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Mediators of Inflammation
Volume 2013, Article ID 971841, 7 pages
http://dx.doi.org/10.1155/2013/971841
Review Article

Low-Grade Inflammation and Spinal Cord Injury: Exercise as Therapy?

1Departamento de Psicobiologia, Universidade Federal de São Paulo, UNIFESP, Campus São Paulo, 04020-050 São Paulo, Brazil
2Centro de Estudos em Psicobiologia e Exercício, (CEPE), 04020-050 São Paulo, Brazil
3Laboratório de Fisiologia e Bioquímica do Exercício, Programa de Pós-Graduação em Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
4Departamento de Biociências, Universidade Federal de São Paulo, UNIFESP, Campus da Baixada Santista, Brazil
5Laboratório do Movimento Humano, Universidade São Judas Tadeu, 04020-050 São Paulo, Brazil

Received 30 November 2012; Accepted 2 February 2013

Academic Editor: Gustavo Duarte Pimentel

Copyright © 2013 Eduardo da Silva Alves et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. D. Wang, Y. H. Wang, T. S. Huang, T. C. Su, S. L. Pan, and S. Y. Chen, “Circulating levels of markers of inflammation and endothelial activation are increased in men with chronic spinal cord injury,” Journal of the Formosan Medical Association, vol. 106, no. 11, pp. 919–928, 2007. View at Publisher · View at Google Scholar
  2. L. H. Van der Woude, S. de Groot, K. Postema, J. B. Bussmann, T. W. Janssen, and M. W. Post, “Active lifestyle rehabilitation interventions in aging spinal cord injury (ALLRISC): a multicentre research program,” Disability and Rehabilitation. In press.
  3. P. G. Shekelle, S. C. Morton, K. A. Clark, M. Pathak, and B. G. Vickrey, “Systematic review of risk factors for urinary tract infection in adults with spinal cord dysfunction,” Journal of Spinal Cord Medicine, vol. 22, no. 4, pp. 258–272, 1999. View at Google Scholar · View at Scopus
  4. M. Cortez, L. S. Carmo, M. M. Rogero, P. Borelli, and R. A. Fock, “A high-fat diet increases IL-1, IL-6, and TNF-α production by increasing NF-κB and attenuating PPAR-γ expression in bone marrow mesenchymal stem cells,” Inflammation. In press.
  5. W. A. Bauman and A. M. Spungen, “Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging,” Metabolism, vol. 43, no. 6, pp. 749–756, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. I. T. Kim, J. H. Mun, P. S. Jun, G. C. Kim, Y. J. Sim, and H. J. Jeong, “Leisure time physical activity of people with spinal cord injury: mainly with clubs of spinal cord injury patients in busan-kyeongnam, Korea,” Annals of Rehabilitation Medicine, vol. 35, no. 5, pp. 613–626, 2011. View at Publisher · View at Google Scholar
  7. “Spinal cord injury facts and figures at a glance,” The Journal of Spinal Cord Medicine, vol. 34, no. 6, pp. 620–621, 2011. View at Publisher · View at Google Scholar
  8. M. J. Devivo, “Epidemiology of traumatic spinal cord injury: trends and future implications,” Spinal Cord, vol. 50, no. 5, pp. 365–372, 2012. View at Publisher · View at Google Scholar
  9. I. G. Fiedler, P. W. Laud, D. J. Maiman, and D. F. Apple, “Economics of managed care in spinal cord injury,” Archives of Physical Medicine and Rehabilitation, vol. 80, no. 11, pp. 1441–1449, 1999. View at Publisher · View at Google Scholar
  10. R. Gupta, M. E. Bathen, J. S. Smith, A. D. Levi, N. N. Bhatia, and O. Steward, “Advances in the management of spinal cord injury,” Journal of the American Academy of Orthopaedic Surgeons, vol. 18, no. 4, pp. 210–222, 2010. View at Google Scholar
  11. L. R. Watkins, E. P. Wiertelak, L. E. Goehler et al., “Neurocircuitry of illness-induced hyperalgesia,” Brain Research, vol. 639, no. 2, pp. 283–299, 1994. View at Google Scholar
