Accumulation of Iron Oxide-Based Contrast Agents in Rabbit Atherosclerotic Plaques in Relation to Plaque Age and Vulnerability Features

References

• Global Burden of Disease Study C. Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;386:743–800. doi:10.1016/S0140-6736(15)60692-4
   PubMed Web of Science ®Google Scholar
• Jackson SA, Thomas RM, Harrison SN. Cross-Sectional Imaging Made Easy. 2nd ed. Churchill Livingstone; 2004.
   Google Scholar
• Zheng KH, Schoormans J, Stiekema LCA, et al. Plaque permeability assessed with DCE-MRI associates with uspio uptake in patients with peripheral artery disease. Jacc Cardiovasc Imag. 2019;12:2081–2083. doi:10.1016/j.jcmg.2019.04.014
   PubMed Web of Science ®Google Scholar
• Rogosnitzky M, Branch S. Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms. Biometals. 2016;29:365–376. doi:10.1007/s10534-016-9931-7
   PubMed Web of Science ®Google Scholar
• Khawaja AZ, Cassidy DB, Al Shakarchi J, McGrogan DG, Inston NG, Jones RG. Revisiting the risks of MRI with Gadolinium based contrast agents - review of literature and guidelines. Insight Imaging. 2015;6:553–558. doi:10.1007/s13244-015-0420-2
   PubMed Web of Science ®Google Scholar
• Errante Y, Cirimele V, Mallio CA, Di Lazzaro V, Zobel BB, Quattrocchi CC. Progressive increase of T1 signal intensity of the dentate nucleus on unenhanced magnetic resonance images is associated with cumulative doses of intravenously administered gadodiamide in patients with normal renal function, suggesting dechelation. Invest Radiol. 2014;49:685–690. doi:10.1097/rli.0000000000000072
   PubMed Web of Science ®Google Scholar
• Kanda T, Ishii K, Kawaguchi H, Kitajima K, Takenaka D. High signal intensity in the dentate nucleus and globus pallidus on unenhanced T1-weighted MR images: relationship with increasing cumulative dose of a gadolinium-based contrast material. Radiology. 2014;270:834–841. doi:10.1148/radiol.13131669
   PubMed Web of Science ®Google Scholar
• Fretellier N, Rasschaert M, Bocanegra J, et al. Safety and gadolinium distribution of the new high-relaxivity gadolinium chelate gadopiclenol in a rat model of severe renal failure. Invest Radiol. 2021;56:826–836. doi:10.1097/Rli.0000000000000793
   PubMed Web of Science ®Google Scholar
• Liu Z, Zhao ML, Wang H, et al. High relaxivity Gd3+-based organic nanoparticles for efficient magnetic resonance angiography. J Nanobiotechnol. 2022;2:20.
   Google Scholar
• Liu SE, Jiang YX, Liu PC, et al. Single-Atom gadolinium nano-contrast agents with high stability for tumor T 1 magnetic resonance imaging. Acs Nano. 2023;17(9):8053–8063. doi:10.1021/acsnano.2c09664
   PubMed Web of Science ®Google Scholar
• Sadek H, Latif S, Collins R, Garry MG, Garry DJ. Use of ferumoxides for stem cell labeling. Regener Med. 2008;3(6):807–816. doi:10.2217/17460751.3.6.807
   PubMed Web of Science ®Google Scholar
• Ruggiero A, Guenoun J, Smit H, et al. In vivo MRI mapping of iron oxide-labeled stem cells transplanted in the heart. Contrast Media Mol Imaging. 2013;8(6):487–494. doi:10.1002/cmmi.1582
   PubMed Web of Science ®Google Scholar
• Saleh A, Schroeter M, Ringelstein A, et al. Iron oxide particle-enhanced MRI suggests variability of brain inflammation at early stages after ischemic stroke. Stroke. 2007;38(10):2733–2737. doi:10.1161/strokeaha.107.481788
   PubMed Web of Science ®Google Scholar
• Trivedi RA, Mallawarachi C, J-M. U-K-I, et al. Identifying inflamed carotid plaques using in vivo USPIO-enhanced MR imaging to label plaque macrophages. Arteriosclerosis Thrombosis Vasc Biol. 2006;26(7):1601–1606. doi:10.1161/01.ATV.0000222920.59760.df
   PubMed Web of Science ®Google Scholar
• Hyafil F, Laissy JP, Mazighi M, et al. Ferumoxtran-10-enhanced MRI of the hypercholesterolemic rabbit aorta: relationship between signal loss and macrophage infiltration. Arteriosclerosis Thrombosis Vasc Biol. 2006;26:176–181. doi:10.1161/01.ATV.0000194098.82677.57
