Biomaterial-based interventions for neuronal regeneration and functional recovery in rodent model of spinal cord injury: A systematic review

Journal of Spinal Cord Medicine

Volumn 36, Issue 3, 2013, Pages 174-190

  Krishna, Vibhor ^a   Konakondla, Sanjay ^b   Nicholas, Joyce ^a   Varma, Abhay ^a   Kindy, Mark ^a   Wen, Xuejun ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b St George's University   (United States)

^c AMRL   (United States)

Author keywords

Axonal regeneration; Biomaterials; Functional recovery; Neuronal bridge; Spinal cord injuries; Translational research

Indexed keywords

BIOMATERIAL; BIOPOLYMER; BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR;

BIODEGRADABLE IMPLANT; CELL TRANSPLANTATION; CONTUSION; CONVALESCENCE; DATA BASE; HUMAN; MEDICAL RESEARCH; MEDLINE; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; PREDICTOR VARIABLE; REVIEW; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; STEM CELL; SURVIVAL TIME; SYSTEMATIC REVIEW; TREATMENT OUTCOME;

ANIMALS; BIOCOMPATIBLE MATERIALS; DISEASE MODELS, ANIMAL; NERVE REGENERATION; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84878227957     PISSN: 10790268     EISSN: 20457723     Source Type: Journal    
DOI: 10.1179/2045772313Y.0000000095     Document Type: Review

References (67)

