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Methods from the Theory of Random Heterogeneous Media for Quantifying Myocardial Morphology in Normal and Dilated Hearts

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Abstract

In the present study, descriptors from the theory of random heterogeneous media were used to characterize the morphology of the myocardial interstitial space in histological sections from hearts of healthy subjects and of patients with idiopathic dilated cardiomyopathy (DCM). Histological sections from resected DCM hearts (n = 9) were compared with donor hearts showing no signs of cardiac disease (n = 6). From control to DCM, the area fraction ϕ1 of the interstitial space increased from 0.13 ± 0.05 to 0.27 ± 0.08, the chord-length z from 1.67 ± 0.61 to 5.56 ± 1.78 μm, the pore-size δ from 0.72 ± 0.13 to 1.73 ± 0.40 μm, the distance r min of the first local minimum in the two-point correlation function from 10.99 ± 1.09 to 18.57 ± 4.36 μm, whereas specific interface length s and decay-rate γ of the lineal-path function decreased from 0.20 ± 0.07 to 0.16 ± 0.04 μm−1 and from 0.39 ± 0.09 to 0.16 ± 0.05 μm−1, respectively. All descriptors (except for s) were significantly different (p < 0.05) between control and DCM, reflecting an increasingly heterogeneous morphology in DCM hearts. Our results suggest that (1) descriptors originally developed to characterize the morphology of random heterogeneous media are well suited for histomorphometry of DCM, and (2) among the descriptors studied, either pore-size δ or chord-length z qualify best to discriminate between control and DCM hearts.

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References

  1. Arbustini, E., A. Pucci, R. Pozzi, M. Grasso, G. Graziano, C. Campana, A. Gavazzi, and M. Vigano. Ultrastructural changes in myocarditis and dilated cardiomyopathy. In: Advances in Cardiomyopathies, edited by G. Baroldi, F. Camerini, and J. F. Goodwin. Berlin: Springer-Verlag, 1999, pp. 274–289.

    Google Scholar 

  2. Basso, C., F. Calabrese, D. Corrado, and G. Thiene. Postmortem diagnosis in sudden cardiac death victims: macroscopic, microscopic and molecular findings. Cardiovasc. Res. 50:290–300, 2001.

    Article  CAS  PubMed  Google Scholar 

  3. Beltrami, C. A., N. Finato, M. Rocco, G. A. Feruglio, C. Puricelli, E. Cigola, E. H. Sonnenblick, G. Olivetti, and P. Anversa. The cellular basis of dilated cardiomyopathy in humans. J. Mol. Cell. Cardiol. 27:291–305, 1995.

    Article  CAS  PubMed  Google Scholar 

  4. Billingham, M. E. Histopathological diagnosis of acute myocarditis and dilated cardiomyopathy. In: Advances in Cardiomyopathies, edited by G. Baroldi, F. Camerini, and J. F. Goodwin. Berlin: Springer-Verlag, 1999, pp. 266–273.

    Google Scholar 

  5. Calabrese, F., and G. Thiene. Myocarditis and inflammatory cardiomyopathy: microbiological and molecular biological aspects. Cardiovasc. Res. 60:11–25, 2003.

    Article  CAS  PubMed  Google Scholar 

  6. Coker, D. A., and S. Torquato. Extraction of morphological quantities from a digitized medium. J. Appl. Phys. 77:6087–6099, 1995.

    Article  CAS  Google Scholar 

  7. Coker, D. A., S. Torquato, and J. H. Dunsmuir. Morphology and physical properties of Fontainebleau sandstone via a tomographic analysis. J. Geophys. Res. B 101:17497–17506, 1996.

    Article  Google Scholar 

  8. Crossley, P. A., L. M. Schwartz, and J. R. Banavar. Image-based models of porous media: application to Vycor glass and carbonate rocks. Appl. Phys. Lett. 59:3553–3555, 1991.

    Article  CAS  Google Scholar 

  9. Dorph-Petersen, K.-A., J. R. Nyengaard, and H. J. G. Gundersen. Tissue shrinkage and unbiased stereological estimation of particle number and size. J. Microsc. 204:232–246, 2001.

