Sports Medicine

, Volume 49, Issue 2, pp 255–268 | Cite as

Effect of Exercise Intervention on Cardiac Function in Type 2 Diabetes Mellitus: A Systematic Review

  • Maxim Verboven
  • Lisa Van Ryckeghem
  • Jamal Belkhouribchia
  • Paul Dendale
  • Bert O. Eijnde
  • Dominique HansenEmail author
  • Virginie Bito
Systematic Review



The effect of exercise on cardiac function/structure in type 2 diabetes mellitus (T2DM) with or without diabetic cardiomyopathy (DCM) is not yet completely understood. To date, results of studies have been controversial with variable outcomes due to the variety of exercise modalities.


The aim of the present review was to examine the impact of exercise intervention, and different types of exercise, on cardiac function and structure in T2DM through a systematic literature review, combining both pre-clinical and clinical studies.


A systematic literature search was performed on PubMed, Web of Science, and PEDro to identify studies up to 2 April 2018. Articles were included when well-defined exercise protocols were provided, and cardiac function in T2DM patients or validated animal models was examined.


In diabetic animals, improvements in both diastolic and systolic function through exercise therapy were mainly attributed to reduced collagen deposition. In T2DM patients, improvements were observed in diastolic function, but not consistently in systolic function, after endurance (and combined resistance) exercise training. Different exercise intervention modalities and exercise types seemed equally effective in improving cardiac structure and function.


Exercise training elicits significant improvements in diastolic function and beneficial remodeling in T2DM and DCM animal models, but not necessarily improvements in systolic function and left ventricular structure, regardless of exercise type. Therefore, exercise intervention should be a cornerstone in the treatment of T2DM patients not only to improve glycemic control but also to specifically enhance cardiac function.


Compliance with Ethical Standards


No sources of funding were used to assist in the preparation of this article. Funding was provided by BOF-scholarship from Hasselt University (Grant no. 15NI06-BOF).

Conflict of interest

Maxim Verboven, Lisa Van Ryckeghem, Jamal Belkhouribchia, Paul Dendale, Bert O. Eijnde, Dominique Hansen, and Virginie Bito declare that they have no conflicts of interest relevant to the content of this review.

Supplementary material

40279_2018_1003_MOESM1_ESM.docx (53 kb)
Supplementary material 1 (DOCX 53 kb)


