MRI-Guided Stem Cell Therapy

  • Tina Ehtiati
  • Dara L. Kraitchman
Part of the Medical Radiology book series (MEDRAD)


In the past several decades, there has been great interest in the transplantation of stem cells to recapitulate organs with limited regenerative capacity. During this same period, the ability to image stem cells by labeling with MRI-visible contrast agents has proved to be an enabling technology for determining the engraftment and fate of these cells. A natural extension of MR-labeling of stem cells is the delivery of stem cells using MR interventional techniques. While the development of these interventional techniques is hindered in part by the need to develop user-friendly imaging interfaces, MR-compatible devices, and advanced physiologic monitoring capabilities, limited clinical trials with MR-labeled stem cells have been performed that suggest MR interventional techniques will offer a safe and more effective method to deliver the stem cell therapies.


Stem Cell Reporter Gene Stem Cell Therapy Chemical Exchange Saturation Transfer Stem Cell Delivery 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Adler ED, Bystrup A, Briley-Saebo KC, Mani V, Young W, Giovanonne S, Altman P, Kattman SJ, Frank JA, Weinmann HJ, Keller GM, Fayad ZA (2009) In vivo detection of embryonic stem cell-derived cardiovascular progenitor cells using Cy3-labeled Gadofluorine M in murine myocardium. JACC Cardiovasc Imaging 2(9):1114–1122PubMedGoogle Scholar
  2. Ahrens ET, Young WB, Xu H, Pusateri LK (2011) Rapid quantification of inflammation in tissue samples using perfluorocarbon emulsion and fluorine-19 nuclear magnetic resonance. Biotechniques 50:229–234PubMedGoogle Scholar
  3. Amsalem Y, Mardor Y, Feinberg MS, Landa N, Miller L, Daniels D, Ocherashvilli A, Holbova R, Yosef O, Barbash IM, Leor J (2007) Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116(Suppl I):I-38–I-45Google Scholar
  4. Arai T, Kofidis T, Bulte JW, De Bruin J, Venook RD, Berry GJ, Mcconnell MV, Quertermous T, Robbins RC, Yang PC (2006) Dual in vivo magnetic resonance evaluation of magnetically labeled mouse embryonic stem cells and cardiac function at 1.5 T. Magn Reson Med 55(1):203–209PubMedGoogle Scholar
  5. Arbab AS, Jordan EK, Wilson LB, Yocum GT, Lewis BK, Frank JA (2004) In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum Gene Ther 15(4):351–360PubMedGoogle Scholar
  6. Arifin DR, Long CM, Gilad AA, Alric C, Roux S, Tillement O, Link TW, Arepally A, Bulte JW (2011) 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 260(3):790–798PubMedGoogle Scholar
  7. Babic M, Horak D, Trchova M, Jendelova P, Glogarova K, Lesny P, Herynek V, Hajek M, Sykova E (2008) Poly(L-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconjug Chem 19(3):740–750PubMedGoogle Scholar
  8. Barnett BP, Arepally A, Karmarkar PV, Qian D, Gilson WD, Walczak P, Howland V, Lawler L, Lauzon C, Stuber M, Kraitchman DL, Bulte JW (2007) Magnetic resonance-guided, real-time targeted delivery and imaging of magnetocapsules immunoprotecting pancreatic islet cells. Nat Med 13(8):986–991PubMedGoogle Scholar
  9. Barnett BP, Ruiz-Cabello J, Hota P, Liddell R, Walczak P, Howland V, Chacko VP, Kraitchman DL, Arepally A, Bulte JW (2010) Fluorocapsules for improved function, immunoprotection, and visualization of cellular therapeutics with MR, US, and CT imaging. Radiology 258(1):182–191PubMedGoogle Scholar
  10. Barnett BP, Arepally A, Stuber M, Arifin DR, Kraitchman DL, Bulte JW (2011a) Synthesis of magnetic resonance-, X-ray- and ultrasound-visible alginate microcapsules for immunoisolation and noninvasive imaging of cellular therapeutics. Nat Protoc 6(8):1142–1151PubMedGoogle Scholar
