Skip to main content
Erschienen in: Diabetologia 4/2016

01.04.2016 | Article

Metabolic and hormonal response to intermittent high-intensity and continuous moderate intensity exercise in individuals with type 1 diabetes: a randomised crossover study

verfasst von: Lia Bally, Thomas Zueger, Tania Buehler, Ayse S. Dokumaci, Christian Speck, Nicola Pasi, Carlos Ciller, Daniela Paganini, Katrin Feller, Hannah Loher, Robin Rosset, Matthias Wilhelm, Luc Tappy, Chris Boesch, Christoph Stettler

Erschienen in: Diabetologia | Ausgabe 4/2016

Einloggen, um Zugang zu erhalten

Abstract

Aims/hypothesis

To investigate exercise-related fuel metabolism in intermittent high-intensity (IHE) and continuous moderate intensity (CONT) exercise in individuals with type 1 diabetes mellitus.

Methods

In a prospective randomised open-label cross-over trial twelve male individuals with well-controlled type 1 diabetes underwent a 90 min iso-energetic cycling session at 50% maximal oxygen consumption (\( \overset{\cdot }{V}{\mathrm{O}}_{2 \max } \)), with (IHE) or without (CONT) interspersed 10 s sprints every 10 min without insulin adaptation. Euglycaemia was maintained using oral 13C-labelled glucose. 13C Magnetic resonance spectroscopy (MRS) served to quantify hepatocellular and intramyocellular glycogen. Measurements of glucose kinetics (stable isotopes), hormones and metabolites complemented the investigation.

Results

Glucose and insulin levels were comparable between interventions. Exogenous glucose requirements during the last 30 min of exercise were significantly lower in IHE (p = 0.02). Hepatic glucose output did not differ significantly between interventions, but glucose disposal was significantly lower in IHE (p < 0.05). There was no significant difference in glycogen consumption. Growth hormone, catecholamine and lactate levels were significantly higher in IHE (p < 0.05).

Conclusions/interpretation

IHE in individuals with type 1 diabetes without insulin adaptation reduced exogenous glucose requirements compared with CONT. The difference was not related to increased hepatic glucose output, nor to enhanced muscle glycogen utilisation, but to decreased glucose uptake. The lower glucose disposal in IHE implies a shift towards consumption of alternative substrates. These findings indicate a high flexibility of exercise-related fuel metabolism in type 1 diabetes, and point towards a novel and potentially beneficial role of IHE in these individuals.

Trial registration:

ClinicalTrials.gov NCT02068638

Funding:

Swiss National Science Foundation (grant number 320030_149321/) and R&A Scherbarth Foundation (Switzerland).
Literatur
1.
Zurück zum Zitat Sonnenberg GE, Kemmer FW, Berger M (1990) Exercise in type 1 (insulin-dependent) diabetic patients treated with continuous subcutaneous insulin infusion. Prevention of exercise induced hypoglycaemia. Diabetologia 33:696–703CrossRefPubMed Sonnenberg GE, Kemmer FW, Berger M (1990) Exercise in type 1 (insulin-dependent) diabetic patients treated with continuous subcutaneous insulin infusion. Prevention of exercise induced hypoglycaemia. Diabetologia 33:696–703CrossRefPubMed
2.
Zurück zum Zitat Gibala MJ, Little JP, Macdonald MJ, Hawley JA (2012) Physiological adaptations to low-volume, high-intensity interval training in health and disease. J Physiol 590:1077–1084CrossRefPubMedPubMedCentral Gibala MJ, Little JP, Macdonald MJ, Hawley JA (2012) Physiological adaptations to low-volume, high-intensity interval training in health and disease. J Physiol 590:1077–1084CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Weston KS, Wisloff U, Coombes JS (2014) High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med 48:1227–1234CrossRefPubMed Weston KS, Wisloff U, Coombes JS (2014) High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med 48:1227–1234CrossRefPubMed
4.
Zurück zum Zitat Bussau VA, Ferreira LD, Jones TW, Fournier PA (2006) The 10-s maximal sprint: a novel approach to counter an exercise-mediated fall in glycemia in individuals with type 1 diabetes. Diabetes Care 29:601–606CrossRefPubMed Bussau VA, Ferreira LD, Jones TW, Fournier PA (2006) The 10-s maximal sprint: a novel approach to counter an exercise-mediated fall in glycemia in individuals with type 1 diabetes. Diabetes Care 29:601–606CrossRefPubMed
5.
Zurück zum Zitat Bussau VA, Ferreira LD, Jones TW, Fournier PA (2007) A 10-s sprint performed prior to moderate-intensity exercise prevents early post-exercise fall in glycaemia in individuals with type 1 diabetes. Diabetologia 50:1815–1818CrossRefPubMed Bussau VA, Ferreira LD, Jones TW, Fournier PA (2007) A 10-s sprint performed prior to moderate-intensity exercise prevents early post-exercise fall in glycaemia in individuals with type 1 diabetes. Diabetologia 50:1815–1818CrossRefPubMed
6.
Zurück zum Zitat Campbell MD, West DJ, Bain SC et al (2014) Simulated games activity vs continuous running exercise: a novel comparison of the glycemic and metabolic responses in T1DM patients. Scand J Med Sci Sports 25:216–222CrossRefPubMed Campbell MD, West DJ, Bain SC et al (2014) Simulated games activity vs continuous running exercise: a novel comparison of the glycemic and metabolic responses in T1DM patients. Scand J Med Sci Sports 25:216–222CrossRefPubMed
7.
Zurück zum Zitat Dube MC, Lavoie C, Weisnagel SJ (2013) Glucose or intermittent high-intensity exercise in glargine/glulisine users with T1DM. Med Sci Sports Exerc 45:3–7CrossRefPubMed Dube MC, Lavoie C, Weisnagel SJ (2013) Glucose or intermittent high-intensity exercise in glargine/glulisine users with T1DM. Med Sci Sports Exerc 45:3–7CrossRefPubMed
8.
Zurück zum Zitat Guelfi KJ, Jones TW, Fournier PA (2005) Intermittent high-intensity exercise does not increase the risk of early postexercise hypoglycemia in individuals with type 1 diabetes. Diabetes Care 28:416–418CrossRefPubMed Guelfi KJ, Jones TW, Fournier PA (2005) Intermittent high-intensity exercise does not increase the risk of early postexercise hypoglycemia in individuals with type 1 diabetes. Diabetes Care 28:416–418CrossRefPubMed
9.
Zurück zum Zitat Guelfi KJ, Ratnam N, Smythe GA, Jones TW, Fournier PA (2007) 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 292:E865–E870CrossRefPubMed Guelfi KJ, Ratnam N, Smythe GA, Jones TW, Fournier PA (2007) 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 292:E865–E870CrossRefPubMed
10.
Zurück zum Zitat Iscoe KE, Riddell MC (2011) 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 28:824–832CrossRefPubMed Iscoe KE, Riddell MC (2011) 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 28:824–832CrossRefPubMed
11.
Zurück zum Zitat Maran A, Pavan P, Bonsembiante B et al (2010) Continuous glucose monitoring reveals delayed nocturnal hypoglycemia after intermittent high-intensity exercise in nontrained patients with type 1 diabetes. Diabetes Technol Ther 12:763–768CrossRefPubMed Maran A, Pavan P, Bonsembiante B et al (2010) Continuous glucose monitoring reveals delayed nocturnal hypoglycemia after intermittent high-intensity exercise in nontrained patients with type 1 diabetes. Diabetes Technol Ther 12:763–768CrossRefPubMed
