The Effect of Regular Exercise on Insulin Sensitivity in Type 2 Diabetes Mellitus: A Systematic Review and Meta-Analysis

Kimberley L Way, Daniel A Hackett, Michael K Baker, Nathan A Johnson, Kimberley L Way, Daniel A Hackett, Michael K Baker, Nathan A Johnson

Abstract

The purpose of this study was to examine the effect of regular exercise training on insulin sensitivity in adults with type 2 diabetes mellitus (T2DM) using the pooled data available from randomised controlled trials. In addition, we sought to determine whether short-term periods of physical inactivity diminish the exercise-induced improvement in insulin sensitivity. Eligible trials included exercise interventions that involved ≥3 exercise sessions, and reported a dynamic measurement of insulin sensitivity. There was a significant pooled effect size (ES) for the effect of exercise on insulin sensitivity (ES, -0.588; 95% confidence interval [CI], -0.816 to -0.359; P<0.001). Of the 14 studies included for meta-analyses, nine studies reported the time of data collection from the last exercise bout. There was a significant improvement in insulin sensitivity in favour of exercise versus control between 48 and 72 hours after exercise (ES, -0.702; 95% CI, -1.392 to -0.012; P=0.046); and this persisted when insulin sensitivity was measured more than 72 hours after the last exercise session (ES, -0.890; 95% CI, -1.675 to -0.105; P=0.026). Regular exercise has a significant benefit on insulin sensitivity in adults with T2DM and this may persist beyond 72 hours after the last exercise session.

Keywords: Aerobic training; Glucose tolerance test; Hyperinsulinaemic euglycaemic clamp; Insulin resistance; Resistance training.

Conflict of interest statement

No potential conflict of interest relevant to this article was reported.

Figures

Fig. 1. Exercise versus control on insulin…
Fig. 1. Exercise versus control on insulin sensitivity. ES, effect size; CI, confidence interval.
Fig. 2. The effect of exercise on…
Fig. 2. The effect of exercise on insulin sensitivity (A) 72 hours after the last bout of exercise. ES, effect size; CI, confidence interval.

