Iron administration before stem cell harvest enables MR imaging tracking after transplantation

Radiology

Volumn 269, Issue 1, 2013, Pages 186-197

  Khurana, Aman ^a   Chapelin, Fanny ^a   Beck, Graham ^a   Lenkov, Olga D ^a   Donig, Jessica ^a   Nejadnik, Hossein ^a   Messing, Solomon ^b   Derugin, Nikita ^d   Chan, Ray Chun Fai ^e   Gaur, Amitabh ^e   Sennino, Barbara ^d   McDonald, Donald M ^d   Kempen, Paul J ^c   Tikhomirov, Grigory A ^a   Rao, Jianghong ^a   Daldrup Link, Heike E ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Stanford University   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Custom Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERUMOXYTOL; IRON OXIDE; NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL LABELING; CELL TRACKING; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EX VIVO STUDY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; IRON TRANSPORT; LYSOSOME; MACROPHAGE; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; STEM CELL TRANSPLANTATION;

ANIMALS; CELL SEPARATION; CELL TRACKING; CELLS, CULTURED; CONTRAST MEDIA; FERUMOXYTOL; MAGNETIC RESONANCE IMAGING; RATS; RATS, SPRAGUE-DAWLEY; STAINING AND LABELING; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84884681760     PISSN: 00338419     EISSN: 15271315     Source Type: Journal    
DOI: 10.1148/radiol.13130858     Document Type: Article

References (92)

1. Total number of discharges for knee arthoplastly in 2010 in US. http://hcupnet.ahrq.gov/HCUPnet.jsp. Published 2010. Accessed October 16, 2012.
2. Brooks PM. Impact of osteoarthritis on individuals and society: how much disability? social consequences and health economic implications. Curr Opin Rheumatol 2002;14(5):573-577. (Pubitemid 34953798)
3. Gupta S, Hawker GA, Laporte A, Croxford R, Coyte PC. The economic burden of disabling hip and knee osteoarthritis (OA) from the perspective of individuals living with this condition. Rheumatology (Oxford) 2005;44(12):1531-1537. (Pubitemid 41742470)
4. Kurtz S, Ong K, Lau E, Mowat F, Halpern M. Projections of primary and revision hip and knee arthroplasty in the United States from 2005 to 2030. J Bone Joint Surg Am 2007;89(4):780-785. (Pubitemid 46564282)
5. Basko-Plluska JL, Thyssen JP, Schalock PC. Cutaneous and systemic hypersensitivity reactions to metallic implants. Dermatitis 2011;22(2):65-79.
6. Gittens RA, Olivares-Navarrete R, Tannenbaum R, Boyan BD, Schwartz Z. Electrical implications of corrosion for osseointegration of titanium implants. J Dent Res 2011;90(12):1389-1397.
7. Daniel J, Ziaee H, Kamali A, Pradhan C, Band T, McMinn DJ. Ten-year results of a double-heat-treated metal-on-metal hip resurfacing. J Bone Joint Surg Br 2010;92(1):20-27.
8. Fary C, Thomas GE, Taylor A, Beard D, Carr A, Glyn-Jones S. Diagnosing and investigating adverse reactions in metal on metal hip implants. BMJ 2011;343:d7441.
9. Murray DW, Grammatopoulos G, Pandit H, Gundle R, Gill HS, McLardy-Smith P. The ten-year survival of the Birmingham hip resurfacing: an independent series. J Bone Joint Surg Br 2012;94(9):1180-1186.
10. Roemer FW, Crema MD, Trattnig S, Guermazi A. Advances in imaging of osteoarthritis and cartilage. Radiology 2011;260(2):332-354.
11. Berner A, Siebenlist S, Reichert JC, Hendrich C, Nöth U. Reconstruction of osteochondral defects with a stem cell-based cartilage-polymer construct in a small animal model [in German]. Z Orthop Unfall 2010;148(1):31-38.
12. Henning TD, Gawande R, Khurana A, et al. Magnetic resonance imaging of ferumoxide-labeled mesenchymal stem cells in cartilage defects: in vitro and in vivo investigations. Mol Imaging 2012;11(3):197-209.
