#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Experimental Treatment of Spinal Cord Injuries


Authors: A. Hejčl 1–3;  P. Jendelová 2,4;  M. Sameš 1;  E. Syková 2,4
Authors‘ workplace: Neurochirurgická klinika UJEP a Krajská zdravotní a. s., Masarykova nemocnice v Ústí nad Labem, o. z. 1;  Ústav experimentální medicíny AV ČR, v. v. i., Praha 2;  Mezinárodní centrum klinického výzkumu, FN u sv. Anny v Brně 3;  Ústav neurověd, 2. LF UK v Praze 4
Published in: Cesk Slov Neurol N 2015; 78/111(4): 377-392
Category: Minimonography
doi: https://doi.org/10.14735/amcsnn2015377

Overview

Spinal cord injuries still remain incurable in current clinical practice. Standard therapy focuses on early decompression and stabilization of the injured spine together with prevention of a secondary injury. On the other hand, several experimental therapies are being developed in laboratories. Some of these showed partial functional and morphological effect in laboratory animals. Over the last 20 years, some of the experimental therapies have been applied in clinical studies but did not provide unambiguous results. In the present paper, we provide an overview of current clinical and experimental therapies of spinal cord injuries.

Key words:
spinal cord injury – stem cells – biomaterials – regeneration – experimental treatment

The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.

The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.


Sources

1. Beneš V. Poranění míchy. Praha: Avicenum 1987.

2. Hughes JT. The Edwin Smith Surgical Papyrus: an analysis of the first case reports of spinal cord injuries. Paraplegia 1988; 26(2): 71– 82.

3. Marketos SG, Skiadas P. Hippocrates. The father of spine surgery. Spine (Phila Pa 1976) 1999; 24(13): 1381– 1387.

4. Marketos SG, Skiadas PK. Galen: a pioneer of spine research. Spine (Phila Pa 1976) 1999; 24(22): 2358– 2362.

5. Knoeller SM, Seifried C. Historical perspective: history of spinal surgery. Spine 2000; 25(21): 2838– 2843.

6. Guttmann L. Spinal cord injuries: comprehensive management and research. Oxford: Blackwell Scientific 1973.

7. Walker AE. A history of neurological surgery. New York: Hafner 1967.

8. Schlesinger EB. Alfred Reginald Allen: the mythic career of a gifted neuroscientist. Surg Neurol 1991; 36(3): 229– 233.

9. Beneš Vr. Spinal cord injury. London: Baillière, Tindall & Cassell 1968.

10. Česká společnost pro míšní léze ČLS JEP. [online]. Dostupné z URL: www.spinalcord.cz.

11. Spinal Cord Injury (SCI), facts and fiures at a glance. [online]. Available from URL: https:/ / www.nscisc.uab.edu/ PublicDocuments/ fact_figures_docs/ Facts%202014.pdf.

12. Reier PJ, Perlow MJ, Guth L. Development of embryonic spinal cord transplants in the rat. Brain Res 1983; 312(2): 201– 219.

13. Bunge RP, Puckett WR, Becerra JL, Marcillo A, Quencer RM. Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 1993; 59: 75– 89.

14. Yoon SH, Shim YS, Park YH, Chung JK, Nam JH, Kim MO et al. Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage‑ colony stimulating factor: Phase I/ II clinical trial. Stem Cells 2007; 25(8): 2066– 2073.

15. Kiwerski J. The natural history of neurological recovery in patients with traumatic tetraplegia. Paraplegia 1989; 27(1): 41– 45.

16. Lim PA, Tow AM. Recovery and regeneration after spinal cord injury: a review and summary of recent literature. Ann Acad Med Singapore 2007; 36(1): 49– 57.

17. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nature Neurosci 2004; 7(3): 269– 277.

18. Nishio T. Axonal regeneration and neural network reconstruction in mammalian CNS. J Neurol 2009; 256 (Suppl 3): 306– 309. doi: 10.1007/ s00415‑ 009‑ 5244‑ x.

