Abstract
This review summarizes small-animal cardiovascular magnetic resonance (CMR) techniques that are being actively developed at present. Taking into account with few exceptions only literature of the past 2 years it shows that small-animal CMR has become an important and versatile analysis tool in many biomedical studies. The relatively complex signal formation and detection in magnetic resonance offers numerous ways of creating and modulating image contrast as a function of the specific needs. Although most new small-animal CMR developments are done within the scientific MR community, the MR manufacturers have readily contributed in making these techniques robust and available for routine application studies. Unlike other cardiovascular imaging techniques, CMR is used in many facets to assess morphology, global and regional function, blood flow, myocardial structure, cell damage, metabolism, and other molecular processes for studying mouse and rat models of human disease as well as general biochemical mechanisms in vivo.
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Bovens SM, te Boekhorst BC, den Ouden K, van de Kolk KW, Nauerth A, Nederhoff MG, et al. Evaluation of infarcted murine heart function: comparison of prospectively triggered with self-gated MRI. NMR Biomed. 2011;24(3):307–15. doi:10.1002/nbm.1593.
Hiba B, Richard N, Thibault H, Janier M. Cardiac and respiratory self-gated cine MRI in the mouse: comparison between radial and rectilinear techniques at 7T. Magn Reson Med. 2007;58(4):745–53. doi:10.1002/mrm.21355.
Schneider JE, Lanz T, Barnes H, Medway D, Stork LA, Lygate CA, et al. Ultra-fast and accurate assessment of cardiac function in rats using accelerated MRI at 9.4 Tesla. Magn Reson Med. 2008;59(3):636–41. doi:10.1002/mrm.21491.
• Schneider JE, Lanz T, Barnes H, Stork LA, Bohl S, Lygate CA et al. Accelerated cardiac magnetic resonance imaging in the mouse using an eight-channel array at 9.4 Tesla. Magn Reson Med. 2011;65(1):60-70. doi:10.1002/mrm.22605. Reports efficient parallel MRI for rodent CMR.
• Ratering D, Baltes C, Dorries C, Rudin M. Accelerated cardiovascular magnetic resonance of the mouse heart using self-gated parallel imaging strategies does not compromise accuracy of structural and functional measures. J Cardiovasc Magn Reson. 2010;12:43. doi:10.1186/1532-429X-12-43. Combination of self-gating with k-space acceleration.
Riegler J, Cheung KK, Man YF, Cleary JO, Price AN, Lythgoe MF. Comparison of segmentation methods for MRI measurement of cardiac function in rats. J Magn Reson Imaging. 2010;32(4):869–77. doi:10.1002/jmri.22305.
Axel L, Dougherty L. MR imaging of motion with spatial modulation of magnetization. Radiology. 1989;171(3):841–5.
Young AA, French BA, Yang Z, Cowan BR, Gilson WD, Berr SS, et al. Reperfused myocardial infarction in mice: 3D mapping of late gadolinium enhancement and strain. J Cardiovasc Magn Reson. 2006;8(5):685–92. doi:10.1080/10976640600721767.
Aletras AH, Ding S, Balaban RS, Wen H. DENSE: displacement encoding with stimulated echoes in cardiac functional MRI. J Magn Reson. 1999;137(1):247–52. doi:10.1006/jmre.1998.1676.
Gilson WD, Yang Z, French BA, Epstein FH. Complementary displacement-encoded MRI for contrast-enhanced infarct detection and quantification of myocardial function in mice. Magn Reson Med. 2004;51(4):744–52. doi:10.1002/mrm.20003.
Herold V, Morchel P, Faber C, Rommel E, Haase A, Jakob PM. In vivo quantitative three-dimensional motion mapping of the murine myocardium with PC-MRI at 17.6 T. Magn Reson Med. 2006;55(5):1058–64. doi:10.1002/mrm.20866.
