Top

Journal of Cardiovascular Magnetic Resonance

Published in:

Open Access 01-12-2017 | Research

Cardiac 4D phase-contrast CMR at 9.4 T using self-gated ultra-short echo time (UTE) imaging

Authors: M. Krämer, A. G. Motaal, K-H. Herrmann, B. Löffler, J. R. Reichenbach, G. J. Strijkers, V. Hoerr

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Abstract

Background

Time resolved 4D phase contrast (PC) cardiovascular magnetic resonance (CMR) in mice is challenging due to long scan times, small animal ECG-gating and the rapid blood flow and cardiac motion of small rodents. To overcome several of these technical challenges we implemented a retrospectively self-gated 4D PC radial ultra-short echo-time (UTE) acquisition scheme and assessed its performance in healthy mice by comparing the results with those obtained with an ECG-triggered 4D PC fast low angle shot (FLASH) sequence.

Methods

Cardiac 4D PC CMR images were acquired at 9.4 T in healthy mice using the proposed self-gated radial center-out UTE acquisition scheme (TE/TR of 0.5 ms/3.1 ms) and a standard Cartesian 4D PC imaging sequence (TE/TR of 2.1 ms/5.0 ms) with a four-point Hadamard flow encoding scheme. To validate the proposed UTE flow imaging technique, experiments on a flow phantom with variable pump rates were performed.

Results

The anatomical images and flow velocity maps of the proposed 4D PC UTE technique showed reduced artifacts and an improved SNR (left ventricular cavity (LV): 8.9 ± 2.5, myocardium (MC): 15.7 ± 1.9) compared to those obtained using a typical Cartesian FLASH sequence (LV: 5.6 ± 1.2, MC: 10.1 ± 1.4) that was used as a reference. With both sequences comparable flow velocities were obtained in the flow phantom as well as in the ascending aorta (UTE: 132.8 ± 18.3 cm/s, FLASH: 134.7 ± 13.4 cm/s) and pulmonary artery (UTE: 78.5 ± 15.4 cm/s, FLASH: 86.6 ± 6.2 cm/s) of the animals. Self-gated navigator signals derived from information of the oversampled k-space center were successfully extracted for all animals with a higher gating efficiency of time spent on acquiring gated data versus total measurement time (UTE: 61.8 ± 11.5%, FLASH: 48.5 ± 4.9%).

Conclusions

The proposed self-gated 4D PC UTE sequence enables robust and accurate flow velocity mapping of the mouse heart in vivo at high magnetic fields. At the same time SNR, gating efficiency, flow artifacts and image quality all improved compared to the images obtained using the well-established, ECG-triggered, 4D PC FLASH sequence.

Firmin DN, Nayler GL, Kilner PJ, Longmore DB. The application of phase shifts in NMR for flow measurement. Magn Reson Med. 1990;14:230–41.CrossRefPubMed

Rebergen SA, van der Wall EE, Doornbos J, De Roos A. Magnetic resonance measurement of velocity and flow: Technique, validation, and cardiovascular applications. Am Heart J. 1993;126:1439–56.CrossRefPubMed

Meir KS, Leitersdorf E. Atherosclerosis in the Apolipoprotein E-Deficient Mouse: A Decade of Progress. Arterioscler Thromb Vasc Biol. 2004;24:1006–14.CrossRefPubMed

Isobe S, Tsimikas S, Zhou J, Fujimoto S, Sarai M, Branks MJ, Fujimoto A, Hofstra L, Reutelingsperger CP, Murohara T, Virmani R, Kolodgie FD, Narula N, Petrov A, Narula J. Noninvasive Imaging of Atherosclerotic Lesions in Apolipoprotein E-Deficient and Low-Density-Lipoprotein Receptor-Deficient Mice with Annexin A5. J Nucl Med. 2006;47:1497–505.PubMed

Jung B, Zaitsev M, Hennig J, Markl M. Navigator gated high temporal resolution tissue phase mapping of myocardial motion. Magn Reson Med. 2006;55:937–42.CrossRefPubMed

Yzet T, Bouzerar R, Baledent O, Renard C, Lumbala DM, Nguyen-Khac E, Regimbeau JM, Deramond H, Meyer ME. Dynamic measurements of total hepatic blood flow with Phase Contrast MRI. Eur J Radiol. 2010;73:119–24.CrossRefPubMed

Markl M, Chan FP, Alley MT, Wedding KL, Draney MT, Elkins CJ, Parker DW, Wicker R, Taylor CA, Herfkens RJ, Pelc NJ. Time-resolved three-dimensional phase-contrast MRI. J Magn Reson Imaging. 2003;17:499–506.CrossRefPubMed

