Non-surgical stem cell delivery strategies and in vivo cell tracking to injured myocardium

International Journal of Cardiovascular Imaging

Volumn 27, Issue 3, 2011, Pages 367-383

  Van Der Spoel, Tycho I G ^a   Lee, Joe Chun Tsu ^b   Vrijsen, Krijn ^a   Sluijter, Joost P G ^a,c   Cramer, Maarten Jan M ^a   Doevendans, Pieter A ^a,c   Van Belle, Eric ^a   Chamuleau, Steven A J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF MALAYA   (Malaysia)

^c ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

Author keywords

Cell delivery; Magnetic resonance imaging; Nuclear imaging; Stem cells

Indexed keywords

CELL LABELING; CELL TRACKING; HEART CATHETERIZATION; HEART FAILURE; HEART MUSCLE INJURY; HUMAN; INTERMETHOD COMPARISON; ISOTOPE LABELING; NONHUMAN; NONSURGICAL INVASIVE THERAPY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT SAFETY; POSITRON EMISSION TOMOGRAPHY; REPORTER GENE; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; STEM CELL TRANSPLANTATION; VEIN CATHETERIZATION;

ANIMALS; CELL TRACKING; HEART FAILURE; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; REGENERATION; STEM CELL TRANSPLANTATION; TIME FACTORS; TREATMENT OUTCOME;

EID: 79958725790     PISSN: 15695794     EISSN: 15730743     Source Type: Journal    
DOI: 10.1007/s10554-010-9658-4     Document Type: Review

References (100)

1. W Rosamond K Flegal K Furie A Go K Greenlund N Haase SM Hailpern M Ho V Howard B Kissela S Kittner D Lloyd-Jones M McDermott J Meigs C Moy G Nichol C O'Donnell V Roger P Sorlie J Steinberger T Thom M Wilson Y Hong for the American Heart Association Statistics Committee, Stroke Statistics Subcommittee 2008 Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee Circulation 117 e25 146 18086926 10.1161/CIRCULATIONAHA.107.187998
2. World Health Organization (2007) The atlas of heart disease and stroke. pp 48-49
3. M Halkos ZQ Zhao F Kerendi NP Wang R Jiang L Schmarkey B Martin A Quyyumi W Few H Kin R Guyton J Vinten-Johansen 2008 Intravenous infusion of mesenchymal stem cells enhances regional perfusion and improves ventricular function in a porcine model of myocardial infarction Basic Res Cardiol 103 525 536 18704259 10.1007/s00395-008-0741-0
4. JM Hare JH Traverse TD Henry N Dib RK Strumpf SP Schulman G Gerstenblith AN DeMaria AE Denktas RS Gammon JB Hermiller Jr MA Reisman GL Schaer W Sherman 2009 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 54 2277 2286 19958962 10.1016/j.jacc.2009.06.055 1:CAS:528:DC%2BC3cXmsl2guw%3D%3D
5. EC Perin HFR Dohmann R Borojevic SA Silva ALS Sousa CT Mesquita MID Rossi AC Carvalho HS Dutra HJF Dohmann GV Silva L Belem R Vivacqua FOD Rangel R Esporcatte YJ Geng WK Vaughn JAR Assad ET Mesquita JT Willerson 2003 Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure Circulation 107 2294 2302 12707230 10.1161/01.CIR.0000070596.30552.8B (Pubitemid 36578498)
6. EC Perin GV Silva JAR Assad D Vela LM Buja ALS Sousa S Litovsky J Lin WK Vaughn S Coulter MR Fernandes JT Willerson 2008 Comparison of intracoronary and transendocardial delivery of allogeneic mesenchymal cells in a canine model of acute myocardial infarction J Mol Cell Cardiol 44 486 495 18061611 10.1016/j.yjmcc.2007.09.012 1:CAS:528:DC%2BD1cXjtl2lsL8%3D (Pubitemid 351374698)
7. S Tomita DAG Mickle RD Weisel ZQ Jia LC Tumiati Y Allidina P Liu RK Li 2002 Improved heart function with myogenesis and angiogenesis after autologous porcine bone marrow stromal cell transplantation J Thorac Cardiovasc Surg 123 1132 1140 12063460 10.1067/mtc.2002.120716
8. D Orlic J Kajstura S Chimenti I Jakoniuk SM Anderson B Li J Pickel R McKay B Nadal-Ginard DM Bodine A Leri P Anversa 2001 Bone marrow cells regenerate infarcted myocardium Nature 410 701 705 11287958 10.1038/35070587 1:CAS:528:DC%2BD3MXivFSmsb4%3D (Pubitemid 32290358)
9. JS Wang D Shum-Tim J Galipeau E Chedrawy N Eliopoulos RC Chiu 2000 Marrow stromal cells for cellular cardiomyoplasty: feasibility and potential clinical advantages J Thorac Cardiovasc Surg 120 999 1006 11044327 10.1067/mtc.2000. 110250 1:STN:280:DC%2BD3M%2FltlOnsA%3D%3D
