Mesenchymal stem cells improve locomotor recovery in traumatic spinal cord injury: Systematic review with meta-analyses of rat models

Neurobiology of Disease

Volumn 62, Issue , 2014, Pages 338-353

  Oliveri, Roberto S ^a   Bello, Segun ^a   Biering Sørensen, Fin ^a  

^a Rigshospitalet   (Denmark)

Author keywords

Locomotor recovery; Mesenchymal stem cells; Meta analysis; Systematic review; Traumatic spinal cord injury

Indexed keywords

IMMUNOSUPPRESSIVE AGENT; PLACEBO;

ARTICLE; BLOOD BRAIN BARRIER; CLINICAL EFFECTIVENESS; EXTERNAL VALIDITY; INTERNAL VALIDITY; LOCOMOTION; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PUBLICATION; RAT STRAIN; SPINAL CORD COMPRESSION; SPINAL CORD INJURY;

ALTERNATIVELY ACTIVATED MACROPHAGE/MICROGLIA; BASSO-BEATTIE-BRESNAHAN; BBB; BETAGALACTOSIDASE; CHONDROITIN SULPHATE PROTEOGLYCANS; CI; CLASSICALLY ACTIVATED MACROPHAGE/MICROGLIA; CONFIDENCE INTERVAL; CSPGS; D2; DIVERSITY; I2; IFNΓ; INCONSISTENCY MEASURE; INTERFERON GAMMA; LACZ; LOCOMOTOR RECOVERY; M1; M2; MAG; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELLS; META-ANALYSIS; MOG; MSC; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; MYELIN-ASSOCIATED GLYCOPROTEIN; NEURITE OUTGROWTH INHIBITOR A; NOGO-A; RISK OF TYPE I ERROR; RISK OF TYPE II ERROR; SCI; SD; SE; SPINAL CORD INJURY; STANDARD DEVIATION; STANDARD ERROR; SYSTEMATIC REVIEW; TRAUMATIC SPINAL CORD INJURY; TRIAL SEQUENTIAL ANALYSIS; TSA; Α; Β;

ANIMALS; BIAS (EPIDEMIOLOGY); DISEASE MODELS, ANIMAL; LOCOMOTION; MESENCHYMAL STEM CELL TRANSPLANTATION; RANDOM ALLOCATION; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TREATMENT OUTCOME;

EID: 84887332963     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.10.014     Document Type: Article

References (175)

1. Abrams M.B., Dominguez C., Pernold K., Reger R., Wiesenfeld-Hallin Z., Olson L., Prockop D. Multipotent mesenchymal stromal cells attenuate chronic inflammation and injury-induced sensitivity to mechanical stimuli in experimental spinal cord injury. Restor. Neurol. Neurosci. 2009, 27:307-321.
2. Adams M., Cavanagh J.F. International Campaign for Cures of Spinal Cord Injury Paralysis (ICCP): another step forward for spinal cord injury research. Spinal Cord 2004, 42:273-280.
3. Akhtar A.Z., Pippin J.J., Sandusky C.B. Animal models in spinal cord injury: a review. Rev. Neurosci. 2008, 19:47-60.
4. Bajpai V., Saraya A. Boom in clinical research industry: a dangerous trend. Trop. Gastroenterol. 2009, 30:177-181.
5. Bakshi A., Hunter C., Swanger S., Lepore A., Fischer I. Minimally invasive delivery of stem cells for spinal cord injury: advantages of the lumbar puncture technique. J. Neurosurg. Spine 2004, 1:330-337.
6. Bartmann C., Rohde E., Schallmoser K., Purstner P., Lanzer G., Linkesch W., Strunk D. Two steps to functional mesenchymal stromal cells for clinical application. Transfusion 2007, 47:1426-1435.
7. Barzilay R., Sadan O., Melamed E., Offen D. Comparative characterization of bone marrow-derived mesenchymal stromal cells from four different rat strains. Cytotherapy 2009, 11:435-442.
8. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
9. Basso D.M., Beattie M.S., Bresnahan J.C. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 1996, 139:244-256.
10. Beattie M.S., Bresnahan J.C. Cell death, repair, and recovery of function after spinal cord injury in rats. Neurobiology of Spinal Cord Injury 2000, 1-22. Humana Press, Totowa. R.G. Kalb, S.M. Strittmatter (Eds.).
11. Bebarta V., Luyten D., Heard K. Emergency medicine animal research: does use of randomization and blinding affect the results?. Acad. Emerg. Med. 2003, 10:684-687.
12. Beck K.D., Nguyen H.X., Galvan M.D., Salazar D.L., Woodruff T.M., Anderson A.J. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 2010, 133:433-447.
13. Berkey C.S., Hoaglin D.C., Mosteller F., Colditz G.A. A random-effects regression model for meta-analysis. Stat. Med. 1995, 14:395-411.
14. Blight A., Curt A., Ditunno J.F., Dobkin B., Ellaway P., Fawcett J., Fehlings M., Grossman R.G., Lammertse D.P., Privat A., Steeves J., Tuszynski M., Kalichman M., Guest J.D. 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, 47:713-714.
