Therapeutic angiogenesis in critical limb Ischemia

Angiology

Volumn 64, Issue 6, 2013, Pages 466-480

  Ouma, Geoffrey O ^a   Zafrir, Barak ^b   Mohler, Emile R ^a   Flugelman, Moshe Y ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CARMEL MEDICAL CENTER   (Israel)

Author keywords

cell therapy; critical limb ischemia; endovascular therapy; gene therapy; medical therapy; surgical therapy; therapeutic angiogenesis

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOTENSIN II; CARNITINE; CILOSTAZOL; CLOPIDOGREL; DIPYRIDAMOLE; ENDOTHELIN 1; GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1; NAFTIDROFURYL; NITRIC OXIDE; PENTOXIFYLLINE; SCATTER FACTOR; VASCULOTROPIN;

ANGIOGENESIS; ANGIOGENIC GENE THERAPY; ANTICOAGULANT THERAPY; BLOOD PRESSURE REGULATION; CARDIOVASCULAR DISEASE; CELL TRANSPLANTATION; CRITICAL LIMB ISCHEMIA; DIABETES MELLITUS; DOWN REGULATION; DRUG MECHANISM; EXERCISE; HUMAN; INTERMITTENT CLAUDICATION; LIFESTYLE MODIFICATION; MESENCHYMAL STEM CELL TRANSPLANTATION; META ANALYSIS (TOPIC); MULTICENTER STUDY (TOPIC); NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRACTICE GUIDELINE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVASCULARIZATION; REVIEW; SMOKING CESSATION; THERAPEUTIC ANGIOGENESIS; VASOCONSTRICTION; WALKING;

CELL THERAPY; CRITICAL LIMB ISCHEMIA; ENDOVASCULAR THERAPY; GENE THERAPY; MEDICAL THERAPY; SURGICAL THERAPY; THERAPEUTIC ANGIOGENESIS;

ANGIOGENIC PROTEINS; ANIMALS; BONE MARROW TRANSPLANTATION; CARDIOVASCULAR AGENTS; CRITICAL ILLNESS; ENDOVASCULAR PROCEDURES; GENETIC THERAPY; HUMANS; ISCHEMIA; LOWER EXTREMITY; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME; VASCULAR SURGICAL PROCEDURES; WOUND HEALING;

EID: 84881249641     PISSN: 00033197     EISSN: 19401574     Source Type: Journal    
DOI: 10.1177/0003319712464514     Document Type: Review

References (118)

1. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-society consensus for the management of peripheral arterial disease (TASC II). J Vasc Surg. 2007 ; 45 (suppl S). S5 - S67
2. Criqui MH. Peripheral arterial disease - epidemiological aspects. Vasc Med. 2001 ; 6 (3 suppl). 3-7
3. Becker F, Robert-Ebadi H, Ricco JB, et al. Chapter I: definitions, epidemiology, clinical presentation and prognosis. Eur J Vasc Endovasc Surg. 2011 ; 42 (suppl 2). S4 - S12
4. Egorova NN, Guillerme S, Gelijns A, et al. An analysis of the outcomes of a decade of experience with lower extremity revascularization including limb salvage, lengths of stay, and safety. J Vasc Surg. 2011 ; 51 (4). 878-885
5. Fernandez N, McEnaney R, Marone LK, et al. Multilevel versus isolated endovascular tibial interventions for critical limb ischemia. J Vasc Surg. 2011 ; 54 (3). 722-729
6. Sachs T, Pomposelli F, Hamdan A, Wyers M, Schermerhorn M. Trends in the national outcomes and costs for claudication and limb threatening ischemia: angioplasty vs bypass graft. J Vasc Surg. 2011 ; 54 (4). 1021-1031
7. Sigala F, Georgopoulos S, Langer S, et al. Outcome of infrainguinal revascularization for critical limb ischemia in diabetics with end stage renal disease. Vasa. 2006 ; 35 (1). 15-20
8. Venermo M, Biancari F, Arvela E, et al. The role of chronic kidney disease as a predictor of outcome after revascularisation of the ulcerated diabetic foot. Diabetologia. 2011 ; 54 (12). 2971-2977
9. Tongers J, Roncalli JG, Losordo DW. Therapeutic angiogenesis for critical limb ischemia: microvascular therapies coming of age. Circulation. 2008 ; 118 (1). 9-16
10. Creager MA, Olin JW, Belch JJ, et al. Effect of hypoxia-inducible factor-1alpha gene therapy on walking performance in patients with intermittent claudication. Circulation. 2011 ; 124 (16). 1765-1773
11. Rooke TW, Hirsch AT, Misra S, et al. ACCF/AHA Focused update of the guideline for the management of patients with peripheral artery disease (updating the 2005 guideline): a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2011 ; 58 (19). 2020-2045
12. Tendera M, Aboyans V, Bartelink ML, et al. ESC Guidelines on the diagnosis and treatment of peripheral artery diseases: document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteries: the Task Force on the Diagnosis and Treatment of Peripheral Artery Diseases of the European Society of Cardiology (ESC). Eur Heart J. 2011 ; 32 (22). 2851-2906
13. Hankey GJ, Norman PE, Eikelboom JW. Medical treatment of peripheral arterial disease. JAMA. 2006 ; 295 (5). 547-553
14. Hobbs SD, Bradbury AW. Smoking cessation strategies in patients with peripheral arterial disease: an evidence-based approach. Eur J Vasc Endovasc Surg. 2003 ; 26 (4). 341-347
15. Gardner AW, Poehlman ET. Exercise rehabilitation programs for the treatment of claudication pain. A meta-analysis. JAMA. 1995 ; 274 (12). 975-980
16. Watson L, Ellis B, Leng GC.. Exercise for intermittent claudication. Cochrane Database Syst Rev. 2008 ; (4). CD000990
17. CAPRIE Steering Committee. Lancet. 1996 ; 348 (9038). 1329-1339
18. Baigent C, Blackwell L, Collins R, et al. Aspirin in the primary and secondary prevention of vascular disease: collaborative meta-analysis of individual participant data from randomised trials. Lancet. 2009 ; 373 (9678). 1849-1860
19. Dorffler-Melly J, Buller HR, Koopman MM, Prins MH.. Antithrombotic agents for preventing thrombosis after infrainguinal arterial bypass surgery. Cochrane Database Syst Rev. 2003 ; (4). CD000536
20. Berger JS, Krantz MJ, Kittelson JM, Hiatt WR. Aspirin for the prevention of cardiovascular events in patients with peripheral artery disease: a meta-analysis of randomized trials. JAMA. 2009 ; 301 (18). 1909-1919
21. Belch J, MacCuish A, Campbell I, et al. The prevention of progression of arterial disease and diabetes (POPADAD) trial: factorial randomised placebo controlled trial of aspirin and antioxidants in patients with diabetes and asymptomatic peripheral arterial disease. BMJ. 2008 ; 337: a1840
22. Ogawa H, Nakayama M, Morimoto T, et al. Low-dose aspirin for primary prevention of atherosclerotic events in patients with type 2 diabetes: a randomized controlled trial. JAMA. 2008 ; 300 (18). 2134-2141