10. JM Hill AJ Dick VK Raman RB Thompson ZX Yu KA Hinds BSS Pessanha MA Guttman TR Varney BJ Martin CE Dunbar ER McVeigh RJ Lederman 2003 Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells Circulation 108 1009 1014 12912822 10.1161/01.CIR.0000084537.66419.7A (Pubitemid 37048233)
11. M Hofmann KC Wollert GP Meyer A Menke L Arseniev B Hertenstein A Ganser WH Knapp H Drexler 2005 Monitoring of bone marrow cell homing into the infarcted human myocardium Circulation 111 2198 2202 15851598 10.1161/01.CIR.0000163546. 27639.AA (Pubitemid 40632435)
12. DL Kraitchman M Tatsumi WD Gilson T Ishimori D Kedziorek P Walczak WP Segars H Chen D Fritzges I Izbudak RG Young M Marcelino MF Pittenger M Solaiyappan RC Boston BMW Tsui RL Wahl JWM Bulte 2005 Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction Circulation 112 1451 1461 16129797 10.1161/CIRCULATIONAHA.105.537480 (Pubitemid 41291771)
13. 1 visibility without affecting glioma cell growth or motility Magn Reson Med 59 1014 1020 18429039 10.1002/mrm.21503 1:CAS:528:DC%2BD1cXmt1CnsLc%3D (Pubitemid 351590514)
14. M Lewin N Carlesso CH Tung XW Tang D Cory DT Scadden R Weissleder 2000 Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells Nat Biotechnol 18 410 414 10748521 10.1038/74464 1:CAS:528:DC%2BD3cXis1Gmt7s%3D (Pubitemid 30217528)
15. JW Bulte T Douglas B Witwer E Strable BK Lewis H Zywicke B Miller P van Gelderen BM Moskowitz ID Duncan JA Frank 2001 Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells Nat Biotechnol 19 1141 1147 11731783 10.1038/nbt1201-1141 1:CAS:528:DC%2BD3MXptV2rt7Y%3D (Pubitemid 33115700)
16. JA Frank BR Miller AS Arbab HA Zywicke EK Jordan BK Lewis LH Bryant Jr JWM Bulte 2003 Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents Radiology 228 480 487 12819345 10.1148/radiol.2281020638 (Pubitemid 36910091)
17. L Kostura DL Kraitchman AM Mackay MF Pittenger JW Bulte 2004 Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis NMR Biomed 17 513 517 15526348 10.1002/nbm.925 (Pubitemid 39549429)
18. N Himes JY Min R Lee C Brown J Shea X Huang YF Xiao JP Morgan D Burstein P Oettgen 2004 In vivo MRI of embryonic stem cells in a mouse model of myocardial infarction Magn Reson Med 52 1214 1219 15508153 10.1002/mrm.20220 (Pubitemid 39453297)
19. KS Cahill S Germain BJ Byrne GA Walter 2004 Non-invasive analysis of myoblast transplants in rodent cardiac muscle Int J Cardiovasc Imaging 20 593 598 15856647 10.1007/s10554-004-3902-8 (Pubitemid 40372376)
20. DJ Stuckey CA Carr E Martin-Rendon DJ Tyler C Willmott PJ Cassidy SJM Hale JE Schneider L Tatton SE Harding GK Radda S Watt K Clarke 2006 Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart Stem Cells 24 1968 1975 16627684 10.1634/stemcells.2006-0074 1:CAS:528:DC%2BD28XhtFKiu77E (Pubitemid 44474173)
21. Y Amsalem Y Mardor MS Feinberg N Landa L Miller D Daniels A Ocherashvilli R Holbova O Yosef IM Barbash J Leor 2007 Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium Circulation 116 I-38 10.1161/CIRCULATIONAHA.106.680231 1:CAS:528:DC%2BD2sXpvFWkt74%3D (Pubitemid 47480768)
22. A Aicher W Brenner M Zuhayra C Badorff S Massoudi B Assmus T Eckey E Henze AM Zeiher S Dimmeler 2003 Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling Circulation 107 2134 2139 12695305 10.1161/01.CIR.0000062649.63838.C9 (Pubitemid 36532196)
23. L Bindslev M Haack-Sorensen K Bisgaard L Kragh S Mortensen B Hesse A Kjær J Kastrup 2006 Labelling of human mesenchymal stem cells with indium-111 for SPECT imaging: effect on cell proliferation and differentiation Eur J Nucl Med Mol Imaging 33 1171 1177 16763813 10.1007/s00259-006-0093-7 1:STN:280:DC%2BD2s3htFWrtw%3D%3D (Pubitemid 44484473)
24. Y Jin H Kong RZ Stodilka RG Wells P Zabel PA Merrifield J Sykes FS Prato 2005 Determining the minimum number of detectable cardiac-transplanted 111In-tropolone-labelled bone-marrow-derived mesenchymal stem cells by SPECT Phys Med Biol 19 4445 4455 10.1088/0031-9155/50/19/001 (Pubitemid 41361509)
