Molecular imaging of myocardial necrosis: an updated mini-review

References

• Roth GA, Johnson C, Abajobir A, et al. Global, regional, and national burden of cardiovascular diseases for 10 causes, 1990 to 2015. J Am Coll Cardiol. 2017;70(1):1–25.
   PubMed Web of Science ®Google Scholar
• Mozaffarian D. Global scourge of cardiovascular disease: time for health care systems reform and precision population health. J Am Coll Cardiol. 2017;70(1):26–28.
   PubMed Web of Science ®Google Scholar
• Anderson JL, Morrow DA. Acute myocardial infarction. N Engl J Med. 2017;376(21):2053–2064.
   PubMed Web of Science ®Google Scholar
• Reed GW, Rossi JE, Cannon CP. Acute myocardial infarction. Lancet. 2017;389(10065):197–210.
   PubMed Web of Science ®Google Scholar
• Heusch G, Gersh BJ. The pathophysiology of acute myocardial infarction and strategies of protection beyond reperfusion: a continual challenge. Eur Heart J. 2017;38(11):774–784.
   PubMed Web of Science ®Google Scholar
• Re DPD, Amgalan D, Linkermann A, et al. Fundamental mechanisms of regulated cell death and implications for heart disease. Physiol Rev. 2019;99:1765–1817.
   PubMed Web of Science ®Google Scholar
• Ibáñez B, Heusch G, Ovize M, et al. Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol. 2015;65(14):1454–1471.
   PubMed Web of Science ®Google Scholar
• Ma S, Wang Y, Chen Y, et al. The role of the autophagy in myocardial ischemia/reperfusion injury. Biochim Biophys Acta. 2015;1852(2):271–276.
   PubMed Web of Science ®Google Scholar
• Chiong M, Wang ZV, Pedrozo Z, et al. Cardiomyocyte death: mechanisms and translational implications. Cell Death Dis. 2011;2(12):e244–e244.
   PubMedGoogle Scholar
• Davidson SM, Ferdinandy P, Andreadou I, et al. Multitarget strategies to reduce myocardial ischemia/reperfusion injury: JACC review topic of the week. J Am Coll Cardiol. 2019;73(1):89–99.
   PubMed Web of Science ®Google Scholar
• Flotats A, Carrio I. Non-invasive in vivo imaging of myocardial apoptosis and necrosis. Eur J Nucl Med Mol Imaging. 2003;30(4):615–630.
   PubMed Web of Science ®Google Scholar
• Jivraj N, Phinikaridou A, Shah AM, et al. Molecular imaging of myocardial infarction. Basic Res Cardiol. 2014;109(1):397.
   PubMed Web of Science ®Google Scholar
• Shekhar A, Heeger P, Reutelingsperger C, et al. Targeted imaging for cell death in cardiovascular disorders. JACC Cardiovasc Imaging. 2018;11(3):476–493.
   PubMed Web of Science ®Google Scholar
• Boutagy NE, Feher A, Alkhalil I, et al. Molecular imaging of the heart. Compr Physiol. 2019;9(2):477–533.
   PubMed Web of Science ®Google Scholar
• Golestani R, Wu C, Tio RA, et al. Small-animal SPECT and SPECT/CT: application in cardiovascular research. Eur J Nucl Med Mol Imaging. 2010;37(9):1766–1777.
   PubMed Web of Science ®Google Scholar
• De Saint-Hubert M, Prinsen K, Mortelmans L, et al. Molecular imaging of cell death. Methods. 2009;48(2):178–187.
   PubMed Web of Science ®Google Scholar
• Cona MM, Oyen R, Ni Y. Necrosis avidity of organic compounds: a natural phenomenon with exploitable theragnostic potentials. CMC. 2015;22(15):1829–1849.
   PubMed Web of Science ®Google Scholar
• Zhang D, Gao M, Jin Q, et al. Updated developments on molecular imaging and therapeutic strategies directed against necrosis. Acta Pharm Sin B. 2019;9(3):455–468.
   PubMed Web of Science ®Google Scholar
• James ML, Gambhir SS. A molecular imaging primer: modalities, imaging agents, and applications. Physiol Rev. 2012;92(2):897–965.
