Dual manganese-enhanced and delayed gadolinium-enhanced mri detects myocardial border zone injury in a pig ischemia-reperfusion model

Circulation: Cardiovascular Imaging

Volumn 4, Issue 5, 2011, Pages 574-582

  Dash, Rajesh ^a   Chung, Jaehoon ^a   Ikeno, Fumiaki ^a   Hahn Windgassen, Annett ^a   Matsuura, Yuka ^a   Bennett, Mihoko V ^b   Lyons, Jennifer K ^a   Teramoto, Tomohiko ^a   Robbins, Robert C ^c   McConnell, Michael V ^a,d   Yeung, Alan C ^a   Brinton, Todd J ^a   Harnish, Phillip P ^e   Yang, Phillip C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Division of Immunology and Rheumatology   (United States)

^c STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^d Stanford University   (United States)

^e Eagle Vision Pharmaceutical Corporation   (United States)

Author keywords

Cell viability; Gadolinium; Ischemia reperfusion injury; Magnetic resonance imaging; Manganese

Indexed keywords

EVP 10011; GADOLINIUM; GADOLINIUM PENTETATE; MANGANESE; TRIPHENYLTETRAZOLIUM; UNCLASSIFIED DRUG; CONTRAST MEDIUM; DIAGNOSTIC AGENT; RADIOISOTOPE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; ELECTRON MICROSCOPY; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HISTOPATHOLOGY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REPERFUSION INJURY; SWINE; ANIMAL; COMPARATIVE STUDY; DIFFERENTIAL DIAGNOSIS; DISEASE MODEL; HEART MUSCLE; HOSPITALIZATION; INTRAVENOUS DRUG ADMINISTRATION; METHODOLOGY; PATHOLOGY; REPRODUCIBILITY;

ANIMALS; CONTRAST MEDIA; DIAGNOSIS, DIFFERENTIAL; DISEASE MODELS, ANIMAL; GADOLINIUM DTPA; INJECTIONS, INTRAVENOUS; MAGNETIC RESONANCE IMAGING, CINE; MANGANESE; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; RADIOISOTOPES; REPRODUCIBILITY OF RESULTS; SEVERITY OF ILLNESS INDEX; SWINE;

EID: 80555157644     PISSN: 19419651     EISSN: 19420080     Source Type: Journal    
DOI: 10.1161/CIRCIMAGING.110.960591     Document Type: Article

References (51)