  1. 1.
    Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40–50.Google Scholar
  2. 2.
    Jia G, DeMarco VG, Sowers JR. Insulin resistance and hyperinsulinaemia in diabetic cardiomyopathy. Nat Rev Endocrinol. 2016;12(3):144–53.Google Scholar
  3. 3.
    Dandamudi S, Slusser J, Mahoney DW, Redfield MM, Rodeheffer RJ, Chen HH. The prevalence of diabetic cardiomyopathy: a population-based study in Olmsted County, Minnesota. J Card Fail. 2014;20(5):304–9.Google Scholar
  4. 4.
    Jorgensen PG, Jensen MT, Mogelvang R, von Scholten BJ, Bech J, Fritz-Hansen T, et al. Abnormal echocardiography in patients with type 2 diabetes and relation to symptoms and clinical characteristics. Diabetes Vasc Dis Res. 2016;13(5):321–30.Google Scholar
  5. 5.
    Asghar O, Al-Sunni A, Khavandi K, Khavandi A, Withers S, Greenstein A, et al. Diabetic cardiomyopathy. Clin Sci (Lond). 2009;116(10):741–60.Google Scholar
  6. 6.
    Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation. 2007;115(25):3213–23.Google Scholar
  7. 7.
    Lee WS, Kim J. Diabetic cardiomyopathy: where we are and where we are going. Korean J Intern Med. 2017;32(3):404–21.Google Scholar
  8. 8.
    Waddingham MT, Edgley AJ, Tsuchimochi H, Kelly DJ, Shirai M, Pearson JT. Contractile apparatus dysfunction early in the pathophysiology of diabetic cardiomyopathy. World J Diabetes. 2015;6(7):943–60.Google Scholar
  9. 9.
    Murarka S, Movahed MR. Diabetic cardiomyopathy. J Card Fail. 2010;16(12):971–9.Google Scholar
  10. 10.
    Cassidy S, Thoma C, Hallsworth K, Parikh J, Hollingsworth KG, Taylor R, et al. High intensity intermittent exercise improves cardiac structure and function and reduces liver fat in patients with type 2 diabetes: a randomised controlled trial. Diabetologia. 2016;59(1):56–66.Google Scholar
  11. 11.
    Li Y, Cai M, Cao L, Qin X, Zheng T, Xu X, et al. Endurance exercise accelerates myocardial tissue oxygenation recovery and reduces ischemia reperfusion injury in mice. PLoS One. 2014;9(12):e114205.Google Scholar
  12. 12.
    Marongiu E, Crisafulli A. Cardioprotection acquired through exercise: the role of ischemic preconditioning. Curr Cardiol Rev. 2014;10(4):336–48.Google Scholar
  13. 13.
    Garza MA, Wason EA, Zhang JQ. Cardiac remodeling and physical training post myocardial infarction. World J Cardiol. 2015;7(2):52–64.Google Scholar
  14. 14.
    Hordern MD, Coombes JS, Cooney LM, Jeffriess L, Prins JB, Marwick TH. Effects of exercise intervention on myocardial function in type 2 diabetes. Heart. 2009;95(16):1343–9.Google Scholar
  15. 15.
    Sagar VA, Davies EJ, Briscoe S, Coats AJ, Dalal HM, Lough F, et al. Exercise-based rehabilitation for heart failure: systematic review and meta-analysis. Open Heart. 2015;2(1):e000163.Google Scholar
  16. 16.
    Boule NG, Haddad E, Kenny GP, Wells GA, Sigal RJ. Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials. JAMA. 2001;286(10):1218–27.Google Scholar
  17. 17.
    Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care. 2010;33(12):2692–6.Google Scholar
  18. 18.
    Kadoglou NP, Iliadis F, Angelopoulou N, Perrea D, Ampatzidis G, Liapis CD, et al. The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur J Cardiovasc Prev Rehabil. 2007;14(6):837–43.Google Scholar
  19. 19.
    Kelley GA, Kelley KS. Effects of aerobic exercise on lipids and lipoproteins in adults with type 2 diabetes: a meta-analysis of randomized-controlled trials. Public Health. 2007;121(9):643–55.Google Scholar
  20. 20.
    Nojima H, Watanabe H, Yamane K, Kitahara Y, Sekikawa K, Yamamoto H, et al. Effect of aerobic exercise training on oxidative stress in patients with type 2 diabetes mellitus. Metabolism. 2008;57(2):170–6.Google Scholar
  21. 21.
    Stratton IM, Adler AI, Neil HA, Matthews DR, Manley SE, Cull CA, et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ. 2000;321(7258):405–12.Google Scholar
  22. 22.
    McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL. Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol. 2010;160(7):1573–6.Google Scholar
  23. 23.
    Sherrington C, Herbert RD, Maher CG, Moseley AM. PEDro. A database of randomized trials and systematic reviews in physiotherapy. Man Ther. 2000;5(4):223–6.Google Scholar
  24. 24.
