Impact of Endurance Exercise Training in the Fasted State on Muscle Biochemistry and Metabolism in Healthy Subjects: Can These Effects be of Particular Clinical Benefit to Type 2 Diabetes Mellitus and Insulin-Resistant Patients?

Abstract

Exercise training intervention is a cornerstone in the care of type 2 diabetes mellitus (T2DM) and insulin resistance (IR), and it is pursued in order to optimize exercise interventions for these patients. In this regard, the nutritional state of patients during exercise (being in the fed or fasted state) can be of particular interest. The aim of the present review is to describe the impact of endurance exercise (training) in the fasted versus fed state on parameters of muscle biochemistry and metabolism linked to glycemic control or insulin sensitivity in healthy subjects. From these data it can then be deduced whether exercise training in the fasted state may be relevant to patients with T2DM or IR. In healthy subjects, acute endurance exercise in the fasted state is accompanied by lower blood insulin and elevated blood free fatty acid concentrations, stable blood glucose concentrations (in the first 60–90 min), superior intramyocellular triacylglycerol oxidation and whole-body lipolysis, and muscle glycogen preservation. Long-term exercise training in the fasted state in healthy subjects is associated with greater improvements in insulin sensitivity, basal muscle fat uptake capacity, and oxidation. Therefore, promising results of exercise (training) in the fasted state have been found in healthy subjects on parameters of muscle biochemistry and metabolism linked to insulin sensitivity and glycemic control. Whether exercise training intervention in which exercise sessions are organized in the fasted state may be more effective in improving insulin sensitivity or glycemic control in T2DM patients and insulin-resistant individuals warrants investigation.

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References

  1. 1.

    Umpierre D, Ribeiro PAB, Kramer CK, et al. Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: a systematic review and meta-analysis. JAMA. 2011;305:1790–9.

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    UK Prospective Diabetes Study Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risks of complications in patients with type 2 diabetes (UKPDS 33). Lancet. 1998;352:837–53.

    Article  Google Scholar 

  3. 3.

    Khaw K, Wareham N, Luben R, et al. Glycated haemoglobin, diabetes and mortality in men in Norfolk cohort of European Prospective Investigation of Cancer and Nutrition (EPICNorfolk). BMJ. 2001;322:15–8.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Sigal RJ, Kenny GP, Boule NG, et al. Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Ann Intern Med. 2007;147:357–69.

    Article  PubMed  Google Scholar 

  5. 5.

    Dunstan DW, Mori TA, Puddey IB, et al. The independent and combined effects of aerobic exercise and dietary fish intake on serum lipids and glycaemic control in NIDDM. Diabetes Care. 1997;20:913–21.

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Praet SF, van Rooij ESJ, Wijtvliet A, et al. Brisk walking compared with an individual medical fitness programme for patients with type 2 diabetes: a randomised controlled trial. Diabetologia. 2008;51:736–46.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Boule NG, Kenny GP, Haddad E, et al. Meta-analysis of the effect of structured exercise training on cardiorespiratory fitness in type 2 diabetes mellitus. Diabetologia. 2003;46:1071–81.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Vanhees L, Geladas N, Hansen D, et al. Importance of characteristics and modalities of physical activity and exercise in the management of cardiovascular health in individuals with cardiovascular risk factors: recommendations from the European Association of Cardiovascular Prevention and Rehabilitation. Eur J Prev Cardiol. 2012;19:1005–33.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Colberg SR, Albright AL, Blissmer BJ, et al. Exercise and type 2 diabetes. American College of Sports Medicine and the American Diabetes Association: joint position statement. Med Sci Sports Exerc. 2010;42:2282–303.

    Article  PubMed  Google Scholar 

  10. 10.

    American Diabetes Association. Standards of medical care in diabetes—2012. Diabetes Care. 2012;35:S11–63.

    Article  Google Scholar 

  11. 11.

    Hansen D, Peeters S, Zwaenepoel B, et al. Exercise assessment and prescription in patients with type 2 diabetes in the private and home care setting: clinical recommendations from AXXON (Belgian Physical Therapy Association). Phys Ther. 2013;93:597–610.

    Article  PubMed  Google Scholar 

  12. 12.

