effect of physical exercise on in vitro production of interleukin 1, interleukin 6, tumour necrosis factor-alpha, interleukin 2 and interferon-gamma. International Journal of Sports Medicine 12: 223–227.CrossRefGoogle ScholarPubMed
47Kindig, C, Gallatin, L, Erickson, H, Fedde, M and Poole, D (2000). Cardiorespiratory impact of the nitric oxide synthase inhibitor l-NAME in the exercising horse. Respiratory Physiology 120: 151–156.CrossRefGoogle ScholarPubMed
48Manohar, M, Goetz, T and Hassan, A (2006). Nitric oxide synthase inhibition in Thoroughbred horses augments O2 extraction at rest and submaximal exercise, but not during short-term maximal exercise. Equine Veterinary Journal Supplement 36: 481–486.Google Scholar
49Mills, P, Marlin, D, Scott, C and Smith, N (1997). Nitric oxide and thermoregulation during exercise in the horse. Journal of Applied Physiology 82: 1035–1039.CrossRefGoogle ScholarPubMed
50Cai, H and Harrison, D (2000). Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circulation Research 87: 841–844.CrossRefGoogle ScholarPubMed
51Tauler, P, Auuilo, A, Cases, N, Sureda, A, Gimenez, F, Villa, G, Cordova, A and Biescas, A (2002). Acute phase immune response to exercise coexists with decreased neutrophil antioxidant enzyme defenses. Free Radical Research 36: 1101–1107.CrossRefGoogle Scholar
52Suzuki, S, Totsuke, M, Nakaji, S, Yamada, M, Kudoh, S, Liu, Q, Sugawara, K, Yamaya, K and Sato, K (1999). Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. Journal of Applied Physiology 87: 1360–1367.CrossRefGoogle ScholarPubMed
53Clarkson, P and Thompson, H (2000). Antioxidants: what role do they play in physical activity and health? The American Journal of Clinical Nutrition Supplement 72: 637S–646S.CrossRefGoogle ScholarPubMed
54Jung, O, Marklund, S, Geiger, H, Pedrazzini, T, Busse, R and Brandes, R (2003). Extracellular superoxide dismutase is a major determinant of nitric oxide bioavailability. Circulation Research 93: 622–629.CrossRefGoogle Scholar
55Jonsson, L, Rees, D, Edlund, T and Marklund, S (2002). Nitric oxide and blood pressure in mice lacking extracellular-superoxide dismutase. Free Radical Research 36: 755–758.CrossRefGoogle ScholarPubMed
56Van den boom, R, Brama, P, Kiers, G, DeGroot, J, Barneveld, A and van Weeren, R (2004). The influence of repeated arthrocentesis and exercise on matrix metalloproteinase and tumour necrosis factor alpha activities in normal equine joints. Equine Veterinary Journal 36: 155–159.CrossRefGoogle ScholarPubMed
57Gronhahl, A and Dolvik, N (1993). Heritability estimations of osteochondrosis in the tibiotarsal joint and of bony fragments in the palmar/plantar portion of the metacarpo- and metatarsophalangeal joints of horses. Journal of the American Veterinary Medical Association 203: 101–104.Google Scholar
58Dutto, D, Hoyt, D, Cogger, E and Wickler, S (2004). Ground reaction forces in horses trotting up an incline and on the level over a range of speeds. Journal of Experimental Biology 207: 3507–3514.Google Scholar
59Fenton, J, Chlebek-Brown, K, Peters, T, Caron, J and Orth, M (2000). Glucosamine HCl reduces equine articular cartilage degradation in explant culture. Osteoarthritis and Cartilage 8: 258–265.Google Scholar
60Tung, J, Fenton, J, Arnold, C, Alexander, L, Yuzbasiyan-Gurkan, V, Venta, P, Peters, T, Orth, M, Richardson, D and Caron, J (2002). Recombinant equine interleukin-1 beta induces putative mediators of articular cartilage degradation in equine chondrocytes. Canadian Journal of Veterinary Research 66: 19–25.Google ScholarPubMed
61Stefanovic-Racic, M, Meyers, K, Meschter, C, Coffey, J, Hoffman, R and Evans, C (1994). N-monomethyl arginine, an inhibitor of nitric oxide synthase, suppresses the development of adjuvant arthritis in rats. Arthritis and Rheumatism 37: 1062–1069.Google Scholar
62Stefanovic-Racic, M, Meyers, K, Meschter, C, Coffey, J, Hoffman, R and Evans, C (1995). Comparison of the nitric oxide synthase inhibitors methylarginine and aminoguanidine as prophylactic and therapeutic agents in rat adjuvant arthritis. Journal of Rheumatology 22: 1922–1928.Google Scholar
63Wiseman, M, Henson, F, Lee, D and Bader, D (2003). Dynamic compressive strain inhibits nitric oxide synthesis by equine chondrocytes isolated from different areas of the cartilage surface. Equine Veterinary Journal 35: 451–456.CrossRefGoogle ScholarPubMed