  11. Barnett BP, Ruiz-Cabello J, Hota P, Ouwerkerk R, Shamblott MJ, Lauzon C, Walczak P, Gilson WD, Chacko VP, Kraitchman DL, Arepally A, Bulte JW (2011b) Use of perfluorocarbon nanoparticles for non-invasive multimodal cell tracking of human pancreatic islets. Contrast Media Mol Imaging 6(4):251–259PubMedGoogle Scholar
  12. Berman SC, Galpoththawela C, Gilad AA, Bulte JW, Walczak P (2011) Long-term MR cell tracking of neural stem cells grafted in immunocompetent versus immunodeficient mice reveals distinct differences in contrast between live and dead cells. Magn Reson Med 65:564–574PubMedGoogle Scholar
  13. Bible E, Chau DY, Alexander MR, Price J, Shakesheff KM, Modo M (2009) The support of neural stem cells transplanted into stroke-induced brain cavities by PLGA particles. Biomaterials 30(16):2985–2994PubMedGoogle Scholar
  14. Bock M, Volz S, Zuhlsdorff S, Umathum R, Fink C, Hallscheidt P, Semmler W (2004) MR-guided intravascular procedures: real-time parameter control and automated slice positioning with active tracking coils. J Magn Reson Imaging 19(5):580–589PubMedGoogle Scholar
  15. Bos C, Delmas Y, Desmouliere A, Solanilla A, Hauger O, Grosset C, Dubus I, Ivanovic Z, Rosenbaum J, Charbord P, Combe C, Bulte JW, Moonen CT, Ripoche J, Grenier N (2004) In vivo MR imaging of intravascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver. Radiology 233(3):781–789PubMedGoogle Scholar
  16. Bulte JW, Kraitchman DL (2004) Monitoring cell therapy using iron oxide MR contrast agents. Curr Pharm Biotechnol 5(6):567–584PubMedGoogle Scholar
  17. Burgess A, Ayala-Grosso CA, Ganguly M, Jordao JF, Aubert I, Hynynen K (2011) Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS ONE 6(11):e27877PubMedGoogle Scholar
  18. Cahill KS, Gaidosh G, Huard J, Silver X, Byrne BJ, Walter GA (2004) Noninvasive monitoring and tracking of muscle stem cell transplants. Transplantation 78(11):1626–1633PubMedGoogle Scholar
  19. Callera F, De Melo CM (2007) 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 16(3):461–466PubMedGoogle Scholar
  20. Chen AP, Hurd RE, Gu YP, Wilson DM, Cunningham CH (2011) (13)C MR reporter probe system using dynamic nuclear polarization. NMR Biomed 24(5):514–520PubMedGoogle Scholar
  21. Cohen B, Dafni H, Meir G, Harmelin A, Neeman M (2005) Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 7(2):109–117PubMedGoogle Scholar
  22. Corti R, Badimon J, Mizsei G, Macaluso F, Lee M, Licato P, Viles-Gonzalez JF, Fuster V, Sherman W (2005) Real time magnetic resonance guided endomyocardial local delivery. Heart 91(3):348–353PubMedGoogle Scholar
  23. Cunningham CH, Arai T, Yang PC, Mcconnell MV, Pauly JM, Conolly SM (2005) Positive contrast magnetic resonance imaging of cells labeled with magnetic nanoparticles. Magn Reson Med 53(5):999–1005PubMedGoogle Scholar
  24. Dahnke H, Liu W, Herzka D, Frank JA, Schaeffter T (2008) Susceptibility gradient mapping (SGM): a new postprocessing method for positive contrast generation applied to superparamagnetic iron oxide particle (SPIO)-labeled cells. Magn Reson Med 60(3):595–603PubMedGoogle Scholar
  25. De Silva R, Gutierrez LF, Raval AN, McVeigh ER, Ozturk C, Lederman RJ (2006) X-Ray fused with magnetic resonance imaging (XFM) to target endomyocardial injections. Validation in a swine model of myocardial infarction. Circulation 114(22):2342–2350PubMedGoogle Scholar
  26. De Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, Van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, Bulte JW, Scheenen TW, Punt CJ, Heerschap A, Figdor CG (2005) Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 23(11):1407–1413PubMedGoogle Scholar
