Progenitor cell therapy in patients with critical limb ischemia without surgical options

Annals of Surgery

Volumn 247, Issue 3, 2008, Pages 411-420

  Sprengers, Ralf W ^a,b   Lips, Daniel J ^a,b   Moll, Frans L ^a   Verhaar, Marianne C ^b  

^a Departments of Vascular Surgery   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANIMAL; BIOLOGICAL THERAPY; CRITICAL ILLNESS; HUMAN; ISCHEMIA; LIMB; PHYSIOLOGY; REVIEW; STEM CELL; VASCULARIZATION;

ANIMALS; CRITICAL ILLNESS; EXTREMITIES; HUMANS; ISCHEMIA; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELLS; TISSUE THERAPY;

EID: 42249088748     PISSN: 00034932     EISSN: 15281140     Source Type: Journal    
DOI: 10.1097/SLA.0b013e318153fdcb     Document Type: Review

References (91)

1. Dormandy J, Heeck L, Vig S. Predicting which patients will develop chronic critical leg ischemia. Semin Vasc Surg. 1999;12:138 -141.
2. Second European consensus document on chronic critical leg ischemia. Circulation. 1991;84:IV1-IV26.
3. Hooi JD, Stoffers HE, Knottnerus JA, et al. The prognosis of non-critical limb ischaemia: a systematic review of population-based evidence. Br J Gen Pract. 1999;49:49 -55.
4. Albers M, Fratezi AC, De LN. Assessment of quality of life of patients with severe ischemia as a result of infrainguinal arterial occlusive disease. J Vasc Surg. 1992;16:54 -59.
5. Gillum RF. Peripheral arterial occlusive disease of the extremities in the United States: hospitalization and mortality. Am Heart J. 1990;120:1414- 1418.
6. Hirsch AT, Haskal ZJ, Hertzer NR, et al. ACC/AHA 2005 practice guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery/ Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation. 2006;113:e463- e654.
7. Hooi JD, Kester AD, Stoffers HE, et al. Asymptomatic peripheral arterial occlusive disease predicted cardiovascular morbidity and mortality in a 7-year follow-up study. J Clin Epidemiol. 2004;57:294 -300.
8. Guidelines for Percutaneous Transluminal Angioplasty. Standards of Practice Committee of the Society of Cardiovascular and Interventional Radiology. Radiology. 1990;177:619-626.
9. Valentine RJ, Myers SI, Inman MH, et al. Late outcome of amputees with premature atherosclerosis. Surgery. 1996;119:487- 493.
10. Hiatt WR. Medical treatment of peripheral arterial disease and claudication. N Engl J Med. 2001;344:1608 -1621.
11. Singh S, Evans L, Datta D, et al. The costs of managing lower limbthreatening ischaemia. Eur J Vasc Endovasc Surg. 1996;12:359-362.
12. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964 -967.
13. Crosby JR, Kaminski WE, Schatteman G, et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res. 2000;87:728 -730.
14. 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;85:221-228.
15. Capla JM, Ceradini DJ, Tepper OM, et al. Skin graft vascularization involves precisely regulated regression and replacement of endothelial cells through both angiogenesis and vasculogenesis. Plast Reconstr Surg. 2006;117:836-844.
16. Shi Q, Rafii S, Wu MH, et al. Evidence for circulating bone marrowderived endothelial cells. Blood. 1998;92:362-367.
17. Rookmaaker MB, Smits AM, Tolboom H, et al. Bone-marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am J Pathol. 2003;163:553-562.
18. Shintani S, Murohara T, Ikeda H, et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation. 2001;103:2776 -2779.
19. Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434-438.
20. Shintani S, Murohara T, Ikeda H, et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation. 2001;103:897-903.
21. Kamihata H, Matsubara H, Nishiue T, et al. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation. 2001;104:1046 -1052.
22. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA. 2000;97:3422-3427.
23. Murohara T, Ikeda H, Duan J, et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest. 2000;105:1527-1536.
24. Finney MR, Greco NJ, Haynesworth SE, et al. Direct comparison of umbilical cord blood versus bone marrow-derived endothelial precursor cells in mediating neovascularization in response to vascular ischemia. Biol Blood Marrow Transplant. 2006;12:585-593.
25. Yoshida M, Horimoto H, Mieno S, et al. Intra-arterial bone marrow cell transplantation induces angiogenesis in rat hindlimb ischemia. Eur Surg Res. 2003;35:86 -91.
26. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001;7:430-436.
27. Kawamoto A, Gwon HC, Iwaguro H, et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001;103:634-637.
28. Dimmeler S, Zeiher AM, Schneider MD. Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest. 2005;115:572-583.
29. Boyle AJ, Schulman SP, Hare JM, et al. Is stem cell therapy ready for patients? Stem cell therapy for cardiac repair. Ready for the next step. Circulation. 2006;114:339 -352.
30. Oettgen P, Boyle AJ, Schulman SP, et al. Cardiac stem cell therapy. Need for optimization of efficacy and safety monitoring. Circulation. 2006;114:353-358.
31. 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;360:427- 435.
