Swim Therapy Reduces Mechanical Allodynia and Thermal Hyperalgesia Induced by Chronic Constriction Nerve Injury in Rats

Pain Medicine (United States)

Volumn 14, Issue 4, 2013, Pages 516-525

  Shen, Jun ^a   Fox, Lyle E ^a   Cheng, Jianguo ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Exercise; Neuralgia; Pain Management; Rehabilitation Medicine

Indexed keywords

HOT WATER;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC CONSTRICTION NERVE INJURY; CONTROLLED STUDY; HYPERALGESIA; MALE; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PAIN THRESHOLD; RAT; SWIMMING;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CONSTRICTION, PATHOLOGIC; EXERCISE THERAPY; HOT TEMPERATURE; HYPERALGESIA; MALE; NEURALGIA; PAIN THRESHOLD; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NEUROPATHY; SWIMMING;

EID: 84876194041     PISSN: 15262375     EISSN: 15264637     Source Type: Journal    
DOI: 10.1111/pme.12057     Document Type: Article

References (77)

1. Toth C, Lander J, Wiebe S. The prevalence and impact of chronic pain with neuropathic pain symptoms in the general population. Pain Med 2009;10:918-929.
2. Baron R, Binder A, Wasner G. Neuropathic pain: Diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol 2010;9:807-819.
3. Kennedy JD. Neuropathic pain: Molecular complexity underlies continuing unmet medical need. J Med Chem 2007;50:2547-2556.
4. O'Connor AB, Dworkin RH. Treatment of neuropathic pain: An overview of recent guidelines. Am J Med 2009;122(10 suppl):S22-32.
5. Santiago-Figueroa J, Kuffler DP. Reducing and eliminating neuropathic pain. P R Health Sci J 2009;28:289-300.
6. Van Boxem K, Cheng J, Patijn J, etal. Lumbosacral radicular pain. Pain Pract 2010;10:339-358.
7. Jensen MP, Chodroff MJ, Dworkin RH. The impact of neuropathic pain on health-related quality of life: Review and implications. Neurology 2007;68:1178-1182.
8. O'Connor AB. Neuropathic pain: Quality-of-life impact, costs and cost effectiveness of therapy. Pharmacoeconomics 2009;27:95-112.
9. Mekhail NA, Cheng J, Narouze S, etal. Clinical applications of neurostimulation: Forty years later. Pain Pract 2010;10:103-112.
10. Penedo FJ, Dahn JR. Exercise and well-being: A review of mental and physical health benefits associated with physical activity. Curr Opin Psychiatry 2005;18:189-193.
11. Vogel T, Brechat PH, Leprêtre PM, etal. Health benefits of physical activity in older patients: A review. Int J Clin Pract 2009;63:303-320.
12. Warburton DE, Nicol CW, Bredin SS. Health benefits of physical activity: The evidence. CMAJ 2006;174:801-809.
13. Janal MN. Pain sensitivity, exercise and stoicism. J R Soc Med 1996;89:376-381.
14. Koltyn KF. Analgesia following exercise: A review. Sports Med 2000;29:85-98.
15. O'Connor PJ, Cook DB. Exercise and pain: The neurobiology, measurement, and laboratory study of pain in relation to exercise in humans. Exerc Sport Sci Rev 1999;27:119-166.
16. Haier RJ, Quaid K, Mills JC. Naloxone alters pain perception after jogging. Psychiatry Res 1981;5:231-232.
17. Koltyn KF, Garvin AW, Gardiner RL, Nelson TF. Perception of pain following aerobic exercise. Med Sci Sports Exerc 1996;28:1418-1421.
18. Butler RK, Finn DP. Stress-induced analgesia. Prog Neurobiol 2009;88:184-202.
19. Costigan M, Scholz J, Woolf CJ. Neuropathic pain: A maladaptive response of the nervous system to damage. Annu Rev Neurosci 2009;32:1-32.
20. Sparling PB, Giuffrida A, Piomelli D, Rosskopf L, Dietrich A. Exercise activates the endocannabinoid system. Neuroreport 2003;14:2209-2211.
21. Tseng LF. Evidence for epsilon-opioid receptor-mediated beta-endorphin-induced analgesia. Trends Pharmacol Sci 2001;22:623-630.
22. Anand P. Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 2004;146:477-492.
23. Dray A. Neuropathic pain: Emerging treatments. Br J Anaesth 2008;101:48-58.
24. Milligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 2009;10:23-36.
