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Muscle energetics in exercising horses

Published online by Cambridge University Press:  01 November 2007

Dominique-Marie Votion ,
Rachel Navet ,
Véronique Anne Lacombe ,
Francis Sluse ,
Birgitta Essén-Gustavsson ,
Kenneth William Hinchcliff ,
José-Luis L. Rivero ,
Didier Serteyn  and
Stephanie Valberg
Dominique-Marie Votion*
Affiliation:
Equine Teaching Hospital, University of Liege, Liège, Belgium Equine European Centre of Mont-Le-Soie, University of Liege, Liège, Belgium
Rachel Navet
Affiliation:
Laboratory of Bioenergetics, University of Liege, Liège, Belgium
Véronique Anne Lacombe
Affiliation:
College of Pharmacy, The Ohio State University, Columbus, OH, USA
Francis Sluse
Affiliation:
Laboratory of Bioenergetics, University of Liege, Liège, Belgium
Birgitta Essén-Gustavsson
Affiliation:
Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
Kenneth William Hinchcliff
Affiliation:
Faculty of Veterinary Science, University of Melbourne, Werribee, Victoria, Australia
José-Luis L. Rivero
Affiliation:
Muscle Biology Laboratory, Department of Comparative Anatomy and Pathological Anatomy, Faculty of Veterinary Science, University of Cordoba, Cordoba, Spain
Didier Serteyn
Affiliation:
Equine Teaching Hospital, University of Liege, Liège, Belgium
Stephanie Valberg
Affiliation:
Department of Veterinary Population Medicine, University of Minnesota, St Paul, MN, USA
*
*Corresponding author: [email protected]
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Abstract

An optimally functional musculoskeletal system is crucial for athletic performance and even minor perturbations can limit athletic ability. The introduction of the muscle biopsy technique in the 1970s created a window of opportunity to examine the form and function of equine skeletal muscle. Muscle histochemical and biochemical analyses have allowed characterization of the properties of equine muscle fibres and their influence on, and adaptation to, physical exertion. Analyses of exercise responses during standardized treadmill exercise and field studies have illustrated the role of cellular energetics in determining athletic suitability for specific disciplines, mechanisms of fatigue, adaptations to training and the affect of diet on metabolic responses. This article provides a review of the tools available to study muscle energetics in the horse, discusses the muscular metabolic pathways and summarizes the energetics of exercise.

Keywords

muscle biopsyexerciseglycogenglucoselipidmuscle fibre
Type
Review Article
Information
Equine and Comparative Exercise Physiology , Volume 4 , Issue 3-4 , November 2007 , pp. 105 - 118
Copyright
Copyright © Cambridge University Press 2008

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References

1Metzler, DE and Metzler, CM (2001). The organisation of metabolism. In: Metzler, DE (ed.) Biochemistry: the Chemical Reactions of Living Cells. 2nd edn. Burlington: Harcourt/Academic Press, pp. 939–1011.Google Scholar
2Metzler, DE and Metzler, CM (2001). The chemistry of movement. In: Metzler, DE (ed.) Biochemistry: the Chemical Reactions of Living Cells. 2nd edn.Burlington: Harcourt/Academic Press, pp. 1089–1127.Google Scholar
3Rivero, JLL and Piercy, RJ (2004). Muscle physiology: responses to exercise and training. In: Hinchliff, KW, Kaneps, AJ and Geor, RJ (eds) Equine Sports Medicine and Surgery. London: Saunders, pp. 45–76.CrossRefGoogle Scholar
4Lindholm, A and Piehl, K (1974). Fibre composition, enzyme activity and concentrations of metabolites and electrolytes in muscles of Standardbred horses. Acta Veterinaria Scandinavica 15: 287–309.CrossRefGoogle ScholarPubMed
5Snow, DH and Guy, PS (1976). Percutaneous needle muscle biopsy in the horse. Equine Veterinary Journal 8: 150–155.CrossRefGoogle ScholarPubMed
6Sewell, DA, Harris, RC and Marlin, DJ (1994). Skeletal muscle characteristics in 2 year-old race-trained Thoroughbred horses. Comparative Biochemistry and Physiology, Comparative Physiology 108: 87–96.CrossRefGoogle ScholarPubMed
7Kline, KH and Bechtel, PJ (1988). Changes in the metabolic profile of the equine gluteus medius as a function of sampling depth. Comparative Biochemistry and Physiology Part A, Molecular & Integrative Physiology 91: 815–819.CrossRefGoogle ScholarPubMed
