Adult stem cells and the clinical arena: Are we able to widely use this therapy in patients with chronic limbs arteriopathy and ischemic ulcers without possibility of revascularization?

Cardiovascular and Hematological Agents in Medicinal Chemistry

Volumn 10, Issue 2, 2012, Pages 99-108

  Casamassimi, Amelia ^a   Grimaldi, Vincenzo ^a   Infante, Teresa ^b   Al Omran, Mohammed ^c   Crudele, Valeria ^a   Napoli, Claudio ^a,b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b IRCCS SDN   (Italy)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Angiogenesis; Autologous transplantation; Bone marrow cells; Circulating endothelial progenitor cells; Clinical trials; Fontaine's stage; Gangrene; Intermittent claudication; Limb ischemia; Peripheral arterial disease; Revascularization

Indexed keywords

ANTITHROMBOCYTIC AGENT; CARNITINE; FIBROBLAST GROWTH FACTOR 2; PENTOXIFYLLINE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ADULT STEM CELL; AMPUTATION; ANGIOGENESIS; ARTICLE; BONE MARROW CELL; CELL THERAPY; CHRONIC DISEASE; DIABETES MELLITUS; DIABETIC FOOT; DYSLIPIDEMIA; ENDOTHELIAL PROGENITOR CELL; GANGRENE; HUMAN; HYPERTENSION; INTERMITTENT CLAUDICATION; ISCHEMIA; LEG REVASCULARIZATION; LEG ULCER; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PERIPHERAL VASCULAR DISEASE; PREVALENCE; REVASCULARIZATION; SMOKING; STEM CELL TRANSPLANTATION;

EID: 84860485821     PISSN: 18715257     EISSN: 18756182     Source Type: Journal    
DOI: 10.2174/187152512800388920     Document Type: Article

References (65)

1. Norgren, L.; Hiatt, W.R.; Dormandy, J.A.; Nehler, M.R.; Harris, K.A.; Fowkes, F.G.; Bell, K.; Caporusso, J.; Durand-Zaleski, I.; Komori, K.; Lammer, J.; Liapis, C.; Novo, S.; Razavi, M.; Robbs, J.; Schaper, N.; Shigematsu, H.; Sapoval, M.; White, C.; White, J.; Clement, D.; Creager, M.; Jaff, M.; Mohler, E., Rutherford, R.B.; Sheehan, P.; Sillesen, H.; Rosenfield, K. Inter-society consensus for the management of peripheral arterial disease [TASC II]. Eur. J. Vasc. Endovasc. Surg., 2007, 33(Suppl. 1), S1-S75.
2. Aranguren, X.L.; Varfaille C.M.; Luttun, A. Emerging hurdles in stem cell therapy for peripheral vascular disease. J. Mol. Med., 2009, 87(1), 3-16.
3. Napoli, C.; Farzati, B.; Sica, V.; Iannuzzi, E.; Coppola, G.; Silvestroni, A.; Balestrieri, M.L.; Florio, A.; Matarazzo, A. Beneficial effects of autologous bone marrow cell infusion and antioxidant/L-arginine in patient with chronic critical limb ischemia. Eur. J. Cardiovasc. Prev. Rehabil., 2008, 15(6), 709-718.
4. Stoffers, H.-E.-J.-H.; Kaiser, V.; Knottnerus, J.-A. Prevalence in general practice. In: Fowkes FGR ed. Epidemiology of peripheral vascular disease. Springer-Verlag: London, 1991.
5. Fowkes, F.G.; Housley, E.; Cawood, E.H.; Macintyre, C.C.; Ruckley, C.V.; Prescott, R.J. Edinburgh Artery Study: prevalence of asymptomatic and symptomatic peripheral arterial disease in the general population. Int. J. Epidemiol., 1991, 20(2), 384-392.
6. Smith, W.-C.-S.; Woodward, M.; Tunstall-Pedoe, H. Intermittent claudication in Scotland. In: Fowkes FGR ed. Epidemiology of peripheral vascular disease. Springer-Verlag: London, 1991.
