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Neural Plasticity
Volume 2015 (2015), Article ID 409625, 8 pages
http://dx.doi.org/10.1155/2015/409625
Review Article

Efficacy of Acute Intermittent Hypoxia on Physical Function and Health Status in Humans with Spinal Cord Injury: A Brief Review

1Department of Kinesiology, CSU San Marcos, San Marcos, CA 92096-0001, USA
2Neuro Ex, Oceanside, CA, USA

Received 28 February 2015; Revised 25 May 2015; Accepted 27 May 2015

Academic Editor: Naweed I. Syed

Copyright © 2015 Todd A. Astorino 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. Spinal Cord Injury Facts and Figures at a Glance, SCIMS/NDIRR, 2013, https://www.nscisc.uab.edu/.
  2. Centers for Disease Control, National Center for Injury Prevention and Control, 2008.
  3. M. J. Castro, D. F. Apple Jr., E. A. Hillegass, and G. A. Dudley, “Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury,” European Journal of Applied Physiology and Occupational Physiology, vol. 80, no. 4, pp. 373–378, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Dauty, B. Perrouin Verbe, Y. Maugars, C. Dubois, and J. F. Mathe, “Supralesional and sublesional bone mineral density in spinal cord-injured patients,” Bone, vol. 27, no. 2, pp. 305–309, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. M. S. Nash, “Exercise as a health-promoting activity following spinal cord injury,” Journal of Neurologic Physical Therapy, vol. 29, no. 2, pp. 87–106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. R. M. Crameri, A. Weston, M. Climstein, G. M. Davis, and J. R. Sutton, “Effects of electrical stimulation-induced leg training on skeletal muscle adaptability in spinal cord injury,” Scandinavian Journal of Medicine & Science in Sports, vol. 12, no. 5, pp. 316–322, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. D. H. Rintala, P. G. Loubser, J. Castro, K. A. Hart, and M. J. Fuhrer, “Chronic pain in a community-based sample of men with spinal cord injury: prevalence, severity, and relationship with impairment, disability, handicap, and subjective well-being,” Archives of Physical Medicine and Rehabilitation, vol. 79, no. 6, pp. 604–614, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Craig, K. N. Perry, R. Guest et al., “Prospective study of the occurrence of psychological disorders and comorbidities after spinal cord injury,” Archives of Physical Medicine and Rehabilitation, 2015. View at Publisher · View at Google Scholar
  9. 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
  10. M. Rosety-Rodriguez, A. Camacho, I. Rosety et al., “Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury,” Archives of Physical Medicine and Rehabilitation, vol. 95, no. 2, pp. 297–302, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Griffin, M. J. Decker, J. Y. Hwang et al., “Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury,” Journal of Electromyography and Kinesiology, vol. 19, no. 4, pp. 614–622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. S. Nash, P. L. Jacobs, A. J. Mendez, and R. B. Goldberg, “Circuit resistance training improves the atherogenic lipid profiles of persons with chronic paraplegia,” Journal of Spinal Cord Medicine, vol. 24, no. 1, pp. 2–9, 2001. View at Google Scholar · View at Scopus
  13. A. L. Behrman and S. J. Harkema, “Locomotor training after human spinal cord injury: a series of case studies,” Physical Therapy, vol. 80, no. 7, pp. 688–700, 2000. View at Google Scholar · View at Scopus
  14. E. Field-Fote, L. L. Ness, and M. Ionno, “Vibration elicits involuntary, step-like behavior in individuals with spinal cord injury,” Neurorehabilitation and Neural Repair, vol. 26, no. 7, pp. 861–869, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. E. T. Harness, N. Yozbatiran, and S. C. Cramer, “Effects of intense exercise in chronic spinal cord injury,” Spinal Cord, vol. 46, no. 11, pp. 733–737, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. T. A. Astorino, E. T. Harness, and K. A. Witzke, “Effect of chronic activity-based therapy on bone mineral density and bone turnover in persons with spinal cord injury,” European Journal of Applied Physiology, vol. 113, no. 12, pp. 3027–3037, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. T. A. Astorino, E. T. Harness, and K. A. Witzke, “Chronic activity-based therapy does not improve body composition, insulin-like growth factor-I, adiponectin, or myostatin in persons with spinal cord injury,” The Journal of Spinal Cord Medicine, 2014. View at Publisher · View at Google Scholar