1. Cameron A, Davis KB, Green G, Schaff HV. Coronary bypass surgery with internal-thoracic-artery grafts- effects on survival over a 15-year period. N Engl J Med. 1996;334:216-219. (Pubitemid 26030671)
2. Cameron AA, Green GE, Brogno DA, Thornton J. Internal thoracic artery grafts: 20-year clinical follow-up. J Am Coll Cardiol. 1995;25:188-192.
3. Fitzgibbon GM, Kafka HP, Leach AJ, Keon WJ, Hooper GD, Burton JR. Coronary bypass graft fate and patient outcome: angiographic follow-up of 5,065 grafts related to survival and reoperation in 1,388 patients during 25 years. J Am Coll Cardiol. 1996;28:616-626. (Pubitemid 26288642)
4. Lytle BW, Cosgrove DM, Loop FD, Borsh J, Goormastic M, Taylor PC. Perioperative risk of bilateral internal mammary artery grafting: analysis of 500 cases from 1971 to 1984. Circulation. 1986;74:III37-III41.
5. Kanderian AS, Renapurkar R, Flamm SD. Myocardial viability and revascularization. Heart Fail Clin. 2009;5:333-348.
6. Hillenbrand HB, Kim RJ, Parker MA, Fieno DS, Judd RM. Early assessment of myocardial salvage by contrast-enhanced magnetic resonance imaging. Circulation. 2000;102:1678-1683.
7. Rogers WJ Jr, Kramer CM, Geskin G, Hu YL, Theobald TM, Vido DA, Petruolo S, Reichek N. Early contrast-enhanced MRI predicts late functional recovery after reperfused myocardial infarction. Circulation. 1999; 99:744-750. (Pubitemid 29083013)
8. Fieno DS, Kim RJ, Chen EL, Lomasney JW, Klocke FJ, Judd RM. Contrast-enhanced magnetic resonance imaging of myocardium at risk: distinction between reversible and irreversible injury throughout infarct healing. J Am Coll Cardiol. 2000;36:1985-1991.
9. Suranyi P, Kiss P, Brott BC, Simor T, Elgavish A, Ruzsics B, Saab-Ismail NH, Elgavish GA. Percent infarct mapping: an R1-map-based CE-MRI method for determining myocardial viability distribution. Magn Reson Med. 2006;56:535-545. (Pubitemid 44338872)
10. Judd RM, Lugo-Olivieri CH, Arai M, Kondo T, Croisille P, Lima JA, Mohan V, Becker LC, Zerhouni EA. Physiological basis of myocardial contrast enhancement in fast magnetic resonance images of 2-day-old reperfused canine infarcts. Circulation. 1995;92:1902-1910.
11. Saeed M, Bremerich J, Wendland MF, Wyttenbach R, Weinmann HJ, Higgins CB. Reperfused myocardial infarction as seen with use of necrosis-specific versus standard extracellular MR contrast media in rats. Radiology. 1999;213:247-257. (Pubitemid 29470434)
12. Saeed M, Lund G, Wendland MF, Bremerich J, Weinmann H, Higgins CB. Magnetic resonance characterization of the peri-infarction zone of reperfused myocardial infarction with necrosis-specific and extracellular nonspecific contrast media. Circulation. 2001;103:871-876. (Pubitemid 32163887)
13. Amado LC, Gerber BL, Gupta SN, Rettmann DW, Szarf G, Schock R, Nasir K, Kraitchman DL, Lima JA. Accurate and objective infarct sizing by contrast-enhanced magnetic resonance imaging in a canine myocardial infarction model. J Am Coll Cardiol. 2004;44:2383-2389. (Pubitemid 39647614)
14. Fenster BE, Chan FP, Valentine HA, Yang E, McConnell MV, Berry GJ, Yang PC. Images in cardiovascular medicine. Cardiac magnetic resonance imaging for myocarditis: effective use in medical decision making. Circulation. 2006;113:e842-e843. (Pubitemid 43947998)
15. Eitel I, Behrendt F, Schindler K, Kivelitz D, Gutberlet M, Schuler G, Thiele H. Differential diagnosis of suspected apical ballooning syndrome enhanced magnetic resonance imaging. Eur Heart J. 2008; 29:2651-2659.
16. Haghi D, Fluechter S, Suselbeck T, Borggrefe M, Papavassiliu T. Delayed hyperenhancement in a case of Takotsubo cardiomyopathy. J Cardiovasc Magn Reson. 2005;7:845-847. (Pubitemid 41770065)
17. Syed IS, Martinez MW, Feng DL, Glockner JF. Cardiac magnetic resonance imaging of eosinophilic endomyocardial disease. Int J Cardiol. 2008;126:e50-e52. (Pubitemid 351636340)
18. Yamada M, Gurney PT, Chung J, Kundu P, Drukker M, Smith AK, Weissman IL, Nishimura D, Robbins RC, Yang PC. Manganese-guided cellular MRI of human embryonic stem cell and human bone marrow stromal cell viability. Magn Reson Med. 2009;62:1047-1054.
