Assessment of inflammation with a very small iron-oxide particle in a murine model of reperfused myocardial infarction

Journal of Magnetic Resonance Imaging

Volumn 39, Issue 3, 2014, Pages 598-608

  Protti, Andrea ^a   Dong, Xuebin ^a   Andia, Marcelo E ^a   Yu, Bin ^a   Dokukina, Kate ^a   Chaubey, Sanjay ^a   Phinikaridou, Alkystis ^a   Vizcay Barrena, Gema ^a   Taupitz, Matthias ^b   Botnar, Rene M ^a   Shah, Ajay M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

inflammation; iron particles; MRI; myocardial infarction

Indexed keywords

CONTRAST MEDIUM; FERRIC ION; FERRIC OXIDE;

ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; DIAGNOSTIC USE; DISEASE MODEL; FEMALE; HEART MUSCLE REPERFUSION; INFLAMMATION; INTRAVENOUS DRUG ADMINISTRATION; MOUSE; MYOCARDIAL INFARCTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PROCEDURES; RANDOMIZATION; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY;

ANIMALS; CONTRAST MEDIA; DISEASE MODELS, ANIMAL; FEMALE; FERRIC COMPOUNDS; INFLAMMATION; INJECTIONS, INTRAVENOUS; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION; RANDOM ALLOCATION; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY;

EID: 84894232650     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.24191     Document Type: Article

References (46)