8Linnane, L, Serrano, AL and Rivero, JLL (1999). Distribution of fast myosin heavy chain-based muscle fibres in the gluteus medius of untrained horses: mismatch between antigenic and ATPase determinants. Journal of Anatomy 194: 363–372.CrossRefGoogle ScholarPubMed
9Grotmol, S, Totland, GK, Kryvi, H, Breistol, A, Essén-Gustavsson, B and Lindholm, A (2002). Spatial distribution of fibre types within skeletal muscle fascicles from Standardbred horses. Anatomical Record 268: 131–136.CrossRefGoogle ScholarPubMed
10Gunn, HM (1978). Differences in the histochemical properties of skeletal muscles of different breeds of horses and dogs. Journal of Anatomy 127: 615–634.Google ScholarPubMed
11Snow, DH and Guy, PS (1980). Muscle fibre type composition of a number of limb muscles in different types of horses. Research in Veterinary Science 28: 137–144.CrossRefGoogle Scholar
12Stull, CL and Albert, WW (1980). Comparison of muscle fiber types from 2-year-old fillies of the Belgian Standardbred, Thoroughbred, Quarter horse and Welsh breeds. Journal of Animal Sciences 51: 340–343.CrossRefGoogle ScholarPubMed
13van den Hoven, R, Wensing, T, Breukink, HJ, Meijer, AE and Kruip, TA (1985). Variation of fiber types in the triceps brachii, longissimus dorsi, gluteus medius, and biceps femoris of horses. American Journal of Veterinary Research 46: 939–941.Google ScholarPubMed
14López-Rivero, JL, Agüera, E, Monterde, JG, Rodríguez-Barbudo, MV and Miró, F (1989). Comparative study of muscle fibre type composition in the middle gluteal muscle of Andalusian Thoroughbred and Arabian horses. Journal of Equine Veterinary Science 9: 337–340.CrossRefGoogle Scholar
15Rivero, JLL, Galisteo, AM, Agüera, E and Miró, F (1993). Skeletal muscle histochemistry in male and female Andalusian and Arabian horses of different ages. Research in Veterinary Science 54: 160–169.CrossRefGoogle ScholarPubMed
16Karlström, K, Essén-Gustavsson, B and Lindholm, A (1994). Fibre type distribution, capillarization and enzymatic profile of locomotor and non-locomotor muscles of horses and steers. Acta Anatomica 151: 97–106.CrossRefGoogle Scholar
17Rivero, JLL, Valera, M, Serrano, AL and Vinuesa, M (1996). Variability of muscle fibre-type composition in a number of genealogical bloodlines in Arabian and Andalousian horses. Pferdeheilkunde 12: 661–665.CrossRefGoogle Scholar
18Essén-Gustavsson, B, Lindholm, A, McMiken, D, Persson, SGB and Thornton, J (1983). Skeletal muscle characteristics of young Standardbreds in relation to growth and early training. In: Snow, DH, Persson, SGB and Rose, RJ (eds) Equine Exercise Physiology. Cambridge: Granta Editions, pp. 200–210.Google Scholar
19Gottlieb, M (1989). Muscle glycogen depletion patterns during draught work in Standardbred horses. Equine Veterinary Journal 21: 110–115.CrossRefGoogle ScholarPubMed
20Snow, DH and Valberg, SJ (1994). Muscle anatomy, physiology, and adaptations to exercise and training. In: Hodgson, DR and Rose, RJ (eds) The Athletic Horse: Principles and Practice of Equine Sports Medicine. Philadelphia, PA: WB Saunders Company, pp. 145–179.Google Scholar
21Rivero, JLL, Ruz, MC, Serrano, AL and Diz, AM (1995). Effects of a 3 month endurance training programme on skeletal muscle histochemistry in Andalusian Arabian and Anglo-Arabian horses. Equine Veterinary Journal 27: 51–59.CrossRefGoogle ScholarPubMed
22Rivero, JLL (1996). Muscle biopsy as a tool for assessing muscular adaptation to training in horses. American Journal of Veterinary Research 57: 1412–1416.CrossRefGoogle ScholarPubMed
23Serrano, AL, Quiroz-Rothe, E and Rivero, JLL (2000). Early and long-term changes of equine skeletal muscle in response to endurance training and detraining. Pflügers Archiv: European Journal of Physiology 441: 263–274.CrossRefGoogle ScholarPubMed
24Serrano, AL and Rivero, JLL (2000). Myosin heavy chain profile of equine gluteus medius muscle following prolonged draught-exercise training and detraining. Journal of Muscle Research and Cell Motility 21: 235–245.CrossRefGoogle ScholarPubMed