Markl M, Draney MT, Miller DC, Levin JM, Williamson EE, Pelc NJ, Liang DH, Herfkens RJ. Time-resolved three-dimensional magnetic resonance velocity mapping of aortic flow in healthy volunteers and patients after valve-sparing aortic root replacement. J Thorac Cardiovasc Surg. 2005;130:456–63.CrossRefPubMed

Markl M, Harloff A, Bley TA, Zaitsev M, Jung B, Weigang E, Langer M, Hennig J, Frydrychowicz A. Time-resolved 3D MR velocity mapping at 3 T: Improved navigator-gated assessment of vascular anatomy and blood flow. J Magn Reson Imaging. 2007;25:824–31.CrossRefPubMed

10.

Markl M, Kilner PJ, Ebbers T. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2011;13:1–22.CrossRef

11.

Hope TA, Markl M, Wigström L, Alley MT, Miller DC, Herfkens RJ. Comparison of flow patterns in ascending aortic aneurysms and volunteers using four-dimensional magnetic resonance velocity mapping. J Magn Reson Imaging. 2007;26:1471–9.CrossRefPubMed

12.

Bovenkamp PR, Brix T, Lindemann F, Holtmeier R, Abdurrachim D, Kuhlmann MT, Strijkers GJ, Stypmann J, Hinrichs KH, Hoerr V. Velocity mapping of the aortic flow at 9.4 T in healthy mice and mice with induced heart failure using time-resolved three-dimensional phase-contrast MRI (4D PC MRI). MAGMA. 2015;28:315–27.CrossRefPubMed

13.

O’Brien KR, Cowan BR, Jain M, Stewart RAH, Kerr AJ, Young AA. MRI phase contrast velocity and flow errors in turbulent stenotic jets. J Magn Reson Imaging. 2008;28:210–8.CrossRefPubMed

14.

Caruthers SD, Lin SJ, Brown P, Watkins MP, Williams TA, Lehr KA, Wickline SA. Practical value of cardiac magn reson imaging for clinical quantification of aortic valve stenosis: comparison with echocardiography. Circulation. 2003;108:2236–43.CrossRefPubMed

15.

Carvalho JLA, Nayak KS. Rapid quantitation of cardiovascular flow using slice-selective fourier velocity encoding with spiral readouts. Magn Reson Med. 2007;57:639–46.CrossRefPubMed

16.

Søndergaard L, Thomsen C, Ståhlberg F, Gymoese E, Lindvig K, Hildebrandt P, Henriksen O. Mitral and aortic valvular flow: quantification with MR phase mapping. J Magn Reson Imaging. 1992;2:295–302.CrossRefPubMed

17.

Rahmer J, Börnert P, Groen J, Bos C. Three-dimensional radial ultrashort echo-time imaging with T2 adapted sampling. Magn Reson Med. 2006;55:1075–82.CrossRefPubMed

18.

Chan CF, Keenan NG, Nielles-Vallespin S, Gatehouse P, Sheppard MN, Boyle JJ, Pennell DJ, Firmin DN. Ultra-short echo time cardiovascular magnetic resonance of atherosclerotic carotid plaque. J Cardiovasc Magn Reson. 2010;12:1–8.CrossRef

19.

Herrmann KH, Krämer M, Reichenbach JR. Time Efficient 3D Radial UTE Sampling with Fully Automatic Delay Compensation on a Clinical 3 T MR Scanner. PLoS ONE. 2016;11:1–16.

20.

Nishimura DG, Irarrazabal P, Meyer CH. A Velocity k-Space Analysis of Flow Effects in Echo-Planar and Spiral Imaging. Magn Reson Med. 1995;33:549–56.CrossRefPubMed

21.

O’Brien KR, Myerson SG, Cowan BR, Young AA, Robson MD. Phase contrast ultrashort TE: A more reliable technique for measurement of high-velocity turbulent stenotic jets. Magn Reson Med. 2009;62:626–36.CrossRefPubMed

22.

Schmalbrock P, Yuan C, Chakeres DW, Kohli J, Pelc NJ. Volume MR angiography: methods to achieve very short echo times. Radiology. 1990;175:861–5.CrossRefPubMed

23.

Ståhlberg F, Thomsen C, Söndergaard L, Henriksen O. Pulse sequence design for MR velocity mapping of complex flow: notes on the necessity of low echo times. Magn Reson Med. 1994;12:1255–62.

24.

Kadbi M, Negahdar M, Traughber M, Martin P, Amini AA. Assessment of flow and hemodynamics in the carotid artery using a reduced TE 4D flow spiral phase-contrast MRI. In: Conf Proc IEEE Eng Med Bio Soc. 2013. p. 1100–3.