  12. M. Okamoto, H. Baba, P. A. Goldstein, H. Higashi, K. Shimoji, and M. Yoshimura, “Functional reorganization of sensory pathways in the rat spinal dorsal horn following peripheral nerve injury,” Journal of Physiology, vol. 532, no. 1, pp. 241–250, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. D. I. Campagnolo, S. E. Keller, J. A. Delisa, T. J. Glick, M. L. Sipski, and S. J. Schleifer, “Alteration of immune system function in tetraplegics: a pilot study,” American Journal of Physical Medicine and Rehabilitation, vol. 73, no. 6, pp. 387–393, 1994. View at Google Scholar · View at Scopus
  14. J. M. Cruse, R. E. Lewis, G. R. Bishop, W. F. Kliesch, and E. Gaitan, “Neuroendocrine-immune interactions associated with loss and restoration of immune system function in spinal cord injury and stroke patients,” Immunologic Research, vol. 11, no. 2, pp. 104–116, 1992. View at Google Scholar · View at Scopus
  15. H. Sabour, A. N. Javidan, M. R. Vafa et al., “Obesity predictors in people with chronic spinal cord injury: an analysis by injury related variables,” Journal of Research in Medical Sciences, vol. 16, no. 3, pp. 335–339, 2011. View at Google Scholar · View at Scopus
  16. S. Rajan, M. J. McNeely, C. Warms, and B. Goldstein, “Clinical assessment and management of obesity in individuals with spinal cord injury: a review,” Journal of Spinal Cord Medicine, vol. 31, no. 4, pp. 361–372, 2008. View at Google Scholar · View at Scopus
  17. J. E. Decaria, C. Sharp, and R. J. Petrella, “Scoping review report: obesity in older adults,” International Journal of Obesity, vol. 36, no. 9, pp. 1141–1150, 2012. View at Google Scholar
  18. M. C. Calle and M. L. Fernandez, “Inflammation and type 2 diabetes,” Diabetes & Metabolism, vol. 38, no. 3, pp. 183–191, 2012. View at Google Scholar
  19. N. Ouchi, J. L. Parker, J. J. Lugus, and K. Walsh, “Adipokines in inflammation and metabolic disease,” Nature Reviews Immunology, vol. 11, no. 2, pp. 85–97, 2011. View at Google Scholar
  20. P. D. Woolf, L. A. Lee, R. W. Hamill, and J. V. McDonald, “Thyroid test abnormalities in traumatic brain injury: correlation with neurologic impairment and sympathetic nervous system activation,” American Journal of Medicine, vol. 84, no. 2, pp. 201–208, 1988. View at Google Scholar · View at Scopus
  21. W. A. Bauman and A. M. Spungen, “Carbohydrate and lipid metabolism in chronic spinal cord injury,” Journal of Spinal Cord Medicine, vol. 24, no. 4, pp. 266–277, 2001. View at Google Scholar · View at Scopus
  22. A. V. Turnbull and C. L. Rivier, “Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action,” Physiological Reviews, vol. 79, no. 1, pp. 1–71, 1999. View at Google Scholar · View at Scopus
  23. H. Y. Li, A. Ericsson, and P. E. Sawchenko, “Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 6, pp. 2359–2364, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Beyaert and W. Fiers, “Molecular mechanisms of tumor necrosis factor-induced cytotoxicity: what we do understand and what we do not,” FEBS Letters, vol. 340, no. 1-2, pp. 9–16, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. A. I. Moldoveanu, R. J. Shephard, and P. N. Shek, “The cytokine response to physical activity and training,” Sports Medicine, vol. 31, no. 2, pp. 115–144, 2001. View at Google Scholar · View at Scopus
  26. M. Baes, W. Allaerts, and C. Denef, “Evidence for functional communication between folliculo-stellate cells and hormone-secreting cells in perifused anterior pituitary cell aggregates,” Endocrinology, vol. 120, no. 2, pp. 685–691, 1987. View at Google Scholar · View at Scopus