25Dingboom, EG, van Oudheusden, H, Eizema, K and Weijs, WA (2002). Changes in fibre type composition of gluteus medius and semitendinosus muscles of Dutch Warmblood foals and the effect of exercise during the first year postpartum. Equine Veterinary Journal 34: 177–183.CrossRefGoogle ScholarPubMed
26Kim, JS, Hinchcliff, KW, Yamaguchi, M, Beard, LA, Markert, CD and Devor, ST (2005). Exercise training increases oxidative capacity and attenuates exercise-induced ultrastructural damage in skeletal muscle of aged horses. Journal of Applied Physiology 98: 334–342.CrossRefGoogle ScholarPubMed
27Rivero, JLL and Henckel, P (1996). Muscle biopsy index for discriminating between endurance horses with different performance records. Research in Veterinary Science 61: 49–54.CrossRefGoogle ScholarPubMed
28Weijs, W, Dingboom, E and van Ginkel, F (2002). Experimental analysis of error sources in fibre type counts of biopsies in horses. European Journal of Morphology 40: 145–152.CrossRefGoogle ScholarPubMed
29Essén, B, Lindholm, A and Thornton, J (1980). Histochemical properties of muscle fibres types and enzyme activities in skeletal muscles of Standardbred trotters of different ages. Equine Veterinary Journal 12: 175–180.CrossRefGoogle ScholarPubMed
30Gottlieb, M, Essén-Gustavsson, B, Lindholm, A and Persson, SGB (1989). Effects of a draft-loaded training program on skeletal muscle in the horse. Journal of Applied Physiology 67: 570–577.CrossRefGoogle ScholarPubMed
31Snow, DH and Harris, RC (1986). Comparison of biochemical changes following exercise at two sites within a muscle. Proceedings of the International Union of Physiological Sciences 16: 404–409.Google Scholar
32Gottlieb, M, Essén-Gustavsson, B, Lindholm, A and Persson, SG (1988). Circulatory and muscle metabolic responses to draught work compared to increasing trotting velocities. Equine Veterinary Journal 20: 430–434.CrossRefGoogle ScholarPubMed
33Lindner, A, Dag, S, Marti-Korff, S, Quiroz-Rothe, E, Rivero, JLL and Drommer, W (2002). Effect of repeated biopsying on muscle tissue in horses. Equine Veterinary Journal 34: 619–624.CrossRefGoogle ScholarPubMed
34Andrews, FM and Spurgeon, TL (1986). Histochemical staining characteristics of normal horse skeletal muscle. American Journal of Veterinary Research 47: 1843–1852.Google ScholarPubMed
35Hodgson, DR, Rose, RJ, Dimauro, J and Allen, JR (1986). Effects of training on muscle composition in horses. American Journal of Veterinary Research 47: 12–15.Google ScholarPubMed
36Roy, RR, Sacks, RD, Baldwin, KM, Short, M and Edgerton, VR (1984). Interrelationships of contraction time Vmax, and myosin ATPase after spinal transection. Journal of Applied Physiology 56: 1594–1601.CrossRefGoogle ScholarPubMed
37Snow, DH, Billeter, R and Jenny, E (1981). Myosin types in equine skeletal muscle fibres. Research in Veterinary Science 30: 381–382.CrossRefGoogle ScholarPubMed
38Weiss, A, McDonough, D, Wertman, B, Acakpo-Satchivi, L, Montgomery, K, Kucherlapati, R, Leinwand, L and Krauter, K (1999). Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proceedings of the National Academy of Sciences of USA 96: 2958–2963.CrossRefGoogle ScholarPubMed
39Rivero, JLL, Serrano, AL, Barrey, E, Valette, JP and Jouglin, M (1999). Analysis of myosin heavy chains at the protein level in horse skeletal muscle. Journal of Muscle Research and Cell Motility 20: 211–221.CrossRefGoogle ScholarPubMed
40Eizema, K, van den Burg, MM, Kiri, A, Dingboom, EG, van Oudheusden, H, Goldspink, G and Weijs, WA (2003). Differential expression of equine myosin heavy-chain mRNA and protein isoforms in a limb muscle. Journal of Histochemistry and Cytochemistry 51: 1207–1216.CrossRefGoogle Scholar
41Eizema, K, van den Burg, MM, de Jonge, HW, Dingboom, EG, Weijs, WA and Everts, ME (2005). Myosin heavy chain isoforms in equine gluteus medius muscle: comparison of mRNA and protein expression profiles. Journal of Histochemistry and Cytochemistry 53: 1383–1390.CrossRefGoogle ScholarPubMed
42Chikuni, K, Muroya, S and Nakajima, I (2004). Absence of the functional myosin heavy chain 2b isoform in equine skeletal muscles. Zoological Science 21: 589–596.CrossRefGoogle ScholarPubMed
43Karlström, K and Essén-Gustavsson, B (2002). Myosin heavy chain-based fibre types in red cell hyper- and normovolaemic Standardbred trotters. Equine Veterinary Journal Supplement 34: 279–282.CrossRefGoogle Scholar