19. Kříž J, Háková R, Hyšperská V, Hlinková Z, Lukáš R, Anděl R. Mezinárodní standardy pro neurologickou klasifikaci míšního poranění –  revize 2013. Cesk Slov Neurol N 2014; 77/ 110(1): 77– 81.

20. Lukas R, Zykova I, Barsa P, Sram J. Current role of methylprednisolone in the treatment of acute spinal cord injury. Acta Chir Orthop Traumatol Cech 2011; 78(4): 305– 313.

21. Bracken MB. Steroids for acute spinal cord injury. The Cochrane database of systematic reviews 2012; 1: CD001046. doi: 10.1002/ 14651858.CD001046.pub2.

22. Bracken MB, Shepard MJ, Collins WF, Holford TR, Young W, Baskin DS et al. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal‑ cord injury. Results of the Second National Acute Spinal Cord Injury Study. New Engl J Med 1990; 322(20): 1405– 1411.

23. Bracken MB, Shepard MJ, Hellenbrand KG, Collins WF, Leo LS, Freeman DF et al. Methylprednisolone and neurological function 1 year after spinal cord injury. Results of the National Acute Spinal Cord Injury Study. J Neurosurg 1985; 63(5): 704– 713.

24. Bracken MB, Shepard MJ, Holford TR, Leo‑ Summers L, Aldrich EF, Fazl M et al. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. JAMA 1997; 277(20): 1597– 1604.

25. Hurlbert RJ, Hadley MN, Walters BC, Aarabi B, Dhall SS, Gelb DE et al. Pharmacological therapy for acute spinal cord injury. Neurosurgery 2013; 72 (Suppl 2): 93– 105.

26. Walters BC, Hadley MN, Hurlbert RJ, Aarabi B, Dhall SS, Gelb DE et al. Guidelines for the management of acute cervical spine and spinal cord injuries: 2013 update. Neurosurgery 2013; 60 (Suppl 1): 82– 91. doi: 10.1227/ 01.neu.0000430319.32247.7f.

27. Vaccaro AR, Daugherty RJ, Sheehan TP, Dante SJ, Cotler JM, Balderston RA et al. Neurologic outcome of early versus late surgery for cervical spinal cord injury. Spine 1997; 22(22): 2609– 2613.

28. Fehlings MG, Vaccaro A, Wilson JR, Singh A, Ca­dotte WD, Harrop JS et al. Early versus delayed decompression for traumatic cervical spinal cord injury: results of the Surgical Timing in Acute Spinal Cord Injury Study (STASCIS). PloS One 2012; 7(2): e32037. doi: 10.1371/ journal.pone.0032037.

29. Lenehan B, Fisher CG, Vaccaro A, Fehlings M, Aarabi B, Dvorak MF. The urgency of surgical decompression in acute central cord injuries with spondylosis and without instability. Spine 2010; 35 (Suppl 21): S180– S186.

30. Carlson GD, Gorden CD, Oliff HS, Pillai JJ, LaManna JC. Sustained spinal cord compression: part I: time‑ dependent effect on long‑term pathophysiology. J Bone Joint Surg Am 2003; 85(1): 86– 94.

31. Dimar JR 2nd, Glassman SD, Raque GH, Zhang YP, Shields CB. The influence of spinal canal narrowing and timing of decompression on neurologic recovery after spinal cord contusion in a rat model. Spine 1999; 24(16): 1623– 1633.

32. De Leon RD, Hodgson JA, Roy RR, Edgerton VR. Full weight‑ bearing hindlimb standing following stand train­ing in the adult spinal cat. J Neurophysiol 1998; 80(1): 83– 91.

33. Ichiyama RM, Courtine G, Gerasimenko YP, Yang GJ, van den Brand R, Lavrov IA et al. Step training reinforces specific spinal locomotor circuitry in adult spinal rats. J Neurosci 2008; 28(29): 7370– 7375. doi: 10.1523/ JNEUROSCI.1881‑ 08.2008.

34. Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, stand­ing and assisted stepping after motor complete paraplegia: a case study. Lancet 2011; 377(9781): 1938– 1947. doi: 10.1016/ S0140‑ 6736(11)60547‑ 3.

35. Tronnier V, Baron R, Birklein F, Eckert S, Harke H, Horstkotte D et al. Epidural spinal cord stimulation for therapy of chronic pain. Summary of the S3 guideline. Schmerz 2011; 25(5): 484– 492. doi: 10.1007/ s00482‑ 011‑ 1094‑ 4.

36. Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor‑like activity. Hum Mov Sci 2007; 26(2): 275– 295.

37. Nornes HO, Das GD. Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study‑ time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 1974; 73(1): 121– 138.

38. Richardson RM, Sun D, Bullock MR. Neurogenesis after traumatic brain injury. Neurosurg Clin N Am 2007; 18(1): 169– 181.

39. Fiorelli R, Cebrian‑ Silla A, Garcia‑ Verdugo JM, Raineteau O. The adult spinal cord harbors a population of GFAP‑ positive progenitors with limited self‑ renewal potential. Glia 2013; 61(12): 2100– 2113. doi: 10.1002/ glia.22579.

40. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997; 276(5309): 71– 74.

41. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000; 61(4): 364– 370.

42. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663– 676.

43. Thomson JA, Itskovitz‑ Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145– 1147.

44. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med 1999; 5(12): 1410– 1412.

45. Hendricks WA, Pak ES, Owensby JP, Menta KJ, Glazova M, Moretto J et al. Predifferentiated embryonic stem cells prevent chronic pain behaviors and restore sensory function following spinal cord injury in mice. Mol Med 2006; 12(1– 3): 34– 46.

46. Lees JG, Lim SA, Croll T, Williams G, Lui S, Cooper‑ -White J et al. Transplantation of 3D scaffolds seeded with human embryonic stem cells: bio­logical features of sur­rogate tissue and teratoma‑ forming potential. Regen Med 2007; 2(3): 289– 300.

47. Suter DM, Krause KH. Neural commitment of embryonic stem cells: molecules, pathways and potential for cell therapy. J Pathol 2008; 215(4): 355– 368. doi: 10.1002/ path.2380.

48. Alper J. Geron gets green light for human trial of ES cell‑ derived product. Nat Biotechnol 2009; 27(3): 213– 214. doi: 10.1038/ nbt0309‑ 213a.

49. Strauss S. Geron trial resumes, but standards for stem cell trials remain elusive. Nat Biotechnol 2010; 28(10): 989– 990. doi: 10.1038/ nbt1010‑ 989.

50. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita Ket al. Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 2009; 27(8): 743– 745. doi: 10.1038/ nbt.1554.

51. Nori S, Okada Y, Yasuda A, Tsuji O, Takahashi Y, Kobayashi Y et al. Grafted human‑induced pluripotent stem‑ cell‑ derived neurospheres promote motor functional recovery after spinal cord injury in mice. Proc Natl Acad Sci U S A 2011; 108(40): 16825– 16830. doi: 10.1073/ pnas.1108077108.

52. Romanyuk N, Amemori T, Turnovcova K, Prochazka P, Onteniente B, Sykova E et al. Beneficial effect of human induced pluripotent stem cell‑ derived neural precursors in spinal cord injury repair. Cell Transplant 2014; 15(8– 9): 675– 687.

53. Kobayashi Y, Okada Y, Itakura G, Iwai H, Nishimura S, Yasuda A 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 2012; 7(12): e52787.

54. Forostyak S, Jendelova P, Sykova E. The role of mesenchymal stromal cells in spinal cord injury, regenerative medicine and possible clinical applications. Biochimie 2013; 95(12): 2257– 2270. doi: 10.1016/ j.bio­chi.2013.08.004.

