Tracking of stem cells in vivo for cardiovascular applications

Journal of Cardiovascular Magnetic Resonance

Dara L Kraitchman²  Jeremy Maurer¹  Yingli Fu¹  Nicole Azene³ 

[1] Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University, Baltimore, MD, USA;Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, 600 N. Wolfe Street, 314 Park Building, Baltimore, MD 21287, USA;Department of Molecular and Comparative Pathobiology, The Johns Hopkins University, Baltimore, MD, USA

关键词: Image-guided therapy;    Ultrasound;    Optical imaging;    Radionuclide imaging;    Cardiovascular magnetic resonance;    Fluoroscopy;    Computed tomography;    Cardiovascular disease;    Stem cells;    Cell labeling;    Cell tracking;   

Others  :  801924
DOI  :  10.1186/1532-429X-16-7

 received in 2012-12-16, accepted in 2013-12-11,  发布年份 2014

【 摘 要 】

In the past ten years, the concept of injecting stem and progenitor cells to assist with rebuilding damaged blood vessels and myocardial tissue after injury in the heart and peripheral vasculature has moved from bench to bedside. Non-invasive imaging can not only provide a means to assess cardiac repair and, thereby, cellular therapy efficacy but also a means to confirm cell delivery and engraftment after administration. In this first of a two-part review, we will review the different types of cellular labeling techniques and the application of these techniques in cardiovascular magnetic resonance and ultrasound. In addition, we provide a synopsis of the cardiac cellular clinical trials that have been performed to-date.

【 授权许可】

   
2014 Azene et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Mingliang R, Bo Z, Zhengguo W: Stem cells for cardiac repair: status, mechanisms, and new strategies. Stem Cells Int 2011, 2011:310928.
• [2]Mohsin S, Siddiqi S, Collins B, Sussman MA: Empowering adult stem cells for myocardial regeneration. Circ Res 2011, 109:1415-1428.
• [3]Schwitter J, Wacker CM, Wilke N, Al-Saadi N, Sauer E, Huettle K, Schonberg SO, Debl K, Strohm O, Ahlstrom H, et al.: Superior diagnostic performance of perfusion-cardiovascular magnetic resonance versus SPECT to detect coronary artery disease: The secondary endpoints of the multicenter multivendor MR-IMPACT II (Magnetic Resonance Imaging for Myocardial Perfusion Assessment in Coronary Artery Disease Trial). J Cardiovasc Magn Reson 2012, 14:61.
• [4]Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, et al.: Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006, 355:1210-1221.
• [5]Leistner DM, Fischer-Rasokat U, Honold J, Seeger FH, Schachinger V, Lehmann R, Martin H, Burck I, Urbich C, Dimmeler S, et al.: Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI): final 5-year results suggest long-term safety and efficacy. Clin Res Cardiol 2011, 100:925-934.
• [6]Traverse JH, Henry TD, Ellis SG, Pepine CJ, Willerson JT, Zhao DX, Forder JR, Byrne BJ, Hatzopoulos AK, Penn MS, et al.: Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the latetime randomized trial. JAMA 2011, 306(19):2110-2119.
• [7]Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, et al.: Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004, 364:141-148.
• [8]Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, Endresen K, Ilebekk A, Mangschau A, Fjeld JG, et al.: Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 2006, 355:1199-1209.
• [9]Chugh AR, Beache GM, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JA, et al.: Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 2012, 126:S54-64.
• [10]Tse HF, Thambar S, Kwong YL, Rowlings P, Bellamy G, McCrohon J, Thomas P, Bastian B, Chan JK, Lo G, et al.: Prospective randomized trial of direct endomyocardial implantation of bone marrow cells for treatment of severe coronary artery diseases (PROTECT-CAD trial). Eur Heart J 2007, 28:2998-3005.
• [11]Chan CW, Kwong YL, Kwong RY, Lau CP, Tse HF: Improvement of myocardial perfusion reserve detected by cardiovascular magnetic resonance after direct endomyocardial implantation of autologous bone marrow cells in patients with severe coronary artery disease. J Cardiovasc Magn Reson 2010, 12:6.
• [12]Abdel-Latif A, Bolli R, Tleyjeh IM, Montori VM, Perin EC, Hornung CA, Zuba-Surma EK, Al-Mallah M, Dawn B: Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis. Arch Intern Med 2007, 167:989-997.
• [13]Kandala J, Upadhyay GA, Pokushalov E, Wu S, Drachman DE, Singh JP: Meta-analysis of stem cell therapy in chronic ischemic cardiomyopathy. AM J Cardiol 2013, 112:217-225.
• [14]Donndorf P, Kundt G, Kaminski A, Yerebakan C, Liebold A, Steinhoff G, Glass A: Intramyocardial bone marrow stem cell transplantation during coronary artery bypass surgery: a meta-analysis. J Thorac Cardiovasc Surg 2011, 142:911-920.
• [15]Sun L, Zhang T, Lan X, Du G: Effects of stem cell therapy on left ventricular remodeling after acute myocardial infarction: a meta-analysis. Clin Cardiol 2010, 33:296-302.
• [16]Fan L, Chen L, Chen X, Fu F: A meta-analysis of stem cell mobilization by granulocyte colony-stimulating factor in the treatment of acute myocardial infarction. Cardiovasc Drugs Ther 2008, 22:45-54.
• [17]Strauer BE, Brehm M, Zeus T, Köstering M, Hernandez A, Sorg RV, Kögler G, Wernet P: Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 2002, 106:1913-1918.
• [18]Kuethe F, Richartz BM, Sayer HG, Kasper C, Werner GS, Hoffken K, Figulla HR: Lack of regeneration of myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans with large anterior myocardial infarctions. Int J Cardiol 2004, 97:123-127.
• [19]Meyer GP, Wollert KC, Lotz J, Steffens J, Lippolt P, Fichtner S, Hecker H, Schaefer A, Arseniev L, Hertenstein B, et al.: Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months’ follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation 2006, 113:1287-1294.
