The impact of type 1 diabetes on the physiological responses to exercise

Type 1 Diabetes: Clinical Management of the Athlete

Volumn 9780857297549, Issue , 2012, Pages 29-45

  Riddell, Michael C ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84949175341     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-85729-754-9_2     Document Type: Chapter

References (100)

1. Wasserman DH. Regulation of glucose fluxes during exercise in the postabsorptive state. Annu Rev Physiol. 1995;57:191-218.
2. Wasserman DH. Berson award lecture 2008 four grams of glucose. Am J Physiol Endocrinol Metab. 2009;296(1):E11-21.
3. Levine SA, Gordon B, Derick CL. Some changes in the chemical constituents of the blood following a marathon race: with special reference to the development of hypoglycemia. J Am Med Assoc. 1924;82(22):1778-9.
4. Frayn KN. Fat as a fuel: emerging understanding of the adipose tissue-skeletal muscle axis. Acta Physiol (Oxf). 2010;199(4):509-18.
5. Dennis SC, Noakes TD, Hawley JA. Nutritional strategies to minimize fatigue during prolonged exercise: fluid, electrolyte and energy replacement. J Sports Sci. 1997;15(3):305-13.
6. Cryer PE. Hypoglycemia: still the limiting factor in the glycemic management of diabetes. Endocr Pract. 2008;14(6):750-6.
7. Cryer PE. Hierarchy of physiological responses to hypoglycemia: relevance to clinical hypoglycemia in type I (insulin dependent) diabetes mellitus. Horm Metab Res. 1997;29(3):92-6.
8. Marliss EB, Vranic M. Intense exercise has unique effects on both insulin release and its roles in glucoregulation: implications for diabetes. Diabetes. 2002;51 Suppl 1:S271-83.
9. Temple MY, Bar-Or O, Riddell MC. The reliability and repeatability of the blood glucose response to prolonged exercise in adolescent boys with IDDM. Diabetes Care. 1995;18(3):326-32.
10. Warburton DE, Nicol CW, Bredin SS. Prescribing exercise as preventive therapy. CMAJ. 2006;174(7):961-74.
11. Zinman B, Murray FT, Vranic M, Albisser AM, Leibel BS, McClean PA, et al. Glucoregulation during moderate exercise in insulin treated diabetics. J Clin Endocrinol Metab. 1977;45(4):641-52.
12. Camacho RC, Galassetti P, Davis SN, Wasserman DH. Glucoregulation during and after exercise in health and insulin-dependent diabetes. Exerc Sport Sci Rev. 2005;33(1):17-23.
13. Tuominen JA, Karonen SL, Melamies L, Bolli G, Koivisto VA. Exercise-induced hypoglycaemia in IDDM patients treated with a short-acting insulin analogue. Diabetologia. 1995;38(1):106-11.
14. Rabasa-Lhoret R, Bourque J, Ducros F, Chiasson JL. Guidelines for premeal insulin dose reduction for postprandial exercise of different intensities and durations in type 1 diabetic subjects treated intensively with a basal-bolus insulin regimen (ultralente-lispro). Diabetes Care. 2001;24(4):625-30.
15. Berger M, Halban PA, Assal JP, Offord RE, Vranic M, Renold AE. Pharmacokinetics of subcutaneously injected tritiated insulin: effects of exercise. Diabetes. 1979;28 Suppl 1:53-7.
16. Gerich JE, Langlois M, Noacco C, Karam JH, Forsham PH. Lack of glucagon response to hypoglycemia in diabetes: evidence for an intrinsic pancreatic alpha cell defect. Science. 1973;182(108):171-3.
17. Orskov L, Alberti KG, Mengel A, Moller N, Pedersen O, Rasmussen O, et al. Decreased hepatic glucagon responses in type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1991;34(7):521-6.
18. Schneider SH, Vitug A, Ananthakrishnan R, Khachadurian AK. Impaired adrenergic response to prolonged exercise in type I diabetes. Metabolism. 1991;40(11):1219-25.