  18. A. C. M. C. Buchholz, C. F. McGillivray, and P. B. Pencharz, “Physical activity levels are low in free-living adults with chronic paraplegia,” Obesity Research, vol. 11, no. 4, pp. 563–570, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. W. T. Phillips, B. J. Kiratli, M. Sarkarati et al., “Effect of spinal cord injury on the heart and cardiovascular fitness,” Current Problems in Cardiology, vol. 23, no. 11, pp. 641–716, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. H.-L. Dong, Y. Zhang, B.-X. Su et al., “Limb remote ischemic preconditioning protects the spinal cord from ischemia-reperfusion injury: a newly identified nonneuronal but reactive oxygen species-dependent pathway,” Anesthesiology, vol. 112, no. 4, pp. 881–891, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Dezfulian, M. Garrett, and N. R. Gonzalez, “Clinical application of preconditioning and postconditioning to achieve neuroprotection,” Translational Stroke Research, vol. 4, no. 1, pp. 19–24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Knaepen, M. Goekint, E. M. Heyman, and R. Meeusen, “Neuroplasticity—exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects,” Sports Medicine, vol. 40, no. 9, pp. 765–801, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Rojas Vega, T. Abel, R. Lindschulten, W. Hollmann, W. Bloch, and H. K. Strüder, “Impact of exercise on neuroplasticity-related proteins in spinal cord injured humans,” Neuroscience, vol. 153, no. 4, pp. 1064–1070, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. P. C. Maisonpierre, M. M. Le Beau, R. Espinosa III et al., “Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations,” Genomics, vol. 10, no. 3, pp. 558–568, 1991. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Niu and H. K. Yip, “Neuroprotective signaling mechanisms of telomerase are regulated by brain-derived neurotrophic factor in rat spinal cord motor neurons,” Journal of Neuropathology and Experimental Neurology, vol. 70, no. 7, pp. 634–652, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. A. F. Schinder, B. Berninger, and M.-M. Poo, “Postsynaptic target specificity of neurotrophin-induced presynaptic potentiation,” Neuron, vol. 25, no. 1, pp. 151–163, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. E. R. Buskirk, J. Kollias, R. F. Akers, E. K. Prokop, and E. P. Reategui, “Maximal performance at altitude and on return from altitude in conditioned runners,” Journal of Applied Physiology, vol. 23, no. 2, pp. 259–266, 1967. View at Google Scholar · View at Scopus
  28. H. Hoppeler, E. Kleiner, C. Schlegel et al., “Morphological adaptations of human skeletal muscle to chronic hypoxia,” International Journal of Sports Medicine, vol. 1, pp. S3–S9, 1990. View at Google Scholar
  29. H. Hoppeler and M. Vogt, “Muscle tissue adaptations to hypoxia,” The Journal of Experimental Biology, vol. 204, no. 18, pp. 3133–3139, 2001. View at Google Scholar · View at Scopus
  30. T. V. Serebrovskaya, “Intermittent hypoxia research in the former Soviet Union and the Commonwealth of Independent States: history and review of the concept and selected applications,” High Altitude Medicine & Biology, vol. 3, no. 2, pp. 205–221, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. E. A. Dale, F. Ben Mabrouk, and G. S. Mitchell, “Unexpected benefits of intermittent hypoxia: enhanced respiratory and nonrespiratory motor function,” Physiology, vol. 29, no. 1, pp. 39–48, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. F. L. Powell and N. Garcia, “Physiological effects of intermittent hypoxia,” High Altitude Medicine and Biology, vol. 1, no. 2, pp. 125–136, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. N. C. Netzer, R. Chytra, and T. Küpper, “Low intense physical exercise in normobaric hypoxia leads to more weight loss in obese people than low intense physical exercise in normobaric sham hypoxia,” Sleep and Breathing, vol. 12, no. 2, pp. 129–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Haufe, S. Wiesner, S. Engeli, F. C. Luft, and J. Jordan, “Influences of normobaric hypoxia training on metabolic risk markers in human subjects,” Medicine and Science in Sports and Exercise, vol. 40, no. 11, pp. 1939–1944, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. R. Lovett-Barr, I. Satriotomo, G. D. Muir et al., “Repetitive intermittent hypoxia induces respiratory and somatic motor recovery after chronic cervical spinal injury,” Journal of Neuroscience, vol. 32, no. 11, pp. 3591–3600, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. T. L. Baker-Herman, D. D. Fuller, R. W. Bavis et al., “BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia,” Nature Neuroscience, vol. 7, no. 1, pp. 48–55, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. D. V. Gutierrez, M. Clark, O. Nwanna, and W. J. Alilain, “Intermittent hypoxia training after C2 hemisection modifies the expression of PTEN and mTOR,” Experimental Neurology, vol. 248, pp. 45–52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Liu, Y. Lu, J. K. Lee et al., “PTEN deletion enhances the regenerative ability of adult corticospinal neurons,” Nature Neuroscience, vol. 13, no. 9, pp. 1075–1081, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. K. J. Christie, C. A. Webber, J. A. Martinez, B. Singh, and