  27. R. Basheer, R. E. Strecker, M. M. Thakkar, and R. W. McCarley, “Adenosine and sleep-wake regulation,” Progress in Neurobiology, vol. 73, no. 6, pp. 379–396, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. J. S. Chen, P. H. Huang, C. H. Wang et al., “Nrf-2 mediated heme oxygenase-1 expression, an antioxidant-independent mechanism, contributes to anti-atherogenesis and vascular protective effects of Ginkgo biloba extract,” Atherosclerosis, vol. 214, no. 2, pp. 301–309, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. E. R. Ropelle, M. B. Flores, D. E. Cintra et al., “IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKbeta and ER stress inhibition,” PLoS Biology, vol. 24, no. 8, 2010. View at Google Scholar
  30. J. M. Aubry, A. V. Turnbull, G. Pozzoli, C. Rivier, and W. Vale, “Endotoxin decreases corticotropin-releasing factor receptor 1 messenger ribonucleic acid levels in the rat pituitary,” Endocrinology, vol. 138, no. 4, pp. 1621–1626, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Bernhagen, T. Calandra, R. A. Mitchell et al., “MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia,” Nature, vol. 365, no. 6448, pp. 756–759, 1993. View at Publisher · View at Google Scholar · View at Scopus
  32. M. R. Opp and L. A. Toth, “Somnogenic and pyrogenic effects of interleukin-1β and lipopolysaccharide in intact and vagotomized rats,” Life Sciences, vol. 62, no. 10, pp. 923–936, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Layé, R. M. Bluthe, S. Kent et al., “Subdiaphragmatic vagotomy blocks induction of IL-1 beta mRNA in mice brain in response to peripheral LPS,” American Journal of Physiology, vol. 268, no. 5, part 2, pp. R1327–R1331, 1995. View at Google Scholar
  34. E. M. Sternberg, “Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens,” Nature Reviews Immunology, vol. 6, no. 4, pp. 318–328, 2006. View at Google Scholar
  35. L. A. Normell, “Distribution of impaired cutaneous vasomotor and sudomotor function in paraplegic man,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 33, no. 138, pp. 25–41, 1974. View at Google Scholar · View at Scopus
  36. B. G. Wallin and L. Stjernberg, “Sympathetic activity in man after spinal cord injury. Outflow to skin below the lesion,” Brain, vol. 107, no. 1, pp. 183–198, 1984. View at Google Scholar · View at Scopus
  37. H. Krum, D. J. Brown, P. R. Rowe, W. J. Louis, and L. G. Howes, “Steady state plasma [3H]-noradrenaline kinetics in quadriplegic chronic spinal cord injury patients,” Journal of Autonomic Pharmacology, vol. 10, no. 4, pp. 221–226, 1990. View at Google Scholar
  38. A. Schmid, M. Huonker, F. Stahl et al., “Free plasma catecholamines in spinal cord injured persons with different injury levels at rest and during exercise,” Journal of the Autonomic Nervous System, vol. 68, no. 1-2, pp. 96–100, 1998. View at Google Scholar
  39. M. Kjær, S. F. Pollack, T. Mohr et al., “Regulation of glucose turnover and hormonal responses during electrical cycling in tetraplegic humans,” American Journal of Physiology, vol. 271, no. 1, Part 2, pp. R191–R199, 1996. View at Google Scholar
  40. A. K. Karlsson, M. Elam, P. Friberg, F. Biering-Sörensen, L. Sullivan, and P. Lönnroth, “Regulation of lipolysis by the sympathetic nervous system: a microdialysis study in normal and spinal cord-injured subjects,” Metabolism, vol. 46, no. 4, pp. 388–394, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. P. D. Thompson, S. F. Crouse, B. Goodpaster, D. Kelley, N. Moyna, and L. Pescatello, “The acute versus the chronic response to exercise,” Medicine & Science in Sports & Exercise, vol. 33, supplement 6, pp. S438–S445, 2001. View at Google Scholar
