Meta analysis of olfactory ensheathing cell transplantation promoting functional recovery of motor nerves in rats with complete spinal cord transection

Neural Regeneration Research

Volumn 9, Issue 20, 2014, Pages 1850-1858

  Liu, Jun ^a   Chen, Ping ^b   Wang, Qi ^a   Chen, Yu ^a   Yu, Hai Long ^a   Ma, Jun Xiong ^a   Guo, Ming Ming ^a   Piao, Mei Hui ^a   Ren, Wei Jian ^a   Xiang, Liang Bi ^a  

^a GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

^b TAIAN CENTRAL HOSPITAL   (China)

Author keywords

BBB scores; Cell transplantation; Complete transection; Meta analysis; Nerve regeneration; Olfactory ensheathing cells; Spinal cord injury

Indexed keywords

ARTICLE; BASSO, BEATTIE AND BRESNAHAN SCORE; CELL TRANSPLANTATION; DATA ANALYSIS; DATA EXTRACTION; HINDLIMB; HUMAN; META ANALYSIS; MOTOR NERVE; NERVE FUNCTION; NERVE REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL TRANSPLANTATION; PUBLICATION; QUALITY CONTROL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RAT; SCORING SYSTEM; SENSITIVITY ANALYSIS; SPINAL CORD TRANSSECTION;

EID: 84908615156     PISSN: 16735374     EISSN: 18767958     Source Type: Journal    
DOI: 10.4103/1673-5374.143434     Document Type: Article

References (87)

