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Review

Advanced clinical imaging for the evaluation of stem cell based therapies

ORCID Icon, , ORCID Icon, ORCID Icon & ORCID Icon
Pages 1253-1264 | Received 01 Dec 2020, Accepted 11 Feb 2021, Published online: 23 Feb 2021

References

  • Wong VW, Sorkin M, Gurtner GC. Enabling stem cell therapies for tissue repair: current and future challenges. Biotechnol Adv. 2013;31(5):744–751.
  • Carstairs A, Genever P. Stem cell treatment for musculoskeletal disease. Curr Opin Pharmacol. 2014;16:1–6.
  • Kim YS, Smoak MM, Melchiorri AJ, et al. An overview of the tissue engineering market in the United States from 2011 to 2018. Tissue Eng Part A. 2018;25(1–2):1–8.
  • De Luca M, Aiuti A, Cossu G, et al. Advances in stem cell research and therapeutic development. Nat Cell Biol. 2019;21(7):801–811.
  • Sipp D, Robey PG, Turner L. Clear up this stem-cell mess. Nature. 2018;561(7724):455–457.
  • Klontzas ME, Karantanas AH. Considerations on the use of ferumoxytol-enhanced MRI for tracking stem cell implants in cartilage defects. Radiology. 2020;294(1):238–239.
  • Karantanas AH. What’s new in the use of MRI in the orthopaedic trauma patient? Injury. 2014;45(6):923–933.
  • Ye Y, Bogaert J. Cell therapy in myocardial infarction: emphasis on the role of MRI. Eur Radiol. 2008;18(3):548–569.
  • Budde MD, Frank JA. Magnetic tagging of therapeutic cells for MRI. J Nucl Med. 2009;50(2):171–174.
  • Feng C, Luo X, He N, et al. Efficacy and persistence of allogeneic adipose-derived mesenchymal stem cells combined with hyaluronic acid in osteoarthritis after intra-articular injection in a sheep model. Tissue Eng Part A. 2018;24(3–4):219–233.
  • Theruvath AJ, Nejadnik H, Lenkov O, et al., Tracking stem cell implants in cartilage defects of minipigs by using ferumoxytol-enhanced MRI. Radiology. 292(1): 129–137. 2019.
  • Emmert MY, Wolint P, Jakab A, et al. Safety and efficacy of cardiopoietic stem cells in the treatment of post-infarction left-ventricular dysfunction – from cardioprotection to functional repair in a translational pig infarction model. Biomaterials. 2017;122:48–62.
  • Carr CA, Stuckey DJ, Tatton L, et al. Bone marrow-derived stromal cells home to and remain in the infarcted rat heart but fail to improve function: an in vivo cine-MRI study. Am J Physiol Hear Circ Physiol. 2008;295(2):H533–42.
  • 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. Cell Transplat. 2013;22(11):1971–1980.
  • Thu MS, Najbauer J, Kendall SE, et al. Iron labeling and pre-clinical MRI visualization of therapeutic human neural stem cells in a murine glioma model. PLoS One. 2009;4(9):e7218.
  • Li L, Jiang Q, Ding G, et al. Effects of administration route on migration and distribution of neural progenitor cells transplanted into rats with focal cerebral ischemia, an MRI study. J Cereb Blood Flow Metab. 2010;30(3):653–662.
  • Magnitsky S, Watson DJ, Walton RM, et al. In vivo and ex vivo MRI detection of localized and disseminated neural stem cell grafts in the mouse brain. Neuroimage. 2005;26(3):744–754.
  • Li K, Qin J, Wang X, et al. Magnetic resonance imaging monitoring dual-labeled stem cells for treatment of mouse nerve injury. Cytotherapy. 2013;15(10):1275–1285.
  • Neuwelt A, Sidhu N, Hu CAA, et al. Iron-based superparamagnetic nanoparticle contrast agents for MRI of infection and inflammation. AJR Am J Roentgenol. 2015;204(3):W302–13.
  • 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 Cells Mater. 2011;21:341–354.