55. Hejčl A, Jendelová P, Sameš M, Syková E. The Use of Mesenchymal Stem Cells in the Experimental and Clinical Therapy of Spinal Cord Injury. Cesk Slov Neurol N 2014; 77/ 110(5): 560– 567.

56. Arboleda D, Forostyak S, Jendelova P, Marekova D, Amemori T, Pivonkova H et al. Transplantation of predifferentiated adipose‑derived stromal cells for the treatment of spinal cord injury. Cell Mol Neurobio­l 2011; 31(7): 1113– 1122. doi: 10.1007/ s10571‑ 011‑ 9712‑ 3.

57. Sasaki M, Honmou O, Akiyama Y, Uede T, Hashi K, Kocsis JD. Transplantation of an acutely isolated bone marrow fraction repairs demyelinated adult rat spinal cord axons. Glia 2001; 35(1): 26– 34.

58. Akiyama Y, Radtke C, Kocsis JD. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 2002; 22(15): 6623– 6630.

59. Ankeny DP, McTigue DM, Jakeman LB. Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats. Exp Neurol 2004; 190(1): 17– 31.

60. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ et al. Marrow stromal cells form guid­ing strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 2002; 99(4): 2199– 2204.

61. Ohta M, Suzuki Y, Noda T, Ejiri Y, Dezawa M, Kataoka K et al. Bone marrow stromal cells infused into the cerebrospinal fluid promote functional recovery of the injured rat spinal cord with reduced cavity formation. Exp Neurol 2004; 187(2): 266– 278.

62. Quertainmont R, Cantinieaux D, Botman O, Sid S, Schoenen J, Franzen R. Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro‑angiogenic actions. PloS One 2012; 7(6): e39500. doi: 10.1371/ journal.pone.0039500.

63. Urdzikova L, Jendelova P, Glogarova K, Burian M, Hajek M, Sykova E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte‑ colony stimulating factor promotes recovery after spinal cord injury in rats. J Neurotrauma 2006; 23(9): 1379– 1391.

64. Urdzikova LM, Ruzicka J, LaBagnara M, Karova K, Kubinova S, Jirakova K et al. Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int J Mol Sci 2014; 15(7): 11275– 11293. doi: 10.3390/ ijms150711275.

65. Spaeth E, Klopp A, Dembinski J, Andreeff M, Marini F. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 2008; 15(10): 730– 738. doi: 10.1038/ gt.2008.39.

66. Nishida H, Nakayama M, Tanaka H, Kitamura M, Hatoya S, Sugiura K et al. Evaluation of transplantation of autologous bone marrow stromal cells into the cerebrospinal fluid for treatment of chronic spinal cord injury in dogs. Am J Vet Res 2011; 72(8): 1118– 1123. doi: 10.2460/ ajvr.72.8.1118.

67. Lim JH, Byeon YE, Ryu HH, Jeong YH, Lee YW, Kim WH et al. Transplantation of canine umbilical cord blood‑ derived mesenchymal stem cells in experimentally induced spinal cord injured dogs. J Vet Sci 2007; 8(3): 275– 282.

68. Sohni A, Verfaillie CM. Mesenchymal stem cells migration homing and tracking. Stem Cells Int 2013; 2013: 130763. doi: 10.1155/ 2013/ 130763.

69. Kim JW, Ha KY, Molon JN, Kim YH. Bone marrow‑ derived mesenchymal stem cell transplantation for chronic spinal cord injury in rats: comparative study between intralesional and intravenous transplantation. Spine 2013; 38(17): E1065– E1074. doi: 10.1097/ BRS.0b013e31829839fa.

70. Vaquero J, Zurita M, Oya S, Santos M. Cell therapy using bone marrow stromal cells in chronic paraplegic rats: systemic or local administration? Neurosci Lett 2006; 398(1– 2): 129– 134.

