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Protective and therapeutic effects of swimming exercise training on diabetic peripheral neuropathy of streptozotocin-induced diabetic rats

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Abstract

Background: Diabetic peripheral neuropathy (DPN) is a typical complication of diabetes. No definitive treatment and prevention of DPN has been established, and very few data on the role of exercise training on DPN have been reported. Aim of the study: The protective and therapeutic effects of aerobic physical activity on the development of DPN in Type 1 were investigated. Methods: Rats were assigned to 5 groups: C (control), E (exercise), D (diabetic), DEx (exercise after diabetic), ExD (diabetic after exercise); C containing 10 animals and E, D, DEx, ExD containing 15 animals. Diabetes was induced with streptozotocin (STZ) (45 mg/kg, ip). Development of diabetes was confirmed by measuring blood glucose levels 2 days after STZ treatment. Body weights of all the animals were evaluated weekly throughout the experiment. Motor dysfunction defined by a significant increase in compound muscle action potential (CMAP) latency was recorded. The amplitude of CMAP which mainly reflects axonal dysfunction was also measured using standard techniques. Sciatic nerve morphometry and blood glucose levels were analyzed in all the groups. Results: Blood glucose level significantly increased 2 days after STZ injection. All diabetic rats showed decreased body weight compared to control rats. An increase in motor latency of CMAP and a decrease in amplitude of CMAP, indicative of neuropathy, were seen in STZ rats. On the completion of the study (the 56th day post-STZ), histological examination revealed significant myelin loss (thinner myelin) in sciatic nerves of STZ rats. Treatment with swimming exercise had no effect on glycemic control but restored body weight, CMAP amplitude, CMAP latency or motor dysfunction in the diabetic animals. Conclusions: This study suggests that swimming exercise training has protective and therapeutic effects on DPN of STZ-induced diabetic rats.

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References

  1. Sugimura K, Windebank AJ, Natarajan V, Lambert EH, Schmid HH, Dyck PJ. Interstitial hyperosmolarity may cause axis cylinder shrinkage in streptozotocin-diabetic nerve. J Neuropathol Exp Neurol 1980, 39: 710–21.

    Article  PubMed  CAS  Google Scholar 

  2. Yasuda H, Terada M, Maeda K, et al. Diabetic neuropathy and nerve regeneration. Prog Neurobiol 2003, 69: 229–85.

    Article  PubMed  CAS  Google Scholar 

  3. Boulton AJ. Lowering the risk of neuropathy, foot ulcers and amputations. Diabet Med 1998, 15 (Suppl 4): S57–9.

    Article  PubMed  Google Scholar 

  4. Poncelet AN. Diabetic polyneuropathy. Risk factors, patterns of presentation, diagnosis, and treatment. Geriatrics 2003, 58: 16–8.

    PubMed  Google Scholar 

  5. Cameron NE, Cotter MA. The relationship of vascular changes to metabolic factors in diabetes mellitus and their role in the development of peripheral nerve complications. Diabetes Metab Rev 1994, 10: 189–224.

    Article  PubMed  CAS  Google Scholar 

  6. Ward JD. Biochemical and vascular factors in the pathogenesis of diabetic neuropathy. Clin Invest Med 1995, 18: 267–74.

    PubMed  Google Scholar 

  7. Kim J, Kyriazi H, Greene DA. Normalization of Na+−K+ ATPase activity in isolated membrane fraction from sciatic nerves of streptozo-tocin-induced diabetic rats by dietary myoinositol supplementation in vivo or protein kinase C agonists in vitro. Diabetes 1991, 40: 558–67.

    Article  PubMed  CAS  Google Scholar 

  8. Bianchi R, Buyukakilli B, Brines M, et al. Erythropoietin both protects from and reverses experimental diabetic neuropathy. Proc Natl Acad Sci USA 2004, 101: 823–8.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  9. Naziroglu M, Simsek M, Kutlu M. Moderate exercise with a dietary vitamin C and E combination protects against streptozotocin-induced oxidative damage to the blood and improves fetal outcomes in pregnant rats. Clin Chem Lab Med 2004, 42: 511–7.