19. Galassetti P, Tate D, Neill RA, Morrey S, Wasserman DH, Davis SN. Effect of antecedent hypoglycemia on counterregulatory responses to subsequent euglycemic exercise in type 1 diabetes. Diabetes. 2003;52(7):1761-9.
20. Cline GW, Rothman DL, Magnusson I, Katz LD, Shulman GI. 13C-nuclear magnetic resonance spectroscopy studies of hepatic glucose metabolism in normal subjects and subjects with insulin-dependent diabetes mellitus. J Clin Invest. 1994;94(6):2369-76.
21. Chokkalingam K, Tsintzas K, Snaar JE, Norton L, Solanky B, Leverton E, et al. Hyperinsulinaemia during exercise does not suppress hepatic glycogen concentrations in patients with type 1 diabetes: a magnetic resonance spectroscopy study. Diabetologia. 2007;50(9):1921-9.
22. Sigal RJ, Purdon C, Fisher SJ, Halter JB, Vranic M, Marliss EB. Hyperinsulinemia prevents prolonged hyperglycemia after intense exercise in insulin-dependent diabetic subjects. J Clin Endocrinol Metab. 1994;79(4):1049-57.
23. Sigal R, Kenny G, Oh P, Perkins BA, Plotnikoff RC, Prud'homme D, et al. Physical activity and diabetes. Canadian diabetes association clinical practice guidelines expert committee. Canadian diabetes association 2008 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes. 2008;32(1):S37-9.
24. Robertson K, Adolfsson P, Scheiner G, Hanas R, Riddell MC. Exercise in children and adolescents with diabetes. Pediatr Diabetes. 2009;10 Suppl 12:154-68.
25. Brooks GA. Cell-cell and intracellular lactate shuttles. J Physiol. 2009;587(Pt 23):5591-600.
26. Lee AD, Hansen PA, Schluter J, Gulve EA, Gao J, Holloszy JO. Effects of epinephrine on insulin-stimulated glucose uptake and GLUT-4 phosphorylation in muscle. Am J Physiol. 1997;273(3 Pt 1):C1082-7.
27. Purdon C, Brousson M, Nyveen SL, Miles PD, Halter JB, Vranic M, et al. The roles of insulin and catecholamines in the glucoregulatory response during intense exercise and early recovery in insulin-dependent diabetic and control subjects. J Clin Endocrinol Metab. 1993;76(3):566-73.
28. Bussau VA, Ferreira LD, Jones TW, Fournier PA. A 10-s sprint performed prior to moderateintensity exercise prevents early post-exercise fall in glycaemia in individuals with type 1 diabetes. Diabetologia. 2007;50(9):1815-8.
29. Bussau VA, Ferreira LD, Jones TW, Fournier PA. The 10-s maximal sprint: a novel approach to counter an exercise-mediated fall in glycemia in individuals with type 1 diabetes. Diabetes Care. 2006;29(3):601-6.
30. Yardley JE, Sigal RJ, Perkins BA, Riddell M. Performing resistance exercise before aerobic exercise reduces the risk of hypoglycemia in type 1 diabetes: a study using continuous glucose monitoring. Can J Diabetes. 2010;34(3):247.
31. Guelfi KJ, Ratnam N, Smythe GA, Jones TW, Fournier PA. Effect of intermittent high-intensity compared with continuous moderate exercise on glucose production and utilization in individuals with type 1 diabetes. Am J Physiol Endocrinol Metab. 2007;292(3):E865-70.
32. Iscoe KE, Riddell MC. Continuous moderate-intensity exercise with or without intermittent high-intensity work: effects on acute and late glycaemia in athletes with type 1 diabetes mellitus. Diabet Med. 2011;28(7):824-32.
33. Delvecchio M, Zecchino C, Salzano G, Faienza MF, Cavallo L, De Luca F, et al. Effects of moderate-severe exercise on blood glucose in type 1 diabetic adolescents treated with insulin pump or glargine insulin. J Endocrinol Invest. 2009;32(6):519-24.
