Abstract
Objectives
To validate deformable registration algorithms (DRAs) for cine balanced steady-state free precession (bSSFP) assessment of global longitudinal strain (GLS) and global circumferential strain (GCS) using harmonic phase (HARP) cardiovascular magnetic resonance as standard of reference (SoR).
Methods
Seventeen patients and 17 volunteers underwent short axis stack and 2-/4-chamber cine bSSFP imaging with matching slice long-axis and mid-ventricular spatial modulation of magnetization (SPAMM) myocardial tagging. Inverse DRA was applied on bSSFP data for assessment of GLS and GCS while myocardial tagging was processed using HARP. Intra- and inter-observer variability assessment was based on repeated analysis by a single observer and analysis by a second observer, respectively. Standard semi-automated short axis stack segmentation was performed for analysis of left ventricular (LV) volumes and ejection fraction (EF).
Results
DRA demonstrated strong relationships to HARP for myocardial GLS (R2 = 0.75; p < 0.0001) and endocardial GLS (R2 = 0.61; p < 0.0001). GCS result comparison also demonstrated significant relationships between DRA and HARP for myocardial strain (R2 = 0.61; p < 0.0001) and endocardial strain (R2 = 0.51; p < 0.0001). Both methods demonstrated small systematic errors for intra- and inter-observer variability but DRA demonstrated consistently lower CV. Global LVEF was significantly lower (p = 0.0099) in patients (53.7%; IQR 43.9/64.0%) than in healthy volunteers (62.6%; IQR 61.1/66.2%). DRA and HARP strain data demonstrated significant relationships to LVEF.
Conclusions
Non-rigid deformation method–based DRA provides a reliable measure of peak systolic GCS and GLS based on cine bSSFP with superior intra- and inter-observer reproducibility compared to HARP.
Key Point
• Myocardial strain can be reliably analyzed using inverse deformable registration algorithms (DRAs) on cine CMR.
• Inverse DRA-derived strain shows higher reproducibility than tagged CMR.
• DRA and tagged CMR-based myocardial strain demonstrate strong relationships to global left ventricular function.
Similar content being viewed by others
Abbreviations
- BSA:
-
Body surface area
- bSSFP:
-
Balanced steady-state free precession
- CMR:
-
Cardiovascular magnetic resonance
- CV:
-
Coefficient of variation
- DENSE:
-
Displacement encoding with stimulated echoes
- DRA:
-
Deformable registration algorithms
- EDV:
-
End-diastolic volume
- EF:
-
Ejection fraction
- ESV:
-
End-systolic volume
- FLASH:
-
Fast low angle shot
- FT:
-
Feature tracking
- GCS:
-
Global circumferential strain
- GLS:
-
Global longitudinal strain
- GRAPPA:
-
Generalized autocalibrating partial parallel acquisition
- GRS:
-
Global radial strain
- HARP:
-
Harmonic phase
- IQR:
-
Interquartile range
- LV:
-
Left ventricle
- LVEF:
-
Left ventricular ejection fraction
- MASS:
-
Myocardial mass
- REB:
-
Research Ethics Board
- SENC:
-
Strain encoded
- SoR:
-
Standard of reference
- SPAMM:
-
Spatial modulation of magnetization
- SV:
-
Stroke volume
- TPM:
-
Tissue phase mapping
References
Sanderson JE (2007) Heart failure with a normal ejection fraction. Heart 93:155–158
Sjøli B, Ørn S, Grenne B et al (2009) Comparison of left ventricular ejection fraction and left ventricular global strain as determinants of infarct size in patients with acute myocardial infarction. J Am Soc Echocardiogr 22:1232–1238
Pattynama PM, De Roos A, Van der Wall EE, Van Voorthuisen AE (1994) Evaluation of cardiac function with magnetic resonance imaging. Am Heart J 128:595–607
Kalam K, Otahal P, Marwick TH (2014) Prognostic implications of global LV dysfunction: a systematic review and meta-analysis of global longitudinal strain and ejection fraction. Heart 100:1673–1680
Mordi I, Bezerra H, Carrick D, Tzemos N (2015) The combined incremental prognostic value of LVEF, late gadolinium enhancement, and global circumferential strain assessed by CMR. JACC Cardiovasc Imaging 8:540–549