• [20]Schaefer A, Meyer GP, Fuchs M, Klein G, Kaplan M, Wollert KC, Drexler H: Impact of intracoronary bone marrow cell transfer on diastolic function in patients after acute myocardial infarction: results from the BOOST trial. Eur Heart J 2006, 27:929-935.
• [21]Meyer GP, Wollert KC, Lotz J, Pirr J, Rager U, Lippolt P, Hahn A, Fichtner S, Schaefer A, Arseniev L, et al.: Intracoronary bone marrow cell transfer after myocardial infarction: 5-year follow-up from the randomized-controlled BOOST trial. Eur Heart J 2009, 30:2978-2984.
• [22]Beitnes JO, Hopp E, Lunde K, Solheim S, Arnesen H, Brinchmann JE, Forfang K, Aakhus S: Long-term results after intracoronary injection of autologous mononuclear bone marrow cells in acute myocardial infarction: the ASTAMI randomised, controlled study. Heart 2009, 95:1983-1989.
• [23]Tendera M, Wojakowski W, Ruzyllo W, Chojnowska L, Kepka C, Tracz W, Musialek P, Piwowarska W, Nessler J, Buszman P, et al.: Intracoronary infusion of bone marrow-derived selected CD34+CXCR4+ cells and non-selected mononuclear cells in patients with acute STEMI and reduced left ventricular ejection fraction: results of randomized, multicentre Myocardial Regeneration by Intracoronary Infusion of Selected Population of Stem Cells in Acute Myocardial Infarction (REGENT) Trial. Eur Heart J 2009, 30:1313-1321.
• [24]Arnold R, Villa A, Gutierrez H, Sanchez PL, Gimeno F, Fernandez ME, Gutierrez O, Mota P, Sanchez A, Garcia-Frade J, et al.: Absence of accelerated atherosclerotic disease progression after intracoronary infusion of bone marrow derived mononuclear cells in patients with acute myocardial infarction--angiographic and intravascular ultrasound--results from the TErapia Celular Aplicada al Miocardio Pilot study. Am Heart J 2010, 159:1154. e1151-1158
• [25]Hopp E, Lunde K, Solheim S, Aakhus S, Arnesen H, Forfang K, Edvardsen T, Smith HJ: Regional myocardial function after intracoronary bone marrow cell injection in reperfused anterior wall infarction - a cardiovascular magnetic resonance tagging study. J Cardiovasc Magn Reson 2011, 13:22.
• [26]Surder D, Schwitter J, Moccetti T, Astori G, Rufibach K, Plein S, Lo Cicero V, Soncin S, Windecker S, Moschovitis A, et al.: Cell-based therapy for myocardial repair in patients with acute myocardial infarction: rationale and study design of the SWiss multicenter Intracoronary Stem cells Study in Acute Myocardial Infarction (SWISS-AMI). Am Heart J 2010, 160:58-64.
• [27]Traverse JH, Henry TD, Pepine CJ, Willerson JT, Zhao DX, Ellis SG, Forder JR, Anderson RD, Hatzopoulos AK, Penn MS, et al.: Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: the TIME randomized trial. JAMA 2012, 308:2380-2389.
• [28]Traverse JH, Henry TD, Pepine CJ, Willerson JT, Ellis SG: One-year follow-up of intracoronary stem cell delivery on left ventricular function following ST-elevation myocardial Infarction. JAMA 2013. doi:10.1001/jama.2013.282674
• [29]Fernandez-Aviles F, San Roman JA, Garcia-Frade J, Fernandez ME, Penarrubia MJ, de la Fuente L, Gomez-Bueno M, Cantalapiedra A, Fernandez J, Gutierrez O, et al.: Experimental and clinical regenerative capability of human bone marrow cells after myocardial infarction. Circ Res 2004, 95:742-748.
• [30]Strauer BE, Brehm M, Zeus T, Bartsch T, Schannwell C, Antke C, Sorg RV, Kogler G, Wernet P, Muller HW, Kostering M: Regeneration of human infarcted heart muscle by intracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: the IACT Study. J Am Coll Cardiol 2005, 46:1651-1658.
• [31]Brehm M, Strauer BE: Stem cell therapy in postinfarction chronic coronary heart disease. Nat Clin Pract Cardiovasc Med 2006, 3(1):S101-104.
• [32]Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, et al.: Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006, 367:113-121.
• [33]Galinanes M, Loubani M, Davies J, Chin D, Pasi J, Bell PR: Autotransplantation of unmanipulated bone marrow into scarred myocardium is safe and enhances cardiac function in humans. Cell Transplant 2004, 13:7-13.
• [34]Fuchs S, Satler LF, Kornowski R, Okubagzi P, Weisz G, Baffour R, Waksman R, Weissman NJ, Cerqueira M, Leon MB, Epstein SE: Catheter-based autologous bone marrow myocardial injection in no-option patients with advanced coronary artery disease: a feasibility study. J Am Coll Cardiol 2003, 41:1721-1724.
• [35]Fuchs S, Kornowski R, Weisz G, Satler LF, Smits PC, Okubagzi P, Baffour R, Aggarwal A, Weissman NJ, Cerqueira M, et al.: Safety and feasibility of transendocardial autologous bone marrow cell transplantation in patients with advanced heart disease. Am J Cardiol 2006, 97:823-829.
• [36]Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, et al.: Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003, 107:2294-2302.
• [37]Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Silva GV, Mesquita CT, Belem L, Vaughn WK, Rangel FO, et al.: Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 2004, 110:II213-218.
• [38]de la Fuente LM, Stertzer SH, Argentieri J, Penaloza E, Miano J, Koziner B, Bilos C, Altman PA: Transendocardial autologous bone marrow in chronic myocardial infarction using a helical needle catheter: 1-year follow-up in an open-label, nonrandomized, single-center pilot study (the TABMMI study). Am Heart J 2007, 154:79-e71-77.
• [39]van Ramshorst J, Antoni ML, Beeres SL, Roes SD, Delgado V, Rodrigo SF, de Roos A, Holman ER, Fibbe WE, Lamb HJ, et al.: Intramyocardial bone marrow-derived mononuclear cell injection for chronic myocardial ischemia: the effect on diastolic function. Circ Cardiovasc Imaging 2011, 4:122-129.