1. Aoki M, Kishima H, Yoshimura K, Ishihara M, Ueno M, Hata K, Yamashita T, Iwatsuki K, Yoshimine T (2010) Limited functional recovery in rats with complete spinal cord injury after transplantation of whole-layer olfactory mucosa. J Neurosurg Spine 12:122-130.
2. Au E, Roskams AJ (2003) Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41:224-236.
3. Bakshi A, Fisher O, Dagci T, Himes BT, Fischer I, Lowman A (2004) Mechanically engineered hydrogel scaffolds for axonal growth and angiogenesis after transplantation in spinal cord injury. J Neurosurg Spine 1:322-329.
4. Barnett SC, Alexander CL, Iwashita Y, Gilson JM, Crowther J, Clark L, Dunn LT, Papanastassiou V, Kennedy PG, Franklin RJ (2000) Identification of a human olfactory ensheathing cell that can effect transplant- mediated remyelination of demyelinated CNS axons. Brain 123:1581-1588.
5. Basso DM, Beattie MS, Bresnahan JC (1996) Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256.
6. Bazley FA, Hu C, Maybhate A, Pourmorteza A, Pashai N, Thakor NV, Kerr CL, All AH (2012) Electrophysiological evaluation of sensory and motor pathways after incomplete unilateral spinal cord contusion. J Neurosurg Spine 16:414-423.
7. Blits B, Boer GJ, Verhaagen J (2002) Pharmacological, cell, and gene therapy strategies to promote spinal cord regeneration. Cell Transplant 11:593-613.
8. Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, Fulga V, Yoles E (2003) Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J Neuroimmunol 142:10- 16.
9. Boyd JG, Doucette R, Kawaja MD (2005) Defining the role of olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. FASEB J 19:694-703.
10. Cao L, Liu L, Chen ZY, Wang LM, Ye JL, Qiu HY, Lu CL, He C (2004) Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127:535-549.
11. Centenaro LA, Jaeger MdC, Ilha J, de Souza MA, Kalil-Gaspar PI, Cunha NB, Marcuzzo S, Achaval M (2011) Olfactory and respiratory lamina propria transplantation after spinal cord transection in rats: Effects on functional recovery and axonal regeneration. Brain Res 1426:54-72.
12. Chau CH, Shum DK, Li H, Pei J, Lui YY, Wirthlin L, Chan YS, Xu XM (2003) Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 18:194-196.
13. Cheng H, Cao Y, Olson L (1996) Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273:510-513.
14. Chuah MI, Hale DM, West AK (2011) Interaction of olfactory ensheathing cells with other cell types in vitro and after transplantation: glial scars and inflammation. Exp Neurol 229:46-53.
15. Chuah MI, Choi-Lundberg D, Weston S, Vincent AJ, Chung RS, Vickers JC, West AK (2004) Olfactory ensheathing cells promote collateral axonal branching in the injured adult rat spinal cord. Exp Neurol 185:15-25.
16. David S, Aguayo AJ (1981) Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science 214:931-933.
17. Demjen D, Klussmann S, Kleber S, Zuliani C, Stieltjes B, Metzger C, Hirt UA, Walczak H, Falk W, Essig M, Edler L, Krammer PH, Martin-Villalba A (2004) Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat Med 10:389-395.
18. Dobkin BH, Harkema S, Requejo P, Edgerton VR (1995) Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J Neurol Rehabil 9:183-190.
19. Dolbeare D, Houle JD (2003) Restriction of axonal retraction and promotion of axonal regeneration by chronically injured neurons after intraspinal treatment with glial cell line-derived neurotrophic factor (GDNF). J Neurotrauma 20:1251-1261.
20. Doucette JR (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 210:385-391.
21. Fan J, Zhang H, He J, Xiao Z, Chen B, Xiaodan J, Dai J, Xu R (2011) Neural regrowth induced by PLGA nerve conduits and neurotrophin- 3 in rats with complete spinal cord transection. J Biomed Mater Res B Appl Biomater 97:271-277.
22. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD (2005) Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 25:1169-1178.
23. Garcia-Alias G, Verdu E, Fores J, Lopez-Vales R, Navarro X (2003) Functional and electrophysiological characterization of photochemical graded spinal cord injury in the rat. J Neurotrauma 20:501-510.
24. Iannotti C, Li H, Yan P, Lu X, Wirthlin L, Xu XM (2003) Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp Neurol 183:379-393.
25. Imaizumi T, Lankford KL, Waxman SG, Greer CA, Kocsis JD (1998) Transplanted olfactory ensheathing cells remyelinate and enhance axonal conduction in the demyelinated dorsal columns of the rat spinal cord. J Neurosci 18:6176-6185.
26. Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, Kobayashi S, Yamasaki M, Momoshima S, Ishii H, Ando K, Tanioka Y, Tamaoki N, Nomura T, Toyama Y, Okano H (2005) Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 80:182-190.
27. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJM, Gavaghan DJ, McQuay HJ (1996) Assessing the quality of reports of randomized clinical trials: Is blinding necessary? Control Clin Trials 17:1-12.
28. Jiang B, Shen YX, Wang PJ, Lu ZF, Fan ZH (2010) Repairing effect of OECs transplantation for spinal cord injury. Suzhou Daxue Xuebao: Yixue Ban 30:34-37.
29. Jones LL, Oudega M, Bunge MB, Tuszynski MH (2001) Neurotrophic factors, cellular bridges and gene therapy for spinal cord injury. J Physiol 533:83-89.
30. Kamada T, Koda M, Dezawa M, Yoshinaga K, Hashimoto M, Koshizuka S, Nishio Y, Moriya H, Yamazaki M (2005) Transplantation of bone marrow stromal cell-derived Schwann cells promotes axonal regeneration and functional recovery after complete transection of adult rat spinal cord. J Neuropathol Exp Neurol 64:37-45.