23. Fowkes FG, Price JF, Stewart MC, et al. Aspirin for prevention of cardiovascular events in a general population screened for a low ankle brachial index: a randomized controlled trial. JAMA. 2010 ; 303 (9). 841-848
24. Mehler PS, Coll JR, Estacio R, Esler A, Schrier RW, Hiatt WR. Intensive blood pressure control reduces the risk of cardiovascular events in patients with peripheral arterial disease and type 2 diabetes. Circulation. 2003 ; 107 (5). 753-756
25. Virkkunen J, Heikkinen M, Lepantalo M, Metsanoja R, Salenius JP. Diabetes as an independent risk factor for early postoperative complications in critical limb ischemia. J Vasc Surg. 2004 ; 40 (4). 761-767
26. Reiner Z, Catapano AL, De Backer G, et al. ESC/EAS Guidelines for the management of dyslipidaemias: the Task Force for the management of dyslipidaemias of the European Society of Cardiology (ESC) and the European Atherosclerosis Society (EAS). Eur Heart J. 2011 ; 32 (14). 1769-1818
27. Schillinger M, Exner M, Mlekusch W, et al. Statin therapy improves cardiovascular outcome of patients with peripheral artery disease. Eur Heart J. 2004 ; 25 (9). 742-748
28. Randomized trial of the effects of cholesterol-lowering with simvastatin on peripheral vascular and other major vascular outcomes in 20,536 people with peripheral arterial disease and other high-risk conditions. J Vasc Surg. 2007 ; 45 (4). 645-654
29. Schanzer A, Hevelone N, Owens CD, Beckman JA, Belkin M, Conte MS. Statins are independently associated with reduced mortality in patients undergoing infrainguinal bypass graft surgery for critical limb ischemia. J Vasc Surg. 2008 ; 47 (4). 774-781
30. Gulcan E, Gulcan A, Erbilen E, Toker S. Statins may be useful in diabetic foot ulceration treatment and prevention. Med Hypotheses. 2007 ; 69 (6). 1313-1315
31. El-Azab MF, Hazem RM, Moustafa YM. Role of simvastatin and/or antioxidant vitamins in therapeutic angiogenesis in experimental diabetic hindlimb ischemia: effects on capillary density, angiogenesis markers, and oxidative stress. Eur J Pharmacol. 2012 ; 690 (1-3). 31-41
32. Undas A, Celinska-Lowenhoff M, Stepien E, Nizankowski R, Tracz W, Szczeklik A. Effects of simvastatin on angiogenic growth factors released at the site of microvascular injury. Thromb Haemost. 2006 ; 95 (6). 1045-1047
33. Zhu XY, Daghini E, Chade AR, et al. Disparate effects of simvastatin on angiogenesis during hypoxia and inflammation. Life Sci. 2008 ; 83 (23-24). 801-809
34. Liu Y, Wei J, Hu S, Hu L. Beneficial effects of statins on endothelial progenitor cells. Am J Med Sci. 2012 ; 344 (3). 220-226
35. Nagaya N. Orally active prostacyclin analogue for cardiovascular disease. Int Angiol. 2010 ; 29 (2 suppl). 14-18
36. Creutzig A, Lehmacher W, Elze M. Meta-analysis of randomised controlled prostaglandin E1 studies in peripheral arterial occlusive disease stages III and IV. Vasa. 2004 ; 33 (3). 137-144
37. Ruffolo AJ, Romano M, Ciapponi A.. Prostanoids for critical limb ischaemia. Cochrane Database Syst Rev. 2010 ; (1). CD006544
38. Gersbach PA, Argitis V, Gardaz JP, von Segesser LK, Haesler E. Late outcome of spinal cord stimulation for unreconstructable and limb-threatening lower limb ischemia. Eur J Vasc Endovasc Surg. 2007 ; 33 (6). 717-724
39. Ubbink DT, Vermeulen H, Spincemaille GH, Gersbach PA, Berg P, Amann W. Systematic review and meta-analysis of controlled trials assessing spinal cord stimulation for inoperable critical leg ischaemia. Br J Surg. 2004 ; 91 (8). 948-955
40. de Haro J, Acin F, Florez A, Bleda S, Fernandez JL. A prospective randomized controlled study with intermittent mechanical compression of the calf in patients with claudication. J Vasc Surg. 2010 ; 51 (4). 857-862
41. Kavros SJ, Delis KT, Turner NS, et al. Improving limb salvage in critical ischemia with intermittent pneumatic compression: a controlled study with 18-month follow-up. J Vasc Surg. 2008 ; 47 (3). 543-549
42. Labropoulos N, Leon LR, Bhatti A, et al. Hemodynamic effects of intermittent pneumatic compression in patients with critical limb ischemia. J Vasc Surg. 2005 ; 42 (4). 710-716
