Bone marrow stromal cell therapy for ischemic stroke: A meta-analysis of randomized control animal trials

International Journal of Stroke

Volumn 12, Issue 3, 2017, Pages 273-284

  Wu, Qing ^a   Wang, Yuexiang ^b   Demaerschalk, Bart M ^c   Ghimire, Saruna ^a   Wellik, Kay E ^d   Qu, Wenchun ^b  

^a UNIVERSITY OF NEVADA   (United States)

^b MAYO CLINIC   (United States)

^c MAYO CLINIC HOSPITAL   (United States)

^d MAYO CLINIC   (United States)

Author keywords

Bone marrow stromal cell; modified Neurological Severity Score; pooled analysis; review; stem cell therapy efficacy; stroke repair; subgroup analysis; total infarction volume

Indexed keywords

ADHESIVE REMOVAL TEST; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW STROMA CELL; BONE MARROW STROMAL CELL THERAPY; BRAIN ISCHEMIA; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; FOLLOW UP; HEMATOPOIETIC STEM CELL TRANSPLANTATION; META ANALYSIS; NEUROLOGIC EXAMINATION; NEUROLOGICAL SEVERITY SCORE; NONHUMAN; RANDOMIZED CONTROLLED TRIAL; ROTAROD TEST; SAMPLE SIZE; SCORING SYSTEM; SENSITIVITY ANALYSIS; TREATMENT OUTCOME; ANIMAL; BONE MARROW TRANSPLANTATION; MESENCHYMAL STEM CELL TRANSPLANTATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); STROKE;

ANIMALS; BONE MARROW TRANSPLANTATION; BRAIN ISCHEMIA; MESENCHYMAL STEM CELL TRANSPLANTATION; RANDOMIZED CONTROLLED TRIALS AS TOPIC; STROKE;

EID: 85018738752     PISSN: 17474930     EISSN: 17474949     Source Type: Journal    
DOI: 10.1177/1747493016676617     Document Type: Article

References (68)

