Effects of combined training with different intensities on vascular health in patients with type 2 diabetes: a 1-year randomized controlled trial

João P Magalhães, Xavier Melo, Inês R Correia, Rogério T Ribeiro, João Raposo, Hélder Dores, Manuel Bicho, Luís B Sardinha, João P Magalhães, Xavier Melo, Inês R Correia, Rogério T Ribeiro, João Raposo, Hélder Dores, Manuel Bicho, Luís B Sardinha

Abstract

Background: Exercise, when performed on a regular basis, is a well-accepted strategy to improve vascular function in patients with type 2 diabetes. However, the exercise intensity that yields maximal adaptations on structural and functional indices in patients with type 2 diabetes remains uncertain. Our objective was to analyze the impact of a 1-year randomized controlled trial of combined high-intensity interval training (HIIT) with resistance training (RT) vs. a combined moderate continuous training (MCT) with RT on structural and functional arterial indices in patients with type 2 diabetes.

Methods: Patients with type 2 diabetes (n = 80) were randomized into an exercise intervention with three groups: control, combined HIIT with RT and combined MCT with RT. The 1-year intervention had 3 weekly exercise sessions. High-resolution ultrasonography of the common carotid artery and central and peripheral applanation tonometry were used to assess the changes in structural and functional arterial indices. Generalized estimating equations were used to model the corresponding outcomes.

Results: After adjusting the models for sex, baseline moderate-to-vigorous physical activity, and mean arterial pressure changes, while using the intention-to-treat analysis, a significant interaction was observed on the carotid intima-media thickness (cIMT) for both the MCT (β = - 4.25, p < 0.01) and HIIT group (β = - 3.61, p < 0.01). However, only the HIIT observed favorable changes from baseline to 1-year on peripheral arterial stiffness indices such as carotid radial arterial pulse wave velocity (β = - 0.10, p = 0.044), carotid to distal posterior tibial artery pulse wave velocity (β = - 0.14, p < 0.01), and on the distensibility coefficient (β = - 0.00, p < 0.01). No effect was found for hemodynamic variables after the intervention.

Conclusions: Following a 1-year intervention in patients with type 2 diabetes, both the MCT and HIIT group reduced their cIMT, whereas only the HIIT group improved their peripheral arterial stiffness indices and distensibility coefficient. Taken together, HIIT may be a meaningful tool to improve long-term vascular complications in type 2 diabetes. Trial registration clinicaltrials.gov ID: NCT03144505.

Keywords: Arterial stiffness; Distensibility coefficient; High-intensity interval training; Intima-media thickness; Moderate continuous training; Pulse wave velocity.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Study flow chart
Fig. 2
Fig. 2
Changes in structural and hemodynamic variables using the per-protocol analysis. Dashed lines represent mean values for each intervention group