• [40]Perin EC, Willerson JT, Pepine CJ, Henry TD, Ellis SG, Zhao DX, Silva GV, Lai D, Thomas JD, Kronenberg MW, et al.: Effect of transendocardial delivery of autologous bone marrow mononuclear cells on functional capacity, left ventricular function, and perfusion in chronic heart failure: the FOCUS-CCTRN trial. JAMA 2012, 307:1717-1726.
• [41]Silva GV, Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Assad JA, Vaughn WK, Mesquita CT, Belem L, et al.: Catheter-based transendocardial delivery of autologous bone-marrow-derived mononuclear cells in patients listed for heart transplantation. Tex Heart Inst J 2004, 31:214-219.
• [42]Perin EC, Silva GV, Henry TD, Cabreira-Hansen MG, Moore WH, Coulter SA, Herlihy JP, Fernandes MR, Cheong BY, Flamm SD, et al.: A randomized study of transendocardial injection of autologous bone marrow mononuclear cells and cell function analysis in ischemic heart failure (FOCUS-HF). Am Heart J 2011, 161:1078-1087. e1073
• [43]Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, et al.: Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 2002, 106:3009-3017.
• [44]Britten MB, Abolmaali ND, Assmus B, Lehmann R, Honold J, Schmitt J, Vogl TJ, Martin H, Schachinger V, Dimmeler S, et al.: Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation 2003, 108:2212-2218.
• [45]Schachinger V, Assmus B, Britten MB, Honold J, Lehmann R, Teupe C, Abolmaali ND, Vogl TJ, Hofmann WK, Martin H, et al.: Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI Trial. J Am Coll Cardiol 2004, 44:1690-1699.
• [46]Assmus B, Walter DH, Lehmann R, Honold J, Martin H, Dimmeler S, Zeiher AM, Schachinger V: Intracoronary infusion of progenitor cells is not associated with aggravated restenosis development or atherosclerotic disease progression in patients with acute myocardial infarction. Eur Heart J 2006, 27:2989-2995.
• [47]Bartunek J, Vanderheyden M, Vandekerckhove B, Mansour S, De Bruyne B, De Bondt P, Van Haute I, Lootens N, Heyndrickx G, Wijns W: Intracoronary injection of CD133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: feasibility and safety. Circulation 2005, 112:I178-183.
• [48]Mansour S, Roy DC, Bouchard V, Stevens LM, Gobeil F, Rivard A, Leclerc G, Reeves F, Noiseux N: One-year safety analysis of the COMPARE-AMI Trial: Comparison of intracoronary injection of CD133 bone marrow stem cells to placebo in patients after acute myocardial infarction and left ventricular dysfunction. Bone Marrow Res 2011, 2011:385124.
• [49]Goussetis E, Manginas A, Koutelou M, Peristeri I, Theodosaki M, Kollaros N, Leontiadis E, Theodorakos A, Paterakis G, Karatasakis G, et al.: Intracoronary infusion of CD133+ and CD133-CD34+ selected autologous bone marrow progenitor cells in patients with chronic ischemic cardiomyopathy: cell isolation, adherence to the infarcted area, and body distribution. Stem Cells 2006, 24:2279-2283.
• [50]Stamm C, Kleine HD, Westphal B, Petzsch M, Kittner C, Nienaber CA, Freund M, Steinhoff G: CABG and bone marrow stem cell transplantation after myocardial infarction. Thorac Cardiovasc Surg 2004, 52:152-158.
• [51]Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schumichen C, Nienaber CA, Freund M, Steinhoff G: Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 2003, 361:45-46.
• [52]Stamm C, Kleine HD, Choi YH, Dunkelmann S, Lauffs JA, Lorenzen B, David A, Liebold A, Nienaber C, Zurakowski D, et al.: Intramyocardial delivery of CD133+ bone marrow cells and coronary artery bypass grafting for chronic ischemic heart disease: safety and efficacy studies. J Thorac Cardiovasc Surg 2007, 133:717-725.
• [53]Losordo DW, Schatz RA, White CJ, Udelson JE, Veereshwarayya V, Durgin M, Poh KK, Weinstein R, Kearney M, Chaudhry M, et al.: Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation 2007, 115:3165-3172.
• [54]Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, et al.: Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ Res 2011, 109:428-436.
• [55]Choi JH, Choi J, Lee WS, Rhee I, Lee SC, Gwon HC, Lee SH, Choe YH, Kim DW, Suh W, et al.: Lack of additional benefit of intracoronary transplantation of autologous peripheral blood stem cell in patients with acute myocardial infarction. Circ J 2007, 71:486-494.
• [56]Kang HJ, Lee HY, Na SH, Chang SA, Park KW, Kim HK, Kim SY, Chang HJ, Lee W, Kang WJ, et al.: Differential effect of intracoronary infusion of mobilized peripheral blood stem cells by granulocyte colony-stimulating factor on left ventricular function and remodeling in patients with acute myocardial infarction versus old myocardial infarction: the MAGIC Cell-3-DES randomized, controlled trial. Circulation 2006, 114:I145-151.
• [57]Chachques JC, Herreros J, Trainini J, Juffe A, Rendal E, Prosper F, Genovese J: Autologous human serum for cell culture avoids the implantation of cardioverter-defibrillators in cellular cardiomyoplasty. Int J Cardiol 2004, 95(1):S29-33.
• [58]Dib N, McCarthy P, Campbell A, Yeager M, Pagani FD, Wright S, MacLellan WR, Fonarow G, Eisen HJ, Michler RE, et al.: Feasibility and safety of autologous myoblast transplantation in patients with ischemic cardiomyopathy. Cell Transplant 2005, 14:11-19.
• [59]Dib N, Michler RE, Pagani FD, Wright S, Kereiakes DJ, Lengerich R, Binkley P, Buchele D, Anand I, Swingen C, et al.: Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: four-year follow-up. Circulation 2005, 112:1748-1755.
• [60]Herreros J, Prosper F, Perez A, Gavira JJ, Garcia-Velloso MJ, Barba J, Sanchez PL, Canizo C, Rabago G, Marti-Climent JM, et al.: Autologous intramyocardial injection of cultured skeletal muscle-derived stem cells in patients with non-acute myocardial infarction. Eur Heart J 2003, 24:2012-2020.
