Effects of different types of acute and chronic (training) exercise on glycaemic control in type 1 diabetes mellitus: A meta-analysis

Sports Medicine

Volumn 42, Issue 12, 2012, Pages 1059-1080

  Tonoli, Cajsa ^a,b   Heyman, Elsa ^b   Roelands, Bart ^a,c   Buyse, Luk ^a   Cheung, Stephen S ^d   Berthoin, Serge ^e   Meeusen, Romain ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIV LILLE   (France)

^c RESEARCH FOUNDATION FLANDERS FWO   (Belgium)

^d BROCK UNIVERSITY   (Canada)

^e NONE   (France)

Author keywords

diabetes mellitus; exercise; exercise intensity; glycaemic control; insulin; resistance training; sports medicine

Indexed keywords

ARTICLE; BLOOD; EXERCISE; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; META ANALYSIS; METHODOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RESISTANCE TRAINING;

BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; EXERCISE; HUMANS; RESISTANCE TRAINING;

EID: 84868683615     PISSN: 01121642     EISSN: 11792035     Source Type: Journal    
DOI: 10.2165/11635380-000000000-00000     Document Type: Review

References (94)

1. Medicine ACoS. ACSM's guidelines for exercise testing and prescription. 6th ed. Philadeplhia (PA): Lippincott Williams, Wilkins; 2000
2. MacDonald MJ. Postexercise late-onset hypoglycemia in insulin-dependent diabetic patients. Diabetes Care. 1987 Sep-Oct; 10 (5): 584-8 (Pubitemid 17158929)
3. Graveling AJ, Frier BM. Risks of marathon running and hypoglycaemia in type 1 diabetes. Diabet Med 2010 May; 27 (5): 585-8
4. Toni S, Reali MF, Barni F, et al. Managing insulin therapy during exercise in type 1 diabetes mellitus. Acta Biomed 2006; 77 Suppl. 1: 34-40 (Pubitemid 351598161)
5. Aussedat B, Dupire-Angel M, Gifford R, et al. Interstitial glucose concentration and glycemia: implications for continuous subcutaneous glucose monitoring. Am J Physiol Endocrinol Metab 2000 Apr; 278 (4): E716-28 (Pubitemid 30215184)
6. Durak EP, Jovanovic-Peterson L, Peterson CM. Randomized crossover study of effect of resistance training on gly-cemic control, muscular strength, and cholesterol in type I diabetic men. Diabetes Care 1990 Oct; 13 (10): 1039-43 (Pubitemid 20333924)
7. Ramalho AC, de Lourdes Lima M, Nunes F, et al. The effect of resistance versus aerobic training on metabolic control in patients with type-1 diabetes mellitus. Diabetes Res Clin Pract 2006 Jun; 72 (3): 271-6 (Pubitemid 43729140)
8. Heyman E, Toutain C, Delamarche P, et al. Exercise training and cardiovascular risk factors in type 1 diabetic adolescent girls. Pediatr Exerc Sci 2007 Nov; 19 (4): 408-19 (Pubitemid 350224173)
9. Guelfi KJ, Jones TW, Fournier PA. The decline in blood glucose levels is less with intermittent high-intensity compared with moderate exercise in individuals with type 1 diabetes. Diabetes Care 2005 Jun; 28(6): 1289-94 (Pubitemid 40756687)
10. Guelfi KJ, Ratnam N, Smythe GA, et al. 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 Mar; 292 (3): E865-70 (Pubitemid 46411066)
11. Harmer AR, Chisholm DJ, McKenna MJ, 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
12. Bussau VA, Ferreira LD, Jones TW, et al. The 10-s maximal sprint: a novel approach to counter an exercise-mediated fall in glycemia in individuals with type1 diabetes. Diabetes Care 2006 Mar; 29 (3): 601-6 (Pubitemid 44115361)
13. Pilcher JJ, Nadler E, Busch C. Effects of hot and cold temperature exposure on performance: a meta-analytic review. Ergonomics 2002 Aug 15; 45 (10): 682-98 (Pubitemid 35331093)
14. Heyman E, Briard D, Gratas-Delamarche A, et al. Normal physical working capacity in prepubertal children with type 1 diabetes compared with healthy controls. Acta Paediatr 2005 Oct; 94 (10): 1389-94 (Pubitemid 41510647)
15. Tansey MJ, Tsalikian E, Beck RW, et al. The effects of aerobic exercise on glucose and counterregulatory hormone concentrations in children with type 1 diabetes. Diabetes Care 2006 Jan; 29 (1): 20-5 (Pubitemid 44033425)