    Article  PubMed  CAS  Google Scholar 

  10. Lee DM, Hoffman WH, Carl GF, Khichi M, Cornwell PE. Lipid peroxidation and antioxidant vitamins prior to, during, and after correction of diabetic ketoacidosis. J Diabetes Complications 2002, 16: 294–300.

    Article  PubMed  Google Scholar 

  11. Atalay M, Laaksonen DE. Diabetes, oxidative stress and physical exercise. J Sports Sci Med 2002, 1: 1–14.

    PubMed Central  PubMed  Google Scholar 

  12. Dahl-Jørgensen K, Brinchmann-Hansen O, Hanssen KF, et al. Effect of near normoglycaemia for two years on progression of early diabetic retinopathy, nephropathy, and neuropathy: The Oslo study. Br Med J (Clin Res Ed) 1986, 293: 1195–9.

    Article  Google Scholar 

  13. Richardson JK, Sandman D, Vela S. A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy. Arch Phys Med Rehabil 2001, 82: 205–9.

    Article  PubMed  CAS  Google Scholar 

  14. Balducci S, Iacobellis G, Parisi L, et al. Exercise training can modify the natural history of diabetic peripheral neuropathy. J Diabetes Complications 2006, 20: 216–23.

    Article  PubMed  Google Scholar 

  15. Thomas PK, Tomlinson DR. Diabetic and hypoglycemic neuropathy. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF eds. Peripheral Neuropathy (vol 3). Philadelphia: WB Saunders. 1993, 1219–50.

    Google Scholar 

  16. Tesfaye S, Harris ND, Wilson RM, Ward JD. Exercise-induced conduction velocity increment: a marker of impaired peripheral nerve blood flow in diabetic neuropathy. Diabetologia 1992, 35: 155–9.

    Article  PubMed  CAS  Google Scholar 

  17. Harri M, Kuusela P. Is swimming exercise or cold exposure for rats? Acta Physiol Scand 1986, 126: 189–97.

    Article  PubMed  CAS  Google Scholar 

  18. Gobatto CA, de Mello MA, Sibuya CY, de Azevedo JR, dos Santos LA, Kokubun E. Maximal lactate steady state in rats submitted to swimming exercise. Comp Biochem Physiol A Mol Integr Physiol 2001,130: 21–7.

    Article  PubMed  CAS  Google Scholar 

  19. de Oliveira CA, Luciano E, de Mello MA. The role of exercise on long-term effects of alloxan administered in neonatal rats. Exp Physiol 2004, 90: 79–86.

    Article  PubMed  CAS  Google Scholar 

  20. Matsuo T, Kang HS, Suzuki H, Suzuki M. Voluntary resistance exercise improves blood hemoglobin concentration in severely irondeficient rats. J Nutr Sci Vitaminol (Tokyo) 2002, 48: 161–4.

    Article  CAS  Google Scholar 

  21. Aminoff MJ. Nerve conduction studies: Basic principles and pathologic correlations. In Aminoff MJ ed. Electromyography in Clinical Practice. London: Churchill Livingstone 1998, 113–45.

    Google Scholar 

  22. Rakieten N, Rakieten ML, Nadkarni MV. Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep 1963, 29: 91–8.

    Google Scholar 

  23. Changrani NR, Chonkar A, Adeghate E, Singh J. Effects of streptozotocin-induced type 1 diabetes mellitus on total protein concentrations and cation contents in the isolated pancreas, parotid, submandibular, and lacrimal glands of rats. Ann N Y Acad Sci 2006, 1084: 503–19.

    Article  PubMed  CAS  Google Scholar 

  24. Andriambeloson E, Baillet C, Vitte PA, Garotta G, Dreano M, Callizot N. Interleukin-6 attenuates the development of experimental diabetes-related neuropathy. Neuropathology 2006, 26: 32–42.