   PubMed Web of Science ®Google Scholar
• Skinner JS, Smeeth L, Kendall JM, et al. NICE guidance. Chest pain of recent onset: assessment and diagnosis of recent onset chest pain or discomfort of suspected cardiac origin. Heart. 2010;96(12):974–978.
   PubMed Web of Science ®Google Scholar
• Fox K, Angeles Alonso Garcia M, Ardissino D, et al. Guidelines on the management of stable angina pectoris: executive summary: The Task Force on the Management of Stable Angina Pectoris of the European Society of Cardiology. Eur Heart J. 2006;27(11):1341–1381.
   PubMed Web of Science ®Google Scholar
• Beller GA, Heede RC. SPECT imaging for detecting coronary artery disease and determining prognosis by noninvasive assessment of myocardial perfusion and myocardial viability. J Cardiovasc Trans Res. 2011;4(4):416–424.
   PubMed Web of Science ®Google Scholar
• Underwood SR, Anagnostopoulos C, Cerqueira M, et al. Myocardial perfusion scintigraphy: the evidence. Eur J Nucl Med Mol Imaging. 2004;31(2):261–291.
   PubMed Web of Science ®Google Scholar
• Nudi F, Di Belardino N, Pinto A, et al. Assessment of the fate of myocardial necrosis by serial myocardial perfusion imaging. J Nucl Cardiol. 2018;25(2):496–505.
   PubMed Web of Science ®Google Scholar
• Morrison AR, Sinusas AJ. Advances in radionuclide molecular imaging in myocardial biology. J Nucl Cardiol. 2010;17(1):116–134.
   PubMed Web of Science ®Google Scholar
• Ni YC, Bormans G, Chen F, et al. Necrosis avid contrast agents: functional similarity versus structural diversity. Invest Radiol. 2005;40(8):526–535.
   PubMed Web of Science ®Google Scholar
• Ni Y. Metalloporphyrins and functional analogues as MRI contrast agents. CMIR. 2008;4(2):96–112.
   Web of Science ®Google Scholar
• Ni Y, Huyghe D, Verbeke K, et al. First preclinical evaluation of mono-[123I]iodohypericin as a necrosis-avid tracer agent. Eur J Nucl Med Mol Imaging. 2006;33(5):595–601.
   PubMed Web of Science ®Google Scholar
• Fonge H, Vunckx K, Wang H, et al. Non-invasive detection and quantification of acute myocardial infarction in rabbits using mono-[123I]iodohypericin microSPECT. Eur Heart J. 2007;29(2):260–269.
   PubMed Web of Science ®Google Scholar
• Feng Y, Cona MM, Vunckx K, et al. Detection and quantification of acute reperfused myocardial infarction in rabbits using DISA-SPECT/CT and 3.0 T cardiac MRI. Int J Cardiol. 2013;168(4):4191–4198.
   PubMed Web of Science ®Google Scholar
• Cona MM, Feng Y, Li Y, et al. Comparative study of iodine-123-labeled-hypericin and Tc-99m-labeled-hexakis [2-methoxyisobutylisonitril] in a rabbit model of myocardial infarction. J Cardiovasc Pharm. 2013;62(3):304–311.
   PubMed Web of Science ®Google Scholar
• Li J, Zhang J, Yang S, et al. Synthesis and preclinical evaluation of radioiodinated hypericin dicarboxylic acid as a necrosis avid agent in rat models of induced hepatic, muscular, and myocardial necroses. Mol Pharm. 2016;13(1):232–240.
   PubMed Web of Science ®Google Scholar
• Duan X, Yin Z, Jiang C, et al. Radioiodinated hypericin disulfonic acid sodium salts as a DNA-binding probe for early imaging of necrotic myocardium. Eur J Pharm Biopharm. 2017;117:151–159.
   PubMed Web of Science ®Google Scholar
• Ishikawa M, Hashimoto Y. Improvement in aqueous solubility in small molecule drug discovery programs by disruption of molecular planarity and symmetry. J Med Chem. 2011;54(6):1539–1554.