16. Heyman E, Delamarche P, Berthon P, et al. Alteration in sympathoadrenergic activity at rest and during intense exercise despite normal aerobic fitness in late pubertal adolescent girls with type 1 diabetes. Diabetes Metab 2007 Dec; 33 (6): 422-9 (Pubitemid 350213454)
17. Poortmans JR, Saerens P, Edelman R, et al. Influence of the degree of metabolic control on physical fitness in type I diabetic adolescents. Int J Sports Med 1986 Aug; 7 (4): 232-5 (Pubitemid 17185808)
18. West DJ, Stephens JW, Bain SC, et al. A combined insulin reduction and carbohydrate feeding strategy 30min before running best preserves blood glucose concentration after exercise through improved fuel oxidation in type 1 diabetes mellitus. J Sports Sci 2011 Feb; 29 (3): 279-89
19. Yamanouchi K, Abe R, Takeda A, et al. The effect of walking before and after breakfast on blood glucose levels in patients with type 1 diabetes treated with intensive insulin therapy. Diabetes Res Clin Pract 2002 Oct; 58 (1): 11-8 (Pubitemid 34823620)
20. Zinman B, Murray FT, Vranic M, et al. Glucoregulation during moderate exercise in insulin treated diabetics. J Clin Endocrinol Metab 1977 Oct; 45 (4): 641-52 (Pubitemid 8212507)
21. Zinman B, Zuniga-Guajardo S, Kelly D. Comparison of the acute and long-term effects of exercise on glucose control in type I diabetes. Diabetes Care 1984 Nov-Dec; 7 (6): 515-9 (Pubitemid 15210455)
22. Huttunen NP, Lankela SL, Knip M, et al. Effect of once-aweek training program on physical fitness and metabolic control in children with IDDM. Diabetes Care 1989 Nov-Dec; 12 (10): 737-40 (Pubitemid 19284097)
23. Rowland TW, Swadba LA, Biggs DE, et al. Glycemic control with physical training in insulin-dependent diabetes mellitus. Am J Dis Child 1985 Mar; 139 (3): 307-10 (Pubitemid 15133718)
24. Wong CH, Chiang YC, Wai JP, et al. Effects of a homebased aerobic exercise programme in children with type 1 diabetes mellitus. J Clin Nurs 2010 Mar; 20 (5-6): 681-91
25. Bernardini AL, Vanelli M, Chiari G, et al. Adherence to physical activity in young people with type 1 diabetes. Acta Biomed 2004 Dec; 75 (3): 153-7
26. Marrero DG, Fremion AS, Golden MP. Improving compliance with exercise in adolescents with insulin-dependent diabetes mellitus: results of a self-motivated home exercise program. Pediatrics 1988 Apr; 81 (4): 519-25
27. Michaliszyn SF, Faulkner MS. Physical activity and sedentary behavior in adolescents with type 1 diabetes. Res Nurs Health 2011 Oct; 33 (5): 441-9
28. Ruzic L, Sporis G, Matkovic BR. High volume-low intensity exercise camp and glycemic control in diabetic children. J Paediatr Child Health 2008 Mar; 44 (3): 122-8 (Pubitemid 351326862)
29. Sideraviciute S, Gailiuniene A, Visagurskiene K, et al. The effect of long-term swimming program on glycemia control in 14-19-year aged healthy girls and girls with type 1 diabetes mellitus. Medicina (Kaunas) 2006; 42 (6): 513-8
30. Laaksonen DE, Atalay M, Niskanen LK, et al. Aerobic exercise and the lipid profile in type 1 diabetic men: a randomized controlled trial. Med Sci Sports Exerc 2000 Sep; 32 (9): 1541-8
31. Lehmann R, Kaplan V, Bingisser R, et al. Impact of physical acitivity on cardiovascular risk factors in IDDM. Diabetes Care 1997; 20 (10): 1603-11 (Pubitemid 27415042)
32. Wallberg-Henriksson H, Gunnarsson R, Rossner S, et al. Long-term physical training in female type 1 (insulin-dependent) diabetic patients: absence of significant effect on glycaemic control and lipoprotein levels. Diabetologia 1986; 29: 53-7 (Pubitemid 16162742)
33. D'Hooge R, Hellinckx T, Van Laethem C, et al. Influence of combined aerobic and resistance training on metabolic control, cardiovascular fitness and quality of life in adolescents with type 1 diabetes: a randomized controlled trial. Clin Rehabil 2011 Apr; 25 (4): 349-59