   PubMed Web of Science ®Google Scholar
• Howarth SP, Tang TY, Trivedi R, et al. Utility of USPIO-enhanced MR imaging to identify inflammation and the fibrous cap: a comparison of symptomatic and asymptomatic individuals. Eur. J. Radiol. 2009;70:555–560. doi:10.1016/j.ejrad.2008.01.047
   PubMed Web of Science ®Google Scholar
• Degnan AJ, Patterson AJ, Tang TY, Howarth SP, Gillard JH. Evaluation of ultrasmall superparamagnetic iron oxide-enhanced MRI of carotid atherosclerosis to assess risk of cerebrovascular and cardiovascular events: follow-up of the ATHEROMA trial. Cerebrovascular Dis. 2012;34:169–173. doi:10.1159/000339984
   PubMed Web of Science ®Google Scholar
• Richards JM, Semple SI, MacGillivray TJ, et al. Abdominal aortic aneurysm growth predicted by uptake of ultrasmall superparamagnetic particles of iron oxide: a pilot study. Circ Cardiovasc Imaging. 2011;4:274–281. doi:10.1161/circimaging.110.959866
   PubMed Web of Science ®Google Scholar
• Sadat U, Howarth SP, Usman A, Tang TY, Graves MJ, Gillard JH. Sequential imaging of asymptomatic carotid atheroma using ultrasmall superparamagnetic iron oxide-enhanced magnetic resonance imaging: a feasibility study. J Stroke Cerebrovascular Dis. 2013;22:e271–276. doi:10.1016/j.jstrokecerebrovasdis.2012.06.015
   PubMed Web of Science ®Google Scholar
• Bernd H, De Kerviler E, Gaillard S, Bonnemain B. Safety and tolerability of ultrasmall superparamagnetic iron oxide contrast agent: comprehensive analysis of a clinical development program. Invest Radiol. 2009;44:336–342. doi:10.1097/RLI.0b013e3181a0068b
   PubMed Web of Science ®Google Scholar
• Elias A, Tsourkas A. Imaging circulating cells and lymphoid tissues with iron oxide nanoparticles. Hematology. 2009;720–726. doi:10.1182/asheducation-2009.1.720
   PubMedGoogle Scholar
• Yilmaz A, Dengler MA, van der Kuip H, et al. Imaging of myocardial infarction using ultrasmall superparamagnetic iron oxide nanoparticles: a human study using a multi-parametric cardiovascular magnetic resonance imaging approach. Eur Heart J. 2013;34:462–475. doi:10.1093/eurheartj/ehs366
   PubMed Web of Science ®Google Scholar
• Alam SR, Shah AS, Richards J, et al. Ultrasmall superparamagnetic particles of iron oxide in patients with acute myocardial infarction: early clinical experience. Circ Cardiovasc Imaging. 2012;5:559–565. doi:10.1161/circimaging.112.974907
   PubMed Web of Science ®Google Scholar
• Bietenbeck M, Florian A, Sechtem U, Yilmaz A. The diagnostic value of iron oxide nanoparticles for imaging of myocardial inflammation--quo vadis? J Cardiovasc Magn Reson. 2015;17:54. doi:10.1186/s12968-015-0165-6
   PubMed Web of Science ®Google Scholar
• Stirrat CG, Alam SR, MacGillivray TJ, et al. Ferumoxytol-enhanced magnetic resonance imaging assessing inflammation after myocardial infarction. Heart. 2017;103:1528–1535. doi:10.1136/heartjnl-2016-311018
   PubMed Web of Science ®Google Scholar
• Usman A, Patterson AJ, Yuan J, et al. Ferumoxytol-enhanced three-dimensional magnetic resonance imaging of carotid atheroma- a feasibility and temporal dependence study. Sci Rep. 2020;10:1808. doi:10.1038/s41598-020-58708-x
   PubMed Web of Science ®Google Scholar
• Smits LP, Tiessens F, Zheng KH, Stroes ES, Nederveen AJ, Coolen BF. Evaluation of ultrasmall superparamagnetic iron-oxide (USPIO) enhanced MRI with ferumoxytol to quantify arterial wall inflammation. Atherosclerosis. 2017;263:211–218. doi:10.1016/j.atherosclerosis.2017.06.020
   PubMed Web of Science ®Google Scholar
• Brittenden J, Houston G, Lambie R, et al. Aortic wall inflammation predicts abdominal aortic aneurysm expansion, rupture, and need for surgical repair. Circulation. 2017;136:787–797. doi:10.1161/Circulationaha.117.028433
   PubMed Web of Science ®Google Scholar