  • Kremen TJ, Stefanovic T, Tawackoli W, et al. A translational porcine model for human cell–based therapies in the treatment of posttraumatic osteoarthritis after anterior cruciate ligament injury. Am J Sport Med. 2020;48(12):3002–3012.
  • Chapman V, Markides H, Sagar DR, et al. Therapeutic benefit for late, but not early, passage mesenchymal stem cells on pain behaviour in an animal model of osteoarthritis. Stem Cells Int. 2017;2017:2017.
  • Kremen TJ, Bez M, Sheyn D, et al. In vivo imaging of exogenous progenitor cells in tendon regeneration via superparamagnetic iron oxide particles. Am J Sport Med. 2019;47(11):2737–2744.
  • Neri M, Maderna C, Cavazzin C, et al. Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: relevance for in vivo cell tracking. Stem Cells. 2008;26(2):505–516.
  • Qiao H, Zhang H, Yamanaka S, et al. Long-term improvement in postinfarct left ventricular global and regional contractile function is mediated by embryonic stem cell-derived cardiomyocytes. Circ Cardiovasc Imaging. 2011;4(1):33–41.
  • Zeng Y, Wang L, Zhou Z, et al. Gadolinium hybrid iron oxide nanocomposites for dual: t 1- and T 2-weighted MR imaging of cell labeling. Biomater Sci. 2017;5(1):50–56.
  • Rahmi G, Pidial L, Silva AKA, et al. Designing 3D mesenchymal stem cell sheets merging magnetic and fluorescent features: when cell sheet technology meets image-guided cell therapy. Theranostics. 2016;6(5):739–751.
  • Magnitsky S, Walton RM, Wolfe JH, et al. Magnetic resonance imaging detects differences in migration between primary and immortalized neural stem cells. Acad Radiol. 2008;15(10):1269–1281.
  • Song M, Kim Y, Kim Y, et al. MRI tracking of intravenously transplanted human neural stem cells in rat focal ischemia model. Neurosci Res. 2009;64(2):235–239.
  • Rice HE, Hsu EW, Sheng H, et al. Superparamagnetic iron oxide labeling and transplantation of adipose-derived stem cells in middle cerebral artery occlusion-injured mice. AJR Am J Roentgenol. 2007;188(4):1101–1108.
  • Hu SL, Zhang JQ, Hu X, et al. In vitro labeling of human umbilical cord mesenchymal stem cells with superparamagnetic iron oxide nanoparticles. J Cell Biochem. 2009;108(2):529–535.
  • Smith EJ, Stroemer RP, Gorenkova N, et al. Implantation site and lesion topology determine efficacy of a human neural stem cell line in a rat model of chronic stroke. Stem Cells. 2012;30(4):785–796.
  • Vandergriff AC, Hensley TM, Henry ET, et al. Magnetic targeting of cardiosphere-derived stem cells with ferumoxytol nanoparticles for treating rats with myocardial infarction. Biomaterials. 2014;35(30):8528–8539.
  • Guo R, Li Q, Yang F, et al. In vivo MR imaging of dual MRI reporter genes and Deltex-1 gene-modified human mesenchymal stem cells in the treatment of closed penile fracture. Mol Imaging Biol. 2018;20(3):417–427.
  • Goodrich LR, Chen A, Werpy NM, et al. Addition of mesenchymal stem cells to autologous platelet-enhanced fibrin scaffolds in chondral defects: does it enhance repair? J Bone J Surg Am. 2016;98(1):23–34.
  • Xiao Z, Tang F, Zhao Y, et al. Significant improvement of acute complete spinal cord injury patients diagnosed by a combined criteria implanted with NeuroRegen scaffolds and mesenchymal stem cells. Cell Transpl. 2018;27(6):907–915.
  • Chen YS, Hsueh YS, Chen YY, et al. Evaluation of a laminin-alginate biomaterial, adipocytes, and adipocyte-derived stem cells interaction in animal autologous fat grafting model using 7-Tesla magnetic resonance imaging. J Mater Sci Mater Med. 2017;28(1):1.
