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Stem Cells International
Volume 2017, Article ID 5160261, 12 pages
https://doi.org/10.1155/2017/5160261
Review Article

Functional Test Scales for Evaluating Cell-Based Therapies in Animal Models of Spinal Cord Injury

Department of Biomedical Sciences, Korea University College of Medicine, Seoul 136-705, Republic of Korea

Correspondence should be addressed to Woon Ryoung Kim; rk.ca.aerok@mikrw and Dongho Geum; rk.ca.aerok@dmueg

Received 5 April 2017; Revised 28 June 2017; Accepted 1 August 2017; Published 4 October 2017

Academic Editor: Ivan Velasco

Copyright © 2017 Woon Ryoung Kim 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. A. Ackery, C. Tator, and A. Krassioukov, “A global perspective on spinal cord injury epidemiology,” Journal of Neurotrauma, vol. 21, no. 10, pp. 1355–1370, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Singh, L. Tetreault, S. Kalsi-Ryan, A. Nouri, and M. G. Fehlings, “Global prevalence and incidence of traumatic spinal cord injury,” Clinical Epidemiology, vol. 6, pp. 309–331, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Thuret, L. D. Moon, and F. H. Gage, “Therapeutic interventions after spinal cord injury,” Nature Reviews Neuroscience, vol. 7, no. 8, pp. 628–643, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Assinck, G. J. Duncan, B. J. Hilton, J. R. Plemel, and W. Tetzlaff, “Cell transplantation therapy for spinal cord injury,” Nature Neuroscience, vol. 20, no. 5, pp. 637–647, 2017. View at Publisher · View at Google Scholar
  5. S. I. Hodgetts, M. Edel, and A. R. Harvey, “The state of play with iPSCs and spinal cord injury models,” Journal of Clinical Medicine, vol. 4, no. 1, pp. 193–203, 2015. View at Publisher · View at Google Scholar
  6. B. G. McMahill, D. L. Borjesson, M. Sieber-Blum, J. A. Nolta, and B. K. Sturges, “Stem cells in canine spinal cord injury--promise for regenerative therapy in a large animal model of human disease,” Stem Cell Reviews, vol. 11, no. 1, pp. 180–193, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Cheriyan, D. J. Ryan, J. H. Weinreb et al., “Spinal cord injury models: a review,” Spinal Cord, vol. 52, no. 8, pp. 588–595, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. D. M. Basso, L. C. Fisher, A. J. Anderson, L. B. Jakeman, D. M. McTigue, and P. G. Popovich, “Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains,” Journal of Neurotrauma, vol. 23, no. 5, pp. 635–659, 2006. View at Publisher · View at Google Scholar
  9. A. Denic, A. J. Johnson, A. J. Bieber, A. E. Warrington, M. Rodriguez, and I. Pirko, “The relevance of animal models in multiple sclerosis research,” Pathophysiology, vol. 18, no. 1, pp. 21–29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. G. C. Koopmans, R. Deumens, W. M. Honig, F. P. Hamers, H. W. Steinbusch, and E. A. Joosten, “The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination,” Journal of Neurotrauma, vol. 22, no. 2, pp. 214–225, 2005. View at Publisher · View at Google Scholar
  11. D. M. Basso, M. S. Beattie, and J. C. Bresnahan, “A sensitive and reliable locomotor rating scale for open field testing in rats,” Journal of Neurotrauma, vol. 12, no. 1, pp. 1–21, 1995. View at Publisher · View at Google Scholar
  12. J. A. Gruner, “A monitored contusion model of spinal cord injury in the rat,” Journal of Neurotrauma, vol. 9, no. 2, pp. 123–128, 1992. View at Publisher · View at Google Scholar
  13. J. C. Gensel, C. A. Tovar, F. P. Hamers, R. J. Deibert, M. S. Beattie, and J. C. Bresnahan, “Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats,” Journal of Neurotrauma, vol. 23, no. 1, pp. 36–54, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Liu, L. T. Chi, Z. Q. Tu, B. Sheng, Z. K. Zhou, and F. X. Pei, “Observation and establishment of an animal model of tractive spinal cord injury in rats,” Chinese Journal of Traumatology, vol. 7, no. 6, pp. 372–377, 2004. View at Google Scholar
  15. Y. P. Zhang, C. Iannotti, L. B. Shields et al., “Dural closure, cord approximation, and clot removal: enhancement of tissue sparing in a novel laceration spinal cord injury model,” Journal of Neurosurgery, vol. 100, Supplement Spine, no. 4, pp. 343–352, 2004. View at Publisher · View at Google Scholar