31. Kang KN, Lee JY, Kim da Y, Lee BN, Ahn HH, Lee B, Khang G, Park SR, Min BH, Kim JH, Lee HB, Kim MS (2011) Regeneration of completely transected spinal cord using scaffold of poly(D,L-lactide-coglycolide)/ small intestinal submucosa seeded with rat bone marrow stem cells. Tissue Eng Part A 17:2143-2152.
32. Kato T, Honmou O, Uede T, Hashi K, Kocsis JD (2000) Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 30:209-218.
33. Kawaguchi S, Iseda T, Nishio T (2004) Effects of an embryonic repair graft on recovery from spinal cord injury. Prog Brain Res 143:155-162.
34. King-Robson J (2011) Encouraging regeneration in the central nervous system: is there a role for olfactory ensheathing cells? Neurosci Res 69:263-275.
35. Kubasak MD, Jindrich DL, Zhong H, Takeoka A, McFarland KC, Munoz-Quiles C, Roy RR, Edgerton VR, Ramon-Cueto A, Phelps PE (2008) OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 131:264-276.
36. Kunkel-Bagden E, Bregman BS (1990) Spinal cord transplants enhance the recovery of locomotor function after spinal cord injury at birth. Exp Brain Res 81:25-34.
37. Kwon BK, Borisoff JF, Tetzlaff W (2002) Molecular targets for therapeutic intervention after spinal cord injury. Mol Interv 2:244-258.
38. Lopez-Vales R, Fores J, Verdu E, Navarro X (2006) Acute and delayed transplantation of olfactory ensheathing cells promote partial recovery after complete transection of the spinal cord. Neurobiol Dis 21:57-68.
39. Lopez-Vales R, Fores J, Navarro X, Verdu E (2007) Chronic transplantation of olfactory ensheathing cells promotes partial recovery after complete spinal cord transection in the rat. Glia 55:303-311.
40. Lee MJ, Chen CJ, Cheng CH, Huang WC, Kuo HS, Wu JC, Tsai MJ, Huang MC, Chang WC, Cheng H (2008) Combined treatment using peripheral nerve graft and FGF-1: Changes to the glial environment and differential macrophage reaction in a complete transected spinal cord. Neurosci Lett 433:163-169.
41. Li BC, Li Y, Chen LF, Chang JY, Duan ZX (2011) Olfactory ensheathing cells can reduce the tissue loss but not the cavity formation in contused spinal cord of rats. J Neurol Sci 303:67-74.
42. Li XF, Dai LY (2009) Three-dimensional finite element model of the cervical spinal cord: preliminary results of injury mechanism analysis. Spine (Phila Pa 1976) 34:1140-1147.
43. Li Y, Zhao Q (2008) The effects of fibrin glue on acute complete transection spinal cord injury. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 22:828-831.
44. Li Y, Field PM, Raisman G (1998) Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 18:10514-10524.
45. Li Y, Sauve Y, Li D, Lund RD, Raisman G (2003) Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. J Neurosci 23:7783-7788.
46. Li Y, Yamamoto M, Raisman G, Choi D, Carlstedt T (2007) An experimental model of ventral root repair showing the beneficial effect of transplanting olfactory ensheathing cells. Neurosurgery 60:734-741.
47. Lu J, Feron F, Mackay-Sim A, Waite PM (2002) Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 125:14-21.
48. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH (2004) Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24:6402-6409.
49. Mackay-Sim A, St John JA (2011) Olfactory ensheathing cells from the nose: Clinical application in human spinal cord injuries. Exp Neurol 229:174-180.
50. Meijs MF, Timmers L, Pearse DD, Tresco PA, Bates ML, Joosten EA, Bunge MB, Oudega M (2004) Basic fibroblast growth factor promotes neuronal survival but not behavioral recovery in the transected and Schwann cell implanted rat thoracic spinal cord. J Neurotrauma 21:1415-1430.
51. Mills CD, Hains BC, Johnson KM, Hulsebosch CE (2001) Strain and model differences in behavioral outcomes after spinal cord injury in rat. J Neurotrauma 18:743-756.
52. Min SH, Lee SH, Shim H, Park JS, Lee YI, Kim HW, Hyun JK (2011) Development of complete thoracic spinal cord transection model in rats for delayed transplantation of stem cells. Spine (Phila Pa 1976) 36:E155-163.
53. Munoz-Quiles C, Santos-Benito FF, Llamusi MB, Ramon-Cueto A (2009) Chronic spinal injury repair by olfactory bulb ensheathing glia and feasibility for autologous therapy. J Neuropathol Exp Neurol 68:1294-1308.
54. Navarro R, Juhas S, Keshavarzi S, Juhasova J, Motlik J, Johe K, Marsala S, Scadeng M, Lazar P, Tomori Z, Schulteis G, Beattie M, Ciacci JD, Marsala M (2012) Chronic spinal compression model in minipigs: a systematic behavioral, qualitative, and quantitative neuropathological study. J Neurotrauma 29:499-513.
55. Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT (2004) The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci U S A 101:8786-8790.
56. Paino CL, Bunge MB (1991) Induction of axon growth into schwann cell implants grafted into lesioned adult rat spinal cord. Exp Neurol 114:254-257.
57. Patist CM, Mulder MB, Gautier SE, Maquet V, Jerome R, Oudega M (2004) 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 25:1569-1582.
58. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616.
59. Pu Y, Guo QS, Wang AM, Wu SY, Xing SX, Zhang ZR (2007) Repair of acutely injured spinal cord through constructing tissue-engineered neural complex in adult rats. Chin J Traumatol 10:171-176.