   PubMed Web of Science ®Google Scholar
• Lewin G, Maciuk A, Moncomble A, et al. Enhancement of the water solubility of flavone glycosides by disruption of molecular planarity of the aglycone moiety. J Nat Prod. 2013;76(1):8–12.
   PubMed Web of Science ®Google Scholar
• Chen Z, Baumeister U, Tschierske C, et al. Effect of core twisting on self-assembly and optical properties of perylene bisimide dyes in solution and columnar liquid crystalline phases. Chem Eur J. 2007;13(2):450–465.
   PubMed Web of Science ®Google Scholar
• Chen Z, Lohr A, Saha-Moeller CR, et al. Self-assembled pi-stacks of functional dyes in solution: structural and thermodynamic features. Chem Soc Rev. 2009;38(2):564–584.
   PubMed Web of Science ®Google Scholar
• Jin Q, Zhao J, Gao M, et al. Evaluation of necrosis avidity and potential for rapid imaging of necrotic myocardium of radioiodinated hypocrellins. Mol Imaging Biol. 2018;20(4):551–561.
   PubMed Web of Science ®Google Scholar
• Wang Q, Yang S, Jiang C, et al. Discovery of radioiodinated monomeric anthraquinones as a novel class of necrosis avid agents for early imaging of necrotic myocardium. Sci Rep. 2016;6(1):21341.
   PubMed Web of Science ®Google Scholar
• Su C, Zhang D, Bao N, et al. Evaluation of radioiodinated 1, 4-naphthoquinones as necrosis avid agents for rapid myocardium necrosis imaging. Mol Imaging Biol. 2018;20(1):74–84.
   PubMed Web of Science ®Google Scholar
• Luo Q, Jin Q, Su C, et al. Radiolabeled rhein as small-molecule necrosis avid agents for imaging of necrotic myocardium. Anal Chem. 2017;89(2):1260–1266.
   PubMed Web of Science ®Google Scholar
• Liang J, Luo Q, Zhang D, et al. SPECT imaging of treatment-related tumor necrosis using technetium-99m-labeled rhein. Mol Imaging Biol. 2019;21(4):660–668.
   PubMed Web of Science ®Google Scholar
• Jin Q, Jiang C, Gao M, et al. Target exploration of rhein as a small-molecule necrosis avid agent by post-treatment click modification. New J Chem. 2019;43(16):6121–6125.
   Web of Science ®Google Scholar
• Zhang D, Huang D, Ji Y, et al. Experimental evaluation of radioiodinated sennoside B as a necrosis-avid tracer agent. J Drug Target. 2015;23(2):180–190.
   PubMed Web of Science ®Google Scholar
• Jiang C, Gao M, Li Y, et al. Exploring diagnostic potentials of radioiodinated sennidin A in rat model of reperfused myocardial infarction. Int J Pharm. 2015;495(1):31–40.
   PubMed Web of Science ®Google Scholar
• Li L, Zhang D, Yang S, et al. Effects of glycosylation on biodistribution and imaging quality of necrotic myocardium of iodine-131-labeled sennidins. Mol Imaging Biol. 2016;18(6):877–886.
   PubMed Web of Science ®Google Scholar
• Ma L, Cai L, Jin Q, et al. Evaluation of necrosis avidity of radioiodinated 5-hydroxytryptophan and its potential applications in myocardial infarction imaging. Chinese Chem Lett. 2019;30(1):83–86.
   Web of Science ®Google Scholar
• Park D, Don AS, Massamiri T, et al. Noninvasive imaging of cell death using an Hsp90 ligand. J Am Chem Soc. 2011;133(9):2832–2835.
   PubMed Web of Science ®Google Scholar
• Tahara N, Zandbergen HR, de Haas HJ, et al. Noninvasive molecular imaging of cell death in myocardial infarction using 111In-GSAO. Sci Rep. 2015;4(1):6826.
   Google Scholar
• Yamaki T, de Haas HJ, Tahara N, et al. Cardioprotection by minocycline in a rabbit model of ischemia/reperfusion injury: Detection of cell death by in vivo 111In-GSAO SPECT. J Nucl Cardiol. 2018;25(1):94–100.