  • Keshtkar S, Azarpira N, Ghahremani MH. Mesenchymal stem cell-derived extracellular vesicles: novel frontiers in regenerative medicine. Stem Cell Res Ther. 2018;9(1):63.
  • Klontzas ME, Karantanas AH. MR imaging of artificial musculoskeletal tissues: bridging the gap between basic science and clinical reality. Hell J Radiol. 2019;5(1):38–49.
  • Chiu GS, Boukelmoune N, Chiang ACA, et al. Nasal administration of mesenchymal stem cells restores cisplatin-induced cognitive impairment and brain damage in mice. Oncotarget. 2018;9(85):35581–35597.
  • Gu M, Nguyen PK, Lee AS, et al. Microfluidic single-cell analysis shows that porcine induced pluripotent stem cell-derived endothelial cells improve myocardial function by paracrine activation. Circ Res. 2012;111(7):882–893.
  • Chow A, Stuckey DJ, Kidher E, et al. Human induced pluripotent stem cell-derived cardiomyocyte encapsulating bioactive hydrogels improve rat heart function post myocardial infarction. Stem Cell Rep. 2017;9(5):1415–1422.
  • Kim PJ, Mahmoudi M, Ge X, et al. Direct evaluation of myocardial viability and stem cell engraftment demonstrates salvage of the injured myocardium. Circ Res. 2015;116(7):e40–50.
  • Moisan A, Pannetier N, Grillon E, et al. Intracerebral injection of human mesenchymal stem cells impacts cerebral microvasculature after experimental stroke: MRI study. NMR Biomed. 2012;25(12):1340–1348.
  • Klontzas ME, Papadakis GZ, Marias K, et al. Musculoskeletal trauma imaging in the era of novel molecular methods and artificial intelligence. Injury. 2020;51(12):2748–2756.
  • Bendtsen M, Bünger CE, Zou X, et al. Autologous stem cell therapy maintains vertebral blood flow and contrast diffusion through the endplate in experimental intervertebral disc degeneration. Spine (Phila Pa 1976). 2011;36(6):373–379.
  • Jiang Q, Qu C, Chopp M, et al., MRI evaluation of axonal reorganization after bone marrow stromal cell treatment of traumatic brain injury. NMR Biomed. 24(9): 1119–1128. 2011.
  • Jiang Q, Zhang ZG, Ding GL, et al. MRI detects white matter reorganization after neural progenitor cell treatment of stroke. Neuroimage. 2006;32(3):1080–1089.
  • Grossman RI, Gomori JM, Ramer KN, et al. Magnetization transfer: theory and clinical applications in neuroradiology. Radiographics. 1994;14(2):279–290.
  • Li W, Hong L, Hu L, et al. Magnetization transfer imaging provides a quantitative measure of chondrogenic differentiation and tissue development. Tissue Eng Part C. 2010;16(6): 1407–1415.
  • Bible E, Dell’Acqua F, Solanky B, et al. Non-invasive imaging of transplanted human neural stem cells and ECM scaffold remodeling in the stroke-damaged rat brain by 19F- and diffusion-MRI. Biomaterials. 2012;33(10):2858–2871.
  • Azzabi F, Rottmar M, Jovaisaite V, et al. Viability, differentiation capacity, and detectability of super-paramagnetic iron oxide-labeled muscle precursor cells for magnetic-resonance imaging. Tissue Eng Part C. 2015;21(2):182–191.
  • Brasil GV, Silva Dos Santos D, Mendonça EA, et al. Therapy with cardiomyocytes derived from pluripotent cells in chronic Chagasic cardiomyopathy. Cells. 2020;9(7):1629.
  • Hu A, Xing R, Jiang L, et al. Thermosensitive hydrogels loaded with human-induced pluripotent stem cells overexpressing growth differentiation factor-5 ameliorate intervertebral disc degeneration in rats. J Biomed Mater Res Part B Appl Biomater. 2020;108(5):2005–2016.
  • Moshayedi P, Nih LR, Llorente IL, et al. Systematic optimization of an engineered hydrogel allows for selective control of human neural stem cell survival and differentiation after transplantation in the stroke brain. Biomaterials. 2016;105:145–155.
