Intramyocardial Injection of Autologous Bone Marrow-Derived Ex Vivo Expanded Mesenchymal Stem Cells in Acute Myocardial Infarction Patients is Feasible and Safe up to 5 Years of Follow-up

Jeevanantham, V., Butler, M., Saad, A., Abdel-Latif, A., Zuba-Surma, E. K., & Dawn, B. (2012). Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation, 126, 551–568. Silva, G. V., Litovsky, S., Assad, J. A., Sousa, A. L., Martin, B. J., Vela, D., Coulter, S. C., Lin, J., Ober, J., Vaughn, W. K., Branco, R. V., Oliveira, E. M., He, R., Geng, Y. J., Willerson, J. T., & Perin, E. C. (2005). Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation, 111, 150–156. Makino, S., Fukuda, K., Miyoshi, S., Konishi, F., Kodama, H., Pan, J., Sano, M., Takahashi, T., Hori, S., Abe, H., Hata, J., Umezawa, A., & Ogawa, S. (1999). Cardiomyocytes can be generated from marrow stromal cells in vitro. The Journal of Clinical Investigation, 103, 697–705. Dai, W., Hale, S. L., Martin, B. J., Kuang, J. Q., Dow, J. S., Wold, L. E., & Kloner, R. A. (2005). Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation, 112, 214–223. Chen, S. L., Fang, W. W., Ye, F., Liu, Y. H., Qian, J., Shan, S. J., Zhang, J. J., Chunhua, R. Z., Liao, L. M., Lin, S., & Sun, J. P. (2004). Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. The American Journal of Cardiology, 94, 92–95. Hare, J. M., Traverse, J. H., Henry, T. D., Dib, N., Strumpf, R. K., Schulman, S. P., Gerstenblith, G., DeMaria, A. N., Denktas, A. E., Gammon, R. S., Hermiller, J. B., Jr., Reisman, M. A., Schaer, G. L., & Sherman, W. (2009). A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. Journal of the American College of Cardiology, 54, 2277–2286. Williams, A. R., Trachtenberg, B., Velazquez, D. L., McNiece, I., Altman, P., Rouy, D., Mendizabal, A. M., Pattany, P. M., Lopera, G. A., Fishman, J., Zambrano, J. P., Heldman, A. W., & Hare, J. M. (2011). Intramyocardial stem cell injection in patients with ischemic cardiomyopathy: functional recovery and reverse remodeling. Circulation Research, 108, 792–796. Vulliet, P. R., Greeley, M., Halloran, S. M., MacDonald, K. A., & Kittleson, M. D. (2004). Intra-coronary arterial injection of mesenchymal stromal cells and microinfarction in dogs. Lancet, 363, 783–784. Moelker, A. D., Baks, T., Wever, K. M., Spitskovsky, D., Wielopolski, P. A., van Beusekom, H. M., van Geuns, R. J., Wnendt, S., Duncker, D. J., & van der Giessen, W. J. (2007). Intracoronary delivery of umbilical cord blood derived unrestricted somatic stem cells is not suitable to improve LV function after myocardial infarction in swine. Journal of Molecular and Cellular Cardiology, 42, 735–745. Hou, D., Youssef, E. A., Brinton, T. J., Zhang, P., Rogers, P., Price, E. T., Yeung, A. C., Johnstone, B. H., Yock, P. G., & March, K. L. (2005). Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation, 112, I150–I156. van Ramshorst, J., Bax, J. J., Beeres, S. L., Dibbets-Schneider, P., Roes, S. D., Stokkel, M. P., de Roos, A., Fibbe, W. E., Zwaginga, J. J., Boersma, E., Schalij, M. J., & Atsma, D. E. (2009). Intramyocardial bone marrow cell injection for chronic myocardial ischemia: a randomized controlled trial. JAMA : The Journal of the American Medical Association, 301, 1997–2004. 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. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet, 371, 1579–1586. Beeres, S. L., Bax, J. J., Dibbets, P., Stokkel, M. P., Zeppenfeld, K., Fibbe, W. E., van der Wall, E. E., Schalij, M. J., & Atsma, D. E. (2006). Effect of intramyocardial injection of autologous bone marrow-derived mononuclear cells on perfusion, function, and viability in patients with drug-refractory chronic ischemia. Journal of Nuclear Medicine, 47, 574–580. Mollema, S. A., Liem, S. S., Suffoletto, M. S., Bleeker, G. B., van der Hoeven, B. L., van de Veire, N. R., Boersma, E., Holman, E. R., van der Wall, E. E., Schalij, M. J., Gorcsan, J., III, & Bax, J. J. (2007). Left ventricular dyssynchrony acutely after myocardial infarction predicts left ventricular remodeling. Journal of the American College of Cardiology, 50, 1532–1540. Liem, S. S., van der Hoeven, B. L., Oemrawsingh, P. V., Bax, J. J., van der Bom, J. G., Bosch, J., Viergever, E. P., van Rees, C., Padmos, I., Sedney, M. I., van Exel, H. J., Verwey, H. F., Atsma, D. E., van der Velde, E. T., Jukema, J. W., van der Wall, E. E., & Schalij, M. J. (2007). MISSION!: optimization of acute and chronic care for patients with acute myocardial infarction. American Heart Journal, 153, 14–11. Dominici, M., Le, B. K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., & Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, 315–317. Amado, L. C., Saliaris, A. P., Schuleri, K. H., St, J. M., Xie, J. S., Cattaneo, S., Durand, D. J., Fitton, T., Kuang, J. Q., Stewart, G., Lehrke, S., Baumgartner, W. W., Martin, B. J., Heldman, A. W., & Hare, J. M. (2005). Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proceedings of the National Academy of Sciences of the United States of America, 102, 11474–11479. Beitnes, J. O., Oie, E., Shahdadfar, A., Karlsen, T., Muller, R. M., Aakhus, S., Reinholt, F. P., & Brinchmann, J. E. (2012). Intramyocardial injections of human mesenchymal stem cells following acute myocardial infarction modulate scar formation and improve left ventricular function. Cell Transplantation, 21, 1697–1709. Toma, C., Pittenger, M. F., Cahill, K. S., Byrne, B. J., & Kessler, P. D. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation, 105, 93–98. Jain, M., Pfister, O., Hajjar, R. J., & Liao, R. (2005). Mesenchymal stem cells in the infarcted heart. Coronary Artery Disease, 16, 93–97. Uccelli, A., Moretta, L., & Pistoia, V. (2006). Immunoregulatory function of mesenchymal stem cells. European Journal of Immunology, 36, 2566–2573. Le Blanc, K., & Ringden, O. (2007). Immunomodulation by mesenchymal stem cells and clinical experience. Journal of Internal Medicine, 262, 509–525. Huang, X. P., Sun, Z., Miyagi, Y., McDonald, K. H., Zhang, L., Weisel, R. D., & Li, R. K. (2010). Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation, 122, 2419–2429. Nauta, A. J., Westerhuis, G., Kruisselbrink, A. B., Lurvink, E. G., Willemze, R., & Fibbe, W. E. (2006). Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood, 108, 2114–2120. Chen, X., Xu, H., Wan, C., McCaigue, M., & Li, G. (2006). Bioreactor expansion of human adult bone marrow-derived mesenchymal stem cells. Stem Cells, 24, 2052–2059. Meliga, E., Strem, B. M., Duckers, H. J., & Serruys, P. W. (2007). Adipose-derived cells. Cell Transplantation, 16, 963–970. Planat-Benard, V., Silvestre, J. S., Cousin, B., Andre, M., Nibbelink, M., Tamarat, R., Clergue, M., Manneville, C., Saillan-Barreau, C., Duriez, M., Tedgui, A., Levy, B., Penicaud, L., & Casteilla, L. (2004). Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation, 109, 656–663. Valina, C., Pinkernell, K., Song, Y. H., Bai, X., Sadat, S., Campeau, R. J., Le Jemtel, T. H., & Alt, E. (2007). Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. European Heart Journal, 28, 2667–2677. Schenke-Layland, K., Strem, B. M., Jordan, M. C., Deemedio, M. T., Hedrick, M. H., Roos, K. P., Fraser, J. K., & MacLellan, W. R. (2009). Adipose tissue-derived cells improve cardiac function following myocardial infarction. The Journal of Surgical Research, 153, 217–223. Katritsis, D. G., Sotiropoulou, P. A., Karvouni, E., Karabinos, I., Korovesis, S., Perez, S. A., Voridis, E. M., & Papamichail, M. (2005). Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheterization and Cardiovascular Interventions, 65, 321–329. Tse, H. F., Thambar, S., Kwong, Y. L., Rowlings, P., Bellamy, G., McCrohon, J., Thomas, P., Bastian, B., Chan, J. K., Lo, G., Ho, C. L., Chan, W. S., Kwong, R. Y., Parker, A., Hauser, T. H., Chan, J., Fong, D. Y., & Lau, C. P. (2007). Prospective randomized trial of direct endomyocardial implantation of bone marrow cells for treatment of severe coronary artery diseases (PROTECT-CAD trial). European Heart Journal, 28, 2998–3005. Losordo, D. W., Henry, T. D., Davidson, C., Sup, L. J., Costa, M. A., Bass, T., Mendelsohn, F., Fortuin, F. D., Pepine, C. J., Traverse, J. H., Amrani, D., Ewenstein, B. M., Riedel, N., Story, K., Barker, K., Povsic, T. J., Harrington, R. A., & Schatz, R. A. (2011). Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circulation Research, 109, 428–436. Fuchs, S., Kornowski, R., Weisz, G., Satler, L. F., Smits, P. C., Okubagzi, P., Baffour, R., Aggarwal, A., Weissman, N. J., Cerqueira, M., Waksman, R., Serrruys, P., Battler, A., Moses, J. W., Leon, M. B., & Epstein, S. E. (2006). Safety and feasibility of transendocardial autologous bone marrow cell transplantation in patients with advanced heart disease. The American Journal of Cardiology, 97, 823–829. Tse, H. F., Kwong, Y. L., Chan, J. K., Lo, G., Ho, C. L., & Lau, C. P. (2003). Angiogenesis in ischaemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation. Lancet, 361, 47–49. Ang, K. L., Chin, D., Leyva, F., Foley, P., Kubal, C., Chalil, S., Srinivasan, L., Bernhardt, L., Stevens, S., Shenje, L. T., & Galinanes, M. (2008). Randomized, controlled trial of intramuscular or intracoronary injection of autologous bone marrow cells into scarred myocardium during CABG versus CABG alone. Nature Clinical Practice. Cardiovascular Medicine, 5, 663–670. Brunskill, S. J., Hyde, C. J., Doree, C. J., Watt, S. M., & Martin-Rendon, E. (2009). Route of delivery and baseline left ventricular ejection fraction, key factors of bone-marrow-derived cell therapy for ischaemic heart disease. European Journal of Heart Failure, 11, 887–896. Krause, K., Jaquet, K., Schneider, C., Haupt, S., Lioznov, M. V., Otte, K. M., & Kuck, K. H. (2009). Percutaneous intramyocardial stem cell injection in patients with acute myocardial infarction: first-in-man study. Heart, 95, 1145–1152. Antoni, M. L., Hoogslag, G. E., Boden, H., Liem, S. S., Boersma, E., Fox, K., Schalij, M. J., Bax, J. J., & Delgado, V. (2012). Cardiovascular mortality and heart failure risk score for patients after ST-segment elevation acute myocardial infarction treated with primary percutaneous coronary intervention (data from the Leiden MISSION! Infarct Registry). The American Journal of Cardiology, 109, 187–194. Bellenger, N. G., Burgess, M. I., Ray, S. G., Lahiri, A., Coats, A. J., Cleland, J. G., & Pennell, D. J. (2000). Comparison of left ventricular ejection fraction and volumes in heart failure by echocardiography, radionuclide ventriculography and cardiovascular magnetic resonance; are they interchangeable? European Heart Journal, 21, 1387–1396.