12.
Zurück zum Zitat Marliss EB, Vranic M (2002) Intense exercise has unique effects on both insulin release and its roles in glucoregulation: implications for diabetes. Diabetes 51(Suppl 1):S271–S283CrossRefPubMed Marliss EB, Vranic M (2002) Intense exercise has unique effects on both insulin release and its roles in glucoregulation: implications for diabetes. Diabetes 51(Suppl 1):S271–S283CrossRefPubMed
13.
Zurück zum Zitat Fahey AJ, Paramalingam N, Davey RJ, Davis EA, Jones TW, Fournier PA (2012) The effect of a short sprint on postexercise whole-body glucose production and utilization rates in individuals with type 1 diabetes mellitus. J Clin Endocrinol Metab 97:4193–4200CrossRefPubMed Fahey AJ, Paramalingam N, Davey RJ, Davis EA, Jones TW, Fournier PA (2012) The effect of a short sprint on postexercise whole-body glucose production and utilization rates in individuals with type 1 diabetes mellitus. J Clin Endocrinol Metab 97:4193–4200CrossRefPubMed
14.
Zurück zum Zitat Jenni S, Oetliker C, Allemann S et al (2008) Fuel metabolism during exercise in euglycaemia and hyperglycaemia in patients with type 1 diabetes mellitus—a prospective single-blinded randomised crossover trial. Diabetologia 51:1457–1465CrossRefPubMed Jenni S, Oetliker C, Allemann S et al (2008) Fuel metabolism during exercise in euglycaemia and hyperglycaemia in patients with type 1 diabetes mellitus—a prospective single-blinded randomised crossover trial. Diabetologia 51:1457–1465CrossRefPubMed
15.
Zurück zum Zitat Riddell MC, Milliken J (2011) 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 13:819–825CrossRefPubMed Riddell MC, Milliken J (2011) 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 13:819–825CrossRefPubMed
16.
Zurück zum Zitat Gerrior S, Juan W, Basiotis P (2006) An easy approach to calculating estimated energy requirements. Prev Chronic Dis 3:A129PubMedPubMedCentral Gerrior S, Juan W, Basiotis P (2006) An easy approach to calculating estimated energy requirements. Prev Chronic Dis 3:A129PubMedPubMedCentral
17.
Zurück zum Zitat Lefebvre PJ (1985) From plant physiology to human metabolic investigations. Diabetologia 28:255–263CrossRefPubMed Lefebvre PJ (1985) From plant physiology to human metabolic investigations. Diabetologia 28:255–263CrossRefPubMed
18.
Zurück zum Zitat Dunand M, Gubian D, Stauffer M, Abid K, Grouzmann E (2013) High-throughput and sensitive quantitation of plasma catecholamines by ultraperformance liquid chromatography-tandem mass spectrometry using a solid phase microwell extraction plate. Anal Chem 85:3539–3544CrossRefPubMed Dunand M, Gubian D, Stauffer M, Abid K, Grouzmann E (2013) High-throughput and sensitive quantitation of plasma catecholamines by ultraperformance liquid chromatography-tandem mass spectrometry using a solid phase microwell extraction plate. Anal Chem 85:3539–3544CrossRefPubMed
19.
Zurück zum Zitat Peronnet F, Massicotte D (1991) Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16:23–29PubMed Peronnet F, Massicotte D (1991) Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16:23–29PubMed
20.
Zurück zum Zitat Wolfe RR, Chinkes DL (2005) Isotope tracers in metabolic research: principles and practice of kinetic analysis, 2nd edn. Wiley, Chichester Wolfe RR, Chinkes DL (2005) Isotope tracers in metabolic research: principles and practice of kinetic analysis, 2nd edn. Wiley, Chichester
21.
Zurück zum Zitat Tounian P, Schneiter P, Henry S, Delarue J, Tappy L (1997) Effects of dexamethasone on hepatic glucose production and fructose metabolism in healthy humans. Am J Physiol 273:E315–E320PubMed Tounian P, Schneiter P, Henry S, Delarue J, Tappy L (1997) Effects of dexamethasone on hepatic glucose production and fructose metabolism in healthy humans. Am J Physiol 273:E315–E320PubMed
22.
Zurück zum Zitat Steele R, Wall JS, De Bodo RC, Altszuler N (1956) Measurement of size and turnover rate of body glucose pool by the isotope dilution method. Am J Physiol 187:15–24PubMed Steele R, Wall JS, De Bodo RC, Altszuler N (1956) Measurement of size and turnover rate of body glucose pool by the isotope dilution method. Am J Physiol 187:15–24PubMed
23.
Zurück zum Zitat Robert JJ, Koziet J, Chauvet D, Darmaun D, Desjeux JF, Young VR (1987) Use of 13C-labeled glucose for estimating glucose oxidation: some design considerations. J Appl Physiol (1985) 63:1725–1732 Robert JJ, Koziet J, Chauvet D, Darmaun D, Desjeux JF, Young VR (1987) Use of 13C-labeled glucose for estimating glucose oxidation: some design considerations. J Appl Physiol (1985) 63:1725–1732
