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Biomechanical Basis of Myocardium/Vessel Interaction: Implications for Pathophysiology and Therapy

  • Dotan Algranati
  • Ghassan S. KassabEmail author
  • Yoram Lanir
Chapter

Abstract

Ischemic heart disease is a major cause of morbidity and mortality worldwide. Interestingly, the onset of ischemia is transmurally heterogeneous, where the deeper (subendocardial) layers are more vulnerable to ischemia than the more superficial (subepicardial) ones (Hoffman 1987). This observation is especially puzzling in light of the opposite manifestation of coronary artery disease, which exclusively affects the epicardial coronary arteries, whereas intramural arteries are athero-protected (Geiringer 1951). Initiation of both atherosclerosis and ischemia depend highly on flow conditions; therefore, investigation of the hemodynamic determinants of both pathologies requires comprehension of the local coronary flow conditions, which are measured in the beating heart. Computer simulation is an attractive approach to study local coronary flow conditions. For hemodynamic simulation to be realistic, however, it must incorporate both a realistic description of the coronary network and the manner by which the contracting myocardium affects coronary flow—the myocardium/vessel interaction (MVI). Such an approach has several inherent challenges: First, the vast number of coronary blood vessels (Kaimovitz et al. 2005) is associated with an extensive computational cost to solve the network dynamic flow. To circumvent this difficulty, previous flow models (Bruinsma et al. 1988; Cornelissen et al. 2000; Flynn et al. 1992; Klocke et al. 1985; Manor et al. 1994) used lumped representations for the coronary vasculature. Although this approach is useful to reveal basic flow characteristics, it cannot address the physical relation between structure, vessel mechanics, and blood flow. Moreover, validation of a lumped model with experimental data is limited due to the inability of the model to describe flow conditions in specific vessels. Asecond challenge stems from paucity of experimental data required for both the flow model representation and for validation. Finally, the physical origins of the MVI, a key determinant in coronary flow analysis, are under a long-standing dispute and hitherto unknown. In fact, none of the mechanisms previously proposed (Downey and Kirk 1975; Krams et al. 1989a; Rabbany et al. 1989; Spaan et al. 1981; Zinemanas et al. 1994) to describe this mechanical interaction predict all of the characteristics of coronary flow (Westerhof et al. 2006), i.e., the blood flow velocities, pressures, and vascular diameters that correspond with the measured data.

Keywords

Coronary Flow Fractional Flow Reserve Left Ventricular Pressure Vascular Stiffness Coronary Vasculature 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Algranati D, Kassab GS, Lanir Y. Flow restoration post revascularization predicted by stenosis indexes: sensitivity to hemodynamic variability. Am J Physiol Heart Circ Physiol. 2013;305:H145–154.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Algranati D, Kassab GS, Lanir Y. Why is the subendocardium more vulnerable to ischemia? Anew paragidm. Am J Physiol Heart Circ Physiol. 2011;300:H1090–100.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Algranati D, Kassab KG, Lanir Y. Consistency of stenosis severity indices. Am J Physiol Heart Circ Physiol. 2012.Google Scholar