44Rivero, JLL, Talmadge, R and Edgerton, VR (1999). Interrelationships of myofibrillar ATPase activity and metabolic properties of myosin heavy chain-based fibre types in rat skeletal muscle. Histochemistry and Cell Biology 111: 277–287.CrossRefGoogle ScholarPubMed
45Quiroz-Rothe, E and Rivero, JL (2001). Co-ordinated expression of contractile and non-contractile features of control equine muscle fibre types characterised by immunostaining of myosin heavy chains. Histochemistry and Cell Biology 116: 299–312.CrossRefGoogle ScholarPubMed
46Snow, DH, Baxter, P and Rose, RJ (1981). Muscle fibre composition and glycogen depletion in horses competing in an endurance ride. The Veterinary Record 108: 374–378.CrossRefGoogle Scholar
47Essen-Gustavsson, B, Karlstrom, K and Lindholm, A (1984). Fibre types, enzyme activities and substrate utilisation in skeletal muscles of horses competing in endurance rides. Equine Veterinary Journal 16: 197–202.CrossRefGoogle ScholarPubMed
48Lindholm, A, Bjerneld, H and Saltin, B (1974). Glycogen depletion pattern in muscle fibres of trotting horses. Acta Physiologica Scandinavica 90: 475–484.CrossRefGoogle ScholarPubMed
49Hodgson, DR, Rose, RJ and Allen, JR (1983). Muscle glycogen depletion and repletion patterns in horses performing various distances of endurance exercise. In: Snow, DH, Persson, SGB and Rose, RJ (eds) Equine Exercise Physiology. Cambridge: Granta Editions, pp. 229–236.Google Scholar
50Hodgson, DR, Rose, RJ, Allen, JR and Dimauro, J (1985). Glycogen depletion patterns in horses competing in day 2 of a three day event. The Cornell Veterinarian 75: 366–374.Google ScholarPubMed
51Valberg, SJ (1986). Glycogen depletion patterns in the muscle of Standardbred trotters after exercise of varying intensities and duration. Equine Veterinary Journal 18: 479–484.CrossRefGoogle Scholar
52Essén-Gustavsson, B, Blomstrand, E, Karlström, K, Lindholm, A and Persson, SGB (1991). Influence of diet on substrate metabolism during exercise. In: Persson, SGB, Lindholm, A and Jeffcott, LB (eds) Equine Exercise Physiology 3. Proceedings of the Third International Conference on Equine Exercise Physiology, Uppsala, Sweden, July 1990Davis, CA: ICEEP Publications, pp. 288–298.Google Scholar
53Yamano, S, Eto, D, Hiraga, A and Miyata, H (2006). Recruitment pattern of muscle fibre type during high intensity exercise (60–100% VO(2)max) in Thoroughbred horses. Research in Veterinary Science 80: 109–115.CrossRefGoogle Scholar
54Annandale, EJ, Valberg, SJ, Mickelson, JR and Seaquist, ER (2004). Insulin sensitivity and skeletal muscle glucose transport in horses with equine polysaccharide storage myopathy. Neuromuscular Disorders 14: 666–674.CrossRefGoogle ScholarPubMed
55van Dam, KG, van Breda, E, Schaart, G, van Ginneken, MM, Wijnberg, ID, de Graaf-Roelfsema, E, van der Kolk, JH and Keizer, HA (2004). Investigation of the expression and localisation of glucose transporter 4 and fatty acid translocase/CD36 in equine skeletal muscle. American Journal of Veterinary Research 65: 951–956.CrossRefGoogle ScholarPubMed
56Palencia, P, Quiroz-Rothe, E and Rivero, JL (2005). New insights into the skeletal muscle phenotype of equine motor neuron disease: a quantitative approach. Acta Neuropathologica (Berlin) 109: 272–284.CrossRefGoogle ScholarPubMed
57Essén-Gustavsson, B, Ronéus, N and Pösö, AR (1997). Metabolic response in skeletal muscle fibres of Standardbred trotters after racing. Comparative Biochemistry and Physiology Part B, Biochemistry and Molecular Biology 117: 431–436.CrossRefGoogle ScholarPubMed
58Ward, TL, Valberg, SJ, Adelson, DL, Abbey, CA, Binns, MM and Mickelson, JR (2004). Glycogen branching enzyme (GBE1) mutation causing equine glycogen storage disease IV. Mammalian Genome 15: 570–577.CrossRefGoogle ScholarPubMed
59Jose-Cunilleras, EJ, Hayes, KA, Toribio, RE, Mathes, LE and Hinchcliff, KW (2005). Expression of equine glucose transporter type 4 in skeletal muscle after glycogen-depleting exercise. American Journal of Veterinary Research 66: 379–385.CrossRefGoogle ScholarPubMed