    Hollekim-Strand SM, Bjorgaas MR, Albrektsen G, Tjonna AE, Wisloff U, Ingul CB. High-intensity interval exercise effectively improves cardiac function in patients with type 2 diabetes mellitus and diastolic dysfunction: a randomized controlled trial. J Am Coll Cardiol. 2014;64(16):1758–60.Google Scholar
  25. 25.
    Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I. Exercise training does not improve myocardial diastolic tissue velocities in type 2 diabetes. Cardiovasc Ultrasound. 2007;5:32.Google Scholar
  26. 26.
    Sacre JW, Jellis CL, Jenkins C, Haluska BA, Baumert M, Coombes JS, et al. A six-month exercise intervention in subclinical diabetic heart disease: effects on exercise capacity, autonomic and myocardial function. Metabolism. 2014;63(9):1104–14.Google Scholar
  27. 27.
    Schmidt JF, Andersen TR, Horton J, Brix J, Tarnow L, Krustrup P, et al. Soccer training improves cardiac function in men with type 2 diabetes. Med Sci Sports Exerc. 2013;45(12):2223–33.Google Scholar
  28. 28.
    Hollekim-Strand SM, Hoydahl SF, Follestad T, Dalen H, Bjorgaas MR, Wisloff U, et al. Exercise training normalizes timing of left ventricular untwist rate, but not peak untwist rate, in individuals with type 2 diabetes and diastolic dysfunction: a pilot study. J Am Soc Echocardiogr. 2016;29(5):421–30.Google Scholar
  29. 29.
    Hafstad AD, Lund J, Hadler-Olsen E, Hoper AC, Larsen TS, Aasum E. High- and moderate-intensity training normalizes ventricular function and mechanoenergetics in mice with diet-induced obesity. Diabetes. 2013;62(7):2287–94.Google Scholar
  30. 30.
    Boardman NT, Hafstad AD, Lund J, Rossvoll L, Aasum E. Exercise of obese mice induces cardioprotection and oxygen sparing in hearts exposed to high-fat load. Am J Physiol Heart Circ Physiol. 2017;313(5):H1054–62.Google Scholar
  31. 31.
    Stolen TO, Hoydal MA, Kemi OJ, Catalucci D, Ceci M, Aasum E, et al. Interval training normalizes cardiomyocyte function, diastolic Ca2+ control, and SR Ca2+ release synchronicity in a mouse model of diabetic cardiomyopathy. Circ Res. 2009;105(6):527–36.Google Scholar
  32. 32.
    Kesherwani V, Chavali V, Hackfort BT, Tyagi SC, Mishra PK. Exercise ameliorates high fat diet induced cardiac dysfunction by increasing interleukin 10. Front Physiol. 2015;6:124.Google Scholar
  33. 33.
    Veeranki S, Givvimani S, Kundu S, Metreveli N, Pushpakumar S, Tyagi SC. Moderate intensity exercise prevents diabetic cardiomyopathy associated contractile dysfunction through restoration of mitochondrial function and connexin 43 levels in db/db mice. J Mol Cell Cardiol. 2016;92:163–73.Google Scholar
  34. 34.
    Wang H, Bei Y, Lu Y, Sun W, Liu Q, Wang Y, et al. Exercise prevents cardiac injury and improves mitochondrial biogenesis in advanced diabetic cardiomyopathy with PGC-1alpha and Akt activation. Cell Physiol Biochem. 2015;35(6):2159–68.Google Scholar
  35. 35.
    Ko TH, Marquez JC, Kim HK, Jeong SH, Lee S, Youm JB, et al. Resistance exercise improves cardiac function and mitochondrial efficiency in diabetic rat hearts. Pflugers Arch. 2018;470(2):263–75.Google Scholar
  36. 36.
    VanHoose L, Sawers Y, Loganathan R, Vacek JL, Stehno-Bittel L, Novikova L, et al. Electrocardiographic changes with the onset of diabetes and the impact of aerobic exercise training in the Zucker Diabetic Fatty (ZDF) rat. Cardiovasc Diabetol. 2010;9:56.Google Scholar
  37. 37.
    American Diabetes Association. 4. Lifestyle management: standards of medical care in diabetes-2018. Diabetes Care. 2018;41(Suppl 1):S38–50.Google Scholar
  38. 38.
    Colberg SR. Key points from the updated guidelines on exercise and diabetes. Front Endocrinol (Lausanne). 2017;8:33.Google Scholar
  39. 39.
    Howorka K, Pumprla J, Haber P, Koller-Strametz J, Mondrzyk J, Schabmann A. Effects of physical training on heart rate variability in diabetic patients with various degrees of cardiovascular autonomic neuropathy. Cardiovasc Res. 1997;34(1):206–14.Google Scholar
  40. 40.
    Hansen D, Coninx K, Dendale P. The EAPC EXPERT tool. Eur Heart J. 2017;38(30):2318–20.Google Scholar
  41. 41.
    Seeger JP, Lenting CJ, Schreuder TH, Landman TR, Cable NT, Hopman MT, et al. Interval exercise, but not endurance exercise, prevents endothelial ischemia–reperfusion injury in healthy subjects. Am J Physiol Heart Circ Physiol. 2015;308(4):H351–7.Google Scholar
  42. 42.
