Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Sports Medicine
Published in: Sports Medicine 11/2013

01-11-2013 | Systematic Review

Effects of Exercise Training on Arterial Function in Type 2 Diabetes Mellitus

A Systematic Review and Meta-Analysis

Authors: David Montero, Guillaume Walther, Eric Benamo, Antonia Perez-Martin, Agnès Vinet

Published in: Sports Medicine | Issue 11/2013

Login to get access

Abstract

Background and Objective

Controversy exists among trials assessing whether exercise can improve arterial function in type 2 diabetes mellitus (T2DM) subjects. Therefore the aim of this study was to systematically review and quantify the effects of exercise on arterial function in T2DM subjects.

Methods

MEDLINE, Cochrane, Scopus and Web of Science were searched up until January 2013 for randomized controlled trials evaluating the effects of exercise interventions lasting 4 weeks or more on arterial function in T2DM subjects. Flow-mediated dilation (FMD) and nitrate-mediated dilation (NMD) of the brachial conduit artery were considered for assessment of arterial endothelial function and smooth muscle function, respectively.

Results

Five randomized trials comparing exercise and control groups (overall n = 217) met the inclusion criteria. The mean exercise characteristics were as follows: 3.6 sessions per week, 67.5 min per session, intensity at 74.4 % of the maximum heart rate (HRmax), for 14 weeks. The post-intervention mean difference in FMD favoured the exercise groups over the control groups (2.23 %; P < 0.0001). No significant post-intervention mean difference in NMD (1.22 %; P = 0.29) was found between the groups. Neither heterogeneity nor publication bias was detected among the trials.