60. Radtke C, Lankford KL, Wewetzer K, Imaizumi T, Fodor WL, Kocsis JD (2010) Impaired spinal cord remyelination by long-term cultured adult porcine olfactory ensheathing cells correlates with altered in vitro phenotypic properties. Xenotransplantation 17:71-80.
61. Ramon-Cueto A, Cordero MI, Santos-Benito FF, Avila J (2000) Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25:425-435.
62. Ramer LM, Au E, Richter MW, Liu J, Tetzlaff W, Roskams AJ (2004) Peripheral olfactory ensheathing cells reduce scar and cavity formation and promote regeneration after spinal cord injury. J Comp Neurol 473:1-15.
63. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M (1998) Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821.
64. Richardson PM, Issa VM, Aguayo AJ (1984) Regeneration of long spinal axons in the rat. J Neurocytol 13:165-182.
65. Richter MW, Fletcher PA, Liu J, Tetzlaff W, Roskams AJ (2005) Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J Neurosci 25:10700-10711.
66. Roonprapunt C, Huang W, Grill R, Friedlander D, Grumet M, Chen S, Schachner M, Young W (2003) Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma 20:871-882.
67. Sasaki M, Lankford KL, Zemedkun M, Kocsis JD (2004) Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 24:8485-8493.
68. Schwab ME (2002) Repairing the injured spinal cord. Science 295:1029-1031.
69. Shen HY, Yin DZ, Tang Y, Wu YF, Cheng ZA, Yang R, Huang L (2004) Influence of cryopreserved olfactory ensheathing cells transplantation on axonal regeneration in spinal cord of adult rats. Chin J Traumatol 7:179-183.
70. Shumsky JS, Tobias CA, Tumolo M, Long WD, Giszter SF, Murray M (2003) Delayed transplantation of fibroblasts genetically modified to secrete BDNF and NT-3 into a spinal cord injury site is associated with limited recovery of function. Exp Neurol 184:114-130.
71. Sobani ZA, Quadri SA, Enam SA (2010) Stem cells for spinal cord regeneration: Current status. Surg Neurol Int 1:93.
72. Steward O, Sharp K, Selvan G, Hadden A, Hofstadter M, Au E, Roskams J (2006) A re-assessment of the consequences of delayed transplantation of olfactory lamina propria following complete spinal cord transection in rats. Exp Neurol 198:483-499.
73. Su Z, He C (2010) Olfactory ensheathing cells: Biology in neural development and regeneration. Prog Neurobiol 92:517-532.
74. Talac R, Friedman JA, Moore MJ, Lu L, Jabbari E, Windebank AJ, Currier BL, Yaszemski MJ (2004) Animal models of spinal cord injury for evaluation of tissue engineering treatment strategies. Biomaterials 25:1505-1510.
75. Tanaka H, Yamashita T, Yachi K, Fujiwara T, Yoshikawa H, Tohyama M (2004) Cytoplasmic p21Cip1/WAF1 enhances axonal regeneration and functional recovery after spinal cord injury in rats. Neuroscience 127:155-164.
76. Tator CH, Duncan EG, Charles D (1990) Comparisons of the clinical and radiological features and surgical management of posterior fossa meningiomas and acoustic neuromas. Can J Neurol Sci 17:170-176.
77. Tetzlaff W, Okon EB, Karimi-Abdolrezaee S, Hill CE, Sparling JS, Plemel JR, Plunet WT, Tsai EC, Baptiste D, Smithson LJ, Kawaja MD, Fehlings MG, Kwon BK (2011) A systematic review of cellular transplantation therapies for spinal cord injury. J Neurotrauma 28:1611-1682.
78. Tharion G, Indirani K, Durai M, Meenakshi M, Devasahayam SR, Prabhav NR, Solomons C, Bhattacharji S (2011) Motor recovery following olfactory ensheathing cell transplantation in rats with spinal cord injury. Neurol India 59:566-572.
79. Tillakaratne NJ, Guu JJ, de Leon RD, Bigbee AJ, London NJ, Zhong H, Ziegler MD, Joynes RL, Roy RR, Edgerton VR (2010) Functional recovery of stepping in rats after a complete neonatal spinal cord transection is not due to regrowth across the lesion site. Neuroscience 166:23-33.
80. Tsai EC, Dalton PD, Shoichet MS, Tator CH (2004) Synthetic hydrogel guidance channels facilitate regeneration of adult rat brainstem motor axons after complete spinal cord transection. J Neurotrauma 21:789-804.
81. Ung RV, Lapointe NP, Rouleau P, Guertin PA (2010) Non-assisted treadmill training does not improve motor recovery and body composition in spinal cord-transected mice. Spinal Cord 48:750-755.
82. Xu G, Nie DY, Chen JT, Wang CY, Yu FG, Sun L, Luo XG, Ahmed S, David S, Xiao ZC (2004) Recombinant DNA vaccine encoding multiple domains related to inhibition of neurite outgrowth: a potential strategy for axonal regeneration. J Neurochem 91:1018-1023.
83. Yates C, Charlesworth A, Allen SR, Reese NB, Skinner RD, Garcia-Rill E (2008) The onset of hyperreflexia in the rat following complete spinal cord transection. Spinal Cord 46:798-803.
84. Yin GD, Tang X, Lin YQ, Xu YQ, Zhou TH (2006) Experimental study of transplantion human embryonic OECs on transected spinal cord of rat. Zhongguo Jiaoxing Waike Zazhi 14:1093-1095.
85. Yui S, Ito D, Fujita N, Nishimura R (2011) Effects of fibroblasts derived from the olfactory bulb and nasal olfactory mucosa on proliferation of olfactory ensheathing cells harvested from the olfactory bulb. J Vet Med Sci 73:133-137.
86. Zhang SX, Huang F, Gates M, White J, Holmberg EG (2011) Histological repair of damaged spinal cord tissue from chronic contusion injury of rat: a LM observation. Histol Histopathol 26:45-58.
87. Zhou L, Shine HD (2003) Neurotrophic factors expressed in both cortex and spinal cord induce axonal plasticity after spinal cord injury. J Neurosci Res 74:221-226.