34. MacDonald MJ. Post-exercise late-onset hypoglycemia in insulin-dependent diabetic patients. Diabetes Care. 1987;10(5):584-8.
35. Taplin CE, Cobry E, Messer L, McFann K, Chase HP, Fiallo-Scharer R. Preventing post-exercise nocturnal hypoglycemia in children with type 1 diabetes. J Pediatr. 2010;157(5):784-8.e1.
36. Iscoe KE, Campbell JE, Jamnik V, Perkins BA, Riddell MC. Efficacy of continuous real-time blood glucose monitoring during and after prolonged high-intensity cycling exercise: spinning with a continuous glucose monitoring system. Diabetes Technol Ther. 2006;8(6):627-35.
37. Iscoe KE, Corcoran M, Riddell MC. High rates of nocturnal hypoglycemia in a unique sports camp for athletes with type 1 diabetes: lessons learned from continuous glucose monitoring. Can J Diabetes. 2008;32(3):182-9.
38. Tsalikian E, Mauras N, Beck RW, Tamborlane WV, Janz KF, Chase HP, et al. Impact of exercise on overnight glycemic control in children with type 1 diabetes mellitus. J Pediatr. 2005;147(4):528-34.
39. Maran A, Pavan P, Bonsembiante B, Brugin E, Ermolao A, Avogaro A, et al. Continuous glucose monitoring reveals delayed nocturnal hypoglycemia after intermittent high-intensity exercise in nontrained patients with type 1 diabetes. Diabetes Technol Ther. 2010;12(10):763-8.
40. McMahon SK, Ferreira LD, Ratnam N, Davey RJ, Youngs LM, Davis EA, et al. Glucose requirements to maintain euglycemia after moderate-intensity afternoon exercise in adolescents with type 1 diabetes are increased in a biphasic manner. J Clin Endocrinol Metab. 2007;92(3):963-8.
41. Krzentowski G, Pirnay F, Pallikarakis N, Luyckx AS, Lacroix M, Mosora F, et al. Glucose utilization during exercise in normal and diabetic subjects. The role of insulin. Diabetes. 1981;30(12):983-9.
42. Ramires PR, Forjaz CL, Strunz CM, Silva ME, Diament J, Nicolau W, et al. Oral glucose ingestion increases endurance capacity in normal and diabetic (type I) humans. J Appl Physiol. 1997;83(2):608-14.
43. Riddell MC, Bar-Or O, Hollidge-Horvat M, Schwarcz HP, Heigenhauser GJ. Glucose ingestion and substrate utilization during exercise in boys with IDDM. J Appl Physiol. 2000;88(4):1239-46.
44. Francescato MP, Geat M, Fusi S, Stupar G, Noacco C, Cattin L. Carbohydrate requirement and insulin concentration during moderate exercise in type 1 diabetic patients. Metabolism. 2004;53(9):1126-30.
45. Robitaille M, Dube MC, Weisnagel SJ, Prud'homme D, Massicotte D, Peronnet F, et al. Substrate source utilization during moderate intensity exercise with glucose ingestion in type 1 diabetic patients. J Appl Physiol. 2007;103(1):119-24.
46. Wahren J, Hagenfeldt L, Felig P. Splanchnic and leg exchange of glucose, amino acids, and free fatty acids during exercise in diabetes mellitus. J Clin Invest. 1975;55(6):1303-14.
47. Murray FT, Zinman B, McClean PA, Denoga A, Albisser AM, Leibel BS, et al. The metabolic response to moderate exercise in diabetic man receiving intravenous and subcutaneous insulin. J Clin Endocrinol Metab. 1977;44(4):708-20.
48. Raguso CA, Coggan AR, Gastaldelli A, Sidossis LS, Bastyr 3rd EJ, Wolfe RR. Lipid and carbohydrate metabolism in IDDM during moderate and intense exercise. Diabetes. 1995;44(9):1066-74.
