Feasibility of real-time cardiac MRI in mice using tiny golden angle radial sparse.
cardiac function
first-pass perfusion
heart failure
mouse cardiac MRI
nexilin
pharmacological stress
real-time
tiny golden angle radial sparse
Journal
NMR in biomedicine
ISSN: 1099-1492
Titre abrégé: NMR Biomed
Pays: England
ID NLM: 8915233
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
23
08
2019
revised:
02
03
2020
accepted:
05
03
2020
pubmed:
1
4
2020
medline:
30
7
2021
entrez:
1
4
2020
Statut:
ppublish
Résumé
Cardiovascular magnetic resonance imaging has proven valuable for the assessment of structural and functional cardiac abnormalities. Even although it is an established imaging method in small animals, the long acquisition times of gated or self-gated techniques still limit its widespread application. In this study, the application of tiny golden angle radial sparse MRI (tyGRASP) for real-time cardiac imaging was tested in 12 constitutive nexilin (Nexn) knock-out (KO) mice, both heterozygous (Het, N = 6) and wild-type (WT, N = 6), and the resulting functional parameters were compared with a well-established self-gating approach. Real-time images were reconstructed for different temporal resolutions of between 16.8 and 79.8 ms per image. The suggested approach was additionally tested for dobutamine stress and qualitative first-pass perfusion imaging. Measurements were repeated twice within 2 weeks for reproducibility assessment. In direct comparison with the high-quality, self-gated technique, the real-time approach did not show any significant differences in global function parameters for acquisition times below 50 ms (rest) and 31.5 ms (stress). Compared with WT, the end-diastolic volume (EDV) and end-systolic volume (ESV) were markedly higher (P < 0.05) and the ejection fraction (EF) was significantly lower in the Het Nexn-KO mice at rest (P < 0.001). For the stress investigation, a clear decrease of EDV and ESV, and an increase in EF, but maintained stroke volume, could be observed in both groups. Combined with ECG-triggering, tyGRASP provided first-pass perfusion data with a temporal resolution of one image per heartbeat, allowing the quantitative assessment of upslope curves in the blood-pool and myocardium. Excellent inter-study reproducibility was achieved in all the functional parameters. The tyGRASP is a valuable real-time MRI technique for mice, which significantly reduces the scan time in preclinical cardiac functional imaging, providing sufficient image quality for deriving accurate functional parameters, and has the potential to investigate real-time and beat-to-beat changes.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4300Informations de copyright
© 2020 The Authors. NMR in Biomedicine published by John Wiley & Sons Ltd.
Références
Nice National Institute for Health and Care Excellence. Chronic heart failure in adults: diagnosis and management. Nice Guideline. 2018. https://www.nice.org.uk/guidance/ng106. Accessed 21 September, 2018.
Messroghli DR, Moon JC, Ferreira VM, et al. Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2* and extracellular volume: A consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI). J Cardiovasc Magn Reson. 2017;19(1):1-24.
Petersen SE, Aung N, Sanghvi MM, et al. Reference ranges for cardiac structure and function using cardiovascular magnetic resonance (CMR) in Caucasians from the UK Biobank population cohort. J Cardiovasc Magn Reson. 2017;19(1):1-19.
Schneider JE, Cassidy PJ, Lygate C, et al. Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system. J Magn Reson Imaging. 2003;18(6):691-701.
Peterzan MA, Rider OJ, Anderson LJ. The role of cardiovascular magnetic resonance imaging in heart failure. Card Fail Rev. 2016;2:115-122.
Wessels A, Sedmera D. Developmental anatomy of the heart: a tale of mice and man. Physiol Genomics. 2003;15(3):165-176.
Rose SE, Wilson SJ, Zelaya FO, Crozier S, Doddrell DM. High resolution high field rodent cardiac imaging with flow enhancement suppression. Magn Reson Imaging. 1994;12(8):1183-1190.
Hiba B, Richard N, Janier M, Croisille P. Cardiac and respiratory double self-gated cine MRI in the mouse at 7 T. Magn Reson Med. 2006;55(3):506-513.