7. Novo, S.; Avellone, G.; Di Garbo, V.; Abrignani, M.G.; Liquori, M.; Panno, A.V.; Strano, A. Prevalence of risk factors in patients with peripheral arterial disease: a clinical and epidemiological evaluation. Int. Angiol., 1992, 11(3), 218-229.
8. Meijer, W.T.; Hoes, A.W.; Rutgers, D.; Bots, M.L.; Hofman, A.; Grobbee, D.E. Peripheral arterial disease in the elderly: the Rotterdam study. Arterioscler. Thromb. Vasc. Biol., 1998, 18(2), 185-192.
9. Collinson, D.J.; Donnelly, R. Therapeutic angiogenesis in peripheral arterial disease: can biotechnology produce an effective collateral circulation? Eur. J. Vasc. Endovasc. Surg., 2004, 28(1), 9-23.
10. Carmeliet, P. Angiogenesis in health and disease. Nat Med., 2003, 9(6), 653-660.
11. Schaper, W.; Buschmann, I. Collateral circulation and diabetes. Circulation, 1999, 99(17), 2224-2226.
12. Rey, S.; Semenza, G.L. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc. Res., 2010, 86(2), 236-242.
13. Unthank, J.L.; Sheridan, K.M.; Dalsing, M.C. Collateral growth in the peripheral circulation: a review. Vasc. Endovascular Surg., 2004, 38(4), 291-313.
14. Schierling, W.; Troidl, K.; Troidl, C.; Schmitz-Rixen, T.; Schaper, W.; Eitenmuller, IK. The role of angiogenic growth factors in arteriogenesis. J. Vasc. Res., 2009, 46(4), 365-374.
15. Pan, S. Molecular mechanisms responsible for the atheroprotective effects of laminar shear stress. Antioxid. Redox. Signal., 2009, 11(7), 1669-1682.
16. Virag, J.I.; Murry, C.E. Myofibroblast and endothelial cell proliferation during murine myocardial infarct repair. Am. J. Pathol., 2003, 163(6), 2433-2440.
17. Tongers, J.; Roncalli, J.G.; Losordo, D.W. Role of endothelial progenitor cells during ischemia-induced vasculogenesis and collateral formation. Microvasc. Res., 2010, 79(3), 200-206.
18. Shintani, S.; Murohara, T.; Ikeda, H.; Ueno, T.; Honma, T.; Katoh, A.; Sasaki, K.; Shimada, T.; Oike, Y.; Imaizumi, T. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation, 2001, 103(23), 2776-2779.
19. Asahara, T.; Takahashi, T.; Masuda, H.; Kalka, C.; Chen, D.; Iwaguro, H.; Inai, Y.; Silver, M.; Isner, J.M. VEGF contributes to postnatal neovascularisation by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J., 1999, 18(14), 3964-3972.
20. Kinnaird, T.; Stabile, E.; Burnett, M.S.; Epstein, S.E. Bone marrow-derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences. Circ. Res., 2004, 95(4), 354-363.
21. Napoli, C.; Hayashi, T.; Cacciatore, F.; Casamassimi, A.; Casini, C.; Al-Omran, M.; Ignarro, L.J. Endothelial progenitor cells as therapeutic agents in the microcirculation: an update. Atherosclerosis, 2011, 215(1), 9-22.
22. Richardson, M.R.; Yoder, M.C. Endothelial progenitor cells: quo vadis? J. Mol. Cell. Cardiol., 2011, 50(2), 266-272.
23. Asahara, T.; Murohara, T.; Sullivan, A.; Silver, M.; van der Zee, R.; Li, T.; Witzenbichler, B.; Schatteman, G.; Isner, J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science, 1997, 275(5302), 964-967.
24. Zampetaki, A.; Kirton, J.P.; Xu, Q. Vascular repair by endothelial progenitor cells. Cardiovasc. Res., 2008, 78(3), 413-421.
