Safety of Intramedullary Autologous Peripheral Nerve Grafts for Post-Rehabilitated Complete Motor Spinal Cord Injuries: A Phase I Study
-
Nazi Derakhshanrad
,
Hooshang Saberi
,
Sajad Shafiee
,
Mir Saeed Yekaninejad
,
Mohammad Reza Hadian
,
Abdolreza Sheikhrezai
,
Zahid Hussain Khan
,
Abbas Noruzi Javidan
,
Amir Hassan Kohan
Abstract
Many experimental studies have reported behavioral improvement after transplantation of peripheral nerve tissue into the contused spinal cord, even in large animals. The safety of this treatment in human remains unknown. In this translational phase 1 study, safety of peripheral nerve grafting for chronic spinal cord injuries and possible outcomes are being reported. Twelve complete motor spinal cord injury patients, who had finished their rehabilitation program, were enrolled. There were 4 thoracic and 8 cervical cases. Patients underwent sural nerve preconditioning in the calf, followed 1 week later, by intramedullary transplantation of the harvested nerve fascicles. The patients were followed up for potential complications periodically, and final assessment by American Spinal Injury association (ASIA) and Spinal Cord Independence Measure (SCIM) III were reported after 2 years of follow-up. The median duration of the spinal cord injury was 31 months. At two years of follow up, out of 7 cases with ASIA Impairment Scale (AIS) A, 4(57.1%) cases improved to AIS B and 1 (14.3%) case became AIS C. There were 1 patient with transient increased spasm, one case of transient cystitis, 3 patients with transient increased neuropathic pain and 1 case with transient episode of autonomic dysreflexia, all being managed medically. There was no case of donor site infection. The above complications were transient as they responded to temporary medical treatment. It may be deduced that after two years follow-up of patients that the procedure may be safe, however further controlled studies are needed to prove its efficacy.
Cripps RA, Lee BB, Wing P, Weerts E, Mackay J, Brown D. A global map for traumatic spinal cord injury epidemiology: towards a living data repository for injury prevention. Spinal Cord 2011;49(4):493-501.
Ning GZ, Yu TQ, Feng SQ, Zhou XH, Ban DX, Liu Y, Jiao XX. Epidemiology of traumatic spinal cord injury in Tianjin, China. Spinal Cord 2011;49(3):386-90.
Ho CH, Wuermser LA, Priebe MM, Chiodo AE, Scelza WM, Kirshblum SC. Spinal cord injury medicine. 1. Epidemiology and classification. Arch Phys Med Rehabil 2007;88(3 Suppl 1):S49-54.
van den Berg ME, Castellote JM, Mahillo-Fernandez I, de Pedro-Cuesta J. Incidence of spinal cord injury worldwide: a systematic review. Neuroepidemiology 2010;34(3):184- 92; discussion 92.
Burke DA, Linden RD, Zhang YP, Maiste AC, Shields CB. Incidence rates and populations at risk for spinal cord injury: A regional study. Spinal Cord 2001;39(5):274-8.
Pirouzmand F. Epidemiological trends of spine and spinal,cord injuries in the largest Canadian adult trauma center from 1986 to 2006. J Neurosurg Spine 2010;12(2):131-40.
Rahimi-Movaghar V, Saadat S, Rasouli MR, Ganji S, Ghahramani M, Zarei MR, Vaccaro AR. Prevalence of spinal cord injury in Tehran, Iran. J Spinal Cord Med 2009;32(4):428-31.
Wyndaele M, Wyndaele JJ. Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord 2006;44(9):523-9.
Chiodo AE, Scelza WM, Kirshblum SC, Wuermser LA, Ho CH, Priebe MM. Spinal cord injury medicine. 5. Longterm medical issues and health maintenance. Arch Phys Med Rehabil 2007;88(3 Suppl 1):S76-83.
McKinley WO, Jackson AB, Cardenas DD, DeVivo MJ. Long-term medical complications after traumatic spinal cord injury: a regional model systems analysis. Arch Phys Med Rehabil 1999;80(11):1402-10.
