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The Correlation of 3D DT-MRI Fiber Disruption with Structural and Mechanical Degeneration in Porcine Myocardium

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Abstract

Evaluation of structural parameters following a myocardial infarction (MI) is important to assess left ventricular function and remodeling. In this study, we assessed the capability of 3D diffusion tensor magnetic resonance imaging (DT-MRI) to assess tissue degeneration shortly after an MI using a porcine model of infarction. Two days after an induced infarction, hearts were explanted and immediately scanned by a 3T MRI scanner with a diffusion tensor imaging protocol. 3D fiber tracks and clustering models were generated from the diffusion-weighted imaging data. We found in a normal explanted heart that DT-MRI fibers showed a multilayered helical structure, with fiber architecture and fiber density reflecting the integrity of muscle fibers. For infarcted heart explants, we observed either a lack of fibers or disruption of fibers in the infarcted regions. Contours of the disrupted DT-MRI fibers were found to be consistent with the infarcted regions. Both histological and mechanical analysis of the infarcted hearts suggested DT-MRI fiber disruption correlated with altered microstructure and tissue mechanics. The ability of 3D DT-MRI to accurately distinguish viable myocardium from dead myocardium only 2 days post infarct without the use of radioisotopes or ionotropic agents makes it a promising approach to evaluate cardiac damage early post-MI.

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References

  1. American Heart Association. Heart and Stroke Statistical Update. Dallas, TX: American Heart Association, 2002.

  2. Baer, F. M., P. Theissen, C. A. Schneider, K. Kettering, E. Voth, U. Sechtem, and H. Schicha. MRI assessment of myocardial viability: comparison with other imaging techniques. Rays 24(1):96–108, 1999.

    CAS  PubMed  Google Scholar 

  3. Baer, F. M., P. Theissen, C. A. Schneider, E. Voth, U. Sechtem, H. Schicha, and E. Erdmann. Dobutamine magnetic resonance imaging predicts contractile recovery of chronically dysfunctional myocardium after successful revascularization. J. Am. Coll. Cardiol. 31(5):1040–1048, 1998.

    Article  CAS  PubMed  Google Scholar 

  4. Basser, P. J., J. Mattiello, and D. LeBihan. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B 103(3):247–254, 1994.

    Article  CAS  PubMed  Google Scholar 

  5. Basser, P. J., S. Pajevic, C. Pierpaoli, J. Duda, and A. Aldroubi. In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 44(4):625–632, 2000.

    Article  CAS  PubMed  Google Scholar 

  6. Bavelaar-Croon, C. D., H. W. Kayser, E. E. van der Wall, A. de Roos, P. Dibbets-Schneider, E. K. Pauwels, G. Germano, and D. E. Atsma. Left ventricular function: correlation of quantitative gated SPECT and MR imaging over a wide range of values. Radiology 217(2):572–575, 2000.

    CAS  PubMed  Google Scholar 

  7. Behrens, T. E., H. Johansen-Berg, M. W. Woolrich, S. M. Smith, C. A. Wheeler-Kingshott, P. A. Boulby, G. J. Barker, E. L. Sillery, K. Sheehan, O. Ciccarelli, A. J. Thompson, J. M. Brady, and P. M. Matthews. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6(7):750–757, 2003.

    Article  CAS  PubMed  Google Scholar 

  8. Chen, W., Z. Yan, S. Zhang, J. A. Crow, D. S. Ebert, R. McLaughlin, K. B. Mullins, R. Cooper, Z. Ding, and J. Liao. Volume illustration of muscle from diffusion tensor images. IEEE Trans. Vis. Comput. Graph. 15(6):1425–1432, 2009.

    Article  PubMed  Google Scholar 

  9. Cigarroa, C. G., C. R. de Filippi, M. E. Brickner, L. G. Alvarez, M. A. Wait, and P. A. Grayburn. Dobutamine stress echocardiography identifies hibernating myocardium and predicts recovery of left ventricular function after coronary revascularization. Circulation 88(2):430–436, 1993.