34. Mosher PE, Nash MS, Perry AC, et al. Aerobic circuit exercise training: effect on adolescents with well-controlled insulin-dependent diabetes mellitus. Arch Phys Med Re-habil 1998 Jun; 79 (6): 652-7 (Pubitemid 28265716)
35. Iscoe KE, Campbell JE, Jamnik V, et al. 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 Dec; 8 (6): 627-35 (Pubitemid 44871492)
36. 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 Jul; 28 (7): 824-32
37. Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. Hillsdale (NJ): Lawrence Erlbaum Associates, 1988
38. Gibala MJ. High-intensity interval training: a time-efficient strategy for health promotion? Curr Sports Med Rep 2007 Jul; 6 (4): 211-3 (Pubitemid 47235574)
39. Harbour R. A new system for grading recommendations in evidence based guidelines. BMJ 2001; 1 (1): 334-6 (Pubitemid 32744465)
40. Perrone C, Laitano O, Meyer F. Effects of carbohydrate ingestion on the glycemic response of type 1 diabetic adolescents during exercise. Diabetes Care 2005 Oct; 28 (10): 2537-8 (Pubitemid 41384307)
41. Raile K, Kapellen T, Schweiger A, et al. Physical activity and competitive sports in children and adolescents with type 1 diabetes. Diabetes Care 1999 Nov; 22 (11): 1904-5 (Pubitemid 29521881)
42. Aman J, Skinner TC, de Beaufort CE, et al. Associations between physical activity, sedentary behavior, and gly-cemic control in a large cohort of adolescents with type 1 diabetes: the Hvidoere Study Group on Childhood Diabetes. Pediatric Diabetes 2009; 10: 234-9
43. Michaliszyn SF, Shaibi GQ, Quinn L, et al. Physical fitness, dietary intake, and metabolic control in adolescents with type 1 diabetes. Pediatr Diabetes 2009 Sep; 10 (6): 389-94
44. Costill DL, Fink WJ, Getchell LH, et al. Lipid metabolism in skeletal muscle of endurance-trained males and females. J Appl Physiol 1979 Oct; 47 (4): 787-91 (Pubitemid 10236252)
45. Wallymahmed ME, Morgan C, Gill GV, et al. Aerobic fitness and hand grip strength in type 1 diabetes: relationship to glycaemic control and body composition. Diabet Med 2007 Nov; 24 (11): 1296-9 (Pubitemid 47621805)
46. Kelly RB. Diet and exercise in the management of hyperlipidemia. Am Fam Physician 2010 May 1; 81 (9): 1097-102
47. Ludvigsson J. Physical exercise in relation to degree of metabolic control in juvenile diabetics. Acta Paediatr Scand Suppl 1980; 283: 45-9
48. Nermoen I, Jorde R, Sager G, et al. Effects of exercise on hypoglycaemic responses in insulin-dependent diabetes mellitus. Diabetes Metab 1998 Apr; 24 (2): 131-6 (Pubitemid 28239810)
49. Roberts L, Jones TW, Fournier PA. Exercise training and glycemic control in adolescents with poorly controlled type 1 diabetes mellitus. J Pediatr Endocrinol Metab 2002 May; 15 (5): 621-7 (Pubitemid 34704821)
50. Sonnenberg GE, Kemmer FW, Berger M. Exercise in type 1 (insulin-dependent) diabetic patients treated with continuous subcutaneous insulin infusion: prevention of exercise induced hypoglycaemia. Diabetologia 1990 Nov; 33 (11): 696-703 (Pubitemid 20377934)
51. Valerio G, Spagnuolo MI, Lombardi F, et al. Physical activity and sports participation in children and adolescents with type 1 diabetes mellitus. Nutr Metab Cardiovasc Dis 2007 Jun; 17 (5): 376-82 (Pubitemid 46880263)
52. Vanelli M, Corchia M, Iovane B, et al. Self-monitoring adherence to physical activity in children and adolescents with type 1 diabetes. Acta Biomed 2006; 77 Suppl. 1: 47-50 (Pubitemid 351598163)
53. Fayolle C, Brun JF, Bringer J, et al. Accuracy of continuous subcutaneous glucose monitoring with the GlucoDay in type 1 diabetic patients treated by subcutaneous insulin infusion during exercise of low versus high intensity. Diabetes Metab 2006 Sep; 32 (4): 313-20 (Pubitemid 44410144)
54. Meinders AE, Willekens FL, Heere LP. Metabolic and hormonal changes in IDDM during long-distance run. Diabetes Care 1988 Jan; 11 (1): 1-7
