Advertisement

Functional Morphology of the Heart

  • Branko Furst
Chapter

Abstract

The primary function of muscles is the generation of force or movement in response to physiological stimulus. The myocardium is a heterogeneous mass of muscle tissue which represents a transition between the involuntary (smooth) and the voluntary (striated) muscles. While the individual muscle fibers in a voluntary muscle are supplied by the nerve endings and can be recruited at will across the spectrum of forces, the cardiomyocytes are electrically connected and function as a single unit, a syncytium that contracts in unison with each impulse autonomously generated by a specialized group of pacemaker cells within the heart itself. Unlike the skeletal muscle and its fibers, the myocardium lacks origin and insertion. Despite hundreds of years of anatomical dissection, many details of the heart’s structure, as related to its function, remain unresolved. Pettigrew demonstrated that the myocardial wall in sheep consists of seven layers which “overlap externally and internally and equilibrate each other according to mathematical law” and maintained that the arrangement of myocardial fibers holds the key to its function. Carl Ludwig introduced the concept of a muscular cylinder as the principal structure of the left ventricle, enveloped by endocardial and epicardial layers, crossing at the right angles of its longitudinal axis in the form of an X. Hunter and Smaill proposed that methods of continuum mechanics provide a suitable theoretical framework for the analysis of the complex interaction between mechanical, metabolic, and electrical functions of the heart. Diffusion tensor magnetic resonance imaging (DTMRI), a novel technique which enables visual “tracking” of the aggregated myocyte chains within ventricular walls, has confirmed the three-dimensional helical fiber patterns proposed by Pettigrew.

Two contrasting models of ventricular function have been developed over the past decades: Torrent-Guasp’s ventricular myocardial band (VMB) and Lunkenheimer’s “antagonistic force” model. Both models assume that the heart functions as a pressure propulsion pump. It is proposed that the vortex-like form of the mature heart, situated at the confluence of the systemic and pulmonary veins, reveals its true, blood-restraining function. This is confirmed by the unique, stretch-resistant myocardial architecture and by the presence of highly organized intracardiac fluid forms, the vortices.

Keywords

Heart-functional morphology Rotational vortex Irrotational vortex Lemniscates Myocardial fibers Myocardial twist Wiggers diagram Ventricular myocardial band Opposing force model Intracardiac flow patterns Helical aortic flow Flow-restraining function 

