Skip to main content

Advertisement

Log in

A Validation of Two-Dimensional In Vivo Regional Strain Computed from Displacement Encoding with Stimulated Echoes (DENSE), in Reference to Tagged Magnetic Resonance Imaging and Studies in Repeatability

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Fast cine displacement encoding with stimulated echoes (DENSE) has comparative advantages over tagged MRI (TMRI) including higher spatial resolution and faster post-processing. This study computed regional radial and circumferential myocardial strains with DENSE displacements and validated it in reference to TMRI, according to American Heart Association (AHA) guidelines for standardized segmentation of regions in the left ventricle (LV). This study was therefore novel in examining agreement between the modalities in 16 AHA recommended LV segments. DENSE displacements were obtained with spatiotemporal phase unwrapping and TMRI displacements obtained with a conventional tag-finding algorithm. A validation study with a rotating phantom established similar shear strain between modalities prior to in vivo studies. A novel meshfree nearest node finite element method (NNFEM) was used for rapid computation of Lagrange strain in both phantom and in vivo studies in both modalities. Also novel was conducting in vivo repeatability studies for observing recurring strain patterns in DENSE and increase confidence in it. Comprehensive regional strain agreements via Bland–Altman analysis between the modalities were obtained. Results from the phantom study showed similar radial-circumferential shear strains from the two modalities. Mean differences in regional in vivo circumferential strains were −0.01 ± 0.09 (95% limits of agreement) from comparing the modalities and −0.01 ± 0.07 from repeatability studies. Differences and means from comparison and repeatability studies were uncorrelated (p > 0.05) indicating no increases in differences with increased strain magnitudes. Bland–Altman analysis and similarities in regional strain distribution within the myocardium showed good agreements between DENSE and TMRI and show their interchangeability. NNFEM was also established as a common framework for computing strain in both modalities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Agarwal, H. K., K. Z. Abd-Elmoniem, and J. L. Prince. Total removal of unwanted harmonic peaks (TruHARP) MRI for single breath-hold high-resolution myocardial motion and strain quantification. Magn. Reson. Med. 64(2):574–585, 2010.

    PubMed Central  PubMed  Google Scholar 

  2. Aletras, A. H., S. Ding, R. S. Balaban, and H. Wen. DENSE: displacement encoding with stimulated echoes in cardiac functional MRI. J. Magn. Reson. 137:247–252, 1999.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Altar, E., and E. R. McVeigh. Optimization of tag thickness for measuring position with magnetic resonance imaging. IEEE Trans. Med. Imaging 13(1):152–160, 1994.

    Article  Google Scholar 

  4. Atkinson, K. A. An Introduction to Numerical Analysis. New York: John Wiley and Sons, p. 108 pp, 1988.

    Google Scholar 

  5. Axel, L., and L. Dougherty. MR imaging of motion with spatial modulation of magnetization. Radiology 171:841–845, 1989.

    CAS  PubMed  Google Scholar 

  6. Babushka, I., U. Banerjee, and J. Osborn. Meshless and generalized finite element methods: a survey of major results. In: Meshfree Methods for Partial Differential Equations, edited by M. Griebel, and M. A. Schweitzer. Berlin: Springer, 2002.

    Google Scholar 

  7. Babushka, I., and B. Q. Guo. The h, p and h-p version of the finite element method; basis theory and applications. Adv. Eng. Softw. 15(3–4):159–174, 1992.

    Article  Google Scholar 

  8. Bayly, P. V., P. G. Massouros, E. Christoforou, A. Sabet, and G. M. Genin. Magnetic resonance measurement of transient shear wave propagation in a viscoelastic gel cylinder. J. Mech. Phys. Solids 56(5):2036–2049, 2008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Bergvall, E., P. Cain, H. Arheden, and G. Sparr. A fast and highly automated approach to myocardial motion analysis using phase contrast magnetic resonance imaging. J. Magn. Res. Imaging 23:652–661, 2006.