   PubMed Web of Science ®Google Scholar
• Ji A-Y, Jin Q-M, Zhang D-J, et al. Novel 18F-labeled 1-hydroxyanthraquinone derivatives for necrotic myocardium imaging. ACS Med Chem Lett. 2017;8(2):191–195.
   PubMed Web of Science ®Google Scholar
• Khaw BA, Nakazawa A, Odonnell SM, et al. Avidity of technetium 99m glucarate for the necrotic myocardium: in vivo and in vitro assessment. J Nucl Cardiol. 1997;4(4):283–290.
   PubMed Web of Science ®Google Scholar
• Narula J, Petrov A, Pak KY, et al. Very early noninvasive detection of acute experimental nonreperfused myocardial infarction with Tc-99m-labeled glucarate. Circulation. 1997;95(6):1577–1584.
   PubMed Web of Science ®Google Scholar
• Beanlands RSB, Ruddy TD, Bielawski L, et al. Differentiation of myocardial ischemia and necrosis by technetium 99m glucaric acid kinetics. J Nucl Cardiol. 1997;4(4):274–282.
   PubMed Web of Science ®Google Scholar
• Mariani G, Villa G, Rossettin PF, et al. Detection of acute myocardial infarction by 99mTc-labeled D-glucaric acid imaging in patients with acute chest pain. J Nucl Med. 1999;40(11):1832–1839.
   PubMed Web of Science ®Google Scholar
• Johnson LL, Schofield L, Mastrofrancesco P, et al. Technetium-99m glucarate uptake in a swine model of limited flow plus increased demand. J Nucl Cardiol. 2000;7(6):590–598.
   PubMed Web of Science ®Google Scholar
• Khaw B, Silva J, Petrov A, et al. Indium 111 antimyosin and Tc-99m glucaric acid for noninvasive identification of oncotic and apoptotic myocardial necrosis. J Nucl Cardiol. 2002;9(5):471–481.
   PubMed Web of Science ®Google Scholar
• Okada DR, Johnson G, Liu Z, et al. Early detection of infarct in reperfused canine myocardium using 99mTc-glucarate. J Nucl Med. 2004;45(4):655–664.
   PubMed Web of Science ®Google Scholar
• Liu Z, Barrett HH, Stevenson GD, et al. High-resolution imaging with 99mTc-glucarate for assessing myocardial injury in rat heart models exposed to different durations of ischemia with reperfusion. J Nucl Med. 2004;45(7):1251–1259.
   PubMed Web of Science ®Google Scholar
• Johnson G, Okada CC, Hocherman SD, et al. 99mTc-glucarate imaging for the early detection of infarct in partially reperfused canine myocardium. Eur J Nucl Med Mol Imaging. 2006;33(3):319–328.
   PubMed Web of Science ®Google Scholar
• Liu Z, Barrett HH, Stevenson GD, et al. Evaluating the protective role of ischaemic preconditioning in rat hearts using a stationary small-animal SPECT imager and 99mTc-glucarate. Nucl Med Commun. 2008;29(2):120–128.
   PubMed Web of Science ®Google Scholar
• Okada DR, Liu Z, Johnson G, et al. 99mTc-glucarate kinetics differentiate normal, stunned, hibernating, and nonviable myocardium in a perfused rat heart model. Eur J Nucl Med Mol Imaging. 2010;37(10):1909–1917.
   PubMed Web of Science ®Google Scholar
• Houson HA, Nkepang GN, Hedrick AF, et al. Imaging of isoproterenol-induced myocardial injury with 18F labeled fluoroglucaric acid in a rat model. Nucl Med Biol. 2018;59:9–15.
   PubMed Web of Science ®Google Scholar
• Buckert D, Kelle S, Buss S, et al. Left ventricular ejection fraction and presence of myocardial necrosis assessed by cardiac magnetic resonance imaging correctly risk stratify patients with stable coronary artery disease: a multi-center all-comers trial. Clin Res Cardiol. 2017;106(3):219–229.