• [61]Gavira JJ, Herreros J, Perez A, Garcia-Velloso MJ, Barba J, Martin-Herrero F, Canizo C, Martin-Arnau A, Marti-Climent JM, Hernandez M, et al.: Autologous skeletal myoblast transplantation in patients with nonacute myocardial infarction: 1-year follow-up. J Thorac Cardiovasc Surg 2006, 131:799-804.
• [62]Ince H, Petzsch M, Rehders TC, Chatterjee T, Nienaber CA: Transcatheter transplantation of autologous skeletal myoblasts in postinfarction patients with severe left ventricular dysfunction. J Endovasc Ther 2004, 11:695-704.
• [63]Hagege AA, Marolleau JP, Vilquin JT, Alheritiere A, Peyrard S, Duboc D, Abergel E, Messas E, Mousseaux E, Schwartz K, et al.: Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation 2006, 114:I108-113.
• [64]Siminiak T, Kalawski R, Fiszer D, Jerzykowska O, Rzezniczak J, Rozwadowska N, Kurpisz M: Autologous skeletal myoblast transplantation for the treatment of postinfarction myocardial injury: phase I clinical study with 12 months of follow-up. Am Heart J 2004, 148:531-537.
• [65]Siminiak T, Fiszer D, Jerzykowska O, Grygielska B, Rozwadowska N, Kalmucki P, Kurpisz M: Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: the POZNAN trial. Eur Heart J 2005, 26:1188-1195.
• [66]Smits PC, van Geuns RJ, Poldermans D, Bountioukos M, Onderwater EE, Lee CH, Maat AP, Serruys PW: Catheter-based intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: clinical experience with six-month follow-up. J Am Coll Cardiol 2003, 42:2063-2069.
• [67]Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin JT, Marolleau JP, Seymour B, Larghero J, et al.: The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 2008, 117:1189-1200.
• [68]Cleland JG, Coletta AP, Abdellah AT, Nasir M, Hobson N, Freemantle N, Clark AL: Clinical trials update from the American Heart Association 2006: OAT, SALT 1 and 2, MAGIC, ABCD, PABA-CHF, IMPROVE-CHF, and percutaneous mitral annuloplasty. Eur J Heart Fail 2007, 9:92-97.
• [69]Veltman CE, Soliman OI, Geleijnse ML, Vletter WB, Smits PC, ten Cate FJ, Jordaens LJ, Balk AH, Serruys PW, Boersma E, et al.: Four-year follow-up of treatment with intramyocardial skeletal myoblasts injection in patients with ischaemic cardiomyopathy. Eur Heart J 2008, 29:1386-1396.
• [70]Chen SL, Fang WW, Qian J, Ye F, Liu YH, Shan SJ, Zhang JJ, Lin S, Liao LM, Zhao RC: Improvement of cardiac function after transplantation of autologous bone marrow mesenchymal stem cells in patients with acute myocardial infarction. Chin Med J (Engl) 2004, 117:1443-1448.
• [71]Chen SL, Fang WW, Ye F, Liu YH, Qian J, Shan SJ, Zhang JJ, Chunhua RZ, Liao LM, Lin S, Sun JP: Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004, 94:92-95.
• [72]Chen S, Liu Z, Tian N, Zhang J, Yei F, Duan B, Zhu Z, Lin S, Kwan TW: Intracoronary transplantation of autologous bone marrow mesenchymal stem cells for ischemic cardiomyopathy due to isolated chronic occluded left anterior descending artery. J Invasive Cardiol 2006, 18:552-556.
• [73]Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, 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, 54:2277-2286.
• [74]Mathiasen AB, Jorgensen E, Qayyum AA, Haack-Sorensen M, Ekblond A, Kastrup J: Rationale and design of the first randomized, double-blind, placebo-controlled trial of intramyocardial injection of autologous bone-marrow derived Mesenchymal Stromal Cells in chronic ischemic Heart Failure (MSC-HF Trial). Am Heart J 2012, 164:285-291.
• [75]Hare JM, Fishman JE, Gerstenblith G, DiFede Velazquez DL, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, et al.: Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012, 308:2369-2379.
• [76]Trachtenberg B, Velazquez DL, Williams AR, McNiece I, Fishman J, Nguyen K, Rouy D, Altman P, Schwarz R, Mendizabal A, et al.: Rationale and design of the Transendocardial Injection of Autologous Human Cells (bone marrow or mesenchymal) in Chronic Ischemic Left Ventricular Dysfunction and Heart Failure Secondary to Myocardial Infarction (TAC-HFT) trial: A randomized, double-blind, placebo-controlled study of safety and efficacy. Am Heart J 2011, 161:487-493.
• [77]Heldman AW, Difede DL, Fishman JE, Zambrano JP, Trachtenberg BH, Karantalis V, Mushtaq M, Williams AR, Suncion VY, McNiece IK, et al.: Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial. JAMA 2013. doi:10.1001/jama.2013.282909
• [78]Qayyum AA, Haack-Sorensen M, Mathiasen AB, Jorgensen E, Ekblond A, Kastrup J: Adipose-derived mesenchymal stromal cells for chronic myocardial ischemia (MyStromalCell Trial): study design. Regen Med 2012, 7:421-428.
• [79]Friis T, Haack-Sorensen M, Mathiasen AB, Ripa RS, Kristoffersen US, Jorgensen E, Hansen L, Bindslev L, Kjaer A, Hesse B, et al.: Mesenchymal stromal cell derived endothelial progenitor treatment in patients with refractory angina. Scand Cardiovasc J 2011, 45:161-168.
• [80]Katritsis DG, Sotiropoulou PA, Karvouni E, Karabinos I, Korovesis S, Perez SA, Voridis EM, Papamichail M: Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheter Cardiovasc Interv 2005, 65:321-329.
• [81]Lasala GP, Silva JA, Kusnick BA, Minguell JJ: Combination stem cell therapy for the treatment of medically refractory coronary ischemia: a Phase I study. Cardiovasc Revasc Med 2011, 12:29-34.