Dionyssiotis Y. Spinal cord injury-related bone impairment and fractures: an update on epidemiology and physiopathological mechanisms. J Musculoskelet Neuronal Interact 2011;11(3):257-65.
Wittenberg RH, Peschke U, Botel U. Heterotopic ossification after spinal cord injury. Epidemiology and risk factors. J Bone Joint Surg Br 1992;74(2):215-8.
Johnson RL, Brooks CA, Whiteneck GG. Cost of traumatic spinal cord injury in a population-based registry. Spinal Cord 1996;34(8):470-80.
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.
Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci. 2006 Aug;7(8):628-43.
Aidinoff E, Front L, Itzkovich M, Bluvshtein V, Gelernter I, Hart J, Biering-Sørensen F, Weeks C, Laramee MT, Craven C, Hitzig SL, Glaser E, Zeilig G, Aito S, Scivoletto G, Mecci M, Chadwick RJ, El Masry WS, Osman A, Glass CA, Soni BM, Gardner BP, Savic G, Bergström EM, Silva P, Catz A. Expected spinal cord independence measure, third version, scores for various neurological levels after complete spinal cord lesions. Spinal Cord 2011;49(8):893-6.
Dawson J, Shamley D, Jamous MA. A structured review of outcome measures used for the assessment of rehabilitation interventions for spinal cord injury. Spinal Cord 2008;46(12):768-80.
Kirshblum SC, Priebe MM, Ho CH, Scelza WM, Chiodo AE, Wuermser LA. Spinal cord injury medicine. 3. Rehabilitation phase after acute spinal cord injury. Arch Phys Med Rehabil 2007;88(3 Suppl 1):S62-70.
Ackerman P, Morrison SA, McDowell S, Vazquez L. Using the Spinal Cord Independence Measure III to measure functional recovery in a post-acute spinal cord injury program. Spinal Cord 2010;48(5):380-7.
Firouzi M, Moshayedi P, Saberi H, Mobasheri H,Abolhassani F, Jahanzad I, Raza M. Transplantation of Schwann cells to subarachnoid space induces repair in contused rat spinal cord. Neurosci Lett 2006; 402(1-2):66-70.
Bartolomei JC, Greer CA. Olfactory ensheathing cells: bridging the gap in spinal cord injury. Neurosurgery 2000;47(5):1057-69.
Hannila SS, Filbin MT. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 2008;209(2):321-32.
Dezawa M, Mutoh T, Dezawa A, Adachi-Usami E. Putative gap junctional communication between axon and regenerating Schwann cells during mammalian peripheral nerve regeneration. Neuroscience 1998;85(3):663-7.
Asada Y, Kawaguchi S, Hayashi H, Nakamura T. Neural repair of the injured spinal cord by grafting: comparison between peripheral nerve segments and embryonic homologous structures as a conduit of CNS axons. Neurosci Res 1998;31(3):241-9.
Saberi H, Firouzi M, Habibi Z, Moshayedi P, Aghayan HR, Arjmand B, Hosseini K, Razavi HE, Yekaninejad MS. Safety of intramedullary Schwann cell transplantation for postrehabilitation spinal cord injuries: 2-year follow-up of 33 cases. J Neurosurg Spine 2011;15(5):515-25.
Cote MP, Hanna A, Lemay MA, Ollivier-Lanvin K, Santi L, Miller K, Monaghan R, Houlé JD. Peripheral nerve grafts after cervical spinal cord injury in adult cats. Exp Neurol 2010;225(1):173-82.
Richardson PM, McGuinness UM, Aguayo AJ. Axons from CNS neurons regenerate into PNS grafts. Nature 1980;284(5753):264-5.
Decherchi P, Gauthier P. Regrowth of acute and chronic injured spinal pathways within supra-lesional post-traumatic nerve grafts. Neuroscience 2000;101(1): 197-210.
Levi AD, Dancausse H, Li X, Duncan S, Horkey L, Oliviera M. Peripheral nerve grafts promoting central nervous system regeneration after spinal cord injury in the primate. J Neurosurg. 2002;96(2 Suppl):197-205.