  16. R. F. Heimburger, “Return of function after spinal cord transection,” Spinal Cord, vol. 43, no. 7, pp. 438–440, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. L. W. Freeman, “Return of function after complete transection of the spinal cord of the rat, cat and dog,” Annals of Surgery, vol. 136, no. 2, pp. 193–205, 1952. View at Publisher · View at Google Scholar
  18. M. Hatami, N. Z. Mehrjardi, S. Kiani et al., “Human embryonic stem cell-derived neural precursor transplants in collagen scaffolds promote recovery in injured rat spinal cord,” Cytotherapy, vol. 11, no. 5, pp. 618–630, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Itosaka, S. Kuroda, H. Shichinohe et al., “Fibrin matrix provides a suitable scaffold for bone marrow stromal cells transplanted into injured spinal cord: a novel material for CNS tissue engineering,” Neuropathology, vol. 29, no. 3, pp. 248–257, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. X. Li, Z. Yang, A. Zhang, T. Wang, and W. Chen, “Repair of thoracic spinal cord injury by chitosan tube implantation in adult rats,” Biomaterials, vol. 30, no. 6, pp. 1121–1132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. B. D. Watson, R. Prado, W. D. Dietrich, M. D. Ginsberg, and B. A. Green, “Photochemically induced spinal cord injury in the rat,” Brain Research, vol. 367, no. 1-2, pp. 296–300, 1986. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Gaviria, H. Haton, F. Sandillon, and A. Privat, “A mouse model of acute ischemic spinal cord injury,” Journal of Neurotrauma, vol. 19, no. 2, pp. 205–221, 2002. View at Publisher · View at Google Scholar
  23. J. X. Hao, X. J. Xu, H. Aldskogius, A. Seiger, and Z. Wiesenfeld-Hallin, “Allodynia-like effects in rat after ischaemic spinal cord injury photochemically induced by laser irradiation,” Pain, vol. 45, no. 2, pp. 175–185, 1991. View at Publisher · View at Google Scholar
  24. I. K. Toumpoulis, C. E. Anagnostopoulos, G. E. Drossos, V. D. Malamou-Mitsi, L. S. Pappa, and D. G. Katritsis, “Does ischemic preconditioning reduce spinal cord injury because of descending thoracic aortic occlusion?” Journal of Vascular Surgery, vol. 37, no. 2, pp. 426–432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. R. P. Yezierski, S. Liu, G. L. Ruenes, K. J. Kajander, and K. L. Brewer, “Excitotoxic spinal cord injury: behavioral and morphological characteristics of a central pain model,” Pain, vol. 75, no. 1, pp. 141–155, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Das Sarma, “A mechanism of virus-induced demyelination,” Interdisciplinary Perspectives on Infectious Diseases, vol. 2010, Article ID 109239, 28 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. E. Ropper, D. K. Thakor, I. Han et al., “Defining recovery neurobiology of injured spinal cord by synthetic matrix-assisted hMSC implantation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 5, pp. E820–E829, 2017. View at Publisher · View at Google Scholar
  28. S. Karimi-Abdolrezaee, E. Eftekharpour, J. Wang, C. M. Morshead, and M. G. Fehlings, “Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury,” The Journal of Neuroscience, vol. 26, no. 13, pp. 3377–3389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. D. Teng, E. B. Lavik, X. Qu et al., “Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 5, pp. 3024–3029, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. B. L. Du, Y. Xiong, C. G. Zeng et al., “Transplantation of artificial neural construct partly improved spinal tissue repair and functional recovery in rats with spinal cord transection,” Brain Research, vol. 1400, pp. 87–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. C. D. Pritchard, J. R. Slotkin, D. Yu et al., “Establishing a model spinal cord injury in the African green monkey for the preclinical evaluation of biodegradable polymer scaffolds seeded with human neural stem cells,” Journal of Neuroscience Methods, vol. 188, no. 2, pp. 258–269, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Bozkurt, A. J. Mothe, T. Zahir, H. Kim, M. S. Shoichet, and C. H. Tator, “Chitosan channels containing spinal cord-derived stem/progenitor cells for repair of subacute spinal cord injury in the rat,” Neurosurgery, vol. 67, no. 6, pp. 1733–1744, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Hejcl, J. Sedy, M. Kapcalova et al., “HPMA-RGD hydrogels seeded with mesenchymal stem cells improve functional outcome in chronic spinal cord injury,” Stem Cells and Development, vol. 19, no. 10, pp. 