  27. Dick AJ, Guttman MA, Raman VK, Peters DC, Pessanha BS, Hill JM, Smith S, Scott G, McVeigh ER, Lederman RJ (2003) Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in swine. Circulation 108(23):2899–2904PubMedGoogle Scholar
  28. Duckett SG, Ginks M, Shetty AK, Knowles BR, Totman JJ, Chiribiri A, Ma YL, Razavi R, Schaeffter T, Carr-White G, Rhode K, Rinaldi CA (2011) 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 13(2):285–286PubMedGoogle Scholar
  29. Dumoulin CL, Mallozzi RP, Darrow RD, Schmidt EJ (2010) Phase-field dithering for active catheter tracking. Magn Reson Med 63(5):1398–1403PubMedGoogle Scholar
  30. Dunning MD, Lakatos A, Loizou L, Kettunen M, Ffrench-Constant C, Brindle KM, Franklin RJ (2004) Superparamagnetic iron oxide-labeled Schwann cells and olfactory ensheathing cells can be traced in vivo by magnetic resonance imaging and retain functional properties after transplantation into the CNS. J Neurosci 24(44):9799–9810PubMedGoogle Scholar
  31. Ebert SN, Taylor DG, Nguyen HL, Kodack DP, Beyers RJ, Xu Y, Yang Z, French BA (2007) Noninvasive tracking of cardiac embryonic stem cells in vivo using magnetic resonance imaging techniques. Stem Cells 25(11):2936–2944PubMedGoogle Scholar
  32. Engberink RD, Van Der Pol SM, Walczak P, Van Der Toorn A, Viergever MA, Dijkstra CD, Bulte JW, De Vries HE, Blezer EL (2010) Magnetic resonance imaging of monocytes labeled with ultrasmall superparamagnetic particles of iron oxide using magnetoelectroporation in an animal model of multiple sclerosis. Mol Imaging 9(5):268–277PubMedGoogle Scholar
  33. Farrar CT, Dai G, Novikov M, Rosenzweig A, Weissleder R, Rosen BR, Sosnovik DE (2008) Impact of field strength and iron oxide nanoparticle concentration on the linearity and diagnostic accuracy of off-resonance imaging. NMR Biomed 21(5):453–463PubMedGoogle Scholar
  34. Frank JA, Zywicke H, Jordan EK, Mitchell J, Lewis BK, Bryant LH Jr, Bulte JWM (2002) Magnetic intracellular labeling of mammalian cells by combining (FDA-approved) superparamagnetic iron oxide MR contrast agents and commonly used transfection agents. Acad Radiol 9:S484–S487PubMedGoogle Scholar
  35. Fu Y, Azene N, Xu Y, Kraitchman DL (2011) Tracking stem cells for cardiovascular applications in vivo: focus on imaging techniques. Imaging Med 3(4):473–486PubMedGoogle Scholar
  36. Garot J, Unterseeh T, Teiger E, Champagne S, Chazaud B, Gherardi R, Hittinger L, Gueret P, Rahmouni A, Sonnet C, Le Corvoisier P, Benhaiem-Sigaux N, Su J, Merlet P (2003) Magnetic resonance imaging of targeted catheter-based implantation of myogenic precursor cells into infarcted left ventricular myocardium. J Am Coll Cardiol 41(10):1841–1846PubMedGoogle Scholar
  37. Gilad AA, Mcmahon MT, Walczak P, Winnard PT Jr, Raman V, Van Laarhoven HW, Skoglund CM, Bulte JW, Van Zijl PC (2007a) Artificial reporter gene providing MRI contrast based on proton exchange. Nat Biotechnol 25(2):217–219PubMedGoogle Scholar
  38. Gilad AA, Winnard PT Jr, Van Zijl PC, Bulte JW (2007b) Developing MR reporter genes: promises and pitfalls. NMR Biomed 20(3):275–290PubMedGoogle Scholar
  39. Gilad AA, Walczak P, Mcmahon MT, Na HB, Lee JH, An K, Hyeon T, Van Zijl PC, Bulte JW (2008) MR tracking of transplanted cells with “positive contrast” using manganese oxide nanoparticles. Magn Reson Med 60(1):1–7PubMedGoogle Scholar
  40. Girard OM, Du J, Agemy L, Sugahara KN, Kotamraju VR, Ruoslahti E, Bydder GM, Mattrey RF (2011) Optimization of iron oxide nanoparticle detection using ultrashort echo time pulse sequences: comparison of T1, T2*, and synergistic T1-T2* contrast mechanisms. Magn Reson Med 65(6):1649–1660PubMedGoogle Scholar
