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Multi-Scale Parameterisation of a Myocardial Perfusion Model Using Whole-Organ Arterial Networks

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Abstract

A method to extract myocardial coronary permeabilities appropriate to parameterise a continuum porous perfusion model using the underlying anatomical vascular network is developed. Canine and porcine whole-heart discrete arterial models were extracted from high-resolution cryomicrotome vessel image stacks. Five parameterisation methods were considered that are primarily distinguished by the level of anatomical data used in the definition of the permeability and pressure-coupling fields. Continuum multi-compartment porous perfusion model pressure results derived using these parameterisation methods were compared quantitatively via a root-mean-square metric to the Poiseuille pressure solved on the discrete arterial vasculature. The use of anatomical detail to parameterise the porous medium significantly improved the continuum pressure results. The majority of this improvement was attributed to the use of anatomically-derived pressure-coupling fields. It was found that the best results were most reliably obtained by using porosity-scaled isotropic permeabilities and anatomically-derived pressure-coupling fields. This paper presents the first continuum perfusion model where all parameters were derived from the underlying anatomical vascular network.

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References

  1. Arts, M. A Mathematical Model of the Dynamics of the Left Ventricle and the Coronary Circulation. Ph.D. Thesis, Rijksuniversiteit Limburg, 1978.

  2. Bear, J. Dynamics of Fluids in Porous Media. 2. New York: Courier Dover Publications, 1972.

  3. Braakman, R., P. Sipkema, and N. Westerhof. A dynamic non-linear lumped parameter model for skeletal muscle circulation. Ann. Biomed. Eng. 17(6):593–616, 1989.

    Article  CAS  PubMed  Google Scholar 

  4. Chapelle, D., J.-F. Gerbeau, J. Sainte-Marie, I. E. Vignon-Clementel. A poroelastic model valid in large strains with applications to perfusion in cardiac modeling. Comput. Mech. 46(1):91–101, 2009.

    Article  Google Scholar 

  5. Chapman, S. J., R. J. Shipley, and R. Jawad. Multiscale modeling of fluid transport in tumors. Bull. Math. Biol. 70(8):2334–2357, 2008.

    Article  PubMed  Google Scholar 

  6. Chilian, W. M. W., C. L. Eastham, and M. L. Marcus. Microvascular distribution of coronary vascular resistance in beating left ventricle. Am. J. Physiol. Heart Circ. Physiol. 251:779–788, 1986.

    Google Scholar 

  7. Chilian, W. M. W., S. M. Layne, E. C. Klausner, C. L. Eastham, M. L. Marcus, C. Klausner, and C. Edward. Redistribution of coronary microvascular resistance produced by dipyridamole. J. Physiol. Heart Circ. Physiol. 256:383–390, 1989.

    Google Scholar 

  8. Cookson, A. N., J. Lee, C. Michler, R. Chabiniok, E. R. Hyde, D. A. Nordsletten, M. Sinclair, M. Siebes, and N. P. Smith. A novel porous mechanical framework for modelling the interaction between coronary perfusion and myocardial mechanics. J. Biomech. 45(5):850–855, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Crick, S., M. Sheppard, S. Ho, L. Gebstein, and R. Anderson. Anatomy of the pig heart: comparisons with normal human cardiac structure. J. Anat. 193(Pt 1):105–119, 1998.

    Google Scholar 

  10. Dellsperger, K. C., D. L. Janzen, C. L. Eastham, and M. L. Marcus. Effects of acute coronary artery occlusion on the coronary microcirculation. Am. J. Physiol. Heart Circ. Physiol. 259:909–916, 1990.

    Google Scholar 

  11. Dijkstra, E. A note on two problems in connexion with graphs. Numer. Math. 1:269–271, 1959.

    Google Scholar 

  12. Fokkema, D. S., J. W. G. E. VanTeeffelen, S. Dekker, I. Vergroesen, J. B. Reitsma, and J. A. E. Spaan. Diastolic time fraction as a determinant of subendocardial perfusion. Am. J. Physiol. Heart Circ. Physiol. 288(5):H2450–H2456, 2005.

    Article  CAS  PubMed  Google Scholar 

  13. Frangi, A., and W. Niessen. Multiscale vessel enhancement filtering. Med. Image Comput. Comput. Assist Interv. 1496:130–137, 1998.

    Google Scholar 

  14. Goyal, A., J. Lee, P. Lamata, V. Grau, J. P. H. M. van den Wijngaard, P. van Horssen, J. A. E. Spaan, M. Siebes, and N. P. Smith. Model-based vasculature extraction from optical fluorescence cryomicrotome images. IEEE TMI 32(1):56–72, 2013.

