Abstract
Background
The acute impact of different types of physical activity on glycemic control in type 1 diabetes has not been well quantified.
Objectives
Our objective was to estimate the rate of change (RoC) in glucose concentration induced acutely during the performance of structured exercise and at recovery in subjects with type 1 diabetes.
Methods
We searched for original articles in the PubMed, MEDLINE, Scopus, and Cochrane databases. Search terms included type 1 diabetes, blood glucose, physical activity, and exercise. Eligible studies (randomized controlled trials and non-randomized experiments) encompassed controlled physical activity sessions (continuous moderate [CONT], intermittent high intensity [IHE], resistance [RESIST], and/or a resting reference [REST]) and reported excursions in glucose concentration during exercise and after its cessation. Data were extracted by graph digitization to compute two RoC measures from population profiles: RoCE during exercise and RoCR in recovery.
Results
Ten eligible studies were found from 540 publications. Meta-analyses of exercise modalities versus rest yielded the following: RoCE −4.43 mmol/L h−1 (p < 0.00001, 95 % confidence interval [CI] −6.06 to −2.79) and RoCR +0.70 mmol/L h−1 (p = 0.46, 95 % CI −1.14 to +2.54) for CONT vs. REST; RoCE −5.25 mmol/L·h−1 (p < 0.00001, 95 % CI −7.02 to −3.48) and RoCR +0.72 mmol/L h−1 (p = 0.71, 95 % CI −3.10 to +4.54) for IHE vs. REST; RoCE −2.61 mmol/L h−1 (p = 0.30, 95 % CI −7.55 to +2.34) and RoCR −0.02 mmol/L h−1 (p = 1.00, 95 % CI −7.58 to +7.53) for RESIST vs. REST.
Conclusions
Novel RoC magnitudes RoCE, RoCR reflected rapid decays of glycemia during CONT exercise and gradual recoveries immediately afterwards. RESIST showed more constrained decays, whereas discrepancies were found for IHE.
Similar content being viewed by others
References
American Diabetes Association. Physical activity/exercise and diabetes. Diabetes Care. 2004;27(S1):S58–62.
Nagi D, editor. Exercise and sport in diabetes, 2nd ed. UK: Wiley; 2006.
Ertl AC, Davis SN. Evidence for a vicious cycle of exercise and hypoglycemia in type 1 diabetes mellitus. Diabetes Metab Res Rev. 2004;20(2):124–30.
Cryer PE. Exercise-related hypoglycemia-associated autonomic failure in diabetes. Diabetes. 2009;58(9):1951–2.
Riddell MC, Burr J. Evidence-based risk assessment and recommendations for physical activity clearance: diabetes mellitus and related comorbidities. Appl Physiol Nutr Metab. 2011;36(S1):154–89.
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;33(11):696–703.
Marliss EB, Vranic M. Intense exercise has unique effects on both insulin release and its roles in glucoregulation: implications for diabetes. Diabetes. 2002;51(S):S271–S283.
Chu L, Hamilton J, Riddell MC. Clinical management of the physically active patient with type I diabetes. Phys Sports Med. 2011;39(2):64–77.
Riddell MC, Perkins B. Type 1 diabetes and vigorous exercise: applications of exercise physiology to patient management. Can J Diabetes. 2006;30(1):63–71.
Lumb AN, Gallen IW. Diabetes management for intense exercise. Curr Opin Endocrinol Diabetes Obes. 2009;16(2):150–5.
Guelfi KJ, Jones TW, Fournier PA. New insights into managing the risk of hypoglycaemia associated with intermittent high-intensity exercise in individuals with type 1 diabetes mellitus—implications for existing guidelines. Sports Med. 2007;37(11):937–46.
Jiménez 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;18(4):564–71.
Harmer AR, Chisholm DJ, McKenna MJ, et al. High-intensity training improves plasma glucose and acid–base regulation during intermittent maximal exercise in type 1 diabetes. Diabetes Care. 2007;30(5):1269–71.
Braken RM, West DJ, Stephens JW, et al. Impact of pre-exercise rapid-acting insulin reductions on ketogenesis following running in type 1 diabetes. Diabet Med. 2011;28(2):218–22.
Kilbride L, Charlton J, Aitken G, et al. Managing blood glucose during and after exercise in type 1 diabetes: reproducibility of glucose response and a trial of a structured algorithm adjusting insulin and carbohydrate intake. J Clin Nurs. 2011;20(23–24):3423–9.
Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097
Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from http://www.cochrane-handbook.org.