    Laaksonen DE, Lindström J, Lakka TA, et al. Finnish diabetes prevention study. physical activity in the prevention of type 2 diabetes: the Finnish Diabetes Prevention Study. Diabetes. 2005;54:158–65.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Hansen D, Dendale P, van Loon LJC, et al. The effects of training modalities on clinical benefits of exercise intervention in cardiovascular disease risk patients or type 2 diabetes mellitus. Sports Med. 2010;40:921–40.

    Article  PubMed  Google Scholar 

  14. 14.

    Umpierre D, Ribeiro PA, Schaan BD, et al. Volume of supervised exercise training impacts glycaemic control in patients with type 2 diabetes: a systematic review with meta-regression analysis. Diabetologia. 2013;56:242–51.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Francois ME, Little JP. Effectiveness and safety of high-intensity interval training in patients with type 2 diabetes. Diabetes Spectr. 2015;28:39–44.

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Haxhi J, Scotto di Palumbo A, Sacchetti M. Exercising for metabolic control: is timing important? Ann Nutr Metab. 2012;62:14–25.

    Article  PubMed  Google Scholar 

  17. 17.

    Horowitz JF, Mora-Rodriguez R, Byerley LO, et al. Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am J Physiol Endocrinol Metab. 1997;273:E768–75.

    CAS  Google Scholar 

  18. 18.

    De Bock K, Richter EA, Russell AP, et al. Exercise in the fasted state facilitates fibre type-specific intramyocellular lipid breakdown and stimulates glycogen resynthesis in humans. J Physiol. 2005;564:649–60.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Bennard P, Doucet E. Acute effects of exercise timing and breakfast meal glycemic index on exercise-induced fat oxidation. Appl Physiol Nutr Metab. 2006;31:502–11.

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Lane SC, Bird SR, Burke LM, et al. Effect of a carbohydrate mouth rinse on simulated cycling time-trial performance commenced in a fed or fasted state. Appl Physiol Nutr Metab. 2013;38:134–9.

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Scott JPR, Sale C, Greeves JP, et al. Effect of fasting versus feeding on the bone metabolic response to running. Bone. 2012;51:990–9.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Paul GL, Rokusek JT, Dykstra GL, et al. Oat, wheat or corn cereal ingestion before exercise alters metabolism in humans. J Nutr. 1996;126:1372–81.

    CAS  PubMed  Google Scholar 

  23. 23.

    DeMarco HM, Sucher KP, Cisar CJ, et al. Pre-exercise carbohydrate meals: application of glycemic index. Med Sci Sports Exerc. 1999;31:164–70.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Wu CL, Nicholas C, Williams C, et al. The influence of high-carbohydrate meals with different glycaemic indices on substrate utilisation during subsequent exercise. Br J Nutr. 2003;90:1049–56.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Coyle EF, Coggan AR, Hemmert MK, et al. Substrate usage during prolonged exercise following a preexercise meal. J Appl Physiol. 1985;59:429–33.

    CAS  PubMed  Google Scholar 

  26. 26.

    Montain SJ, Hopper MK, Coggan AR, Coyle EF. Exercise metabolism at different time intervals after a meal. J Appl Physiol. 1991;70(2):882–8.

    CAS  PubMed  Google Scholar 

  27. 27.

    de Lima FD, Correia AL, Teixeira Dda S, et al. Acute metabolic response to fasted and postprandial exercise. Int J Gen Med. 2015;8:255–60.

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Enevoldsen LH, Simonsen L, Macdonald IA, et al. The combined effects of exercise and food intake on adipose tissue and splanchnic metabolism. J Physiol. 2004;561:871–82.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Schwalm C, Jamart C, Benoit N, et al. Activation of autophagy in human skeletal muscle is dependent on exercise intensity and AMPK activation. FASEB J. 2015;29:3515–26.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Loy SF, Conlee RK, Winder WW, et al. Effects of 24-hour fast on cycling endurance time at two different intensities. J Appl Physiol. 1986;61:654–9.

    CAS  PubMed  Google Scholar 

  31. 31.

    Whitley HA, Humphreys SM, Campbell IT, et al. Metabolic and performance responses during endurance exercise after high-fat and high-carbohydrate meals. J Appl Physiol. 1998;85:418–24.

    CAS  PubMed  Google Scholar 

  32. 32.