  41. Glud AN, Hedegaard C, Nielsen MS, Soorensen JC, Bendixen C, Jensen PH, Mogensen PH, Larsen K, Bjarkam CR (2011) Direct MRI-guided stereotaxic viral mediated gene transfer of alpha-synuclein in the Gottingen minipig CNS. Acta Neurobiol Exp (Wars) 71(4):508–518Google Scholar
  42. Golovko DM, Henning T, Bauer JS, Settles M, Frenzel T, Mayerhofer A, Rummeny EJ, Daldrup-Link HE (2010) Accelerated stem cell labeling with ferucarbotran and protamine. Eur Radiol 20(3):640–648PubMedGoogle Scholar
  43. Gutierrez LF, Schechter G, Lederman RJ, McVeigh ER, Ozturk C (2005) Distortion correction, calibration and registration: toward and integrated MR and X-ray interventional suite. Proc SPIE 5744:146–156Google Scholar
  44. Guttman MA, Lederman RJ, Sorger JM, McVeigh ER (2002) Real-time volume rendered MRI for interventional guidance. J Cardiovasc Magn Reson 4(4):431–442PubMedGoogle Scholar
  45. Guttman MA, Ozturk C, Raval AN, Raman VK, Dick AJ, Desilva R, Karmarkar P, Lederman RJ, McVeigh ER (2007) Interventional cardiovascular procedures guided by real-time MR imaging: an interactive interface using multiple slices, adaptive projection modes and live 3D renderings. J Magn Reson Imaging 26(6):1429–1435PubMedGoogle Scholar
  46. Guzman R, Uchida N, Bliss TM, He D, Christopherson KK, Stellwagen D, Capela A, Greve J, Malenka RC, Moseley ME, Palmer TD, Steinberg GK (2007) Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci U S A 104(24):10211–10216PubMedGoogle Scholar
  47. He G, Zhang H, Wei H, Wang Y, Zhang X, Tang Y, Wei Y, Hu S (2007) In vivo imaging of bone marrow mesenchymal stem cells transplanted into myocardium using magnetic resonance imaging: a novel method to trace the transplanted cells. Int J Cardiol 114(1):4–10PubMedGoogle Scholar
  48. Higuchi T, Anton M, Dumler K, Seidl S, Pelisek J, Saraste A, Welling A, Hofmann F, Oostendorp RA, Gansbacher B, Nekolla SG, Bengel FM, Botnar RM, Schwaiger M (2009) Combined reporter gene PET and iron oxide MRI for monitoring survival and localization of transplanted cells in the rat heart. J Nucl Med 50(7):1088–1094PubMedGoogle Scholar
  49. Hill JM, Dick AJ, Raman VK, Thompson RB, Yu ZX, Hinds KA, Pessanha BS, Guttman MA, Varney TR, Martin BJ, Dunbar CE, McVeigh ER, Lederman RJ (2003) Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 108(8):1009–1014PubMedGoogle Scholar
  50. Hoehn M, Kustermann E, Blunk J, Wiedermann D, Trapp T, Wecker S, Focking M, Arnold H, Hescheler J, Fleischmann BK, Schwindt W, Buhrle C (2002) Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A 99(25):16267–16272PubMedGoogle Scholar
  51. Jendelova P, Herynek V, Urdzikova L, Glogarova K, Kroupova J, Andersson B, Bryja V, Burian M, Hajek M, Sykova E (2004) Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 76(2):232–243PubMedGoogle Scholar
  52. Jiang Q, Zhang ZG, Ding GL, Zhang L, Ewing JR, Wang L, Zhang R, Li L, Lu M, Meng H, Arbab AS, Hu J, Li QJ, Pourabdollah Nejad DS, Athiraman H, Chopp M (2005) Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage 28(3):698–707PubMedGoogle Scholar
  53. Karmarkar PV, Kraitchman DL, Izbudak I, Hofmann LV, Amado LC, Fritzges D, Young R, Pittenger M, Bulte JW, Atalar E (2004) MR-trackable intramyocardial injection catheter. Mag Reson Med 51(6):1163–1172Google Scholar
  54. 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 (2010) Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 67(10):1187–1194PubMedGoogle Scholar
  55. Kedziorek DA, Kraitchman DL (2010) Superparamagnetic iron oxide labeling of stem cells for MRI tracking and delivery in cardiovascular disease. Methods Mol Biol 660:171–183PubMedGoogle Scholar
  56. Kim D, Chun BG, Kim YK, Lee YH, Park CS, Jeon I, Cheong C, Hwang TS, Chung H, Gwag BJ, Hong KS, Song J (2008) In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant 16(10):1007–1012PubMedGoogle Scholar