60van den Hoven, R, Meijer, AE, Wensing, T and Breukink, HJ (1985). Enzyme histochemical features of equine gluteus muscle fibers. American Journal of Veterinary Research 46: 1755–1761.Google ScholarPubMed
61Valberg, S, Essén Gustavsson, B and Skoglund Wallberg, H (1988). Oxidative capacity of skeletal muscle fibres in racehorses: histochemical versus biochemical analysis. Equine Veterinary Journal 20: 291–295.CrossRefGoogle ScholarPubMed
62Geor, RJ (2001). New methods for assessing substrate utilization in horses during exercise. In: Pagan, JD and Geor, RJ (eds) Advances in Equine Nutrition II. Nottingham: Nottingham University Press, pp. 73–86.Google Scholar
63Geor, RJ, Hinchcliff, KW and Sams, RA (2000). Beta-adrenergic blockade augments glucose utilization in horses during graded exercise. Journal of Applied Physiology 89: 1086–1098.CrossRefGoogle ScholarPubMed
64Geor, RJ, Hinchcliff, KW, McCutcheon, J and Sams, RA (2000). Epinephrine inhibits exogenous glucose utilization in exercising horses. Journal of Applied Physiology 88: 1777–1790.CrossRefGoogle ScholarPubMed
65Jose-Cunilleras, E, Hinchcliff, KW, Sams, RA, Devor, ST and Linderman, JK (2002). Glycemic index of a meal fed before exercise alters substrate use and glucose flux in exercising horses. Journal of Applied Physiology 92: 117–128.CrossRefGoogle ScholarPubMed
66Pagan, JD, Geor, RJ, Harris, PA, Hoekstra, K, Gardner, S, Hudson, C and Prince, A (2002). Effects of fat adaptation on glucose kinetics and substrate oxidation during low-intensity exercise. Equine Veterinary Journal Supplement 34: 33–38.CrossRefGoogle Scholar
67Jose-Cunilleras, E, Hinchcliff, KW, Lacombe, VA, Sams, RA, Kohn, CW, Taylor, LE and Devor, ST (2006). Ingestion of starch-rich meals after exercise increases glucose kinetics but fails to enhance muscle glycogen replenishment in horses. The Veterinary Journal 171: 468–477.CrossRefGoogle ScholarPubMed
68Hayashi, T, Wojtaszewski, JFP and Goodyear, LJ (1997). Exercise regulation of glucose transport in skeletal muscle. American Journal of Physiology 273: E1039–E1051.Google ScholarPubMed
69Holloszy, JO, Constable, SH and Young, DA (1986). Activation of glucose transport in muscle by exercise. Diabetes and Metabolism Review 1: 409–423.CrossRefGoogle ScholarPubMed
70Lindholm, A and Saltin, B (1974). The physiological and biochemical response of Standardbred horses to exercise of varying speed and duration. Acta Veterinaria Scandinavica 15: 1–15.CrossRefGoogle ScholarPubMed
71Valberg, SJ, Essén-Gustavsson, B, Lindholm, A and Persson, SGB (1989). Blood chemistry and skeletal muscle metabolic responses during and after different speeds and duration of trotting. Equine Veterinary Journal 21: 91–95.CrossRefGoogle ScholarPubMed
72Essén-Gustavsson, B, Karlström, K and Lindholm, A (1984). Fibre types, enzyme activities and substrate utilization in skeletal muscles of horses competing in endurance rides. Equine Veterinary Journal 16: 197–202.CrossRefGoogle ScholarPubMed
73Essén-Gustavsson, B and Jensen-Waern, M (2002). Effect of an endurance race on muscle amino acids, pro- and macroglycogen and triglycerides. Equine Veterinary Journal Supplement 34: 209–213.CrossRefGoogle Scholar
74Harris, RC, Marlin, DJ, Snow, DH and Harkness, RA (1991). Muscle ATP loss and lactate accumulation at different work intensities in the exercising Thoroughbred horse. European Journal of Applied Physiology 62: 235–244.CrossRefGoogle ScholarPubMed
75Schuback, K and Essén-Gustavsson, B (1998). Muscle anaerobic response to a maximal treadmill exercise test in Standardbred trotters. Equine Veterinary Journal 30: 504–510.CrossRefGoogle ScholarPubMed
76Räsänen, LA, Lampinen, KJ and Pösö, RA (1995). Responses of blood and plasma lactate and plasma purines to maximal exercise and their relationship to performance in Standardbred trotters. American Journal of Veterinary Research 56: 1651–1656.CrossRefGoogle Scholar
77Essén-Gustavsson, B, Gottlieb-Vedi, M and Lindholm, A (1999). Muscle adenine nucleotide degradation during submaximal treadmill exercise to fatigue. Equine Veterinary Journal Supplement 30: 298–302.CrossRefGoogle Scholar