1. Centers for Disease Control and Prevention. Leading causes of death. Atlanta, GA: Centers for Disease Control and Prevention, http://www.cdc.gov/nchs/fastats/leading-causes-of-death.htm (2015, 1 November 2015)
2. Donnan GA, Fisher M, Macleod M, Davis SM. Stroke. Lancet 2008; 371: 1612–1623.
3. American Heart Association. Types of stroke. Dallas, TX: American Heart Association, http://www.strokeassociation.org/STROKEORG/AboutStroke/TypesofStroke/Types-of-Stroke_UCM_308531_SubHomePage.jsp (2015, 1 November 2015)
4. Bendszus M, Urbach H, Ries F, Solymosi L. Outcome after local intra-arterial fibrinolysis compared with the natural course of patients with a dense middle cerebral artery on early CT. Neuroradiology 1998; 40: 54–58.
5. Ciccone A, Valvassori L. Synthesis Expansion Investigators. Endovascular treatment for acute ischemic stroke. N Engl J Med 2013; 368: 2433–2434.
6. Fields JD, Khatri P, Nesbit GM. Meta-analysis of randomized intra-arterial thrombolytic trials for the treatment of acute stroke due to middle cerebral artery occlusion. J Neurointerv Surg 2011; 3: 151–155.
7. Adams HP, Jr Adams RJ, Brott T. Stroke Council of the American Stroke Association. Guidelines for the early management of patients with ischemic stroke: a scientific statement from the Stroke Council of the American Stroke Association. Stroke 2003; 34: 1056–1083.
8. Krampera M, Marconi S, Pasini A. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 2007; 40: 382–390.
9. Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 2005; 23: 392–402.
10. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076–1084.
11. Meirelles Lda S, Fontes AM, Covas DT, Caplan AI. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 2009; 20: 419–427.
12. Uccelli A, Benvenuto F, Laroni A, Giunti D. Neuroprotective features of mesenchymal stem cells. Best Pract Res Clin Haematol 2011; 24: 59–64.
13. Augello A, Kurth TB, De Bari C. Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. Eur Cell Mater 2010; 20: 121–133.
14. Janowski M, Walczak P, Date I. Intravenous route of cell delivery for treatment of neurological disorders: a meta-analysis of preclinical results. Stem Cells Dev 2010; 19: 5–16.
15. Lees JS, Sena ES, Egan KJ. Stem cell-based therapy for experimental stroke: a systematic review and meta-analysis. Int J Stroke 2012; 7: 582–588.
16. Dharmasaroja P. Bone marrow-derived mesenchymal stem cells for the treatment of ischemic stroke. J Clin Neurosci 2009; 16: 12–20.
17. Vu Q, Xie K, Eckert M, Zhao W, Cramer SC. Meta-analysis of preclinical studies of mesenchymal stromal cells for ischemic stroke. Neurology 2014; 82: 1277–1286.
18. Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010; 8: 336–341. Erratum in: Int J Surg 2010; 8: 658.
19. Zhao LR, Duan WM, Reyes M, Keene CD, Verfaillie CM, Low WC. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 2002; 174: 11–20.
20. Borlongan CV, Lind JG, Dillon-Carter O. Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats. Brain Res 2004; 1010: 108–116.
21. Li Y, Chen J, Zhang CL. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 2005; 49: 407–417.
22. Zhang J, Li Y, Chen J. Expression of insulin-like growth factor 1 and receptor in ischemic rats treated with human marrow stromal cells. Brain Res 2004; 1030: 19–27.
23. Shen LH, Li Y, Chen J. Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience 2006; 137: 393–399.
24. Li Y, McIntosh K, Chen J. Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp Neurol 2006; 198: 313–325.
25. Shen LH, Li Y, Chen J. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 2007; 27: 6–13.
26. Zhang C, Li Y, Chen J. Bone marrow stromal cells upregulate expression of bone morphogenetic proteins 2 and 4, gap junction protein connexin-43 and synaptophysin after stroke in rats. Neuroscience 2006; 141: 687–695.
27. Shen LH, Li Y, Chen J. One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke 2007; 38: 2150–2156.
28. Okazaki T, Magaki T, Takeda M. Intravenous administration of bone marrow stromal cells increases survivin and Bcl-2 protein expression and improves sensorimotor function following ischemia in rats. Neurosci Lett 2008; 430: 109–114.
29. Chen JR, Cheng GY, Sheu CC, Tseng GF, Wang TJ, Huang YS. Transplanted bone marrow stromal cells migrate, differentiate and improve motor function in rats with experimentally induced cerebral stroke. J Anat 2008; 213: 249–258.
30. Pavlichenko N, Sokolova I, Vijde S. Mesenchymal stem cell transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res 2008; 1233: 203–213.
31. Omori Y, Honmou O, Harada K, Suzuki J, Houkin K, Kocsis JD. Optimization of a therapeutic protocol for intravenous injection of human mesenchymal stem cells after cerebral ischemia in adult rats. Brain Res 2008; 1236: 30–38.
32. Detante O, Moisan A, Dimastromatteo J. Intravenous administration of 99mTc-HMPAO-labeled human mesenchymal stem cells after stroke: in vivo imaging and biodistribution. Cell Transplant 2009; 18: 1369–1379.
33. Li J, Zhu H, Liu Y. Human mesenchymal stem cell transplantation protects against cerebral ischemic injury and upregulates interleukin-10 expression in Macacafascicularis. Brain Res 2010; 1334: 65–72.
34. Shen LH, Li Y, Chopp M. Astrocytic endogenous glial cell derived neurotrophic factor production is enhanced by bone marrow stromal cell transplantation in the ischemic boundary zone after stroke in adult rats. Glia 2010; 58: 1074–1081.
35. Bao X, Wei J, Feng M. Transplantation of human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and endogenous neurogenesis after cerebral ischemia in rats. Brain Res 2011; 1367: 103–113.