19. Bruvold M, Nordhoy W, Anthonsen HW, Brurok H, Jynge P. Manganesecalcium interactions with contrast media for cardiac magnetic resonance imaging: a study of manganese chloride supplemented with calcium gluconate in isolated guinea pig hearts. Invest Radiol. 2005;40:117-125. (Pubitemid 40289438)
20. Mendonca-Dias MH, Gaggelli E, Lauterbur PC. Paramagnetic contrast agents in nuclear magnetic resonance medical imaging. Semin Nucl Med. 1983;13:364-376.
21. Wendland MF. Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to imaging of the heart. NMR Biomed. 2004;17: 581-594. (Pubitemid 40124783)
22. Storey P, Danias PG, Post M, Li W, Seoane PR, Harnish PP, Edelman RR, Prasad PV. Preliminary evaluation of EVP 1001-1: a new cardiacspecific magnetic resonance contrast agent with kinetics suitable for steady-state imaging of the ischemic heart. Invest Radiol. 2003;38: 642-652. (Pubitemid 37140287)
23. Storey P, Chen Q, Li W, Seoane PR, Harnish PP, Fogelson L, Harris KR, Prasad PV. Magnetic resonance imaging of myocardial infarction using a manganese-based contrast agent (EVP 1001-1): preliminary results in a dog model. J Magn Reson Imaging. 2006;23:228-234. (Pubitemid 43191079)
24. Delattre BM, Braunersreuther V, Hyacinthe JN, Crowe LA, Mach F, Vallee JP. Myocardial infarction quantification with manganeseenhanced MRI (MEMRI) in mice using a 3T clinical scanner. NMR Biomed. 2010;23:503-513.
25. Kaneda H, Ikeno F, Inagaki K, Mochly-Rosen D. Preserved coronary endothelial function by inhibition of delta protein kinase C in a porcine acute myocardial infarction model. Int J Cardiol. 2009;133:256-259.
26. Suzuki Y, Lyons JK, Yeung AC, Ikeno F. The porcine restenosis model using thermal balloon injury: comparison with the model by coronary stenting. J Invasive Cardiol. 2008;20:142-146. (Pubitemid 351346276)
27. Heidary S, Patel H, Chung J, Yokota H, Gupta SN, Bennett MV, Katikireddy C, Nguyen P, Pauly JM, Terashima M, McConnell MV, Yang PC. Quantitative tissue characterization of infarct core and border zone in patients with ischemic cardiomyopathy by magnetic resonance is associated with future cardiovascular events. J Am Coll Cardiol. 2010; 55:2762-2768.
28. Klein HH, Puschmann S, Schaper J, Schaper W. The Mechanism of the Tetrazolium Reaction in Identifying Experimental Myocardial Infarction. Virchows Archiv. 1981;393:287-297. (Pubitemid 11031537)
29. Misfeld M, Szabo K, Kraatz EG, Grossherr M, Schmidtke C, Pilgrim M, Kuhnel W, Sievers HH. Electron-microscopic findings after transmyocardial laser revascularization in an acute ischemic pig model. Eur J Cardiothorac Surg. 1998;13:398-403. (Pubitemid 28231350)
30. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res. 1999;8:135-160. (Pubitemid 29425900)
31. Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, O'Donnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y. Heart disease and stroke statistics-2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2009;119:480-486.
32. Mielniczuk LM, Lamas GA, Flaker GC, Mitchell G, Smith SC, Gersh BJ, Solomon SD, Moye LA, Rouleau JL, Rutherford JD, Pfeffer MA. Left ventricular end-diastolic pressure and risk of subsequent heart failure in patients following an acute myocardial infarction. Congest Heart Fail. 2007;13:209-214.
33. Olivetti G, Quaini F, Sala R, Lagrasta C, Corradi D, Bonacina E, Gambert SR, Cigola E, Anversa P. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol. 1996;28:2005-2016. (Pubitemid 26340560)
34. van den Borne SW, Isobe S, Zandbergen HR, Li P, Petrov A, Wong ND, Fujimoto S, Fujimoto A, Lovhaug D, Smits JF, Daemen MJ, Blankesteijn WM, Reutelingsperger C, Zannad F, Narula N, Vannan MA, Pitt B, Hofstra L, Narula J. Molecular imaging for efficacy of pharmacologic intervention in myocardial remodeling. J Am Coll Cardiol Cardiovasc Imaging. 2009;2:187-198.
35. Misra P, Lebeche D, Ly H, Schwarzkopf M, Diaz G, Hajjar RJ, Schecter AD, Frangioni JV. Quantitation of CXCR4 expression in myocardial infarction using 99mTc-labeled SDF-1alpha. J Nucl Med. 2008;49: 963-969. (Pubitemid 351793437)
36. Zhao M, Zhu X, Ji S, Zhou J, Ozker KS, Fang W, Molthen RC, Hellman RS. 99mTc-labeled C2A domain of synaptotagmin I as a target-specific molecular probe for noninvasive imaging of acute myocardial infarction. J Nucl Med. 2006;47:1367-1374. (Pubitemid 47544893)