1535–1546, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. K. N. Kang, J. Y. Lee, D. Y. Kim et al., “Regeneration of completely transected spinal cord using scaffold of poly(D,L-lactide-co-glycolide)/small intestinal submucosa seeded with rat bone marrow stem cells,” Tissue Engineering Part A, vol. 17, no. 17-18, pp. 2143–2152, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Lu, G. Woodruff, Y. Wang et al., “Long-distance axonal growth from human induced pluripotent stem cells after spinal cord injury,” Neuron, vol. 83, no. 4, pp. 789–796, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Nomura, T. Zahir, H. Kim et al., “Extramedullary chitosan channels promote survival of transplanted neural stem and progenitor cells and create a tissue bridge after complete spinal cord transection,” Tissue Engineering Part A, vol. 14, no. 5, pp. 649–665, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. P. J. Johnson, A. Tatara, D. A. McCreedy, A. Shiu, and S. E. Sakiyama-Elbert, “Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI,” Soft Matter, vol. 6, no. 20, pp. 5127–5137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Kobayashi, Y. Okada, G. Itakura et al., “Pre-evaluated safe human iPSC-derived neural stem cells promote functional recovery after spinal cord injury in common marmoset without tumorigenicity,” PLoS One, vol. 7, no. 12, article e52787, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. E. Nutt, E. A. Chang, S. T. Suhr et al., “Caudalized human iPSC-derived neural progenitor cells produce neurons and glia but fail to restore function in an early chronic spinal cord injury model,” Experimental Neurology, vol. 248, pp. 491–503, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Montgomery, A. Wong, N. Gabers, and S. M. Willerth, “Engineering personalized neural tissue by combining induced pluripotent stem cells with fibrin scaffolds,” Biomaterials Science, vol. 3, no. 2, pp. 401–413, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Saadai, A. Wang, Y. S. Nout et al., “Human induced pluripotent stem cell-derived neural crest stem cells integrate into the injured spinal cord in the fetal lamb model of myelomeningocele,” Journal of Pediatric Surgery, vol. 48, no. 1, pp. 158–163, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Ma, X. Li, B. Yi et al., “Transplanted iNSCs migrate through SDF-1/CXCR4 signaling to promote neural recovery in a rat model of spinal cord injury,” Neuroreport, vol. 25, no. 6, pp. 391–397, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Y. Hong, S. H. Lee, S. C. Lee et al., “Therapeutic potential of induced neural stem cells for spinal cord injury,” The Journal of Biological Chemistry, vol. 289, no. 47, pp. 32512–32525, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Liu, Y. Huang, M. Pang et al., “Tissue-engineered regeneration of completely transected spinal cord using induced neural stem cells and gelatin-electrospun poly (lactide-co-glycolide)/polyethylene glycol scaffolds,” PLoS One, vol. 10, no. 3, article e0117709, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Hurtado, L. D. Moon, V. Maquet, B. Blits, R. Jerome, and M. Oudega, “Poly (D,L-lactic acid) macroporous guidance scaffolds seeded with Schwann cells genetically modified to secrete a bi-functional neurotrophin implanted in the completely transected adult rat thoracic spinal cord,” Biomaterials, vol. 27, no. 3, pp. 430–442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. H. E. Olson, G. E. Rooney, L. Gross et al., “Neural stem cell- and Schwann cell-loaded biodegradable polymer scaffolds support axonal regeneration in the transected spinal cord,” Tissue Engineering Part A, vol. 15, no. 7, pp. 1797–1805, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Wang, Y. S. Zeng, J. L. Wu, Y. Li, and Y. D. Teng, “Cograft of neural stem cells and Schwann cells overexpressing TrkC and neurotrophin-3 respectively after rat spinal cord transection,” Biomaterials, vol. 32, no. 30, pp. 7454–7468, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. E. A. Joosten, W. B. Veldhuis, and F. P. Hamers, “Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury,” Journal of Neuroscience Research, vol. 77, no. 1, pp. 127–142, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Rochkind, A. Shahar, D. Fliss et al., “Development of a tissue-engineered composite implant for treating traumatic paraplegia in rats,” European Spine Journal, vol. 