13. Khurana A, Nejadnik H, Gawande R, et al. Intravenous ferumoxytol allows noninvasive MR imaging monitoring of macrophage migration into stem cell transplants. Radiology 2012;264(3):803-811.
14. Toh WS, Lee EH, Guo XM, et al. Cartilage repair using hyaluronan hydrogel-encapsulated human embryonic stem cell-derived chondrogenic cells. Biomaterials 2010;31(27):6968-6980.
15. Beyer Nardi N, da Silva Meirelles L. Mesenchymal stem cells: isolation, in vitro expansion and characterization. Handbook Exp Pharmacol 2006;174(174):249-282.
16. Caplan AI. Review: mesenchymal stem cells - cell-based reconstructive therapy in orthopedics. Tissue Eng 2005;11(7-8):1198-1211. (Pubitemid 41321423)
17. Osugi M, Katagiri W, Yoshimi R, Inukai T, Hibi H, Ueda M. Conditioned media from mesenchymal stem cells enhanced bone regeneration in rat calvarial bone defects. Tissue Eng Part A 2012;18(13-14):1479-1489.
18. Cao J, Wang YN, Shi XL, et al. In vivo and in vitro imaging tracing of dual-labeled bone mesenchymal stem cells transplanted into myocardium of F344 rats. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 2012;34(5):474-479.
19. Drey F, Choi YH, Neef K, et al. Noninvasive in vivo tracking of mesenchymal stem cells and evaluation of cell therapeutic effects in a murine model using a clinical 3.0 T MRI [abstr]. Cell Transplant http://www.ncbi.nlm. nih.gov/pubmed/23050950. Published October 8, 2012. Accessed April 3, 2013.
20. Kraitchman DL, Bulte JW. Imaging of stem cells using MRI. Basic Res Cardiol 2008;103(2):105-113. (Pubitemid 351356753)
21. Lalande C, Miraux S, Derkaoui SM, et al. Magnetic resonance imaging tracking of human adipose derived stromal cells within three-dimensional scaffolds for bone tissue engineering. Eur Cell Mater 2011;21:341-354.
22. Lin Y, Tang W, Wu L, et al. Bone regeneration by BMP-2 enhanced adipose stem cells loading on alginate gel. Histochem Cell Biol 2008;129(2):203-210.
23. Sun JH, Zhang YL, Qian SP, et al. Assessment of biological characteristics of mesenchymal stem cells labeled with superparamagnetic iron oxide particles in vitro. Mol Med Rep 2012;5(2):317-320.
24. U.S. Food and Drug Administration. Inspection of human cells, tissues, and cellular and tissue-based products HCT/Ps. Silver Spring, Md: U.S. Food and Drug Administration, 2012.
25. Kuroda T, Yasuda S, Sato Y. Tumorigenicity studies for human pluripotent stem cell-derived products. Biol Pharm Bull 2013;36(2):189-192.
26. Motaln H, Schichor C, Lah TT. Human mesenchymal stem cells and their use in cell-based therapies. Cancer 2010;116(11):2519-2530.
27. Soenen SJ, De Cuyper M. Assessing cytotoxicity of (iron oxide-based) nanoparticles: an overview of different methods exemplified with cationic magnetoliposomes. Contrast Media Mol Imaging 2009;4(5):207-219.
28. Arbab AS, Yocum GT, Wilson LB, et al. Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability. Mol Imaging 2004;3(1):24-32.
29. Kostura L, Kraitchman DL, Mackay AM, Pittenger MF, Bulte JW. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 2004;17(7):513-517. (Pubitemid 39549429)
30. Sykova E, Jendelova P. In vivo tracking of stem cells in brain and spinal cord injury. Prog Brain Res 2007;161:367-383. (Pubitemid 47023095)
31. Mailänder V, Lorenz MR, Holzapfel V, et al. Carboxylated superparamagnetic iron oxide particles label cells intracellularly without transfection agents. Mol Imaging Biol 2008;10(3):138-146.