• Dall’armellina E, Jung BA, Lygate CA, Neubauer S, Markl M, Schneider JE. Improved method for quantification of regional cardiac function in mice using phase-contrast MRI. Magn Reson Med. 2011. doi:10.1002/mrm.23022. Method for efficiently using tissue-phase-contrast MRI in CMR.
Zhong J, Yu X. Strain and torsion quantification in mouse hearts under dobutamine stimulation using 2D multiphase MR DENSE. Magn Reson Med. 2010;64(5):1315–22. doi:10.1002/mrm.22530.
• Jacquier A, Kober F, Bun S, Giorgi R, Cozzone PJ, Bernard M. Quantification of myocardial blood flow and flow reserve in rats using arterial spin labeling MRI: comparison with a fluorescent microsphere technique. NMR Biomed. 2011. doi:10.1002/nbm.1645. Validation MBF reserve under isoflurane anesthesia using ASL.
Vandsburger MH, Janiczek RL, Xu Y, French BA, Meyer CH, Kramer CM, et al. Improved arterial spin labeling after myocardial infarction in mice using cardiac and respiratory gated look-locker imaging with fuzzy C-means clustering. Magn Reson Med. 2010;63(3):648–57. doi:10.1002/mrm.22280.
Belle V, Kahler E, Waller C, Rommel E, Voll S, Hiller K, et al. In vivo quantitative mapping of cardiac perfusion in rats using a noninvasive MR spin-labeling method. J Magn Reson Imaging. 1998;8(6):1240–5.
Kober F, Iltis I, Cozzone PJ, Bernard M. Myocardial blood flow mapping in mice using high-resolution spin labeling magnetic resonance imaging: influence of ketamine/xylazine and isoflurane anesthesia. Magn Reson Med. 2005;53(3):601–6. doi:10.1002/mrm.20373.
Kober F, Iltis I, Izquierdo M, Desrois M, Ibarrola D, Cozzone PJ, et al. High-resolution myocardial perfusion mapping in small animals in vivo by spin-labeling gradient-echo imaging. Magn Reson Med. 2004;51(1):62–7.
• Coolen BF, Moonen RP, Paulis LE, Geelen T, Nicolay K, Strijkers GJ. Mouse myocardial first-pass perfusion MR imaging. Magn Reson Med. 2010;64(6):1658-63. doi:10.1002/mrm.22588. Demonstration of first-pass perfusion MRI in mice.
• Makowski M, Jansen C, Webb I, Chiribiri A, Nagel E, Botnar R et al. First-pass contrast-enhanced myocardial perfusion MRI in mice on a 3-T clinical MR scanner. Magn Reson Med. 2010;64(6):1592-8. doi:10.1002/mrm.22470. Demonstration of first-pass perfusion MRI in mice.
Li W, Griswold M, Yu X. Rapid T1 mapping of mouse myocardium with saturation recovery Look-Locker method. Magn Reson Med. 2010;64(5):1296–303. doi:10.1002/mrm.22544.
• Coolen BF, Geelen T, Paulis LE, Nauerth A, Nicolay K, Strijkers GJ. Three-dimensional T1 mapping of the mouse heart using variable flip angle steady-state MR imaging. NMR Biomed. 2011;24(2):154-62. doi:10.1002/nbm.1566. Original novel method for rapid T1 mapping.
Lefrancois W, Miraux S, Calmettes G, Pourtau L, Franconi JM, Diolez P, et al. A fast black-blood sequence for four-dimensional cardiac manganese-enhanced MRI in mouse. NMR Biomed. 2011;24(3):291–8. doi:10.1002/nbm.1588.
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(4):878–86. doi:10.1002/jmri.22325.
• Beyers RJ, Smith RS, Xu Y, Piras BA, Salerno M, Berr SS et al. T(2) -weighted MRI of post-infarct myocardial edema in mice. Magn Reson Med. 2011. doi:10.1002/mrm.22975. Optimization of myocardial T2 mapping with excellent quality.