• [82]Frangioni JV, Hajjar RJ: In vivo tracking of stem cells for clinical trials in cardiovascular disease. Circulation 2004, 110:3378-3383.
• [83]Bulte JW, Kraitchman DL: Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004, 17:484-499.
• [84]Bulte JW, Kraitchman DL: Monitoring cell therapy using iron oxide MR contrast agents. Curr Pharm Biotechnol 2004, 5:567-584.
• [85]Rogers WJ, Meyer CH, Kramer CM: Technology insight: in vivo cell tracking by use of MRI. Nat Clin Pract Cardiovasc Med 2006, 3:554-562.
• [86]Kraitchman DL, Bulte JW: In vivo imaging of stem cells and Beta cells using direct cell labeling and reporter gene methods. Arterioscler Thromb Vasc Biol 2009, 29:1025-1030.
• [87]Lau JF, Anderson SA, Adler E, Frank JA: Imaging approaches for the study of cell-based cardiac therapies. Nat Rev Cardiol 2010, 7:97-105.
• [88]Mathiasen AB, Haack-Sorensen M, Kastrup J: Mesenchymal stromal cells for cardiovascular repair: current status and future challenges. Future Cardiol 2009, 5:605-617.
• [89]Ferreira L, Pedroso DC, Vazao H, Gomes RS: Stem cell-based therapies for heart regeneration: what did the bench teach us? Cardiovasc Hematol Disord Drug Targets 2010, 10:173-185.
• [90]Fu Y, Kraitchman DL: Stem cell labeling for noninvasive delivery and tracking in cardiovascular regenerative therapy. Expert Rev Cardiovasc Ther 2010, 8:1149-1160.
• [91]Ransohoff KJ, Wu JC: Advances in cardiovascular molecular imaging for tracking stem cell therapy. Thromb Haemost 2010, 104:13-22.
• [92]Guyette JP, Cohen IS, Gaudette GR: Strategies for regeneration of heart muscle. Crit Rev Eukaryot Gene Expr 2010, 20:35-50.
• [93]Terrovitis JV, Smith RR, Marban E: Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res 2010, 106:479-494.
• [94]Wei H, Ooi TH, Tan G, Lim SY, Qian L, Wong P, Shim W: Cell delivery and tracking in post-myocardial infarction cardiac stem cell therapy: an introduction for clinical researchers. Heart Fail Rev 2010, 15:1-14.
• [95]Wu JC, Abraham MR, Kraitchman DL: Current perspectives on imaging cardiac stem cell therapy. J Nucl Med 2010, 51(1):128S-136S.
• [96]van der Spoel TI, Lee JC, Vrijsen K, Sluijter JP, Cramer MJ, Doevendans PA, van Belle E, Chamuleau SA: Non-surgical stem cell delivery strategies and in vivo cell tracking to injured myocardium. Int J Cardiovasc Imaging 2011, 27:367-383.
• [97]Winter P, Caruthers S, Lanza G, Wickline S: Quantitative cardiovascular magnetic resonance for molecular imaging. J Cardiovasc Magn Reson 2010, 12:62.
• [98]Carballo D, Nkoulou R, Vincenti G, Quercioli A, Heinzer S, Didier D, Stuber M, Schindler T, Ratib O, Vallee J: Value of a hybrid PET/MRI in the assessment of cardiac viability. J Cardiovasc Magn Reson 2012, 14:P80.
• [99]Beller GA, Sinusas AJ: Experimental studies of the physiologic properties of technetium-99m isonitriles. Am J Cardiol 1990, 66:5E-8E.
• [100]Kuliszewski MA, Fujii H, Liao C, Smith AH, Xie A, Lindner J, Leong-Poi H: Molecular imaging of endothelial progenitor cell engraftment using contrast-enhanced ultrasound and targeted microbubbles. Cardiovasc Res 2009. doi:10.1093/cvr/cvp218
• [101]Herbst SM, Klegerman ME, Kim H, Qi J, Shelat H, Wassler M, Moody MR, Yang CM, Ge X, Zou Y, et al.: Delivery of stem cells to porcine arterial wall with echogenic liposomes conjugated to antibodies against CD34 and intercellular adhesion molecule-1. Mol Pharm 2010, 7:3-11.
• [102]Toma C, Fisher A, Wang J, Chen X, Grata M, Leeman J, Winston B, Kaya M, Fu H, Lavery L, et al.: Vascular endoluminal delivery of mesenchymal stem cells using acoustic radiation force. Tissue Eng Part A 2011, 17:1457-1464.
• [103]Kaya M, Toma C, Wang J, Grata M, Fu H, Villanueva FS, Chen X: Acoustic radiation force for vascular cell therapy: in vitro validation. Ultrasound Med Biol 2012, 38:1989-1997.
• [104]Nam SY, Ricles LM, Suggs LJ, Emelianov SY: In vivo Ultrasound and Photoacoustic Monitoring of Mesenchymal Stem Cells Labeled with Gold Nanotracers. PLoS One 2012, 7:e37267.
• [105]Cui W, Wang J, Chen X, Fisher A, Kim K, Carson A, Kripfgans OD, Haworth KJ, Wagner WR, Villanueva FS: Stem cell tracking using ultrasound contrast agents. Circulation 2008, 118:S642.
• [106]Hoshino K, Ly HQ, Frangioni JV, Hajjar RJ: In vivo tracking in cardiac stem cell-based therapy. Prog Cardiovasc Dis 2007, 49:414-420.
• [107]Ziadloo A, Burks SR, Gold EM, Lewis BK, Chaudhry A, Merino MJ, Frenkel V, Frank JA: Enhanced homing permeability and retention of bone marrow stromal cells by noninvasive pulsed focused ultrasound. Stem Cells 2012, 30:1216-1227.
• [108]Kraitchman DL, Bulte JW: Imaging of stem cells using MRI. Basic Res Cardiol 2008, 103:105-113.
• [109]Toso C, Vallee JP, Morel P, Ris F, Demuylder-Mischler S, Lepetit-Coiffe M, Marangon N, Saudek F, James Shapiro AM, Bosco D, Berney T: Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant 2008, 8:701-706.