32. Esato K, Hamano K, Li TS, et al. Neovascularization induced by autologous bone marrow cell implantation in peripheral arterial disease. Cell Transplant. 2002;11:747-752.
33. Higashi Y, Kimura M, Hara K, et al. Autologous bone-marrow mononuclear cell implantation improves endothelium-dependent vasodilation in patients with limb ischemia. Circulation. 2004;109:1215-1218.
34. Miyamoto M, Yasutake M, Takano H, et al. Therapeutic angiogenesis by autologous bone marrow cell implantation for refractory chronic peripheral arterial disease using assessment of neovascularization by 99mTc-tetrofosmin (TF) perfusion scintigraphy. Cell Transplant. 2004;13:429-437.
35. Saigawa T, Kato K, Ozawa T, et al. Clinical application of bone marrow implantation in patients with arteriosclerosis obliterans, and the associ- ation between efficacy and the number of implanted bone marrow cells. Circ J. 2004;68:1189 -1193.
36. Bartsch T, Falke T, Brehm M, et al. [Transplantation of autologous adult bone marrow stem cells in patients with severe peripheral arterial occlusion disease]. Med Klin (Munich). 2006;101(suppl 1):195-197.
37. Durdu S, Akar AR, Arat M, et al. Autologous bone-marrow mononuclear cell implantation for patients with Rutherford grade II-III thromboangiitis obliterans. J Vasc Surg. 2006;44:732-739.
38. Miyamoto K, Nishigami K, Nagaya N, et al. Unblinded pilot study of autologous transplantation of bone marrow mononuclear cells in patients with thromboangiitis obliterans. Circulation. 2006;114:2679 -2684.
39. Kajiguchi M, Kondo T, Izawa H, et al. Safety and efficacy of autologous progenitor cell transplantation for therapeutic angiogenesis in patients with critical limb ischemia. Circ J. 2007;71:196 -201.
40. Honold J, Lehmann R, Heeschen C, et al. Effects of granulocyte colony simulating factor on functional activities of endothelial progenitor cells in patients with chronic ischemic heart disease. Arterioscler Thromb Vasc Biol. 2006;26:2238 -2243.
41. Huang P, Li S, Han M, et al. Autologous transplantation of granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care. 2005;28: 2155-2160.
42. Huang PP, Li SZ, Han MZ, et al. Autologous transplantation of peripheral blood stem cells as an effective therapeutic approach for severe arteriosclerosis obliterans of lower extremities. Thromb Haemost. 2004; 91:606-609.
43. Kawamura A, Horie T, Tsuda I, et al. Prevention of limb amputation in patients with limbs ulcers by autologous peripheral blood mononuclear cell implantation. Ther Apher Dial. 2005;9:59-63.
44. Ishida A, Ohya Y, Sakuda H, et al. Autologous peripheral blood mononuclear cell implantation for patients with peripheral arterial disease improves limb ischemia. Circ J. 2005;69:1260 -1265.
45. Kawamura A, Horie T, Tsuda I, et al. Clinical study of therapeutic angiogenesis by autologous peripheral blood stem cell (PBSC) transplantation in 92 patients with critically ischemic limbs. J Artif Organs. 2006;9:226 -233.
46. Kudo FA, Nishibe T, Nishibe M, et al. Autologous transplantation of peripheral blood endothelial progenitor cells (CD34+) for therapeutic angiogenesis in patients with critical limb ischemia. Int Angiol. 2003; 22:344 -348.
47. Canizo MC, Lozano F, Gonzalez-Porras JR, et al. Peripheral endothelial progenitor cells (CD133+) for therapeutic vasculogenesis in a patient with critical limb ischemia. One year follow-up. Cytotherapy. 2007;9:99-102.
48. Sugihara S, Yamamoto Y, Matsubara K, et al. Autoperipheral blood mononuclear cell transplantation improved giant ulcers due to chronic arteriosclerosis obliterans. Heart Vessels. 2006;21:258 -262.
49. Lenk K, Adams V, Lurz P, et al. Therapeutical potential of blood-derived progenitor cells in patients with peripheral arterial occlusive disease and critical limb ischaemia. Eur Heart J. 2005;26:1903-1909.
50. Bartsch T, Brehm M, Zeus T, et al. Autologous mononuclear stem cell transplantation in patients with peripheral occlusive arterial disease. J Cardiovasc Nurs. 2006;21:430-432.
51. Bartsch T, Falke T, Brehm M, et al. [Intra-arterial and intramuscular transplantation of adult, autologous bone marrow stem cells. Novel treatment for therapy-refractory peripheral arterial occlusive disease]. Dtsch Med Wochenschr. 2006;131:79-83.
52. Rookmaaker MB, Verhaar MC, Loomans CJ, et al. CD34+ cells home, proliferate, and participate in capillary formation, and in combination with. Arterioscler Thromb Vasc Biol. 2005;25:1843-1850.
53. Harraz M, Jiao C, Hanlon HD, et al. CD34- blood-derived human endothelial cell progenitors. Stem Cells. 2001;19:304 -312.
54. Fernandez PB, Lucibello FC, Gehling UM, et al. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation. 2000; 65:287-300.
55. Rehman J, Li J, Orschell CM, et al. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003;107:1164 -1169.
56. Urbich C, Heeschen C, Aicher A, et al. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation. 2003;108:2511-2516.