1. Di Giovanni S. Regeneration following spinal cord injury, from experimental models to humans: where are we? Expert Opin Ther Targets 2006;10(3):363-76. Available from: Epub 2006 May 19.
2. Rossignol S, Schwab M, Schwartz M, Fehlings MG. Spinal cord injury: time to move? J Neurosci 2007;27(44):11782-92. Available from: Epub 2007 Nov. 6.
3. Assina R, Sankar T, Theodore N, Javedan SP, Gibson AR, Horn KM, et al. Activated autologous macrophage implantation in a large-animal model of spinal cord injury. Neurosurg Focus 2008;25(5):pE3. Available from: Epub 2008 Nov. 5.
4. Bouhy D, Malgrange B, Multon S, Poirrier AL, Scholtes F, Schoenen J, et al. Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J 2006;20(8):1239-41. Epub 2006 Apr. 26.
5. Horn KP, Busch SA, Hawthorne AL, Van Rooijen N, Silver J. Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J Neurosci 2008;28(38):9330-41. Epub 2008 Sep. 19.
6. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009;29(43):13435-44. Epub 2009 Oct. 30.
7. Zhang N, Yan H, Wen X. Tissue-engineering approaches for axonal guidance. Brain Res Brain Res Rev 2005;49(1):48-64. Epub 2005 Jun. 18.
8. Straley KS, Foo CW, Heilshorn SC. Biomaterial design strategies for the treatment of spinal cord injuries. J Neurotrauma 2010;27(1):1-19. Epub 2009 Aug. 25.
9. Fan J, Xiao Z, Zhang H, Chen B, Tang G, Hou X, et al. Linear ordered collagen scaffolds loaded with collagen-binding neurotrophin-3 promotes axonal regeneration and partial functional recovery after complete spinal cord transection. J Neurotrauma 2010;27(9):1671-83.
10. Gros T, Sakamoto JS, Blesch A, Havton LA, Tuszynski MH. Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. Biomaterials 2010;31(26):6719-29. Epub 2010 Jul. 14.
11. Guo JS, Zeng YS, Li HB, Huang WL, Liu RY, Li XB, et al. Cotransplant of neural stem cells and NT-3 gene modified Schwann cells promote the recovery of transected spinal cord injury. Spinal Cord 2007;45(1):15-24. Epub 2006 Jun. 15.
12. Han Q, Sun W, Lin H, Zhao W, Gao Y, Zhao Y, et al. Linear ordered collagen scaffolds loaded with collagen-binding brainderived neurotrophic factor improve the recovery of spinal cord injury in rats. Tissue Eng Part A 2009;15(10):2927-35. Epub 2009 Mar. 18.
13. Hatami M, Mehrjardi NZ, Kiani S, Hemmesi K, Azizi H, Shahverdi A, et al. Human embryonic stem cell-derived neural precursor transplants in collagen scaffolds promote recovery in injured rat spinal cord. Cytotherapy 2009;11(5):618-30. Available from: Epub 2009 Jun. 24.
14. Hurtado A, Moon LD, Maquet V, Blits B, Jerome R, Oudega M. 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 2006;27(3):430-42. Available from: Epub 2005 Aug. 17.
15. Itosaka H, Kuroda S, Shichinohe H, Yasuda H, Yano S, Kamei S, 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 2009;29(3):248-57. Available from: Epub 2008 Nov. 11.
16. Iwata A, Browne KD, Pfister BJ, Gruner JA, Smith DH. Longterm survival and outgrowth of mechanically engineered nervous tissue constructs implanted into spinal cord lesions. Tissue Eng 2006;12(1):101-10. Available from: Epub 2006 Feb. 28.
17. Johnson PJ, Parker SR, Sakiyama-Elbert SE. Controlled release of neurotrophin-3 from fibrin-based tissue engineering scaffolds enhances neural fiber sprouting following subacute spinal cord injury. Biotechnol Bioeng 2009;104(6):1207-14. Available from: Epub 2009 Jul. 16.
18. Joosten EA, Veldhuis WB, Hamers FP. Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury. J Neurosci Res 2004;77(1):127-42. Available from: Epub 2004 Jun. 16.
19. King VR, Henseler M, Brown RA, Priestley JV. Mats made from fibronectin support oriented growth of axons in the damaged spinal cord of the adult rat. Exp Neurol 2003;182(2):383-98. Available from: Epub 2003 Aug. 5.
20. Nomura H, Baladie B, Katayama Y, Morshead CM, Shoichet MS, Tator CH. Delayed implantation of intramedullary chitosan channels containing nerve grafts promotes extensive axonal regeneration after spinal cord injury. Neurosurgery 2008;63(1):127-41 [discussion 41-3]. Available from: Epub 2008 Aug. 30.
21. Nomura H, Zahir T, Kim H, Katayama Y, Kulbatski I, Morshead CM, 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 Eng Part A 2008;14(5):649-65. Available from: Epub 2008 Apr. 19.
22. Novikov LN, Novikova LN, Mosahebi A, Wiberg M, Terenghi G, Kellerth JO. A novel biodegradable implant for neuronal rescue and regeneration after spinal cord injury. Biomaterials 2002;23(16):3369-76. Available from: Epub 2002 Jul. 9.
23. Olson HE, Rooney GE, Gross L, Nesbitt JJ, Galvin KE, Knight A, et al. Neural stem cell-and Schwann cell-loaded biodegradable polymer scaffolds support axonal regeneration in the transected spinal cord. Tissue Eng Part A 2009;15(7):1797-805. Available from: Epub 2009 Feb. 5.