• Unterweger H, Janko C, Folk T, et al. Comparative in vitro and in vivo evaluation of different iron oxide-based contrast agents to promote clinical translation in compliance with patient safety. Int J Nanomed. 2023 ;18: 2071–2086. doi:10.2147/IJN.S402320
   PubMed Web of Science ®Google Scholar
• Shokrollahi H. Contrast agents for MRI. Mater Sci Eng C. 2013;33:4485–4497. doi:10.1016/j.msec.2013.07.012
   PubMed Web of Science ®Google Scholar
• Unterweger H, Janko C, Schwarz M, et al. Non-immunogenic dextran-coated superparamagnetic iron oxide nanoparticles: a biocompatible, size-tunable contrast agent for magnetic resonance imaging. Int j Nanomed. 2017;12:5223–5238. doi:10.2147/ijn.s138108
   PubMed Web of Science ®Google Scholar
• Unterweger H, Dezsi L, Matuszak J, et al. Dextran-coated superparamagnetic iron oxide nanoparticles for magnetic resonance imaging: evaluation of size-dependent imaging properties, storage stability and safety. Int j Nanomed. 2018;13:1899–1915. doi:10.2147/Ijn.S156528
   PubMed Web of Science ®Google Scholar
• Moonen RPM, Coolen BE, Sluimer JC, Daemen MJAP, Strijkers GJ. Iron oxide nanoparticle uptake in mouse brachiocephalic artery atherosclerotic plaque quantified by T-2-mapping MRI. Pharmaceutics. 2021;13. doi:10.3390/pharmaceutics13020279
   PubMed Web of Science ®Google Scholar
• Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation. 2001;103:415–422.
   PubMed Web of Science ®Google Scholar
• Kaneko C, Nitta N, Tsuchiya K, et al. MRI study of atherosclerotic plaque progression using ultrasmall superparamagnetic iron oxide in Watanabe heritable hyperlipidemic rabbits. Br J Radiol. 2015;3:88.
   Google Scholar
• Durand E, Raynaud JS, Bruneval P, et al. Magnetic resonance imaging of ruptured plaques in the rabbit with ultrasmall superparamagnetic particles of iron oxide. J Vasc Res. 2007;44:119–128. doi:10.1159/000098484
   PubMed Web of Science ®Google Scholar
• Bai Q, Xiao Y, Hong H, et al. Scavenger receptor-targeted plaque delivery of microRNA-coated nanoparticles for alleviating atherosclerosis. Proc Natl Acad Sci U S A. 2022;119:e2201443119. doi:10.1073/pnas.2201443119
   PubMed Web of Science ®Google Scholar
• Nakamura M, Kosuge H, Oyane A, Kuroiwa K, Shimizu Y, Aonuma K. In vivostudy of iron oxide-calcium phosphate composite nanoparticles for delivery to atherosclerosis. Nanotechnology. 2021;32. doi:10.1088/1361-6528/ac007d
   Web of Science ®Google Scholar
• Yancy AD, Olzinski AR, Hu TC, et al. Differential uptake of ferumoxtran-10 and ferumoxytol, ultrasmall superparamagnetic iron oxide contrast agents in rabbit: critical determinants of atherosclerotic plaque labeling. J Magn Reson Imaging. 2005;21:432–442. doi:10.1002/jmri.20283
   PubMed Web of Science ®Google Scholar
• Matuszak J, Baumgartner J, Zaloga J, et al. Nanoparticles for intravascular applications: physicochemical characterization and cytotoxicity testing. Nanomedicine. 2016;11:597–616. doi:10.2217/nnm.15.216
   PubMed Web of Science ®Google Scholar
• Matuszak J, Zaloga J, Friedrich RP, et al. Endothelial biocompatibility and accumulation of SPION under flow conditions. J Magn Magn Mater. 2015;380:20–26.
   Web of Science ®Google Scholar
• Cicha I, Beronov K, Ramirez EL, et al. Shear stress preconditioning modulates endothelial susceptibility to circulating TNF-alpha and monocytic cell recruitment in a simplified model of arterial bifurcations. Atherosclerosis. 2009;207:93–102. doi:10.1016/j.atherosclerosis.2009.04.034
   PubMed Web of Science ®Google Scholar
• Diehl KH, Hull R, Morton D, et al. European federation of pharmaceutical industries a, european centre for the validation of alternative M. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J Appl Toxicol. 2001;21:15–23. doi:10.1002/jat.727
   PubMed Web of Science ®Google Scholar
• Constantinides P, Booth J, Carlson G. Production of advanced cholesterol atherosclerosis in the rabbit. Arch Pathol. 1960;70:712–724.