    Article  Google Scholar 

  10. Bland, J. M., and D. G. Altman. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 8476:307–310, 1986.

    Article  Google Scholar 

  11. Cerqueira, M. D., N. J. Weissman, V. Dilsizian, A. K. Jacobs, S. Kaul, W. K. Laskey, D. J. Pennell, J. A. Rumberger, T. Ryan, and M. S. Verani. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart: a statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 105:539–542, 2002.

    Article  PubMed  Google Scholar 

  12. Constable, R. T., K. M. Rath, A. J. Sinusas, and J. C. Gore. Development and evaluation of tracking algorithms for cardiac wall motion analysis using phase velocity MR imaging. Magn. Reson. Med. 32:33–42, 1994.

    Article  CAS  PubMed  Google Scholar 

  13. Cupps, B. P., A. K. Taggar, L. M. Reynolds, J. S. Lawton, and M. K. Pasque. Regional myocardial contractile function: multiparametric strain mapping. Interact. Cardiovasc. Thorac. Surg. 10:953–957, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Dougherty, L., J. C. Asmuth, A. S. Blom, L. Axel, and R. Kumar. Validation of an optical flow method for tag displacement estimation. IEEE Trans. Med. Imaging 18(4):359–363, 1999.

    Article  CAS  PubMed  Google Scholar 

  15. Edvardsen, T., B. L. Gerber, J. Garot, D. A. Bluemke, J. A. Lima, and O. A. Smiseth. Quantitative assessment of intrinsic regional myocardial deformation by Doppler strain rate echocardiography in humans: validation against 3-dimensional tagged magnetic resonance imaging. Circulation 106:50–56, 2002.

    Article  PubMed  Google Scholar 

  16. Garot, J., D. A. Bluemke, N. F. Osman, C. E. Rochitte, E. R. McVeigh, E. A. Zerhouni, J. L. Prince, and J. A. C. Lima. Fast determination of regional myocardial strain fields from tagged cardiac images using harmonic phase MRI. Circulation 101:981–988, 2000.

    Article  CAS  PubMed  Google Scholar 

  17. Ghiglia, D. C., and M. D. Pritt. Two-Dimensional Phase Unwrapping: Theory, Algorithms, and Software. New York: Wiley, p. 56 pp, 1998.

    Google Scholar 

  18. Hexeberg, E., D. C. Homans, and R. J. Bache. Interpretation of systolic wall thickening: can thickening of a discrete layer reflect fibre performance? Cardiovasc. Res. 29:16–21, 1995.

    Article  CAS  PubMed  Google Scholar 

  19. Itoh, K. Analysis of the phase unwrapping problem. Appl. Opt. 21(14):2470, 1980.

    Article  Google Scholar 

  20. Jenkinson, M. Fast, automated N-dimensional phase-unwrapping algorithm. Magn. Reson. Med. 48:193–197, 2003.

    Article  Google Scholar 

  21. Kim, D., W. D. Gilson, C. M. Kramer, and F. H. Epstein. Myocardial tissue tracking with 2D cine displacement-encoded MRI—development and initial evaluation. Radiology 230:862–871, 2004.

    Article  PubMed  Google Scholar 

  22. Knutsen, A. K., N. Ma, A. K. Taggar, B. D. Brady, B. P. Cupps, and M. K. Pasque. Heterogeneous distribution of left ventricular contractile injury in chronic aortic insufficiency. Ann. Thorac. Surg. 93:1121–1127, 2012.

    Article  PubMed Central  PubMed  Google Scholar 

  23. Korosoglou, S., P. M. Humpert. Futterer, N. Riedle, D. Lossnitzer, B. Hoerig, H. Steen, E. Giannitsis, N. F. Osman, and H. A. Katus. Strain-encoded cardiac MR during high-dose dobutamine stress testing: comparison to cine imaging and to myocardial tagging. J. Magn. Res. Imaging 29:1053–1061, 2009.