43. Kranke P, Bennett M, Roeckl-Wiedmann I, Debus S.. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev. 2004 ; (2). CD004123
44. Arain SA, White CJ. Endovascular therapy for critical limb ischemia. Vasc Med. 2008 ; 13 (3). 267-279
45. Dosluoglu HH, O'Brien-Irr MS, Lukan J, Harris LM, Dryjski ML, Cherr GS. Does preferential use of endovascular interventions by vascular surgeons improve limb salvage, control of symptoms, and survival of patients with critical limb ischemia?. Am J Surg. 2006 ; 192 (5). 572-576
46. Kudo T, Chandra FA, Kwun WH, Haas BT, Ahn SS. Changing pattern of surgical revascularization for critical limb ischemia over 12 years: endovascular vs. open bypass surgery. J Vasc Surg. 2006 ; 44 (2). 304-313
47. Adam DJ, Beard JD, Cleveland T, et al. Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet. 2005 ; 366 (9501). 1925-1934
48. Melliere D, Cron J, Allaire E, Desgranges P, Becquemin JP. Indications and benefits of simultaneous endoluminal balloon angioplasty and open surgery during elective lower limb revascularization. Cardiovasc Surg. 1999 ; 7 (2). 242-246
49. Kalka C, Baumgartner I. Gene and stem cell therapy in peripheral arterial occlusive disease. Vasc Med. 2008 ; 13 (2). 157-172
50. Dedieu JF, Mahfoudi A, Le Roux A, Branellec D. Vectors for gene therapy of cardiovascular disease. Curr Cardiol Rep. 2000 ; 2 (1). 39-47
51. Baffour R, Berman J, Garb JL, Rhee SW, Kaufman J, Friedmann P. Enhanced angiogenesis and growth of collaterals by in vivo administration of recombinant basic fibroblast growth factor in a rabbit model of acute lower limb ischemia: dose-response effect of basic fibroblast growth factor. J Vasc Surg. 1992 ; 16 (2). 181-191
52. Bobek V, Taltynov O, Pinterova D, Kolostova K. Gene therapy of the ischemic lower limb - Therapeutic angiogenesis. Vascul Pharmacol. 2006 ; 44 (6). 395-405
53. Takeshita S, Zheng LP, Brogi E, et al. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest. 1994 ; 93 (2). 662-670
54. Kusumanto YH, van Weel V, Mulder NH, et al. Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial. Hum Gene Ther. 2006 ; 17 (6). 683-691
55. Makinen K, Manninen H, Hedman M, et al. Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase II study. Mol Ther. 2002 ; 6 (1). 127-133
56. Rajagopalan S, Mohler ER, Lederman RJ, et al. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation. 2003 ; 108 (16). 1933-1938
57. Nikol S, Baumgartner I, Van Belle E, et al. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther. 2008 ; 16 (5). 972-978
58. Belch J, Hiatt WR, Baumgartner I, et al. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet. 2011 ; 377 (9781). 1929-1937
59. Lederman RJ, Mendelsohn FO, Anderson RD, et al. Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study): a randomised trial. Lancet. 2002 ; 359 (9323). 2053-2058
60. Powell RJ, Simons M, Mendelsohn FO, et al. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation. 2008 ; 118 (1). 58-65
61. Powell RJ, Goodney P, Mendelsohn FO, Moen EK, Annex BH. Safety and efficacy of patient specific intramuscular injection of HGF plasmid gene therapy on limb perfusion and wound healing in patients with ischemic lower extremity ulceration: results of the HGF-0205 trial. J Vasc Surg. 2010 ; 52 (6). 1525-1530
62. Shigematsu H, Yasuda K, Iwai T, et al. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther. 2010 ; 17 (9). 1152-1161
63. Yla-Herttuala S. Gene therapy with vascular endothelial growth factors. Biochem Soc Trans. 2009 ; 37 (6). 1198-2000
64. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003 ; 9 (6). 669-676
65. Yla-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J. Vascular endothelial growth factors: biology and current status of clinical applications in cardiovascular medicine. J Am Coll Cardiol. 2007 ; 49 (10). 1015-1026
66. Isner JM, Pieczek A, Schainfeld R, et al. Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb. Lancet. 1996 ; 348 (9024). 370-374
67. Baumgartner I, Pieczek A, Manor O, et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation. 1998 ; 97 (12). 1114-1123