37. Beller GA, Smith TW, Hood WB Jr. Effects of ischemia and coronary reperfusion on myocardial digoxin uptake. Am J Cardiol. 1975;36: 902-907.
38. Kenis H, Zandbergen HR, Hofstra L, Petrov AD, Dumont EA, Blankenberg FD, Haider N, Bitsch N, Gijbels M, Verjans JW, Narula N, Narula J, Reutelingsperger CP. Annexin A5 uptake in ischemic myocardium: demonstration of reversible phosphatidylserine externalization and feasibility of radionuclide imaging. J Nucl Med. 2010;51: 259-267.
39. Flett AS, Hasleton J, Cook C, Hausenloy D, Quarta G, Ariti C, Muthurangu V, Moon JC. Evaluation of techniques for the quantification of myocardial scar of differing etiology using cardiac magnetic resonance. J Am Coll Cardiol Cardiovasc Imaging. 2011;4:150-156.
40. Harrigan CJ, Peters DC, Gibson CM, Maron BJ, Manning WJ, Maron MS, Appelbaum E. Hypertrophic cardiomyopathy: quantification of late gadolinium enhancement with contrast-enhanced cardiovascular MR imaging. Radiology. 2011;258:128-133.
41. Silva AC, Lee JH, Aoki I, Koretsky AP. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 2004;17:532-543. (Pubitemid 40124779)
42. Federle M, Chezmar J, Rubin DL, Weinreb J, Freeny P, Schmiedl UP, Brown JJ, Borrello JA, Lee JK, Semelka RC, Mattrey R, Dachman AH, Saini S, Harms SE, Mitchell DG, Anderson MW, Halford HH III, Bennett WF, Young SW, Rifkin M, Gay SB, Ballerini R, Sherwin PF, Robison RO. Efficacy and safety of mangafodipir trisodium (MnDPDP) injection for hepatic MRI in adults: results of the U.S. multicenter phase III clinical trials. Efficacy of early imaging. J Magn Reson Imaging. 2000;12: 689-701.
43. Cury RC, Shash K, Nagurney JT, Rosito G, Shapiro MD, Nomura CH, Abbara S, Bamberg F, Ferencik M, Schmidt EJ, Brown DF, Hoffmann U, Brady TJ. Cardiac magnetic resonance with T2-weighted imaging improves detection of patients with acute coronary syndrome in the emergency department. Circulation. 2008;118:837-844.
44. Edwards NC, Routledge H, Steeds RP. T2-weighted magnetic resonance imaging to assess myocardial oedema in ischaemic heart disease. Heart. 2009;95:1357-1361.
45. Raman SV, Simonetti OP, Winner MW III, Dickerson JA, He X, Mazzaferri EL Jr, Ambrosio G. Cardiac magnetic resonance with edema imaging identifies myocardium at risk and predicts worse outcome in patients with non-ST-segment elevation acute coronary syndrome. J Am Coll Cardiol. 2010;55:2480-2488.
46. Schulz-Menger J, Gross M, Messroghli D, Uhlich F, Dietz R, Friedrich MG. Cardiovascular magnetic resonance of acute myocardial infarction at a very early stage. J Am Coll Cardiol. 2003;42:513-518. (Pubitemid 36951720)
47. Nilsson JC, Nielsen G, Groenning BA, Fritz-Hansen T, Sondergaard L, Jensen GB, Larsson HB. Sustained postinfarction myocardial oedema in humans visualised by magnetic resonance imaging. Heart. 2001;85: 639-642. (Pubitemid 32973458)
48. Ripa RS, Nilsson JC, Wang Y, Sondergaard L, Jorgensen E, Kastrup J. Short- and long-term changes in myocardial function, morphology, edema, and infarct mass after ST-segment elevation myocardial infarction evaluated by serial magnetic resonance imaging. Am Heart J. 2007;154: 929-936. (Pubitemid 47632488)
49. Dall'armellina E, Karia N, Lindsay AC, Karamitsos TD, Ferreira V, Robson MD, Kellman P, Francis JM, Forfar C, Prendergast B, Banning AP, Channon KM, Kharbanda RK, Neubauer S, Choudhury RP.Dynamic changes of edema and late gadolinium enhancement after acute myocardial infarction and their relationship to functional recovery and salvage index. Circ Cardiovasc Imaging. 2011;4:228-236.
50. Payne AR, Casey M, McClure J, McGeoch R, Murphy A, Woodward R, Saul A, Bi X, Zuehlsdorff S, Oldroyd KG, Tzemos N, Berry C. Bright blood T2 weighted MRI has higher diagnostic accuracy than dark blood STIR MRI for detection of acute myocardial infarction and for assessment of the ischemic area-at-risk and myocardial salvage. Circ Cardiovasc Imaging. 2011;4:210-219.
51. Schmidt A, Azevedo CF, Cheng A, Gupta SN, Bluemke DA, Foo TK, Gerstenblith G, Weiss RG, Marban E, Tomaselli GF, Lima JA, Wu KC. Infarct tissue heterogeneity by magnetic resonance imaging identifies enhanced cardiac arrhythmia susceptibility in patients with left ventricular dysfunction. Circulation. 2007;115:2006 -2014. (Pubitemid 46625951)