49. Nathan DM, Madnek SF, Delahanty L. Programming pre-exercise snacks to prevent postexercise hypoglycemia in intensively treated insulin-dependent diabetics. Ann Intern Med. 1985;102(4):483-6.
50. Riddell MC, Bar-Or O, Ayub B V, Calvert RE, Heigenhauser GJ. Glucose ingestion matched with total carbohydrate utilization attenuates hypoglycemia during exercise in adolescents with IDDM. Int J Sport Nutr. 1999;9(1):24-34.
51. Shilo S, Shamoon H. Abnormal growth hormone responses to hypoglycemia and exercise in adults with type I diabetes. Isr J Med Sci. 1990;26(3):136-41.
52. Shilo S, Sotsky M, Shamoon H. Islet hormonal regulation of glucose turnover during exercise in type 1 diabetes. J Clin Endocrinol Metab. 1990;70(1):162-72.
53. Simonson DC, Koivisto V, Sherwin RS, Ferrannini E, Hendler R, Juhlin-Dannfelt A, et al. Adrenergic blockade alters glucose kinetics during exercise in insulin-dependent diabetics. J Clin Invest. 1984;73(6):1648-58.
54. West DJ, Stephens JW, Bain SC, Kilduff LP, Luzio S, Still R, et al. A combined insulin reduction and carbohydrate feeding strategy 30 min before running best preserves blood glucose concentration after exercise through improved fuel oxidation in type 1 diabetes mellitus. J Sports Sci. 2011;29(3):279-89.
55. Francescato MP, Carrato S. Management of exercise-induced glycemic imbalances in type 1 diabetes. Curr Diabetes Rev. 2011;7(4):253-63.
56. Chase HP, Lockspeiser T, Peery B, Shepherd M, MacKenzie T, Anderson J, et al. The impact of the diabetes control and complications trial and humalog insulin on glycohemoglobin levels and severe hypoglycemia in type 1 diabetes. Diabetes Care. 2001;24(3):430-4.
57. Hamilton J, Daneman D. Deteriorating diabetes control during adolescence: physiological or psychosocial? J Pediatr Endocrinol Metab. 2002;15(2):115-26.
58. Komatsu WR, Gabbay MA, Castro ML, Saraiva GL, Chacra AR, de Barros Neto TL, et al. Aerobic exercise capacity in normal adolescents and those with type 1 diabetes mellitus. Pediatr Diabetes. 2005;6(3):145-9.
59. Baraldi E, Monciotti C, Filippone M, Santuz P, Magagnin G, Zanconato S, et al. Gas exchange during exercise in diabetic children. Pediatr Pulmonol. 1992;13(3):155-60.
60. Gusso S, Hofman P, Lalande S, Cutfield W, Robinson E, Baldi JC. Impaired stroke volume and aerobic capacity in female adolescents with type 1 and type 2 diabetes mellitus. Diabetologia. 2008;51(7):1317-20.
61. Huttunen NP, Kaar ML, Knip M, Mustonen A, Puukka R, Akerblom HK. Physical fitness of children and adolescents with insulin-dependent diabetes mellitus. Ann Clin Res. 1984;16(1):1-5.
62. Larsson Y, Persson B, Sterky G, Thoren C. Functional adaptation to rigorous training and exercise in diabetic and nondiabetic adolescents. J Appl Physiol. 1964;19:629-35.
63. Larsson YA, Sterky GC, Ekengren KE, Moller TG. Physical fitness and the influence of training in diabetic adolescent girls. Diabetes. 1962;11:109-17.
64. Poortmans JR, Saerens P, Edelman R, Vertongen F, Dorchy H. Influence of the degree of metabolic control on physical fitness in type I diabetic adolescents. Int J Sports Med. 1986;7(4):232-5.
65. Larsen S, Brynjolf I, Birch K, Munck O, Sestoft L. The effect of continuous subcutaneous insulin infusion on cardiac performance during exercise in insulin-dependent diabetics. Scand J Clin Lab Invest. 1984;44(8):683-91.