Conclusion

Exercise training alone improved FMD, showing its capacity to restore arterial endothelial function in T2DM subjects. However, further research is needed to determine whether longer and/or more intense exercise interventions could enhance arterial smooth muscle function in this population.
Appendix
Available only for authorised users
Literature
1.
Sigal RJ, Kenny GP, Wasserman DH, et al. Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care. 2006;29(6):1433–8.PubMedCrossRef
2.
Boule NG, Haddad E, Kenny GP, et al. 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.PubMedCrossRef
3.
Balducci S, Leonetti F, Di Mario U, et al. Is a long-term aerobic plus resistance training program feasible for and effective on metabolic profiles in type 2 diabetic patients? Diabetes Care. 2004;27(3):841–2.PubMedCrossRef
4.
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(8):1071–81.PubMedCrossRef
5.
Hakim AA, Petrovitch H, Burchfiel CM, et al. Effects of walking on mortality among nonsmoking retired men. N Engl J Med. 1998;338(2):94–9.PubMedCrossRef
6.
Hu FB, Stampfer MJ, Solomon C, et al. Physical activity and risk for cardiovascular events in diabetic women. Ann Intern Med. 2001;134(2):96–105.PubMedCrossRef
7.
Wei M, Gibbons LW, Kampert JB, et al. Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med. 2000;132(8):605–11.PubMedCrossRef
8.
Mora S, Cook N, Buring JE, et al. Physical activity and reduced risk of cardiovascular events: potential mediating mechanisms. Circulation. 2007;116(19):2110–8.PubMedCrossRef
9.
Joyner MJ, Green DJ. Exercise protects the cardiovascular system: effects beyond traditional risk factors. J Physiol. 2009;587(Pt 23):5551–8.PubMedCrossRef
10.
Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol. 2002;53(4 Pt 1):503–14.PubMed
11.
Deanfield JE, Halcox JP, Rabelink TJ. Endothelial function and dysfunction: testing and clinical relevance. Circulation. 2007;115(10):1285–95.PubMed
12.
Corretti MC, Anderson TJ, Benjamin EJ, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol. 2002;39(2):257–65.PubMedCrossRef
13.
Celermajer DS, Sorensen KE, Gooch VM, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet. 1992;340(8828):1111–5.PubMedCrossRef
14.
Harris RA, Nishiyama SK, Wray DW, et al. Ultrasound assessment of flow-mediated dilation. Hypertension. 2010;55(5):1075–85.PubMedCrossRef
15.
Thijssen DH, Black MA, Pyke KE, et al. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol. 2011;300(1):H2–12.PubMedCrossRef
16.
Shechter M, Issachar A, Marai I, et al. Long-term association of brachial artery flow-mediated vasodilation and cardiovascular events in middle-aged subjects with no apparent heart disease. Int J Cardiol. 2009;134(1):52–8.PubMedCrossRef
17.
Yeboah J, Folsom AR, Burke GL, et al. Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis. Circulation. 2009;120(6):502–9.PubMedCrossRef
18.
Kullo IJ, Malik AR, Bielak LF, et al. Brachial artery diameter and vasodilator response to nitroglycerine, but not flow-mediated dilatation, are associated with the presence and quantity of coronary artery calcium in asymptomatic adults. Clin Sci (Lond). 2007;112(3):175–82.CrossRef
19.
Akamatsu D, Sato A, Goto H, et al. Nitroglycerin-mediated vasodilatation of the brachial artery may predict long-term cardiovascular events irrespective of the presence of atherosclerotic disease. J Atheroscler Thromb. 2010;17(12):1266–74.PubMedCrossRef
20.
Kawano N, Emoto M, Mori K, et al. Association of endothelial and vascular smooth muscle dysfunction with cardiovascular risk factors, vascular complications, and subclinical carotid atherosclerosis in type 2 diabetic patients. J Atheroscler Thromb. 2012;19(3):276–84.PubMedCrossRef
21.
Bruno RM, Penno G, Daniele G, et al. Type 2 diabetes mellitus worsens arterial stiffness in hypertensive patients through endothelial dysfunction. Diabetologia. 2012;55(6):1847–55.PubMedCrossRef
22.
Tan KC, Chow WS, Ai VH, et al. Advanced glycation end products and endothelial dysfunction in type 2 diabetes. Diabetes Care. 2002;25(6):1055–9.PubMedCrossRef
23.
Hamdy O, Ledbury S, Mullooly C, et al. Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome. Diabetes Care. 2003;26(7):2119–25.PubMedCrossRef
24.
Barone Gibbs B, Dobrosielski DA, Bonekamp S, Stewart KJ, Clark JM. A randomized trial of exercise for blood pressure reduction in type 2 diabetes: effect on flow-mediated dilation and circulating biomarkers of endothelial function. Atherosclerosis. 2012;224(2):446–53. doi:10.​1016/​j.​atherosclerosis.​2012.​07.​035.
25.
Kwon HR, Min KW, Ahn HJ, et al. Effects of aerobic exercise vs. resistance training on endothelial function in women with type 2 diabetes mellitus. Diabetes Metab J. 2011;35(4):364–73.PubMedCrossRef
26.
Maiorana A, O’Driscoll G, Cheetham C, et al. The effect of combined aerobic and resistance exercise training on vascular function in type 2 diabetes. J Am Coll Cardiol. 2001;38(3):860–6.PubMedCrossRef
27.
Okada S, Hiuge A, Makino H, et al. Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010;17(8):828–33.PubMedCrossRef
28.
Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–12.PubMedCrossRef
29.
Ainsworth BE, Haskell WL, Herrmann SD, et al. 2011 compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc. 2011;43(8):1575–81.PubMedCrossRef
30.
Garber CE, Blissmer B, Deschenes MR, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–59.PubMedCrossRef
31.
Bhogal SK, Teasell RW, Foley NC, et al. The PEDro scale provides a more comprehensive measure of methodological quality than the Jadad scale in stroke rehabilitation literature. J Clin Epidemiol. 2005;58(7):668–73.PubMedCrossRef
32.
de Morton NA. The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother. 2009;55(2):129–33.PubMedCrossRef