15. Boakye M., Leigh B.C., Skelly A.C. Quality of life in persons with spinal cord injury: comparisons with other populations. J. Neurosurg. Spine 2012, 17:29-37.
16. Borenstein M., Hedges L.V., Higgins J.P.T., Rothstein H.R. Meta-regression. Introduction to Meta-analysis 2009, 187-203. John Wiley & Sons, Chichester.
17. Borenstein M., Hedges L.V., Higgins J.P.T., Rothstein H.R. Subgroup analyses. Introduction to Meta-analysis 2009, 149-186. John Wiley & Sons, Chichester.
18. Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 1995, 378:498-501.
19. Breslin K., Agrawal D. The use of methylprednisolone in acute spinal cord injury: a review of the evidence, controversies, and recommendations. Pediatr. Emerg. Care 2012, 28:1238-1245.
20. Brok J., Thorlund K., Gluud C., Wetterslev J. Trial sequential analysis reveals insufficient information size and potentially false positive results in many meta-analyses. J. Clin. Epidemiol. 2008, 61:763-769.
21. Burke D.A., Magnuson D.S.K. Basso, Beattie, and Bresnahan scale locomotor assessment following spinal cord injury and its utility as a criterion for other assessments. Animal Models of Acute Neurological Injuries II 2012, 591-604. Humana Press, New York City. J. Chen, X.-M. Xu, Z.C. Xu, J.H. Zhang (Eds.).
22. Cadotte D.W., Fehlings M.G. Spinal cord injury: a systematic review of current treatment options. Clin. Orthop. Relat. Res. 2011, 469:732-741.
23. Caplan A.I., Correa D. The MSC: an injury drugstore. Cell Stem Cell 2011, 9:11-15.
24. Chalmers I. The lethal consequences of failing to make use of all relevant evidence about the effects of medical treatments: the need for systematic reviews. Treating Individuals: From Randomized Trials to Personalised Medicine 2009, 37-58. Elsevier, London. P. Rothwell (Ed.).
25. Chen Y., Teng F.Y., Tang B.L. Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: progress and uncertainties. Cell. Mol. Life Sci. 2006, 63:1649-1657.
26. Clarke M., Hopewell S., Chalmers I. Reports of clinical trials should begin and end with up-to-date systematic reviews of other relevant evidence: a status report. J. R. Soc. Med. 2007, 100:187-190.
27. Cohen C.B., Cohen P.J. International stem cell tourism and the need for effective regulation. Part I: Stem cell tourism in Russia and India: clinical research, innovative treatment, or unproven hype?. Kennedy Inst. Ethics J. 2010, 20:27-49.
28. Crigler L., Robey R.C., Asawachaicharn A., Gaupp D., Phinney D.G. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol. 2006, 198:54-64.
29. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.J., Giacobino J.P., Lazzari L., Huard J., Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
30. Crossley N.A., Sena E., Goehler J., Horn J., van der Worp B., Bath P.M., Macleod M., Dirnagl U. Empirical evidence of bias in the design of experimental stroke studies: a metaepidemiologic approach. Stroke 2008, 39:929-934.
31. Crowley P., Chalmers I., Keirse M.J. The effects of corticosteroid administration before preterm delivery: an overview of the evidence from controlled trials. Br. J. Obstet. Gynaecol. 1990, 97:11-25.
32. Cui Q., Hodgetts S.I., Hu Y., Luo J.M., Harvey A.R. Strain-specific differences in the effects of cyclosporin A and FK506 on the survival and regeneration of axotomized retinal ganglion cells in adult rats. Neuroscience 2007, 146:986-999.
33. Culme-Seymour E.J., Davie N.L., Brindley D.A., Edwards-Parton S., Mason C. A decade of cell therapy clinical trials (2000-2010). Regen. Med. 2012, 7:455-462.
34. Curt A. The translational dialogue in spinal cord injury research. Spinal Cord 2012, 50:352-357.
35. Deeks J.J., Higgins J.P.T., Altman D.G. Analysing data and undertaking meta-analyses. Cochrane Handbook for Systematic Reviews of Interventions 2008, 151-185. Wiley-Blackwell, Chichester. J.P.T. Higgins, S. Green (Eds.).
36. DerSimonian R., Laird N. Meta-analysis in clinical trials. Control. Clin. Trials 1986, 7:177-188.
37. Devivo M.J. Epidemiology of traumatic spinal cord injury: trends and future implications. Spinal Cord 2012, 50:365-372.
38. Diaz-Ruiz A., Rios C., Duarte I., Correa D., Guizar-Sahagun G., Grijalva I., Ibarra A. Cyclosporin-A inhibits lipid peroxidation after spinal cord injury in rats. Neurosci. Lett. 1999, 266:61-64.
39. Diaz-Ruiz A., Vergara P., Perez-Severiano F., Segovia J., Guizar-Sahagun G., Ibarra A., Rios C. Cyclosporin-A inhibits inducible nitric oxide synthase activity and expression after spinal cord injury in rats. Neurosci. Lett. 2004, 357:49-52.