32. Wilhelm C, Gazeau F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 2008;29(22):3161-3174.
33. Schäfer R, Kehlbach R, Wiskirchen J, et al. Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology 2007;244(2):514-523. (Pubitemid 47080884)
34. Neuwelt EA, Hamilton BE, Varallyay CG, et al. Ultrasmall superparamagnetic iron oxides (USPIOs): a future alternative magnetic resonance (MR) contrast agent for patients at risk for nephrogenic systemic fibrosis (NSF)? Kidney Int 2009;75(5):465-474.
35. Daldrup-Link HE, Golovko D, Ruffell B, et al. MRI of tumor-associated macrophages with clinically applicable iron oxide nanoparticles. Clin Cancer Res 2011;17(17):5695-5704.
36. Hasan DM, Mahaney KB, Magnotta VA, et al. Macrophage imaging within human cerebral aneurysms wall using ferumoxytol-enhanced MRI: a pilot study. Arterioscler Thromb Vasc Biol 2012;32(4):1032-1038.
37. Leung K. Ferumoxides. In: Molecular imaging and contrast agent database (MICAD) [Internet]. Bethesda, Md: U.S. National Center for Biotechnology Information, 2004-2013. http://www.ncbi.nlm.nih.gov/books/NBK23037/. Accessed April 3, 2013.
38. Metz S, Lohr S, Settles M, et al. Ferumoxtran-10-enhanced MR imaging of the bone marrow before and after conditioning therapy in patients with non-Hodgkin lymphomas. Eur Radiol 2006;16(3):598-607. (Pubitemid 44149372)
39. Trivedi RA, U-King-Im JM, Graves MJ, et al. In vivo detection of macrophages in human carotid atheroma: temporal dependence of ultrasmall superparamagnetic particles of iron oxide-enhanced MRI. Stroke 2004;35(7):1631-1635.
40. Hamilton BE, Nesbit GM, Dosa E, et al. Comparative analysis of ferumoxytol and gadoteridol enhancement using T1- and T2-weighted MRI in neuroimaging. AJR Am J Roentgenol 2011;197(4):981-988.
41. Hasan DM, Amans M, Tihan T, et al. Ferumoxytol-enhanced MRI to image inflammation within human brain arteriovenous malformations: a pilot investigation. Transl Stroke Res 2012;3(suppl 1):166-173.
42. Simon GH, von Vopelius-Feldt J, Fu Y, et al. Ultrasmall supraparamagnetic iron oxide-enhanced magnetic resonance imaging of antigen-induced arthritis: a comparative study between SHU 555 C, ferumoxtran-10, and ferumoxytol. Invest Radiol 2006;41(1):45-51. (Pubitemid 44378278)
43. Simon GH, Raatschen HJ, Wendland MF, et al. Ultrasmall superparamagnetic iron-oxide-enhanced MR imaging of normal bone marrow in rodents: original research original research. Acad Radiol 2005;12(9):1190-1197. (Pubitemid 41160566)
44. Wang J, Chen Y, Chen B, et al. Pharmacokinetic parameters and tissue distribution of magnetic Fe(3)O(4) nanoparticles in mice. Int J Nanomedicine 2010;5:861-866.
45. Li X, Zhang Y, Qi G. Evaluation of isolation methods and culture conditions for rat bone marrow mesenchymal stem cells. Cytotechnology 2013;65(3):323-334.
46. Rouger K, Fornasari B, Armengol V, et al. Progenitor cell isolation from muscle-derived cells based on adhesion properties. J Histochem Cytochem 2007;55(6):607-618. (Pubitemid 46791943)
47. Castaneda RT, Khurana A, Khan R, Daldrup-Link HE. Labeling stem cells with ferumoxytol, an FDA-approved iron oxide nanoparticle [abstr]. J Vis Exp 2011 Nov 4;(57):e3482.
48. Inai T, Mancuso M, Hashizume H, et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004;165(1):35-52. (Pubitemid 38821812)
49. Kircher MF, de la Zerda A, Jokerst JV, et al. A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacous-tic-Raman nanoparticle. Nat Med 2012;18(5):829-834.
50. Henning TD, Sutton EJ, Kim A, et al. The influence of ferucarbotran on the chondrogenesis of human mesenchymal stem cells. Contrast Media Mol Imaging 2009;4(4):165-173.
51. Baker BM, Chen CS. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J Cell Sci 2012;125(pt 13):3015-3024.
52. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 2009;11(4):377-391.
