Resistance Training for Glycemic Control, Muscular Strength, and Lean Body Mass in Old Type 2 Diabetic Patients: A Meta-Analysis

JungHoon Lee, DoHoun Kim, ChangKeun Kim, JungHoon Lee, DoHoun Kim, ChangKeun Kim

Abstract

Introduction: Type 2 diabetes (T2D) in elderly patients is associated with accelerated loss of skeletal muscle mass and strength. However, there are few meta-analysis reviews which investigate the effects of resistance training (RT) on glycemic control and skeletal muscle in the patients.

Methods: Three electronic databases were searched (from the earliest date available to November 2016). Studies were included according to the inclusion criteria: T2D patients at least 60 years old, fasting plasma glucose of at least 7.0, and at least 8 weeks of RT.

Results: Fifteen cohorts of eight studies (360 patients, average age 66 years) met the inclusion criteria. RT groups lowered glycosylated hemoglobin (HbA1c) (mean ES = -0.37, 95% CI = -0.55 to -0.20, P < 0.01) but did not result in a significant effect on lean body mass (LBM) (mean ES = 0.08, 95% CI = -0.15 to 0.30, P = 0.50). Homogeneity was shown between studies regarding HbA1c and LBM (Q = 15.70, df = 9, P = 0.07 and Q = 0.12, df = 4, P = 0.998, respectively). High-intensity subgroups showed a slight tendency to improve (rather than duration, frequency, and weekly volume) and to decrease HbA1c levels more than low-intensity subgroups (P = 0.37). RT increased muscular strength (mean ES = 1.05, 95% CI = 0.26-1.84, P = 0.01). No training components explained the heterogeneity between studies with changes in muscle strength.

Conclusion: RT improves glycemic control and muscle strength in elderly patients with T2D. RT with high intensity can be a strategy to treat patients with T2D and sarcopenia associated with aging.

Keywords: Aging; Glycosylated hemoglobin; Insulin sensitivity; Sarcopenia.

Figures

Fig. 1
Fig. 1
Forest plot of effect sizes and 95% confidence Intervals for all ten cohorts (8 studies) representing glycated hemoglobin, based on the fixed effects meta-analysis results. CON control group
Fig. 2
Fig. 2
Forest plot of effect sizes and 95% confidence intervals for all 4 cohorts (4 studies) representing muscular strength, based on the random effects meta-analysis results
Fig. 3
Fig. 3
Forest plot of effect sizes and 95% confidence intervals for all five cohorts (4 studies) representing lean body mass, based on the fixed effects meta-analysis results. CON control group

References

    1. American Diabetes Association. National Diabetes Statistics Report Estimates of diabetes and its burden in the epidemiologic estimation methods. Natl Diabetes Stat Rep. 2014;2014:2009–2012.
    1. Coon PJ, Rogus EM, Drinkwater D, Muller DC, Goldberg AP. Role of body fat distribution in the decline in insulin sensitivity and glucose tolerance with age. J Clin Endocrinol Metab. 1992;75(4):1125–1132.
    1. Gregg EW, Engelgau MM, Narayan V. Complications of diabetes in elderly people. BMJ. 2002;325:916–7.
    1. Park SW, Goodpaster BH, Strotmeyer ES, et al. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes. 2006;55(6):1813–1818. doi: 10.2337/db05-1183.
    1. Schwartz AV, Hillier TA, Sellmeyer DE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care. 2002;25(10):1749–1754. doi: 10.2337/diacare.25.10.1749.
    1. Fielding RA, Vellas B, Evans WJ, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–256. doi: 10.1016/j.jamda.2011.01.003.
    1. Park SW, Goodpaster BH, Strotmeyer ES, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care. 2007;30(6):1507–1512. doi: 10.2337/dc06-2537.
    1. DeFronzo R. Pathogenesis of type 2 diabetes mellitus. Med Clin N Am. 2004;88(4):787–835. doi: 10.1016/j.mcna.2004.04.013.
    1. Borghouts LB, Keizer H. Exercise and insulin sensitivity: a review. Int J Sports Med. 2000;21(1):1–12. doi: 10.1055/s-2000-8847.
    1. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JFP, 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. doi: 10.2337/diabetes.53.2.294.
    1. Mourier A, Gautier JF, De Kerviler E, et al. 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(3):385–391. doi: 10.2337/diacare.20.3.385.
    1. Venables MC, Jeukendrup AE. Aerobic training and obesity: effect on substrate metabolism and insulin sensitivity. Med Sci Sports Exerc. 2008;40(3):495–502. doi: 10.1249/MSS.0b013e31815f256f.
    1. Ibañez J, Izquierdo M, Argüelles I, et al. Twice-weekly progressive resistance training decreases abdominal fat and improves insulin sensitivity in older men with type 2 diabetes. Diabetes Care. 2005;28(3):662–667. doi: 10.2337/diacare.28.3.662.
    1. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol. 2006;576(Pt 2):613–624. doi: 10.1113/jphysiol.2006.113175.
    1. Castaneda C, Layne JE, Munoz-Orians L, 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):2335–2341. doi: 10.2337/diacare.25.12.2335.
    1. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh M, et al. American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc. 2009;41(7):1510–1530. doi: 10.1249/MSS.0b013e3181a0c95c.
    1. Cauza E, Hanusch-Enserer U, Strasser B, et al. The relative benefits of endurance and strength training on the metabolic factors and muscle function of people with type 2 diabetes mellitus. Arch Phys Med Rehabil. 2005;86(8):1527–1533. doi: 10.1016/j.apmr.2005.01.007.
    1. 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):1353–1355. doi: 10.2337/diacare.21.8.1353.
    1. Cauza E, Strehblow C, Metz-Schimmerl S, et al. Effects of progressive strength training on muscle mass in type 2 diabetes mellitus patients determined by computed tomography. Wien Med Wochenschr. 2009;159(5–6):141–147. doi: 10.1007/s10354-009-0641-4.
    1. Umpierre D, Ribeiro PB, 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;56:242–251. doi: 10.1007/s00125-012-2774-z.
    1. 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):487–499. doi: 10.1007/s40279-013-0128-8.
    1. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009;151:W-65–94. doi: 10.7326/0003-4819-151-4-200908180-00136.
    1. Cohen ND, Dunstan DW, Robinson C, Vulikh E, Zimmet PZ, Shaw JE. Improved endothelial function following a 14-month resistance exercise training program in adults with type 2 diabetes. Diabetes Res Clin Pract. 2008;79(3):405–411. doi: 10.1016/j.diabres.2007.09.020.
    1. Srinivas-Shankar U, Roberts SA, Connolly MJ, et al. Effects of testosterone on muscle strength, physical function, body composition, and quality of life in intermediate-frail and frail elderly men: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab. 2010;95(2):639–650. doi: 10.1210/jc.2009-1251.
    1. Cochran WG. Some methods for strengthening the common χ 2 tests. Biometrics. 1954;10(4):417–451. doi: 10.2307/3001616.
    1. Cohen J. Statistical power analysis for the behavioral sciences (rev. ed.). Hillsdale: Lawrence Erlbaum Associates; 1988.
    1. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. doi: 10.1136/bmj.327.7414.557.
    1. Dunstan DW, Daly RM, Owen N, et al. High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care. 2002;25:1729–1736. doi: 10.2337/diacare.25.10.1729.
    1. Honkola A, Forsén T, Eriksson J. Resistance training improves the metabolic profile in individuals with type 2 diabetes. Acta Diabetol. 1997;34:245–248. doi: 10.1007/s005920050082.
    1. Baldi JC, Snowling N. Resistance training improves glycaemic control in obese type 2 diabetic men. Int J Sports Med. 2003;24(6):419–423. doi: 10.1055/s-2003-41173.
    1. de Lade CG, Marins JC, Lima LM, et al. Effects of different exercise programs and minimal detectable changes in hemoglobin A1c in patients with type 2 diabetes. Diabetol Metab Syndr. 2016;8(13):1–9.
    1. Fenicchia LM, Kanaley JA, Azevedo JL, et al. Influence of resistance exercise training on glucose control in women with type 2 diabetes. Metabolism. 2004;55(3):284–289. doi: 10.1016/j.metabol.2003.10.007.
    1. Cauza E, Hanusch-Enserer U, Strasser B, et al. The metabolic effects of long term exercise in type 2 diabetes patients. Wien Med Wochenschr. 2006;156:515–519. doi: 10.1007/s10354-006-0337-y.
    1. Dunstan DW, Daly RM, Owen N, 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. doi: 10.2337/diacare.28.1.3.
    1. Simpson KA, Mavros Y, Kay S, et al. Graded resistance exercise and type 2 diabetes in older adults (the GREAT2DO study): methods and baseline cohort characteristics of a randomized controlled trial. Trials. 2015;16:512. doi: 10.1186/s13063-015-1037-y.
    1. Geirsdottir OG, Arnarson A, Briem K, Ramel A, Jonsson PV, Thorsdottir I. Effect of 12-week resistance exercise program on body composition, muscle strength, physical function, and glucose metabolism in healthy, insulin-resistant, and diabetic elderly Icelanders. J Gerontol A Biol Sci Med Sci. 2012;67(11):1259–1265. doi: 10.1093/gerona/gls096.
    1. Daly RM, Miller EG, Dunstan DW, et al. The effects of progressive resistance training combined with a whey-protein drink and vitamin D supplementation on glycaemic control, body composition and cardiometabolic risk factors in older adults with type 2 diabetes: study protocol for a randomized controlled trial. Trials. 2014;15:431. doi: 10.1186/1745-6215-15-431.
    1. Park SP, Lee IH. Effects on training and detraining on physical function, control of diabetes and anthropometrics in type 2 diabetes; a randomized controlled trial. Physiother Theory Pract. 2015;31(2):83–88. doi: 10.3109/09593985.2014.958265.
    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(3):495–501.
    1. Gordon BA, Bird SR, MacIsaac RJ, Benson AC. Does a single bout of resistance or aerobic exercise after insulin dose reduction modulate glycaemic control in type 2 diabetes? A randomised cross-over trial. J Sci Med Sport. 2016;19(10):795–799. doi: 10.1016/j.jsams.2016.01.004.
    1. Heden TD, Winn NC, Mari A, et al. Postdinner resistance exercise improves postprandial risk factors more effectively than predinner resistance exercise in patients with type 2 diabetes. J Appl Physiol. 2015;118(5):624–634. doi: 10.1152/japplphysiol.00917.2014.
    1. Mavros Y, Kay S, Anderberg KA, 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):2372–2379. doi: 10.2337/dc12-2196.
    1. Brooks N, Layne JE, Gordon PL, Roubenoff R, Nelson ME, Castaneda-Sceppa C. Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes. Int J Med Sci. 2006;4(1):19–27.
    1. 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):561–569. doi: 10.1007/s12020-012-9650-y.
    1. Church TS, Blair SN, Cocreham S, et al. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA. 2010;304:2253–2262. doi: 10.1001/jama.2010.1710.
    1. Sigal RJ, Kenny GP, Boulé NG, et al. Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Ann Intern Med. 2007;147:357–369. doi: 10.7326/0003-4819-147-6-200709180-00005.
    1. Umpierre D, Ribeiro PA, Kramer CK, et al. 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. doi: 10.1001/jama.2011.576.
    1. Gordon BA, Benson AC, Bird SR, Fraser SF. Resistance training improves metabolic health in type 2 diabetes: a systematic review. Diabetes Res Clin Pract. 2009;83(2):157–175. doi: 10.1016/j.diabres.2008.11.024.
    1. 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):237–246. doi: 10.1016/S0004-9514(09)70003-0.
    1. Peterson MD, Rhea MR, Sen A, Gordon PM. Resistance exercise for muscular strength in older adults: a meta-analysis. Ageing Res Rev. 2010;9(3):226–237. doi: 10.1016/j.arr.2010.03.004.
    1. Schuller G, Linke A. Diabetes, exercise. In: Goldstein B, Muller-Wieland D, editors. Type 2 diabetes: principles, practice. New York: Informa Healthcare; 2008.
    1. Miller WJ, Sherman WM, Ivy JL. Effect of strength training on glucose tolerance and post-glucose insulin response. Med Sci Sports Exerc. 1984;16:539–543.
    1. Evans WJ. Effects of exercise on body composition and functional capacity of the elderly. J Gerontol A Biol Sci Med Sci. 1995;50A:147–150. doi: 10.1093/gerona/50A.Special_Issue.147.
    1. Fielding RA. The role of progressive resistance training and nutrition in the preservation of lean body mass in the elderly. J Am Coll Nutr. 1995;14:587–594. doi: 10.1080/07315724.1995.10718547.
    1. Tarnopolsky MA. Mitochondrial DNA shifting in older adults following resistance exercise training. Appl Physiol Nutr Metab. 2009;34:348–354. doi: 10.1139/H09-022.
    1. Tzankoff SP, Norris AH. Effect of muscle mass decrease on agerelated BMR changes. J Appl Physiol. 1977;43:1001–1006.
    1. DeFronzo RA, Ferrannini E, Sato Y, Felig P, Wahren J. Synergistic interaction between exercise and insulin on peripheral glucose uptake. J Clin Investig. 1981;68:1468–1474. doi: 10.1172/JCI110399.
    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. doi: 10.2337/diacare.26.11.2977.
    1. Peterson MD, Sen A, Gordon PM. Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc. 2011;43(2):249–258. doi: 10.1249/MSS.0b013e3181eb6265.
    1. Zierath JR, Krook A, Wallberg-Henriksson H. Insulin action and insulin resistance in human skeletal muscle. Diabetologia. 2000;43:821–835. doi: 10.1007/s001250051457.
    1. Terada S, Yokozeki T, Kawanaka K, et al. Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle. J Appl Physiol. 2001;90(6):2019–2024.
    1. Tabata I, Suzuki Y, Fukunaga T, Yokozeki T, Akima H, Funato K. Resistance training affects GLUT-4 content in skeletal muscle of humans after 19 days of head-down bed rest. J Appl Physiol. 1999;86:909–914. doi: 10.1063/1.370822.
    1. Boden G, Shulman GI. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur J Clin Investig. 2002;32(Suppl 3):14–23. doi: 10.1046/j.1365-2362.32.s3.3.x.
    1. Hurley B, Hagberg JM. Optimizing health in older persons: aerobic or strength training? Exerc Sports Sci Rev. 1998;26:61–89. doi: 10.1249/00003677-199800260-00005.
    1. Taylor N, Dodd K, Shields N, Bruder A. Therapeutic exercise in physiotherapy practice is beneficial: a summary of systematic reviews 2002–2005. Aust J Physiother. 2007;53:7–16. doi: 10.1016/S0004-9514(07)70057-0.
    1. Snowling N, Hopkins W. Effects of different modes of exercise training on glucose control, risk factors for complications in type 2 diabetic patients: a meta-analysis. Diabetes Care. 2006;29:2518–2527. doi: 10.2337/dc06-1317.
    1. Poehlman ET, Dvorak RV, de Nino WF, Brochu M, Ades PA. Effects of resistance training and endurance training on insulin sensitivity in nonobese, young women: a randomized controlled trial. J Clin Endocrinol Metab. 2000;85:2463–2468.
    1. Plowman SA, Smith DL. Exercise physiology for health, fitness, and performance. 2. San Francisco: Benjamin Cummings; 2007.
    1. Dela F, Kjaer M. Resistance training, insulin sensitivity and muscle function in the elderly. Essays Biochem. 2006;42:75–88. doi: 10.1042/bse0420075.
    1. Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C. Physical activity/exercise and type 2 diabetes. Diabetes Care. 2004;27(10):2518–2539. doi: 10.2337/diacare.27.10.2518.
    1. Lindle RS, Metter EJ, Lynch NA, et al. Age and gender comparisons of muscle strength in 654 women and men aged 20–93 yr. J Appl Physiol. 1997;83(5):1581–1587.
    1. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147(8):755–763. doi: 10.1093/oxfordjournals.aje.a009520.
    1. Benson K, Hartz AJ. A comparison of observational studies and randomized, controlled trials. N Engl J Med. 2000;342:1878–1886. doi: 10.1056/NEJM200006223422506.
    1. Concato J, Shah N, Horwitz RI. Randomized, controlled trials, observational studies, and the hierarchy of research designs. N Engl J Med. 2000;342:1887–1892. doi: 10.1056/NEJM200006223422507.

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