Solomon SD, Anavekar N, Skali H et al (2005) Influence of ejection fraction on cardiovascular outcomes in a broad spectrum of heart failure patients. Circulation 112:3738–3744
Smedsrud MK, Pettersen E, Gjesdal O et al (2011) Detection of left ventricular dysfunction by global longitudinal systolic strain in patients with chronic aortic regurgitation. J Am Soc Echocardiogr 24:1253–1259
Zerhouni EA, Parish DM, Rogers WJ, Yang A, Shapiro EP (1988) Human heart: tagging with MR imaging--a method for noninvasive assessment of myocardial motion. Radiology 169:59–63
Young AA, Axel L, Dougherty L, Bogen DK, Parenteau CS (1993) Validation of tagging with MR imaging to estimate material deformation. Radiology 188:101–108
Osman NF, Sampath S, Atalar E, Prince JL (2001) Imaging longitudinal cardiac strain on short-axis images using strain-encoded MRI. Magn Reson Med 46:324–334
Aletras AH, Ding S, Balaban RS, Wen H (1999) DENSE: displacement encoding with stimulated echoes in cardiac functional MRI. J Magn Reson 137:247–252
Codreanu I, Pegg TJ, Selvanayagam JB et al (2014) Normal values of regional and global myocardial wall motion in young and elderly individuals using navigator gated tissue phase mapping. Age (Dordr) 36:231–241
Osman NF, Kerwin WS, McVeigh ER, Prince JL (1999) Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging. Magn Reson Med 42:1048–1060
Axel L, Dougherty L (1989) MR imaging of motion with spatial modulation of magnetization. Radiology 171:841–845
Kuetting D, Sprinkart AM, Doerner J, Schild H, Thomas D (2015) Comparison of magnetic resonance feature tracking with harmonic phase imaging analysis (CSPAMM) for assessment of global and regional diastolic function. Eur J Radiol 84:100–107
Onishi T, Saha SK, Ludwig DR et al (2013) Feature tracking measurement of dyssynchrony from cardiovascular magnetic resonance cine acquisitions: comparison with echocardiographic speckle tracking. J Cardiovasc Magn Reson 15:95
Kempny A, Fernández-Jiménez R, Orwat S et al (2012) Quantification of biventricular myocardial function using cardiac magnetic resonance feature tracking, endocardial border delineation and echocardiographic speckle tracking in patients with repaired tetralogy of Fallot and healthy controls. J Cardiovasc Magn Reson 14:32
Hor KN, Baumann R, Pedrizzetti G et al (2011) Magnetic resonance derived myocardial strain assessment using feature tracking. J Vis Exp. https://doi.org/10.3791/2356
Collins JD (2015) Global and regional functional assessment of ischemic heart disease with cardiac MR imaging. Radiol Clin North Am 53:369–395
Onishi T, Saha SK, Delgado-Montero A et al (2015) Global longitudinal strain and global circumferential strain by speckle-tracking echocardiography and feature-tracking cardiac magnetic resonance imaging: comparison with left ventricular ejection fraction. J Am Soc Echocardiogr. https://doi.org/10.1016/j.echo.2014.11.018
Augustine D, Lewandowski AJ, Lazdam M et al (2013) Global and regional left ventricular myocardial deformation measures by magnetic resonance feature tracking in healthy volunteers: comparison with tagging and relevance of gender. J Cardiovasc Magn Reson 15:8
Lamacie MM, Thavendiranathan P, Hanneman K et al (2017) Quantification of global myocardial function by cine MRI deformable registration-based analysis: comparison with MR feature tracking and speckle-tracking echocardiography. Eur Radiol 27:1404–1415
Keller EJ, Fang S, Lin K et al (2017) The consistency of myocardial strain derived from heart deformation analysis. Int J Cardiovasc Imaging 33:1169–1177
Doesch C, Papavassiliu T, Michaely HJ et al (2013) Detection of myocardial ischemia by automated, motion-corrected, color-encoded perfusion maps compared with visual analysis of adenosine stress cardiovascular magnetic resonance imaging at 3 T: a pilot study. Invest Radiol 48:678–686
Jolly MP, Jordan JH, Meléndez GC, McNeal GR, D'Agostino RB Jr, Hundley WG (2017) Automated assessments of circumferential strain from cine CMR correlate with LVEF declines in cancer patients early after receipt of cardio-toxic chemotherapy. J Cardiovasc Magn Reson 19:59