    Article  PubMed  Google Scholar 

  25. Vinik AI. Diabetic neuropathy: pathogenesis and therapy. Am J Med 1999, 107(2B): 17S–26S.

    Article  PubMed  CAS  Google Scholar 

  26. Coskun O, Ocakcı A, Bayraktaroglu T, Kanter M. Exercise training prevents and protects streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. Tohoku J Exp Med 2004, 203: 145–54.

    Article  PubMed  CAS  Google Scholar 

  27. Wallberg-Henriksson H, Gunnarsson R, Henriksson J, et al. Increased peripheral insulin sensitivity and muscle mitochondrial enzymes but unchanged blood glucose control in type I diabetes after physical training. Diabetes 1982, 31: 1044–50.

    Article  PubMed  CAS  Google Scholar 

  28. Franz MJ. Exercise and the management of diabetes mellitus. J Am Diet Assoc 1987, 87: 872–80.

    PubMed  CAS  Google Scholar 

  29. Carrington AL, Calcutt NA, Ettlinger CB, Gustafsson T, Tomlinson DR. Effects of treatment with myo-inositol or its 1,2,6-trisphosphate (PP56) on nerve conduction in streptozotocin-diabetes. Eur J Pharmacol 1993:237: 257–63.

    Article  PubMed  CAS  Google Scholar 

  30. Lee HH, Shin MS, Kim YS, et al. Early treadmill exercise decreases intrastriatal hemorrhage-induced neuronal cell death and increases cell proliferation in the dentate gyrus of streptozotocin-induced hyperglycemic rats. J Diabetes Complications 2005, 19: 339–46.

    Article  PubMed  Google Scholar 

  31. Kihara M, Mitsui MK, Mitsui Y, et al. Altered vasoreactivity to angiotensin II in experimental diabetic neuropathy: role of nitric oxide. Muscle Nerve 1999, 22: 920–5.

    Article  PubMed  CAS  Google Scholar 

  32. Tomlinson DR, Holmes PR, Mayer JH. Reversal, by treatment with an aldose reductase inhibitor, of impaired axonal transport and motor nerve conduction velocity in experimental diabetes mellitus. Neurosci Lett 1982, 31: 189–93.

    Article  PubMed  CAS  Google Scholar 

  33. Saini AK, Arun KH, Kaul CL, Sharma SS. Acute hyperglycemia attenuatesnerve conduction velocity and nerve blood flow in male Sprague-Dawley rats: reversal by adenosine. Pharmacol Res 2004, 50: 593–9.

    Article  PubMed  CAS  Google Scholar 

  34. Yang O, Kaji R, Takagi T, et al. Abnormal axonal inward rectifier in streptozocin-induced experimental diabetic neuropathy. Brain 2001,124: 1149–55.

    Article  PubMed  CAS  Google Scholar 

  35. Greene DA, Feldman EL, Stevens MJ, Sima AAF, Albers JW, Pfeifer MA. Diabetic neuropathy. In: Porte D, Sherwin Reds. Ellenberg & Rifkins’s diabetes mellitus. Stamford (CO): Appleton & Lange. 1997, 1009–76.

    Google Scholar 

  36. Kjeldsen K, Richter EA, Galbo H, Lortie G, Clausen T. Training increases the concentration of [3H]ouabain-binding sites in rat skeletal muscle. Biochim Biophys Acta 1986, 860: 708–12.

    Article  PubMed  CAS  Google Scholar 

  37. Bestetti G, Zemp C, Probst D, Rossi GL Neuropathy and myopathy in the diaphragm of rats after 12 months of streptozotocin-induced diabetes mellitus. A light-, electron-microscopic, and morphometric study. Acta Neuropathol 1981, 55: 11–20.

    Article  PubMed  CAS  Google Scholar 

  38. Birrell AM, Heffernan SJ, Ansselin AD, et al. Functional and structural abnormalities in the nerves of type I diabetic baboons: aminoguanidine treatment does not improve nerve function. Diabetologia 2000, 43: 110–6.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to B. Buyukakilli PhD.

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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 Invest 31, 971–978 (2008). https://doi.org/10.1007/BF03345634

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