    Chilibeck PD, Bell GJ, Farrar RP, Martin TP. Higher mitochondrial fatty acid oxidation following intermittent versus continuous endurance exercise training. Can J Physiol Pharmacol. 1998;76(9):891–4.Google Scholar
  43. 43.
    Miele EM, Headley SAE. The effects of chronic aerobic exercise on cardiovascular risk factors in persons with diabetes mellitus. Curr Diab Rep. 2017;17(10):97.Google Scholar
  44. 44.
    Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther. 2010;128(1):191–227.Google Scholar
  45. 45.
    Nakamura M, Sadoshima J. Mechanisms of physiological and pathological cardiac hypertrophy. Nat Rev Cardiol. 2018;15(7):387–407.Google Scholar
  46. 46.
    Schultz MG, Hordern MD, Leano R, Coombes JS, Marwick TH, Sharman JE. Lifestyle change diminishes a hypertensive response to exercise in type 2 diabetes. Med Sci Sports Exerc. 2011;43(5):764–9.Google Scholar
  47. 47.
    Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90(1):207–58.Google Scholar
  48. 48.
    Drosatos K, Schulze PC. Cardiac lipotoxicity: molecular pathways and therapeutic implications. Curr Heart Fail Rep. 2013;10(2):109–21.Google Scholar
  49. 49.
    Anderson EJ, Kypson AP, Rodriguez E, Anderson CA, Lehr EJ, Neufer PD. Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol. 2009;54(20):1891–8.Google Scholar
  50. 50.
    Pulinilkunnil T, Kienesberger PC, Nagendran J, Waller TJ, Young ME, Kershaw EE, et al. Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes. 2013;62(5):1464–77.Google Scholar
  51. 51.
    Diez J, Querejeta R, Lopez B, Gonzalez A, Larman M, Martinez Ubago JL. Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients. Circulation. 2002;105(21):2512–7.Google Scholar
  52. 52.
    Motoyasu M, Kurita T, Onishi K, Uemura S, Tanigawa T, Okinaka T, et al. Correlation between late gadolinium enhancement and diastolic function in hypertrophic cardiomyopathy assessed by magnetic resonance imaging. Circ J. 2008;72(3):378–83.Google Scholar
  53. 53.
    Duncan JG. Mitochondrial dysfunction in diabetic cardiomyopathy. Biochim Biophys Acta. 2011;1813(7):1351–9.Google Scholar
  54. 54.
    Hafstad AD, Boardman N, Aasum E. How exercise may amend metabolic disturbances in diabetic cardiomyopathy. Antioxid Redox Signal. 2015;22(17):1587–605.Google Scholar
  55. 55.
    Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging. 2016;17(12):1321–60.Google Scholar
  56. 56.
    Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R, et al. Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. J Am Soc Echocardiogr. 2015;28(2):183–93.Google Scholar
  57. 57.
    Brassard P, Legault S, Garneau C, Bogaty P, Dumesnil JG, Poirier P. Normalization of diastolic dysfunction in type 2 diabetics after exercise training. Med Sci Sports Exerc. 2007;39(11):1896–901.Google Scholar
  58. 58.
    Cugusi L, Cadeddu C, Nocco S, Orru F, Bandino S, Deidda M, et al. Effects of an aquatic-based exercise program to improve cardiometabolic profile, quality of life, and physical activity levels in men with type 2 diabetes mellitus. PM&R. 2015;7(2):141–8 (quiz 8).Google Scholar
  59. 59.
    Jonker JT, de Mol P, de Vries ST, Widya RL, Hammer S, van Schinkel LD, et al. Exercise and type 2 diabetes mellitus: changes in tissue-specific fat distribution and cardiac function. Radiology. 2013;269(2):434–42.Google Scholar
  60. 60.
    Schrauwen-Hinderling VB, Meex RC, Hesselink MK, van de Weijer T, Leiner T, Schar M, et al. Cardiac lipid content is unresponsive to a physical activity training intervention in type 2 diabetic patients, despite improved ejection fraction. Cardiovasc Diabetol. 2011;10:47.Google Scholar
  61. 61.
    The Norwegian Diabetes Association. Type 2-diabetes og fysisk aktivitet. Accessed Sept 2015.

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Maxim Verboven
    • 1
  • Lisa Van Ryckeghem
    • 1
    • 2
  • Jamal Belkhouribchia
    • 1
    • 2
  • Paul Dendale
    • 1
    • 3
  • Bert O. Eijnde
    • 1
  • Dominique Hansen
    • 1
    • 2
    • 3
    Email author
  • Virginie Bito
    • 1
  1. 1.BIOMED-Biomedical Research Centre, Faculty of Medicine and Life SciencesHasselt UniversityDiepenbeekBelgium
  2. 2.REVAL-Rehabilitation Research Centre, Faculty of Rehabilitation SciencesHasselt UniversityDiepenbeekBelgium
  3. 3.Heart Centre Hasselt, Jessa HospitalHasseltBelgium

Personalised recommendations