55. Herbst A, Kordonouri O, Schwab K, et al. Impact of physical activity on cardiovascular risk factors in children with type 1 diabetes. Diabetes Care 2007; 30 (8): 2098-100 (Pubitemid 47219428)
56. Sackey AH, Jefferson IG. Physical activity and glycaemic control in children with diabetes mellitus. Diabet Med 1996 Sep; 13 (9): 789-93 (Pubitemid 26316263)
57. Faulkner MS, Michaliszyn SF, Hepworth JT. A personalized approach to exercise promotion in adolescents with type 1 diabetes. Pediatr Diabetes 2010 May; 11 (3): 166-74
58. Ligtenberg PC, Blans M, Hoekstra JB, et al. No effect of long-term physical activity on the glycemic control in type 1 diabetes patients: a cross-sectional study. Neth J Med 1999 Aug; 55 (2): 59-63 (Pubitemid 29325008)
59. Dahl-Jorgensen K, Meen HD, Hanssen KF, et al. The effect of exercise on diabetic control and hemoglobin A1 (HbA1) in children. Acta Paediatr Scand Suppl 1980; 283: 53-6
60. Nugent AM, Steele IC, al-Modaris F, et al. Exercise responses in patients with IDDM. Diabetes Care 1997 Dec; 20 (12): 1814-21 (Pubitemid 27522888)
61. Clarke WL, Cox DJ, Gonder-Frederick LA, et al. The relationship between nonroutine use of insulin, food, and exercise and the occurrence of hypoglycemia in adults with IDDM and varying degrees of hypoglycemic awareness and metabolic control. Diabetes Educ 1997 Jan-Feb; 23 (1): 55-8 (Pubitemid 127459592)
62. Szmigiel C, Dziadkowiak H, Jesionek D, et al. The influence of physical effort of variable intensity on glycemia in children with diabetes. Pediatr Pol 1996 May; 71 (5): 423-30
63. McCargar LJ, Taunton J, Pare S. Benefits of exercise training for men with insulin-dependent diabetes mellitus. Diabetes Educ 1991 May-Jun; 17 (3): 179-84
64. Stratton R, Wilson DP, Endres RK, et al. Improved glycemic control after supervised 8-wk exercise program in insulin-dependent diabetic adolescents. Diabetes Care 1987 Sep-Oct; 10 (5): 589-93 (Pubitemid 17158930)
65. Jensen MD, Miles JM. The roles of diet and exercise in the management of patients with insulin-dependent diabetes mellitus. Mayo Clin Proc 1986 Oct; 61 (10): 813-9 (Pubitemid 16002388)
66. Hubinger A, Ridderskamp I, Lehmann E, et al. Metabolic response to different forms of physical exercise in type I diabetics and the duration of the glucose lowering effect. Eur J Clin Invest 1985 Aug; 15 (4): 197-203 (Pubitemid 16239883)
67. Schiffrin A, Parikh S, Marliss EB, et al. Metabolic response to fasting exercise in adolescent insulin-dependent diabetic subjects treated with continuous subcutaneous insulin infusion and intensive conventional therapy. Diabetes Care 1984 May-Jun; 7 (3): 255-60 (Pubitemid 14105307)
68. Sills IN, Cerny FJ. Responses to continuous and intermittent exercise in healthy and insulin-dependent diabetic children. Med Sci Sports Exerc 1983; 15 (6): 450-4 (Pubitemid 14197107)
69. Guler HP, Walter H, Morell B, et al. Effect of prolonged optimal blood sugar control by i.v. insulin administration on plasma free fatty acid and glycerol concentrations of insulin-dependent diabetics during exercise. Acta Diabetol Lat 1982 Jul-Sep; 19 (3): 261-71 (Pubitemid 13242009)
70. Zander E, Schulz B, Chlup R, et al. Muscular exercise in type I-diabetics, II: hormonal and metabolic responses to moderate exercise. Exp Clin Endocrinol 1985 Feb; 85 (1): 95-104 (Pubitemid 15105746)
71. Baharlouei K. The effect of aerobic training on selected variables in patients with type 1 diabetes mellitus. Br J Sports Med 2010; 44 Suppl. 1: i21
72. Jette DU. Physiological effects of exercise in the diabetic. Phys Ther 1984 Mar; 64 (3): 339-42 (Pubitemid 14196604)
73. Riddell MC, Iscoe KE. Physical activity, sport, and pediatric diabetes. Pediatr Diabetes 2006 Feb; 7 (1): 60-70 (Pubitemid 43732643)
74. Riddell MC, Milliken J. Preventing exercise-induced hypoglycemia in type 1 diabetes using real-time continuous glucose monitoring and a new carbohydrate intake algorithm: an observational field study. Diabetes Technol Ther 2011 Aug; 13 (8): 819-25