Huang S, Sosnovik DE. Molecular and Microstructural Imaging of the Myocardium. Curr Cardiovasc Imaging Rep. 2010;3(1):26–33. doi:10.1007/s12410-010-9007-y.
Sosnovik DE, Wang R, Dai G, Reese TG, Wedeen VJ. Diffusion MR tractography of the heart. J Cardiovasc Magn Reson. 2009;11:47. doi:10.1186/1532-429X-11-47.
• Sosnovik DE, Wang R, Dai G, Wang T, Aikawa E, Novikov M et al. Diffusion spectrum MRI tractography reveals the presence of a complex network of residual myofibers in infarcted myocardium. Circ Cardiovasc Imaging. 2009;2(3):206-12. doi:10.1161/CIRCIMAGING.108.815050. Application of ex vivo and challenging in vivo diffusion MRI.
Gupta A, Chacko VP, Weiss RG. Abnormal energetics and ATP depletion in pressure-overload mouse hearts: in vivo high-energy phosphate concentration measures by noninvasive magnetic resonance. Am J Physiol Heart Circ Physiol. 2009;297(1):H59–64. doi:10.1152/ajpheart.00178.2009.
Maslov MY, Chacko VP, Hirsch GA, Akki A, Leppo MK, Steenbergen C, et al. Reduced in vivo high-energy phosphates precede adriamycin-induced cardiac dysfunction. Am J Physiol Heart Circ Physiol. 2010;299(2):H332–7. doi:10.1152/ajpheart.00727.2009.
• Gupta A, Chacko VP, Schar M, Akki A, Weiss RG. Impaired ATP kinetics in failing in vivo mouse heart. Circ Cardiovasc Imaging. 2011;4(1):42-50. doi:10.1161/CIRCIMAGING.110.959320. Link between phosphorus metabolites and heart failure established in mice in vivo.
Schar M, El-Sharkawy AM, Weiss RG, Bottomley PA. Triple repetition time saturation transfer (TRiST) 31P spectroscopy for measuring human creatine kinase reaction kinetics. Magn Reson Med. 2010;63(6):1493–501. doi:10.1002/mrm.22347.
Ruiz-Cabello J, Barnett BP, Bottomley PA, Bulte JW. Fluorine (19F) MRS and MRI in biomedicine. NMR Biomed. 2011;24(2):114–29. doi:10.1002/nbm.1570.
Flogel U, Su S, Kreideweiss I, Ding Z, Galbarz L, Fu J, et al. Noninvasive detection of graft rejection by in vivo (19) F MRI in the early stage. Am J Transplant. 2011;11(2):235–44. doi:10.1111/j.1600-6143.2010.03372.x.
Atherton HJ, Dodd MS, Heather LC, Schroeder MA, Griffin JL, Radda GK, et al. Role of pyruvate dehydrogenase inhibition in the development of hypertrophy in the hyperthyroid rat heart: a combined magnetic resonance imaging and hyperpolarized magnetic resonance spectroscopy study. Circulation. 2011;123(22):2552–61. doi:10.1161/CIRCULATIONAHA.110.011387.
Schroeder MA, Swietach P, Atherton HJ, Gallagher FA, Lee P, Radda GK, et al. Measuring intracellular pH in the heart using hyperpolarized carbon dioxide and bicarbonate: a 13C and 31P magnetic resonance spectroscopy study. Cardiovasc Res. 2010;86(1):82–91. doi:10.1093/cvr/cvp396.
Lau AZ, Chen AP, Ghugre NR, Ramanan V, Lam WW, Connelly KA, et al. Rapid multislice imaging of hyperpolarized 13C pyruvate and bicarbonate in the heart. Magn Reson Med. 2010;64(5):1323–31. doi:10.1002/mrm.22525.
• Tyler DJ. Cardiovascular Applications of Hyperpolarized MRI. Curr Cardiovasc Imaging Rep. 2011;4(2):108-15. doi:10.1007/s12410-011-9066-8. Excellent review on hyperpolarized 13C MR and potential applications.