24. Oudega M, Gautier SE, Chapon P, Fragoso M, Bates ML, Parel JM, et al. Axonal regeneration into Schwann cell grafts within resorbable poly (alpha-hydroxyacid) guidance channels in the adult rat spinal cord. Biomaterials 2001;22(10):1125-36. Available from: Epub 2001 May 16.
25. Pan HC, Cheng FC, Lai SZ, Yang DY, Wang YC, Lee MS. Enhanced regeneration in spinal cord injury by concomitant treatment with granulocyte colony-stimulating factor and neuronal stem cells. J Clin Neurosci 2008;15(6):656-64. Available from: Epub 2008 Apr. 15.
26. Patist CM, Mulder MB, Gautier SE, Maquet V, Jerome R, Oudega M. Freeze-dried poly (D, L-lactic acid) macroporous guidance scaffolds impregnated with brain-derived neurotrophic factor in the transected adult rat thoracic spinal cord. Biomaterials 2004;25(9):1569-82. Available from: Epub 2003 Dec. 31.
27. Piantino J, Burdick JA, Goldberg D, Langer R, Benowitz LI. An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury. Exp Neurol 2006;201(2):359-67. Available from: Epub 2006 Jun. 13.
28. Rochkind S, Shahar A, Fliss D, El-Ani D, Astachov L, Hayon T, et al. Development of a tissue-engineered composite implant for treating traumatic paraplegia in rats. Eur Spine J 2006;15(2):234-45. Available from: Epub 2005 Nov. 18.
29. Stokols S, Sakamoto J, Breckon C, Holt T, Weiss J, Tuszynski MH. Templated agarose scaffolds support linear axonal regeneration. Tissue Eng 2006;12(10):2777-87. Available from: Epub 2007 May 24.
30. Teng YD, Lavik EB, Qu X, Park KI, Ourednik J, Zurakowski D, et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA 2002;99(5):3024-29. Available from: Epub 2002 Feb. 28.
31. Yarygin VN, Banin VV, Yarygin KN. Regeneration of the rat spinal cord after thoracic segmentectomy: restoration of the anatomical integrity of the spinal cord. Neurosci Behav Physiol 2006;36(5):483-90. Available from: Epub 2006 Apr. 29.
32. Zhang X, Zeng Y, Zhang W, Wang J, Wu J, Li J. Co-transplantation of neural stem cells and NT-3-overexpressing Schwann cells in transected spinal cord. J Neurotrauma 2007;24(12):1863-77. Available from: Epub 2007 Dec. 28.
33. Fehlings MG, Cadotte DW, Fehlings LN. A series of systematic reviews on the treatment of acute spinal cord injury: a foundation for best medical practice. J Neurotrauma 2011;28(8):1329-33. Available from: Epub 2011 Jun. 10.
34. Egger M S G, Altman DG. Systematic reviews in health care. 2nd ed. London, UK: BMJ Publishing Group; 2001.
35. Kwon BK, Okon E, Hillyer J, Mann C, Baptiste D, Weaver LC, et al. A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury. J Neurotrauma 2011;28(8):1545-88. Available from: Epub 2010 Feb. 12.
36. Tetzlaff W, Okon EB, Karimi-Abdolrezaee S, Hill CE, Sparling JS, Plemel JR, et al. A systematic review of cellular transplantation therapies for spinal cord injury. J Neurotrauma 2011;28(8):1611-82. Available from: Epub 2010 Feb. 12.
37. Kwon BK, Okon EB, Plunet W, Baptiste D, Fouad K, Hillyer J, et al. A systematic review of directly applied biologic therapies for acute spinal cord injury. J Neurotrauma 2011;28(8):1589-610. Available from: Epub 2010 Jan 20.
38. Kwon BK, Casha S, Hurlbert RJ, Yong VW. Inflammatory and structural biomarkers in acute traumatic spinal cord injury. Clin chem lab med: CCLM/FESCC 2011;49(3):425-33. Available from: Epub 2010 Dec. 24.
39. Gupta D, Tator CH, Shoichet MS. Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 2006;27(11):2370-79. Available from: Epub 2005 Dec. 6.
40. Basso DM. Behavioral testing after spinal cord injury: congruities, complexities, and controversies. J Neurotrauma 2004;21(4):395-404. Available from: Epub 2004 Apr. 30.
41. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12(1):1-21. Available from: Epub 1995 Feb. 1.
42. Basso DM, Beattie MS, Bresnahan JC. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 1996;139(2):244-56. Available from: Epub 1996 Jun. 1.
43. Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF. Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Quality of Reporting of Meta-analyses. Lancet 1999;354(9193):1896- 900. Available from: Epub 1999 Dec. 10.
44. Chen BK, Knight AM, De Ruiter GC, Spinner RJ, Yaszemski MJ, Currier BL, et al. Axon regeneration through scaffold into distal spinal cord after transection. J Neurotrauma 2009;26(10):1759-71. Available from: Epub 2009 May 6.
45. He L, Zhang Y, Zeng C, Ngiam M, Liao S, Quan D, et al. Manufacture of PLGA multiple-channel conduits with precise hierarchical pore architectures and in vitro/vivo evaluation for spinal cord injury. Tissue Eng Part C Methods 2009;15(2):243-55. Available from: Epub 2009 Feb. 7.
46. Johnson PJ, Tatara A, Shiu A, Sakiyama-Elbert SE. Controlled release of neurotrophin-3 and platelet-derived growth factor from fibrin scaffolds containing neural progenitor cells enhances survival and differentiation into neurons in a subacute model of SCI. Cell Transplant 2010;19(1):89-101. Available from: Epub 2009 Oct. 13.
