Abstract
Background
Resistance training (RT) is effective for glycemic control in type 2 diabetes mellitus (T2DM) patients. However, the characteristics of an RT program that will maximize its effect and those of patients that will especially benefit from RT are unknown.
Objective
The objectives of this systematic review were to identify via a comprehensive meta-analysis the characteristics of an RT program for patients with T2DM that might increase the patients’ improvement in glycemic control and the characteristics of patients that will benefit from RT.
Data Sources
Electronic-based literature searches of MEDLINE and EMBASE entries from 1 January 1966 to 25 August 2014 were conducted to identify clinical trials examining the effect of RT on glycemic control among patients with T2DM. Study keywords were text words and thesaurus terms related to RT and T2DM.
Study Selection
Studies were included if they (1) were clinical trials consisting of two groups with and without RT exercise intervention; (2) had an intervention period of at least 5 weeks; (3) clarified that all patients had T2DM; and (4) reported or made it possible to estimate the effect size [i.e., change in glycosylated hemoglobin (HbA1c) in the RT group minus that in the control group] and its corresponding standard error.
Study Appraisal and Synthesis Methods
The effect size in each study was pooled with a random-effects model. Analyses were stratified by several key characteristics of the patients and RT exercise programs; meta-regression analysis was then used to detect a difference in the effect size among strata within each factor. Linear regression analyses were added by entering each of the following profiles: patients’ baseline characteristics [mean baseline age, body mass index (BMI), and HbA1c levels] and exercise characteristics (total sets per week, total sets per bout of exercise, frequency, and intensity).
Results
There were 23 eligible studies comprising 954 patients with T2DM. The pooled effect size (95 % confidence interval) was −0.34 % (−0.53 to −0.16). A program with multiple sets (≥21 vs. <21) per one RT bout was associated with a large effect size (P = 0.03); however, the linear correlation between the number of sets and effect size was not significant (P = 0.56). A larger effect size was observed in studies with participants with diabetes of a relatively short duration (<6 vs. ≥6 years; P = 0.04) or a high baseline HbA1c [≥7.5 % (58 mmol/mol) vs. <7.5 %; P = 0.01] while a smaller effect size was observed in studies with a particularly high mean baseline BMI value (≥32 vs. <32 kg/m2; P = 0.03). Linear regression analyses predicted that each increment of 1 % in the baseline HbA1c would enlarge the effect size by 0.036 %, while each increment of 1 kg/m2 in the baseline BMI decreased it by 0.070 % in the range between 22.3 and 38.8 kg/m2.
Conclusion
In terms of glycemic control, RT could be recommended in the early stage of T2DM, especially for patients with relatively poor glycemic control. More benefit would be elicited in less obese patients within a limited range of the BMI. A substantial amount of exercise might be required to stimulate post-exercise glucose uptake, although the dose-dependency was not specifically clarified.
Similar content being viewed by others
References
Yang Z, Scott CA, Mao C, Tang J, Farmer AJ. Resistance exercise versus aerobic exercise for type 2 diabetes: a systematic review and meta-analysis. Sports Med. 2014;44(4):487–99. doi:10.1007/s40279-013-0128-8.
Wood RJ, O’Neill EC. Resistance training in type II diabetes mellitus: impact on areas of metabolic dysfunction in skeletal muscle and potential impact on bone. J Nutr Metab. 2012;2012:268197. doi:10.1155/2012/268197.
Irvine C, Taylor NF. Progressive resistance exercise improves glycaemic control in people with type 2 diabetes mellitus: a systematic review. Aust J Physiother. 2009;55(4):237–46.
Umpierre D, Ribeiro PA, Schaan BD, Ribeiro JP. Volume of supervised exercise training impacts glycaemic control in patients with type 2 diabetes: a systematic review with meta-regression analysis. Diabetologia. 2013;56(2):242–51. doi:10.1007/s00125-012-2774-z.
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ (Clin Res Ed). 2009;339:b2700. doi:10.1136/bmj.b2700.
Mortensen HB, Volund A. Application of a biokinetic model for prediction and assessment of glycated haemoglobins in diabetic patients. Scand J Clin Lab Invest. 1988;48(6):595–602.
Brzycki M. Strength testing—predicting a one-rep max from reps-to-fatigue. JOPERD. 1993;64(1):88–90.
Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR, Bemben MG. Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitn. 1995;35(2):108–13.
do Nascimento MA, Cyrino ES, Nakamura FY, Romanzini M, Pianca HJC, Queiróga MR. Validation of the Brzycki equation for estimation of the 1-RM in the bench press. Rev Braz Med Esporte. 2007;13:47–50.
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.
Follmann D, Elliott P, Suh I, Cutler J. Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol. 1992;45(7):769–73.
Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. doi:10.1002/sim.1186.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clin Res Ed). 1997;315(7109):629–34.
Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–63.