71. Sykova E, Homola A, Mazanec R, Lachmann H, Konradova SL, Kobylka P et al. Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant 2006; 15(8– 9): 675– 687.

72. Kadota R, Koda M, Kawabe J, Hashimoto M, Nishio Y, Mannoji C et al. Granulocyte colony‑ stimulating factor (G‑CSF) protects oligodendrocyte and promotes hindlimb functional recovery after spinal cord injury in rats. PloS One 2012; 7(11): e50391. doi: 10.1371/ journal.pone.0050391.

73. Sykova E, Jendelova P. Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann NY Acad Sci 2005; 1049: 146– 160.

74. Jendelova P, Herynek V, Urdzikova L, Glogarova K, Kroupova J, Andersson B et al. Magnetic resonance track­ing of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 2004; 76(2): 232– 243.

75. Sykova E, Jendelova P. Magnetic resonance tracking of transplanted stem cells in rat brain and spinal cord. Neurodegener Dis 2006; 3(1– 2): 62– 67.

76. Sykova E, Jendelova P. In vivo tracking of stem cells in brain and spinal cord injury. Prog Brain Res 2007; 161: 367– 383.

77. Arthur‑ Farraj PJ, Latouche M, Wilton DK, Quintes S, Chabrol E, Banerjee A et al. C‑ Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 2012; 75(4): 633– 647. doi: 10.1016/ j.neuron.2012.06.021.

78. Guest J, Santamaria AJ, Benavides FD. Clinical translation of autologous Schwann cell transplantation for the treatment of spinal cord injury. Curr Opin Organ Tran 2013; 18(6): 682– 689. doi: 10.1097/ MOT.0000000000000026.

79. David S, Aguayo AJ. Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science 1981; 214(4523): 931– 933.

80. 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– 442.

81. Sun T, Ye C, Zhang Z, Wu J, Huang H. Cotransplantation of olfactory ensheathing cells and Schwann cells combined with treadmill training promotes functional recovery in rats with contused spinal cords. Cell Transplant 2013; 22 (Suppl 1): S27– S38. doi: 10.3727/ 096368913X672118.

82. 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– 1136.

83. Saberi H, Moshayedi P, Aghayan HR, Arjmand B, Hos­seini SK, Emami‑ Razavi SH et al. Treatment of chronic thoracic spinal cord injury patients with autologous Schwann cell transplantation: an interim report on safety considerations and possible outcomes. Neurosci Lett 2008; 443(1): 46– 50. doi: 10.1016/ j.neulet.2008.07.041.

84. Saberi H, Firouzi M, Habibi Z, Moshayedi P, Aghayan HR, Arjmand B et al. Safety of intramedullary Schwann cell transplantation for postrehabilitation spinal cord injuries: 2‑year follow‑up of 33 cases. J Neurosurg Spine 2011; 15(5): 515– 525. doi: 10.3171/ 2011.6.SPINE10917.

85. Zhou XH, Ning GZ, Feng SQ, Kong XH, Chen JT, Zheng YF et al. Transplantation of autologous activated Schwann cells in the treatment of spinal cord injury: six cases, more than five years of follow‑up. Cell Transplant 2012; 21 (Suppl 1): S39– S47. doi: 10.3727/ 096368912X633752.

86. Doucette JR. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 1984; 210(2): 385– 391.

87. Pixley SK. The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia 1992; 5(4): 269– 284.

88. Huang ZH, Wang Y, Cao L, Su ZD, Zhu YL, Chen YZ et al. Migratory properties of cultured olfactory ensheathing cells by single‑cell migration assay. Cell Res 2008; 18(4): 479– 490. doi: 10.1038/ cr.2008.38.

89. Lu J, Ashwell K. Olfactory ensheathing cells: their potential use for repairing the injured spinal cord. Spine 2002; 27(8): 887– 892.