• [110]de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, et al.: Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 2005, 23:1407-1413.
• [111]Zhu J, Zhou L, XingWu F: Tracking neural stem cells in patients with brain trauma. N Engl J Med 2006, 355:2376-2378.
• [112]Callera F, de Melo CM: Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells’ migration into the injured site. Stem Cells Dev 2007, 16:461-466.
• [113]Callera F, do Nascimento RX: Delivery of autologous bone marrow precursor cells into the spinal cord via lumbar puncture technique in patients with spinal cord injury: a preliminary safety study. Exp Hematol 2006, 34:130-131.
• [114]Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S: Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010, 67:1187-1194.
• [115]Kraitchman DL, Heldman AW, Atalar E, Amado LC, Martin BJ, Pittenger MF, Hare JM, Bulte JW: In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 2003, 107:2290-2293.
• [116]Hill JM, Dick AJ, Raman VK, Thompson RB, Yu ZX, Hinds KA, Pessanha BS, Guttman MA, Varney TR, Martin BJ, et al.: Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 2003, 108:1009-1014.
• [117]Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, Lewis BK, Bryant LH Jr, Bulte JWM: Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003, 228:480-487.
• [118]Dick AJ, Guttman MA, Raman VK, Peters DC, Pessanha BS, Hill JM, Smith S, Scott G, McVeigh ER, Lederman RJ: Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in swine. Circulation 2003, 108:2899-2904.
• [119]Lima JA, Judd RM, Bazille A, Schulman SP, Atalar E, Zerhouni EA: Regional heterogeneity of human myocardial infarcts demonstrated by contrast-enhanced MRI. Potential mechanisms. Circulation 1995, 92:117-1125.
• [120]Soto AV, Gilson WD, Kedziorek D, Fritzges D, Izbudak I, Young RG, Pittenger MF, Bulte JW, Kraitchman DL: MRI tracking of regional persistence of feridex-labeled mesenchymal stem cells in a canine myocardial infarction model. J Cardiovasc Magn Reson 2006, 8:89-90.
• [121]Garot J, Unterseeh T, Teiger E, Champagne S, Chazaud B, Gherardi R, Hittinger L, Gueret P, Rahmouni A, Sonnet C, et al.: Magnetic resonance imaging of targeted catheter-based implantation of myogenic precursor cells into infarcted left ventricular myocardium. J Am Coll Cardiol 2003, 41:1841-1846.
• [122]Weber A, Pedrosa I, Kawamoto A, Himes N, Munasinghe J, Asahara T, Rofsky NM, Losordo DW: Magnetic resonance mapping of transplanted endothelial progenitor cells for therapeutic neovascularization in ischemic heart disease. Eur J Cardiothorac Surg 2004, 26:137-143.
• [123]Tallheden T, Nannmark U, Lorentzon M, Rakotonirainy O, Soussi B, Waagstein F, Jeppsson A, Sjogren-Jansson E, Lindahl A, Omerovic E: In vivo MR imaging of magnetically labeled human embryonic stem cells. Life Sci 2006, 79:999-1006.
• [124]Stuckey DJ, Carr CA, Martin-Rendon E, Tyler DJ, Willmott C, Cassidy PJ, Hale SJ, Schneider JE, Tatton L, Harding SE, et al.: Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart. Stem Cells 2006, 24:1968-1975.
• [125]Ebert SN, Taylor DG, Nguyen HL, Kodack DP, Beyers RJ, Xu Y, Yang Z, French BA: Noninvasive tracking of cardiac embryonic stem cells in vivo using magnetic resonance imaging techniques. Stem Cells 2007, 25:2936-2944.
• [126]Delo D, Olson J, Baptista P, D'Agostino R Jr, Atala A, Zhu JM, Soker S: Non-invasive longitudinal tracking of human amniotic fluid stem cells in the mouse heart. Stem Cells Dev 2008, 17(6):1185-1194.
• [127]Chapon C, Jackson JS, Aboagye EO, Herlihy AH, Jones WA, Bhakoo KK: An in vivo multimodal imaging study using MRI and PET of stem cell transplantation after myocardial infarction in rats. Mol Imaging Biol 2009, 11:31-38.
• [128]Josephson L, Tung CH, Moore A, Weissleder R: High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug Chem 1999, 10:186-191.
• [129]Amado LC, Schuleri KH, Saliaris AP, Boyle AJ, Helm R, Oskouei B, Centola M, Eneboe V, Young R, Lima JA, et al.: Multimodality noninvasive imaging demonstrates in vivo cardiac regeneration after mesenchymal stem cell therapy. J Am Coll Cardiol 2006, 48:2116-2124.
• [130]Schuleri KH, Amado LC, Boyle AJ, Centola M, Saliaris AP, Gutman MR, Hatzistergos KE, Oskouei BN, Zimmet JM, Young RG, et al.: Early improvement in cardiac tissue perfusion due to mesenchymal stem cells. Am J Physiol Heart Circ Physiol 2008, 294:H2002-2011.
• [131]Axel L, Dougherty L: MR imaging of motion with spatial modulation of magnetization. Radiology 1989, 171:841-845.
• [132]Zerhouni EA, Parish DM, Rogers WJ, Yang A, Shapiro EP: Human heart: tagging with MR imaging-a method for noninvasive assessment of myocardial motion. Radiology 1988, 169:59-63.
• [133]Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, Schar M, Gerstenblith G, Weiss RG, Marban E, Abraham MR: Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 2008, 117:1555-1562.
• [134]Higuchi T, Anton M, Dumler K, Seidl S, Pelisek J, Saraste A, Welling A, Hofmann F, Oostendorp RA, Gansbacher B, et al.: Combined reporter gene PET and iron oxide MRI for monitoring survival and localization of transplanted cells in the rat heart. J Nucl Med 2009, 50:1088-1094.
• [135]Li Z, Suzuki Y, Huang M, Cao F, Xie X, Connolly AJ, Yang PC, Wu JC: Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells 2008, 26:864-873.