Jorge ML, de Oliveira VN, Resende NM, Paraiso LF, Calixto A, Diniz AL, et al. The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocytokines, and muscle insulin signaling in patients with type 2 diabetes mellitus. Metabolism. 2011;60(9):1244–52. doi:10.1016/j.metabol.2011.01.006.
de Oliveira VN, Bessa A, Jorge ML, Oliveira RJ, de Mello MT, De Agostini GG, et al. The effect of different training programs on antioxidant status, oxidative stress, and metabolic control in type 2 diabetes. Appl Physiol Nutr Metab. 2012;37(2):334–44. doi:10.1139/h2012-004.
Dunstan DW, Daly RM, Owen N, Jolley D, Vulikh E, Shaw J, et al. Home-based resistance training is not sufficient to maintain improved glycemic control following supervised training in older individuals with type 2 diabetes. Diabetes Care. 2005;28(1):3–9.
Dunstan DW, Daly RM, Owen N, Jolley D, De Courten M, Shaw J, et al. High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care. 2002;25(10):1729–36.
Hameed UA, Manzar D, Raza S, Shareef MY, Hussain ME. Resistance training leads to clinically meaningful improvements in control of glycemia and muscular strength in untrained middle-aged patients with type 2 diabetes mellitus. N Am J Med Sci. 2012;4(8):336–43. doi:10.4103/1947-2714.99507.
Mavros Y, Kay S, Anderberg KA, Baker MK, Wang Y, Zhao R, et al. Changes in insulin resistance and HbA1c are related to exercise-mediated changes in body composition in older adults with type 2 diabetes: interim outcomes from the GREAT2DO trial. Diabetes Care. 2013;36(8):2372–9. doi:10.2337/dc12-2196.
Kadoglou NP, Fotiadis G, Kapelouzou A, Kostakis A, Liapis CD, Vrabas IS. The differential anti-inflammatory effects of exercise modalities and their association with early carotid atherosclerosis progression in patients with type 2 diabetes. Diabet Med. 2012;30(2):e41–50. doi:10.1111/dme.12055.
Kadoglou NP, Fotiadis G, Athanasiadou Z, Vitta I, Lampropoulos S, Vrabas IS. The effects of resistance training on ApoB/ApoA-I ratio, Lp(a) and inflammatory markers in patients with type 2 diabetes. Endocrine. 2012;42(3):561–9. doi:10.1007/s12020-012-9650-y.
Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, et al. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA. 2010;304(20):2253–62. doi:10.1001/jama.2010.1710.
Plotnikoff RC, Eves N, Jung M, Sigal RJ, Padwal R, Karunamuni N. Multicomponent, home-based resistance training for obese adults with type 2 diabetes: a randomized controlled trial. Int J Obes (Lond). 2010;34(12):1733–41. doi:10.1038/ijo.2010.109.
Hazley L, Ingle L, Tsakirides C, Carroll S, Nagi D. Impact of a short-term, moderate intensity, lower volume circuit resistance training programme on metabolic risk factors in overweight/obese type 2 diabetics. Res Sports Med. 2010;18(4):251–62. doi:10.1080/15438627.2010.510049.
Wycherley TP, Noakes M, Clifton PM, Cleanthous X, Keogh JB, Brinkworth GD. A high-protein diet with resistance exercise training improves weight loss and body composition in overweight and obese patients with type 2 diabetes. Diabetes Care. 2010;33(5):969–76. doi:10.2337/dc09-1974.
Ku YH, Han KA, Ahn H, Kwon H, Koo BK, Kim HC, et al. Resistance exercise did not alter intramuscular adipose tissue but reduced retinol-binding protein-4 concentration in individuals with type 2 diabetes mellitus. J Int Med Res. 2010;38(3):782–91.
Arora E, Shenoy S, Sandhu JS. Effects of resistance training on metabolic profile of adults with type 2 diabetes. Indian J Med Res. 2009;129(5):515–9.
Shenoy S, Arora E, Jaspal S. Effects of progressive resistance training and aerobic exercise on type 2 diabetics in Indian population. Int J Diabetes Metab. 2009;17(1):27–30.
Sigal RJ, Kenny GP, Boule NG, Wells GA, Prud’homme D, Fortier M, 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(6):357–69.
Cheung NW, Cinnadaio N, Russo M, Marek S. A pilot randomised controlled trial of resistance exercise bands in the management of sedentary subjects with type 2 diabetes. Diabetes Res Clin Pract. 2009;83(3):e68–71. doi:10.1016/j.diabres.2008.12.009.
Baum K, Votteler T, Schiab J. Efficiency of vibration exercise for glycemic control in type 2 diabetes patients. Int J Med Sci. 2007;4(3):159–63.
Baldi JC, Snowling N. Resistance training improves glycaemic control in obese type 2 diabetic men. Int J Sports Med. 2003;24(6):419–23. doi:10.1055/s-2003-41173.