References

    1. Colberg SR, Albright AL, Blissmer BJ, Braun B, Chasan-Taber L, Fernhall B, Regensteiner JG, Rubin RR, Sigal RJ American College of Sports Medicine; American Diabetes Association. Exercise and type 2 diabetes: American College of Sports Medicine and the American Diabetes Association: joint position statement. Exercise and type 2 diabetes. Med Sci Sports Exerc. 2010;42:2282–2303.
    1. Marwick TH, Hordern MD, Miller T, Chyun DA, Bertoni AG, Blumenthal RS, Philippides G, Rocchini A Council on Clinical Cardiology, American Heart Association Exercise, Cardiac Rehabilitation, and Prevention Committee; Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing; Council on Nutrition, Physical Activity, and Metabolism; Interdisciplinary Council on Quality of Care and Outcomes Research. Exercise training for type 2 diabetes mellitus: impact on cardiovascular risk: a scientific statement from the American Heart Association. Circulation. 2009;119:3244–3262.
    1. Umpierre D, Ribeiro PA, Kramer CK, Leitao CB, Zucatti AT, Azevedo MJ, Gross JL, Ribeiro JP, Schaan BD. 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;305:1790–1799.
    1. Bonora E, Formentini G, Calcaterra F, Lombardi S, Marini F, Zenari L, Saggiani F, Poli M, Perbellini S, Raffaelli A, Cacciatori V, Santi L, Targher G, Bonadonna R, Muggeo M. HOMA-estimated insulin resistance is an independent predictor of cardiovascular disease in type 2 diabetic subjects: prospective data from the Verona Diabetes Complications Study. Diabetes Care. 2002;25:1135–1141.
    1. Facchini FS, Hua N, Abbasi F, Reaven GM. Insulin resistance as a predictor of age-related diseases. J Clin Endocrinol Metab. 2001;86:3574–3578.
    1. Borghouts LB, Keizer HA. Exercise and insulin sensitivity: a review. Int J Sports Med. 2000;21:1–12.
    1. Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93:993–1017.
    1. Kraniou GN, Cameron-Smith D, Hargreaves M. Acute exercise and GLUT4 expression in human skeletal muscle: influence of exercise intensity. J Appl Physiol (1985) 2006;101:934–937.
    1. Praet SF, van Loon LJ. Optimizing the therapeutic benefits of exercise in type 2 diabetes. J Appl Physiol (1985) 2007;103:1113–1120.
    1. O'Gorman DJ, Karlsson HK, McQuaid S, Yousif O, Rahman Y, Gasparro D, Glund S, Chibalin AV, Zierath JR, Nolan JJ. Exercise training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein content in patients with type 2 diabetes. Diabetologia. 2006;49:2983–2992.
    1. Singh B, Saxena A. Surrogate markers of insulin resistance: a review. World J Diabetes. 2010;1:36–47.
    1. Conn VS, Koopman RJ, Ruppar TM, Phillips LJ, Mehr DR, Hafdahl AR. Insulin sensitivity following exercise interventions: systematic review and meta-analysis of outcomes among healthy adults. J Prim Care Community Health. 2014;5:211–222.
    1. Wallace TM, Matthews DR. The assessment of insulin resistance in man. Diabet Med. 2002;19:527–534.
    1. Nijpels G, van der Wal PS, Bouter LM, Heine RJ. Comparison of three methods for the quantification of beta-cell function and insulin sensitivity. Diabetes Res Clin Pract. 1994;26:189–195.
    1. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377–384.
    1. Higgins JP, Green S Cochrane Collaboration. Cochrane handbook for systematic reviews of interventions. Chichester: Wiley-Blackwell; 2008.
    1. Dunstan DW, Mori TA, Puddey IB, Beilin LJ, Burke V, Morton AR, Stanton KG. The independent and combined effects of aerobic exercise and dietary fish intake on serum lipids and glycemic control in NIDDM. A randomized controlled study. Diabetes Care. 1997;20:913–921.
    1. Tamura Y, Tanaka Y, Sato F, Choi JB, Watada H, Niwa M, Kinoshita J, Ooka A, Kumashiro N, Igarashi Y, Kyogoku S, Maehara T, Kawasumi M, Hirose T, Kawamori R. Effects of diet and exercise on muscle and liver intracellular lipid contents and insulin sensitivity in type 2 diabetic patients. J Clin Endocrinol Metab. 2005;90:3191–3196.
    1. Cuff DJ, Meneilly GS, Martin A, Ignaszewski A, Tildesley HD, Frohlich JJ. Effective exercise modality to reduce insulin resistance in women with type 2 diabetes. Diabetes Care. 2003;26:2977–2982.
    1. Baldi JC, Snowling N. Resistance training improves glycaemic control in obese type 2 diabetic men. Int J Sports Med. 2003;24:419–423.
    1. Boudou P, Sobngwi E, Mauvais-Jarvis F, Vexiau P, Gautier JF. Absence of exercise-induced variations in adiponectin levels despite decreased abdominal adiposity and improved insulin sensitivity in type 2 diabetic men. Eur J Endocrinol. 2003;149:421–424.