    Article  Google Scholar 

  24. Kreyszig, E. Advanced Engineering Mathematics. New York: Wiley, p. 333 pp, 1997.

    Google Scholar 

  25. Lauterbur, P. C. Image formation by induced local interactions: examples of employing nuclear magnetic resonance. Nature 242(5394):190–191, 1973.

    Article  CAS  Google Scholar 

  26. Liu, G. R. Meshfree Methods: Moving Beyond the Finite Element Method. Boca Raton: CRC Press, 2009.

    Book  Google Scholar 

  27. Lotz, J., C. Meier, A. Leppert, and M. Galanski. Cardiovascular flow measurement with phase-contrast MR imaging: basic facts and implementation. Radiographics 22:651–671, 2002.

    Article  PubMed  Google Scholar 

  28. Lutz, A., A. Bornstedt, R. Manzke, P. Etyngier, G. U. Nienhaus, W. Rottbauer, and V. Rasche. Volumetric motion quantification by 3D tissue phase mapped CMR. J. Cardiovasc. Magn. Reson. 14:74, 2012.

    Article  PubMed  Google Scholar 

  29. Lutz, A., J. Paul, A. Bornstedt, G. U. Nienhaus, P. Etyngier, P. Bernhardt, W. Rottbauer, and V. Rosche. Combination of tagging and tissue phase mapping to accelerate myocardial motion measurements in three directions. Magn. Reson. Mater. Phys. 26:239–247, 2013.

    Article  Google Scholar 

  30. McVeigh, E. R., and E. A. Zerhouni. Noninvasive measurement of transmural gradients in myocardial strain with MR imaging. Radiology 180:677–683, 1991.

    CAS  PubMed Central  PubMed  Google Scholar 

  31. Meyer, F. G., R. T. Constable, A. J. Sinusas, and J. S. Duncan. Tracking myocardial deformation using phase contrast MR velocity fields: a stochastic approach. IEEE Trans. Med. Imaging 15(4):453–465, 1996.

    Article  CAS  PubMed  Google Scholar 

  32. Moore, C. C., S. B. Reeder, and E. R. McVeigh. Tagged MR imaging in a deformable phantom: photographic validation. Radiology 190:765–769, 1994.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Moulton, M. J., L. L. Creswell, S. W. Downing, R. L. Actis, B. A. Szabo, M. W. Vannier, and M. K. Pasque. Spline surface interpolation for calculating 3-D ventricular strains from MRI tissue tagging. Am. J. Physiol. 270:H281–H297, 1996.

    CAS  PubMed  Google Scholar 

  34. Moustakidis, P., B. P. Cupps, B. J. Pomerantz, R. P. Scheri, H. S. Maniar, A. M. Kates, R. J. Gropler, M. K. Pasque, and T. M. Sundt. Noninvasive, quantitative assessment of left ventricular function in ischemic cardiomyopathy. J. Surg. Res. 116:187–196, 2004.

    Article  PubMed  Google Scholar 

  35. Osman, N. F., W. S. Kerwin, E. R. McVeigh, and J. L. Prince. Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging. Magn. Reson. Med. 42:1048–1060, 1999.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Osman, N. F., S. Sampath, E. Atalar, and J. L. Prince. Imaging longitudinal cardiac strain on short-axis images using strain-encoded MRI. Magn. Reson. Med. 46:324–334, 2001.

    Article  CAS  PubMed  Google Scholar 

  37. Sampath, S., J. A. Debryshire, E. Atalar, N. F. Osman, and J. L. Prince. Real-time imaging of two-dimensional cardiac strain using a harmonic phase magnetic resonance imaging (HARP-MRI) pulse sequence. Magn. Reson. Med. 50:154–163, 2003.

    Article  PubMed  Google Scholar 

  38. Shimizu, Y., A. Amano, and T. Matsuda. Oblique 3D MRI tags for the estimation of true 3D cardiac motion parameters. Int. J. Cardiovasc. Imaging 26(8):905–921, 2010.