   PubMed Web of Science ®Google Scholar
• Schuster A, Hor KN, Kowallick JT, et al. Cardiovascular magnetic resonance myocardial feature tracking: concepts and clinical applications. Circ Cardiovasc Imaging. 2016;9(4):e004077.
   PubMed Web of Science ®Google Scholar
• Ni Y. MR contrast agents for cardiac imaging. In: Bogaert J, Dymarkowski S, Taylor AM, et al., editors. Clinical Cardiac MRI. Berlin, Heidelberg: Springer Berlin Heidelberg; 2012. p. 31–51.
   Google Scholar
• Barkhausen J, Ebert W, Debatin JF, et al. Imaging of myocardial infarction: comparison of magnevist and gadophrin-3 in rabbits. J Am Coll Cardiol. 2002;39(8):1392–1398.
   PubMed Web of Science ®Google Scholar
• Lee SS, Goo HW, Park SB, et al. MR imaging of reperfused myocardial infarction: comparison of necrosis-specific and intravascular contrast agents in a cat model. Radiology. 2003;226(3):739–747.
   PubMed Web of Science ®Google Scholar
• Choi SH, Lee SS, Choi SI, et al. Occlusive myocardial infarction: investigation of bis-Gadolinium mesoporphyrins–enhanced T1-weighted MR imaging in a cat model. Radiology. 2001;220(2):436–440.
   PubMed Web of Science ®Google Scholar
• Ni Y, Dymarkowski S, Chen F, et al. Occlusive myocardial infarction enhanced or not enhanced with necrosis-avid contrast agents at MR imaging. Radiology. 2002;225(2):603–605.
   PubMed Web of Science ®Google Scholar
• Pislaru SV, Ni Y, Pislaru C, et al. Noninvasive measurements of infarct size after thrombolysis with a necrosis-avid MRI contrast agent. Circulation. 1999;99(5):690–696.
   PubMed Web of Science ®Google Scholar
• Saeed M, Bremerich J, Wendland MF, et al. Reperfused myocardial infarction as seen with use of necrosis-specific versus standard extracellular MR contrast media in rats. Radiology. 1999;213(1):247–257.
   PubMed Web of Science ®Google Scholar
• Choi SI, Choi SH, Kim ST, et al. Irreversibly damaged myocardium at MR imaging with a necrotic tissue-specific contrast agent in a cat model. Radiology. 2000;215(3):863–868.
   PubMed Web of Science ®Google Scholar
• Saeed M, Lund G, Wendland MF, et al. Magnetic resonance characterization of the peri-infarction zone of reperfused myocardial infarction with necrosis-specific and extracellular nonspecific contrast media. Circulation. 2001;103(6):871–876.
   PubMed Web of Science ®Google Scholar
• Ni Y, Pislaru C, Bosmans H, et al. Intracoronary delivery of Gd-DTPA and Gadophrin-2 for determination of myocardial viability with MR imaging. Eur Radiol. 2001;11(5):876–883.
   PubMed Web of Science ®Google Scholar
• Dymarkowski S, Ni Y, Miao Y, et al. Value of T2-weighted MRI early after myocardial infarction in dogs: comparison with bis-gadolinium-mesoporphyrin enhanced T1-weighted MRI and functional data from cine MRI. Invest Radiol. 2002;37(2):77–85.
   PubMed Web of Science ®Google Scholar
• Ni Y, Cresens E, Adriaens P, et al. Necrosis-avid contrast agents: introducing nonporphyrin species. Acad Radiol. 2002;9(1):S98–S101.
   PubMedGoogle Scholar
• Jin J, Teng G, Feng Y, et al. Magnetic resonance imaging of acute reperfused myocardial infarction: intraindividual comparison of ECIII-60 and Gd-DTPA in a swine model. Cardiovasc Intervent Radiol. 2007;30(2):248–256.
   PubMed Web of Science ®Google Scholar
• Saab-Ismail NH, Simor T, Gaszner B, et al. Synthesis and in vivo evaluation of new contrast agents for cardiac MRI. J Med Chem. 1999;42(15):2852–2861.
   PubMed Web of Science ®Google Scholar
• Simor T, Gaszner B, Oshinski JN, et al. Gd(ABE-DTTA)-enhanced cardiac MRI for the diagnosis of ischemic events in the heart. J Magn Reson Imaging. 2005;21(5):536–545.
