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Muscle Glycogen Metabolism in Horses: Interactions Between Substrate Availability, Exercise Performance and Carbohydrate Administration

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Muscle Glycogen Metabolism in Horses: Interactions Between Substrate Availability, Exercise Performance and Carbohydrate Administration MUSCLE GLYCOGEN METABOLISM IN HORSES: INTERACTIONS BETWEEN SUBSTRATE AVAILABILITY, EXERCISE PERFORMANCE AND CARBOHYDRATE ADMINISTRATION DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Véronique A. Lacombe, D.V.M * * * * The Ohio State University 2003 Dissertation Committee: Kenneth W. Hinchcliff, BVSc, Ph.D., Adviser Approved by Stephen T. Devor, Ph.D. Catherine W. Kohn, V.M.D ________________________ Stephen M. Reed, D.V.M Adviser Lynn E. Taylor, Ph.D. Department of Veterinary Clinical Sciences ABSTRACT Horses undertake recreational activities that decrease muscle glycogen stores. Similar to humans, muscle glycogen availability may influence exercise performance. In the first study, a model of glycogen depletion was developed and used to investigate the effect of muscle glycogen availability on the athletic capacity of horses. We demonstrated that exercise-induced muscle glycogen depletion was associated with a 60% decrease in anaerobic capacity during subsequent exercise, without effect on aerobic capacity. To rule out any confounding effects of other exercise-induced changes, a second study investigated the effects of muscle glycogen depletion and subsequent replenishment on athletic capacity. In a blinded crossover study, seven fit horses received either an intravenous glucose or saline infusion after exercise. Run time to fatigue, accumulated oxygen deficit and blood lactate concentration during a subsequent high- speed exercise test were greater for the horses with normal muscle glycogen concentration than for the horses with persistent muscle glycogen depletion. It was concluded that muscle glycogen availability influences anaerobic capacity and ability to perform high-intensity exercise in horses. ii Given the critical role of adequate glycogen stores in enabling optimal performance, the factors and mechanisms affecting muscle glycogen replenishment in horses were studied. We first demonstrated that intravenous glucose infusion (6g/kg) hastened muscle glycogen resynthesis compared to saline infusion. The effect of 3 isoenergetic diets of varying glycemic indices on the rates of muscle glycogen synthesis after exercise was evaluated in a crossover study. Seven horses received either a high soluble carbohydrate diet (grain, HCO), or a low soluble carbohydrate diet (hay, LCO), or a mixed diet (M) every 8 hours for 72 hours after exercise. We demonstrated that muscle glycogen resynthesis is slower in horses than in humans. Feeding high-glycemic index (HCO) meals hastened muscle glycogen replenishment compared to LCO and MCO diets by increasing blood glucose and insulin availability to skeletal muscle. Finally, insulin-sensitive glucose transporters (GLUT-4) were characterized in equine muscles by Western blotting. We demonstrated that exercise increased GLUT-4 protein content by 27%. Replenishment of muscle glycogen stores after carbohydrate administration, either by glucose infusion or diet, attenuated the increase in GLUT-4 protein content of skeletal muscle. iii To Claude, The one who makes it all worthwhile iv ACKNOWLEDGMENTS I wish to thank my adviser, Dr. Kenneth Hinchcliff, for his intellectual support, his scientific guidance and his patience throughout my graduate program at The Ohio State University. I would like also to thank Dr. Catherine Kohn and Dr. Stephen Reed for their advice and support throughout my residency and doctoral studies. A special thank you is extended to Dr. David Lamb and Dr. Stephen Devor for allowing me to use the biochemistry laboratory of the School of Physical Activity and Educational Services, and for their advice. I also thank to Dr. Lynn Taylor for her assistance in designing the experimental diets described in Chapter 5. I also wish to acknowledge Dr. Stephen Devor, Dr. Lorraine Turcotte, and Dr. Jill McCutcheon for providing me the initial instructions for the Western blot analysis. I am indebted to Marc Todd, Dr. Kate Hayes, Dr. Wayne Buck and Dr. Nongnuch Inpanbutr for assistance in setting up the immunoblot technique to characterize GLUT-4 glucose transporters in horses. I am also grateful to all the graduate and undergraduate students from The Ohio State University who assisted me at the Equine Exercise Physiology Laboratory. In particular, the assistance of Dr. Carole Baskin, Dr. Ray Geor, Maggie Lauderdale, Monica Kuklielka, Leia Hill, Samantha Siclair and Anna Wiebe was always greatly appreciated. Thanks also to Judith Dutson for her technical assistance. I also wish v to thank Tim Vojt who helped me to make the figures in Chapter 1 and to handle some computer problems. My most