    CAS  PubMed  Google Scholar 

  10. Cwajg, J. M., E. Cwajg, S. F. Nagueh, Z. X. He, U. Qureshi, L. I. Olmos, M. A. Quinones, M. S. Verani, W. L. Winters, and W. A. Zoghbi. End-diastolic wall thickness as a predictor of recovery of function in myocardial hibernation: relation to rest-redistribution T1-201 tomography and dobutamine stress echocardiography. J. Am. Coll. Cardiol. 35(5):1152–1161, 2000.

    Article  CAS  PubMed  Google Scholar 

  11. Dou, J., T. G. Reese, W. Y. Tseng, and V. J. Wedeen. Cardiac diffusion MRI without motion effects. Magn. Reson. Med. 48(1):105–114, 2002.

    Article  PubMed  Google Scholar 

  12. Dou, J., W. Y. Tseng, T. G. Reese, and V. J. Wedeen. Combined diffusion and strain MRI reveals structure and function of human myocardial laminar sheets in vivo. Magn. Reson. Med. 50(1):107–113, 2003.

    Article  PubMed  Google Scholar 

  13. Etoh, T., C. Joffs, A. M. Deschamps, J. Davis, K. Dowdy, J. Hendrick, S. Baicu, R. Mukherjee, M. Manhaini, and F. G. Spinale. Myocardial and interstitial matrix metalloproteinase activity after acute myocardial infarction in pigs. Am. J. Physiol. Heart Circ. Physiol. 281(3):H987–H994, 2001.

    CAS  PubMed  Google Scholar 

  14. Fishbein, M. C., D. Maclean, and P. R. Maroko. The histopathologic evolution of myocardial infarction. Chest 73(6):843–849, 1978.

    Article  CAS  PubMed  Google Scholar 

  15. Forrester, J. S., G. Diamond, W. W. Parmley, and H. J. Swan. Early increase in left ventricular compliance after myocardial infarction. J. Clin. Invest. 51(3):598–603, 1972.

    Article  CAS  PubMed  Google Scholar 

  16. Goldberg, R. J., J. M. Gore, J. S. Alpert, V. Osganian, J. de Groot, J. Bade, Z. Chen, D. Frid, and J. E. Dalen. Cardiogenic shock after acute myocardial infarction. Incidence and mortality from a community-wide perspective, 1975 to 1988. N. Engl. J. Med. 325(16):1117–1122, 1991.

    Article  CAS  PubMed  Google Scholar 

  17. Grashow, J. S., A. P. Yoganathan, and M. S. Sacks. Biaxial stress–stretch behavior of the mitral valve anterior leaflet at physiologic strain rates. Ann. Biomed. Eng. 34(2):315–325, 2006.

    Article  PubMed  Google Scholar 

  18. Holmes, J. W., T. K. Borg, and J. W. Covell. Structure and mechanics of healing myocardial infarcts. Annu. Rev. Biomed. Eng. 7:223–253, 2005.

    Article  CAS  PubMed  Google Scholar 

  19. Holmes, A. A., D. F. Scollan, and R. L. Winslow. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn. Reson. Med. 44(1):157–161, 2000.

    Article  CAS  PubMed  Google Scholar 

  20. Hoyt, R. H., M. L. Cohen, and J. E. Saffitz. Distribution and three-dimensional structure of intercellular junctions in canine myocardium. Circ. Res. 64(3):563–574, 1989.

    CAS  PubMed  Google Scholar 

  21. Hsu, E. W., and C. S. Henriquez. Myocardial fiber orientation mapping using reduced encoding diffusion tensor imaging. J. Cardiovasc. Magn. Reson. 3(4):339–347, 2001.

    Article  CAS  PubMed  Google Scholar 

  22. Hsu, E. W., A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am. J. Physiol. 274(5 Pt 2):H1627–H1634, 1998.

    CAS  PubMed  Google Scholar 

  23. Hunter, P. J., B. H. Smaill, P. Nielsen, and I. J. L. Grice. Chapter 6: A mathematical model of cardiac anatomy. In: Computational Biology of the Heart. J. Wiley, 1996.

  24. Kim, R. J., D. S. Fieno, T. B. Parrish, K. Harris, E. L. Chen, O. Simonetti, J. Bundy, J. P. Finn, F. J. Klocke, and R. M. Judd. Relationship of MRI delayed contrast enhancement to irreversible injury, infarct age, and contractile function. Circulation 100(19):1992–2002, 1999.