References

    1. Budoff MJ, Raggi P, Beller GA, Berman DS, Druz RS, Malik S, et al. Noninvasive cardiovascular risk assessment of the asymptomatic diabetic patient: the imaging council of the american college of cardiology. JACC Cardiovasc Imaging. 2016;9(2):176–192.
    1. Eringa EC, Serne EH, Meijer RI, Schalkwijk CG, Houben AJ, Stehouwer CD, et al. Endothelial dysfunction in (pre)diabetes: characteristics, causative mechanisms and pathogenic role in type 2 diabetes. Rev Endocr Metab disord. 2013;14(1):39–48.
    1. Fox CS, Coady S, Sorlie PD, D’Agostino RB, Pencina MJ, Vasan RS, et al. Increasing cardiovascular disease burden due to diabetes mellitus—the Framingham Heart Study. Circulation. 2007;115(12):1544–1550.
    1. Miyamoto M, Kotani K, Okada K, Ando A, Hasegawa H, Kanai H, et al. Arterial wall elasticity measured using the phased tracking method and atherosclerotic risk factors in patients with type 2 diabetes. J Atheroscler Thromb. 2013;20(8):678–687.
    1. Teoh WL, Price JF, Williamson RM, Payne RA, Van Look LAF, Reynolds RM, et al. Metabolic parameters associated with arterial stiffness in older adults with Type 2 diabetes: the Edinburgh Type 2 Diabetes Study. J Hypertens. 2013;31(5):1010–1017.
    1. Lorenz MW, Sitzer M, Markus HS, Bots ML, Rosvall M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis—response. Circulation. 2007;116(9):E318.
    1. Mitchell GF, Hwang SJ, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, et al. Arterial stiffness and cardiovascular events the framingham heart study. Circulation. 2010;121(4):505–511.
    1. Kotb NA, Gaber R, Salama M, Nagy HM, Elhendy A. Clinical and biochemical predictors of increased carotid intima-media thickness in overweight and obese adolescents with type 2 diabetes. Diabetes Vasc Dis Res. 2012;9(1):35–41.
    1. Kim SH, Lee SJ, Kang ES, Kang S, Hur KY, Lee HJ, et al. Effects of lifestyle modification on metabolic parameters and carotid intima-media thickness in patients with type 2 diabetes mellitus. Metabolism. 2006;55(8):1053–1059.
    1. Way KL, Keating SE, Baker MK, Chuter VH, Johnson NA. The effect of exercise on vascular function and stiffness in type 2 diabetes: a systematic review and meta-analysis. Curr Diabetes Rev. 2016;12(4):369–383.
    1. Colberg SR, Albright AL, Blissmer BJ, Braun B, Chasan-Taber L, Fernhall B, et al. 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(12):2282–2303.
    1. WHO . WHO global recommendations on physical activity for health. In: Organization WH, editor. WHO global recommendations on physical activity for health. WHO guidelines approved by the guidelines review committee. Geneva: World Health Organisation; 2010.
    1. Wormgoor SG, Dalleck LC, Zinn C, Harris NK. Effects of high-intensity interval training on people living with type 2 diabetes: a narrative review. Can J Diabetes. 2017;41(5):536–547.
    1. Batacan RB, Duncan MJ, Dalbo VJ, Tucker PS, Fenning AS. Effects of high-intensity interval training on cardiometabolic health: a systematic review and meta-analysis of intervention studies. Br J Sport Med. 2017;51(6):494–503.
    1. Magalhaes JP, Judice PB, Ribeiro R, Andrade R, Raposo J, Dores H, et al. Effectiveness of high intensity interval training combined with resistance training vs. continuous moderate intensity training combined with resistance training in patients with type 2 diabetes—1 year randomized controlled trial. Diabetes Obes Metab. 2018;1:1.
    1. Francois ME, Pistawka KJ, Halperin FA, Little JP. Cardiovascular benefits of combined interval training and post-exercise nutrition in type 2 diabetes. J Diabetes Complicat. 2018;32(2):226–233.
    1. Davies MJ, D’Alessio DA, Fradkin J, Kernan WN, Mathieu C, Mingrone G, et al. Management of hyperglycaemia in type 2 diabetes, 2018. A consensus report by the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetologia. 2018.
    1. Hove-Skovsgaard M, Gaardbo JC, Kolte L, Winding K, Seljeflot I, Svardal A, et al. HIV-infected persons with type 2 diabetes show evidence of endothelial dysfunction and increased inflammation. BMC Infect Dis. 2017;17(1):234.
    1. 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):1218–1227.