40. Dietz V., Curt A. Neurological aspects of spinal-cord repair: promises and challenges. Lancet Neurol. 2006, 5:688-694.
41. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
42. Donnelly E.M., Lamanna J., Boulis N.M. Stem cell therapy for the spinal cord. Stem Cell Res Ther 2012, 3:24.
43. Duijvestein M., Vos A.C., Roelofs H., Wildenberg M.E., Wendrich B.B., Verspaget H.W., Kooy-Winkelaar E.M., Koning F., Zwaginga J.J., Fidder H.H., Verhaar A.P., Fibbe W.E., van den Brink G.R., Hommes D.W. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 2010, 59:1662-1669.
44. Duval S., Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000, 56:455-463.
45. Egger M., Davey S.G., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315:629-634.
46. Fergusson D., Glass K.C., Hutton B., Shapiro S. Randomized controlled trials of aprotinin in cardiac surgery: could clinical equipoise have stopped the bleeding?. Clin. Trials 2005, 2:218-229.
47. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 2003, 4:703-713.
48. Fischer U.M., Harting M.T., Jimenez F., Monzon-Posadas W.O., Xue H., Savitz S.I., Laine G.A., Cox C.S. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 2009, 18:683-692.
49. Fleming J.C., Norenberg M.D., Ramsay D.A., Dekaban G.A., Marcillo A.E., Saenz A.D., Pasquale-Styles M., Dietrich W.D., Weaver L.C. The cellular inflammatory response in human spinal cords after injury. Brain 2006, 129:3249-3269.
50. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 2006, 12:790-792.
51. Geyh S., Ballert C., Sinnott A., Charlifue S., Catz A., D'Andrea Greve J.M., Post M.W. Quality of life after spinal cord injury: a comparison across six countries. Spinal Cord 2013, 51:322-326.
52. Gilbert R., Salanti G., Harden M., See S. Infant sleeping position and the sudden infant death syndrome: systematic review of observational studies and historical review of recommendations from 1940 to 2002. Int. J. Epidemiol. 2005, 34:874-887.
53. Giunti D., Parodi B., Usai C., Vergani L., Casazza S., Bruzzone S., Mancardi G., Uccelli A. Mesenchymal stem cells shape microglia effector functions through the release of CX3CL1. Stem Cells 2012, 30:2044-2053.
54. 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, 84:267-279.
55. Hackam D.G., Redelmeier D.A. Translation of research evidence from animals to humans. JAMA 2006, 296:1731-1732.
56. Harbord R.M., Higgins J.P.T. Meta-regression in Stata. Stata J. 2008, 8:493-519.
57. Hare J.M., Fishman J.E., Gerstenblith G., DiFede Velazquez D.L., Zambrano J.P., Suncion V.Y., Tracy M., Ghersin E., Johnston P.V., Brinker J.A., Breton E., Davis-Sproul J., Schulman I.H., Byrnes J., Mendizabal A.M., Lowery M.H., Rouy D., Altman P., Wong Po F.C., Ruiz P., Amador A., Da S.J., McNiece I.K., Heldman A.W. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012, 308:2369-2379.
58. Harting M., Jimenez F., Pati S., Baumgartner J., Cox C. Immunophenotype characterization of rat mesenchymal stromal cells. Cytotherapy 2008, 10:243-253.
59. Hausmann O.N. Post-traumatic inflammation following spinal cord injury. Spinal Cord 2003, 41:369-378.
60. Hawryluk G.W., Rowland J., Kwon B.K., Fehlings M.G. 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:E14.
61. Hawryluk G.W., Mothe A., Wang J., Wang S., Tator C., Fehlings M.G. An in vivo characterization of trophic factor production following neural precursor cell or bone marrow stromal cell transplantation for spinal cord injury. Stem Cells Dev. 2012, 21:2222-2238.
62. Heazlewood C., Atkinson K. Optimal tissue sources of mesenchymal stromal cells for clinical applications. Mesenchymal Stem Cell Therapy 2013, 355-372. Springer, New York. L.G. Chase, M.C. Vemuri (Eds.).
63. Higgins J.P.T., Deeks J.J. Selecting studies and collecting data. Cochrane Handbook for Systematic Reviews of Interventions 2008, 151-185. Wiley-Blackwell, Chichester. J.P.T. Higgins, S. Green (Eds.).
64. Higgins J.P.T., Green S. Cochrane Handbook for Systematic Reviews of Intervention 2008, Chichester, Wiley-Blackwell.
65. Higgins J.P., Thompson S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002, 21:1539-1558.
66. Higgins J.P.T., Deeks J.J., Altman D.G. Special Topics in Statistics 2008, 481-529. Wiley-Blackwell, Chichester. J.P.T. Higgins, S. Green (Eds.).
67. Hill C.L., LaValley M.P., Felson D.T. Discrepancy between published report and actual conduct of randomized clinical trials. J. Clin. Epidemiol. 2002, 55:783-786.