53. Adult stem cell therapy for repairing articular cartilage in gonarthrosis. http://clinicaltrials.gov/ct2/show/NCT01227694. Published October 22, 2010. Updated July 22, 2011. Accessed October 16, 2012.
54. Coyne DW. Ferumoxytol for treatment of iron deficiency anemia in patients with chronic kidney disease. Expert Opin Pharmacother 2009;10(15):2563-2568.
55. Schwenk MH. Ferumoxytol: a new intravenous iron preparation for the treatment of iron deficiency anemia in patients with chronic kidney disease. Pharmacotherapy 2010;30(1):70-79.
56. Singh A, Patel T, Hertel J, Bernardo M, Kausz A, Brenner L. Safety of ferumoxytol in patients with anemia and CKD. Am J Kidney Dis 2008;52(5):907-915.
57. Spinowitz BS, Schwenk MH, Jacobs PM, et al. The safety and efficacy of ferumoxytol therapy in anemic chronic kidney disease patients. Kidney Int 2005;68(4):1801-1807. (Pubitemid 43169925)
58. Ma X, de Bruijn M, Robin C, et al. Expression of the Ly-6A (Sca-1) lacZ transgene in mouse haematopoietic stem cells and embryos. Br J Haematol 2002;116(2):401-408. (Pubitemid 34155515)
59. Ozdemir M, Attar A, Kuzu I, et al. Stem cell therapy in spinal cord injury: in vivo and postmortem tracking of bone marrow mononuclear or mesenchymal stem cells. Stem Cell Rev 2012;8(3):953-962.
60. Srinivas M, Aarntzen EH, Bulte JW, et al. Imaging of cellular therapies. Adv Drug Deliv Rev 2010;62(11):1080-1093.
61. Chung E, Nam SY, Ricles LM, Emelianov SY, Suggs LJ. Evaluation of gold nanotracers to track adipose-derived stem cells in a PEGylated fibrin gel for dermal tissue engineering applications. Int J Nanomedicine 2013;8:325-336.
62. Guenoun J, Ruggiero A, Doeswijk G, et al. In vivo quantitative assessment of cell viability of gadolinium or iron-labeled cells using MRI and bioluminescence imaging. Contrast Media Mol Imaging 2013;8(2):165-174.
63. Templin C, Zweigerdt R, Schwanke K, et al. Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression. Circulation 2012;126(4):430-439.
64. Loeuille D, Chary-Valckenaere I. MRI in OA: from cartilage to bone marrow lesion. Osteoporos Int 2012;23(suppl 8):S867-S869.
65. Shen Y, Shao Y, He H, et al. Gadolinium(3+)-doped mesoporous silica nanoparticles as a potential magnetic resonance tracer for monitoring the migration of stem cells in vivo. Int J Nanomedicine 2013;8:119-127.
66. Guenoun J, Koning GA, Doeswijk G, et al. Cationic Gd-DTPA liposomes for highly efficient labeling of mesenchymal stem cells and cell tracking with MRI. Cell Transplant 2012;21(1):191-205.
67. Nejadnik H, Henning TD, Do T, et al. MR imaging features of gadofluorine-labeled matrix-associated stem cell implants in cartilage defects. PLoS ONE 2012;7(12):e49971.
68. Khurana A, Nejadnik H, Chapelin F, et al. Ferumoxytol: a new, clinically applicable label for stem-cell tracking in arthritic joints with MRI [abstr]. Nanomedicine (Lond) http://www.ncbi.nlm.nih.gov/pubmed/?term=23534832. Published March 27, 2013. Accessed March 28, 2013.
69. Nedopil A, Klenk C, Kim C, et al. MR signal characteristics of viable and apoptotic human mesenchymal stem cells in matrix-associated stem cell implants for treatment of osteoarthritis. Invest Radiol 2010;45(10):634-640.