  57. Kim J, Arifin DR, Muja N, Kim T, Gilad AA, Kim H, Arepally A, Hyeon T, Bulte JW (2011) Multifunctional capsule-in-capsules for immunoprotection and trimodal imaging. Angew Chem Int Ed Engl 50(10):2317–2321PubMedGoogle Scholar
  58. Kraitchman DL, Bulte JW (2008) Imaging of stem cells using MRI. Basic Res Cardiol 103(2):105–113PubMedGoogle Scholar
  59. Kraitchman DL, Gilson WD, Lorenz CH (2008) Stem cell therapy: MRI guidance and monitoring. J Magn Reson Imaging 27(2):299–310PubMedGoogle Scholar
  60. Kraitchman DL, Heldman AW, Atalar E, Amado LC, Martin BJ, Pittenger MF, Hare JM, Bulte JW (2003) In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 107(18):2290–2293PubMedGoogle Scholar
  61. Larson PS, Starr PA, Bates G, Tansey L, Richardson RM, Martin AJ (2012) An optimized system for interventional magnetic resonance imaging-guided stereotactic surgery: preliminary evaluation of targeting accuracy. Neurosurgery 70 Operative Neurosurgery 1:ons95–ons103Google Scholar
  62. Lee ES, Chan J, Shuter B, Tan LG, Chong MS, Ramachandra DL, Dawe GS, Ding J, Teoh SH, Beuf O, Briguet A, Tam KC, Choolani M, Wang SC (2009) Microgel iron oxide nanoparticles for tracking human fetal mesenchymal stem cells through magnetic resonance imaging. Stem Cells 27(8):1921–1931PubMedGoogle Scholar
  63. Leung DA, Debatin JF, Wildermuth S, Mckinnon GC, Holtz D, Dumoulin CL, Darrow RD, Hofmann E, Von Schulthess GK (1995) Intravascular MR tracking catheter: preliminary experimental evaluation. AJR Am J Roentgenol 164(5):1265–1270PubMedGoogle Scholar
  64. Li Z, Suzuki Y, Huang M, Cao F, Xie X, Connolly AJ, Yang PC, Wu JC (2008) 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 26(4):864–873PubMedGoogle Scholar
  65. Lim F, Sun AM (1980) Microencapsulated islets as bioartificial endocrine pancreas. Science 210(4472):908–910PubMedGoogle Scholar
  66. Link TW, Woodrum D, Gilson WD, Pan L, Qian D, Kraitchman DL, Bulte JW, Arepally A, Weiss CR (2011) MR-guided portal vein delivery and monitoring of magnetocapsules: assessment of physiologic effects on the liver. J Vasc Interv Radiol 22(9):1335–1340PubMedGoogle Scholar
  67. Mani V, Adler E, Briley-Saebo KC, Bystrup A, Fuster V, Keller G, Fayad ZA (2008) 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 60(1):73–81PubMedGoogle Scholar
  68. Mani V, Briley-Saebo KC, Hyafil F, Itskovich V, Fayad ZA (2006a) 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 8(1):49–50Google Scholar
  69. Mani V, Saebo KC, Itskovich V, Samber DD, Fayad ZA (2006b) GRadient echo acquisition for superparamagnetic particles with positive contrast (GRASP): sequence characterization in membrane and glass superparamagnetic iron oxide phantoms at 1.5 T and 3 T. Magn Reson Med 55:126–135PubMedGoogle Scholar
  70. Martin AJ, Larson PS, Ostrem JL, Starr PA (2009) Interventional magnetic resonance guidance of deep brain stimulator implantation for Parkinson disease. Top Magn Reson Imaging 19(4):213–221PubMedGoogle Scholar
  71. Mcmahon MT, Gilad AA, Deliso MA, Berman SM, Bulte JW, Van Zijl PC (2008) New “multicolor” polypeptide diamagnetic chemical exchange saturation transfer (DIACEST) contrast agents for MRI. Magn Reson Med 60(4):803–812PubMedGoogle Scholar
  72. Mills PH, Hitchens TK, Foley LM, Link T, Ye Q, Weiss CR, Thompson JD, Gilson WD, Arepally A, Melick JA, Kochanek PM, Ho C, Bulte JW, Ahrens ET (2012) Automated detection and characterization of SPIO-labeled cells and capsules using magnetic field perturbations. Magn Reson Med 67(1):278–289PubMedGoogle Scholar