24.
Zurück zum Zitat Schneiter P, Pasche O, Di Vetta V, Jequier E, Tappy L (1994) Noninvasive assessment of in vivo glycogen kinetics in humans: effect of increased physical activity on glycogen breakdown and synthesis. Eur J Appl Physiol Occup Physiol 69:557–563CrossRefPubMed Schneiter P, Pasche O, Di Vetta V, Jequier E, Tappy L (1994) Noninvasive assessment of in vivo glycogen kinetics in humans: effect of increased physical activity on glycogen breakdown and synthesis. Eur J Appl Physiol Occup Physiol 69:557–563CrossRefPubMed
25.
Zurück zum Zitat Taylor R, Price TB, Rothman DL, Shulman RG, Shulman GI (1992) Validation of 13C NMR measurement of human skeletal muscle glycogen by direct biochemical assay of needle biopsy samples. Magn Reson Med 27:13–20CrossRefPubMed Taylor R, Price TB, Rothman DL, Shulman RG, Shulman GI (1992) Validation of 13C NMR measurement of human skeletal muscle glycogen by direct biochemical assay of needle biopsy samples. Magn Reson Med 27:13–20CrossRefPubMed
26.
Zurück zum Zitat Gruetter R, Magnusson I, Rothman DL, Avison MJ, Shulman RG, Shulman GI (1994) Validation of 13C NMR measurements of liver glycogen in vivo. Magn Reson Med 31:583–588CrossRefPubMed Gruetter R, Magnusson I, Rothman DL, Avison MJ, Shulman RG, Shulman GI (1994) Validation of 13C NMR measurements of liver glycogen in vivo. Magn Reson Med 31:583–588CrossRefPubMed
27.
Zurück zum Zitat Moller N, Jorgensen JO, Schmitz O et al (1990) Effects of a growth hormone pulse on total and forearm substrate fluxes in humans. Am J Physiol 258:E86–E91PubMed Moller N, Jorgensen JO, Schmitz O et al (1990) Effects of a growth hormone pulse on total and forearm substrate fluxes in humans. Am J Physiol 258:E86–E91PubMed
28.
Zurück zum Zitat Capaldo B, Napoli R, Di Marino L, Sacca L (1992) Epinephrine directly antagonizes insulin-mediated activation of glucose uptake and inhibition of free fatty acid release in forearm tissues. Metabolism 41:1146–1149CrossRefPubMed Capaldo B, Napoli R, Di Marino L, Sacca L (1992) Epinephrine directly antagonizes insulin-mediated activation of glucose uptake and inhibition of free fatty acid release in forearm tissues. Metabolism 41:1146–1149CrossRefPubMed
29.
Zurück zum Zitat Lembo G, Capaldo B, Rendina V et al (1994) Acute noradrenergic activation induces insulin resistance in human skeletal muscle. Am J Physiol 266:E242–E247PubMed Lembo G, Capaldo B, Rendina V et al (1994) Acute noradrenergic activation induces insulin resistance in human skeletal muscle. Am J Physiol 266:E242–E247PubMed
30.
Zurück zum Zitat Miller BF, Fattor JA, Jacobs KA et al (2002) Lactate and glucose interactions during rest and exercise in men: effect of exogenous lactate infusion. J Physiol 544:963–975CrossRefPubMedPubMedCentral Miller BF, Fattor JA, Jacobs KA et al (2002) Lactate and glucose interactions during rest and exercise in men: effect of exogenous lactate infusion. J Physiol 544:963–975CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Lombardi AM, Fabris R, Bassetto F et al (1999) Hyperlactatemia reduces muscle glucose uptake and GLUT-4 mRNA while increasing (E1alpha)PDH gene expression in rat. Am J Physiol 276:E922–E929PubMed Lombardi AM, Fabris R, Bassetto F et al (1999) Hyperlactatemia reduces muscle glucose uptake and GLUT-4 mRNA while increasing (E1alpha)PDH gene expression in rat. Am J Physiol 276:E922–E929PubMed
32.
Zurück zum Zitat Vettor R, Lombardi AM, Fabris R et al (1997) Lactate infusion in anesthetized rats produces insulin resistance in heart and skeletal muscles. Metabolism 46:684–690CrossRefPubMed Vettor R, Lombardi AM, Fabris R et al (1997) Lactate infusion in anesthetized rats produces insulin resistance in heart and skeletal muscles. Metabolism 46:684–690CrossRefPubMed
33.
Zurück zum Zitat Choi CS, Kim YB, Lee FN, Zabolotny JM, Kahn BB, Youn JH (2002) Lactate induces insulin resistance in skeletal muscle by suppressing glycolysis and impairing insulin signaling. Am J Physiol Endocrinol Metab 283:E233–E240CrossRefPubMed Choi CS, Kim YB, Lee FN, Zabolotny JM, Kahn BB, Youn JH (2002) Lactate induces insulin resistance in skeletal muscle by suppressing glycolysis and impairing insulin signaling. Am J Physiol Endocrinol Metab 283:E233–E240CrossRefPubMed
34.
Zurück zum Zitat Ahlborg G (1985) Mechanism for glycogenolysis in nonexercising human muscle during and after exercise. Am J Physiol 248:E540–E545PubMed Ahlborg G (1985) Mechanism for glycogenolysis in nonexercising human muscle during and after exercise. Am J Physiol 248:E540–E545PubMed