25.

Kadbi M, Negahdar M, Jw C, Traughber M, Martin P, Stoddard MF, Amini AA. 4d ute flow: A phase-contrast mri technique for assessment and visualization of stenotic flows. Magn Reson Med. 2015;73:939–50.CrossRefPubMed

26.

Janiczek RL, Blackman BR, Roy RJ, Meyer CH, Acton ST, Epstein FH. Three-dimensional phase contrast angiography of the mouse aortic arch using spiral mri. Magn Reson Med. 2011;66:1382–90.CrossRefPubMedPubMedCentral

27.

Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med. 2002;47:1202–10.CrossRefPubMed

28.

Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P. SENSE: Sensitivity encoding for fast MRI. Magn Reson Med. 1999;42:952–62.CrossRefPubMed

29.

Polson MJR, Barker AT, Gardiner S. The effect of rapid rise-time magnetic fields on the ECG of the rat. Clin Phys Physiol Meas. 1982;3:231.CrossRefPubMed

30.

Shetty AN. Suppression of radiofrequency interference in cardiac gated MRI: A simple design. Magn Reson Med. 1988;8:84–8.CrossRefPubMed

31.

Crowe ME, Larson AC, Zhang Q, Carr J, White RD, Li D, Simonetti OP. Automated rectilinear self-gated cardiac cine imaging. Magn Reson Med. 2004;52:782–8.CrossRefPubMed

32.

Larson AC, White RD, Laub G, McVeigh ER, Li D, Simonetti OP. Self-gated cardiac cine MRI. Magn Reson Med. 2004;51:93–102.CrossRefPubMedPubMedCentral

33.

Krämer M, Herrmann KH, Biermann J, Reichenbach JR. Retrospective reconstruction of cardiac cine images from golden-ratio radial MRI using one-dimensional. J Magn Reson Imaging. 2014;40:413–22.CrossRefPubMed

34.

Krämer M, Herrmann KH, Biermann J, Freiburger S, Schwarzer M, Reichenbach JR. Self-gated cardiac Cine MRI of the rat on a clinical 3 T MRI system. NMR Biomed. 2015;28:162–7.CrossRefPubMed

35.

Hoerr V, Nagelmann N, Nauerth A, Kuhlmann M, 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(59):1–8.

36.

Motaal AG, Noorman N, De Graaf WL, Hoerr V, Florack LMJ, Nicolay K, Strijkers GJ. Functional imaging of murine hearts using accelerated self-gated UTE cine MRI. Int J Cardiovasc Imaging. 2015;31:83–94.CrossRefPubMed

37.

Piccini D, Feng L, Bonanno G, Coppo S, Yerly J, Lim RP, Schwitter J, Sodickson DK, Otazo R, Stuber M. Four-dimensional respiratory motion-resolved whole heart coronary MR angiography. Magn Reson Med 2016;p n/a–n/a.

38.

Dumoulin CL, Souza SP, Darrow RD, Pelc NJ, Adams WJ, Ash SA. Simultaneous acquisition of phase-contrast angiograms and stationary-tissue images with Hadamard encoding of flow-induced phase shifts. J Magn Reson Imaging. 1991;1:399–404.CrossRefPubMed

39.

Pelc NJ, Bernstein MA, Shimakawa A, Glover GH. Encoding strategies for three-direction phase-contrast MR imaging of flow. J Magn Reson Imaging. 1991;1:405–13.CrossRefPubMed

40.

Savitzky A, Golay MJE. Smoothing and Differentiation of Data by Simplified Least Squares Procedures. Anal Chem. 1964;36:1627–39.CrossRef

41.

Riederer SJ, Tasciyan T, Farzaneh F, Lee JN, Wright RC, Herfkens RJ. MR fluoroscopy: Technical feasibility. Magn Reson Med. 1988;8:1–15.CrossRefPubMed

42.

Duyn JH, Yang Y, Frank JA, van der Veen JW. Simple Correction Method for k-Space Trajectory Deviations in MRI. J Magn Reson Imaging. 1998;132:150–3.CrossRef

43.

Zwart NR, Johnson KO, Pipe JG. Efficient sample density estimation by combining gridding and an optimized kernel. Magn Reson Med. 2012;67:701–10.CrossRefPubMed

44.

Abdul-Rahman HS, Gdeisat MA, Burton DR, Lalor MJ, Lilley F, Moore CJ. Fast and robust three-dimensional best path phase unwrapping algorithm. Appl Opt. 2007;46:6623–35.CrossRefPubMed

45.

Johnson PM, Liu J, Wade T, Tavallaei MA, Drangova M. Retrospective 3d motion correction using spherical navigator echoes. Magn Reson Imaging. 2016;34(9):1274–82.CrossRefPubMed

46.