   PubMedGoogle Scholar
• Abela GS, Picon PD, Friedl SE, et al. Triggering of plaque disruption and arterial thrombosis in an atherosclerotic rabbit model. Circulation. 1995;91:776–784. doi:10.1161/01.Cir.91.3.776
   PubMed Web of Science ®Google Scholar
• Phinikaridou A, Hallock KJ, Qiao Y, Hamilton JA. A robust rabbit model of human atherosclerosis and atherothrombosis. J Lipid Res. 2009;50:787–797. doi:10.1194/jlr.M800460-JLR200
   PubMed Web of Science ®Google Scholar
• Matuszak J, Dorfler P, Lyer S, et al. Comparative analysis of nanosystems’ effects on human endothelial and monocytic cell functions. Nanotoxicology. 2018;12:957–974. doi:10.1080/17435390.2018.1502375
   PubMed Web of Science ®Google Scholar
• Matuszak J, Lutz B, Sekita A, et al. Drug delivery to atherosclerotic plaques using superparamagnetic iron oxide nanoparticles. Int J Nanomed. 2018;13:8443–8460. doi:10.2147/IJN.S179273
   PubMed Web of Science ®Google Scholar
• Chao Y, Makale M, Karmali PP, et al. Recognition of dextran-superparamagnetic iron oxide nanoparticle conjugates (Feridex) via macrophage scavenger receptor charged domains. Bioconjug Chem. 2012;23:1003–1009. doi:10.1021/bc200685a
   PubMed Web of Science ®Google Scholar
• Tang TY, Howarth SP, Miller SR, et al. Comparison of the inflammatory burden of truly asymptomatic carotid atheroma with atherosclerotic plaques contralateral to symptomatic carotid stenosis: an ultra small superparamagnetic iron oxide enhanced magnetic resonance study. J Neurol Neurosurg. 2007;78:1337–1343. doi:10.1136/jnnp.2007.118901
   PubMed Web of Science ®Google Scholar
• Tang TY, Howarth SP, Miller SR, et al. Comparison of the inflammatory burden of truly asymptomatic carotid atheroma with atherosclerotic plaques in patients with asymptomatic carotid stenosis undergoing coronary artery bypass grafting: an ultrasmall superparamagnetic iron oxide enhanced magnetic resonance study. Eur J Vasc Endovascular Surg. 2008;35:392–398. doi:10.1016/j.ejvs.2007.10.019
   PubMed Web of Science ®Google Scholar
• Knobloch G, Colgan T, Wiens CN, et al. Relaxivity of Ferumoxytol at 1.5 T and 3.0 T. Invest Radiol. 2018;53:257–263. doi:10.1097/RLI.0000000000000434
   PubMed Web of Science ®Google Scholar
• Weinstein JS, Varallyay CG, Dosa E, et al. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab. 2010;30:15–35. doi:10.1038/jcbfm.2009.192
   PubMed Web of Science ®Google Scholar
• van Hoof RHM, Schreuder F, Nelemans P, et al. Ischemic stroke patients demonstrate increased carotid plaque microvasculature compared to (ocular) transient ischemic attack patients. Cerebrovascular Dis. 2017;44:297–303. doi:10.1159/000481146
   PubMed Web of Science ®Google Scholar
• Cicha I, Worner A, Urschel K, et al. Carotid plaque vulnerability: a positive feedback between hemodynamic and biochemical mechanisms. Stroke. 2011;42:3502–3510. doi:10.1161/STROKEAHA.111.627265
   PubMed Web of Science ®Google Scholar
• Banda NK, Mehta G, Chao Y, et al. Mechanisms of complement activation by dextran-coated superparamagnetic iron oxide (SPIO) nanoworms in mouse versus human serum. Part Fib Toxicol. 2014;11:1–10. doi:10.1186/s12989-014-0064-2
   PubMed Web of Science ®Google Scholar
• Wang G, Chen F, Banda NK, et al. Activation of human complement system by dextran-coated iron oxide nanoparticles is not affected by dextran/Fe ratio, hydroxyl modifications, and crosslinking. Front Immunol. 2016;7:418. doi:10.3389/fimmu.2016.00418
   PubMed Web of Science ®Google Scholar
• Szebeni J, Fishbane S, Hedenus M, et al. Hypersensitivity to intravenous iron: classification, terminology, mechanisms and management. Br. J. Pharmacol. 2015;172:5025–5036. doi:10.1111/bph.13268
   PubMed Web of Science ®Google Scholar
• Smits LP, Coolen BF, Panno MD, et al. Noninvasive differentiation between hepatic steatosis and steatohepatitis with MR imaging enhanced with USPIOs in patients with nonalcoholic fatty liver disease: a proof-of-concept study. Radiology. 2016;278:782–791. doi:10.1148/radiol.2015150952
   PubMed Web of Science ®Google Scholar
• Department of Health and Human Services FaDA. Guidance for Industry: Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. U.S: Department of Health and Human Services FaDA; 2005.
   Google Scholar