Castaneda C, Layne JE, Munoz-Orians L, Gordon PL, Walsmith J, Foldvari M, et al. A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care. 2002;25(12):2335–41.
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(1):53–61.
Ishii T, Yamakita T, Sato T, Tanaka S, Fujii S. Resistance training improves insulin sensitivity in NIDDM subjects without altering maximal oxygen uptake. Diabetes Care. 1998;21(8):1353–5.
Honkola A, Forsen T, Eriksson J. Resistance training improves the metabolic profile in individuals with type 2 diabetes. Acta Diabetol. 1997;34(4):245–8.
Yavari A, Najafipoor F, Aliasgharzadeh A, Niafar M, Mobasseri M. Effect of aerobic exercise, resistance training or combined training on glycaemic control and cardiovascular risk factors in patients with type 2 diabetes. Biol Sport. 2012;29:135–43.
Kwon HR, Min KW, Ahn HJ, Seok HG, Lee JH, Park GS, 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. doi:10.4093/dmj.2011.35.4.364.
Berkman ND, Lohr KN, Ansari M, McDonagh M, Balk E, Whitlock E, et al. AHRQ methods for effective health care grading the strength of a body of evidence when assessing health care interventions for the effective health care program of the Agency for Healthcare Research and Quality: an update. Methods guide for effectiveness and comparative effectiveness reviews. Rockville: Agency for Healthcare Research and Quality (US); 2008.
Saenz A, Fernandez-Esteban I, Mataix A, Ausejo M, Roque M, Moher D. Metformin monotherapy for type 2 diabetes mellitus. Cochrane Database Syst Rev. 2005(3):Cd002966. doi:10.1002/14651858.CD002966.pub3.
van de Laar FA, Lucassen PL, Akkermans RP, van de Lisdonk EH, Rutten GE, van Weel C. Alpha-glucosidase inhibitors for patients with type 2 diabetes: results from a Cochrane systematic review and meta-analysis. Diabetes Care. 2005;28(1):154–63.
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. Diabetes Care. 2010;33(12):e147–67. doi:10.2337/dc10-9990.
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(2):294–305.
Foran PG, Fletcher LM, Oatey PB, Mohammed N, Dolly JO, Tavare JM. Protein kinase B stimulates the translocation of GLUT4 but not GLUT1 or transferrin receptors in 3T3-L1 adipocytes by a pathway involving SNAP-23, synaptobrevin-2, and/or cellubrevin. J Biol Chem. 1999;274(40):28087–95.
Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W, Berria R, Belfort R, Kashyap S, et al. Exercise training increases glycogen synthase activity and GLUT4 expression but not insulin signaling in overweight nondiabetic and type 2 diabetic subjects. Metabolism. 2004;53(9):1233–42.
Niskanen L, Karjalainen J, Siitonen O, Uusitupa M. Metabolic evolution of type 2 diabetes: a 10-year follow-up from the time of diagnosis. J Intern Med. 1994;236(3):263–70.
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 (Clin Res Ed). 2000;321(7258):405–12.
Acknowledgments
All authors thank Ms Mami Haga and Ms Natsuko Tada of the University of Niigata for their excellent secretarial work.
All study members contributed substantially to the following: (1) conception and design of the study or acquisition of data, or analysis and interpretation of data; (2) drafting the article or reviewing it; and (3) providing final approval of the version to be published. In addition, all of the authors certify that they have participated sufficiently in the work to believe in its overall validity and to take public responsibility for appropriate portions of its context. HI, SK, and HS played leading roles in the conception and design of the study, all processes of the study methods, and drafting all sections of the manuscript. KF and ASH selected studies that met the inclusion criteria and acquired the full-paper version of studies that underwent further review. RH and YY gave various opinions in interpretation of the study results and helped to draft the manuscript. NO and HS designed the study’s analytic strategy and provided technical support in carrying out the statistical analyses. OH supervised the study and revised the draft critically for important intellectual content. HI, SK, and HS had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Dr Sone and Dr Kodama are recipients of a Grant-in-Aid for Scientific Research (#20300227 and #26870208, respectively), both from the Japan Society for the Promotion of Science (JSPS). The sponsors had no influence over the design or conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Hajime Ishiguro, Satoru Kodama, Chika Horikawa, Kazuya Fujihara, Ayumi Sugawara Hirose, Reiko Hirasawa, Yoko Yachi, Nobumasa Ohara, Hitoshi Shimano, Osamu Hanyu, and Hirohito Sone declare that they have no conflict of interest.
Ethical standards
This manuscript does not include clinical studies or patient data.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ishiguro, H., Kodama, S., Horikawa, C. et al. In Search of the Ideal Resistance Training Program to Improve Glycemic Control and its Indication for Patients with Type 2 Diabetes Mellitus: A Systematic Review and Meta-Analysis. Sports Med 46, 67–77 (2016). https://doi.org/10.1007/s40279-015-0379-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40279-015-0379-7