33.
Maher CG, Sherrington C, Herbert RD, et al. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–21.PubMed
34.
35.
36.
Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.PubMedCrossRef
37.
Sixt S, Beer S, Bluher M, et al. Long- but not short-term multifactorial intervention with focus on exercise training improves coronary endothelial dysfunction in diabetes mellitus type 2 and coronary artery disease. Eur Heart J. 2010;31(1):112–9.PubMedCrossRef
38.
Wycherley TP, Brinkworth GD, Noakes M, et al. Effect of caloric restriction with and without exercise training on oxidative stress and endothelial function in obese subjects with type 2 diabetes. Diabetes Obes Metab. 2008;10(11):1062–73.PubMedCrossRef
39.
Green DJ, Maiorana AJ, Tschakovsky ME, et al. Relationship between changes in brachial artery flow-mediated dilation and basal release of nitric oxide in subjects with type 2 diabetes. Am J Physiol Heart Circ Physiol. 2006;291(3):H1193–9.PubMedCrossRef
40.
Green DJ, Walsh JH, Maiorana A, et al. Exercise-induced improvement in endothelial dysfunction is not mediated by changes in CV risk factors: pooled analysis of diverse patient populations. Am J Physiol Heart Circ Physiol. 2003;285(6):H2679–87.PubMed
41.
Middlebrooke AR, Elston LM, Macleod KM, et al. Six months of aerobic exercise does not improve microvascular function in type 2 diabetes mellitus. Diabetologia. 2006;49(10):2263–71.PubMedCrossRef
42.
Choi KM, Han KA, Ahn HJ, et al. Effects of exercise on sRAGE levels and cardiometabolic risk factors in patients with type 2 diabetes: a randomized controlled trial. J Clin Endocrinol Metab. 2012;97(10):3751–8.PubMedCrossRef
43.
Enderle MD, Benda N, Schmuelling RM, et al. Preserved endothelial function in IDDM patients, but not in NIDDM patients, compared with healthy subjects. Diabetes Care. 1998;21(2):271–7.PubMedCrossRef
44.
Ifrim S, Vasilescu R. Early detection of atherosclerosis in type 2 diabetic patients by endothelial dysfunction and intima-media thickness. Rom J Intern Med. 2004;42(2):343–54.PubMed
45.
Ihlemann N, Stokholm KH, Eskildsen PC. Impaired vascular reactivity is present despite normal levels of von Willebrand factor in patients with uncomplicated type 2 diabetes. Diabet Med. 2002;19(6):476–81.PubMedCrossRef
46.
Woodman RJ, Watts GF, Puddey IB, et al. Leukocyte count and vascular function in type 2 diabetic subjects with treated hypertension. Atherosclerosis. 2002;163(1):175–81.PubMedCrossRef
47.
Brooks BA, Franjic B, Ban CR, et al. Diastolic dysfunction and abnormalities of the microcirculation in type 2 diabetes. Diabetes Obes Metab. 2008;10(9):739–46.PubMedCrossRef
48.
Vehkavaara S, Yki-Jarvinen H. 3.5 years of insulin therapy with insulin glargine improves in vivo endothelial function in type 2 diabetes. Arterioscler Thromb Vasc Biol. 2004;24(2):325–30.PubMedCrossRef
49.
Inaba Y, Chen JA, Bergmann SR. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis. Int J Cardiovasc Imaging. 2010;26(6):631–40.PubMedCrossRef
50.
Tinken TM, Thijssen DH, Black MA, et al. Time course of change in vasodilator function and capacity in response to exercise training in humans. J Physiol. 2008;586(Pt 20):5003–12.PubMedCrossRef
51.
Tinken TM, Thijssen DH, Hopkins N, et al. Shear stress mediates endothelial adaptations to exercise training in humans. Hypertension. 2010;55(2):312–8.PubMedCrossRef
52.
da Silva CA, Ribeiro JP, Canto JC, et al. High-intensity aerobic training improves endothelium-dependent vasodilation in patients with metabolic syndrome and type 2 diabetes mellitus. Diabetes Res Clin Pract. 2012;95(2):237–45.PubMedCrossRef
53.
Miche E, Herrmann G, Nowak M, et al. Effect of an exercise training program on endothelial dysfunction in diabetic and non-diabetic patients with severe chronic heart failure. Clin Res Cardiol. 2006;95(Suppl 1):i117–24.PubMedCrossRef
54.
Thijssen DH, Dawson EA, Black MA, et al. Brachial artery blood flow responses to different modalities of lower limb exercise. Med Sci Sports Exerc. 2009;41(5):1072–9.PubMedCrossRef
55.
Green DJ, Bilsborough W, Naylor LH, et al. Comparison of forearm blood flow responses to incremental handgrip and cycle ergometer exercise: relative contribution of nitric oxide. J Physiol. 2005;562(Pt 2):617–28.PubMedCrossRef
56.
Ayer JG, Harmer JA, David C, et al. Severe obesity is associated with impaired arterial smooth muscle function in young adults. Obesity (Silver Spring). 2011;19(1):54–60.CrossRef
57.
Leeson P, Thorne S, Donald A, et al. Non-invasive measurement of endothelial function: effect on brachial artery dilatation of graded endothelial dependent and independent stimuli. Heart. 1997;78(1):22–7.PubMed
Metadata
Title
Effects of Exercise Training on Arterial Function in Type 2 Diabetes Mellitus
A Systematic Review and Meta-Analysis
Authors
David Montero
Guillaume Walther
Eric Benamo
Antonia Perez-Martin
Agnès Vinet
Publication date
01-11-2013
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 11/2013
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-013-0085-2

Other articles of this Issue 11/2013

Sports Medicine 11/2013 Go to the issue

Review Article

Prevention and Management of Non-Communicable Disease: The IOC Consensus Statement, Lausanne 2013

Current Opinion

Pacing and Awareness: Brain Regulation of Physical Activity

Review Article

How Sex Hormones Promote Skeletal Muscle Regeneration

Systematic Review

Effects of Exercise Training on Airway Hyperreactivity in Asthma: A Systematic Review and Meta-Analysis

Letter to the Editor

Kayaking Fatalities: Could More Appropriate Helmets Prevent Fatal Consequences?

Review Article

The Use of Carbohydrates During Exercise as an Ergogenic Aid