  • Rutland JW, Delman BN, Gill CM, et al. Emerging use of ultra-high-field 7T MRI in the study of intracranial vascularity: state of the field and future directions. AJNR Am J NeuroradiolAm J Neuroradiol. 2020;41(1):2–9.
  • Ladd ME, Bachert P, Meyerspeer M, et al. Pros and cons of ultra-high-field MRI/MRS for human application. Progr Nucl Magn Reson Spectrosc. 2018;109:1–50.
  • Elmi A, Kajbafzadeh AM, Oghabian MA, et al. Anal sphincter repair with muscle progenitor cell transplantation: serial assessment with iron oxide - enhanced MRI. AJR Am J Roentgenol. 2014;202(3):619–625.
  • Lebouvier A, Poignard A, Cavet M, et al. Development of a simple procedure for the treatment of femoral head osteonecrosis with intra-osseous injection of bone marrow mesenchymal stromal cells: study of their biodistribution in the early time points after injection. Stem Cell Res Ther. 2015;6(1):1–14.
  • Otrakji A, Digumarthy SR, Lo GR, et al. Dual-energy CT: spectrum of thoracic abnormalities. Radiographics. 2016;36(1):38–52.
  • Gibney B, Dual-energy MN. CT of spinal tophaceous gout. Radiology. 2020;296(2):276.
  • Gosangi B, Mandell JC, Weaver MJ, et al. Bone marrow edema at dual-energy CT: a game changer in the emergency department. Radiographics. 2020;40(3):859–874.
  • Wan D, Chen D, Li K, et al. Gold nanoparticles as a potential cellular probe for tracking of stem cells in bone regeneration using dual-energy computed tomography. ACS Appl Mater Interfac. 2016;8(47):32241–32249.
  • Chen D, Wan D, Wang R, et al. Multimodal nanoprobe based on upconversion nanoparticles for monitoring implanted stem cells in bone defect of big animal. ACS Biomater Sci Eng. 2018;4(2):626–634.
  • Allmendinger AM, Tang ER, Lui YW, et al. Imaging of stroke: part 1, perfusion CT - overview of imaging technique, interpretation pearls, and common pitfalls. AJR Am J Roentgenol. 2012;198(1):52–62.
  • Kim SH, Kamaya A, Willmann JK. CT perfusion of the liver in oncology. Radiology. 2014;272(2):322–344.
  • Galanakis N, Maris TG, Kontopodis N, et al. CT foot perfusion examination for evaluation of percutaneous transluminal angioplasty outcome in patients with critical limb ischemia: a feasibility study. J Vasc Interv Radiol. 2019;30(4):560–568.
  • Wen Q, Ma L, Chen YP, et al., Treatment of avascular necrosis of the femoral head by hepatocyte growth factor-transgenic bone marrow stromal stem cells. Gene Ther. 15(23): 1523–1535. 2008.
  • Wang Y, Lian F, Li J, et al. Adipose derived mesenchymal stem cells transplantation via portal vein improves microcirculation and ameliorates liver fibrosis induced by CCl4 in rats. J Transl Med. 2012;10(1):1–9.
  • Rouwkema J, Khademhosseini A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 2016;34(9):733–745.
  • P V G, Dinopoulos H, Tsiridis E. Bone substitutes: an update. Injury. 2005;36(3):S20–7.
  • Li X, Hacker M. Molecular imaging in stem cell-based therapies of cardiac diseases. Adv Drug Deliv Rev. 2017;120:71–88.
  • Delso G, Fürst S, Jakoby B, et al. Performance measurements of the siemens mMR integrated whole-body PET/MR scanner. J Nucl Med. 2011;52(12):1914–1922.
  • Levin CS, Maramraju SH, Khalighi MM, et al. Design features and mutual compatibility studies of the time-of-flight PET capable GE SIGNA PET/MR system. IEEE Trans Med Imaging. 2016;35(8):1907–1914.