    CAS  PubMed  Google Scholar 

  25. Kim, R. J., E. Wu, A. Rafael, E. L. Chen, M. A. Parker, O. Simonetti, F. J. Klocke, R. O. Bonow, and R. M. Judd. The use of contrast-enhanced magnetic resonance imaging to identify reversible myocardial dysfunction. N. Engl. J. Med. 343(20):1445–1453, 2000.

    Article  CAS  PubMed  Google Scholar 

  26. Kubicki, M., C. F. Westin, S. E. Maier, H. Mamata, M. Frumin, H. Ersner-Hershfield, R. Kikinis, F. A. Jolesz, R. McCarley, and M. E. Shenton. Diffusion tensor imaging and its application to neuropsychiatric disorders. Harv. Rev. Psychiatry 10(6):324–336, 2002.

    Article  PubMed  Google Scholar 

  27. Leor, J., S. Aboulafia-Etzion, A. Dar, L. Shapiro, I. M. Barbash, A. Battler, Y. Granot, and S. Cohen. Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium? Circulation 102(19 Suppl. 3):III56–III61, 2000.

    CAS  PubMed  Google Scholar 

  28. Liao, J., E. M. Joyce, and M. S. Sacks. Effects of decellularization on mechanical and structural properties of the porcine aortic valve leaflets. Biomaterials 29(8):1065–1074, 2008.

    Article  CAS  PubMed  Google Scholar 

  29. Lim, K. O., and J. A. Helpern. Neuropsychiatric applications of DTI—a review. NMR Biomed. 15(7–8):587–593, 2002.

    Article  CAS  PubMed  Google Scholar 

  30. Lipton, M. J., C. B. Higgins, and D. P. Boyd. Computed tomography of the heart: evaluation of anatomy and function. J. Am. Coll. Cardiol. 5(1 Suppl):55S–69S, 1985.

    Article  CAS  PubMed  Google Scholar 

  31. Mahnken, A. H., P. Bruners, S. Kinzel, M. Katoh, G. Muhlenbruch, R. W. Gunther, and J. E. Wildberger. Late-phase MSCT in the different stages of myocardial infarction: animal experiments. Eur. Radiol. 17(9):2310–2317, 2007.

    Article  PubMed  Google Scholar 

  32. O’Sullivan, M., D. K. Jones, P. E. Summers, R. G. Morris, S. C. Williams, and H. S. Markus. Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology 57(4):632–638, 2001.

    PubMed  Google Scholar 

  33. Peters, N. S., J. Coromilas, N. J. Severs, and A. L. Wit. Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 95(4):988–996, 1997.

    CAS  PubMed  Google Scholar 

  34. Pfefferbaum, A., E. V. Sullivan, M. Hedehus, K. O. Lim, E. Adalsteinsson, and M. Moseley. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn. Reson. Med. 44(2):259–268, 2000.

    Article  CAS  PubMed  Google Scholar 

  35. Pirzada, F. A., E. A. Ekong, P. S. Vokonas, C. S. Apstein, and W. B. Hood, Jr. Experimental myocardial infarction. XIII. Sequential changes in left ventricular pressure-length relationships in the acute phase. Circulation 53(6):970–975, 1976.

    CAS  PubMed  Google Scholar 

  36. Reddy, V. Y., D. Wrobleski, C. Houghtaling, M. E. Josephson, and J. N. Ruskin. Combined epicardial and endocardial electroanatomic mapping in a porcine model of healed myocardial infarction. Circulation 107(25):3236–3242, 2003.

    Article  PubMed  Google Scholar 

  37. Rohmer, D., A. Sitek, and G. T. Gullberg. Reconstruction and visualization of fiber and laminar structure in the normal human heart from ex vivo diffusion tensor magnetic resonance imaging (DTMRI) data. Invest. Radiol. 42(11):777–789, 2007.

    Article  PubMed  Google Scholar 

  38. Sacks, M. S., and C. J. Chuong. Biaxial mechanical properties of passive right ventricular free wall myocardium. J. Biomech. Eng. 115:202–205, 1992.

    Article  Google Scholar 

  39. Sato, S., M. Ashraf, R. W. Millard, H. Fujiwara, and A. Schwartz. Connective tissue changes in early ischemia of porcine myocardium: an ultrastructural study. J. Mol. Cell. Cardiol. 15(4):261–275, 1983.