68. Shyu KG, Chang H, Wang BW, Kuan P. Intramuscular vascular endothelial growth factor gene therapy in patients with chronic critical leg ischemia. Am J Med. 2003 ; 114 (2). 85-92
69. Rajagopalan S, Trachtenberg J, Mohler E, et al. Phase I study of direct administration of a replication deficient adenovirus vector containing the vascular endothelial growth factor cDNA (CI-1023) to patients with claudication. Am J Cardiol. 2002 ; 90 (5). 512-516
70. Mohler ER, Rajagopalan S, Olin JW, et al. Adenoviral-mediated gene transfer of vascular endothelial growth factor in critical limb ischemia: safety results from a phase I trial. Vasc Med. 2003 ; 8 (1). 9-13
71. Dor Y, Djonov V, Abramovitch R, et al. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 2002 ; 21 (8). 1939-1947
72. Murakami M, Simons M. Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 2008 ; 15 (3). 215-220
73. Comerota AJ, Throm RC, Miller KA, et al. Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase I trial. J Vasc Surg. 2002 ; 35 (5). 930-936
74. Baumgartner I, Chronos N, Comerota A, et al. Local gene transfer and expression following intramuscular administration of FGF-1 plasmid DNA in patients with critical limb ischemia. Mol Ther. 2009 ; 17 (5). 914-921
75. Fowkes FG, Price JF. Gene therapy for critical limb ischaemia: the TAMARIS trial. Lancet. 2011 ; 377 (9781). 1894-1896
76. Morishita R, Nakamura S, Hayashi S, et al. Therapeutic angiogenesis induced by human recombinant hepatocyte growth factor in rabbit hind limb ischemia model as cytokine supplement therapy. Hypertension. 1999 ; 33 (6). 1379-1384
77. Morishita R, Aoki M, Hashiya N, et al. Safety evaluation of clinical gene therapy using hepatocyte growth factor to treat peripheral arterial disease. Hypertension. 2004 ; 44 (2). 203-209
78. Morishita R, Makino H, Aoki M, et al. Phase I/IIa clinical trial of therapeutic angiogenesis using hepatocyte growth factor gene transfer to treat critical limb ischemia. Arterioscler Thromb Vasc Biol. 2011 ; 31 (3). 713-720
79. Shigematsu H, Yasuda K, Sasajima T, et al. Transfection of human HGF plasmid DNA improves limb salvage in Buerger's disease patients with critical limb ischemia. Int Angiol. 2011 ; 30 (2). 140-149
80. Henry TD, Hirsch AT, Goldman J, et al. Safety of a non-viral plasmid-encoding dual isoforms of hepatocyte growth factor in critical limb ischemia patients: a phase I study. Gene Ther. 2011 ; 18 (8). 788-794
81. Ho TK, Abraham DJ, Black CM, Baker DM. Hypoxia-inducible factor 1 in lower limb ischemia. Vascular. 2006 ; 14 (6). 321-327
82. Yamakawa M, Liu LX, Date T, et al. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ Res. 2003 ; 93 (7). 664-673
83. Rajagopalan S, Olin J, Deitcher S, et al. Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase I dose-escalation experience. Circulation. 2007 ; 115 (10). 1234-1243
84. Giacca M. Virus-mediated gene transfer to induce therapeutic angiogenesis: where do we stand?. Int J Nanomedicine. 2007 ; 2 (4). 527-540
85. Gupta R, Tongers J, Losordo DW. Human studies of angiogenic gene therapy. Circ Res. 2009 ; 105 (8). 724-736
86. Rey S, Semenza GL. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res. 2010 ; 86 (2). 236-242
87. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A. 2000 ; 97 (7). 3422-3427
88. Yamaguchi J, Kusano KF, Masuo O, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation. 2003 ; 107 (9). 1322-1328
89. Kawamoto A, Katayama M, Handa N, et al. Intramuscular transplantation of G-CSF-mobilized CD34(+) cells in patients with critical limb ischemia: a phase I/IIa, multicenter, single-blinded, dose-escalation clinical trial. Stem Cells. 2009 ; 27 (11). 2857-2864
90. Burt RK, Testori A, Oyama Y, et al. Autologous peripheral blood CD133+ cell implantation for limb salvage in patients with critical limb ischemia. Bone Marrow Transplant. 2010 ; 45 (1). 111-116
91. Walter DH, Krankenberg H, Balzer JO, et al. Intraarterial administration of bone marrow mononuclear cells in patients with critical limb ischemia: a randomized-start, placebo-controlled pilot trial (PROVASA). Circ Cardiovasc Interv. 2011 ; 4 (1). 26-37