90. Lu J, Feron F, Ho SM, Mackay‑ Sim A, Waite PM. Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res 2001; 889(1– 2): 344– 357.

91. Lu J, Feron F, Mackay‑ Sim A, Waite PM. Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 2002; 125(1): 14– 21.

92. Ramon‑ Cueto A. Olfactory ensheathing glia transplantation into the injured spinal cord. Prog Brain Res 2000; 128: 265– 272.

93. Ramon‑ Cueto A, Cordero MI, Santos‑ Benito FF, Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000; 25(2): 425– 435.

94. Rubio­ MP, Munoz‑ Quiles C, Ramon‑ Cueto A. Adult olfactory bulbs from primates provide reliable ensheathing glia for cell therapy. Glia 2008; 56(5): 539– 551. doi: 10.1002/ glia.20635.

95. Feron F, Perry C, Cochrane J, Licina P, Nowitzke A, Urquhart S et al. Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 2005; 128(12): 2951– 2960.

96. Mackay‑ Sim A, Feron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W et al. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3‑year clinical trial. Brain 2008; 131(9): 2376– 2386. doi: 10.1093/ brain/ awn173.

97. Chen L, Huang H, Xi H, Zhang F, Liu Y, Chen D et al. A prospective randomized double blind clinical trial using a combination of olfactory ensheathing cells and Schwann cells for the treatment of chronic complete spinal cord injuries. Cell Transplant 2014; 23 (Suppl 1): S35– S44. doi: 10.3727/ 096368914X685014.

98. Tabakow P, Raisman G, Fortuna W, Czyz M, Huber J, Li D et al. Functional regeneration of supraspinal con­nections in a patient with transected spinal cord fol­lowing transplantation of bulbar olfactory ensheathing cells with peripheral nerve bridging. Cell Transplant 2014; 23(12): 1631– 1655. doi: 10.3727/ 096368914X685131.

99. Dlouhy BJ, Awe O, Rao RC, Kirby PA, Hitchon PW. Autograft‑ derived spinal cord mass following olfactory mucosal cell transplantation in a spinal cord injury patient. J Neurosurg Spine 2014; 21(4): 618– 622. doi: 10.3171/ 2014.5.SPINE13992.

100. Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 2008; 209(2): 378– 388.

101. Schwartz M, Yoles E. Immune‑based therapy for spinal cord repair: autologous macrophages and beyond. J Neurotrauma 2006; 23(3– 4): 360– 370.

102. Lammertse DP, Jones LA, Charlifue SB, Kirsh­blum SC, Apple DF, Ragnarsson KT et al. Autologous incubated macrophage therapy in acute, complete spinal cord injury: results of the phase 2 randomized controlled multicenter trial. Spinal Cord 2012; 50(9): 661– 671. doi: 10.1038/ sc.2012.39.

103. Gensel JC, Zhang B. Macrophage activation and its role in repair and pathology after spinal cord injury. Brain Res 2015. doi: 10.1016/ j.brainres.2014.12.045.

104. Schwab ME, Caroni P. Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci 1988; 8(7): 2381– 2393.

105. Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME. Patterns of Nogo mRNA and protein expres­sion in the developing and adult rat and after CNS lesions. J Neurosci 2002; 22(9): 3553– 3567.

106. Schwab ME. Nogo and axon regeneration. Curr Opin Neurobio­l 2004; 14(1): 118– 124.

107. Hawryluk GW, Rowland J, Kwon BK, Fehlings MG. Protection and repair of the injured spinal cord: a review of completed, ongoing and planned clinical trials for acute spinal cord injury. Neurosurg Focus 2008; 25(5): E14. doi: 10.3171/ FOC.2008.25.11.E14.

108. Fitch MT, Silver J. Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res 1997; 290(2): 379– 384.

109. McKeon RJ, Schreiber RC, Rudge JS, Silver J. Reduction of neurite outgrowth in a model of glial scarring fol­lowing CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 1991; 11(11): 3398– 3411.