  73. Mintorovitch J, Shamsi K (2000) Eovist injection and resovist injection: two new liver-specific contrast agents for MRI. Oncology (Williston Park) 14(6 Suppl 3):37–40Google Scholar
  74. Misselwitz B, Platzek J, Weinmann HJ (2004) Early MR lymphography with gadofluorine M in rabbits. Radiology 231(3):682–688PubMedGoogle Scholar
  75. Modo M, Beech JS, Meade TJ, Williams SC, Price J (2009) A chronic 1 year assessment of MRI contrast agent-labelled neural stem cell transplants in stroke. Neuroimage 47(Suppl 2):T133–T142PubMedGoogle Scholar
  76. Modo M, Mellodew K, Cash D, Fraser SE, Meade TJ, Price J, Williams SC (2004) Mapping transplanted stem cell migration after a stroke: a serial, in vivo magnetic resonance imaging study. Neuroimage 21(1):311–317PubMedGoogle Scholar
  77. Muja N, Cohen ME, Zhang J, Kim H, Gilad AA, Walczak P, Ben-Hur T, Bulte JW (2011) Neural precursors exhibit distinctly different patterns of cell migration upon transplantation during either the acute or chronic phase of EAE: a serial MR imaging study. Magn Reson Med 65(6):1738–1749PubMedGoogle Scholar
  78. Nazarian S, Kolandaivelu A, Zviman MM, Meininger GR, Kato R, Susil RC, Roguin A, Dickfeld TL, Ashikaga H, Calkins H, Berger RD, Bluemke DA, Lardo AC, Halperin HR (2008) Feasibility of real-time magnetic resonance imaging for catheter guidance in electrophysiology studies. Circulation 118(3):223–229PubMedGoogle Scholar
  79. Nolte IS, Gungor S, Erber R, Plaxina E, Scharf J, Misselwitz B, Gerigk L, Przybilla H, Groden C, Brockmann MA (2008) In vitro labeling of glioma cells with gadofluorine M enhances T1 visibility without affecting glioma cell growth or motility. Magn Reson Med 59(5):1014–1020PubMedGoogle Scholar
  80. Ocali O, Atalar E (1997) Intravascular magnetic resonance imaging using a loopless catheter antenna. Magn Reson Med 37(1):112–118PubMedGoogle Scholar
  81. Partlow KC, Chen J, Brant JA, Neubauer AM, Meyerrose TE, Creer MH, Nolta JA, Caruthers SD, Lanza GM, Wickline SA (2007) 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J 21(8):1647–1654PubMedGoogle Scholar
  82. Politi LS, Bacigaluppi M, Brambilla E, Cadioli M, Falini A, Comi G, Scotti G, Martino G, Pluchino S (2007) Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells 25(10):2583–2592PubMedGoogle Scholar
  83. Richardson RM, Kells AP, Rosenbluth KH, Salegio EA, Fiandaca MS, Larson PS, Starr PA, Martin AJ, Lonser RR, Federoff HJ, Forsayeth JR, Bankiewicz KS (2011) Interventional MRI-guided putaminal delivery of AAV2-GDNF for a planned clinical trial in Parkinson’s disease. Mol Ther 19(6):1048–1057PubMedGoogle Scholar
  84. Ruiz-Cabello J, Walczak P, Kedziorek DA, Chacko VP, Schmieder AH, Wickline SA, Lanza GM, Bulte JW (2008) In vivo “hot spot” MR imaging of neural stem cells using fluorinated nanoparticles. Magn Reson Med 60(6):1506–1511PubMedGoogle Scholar
  85. Runge VM, Ai T, Hao D, Hu X (2011) The developmental history of the gadolinium chelates as intravenous contrast media for magnetic resonance. Invest Radiol 46(12):807–816PubMedGoogle Scholar
  86. Saeed M, Lee R, Martin A, Weber O, Krombach GA, Schalla S, Lee M, Saloner D, Higgins CB (2004) Transendocardial delivery of extracellular myocardial markers by using combination X-ray/MR fluoroscopic guidance: feasibility study in dogs. Radiology 231(3):689–696PubMedGoogle Scholar
  87. Schmidt PP, Toft KG, Skotland T, Andersson K (2002) Stability and transmetallation of the magnetic resonance contrast agent MnDPDP measured by EPR. J Biol Inorg Chem 7(3):241–248PubMedGoogle Scholar
  88. Shapiro EM, Koretsky AP (2008) Convertible manganese contrast for molecular and cellular MRI. Magn Reson Med 60(2):265–269PubMedGoogle Scholar