15, no. 2, pp. 234–245, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Zhang, X. Lu, G. Feng et al., “Chitosan scaffolds induce human dental pulp stem cells to neural differentiation: potential roles for spinal cord injury therapy,” Cell and Tissue Research, vol. 366, no. 1, pp. 129–142, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Shrestha, K. Coykendall, Y. Li, A. Moon, P. Priyadarshani, and L. Yao, “Repair of injured spinal cord using biomaterial scaffolds and stem cells,” Stem Cell Research & Therapy, vol. 5, no. 4, p. 91, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. C. Gensel, D. J. Donnelly, and P. G. Popovich, “Spinal cord injury therapies in humans: an overview of current clinical trials and their potential effects on intrinsic CNS macrophages,” Expert Opinion on Therapeutic Targets, vol. 15, no. 4, pp. 505–518, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. R. R. Smith, D. A. Burke, A. D. Baldini et al., “The Louisville swim scale: a novel assessment of hindlimb function following spinal cord injury in adult rats,” Journal of Neurotrauma, vol. 23, no. 11, pp. 1654–1670, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. M. D. Schechter and W. T. Chance, “Non-specificity of “behavioral despair” as an animal model of depression,” European Journal of Pharmacology, vol. 60, no. 2-3, pp. 139–142, 1979. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Gale, H. Kerasidis, and J. R. Wrathall, “Spinal cord contusion in the rat: behavioral analysis of functional neurologic impairment,” Experimental Neurology, vol. 88, no. 1, pp. 123–134, 1985. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Martinez, J. M. Brezun, L. Bonnier, and C. Xerri, “A new rating scale for open-field evaluation of behavioral recovery after cervical spinal cord injury in rats,” Journal of Neurotrauma, vol. 26, no. 7, pp. 1043–1053, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. J. Lankhorst, M. P. ter Laak, T. J. van Laar et al., “Effects of enriched housing on functional recovery after spinal cord contusive injury in the adult rat,” Journal of Neurotrauma, vol. 18, no. 2, pp. 203–215, 2001. View at Publisher · View at Google Scholar
  58. F. P. Hamers, A. J. Lankhorst, T. J. van Laar, W. B. Veldhuis, and W. H. Gispen, “Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries,” Journal of Neurotrauma, vol. 18, no. 2, pp. 187–201, 2001. View at Publisher · View at Google Scholar
  59. D. A. Houweling, A. J. Lankhorst, W. H. Gispen, P. R. Bar, and E. A. Joosten, “Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery,” Experimental Neurology, vol. 153, no. 1, pp. 49–59, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. A. S. Rivlin and C. H. Tator, “Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat,” Surgical Neurology, vol. 10, no. 1, pp. 38–43, 1978. View at Google Scholar
  61. R. Suresh Babu, R. Muthusamy, and A. Namasivayam, “Behavioural assessment of functional recovery after spinal cord hemisection in the bonnet monkey (Macaca radiata),” Journal of the Neurological Sciences, vol. 178, no. 2, pp. 136–152, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. S. Nout, A. R. Ferguson, S. C. Strand et al., “Methods for functional assessment after C7 spinal cord hemisection in the rhesus monkey,” Neurorehabilitation and Neural Repair, vol. 26, no. 6, pp. 556–569, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. S. H. Lee, Y. N. Chung, Y. H. Kim et al., “Effects of human neural stem cell transplantation in canine spinal cord hemisection,” Neurological Research, vol. 31, no. 9, pp. 996–1002, 2009. View at Publisher · View at Google Scholar
  64. N. J. Olby, L. D. Risio, K. R. Munana et al., “Development of a functional scoring system in dogs with acute spinal cord injuries,” American Journal of Veterinary Research, vol. 62, no. 10, pp. 1624–1628, 2001. View at Publisher · View at Google Scholar
  65. I. M. Tarlov, H. Klinger, and S. Vitale, “Spinal cord compression studies. I. Experimental techniques to produce acute and gradual compression,” A.M.A. Archives of Neurology and Psychiatry, vol. 70, no. 6, pp. 813–819, 1953. View at Google Scholar
  66. N. J. Olby, J. H. Lim, K. Babb et al., “Gait scoring in dogs with thoracolumbar spinal cord injuries when walking on a treadmill,” BMC Veterinary Research, vol. 10, p. 58, 2014. View at Publisher · View at Google Scholar · View at Scopus