    1. Guimaraes GV, Ciolac EG, Carvalho VO, D’Avila VM, Bortolotto LA, Bocchi EA. Effects of continuous vs. interval exercise training on blood pressure and arterial stiffness in treated hypertension. Hypertens Res. 2010;33(6):627–632.
    1. Lohman TG, Roche AS, Martorell R. Anthropometric standardization reference manual. Champaign: Human Kinetics; 1988. p. 177.
    1. CDC. National health and nutrition examination survey (NHANES)—anthropometry procedures manual. . Accessed 26 July 2018.
    1. Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, et al. Recommendations for blood pressure measurement in humans and experimental animals: part 1: blood pressure measurement in humans: a statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Circulation. 2005;111(5):697–716.
    1. Hoeks AP, Willekes C, Boutouyrie P, Brands PJ, Willigers JM, Reneman RS. Automated detection of local artery wall thickness based on M-line signal processing. Ultrasound Med Biol. 1997;23(7):1017–1023.
    1. Van Bortel LM, Balkestein EJ, van der Heijden-Spek JJ, Vanmolkot FH, Staessen JA, Kragten JA, et al. Non-invasive assessment of local arterial pulse pressure: comparison of applanation tonometry and echo-tracking. J Hypertens. 2001;19(6):1037–1044.
    1. Troiano RP, Berrigan D, Dodd KW, Masse LC, Tilert T, McDowell M. Physical activity in the United States measured by accelerometer. Med Sci Sports Exerc. 2008;40(1):181–188.
    1. Intention to treat analysis and per protocol analysis: complementary information. Prescrire Int. 2012;21(133):304–6.
    1. Sutton-Tyrrell K, Newman A, Simonsick EM, Havlik R, Pahor M, Lakatta E, et al. Aortic stiffness is associated with visceral adiposity in older adults enrolled in the study of health, aging, and body composition. Hypertension. 2001;38(3):429–433.
    1. Ryden L, Standl E, Bartnik M, den Berghe G, Betteridge J, de Boer MJ, et al. Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: executive summary—The Task Force on Diabetes and Cardiovascular Diseases of the European Society of Cardiology (ESC) and of the European Association for the Study of Diabetes (EASD) Eur Heart J. 2007;28(1):88–136.
    1. Shin JY, Lee HR, Lee DC. Increased arterial stiffness in healthy subjects with high-normal glucose levels and in subjects with pre-diabetes. Cardiovasc Diabetol. 2011;10:30.
    1. Zhang MH, Bai YY, Ye P, Luo LM, Xiao WK, Wu HM, et al. Type 2 diabetes is associated with increased pulse wave velocity measured at different sites of the arterial system but not augmentation index in a chinese population. Clin Cardiol. 2011;34(10):622–627.
    1. Qiu S, Cai X, Yin H, Sun Z, Zugel M, Steinacker JM, et al. Exercise training and endothelial function in patients with type 2 diabetes: a meta-analysis. Cardiovasc Diabetol. 2018;17(1):64.
    1. Miele EM, Headley SAE. The effects of chronic aerobic exercise on cardiovascular risk factors in persons with diabetes mellitus. Curr DiabRep. 2017;17(10):97.
    1. Ramos JS, Dalleck LC, Tjonna AE, Beetham KS, Coombes JS. The impact of high-intensity interval training versus moderate-intensity continuous training on vascular function: a systematic review and meta-analysis. Sports Med. 2015;45(5):679–692.
    1. Lee JH, Lee R, Hwang MH, Hamilton MT, Park Y. The effects of exercise on vascular endothelial function in type 2 diabetes: a systematic review and meta-analysis. Diabetol Metab Syndr. 2018;10:15.
    1. Green DJ, Hopman MTE, Padilla J, Laughlin MH, Thijssen DHJ. Vascular adaptation to exercise in humans: role of hemodynamic stimuli. Physiol Rev. 2017;97(2):495–528.
    1. Goto C, Higashi Y, Kimura M, Noma K, Hara K, Nakagawa K, et al. Effect of different intensities of exercise on endothelium-dependent vasodilation in humans - Role of endothelium-dependent nitric oxide and oxidative stress. Circulation. 2003;108(5):530–535.
    1. Bergholm R, Makimattila S, Valkonen M, Liu ML, Lahdenpera S, Taskinen MR, et al. Intense physical training decreases circulating antioxidants and endothelium-dependent vasodilatation in vivo. Atherosclerosis. 1999;145(2):341–349.