• [136]Seppenwoolde JH, Viergever MA, Bakker CJ: Passive tracking exploiting local signal conservation: the white marker phenomenon. Magn Reson Med 2003, 50:784-790.
• [137]Bowen CV, Zhang X, Saab G, Gareau PJ, Rutt BK: Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med 2002, 48:52-61.
• [138]Mani V, Adler E, Briley-Saebo KC, Bystrup A, Fuster V, Keller G, Fayad ZA: Serial in vivo positive contrast MRI of iron oxide-labeled embryonic stem cell-derived cardiac precursor cells in a mouse model of myocardial infarction. Magn Reson Med 2008, 60:73-81.
• [139]Mani V, Briley-Saebo KC, Hyafil F, Itskovich V, Fayad ZA: Positive magnetic resonance signal enhancement from ferritin using a GRASP (GRE acquisition for superparamagnetic particles) sequence: ex vivo and in vivo study. J Cardiovasc Magn Reson 2006, 8:49-50.
• [140]Mani V, Saebo KC, Itskovich V, Samber DD, Fayad ZA: GRadient echo Acquisition for Superparamagnetic particles with Positive contrast (GRASP): Sequence characterization in membrane and glass superparamagnetic iron oxide phantoms at 1.5T and 3T. Magn Reson Med 2006, 55:126-135.
• [141]Cunningham CH, Arai T, Yang PC, McConnell MV, Pauly JM, Conolly SM: Positive contrast magnetic resonance imaging of cells labeled with magnetic nanoparticles. Magn Reson Med 2005, 53:999-1005.
• [142]Stuber M, Gilson WD, Schar M, Kedziorek DA, Hofmann LV, Shah S, Vonken EJ, Bulte JW, Kraitchman DL: Positive contrast visualization of iron oxide-labeled stem cells using inversion-recovery with ON-resonant water suppression (IRON). Magn Reson Med 2007, 58:1072-1077.
• [143]Shah SS, Gilson WD, Weiss RG, Barnett BP, Bulte JW, Kraitchman DL, Stuber M: Fat suppression strategies for off-resonance (IRON) imaging of magnetically-labeled stem cells. J Cardiovasc Magn Reson 2006, 8:87-88.
• [144]Dahnke H, Liu W, Herzka D, Frank JA, Schaeffter T: Susceptibility gradient mapping (SGM): a new postprocessing method for positive contrast generation applied to superparamagnetic iron oxide particle (SPIO)-labeled cells. Magn Reson Med 2008, 60:595-603.
• [145]Zhou R, Idiyatullin D, Moeller S, Corum C, Zhang H, Qiao H, Zhong J, Garwood M: SWIFT detection of SPIO-labeled stem cells grafted in the myocardium. Magn Reson Med 2010, 63:1154-1161.
• [146]Girard OM, Du J, Mattrey RM: Investigation of SPIO T1-signature: positive contrast using ultrashort TE imaging. Honolulu, Hawaii: 17th Proc Intl Soc Mag Reson Med; 2009:2769.
• [147]Seethamraju RT, Nielles-Vallespin S, Weissleder R, Sosnovik DE: Ultrashort TE imaging of iron-oxide nanoparticles produces positive contrast with low nanomolar sensitivity at clinical field strengths. Montreal, Canada: World Molecular Imaging Conference; 2009:219.
• [148]Corot C, Warlin D: Superparamagnetic iron oxide nanoparticles for MRI: contrast media pharmaceutical company R&D perspective. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2013, 5:411-422.
• [149]Chen S, Alcantara D, Josephson L: A magnetofluorescent nanoparticle for ex-vivo cell labeling by covalently linking the drugs protamine and Feraheme. J Nanosci Nanotechnol 2011, 11:3058-3064.
• [150]Thu MS, Bryant LH, Coppola T, Jordan EK, Budde MD, Lewis BK, Chaudhry A, Ren J, Varma NR, Arbab AS, Frank JA: Self-assembling nanocomplexes by combining ferumoxytol, heparin and protamine for cell tracking by magnetic resonance imaging. Nat Med 2012, 18:463-467.
• [151]Ahrens ET, Flores R, Xu H, Morel PA: In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 2005, 23:983-987.
• [152]Partlow KC, Chen J, Brant JA, Neubauer AM, Meyerrose TE, Creer MH, Nolta JA, Caruthers SD, Lanza GM, Wickline SA: 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. Faseb J 2007, 21:1647-1654.
• [153]Barnett BP, Ruiz-Cabello J, Hota P, Ouwerkerk R, Shamblott MJ, Lauzon C, Walczak P, Gilson WD, Chacko VP, Kraitchman DL, et al.: Use of perfluorocarbon nanoparticles for non-invasive multimodal cell tracking of human pancreatic islets. Contrast Media Mol Imaging 2011, 6:251-259.
• [154]Lim F, Sun AM: Microencapsulated islets as bioartificial endocrine pancreas. Science 1980, 210:908-910.
• [155]Barnett BP, Arepally A, Karmarkar PV, Qian D, Gilson WD, Walczak P, Howland V, Lawler L, Lauzon C, Stuber M, et al.: Magnetic resonance-guided, real-time targeted delivery and imaging of magnetocapsules immunoprotecting pancreatic islet cells. Nat Med 2007, 13:986-991.
• [156]Barnett BP, Arepally A, Stuber M, Arifin DR, Kraitchman DL, Bulte JW: Synthesis of magnetic resonance-, X-ray- and ultrasound-visible alginate microcapsules for immunoisolation and noninvasive imaging of cellular therapeutics. Nat Protoc 2011, 6:1142-1151.
• [157]Barnett BP, Ruiz-Cabello J, Hota P, Liddell R, Walczak P, Howland V, Chacko VP, Kraitchman DL, Arepally A, Bulte JW: Fluorocapsules for improved function, immunoprotection, and visualization of cellular therapeutics with MR, US, and CT imaging. Radiology 2011, 258:182-191.
• [158]Fu Y, Kedziorek D, Ouwerkerk R, Crisostomo V, Gilson W, Azene N, Arepally A, Lorenz C, Shea S, Krieg R, et al.: Multifunctional perfluorooctylbromide alginate microcapsules for monitoring of mesenchymal stem cell delivery using CT and MRI. J Cardiovasc Magn Reson 2009, 11:O7.