25. W Brenner A Aicher T Eckey S Massoudi M Zuhayra U Koehl C Heeschen WU Kampen AM Zeiher S Dimmeler E Henze 2004 111In-labeled CD34 + hematopoietic progenitor cells in a rat myocardial infarction model J Nucl Med 45 512 518 15001696 1:CAS:528:DC%2BD2cXivVCju7c%3D (Pubitemid 47618629)
26. B Nowak C Weber A Schober U Zeiffer E Liehn P von Hundelshausen P Reinartz W Schaefer U Buell 2007 Indium-111 oxine labelling affects the cellular integrity of haematopoietic progenitor cells Eur J Nucl Med Mol Imaging 34 715 721 17096094 10.1007/s00259-006-0275-3 1:CAS:528:DC%2BD2sXks1agsb4%3D (Pubitemid 46669358)
27. BB Chin Y Nakamoto JW Bulte MF Pittenger R Whal DL Kraitchman 2003 111In oxine labelled mesenchymal stem cell SPECT after intravenous administration in myocardial infarction Nucl Med Commun 24 1149 1154 14569169 10.1097/00006231- 200311000-00005 1:STN:280:DC%2BD2czktFCjtg%3D%3D (Pubitemid 39625401)
28. RB Patterson G Mayfield EB Silberstein RF Kempczinski 1989 The potential unreliability of indium 111 oxine labeling in studies of endothelial cell kinetics J Vasc Surg 10 650 655 2511341 10.1067/mva.1989.15992 1:STN:280:DyaK3c%2FmsVyqtQ%3D%3D (Pubitemid 20024958)
29. M Penicka O Lang P Widimsky P Kobylka T Kozak T Vanek J Dvorak J Tintera J Bartunek 2007 One-day kinetics of myocardial engraftment after intracoronary injection of bone marrow mononuclear cells in patients with acute and chronic myocardial infarction Heart 93 837 841 17309910 10.1136/hrt.2006.091934 1:STN:280:DC%2BD2szlsVCqsQ%3D%3D (Pubitemid 46998985)
30. IM Barbash P Chouraqui J Baron MS Feinberg S Etzion A Tessone L Miller E Guetta D Zipori LH Kedes RA Kloner J Leor 2003 Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution Circulation 108 863 868 12900340 10.1161/01.CIR.0000084828.50310.6A (Pubitemid 37022130)
31. D Hou EA-S Youssef TJ Brinton P Zhang P Rogers ET Price AC Yeung BH Johnstone PG Yock KL March 2005 Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials Circulation 112 I-150
32. C Kupatt R Hinkel M Lamparter ML von Bruhl T Pohl J Horstkotte H Beck S Muller S Delker FJ Gildehaus H Buning AK Hatzopoulos P Boekstegers 2005 Retroinfusion of embryonic endothelial progenitor cells attenuates ischemia-reperfusion injury in pigs: role of phosphatidylinositol 3-kinase/AKT kinase Circulation 112 I-117
33. S Lyngbaek R Ripa M Haack-Sorensen A Cortsen L Kragh C Andersen E Jorgensen A Kjaer J Kastrup B Hesse 2010 Serial in vivo imaging of the porcine heart after percutaneous, intramyocardially injected 111In-labeled human mesenchymal stromal cells Int J Cardiovasc Imaging 26 273 284 19921546 10.1007/s10554-009-9532-4
34. R Zhou DH Thomas H Qiao HS Bal SR Choi A Alavi VA Ferrari HF Kung PD Acton 2005 In vivo detection of stem cells grafted in infarcted rat myocardium J Nucl Med 46 816 822 15872356 1:CAS:528:DC%2BD28XitFSqsbw%3D
35. A Caveliers G De Keulenaer H Everaert H Everaert G Van Camp S Verheye J Roland D Schoors PR Franken R Schots 2007 In vivo visualization of 111In labeled CD133 + peripheral blood stem cells after intracoronary administration in patients with chronic ischemic heart disease Q J Nucl Med Mol Imaging 51 61 66 17372574 1:STN:280:DC%2BD2s7nsVWqtA%3D%3D (Pubitemid 46824662)
36. V Schachinger A Aicher N Dobert R Rover J Diener S Fichtlscherer B Assmus FH Seeger C Menzel W Brenner S Dimmeler AM Zeiher 2008 Pilot trial on determinants of progenitor cell recruitment to the infarcted human myocardium Circulation 118 1425 1432 18794392 10.1161/CIRCULATIONAHA.108.777102
37. B Doyle BJ Kemp P Chareonthaitawee C Reed J Schmeckpeper P Sorajja S Russell P Araoz SJ Riederer NM Caplice 2007 Dynamic tracking during intracoronary injection of 18F-FDG-labeled progenitor cell therapy for acute myocardial infarction J Nucl Med 48 1708 1714 17909258 10.2967/jnumed.107.042838 (Pubitemid 47572719)