35.
Zurück zum Zitat Bergman BC, Wolfel EE, Butterfield GE et al (1999) Active muscle and whole body lactate kinetics after endurance training in men. J Appl Physiol (1985) 87:1684–1696 Bergman BC, Wolfel EE, Butterfield GE et al (1999) Active muscle and whole body lactate kinetics after endurance training in men. J Appl Physiol (1985) 87:1684–1696
36.
Zurück zum Zitat Wilson TH (1956) The role of lactic acid production in glucose absorption from the intestine. J Biol Chem 222:751–763PubMed Wilson TH (1956) The role of lactic acid production in glucose absorption from the intestine. J Biol Chem 222:751–763PubMed
37.
Zurück zum Zitat Renold AE, Hastings AB, Nesbett FB, Ashmore J (1955) Studies on carbohydrate metabolism in rat liver slices. IV. Biochemical sequence of events after insulin administration. J Biol Chem 213:135–146PubMed Renold AE, Hastings AB, Nesbett FB, Ashmore J (1955) Studies on carbohydrate metabolism in rat liver slices. IV. Biochemical sequence of events after insulin administration. J Biol Chem 213:135–146PubMed
38.
Zurück zum Zitat Moberg E, Sjoberg S, Hagstrom-Toft E, Bolinder J (2002) No apparent suppression by insulin of in vivo skeletal muscle lipolysis in nonobese women. Am J Physiol Endocrinol Metab 283:E295–E301CrossRefPubMed Moberg E, Sjoberg S, Hagstrom-Toft E, Bolinder J (2002) No apparent suppression by insulin of in vivo skeletal muscle lipolysis in nonobese women. Am J Physiol Endocrinol Metab 283:E295–E301CrossRefPubMed
39.
Zurück zum Zitat Watt MJ, Stellingwerff T, Heigenhauser GJ, Spriet LL (2003) Effects of plasma adrenaline on hormone-sensitive lipase at rest and during moderate exercise in human skeletal muscle. J Physiol 550:325–332CrossRefPubMedPubMedCentral Watt MJ, Stellingwerff T, Heigenhauser GJ, Spriet LL (2003) Effects of plasma adrenaline on hormone-sensitive lipase at rest and during moderate exercise in human skeletal muscle. J Physiol 550:325–332CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat Hodgetts V, Coppack SW, Frayn KN, Hockaday TD (1991) Factors controlling fat mobilization from human subcutaneous adipose tissue during exercise. J Appl Physiol (1985) 71:445–451 Hodgetts V, Coppack SW, Frayn KN, Hockaday TD (1991) Factors controlling fat mobilization from human subcutaneous adipose tissue during exercise. J Appl Physiol (1985) 71:445–451
41.
Zurück zum Zitat Chokkalingam K, Tsintzas K, Norton L, Jewell K, Macdonald IA, Mansell PI (2007) Exercise under hyperinsulinaemic conditions increases whole-body glucose disposal without affecting muscle glycogen utilisation in type 1 diabetes. Diabetologia 50:414–421CrossRefPubMed Chokkalingam K, Tsintzas K, Norton L, Jewell K, Macdonald IA, Mansell PI (2007) Exercise under hyperinsulinaemic conditions increases whole-body glucose disposal without affecting muscle glycogen utilisation in type 1 diabetes. Diabetologia 50:414–421CrossRefPubMed
42.
Zurück zum Zitat Robitaille M, Dube MC, Weisnagel SJ et al (2007) Substrate source utilization during moderate intensity exercise with glucose ingestion in type 1 diabetic patients. J Appl Physiol (1985) 103:119–124CrossRef Robitaille M, Dube MC, Weisnagel SJ et al (2007) Substrate source utilization during moderate intensity exercise with glucose ingestion in type 1 diabetic patients. J Appl Physiol (1985) 103:119–124CrossRef
43.
Zurück zum Zitat Keytel LR, Goedecke JH, Noakes TD et al (2005) Prediction of energy expenditure from heart rate monitoring during submaximal exercise. J Sports Sci 23:289–297CrossRefPubMed Keytel LR, Goedecke JH, Noakes TD et al (2005) Prediction of energy expenditure from heart rate monitoring during submaximal exercise. J Sports Sci 23:289–297CrossRefPubMed
Metadaten
Titel
Metabolic and hormonal response to intermittent high-intensity and continuous moderate intensity exercise in individuals with type 1 diabetes: a randomised crossover study
verfasst von
Lia Bally
Thomas Zueger
Tania Buehler
Ayse S. Dokumaci
Christian Speck
Nicola Pasi
Carlos Ciller
Daniela Paganini
Katrin Feller
Hannah Loher
Robin Rosset
Matthias Wilhelm
Luc Tappy
Chris Boesch
Christoph Stettler
Publikationsdatum
01.04.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Diabetologia / Ausgabe 4/2016
Print ISSN: 0012-186X
Elektronische ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-015-3854-7

Weitere Artikel der Ausgabe 4/2016

Diabetologia 4/2016 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.