  4. Bache RJ, Schwartz JS. Effect of perfusion pressure distal to a coronary stenosis on transmural myocardial blood flow. Circulation. 1982;65:928–35.PubMedCrossRefGoogle Scholar
  5. Baptista J, Arnese M, Roelandt JR, Fioretti P, Keane D, Escaned J, Boersma E, di Mario C, Serruys PW. Quantitative coronary angiography in the estimation of the functional significance of coronary stenosis: correlations with dobutamine-atropine stress test. J Am Coll Cardiol. 1994;23:1434–9.PubMedCrossRefGoogle Scholar
  6. Boatwright RB, Downey HF, Bashour FA, Crystal GJ. Transmural variation in autoregulation of coronary blood flow in hyperperfused canine myocardium. Circ Res. 1980;47:599–609.PubMedCrossRefGoogle Scholar
  7. Bruinsma P, Arts T, Dankelman J, Spaan JA. Model of the coronary circulation based on pressure dependence of coronary resistance and compliance. Basic Res Cardiol. 1988;83:510–24.PubMedCrossRefGoogle Scholar
  8. Buckberg GD, Fixler DE, Archie JP, Hoffman JI. Experimental subendocardial ischemia in dogs with normal coronary arteries. Circ Res. 1972;30:67–81.PubMedCrossRefGoogle Scholar
  9. Caro CG. Discovery of the role of wall shear in atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:158–61.PubMedCrossRefGoogle Scholar
  10. Caulfield JB, Borg TK. The collagen network of the heart. Lab Invest. 1979;40:364–72.PubMedGoogle Scholar
  11. Chilian WM. Microvascular pressures and resistances in the left ventricular subepicardium and subendocardium. Circ Res. 1991;69:561–70.PubMedCrossRefGoogle Scholar
  12. Chilian WM, Layne SM. Coronary microvascular responses to reductions in perfusion pressure. Evidence for persistent arteriolar vasomotor tone during coronary hypoperfusion. Circ Res. 1990;66:1227–38.PubMedCrossRefGoogle Scholar
  13. Cornelissen AJ, Dankelman J, VanBavel E, Stassen HG, Spaan JA. Myogenic reactivity and resistance distribution in the coronary arterial tree: a model study. Am J Physiol Heart Circ Physiol. 2000;278:H1490–9.PubMedGoogle Scholar
  14. Downey JM, Kirk ES. Inhibition of coronary blood flow by a vascular waterfall mechanism. Circ Res. 1975;36:753–60.PubMedCrossRefGoogle Scholar
  15. Fibich G, Lanir Y, Liron N. Mathematical model of blood flow in a coronary capillary. Am J Physiol. 1993;265:H1829–40.PubMedGoogle Scholar
  16. Flynn AE, Coggins DL, Goto M, Aldea GS, Austin RE, Doucette JW, Husseini W, Hoffman JI. Does systolic subepicardial perfusion come from retrograde subendocardial flow? Am J Physiol. 1992;262:H1759–69.PubMedGoogle Scholar
  17. Geiringer E. The mural coronary. Am Heart J. 1951;41:359–68.PubMedCrossRefGoogle Scholar
  18. Gould KL. Quantification of coronary artery stenosis in vivo. Circ Res. 1985;57:341–53.PubMedCrossRefGoogle Scholar
  19. Hamza LH, Dang Q, Lu X, Mian A, Molloi S, Kassab GS. Effect of passive myocardium on the compliance of porcine coronary arteries. Am J Physiol Heart Circ Physiol. 2003;285:H653–60.PubMedCrossRefGoogle Scholar
  20. Heineman FW, Grayson J. Transmural distribution of intramyocardial pressure measured by micropipette technique. Am J Physiol. 1985;249:H1216–23.PubMedGoogle Scholar
  21. Hiramatsu O, Goto M, Yada T, Kimura A, Chiba Y, Tachibana H, Ogasawara Y, Tsujioka K, Kajiya F. In vivo observations of the intramural arterioles and venules in beating canine hearts. J Physiol. 1998;509(Pt 2):619–28.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Hoffman JI. Transmural myocardial perfusion. Prog Cardiovasc Dis. 1987;29:429–64.PubMedCrossRefGoogle Scholar