38. H Qian Y Yang J Huang R Gao K Dou G Yang J Li R Shen Z He M Lu S Zhao 2010 Intracoronary delivery of autologous bone marrow mononuclear cells radiolabeled by 18F-fluoro-deoxy-glucose: tissue distribution and impact on post-infarct swine hearts J Cell Biochem 102 64 74 10.1002/jcb.21277 (Pubitemid 47381281)
39. AY Louie MM Hüber ET Ahrens U Rothbächer R Moats RE Jacobs SE Fraser TJ Meade 2000 In vivo visualization of gene expression using magnetic resonance imaging Nat Biotechnol 18 321 325 10700150 10.1038/73780 1:CAS:528:DC%2BD3cXhvVyru7c%3D (Pubitemid 30159486)
40. JG Tjuvajev R Finn K Watanabe R Joshi T Oku J Kennedy B Beattie J Koutcher S Larson RG Blasberg 1996 Noninvasive imaging of herpes virus thymidine kinase gene transfer and expression: a potential method for monitoring clinical gene therapy Cancer Res 56 4087 4095 8797571 1:CAS:528:DyaK28XlslGgsLc%3D (Pubitemid 26304995)
41. R Weissleder A Moore U Mahmood R Bhorade H Benveniste JP Basilion 2000 In vivo magnetic resonance imaging of transgene expression Nat Med 6 351 355 10700241 10.1038/73219 1:CAS:528:DC%2BD3cXhslygs7c%3D (Pubitemid 30148631)
42. A Moore L Josephson RM Bhorade JP Basilion R Weissleder 2001 Human transferrin receptor gene as a marker gene for MR imaging Radiology 221 244 250 11568347 10.1148/radiol.2211001784 1:CAS:528:DC%2BD3MXns1yrtbs%3D (Pubitemid 32880396)
43. JC Wu IY Chen G Sundaresan JJ Min A De JH Qiao MC Fishbein SS Gambhir 2003 Molecular imaging of cardiac cell transplantation in living animals using optical bioluminescence and positron emission tomography Circulation 108 1302 1305 12963637 10.1161/01.CIR.0000091252.20010.6E (Pubitemid 37174406)
44. JK Willmann R Paulmurugan M Rodriguez-Porcel W Stein TJ Brinton AJ Connolly CH Nielsen AM Lutz J Lyons F Ikeno Y Suzuki J Rosenberg IY Chen JC Wu AC Yeung P Yock RC Robbins SS Gambhir 2009 Imaging gene expression in human mesenchymal stem cells: from small to large animals Radiology 252 117 127 19366903 10.1148/radiol.2513081616
45. M Gyongyosi J Blanco T Marian L Tron O Petnehazy Z Petrasi R Hemetsberger J Rodriguez G Font IJ Pavo I Kertesz L Balkay N Pavo A Posa M Emri L Galuska DL Kraitchman J Wojta K Huber D Glogar 2008 Serial noninvasive in vivo positron emission tomographic tracking of percutaneously intramyocardially injected autologous porcine mesenchymal stem cells modified for transgene reporter gene expression Circ Cardiovasc Imaging 1 94 103 19808526 10.1161/CIRCIMAGING.108. 797449
46. M Miyagawa M Beyer B Wagner M Anton C Spitzweg B Gansbacher M Schwaiger FM Bengel 2005 Cardiac reporter gene imaging using the human sodium/iodide symporter gene Cardiovasc Res 65 195 202 15621047 10.1016/j.cardiores.2004.10. 001 1:CAS:528:DC%2BD2cXhtFCqt7bN (Pubitemid 40038492)
47. D Shen D Liu Z Cao P Acton R Zhou 2007 Coregistration of magnetic resonance and single photon emission computed tomography images for noninvasive localization of stem cells grafted in the infarcted rat myocardium Mol Imaging Biol 9 24 31 17053860 10.1007/s11307-006-0062-3 (Pubitemid 46050144)
48. I Chen J Greve O Gheysens J Willmann M Rodriguez-Porcel P Chu A Sheikh A Faranesh R Paulmurugan P Yang J Wu S Gambhir 2009 Comparison of optical bioluminescence reporter gene and superparamagnetic iron oxide MR contrast agent as cell markers for noninvasive imaging of cardiac cell transplantation Mol Imaging Biol 11 178 187 19034584 10.1007/s11307-008-0182-z
49. K Hamano M Nishida K Hirata A Mikamo TS Li M Harada T Miura M Matsuzaki K Esato 2001 Local implantation of autologous bone marrow cells for therapeutic angiogenesis in patients with ischemic heart disease clinical trial and preliminary results Jpn Circ J 65 845 847 11548889 10.1253/jcj.65.845 1:STN:280:DC%2BD3MvpvFOlsQ%3D%3D (Pubitemid 32845720)
50. BE Strauer M Brehm T Zeus M Kostering A Hernandez RV Sorg G Kogler P Wernet 2002 Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans Circulation 106 1913 1918 12370212 10.1161/01.CIR.0000034046.87607.1C (Pubitemid 35176294)