25. Yoder, M.C.; Mead, L.E.; Prater, D.; Krier, T.R.; Mroueh, K.N.; Li, F.; Krasich, R.; Temm, C.J.; Prchal, J.T.; Ingram, D.A. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood, 2007, 109(5), 1801-1809.
26. Jeong, J.O.; Kim, M.O.; Kim, H.; Lee, M.Y.; Kim, S.W.; Ii, M.; Lee, J.U.; Lee, J.; Choi, Y.J.; Cho, H.J.; Lee, N.; Silver, M.; Wecker, A.; Kim, D.W.; Yoon, Y.S. Dual angiogenic and neurotrophic effects of bone marrow-derived endothelial progenitor cells on diabetic neuropathy. Circulation, 2009, 119(5), 699-708.
27. Cho, H.J.; Lee, N.; Lee, J.Y.; Choi, Y.J.; Ii, M.; Wecker, A.; Jeong, J.O.; Curry, C.; Qin, G.; Yoon, Y.S. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J. Exp. Med., 2007, 204(13), 3257-3269.
28. Rehman, J.; Li, J.; Orschell, C.M.; March, K.L. Peripheral blood "endothelial progenitor cells" are derived from monocyte/ macrophages and secrete angiogenic growth factors. Circulation, 2003, 107(8), 1164-1169.
29. Gnecchi, M.; Zhang, Z.; Ni, A.; Dzau, V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res., 2008, 103(11), 1204-1219.
30. Tateishi-Yuyama, E.; Matsubara, H.; Murohara, T.; Ikeda, U.; Shintani, S.; Masaki, H.; Amano, K.; Kishimoto, Y.; Yoshimoto, K.; Akashi, H.; Shimada, K.; Iwasaka, T.; Imaizumi, T. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Therapeutic Angiogenesis using Cell Transplantation (TACT) Study Investigators. Lancet, 2002, 360(9331), 427-435.
31. Esato, K.; Hamano, K.; Li, T.S.; Furutani, A.; Seyama, A.; Takenaka, H.; Zempo, N. Neovascularization induced by autologous bone marrow cell implantation in peripheral arterial disease. Cell Transplant., 2002, 11(8), 747-752.
32. Saigawa, T.; Kato, K.; Ozawa, T.; Toba, K.; Makiyama, Y.; Minagawa, S.; Hashimoto, S.; Furukawa, T.; Nakamura, Y.; Hanawa, H.; Kodama, M.; Yoshimura, N.; Fujiwara, H.; Namura, O.; Sogawa, M.; Hayashi, J.; Aizawa, Y. Clinical application of bone marrow implantation in patients with arteriosclerosis obliterans, and the association between efficacy and the number of implanted bone marrow cells. Circ. J., 2004, 68(12), 1189-1193.
33. Higashi, Y.; Kimura, M.; Hara, K.; Noma, K.; Jitsuiki, D.; Nakagawa, K.; Oshima, T.; Chayama, K.; Sueda, T.; Goto, C.; Matsubara, H.; Murohara, T.; Yoshizumi, M. Autologous bone-marrow mononuclear cell implantation improves endothelium-dependent vasodilation in patients with limb ischemia. Circulation, 2004, 109(10), 1215-1218.
34. Miyamoto, M.; Yasutake, M.; Takano, H.; Takagi, H.; Takagi, G.; Mizuno, H.; Kumita, S.; Takano, T. 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(4), 429-437.
35. Huang, P.P.; Li, S.Z.; Han, M.Z.; Xiao, Z.J.; Yang, R.C.; Qiu, L.G.; Han, Z.C. Autologous transplantation of peripheral blood stem cells as an effective therapeutic approach for severe arteriosclerosis obliterans of lower extremities. Thromb. Haemost., 2004, 91(3), 606-609.