57. Iba O, Matsubara H, Nozawa Y, et al. Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation. 2002;106:2019 -2025.
58. Tateno K, Minamino T, Toko H, et al. Critical roles of muscle-secreted angiogenic factors in therapeutic neovascularization. Circ Res. 2006;98: 1194-1202.
59. Ziegelhoeffer T, Fernandez B, Kostin S, et al. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res. 2004;94:230 -238.
60. Heil M, Ziegelhoeffer T, Mees B, et al. A different outlook on the role of bone marrow stem cells in vascular growth: bone marrow delivers software not hardware. Circ Res. 2004;94:573-574.
61. Dzau VJ, Gnecchi M, Pachori AS, et al. Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension. 2005;46:7-18.
62. Assmus B, Schachinger V, Teupe C, et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation. 2002;106:3009 -3017.
63. Seeger FH, Tonn T, Krzossok N, et al. Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J. 2007;28:766 -772.
64. Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:E1-E7.
65. Fadini GP, Sartore S, Albiero M, et al. Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler Thromb Vasc Biol. 2006;26:2140 -2146.
66. Heeschen C, Lehmann R, Honold J, et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation. 2004;109: 1615-1622.
67. Dimmeler S, Aicher A, Vasa M, et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest. 2001;108:391-397.
68. Llevadot J, Murasawa S, Kureishi Y, et al. HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest. 2001;108:399-405.
69. Vasa M, Fichtlscherer S, Adler K, et al. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation. 2001;103:2885-2890.
70. Assmus B, Urbich C, Aicher A, et al. HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res. 2003;92: 1049-1055.
71. Shantsila E, Watson T, Lip GY. Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol. 2007;49:741-752.
72. Pistrosch F, Herbrig K, Oelschlaegel U, et al. PPARgamma-agonist rosiglitazone increases number and migratory activity of cultured endothelial progenitor cells. Atherosclerosis. 2005;183:163-167.
73. Wang CH, Ting MK, Verma S, et al. Pioglitazone increases the numbers and improves the functional capacity of endothelial progenitor cells in patients with diabetes mellitus. Am Heart J. 2006;152:1051-1058.
74. Sasaki K, Heeschen C, Aicher A, et al. Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy. Proc Natl Acad Sci USA. 2006;103:14537-14541.
75. Akita T, Murohara T, Ikeda H, et al. Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Lab Invest. 2003;83:65-73.
76. Iwaguro H, Yamaguchi J, Kalka C, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation. 2002;105:732-738.
77. Yi C, Xia W, Zheng Y, et al. Transplantation of endothelial progenitor cells transferred by vascular endothelial growth factor gene for vascular regeneration of ischemic flaps. J Surg Res. 2006;135:100 -106.
78. Choi JH, Hur J, Yoon CH, et al. Augmentation of therapeutic angiogenesis using genetically modified human endothelial progenitor cells with altered glycogen synthase kinase-3beta activity. J Biol Chem. 2004;279: 49430-49438.
79. Napoli C, Williams-Ignarro S, de NF, et al. Beneficial effects of concurrent autologous bone marrow cell therapy and metabolic inter- vention in ischemia-induced angiogenesis in the mouse hindlimb. Proc Natl Acad Sci USA. 2005;102:17202-17206.
80. Zhou B, Poon MC, Pu WT, et al. Therapeutic neovascularization for peripheral arterial diseases: advances and perspectives. Histol Histopathol. 2007;22:677- 686.
81. Zhang M, Methot D, Poppa V, et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol. 2001;33:907-921.
82. Toma C, Pittenger MF, Cahill KS, et al. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105:93-98.
83. Strauer BE, Brehm M, Zeus T, et al. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation. 2002;106:1913-1918.
84. Chavakis E, Aicher A, Heeschen C, et al. Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med. 2005;201:63-72.
85. Hayashi M, Li TS, Ito H, et al. Comparison of intramyocardial and intravenous routes of delivering bone marrow cells for the treatment of ischemic heart disease: an experimental study. Cell Transplant. 2004; 13:639-647.
86. Hou D, Youssef EA, Brinton TJ, et al. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation. 2005;112:I150 -I156.
87. Iwasaki H, Kawamoto A, Ishikawa M, et al. Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation. 2006;113:1311-1325.
88. Britten MB, Abolmaali ND, Assmus B, et al. Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrastenhanced magnetic resonance imaging. Circulation. 2003;108:2212-2218.
89. Choksy SA, Chan P. Therapeutic angiogenesis. Br J Surg. 2006;93:261-263.
90. Norgren L, Hiatt WR, Dormandy JA, et al. Inter-society consensus for the management of peripheral arterial disease (TASC II). J Vasc Surg. 2007;45:S5-S67.
91. Rutherford RB, Baker JD, Ernst C, et al. Recommended standards for reports dealing with lower extremity ischemia: revised version. J Vasc Surg. 1997;26:517-538.