51. Sl Chen Ww Fang F Ye YH Liu J Qian Sj Shan Jj Zhang RZ Chunhua Lm Liao S Lin Jp Sun 2004 Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction Am J Cardiol 94 92 95 15219514 10.1016/j.amjcard. 2004.03.034 (Pubitemid 38813459)
52. S Erbs A Linke V Schachinger B Assmus H Thiele KW Diederich C Hoffmann S Dimmeler T Tonn R Hambrecht AM Zeiher G Schuler 2007 Restoration of microvascular function in the infarct-related artery by intracoronary transplantation of bone marrow progenitor cells in patients with acute myocardial infarction: the Doppler substudy of the reinfusion of enriched progenitor cells and infarct remodeling in acute myocardial infarction (REPAIR-AMI) trial Circulation 116 366 374 17620510 10.1161/CIRCULATIONAHA.106. 671545 (Pubitemid 47196542)
53. A Hirsch R Nijveldt PA van der Vleuten BJ Biemond PA Doevendans AC van Rossum JG Tijssen F Zijlstra JJ Piek 2006 Intracoronary infusion of autologous mononuclear bone marrow cells or peripheral mononuclear blood cells after primary percutaneous coronary intervention: rationale and design of the HEBE trial-a prospective, multicenter, randomized trial Am Heart J 152 434 441 16923409 10.1016/j.ahj.2006.02.007 (Pubitemid 44233416)
54. S Janssens C Dubois J Bogaert K Theunissen C Deroose W Desmet M Kalantzi L Herbots P Sinnaeve J Dens J Maertens F Rademakers S Dymarkowski O Gheysens J Van Cleemput G Bormans J Nuyts A Belmans L Mortelmans M Boogaerts F Van de Werf 2006 Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial Lancet 367 113 121 16413875 10.1016/S0140-6736(05)67861-0 (Pubitemid 43077127)
55. HJ Kang HS Kim SY Zhang KW Park HJ Cho BK Koo YJ Kim DS Lee DW Sohn KS Han BH Oh MM Lee YB Park 2004 Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial Lancet 363 751 756 15016484 10.1016/S0140-6736(04)15689-4 1:CAS:528:DC%2BD2cXhvVOqtro%3D (Pubitemid 38315164)
56. K Lunde S Solheim S Aakhus H Arnesen M Abdelnoor T Egeland K Endresen A Ilebekk A Mangschau JG Fjeld HJ Smith E Taraldsrud HK Grogaard R Bjornerheim M Brekke C Muller E Hopp A Ragnarsson JE Brinchmann K Forfang 2006 Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction N Engl J Med 355 1199 1209 16990383 10.1056/NEJMoa055706 1:CAS:528: DC%2BD28XpvFKgsr0%3D (Pubitemid 44427444)
57. V Schachinger B Assmus MB Britten J Honold R Lehmann C Teupe ND Abolmaali TJ Vogl WK Hofmann H Martin S Dimmeler AM Zeiher 2004 Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI trial J Am Coll Cardiol 44 1690 1699 15489105 10.1016/j.jacc.2004.08.014 (Pubitemid 39369805)
58. BE Strauer M Brehm T Zeus T Bartsch C Schannwell C Antke RV Sorg G Kogler P Wernet HW Mnller M Kostering 2005 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 46 1651 1658 16256864 10.1016/j.jacc.2005.01.069 (Pubitemid 41531618)
59. KC Wollert GP Meyer J Lotz S Ringes Lichtenberg P Lippolt C Breidenbach S Fichtner T Korte B Hornig D Messinger L Arseniev B Hertenstein A Ganser H Drexler 2004 Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial Lancet 364 141 148 15246726 10.1016/S0140-6736(04)16626-9 (Pubitemid 38891685)
60. J Ge Y Li J Qian J Shi Q Wang Y Niu B Fan X Liu S Zhang A Sun Y Zou 2006 Efficacy of emergent transcatheter transplantation of stem cells for treatment of acute myocardial infarction (TCT-STAMI) Heart 92 1764 1767 16775089 10.1136/hrt.2005.085431 1:STN:280:DC%2BD28nmvFSqtg%3D%3D (Pubitemid 44851319)
61. A Schaefer C Zwadlo M Fuchs GP Meyer P Lippolt KC Wollert H Drexler 2010 Long-term effects of intracoronary bone marrow cell transfer on diastolic function in patients after acute myocardial infarction: 5-year results from the randomized-controlled BOOST trial-an echocardiographic study Eur J Echocardiogr 11 165 171 19946118 10.1093/ejechocard/jep191
62. M Yousef CM Schannwell M Kostering T Zeus M Brehm BE Strauer 2009 The BALANCE study: clinical benefit and long-term outcome after intracoronary autologous bone marrow cell transplantation in patients with acute myocardial infarction J Am Coll Cardiol 53 2262 2269 19520249 10.1016/j.jacc.2009.02.051