110. Davies SJ, Goucher DR, Doller C, Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 1999; 19(14): 5810– 5822.

111. Bradbury EJ, Moon LD, Popat RJ, King VR, Ben­nett GS, Patel PN et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002; 416(6881): 636– 640.

112. Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 2007; 27(9): 2176– 2185.

113. Hejcl A, Sedy J, Kapcalova M, Toro DA, Amemori T, Lesny P et al. HPMA‑ RGD hydrogels seeded with mesenchymal stem cells improve functional outcome in chronic spinal cord injury. Stem Cells Dev 2010; 19(10): 1535– 1546. doi: 10.1089/ scd.2009.0378.

114. Hejcl A, Lesny P, Pradny M, Michalek J, Jendelova P, Stulik J et al. Biocompatible hydrogels in spinal cord injury repair. Physiol Res 2008; 57 (Suppl 3): S121– S132.

115. Sykova E, Jendelova P, Urdzikova L, Lesny P, Hejcl A. Bone marrow stem cells and polymer hydrogels‑ two strategies for spinal cord injury repair. Cell Mol Neurobio­l 2006; 26(7– 8): 1113– 1129.

116. Kubinova S, Sykova E. Biomaterials combined with cell therapy for treatment of spinal cord injury. Regen Med 2012; 7(2): 207– 224. doi: 10.2217/ rme.11.121.

117. King VR, Alovskaya A, Wei DY, Brown RA, Priestley JV. The use of injectable forms of fibrin and fibronectin to support axonal ingrowth after spinal cord injury. Biomaterials 2010; 31(15): 4447– 4456. doi: 10.1016/ j.bio­materials.2010.02.018.

118. Novikova LN, Novikov LN, Kellerth JO. Biopolymers and bio­degradable smart implants for tissue regeneration after spinal cord injury. Curr Opin Neurol 2003; 16(6): 711– 715.

119. Pradny M, Michalek J, Lesny P, Hejcl A, Vacik J, Slouf M et al. Macroporous hydrogels based on 2‑ hydroxyethyl methacrylate. Part 5: hydrolytically degradable materials. J Mater Sci Mater Med 2006; 17(12): 1357– 1364.

120. Kubinova S, Horak D, Hejcl A, Plichta Z, Kotek J, Proks V et al. SIKVAV‑ modified highly superporous PHEMA scaffolds with oriented pores for spinal cord injury repair. J Tissue Eng Regen Med 2013. doi: 10.1002/ term.1694.

121. Hejcl A, Ruzicka J, Kapcalova M, Turnovcova K, Krumb­holcova E, Pradny M et al. Adjusting the chemical and physical properties of hydrogels leads to improved stem cell survival and tissue ingrowth in spinal cord injury reconstruction: a comparative study of four methacrylate hydrogels. Stem Cells Dev 2013; 22(20): 2794– 2805. doi: 10.1089/ scd.2012.0616.

122. Kubinova S, Sykova E. Nanotechnologies in regenerative medicine. Minimally invasive therapy & allied technologies: MITAT 2010; 19(3): 144– 156. doi: 10.3109/ 13645706.2010.481398.

123. Medberry CJ, Crapo PM, Siu BF, Carruthers CA, Wolf MT, Nagarkar SP et al. Hydrogels derived from central nervous system extracellular matrix. Biomaterials 2013; 34(4): 1033– 1040. doi: 10.1016/ j.bio­materials.2012.10.062.

124. Li C, Zhang X, Cao R, Yu B, Liang H, Zhou M et al. Allografts of the acellular sciatic nerve and brain‑derived neurotrophic factor repair spinal cord injury in adult rats. PloS One 2012; 7(8): e42813. doi: 10.1371/ journal.pone.0042813.