  42. J. F. Horowitz and S. Klein, “Whole body and abdominal lipolytic sensitivity to epinephrine is suppressed in upper body obese women,” American Journal of Physiology, vol. 278, no. 6, pp. E1144–E1152, 2000. View at Google Scholar · View at Scopus
  43. K. J. Tracey, “The inflammatory reflex,” Nature, vol. 420, no. 6917, pp. 853–859, 2002. View at Google Scholar
  44. I. J. Elenkov, R. L. Wilder, G. P. Chrousos, and E. S. Vizi, “The sympathetic nerve—an integrative interface between two supersystems: the brain and the immune system,” Pharmacological Reviews, vol. 52, no. 4, pp. 595–638, 2000. View at Google Scholar · View at Scopus
  45. R. H. Straub, “Complexity of the bi-directional neuroimmune junction in the spleen,” Trends in Pharmacological Sciences, vol. 25, no. 12, pp. 640–646, 2004. View at Google Scholar
  46. M. A. Swanson, W. T. Lee, and V. M. Sanders, “IFNgamma production by Th1 cells generated from naive CD4+ T cells exposed to norepinephrine,” The Journal of Immunology, vol. 166, no. 1, pp. 232–240, 2001. View at Google Scholar
  47. V. M. Sanders, R. A. Baker, D. S. Ramer-Quinn, D. J. Kasprowicz, B. A. Fuchs, and N. E. Street, “Differential Expression of the β2-Adrenergic Receptor by Th1 and Th2 Clones Implications for Cytokine Production and B Cell Help,” Journal of Immunology, vol. 158, no. 9, pp. 4200–4210, 1997. View at Google Scholar · View at Scopus
  48. K. C. L. Torres, L. R. V. Antonelli, A. L. S. Souza, M. M. Teixeira, W. O. Dutra, and K. J. Gollob, “Norepinephrine, dopamine and dexamethasone modulate discrete leukocyte subpopulations and cytokine profiles from human PBMC,” Journal of Neuroimmunology, vol. 166, no. 1-2, pp. 144–157, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. Y. P. Peng, Y. H. Qiu, J. L. Jiang, and J. J. Wang, “Effect of catecholamines on IL-2 production and NK cytotoxicity of rats in vitro,” Acta Pharmacologica Sinica, vol. 25, no. 10, pp. 1354–1360, 2004. View at Google Scholar
  50. R. N. Spengler, R. M. Allen, D. G. Remick, R. M. Strieter, and S. L. Kunkel, “Stimulation of α-adrenergic receptor augments the production of macrophage-derived tumor necrosis factor,” Journal of Immunology, vol. 145, no. 5, pp. 1430–1434, 1990. View at Google Scholar · View at Scopus
  51. M. A. Flierl, D. Rittirsch, B. A. Nadeau et al., “Phagocyte-derived catecholamines enhance acute inflammatory injury,” Nature, vol. 449, no. 7163, pp. 721–725, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Marino, M. Cosentino, R. Bombelli, M. Ferrari, S. Lecchini, and G. Frigo, “Endogenous catecholamine synthesis, metabolism, storage, and uptake in human peripheral blood mononuclear cells,” Experimental Hematology, vol. 27, no. 3, pp. 489–495, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Lindström, A. Louheranta, M. Mannelin et al., “The Finnish Diabetes Prevention Study (DPS): lifestyle intervention and 3-year results on diet and physical activity,” Diabetes Care, vol. 26, no. 12, pp. 3230–3236, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Saito, M. Watanabe, J. Nishida et al., “Lifestyle modification and prevention of type 2 diabetes in overweight Japanese with impaired fasting glucose levels: a randomized controlled trial,” Archives of Internal Medicine, vol. 171, no. 15, pp. 1352–1360, 2011. View at Publisher · View at Google Scholar
  55. C. Kasapis and P. D. Thompson, “The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review,” Journal of the American College of Cardiology, vol. 45, no. 10, pp. 1563–1569, 2005. View at Google Scholar