  23. Hoffman JI, Spaan JA. Pressure-flow relations in coronary circulation. Physiol Rev. 1990;70:331–90.PubMedGoogle Scholar
  24. Hoffman JI, Baer RW, Hanley FL, Messina LM. Regulation of transmural myocardial blood flow. J Biomech Eng. 1985;107:2–9.PubMedCrossRefGoogle Scholar
  25. Huo Y, Svendsen M, Choy JS, Zhang ZD, Kassab GS. A validated predictive model of coronary fractional flow reserve. J R Soc Interface. 2012;9(71):1325–38.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Iwanaga S, Ewing SG, Husseini WK, Hoffman JI. Changes in contractility and afterload have only slight effects on subendocardial systolic flow impediment. Am J Physiol. 1995;269:H1202–12.PubMedGoogle Scholar
  27. Jacobs J, Algranati D, Lanir Y. Lumped flow modeling in dynamically loaded coronary vessels. JBiomech Eng. 2008;130:054504.PubMedCrossRefGoogle Scholar
  28. Jones CJ, Kuo L, Davis MJ, DeFily DV, Chilian WM. Role of nitric oxide in the coronary microvascular responses to adenosine and increased metabolic demand. Circulation. 1995;91:1807–13.PubMedCrossRefGoogle Scholar
  29. Kaimovitz B, Lanir Y, Kassab GS. Large-scale 3-D geometric reconstruction of the porcine coronary arterial vasculature based on detailed anatomical data. Ann Biomed Eng. 2005;33:1517–35.PubMedCrossRefGoogle Scholar
  30. Kajiya F, Yada T, Hiramatsu O, Ogasawara Y, Inai Y, Kajiya M. Coronary microcirculation in the beating heart. Med Biol Eng Comput. 2008;46:411–9.PubMedCrossRefGoogle Scholar
  31. Kassab GS, Fung YC. Topology and dimensions of pig coronary capillary network. Am J Physiol. 1994;267:H319–25.PubMedGoogle Scholar
  32. Kassab GS, Imoto K, White FC, Rider CA, Fung YC, Bloor CM. Coronary arterial tree remodeling in right ventricular hypertrophy. Am J Physiol. 1993a;265:H366–75.PubMedGoogle Scholar
  33. Kassab GS, Rider CA, Tang NJ, Fung YC. Morphometry of pig coronary arterial trees. Am J Physiol. 1993b;265:H350–65.PubMedGoogle Scholar
  34. Kassab GS, Lin DH, Fung YC. Morphometry of pig coronary venous system. Am J Physiol. 1994;267:H2100–13.PubMedGoogle Scholar
  35. Kassab GS, Le KN, Fung YC. A hemodynamic analysis of coronary capillary blood flow based on anatomic and distensibility data. Am J Physiol. 1999;277:H2158–66.PubMedGoogle Scholar
  36. Kini AS, Kim MC, Moreno PR, Krishnan P, Ivan OC, Sharma SK. Comparison of coronary flow reserve and fractional flow reserve in patients with versus without diabetes mellitus and having elective percutaneous coronary intervention and abciximab therapy (from the PREDICT Trial). Am J Cardiol. 2008;101:796–800.PubMedCrossRefGoogle Scholar
  37. Klocke FJ, Mates RE, Canty Jr JM, Ellis AK. Coronary pressure-flow relationships. Controversial issues and probable implications. Circ Res. 1985;56:310–23.PubMedCrossRefGoogle Scholar
  38. Kouwenhoven E, Vergroesen I, Han Y, Spaan JA. Retrograde coronary flow is limited by time-varying elastance. Am J Physiol. 1992;263:H484–90.PubMedGoogle Scholar
  39. Krams R, Sipkema P, Westerhof N. Varying elastance concept may explain coronary systolic flow impediment. Am J Physiol. 1989a;257:H1471–9.PubMedGoogle Scholar
  40. Krams R, Sipkema P, Zegers J, Westerhof N. Contractility is the main determinant of coronary systolic flow impediment. Am J Physiol. 1989b;257:H1936–44.PubMedGoogle Scholar
  41. Kuo L, Davis MJ, Chilian WM. Myogenic activity in isolated subepicardial and subendocardial coronary arterioles. Am J Physiol. 1988;255:H1558–62.PubMedGoogle Scholar