63. VFM Segers RT Lee 2008 Stem-cell therapy for cardiac disease Nature 451 937 942 18288183 10.1038/nature06800 1:CAS:528:DC%2BD1cXit1ynsbk%3D (Pubitemid 351301749)
64. A Hirsch R Nijveldt PA van der Vleuten RA Tio WJ van der Giessen KMJ Marques PA Doevendans J Waltenberger JM ten Berg WRM Aengevaeren BJ Biemond JG Tijssen AC van Rossum JJ Piek F Zijlstra 2008 Intracoronary infusion of autologous mononuclear bone marrow cells in patients with acute myocardial infarction treated with primary PCI: pilot study of the multicenter HEBE trial Catheter Cardiovasc Interv 71 273 281 18288734 10.1002/ccd.21337 (Pubitemid 351428139)
65. J Meluzin J Mayer L Groch S Janousek I Hornacek O Hlinomaz P Kala R Panovsky J Prasek M Kaminek J Stanicek M Klabusay Z Koristek M Navratil L Dusek J Vinklarkova 2006 Autologous transplantation of mononuclear bone marrow cells in patients with acute myocardial infarction: the effect of the dose of transplanted cells on myocardial function Am Heart J 152 975 17070173 10.1016/j.ahj.2006.08.004 (Pubitemid 44754706)
66. PR Vulliet M Greeley SM Halloran KA MacDonald MD Kittleson 2004 Intra-coronary arterial injection of mesenchymal stromal cells and microinfarction in dogs Lancet 363 783 784 15016490 10.1016/S0140-6736(04)15695- X (Pubitemid 38315169)
67. J Bartunek M Vanderheyden B Vandekerckhove S Mansour B De Bruyne P De Bondt I Van Haute N Lootens G Heyndrickx W Wijns 2005 Intracoronary injection of CD133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: feasibility and safety Circulation 112 I-178
68. P Tossios B Krausgrill M Schmidt T Fischer M Halbach JWU Fries S Fahnenstich P Frommolt I Heppelmann A Schmidt K Schomacker JH Fischer W Bloch U Mehlhorn RHG Schwinger J Muller-Ehmsen 2008 Role of balloon occlusion for mononuclear bone marrow cell deposition after intracoronary injection in pigs with reperfused myocardial infarction Eur Heart J 29 1911 1921 18544545 10.1093/eurheartj/ehn218 1:CAS:528:DC%2BD1cXhtVGmur7L
69. T Freyman G Polin H Osman J Crary M Lu L Cheng M Palasis RL Wilensky 2006 A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction Eur Heart J 27 1114 1122 16510464 10.1093/eurheartj/ehi818
70. MJ Price CC Chou M Frantzen T Miyamoto S Kar S Lee PK Shah BJ Martin M Lill JS Forrester PS Chen RR Makkar 2006 Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties Int J Cardiol 111 231 239 16246440 10.1016/j.ijcard.2005.07.036
71. P Boekstegers W Giehrl Gv Degenfeld G Steinbeck 1998 Selective suction and pressure-regulated retroinfusion: an effective and safe approach to retrograde protection against myocardial ischemia in patients undergoing normal and high risk percutaneous transluminal coronary angioplasty J Am Coll Cardiol 31 1525 1533 9626830 10.1016/S0735-1097(98)00135-1 1:STN:280: DyaK1c3ovVGiuw%3D%3D (Pubitemid 28273294)
72. KH Schuleri LC Amado AJ Boyle M Centola AP Saliaris MR Gutman KE Hatzistergos BN Oskouei JM Zimmet RG Young AW Heldman AC Lardo JM Hare 2008 Early improvement in cardiac tissue perfusion due to mesenchymal stem cells Am J Physiol Heart Circ Physiol 294 H2002 H2011 18310523 10.1152/ajpheart.00762.2007 1:CAS:528:DC%2BD1cXmtVWgtbs%3D
73. HF Tse YL Kwong JK Chan G Lo CL Ho CP Lau 2003 Angiogenesis in ischaemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation Lancet 361 47 49 12517468 10.1016/S0140-6736(03)12111-3 (Pubitemid 36050963)
74. R Kornowski MB Leon S Fuchs Y Vodovotz MA Flynn DA Gordon A Pierre I Kovesdi JA Keiser SE Epstein 2000 Electromagnetic guidance for catheter-based transendocardial injection: a platform for intramyocardial angiogenesis therapy: results in normal and ischemic porcine models J Am Coll Cardiol 35 1031 1039 10732905 10.1016/S0735-1097(99)00642-7 1:STN:280:DC%2BD3c7psFSnsQ%3D%3D (Pubitemid 30189938)
75. DW Losordo PR Vale RC Hendel CE Milliken FD Fortuin N Cummings RA Schatz T Asahara JM Isner RE Kuntz 2002 Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia Circulation 105 2012 2018 11980678 10.1161/01.CIR.0000015982.70785.B7 1:CAS:528:DC%2BD38Xkt1Cht70%3D (Pubitemid 34465261)