66. Nugent AM, Steele IC, al-Modaris F, Vallely S, Moore A, Campbell NP, et al. Exercise responses in patients with IDDM. Diabetes Care. 1997;20(12):1814-21.
67. Veves A, Saouaf R, Donaghue VM, Mullooly CA, Kistler JA, Giurini JM, et al. Aerobic exercise capacity remains normal despite impaired endothelial function in the micro- and macrocirculation of physically active IDDM patients. Diabetes. 1997;46(11):1846-52.
68. Ditzel J, Standl E. The problem of tissue oxygenation in diabetes mellitus. Acta Med Scand Suppl. 1975;578:59-68.
69. Kivela R, Silvennoinen M, Touvra AM, Lehti TM, Kainulainen H, Vihko V. Effects of experimental type 1 diabetes and exercise training on angiogenic gene expression and capillarization in skeletal muscle. FASEB J. 2006;20(9):1570-2.
70. Valerio G, Spagnuolo MI, Lombardi F, Spadaro R, Siano M, Franzese A. Physical activity and sports participation in children and adolescents with type 1 diabetes mellitus. Nutr Metab Cardiovasc Dis. 2007;17(5):376-82.
71. Krause MP, Riddell MC, Hawke TJ. Effects of type 1 diabetes mellitus on skeletal muscle: clinical observations and physiological mechanisms. Pediatr Diabetes. 2011;12(4 Pt 1):345-64.
72. Andersen H, Gadeberg PC, Brock B, Jakobsen J. Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia. 1997;40(9):1062-9.
73. Andersen H, Stalberg E, Gjerstad MD, Jakobsen J. Association of muscle strength and electrophysiological measures of reinnervation in diabetic neuropathy. Muscle Nerve. 1998;21(12):1647-54.
74. Andersen H. Muscular endurance in long-term IDDM patients. Diabetes Care. 1998;21(4):604-9.
75. Andersen H, Gjerstad MD, Jakobsen J. Atrophy of foot muscles: a measure of diabetic neuropathy. Diabetes Care. 2004;27(10):2382-5.
76. Andreassen CS, Jakobsen J, Ringgaard S, Ejskjaer N, Andersen H. Accelerated atrophy of lower leg and foot muscles-a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI). Diabetologia. 2009;52(6):1182-91.
77. Andreassen CS, Jakobsen J, Flyvbjerg A, Andersen H. Expression of neurotrophic factors in diabetic muscle-relation to neuropathy and muscle strength. Brain. 2009;132(Pt 10):2724-33.
78. Almeida S, Riddell MC, Cafarelli E. Slower conduction velocity and motor unit discharge frequency are associated with muscle fatigue during isometric exercise in type 1 diabetes mellitus. Muscle Nerve. 2008;37(2):231-40.
79. Surridge DH, Erdahl DL, Lawson JS, Donald MW, Monga TN, Bird CE, et al. Psychiatric aspects of diabetes mellitus. Br J Psychiatry. 1984;145:269-76.
80. Van der Does FE, De Neeling JN, Snoek FJ, Kostense PJ, Grootenhuis PA, Bouter LM, et al. Symptoms and well-being in relation to glycemic control in type II diabetes. Diabetes Care. 1996;19(3):204-10.
81. Riddell MC, Bar-Or O, Gerstein HC, Heigenhauser GJ. Perceived exertion with glucose ingestion in adolescent males with IDDM. Med Sci Sports Exerc. 2000;32(1):167-73.
82. Crowther GJ, Milstein JM, Jubrias SA, Kushmerick MJ, Gronka RK, Conley KE. Altered energetic properties in skeletal muscle of men with well-controlled insulin-dependent (type 1) diabetes. Am J Physiol Endocrinol Metab. 2003;284(4):E655-62.
83. Jenni S, Oetliker C, Allemann S, Ith M, Tappy L, Wuerth S, et al. Fuel metabolism during exercise in euglycaemia and hyperglycaemia in patients with type 1 diabetes mellitus-a prospective single-blinded randomised crossover trial. Diabetologia. 2008;51(8):1457-65.