    Article  CAS  PubMed  Google Scholar 

  10. El-Kareh, A. W., S. L. Braunstein, and T. W. Secomb. Effect of cell arrangement and interstitial volume fraction on the diffusivity of monoclonal antibodies in tissue. Biophys. J. 64:1638–1646, 1993.

    Article  CAS  PubMed  Google Scholar 

  11. Fujimoto, S., R. Mizuno, Y. Nakagawa, A. Kimura, K. Yamaji, C. Yutani, K. Dohi, and H. Nakano. Ultrasonic tissue characterization in patients with dilated cardiomyopathy: comparison with findings from right ventricular endomyocardial biopsy. Int. J. Cardiac Imaging 15:391–396, 1999.

    Article  CAS  Google Scholar 

  12. Gonzalez, R. C., R. E. Woods, and S. L. Eddins. Digital Image Processing Using MATLAB. Upper Saddle River, NJ: Prentice Hall, 2004.

    Google Scholar 

  13. Grimm, W., S. Rudolph, M. Christ, S. Pankuweit, and B. Maisch. Prognostic significance of morphometric endomyocardial biopsy analysis in patients with idiopathic dilated cardiomyopathy. Am. Heart J. 146:372–376, 2003.

    Article  PubMed  Google Scholar 

  14. Image Processing Toolbox, Users Guide, Version 6. Natick, MA: The MathWorks, Inc., 2007, 1256 pp.

  15. Jiao, Y., F. H. Stillinger, and S. Torquato. Modeling heterogeneous materials via two-point correlation functions: basic principles. Phys. Rev. E 76:031110–031115, 2007.

    Article  CAS  Google Scholar 

  16. Lu, B., and S. Torquato. Lineal-path function for random heterogeneous materials. Phys. Rev. A 45:922–929, 1992.

    Article  CAS  PubMed  Google Scholar 

  17. Maehashi, N., Y. Yokota, A. Takarada, S. Usuki, S. Maeda, H. Yoshida, T. Sugiyama, and H. Fukuzaki. The role of myocarditis and myocardial fibrosis in dilated cardiomyopathy. Analysis of 28 necropsy cases. Jpn. Heart J. 32:1–15, 1991.

    CAS  PubMed  Google Scholar 

  18. Mehrabi, M. R., C. Ekmekcioglu, B. Stanek, T. Thalhammer, F. Tamaddon, R. Pacher, G. E. Steiner, T. Wild, M. Grimm, P. G. Spieckermann, G. Mall, and H. D. Glogar. Angiogenesis stimulation in explanted hearts from patients pre-treated with intravenous prostaglandin E1. J. Heart Lung Transplant. 20:465–473, 2001.

    Article  CAS  PubMed  Google Scholar 

  19. Otasevic, P., Z. B. Popovic, J. D. Vasiljevic, R. Vidakovic, L. Pratali, A. Vlahovic, and A. N. Neskovic. Relation of myocardial histomorphometric features and left ventricular contractile reserve assessed by high-dose dobutamine stress echocardiography in patients with idiopathic dilated cardiomyopathy. Eur. J. Heart Fail. 7:49–56, 2005.

    Article  PubMed  Google Scholar 

  20. Rowan, R. A., M. A. Masek, and M. E. Billingham. Ultrastructural morphometric analysis of endomyocardial biopsies. Idiopathic dilated cardiomyopathy, anthracycline cardiotoxicity, and normal myocardium. Am. J. Cardiovasc. Pathol. 2:137–144, 1988.

    CAS  PubMed  Google Scholar 

  21. Ruocco, G., M. Sampoli, and R. Vallauri. Analysis of the network topology in liquid water and hydrogen sulphide by computer simulation. J. Chem. Phys. 96:6167–6176, 1992.