  • Abbas F, Wu JC, Gambhir SS, et al. Molecular imaging of stem cells. StemJournal. 2019;1(1):27–46.
  • Tamura M, Unno K, Yonezawa S, et al. In vivo trafficking of endothelial progenitor cells their possible involvement in the tumor neovascularization. Life Sc. 2004;75(5):575–584.
  • Won JK, Kang HJ, Kim HS, et al. Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction. J Nucl Med. 2006;47(8):1295–1301.
  • Hofmann M, Wollert KC, Meyer GP, et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation. 2005;111(17):2198–2202.
  • Wolfs E, Struys T, Notelaers T, et al. 18F-FDG labeling of mesenchymal stem cells and multipotent adult progenitor cells for PET imaging: effects on ultrastructure and differentiation capacity. J Nucl Med. 2013;54(3):447–454.
  • Klontzas ME, Vernardis SI, Heliotis M, et al. Metabolomics analysis of the osteogenic differentiation of umbilical cord blood mesenchymal stem cells reveals differential sensitivity to osteogenic agents. Stem Cells Dev. 2017;26(10):723–733.
  • Devito L, Klontzas ME, Cvoro A, et al. Comparison of human isogeneic Wharton’s jelly MSCs and iPSC-derived MSCs reveals differentiation-dependent metabolic responses to IFNG stimulation. Cell Death Dis. 2019;10(4):1–13.
  • Klontzas ME, Reakasame S, Silva R, et al. Oxidized alginate hydrogels with the GHK peptide enhance cord blood mesenchymal stem cell osteogenesis: a paradigm for metabolomics-based evaluation of biomaterial design. Acta Biomater. 2019;88:88.
  • Winkler J, Lukovic D, Mester-Tonczar J, et al. Quantitative hybrid cardiac [18F]FDG-PET-MRI images for assessment of cardiac repair by preconditioned cardiosphere-derived cells. Mol Ther Methods Clin Dev. 2020;18:354–366.
  • Sood V, Mittal BR, Bhansali A, et al. Biodistribution of 18F-FDG-labeled autologous bone marrow-derived stem cells in patients with type 2 Diabetes mellitus: exploring targeted and intravenous routes of delivery. Clin Nucl Med. 2015;40(9):697–700.
  • Jackson J, Chapon C, Jones W, et al. In vivo multimodal imaging of stem cell transplantation in a rodent model of Parkinson’s disease. J Neurosci Methods. 2009;183(2):141–148.
  • Asiedu KO, Ferdousi M, Ton PT, et al. Bone marrow cell homing to sites of acute tibial fracture: 89 Zr-oxine cell labeling with positron emission tomographic imaging in a mouse model. EJNMMI Res. 2018;8(1):109.
  • Collignon AM, Lesieur J, Anizan N, et al. Early angiogenesis detected by PET imaging with 64Cu-NODAGA-RGD is predictive of bone critical defect repair. Acta Biomater. 2018;82:111–121.
  • Yaghoubi SS, Campbell DO, Radu CG, et al. Positron emission tomography reporter genes and reporter probes: gene and cell therapy applications. Theranostics. 2012;2(4):374–391.
  • Liang Q, Satyamurthy N, Barrio JR, et al. Noninvasive, quantitative imaging in living animals of a mutant dopamine D2 receptor reporter gene in which ligand binding is uncoupled from signal transduction. Gene Ther. 2001;8(19):1490–1498.
  • Wolfs E, Holvoet B, Ordovas L, et al. Molecular imaging of human embryonic stem cells stably expressing human PET reporter genes after zinc finger nuclease-mediated genome editing. J Nucl Med. 2017;58(10):1659–1665.
  • McCracken MN, Gschweng EH, Nair-Gill E, et al., Long-term in vivo monitoring of mouse and human hematopoietic stem cell engraftment with a human positron emission tomography reporter gene. Proc Natl Acad Sci USA. 110(5): 1857–1862. 2013.