36. Gutierrez-Fernandez M, Rodriguez-Frutos B, Alvarez-Grech J. Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience 2011; 175: 394–405.
37. Shen LH, Xin H, Li Y. Endogenous tissue plasminogen activator mediates bone marrow stromal cell-induced neurite remodeling after stroke in mice. Stroke 2011; 42: 459–464.
38. Bao X, Feng M, Wei J. Transplantation of Flk-1+ human bone marrow-derived mesenchymal stem cells promotes angiogenesis and neurogenesis after cerebral ischemia in rats. Eur J Neurosci 2011; 34: 87–98.
39. Chen J, Ye X, Yan T. Adverse effects of bone marrow stromal cell treatment of stroke in diabetic rats. Stroke 2011; 42: 3551–3558.
40. Steiner B, Roch M, Holtkamp N, Kurtz A. Systemically administered human bone marrow-derived mesenchymal stem home into peripheral organs but do not induce neuroprotective effects in the MCAo-mouse model for cerebral ischemia. Neurosci Lett 2012; 513: 25–30.
41. Shen LH, Ye M, Ding XS. Protective effects of MCI-186 on transplantation of bone marrow stromal cells in rat ischemic stroke model. Neuroscience 2012; 223: 315–324.
42. Lee SH, Jin KS, Bang OY. Differential migration of mesenchymal stem cells to ischemic regions after middle cerebral artery occlusion in rats. PLoS One 2015; 10: e0134920.
43. Fukuda Y, Horie N, Satoh K. Intra-arterial transplantation of low-dose stem cells provides functional recovery without adverse effects after stroke. Cell Mol Neurobiol 2015; 35: 399–406.
44. Xu Y, Du S, Yu X, Han X, Hou J, Guo H. Human bone marrow mesenchymal stem cell transplantation attenuates axonal injury in stroke rats. Neural Regen Res 2014; 9: 2053–2058.
45. Calio ML, Marinho DS, Ko GM. Transplantation of bone marrow mesenchymal stem cells decreases oxidative stress, apoptosis, and hippocampal damage in brain of a spontaneous stroke model. Free Radic Biol Med 2014; 70: 141–154.
46. Ruan GP, Han YB, Wang TH. Comparative study among three different methods of bone marrow mesenchymal stem cell transplantation following cerebral infarction in rats. Neurol Res 2013; 35: 212–220.
47. Huang W, Mo X, Qin C, Zheng J, Liang Z, Zhang C. Transplantation of differentiated bone marrow stromal cells promotes motor functional recovery in rats with stroke. Neurol Res 2013; 35: 320–328.
48. Gutierrez-Fernandez M, Rodriguez-Frutos B, Ramos-Cejudo J. Effects of intravenous administration of allogenic bone marrow- and adipose tissue-derived mesenchymal stem cells on functional recovery and brain repair markers in experimental ischemic stroke. Stem Cell Res Ther 2013; 4: 11.
49. Ding X, Li Y, Liu Z. The sonic hedgehog pathway mediates brain plasticity and subsequent functional recovery after bone marrow stromal cell treatment of stroke in mice. J Cereb Blood Flow Metab 2013; 33: 1015–1024.
50. Bilen S, Pinarli F, Ak F. Treatment efficacy with bone marrow derived mesenchymal stem cells and minocycline in rats after cerebral ischemic injury. Stem Cell Rev 2013; 9: 219–225.
51. Zhang YX, Yuan MZ, Cheng L. Treadmill exercise enhances therapeutic potency of transplanted bone mesenchymal stem cells in cerebral ischemic rats via anti-apoptotic effects. BMC Neurosci 2015; 16: 56.
52. Jin-Yan L, Liang W. Therapeutic effect of erythropoietin gene-modified bone marrow mesenchymal stem cell transplantation on rat cerebral infarction. J Clin Rehabil Tissue Engin Res 2014; 23: 3664–3669.
53. Jin-Yan L, Zhang Z-C. Effect of bone marrow mesenchymal stem cells combined with Danhong injection on expression of GAP-43 and Bcl-2 after cerebral infarction. J Clin Rehabil Tissue Engin Res 2013; 32: 5871–5876.
54. Jing-jing S, Peng Z, Guo-Qing Z. Bone marrow mesencyhmal stem cell transplantation combined with edaravone for the treatment of cerebral infarction in rats. J Clin Rehabil Tissue Engin Res 2013; 19: 3467–3473.
55. Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001; 189: 49–57.
56. Chen J, Li Y, Wang L. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001; 32: 1005–1011.
57. Chen J, Li Y, Katakowski M. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 2003; 73: 778–786.
58. Li WY, Choi YJ, Lee PH. Mesenchymal stem cells for ischemic stroke: changes in effects after ex vivo culturing. Cell Transplant 2008; 17: 1045–1059.
59. Xin H, Li Y, Shen LH, Liu X. Increasing tPA activity in astrocytes induced by multipotent mesenchymal stromal cells facilitate neurite outgrowth after stroke in the mouse. PLoS One 2010; 5: e9027.
60. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap): a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 2009; 42: 377–381.
61. Stroke Therapy Academic Industry Roundtable (STAIR). Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999; 30: 2752–2758.
62. Fisher M, Feuerstein G, Howells DW. STAIR Group. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009; 40: 2244–2250.
63. Stroup DF, Berlin JA, Morton SC. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000; 283: 2008–2012.
64. Crossley NA, Sena E, Goehler J. Empirical evidence of bias in the design of experimental stroke studies: a metaepidemiologic approach. Stroke 2008; 39: 929–934.
65. Cohen J. Statistical power analysis for the behavioral sciences, 2nd ed. Hillsdale, NJ: L. Erlbaum Associates, 1988.
66. Borenstein M, Hedges LV, Higgins JPT and Rothstein HR. Introduction to meta-analysis. In: Effect sizes based on means. Chapter 4. Chichester, UK: John Wiley & Sons, 2009, pp.21–32
67. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557–560.
68. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629–634.