75. Steppel JH, Horton ES. Exercise in the management of type 1 diabetes mellitus. Rev Endocr Metab Disord 2003 Dec; 4 (4): 355-60 (Pubitemid 37493651)
76. Smith NJ, Stanitski CL, Dyment CL, et al. Glycemic control with physical trainin in insulin-dependent diabetes melli-tus. Sports Med 1985; 139: 307-10
77. Rabasa-Lhoret R, Bourque J, Ducros F, et al. 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 Apr; 24 (4): 625-30 (Pubitemid 32888838)
78. Riddell M, Perkins BA. Exercise and glucose metabolism in persons with diabetes mellitus: perspectives on the role for continuous glucose monitoring. J Diabetes Sci Technol 2009; 3 (4): 914-23
79. Jimenez C, Santiago M, Sitler M, et al. Insulin-sensitivity response to a single bout of resistive exercise in type 1 diabetes mellitus. J Sport Rehabil 2009 Nov; 18 (4): 564-71
80. Iafusco D. Diet and physical activity in patients with type 1 diabetes. Acta Biomed 2006; 77 Suppl 1: 41-6 (Pubitemid 351598162)
81. Zander E, Bruns W, Wulfert P, et al. Muscular exercise in type I-diabetics, I: different metabolic reactions during heavy muscular work in dependence on actual insulin availability. Exp Clin Endocrinol 1983 Jul; 82 (1): 78-90 (Pubitemid 13020528)
82. Bussau VA, Ferreira LD, Jones TW, et al. A 10-s sprint performed prior to moderate-intensity exercise prevents early post-exercise fall in glycaemia in individuals with type 1 diabetes. Diabetologia 2007 Sep; 50 (9): 1815-8 (Pubitemid 47222848)
83. Baldi JC, Cassuto NA, Foxx-Lupo WT, et al. Glycemic status affects cardiopulmonary exercise response in athletes with type I diabetes. Med Sci Sports Exerc 2011 Aug; 42 (8): 1454-9
84. Khoharo HK, Ansari S, Ali Shaikh I, et al. Cardiac autonomic neuropathy (CAN) in type-1 diabetes mellitus patients and its association with the duration of disease and glycemic control. J Coll Physicians Surg Pak 2009 Apr; 19 (4): 232-5
85. Ismail I, Keating SE, Baker MK, et al. A systematic review and meta-analysis of the effect of aerobic vs. resistance exercise training on visceral fat. Obes Rev 2012 Jan; 13 (1): 68-91
86. Svensson MK, Eriksson JW. Change in the amount of body fat and IL-6 levels is related to altered insulin sensitivity in type 1 diabetes patients with or without diabetic nephro-pathy. Horm Metab Res 2011 Mar; 43 (3): 209-15
87. Tresierras MA, Balady GJ. Resistance training in the treatment of diabetes and obesity: mechanisms and outcomes. J Cardiopulm Rehabil Prev 2009 Mar-Apr; 29 (2): 67-75
88. Irvine C, Taylor NF. Progressive resistance exercise improves glycaemic control in people with type 2 diabetes mellitus: a systematic review. Aust J Physiother 2009; 55 (4): 237-46
89. Sundell J. Resistance training is an effective tool against metabolic and frailty syndromes. Adv Prev Med 2011; 984683-7
90. Heymsfield SB, Gallagher D, Kotler DP, et al. Body-size dependence of resting energy expenditure can be attributed to nonenergetic homogeneity of fat-free mass. Am J Phy-siol Endocrinol Metab 2002 Jan; 282 (1): E132-8
91. Brun J-F, Marti B, Fedou C, et al. Two parameters statistically explain blood glucose decrease during exercise at steady state in type 1 diabetics: pre-exercise blood glucose and insulinemia. Sci Sports. In press
92. Brazeau AS, Rabasa-Lhoret R, Strychar I, et al. Barriers to physical activity among patients with type 1 diabetes. Diabetes Care 2008 Nov; 31 (11): 2108-9
93. Duval S, Tweedie R. Trim and fill: a simple funnel-plotbased method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000 Jun; 56 (2): 455-63 (Pubitemid 30422636)
94. Song F, Gilbody S. Bias in meta-analysis detected by a simple, graphical test. Increase in studies of publication bias coincided with increasing use of meta-analysis. BMJ 1998 Feb 7; 316 (7129): 469-71