  56. K. E. Fallon, S. K. Fallon, and T. Boston, “The acute phase response and exercise: court and field sports,” British Journal of Sports Medicine, vol. 35, no. 3, pp. 170–173, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Chen, G. F. Buchanan, J. M. Ding, J. Hannibal, and M. U. Gillette, “Pituitary adenylyl cyclase-activating peptide: a pivotal modulator of glutamatergic regulation of the suprachiasmatic circadian clock,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 23, pp. 13468–13473, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. U. N. Das, “Anti-inflammatory nature of exercise,” Nutrition, vol. 20, no. 3, pp. 323–326, 2004. View at Google Scholar
  59. A. M. Petersen and B. K. Pedersen, “The anti-inflammatory effect of exercise,” Journal of Applied Physiology, vol. 98, no. 4, pp. 1154–1162, 2005. View at Google Scholar
  60. R. Starkie, S. R. Ostrowski, S. Jauffred, M. Febbraio, and B. K. Pedersen, “Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans.,” The FASEB Journal, vol. 17, no. 8, pp. 884–886, 2003. View at Google Scholar · View at Scopus
  61. B. K. Pedersen and M. A. Febbraio, “Muscle as an endocrine organ: focus on muscle-derived interleukin-6,” Physiological Reviews, vol. 88, no. 4, pp. 1379–1406, 2008. View at Google Scholar
  62. E. Z. Fisman and A. Tenenbaum, “The ubiquitous interleukin-6: a time for reappraisal,” Cardiovascular Diabetology, vol. 9, article no. 62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. B. K. Pedersen, “IL-6 signalling in exercise and disease,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1295–1297, 2007. View at Google Scholar
  64. F. S. Lira, J. C. Rosa, N. E. Zanchi et al., “Regulation of inflammation in the adipose tissue in cancer cachexia: effect of exercise,” Cell Biochemistry and Function, vol. 27, no. 2, pp. 71–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. J. C. Rosa Neto, F. S. Lira, L. M. Oyama et al., “Exhaustive exercise causes an anti-inflammatory effect in skeletal muscle and a pro-inflammatory effect in adipose tissue in rats,” European Journal of Applied Physiology, vol. 106, no. 5, pp. 697–704, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. K. A. Martin, C. A. Ginis, Pelletier, D. S. Ditor, B. Foulon, and D. L. Wolfe, “The effects of exercise training on physical capacity, strength, body composition and functional performance among adults with spinal cord injury: a systematic review,” Spinal Cord, vol. 49, no. 11, pp. 1103–1127, 2011. View at Google Scholar
  67. A. E. Mendham, C. E. Donges, E. A. Liberts, and R. Duffield, “Effects of mode and intensity on the acute exercise-induced IL-6 and CRP responses in a sedentary, overweight population,” European Journal of Applied Physiology, vol. 111, no. 6, pp. 1035–1045, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. D. P. Andersson, P. Löfgren, A. Thorell, P. Arner, and J. Hoffstedt, “Visceral fat cell lipolysis and cardiovascular risk factors in obesity,” Hormone and Metabolic Research, vol. 43, no. 11, pp. 809–815, 2011. View at Google Scholar
  69. P. Vargovic, J. Ukropec, M. Laukova et al., “Adipocytes as a new source of catecholamine production,” FEBS Letters, vol. 585, no. 14, pp. 2279–2284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Mitsui, T. Nakamura, T. Ito et al., “Exercise significantly increases plasma adrenaline and oxidized low-density lipoprotein in normal healthy subjects but not in persons with spinal cord injury,” Archives of Physical Medicine and Rehabilitation, vol. 93, no. 4, pp. 725–727, 2012. View at Google Scholar