  • Gao Y, Wu S, Pan J, et al. CRISPR/Cas9-edited triple-fusion reporter gene imaging of dynamics and function of transplanted human urinary-induced pluripotent stem cell-derived cardiomyocytes. Eur J Nucl Med Mol Imaging. 2020. https://do(Epub ahead of print). https://doi.org/10.1007/s00259-020-05087-0
  • Jin J, Jeong SI, Shin YM, et al. Transplantation of mesenchymal stem cells within a poly(lactide-co-ε- caprolactone) scaffold improves cardiac function in a rat myocardial infarction model. Eur J Hear Fail. 2009;11(2):147–153.
  • Wolf D, Reinhard A, Krause U, et al. Stem cell therapy improves myocardial perfusion and cardiac synchronicity: new application for echocardiography. J Am Soc Echocardiogr. 2007;20(5):512–520.
  • Inaba Y, Davidson BP, Kim S, et al. Echocardiographic evaluation of the effects of stem cell therapy on perfusion and function in ischemic cardiomyopathy. J Am Soc Echocardiogr. 2014;27(2):192–199.
  • J V J, Khademi C, Gambhir SS. Intracellular aggregation of multimodal silica nanoparticles for ultrasound-guided stem cell implantation. Sci Transl Med. 2013;20(5):177.
  • Bulte JWM, Daldrup-Link HE. Clinical tracking of cell transfer and cell transplantation: trials and tribulations. Radiology. 2018;289(3):604–615.
  • Wang J, Jokerst JV. Stem cell imaging: tools to improve cell delivery and viability. Stem Cells Int. 2016;2016:9240652.
  • Leong-Poi H. Molecular imaging using contrast-enhanced ultrasound: evaluation of angiogenesis and cell therapy. Cardiovasc Res. 2009;84(2):190–200.
  • Villanueva FS. Molecular imaging of cardiovascular disease using ultrasound. J Nucl Cardiol. 2008;15(4):576–586.
  • Lindner JR. Molecular imaging with contrast ultrasound and targeted microbubbles. J Nucl Cardiol. 2004;11(2):215–221.
  • Foroutan F, J V J, Gambhir SS, et al. Sol-gel synthesis and electrospraying of biodegradable (P2O5)55-(CaO)39-(Na2O)15 glass nanospheres as a transient contrast agent for ultrasound stem cell imaging. ACS Nano. 2015;9(2):1868–1877.
  • Kempen PJ, Greasley S, Parker KA, et al., Theranostic mesoporous silica nanoparticles biodegrade after pro-survival drug delivery and ultrasound/magnetic resonance imaging of stem cells. Theranostics. 5(6): 631–642. 2015.
  • Nam SY, Ricles LM, Suggs LJ, et al. In vivo ultrasound and photoacoustic monitoring of mesenchymal stem cells labeled with gold nanotracers. PLoS One. 2012;7(5):1–9.
  • Imada T, Tatsumi T, Mori Y, et al. Targeted delivery of bone marrow mononuclear cells by ultrasound destruction of microbubbles induces both angiogenesis and arteriogenesis response. Arter Thromb Vasc Biol. 2005;25(10):2128–2134.
  • Xu YL, Gao YH, Liu Z, et al. Myocardium-targeted transplantation of mesenchymal stem cells by diagnostic ultrasound-mediated microbubble destruction improves cardiac function in myocardial infarction of New Zealand rabbits. Int J Cardiol. 2010;138(2):182–195.
  • Wang G, Zhang Q, Zhuo Z, et al., Effects of diagnostic ultrasound-targeted microbubble destruction on the homing ability of bone marrow stromal cells to the kidney parenchyma. Eur Radiol. 26(9): 3006–3016. 2016.
  • Wang G, Zhuo Z, Yang B, et al. Enhanced homing ability and retention of bone marrow stromal cells to diabetic nephropathy by microbubble-mediated diagnostic ultrasound irradiation. Ultrasound Med Biol. 2015;41(11):2977–2989.
  • Liu DD, Ullah M, Concepcion W, et al. The role of ultrasound in enhancing mesenchymal stromal cell-based therapies. Stem Cells Transl Med. 2020;9(8):850–866.

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