    Article  CAS  Google Scholar 

  22. Seidman, J. G., and C. Seidman. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104:557–567, 2001.

    Article  CAS  PubMed  Google Scholar 

  23. Sykova, E., and C. Nicholson. Diffusion in brain extracellular space. Physiol. Rev. 88:1277–1340, 2008.

    Article  CAS  PubMed  Google Scholar 

  24. Takemura, G., Y. Takatsu, and H. Fujiwara. Luminal narrowing of coronary capillaries in human hypertrophic hearts: an ultrastructural morphometrical study using endomyocardial biopsy specimens. Heart 79:78–85, 1998.

    CAS  PubMed  Google Scholar 

  25. Tanganelli, P., A. Di Lenarda, G. Bianciardi, A. Salvi, F. Silvestri, L. Mestroni, and F. Camerini. Correlation between histomorphometric findings on endomyocardial biopsy and clinical findings in idiopathic dilated cardiomyopathy. Am. J. Cardiol. 64:504–506, 1989.

    Article  CAS  PubMed  Google Scholar 

  26. Torquato, S. Random Heterogeneous Materials: Microstructure and Macroscopic Properties. New York: Springer-Verlag, 2002.

    Google Scholar 

  27. Torquato, S. Statistical description of microstructures. Annu. Rev. Mater. Res. 32:77–111, 2002.

    Article  CAS  Google Scholar 

  28. Torquato, S., and M. Avellaneda. Diffusion and reaction in heterogeneous media: pore size distribution, relaxation times, and mean survival time. J. Chem. Phys. 95:6477–6489, 1991.

    Article  CAS  Google Scholar 

  29. Torquato, S., C. L. Y. Yeong, M. D. Rintoul, D. L. Milius, and I. A. Aksay. Elastic properties and structure of interpenetrating boron carbide/aluminum multiphase composites. J. Am. Ceram. Soc. 82:1263–1268, 1999.

    Article  CAS  Google Scholar 

  30. Towbin, J. A., and N. E. Bowles. The failing heart. Nature 415:227–233, 2002.

    Article  CAS  PubMed  Google Scholar 

  31. Vasiljevic, J. D., Z. B. Popovic, P. Otasevic, Z. V. Popovic, R. Vidakovic, M. Miric, and A. N. Neskovic. Myocardial fibrosis assessment by semiquantitative, point-counting and computer-based methods in patients with heart muscle disease: a comparative study. Histopathology 38:338–343, 2001.

    Article  CAS  PubMed  Google Scholar 

  32. Westfall, P. J., and S. S. Young. Resampling-Based Multiple Testing. New York: John Wiley & Sons, 1993.

    Google Scholar 

  33. Yeong, C. L. Y., and S. Torquato. Reconstructing random media. Phys. Rev. E 57:495–506, 1998.

    Article  CAS  Google Scholar 

  34. Yeong, C. L. Y., and S. Torquato. Reconstructing random media. II. Three-dimensional media from two-dimensional cuts. Phys. Rev. E 58:224–233, 1998.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Medical Statistics and Informatics, Medical University of Vienna, Spitalgasse 23, A-1090, Vienna, Austria

    Rudolf Karch, Friederike Neumann & Georg Heinze

  2. Clinical Institute for Pathology, Medical University of Vienna, Vienna, Austria

    Robert Ullrich

  3. Center for Anatomy and Cell Biology, Department of Cell Biology and Ultrastructure Research, Medical University of Vienna, Vienna, Austria

    Josef Neumüller

  4. Ludwig Boltzmann Cluster for Cardiovascular Research, Medical University of Vienna, Vienna, Austria

    Bruno K. Podesser

  5. Faculty of Physics, University of Vienna, Vienna, Austria

    Martin Neumann

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  1. Rudolf Karch
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Correspondence to Rudolf Karch.

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Karch, R., Neumann, F., Ullrich, R. et al. Methods from the Theory of Random Heterogeneous Media for Quantifying Myocardial Morphology in Normal and Dilated Hearts. Ann Biomed Eng 38, 308–318 (2010). https://doi.org/10.1007/s10439-009-9848-1

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  • DOI: https://doi.org/10.1007/s10439-009-9848-1

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