68. Hodgetts S.I., Simmons P.J., Plant G.W. Human mesenchymal precursor cells (Stro-1+) from spinal cord injury patients improve functional recovery and tissue sparing in an acute spinal cord injury rat model. Cell Transplant. 2013, http://dx.doi.org/10.3727/096368912X656081 (in press).
69. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El M.A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2199-2204.
70. Howells D.W., Porritt M.J., Rewell S.S., O'Collins V., Sena E.S., van der Worp H.B., Traystman R.J., Macleod M.R. Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2010, 30:1412-1431.
71. Hrobjartsson A., Pildal J., Chan A.W., Haahr M.T., Altman D.G., Gotzsche P.C. Reporting on blinding in trial protocols and corresponding publications was often inadequate but rarely contradictory. J. Clin. Epidemiol. 2009, 62:967-973.
72. Hrobjartsson A., Thomsen A.S., Emanuelsson F., Tendal B., Hilden J., Boutron I., Ravaud P., Brorson S. Observer bias in randomized clinical trials with measurement scale outcomes: a systematic review of trials with both blinded and nonblinded assessors. CMAJ 2013, 185:E201-E211.
73. Huwiler-Muntener K., Juni P., Junker C., Egger M. Quality of reporting of randomized trials as a measure of methodologic quality. JAMA 2002, 287:2801-2804.
74. Ibarra A., Correa D., Willms K., Merchant M.T., Guizar-Sahagun G., Grijalva I., Madrazo I. Effects of cyclosporin-A on immune response, tissue protection and motor function of rats subjected to spinal cord injury. Brain Res. 2003, 979:165-178.
75. Inoue M., Honmou O., Oka S., Houkin K., Hashi K., Kocsis J.D. Comparative analysis of remyelinating potential of focal and intravenous administration of autologous bone marrow cells into the rat demyelinated spinal cord. Glia 2003, 44:111-118.
76. Jacobs S.E., Berg M., Hunt R., Tarnow-Mordi W.O., Inder T.E., Davis P.G. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev. 2013, 1. CD003311.
77. Jing W.-L., Yan F.-X., Zuo Y.-Z. Comparison of various mesenchymal stem cell transplatation pathways for treatment of spinal cord injury in rats. J. Clin. Rehab. Tissue Eng. Res. 2008, 12:10045-10049. ([serial online],Avaialbe from: Journal of Clinical Rehabilitative (P.O. Box 1200, Shenyang 110004, China).
78. Kang E.S., Ha K.Y., Kim Y.H. Fate of transplanted bone marrow derived mesenchymal stem cells following spinal cord injury in rats by transplantation routes. J. Korean Med. Sci. 2012, 27:586-593.
79. Karp J.M., Leng Teo G.S. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009, 4:206-216.
80. Khalatbary A.R., Tiraihi T. A comparative study of therapeutic benefits of intraspinal and intravenous bone marrow stromal cell administration to spinal cord injuries. Iran. Biomed. J. 2009, 13:43-48.
81. Kim J., Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp. Hematol. 2009, 37:1445-1453.
82. Kim J.W., Ha K.Y., Molon J.N., Kim Y.H. Bone marrow derived mesenchymal stem cell transplantation for chronic spinal cord injury in rats: comparative study between intralesional and intravenous transplantation (in press). Spine 2013, (Phila Pa 1976).
83. Knapp G., Hartung J. Improved tests for a random effects meta-regression with a single covariate. Stat. Med. 2003, 22:2693-2710.
84. Koc O.N., Day J., Nieder M., Gerson S.L., Lazarus H.M., Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant. 2002, 30:215-222.
85. Krabbe C., Zimmer J., Meyer M. Neural transdifferentiation of mesenchymal stem cells-a critical review. APMIS 2005, 113:831-844.
86. Kwon B.K., Stammers A.M., Belanger L.M., Bernardo A., Chan D., Bishop C.M., Slobogean G.P., Zhang H., Umedaly H., Giffin M., Street J., Boyd M.C., Paquette S.J., Fisher C.G., Dvorak M.F. Cerebrospinal fluid inflammatory cytokines and biomarkers of injury severity in acute human spinal cord injury. J. Neurotrauma 2010, 27:669-682.
87. Kwon B.K., Okon E., Hillyer J., Mann C., Baptiste D., Weaver L.C., Fehlings M.G., Tetzlaff W. A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury. J. Neurotrauma 2011, 28:1545-1588.
88. Kwon B.K., Okon E.B., Plunet W., Baptiste D., Fouad K., Hillyer J., Weaver L.C., Fehlings M.G., Tetzlaff W. A systematic review of directly applied biologic therapies for acute spinal cord injury. J. Neurotrauma 2011, 28:1589-1610.
89. Kwon B.K., Okon E.B., Tsai E., Beattie M.S., Bresnahan J.C., Magnuson D.K., Reier P.J., McTigue D.M., Popovich P.G., Blight A.R., Oudega M., Guest J.D., Weaver L.C., Fehlings M.G., Tetzlaff W. 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, 28:1525-1543.