    Google Scholar 

  15. Horssen, P. V., J. P. H. M. van den Wijngaard, F. Nolte, I. Hoefer, R. Haverslag, J. A. E. Spaan, and M. Siebes. Extraction of coronary vascular tree and myocardial perfusion data from stacks of cryomicrotome images. In: FIMH, Vol. 5528, edited by N. Ayache, H. Delingette, and M. Sermesant. Berlin: Springer, 2009, pp. 486–494.

  16. Huyghe, J. M., T. Arts, D. H. van Campen, R. S. Reneman. Porous medium finite element model of the beating left ventricle. Am. J. Physiol. Heart Circ. Physiol. 262(4):H1256–H1267, 1992.

    CAS  Google Scholar 

  17. Huyghe, J. M., and D. H. van Campen. Finite deformation theory of hierarchically arranged porous solids. II: constitutive behaviour. Int. J. Eng. Sci. 33(13):1873–1886, 1995.

    Article  Google Scholar 

  18. Hyde, E. R., C. Michler, J. Lee, A. N. Cookson, R. Chabiniok, D. A. Nordsletten, and N. P. Smith. Parameterisation of multi-scale continuum perfusion models from discrete vascular networks. Med. Biol. Eng. Comput. 51(5):557–570, 2013.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Kanatsuka, H., K. G. Lamping, C. L. Eastham, and M. L. Marcus. Heterogeneous changes in epimyocardial microvascular size during graded coronary stenosis. Evidence of the microvascular site for autoregulation. Circ. Res. 66(2):389–396, 1990.

    Article  CAS  PubMed  Google Scholar 

  20. Kassab, G. S., J. Berkley, and Y. C. Fung. Analysis of pig’s coronary arterial blood flow with detailed anatomical data. Ann. Biomed. Eng. 25(1):204–217, 1997.

    Article  CAS  PubMed  Google Scholar 

  21. Kassab, G. S., and Y. C. Fung. Topology and dimensions of pig coronary capillary network. Am. J. Physiol Heart Circ. Physiol. 267(6):H319–H25, 1994.

    CAS  Google Scholar 

  22. Kassab, G. S., D. H. Lin, and Y. C. Fung. Morphometry of pig coronary venous system. Am. J. Physiol. Heart Circ. Physiol. 267(6):H2100–H2113, 1994.

    CAS  Google Scholar 

  23. Lamata, P., S. Niederer, D. Nordsletten, D. C. Barber, I. Roy, D. R. Hose, and N. P. Smith. An accurate, fast and robust method to generate patient-specific cubic Hermite meshes. Med. Image Anal. 15(6):801–813, 2011.

    Article  PubMed  Google Scholar 

  24. Lee, J., P. E. Beighley, E. L. Ritman, and N. P. Smith. Automatic segmentation of 3D micro-CT coronary vascular images. Med. Image Anal. 11(6):630–647, 2007.

    Article  PubMed  Google Scholar 

  25. Lee, J., and N. P. Smith. Development and application of a one-dimensional blood flow model for microvascular networks. Proc. Inst. Mech. Eng., H J. Eng. Med. 222(4):487–512, 2008.

    Article  CAS  Google Scholar 

  26. Lee, J., and N. P. Smith. The multi-scale modelling of coronary blood flow. Ann. Biomed. Eng. 40(11):2399–2413, 2012.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Linninger, A., I. G. Gould, T. Marinnan, C.-Y. Hsu, M. Chojecki, and A. Alaraj. Cerebral microcirculation and oxygen tension in the human secondary cortex. Ann. Biomed. Eng. 41(11):2264–2284, 2013.

    Google Scholar 

  28. Maxwell, M. P., D. J. Hearse, and D. M. Yellon. Species variation in the coronary collateral circulation during regional myocardial ischaemia: a critical determinant of the rate of evolution and extent of myocardial infarction. Cardiovasc. Res. 21(10):737–746, 1987.

    Article  CAS  PubMed  Google Scholar 

  29. Michler, C., A. N. Cookson, R. Chabiniok, E. R. Hyde, J. Lee, M. Sinclair, T. Sochi, A. Goyal, G. Vigueras, D. A. Nordsletten, and N. P. Smith. A computationally efficient framework for the simulation of cardiac perfusion using a multi-compartment Darcy porous-media flow model. Int. J. Numer. Methods Biomed. Eng. 29(2):217–232, 2013.

    Article  CAS  Google Scholar 

  30. Muehling, O., M. Jerosch-Herold, P. Panse, A. Zenovich, B. Wilson, R. Wilson, and N. Wilke. Regional heterogeneity of myocardial perfusion in healthy human myocardium: assessment with magnetic resonance perfusion imaging. J. Cardiovasc. Magn. Reson. 6(2):499–507, 2004.