Hoerr V, Nagelmann N, Nauerth A, Kuhlmann MT, Stypmann J, Faber C. Cardiac-respiratory self-gated cine ultra-short echo time (UTE) cardiovascular magnetic resonance for assessment of functional cardiac parameters at high magnetic fields. J Cardiovasc Magn Reson. 2013;15(1):1-8.
Zuo Z, Subgang A, Abaei A, et al. Assessment of longitudinal reproducibility of mice LV function parameters at 11.7 T derived from self-gated CINE MRI. Biomed Res Int. 2017;2017:1-10.
Joubert M, Tager P, Legallois D, et al. Test-retest reproducibility of cardiac magnetic resonance imaging in healthy mice at 7-Tesla: effect of anesthetic procedures. Sci Rep. 2017;7(1):1-11.
Griswold MA, Jakob PM, Heidemann RM, et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med. 2002;47(6):1202-1210.
Seiberlich N, Ehses P, Duerk J, Gilkeson R, Griswold M. Improved radial GRAPPA calibration for real-time free-breathing cardiac imaging. Magn Reson Med. 2011;65(2):492-505.
Breuer FA, Kellman P, Griswold MA, Jakob PM. Dynamic autocalibrated parallel imaging using temporal GRAPPA (TGRAPPA). Magn Reson Med. 2005;53(4):981-985.
Feng L, Srichai MB, Lim RP, et al. Highly accelerated real-time cardiac cine MRI using k - t SPARSE-SENSE. Magn Reson Med. 2013;70(1):64-74.
Bollache E, Barker AJ, Dolan RS, et al. k-t accelerated aortic 4D flow MRI in under two minutes: Feasibility and impact of resolution, k-space sampling patterns, and respiratory navigator gating on hemodynamic measurements. Magn Reson Med. 2018;79(1):195-207.
Schnell S, Markl M, Entezari P, et al. k-t GRAPPA accelerated four-dimensional flow MRI in the aorta: Effect on scan time, image quality, and quantification of flow and wall shear stress. Magn Reson Med. 2014;72(2):522-533.
Lustig M, Donoho D, Pauly JM. Sparse MRI: The application of compressed sensing for rapid MR imaging. Magn Reson Med. 2007;58(6):1182-1195.
Kido T, Kido T, Nakamura M, et al. Compressed sensing real-time cine cardiovascular magnetic resonance: accurate assessment of left ventricular function in a single-breath-hold. J Cardiovasc Magn Reson. 2016;18(1):1-11.
Otazo R, Kim D, Axel L, Sodickson DK. Combination of compressed sensing and parallel imaging for highly accelerated first-pass cardiac perfusion MRI. Magn Reson Med. 2010;64(3):767-776.
Wech T, Seiberlich N, Schindele A, et al. Development of real-time magnetic resonance imaging of mouse hearts at 9.4 Tesla - simulations and first application. IEEE Trans Med Imaging. 2016;35(3):912-920.
Uecker M, Zhang S, Voit D, Merboldt K-D, Frahm J. Real-time MRI: recent advances using radial FLASH. Imaging Med. 2012;4(4):461-476.
Winkelmann S, Schaeffter T, Koehler T, Eggers H, Doessel O. An optimal radial profile order based on the golden ratio for time-resolved MRI. IEEE Trans Med Imaging. 2007;26(1):68-76.
Wundrak S, Paul J, Ulrici J, Hell E, Rasche V. A small surrogate for the golden angle in time-resolved radial MRI based on generalized Fibonacci sequences. IEEE Trans Med Imaging. 2015;34(6):1262-1269.
Wundrak S, Paul J, Ulrici J, et al. Golden ratio sparse MRI using tiny golden angles. Magn Reson Med. 2016;75(6):2372-2378.
Haris K, Hedström E, Bidhult S, et al. Self-gated fetal cardiac MRI with tiny golden angle iGRASP: A feasibility study. J Magn Reson Imaging. 2017;46(1):207-217.