36. Kawamura, A.; Horie, T.; Tsuda, I.; Ikeda, A.; Egawa, H.; Imamura, E.; Iida, J.; Sakata, H.; Tamaki, T.; Kukita, K.; Meguro, J.; Yonekawa, M.; Kasai, M. Prevention of limb amputation in patients with limbs ulcers by autologous peripheral blood mononuclear cell implantation. Ther. Apher. Dial., 2005, 9(1), 59-63.
37. Lenk, K.; Adams, V.; Lurz, P.; Erbs, S.; Linke, A.; Gielen, S.; Schmidt, A.; Scheinert, D.; Biamino, G.; Emmrich, F.; Schuler, G.; Hambrecht, R. Therapeutical potential of blood-derived progenitor cells in patients with peripheral arterial occlusive disease and critical limb ischaemia. Eur. Heart J., 2005, 26(18), 1903-1909.
38. Huang, P.; Li, S.; Han, M.; Xiao, Z.; Yang, R.; Han, Z.C. Autologous transplantation of granulocyte colony stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care, 2005, 28(9), 2155-2160.
39. Ishida, A.; Ohya, Y.; Sakuda, H.; Ohshiro, K.; Higashiuesato, Y.; Nakaema, M., Matsubara, S.; Yakabi, S.; Kakihana, A.; Ueda, M.; Miyagi, C.; Yamane, N.; Koja, K.; Komori, K.; Takishita, S. Autologous peripheral blood mononuclear cell implantation for patients with peripheral arterial disease improves limb ischemia. Circ. J., 2005, 69(10), 1260-1265.
40. Durdu, S.; Akar, A.R.; Arat, M.; Sancak, T.; Eren, N.T.; Ozyurda, U. Autologous bone-marrow mononuclear cell implantation for patients with Rutherford grade II-III thromboangiitis obliterans. J. Vasc. Surg., 2006, 44(4), 732-739.
41. Miyamoto, K.; Nishigami, K.; Nagaya, N.; Akutsu, K.; Chiku, M.; Kamei, M.; Soma, T.; Miyata, S.; Higashi, M.; Tanaka, R.; Nakatani, T.; Nonogi, H.; Takeshita, S. Unblinded pilot study of autologous transplantation of bone marrow mononuclear cells in patients with thromboangiitis obliterans. Circulation, 2006, 114(24), 2679-2684.
42. Kawamura, A.; Horie, T.; Tsuda, I.; Abe, Y.; Yamada, M., Egawa, H.; Iida, J.; Sakata, H.; Onodera, K.; Tamaki, T.; Furui, H.; Kukita, K.; Meguro, J.; Yonekawa, M.; Tanaka, S. 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(4), 226-233.
43. Bartsch, T.; Brehm, M.; Zeus, T.; Kögler, G.; Wernet, P.; Strauer, B.E. Transplantation of autologous mononuclear bone marrow stem cells in patients with peripheral arterial disease (the TAM-PAD study). Clin. Res. Cardiol., 2007, 96(12), 891-899.
44. Huang, P.P.; Yang, X.F.; Li, S.Z.; Wen, J.C.; Zhang, Y.; Han, Z.C. Randomised comparison of G-CSF-mobilized peripheral blood mononuclear cells versus bone marrow-mononuclear cells for the treatment of patients with lower limb arteriosclerosis obliterans. Thromb. Haemost., 2007, 98(6), 1335-1342.
45. Kajiguchi, M.; Kondo, T.; Izawa, H.; Kobayashi, M.; Yamamoto, K.; Shintani, S.; Numaguchi, Y.; Naoe, T.; Takamatsu, J.; Komori, K.; Murohara, T. Safety and efficacy of autologous progenitor cell transplantation for therapeutic angiogenesis in patients with critical limb ischemia. Circ. J., 2007, 71(2), 196-201.