• [159]Arifin DR, Long CM, Gilad AA, Alric C, Roux S, Tillement O, Link TW, Arepally A, Bulte JW: Trimodal gadolinium-gold microcapsules containing pancreatic islet cells restore normoglycemia in diabetic mice and can be tracked by using US, CT, and positive-contrast MR imaging. Radiology 2011, 260:790-798.
• [160]Louie AY, Huber MM, Ahrens ET, Rothbacher U, Moats R, Jacobs RE, Fraser SE, Meade TJ: In vivo visualization of gene expression using magnetic resonance imaging. Nat Biotechnol 2000, 18:321-325.
• [161]Campan M, Lionetti V, Aquaro GD, Forini F, Matteucci M, Vannucci L, Chiuppesi F, Di Cristofano C, Faggioni M, Maioli M, et al.: Ferritin as a reporter gene for in vivo tracking of stem cells by 1.5-T cardiac MRI in a rat model of myocardial infarction. Am J Physiol Heart Circ Physiol 2011, 300:H2238-2250.
• [162]Gilad AA, McMahon MT, Walczak P, Winnard PT Jr, Raman V, van Laarhoven HW, Skoglund CM, Bulte JW, van Zijl PC: Artificial reporter gene providing MRI contrast based on proton exchange. Nat Biotechnol 2007, 25:217-219.
• [163]Zhou J, Wilson DA, Sun PZ, Klaus JA, Van Zijl PC: Quantitative description of proton exchange processes between water and endogenous and exogenous agents for WEX, CEST, and APT experiments. Magn Reson Med 2004, 51:945-952.
• [164]Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LEJ, Berman D, Czer LSC, Marbán L, Mendizabal A, Johnston PV, et al.: Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. The Lancet 2012, 379:895-904.
• [165]Bolli R, Chugh AR, D'Amario D, Loughran JH, Stoddard MF, Ikram S, Beache GM, Wagner SG, Leri A, Hosoda T, et al.: Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378(9806):1847-1857.
• [166]Ricles LM, Nam SY, Sokolov K, Emelianov SY, Suggs LJ: Function of mesenchymal stem cells following loading of gold nanotracers. Int J Nanomedicine 2011, 6:407-416.
• [167]Chithrani BD, Chan WC: Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 2007, 7:1542-1550.
• [168]Barnett BP, Kraitchman DL, Lauzon C, Magee CA, Walczak P, Gilson WD, Arepally A, Bulte JW: Radiopaque alginate microcapsules for X-ray visualization and immunoprotection of cellular therapeutics. Mol Pharm 2006, 3:531-538.
• [169]Nahrendorf M, Sosnovik D, French B, Swirski FK, Bengel FM, Sadeghi M, Lindner J, Wu J, Kraitchman D, Fayad Z, Sinusas A: Multimodality cardiovascular molecular imaging - Part II. Circ Cardiovasc Imaging 2009, 2:56-70.
• [170]Cosby KM, Hofmann LV, Barnett BP, Kediorek DA, Gilson W, Korosoglou G, Huang G, Bulte JWM, Kraitchman DL: A novel radio-opaque barium/alginate microencapsulation technique for allogeneic mesenchymal stem cell delivery and localization. J Cardiovasc Magn Reson 2007, 9(2):401-402.
• [171]Kedziorek DA, Hofmann LV, Fu Y, Gilson WD, Cosby KM, Kohl B, Barnett BP, Simons BW, Walczak P, Bulte JW, et al.: X-ray-visible microcapsules containing mesenchymal stem cells improve hind limb perfusion in a rabbit model of peripheral arterial disease. Stem Cells 2012, 30:1286-1296.
• [172]Fu Y, Xie Y, Kediorek DA, Shea SM, Ouwerkerk R, Ehtiati T, Huang G, Krieg R, Wacker F, Bulte JWM, Kraitchman DL: MRI and CT tracking of mesenchymal stem cells with novel perfluorinated alginate microcapsules. J Cardiovasc Magn Reson 2010, 12:O14.
• [173]Azene NM, Ehtiati T, Fu Y, Flammang A, Guehring J, Gilson WD, Kedziorek DA, Cook J, P.V J, Kraitchman DL: Intrapericardial delivery of visible microcapsules containing stem cells using XFM (X-ray fused with magnetic resonance imaging). J Cardiovasc Magn Reson 2011, 13:P26.
• [174]Rhode KS, Hill DL, Edwards PJ, Hipwell J, Rueckert D, Sanchez-Ortiz G, Hegde S, Rahunathan V, Razavi R: Registration and tracking to integrate X-ray and MR images in an XMR facility. IEEE Trans Med Imaging 2003, 22:1369-1378.
• [175]de Silva R, Gutierrez LF, Raval AN, McVeigh ER, Ozturk C, Lederman RJ: X-Ray fused With magnetic resonance imaging (XFM) to target endomyocardial injections: Validation in a swine model of myocardial infarction. Circulation 2006, 114:2342-2350.
• [176]Barbash IM, Cecchini S, Faranesh AZ, Virag T, Li L, Yang Y, Hoyt RF, Kornegay JN, Bogan JR, Garcia L, et al.: MRI roadmap-guided transendocardial delivery of exon-skipping recombinant adeno-associated virus restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Gene Ther 2013, 20:274-282.
• [177]Razavi R, Hill DL, Keevil SF, Miquel ME, Muthurangu V, Hegde S, Rhode K, Barnett M, van Vaals J, Hawkes DJ, Baker E: Cardiac catheterisation guided by MRI in children and adults with congenital heart disease. Lancet 2003, 362:1877-1882.
• [178]Duckett SG, Ginks M, Shetty AK, Knowles BR, Totman JJ, Chiribiri A, Ma YL, Razavi R, Schaeffter T, Carr-White G, et al.: Realtime fusion of cardiac magnetic resonance imaging and computed tomography venography with X-ray fluoroscopy to aid cardiac resynchronisation therapy implantation in patients with persistent left superior vena cava. Europace 2011, 13:285-286.