    Article  CAS  PubMed  Google Scholar 

  40. Scollan, D. F., A. Holmes, R. Winslow, and J. Forder. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am. J. Physiol. 275(6 Pt 2):H2308–H2318, 1998.

    CAS  PubMed  Google Scholar 

  41. Simon, J. H., S. Zhang, D. H. Laidlaw, D. E. Miller, M. Brown, J. Corboy, and J. Bennett. Identification of fibers at risk for degeneration by diffusion tractography in patients at high risk for MS after a clinically isolated syndrome. J. Magn. Reson. Imaging 24(5):983–988, 2006.

    Article  PubMed  Google Scholar 

  42. Slart, R. H., J. J. Bax, R. M. de Jong, J. de Boer, H. J. Lamb, P. H. Mook, A. T. Willemsen, W. Vaalburg, D. J. van Veldhuisen, and P. L. Jager. Comparison of gated PET with MRI for evaluation of left ventricular function in patients with coronary artery disease. J. Nucl. Med. 45(2):176–182, 2004.

    PubMed  Google Scholar 

  43. Smart, S. C., S. Sawada, T. Ryan, D. Segar, L. Atherton, K. Berkovitz, P. D. Bourdillon, and H. Feigenbaum. Low-dose dobutamine echocardiography detects reversible dysfunction after thrombolytic therapy of acute myocardial infarction. Circulation 88(2):405–415, 1993.

    CAS  PubMed  Google Scholar 

  44. Smith, R. R., L. Barile, H. C. Cho, M. K. Leppo, J. M. Hare, E. Messina, A. Giacomello, M. R. Abraham, and E. Marban. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7):896–908, 2007.

    Article  PubMed  Google Scholar 

  45. Sosnovik, D. E., R. Wang, G. Dai, T. Wang, E. Aikawa, M. Novikov, A. Rosenzweig, R. J. Gilbert, and V. J. Wedeen. Diffusion spectrum MRI tractography reveals the presence of a complex network of residual myofibers in infarcted myocardium. Circ. Cardiovasc. Imaging 2(3):206–212, 2009.

    Article  PubMed  Google Scholar 

  46. Sundgren, P. C., Q. Dong, D. Gomez-Hassan, S. K. Mukherji, P. Maly, and R. Welsh. Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 46(5):339–350, 2004.

    Article  CAS  PubMed  Google Scholar 

  47. Swynghedauw, B. Molecular mechanisms of myocardial remodeling. Physiol. Rev. 79(1):215–262, 1999.

    CAS  PubMed  Google Scholar 

  48. Tio, R. A., E. S. Tan, G. A. Jessurun, N. Veeger, P. L. Jager, R. H. Slart, R. M. de Jong, J. Pruim, G. A. Hospers, A. T. Willemsen, M. J. de Jongste, A. J. van Boven, D. J. van Veldhuisen, and F. Zijlstra. PET for evaluation of differential myocardial perfusion dynamics after VEGF gene therapy and laser therapy in end-stage coronary artery disease. J. Nucl. Med. 45(9):1437–1443, 2004.

    PubMed  Google Scholar 

  49. Tseng, W. Y., T. G. Reese, R. M. Weisskoff, T. J. Brady, and V. J. Wedeen. Myocardial fiber shortening in humans: initial results of MR imaging. Radiology 216(1):128–139, 2000.

    CAS  PubMed  Google Scholar 

  50. Tseng, W. Y., T. G. Reese, R. M. Weisskoff, and V. J. Wedeen. Cardiac diffusion tensor MRI in vivo without strain correction. Magn. Reson. Med. 42(2):393–403, 1999.

    Article  CAS  PubMed  Google Scholar 

  51. Urasawa, K., S. Kakinoki, I. Sakuma, K. Kanamori, S. Sakamoto, and H. Yasuda. Analysis of ventricular wall motion using multislice ECG-gated cardiac X-ray CT: application of the three-dimensional reconstruction technique. J. Cardiogr. 16(1):19–32, 1986.