Reier PJ. Cellular transplantation strategies for spinal cord injury and translational neurobiology. Neuro Rx 2004;1(4):424-51.
Houle JD, Amin A, Cote MP, Lemay M, Miller K, Sandrow H, Santi L, Shumsky J, Tom V. Combining peripheral nerve grafting and matrix modulation to repair the injured rat spinal cord. J Vis Exp 2009 (33).
Ma WQ, Zhang SC, Li M, Yan YB, Ni CR. [Experimental study of peripheral nerve grafts for repairing of chronic spinal cord injury in adult rats]. Zhongguo Gu Shang 2008;21(7):519-21.
Farin A, Liu CY, Langmoen IA, Apuzzo ML. Biological restoration of central nervous system architecture and function: part 3-stem cell- and cell-based applications and realities in the biological management of central nervous system disorders: traumatic, vascular, and epilepsy disorders. Neurosurgery 2009;65(5):831-59; discussion 59.
Jin Y, Tay D, So KF, Wu W. Expression of c-jun in the lateral vestibular nucleus following spinal cord injury and peripheral nerve graft transplantation in adult rats. J Neurocytol 2000;29(2):91-7.
Xu XM, Onifer SM. Transplantation-mediated strategies to promote axonal regeneration following spinal cord injury. Respir Physiol Neurobiol. 2009 Nov 30;169(2):171-82.
Lavdas AA, Matsas R. Towards personalized cellreplacement therapies for brain repair. Personalized Medicine 2009;6(3):293-313.
Saberi H, Moshayedi P, Aghayan HR, Arjmand B, Hosseini SK, Emami-Razavi SH, Rahimi-Movaghar V, Raza M, Firouzi M. Treatment of chronic thoracic spinal cord injury patients with autologous Schwann cell transplantation: an interim report on safetyconsiderations and possible outcomes. Neurosci Lett 2008;443(1):46-50.
Tuszynski MH, Steeves JD, Fawcett JW, Lammertse D, Kalichman M, Rask C, Curt A, Ditunno JF, Fehlings MG, Guest JD, Ellaway PH, Kleitman N, Bartlett PF, Blight AR, Dietz V, Dobkin BH, Grossman R, Privat A. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP Panel: clinical trial inclusion/exclusion criteria and ethics. Spinal Cord 2007;45(3):222-31.
Wu JC, Huang WC, Tsai YA, Chen YC, Cheng H. Nerve repair using acidic fibroblast growth factor in human cervical spinal cord injury: a preliminary Phase I clinical study. J Neurosurg Spine 2008;8(3):208-14.
Hill CE, Brodak DM, Bartlett Bunge M. Dissociated predegenerated peripheral nerve transplants for spinal cord injury repair: a comprehensive assessment of their effects on regeneration and functional recovery compared to Schwann cell transplants. J Neurotrauma 2012;29(12): 2226-43.
Hanna AS, Cote MP, Houle J, Dempsey R. Nerve grafting for spinal cord injury in cats: are we close to translational research? Neurosurgery 2011;68(4):N14-5.
Fehlings MG, Vawda R. Cellular treatments for spinal cord injury: the time is right for clinical trials. Neurotherapeutics 2011;8(4):704-20.
Lammertse D, Tuszynski MH, Steeves JD, Curt A, Fawcett JW, Rask C, Ditunno JF, Fehlings MG, Guest JD, Ellaway PH, Kleitman N, Blight AR, Dobkin BH, Grossman R, Katoh H, Privat A, Kalichman M. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: clinical trial design. Spinal Cord 2007;45(3):232-42.
Steeves JD, Lammertse D, Curt A, Fawcett JW, Tuszynski MH, Ditunno JF, Ellaway PH, Fehlings MG, Guest JD, Kleitman N, Bartlett PF, Blight AR, Dietz V, Dobkin BH, Grossman R, Short D, Nakamura M, Coleman WP, Gaviria M, Privat A. Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord 2007;45(3):206-21.