90. Kwon B.K., Ghag A., Dvorak M.F., Tetzlaff W., Illes J. Expectations of benefit and tolerance to risk of individuals with spinal cord injury regarding potential participation in clinical trials. J. Neurotrauma 2012, 29:2727-2737.
91. Lalu M.M., McIntyre L., Pugliese C., Fergusson D., Winston B.W., Marshall J.C., Granton J., Stewart D.J. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One 2012, 7:e47559.
92. Lanza C., Morando S., Voci A., Canesi L., Principato M.C., Serpero L.D., Mancardi G., Uccelli A., Vergani L. Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo. J. Neurochem. 2009, 110:1674-1684.
93. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., Lanino E., Sundberg B., Bernardo M.E., Remberger M., Dini G., Egeler R.M., Bacigalupo A., Fibbe W., Ringden O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008, 371:1579-1586.
94. Li Y., Chen J., Chen X.G., Wang L., Gautam S.C., Xu Y.X., Katakowski M., Zhang L.J., Lu M., Janakiraman N., Chopp M. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 2002, 59:514-523.
95. Li Q.M., Fu Y.M., Shan Z.Y., Shen J.L., Zhang X.M., Lei L., Jin L.H. MSCs guide neurite directional extension and promote oligodendrogenesis in NSCs. Biochem. Biophys. Res. Commun. 2009, 384:372-377.
96. Li H., Wen Y., Luo Y., Lan X., Wang D., Sun Z., Hu L. Transplantation of bone marrow mesenchymal stem cells into spinal cord injury: a comparison of delivery different times. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2010, 24:180-184.
97. Lu S., Lu C., Han Q., Li J., Du Z., Liao L., Zhao R.C. Adipose-derived mesenchymal stem cells protect PC12 cells from glutamate excitotoxicity-induced apoptosis by upregulation of XIAP through PI3-K/Akt activation. Toxicology 2011, 279:189-195.
98. Malakoff D. Clinical trials and tribulations. Spiraling costs threaten gridlock. Science 2008, 322:210-213.
99. Manochantr S., Pratya Y., Kheolamai P., Rojphisan S., Chayosumrit M., Tantrawatpan C., Supokawej A., Issaragrisil S. Immunosuppressive properties of mesenchymal stromal cells derived from amnion, placenta, Wharton's jelly and umbilical cord. Intern. Med. J. 2013, 43:430-439.
100. McMahon D.S., Thorsteinsdottir H., Singer P.A., Daar A.S. Cultivating regenerative medicine innovation in China. Regen. Med. 2010, 5:35-44.
101. Metz G.A., Curt A., van de Meent H., Klusman I., Schwab M.E., Dietz V. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J. Neurotrauma 2000, 17:1-17.
102. Meyerrose T., Olson S., Pontow S., Kalomoiris S., Jung Y., Annett G., Bauer G., Nolta J.A. Mesenchymal stem cells for the sustained in vivo delivery of bioactive factors. Adv. Drug Deliv. Rev. 2010, 62:1167-1174.
103. Middleton J.W., Dayton A., Walsh J., Rutkowski S.B., Leong G., Duong S. Life expectancy after spinal cord injury: a 50-year study. Spinal Cord 2012, 50:803-811.
104. Mills C.D., Hains B.C., Johnson K.M., Hulsebosch C.E. Strain and model differences in behavioral outcomes after spinal cord injury in rat. J. Neurotrauma 2001, 18:743-756.
105. Moll G., Rasmusson-Duprez I., von Bahr L., Connolly-Andersen A.M., Elgue G., Funke L., Hamad O.A., Lonnies H., Magnusson P.U., Sanchez J., Teramura Y., Nilsson-Ekdahl K., Ringden O., Korsgren O., Nilsson B., Le Blanc K. Are therapeutic human mesenchymal stromal cells compatible with human blood?. Stem Cells 2012, 30:1565-1574.
106. Morando S., Vigo T., Esposito M., Casazza S., Novi G., Principato M.C., Furlan R., Uccelli A. The therapeutic effect of mesenchymal stem cell transplantation in experimental autoimmune encephalomyelitis is mediated by peripheral and central mechanisms. Stem. Cell Res. Ther. 2012, 3:3.
107. Najar M., Raicevic G., Fayyad-Kazan H., De B.C., Bron D., Toungouz M., Lagneaux L. Immune-related antigens, surface molecules and regulatory factors in human-derived mesenchymal stromal cells: the expression and impact of inflammatory priming. Stem Cell Rev. 2012, 8:1188-1198.
108. Nakajima H., Uchida K., Guerrero A.R., Watanabe S., Sugita D., Takeura N., Yoshida A., Long G., Wright K.T., Johnson W.E., Baba H. Transplantation of mesenchymal stem cells promotes an alternative pathway of macrophage activation and functional recovery after spinal cord injury. J. Neurotrauma 2012, 29:1614-1625.