Coletti MH, Bleich HL. Medical subject headings used to search the biomedical literature. J Am Med Inform Assoc. 2001;8(4):317–23.
Review Manager (RevMan) [Computer program]. Version 5.2. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration; 2012.
Dubé MC, Weisnagel SJ, Prud’homme D, et al. Exercise and newer insulins: how much glucose supplement to avoid hypoglycemia? Med Sci Sports Exerc. 2005;37(8):1276–82.
Dubé MC, Weisnagel SJ, Prud’homme D, et al. Is early and late post-meal exercise so different in type 1 diabetic lispro users? Diabetes Res Clin Pract. 2006;72(2):128–34.
Dubé MC, Lavoie C, Weisnagel SJ. Glucose or intermittent high-intensity exercise in glargine/glulisine users with T1DM. Med Sci Sports Exerc. 2013;45(1):3–7.
Yardley JE, Kenny GP, Perkins BA, et al. Effects of performing resistance exercise before versus after aerobic exercise on glycemia in type 1 diabetes. Diabetes Care. 2012;35(4):669–75.
Yardley JE, Kenny GP, Perkins BA, et al. Resistance versus aerobic exercise: acute effects on glycemia in type 1 diabetes. Diabetes Care. 2013;36(3):537–42.
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 type 1 diabetes. Diabetes Care. 2006;29(3):601–6.
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;50(9):1815–8.
Tsalikian E, Mauras N, Beck RW, et al. Impact of exercise on overnight glycemic control in children with type 1 diabetes mellitus. J Pediatr. 2005;147(4):528–34.
Yardley JE, Sigal RJ, Kenny GP, et al. Point accuracy of interstitial continuous glucose monitoring during exercise in type 1 diabetes. Diabetes Technol Ther. 2013;15(1):46–9.
Guelfi KJ, Jones TW, Fournier PA. Intermittent high-intensity exercise does not increase the risk of early postexercise hypoglycemia in individuals with type 1 diabetes. Diabetes Care. 2005;28(2):416–8.
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;28(6):1289–94.
Iscoe KE, Riddell MC. Continuous moderate-intensity exercise with or without intermittent high-intensity work: effects on acute and late glycaemia in athletes with type1 diabetes mellitus. Diabet Med. 2011;28(7):824–32.
Jankovec Z, Krcma M, Gruberova J, et al. Influence of physical activity on metabolic state within a 3-h interruption of continuous subcutaneous insulin infusion in patients with type 1 diabetes. Diabetes Technol Ther. 2011;13(12):1234–9.
Maran A, Pavan P, Bonsembiante B, et al. Continuous glucose monitoring reveals delayed nocturnal hypoglycemia afterintermittent high-intensity exercise in nontrained patients with type 1 diabetes. Diabetes Technol Ther. 2010;12(10):763–8.
Peter R, Luzio SD, Dunseath G, et al. Effects of exercise on the absorption of insulin glargine in patients with type 1 diabetes. Diabetes Care. 2005;28(3):560–5.
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;24(4):625–30.
Soo K, Furler SM, Samaras K, et al. Glycemic responses to exercise in IDDM after simple and complex carbohydrate supplementation. Diabetes Care. 1996;19(6):575–9.
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;58(1):11–8.
da Cunha FA, Farinatti PTV, Midgley AW. Methodological and practical application issues in exercise prescription using the heart rate reserve and oxygen uptake reserve methods. J Sci Med Sport. 2011;14(1):46–57.
Gaskill SE, Bouchard C, Rankinen T, et al. %Heart rate reserve is better related to %VO2max than to %VO2reserve: the HERITAGE family study. Med Sci Sports Exerc. 2004;36(5):S3.
Rotstein A, Meckel Y. Estimation of %VO2 reserve from heart rate during arm exercise and running. Eur J Appl Physiol. 2000;83(6):545–50.
Arutchelvam V, Heise T, Dellweg S, et al. Plasma glucose and hypoglycaemia following exercise in people with type 1 diabetes: a comparison of three basal insulins. Diabet Med. 2009;26(10):1027–32.
Tsalikian E, Fox L, Janz KF, et al. Prevention of hypoglycemia during exercise in children with type 1 diabetes by suspending basal insulin. Diabetes Care. 2006;29(10):2200–4.
West DJ, Morton RD, Bain SC, et al. Blood glucose responses to reductions in pre-exercise rapid-acting insulin for 24 h after running in individuals with type 1 diabetes. J Sports Sci. 2010;28(7):781–8.