Maynard FM, Jr., Bracken MB, Creasey G, Ditunno JF, Jr., Donovan WH, Ducker TB, Garber SL, Marino RJ, Stover SL, Tator CH, Waters RL, Wilberger JE, Young W. International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 1997;35(5):266-74.
Kirshblum SC, Waring W, Biering-Sorensen F, Burns SP, Johansen M, Schmidt-Read M, Donovan W, Graves DE, Jha A, Jones L, Mulcahey MJ, Krassioukov A. Reference for the 2011 revision of the International Standards for Neurological Classification of Spinal Cord Injury. J Spinal Cord Med 2011;34(6):547-54.
Krassioukov A, Biering-Sorensen F, Donovan W, Kennelly M, Kirshblum S, Krogh K, Alexander MS, Vogel,L, Wecht J. International standards to document remaining autonomic function after spinal cord injury. J Spinal Cord Med 2012;35(4):201-10.
Aghayan HR, Arjmand B, Norouzi-Javidan A, Saberi H, Soleimani M, Tavakoli SA, Abbas Khodadadi, Niloufar Tirgar, Fereshteh Mohammadi-Jahani. Clinical grade cultivation of human Schwann cell, by the using of human autologous serum instead of fetal bovine serum and without growth factors. Cell Tissue Bank 2011.
Bunge MB. Novel combination strategies to repair the injured mammalian spinal cord. J Spinal Cord Med. 2008;31(3):262-9.
Alexander MS, Anderson KD, Biering-Sorensen F, Blight AR, Brannon R, Bryce TN, Creasey G, Catz A, Curt A, Donovan W, Ditunno J, Ellaway P, Finnerup NB, Graves DE, Haynes BA, Heinemann AW, Jackson AB, Johnston MV, Kalpakjian CZ, Kleitman N, Krassioukov A, Krogh K, Lammertse D, Magasi S, Mulcahey MJ, Schurch B, Sherwood A, Steeves JD, Stiens S, Tulsky DS, van Hedel HJ, Whiteneck G. Outcome measures in spinal cord injury: recent assessments and recommendations for future directions. Spinal Cord 2009;47(8):582-91.
Fawcett JW, Curt A, Steeves JD, Coleman WP, Tuszynski MH, Lammertse D, Bartlett PF, Blight AR, Dietz V, Ditunno J, Dobkin BH, Havton LA, Ellaway PH, Fehlings MG, Privat A, Grossman R, Guest JD, Kleitman N, Nakamura M, Gaviria M, Short D. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007;45(3):190-205.
Blight A, Curt A, Ditunno JF, Dobkin B, Ellaway P, Fawcett J, Fehlings M, Grossman RG, Lammertse DP, Privat A, Steeves J, Tuszynski M, Kalichman M, Guest JD. Position statement on the sale of unproven cellular therapies for spinal cord injury: the international campaign for cures of spinal cord injury paralysis. Spinal Cord 2009;47(9):713-4.
Curt A, Dietz V. Controversial treatments for spinal-cord injuries. Lancet 2005;365(9462):841.
Dobkin BH, Curt A, Guest J. Cellular transplants in China: observational study from the largest human experiment in chronic spinal cord injury. Neurorehabil Neural Repair 2006;20(1):5-13.
Ronsyn MW, Berneman ZN, Van Tendeloo VF, Jorens PG, Ponsaerts P. Can cell therapy heal a spinal cord injury? Spinal Cord 2008;46(8):532-9.
Eftekharpour E, Karimi-Abdolrezaee S, Fehlings MG. Current status of experimental cell replacement approaches to spinal cord injury. Neurosurg Focus. 2008;24(3-4):E19.
Decherchi P, Gauthier P. Regeneration of acutely and chronically injured descending respiratory pathways within post-traumatic nerve grafts. Neuroscience 2002;112(1):141-52.
David S, Aguayo AJ. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 1981;214(4523):931-3.