    1. Amadid H, Johansen NB, Bjerregaard AL, Brage S, Faerch K, Lauritzen T, et al. The role of physical activity in the development of first cardiovascular disease event: a tree-structured survival analysis of the Danish ADDITION-PRO cohort. Cardiovasc Diabetol. 2018;17(1):126.
    1. Guerin AP, Blacher J, Pannier B, Marchais SJ, Safar ME, London GM. Impact of aortic stiffness attenuation on survival of patients in end-stage renal failure. Circulation. 2001;103(7):987–992.
    1. Ashor AW, Lara J, Siervo M, Celis-Morales C, Mathers JC. Effects of exercise modalities on arterial stiffness and wave reflection: a systematic review and meta-analysis of randomized controlled trials. PLoS ONE. 2014;9(10):e110034.
    1. Olver TD, Laughlin MH. Endurance, interval sprint, and resistance exercise training: impact on microvascular dysfunction in type 2 diabetes. Am J Physiol Heart Circ Physiol. 2016;310(3):H337–H350.
    1. Wisloff U, Stoylen A, Loennechen JP, Bruvold M, Rognmo O, Haram PM, et al. Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation. 2007;115(24):3086–3094.
    1. Tjonna AE, Lee SJ, Rognmo O, Stolen TO, Bye A, Haram PM, et al. Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome—a pilot study. Circulation. 2008;118(4):346–354.
    1. Valle I, Alvarez-Barrientos A, Arza E, Lamas S, Monsalve M. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc Res. 2005;66(3):562–573.
    1. Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, et al. Aging and endothelial function in normotensive subjects and patients with essential-hypertension. Circulation. 1995;91(7):1981–1987.
    1. Laurent S, Caviezel B, Beck L, Girerd X, Billaud E, Boutouyrie P, et al. Carotid-artery distensibility and distending pressure in hypertensive humans. Hypertension. 1994;23(6):878–883.
    1. Bernard S, Serusclat A, Targe F, Charriere S, Roth O, Beaune J, et al. Incremental predictive value of carotid ultrasonography in the assessment of coronary risk in a cohort of asymptomatic type 2 diabetic subjects. Diabetes Care. 2005;28(5):1158–1162.
    1. Sibal L, Agarwal SC, Home PD. Carotid intima-media thickness as a surrogate marker of cardiovascular disease in diabetes. Diabetes Metab Syndr Obes Targets Ther. 2011;4:23–34.
    1. Byrkjeland R, Stensaeth KH, Anderssen S, Njerve IU, Arnesen H, Seljeflot I, et al. Effects of exercise training on carotid intima-media thickness in patients with type 2 diabetes and coronary artery disease. Influence of carotid plaques. Cardiovasc Diabetol. 2016;15:13.
    1. Tuttle JL, Nachreiner RD, Bhuller AS, Condict KW, Connors BA, Herring BP, et al. Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression. Am J Physiol Heart Circ Physiol. 2001;281(3):H1380–H1389.
    1. O’Keeffe LM, Muir G, Piterina AV, McGloughlin T. Vascular cell adhesion molecule-1 expression in endothelial cells exposed to physiological coronary wall shear stresses. J Biomech Eng. 2009;131(8):081003.
    1. Grace A, Chan E, Giallauria F, Graham PL, Smart NA. Clinical outcomes and glycaemic responses to different aerobic exercise training intensities in type II diabetes: a systematic review and meta-analysis. Cardiovasc Diabetol. 2017;16(1):37.
    1. Buscemi S, Canino B, Batsis JA, Buscemi C, Calandrino V, Mattina A, et al. Relationships between maximal oxygen uptake and endothelial function in healthy male adults: a preliminary study. Acta Diabetol. 2013;50(2):135–141.
    1. Boreham CA, Ferreira I, Twisk JW, Gallagher AM, Savage MJ, Murray LJ. Cardiorespiratory fitness, physical activity, and arterial stiffness: the Northern Ireland Young Hearts Project. Hypertension. 2004;44(5):721–726.
    1. Church TS, LaMonte MJ, Barlow CE, Blair SN. Cardiorespiratory fitness and body mass index as predictors of cardiovascular disease mortality among men with diabetes. Arch Intern Med. 2005;165(18):2114–2120.
    1. Katzmarzyk PT, Church TS, Janssen I, Ross R, Blair SN. Metabolic syndrome, obesity, and mortality: impact of cardiorespiratory fitness. Diabetes Care. 2005;28(2):391–397.
    1. Pandey A, Swift DL, McGuire DK, Ayers CR, Neeland IJ, Blair SN, et al. Metabolic effects of exercise training among fitness-nonresponsive patients with type 2 diabetes: the HART-D study. Diabetes Care. 2015;38(8):1494–1501.

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