70. Zhu J, Zhou L, Xing Wu F. Tracking neural stem cells in patients with brain trauma. N Engl J Med 2006;355(22):2376-2378. (Pubitemid 44837805)
71. 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(3):461-466. (Pubitemid 47016231)
72. de Vries IJ, Lesterhuis WJ, Barentsz JO, et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 2005;23(11):1407-1413. (Pubitemid 41679393)
73. Toso C, Vallee JP, Morel P, et al. Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant 2008;8(3):701-706. (Pubitemid 351287550)
74. Bulte JW. In vivo MRI cell tracking: clinical studies. AJR Am J Roentgenol 2009;193(2):314-325.
75. Richards JM, Shaw CA, Lang NN, et al. In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: feasibility and safety in humans. Circ Cardiovasc Imaging 2012;5(4):509-517.
76. Thu MS, Bryant LH, Coppola T, et al. Self-assembling nanocomplexes by combining ferumoxytol, heparin and protamine for cell tracking by magnetic resonance imaging. Nat Med 2012;18(3):463-467.
77. Brown CC, Balian G. Effect of heparin on synthesis of short chain collagen by chondrocytes and smooth muscle cells. J Cell Biol 1987;105(2):1007-1012. (Pubitemid 18043861)
78. Roosendaal G, Vianen ME, van den Berg HM, Lafeber FP, Bijlsma JW. Cartilage damage as a result of hemarthrosis in a human in vitro model. J Rheumatol 1997;24(7):1350-1354. (Pubitemid 27353380)
79. Arbab AS, Janic B, Haller J, Pawelczyk E, Liu W, Frank JA. In vivo cellular imaging for translational medical research. Curr Med Imaging Rev 2009;5(1):19-38.
80. Nejadnik H, Henning TD, Castaneda RT, et al. Somatic differentiation and MR imaging of magnetically labeled human embryonic stem cells. Cell Transplant 2012;21(12):2555-2567.
81. Henning TD, Wendland MF, Golovko D, et al. Relaxation effects of ferucarbotran-labeled mesenchymal stem cells at 1.5T and 3T: discrimination of viable from lysed cells. Magn Reson Med 2009;62(2):325-332.
82. Bhat S, Tripathi A, Kumar A. Supermacroprous chitosan-agarose-gelatin cryogels: in vitro characterization and in vivo assessment for cartilage tissue engineering. J R Soc Interface 2011;8(57):540-554.
83. Xu H, Othman SF, Magin RL. Monitoring tissue engineering using magnetic resonance imaging. J Biosci Bioeng 2008;106(6):515-527.
84. Daldrup-Link HE, Rummeny EJ, Ihssen B, Kienast J, Link TM. Iron-oxide-enhanced MR imaging of bone marrow in patients with non-Hodgkin's lymphoma: differentiation between tumor infiltration and hypercellular bone marrow. Eur Radiol 2002;12(6):1557-1566. (Pubitemid 36940237)
85. Usman AA, Taimen K, Wasielewski M, et al. Cardiac magnetic resonance T2 mapping in the monitoring and follow-up of acute cardiac transplant rejection: a pilot study. Circ Cardiovasc Imaging 2012;5(6):782-790.
86. Centeno CJ, Busse D, Kisiday J, Keohan C, Freeman M, Karli D. Regeneration of meniscus cartilage in a knee treated with percutaneously implanted autologous mesenchymal stem cells. Med Hypotheses 2008;71(6):900-908.
87. Orozco L, Soler R, Morera C, Alberca M, Sánchez A, García-Sancho J. Intervertebral disc repair by autologous mesenchymal bone marrow cells: a pilot study. Transplantation 2011;92(7):822-828.
88. Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002;10(3):199-206. (Pubitemid 34189569)
89. Beitzel K, McCarthy MB, Cote MP, et al. Rapid isolation of human stem cells (connective progenitor cells) from the distal femur during arthroscopic knee surgery. Arthroscopy 2012;28(1):74-84.
90. Spahr L, Chalandon Y, Terraz S, et al. Autologous bone marrow mononuclear cell transplantation in patients with decompensated alcoholic liver disease: a randomized controlled trial. PLoS ONE 2013;8(1):e53719.
91. Lu M, Cohen MH, Rieves D, Pazdur R. FDA report: ferumoxytol for intravenous iron therapy in adult patients with chronic kidney disease. Am J Hematol 2010;85(5):315-319.
92. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010;67(10):1187-1194.