46. Hernández, P.; Cortina, L.; Artaza, H.; Pol, N.; Lam, R.M.; Dorticós, E.; Macías, C.; Hernández, C.; del Valle, L.; Blanco, A.; Martínez, A.; Díaz, F. Autologous bone-marrow mononuclear cell implantation in patients with severe lower limb ischaemia: a comparison of using blood cell separator and Ficoll density gradient centrifugation. Atherosclerosis, 2007, 194(2), e52-e56.
47. Saito, S.; Nishikawa, K.; Obata, H.; Goto, F. Autologous bone marrow transplantation and hyperbaric oxygen therapy for patients with thromboangiitis obliterans. Angiology, 2007, 58(4), 429-434.
48. Matoba, S.; Tatsumi, T.; Murohara, T., Imaizumi, T.; Katsuda, Y.; Ito, M.; Saito, Y.; Uemura, S.; Suzuki, H.; Fukumoto, S.; Yamamoto, Y.; Onodera, R.; Teramukai, S.; Fukushima, M.; Matsubara, H. Long-term clinical outcome after intramuscular implantation of bone marrow mononuclear cells (Therapeutic Angiogenesis by Cell Transplantation [TACT] trial) in patients with chronic limb ischemia. TACT Follow-up Study Investigators. Am. Heart J., 2008, 156(5), 1010-1018.
49. Gu, Y.Q.; Zhang, J.; Guo, L.R.; Qi, L.X.; Zhang, S.W.; Xu, J.; Li, J.X.; Luo, T.; Ji, B.X.; Li, X.F.; Yu, H.X.; Cui, S.J.; Wang, Z.G. Transplantation of autologous bone marrow mononuclear cells for patients with lower limb ischemia. Chin. Med. J. (Engl.), 2008, 121(11), 963-967.
50. Chochola, M.; Pytlík, R.; Kobylka, P.; Skalická, L.; Kideryová, L.; Beran, S.; Varejka, P.; Jirát, S.; Køivánek, J.; Aschermann, M.; Linhart, A. Autologous intra-arterial infusion of bone marrow mononuclear cells in patients with critical leg ischemia. Int. Angiol., 2008, 27(4), 281-290.
51. Wester, T.; Jørgensen, J.J.; Stranden, E.; Sandbaek, G.; Tjønnfjord, G.; Bay, D.; Kollerøs, D.; Kroese, A.J.; Brinchmann, J.E. Treatment with autologous bone marrow mononuclear cells in patients with critical lower limb ischaemia. A pilot study. Scand. J. Surg., 2008, 97(1), 56-62.
52. Van Tongeren, R.B.; Hamming, J.F.; Fibbe, W.E.; Van Weel, V.; Frerichs, S.J.; Stiggelbout, A.M.; Van Bockel, J.H.; Lindeman, J.H. Intramuscular or combined intramuscular/intra-arterial administration of bone marrow mononuclear cells: a clinical trial in patients with advanced limb ischemia. J. Cardiovasc. Surg., 2008, 49(1), 51-58.
53. De Vriese, A.S.; Billiet, J.; Van Droogenbroeck, J.; Ghekiere, J.; De Letter, J.A. Autologous transplantation of bone marrow mononuclear cells for limb ischemia in a caucasian population with atherosclerosis obliterans. J. Intern. Med., 2008, 263(4), 395-403.
54. Cobellis, G.; Silvestroni, A.; Lillo, S.; Sica, G.; Botti, C.; Maione, C.; Schiavone, V.; Rocco, S.; Brando, G.; Sica, V. Long-term effects of repeated autologous transplantation of bone marrow cells in patients affected by peripheral arterial disease. Bone Marrow Transplant., 2008, 42(10), 667-672.
55. Amann, B.; Lüdemann, C.; Rückert, R.; Lawall, H.; Liesenfeld, B.; Schneider, M.; Schmidt-Lucke, J. Design and rationale of a randomized, double-blind, placebo-controlled phase III study for autologous bone marrow cell transplantation in critical limb ischemia: the Bone Marrow Outcomes Trial in Critical Limb Ischemia (BONMOT-CLI). Vasa, 2008, 37(4), 319-325.