   PubMed Web of Science ®Google Scholar
• Kiss P, Suranyi P, Simor T, et al. In vivo R1-enhancement mapping of canine myocardium using ceMRI with Gd(ABE-DTTA) in an acute ischemia-reperfusion model. J Magn Reson Imaging. 2006;24(3):571–579.
   PubMed Web of Science ®Google Scholar
• Surányi P, Kiss P, Ruzsics B, et al. In vivo myocardial tissue kinetics of Gd(ABE-DTTA), a tissue-persistent contrast agent. Magn Reson Med. 2007;58(1):55–64.
   PubMed Web of Science ®Google Scholar
• Ruzsics B, Surányi P, Kiss P, et al. Gd(ABE-DTTA), a novel contrast agent, at the MRI-effective dose shows absence of deleterious physiological effects in dogs. Pharmacology. 2006;77(4):188–194.
   PubMed Web of Science ®Google Scholar
• Surányi P, Kiss P, Brott BC, et al. Percent infarct mapping: an R1-map-based CE-MRI method for determining myocardial viability distribution. Magn Reson Med. 2006;56(3):535–545.
   PubMed Web of Science ®Google Scholar
• Ruzsics B, Surányi P, Kiss P, et al. Head-to-head comparison between delayed enhancement and percent infarct mapping for assessment of myocardial infarct size in a canine model. J Magn Reson Imaging. 2008;28(6):1386–1392.
   PubMed Web of Science ®Google Scholar
• Kirschner R, Toth L, Varga-Szemes A, et al. Differentiation of acute and four-week old myocardial infarct with Gd(ABE-DTTA)-enhanced CMR. J Cardiovasc Magn Reson. 2010;12(1):22.
   PubMedGoogle Scholar
• Kirschner R, Varga-Szemes A, Simor T, et al. Acute infarct selective MRI contrast agent. Int J Cardiovasc Imaging. 2012;28(2):285–293.
   PubMed Web of Science ®Google Scholar
• Varga-Szemes A, Kiss P, Rab A, et al. In vitro longitudinal relaxivity profile of Gd (ABE-DTTA), an investigational magnetic resonance imaging contrast agent. PLoS One. 2016;11(2):e0149260.
   PubMed Web of Science ®Google Scholar
• Huang S, Chen HH, Yuan H, et al. Molecular MRI of acute necrosis with a novel DNA-binding Gadolinium chelate: kinetics of cell death and clearance in infarcted myocardium. Circ Cardiovasc Imaging. 2011;4(6):729–737.
   PubMed Web of Science ®Google Scholar
• Cho H, Guo Y, Sosnovik DE, et al. Imaging DNA with fluorochrome bearing metals. Inorg Chem. 2013;52(21):12216–12222.
   PubMed Web of Science ®Google Scholar
• Chen HH, Yuan H, Cho H, et al. Theranostic nucleic acid binding nanoprobe exerts anti-inflammatory and cytoprotective effects in ischemic injury. Theranostics. 2017;7(4):814–825.
   PubMed Web of Science ®Google Scholar
• Gallagher FA, Kettunen MI, Hu D-E, et al. Production of hyperpolarized [1, 4-13C2]malate from [1, 4-13C2]fumarate is a marker of cell necrosis and treatment response in tumors. Proc Natl Acad Sci U S A. 2009;106(47):19801–19806.
   PubMed Web of Science ®Google Scholar
• Clatworthy MR, Kettunen MI, Hu D-E, et al. Magnetic resonance imaging with hyperpolarized [1, 4-13C2]fumarate allows detection of early renal acute tubular necrosis. Proc Natl Acad Sci U S A. 2012;109(33):13374–13379.
   PubMed Web of Science ®Google Scholar
• Miller JJ, Lau AZ, Nielsen PM, et al. Hyperpolarized [1, 4-13C2]fumarate enables magnetic resonance-based imaging of myocardial necrosis. JACC Cardiovasc Imaging. 2018;11(11):1594–1606.
   PubMed Web of Science ®Google Scholar