Duchossoy Y, Kassar-Duchossoy L, Orsal D, Stettler O, Horvat JC. Reinnervation of the biceps brachii muscle following cotransplantation of fetal spinal cord and autologous peripheral nerve into the injured cervical spinal cord of the adult rat. Exp Neurol. 2001 Feb;167(2):329-40.
Papastefanaki F, Chen J, Lavdas AA, Thomaidou D, Schachner M, Matsas R. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 2007;130(Pt8):2159-74.
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.
Nomura H, Tator CH, Shoichet MS. Bioengineered strategies for spinal cord repair. J Neurotrauma 2006;23(3-4):496-507.
Wong DY, Leveque JC, Brumblay H, Krebsbach PH, Hollister SJ, Lamarca F. Macro-architectures in spinal cord scaffold implants influence regeneration. J Neurotrauma 2008;25(8):1027-37.
Nordblom J, Persson JK, Svensson M, Mattsson P. Peripheral nerve grafts in a spinal cord prosthesis result in regeneration and motor evoked potentials following spinal cord resection. Restor Neurol Neurosci 2009;27(4):285-95.
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):4447-56.
Yiu G, He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci. 2006 Aug;7(8):617-27.
Deng LX, Hu J, Liu N, Wang X, Smith GM, Wen X, Smith GM, Wen X, Xu XM. GDNF modifies reactive astrogliosis allowing robust axonal regeneration through Schwann cell-seeded guidance channels after spinal cord injury. Exp Neurol 2011;229(2):238-50.
Tom VJ, Houle JD. Intraspinal microinjection of chondroitinase ABC following injury promotes axonal regeneration out of a peripheral nerve graft bridge. Exp Neurol 2008;211(1):315-9.
Tom VJ, Sandrow-Feinberg HR, Miller K, Santi L, Connors T, Lemay MA Houlé JD. Combining peripheral nerve grafts and chondroitinase promotes functional axonal regeneration in the chronically injured spinal cord. J Neurosci 2009;29(47):14881-90.
Hsu JY, McKeon R, Goussev S, Werb Z, Lee JU, Trivedi A, Noble-Haeusslein LJ. Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J Neurosci 2006;26(39):9841-50.
Kuo HS, Tsai MJ, Huang MC, Huang WC, Lee MJ, Kuo WC, You LH, Szeto KC, Tsai IL, Chang WC, Chiu CW, Ma H, Chak KF, Cheng H. The combination of peripheral nerve grafts and acidic fibroblast growth factor enhances arginase I and polyamine spermine expression in transected rat spinal cords. Biochem Biophys Res Commun 2007;357(1):1-7.
Guzen FP, de Almeida Leme RJ, de Andrade MS, de Luca BA, Chadi G. Glial cell line-derived neurotrophic factor added to a sciatic nerve fragment grafted in a spinal cord gap ameliorates motor impairments in rats and increases local axonal growth. Restor Neurol Neurosci 2009;27(1):1-16.
Blits B, Dijkhuizen PA, Boer GJ, Verhaagen J. Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp Neurol 2000;164(1):25-37.
Storer PD, Houle JD, Oblinger M, Jones KJ. Combination of gonadal steroid treatment and peripheral nerve grafting results in a peripheral motoneuron-like pattern of beta IItubulin mRNA expression in axotomized hamster rubrospinal motoneurons. J Comp Neurol 2002;449(4):364-73.
Welin D, Novikova LN, Wiberg M, Kellerth JO, Novikov LN. Effects of N-acetyl-cysteine on the survival and regeneration of sural sensory neurons in adult rats. Brain Res 2009;1287:58-66.
Lee YS, Lin CY, Robertson RT, Hsiao I, Lin VW. Motor recovery and anatomical evidence of axonal regrowth in spinal cord-repaired adult rats. J Neuropathol Exp Neurol. 2004 Mar;63(3):233-45.
Mortazavi MM, Verma K, Tubbs RS, Theodore N. Cellular and paracellular transplants for spinal cord injury: a review of the literature. Childs Nerv Syst. 2011;27(2):237-43.