109. Nakano N., Nakai Y., Seo T.B., Yamada Y., Ohno T., Yamanaka A., Nagai Y., Fukushima M., Suzuki Y., Nakatani T., Ide C. Characterization of conditioned medium of cultured bone marrow stromal cells. Neurosci. Lett. 2010, 483:57-61.
110. New P.W., Cripps R.A., Bonne L.B. Global maps of non-traumatic spinal cord injury epidemiology: towards a living data repository. Spinal Cord 2013, http://dx.doi.org/10.1038/sc.2012.165 (in press).
111. Nguyen H.X., O'Barr T.J., Anderson A.J. Polymorphonuclear leukocytes promote neurotoxicity through release of matrix metalloproteinases, reactive oxygen species, and TNF-alpha. J. Neurochem. 2007, 102:900-912.
112. Noble L.J., Donovan F., Igarashi T., Goussev S., Werb Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 2002, 22:7526-7535.
113. Noonan V.K., Fingas M., Farry A., Baxter D., Singh A., Fehlings M.G., Dvorak M.F. Incidence and prevalence of spinal cord injury in Canada: a national perspective. Neuroepidemiology 2012, 38:219-226.
114. O'Brien P.C., Fleming T.R. A multiple testing procedure for clinical trials. Biometrics 1979, 35:549-556.
115. Oliveri R.S. Epigenetic dedifferentiation of somatic cells into pluripotency: cellular alchemy in the age of regenerative medicine?. Regen. Med. 2007, 2:795-816.
116. Onifer S.M., Rabchevsky A.G., Scheff S.W. Rat models of traumatic spinal cord injury to assess motor recovery. ILAR J. 2007, 48:385-395.
117. Osaka M., Honmou O., Murakami T., Nonaka T., Houkin K., Hamada H., Kocsis J.D. Intravenous administration of mesenchymal stem cells derived from bone marrow after contusive spinal cord injury improves functional outcome. Brain Res. 2010, 1343:226-235.
118. Oyinbo C.A. Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade. Acta Neurobiol. Exp. (Wars) 2011, 71:281-299.
119. Pal R., Gopinath C., Rao N.M., Banerjee P., Krishnamoorthy V., Venkataramana N.K., Totey S. Functional recovery after transplantation of bone marrow-derived human mesenchymal stromal cells in a rat model of spinal cord injury. Cytotherapy 2010, 12:792-806.
120. Panagiotou O.A., Contopoulos-Ioannidis D.G., Ioannidis J.P., Rehnborg C.F. Comparative effect sizes in randomised trials from less developed and more developed countries: meta-epidemiological assessment. BMJ 2013, 346:f707.
121. Pati S., Gerber M.H., Menge T.D., Wataha K.A., Zhao Y., Baumgartner J.A., Zhao J., Letourneau P.A., Huby M.P., Baer L.A., Salsbury J.R., Kozar R.A., Wade C.E., Walker P.A., Dash P.K., Cox C.S., Doursout M.F., Holcomb J.B. Bone marrow derived mesenchymal stem cells inhibit inflammation and preserve vascular endothelial integrity in the lungs after hemorrhagic shock. PLoS One 2011, 6:e25171.
122. Perel P., Roberts I., Sena E., Wheble P., Briscoe C., Sandercock P., Macleod M., Mignini L.E., Jayaram P., Khan K.S. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 2007, 334:197.
123. Pildal J., Chan A.W., Hrobjartsson A., Forfang E., Altman D.G., Gotzsche P.C. Comparison of descriptions of allocation concealment in trial protocols and the published reports: cohort study. BMJ 2005, 330:1049.
124. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
125. Prockop D.J. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin. Pharmacol. Ther. 2007, 82:241-243.
126. Prockop D.J., Oh J.Y. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol. Ther. 2012, 20:14-20.
127. Prockop D.J., Brenner M., Fibbe W.E., Horwitz E., Le B.K., Phinney D.G., Simmons P.J., Sensebe L., Keating A. Defining the risks of mesenchymal stromal cell therapy. Cytotherapy 2010, 12:576-578.
128. Raffaghello L., Bianchi G., Bertolotto M., Montecucco F., Busca A., Dallegri F., Ottonello L., Pistoia V. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Stem Cells 2008, 26:151-162.
129. Regenberg A.C., Hutchinson L.A., Schanker B., Mathews D.J. Medicine on the fringe: stem cell-based interventions in advance of evidence. Stem Cells 2009, 27:2312-2319.
130. Rex A., Kolbasenko A., Bert B., Fink H. Choosing the right wild type: behavioral and neurochemical differences between 2 populations of Sprague-Dawley rats from the same source but maintained at different sites. J. Am. Assoc. Lab. Anim. Sci. 2007, 46:13-20.
131. Rivera F.J., Couillard-Despres S., Pedre X., Ploetz S., Caioni M., Lois C., Bogdahn U., Aigner L. Mesenchymal stem cells instruct oligodendrogenic fate decision on adult neural stem cells. Stem Cells 2006, 24:2209-2219.
