This overview will discuss expectations, solutions, advantages and limitations related to measuring perfusion in the human heart without contrast agents. The major existing approaches to Arterial Spin Labeling (ASL) in the heart will be outlined. The reasons why myocardial ASL is challenging compared with other organs will be outlined. It should also become clear why cardiac ASL is a well-working and validated method in the rodent heart whereas human applications are still scarce.
Objectives
Purpose
This talk will give an overview over expectations, solutions, advantages and limitations related to measuring perfusion in the heart without contrast agents. I will discuss the major existing approaches to Arterial Spin Labeling (ASL) in the heart, but also recall coronary sinus flow measurements as an alternative. The reasons why myocardial ASL is challenging compared with other organs will be outlined. It should also become clear why cardiac ASL is a well-working and validated method in the rodent heart whereas human applications are still scarce.
Patient populations with cardiac disease (and heart failure in particular) also over-proportionally expose kidney failure, which is why many centers are reluctant to using contrast agents especially in these populations. Left aside the known contrast-agent-related risks, non-contrast myocardial perfusion techniques might also open new ways of improving quantification accuracy due to their ease of use and due to their free repeatability within an MRI exam. These arguments have been motivating developments in cardiac ASL despite the technical challenges.
Methods and Results
Flow-sensitive alternating recovery (FAIR) ASL techniques with various modifications have been proposed and shown feasible in the human heart since the late 90’s (1,2) when the signal-efficient balanced SSFP methods had not yet found their entry in cardiovascular MRI. The first results were considered reliable only under pharmacologic stress conditions, when myocardial blood flow is high. Since then, developments have taken advantage of more efficient readout schemes (3), and the origins of variability in the measured blood flow were analyzed more thoroughly (4). More recently, different labeling approaches are being explored such as velocity-selective labeling (VS-ASL) (5) or steady-pulsed labeling (spASL) (6,7) under free breathing to make the acquisition as efficient as possible and to benefit from a steady labeling despite the strongly pulsatile blood flow in cardiac vessels. Breathing-motion correction methods are being used for both free breathing and breath-hold techniques (8). Finally, it is noteworthy that global myocardial perfusion can also be estimated using coronary sinus flow quantification via phase contrast cine-MRI (9,10). In parallel to these developments for the human heart, a variety of cardiac ASL methods have been developed specifically for rodent myocardial perfusion mapping (11–15). Due to higher heart rate and blood flow in rodents than in humans, these methods have quickly become stable, and they are now routinely used for exploring pathologies in animal models.1. Poncelet BP, Koelling TM, Schmidt CJ, Kwong KK, Reese TG, Ledden P, Kantor HL, Brady TJ, Weisskoff RM. Measurement of human myocardial perfusion by double-gated flow alternating inversion recovery EPI. Magn Reson Med 1999;41:510–9.
2. Wacker CM, Fidler F, Dueren C, Hirn S, Jakob PM, Ertl G, Haase A, Bauer WR. Quantitative assessment of myocardial perfusion with a spin-labeling technique: preliminary results in patients with coronary artery disease. J Magn Reson Imaging 2003;18:555–60. doi: 10.1002/jmri.10386.
3. Northrup BE, McCommis KS, Zhang H, Ray S, Woodard PK, Gropler RJ, Zheng J. Resting myocardial perfusion quantification with CMR arterial spin labeling at 1.5 T and 3.0 T. J Cardiovasc Magn Reson 2008;10:53. doi: 10.1186/1532-429X-10-53.
4. Zun Z, Wong EC, Nayak KS. Assessment of myocardial blood flow (MBF) in humans using arterial spin labeling (ASL): feasibility and noise analysis. Magn Reson Med 2009;62:975–983. doi: 10.1002/mrm.22088.
5. Jao TR, Nayak KS. Demonstration of velocity selective myocardial arterial spin labeling perfusion imaging in humans. Magn Reson Med 2018;80:272–278. doi: 10.1002/mrm.26994.
6. Capron T, Troalen T, Robert B, Jacquier A, Bernard M, Kober F. Myocardial perfusion assessment in humans using steady-pulsed arterial spin labeling. Magn. Reson. Med. 2015;74:990–998. doi: 10.1002/mrm.25479. 7. Capron T, Troalen T, Cozzone PJ, Bernard M, Kober F. Cine-ASL: A steady-pulsed arterial spin labeling method for myocardial perfusion mapping in mice. Part II. Theoretical model and sensitivity optimization. Magnetic Resonance in Medicine 2013;70:1399–1408. doi: 10.1002/mrm.24588.
8. Aramendía-Vidaurreta V, García-Osés A, Vidorreta M, Bastarrika G, Fernández-Seara MA. Optimal repetition time for free breathing myocardial arterial spin labeling. NMR Biomed 2019:e4077. doi: 10.1002/nbm.4077.
9. Lund GK, Wendland MF, Shimakawa A, Arheden H, Ståhlberg F, Higgins CB, Saeed M. Coronary sinus flow measurement by means of velocity-encoded cine MR imaging: validation by using flow probes in dogs. Radiology 2000;217:487–493. doi: 10.1148/radiology.217.2.r00nv10487.
10. Moro P-J, Jacquier A, Kober F, Bonnet J-L, Cozzone P, Bernard M. Coronary sinus flow quantification at 3T and cold pressor test for non invasive evaluation of coronary endothelial function. In: Proc. Intl. Soc. Mag. Reson. Med. 18. 18th Annual Meeting of the International Society for Magnetic Resonance in Medicine, Stockholm, Sweden, 1-7 May. ; 2010. p. 3669.
11. Belle V, Kahler E, Waller C, Rommel E, Voll S, Hiller K, Bauer W, Haase A. In vivo quantitative mapping of cardiac perfusion in rats using a noninvasive MR spin-labeling method. J Magn Reson Imaging 1998;8:1240–5.
12. Kober F, Iltis I, Izquierdo M, Desrois M, Ibarrola D, Cozzone PJ, Bernard M. High-resolution myocardial perfusion mapping in small animals in vivo by spin-labeling gradient-echo imaging. Magn Reson Med 2004;51:62–67. doi: 10.1002/mrm.10676.
13. Vandsburger MH, Janiczek RL, Xu Y, French BA, Meyer CH, Kramer CM, Epstein FH. 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;63:648–57. doi: 10.1002/mrm.22280.
14. Campbell-Washburn AE, Price AN, Wells JA, Thomas DL, Ordidge RJ, Lythgoe MF. Cardiac arterial spin labeling using segmented ECG-gated Look-Locker FAIR: variability and repeatability in preclinical studies. Magn Reson Med 2013;69:238–247. doi: 10.1002/mrm.24243.
15. Troalen T, Capron T, Cozzone PJ, Bernard M, Kober F. Cine-ASL: A steady-pulsed arterial spin labeling method for myocardial perfusion mapping in mice. Part I. Experimental study. Magnetic Resonance in Medicine 2013;70:1389–1398. doi: 10.1002/mrm.24565.
16. Zun Z, Varadarajan P, Pai RG, Wong EC, Nayak KS. Arterial Spin Labeled CMR Detects Clinically Relevant Increase in Myocardial Blood Flow With Vasodilation. JACC: Cardiovascular Imaging 2011;4:1253–1261. doi: 10.1016/j.jcmg.2011.06.023.