  89. Sponarova D, Horak D, Trchova M, Jendelova P, Herynek V, Mitina N, Zaichenko A, Stoika R, Lesny P, Sykova E (2011) The use of oligoperoxide-coated magnetic nanoparticles to label stem cells. J Biomed Nanotechnol 7(3):384–394PubMedGoogle Scholar
  90. Starr PA, Martin AJ, Larson PS (2009) Implantation of deep brain stimulator electrodes using interventional MRI. Neurosurg Clin N Am 20(2):193–203PubMedGoogle Scholar
  91. Stuber M, Gilson WD, Schar M, Kedziorek DA, Hofmann LV, Shah S, Vonken EJ, Bulte JW, Kraitchman DL (2007) Positive contrast visualization of iron oxide-labeled stem cells using inversion-recovery with ON-resonant water suppression (IRON). Magn Reson Med 58(5):1072–1077PubMedGoogle Scholar
  92. Stuckey DJ, Carr CA, Martin-Rendon E, Tyler DJ, Willmott C, Cassidy PJ, Hale SJ, Schneider JE, Tatton L, Harding SE, Radda GK, Watt S, Clarke K (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(8):1968–1975PubMedGoogle Scholar
  93. Sumner JP, Shapiro EM, Maric D, Conroy R, Koretsky AP (2009) In vivo labeling of adult neural progenitors for MRI with micron sized particles of iron oxide: quantification of labeled cell phenotype. Neuroimage 44(3):671–678PubMedGoogle Scholar
  94. Sykova E, Jendelova P (2005) Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann N Y Acad Sci 1049:146–160PubMedGoogle Scholar
  95. Sykova E, Jendelova P (2006) Magnetic resonance tracking of transplanted stem cells in rat brain and spinal cord. Neurodegener Dis 3(1–2):62–67PubMedGoogle Scholar
  96. Tallheden T, Nannmark U, Lorentzon M, Rakotonirainy O, Soussi B, Waagstein F, Jeppsson A, Sjogren-Jansson E, Lindahl A, Omerovic E (2006) In vivo MR imaging of magnetically labeled human embryonic stem cells. Life Sci 79(10):999–1006PubMedGoogle Scholar
  97. Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, Schar M, Gerstenblith G, Weiss RG, Marban E, Abraham MR (2008) Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 117(12):1555–1562PubMedGoogle Scholar
  98. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147PubMedGoogle Scholar
  99. Toft KG, Hustvedt SO, Grant D, Martinsen I, Gordon PB, Friisk GA, Korsmo AJ, Skotland T (1997) Metabolism and pharmacokinetics of MnDPDP in man. Acta Radiol 38(4 Pt 2):677–689PubMedGoogle Scholar
  100. Tomkowiak MT, Klein AJ, Vigen KK, Hacker TA, Speidel MA, Vanlysel MS, Raval AN (2011) Targeted transendocardial therapeutic delivery guided by MRI-X-ray image fusion. Catheter Cardiovasc Interv 78(3):468–478PubMedGoogle Scholar
  101. 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 (2008) Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant 8(3):701–706PubMedGoogle Scholar
  102. Tseng CL, Shih IL, Stobinski L, Lin FH (2010) Gadolinium hexanedione nanoparticles for stem cell labeling and tracking via magnetic resonance imaging. Biomaterials 31(20):5427–5435PubMedGoogle Scholar
  103. Tzifa A, Krombach GA, Kramer N, Kruger S, Schutte A, Von Walter M, Schaeffter T, Qureshi S, Krasemann T, Rosenthal E, Schwartz CA, Varma G, Buhl A, Kohlmeier A, Bucker A, Gunther RW, Razavi R (2010) Magnetic resonance-guided cardiac interventions using magnetic resonance-compatible devices: a preclinical study and first-in-man congenital interventions. Circ Cardiovasc Interv 3(6):585–592PubMedGoogle Scholar
  104. Vuu K, Xie J, Mcdonald MA, Bernardo M, Hunter F, Zhang Y, Li K, Bednarski M, Guccione S (2005) Gadolinium-rhodamine nanoparticles for cell labeling and tracking via magnetic resonance and optical imaging. Bioconjug Chem 16(4):995–999PubMedGoogle Scholar
  105. Wacker FK, Elgort D, Hillenbrand CM, Duerk JL, Lewin JS (2004) The catheter-driven MRI scanner: a new approach to intravascular catheter tracking and imaging-parameter adjustment for interventional MRI. AJR Am J Roentgenol 183(2):391–395PubMedGoogle Scholar