78Essén-Gustavsson, B and Valberg, S (1987). Blood and muscle ammonia levels in horses during treadmill exercise and after racing. In: Gillespie, JR and Robinson, NE (eds) Equine Exercise Physiology 2. Proceedings of the Second International Conference on Equine Exercise Physiology, San Diego, August, 1986. Davis, CA: ICEEP Publications, pp. 456–463.Google Scholar
79Gottlieb, M, Essén-Gustavsson, B, Lindholm, A and Persson, SGB (1987). Cardiorespiratory and muscle metabolic responses to draught work on a treadmill in Standardbred horses. In: Gillespie, JR and Robinson, NE (eds) Equine Exercise Physiology 2. Proceedings of the Second International Conference on Equine Exercise Physiology, San Diego, August, 1986. Davis, CA: ICEEP Publications, pp. 384–392.Google Scholar
80Lacombe, VA, Hinchcliff, KW, Geor, RJ and Lauderdale, MA (1999). Exercise that induces substantial muscle glycogen depletion impairs subsequent anaerobic capacity. Equine Veterinary Journal Supplement 30: 293–297.CrossRefGoogle Scholar
81Lacombe, VA, Hinchcliff, KW, Geor, RJ and Baskin, CR (2001). Muscle glycogen depletion and subsequent replenishment affect anaerobic capacity of horses. Journal of Applied Physiology 91: 1782–1790.CrossRefGoogle ScholarPubMed
82Topliff, DR, Potter, GD, Krieder, JL, Dutson, TR and Jessup, GT (1985). Diet manipulation, muscle glycogen metabolism and anaerobic work performance in the equine. Proceedings of the 9th Equine Nutrition and Physiology Symposium. East Lansing, MI: The Equine Nutrition and Physiology Society and Michigan State University, pp. 224–229.Google Scholar
83Hyyppä, S and Pösö, AR (1998). Fluid, electrolyte, and acid-base responses to exercise in racehorses. Veterinary Clinics of North America: Equine Practice 14: 121–136.Google ScholarPubMed
84Byrd, SK, McCutcheon, LJ, Hodgson, DR and Gollnick, PD (1989). Altered sarcoplasmic reticulum function after high-intensity exercise. Journal of Applied Physiology 67: 2072–2077.CrossRefGoogle ScholarPubMed
85Wilson, JA, Kronfeld, DS, Gay, LS, Williams, JH, Wilson, TM and Lindinger, MI (1998). Sarcoplasmic reticulum responses to repeated sprints are affected by conditioning of horses. Journal of Animal Sciences 76: 3065–3071.CrossRefGoogle ScholarPubMed
86Xu, KY and Becker, LC (1998). Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. Journal of Histochemistry and Cytochemistry 46: 419–427.CrossRefGoogle ScholarPubMed
87Xu, KY, Zweier, JL and Becker, LC (1995). Functional coupling between glycolysis and SR Ca transport. Circulation Research 77: 88–97.CrossRefGoogle Scholar
88Lees, SJ and Williams, JH (2004). Skeletal muscle sarcoplasmic reticulum glycogen status influences Ca2+ uptake supported by endogenously synthesized ATP. American Journal of Physiology Cellular Physiology 286: C97–C104.CrossRefGoogle ScholarPubMed
89Snow, DH, Harris, RC and Gash, SP (1985). Metabolic response of equine muscle to intermittent maximal exercise. Journal of Applied Physiology 58: 1689–1697.CrossRefGoogle ScholarPubMed
90Sewell, DA and Harris, RC (1992). Adenine nucleotide degradation in the Thoroughbred horse with increasing exercise duration. European Journal of Applied Physiology and Occupational Physiology 65: 271–277.CrossRefGoogle ScholarPubMed
91Valberg, SJ, Essén-Gustavsson, B, Lindholm, A and Persson, SGB (1985). Energy metabolism in relation to skeletal muscle fibre properties during treadmill exercise. Equine Veterinary Journal 17: 439–449.CrossRefGoogle ScholarPubMed
92Karlström, K, Essén-Gustavsson, B, Lindholm, A and Persson, S (1991). Capillary supply in relation to muscle metabolic profile and cardiocirculatory parameters. In: Persson, SGB, Lindholm, A and Jeffcott, LB (eds) Equine Exercise Physiology 3. Proceedings of the Third International Conference on Equine Exercise Physiology, Uppsala, Sweden, July 1990. Davis, CA: ICEEP Publications, pp. 239–244.Google Scholar
93Jensen-Waern, M, Lindberg, A, Johannisson, A, Grondahl, G, Lindgren, JA and Essén-Gustavsson, B (1999). The effects of an endurance ride on metabolism and neutrophil function. Equine Veterinary Journal Supplement 30: 605–609.CrossRefGoogle Scholar
94Lacombe, VA, Hinchcliff, KW and Taylor, LE (2003). Interactions of substrate availability, exercise performance, and nutrition with muscle glycogen metabolism in horses. Journal of the American Veterinary Medical Association 223: 1576–1578.CrossRefGoogle ScholarPubMed