76. C Briguori B Reimers C Sarais M Napodano P Pascotto G Azzarello M Bregni A Porcellini O Vinante P Zanco C Peschle G Condorelli A Colombo 2006 Direct intramyocardial percutaneous delivery of autologous bone marrow in patients with refractory myocardial angina Am Heart J 151 674 680 16504630 10.1016/j.ahj.2005.04.033 (Pubitemid 43290259)
77. K Krause K Jaquet C Schneider S Haupt MV Lioznov KM Otte KH Kuck 2009 Percutaneous intramyocardial stem cell injection in patients with acute myocardial infarction: first-in-man study Heart 95 1145 1152 19336430 10.1136/hrt.2008.155077 1:STN:280:DC%2BD1MvltV2lsg%3D%3D
78. N Nyolczas M Gyongyosi G Beran M Dettke S Graf H Sochor G Christ I Edes L Balogh KT Krause K Jaquet KH Kuck I Benedek T Hintea Kiss Rb I Prada V Kotevski H Pejkov D Dudek G Heba C Sylven S Charwat R Jacob G Maurer I Lang D Glogar 2007 Design and rationale for the myocardial stem cell administration after acute myocardial infarction (MYSTAR) study: a multicenter, prospective, randomized, single-blind trial comparing early and late intracoronary or combined (percutaneous intramyocardial and intracoronary) administration of nonselected autologous bone marrow cells to patients after acute myocardial infarction Am Heart J 153 212 17239678 10.1016/j.ahj.2006.10.027 (Pubitemid 46096854)
79. J van Ramshorst JJ Bax SLMA Beeres P bbets-Schneider SD Roes MPM Stokkel A de Roos WE Fibbe JJ Zwaginga E Boersma MJ Schalij DE Atsma 2009 Intramyocardial bone marrow cell injection for chronic myocardial ischemia: a randomized controlled trial JAMA 301 1997 2004 19454638 10.1001/jama.2009.685
80. M Gyongyosi I Lang M Dettke G Beran S Graf H Sochor N Nyolczas S Charwat R Hemetsberger G Christ I Edes L Balogh KT Krause K Jaquet KH Kuck I Benedek T Hintea R Kiss I Preda V Kotevski H Pejkov S Zamini A Khorsand G Sodeck A Kaider G Maurer D Glogar 2009 Combined delivery approach of bone marrow mononuclear stem cells early and late after myocardial infarction: the MYSTAR prospective, randomized study Nat Clin Pract Cardiovasc Med 6 70 81 19002124 10.1038/ncpcardio1388
81. DE Gutstein GE Morley H Tamaddon D Vaidya MD Schneider J Chen KR Chien H Stuhlmann GI Fishman 2001 Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of Connexin43 Circ Res 88 333 339 11179202 1:CAS:528:DC%2BD3MXhtlyktr4%3D (Pubitemid 32173758)
82. RM Klein EG Vester MU Brehm H Dees F Picard D Niederacher MW Beckmann BE Strauer 2000 Inflammation of the myocardium as an arrhythmia trigger Z Kardiol 89 24 35 10810782 10.1007/s003920070080
83. CA Thompson BA Nasseri J Makower S Houser M McGarry T Lamson I Pomerantseva JY Chang HK Gold JP Vacanti SN Oesterle 2003 Percutaneous transvenous cellular cardiomyoplasty: a novel nonsurgical approach for myocardial cell transplantation J Am Coll Cardiol 41 1964 1971 12798567 10.1016/S0735-1097(03)00397-8 (Pubitemid 36677117)
84. SI Yokoyama N Fukuda Y Li K Hagikura T Takayama S Kunimoto J Honye S Saito M Wada A Satomi M Kato H Mugishima Y Kusumi M Mitsumata T Murohara 2006 A strategy of retrograde injection of bone marrow mononuclear cells into the myocardium for the treatment of ischemic heart disease J Mol Cell Cardiol 40 24 34 16271723 10.1016/j.yjmcc.2005.06.008 1:CAS:528:DC%2BD28XkvFCh (Pubitemid 43012114)
85. T Siminiak D Fiszer O Jerzykowska B Grygielska N Rozwadowska P Kalmucki M Kurpisz 2005 Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: the POZNAN trial Eur Heart J 26 1188 1195 15764613 10.1093/eurheartj/ehi159 (Pubitemid 40863125)
86. C Brasselet MC Morichetti E Messas C Carrion A Bissery P Bruneval JT Vilquin A Lafont AA Hagege P Menasche M Desnos 2005 Skeletal myoblast transplantation through a catheter-based coronary sinus approach: an effective means of improving function of infarcted myocardium Eur Heart J 26 1551 1556 15728646 10.1093/eurheartj/ehi151 (Pubitemid 41373498)
87. DM Hou KL March 2003 A novel percutaneous technique for accessing the normal pericardium: a single-center successful experience of 53 porcine procedures J Invasive Cardiol 15 13 17 12499522