    CAS  PubMed  Google Scholar 

  52. Vokonas, P. S., F. Pirzada, and W. B. Hood, Jr. Experimental myocardial infarction: XII. Dynamic changes in segmental mechanical behavior of infarcted and non-infarcted myocardium. Am. J. Cardiol. 37(6):853–859, 1976.

    Article  CAS  PubMed  Google Scholar 

  53. Westerhausen, R., C. Walter, F. Kreuder, R. A. Wittling, E. Schweiger, and W. Wittling. The influence of handedness and gender on the microstructure of the human corpus callosum: a diffusion-tensor magnetic resonance imaging study. Neurosci. Lett. 351(2):99–102, 2003.

    Article  CAS  PubMed  Google Scholar 

  54. Westin, C. F., S. E. Maier, H. Mamata, A. Nabavi, F. A. Jolesz, and R. Kikinis. Processing and visualization for diffusion tensor MRI. Med. Image Anal. 6(2):93–108, 2002.

    Article  PubMed  Google Scholar 

  55. Wu, M. T., W. Y. Tseng, M. Y. Su, C. P. Liu, K. R. Chiou, V. J. Wedeen, T. G. Reese, and C. F. Yang. Diffusion tensor magnetic resonance imaging mapping the fiber architecture remodeling in human myocardium after infarction: correlation with viability and wall motion. Circulation 114(10):1036–1045, 2006.

    Article  PubMed  Google Scholar 

  56. Zhang, S., M. E. Bastin, D. H. Laidlaw, S. Sinha, P. A. Armitage, and T. S. Deisboeck. Visualization and analysis of white matter structural asymmetry in diffusion tensor MRI data. Magn. Reson. Med. 51(1):140–147, 2004.

    Article  PubMed  Google Scholar 

  57. Zhang, S., S. Correia, and D. H. Laidlaw. Identifying white-matter fiber bundles in DTI data using an automated proximity-based fiber-clustering method. IEEE Trans. Vis. Comput. Graph. 14(5):1104–1053, 2008.

    Google Scholar 

  58. Zhang, S., C. Demiralp, and D. H. Laidlaw. Visualizing Diffusion Tensor MR Images Using Streamtubes and Streamsurfaces. IEEE Trans. Vis. Comput. Graph. 9(4):454–462, 2003.

    Article  Google Scholar 

  59. Zhukov, L., and A. H. Barr. Heart-muscle fiber reconstruction from diffusion tensor MRI. In: Proceedings of IEEE Visualization ‘03, 2003.

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Acknowledgments

This project is supported by MAFES Strategic Research Initiative (CSREES MIS-741110) and MSU Research Initiation Program. JL is funded in part by National Heart, Lung, and Blood Institute (HL097321). The authors thank Dr. Michael S. Sacks (University of Pittsburgh) for support on biaxial device building. The authors would like to thank Amecha Landrum and Cade Austin from MSU INST for their help in MRI experiment and invaluable discussion and help from Dr. Shane Burgess.

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Authors and Affiliations

  1. Cardiovascular Tissue Biomechanics Laboratory, Department of Agricultural and Biological Engineering, Mississippi State University, Room 222, 130 Creelman Street, Mississippi State, MS, 39762, USA

    Joseph Chen, Ali Borazjani & Jun Liao

  2. Department of Computer Science and Engineering, Mississippi State University, Mississippi State, MS, USA

    Song Zhang & Xiaoyong Yang

  3. College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, USA

    Katie B. Mullins, Robert C. Cooper & Ronald M. McLaughlin

  4. Center for Environmental Health Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39762, USA

    J. Allen Crow

  5. The State Key Lab of CAD&CG, Zhejiang University, Hangzhou, China

    Wei Chen

  6. Computational Manufacturing and Design, CAVS, Mississippi State University, Mississippi State, MS, USA

    Joseph Chen, Ali Borazjani & Jun Liao

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  1. Song Zhang
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  2. J. Allen Crow
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Correspondence to Jun Liao.

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Associate Editor Ioannis Kakadiaris oversaw the review of this article.

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Zhang, S., Crow, J.A., Yang, X. et al. The Correlation of 3D DT-MRI Fiber Disruption with Structural and Mechanical Degeneration in Porcine Myocardium. Ann Biomed Eng 38, 3084–3095 (2010). https://doi.org/10.1007/s10439-010-0073-8

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