95Snow, DH and Harris, RC (1991). Effects of daily exercise on muscle glycogen in the Thoroughbred racehorse. In: Persson, SGB, Lindholm, A and Jeffcott, LB (eds) Equine Exercise Physiology 3. Proceedings of the Third International Conference on Equine Exercise Physiology, Uppsala, Sweden, July 1990. Davis, CA: ICEEP Publications, pp. 299–304.Google Scholar
96Lacombe, VA, Hinchcliff, KW, Kohn, CW, Devor, ST and Taylor, LE (2004). Effects of feeding meals with various soluble-carbohydrate content on muscle glycogen synthesis after exercise in horses. American Journal of Veterinary Research 65: 916–923.CrossRefGoogle ScholarPubMed
97Bröjer, JT, Holm, S, Jonasson, R, Hedenström, U and Essén-Gustavsson, B (2006). Synthesis of proglycogen and macroglycogen in skeletal muscle of Standardbred trotters after intermittent execise. Equine Veterinary Journal Supplement 36: 335–339.CrossRefGoogle Scholar
98Lacombe, VA, Hinchcliff, KW, Kohn, CW, Devor, ST and Taylor, LE (2006). Effect of dietary glycemic index after exercise on blood concentrations of substrates used for muscle glycogenesis. Equine Veterinary Journal Supplement 36: 585–589.CrossRefGoogle Scholar
99Lacombe, VA, Hinchcliff, KW and Devor, ST (2003). Effects of exercise and glucose administration on content of insulin-sensitive glucose transporter in equine skeletal muscle. American Journal of Veterinary Research 64: 1500–1506.CrossRefGoogle ScholarPubMed
100Barrey, E, Valette, JP, Jouglin, M, Blouin, C and Langlois, B (1999). Heritability of percentage of fast myosin heavy chains in skeletal muscles and relationship with performance. Equine Veterinary Journal Supplement 30: 289–292.CrossRefGoogle Scholar
101Rivero, JLL, Serrano, AL and Henckel, P (1995). Activities of selected aerobic and anaerobic enzymes in the gluteus medius muscle of endurance horses with different performance records. The Veterinary Record 137: 187–192.CrossRefGoogle ScholarPubMed
102Barlow, DA, Lloyd, TT, Hellhake, P and Seder, JA (1984). Equine fibre types: a histological analysis of select Thouroughbreds yearlings. Journal of Equine Veterinary Science 4: 60–66.CrossRefGoogle Scholar
103Wood, HC, Ross, TT, Amstrong, JB and Hall, DC (1988). Variation in muscle fibre composition between successfully and unsuccessfully raced Quarter horse. Journal of Equine Veterinary Science 8: 217–220.CrossRefGoogle Scholar
104Rivero, JLL and Barrey, E (2001). Heritabilities and genetic and phenotypic parameters for gluteus medius muscle fibre type composition, fibre size and capillaries in purebred Spanish horses. Livestock Production Science 72: 233–241.CrossRefGoogle Scholar
105Essén-Gustavsson, B and Lindholm, A (1985). Muscle fibre characteristics of active and inactive Standardbred horses. Equine Veterinary Journal 17: 434–438.CrossRefGoogle ScholarPubMed
106Ronéus, M, Essén-Gustavsson, B and Arnason, T (1993). Racing performance and longitudinal changes in muscle characteristics in Standardbred trotters. Journal of Veterinary Science 13: 355–361.Google Scholar
107Kim, JS, Hinchcliff, KW, Yamaguchi, M, Beard, LA, Markert, CD and Devor, ST (2005). Age-related changes in metabolic properties of equine skeletal muscle associated with muscle plasticity. The Veterinary Journal 169: 397–403.CrossRefGoogle ScholarPubMed
108Ronéus, M, Lindholm, A and Asheim, A (1991). Muscle characteristics in Thoroughbreds of different ages and sexes. Equine Veterinary Journal 23: 207–210.CrossRefGoogle ScholarPubMed
109Guy, PS and Snow, DH (1977). The effect of training and detraining on muscle composition in the horse. Journal of Physiology 269: 33–51.CrossRefGoogle ScholarPubMed
110Snow, DH and Guy, PS (1979). The effect of training and detraining on several enzymes in horse skeletal muscle. Archives Internationales de Physiologie et de Biochimie 87: 87–93.CrossRefGoogle ScholarPubMed
111Cutmore, CM, Snow, DH and Newsholme, EA (1985). Activities of key enzymes of aerobic and anaerobic metabolism in middle gluteal muscle from trained and untrained horses. Equine Veterinary Journal 17: 354–356.CrossRefGoogle ScholarPubMed