Dubé MC, Lavoie C, Galibois I, et al. Nutritional strategies to prevent hypoglycemia at exercise in diabetic adolescents. Med Sci Sports Exerc. 2012;44(8):1427–32.
Perrone C, Laitano O, Meyer F. Effect of carbohydrate ingestion on the glycemic response of type 1 diabetic adolescents during exercise. Diabetes Care. 2005;28(10):2537–8.
West DJ, Stephens JW, Bain SC, 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.
Marliss EB, Vranic M. Intense exercise has unique effects on both insulin release and its roles on glucoregulation—implications for diabetes. Diabetes. 2002;51(Suppl. 1):S271–83.
Sigal RJ, Fisher SJ, Manzon A, et al. Glucoregulation during and after intense exercise: effects on α-adrenergic blockade. Metabolism. 2000;49(3):386–94.
Sigal RJ, Fisher SJ, Halter JB, et al. Glucoregulation during and after intense exercise: effects on β-adrenergic blockade in subjects with type 1 diabetes mellitus. J Clin Endocrinol Metab. 1999;84:3961–71.
Kumareswaran K, Elleri D, Allen JM, et al. Accuracy of continuous glucose monitoring during exercise in type 1 diabetes pregnancy. Diabetes Technol Ther. 2013;15(3):223–9.
Jenni S, Oetliker C, Allemann 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;51:1457–65.
Chokkalingam K, Tsintzas K, Norton L, et al. Exercise under hyperinsulinaemic conditions increases whole-body glucose disposal without affecting muscle glycogen utilisation in type 1 diabetes. Diabetologia. 2007;50:414–21.
MacMahon SK, Ferreira LD, Ratnam N, 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.
Davey RJ, Howe W, Paramalingam N, et al. The effect of midday moderate-intensity exercise on postexercise hypoglycemia risk in individuals with type 1 diabetes. J Clin Endocrinol Metab. 2013;98(7):2908–14.
Fujimoto T, Kemppainen J, Kalliokoski KK, et al. Skeletal muscle glucose uptake response to exercise in trained and untrained men. Med Sci Sports Exerc. 2003;35(5):777–83.
Riddell MC. The endocrine response and substrate utilization during exercise in children and adolescents. J Appl Physiol. 2008;105(2):725–33.
Tonoli C, Heyman E, Roelands B, et al. Effects of different types of acute and chronic (training) exercise on glycaemic control in type 1 diabetes mellitus: a meta-analysis. Sports Med. 2012;42(12):1059–80.
Cohen J. Statistical power analysis for the behavioral sciences, 2nd ed. USA: Lawrence Erlbaum Assoc. Inc.; 1988.
Acknowledgments
The authors would like to thank the reviewers for their comments, which led to a substantial improvement of our work. In particular, their identification of the study by Yardley et al. [28] is of special note. This work was partly supported by a doctoral research Grant from the Technical University of Madrid, by a fellowship from the Spanish Ministry of Education, and by the ‘APRIORI’ Project (FIS PS09/01318) from the Spanish Ministry of Science and Innovation. Funders were not involved in the research or its publication. The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the review reported.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
40279_2015_302_MOESM1_ESM.tiff
Figure S1. Funnel plots depicting standard errors (SE) versus mean differences (MD) for studies in the meta-analysis. Panels (a) and (b) show outcomes for RoC E and RoC R , respectively, in the case of studies comparing CONT versus REST periods. Panels (c) and (d): outcomes for RoC E and RoC R , respectively, in IHE versus REST studies. Panels (e), (f): RoC E , RoC R in RESIST vs REST. Panels (g), (h): RoC E , RoC R in IHE vs CONT. Panels (i), (j): RoC E , RoC R in RESIST vs CONT. All axes are in units [mmol/L·h–1]. SE = standard error, MD = mean difference, RoC E = glycaemia rate-of-change during exercise, RoC R = glycaemia rate-of-change at recovery, CONT = continuous physical activity, IHE = intermittent high-intensity exercise, RESIST = resistance exercise, REST = resting control period. (TIFF 382 kb)
Rights and permissions
About this article
Cite this article
García-García, F., Kumareswaran, K., Hovorka, R. et al. Quantifying the Acute Changes in Glucose with Exercise in Type 1 Diabetes: A Systematic Review and Meta-Analysis. Sports Med 45, 587–599 (2015). https://doi.org/10.1007/s40279-015-0302-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40279-015-0302-2