  106. Walczak P, Kedziorek DA, Gilad AA, Lin S, Bulte JW (2005) Instant MR labeling of stem cells using magnetoelectroporation. Magn Reson Med 54(4):769–774PubMedGoogle Scholar
  107. Walczak P, Ruiz-Cabello J, Kedziorek DA, Gilad AA, Lin S, Barnett B, Qin L, Levitsky H, Bulte JW (2006) Magnetoelectroporation: improved labeling of neural stem cells and leukocytes for cellular magnetic resonance imaging using a single FDA-approved agent. Nanomedicine 2(2):89–94PubMedGoogle Scholar
  108. Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG, Pittenger MF, Van Zijl PC, Huang J, Bulte JW (2008) Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 39(5):1569–1574PubMedGoogle Scholar
  109. Weissleder R, Moore A, Mahmood U, Bhorade R, Benveniste H, Chiocca EA, Basilion JP (2000) In vivo magnetic resonance imaging of transgene expression. Nat Med 6(3):351–355PubMedGoogle Scholar
  110. Xie TD, Sun L, Tsong TY (1990) Study of mechanisms of electric field-induced DNA transfection. I. DNA entry by surface binding and diffusion through membrane pores. Biophys J 58(1):13–19PubMedGoogle Scholar
  111. Yamada M, Gurney PT, Chung J, Kundu P, Drukker M, Smith AK, Weissman IL, Nishimura D, Robbins RC, Yang PC (2009) Manganese-guided cellular MRI of human embryonic stem cell and human bone marrow stromal cell viability. Magn Reson Med 62(4):1047–1054PubMedGoogle Scholar
  112. Yang L, Xia Y, Zhao H, Zhao J, Zhu X (2006) Magnetic resonance imaging of transplanted neural stem cells in Parkinson disease rats. J Huazhong Univ Sci Technol Med Sci 26(4):489–492PubMedGoogle Scholar
  113. Ye Q, Wu YL, Foley LM, Hitchens TK, Eytan DF, Shirwan H, Ho C (2008) Longitudinal tracking of recipient macrophages in a rat chronic cardiac allograft rejection model with noninvasive magnetic resonance imaging using micrometer-sized paramagnetic iron oxide particles. Circulation 118(2):149–156PubMedGoogle Scholar
  114. Yeh TC, Zhang W, Ildstad ST, Ho C (1995) In vivo dynamic MRI tracking of rat T-cells labeled with superparamagnetic iron-oxide particles. Magn Reson Med 33(2):200–208PubMedGoogle Scholar
  115. Yu J-X, Kodibagkar VD, Hallac RR, Liu L, Mason RP (2012) Dual 19F/1H MR gene reporter molecules for in vivo detection of β-galactosidase. Bioconjugate Chem 23(3):596–603Google Scholar
  116. Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE (2001) Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 33(5):907–921PubMedGoogle Scholar
  117. Zhang ZG, Jiang Q, Zhang R, Zhang L, Wang L, Arniego P, Ho KL, Chopp M (2003) Magnetic resonance imaging and neurosphere therapy of stroke in rat. Ann Neurol 53(2):259–263PubMedGoogle Scholar
  118. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5):381–384PubMedGoogle Scholar
  119. Zhou R, Idiyatullin D, Moeller S, Corum C, Zhang H, Qiao H, Zhong J, Garwood M (2010) SWIFT detection of SPIO-labeled stem cells grafted in the myocardium. Magn Reson Med 63(5):1154–1161PubMedGoogle Scholar
  120. Zhu J, Zhou L, Xingwu F (2006) Tracking neural stem cells in patients with brain trauma. N Engl J Med 355(22):2376–2378PubMedGoogle Scholar
  121. Zuehlsdorff S, Umathum R, Volz S, Hallscheidt P, Fink C, Semmler W, Bock M (2004) MR coil design for simultaneous tip tracking and curvature delineation of a catheter. Magn Reson Med 52(1):214–218PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Siemens Corporate ResearchCenter for Applied Medical ImagingBaltimoreUSA
  2. 2.Russell H. Morgan Department of Radiology and Radiological Science, Department of Molecular and Comparative PathobiologyJohns Hopkins UniversityBaltimoreUSA

Personalised recommendations