125. Bible E, Dell’Acqua F, Solanky B, Balducci A, Crapo PM, Badylak SF et al. Non‑ invasive imaging of transplanted human neural stem cells and ECM scaffold remodel­ing in the stroke‑ damaged rat brain by (19)F‑  and dif­fusion‑ MRI. Biomaterials 2012; 33(10): 2858– 2871. doi: 10.1016/ j.bio­materials.2011.12.033.

126. Ruzicka J, Romanyuk N, Hejcl A, Vetrik M, Hruby M, Cocks G et al. Treating spinal cord injury in rats with a combination of human fetal neural stem cells and hydrogels modified with serotonin. Acta Neurobio­l Exp 2013; 73(1): 102– 115.

127. Liu S, Kadi K, Boisset N, Lacroix C, Said G, Tadie M. Reinnervation of denervated lumbar ventral roots and their target muscle by thoracic spinal motoneurons via an implanted nerve autograft in adult rats after spinal cord injury. J Neurosci Res 1999; 56(5): 506– 517.

128. Liu S, Aghakhani N, Boisset N, Said G, Tadie M. Innervation of the caudal denervated ventral roots and their target muscles by the rostral spinal motoneurons after implanting a nerve autograft in spinal cord‑ injured adult marmosets. J Neurosurg 2001; 94 (Suppl 1): 82– 90.

129. Emery E, Rhrich‑ Haddout F, Kassar‑ Duchossoy L, Lyoussi B, Tadié M, Horvat JC. Motoneurons of the adult marmoset can grow axons and reform motor end­plates through a peripheral nerve bridge joining the locally injured cervical spinal cord to the denervat­ed biceps brachii muscle. J Neurosci Res 2000; 62(6): 821– 829.

130. Tadie M, Liu S, Robert R, Guiheneuc P, Pereon Y, Per­rouin‑Verbe B et al. Partial return of motor function in paralyzed legs after surgical bypass of the lesion site by nerve autografts three years after spinal cord injury. J Neurotrauma 2002; 19(8): 909– 916.

131. Amemori T, Jendelova P, Ruzickova K, Arboleda D, Sykova E. Co‑ transplantation of olfactory ensheathing glia and mesenchymal stromal cells does not have synergistic effects after spinal cord injury in the rat. Cytotherapy 2010; 12(2): 212– 225. doi: 10.3109/ 14653240903440103.

132. Zhang J, Liu Z, Chen H, Duan Z, Zhang L, Chen L et al. Synergic effects of EPI‑ NCSCs and OECs on the donor cells migration, the expression of neurotrophic factors, and locomotor recovery of contused spinal cord of rats. J Mol Neurosci 2015; 55(3): 760– 769. doi: 10.1007/ s12031‑ 014‑ 0416‑ 2.

133. Chen B, He J, Yang H, Zhang Q, Zhang L, Zhang X et al. Repair of spinal cord injury by implantation of bFGF‑ incorporated HEMA‑ MOETACL hydrogel in rats. Sci Rep 2015; 5: 9017. doi: 10.1038/ srep09017.

134. Han Q, Jin W, Xiao Z, Ni H, Wang J, Kong J et al. The promotion of neural regeneration in an extreme rat spinal cord injury model using a collagen scaffold contain­ing a collagen binding neuroprotective protein and an EGFR neutralizing antibody. Biomaterials 2010; 31(35): 9212– 9220. doi: 10.1016/ j.bio­materials.2010.08.040.

135. 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 2005; 25(5): 1169– 1178.

136. Kwon BK, Soril LJ, Bacon M, Beattie MS, Blesch A, Bresnahan JC et al. Demonstrating efficacy in preclinical studies of cellular therapies for spinal cord injury –  how much is enough? Exp Neurol 2013; 248: 30– 44. doi: 10.1016/ j.expneurol.2013.05.012.

Labels
Paediatric neurology Neurosurgery Neurology

Article was published in

Czech and Slovak Neurology and Neurosurgery

Issue 4

2015 Issue 4

Most read in this issue
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#