88. S Waxman TC Pulerwitz KA Rowe WC Quist RL Verrier 2000 Preclinical safety testing of percutaneous transatrial access to the normal pericardial space for local cardiac drug delivery and diagnostic sampling Catheter Cardiovasc Interv 49 472 477 10751782 10.1002/(SICI)1522-726X(200004)49:4<472::AID-CCD28>3. 0.CO;2-Y 1:STN:280:DC%2BD3c3hslartA%3D%3D (Pubitemid 30183683)
89. MP Macris SR Igo 1999 Minimally invasive access of the normal pericardium: initial clinical experience with a novel device Clin Cardiol 22 36 39 10.1002/clc.4960221310
90. Hagikura K, Fukuda N, Yokoyama SI, Yuxin L, Kusumi Y, Matsumoto T, Ikeda Y, Kunimoto S, Takayama T, Jumabay M, Mitsumata M, Saito S, Hirayama A, Mugishima H (2009) Low invasive angiogenic therapy for myocardial infarction by retrograde transplantation of mononuclear cells expressing the VEGF gene. Int J Cardiol (in press, corrected proof)
91. E Corday S Meerbaum JK Drury 1986 The coronary sinus: an alternate channel for administration of arterial blood and pharmacologic agents for protection and treatment of acute cardiac ischemia J Am Coll Cardiol 7 711 714 3512660 10.1016/S0735-1097(86)80487-9 1:STN:280:DyaL287ktFeiuw%3D%3D (Pubitemid 16164404)
92. NA Herity ST Lo F Oei DP Lee MR Ward SD Filardo A Hassan T Suzuki M Rezaee AJ Carter PG Yock PJ Fitzgerald 2000 Selective regional myocardial infiltration by the percutaneous coronary venous route: a novel technique for local drug delivery Catheter Cardiovasc Interv 51 358 363 11066126 10.1002/1522-726X(200011)51:3<358::AID-CCD27>3.0.CO;2-F 1:STN:280:DC%2BD3M%2Flt1emtA%3D%3D
93. J Vicario J Piva A Pierini HH Ortega A Canal L Gerardo H Pfeiffer C Campos I Fendrich R Novero A Monti 2004 Transcoronary sinus delivery of autologous bone marrow and angiogenesis in pig models with myocardial injury Cardiovasc Radiat Med 3 91 94 10.1016/S1522-1865(03)00002-7
94. J Vicario C Campos J Piva F Faccio L Gerardo C Becker HH Ortega A Pierini C Lofeudo R Novero A Licheri R Milesi N Perez Balino A Monti A Amin H Pfeiffer E De Giovanni I Fendrich 2004 Transcoronary sinus administration of autologous bone marrow in patients with chronic refractory stable angina: phase 1 Cardiovasc Radiat Med 5 71 76 15464943 1:STN:280:DC%2BD2cvpsFGjtA%3D%3D (Pubitemid 39349631)
95. DV Baklanov KM Moodie FE McCarthy E Mandrusov J Chiu G Aswonge J Cheng M Chow M Simons ED de Muinck 2006 Comparison of transendocardial and retrograde coronary venous intramyocardial catheter delivery systems in healthy and infarcted pigs Catheter Cardiovasc Interv 68 416 423 16892441 10.1002/ccd.20841
96. JC George J Goldberg M Joseph N Abdulhameed J Crist H Das VJ Pompili 2009 Transvenous intramyocardial cellular delivery increases retention in comparison to intracoronary delivery in a porcine model of acute myocardial infarction J Interv Cardiol 21 424 431 10.1111/j.1540-8183.2008.00390.x
97. D Blocklet M Toungouz G Berkenboom M Lambermont P Unger N Preumont E Stoupel D Egrise JP Degaute M Goldman S Goldman 2006 Myocardial homing of nonmobilized peripheral-blood CD34 + cells after intracoronary injection Stem Cells 24 333 336 16223854 10.1634/stemcells.2005-0201 (Pubitemid 44464802)
98. WJ Kang HJ Kang HS Kim JK Chung MC Lee DS Lee 2006 Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction J Nucl Med 47 1295 1301 16883008
99. AJ Mitchell E Sabondjian J Sykes L Deans W Zhu X Lu Q Feng FS Prato G Wisenberg 2010 Comparison of initial cell retention and clearance kinetics after subendocardial or subepicardial injections of endothelial progenitor cells in a canine myocardial infarction model J Nucl Med 51 413 417 20150266 10.2967/jnumed.109.069732
100. N Dib A Campbell DB Jacoby A Zawadzka J Ratliff BM Miedzybrocki A Gahremanpour EB Diethrich SR Opie 2007 Safety and feasibility of percutaneous autologous skeletal myoblast transplantation in the coil-infarcted swine myocardium J Pharmacol Toxicol Methods 54 71 77 10.1016/j.vascn.2005.12.002 (Pubitemid 43975018)