132. Ryan K.A., Sanders A.N., Wang D.D., Levine A.D. Tracking the rise of stem cell tourism. Regen. Med. 2010, 5:27-33.
133. Sahni V., Kessler J.A. Stem cell therapies for spinal cord injury. Nat. Rev. Neurol. 2010, 6:363-372.
134. Salter B., Cooper M., Dickins A., Cardo V. Stem cell science in India: emerging economies and the politics of globalization. Regen. Med. 2007, 2:75-89.
135. Sandercock P., Roberts I. Systematic reviews of animal experiments. Lancet 2002, 360:586.
136. Savovic J., Jones H., Altman D., Harris R., Juni P., Pildal J., Als-Nielsen B., Balk E., Gluud C., Gluud L., Ioannidis J., Schulz K., Beynon R., Welton N., Wood L., Moher D., Deeks J., Sterne J. Influence of reported study design characteristics on intervention effect estimates from randomised controlled trials: combined analysis of meta-epidemiological studies. Health Technol. Assess. 2012, 16:1-82.
137. Schallmoser K., Rohde E., Reinisch A., Bartmann C., Thaler D., Drexler C., Obenauf A.C., Lanzer G., Linkesch W., Strunk D. Rapid large-scale expansion of functional mesenchymal stem cells from unmanipulated bone marrow without animal serum. Tissue Eng. Part C. Methods 2008, 14:185-196.
138. Sedy J., Urdzikova L., Jendelova P., Sykova E. Methods for behavioral testing of spinal cord injured rats. Neurosci. Biobehav. Rev. 2008, 32:550-580.
139. Sena E.S., van der Worp H.B., Bath P.M., Howells D.W., Macleod M.R. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol. 2010, 8:e1000344.
140. Simpson L.A., Eng J.J., Hsieh J.T., Wolfe D.L. The health and life priorities of individuals with spinal cord injury: a systematic review. J. Neurotrauma 2012, 29:1548-1555.
141. Singer N.G., Caplan A.I. Mesenchymal stem cells: mechanisms of inflammation. Annu. Rev. Pathol. 2011, 6:457-478.
142. Soares H.P., Daniels S., Kumar A., Clarke M., Scott C., Swann S., Djulbegovic B. Bad reporting does not mean bad methods for randomised trials: observational study of randomised controlled trials performed by the Radiation Therapy Oncology Group. BMJ 2004, 328:22-24.
143. Sroga J.M., Jones T.B., Kigerl K.A., McGaughy V.M., Popovich P.G. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J. Comp. Neurol. 2003, 462:223-240.
144. Stammers A.T., Liu J., Kwon B.K. Expression of inflammatory cytokines following acute spinal cord injury in a rodent model. J. Neurosci. Res. 2012, 90:782-790.
145. Steffenhagen C., Dechant F.X., Oberbauer E., Furtner T., Weidner N., Kury P., Aigner L., Rivera F.J. Mesenchymal stem cells prime proliferating adult neural progenitors toward an oligodendrocyte fate. Stem Cells Dev. 2012, 21:1838-1851.
146. Suarez-Almazor M.E., Belseck E., Homik J., Dorgan M., Ramos-Remus C. Identifying clinical trials in the medical literature with electronic databases: MEDLINE alone is not enough. Control. Clin. Trials 2000, 21:476-487.
147. Tan J., Wu W., Xu X., Liao L., Zheng F., Messinger S., Sun X., Chen J., Yang S., Cai J., Gao X., Pileggi A., Ricordi C. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. JAMA 2012, 307:1169-1177.
148. Tator C.H., Hashimoto R., Raich A., Norvell D., Fehlings M.G., Harrop J.S., Guest J., Aarabi B., Grossman R.G. Translational potential of preclinical trials of neuroprotection through pharmacotherapy for spinal cord injury. J. Neurosurg. Spine 2012, 17:157-229.
149. Teixeira F.G., Carvalho M.M., Sousa N., Salgado A.J. Mesenchymal stem cells secretome: a new paradigm for central nervous system regeneration?. Cell. Mol. Life Sci. 2013, 70:3871-3882.
150. Teo K.K., Yusuf S., Furberg C.D. Effects of prophylactic antiarrhythmic drug therapy in acute myocardial infarction. An overview of results from randomized controlled trials. JAMA 1993, 270:1589-1595.
151. Tetzlaff W., Okon E.B., Karimi-Abdolrezaee S., Hill C.E., Sparling J.S., Plemel J.R., Plunet W.T., Tsai E.C., Baptiste D., Smithson L.J., Kawaja M.D., Fehlings M.G., Kwon B.K. A systematic review of cellular transplantation therapies for spinal cord injury. J. Neurotrauma 2011, 28:1611-1682.
152. Thompson S.G., Higgins J.P. How should meta-regression analyses be undertaken and interpreted?. Stat. Med. 2002, 21:1559-1573.
153. Thorlund K., Devereaux P.J., Wetterslev J., Guyatt G., Ioannidis J.P., Thabane L., Gluud L.L., Als-Nielsen B., Gluud C. Can trial sequential monitoring boundaries reduce spurious inferences from meta-analyses?. Int. J. Epidemiol. 2009, 38:276-286.