25. Hutchinson KJ, Gómez-Pinilla F, Crowe MJ, Ying Z, Basso DM. Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain 2004;127:1403-1414.
26. Kuphal KE, Fibuch EE, Taylor BK. Extended swimming exercise reduces inflammatory and peripheral neuropathic pain in rodents. J Pain 2007;8:989-997.
27. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988;33:87-107.
28. Attal N, Jazat F, Kayser V, Guilbaud G. Further evidence for "pain-related" behaviours in a model of unilateral peripheral mononeuropathy. Pain 1990;41:235-251.
29. Shen J, Fox LE, Cheng J. Swim training reduces neuropathic pain induced by chronic constriction injury in rats. Program No. 158.16. 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010. Online.
30. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988;32:77-88.
31. Shen J, Fox L, Cheng J. Differential effects of peripheral versus neuroaxial co-administration of capsaicin and QX-314 on neuropathic pain in rats. Anesthesiology 2012;117:365-380.
32. Black J, Chesher GB, Starmer GA, Egger G. The painlessness of the long distance runner. Med J Aust 1979;1:522-523.
33. Cooper K, Carmody J. The characteristics of the opioid-related analgesia induced by the stress of swimming in the mouse. Neurosci Lett 1982;31:165-170.
34. Tierney G, Carmody J, Jamieson D. Stress analgesia: The opioid analgesia of long swims suppresses the non-opioid analgesia induced by short swims in mice. Pain 1991;46:89-95.
35. Benoist JM, Pincedé I, Ballantyne K, Plaghki L, Le Bars D. Peripheral and central determinants of a nociceptive reaction: An approach to psychophysics in the rat. Plos ONE 2008;3:e3125.
36. Eide PK, Tjølsen A. Effects of serotonin receptor antagonists and agonists on the tail-flick response in mice involve altered tail-skin temperature. Neuropharmacology 1988;27:889-893.
37. O'Connor P, Chipkin RE. Comparisons between warm and cold water swim stress in mice. Life Sci 1984;35:631-639.
38. Quintero L, Moreno M, Avila C, etal. Long-lasting delayed hyperalgesia after subchronic swim stress. Pharmacol Biochem Behav 2000;67:449-458.
39. Byun YH, Lee MH, Kim SS, etal. Treadmill running promotes functional recovery and decreases brain-derived neurotrophic factor mRNA expression following sciatic crushed nerve injury in rats. J Sports Med Phys Fitness 2005;45:222-228.
40. Cha J, Heng C, Reinkensmeyer DJ, etal. Locomotor ability in spinal rats is dependent on the amount of activity imposed on the hindlimbs during treadmill training. J Neurotrauma 2007;24:1000-1012.
41. Doyle LM, Roberts BL. Exercise enhances axonal growth and functional recovery in the regenerating spinal cord. Neuroscience 2006;141:321-327.
42. Heng C, de Leon RD. Treadmill training enhances the recovery of normal stepping patterns in spinal cord contused rats. Exp Neurol 2009;216:139-147.
43. Smith RR, Shum-Siu A, Baltzley R, etal. Effects of swimming on functional recovery after incomplete spinal cord injury in rats. J Neurotrauma 2006;23:908-919.
44. Kim KJ, Yoon YW, Chung JM. Comparison of three rodent neuropathic pain models. Exp Brain Res 1997;113:200-206.
45. Malmberg AB, Chen C, Tonegawa S, Basbaum AI. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 1997;278:279-283.
46. Martinez-Caro L, Laird JM. Allodynia and hyperalgesia evoked by sciatic mononeuropathy in NKI receptor knockout mice. Neuroreport 2000;11:1213-1217.
47. Seltzer Z, Dubner R, Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990;43:205-218.
48. Cobianchi S, Marinelli S, Florenzano F, Pavone F, Luvisetto S. Short- but not long-lasting treadmill running reduces allodynia and improves functional recovery after peripheral nerve injury. Neuroscience 2010;168:273-287.
49. Goff JR, Burkey AR, Goff DJ, Jasmin L. Reorganization of the spinal dorsal horn in models of chronic pain: Correlation with behaviour. Neuroscience 1998;82:559-574.
50. Lee BH, Yoon YW, Chung K, Chung JM. Comparison of sympathetic sprouting in sensory ganglia in three animal models of neuropathic pain. Exp Brain Res 1998;120:432-438.
51. Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med 2005;35:339-361.
52. Boone JB Jr, Sherraden T, Pierzchala K, Berger R, Van Loon GR. Plasma Met-enkephalin and catecholamine responses to intense exercise in humans. J Appl Physiol 1992;73:388-392.
53. Debruille C, Luyckx M, Ballester L, etal. Serum opioid activity after physical exercise in rats. Physiol Res 1999;48:129-133.
54. Goldfarb AH, Jamurtas AZ. Beta-endorphin response to exercise. An update. Sports Med 1997;24:8-16.
55. Schwarz L, Kindermann W. Changes in beta-endorphin levels in response to aerobic and anaerobic exercise. Sports Med 1992;13:25-36.
56. Bement MK, Sluka KA. Low-intensity exercise reverses chronic muscle pain in the rat in a naloxone-dependent manner. Arch Phys Med Rehabil 2005;86:1736-1740.
57. Carmody J, Cooper K. Swim stress reduces chronic pain in mice through an opioid mechanism. Neurosci Lett 1987;74:358-363.
58. Cho HJ, Kim JK, Park HC, etal. Changes in brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia, spinal cord, and gracile nuclei following cut or crush injuries. Exp Neurol 1998;154:224-230.
59. Gómez-Pinilla F, Ying Z, Opazo P, Roy RR, Edgerton VR. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 2001;13:1078-1084.
60. Gómez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 2002;88:2187-2195.
61. Herzberg U, Eliav E, Dorsey JM, Gracely RH, Kopin IJ. NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve. Neuroreport 1997;8:1613-1618.
62. Miletic G, Miletic V. Increases in the concentration of brain derived neurotrophic factor in the lumbar spinal dorsal horn are associated with pain behavior following chronic constriction injury in rats. Neurosci Lett 2002;319:137-140.
63. Obata K, Yamanaka H, Fukuoka T, etal. Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain 2003;101:65-77.
64. Vanelderen P, Rouwette T, Kozicz T, etal. The role of brain-derived neurotrophic factor in different animal models of neuropathic pain. Eur J Pain 2010;14:473.e1-4739.
65. Cirillo G, Cavaliere C, Bianco MR, etal. Intrathecal NGF administration reduces reactive astrocytosis and changes neurotrophin receptors expression pattern in a rat model of neuropathic pain. Cell Mol Neurobiol 2010;30:51-62.
66. Ro LS, Chen ST, Tang LM, Jacobs JM. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 1999;79:265-274.
67. Wilson-Gerwing TD, Dmyterko MV, Zochodne DW, Johnston JM, Verge VM. Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons. J Neurosci 2005;25:758-767.
68. Yajima Y, Narita M, Usui A, etal. Direct evidence for the involvement of brain-derived neurotrophic factor in the development of a neuropathic pain-like state in mice. J Neurochem 2005;93:584-594.
69. Bridges D, Ahmad K, Rice AS. The synthetic cannabinoid WIN55, 212-2 attenuates hyperalgesia and allodynia in a rat model of neuropathic pain. Br J Pharmacol 2001;133(4):586-594.
70. Costa B, Colleoni M, Conti S, etal. Repeated treatment with the synthetic cannabinoid WIN 55, 212-2 reduces both hyperalgesia and production of pronociceptive mediators in a rat model of neuropathic pain. Br J Pharmacol 2004;141:4-8.
71. Fox A, Kesingland A, Gentry C, etal. The role of central and peripheral cannabinoid1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain. Pain 2001;92:91-100.
72. Kinsey SG, Long JZ, O'Neal ST, etal. Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J Pharmacol Exp Ther 2009;330:902-910.
73. 2+ influx and neurotoxicity in dorsal root ganglion neurons. J Pharmacol Exp Ther 2009;331:1062-1070.
74. Chaouloff F. Physical exercise and brain monoamines: A review. Acta Physiol Scand 1989;137:1-13.
75. Meeusen R, De Meirleir K. Exercise and brain neurotransmission. Sports Med 1995;20:160-188.
76. Millan MJ. The induction of pain: An integrative review. Prog Neurobiol 1999;57:1-164.
77. Millan MJ. Descending control of pain. Prog Neurobiol 2002;66:355-474.