sincere gratitude goes to all the horses, which were involved in the studies. This research was supported by 3 grants from the Equine Research Funds of the Ohio State University and the Grayson-Jockey Club Research Foundation. My up most gratitude goes to my family and friends for the support they have given me throughout my studies, and in particular to my father. Finally, I would like to thank Claude for his love, patience and encouragement. Without his unfailing support, the completion of this work would have been neither possible nor worthwhile. vi VITA May 18, 1969 ……………………………… Born – Limoges, France 1987 ……………………………………….. Baccalaureate, France Major: Biological Sciences 1988 ……………………………………….. Baccalaureate, France Major: Mathematics and Physics 1994 ……………………………………….. D.V.M (equivalent) National Veterinary School of Alfort, France 1995……………………………………….. Dr. Med. Vet. National Veterinary School of Alfort, France 1994-1996 ………………………………… Internship, Equine Hospital National Veterinary School of Alfort, France 1996-1999 ………………………………… Resident in Equine Medicine The Ohio State University 1999-2000 ………………………………… Clinical Instructor in Equine Medicine The Ohio State University 2000-2002 ………………………………… Graduate Research Associate The Ohio State University vii PUBLICATIONS Research Publication 1. Lacombe, V.A., K.W. Hinchcliff, R.J. Geor, and C. Baskin. Muscle glycogen depletion and subsequent replenishment affect anaerobic capacity in Standardbred horses. J. Appl. Physiol. 91: 1782-1790, 2001. 2. Lacombe, V.A., M. Podell, M. Furr, S.M. Reed, M. Oglesbee, K.W. Hinchcliff, and C.W. Kohn. Diagnostic validity of electroencephalography in equine intracranial disorders. J. Vet. Int. Med. 15: 385-393, 2001. 3. Lacombe, V., K.W. Hinchcliff, R.J. Geor, and M.A. Lauderdale. Exercise that induces substantial muscle glycogen depletion impairs subsequent anaerobic capacity. Equine Vet. J. Suppl. 30: 293-297, 1999. 4. Flaminio, M.J., V.A. Lacombe, C.W. Kohn, and D.F. Antczak. Common variable immunodeficiency in a mare. J.A.V.M.A. 221: 1296-302, 1267, 2002. 5. Denoix, J.M., and V. Lacombe. Ultrasound diagnosis of meniscal injuries in horses. Pferdeheilkunde. 12: 629-631, 1996. 6. Hinchcliff, K.W., M.A. Lauderdale, J. Dutson, R.J. Geor, V.A. Lacombe, and L.E. Taylor. High-intensity exercise conditioning increases accumulated oxygen deficit of horses. Equine Vet. J. 34: 9-16, 2002. 7. Lacombe, V.A, K.W. Hinchcliff, C.W. Kohn, and L.E. Taylor. Post-exercise feeding of meals of varying glycemic index affects muscle glycogen resynthesis in horses. J. Vet. Intern. Med. 16: 336, 2002. 8. Lacombe, V.A., K.W. Hinchcliff, R.J. Geor, and C. Baskin. Enhanced muscle glycogen replenishment restores anaerobic capacity during high-intensity exercise in horses. J. Vet. Intern. Med. 14: 330, 2000. 9. Lacombe, V, S.M. Reed, K.W. Hinchcliff, C.W. Kohn, and M. Podell. Diagnostic utility of electroencephalography in equine cerebral disorders: a retrospective study. J. Vet. Intern. Med. 12: 252, 1998. 10. Lauderdale, M.A., K.W. Hinchcliff, J. Dutson, R. Geor, V. Lacombe and R. Lehnhard. High-intensity training increases anaerobic capacity but not muscle buffering capacity of Standardbreds horses. J. Vet. Intern. Med. 11: 109, 1997. viii FIELDS OF STUDY Major Field: Veterinary Clinical Sciences. Minor Field: Equine Exercise Physiology. Equine Internal Medicine. ix TABLE OF CONTENTS Page Abstract .......................................................................................................................... ii Dedication .....................................................................................................................iv Acknowledgments .......................................................................................................... v Vita ............................................................................................................................. vii List of Tables .............................................................................................................. xiii List of Figures.............................................................................................................. xiv Introduction .................................................................................................................... 1 Chapters: 1. Literature review ................................................................................................ 6 1.1 Importance of muscle glycogen as a fuel during exercise ........................... 7 1.1.1 Importance of muscle glycogen depletion during exercise ....... 7 1.1.1.1 In humans ....................................................................... 7 1.1.1.2 In horses ......................................................................... 8 1.1.2 Effect of muscle glycogen availability on endurance performance ............................................................................
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