  42. Kuo L, Davis MJ, Chilian WM. Longitudinal gradients for endothelium-dependent and -independent vascular responses in the coronary microcirculation. Circulation. 1995;92:518–25.PubMedCrossRefGoogle Scholar
  43. Liao JC, Kuo L. Interaction between adenosine and flow-induced dilation in coronary microvascular network. Am J Physiol. 1997;272:H1571–81.PubMedGoogle Scholar
  44. Loutzenhiser R, Bidani A, Chilton L. Renal myogenic response: kinetic attributes and physiological role. Circ Res. 2002;90:1316–24.PubMedCrossRefGoogle Scholar
  45. Manor D, Sideman S, Dinnar U, Beyar R. Analysis of flow in coronary epicardial arterial tree and intramyocardial circulation. Med Biol Eng Comput. 1994;32:S133–43.PubMedCrossRefGoogle Scholar
  46. Marzilli M, Goldstein S, Sabbah HN, Lee T, Stein PD. Modulating effect of regional myocardial performance on local myocardial perfusion in the dog. Circ Res. 1979;45:634–41.PubMedCrossRefGoogle Scholar
  47. Mihailescu LS, Abel FL. Intramyocardial pressure gradients in working and nonworking isolated cat hearts. Am J Physiol. 1994;266:H1233–41.PubMedGoogle Scholar
  48. Mittal N, Zhou Y, Linares C, Ung S, Kaimovitz B, Molloi S, Kassab GS. Analysis of blood flow in the entire coronary arterial tree. Am J Physiol Heart Circ Physiol. 2005;289:H439–46.PubMedCrossRefGoogle Scholar
  49. Moir TW. Subendocardial distribution of coronary blood flow and the effect of antianginal drugs. Circ Res. 1972;30:621–7.PubMedCrossRefGoogle Scholar
  50. Pijls NH, van Son JA, Kirkeeide RL, De Bruyne B, Gould KL. Experimental basis of determining maximum coronary, myocardial, and collateral blood flow by pressure measurements for assessing functional stenosis severity before and after percutaneous transluminal coronary angioplasty. Circulation. 1993;87:1354–67.PubMedCrossRefGoogle Scholar
  51. Pries AR, Secomb TW, Gessner T, Sperandio MB, Gross JF, Gaehtgens P. Resistance to blood flow in microvessels in vivo. Circ Res. 1994;75:904–15.PubMedCrossRefGoogle Scholar
  52. Rabbany SY, Kresh JY, Noordergraaf A. Intramyocardial pressure: interaction of myocardial fluid pressure and fiber stress. Am J Physiol. 1989;257:H357–64.PubMedGoogle Scholar
  53. Rabbany SY, Funai JT, Noordergraaf A. Pressure generation in a contracting myocyte. Heart Vessels. 1994;9:169–74.PubMedCrossRefGoogle Scholar
  54. Robicsek F, Thubrikar MJ. The freedom from atherosclerosis of intramyocardial coronary arteries: reduction of mural stress–a key factor. Eur J Cardiothorac Surg. 1994;8:228–35.PubMedCrossRefGoogle Scholar
  55. Rogers PA, Kiyooka T, Chilian WM. Is there a need for another model on the pulsatile nature of coronary blood flow? Am J Physiol Heart Circ Physiol. 2006;291:H1034–5.PubMedCrossRefGoogle Scholar
  56. Scaramucci J. Theoremata familiaria viros eruditos consulentia de variis physico-medicis lucubrationibus juxta leges mecanicas. Apud Joannem Baptistam Bustum. 1696;70–81.Google Scholar
  57. Siebes M, Chamuleau SA, Meuwissen M, Piek JJ, Spaan JA. Influence of hemodynamic conditions on fractional flow reserve: parametric analysis of underlying model. Am J Physiol Heart Circ Physiol. 2002;283:H1462–70.PubMedCrossRefGoogle Scholar
  58. Siebes M, Verhoeff BJ, Meuwissen M, de Winter RJ, Spaan JA, Piek JJ. Single-wire pressure and flow velocity measurement to quantify coronary stenosis hemodynamics and effects of percutaneous interventions. Circulation. 2004;109:756–62.PubMedCrossRefGoogle Scholar