    1. Dunstan DW, Puddey IB, Beilin LJ, Burke V, Morton AR, Stanton KG. Effects of a short-term circuit weight training program on glycaemic control in NIDDM. Diabetes Res Clin Pract. 1998;40:53–61.
    1. Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, Goto Y, Yoshimasa Y, Miyamoto Y. Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010;17:828–833.
    1. Karstoft K, Winding K, Knudsen SH, Nielsen JS, Thomsen C, Pedersen BK, Solomon TP. The effects of free-living interval-walking training on glycemic control, body composition, and physical fitness in type 2 diabetic patients: a randomized, controlled trial. Diabetes Care. 2013;36:228–236.
    1. Tan S, Li W, Wang J. Effects of six months of combined aerobic and resistance training for elderly patients with a long history of type 2 diabetes. J Sports Sci Med. 2012;11:495–501.
    1. Tessier D, Menard J, Fulop T, Ardilouze J, Roy M, Dubuc N, Dubois M, Gauthier P. Effects of aerobic physical exercise in the elderly with type 2 diabetes mellitus. Arch Gerontol Geriatr. 2000;31:121–132.
    1. Winnick JJ, Sherman WM, Habash DL, Stout MB, Failla ML, Belury MA, Schuster DP. Short-term aerobic exercise training in obese humans with type 2 diabetes mellitus improves whole-body insulin sensitivity through gains in peripheral, not hepatic insulin sensitivity. J Clin Endocrinol Metab. 2008;93:771–778.
    1. Ligtenberg PC, Hoekstra JB, Bol E, Zonderland ML, Erkelens DW. Effects of physical training on metabolic control in elderly type 2 diabetes mellitus patients. Clin Sci (Lond) 1997;93:127–135.
    1. Middlebrooke AR, Elston LM, Macleod KM, Mawson DM, Ball CI, Shore AC, Tooke JE. Six months of aerobic exercise does not improve microvascular function in type 2 diabetes mellitus. Diabetologia. 2006;49:2263–2271.
    1. Mourier A, Gautier JF, De Kerviler E, Bigard AX, Villette JM, Garnier JP, Duvallet A, Guezennec CY, Cathelineau G. Mobilization of visceral adipose tissue related to the improvement in insulin sensitivity in response to physical training in NIDDM. Effects of branched-chain amino acid supplements. Diabetes Care. 1997;20:385–391.
    1. Ronnemaa T, Mattila K, Lehtonen A, Kallio V. A controlled randomized study on the effect of long-term physical exercise on the metabolic control in type 2 diabetic patients. Acta Med Scand. 1986;220:219–224.
    1. Wing RR, Epstein LH, Paternostro-Bayles M, Kriska A, Nowalk MP, Gooding W. Exercise in a behavioural weight control programme for obese patients with type 2 (non-insulin-dependent) diabetes. Diabetologia. 1988;31:902–909.
    1. Seidell JC, Flegal KM. Assessing obesity: classification and epidemiology. Br Med Bull. 1997;53:238–252.
    1. MacLeod SF, Terada T, Chahal BS, Boule NG. Exercise lowers postprandial glucose but not fasting glucose in type 2 diabetes: a meta-analysis of studies using continuous glucose monitoring. Diabetes Metab Res Rev. 2013;29:593–603.
    1. Muniyappa R, Lee S, Chen H, Quon MJ. Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab. 2008;294:E15–E26.
    1. Bogardus C, Thuillez P, Ravussin E, Vasquez B, Narimiga M, Azhar S. Effect of muscle glycogen depletion on in vivo insulin action in man. J Clin Invest. 1983;72:1605–1610.
    1. Devlin JT, Hirshman M, Horton ED, Horton ES. Enhanced peripheral and splanchnic insulin sensitivity in NIDDM men after single bout of exercise. Diabetes. 1987;36:434–439.
    1. McCoy M, Proietto J, Hargreves M. Effect of detraining on GLUT-4 protein in human skeletal muscle. J Appl Physiol (1985) 1994;77:1532–1536.
    1. Mikines KJ, Sonne B, Farrell PA, Tronier B, Galbo H. Effect of training on the dose-response relationship for insulin action in men. J Appl Physiol (1985) 1989;66:695–703.
    1. Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W, Berria R, Belfort R, Kashyap S, Mandarino LJ. Exercise training increases glycogen synthase activity and GLUT4 expression but not insulin signaling in overweight nondiabetic and type 2 diabetic subjects. Metabolism. 2004;53:1233–1242.
    1. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JF, Dela F. Strength training increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling in skeletal muscle in patients with type 2 diabetes. Diabetes. 2004;53:294–305.
    1. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol. 1984;56:831–838.
    1. Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with type 2 diabetes. Diabetologia. 2004;47:23–30.

Source: PubMed

3
Abonneren