154. Thorlund K., Imberger G., Walsh M., Chu R., Gluud C., Wetterslev J., Guyatt G., Devereaux P.J., Thabane L. The number of patients and events required to limit the risk of overestimation of intervention effects in meta-analysis-a simulation study. PLoS One 2011, 6:e25491.
155. Trivedi A., Olivas A.D., Noble-Haeusslein L.J. Inflammation and spinal cord injury: infiltrating leukocytes as determinants of injury and repair processes. Clin. Neurosci. Res. 2006, 6:283-292.
156. Trojahn Kølle S.F., Oliveri R.S., Glovinski P.V., Kirchoff M., Mathiasen A.B., Elberg J.J., Andersen P.S., Drzewiecki T.D., Fischer-Nielsen A. Pooled human platelet lysate versus fetal bovine serum-investigating the proliferation rate, chromosome stability and angiogenic potential of human adipose tissue-derived stem cells intended for clinical use. Cytotherapy 2013, 15:1086-1097.
157. Uccelli A. Mesenchymal stem cells exert a remarkable regenerative effect requiring minimal CNS integration. Exp. Neurol. 2013, 247:292-295.
158. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 2008, 8:726-736.
159. Uccelli A., Milanese M., Principato M.C., Morando S., Bonifacino T., Vergani L., Giunti D., Voci A., Carminati E., Giribaldi F., Caponnetto C., Bonanno G. Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol. Med. 2012, 18:794-804.
160. 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, 398:129-134.
161. Varawalla N. India's growing clinical research sector: opportunity for global companies. IDrugs 2007, 10:391-394.
162. Vesterinen H.M., Sena E.S., ffrench-Constant C., Williams A., Chandran S., Macleod M.R. Improving the translational hit of experimental treatments in multiple sclerosis. Mult. Scler. 2010, 16:1044-1055.
163. Vickers A., Goyal N., Harland R., Rees R. Do certain countries produce only positive results? A systematic review of controlled trials. Control. Clin. Trials 1998, 19:159-166.
164. von Bahr L., Batsis I., Moll G., Hagg M., Szakos A., Sundberg B., Uzunel M., Ringden O., Le B.K. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells 2012, 30:1575-1578.
165. Voulgari-Kokota A., Fairless R., Karamita M., Kyrargyri V., Tseveleki V., Evangelidou M., Delorme B., Charbord P., Diem R., Probert L. Mesenchymal stem cells protect CNS neurons against glutamate excitotoxicity by inhibiting glutamate receptor expression and function. Exp. Neurol. 2012, 236:161-170.
166. Wetterslev J., Thorlund K., Brok J., Gluud C. Trial sequential analysis may establish when firm evidence is reached in cumulative meta-analysis. J. Clin. Epidemiol. 2008, 61:64-75.
167. Wetterslev J., Thorlund K., Brok J., Gluud C. Estimating required information size by quantifying diversity in random-effects model meta-analyses. BMC Med. Res. Methodol. 2009, 9:86.
168. Wood L., Egger M., Gluud L.L., Schulz K.F., Juni P., Altman D.G., Gluud C., Martin R.M., Wood A.J., Sterne J.A. Empirical evidence of bias in treatment effect estimates in controlled trials with different interventions and outcomes: meta-epidemiological study. BMJ 2008, 336:601-605.
169. Wright K.T., El Masri W., Osman A., Roberts S., Chamberlain G., Ashton B.A., Johnson W.E. Bone marrow stromal cells stimulate neurite outgrowth over neural proteoglycans (CSPG), myelin associated glycoprotein and Nogo-A. Biochem. Biophys. Res. Commun. 2007, 354:559-566.
170. Wright K.T., El Masri W., Osman A., Chowdhury J., Johnson W.E. Bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 2011, 29:169-178.
171. Wu T., Li Y., Bian Z., Liu G., Moher D. Randomized trials published in some Chinese journals: how many are randomized?. Trials 2009, 10:46.
172. Yuan W., Sipp D., Wang Z.Z., Deng H., Pei D., Zhou Q., Cheng T. Stem cell science on the rise in China. Cell Stem Cell 2012, 10:12-15.
173. Zhang Q.Z., Su W.R., Shi S.H., Wilder-Smith P., Xiang A.P., Wong A., Nguyen A.L., Kwon C.W., Le A.D. Human gingiva-derived mesenchymal stem cells elicit polarization of M2 macrophages and enhance cutaneous wound healing. Stem Cells 2010, 28:1856-1868.
174. Zhang D., Freemantle N., Cheng K.K. Are randomized trials conducted in China or India biased? A comparative empirical analysis. J. Clin. Epidemiol. 2011, 64:90-95.
175. Zhou C., Zhang C., Chi S., Xu Y., Teng J., Wang H., Song Y., Zhao R. Effects of human marrow stromal cells on activation of microglial cells and production of inflammatory factors induced by lipopolysaccharide. Brain Res. 2009, 1269:23-30.