  59. Spaan JA. Coronary blood flow: mechanics, distribution, and control. Dordrecht: Kluwer; 1991.CrossRefGoogle Scholar
  60. Spaan JA. Mechanical determinants of myocardial perfusion. Basic Res Cardiol. 1995;90:89–102.PubMedCrossRefGoogle Scholar
  61. Spaan JA, Breuls NP, Laird JD. Diastolic-systolic coronary flow differences are caused by intramyocardial pump action in the anesthetized dog. Circ Res. 1981;49:584–93.PubMedCrossRefGoogle Scholar
  62. Spaan JA, Piek JJ, Hoffman JI, Siebes M. Physiological basis of clinically used coronary hemodynamic indices. Circulation. 2006;113:446–55.PubMedCrossRefGoogle Scholar
  63. Suga H. Total mechanical energy of a ventricle model and cardiac oxygen consumption. Am J Physiol. 1979;236:H498–505.PubMedGoogle Scholar
  64. Tonino PA, De Bruyne B, Pijls NH, Siebert U, Ikeno F, van’t Veer M, et al. Fractional flow reserve versus angiography for guiding percutaneous coronary intervention. N Engl J Med. 2009;360:213–24.PubMedCrossRefGoogle Scholar
  65. van den Wijngaard JP, Kolyva C, Siebes M, Dankelman J, van Gemert MJ, Piek JJ, Spaan JA. Model prediction of subendocardial perfusion of the coronary circulation in the presence of an epicardial coronary artery stenosis. Med Biol Eng Comput. 2008;46:421–32.PubMedPubMedCentralCrossRefGoogle Scholar
  66. VanTeeffelen JW, Merkus D, Bos LJ, Vergroesen I, Spaan JA. Impairment of contraction increases sensitivity of epicardial lymph pressure for left ventricular pressure. Am J Physiol. 1998;274:H187–92.PubMedGoogle Scholar
  67. Vis MA, Sipkema P, Westerhof N. Modeling pressure-area relations of coronary blood vessels embedded in cardiac muscle in diastole and systole. Am J Physiol. 1995;268:H2531–43.PubMedGoogle Scholar
  68. Vis MA, Bovendeerd PH, Sipkema P, Westerhof N. Effect of ventricular contraction, pressure, and wall stretch on vessels at different locations in the wall. Am J Physiol. 1997;272:H2963–75.PubMedGoogle Scholar
  69. Westerhof N. Physiological hypotheses–intramyocardial pressure. A new concept, suggestions for measurement. Basic Res Cardiol. 1990;85:105–19.PubMedCrossRefGoogle Scholar
  70. Westerhof N, Boer C, Lamberts RR, Sipkema P. Cross-talk between cardiac muscle and coronary vasculature. Physiol Rev. 2006;86:1263–308.PubMedCrossRefGoogle Scholar
  71. Yanagisawa H, Chikamori T, Tanaka N, Hatano T, Morishima T, Hida S, Iino H, Amaya K, Takazawa K, Yamashina A. Correlation between thallium-201 myocardial perfusion defects and the functional severity of coronary artery stenosis as assessed by pressure-derived myocardial fractional flow reserve. Circ J. 2002;66:1105–9.PubMedCrossRefGoogle Scholar
  72. Young DF. Fluid mechanics of arterial stenoses. J Biomech Eng. 1979;101:157–75.CrossRefGoogle Scholar
  73. Zhang W, Liu Y, Kassab GS. Viscoelasticity reduces the dynamic stresses and strains in the vessel wall: implications for vessel fatigue. Am J Physiol Heart Circ Physiol. 2007;293:H2355–60.PubMedCrossRefGoogle Scholar
  74. Zinemanas D, Beyar R, Sideman S. Relating mechanics, blood flow and mass transport in the cardiac muscle. Int J Heat Mass Transf. 1994;37:191–205.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2016

Authors and Affiliations

  • Dotan Algranati
    • 1
  • Ghassan S. Kassab
    • 2
    Email author
  • Yoram Lanir
    • 1
  1. 1.Faculty of Biomedical EngineeringTechnionIsrael
  2. 2.California Medical Innovations InstituteSan DiegoUSA

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