    Article  PubMed  Google Scholar 

  31. Otsu, N. A threshold selection method from gray-level histograms. Automatica 20(1):62–66, 1975.

    Google Scholar 

  32. Pries, A. R., T. W. Secomb, and P. Gaehtgens. Biophysical aspects of blood flow in the microvasculature. Cardiovasc. Res. 32(4):654–667, 1996.

    Article  CAS  PubMed  Google Scholar 

  33. Pudney, C. Distance-ordered homotopic thinning: a skeletonization algorithm for 3D digital images. Comput. Vis. Image Underst. 72(3):404–413, 1998.

    Article  Google Scholar 

  34. Sands, G. B., D. A. Gerneke, D. A. Hooks, C. R. Green, B. H. Smaill, and I. J. Legrice. Automated imaging of extended tissue volumes using confocal microscopy. Microsc. Res. Tech. 67(5):227–239, 2005.

    Article  PubMed  Google Scholar 

  35. Sauvola, J., and M. Pietikäinen. Adaptive document image binarization. Pattern Recogn. 33:225–236, 2000.

    Article  Google Scholar 

  36. Sellke, F. W., P. R. Myers, J. N. Bates, and G. Harrison. Influence of vessel size on the sensitivity of porcine coronary microvessels to nitroglycerin. Am. J. Physiol. Heart Circ. Physiol. 258:H515–H520, 1990.

    CAS  Google Scholar 

  37. Sherwin, S., V. Franke, J. Peiró, K. Parker. One-dimensional modelling of a vascular network in space–time variables. J. Eng. Math. 47(3/4):217–250, 2003.

    Article  Google Scholar 

  38. Shipley, R. J., and S. J. Chapman. Multiscale modelling of fluid and drug transport in vascular tumours. Bull. Math. Biol. 72(6):1464–1491, 2010.

    Article  PubMed  Google Scholar 

  39. Smith, N. P., A. J. Pullan, and P. J. Hunter. An anatomically based model of transient coronary blood flow in the heart. SIAM J. Appl. Math. 62(3):990–1018, 2001.

    Article  Google Scholar 

  40. Spaan, J. A. E., M. Siebes, R. Wee, C. Kolyva, H. Vink, D. S. Fokkema, G. Streekstra, and E. Vanbavel. Visualisation of intramural coronary vasculature by an imaging cryomicrotome suggests compartmentalisation of myocardial perfusion areas. Med. Biol. Eng. Comput. 43:431–435, 2005.

    Article  CAS  PubMed  Google Scholar 

  41. Taylor, C. A., and C. A. Figueroa. Patient-specific modeling of cardiovascular mechanics. Annu. Rev. Biomed. Eng. 11:109–134, 2009.

    Article  CAS  PubMed  Google Scholar 

  42. van den Wijngaard, J. P. H. M., H. Schulten, P. van Horssen, R. D. Ter Wee, M. Siebes, M. J. Post, and J. A. E. Spaan. Porcine coronary collateral formation in the absence of a pressure gradient remote of the ischemic border zone. Am. J. Physiol. Heart Circ. Physiol. 300(5):H1930–H1977, 2011.

    Article  PubMed  Google Scholar 

  43. Vankan, W. J., J. M. Huyghe, J. D. Janssen, A. Huson, and W. Schreiner. Finite element blood flow through biological tissue. Int. J. Eng. Sci. 35(4):375–385, 1997.

    Article  Google Scholar 

  44. Westerhof, N., C. Boer, R. R. Lamberts, and P. Sipkema. Cross-talk between cardiac muscle and coronary vasculature. Physiol. Rev. 86(4):1263–1308, 2006.

    Article  CAS  PubMed  Google Scholar 

  45. Wüsten, B., D. D. Buss, H. Deist, and W. Schaper. Dilatory capacity of the coronary circulation and its correlation to the arterial vasculature in the canine left ventricle. Basic Res. Cardiol. 72(6):636–650, 1977.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to acknowledge funding from the Engineering and Physical Sciences Research Council (EP/G007527/2) European Community’s Seventh Framework Program FP7-ICT Grant No. 224495: euHeart, the Wellcome Trust Medical Engineering Centre at King’s College London, the National University of Ireland (ERH), the Netherlands Heart Foundation Grant 2006B226 (JAS and MS). JvdW was supported by a Veni grant from the Netherlands Organization for Scientific Research (NWO 91611171).

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Correspondence to Eoin R. Hyde.

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Hyde, E.R., Cookson, A.N., Lee, J. et al. Multi-Scale Parameterisation of a Myocardial Perfusion Model Using Whole-Organ Arterial Networks. Ann Biomed Eng 42, 797–811 (2014). https://doi.org/10.1007/s10439-013-0951-y

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