Haji-Valizadeh H, Rahsepar AA, Collins JD, et al. Validation of highly accelerated real-time cardiac cine MRI with radial k-space sampling and compressed sensing in patients at 1.5T and 3T. Magn Reson Med. 2018;79(5):2745-2751.
Aherrahrou Z, Schlossarek S, Stoelting S, et al. Knock-out of nexilin in mice leads to dilated cardiomyopathy and endomyocardial fibroelastosis. Basic Res Cardiol. 2016;111(1):6-10.
Haas J, Frese KS, Peil B, et al. Atlas of the clinical genetics of human dilated cardiomyopathy. Eur Heart J. 2015;36(18):1123-1135.
Hassel D, Dahme T, Erdmann J, et al. Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat Med. 2009;15(11):1281-1288.
Liu C, Spinozzi S, Chen J-Y, et al. Nexilin is a new component of junctional membrane complexes required for cardiac T-tubule formation. Circulation. 2019;140(1):55-66.
Zhang Y, Hetherington HP, Stokely EM, Mason GF, Twieg DB. A novel k-space trajectory measurement technique. Magn Reson Med. 1998;39(6):999-1004.
Heiberg E, Sjögren J, Ugander M, Carlsson M, Engblom H, Arheden H. Design and validation of Segment - freely available software for cardiovascular image analysis. BMC Med Imaging. 2010;10(1):1-13.
Wiesmann F, Ruff J, Engelhardt S, et al. Dobutamine-stress magnetic resonance microimaging in mice: acute changes of cardiac geometry and function in normal and failing murine hearts. Circ Res. 2001;88(6):563-569.
Tyrankiewicz U, Skorka T, Jablonska M, Petkow-Dimitrow P, Chlopicki S. Characterization of the cardiac response to a low and high dose of dobutamine in the mouse model of dilated cardiomyopathy by MRI in vivo. J Magn Reson Imaging. 2013;37(3):669-677.
Schultheiss H-P, Fairweather D, Caforio ALP, et al. Dilated cardiomyopathy. Nat Rev Dis Primers. 2019;5(1):1-19.
Stuckey DJ, Carr CA, Camelliti P, Tyler DJ, Davies KE, Clarke K. In vivo MRI characterization of progressive cardiac dysfunction in the mdx mouse model of muscular dystrophy. PLoS ONE. 2012;7(1):1-8.
Motaal AG, Coolen BF, Abdurrachim D, et al. Accelerated high-frame-rate mouse heart cine-MRI using compressed sensing reconstruction. NMR Biomed. 2013;26(4):451-457.
Wolff SD, Schwitter J, Coulden R, et al. Myocardial first-pass perfusion magnetic resonance imaging. Circulation. 2004;110(6):732-737.
Sun W, Sun L, Yang F, Zhao X, Cai R, Yuan W. Evaluation of myocardial viability in myocardial infarction patients by magnetic resonance perfusion and delayed enhancement imaging. Herz. 2018;44(8):735-742.
Bethke A, Shanmuganathan L, Andersen GØ, et al. Microvascular perfusion in infarcted and remote myocardium after successful primary PCI: angiographic and CMR findings. Eur Radiol. 2019;29(2):941-950.
Coolen BF, Moonen RPM, Paulis LEM, Geelen T, Nicolay K, Strijkers GJ. Mouse myocardial first-pass perfusion MR imaging. Magn Reson Med. 2010;64(6):1658-1663.
van Nierop BJ, Coolen BF, Dijk WJR, et al. Quantitative first-pass perfusion MRI of the mouse myocardium. Magn Reson Med. 2013;69(6):1735-1744.
Naresh NK, Chen X, Roy RJ, Antkowiak PF, Annex BH, Epstein FH. Accelerated dual-contrast first-pass perfusion MRI of the mouse heart: Development and application to diet-induced obese mice. Magn Reson Med. 2015;73(3):1237-1245.