112Essén-Gustavsson, B, McMiken, D, Karlstrom, K, Lindholm, A, Persson, S and Thornton, J (1989). Muscular adaptation of horses during intensive training and detraining. Equine Veterinary Journal 21: 27–33.CrossRefGoogle ScholarPubMed
113Rivero, JLL and Serrano, AL (1999). Skeletal myosin heavy chain composition and carriage training. Equine Veterinary Journal Supplement 30: 318–323.CrossRefGoogle Scholar
114Roneús, M, Essén-Gustavsson, B, Lindholm, A and Persson, S (1992). Skeletal muscle characteristics of young trained and untrained Standardbred trotters. Equine Veterinary Journal Supplement 24: 292–294.CrossRefGoogle ScholarPubMed
115Lindholm, A, Essén-Gustavsson, B, McMiken, D, Persson, S and Thornton, JR (1983). Muscle histochemistry and biochemistry of Thoroughbred horses during growth and training. In: Snow, DH, Persson, SGB and Rose, RJ (eds) Equine Exercise Physiology. Cambridge: Granta Editions, pp. 211–217.Google Scholar
116Ronéus, M, Essén-Gustavsson, B, Lindholm, A and Persson, S (1987). A field study of circulatory response and muscle characteristics in young Thoroughbreds. In: Gillespie, JR and Robinson, NE (eds) Equine Exercise Physiology 2. Proceedings of the Second International Conference on Equine Exercise Physiology, San Diego, August, 1986. Davis, CA: ICEEP Publications, pp. 376–383.Google Scholar
117Miyata, H, Sugiura, T, Kai, M, Hiraga, A and Tokuriki, M (1999). Muscle adaptation of Thoroughbred racehorses trained on a flat or sloped track. American Journal of Veterinary Research 60: 1536–1539.CrossRefGoogle ScholarPubMed
118Yamano, S, Eto, D, Sugiura, T, Kai, M, Hiraga, A, Tokuriki, M and Miyata, H (2002). Effect of growth and training on muscle adaptation in Thoroughbred horses. American Journal of Veterinary Research 63: 1408–1412.CrossRefGoogle ScholarPubMed
119Hinchcliff, KW, Lauderdale, MA, Dutson, J, Geor, RJ, Lacombe, VA and Taylor, LE (2002). High intensity exercise conditioning increases accumulated oxygen deficit of horses. Equine Veterinary Journal 34: 9–16.CrossRefGoogle ScholarPubMed
120Eto, D, Yamano, S, Mukai, K, Sugiura, T, Nasu, T, Tokuriki, M and Miyata, H (2004). Effect of high intensity training on anaerobic capacity of middle gluteal muscle in Thoroughbred horses. Research in Veterinary Science 76: 139–144.CrossRefGoogle ScholarPubMed
121Gansen, S, Lindner, A, Marx, S, Mosen, H and Sallmann, HP (1999). Effects of conditioning horses with lactate-guided exercise on muscle glycogen content. Equine Veterinary Journal Supplement 30: 329–331.CrossRefGoogle Scholar
122Foreman, JH, Bayly, WM, Allen, JR, Matoba, H, Grant, BD and Gollnick, PD (1990). Muscle responses of Thoroughbreds to conventional race training and detraining. American Journal of Veterinary Research 51: 909–913.CrossRefGoogle ScholarPubMed
123McCutcheon, LJ, Geor, RJ and Hinchcliff, KW (2002). Changes in skeletal muscle GLUT4 content and muscle membrane glucose transport following 6 weeks of exercise training. Equine Veterinary Journal Supplement 34: 199–204.CrossRefGoogle Scholar
124Karlström, K, Essén-Gustavsson, B and Persson, S (1995). Capillaries of muscle of red cell hypervolaemic vs. normovolaemic Standardbred horses. Equine Veterinary Journal Supplement 18: 228–230.CrossRefGoogle Scholar
125Ronéus, M, Persson, SG, Essén-Gustavsson, B and Arnason, T (1994). Skeletal muscle characteristics in red blood cell normovolaemic and hypervolaemic Standardbred racehorses. Equine Veterinary Journal 26: 319–322.CrossRefGoogle ScholarPubMed
126Pagan, JD, Essén-Gustavsson, B, Lindholm, A and Thornton, J (1987). The effect of dietary energy sources on exercise performance in Standardbred horses. In: Gillespie, JR and Robinson, NE (eds) Equine Exercise Physiology 2. Proceedings of the Second International Conference on Equine Exercise Physiology, San Diego, August, 1986. Davis, CA: ICEEP Publications, pp. 686–700.Google Scholar
127Palmgren Karlsson, C, Jansson, A, Essén-Gustavsson, B and Lindberg, JE (2002). Effect of molassed sugar beet pulp on nutrient utilisation and metabolic parameters during exercise. Equine Veterinary Journal Supplement 34: 44–49.CrossRefGoogle Scholar
128Ronéus, M and Lindholm, A (1991). Muscle characteristics in Thoroughbreds of different ages and sexes. Equine Veterinary Journal 23: 207–210.CrossRefGoogle ScholarPubMed