References

  1. 1.
    Mann DL, Bristow MR. Mechanisms and models in heart failure: the biomechanical model and beyond. Circulation. 2005;111(21):2837–49.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Buckberg GD, et al. Left ventricular form and function. Circulation. 2004;110(14):e333–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Pettigrew JB. On the arrangement of the muscular fibres in the ventricles of the vertebrate heart, with physiological remarks. Philos Trans R Soc Lond. 1864;154:445–500.CrossRefGoogle Scholar
  4. 4.
    Benninghoff A. Die Architektur des Herzmuskels. Eine vergleichend anatomische und vergleichend funktionelle Betrachtung. Morph Jarhb. 1931;67:262–317.Google Scholar
  5. 5.
    Siegel RE. Galen’s views on the heart and blood flow. In: Galen’s system of physiology and medicine. Basel: Karger; 1968. p. 30–134.Google Scholar
  6. 6.
    Prioreschi P. A history of medicine, vol. 3. Omaha: Horatius Press; 1996.Google Scholar
  7. 7.
    McMurrich JP. Leonardo da Vinci, the anatomist (1452-1519), vol. 411. Baltimore: Williams & Wilkins, for Carnegie Institution of Washington; 1930.Google Scholar
  8. 8.
    Pasipoularides A. Heart’s vortex: intracardiac blood flow phenomena. Shelton: People’s Medical Publishing House-USA; 2010. p. 119–27.Google Scholar
  9. 9.
    Wandt B. Long-axis contraction of the ventricles: a modern approach, but described already by Leonardo da Vinci. J Am Soc Echocardiogr. 2000;13(7):699–706.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Lower R. Tractatus de Corde. Early Science in Oxford; 1932 (Transl KJ Franklin).Google Scholar
  11. 11.
    Torrent-Guasp F, et al. Systolic ventricular filling. Eur J Cardiothorac Surg. 2004;25(3):376–86.PubMedCrossRefGoogle Scholar
  12. 12.
    Buckberg GD. Basic science review: the helix and the heart. J Thorac Cardiovasc Surg. 2002;124(5):863.PubMedCrossRefGoogle Scholar
  13. 13.
    Greenbaum R, et al. Left ventricular fibre architecture in man. Br Heart J. 1981;45(3):248–63.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Pettigrew JB. Design in nature, vol. 2. London: Longmans, Green and Co; 1908.Google Scholar
  15. 15.
    Pettigrew JB. Anatomical preparation making as devised and practised at the University of Edinburgh and at the Hunterian Museum of the Royal College of Surgeons of England. Lancet. 1901;158(4083):1479–84.CrossRefGoogle Scholar
  16. 16.
    Pasipoularides A. Heart’s vortex: intracardiac blood flow phenomena. Shelton: People’s Medical Publishing House-USA; 2010. p. 301–2.Google Scholar
  17. 17.
    Rushmer R. Cardiovascular dynamics. 2nd ed. Philadelphia: WB Saunders; 1961. p. 35.Google Scholar
  18. 18.
    Brecher G, Galletti P. Functional anatomy of cardiac pumping. In: Hamilton W, editor. Handbook of physiology: circulation. Washington, DC: American Physiological Society; 1963. p. 759–98.Google Scholar
  19. 19.
    Ludwig C. Ueber den Bau und die Bewegungen der Herzventrikel. Z Rationelle Medicin. 1849;7:189–220.Google Scholar
  20. 20.
    von Krehl L. Beitraege zur Kenntniss der Fuellung und Entleerung des Herzens. Abhandlungen der Mathematisch-Physischen Classe der Koenigl.-Saechs. Gesellschaft der Wissenschaften. 1881;17:340–83.Google Scholar
  21. 21.
    MacCallum JB. On the muscular architecture and growth of the ventricles of the heart. Johns Hopkins Hosp Rep. 1900;9:307–35.Google Scholar
  22. 22.
    Mall FP. On the muscular architecture of the ventricles of the human heart. Am J Anat. 1911;11(3):211–66.CrossRefGoogle Scholar
  23. 23.
    Frank O. On the dynamics of cardiac muscle (Translated By Chapman CB and Wasserman E). Am Heart J. 1959;58(2):282–317.CrossRefGoogle Scholar
  24. 24.
    Starling EH. The Linacre lecture on the Law of the Heart. London: Longmans, Green & Co; 1918.Google Scholar
  25. 25.
    Patterson S, Piper H, Starling E. The regulation of the heart beat. J Physiol. 1914;48(6):465.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Katz AM. Ernest Henry starling, his predecessors, and the Law of the Heart. Circulation. 2002;106(23):2986–92.PubMedCrossRefGoogle Scholar
  27. 27.
    Mommaerts WFM. Heart Muscle. In: Fishman AP, Richards DW, editors. Circulation of the blood: men and ideas. Washington, DC: American Physiological Society; 1982. p. 127–98.Google Scholar
  28. 28.
    Lunkenheimer PP, Redmann K, Anderson RH. The architecture of the ventricular mass and its functional implications for organ-preserving surgery. Eur J Cardiothorac Surg. 2005;27(2):183–90.PubMedCrossRefGoogle Scholar
  29. 29.
    Lunkenheimer PP, et al. Models of ventricular structure and function reviewed for clinical cardiologists. J Cardiovasc Transl Res. 2013;6(2):176–86.PubMedCrossRefGoogle Scholar
  30. 30.
    Lev M, Simkins C. