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Exercise as Therapy for Diabetic and Prediabetic Neuropathy

  • Microvascular Complications—Neuropathy (R Pop-Busui, Section Editor)
  • Published:
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Abstract

Length-dependent neuropathy is the most common and costly complication of diabetes and frequently causes injury primarily to small-diameter cutaneous nociceptive fibers. Not only persistent hyperglycemia but also metabolic, endocrine, and inflammatory effects of obesity and dyslipidemia appear to play an important role in the development of diabetic neuropathy. Rational therapies aimed at direct control of glucose or its increased entry into the polyol pathway, oxidative or nitrosative stress, advanced glycation end product formation or signaling, microvascular ischemia, or adipocyte-derived toxicity have each failed in human trials of diabetic neuropathy. Aerobic exercise produces salutary effects in many of these pathogenic pathways simultaneously and, in both animal models and human trials, has been shown to improve symptoms of neuropathy and promote re-growth of cutaneous small-diameter fibers. Behavioral reduction in periods of seated, awake inactivity produces multimodal metabolic benefits similar to exercise, and the two strategies when combined may offer sustained benefit to peripheral nerve function.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Dyck PJ, Kratz JM, Karnes JL, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43:817–24.

    Article  CAS  PubMed  Google Scholar 

  2. Pop-Busui R, Lu J, Lopes N, et al. Prevalence of diabetic peripheral neuropathy and relation to glycemic control therapies at baseline in the BARI 2D cohort. J Peripher Nerv Syst. 2009;14:1–13.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Gordois A, Scuffham P, Shearer A, et al. The health care costs of diabetic peripheral neuropathy in the US. Diabetes Care. 2003;26:1790–5.

    Article  PubMed  Google Scholar 

  4. Guy RJ, Clark CA, Malcolm PN, et al. Evaluation of thermal and vibration sensation in diabetic neuropathy. Diabetologia. 1985;28:131–7.

    CAS  PubMed  Google Scholar 

  5. Thomas PK. Classification, differential diagnosis, and staging of diabetic peripheral neuropathy. Diabetes. 1997;46 Suppl 2:S54–7.

    Article  CAS  PubMed  Google Scholar 

  6. Kennedy JM, Zochodne DW. Experimental diabetic neuropathy with spontaneous recovery: is there irreparable damage? Diabetes. 2005;54:830–7.

    Article  CAS  PubMed  Google Scholar 

  7. Griffin JW, Thompson WJ. Biology and pathology of nonmyelinating Schwann cells. Glia. 2008;56:1518–31.

    Article  PubMed  Google Scholar 

  8. Smith AG, Howard JR, Kroll R, et al. The reliability of skin biopsy with measurement of intraepidermal nerve fiber density. J Neurol Sci. 2005;228:65–9.

    Article  PubMed  Google Scholar 

  9. Lauria G, Bakkers M, Schmitz C, et al. Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. J Peripher Nerv Syst. 2010;15:202–7.

    Article  PubMed  Google Scholar 

  10. Lauria G, Hsieh ST, Johansson O, et al. European Federation of Neurological Societies/Peripheral Nerve Society guideline on the use of skin biopsy in the diagnosis of small fiber neuropathy. Report of a joint task force of the European Federation of Neurological Societies and the Peripheral Nerve Society. Eur J Neurol. 2010;17:903–12. e944-909.

    Article  CAS  PubMed  Google Scholar 

  11. Dyck PJ, Norell JE, Tritschler H, et al. Challenges in design of multicenter trials: end points assessed longitudinally for change and monotonicity. Diabetes Care. 2007;30:2619–25.

    Article  PubMed  Google Scholar 

  12. Costa LA, Canani LH, Lisboa HR, et al. Aggregation of features of the metabolic syndrome is associated with increased prevalence of chronic complications in type 2 diabetes. Diabet Med. 2004;21:252–5.

    Article  CAS  PubMed  Google Scholar 

  13. Smith AG, Singleton JR. Obesity and hyperlipidemia are risk factors for early diabetic neuropathy. J Diabetes Complicat. 2013;27:436–42. This study demonstrates the epidemiological link between nonglycemic features of metabolic syndrome and diabetic neuropathy.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Tesfaye S, Stevens LK, Stephenson JM, et al. Prevalence of diabetic peripheral neuropathy and its relation to glycaemic control and potential risk factors: the EURODIAB IDDM Complications Study. Diabetologia. 1996;39:1377–84.

    Article  CAS  PubMed  Google Scholar 

  15. Gaede P, Vedel P, Larsen N, et al. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med. 2003;348:383–93.

    Article  PubMed  Google Scholar 

  16. Straub RH, Thum M, Hollerbach C, et al. Impact of obesity on neuropathic late complications in NIDDM. Diabetes Care. 1994;17:1290–4.

    Article  CAS  PubMed  Google Scholar 

  17. Tesfaye S, Selvarajah D. The Eurodiab Study: what has this taught us about diabetic peripheral neuropathy? Curr Diab Rep. 2009;9:432–4.

    Article  PubMed  Google Scholar 

  18. Callaghan B, Feldman E. The metabolic syndrome and neuropathy: therapeutic challenges and opportunities. Ann Neurol. 2013;74:397–403.

    Article  CAS  PubMed  Google Scholar 

  19. Obrosova IG. Diabetic painful and insensate neuropathy: pathogenesis and potential treatments. Neurotherapeutics. 2009;6:638–47.

    Article  CAS  PubMed  Google Scholar 

  20. Watcho P, Stavniichuk R, Ribnicky DM, et al. High-fat diet-induced neuropathy of prediabetes and obesity: effect of PMI-5011, an ethanolic extract of Artemisia dracunculus L. Mediat Inflamm. 2010;2010:268547.

    Article  Google Scholar 

  21. Davidson EP, Coppey LJ, Calcutt NA, et al. Diet-induced obesity in Sprague-Dawley rats causes microvascular and neural dysfunction. Diabetes Metab Res Rev. 2010;26:306–18.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Lupachyk S, Watcho P, Hasanova N, et al. Triglyceride, nonesterified fatty acids, and prediabetic neuropathy: role for oxidative-nitrosative stress. Free Radic Biol Med. 2012;52:1255–63.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Groover AL, Ryals JM, Guilford BL, et al. Exercise-mediated improvements in painful neuropathy associated with prediabetes in mice. Pain. 2013;154:2658–67. Behavioral therapy improves indices of neuropathic pain in a mouse model of prediabetic neuropathy.

    Article  PubMed  Google Scholar 

  24. Vincent AM, Hayes JM, McLean LL, et al. Dyslipidemia-induced neuropathy in mice: the role of oxLDL/LOX-1. Diabetes. 2009;58:2376–85.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Guilford BL, Ryals JM, Wright DE. Phenotypic changes in diabetic neuropathy induced by a high-fat diet in diabetic C57BL/6 mice. Exp Diabetes Res. 2011;2011:848307.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Singleton JR, Smith AG, Russell JW, et al. Microvascular complications of impaired glucose tolerance. Diabetes. 2003;52:2867–73.

    Article  CAS  PubMed  Google Scholar 

  27. Lewis GF, Carpentier A, Adeli K, et al. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev. 2002;23:201–29.

    Article  CAS  PubMed  Google Scholar 

  28. Oltman CL, Coppey LJ, Gellett JS, et al. Progression of vascular and neural dysfunction in sciatic nerves of Zucker diabetic fatty and Zucker rats. Am J Physiol Endocrinol Metab. 2005;289:E113–22.

    Article  CAS  PubMed  Google Scholar 

  29. Obrosova IG, Drel VR, Oltman CL, et al. Role of nitrosative stress in early neuropathy and vascular dysfunction in streptozotocin-diabetic rats. Am J Physiol Endocrinol Metab. 2007;293:E1645–55.

    Article  CAS  PubMed  Google Scholar 

  30. Esenabhalu VE, Schaeffer G, Graier WF. Free fatty acid overload attenuates Ca(2+) signaling and NO production in endothelial cells. Antioxid Redox Signal. 2003;5:147–53.

    Article  CAS  PubMed  Google Scholar 

  31. Pleiner J, Schaller G, Mittermayer F, et al. FFA-induced endothelial dysfunction can be corrected by vitamin C. J Clin Endocrinol Metab. 2002;87:2913–7.

    Article  CAS  PubMed  Google Scholar 

  32. Vincent AM, McLean LL, Backus C, et al. Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB J. 2005;19:638–40.

    CAS  PubMed  Google Scholar 

  33. Ahmed FN, Naqvi FN, Shafiq F. Lipid peroxidation and serum antioxidant enzymes in patients with type 2 diabetes mellitus. Ann N Y Acad Sci. 2006;1084:481–9.

    Article  CAS  PubMed  Google Scholar 

  34. Cruz NG, Sousa LP, Sousa MO, et al. The linkage between inflammation and type 2 diabetes mellitus. Diabetes Res Clin Pract. 2013;99:85–92.

    Article  CAS  PubMed  Google Scholar 

  35. Boyanovsky B, Karakashian A, King K, et al. Uptake and metabolism of low density lipoproteins with elevated ceramide content by human microvascular endothelial cells: implications for the regulation of apoptosis. J Biol Chem. 2003;278:26992–9.

    Article  CAS  PubMed  Google Scholar 

  36. Cheng HT, Dauch JR, Hayes JM, et al. Nerve growth factor/p38 signaling increases intraepidermal nerve fiber densities in painful neuropathy of type 2 diabetes. Neurobiol Dis. 2012;45:280–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Casanova-Molla J, Morales M, Planas-Rigol E, et al. Epidermal Langerhans cells in small fiber neuropathies. Pain. 2012;153:982–9.

    Article  PubMed  Google Scholar 

  38. Dauch JR, Bender DE, Luna-Wong LA, et al. Neurogenic factor-induced Langerhans cell activation in diabetic mice with mechanical allodynia. J Neuroinflammation. 2013;10:64.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Diabetes Control and Complications Trial Research Group. The effect of intensive diabetes therapy on the development and progression of neuropathy. Ann Intern Med. 1995;122:561.

    Article  Google Scholar 

  40. Ismail-Beigi F, Craven T, Banerji MA, et al. Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: an analysis of the ACCORD randomised trial. Lancet. 2010;376:419–30.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Callaghan BC, Little A, Feldman E, et al. Enhanced glycemic control for preventing and treating diabetic neuropathy. Cochrane Database Syst Rev. 2012; in press.

  42. Yagihashi S, Yamagishi SI, Wada Ri R, et al. Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain. 2001;124:2448–58.

    Article  CAS  PubMed  Google Scholar 

  43. Krentz AJ, Honigsberger L, Ellis SH, et al. A 12-month randomized controlled study of the aldose reductase inhibitor ponalrestat in patients with chronic symptomatic diabetic neuropathy. Diabet Med. 1992;9:463–8.

    Article  CAS  PubMed  Google Scholar 

  44. Coppey LJ, Davidson EP, Rinehart TW, et al. ACE inhibitor or angiotensin II receptor antagonist attenuates diabetic neuropathy in streptozotocin-induced diabetic rats. Diabetes. 2006;55:341–8.

    Article  CAS  PubMed  Google Scholar 

  45. Malik R, Williamson S, Abbott C. Effect of the angiotensin converting enzyme inhibitor trandoalapril on human diabetic neuropathy: a randomised controlled trial. Lancet. 1998;352:1978–81.

    Article  CAS  PubMed  Google Scholar 

  46. Ziegler D, Gries FA. Alpha-lipoic acid in the treatment of diabetic peripheral and cardiac autonomic neuropathy. Diabetes. 1997;46:S62–6.

    Article  CAS  PubMed  Google Scholar 

  47. Ziegler D, Nowak H, Kempler P, et al. Treatment of symptomatic diabetic polyneuropathy with the antioxidant alpha-lipoic acid: a meta-analysis. Diabet Med. 2004;21:114–21.

    Article  CAS  PubMed  Google Scholar 

  48. Cameron N, Tuck S, McCabe L, et al. Effects of the hydroxyl radical scavenger, dimethylthiorurea, on peripheral nerve tissue perfusion, conduction velocity and nociception in experimental diabetes. Diabetologia. 2001;44:1161–9.

    Article  CAS  PubMed  Google Scholar 

  49. Greene DA, Arezzo JC, Brown MB. Effect of aldose reductase inhibition on nerve conduction and morphometry in diabetic neuropathy. Zenarestat Study Group. Neurology. 1999;53:580–91.

    Article  CAS  PubMed  Google Scholar 

  50. Kihara M, Mitsui Y, Shioyama M, et al. Effect of zenarestat, an aldose reductase inhibitor, on endoneurial blood flow in experimental diabetic neuropathy of rat. Neurosci Lett. 2001;310:81–4.

    Article  CAS  PubMed  Google Scholar 

  51. Pfeifer MA, Schumer MP. Clinical trials of diabetic neuropathy: past present and future. Diabetes. 1995;44:1355–61.

    Article  CAS  PubMed  Google Scholar 

  52. Mojaddidi M, Quattrini C, Tavakoli M, et al. Recent developments in the assessment of efficacy in clinical trials of diabetic neuropathy. Curr Diab Rep. 2005;5:417–22.

    Article  PubMed  Google Scholar 

  53. Malik RA, Tesfaye S, Newrick PG, et al. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia. 2005;48:578–85.

    Article  CAS  PubMed  Google Scholar 

  54. Simone DA, Nolano M, Johnson T, et al. Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function. J Neurosci. 1998;18:8947–59.

    CAS  PubMed  Google Scholar 

  55. Polydefkis M, Hauer P, Sheth S, et al. The time course of epidermal nerve fibre regeneration: studies in normal controls and in people with diabetes, with and without neuropathy. Brain. 2004;127:1606–15.

    Article  PubMed  Google Scholar 

  56. Singleton JR, Marcus RL, Lessard MK, et al. Supervised exercise improves cutaneous reinnervation capacity in metabolic syndrome patients. Ann Neurol. 2015;77:146–53. Exercise alters the biology of cutaneous nociceptive fibers in the absence of neuropathy disease state.

    Article  PubMed  Google Scholar 

  57. Huang HH, Farmer K, Windscheffel J, et al. Exercise increases insulin content and basal secretion in pancreatic islets in type 1 diabetic mice. Exp Diabetes Res. 2011;2011:481427.

    PubMed Central  PubMed  Google Scholar 

  58. Kiraly MA, Bates HE, Yue JT, et al. Attenuation of type 2 diabetes mellitus in the male Zucker diabetic fatty rat: the effects of stress and non-volitional exercise. Metabolism. 2007;56:732–44.

    Article  CAS  PubMed  Google Scholar 

  59. Chen YW, Li YT, Chen YC, et al. Exercise training attenuates neuropathic pain and cytokine expression after chronic constriction injury of rat sciatic nerve. Anesth Analg. 2012;114:1330–7.

    Article  CAS  PubMed  Google Scholar 

  60. Sharma NK, Ryals JM, Gajewski BJ, et al. Aerobic exercise alters analgesia and neurotrophin-3 synthesis in an animal model of chronic widespread pain. Phys Ther. 2010;90:714–25.

    Article  PubMed Central  PubMed  Google Scholar 

  61. Selagzi H, Buyukakilli B, Cimen B, et al. Protective and therapeutic effects of swimming exercise training on diabetic peripheral neuropathy of streptozotocin-induced diabetic rats. J Endocrinol Investig. 2008;31:971–8.

    Article  CAS  Google Scholar 

  62. Orchard TJ, Temprosa M, Goldberg R, et al. The effect of metformin and intensive lifestyle intervention on the metabolic syndrome: the Diabetes Prevention Program randomized trial. Ann Intern Med. 2005;142:611–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Knowler WC, Barrett-Connor E, Fowler SE, et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002;346:393–403.

    Article  CAS  PubMed  Google Scholar 

  64. Tuomilehto J, Del Prato S. Mealtime glucose regulation in type 2 diabetes. Int J Clin Pract. 2001;55:380–3.

    CAS  PubMed  Google Scholar 

  65. Balducci S, Iacobellis G, Parisi L, et al. Exercise training can modify the natural history of diabetic peripheral neuropathy. J Diabetes Complicat. 2006;20:216–23. First study to show effect of exercise on diabetic neuropathy prevention.

    Article  PubMed  Google Scholar 

  66. Singleton JR, Marcus RL, Jackson JE, et al. Exercise increases cutaneous nerve density in diabetic patients without neuropathy. Ann Clin Transl Neurol. 2014;1:844–9.

    Article  PubMed Central  PubMed  Google Scholar 

  67. Allet L, Armand S, de Bie RA, et al. The gait and balance of patients with diabetes can be improved: a randomised controlled trial. Diabetologia. 2010;53:458–66.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. The Expert Panel on Detection and Treatment of High Blood Cholesterol in Adults, The Third Report of the ATP III. NIH publication 01-3670. http://www.nhlbi.nih.gov/guidelines/cholesterol/index.htm.2001, Bethesda Maryland: National Institutes of Health National Heart Lung and Blood Institute.

  69. Smith AG, Russell J, Feldman EL, et al. Lifestyle intervention for pre-diabetic neuropathy. Diabetes Care. 2006;29:1294–9.

    Article  PubMed  Google Scholar 

  70. Kluding PM, Pasnoor M, Singh R, et al. The effect of exercise on neuropathic symptoms, nerve function, and cutaneous innervation in people with diabetic peripheral neuropathy. J Diabetes Complicat. 2012. First human study to demonstrate improvement in diabetic neuropathy indices with exercise.

  71. Kluding PM, Pasnoor M, Singh R, et al. Safety of aerobic exercise in people with diabetic peripheral neuropathy: single-group clinical trial. Phys Ther. 2015;95:223–34.

    Article  PubMed  Google Scholar 

  72. Yoo M, D’Silva LJ, Martin K, et al. Pilot study of exercise therapy on painful diabetic peripheral neuropathy. Pain Med. 2015;16:1482–9.

    Article  PubMed  Google Scholar 

  73. Morrison S, Colberg SR, Parson HK, et al. Exercise improves gait, reaction time and postural stability in older adults with type 2 diabetes and neuropathy. J Diabetes Complicat. 2014;28:715–22.

    Article  PubMed  Google Scholar 

  74. Handsaker JC, Brown SJ, Bowling FL, et al. Contributory factors to unsteadiness during walking up and down stairs in patients with diabetic peripheral neuropathy. Diabetes Care. 2014;37:3047–53. Careful study of physical contributors to altered balance in diabetic neuropathy.

    Article  PubMed  Google Scholar 

  75. Handsaker JC, Brown SJ, Bowling FL, et al. Resistance exercise training increases lower limb speed of strength generation during stair ascent and descent in people with diabetic peripheral neuropathy. Diabet Med. 2015. doi:10.1111/dme.12841.

    Google Scholar 

  76. Streckmann F, Zopf EM, Lehmann HC, et al. Exercise intervention studies in patients with peripheral neuropathy: a systematic review. Sports Med. 2014;44:1289–304.

    Article  PubMed  Google Scholar 

  77. Lemaster JW, Mueller MJ, Reiber GE, et al. Effect of weight-bearing activity on foot ulcer incidence in people with diabetic peripheral neuropathy: feet first randomized controlled trial. Phys Ther. 2008;88:1385–98.

    Article  PubMed  Google Scholar 

  78. Armstrong DG, Lavery LA, Holtz-Neiderer K, et al. Variability in activity may precede diabetic foot ulceration. Diabetes Care. 2004;27:1980–4.

    Article  PubMed  Google Scholar 

  79. Kruse RL, Lemaster JW, Madsen RW. Fall and balance outcomes after an intervention to promote leg strength, balance, and walking in people with diabetic peripheral neuropathy: “feet first” randomized controlled trial. Phys Ther. 2010;90:1568–79.

    Article  PubMed  Google Scholar 

  80. Donnelly JE, Blair SN, Jakicic JM, et al. American College of Sports Medicine Position Stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc. 2009;41:459–71.

    Article  PubMed  Google Scholar 

  81. Praet SF, van Rooij ES, Wijtvliet A, et al. Brisk walking compared with an individualised medical fitness programme for patients with type 2 diabetes: a randomised controlled trial. Diabetologia. 2008;51:736–46.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  82. Tremblay M, Sedentary Behaviour Research N. Letter to the editor: standardized use of the terms “sedentary” and “sedentary behaviours”. Appl Physiol Nutr Metab. 2012;37:540–2.

    Article  Google Scholar 

  83. Koster A, Caserotti P, Patel KV, et al. Association of sedentary time with mortality independent of moderate to vigorous physical activity. PLoS One. 2012;7, e37696.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Bey L, Hamilton MT. Suppression of skeletal muscle lipoprotein lipase activity during physical inactivity: a molecular reason to maintain daily low-intensity activity. J Physiol. 2003;551:673–82.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Hamilton MT, Hamilton DG, Zderic TW. Role of low energy expenditure and sitting in obesity, metabolic syndrome, type 2 diabetes, and cardiovascular disease. Diabetes. 2007;56:2655–67.

    Article  CAS  PubMed  Google Scholar 

  86. Harrison M, O’Gorman DJ, McCaffrey N, et al. Influence of acute exercise with and without carbohydrate replacement on postprandial lipid metabolism. J Appl Physiol (1985). 2009;106:943–9.

    Article  CAS  Google Scholar 

  87. Stephens BR, Granados K, Zderic TW, et al. Effects of 1 day of inactivity on insulin action in healthy men and women: interaction with energy intake. Metabolism. 2011;60:941–9.

    Article  CAS  PubMed  Google Scholar 

  88. Thorp AA, Owen N, Neuhaus M, et al. Sedentary behaviors and subsequent health outcomes in adults a systematic review of longitudinal studies, 1996-2011. Am J Prev Med. 2011;41:207–15.

    Article  PubMed  Google Scholar 

  89. Duvivier BM, Schaper NC, Bremers MA, et al. Minimal intensity physical activity (standing and walking) of longer duration improves insulin action and plasma lipids more than shorter periods of moderate to vigorous exercise (cycling) in sedentary subjects when energy expenditure is comparable. PLoS One. 2013;8, e55542.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  90. Swartz AM, Squires L, Strath SJ. Energy expenditure of interruptions to sedentary behavior. Int J Behav Nutr Phys Act. 2011;8:69.

    Article  PubMed Central  PubMed  Google Scholar 

  91. Nygaard H, Tomten SE, Hostmark AT. Slow postmeal walking reduces postprandial glycemia in middle-aged women. Appl Physiol Nutr Metab. 2009;34:1087–92.

    Article  PubMed  Google Scholar 

  92. Healy GN, Wijndaele K, Dunstan DW, et al. Objectively measured sedentary time, physical activity, and metabolic risk: the Australian Diabetes, Obesity and Lifestyle Study (AusDiab). Diabetes Care. 2008;31:369–71.

    Article  PubMed  Google Scholar 

  93. Dunstan DW, Kingwell BA, Larsen R, et al. Breaking up prolonged sitting reduces postprandial glucose and insulin responses. Diabetes Care. 2012;35:976–83.

    Article  PubMed Central  PubMed  Google Scholar 

  94. Cooper JN, Columbus ML, Shields KJ, et al. Effects of an intensive behavioral weight loss intervention consisting of caloric restriction with or without physical activity on common carotid artery remodeling in severely obese adults. Metabolism. 2012;61:1589–97.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  95. Gardiner PA, Eakin EG, Healy GN, et al. Feasibility of reducing older adults’ sedentary time. Am J Prev Med. 2011;41:174–7.

    Article  PubMed  Google Scholar 

  96. De Greef KP, Deforche BI, Ruige JB, et al. The effects of a pedometer-based behavioral modification program with telephone support on physical activity and sedentary behavior in type 2 diabetes patients. Patient Educ Couns. 2011;84:275–9.

    Article  PubMed  Google Scholar 

  97. Lyden K, Kozey Keadle SL, Staudenmayer JW, et al. Validity of two wearable monitors to estimate breaks from sedentary time. Med Sci Sports Exerc. 2012;44:2243–52.

    Article  PubMed Central  PubMed  Google Scholar 

  98. Kozey-Keadle S, Libertine A, Lyden K, et al. Validation of wearable monitors for assessing sedentary behavior. Med Sci Sports Exerc. 2011;43:1561–7.

    Article  PubMed  Google Scholar 

  99. Kozey-Keadle S, Libertine A, Staudenmayer J, et al. The feasibility of reducing and measuring sedentary time among overweight, non-exercising office workers. J Obes 2012; 2012: 282303.

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Acknowledgments

All authors of this paper have funding from NIH that is supporting this work (NIH R01 DK064814).

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Authors and Affiliations

  1. Department of Neurology, University of Utah, Salt Lake City, UT, USA

    J. Robinson Singleton & A. Gordon Smith

  2. Department of Physical Therapy, University of Utah, Salt Lake City, UT, USA

    Robin L. Marcus

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  1. J. Robinson Singleton
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J. Robinson Singleton, A. Gordon Smith, and Robin L. Marcus declare that they have no conflict of interest.

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This article is part of the Topical Collection on Microvascular Complications—Neuropathy

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Singleton, J.R., Smith, A.G. & Marcus, R.L. Exercise as Therapy for Diabetic and Prediabetic Neuropathy. Curr Diab Rep 15, 120 (2015). https://doi.org/10.1007/s11892-015-0682-6

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