Osman NF, McVeigh ER, Prince JL (2000) Imaging heart motion using harmonic phase MRI. IEEE Trans Med Imaging 19:186–202
Castillo E, Osman NF, Rosen BD et al (2005) Quantitative assessment of regional myocardial function with MR-tagging in a multi-center study: interobserver and intraobserver agreement of fast strain analysis with harmonic phase (HARP) MRI. J Cardiovasc Magn Reson 7:783–791
Simpson RM, Keegan J, Firmin DN (2013) MR assessment of regional myocardial mechanics. J Magn Reson Imaging 37:576–599
Lu JC, Connelly JA, Zhao L, Agarwal PP, Dorfman AL (2014) Strain measurement by cardiovascular magnetic resonance in pediatric cancer survivors: validation of feature tracking against harmonic phase imaging. Pediatr Radiol 44:1070–1076
Hor KN, Gottliebson WM, Carson C et al (2010) Comparison of magnetic resonance feature tracking for strain calculation with harmonic phase imaging analysis. JACC Cardiovasc Imaging 3:144–151
Schuster A, Kutty S, Padiyath A et al (2011) Cardiovascular magnetic resonance myocardial feature tracking detects quantitative wall motion during dobutamine stress. J Cardiovasc Magn Reson 13:58
Schuster A, Stahnke VC, Unterberg-Buchwald C et al (2015) Cardiovascular magnetic resonance feature-tracking assessment of myocardial mechanics: Intervendor agreement and considerations regarding reproducibility. Clin Radiol 70:989–998
Barreiro-Pérez M, Curione D, Symons R, Claus P, Voigt JU, Bogaert J (2018) Left ventricular global myocardial strain assessment comparing the reproducibility of four commercially available CMR-feature tracking algorithms. Eur Radiol. https://doi.org/10.1007/s00330-018-5538-4
Hor KN, Wansapura J, Markham LW et al (2009) Circumferential strain analysis identifies strata of cardiomyopathy in Duchenne muscular dystrophy: a cardiac magnetic resonance tagging study. J Am Coll Cardiol 53:1204–1210
Feisst A, Kuetting DLR, Dabir D et al (2018) Influence of observer experience on cardiac magnetic resonance strain measurements using feature tracking and conventional tagging. Int J Cardiol Heart Vasc 18:46–51
Shehata ML, Cheng S, Osman NF, Bluemke DA, Lima JA (2009) Myocardial tissue tagging with cardiovascular magnetic resonance. J Cardiovasc Magn Reson 11:55
Venkatesh BA, Donekal S, Yoneyama K et al (2015) Regional myocardial functional patterns: quantitative tagged magnetic resonance imaging in an adult population free of cardiovascular risk factors: the multi-ethnic study of atherosclerosis (MESA). J Magn Reson Imaging 42:153–159
Acknowledgments
Results of this study have in part been presented at RSNA 2017 (oral presentation).
Funding
The authors state that this work has not received any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is Dr. Bernd J. Wintersperger.
Conflict of interest
The authors of this manuscript declare relationships with the following companies:
Bernd J. Wintersperger, Research Support Siemens Healthineers
Bernd J. Wintersperger, Speakers Honorarium Siemens Healthineers
Andreas Greiser, Employee Siemens Healthineers, Erlangen, Germany
Marie-Pierre Jolly, Employee (former, at time of study) Siemens Healthineers, Medical Imaging Technologies, Princeton, NJ, USA
The study was performed under a Master Research Agreement (MRA) between the University Health Network and Siemens Healthineers.
Statistics and biometry
One of the authors has significant statistical expertise (Dr. Thavendiranathan).
Informed consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical approval
Institutional Review Board approval was obtained.
Methodology
• prospective
• case-control study
• performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lamacie, M.M., Houbois, C.P., Greiser, A. et al. Quantification of myocardial deformation by deformable registration–based analysis of cine MRI: validation with tagged CMR. Eur Radiol 29, 3658–3668 (2019). https://doi.org/10.1007/s00330-019-06019-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-019-06019-9