Qiao H, Zhang H, Yamanaka S, Patel VV, Petrenko NB, Huang B, 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. doi:10.1161/CIRCIMAGING.110.957431.
Campan M, Lionetti V, Aquaro GD, Forini F, Matteucci M, Vannucci L, et al. Ferritin as a reporter gene for in vivo tracking of stem cells by 1.5-T cardiac MRI in a rat model of myocardial infarction. Am J Physiol Heart Circ Physiol. 2011;300(6):H2238–50. doi:10.1152/ajpheart.00935.2010.
Kraehenbuehl TP, Ferreira LS, Hayward AM, Nahrendorf M, van der Vlies AJ, Vasile E, et al. Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials. 2011;32(4):1102–9. doi:10.1016/j.biomaterials.2010.10.005.
Sosnovik DE, Nahrendorf M, Panizzi P, Matsui T, Aikawa E, Dai G, et al. Molecular MRI detects low levels of cardiomyocyte apoptosis in a transgenic model of chronic heart failure. Circ Cardiovasc Imaging. 2009;2(6):468–75. doi:10.1161/CIRCIMAGING.109.863779.
Dash R, Chung J, Chan T, Yamada M, Barral J, Nishimura D et al. A molecular MRI probe to detect treatment of cardiac apoptosis in vivo. Magn Reson Med. 2011. doi:10.1002/mrm.22876.
• Harel-Adar T, Ben Mordechai T, Amsalem Y, Feinberg MS, Leor J, Cohen S. Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc Natl Acad Sci U S A. 2011;108(5):1827-32. doi:10.1073/pnas.1015623108. Use of in vivo CMR to strengthen a major finding in treatment of MI.
Aksentijevic D, Lygate CA, Makinen K, Zervou S, Sebag-Montefiore L, Medway D, et al. High-energy phosphotransfer in the failing mouse heart: role of adenylate kinase and glycolytic enzymes. Eur J Heart Fail. 2010;12(12):1282–9. doi:10.1093/eurjhf/hfq174.
Gros D, Theveniau-Ruissy M, Bernard M, Calmels T, Kober F, Sohl G, et al. Connexin 30 is expressed in the mouse sino-atrial node and modulates heart rate. Cardiovasc Res. 2010;85(1):45–55. doi:10.1093/cvr/cvp280.
Tsika RW, Ma L, Kehat I, Schramm C, Simmer G, Morgan B, et al. TEAD-1 overexpression in the mouse heart promotes an age-dependent heart dysfunction. J Biol Chem. 2010;285(18):13721–35. doi:10.1074/jbc.M109.063057.
Wansapura JP, Millay DP, Dunn RS, Molkentin JD, Benson DW. Magnetic resonance imaging assessment of cardiac dysfunction in delta-sarcoglycan null mice. Neuromuscul Disord. 2011;21(1):68–73. doi:10.1016/j.nmd.2010.09.007.
Banquet S, Gomez E, Nicol L, Edwards-Levy F, Henry JP, Cao R, et al. Arteriogenic therapy by intramyocardial sustained delivery of a novel growth factor combination prevents chronic heart failure. Circulation. 2011;124(9):1059–69. doi:10.1161/CIRCULATIONAHA.110.010264.
• Hiller KH, Ruile P, Kraus G, Bauer WR, Waller C. Tissue ACE inhibition improves microcirculation in remote myocardium after coronary stenosis: MR imaging study in rats. Microvasc Res. 2010;80(3):484-90. doi:10.1016/j.mvr.2010.05.007. Use of multimodal CMR to perform a complete assessment of function and microcirculation in vivo.
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Kober, F., Bernard, M., Troalen, T. et al. Cardiovascular Magnetic Resonance of Myocardial Structure, Function, and Perfusion in Mouse and Rat Models. Curr Cardiovasc Imaging Rep 5, 109–115 (2012). https://doi.org/10.1007/s12410-012-9122-z
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DOI: https://doi.org/10.1007/s12410-012-9122-z