1. Jennings RB, Murry CE, Steenbergen C Jr, Reimer KA,. Development of cell injury in sustained acute ischemia. Circulation 1990; 82 (Suppl): II2-II12.
2. Pfeffer MA, Braunwald E,. Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications. Circulation 1990; 81: 1161-1172.
3. Pfeffer JM, Pfeffer MA, Fletcher PJ, Braunwald E,. Progressive ventricular remodeling in rat with myocardial infarction. Am J Physiol 1991; 260 (Pt 2): H1406-H1414.
4. Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA,. Controversies in ventricular remodelling. Lancet 2006; 367: 356-367.
5. Frangogiannis NG, Smith CW, Entman ML,. The inflammatory response in myocardial infarction. Cardiovasc Res 2002; 53: 31-47.
6. Corot C, Robert P, Idee JM, Port M,. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006; 58: 1471-1504.
7. Nahrendorf M, Pittet MJ, Swirski FK,. Monocytes: protagonists of infarct inflammation and repair after myocardial infarction. Circulation 2010; 121: 2437-2445.
8. Steffens S, Montecucco F, Mach F,. The inflammatory response as a target to reduce myocardial ischaemia and reperfusion injury. Thromb Haemost 2009; 102: 240-247.
9. Touboul P, Andre-Fouet X, Leizorovicz A, et al. Risk stratification after myocardial infarction. A reappraisal in the era of thrombolysis. The Groupe d'Etude du Pronostic de l'Infarctus du Myocarde (GREPI). Eur Heart J 1997; 18: 99-107.
10. Michael LH, Ballantyne CM, Zachariah JP, et al. Myocardial infarction and remodeling in mice: effect of reperfusion. Am J Physiol 1999; 277 (Pt 2): H660-H668.
11. Yang Y, Yanasak N, Schumacher A, Hu TC,. Temporal and noninvasive monitoring of inflammatory-cell infiltration to myocardial infarction sites using micrometer-sized iron oxide particles. Magn Reson Med 2010; 63: 33-40.
12. Sosnovik DE, Nahrendorf M, Deliolanis N, et al. Fluorescence tomography and magnetic resonance imaging of myocardial macrophage infiltration in infarcted myocardium in vivo. Circulation 2007; 115: 1384-1391.
13. Ren G, Dewald O, Frangogiannis NG,. Inflammatory mechanisms in myocardial infarction. Curr Drug Targets Inflamm Allergy 2003; 2: 242-256.
14. Beckmann N, Cannet C, Babin AL, et al. In vivo visualization of macrophage infiltration and activity in inflammation using magnetic resonance imaging. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009; 1: 272-298.
15. Williams JB, Ye Q, Hitchens TK, Kaufman CL, Ho C,. MRI detection of macrophages labeled using micrometer-sized iron oxide particles. J Magn Reson Imaging 2007; 25: 1210-1218.
16. Raynal I, Prigent P, Peyramaure S, Najid A, Rebuzzi C, Corot C,. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles: mechanisms and comparison of ferumoxides and ferumoxtran-10. Invest Radiol 2004; 39: 56-63.
17. Nahrendorf M, Sosnovik DE, French BA, et al. Multimodality cardiovascular molecular imaging, Part II. Circ Cardiovasc Imaging 2009; 2: 56-70.
18. Wiart M, Davoust N, Pialat JB, Berthezene Y, Nighoghossian N,. Magnetic resonance imaging (MRI) of inflammation in stroke. Conf Proc IEEE Eng Med Biol Soc 2007; 2007: 4316-4319.
19. Modo M, Hoehn M, Bulte JW,. Cellular MR imaging. Mol Imaging 2005; 4: 143-164.
20. 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.
21. Makowski MR, Varma G, Wiethoff AJ, et al. Noninvasive assessment of atherosclerotic plaque progression in ApoE-/- mice using susceptibility gradient mapping. Circ Cardiovasc Imaging 2011; 4: 295-303.
22. Corot C, Petry KG, Trivedi R, et al. Macrophage imaging in central nervous system and in carotid atherosclerotic plaque using ultrasmall superparamagnetic iron oxide in magnetic resonance imaging. Invest Radiol 2004; 39: 619-625.
23. Rausch M, Sauter A, Frohlich J, Neubacher U, Radu EW, Rudin M,. Dynamic patterns of USPIO enhancement can be observed in macrophages after ischemic brain damage. Magn Reson Med 2001; 46: 1018-1022.
24. Kleinschnitz C, Bendszus M, Frank M, Solymosi L, Toyka KV, Stoll G,. In vivo monitoring of macrophage infiltration in experimental ischemic brain lesions by magnetic resonance imaging. J Cereb Blood Flow Metab 2003; 23: 1356-1361.
25. Gaglia JL, Guimaraes AR, Harisinghani M, et al. Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest 2011; 121: 442-445.
26. Denis MC, Mahmood U, Benoist C, Mathis D, Weissleder R,. Imaging inflammation of the pancreatic islets in type 1 diabetes. Proc Natl Acad Sci U S A 2004; 101: 12634-12639.
27. Bulte JW, Kraitchman DL,. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004; 17: 484-499.
28. Kustermann E, Roell W, Breitbach M, et al. Stem cell implantation in ischemic mouse heart: a high-resolution magnetic resonance imaging investigation. NMR Biomed 2005; 18: 362-370.
29. Montet-Abou K, Daire JL, Hyacinthe JN, et al. In vivo labelling of resting monocytes in the reticuloendothelial system with fluorescent iron oxide nanoparticles prior to injury reveals that they are mobilized to infarcted myocardium. Eur Heart J 2010; 31: 1410-1420.
30. 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.
31. Taupitz M, Schnorr J, Abramjuk C, et al. New generation of monomer-stabilized very small superparamagnetic iron oxide particles (VSOP) as contrast medium for MR angiography: preclinical results in rats and rabbits. J Magn Reson Imaging 2000; 12: 905-911.
32. Wagner S, Schnorr J, Pilgrimm H, Hamm B, Taupitz M,. Monomer-coated very small superparamagnetic iron oxide particles as contrast medium for magnetic resonance imaging: preclinical in vivo characterization. Invest Radiol 2002; 37: 167-177.
33. Renshaw PF, Owen CS, McLaughlin AC, Frey TG, Leigh JS Jr,. Ferromagnetic contrast agents: a new approach. Magn Reson Med 1986; 3: 217-225.
34. Michael LH, Entman ML, Hartley CJ, et al. Myocardial ischemia and reperfusion: a murine model. Am J Physiol 1995; 269 (Pt 2): H2147-H2154.
35. Looi YH, Grieve DJ, Siva A, et al. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 2008; 51: 319-325.
36. Protti A, Sirker A, Shah AM, Botnar R,. Late gadolinium enhancement of acute myocardial infarction in mice at 7T: cine-FLASH versus inversion recovery. J Magn Reson Imaging 2010; 32: 878-886.
37. Schneider JE, Wiesmann F, Lygate CA, Neubauer S,. How to perform an accurate assessment of cardiac function in mice using high-resolution magnetic resonance imaging. J Cardiovasc Magn Reson 2006; 8: 693-701.
38. Franco F, Thomas GD, Giroir B, et al. Magnetic resonance imaging and invasive evaluation of development of heart failure in transgenic mice with myocardial expression of tumor necrosis factor-alpha. Circulation 1999; 99: 448-454.
39. Albert B, Johnson A, Lewis J, Raff M, Robert K, Walter P,. Molecular biology of the cell. New York: Garland Science; 2008.
40. Swirski FK, Nahrendorf M, Etzrodt M, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009; 325: 612-616.
41. 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: 1190-1197.
42. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007; 204: 3037-3047.
43. Geissmann F, Jung S, Littman DR,. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19: 71-82.
44. Levy M, Lagarde F, Maraloiu VA, et al. Degradability of superparamagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties. Nanotechnology 2010; 21: 395103.
45. Ishida M, Ichihara T, Nagata M, et al. Quantification of myocardial blood flow using model based analysis of first-pass perfusion MRI: extraction fraction of Gd-DTPA varies with myocardial blood flow in human myocardium. Magn Reson Med 2011; 66: 1391-1399.
46. Bettencourt N, Chiribiri A, Schuster A, Nagel E,. Assessment of myocardial ischemia and viability using cardiac magnetic resonance. Curr Heart Fail Reports 2009; 6: 142-153.