92. Powell RJ, Comerota AJ, Berceli SA, et al. Interim analysis results from the RESTORE-CLI, a randomized, double-blind multicenter phase II trial comparing expanded autologous bone marrow-derived tissue repair cells and placebo in patients with critical limb ischemia. J Vasc Surg. 2011 ; 54 (4). 1032-1041
93. Idei N, Soga J, Hata T, et al. Autologous bone-marrow mononuclear cell implantation reduces long-term major amputation risk in patients with critical limb ischemia: a comparison of atherosclerotic peripheral arterial disease and Buerger disease. Circ Cardiovasc Interv. 2011 ; 4 (1). 15-25
94. Lasala GP, Silva JA, Gardner PA, Minguell JJ. Combination stem cell therapy for the treatment of severe limb ischemia: safety and efficacy analysis. Angiology. 2010 ; 61 (6). 551-556
95. Lasala GP, Silva JA, Minguell JJ. Therapeutic angiogenesis in patients with severe limb ischemia by transplantation of a combination stem cell product. J Thorac Cardiovasc Surg. 2012 ; 144 (2). 377-382
96. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997 ; 275 (5302). 964-967
97. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999 ; 85 (3). 221-228
98. Shintani S, Murohara T, Ikeda H, et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation. 2001 ; 103 (6). 897-903
99. Mayr M, Niederseer D, Niebauer J. From bench to bedside: what physicians need to know about endothelial progenitor cells. Am J Med. 2011 ; 124 (6). 489-497
100. Rustemeyer P, Wittkowski W, Greve B, Stehling M. Flow-cytometric identification, enumeration, purification, and expansion of CD133+ and VEGF-R2+ endothelial progenitor cells from peripheral blood. J Immunoassay Immunochem. 2007 ; 28 (1). 13-23
101. Case J, Mead LE, Bessler WK, et al. Human CD34+AC133+VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol. 2007 ; 35 (7). 1109-1118
102. Timmermans F, Van Hauwermeiren F, De Smedt M, et al. Endothelial outgrowth cells are not derived from CD133+ cells or CD45+ hematopoietic precursors. Arterioscler Thromb Vasc Biol. 2007 ; 27 (7). 1572-1579
103. Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003 ; 348 (7). 593-600
104. van Royen N, Schirmer SH, Atasever B, et al. START Trial: a pilot study on STimulation of ARTeriogenesis using subcutaneous application of granulocyte-macrophage colony-stimulating factor as a new treatment for peripheral vascular disease. Circulation. 2005 ; 112 (7). 1040-1046
105. Kawamoto A, Iwasaki H, Kusano K, et al. CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation. 2006 ; 114 (20). 2163-2169
106. Murohara T, Ikeda H, Duan J, et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest. 2000 ; 105 (11). 1527-1536
107. Sieveking DP, Ng MK. Cell therapies for therapeutic angiogenesis: back to the bench. Vasc Med. 2009 ; 14 (2). 153-166
108. Tateishi-Yuyama E, Matsubara H, Murohara T, et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet. 2002 ; 360 (9331). 427-435
109. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002 ; 418 (6893). 41-49
110. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007 ; 25 (11). 2739-2749
111. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003 ; 31 (10). 890-896
112. Minguell JJ, Erices A. Mesenchymal stem cells and the treatment of cardiac disease. Exp Biol Med (Maywood). 2006 ; 231: 39-49
113. Kim HG, Choi OH. Neovascularization in a mouse model via stem cells derived from human fetal amniotic membranes. Heart Vessels. 2010 ; 26 (2). 196-205
114. Poncelet AJ, Hiel AL, Vercruysse J, Hermans D, Zech F, Gianello P. Intracardiac allogeneic mesenchymal stem cell transplantation elicits neo-angiogenesis in a fully immunocompetent ischaemic swine model. Eur J Cardiothorac Surg. 2010 ; 38 (6). 781-787
115. Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A. 2002 ; 99 (13). 8932-8937
116. Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 1995 ; 16 (4). 557-564
117. Hare JM, Traverse JH, Henry TD, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol. 2009 ; 54 (24). 2277-2286
118. Poh KK, Sperry E, Young RG, Freyman T, Barringhaus KG, Thompson CA. Repeated direct endomyocardial transplantation of allogeneic mesenchymal stem cells: safety of a high dose, "off-the-shelf", cellular cardiomyoplasty strategy. Int J Cardiol. 2007 ; 117 (3). 360-364