56. Amann, B.; Luedemann, C.; Ratei, R.; Schmidt-Lucke, J.A. Autologous bone marrow cell transplantation increases leg perfusion and reduces amputations in patients with advanced critical limb ischemia due to peripheral artery disease. Cell. Transplant., 2009, 18(3), 371-380.
57. Capiod, J.C.; Tournois, C.; Vitry, F.; Sevestre, M.A.; Daliphard, S.; Reix, T.; Nguyen, P.; Lefrère, J.J.; Pignon, B. Characterization and comparison of bone marrow and peripheral blood mononuclear cells used for cellular therapy in critical leg ischaemia: towards a new cellular product. Vox Sang., 2009, 96(3), 256-265.
58. Franz, R.W.; Parks, A.; Shah, K.J.; Hankins, T.; Hartman, J.F.; Wright, M.L. Use of autologous bone marrow mononuclear cell implantation therapy as a limb salvage procedure in patients with severe peripheral arterial disease. J. Vasc. Surg., 2009, 50(6) 1378-1390.
59. Franz, R.W.; Shah, K.J.; Johnson, J.D.; Pin, R.H.; Parks, A.M.; Hankins, T.; Hartman, J.F.; Wright, M.L. Short-to mid-term results using autologous bone-marrow mononuclear cell implantation therapy as a limb salvage procedure in patients with severe peripheral arterial disease. Vasc. Endovascular Surg., 2011, 45(5), 398-406.
60. Zafarghandi, M.R.; Ravari, H.; Aghdami, N.; Namiri, M.; Moazzami, K.; Taghiabadi, E.; Fazel, A.; Pournasr, B.; Farrokhi, A.; Sharifian, R.A.; Salimi, J.; Moini, M.; Baharvand, H. Safety and efficacy of granulocyte-colony-stimulating factor administration following autologous intramuscular implantation of bone marrow mononuclear cells: a randomized controlled trial in patients with advanced lower limb ischemia. Cytotherapy, 2010, 12(6), 783-791.
61. Procházka, V.; Gumulec, J.; Jaluvka, F.; Salounová, D.; Jonszta, T.; Czerny, D.; Krajca, J.; Urbanec, R.; Klement, P.; Martinek, J.; Klement, G.L. Cell therapy, a new standard in management of chronic critical limb ischemia and foot ulcer. Cell Transplant., 2010, 19(11), 1413-1424.
62. Lara-Hernandez, R.; Lozano-Vilardell, P.; Blanes, P.; Torreguitart-Mirada, N.; Galmés, A.; Besalduch, J. Safety and efficacy of therapeutic angiogenesis as a novel treatment in patients with critical limb ischemia. Ann. Vasc. Surg., 2010, 24(2), 287-294.
63. Walter, D.H.; Krankenberg, H.; Balzer, J.O.; Kalka, C; Baumgartner, I.; Schlüter, M.; Tonn, T.; Seeger, F.; Dimmeler, S.; Lindhoff-Last, E.; Zeiher, A.M. Intraarterial administration of bone marrow mononuclear cells in patients with critical limb ischemia: a randomized-start, placebo-controlled pilot trial (PROVASA). PROVASA Investigators. Cardiovasc. Interv., 2011, 4(1), 26-37.
64. Murphy, M.P.; Lawson, J.H.; Rapp, B.M.; Dalsing, M.C.; Klein, J.; Wilson, M.G.; Hutchins, G.D.; March, K.L. Autologous bone marrow mononuclear cell therapy is safe and promotes amputation-free survival in patients with critical limb ischemia. J. Vasc. Surg., 2011, 53(6) 1565-1574.
65. Yoshida, M.; Horimoto, H.; Mieno, S.; Nomura, Y.; Okawa, H.; Nakahara, K.; Sasaki, S. Intra-arterial bone marrow cell transplantation induces angiogenesis in rat hindlimb ischemia. Eur. Surg. Res., 2003, 35(2) 86-91.