Barger AV, Block WF, Toropov Y, Grist TM, Mistretta CA. Time-resolved contrast-enhanced imaging with isotropic resolution and broad coverage using an undersampled 3d projection trajectory. Magn Reosn Med. 2002;48:297–305.CrossRef

47.

Gu T, Korosec FR, Block WF, Fain SB, Turk Q, Lum D, Zhou Y, Grist TM, Haughton V, Mistretta CA. Pc vipr: A high-speed 3d phase-contrast method for flow quantification and high-resolution angiography. Am J Neuroradiol. 2005;26:743–9.PubMed

48.

Peters DC, Derbyshire JA, McVeigh ER. Centering the projection reconstruction trajectory: Reducing gradient delay errors. Magn Reson Med. 2003;50:1–6.CrossRefPubMedPubMedCentral

49.

Winter P, Kampf T, Helluy X, Gutjahr FT, Meyer CB, Rommel E, Bauer WR, Jakob PM, Herold V. Fast retrospectively triggered local pulse-wave velocity measurements in mice with CMR-microscopy using a radial trajectory. J Cardiovasc Magn Reson. 2013;15:1–11.CrossRef

50.

Brodsky EK, Samsonov AA, Block WF. Characterizing and correcting gradient errors in non-cartesian imaging: Are gradient errors linear time-invariant (LTI)? Magn Reson Med. 2009;62:1466–76.CrossRefPubMedPubMedCentral

51.

Lustig M, Donoho D, Sparse PJM, MRI. The application of compressed sensing for rapid MR imaging. Magn Reson Med. 2007;58:1182–95.CrossRefPubMed

52.

Wright KL, Lee GR, Ehses P, Griswold MA, Gulani V, Seiberlich N. Three-dimensional through-time radial GRAPPA for renal MR angiography. J Magn Reson Imaging. 2014;40:864–74.CrossRefPubMedPubMedCentral

53.

Chandarana H, Feng L, Block TK, Rosenkrantz AB, Lim RP, Babb JS, Sodickson DK, Otazo R. Free-Breathing Contrast-Enhanced Multiphase MRI of the Liver Using a Combination of Compressed Sensing, Parallel Imaging, and Golden-Angle Radial Sampling. Invest Radiol. 2013;48:10–6.CrossRefPubMedPubMedCentral

54.

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;26:68–76.CrossRefPubMed

55.

Chan RW, Ramsay EA, Cunningham CH, Plewes DB. Temporal stability of adaptive 3D radial MRI using multidimensional golden means. Magn Reson Med. 2009;61:354–63.CrossRefPubMed

56.

Park J, Shin T, Yoon SH, Goo JM, Park JY. A radial sampling strategy for uniform k-space coverage with retrospective respiratory gating in 3D ultrashort-echo-time lung imaging. NMR Biomed. 2016;29:576–87.CrossRefPubMed

57.

Gatehouse P, Firmin D. Flow distortion and signal loss in spiral imaging. Magn Reson Med. 1999;41:1023–31.CrossRefPubMed

58.

Feng L, Axel L, Chandarana H, Block KT, Sodickson DK, Otazo R. Xd-grasp: Golden-angle radial mri with reconstruction of extra motion-state dimensions using compressed sensing. Magn Reson Med. 2016;75:775–88.CrossRefPubMed

Title: Cardiac 4D phase-contrast CMR at 9.4 T using self-gated ultra-short echo time (UTE) imaging
Authors: M. Krämer
A. G. Motaal
K-H. Herrmann
B. Löffler
J. R. Reichenbach
G. J. Strijkers
V. Hoerr
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/s12968-017-0351-9

At a glance: The STEP trials

Springer Medicine

Cardiac 4D phase-contrast CMR at 9.4 T using self-gated ultra-short echo time (UTE) imaging

Abstract

Background

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2017

CMR-based blood oximetry via multi-parametric estimation using multiple T2 measurements

Effects of heart valve prostheses on phase contrast flow measurements in Cardiovascular Magnetic Resonance – a phantom study

Hemorrhage promotes inflammation and myocardial damage following acute myocardial infarction: insights from a novel preclinical model and cardiovascular magnetic resonance

Non-contrast MR angiography at 1.5 Tesla for aortic monitoring in Marfan patients after aortic root surgery

Feature tracking CMR reveals abnormal strain in preclinical arrhythmogenic right ventricular dysplasia/ cardiomyopathy: a multisoftware feasibility and clinical implementation study

The impact of trans-catheter aortic valve replacement induced left-bundle branch block on cardiac reverse remodeling