47. Prang P, Muller R, Eljaouhari A, Heckmann K, Kunz W, Weber T, et al. The promotion of oriented axonal regrowth in the injured spinal cord by alginate-based anisotropic capillary hydrogels. Biomaterials 2006;27(19):3560-69. Available from: Epub 2006 Feb. 28.
48. Qian LM, Zhang ZJ, Gong AH, Qin RJ, Sun XL, Cao XD, et al. A novel biosynthetic hybrid scaffold seeded with olfactory ensheathing cells for treatment of spinal cord injuries. Chin Med J (Engl) 2009;122(17):2032-40. Available from: Epub 2009 Sep. 29.
49. Yang Y, De Laporte L, Rives CB, Jang JH, Lin WC, Shull KR, et al. Neurotrophin releasing single and multiple lumen nerve conduits. J Control Release 2005;104(3):433-46. Available from: Epub 2005 May 25.
50. Zahir T, Nomura H, Guo XD, Kim H, Tator C, Morshead C, et al. Bioengineering neural stem/progenitor cell-coated tubes for spinal cord injury repair. Cell Transplant 2008;17(3):245-54. Available from: Epub 2008 Jun. 5.
51. Chau CH, Shum DK, Li H, Pei J, Lui YY, Wirthlin L, et al. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 2004;18(1):194-6. Available from: Epub 2003 Nov. 25.
52. Friedman JA, Lewellyn EB, Moore MJ, Schermerhorn TC, Knight AM, Currier BL, et al. Synthes award for resident research in spinal cord & spinal column injury: surgical repair of the injured spinal cord using biodegradable polymer implants to facilitate axon regeneration. Clin Neurosurg 2004;51:314-9. Available from: Epub 2004 Dec. 2.
53. Taylor SJ, McDonald JW, 3rd, Sakiyama-Elbert SE. Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury. J Control Release 2004;98(2):281-94. Epub 2004 July 21.
54. Taylor SJ, Rosenzweig ES, McDonald JW, 3rd, Sakiyama-Elbert SE. Delivery of neurotrophin-3 from fibrin enhances neuronal fiber sprouting after spinal cord injury. J Control Release 2006;113(3):226-35. Epub 2006 June 27.
55. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 25(5):1169-78. Epub 2005 Feb. 4.
56. Houle JD, Ziegler MK. Bridging a complete transection lesion of adult rat spinal cord with growth factor-treated nitrocellulose implants. J Neural Transplant Plast 1994;5(2):115-24. Epub 1994 Apr. 1.
57. Meijs MF, Timmers L, Pearse DD, Tresco PA, Bates ML, Joosten EA, et al. Basic fibroblast growth factor promotes neuronal survival but not behavioral recovery in the transected and Schwann cell implanted rat thoracic spinal cord. J Neurotrauma 2004;21(10):1415-30. Epub 2005 Jan 288.
58. Park J, Lim E, Back S, Na H, Park Y, Sun K. Nerve regeneration following spinal cord injury using matrix metalloproteinase-sensitive, hyaluronic acid-based biomimetic hydrogel scaffold containing brain-derived neurotrophic factor. J Biomed Mater Res A 2010;93(3):1091-99. Epub 2009 Sep. 22.
59. Rochkind S, Shahar A, Amon M, Nevo Z. Transplantation of embryonal spinal cord nerve cells cultured on biodegradable microcarriers followed by low power laser irradiation for the treatment of traumatic paraplegia in rats. Neurol Res 2002;24(4):355-60. Epub 2002 Jun. 19.
60. Wang YC, Wu YT, Huang HY, Lin HI, Lo LW, Tzeng SF, et al. Sustained intraspinal delivery of neurotrophic factor encapsulated in biodegradable nanoparticles following contusive spinal cord injury. Biomaterials 2008;29(34):4546-53. Epub 2008 Sep. 9.
61. Guest J, Benavides F, Padgett K, Mendez E, Tovar D. Technical aspects of spinal cord injections for cell transplantation. Clinical and translational considerations. Brain Res Bull 2011;84(4/5):267-79. Epub 2010/Nov. 20.
62. Norenberg MD, Smith J, Marcillo A. The pathology of human spinal cord injury: defining the problems. J Neurotrauma 2004;21(4):429-40. Epub 2004 Apr. 30.
63. Madigan NN, McMahon S, O'Brien T, Yaszemski MJ, Windebank AJ. Current tissue engineering and novel therapeutic approaches to axonal regeneration following spinal cord injury using polymer scaffolds. Respir Physiol Neurobiol 2009;169(2):183-99. Epub 2009 Sep. 10.
64. Kwon BK, Okon EB, Tsai E, Beattie MS, Bresnahan JC, Magnuson DK, et al. A grading system to evaluate objectively the strength of pre-clinical data of acute neuroprotective therapies for clinical translation in spinal cord injury. J Neurotrauma 2011;28(8):1525-43. Epub 2010 May 29.
65. Teward O, Opovich PG, Ietrich WD, Leitman N. Replication and reproducibility in spinal cord injury research. Exp Neurol 2012;233(2):597-605. Epub 2011 Nov. 15.
66. Metz GA, Merkler D, Dietz V, Schwab ME, Fouad K. Efficient testing of motor function in spinal cord injured rats. Brain Res 2000;883(2):165-77. Epub 2000 Nov. 14.
67. Harvey LA, Lin CW, Glinsky JV, De Wolf A. The effectiveness of physical interventions for people with spinal cord injuries: a systematic review. Spinal Cord 2009;47(3):184-95. Epub 2008 Aug. 30.