    Article  PubMed  Google Scholar 

  39. Spottiswoode, B. S., X. Zhong, A. T. Hess, C. M. Kramer, E. M. Meintjes, B. M. Mayosi, and F. H. Epstein. Tracking myocardial motion from cine DENSE images using spatiotemporal phase unwrapping and temporal fitting. IEEE Trans. Med. Imaging 26(1):15–30, 2007.

    Article  CAS  PubMed  Google Scholar 

  40. Spottiswoode, B. S., X. Zhong, C. H. Lorenz, B. Mayosi, E. M. Meintjes, and F. H. Epstein. Motion guided segmentation for cine DENSE MRI. Med. Image Anal. 3(1):105–115, 2009.

    Article  Google Scholar 

  41. Szabo, B. A., and I. Babuska. Finite Element Analysis. New York: Wiley, pp. 57–69, 1991.

    Google Scholar 

  42. Young, A. A., D. L. Kraitchman, L. Dougherty, and L. Axel. Tracking and finite element analysis of stripe deformation in magnetic resonance tagging. IEEE Trans. Med. Imaging 14(3):413–421, 1995.

    Article  CAS  PubMed  Google Scholar 

  43. Young, A. A., B. Li, R. S. Kirton, and B. R. Cowan. Generalized spatiotemporal myocardial strain analysis for DENSE and SPAMM imaging. Magn. Reson. Med. 67:1590–1599, 2012.

    Article  PubMed  Google Scholar 

  44. Zerhouni, E. A., D. M. Parish, W. J. Rogers, A. Yang, and E. P. Shapiro. Human heart: tagging with MR imaging—a method for noninvasive assessment of myocardial motion. Radiology 169:59–63, 1988.

    CAS  PubMed  Google Scholar 

  45. Zhong, X., L. B. Gibberman, B. S. Spottiswoode, A. D. Gilliam, C. H. Meyer, B. A. French, and F. H. Epstein. Comprehensive cardiovascular magnetic resonance of myocardial mechanics in mice using three-dimensional cine DENSE. J. Cardiovasc. Magn. Reson. 13:83–92, 2011.

    Article  PubMed  Google Scholar 

  46. Zhong, X., B. S. Spottiswoode, C. H. Meyer, M. K. Kramer, and F. H. Epstein. Imaging three-dimensional myocardial mechanics using navigator-gated volumetric spiral cine DENSE MRI. Magn. Reson. Med. 64:1089–1097, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Zienkiewicz, O. C., R. L. Taylor, and J. Z. Zhu. The Finite Element Method: Its Basis and Fundamentals. Oxford: Butterworth-Heinemann, p. 54 pp, 2000.

    Google Scholar 

  48. Zwanenburg, J. J., J. P. Kuijer, J. T. Marcus, and R. M. Heethaar. Steady-state free precession with myocardial tagging: CSPAMM in a single breathhold. Magn. Reson. Med. 49(4):722–730, 2003.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to Ms. Lina Reynolds and Ms. Beckah Brady for their active role in recruiting healthy subjects for our study. We also thank Siemens (Dr. Xiaodong Zhong) for the imaging software for DENSE. This study was partly funded by NIH Grant R01 HL112804.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia Kar.

Additional information

Associate Editor Jane Grande-Allen oversaw the review of this article.

Appendix A

Appendix A

Radial-circumferential shear strain (ε rθ ) calculated using two different FEA techniques which were (left) nearest neighbor finite element method (NNFEM) and (right) Measurement Analysis (MEA). MEA involved division into six unequal tetrahedron elements in the same way a single 2D myocardial slice is segmented.

figure a
Table A1 Regional radial-circumferential shear strain (ε rθ ) values using NNFEM and MEA

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kar, J., Knutsen, A.K., Cupps, B.P. et al. A Validation of Two-Dimensional In Vivo Regional Strain Computed from Displacement Encoding with Stimulated Echoes (DENSE), in Reference to Tagged Magnetic Resonance Imaging and Studies in Repeatability. Ann Biomed Eng 42, 541–554 (2014). https://doi.org/10.1007/s10439-013-0931-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-013-0931-2

Keywords

Navigation