    Dohm GL, Beeker RT, Israel RG, et al. Metabolic responses to exercise after fasting. J Appl Physiol. 1986;61:1363–8.

    CAS  PubMed  Google Scholar 

  33. 33.

    Schneiter P, Di Vetta V, Jequier E, et al. Effect of physical exercise on glycogen turnover and net substrate utilization according to nutritional state. Am J Physiol Endocrinol Metab. 1995;32:E1031–6.

    Google Scholar 

  34. 34.

    Dumas JF, Simard G, Flamment M, et al. Is skeletal muscle mitochondrial dysfunction a cause or an indirect consequence of insulin resistance in humans? Diabetes Metab. 2009;35:159–67.

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    De Bock K, Derave W, Eijnde BO, et al. Effect of training in the fasted state on metabolic responses during exercise with carbohydrate intake. J Appl Physiol. 2008;104:1045–55.

    Article  PubMed  Google Scholar 

  36. 36.

    Van Proeyen K, Szlufcik K, Nielens H, et al. Training in the fasted state improves glucose tolerance during fat-rich diet. J Physiol. 2010;588:4289–302.

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Stannard SR, Buckley AJ, Edge JA, et al. Adaptations to skeletal muscle with endurance exercise training in the acutely fed versus overnight-fasted state. J Sci Med Sport. 2010;13:465–9.

    Article  PubMed  Google Scholar 

  38. 38.

    Van Proeyen K, Szlufcik K, Nielens H, et al. High-fat diet overrules the effects of training on fiber-specific intramyocellular lipid utilization during exercise. J Appl Physiol. 2011;111:108–16.

    Article  PubMed  Google Scholar 

  39. 39.

    Van Proeyen K, Szlufcik K, Nielens H, et al. Beneficial metabolic adaptations due to endurance exercise training in the fasted state. J Appl Physiol. 2011;110:236–45.

    Article  PubMed  Google Scholar 

  40. 40.

    Van Proeyen K, De Bock K, Hespel P. Training in the fasted state facilitates re-activation of eEF2 activity during recovery from endurance exercise. Eur J Appl Physiol. 2011;111:1297–305.

    Article  PubMed  Google Scholar 

  41. 41.

    Schoenfeld BJ, Aragon AA, Wilborn CD, et al. Body composition changes associated with fasted versus non-fasted aerobic exercise. J Int Soc Sports Nutr. 2014;11:54.

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Gillen JB, Percival ME, Ludzki A, et al. Interval training in the fed or fasted state improves body composition and muscle oxidative capacity in overweight women. Obesity. 2013;21:2249–55.

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Nieman DC, Carlson KA, Brandstater ME, et al. Running endurance in 27-h-fasted humans. J Appl Physiol. 1987;63:2502–9.

    CAS  PubMed  Google Scholar 

  44. 44.

    Bergman BC, Brooks GA. Respiratory gas-exchange ratios during graded exercise in fed and fasted trained and untrained men. J Appl Physiol. 1999;86:479–87.

    CAS  PubMed  Google Scholar 

  45. 45.

    Kang J, Raines E, Rosenberg J, et al. Metabolic responses during postprandial exercise. Res Sports Med. 2013;21:240–52.

    PubMed  Google Scholar 

  46. 46.

    Peake JM, Tan SJ, Markworth JF, et al. Metabolic and hormonal responses to isoenergetic high-intensity interval exercise and continuous moderate-intensity exercise. Am J Physiol Endocrinol Metab. 2014;307:E539–52.

    CAS  Article  PubMed  Google Scholar 

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Correspondence to Dominique Hansen.

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Dominique Hansen, Dorien De Strijcker, and Patrick Calders declare that they have no conflicts of interest relevant to the content of this review.

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Hansen, D., De Strijcker, D. & Calders, P. Impact of Endurance Exercise Training in the Fasted State on Muscle Biochemistry and Metabolism in Healthy Subjects: Can These Effects be of Particular Clinical Benefit to Type 2 Diabetes Mellitus and Insulin-Resistant Patients?. Sports Med 47, 415–428 (2017). https://doi.org/10.1007/s40279-016-0594-x

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Keywords

  • Glycemic Control
  • Exercise Training
  • Fast State
  • Endurance Exercise
  • Muscle Glycogen