84. Magee MF, Bhatt BA. Management of decompensated diabetes. Diabetic ketoacidosis and hyperglycemic hyperosmolar syndrome. Crit Care Clin. 2001;17(1):75-106.
85. Andersen H, Schmitz O, Nielsen S. Decreased isometric muscle strength after acute hyperglycaemia in type 1 diabetic patients. Diabet Med. 2005;22(10):1401-7.
86. Boehncke S, Poettgen K, Maser-Gluth C, Reusch J, Boehncke WH, Badenhoop K. Endurance capabilities of triathlon competitors with type 1 diabetes mellitus. Dtsch Med Wochenschr. 2009;134(14):677-82.
87. Bosch AN, Kirkman MC. Maintenance of hyperglycaemia does not improve performance in a 100 km cycling time trial. S Afr J Sports Med. 2007;19(3):94-8.
88. Heyman E, Briard D, Dekerdanet M, Gratas-Delamarche A, Delamarche P. Accuracy of physical working capacity 170 to estimate aerobic fitness in prepubertal diabetic boys and in 2 insulin dose conditions. J Sports Med Phys Fitness. 2006;46(2):315-21.
89. Stettler C, Jenni S, Allemann S, Steiner R, Hoppeler H, Trepp R, et al. Exercise capacity in subjects with type 1 diabetes mellitus in eu- and hyperglycaemia. Diabetes Metab Res Rev. 2006;22(4):300-6.
90. Kelly D, Hamilton JK, Riddell MC. Blood glucose levels and performance in a sports camp for adolescents with type 1 diabetes mellitus: a field study. Int J Pediatr. 2010;2010. doi:10.1155/2010/216167. 216167. Epub 2010 Aug. 2.
91. Gonder-Frederick LA, Zrebiec JF, Bauchowitz AU, Ritterband LM, Magee JC, Cox DJ, et al. Cognitive function is disrupted by both hypo- and hyperglycemia in school-aged children with type 1 diabetes: a field study. Diabetes Care. 2009;32(6):1001-6.
92. Jimenez CC, Corcoran MH, Crawley JT, Guyton Hornsby W, Peer KS, Philbin RD, et al. National athletic trainers' association position statement: management of the athlete with type 1 diabetes mellitus. J Athl Train. 2007;42(4):536-45.
93. Goodyear LJ, Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med. 1998;49:235-61.
94. Chu L, Hamilton J, Riddell MC. Clinical management of the physically active patient with type 1 diabetes. Phys Sportsmed. 2011;39(2):64-77.
95. Seeger JP, Thijssen DH, Noordam K, Cranen ME, Hopman MT, Nijhuis-van der Sanden MW. Exercise training improves physical fitness and vascular function in children with type 1 diabetes. Diabetes Obes Metab. 2011;13(4):382-4.
96. Heyman E, Toutain C, Delamarche P, Berthon P, Briard D, Youssef H, et al. Exercise training and cardiovascular risk factors in type 1 diabetic adolescent girls. Pediatr Exerc Sci. 2007;19(4):408-19.
97. Harmer AR, Chisholm DJ, McKenna MJ, Hunter SK, Ruell PA, Naylor JM, et al. Sprint training increases muscle oxidative metabolism during high-intensity exercise in patients with type 1 diabetes. Diabetes Care. 2008;31(11):2097-102.
98. Krause Mda S, de Bittencourt Jr PI. Type 1 diabetes: can exercise impair the autoimmune event? The L-arginine/glutamine coupling hypothesis. Cell Biochem Funct. 2008;26(4):406-33.
99. Moy CS, Songer TJ, LaPorte RE, Dorman JS, Kriska AM, Orchard TJ, et al. Insulindependent diabetes mellitus, physical activity, and death. Am J Epidemiol. 1993;137(1):74-81.
100. Coker RH, Kjaer M. Glucoregulation during exercise: the role of the neuroendocrine system. Sports Med. 2005;35(7):575-83.