Lee MJ, Chen CJ, Cheng CH, Huang WC, Kuo HS, Wu JC, Tsai MJ, HuangM Ch, Chang W Ch, Cheng H. 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 2008;433(3):163-9.
Lee YS, Hsiao I, Lin VW. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J Neurotrauma 2002;19(10):1203-16.
Lee YS, Sindhu RK, Lin CY, Ehdaie A, Lin VW, Vaziri ND. Effects of nerve graft on nitric oxide synthase, NAD(P)H oxidase, and antioxidant enzymes in chronic spinal cord injury. Free Radic Biol Med 2004;36(3):330-9.
Lee YS, Zdunowski S, Edgerton VR, Roy RR, Zhong H, Hsiao I, Lin VW. Improvement of gait patterns in steptrained, complete spinal cord-transected rats treated with a peripheral nerve graft and acidic fibroblast growth factor. Exp Neurol 2010;224(2):429-37.
Cote MP, Amin AA, Tom VJ, Houle JD. Peripheral nerve grafts support regeneration after spinal cord injury. Neurotherapeutics 2011;8(2):294-303.
Dinh P, Bhatia N, Rasouli A, Suryadevara S, Cahill K, Gupta R. Transplantation of preconditioned Schwann cells following hemisection spinal cord injury. Spine (Phila Pa 1976) 2007;32(9):943-9.
Feng SQ, Zhou XF, Rush RA, Ferguson IA. Graft of preinjured sural nerve promotes regeneration of corticospinal tract and functional recovery in rats with chronic spinal cord injury. Brain Res 2008;1209:40-8.
Illes J, Reimer JC, Kwon BK. Stem cell clinical trials for spinal cord injury: readiness, reluctance, redefinition. Stem Cell Rev 2011;7(4):997-1005.
Houle JD, Tessler A. Repair of chronic spinal cord injury. Exp Neurol 2003;182(2):247-60.
Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci 2006;26(28):7405-15.
Huang H, Chen L, Wang H, Xi H, Gou C, Zhang J, Zhang F, Liu Y. Safety of fetal olfactory ensheathing cell transplantation in patients with chronic spinal cord injury. A 38-month follow-up with MRI. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2006;20(4):439-43.
Rabinovich SS, Seledtsov VI, Poveschenko OV, Senuykov VV, Taraban VY, Yarochno VI, Kolosov NG, Savchenko SA, Kozlov VA. Transplantation treatment of spinal cord injury patients. Biomed Pharmacother 2003;57(9):428-33.
Mackay-Sim A, Feron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W, . Fronek P, Gray C, Kerr G, Licina P, Nowitzke A, Perry C, Silburn PAS, Urquhart S, Geraghty T. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008;131(Pt 9):2376-86.
Callera F, do Nascimento RX. Delivery of autologous bone marrow precursor cells into the spinal cord via lumbar puncture technique in patients with spinal cord injury: a preliminary safety study. Exp Hematol 2006;34(2):130-1.
Chhabra HS, Lima C, Sachdeva S, Mittal A, Nigam V, Chaturvedi D, Arora M, Aggarwal A, Kapur R, Khan TAH. Autologous olfactory [corrected] mucosal transplant in chronic spinal cord injury: an Indian Pilot Study. Spinal Cord 2009;47(12):887-95.
Lima C, Escada P, Pratas-Vital J, Branco C, Arcangeli CA, Lazzeri G, Santana Maia CA, Capucho C, Hasse-Ferreira A, Peduzzi JD. Olfactory mucosal autografts and rehabilitation for chronic traumatic spinal cord injury. Neurorehabil Neural Repair 2010;24(1):10-22.
Cheng H, Liao KK, Liao SF, Chuang TY, Shih YH. Spinal cord repair with acidic fibroblast growth factor as a treatment for a patient with chronic paraplegia. Spine(Phila Pa 1976) 2004;29(14):E284-8.
| Files | ||
| Issue | Vol 51, No 12 (2013) | |
| Section | Articles | |
| Keywords | ||
| Spinal Cord Injury Peripheral Nerve Graft Safety | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