D. W. Zochodne, “PTEN inhibition to facilitate intrinsic regenerative outgrowth of adult peripheral axons,” The Journal of Neuroscience, vol. 30, no. 27, pp. 9306–9315, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. K. K. Park, K. Liu, Y. Hu, J. L. Kanter, and Z. He, “PTEN/mTOR and axon regeneration,” Experimental Neurology, vol. 223, no. 1, pp. 45–50, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Hay and N. Sonenberg, “Upstream and downstream of mTOR,” Genes and Development, vol. 18, no. 16, pp. 1926–1945, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. P. B. Jaiswal, N. J. Tester, and P. W. Davenport, “Effect of acute intermittent hypoxia treatment on ventilatory load compensation and magnitude estimation of inspiratory resistive loads in an individual with chronic incomplete cervical spinal cord injury,” The Journal of Spinal Cord Medicine, 2014. View at Publisher · View at Google Scholar
  43. R. D. Trumbower, A. Jayaraman, G. S. Mitchell, and W. Z. Rymer, “Exposure to acute intermittent hypoxia augments somatic motor function in humans with incomplete spinal cord injury,” Neurorehabilitation and Neural Repair, vol. 26, no. 2, pp. 163–172, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. H. B. Hayes, A. Jayaraman, M. Herrmann, G. S. Mitchell, W. Z. Rymer, and R. D. Trumbower, “Daily intermittent hypoxia enhances walking after chronic spinal cord injury: a randomized trial,” Neurology, vol. 82, no. 2, pp. 104–113, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Navarette-Opazo and G. S. Mitchell, “Therapeutic potential of intermittent hypoxia: a matter of dose,” American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, vol. 307, no. 10, pp. R1181–R1197, 2014. View at Publisher · View at Google Scholar
  46. K. Axen, “Ventilatory responses to mechanical loads in cervical cord-injured humans,” Journal of Applied Physiology: Respiratory Environmental and Exercise Physiology, vol. 52, no. 3, pp. 748–756, 1982. View at Google Scholar · View at Scopus
  47. C. Winslow and J. Rozovsky, “Effect of spinal cord injury on the respiratory system,” American Journal of Physical Medicine and Rehabilitation, vol. 82, no. 10, pp. 803–814, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. N. J. Tester, D. D. Fuller, J. S. Fromm, M. R. Spiess, A. L. Behrman, and J. H. Mateika, “Long-term facilitation of ventilation in humans with chronic spinal cord injury,” American Journal of Respiratory and Critical Care Medicine, vol. 189, no. 1, pp. 57–65, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. M. McGuire, Y. Zhang, D. P. White, and L. Ling, “Chronic intermittent hypoxia enhances ventilatory long-term facilitation in awake rats,” Journal of Applied Physiology, vol. 95, no. 4, pp. 1499–1508, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Gómez-Pinilla, Z. Ying, R. R. Roy, R. Molteni, and V. Reggie Edgerton, “Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity,” Journal of Neurophysiology, vol. 88, no. 5, pp. 2187–2195, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. S.-F. Tian, H.-H. Yang, D.-P. Xiao et al., “Mechanisms of neuroprotection from hypoxia-ischemia (HI) brain injury by up-regulation of cytoglobin (CYGB) in a neonatal rat model,” The Journal of Biological Chemistry, vol. 288, no. 22, pp. 15988–16003, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Zhong, Y. Zhang, Q.-Z. Fang, and Z.-N. Zhou, “Intermittent hypoxia exposure-induced heat-shock protein 70 expression increases resistance of rat heart to ischemic injury,” Acta Pharmacologica Sinica, vol. 21, no. 5, pp. 467–472, 2000. View at Google Scholar · View at Scopus
  53. T. Huang, W. Huang, Z. Zhang et al., “Hypoxia-inducible factor-1α upregulation in microglia following hypoxia protects against ischemia-induced cerebral infarction,” NeuroReport, vol. 25, no. 14, pp. 1122–1128, 2014. View at Publisher · View at Google Scholar
  54. G. Yuan, J. Nanduri, S. Khan, G. L. Semenza, and N. R. Prabhakar, “Induction of HIF-1α expression by intermittent hypoxia: involvement of NADPH oxidase, Ca2+ signaling, prolyl hydroxylases, and mTOR,” Journal of Cellular Physiology, vol. 217, no. 3, pp. 674–685, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. I. Satriotomo, E. A. Dale, J. M. Dahlberg, and G. S. Mitchell, “Repetitive acute intermittent hypoxia increases expression of proteins associated with plasticity in the phrenic motor nucleus,” Experimental Neurology, vol. 237, no. 1, pp. 103–115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Nair, V. Ramesh, R. C. Li, A. V. Schally, and D. Gozal, “Growth hormone releasing hormone (GHRH) signaling modulates intermittent hypoxia-induced oxidative stress and cognitive deficits in mouse,” Journal of Neurochemistry, vol. 127, no. 4, pp. 531–540, 2013. View at Publisher · View at Google Scholar · View at Scopus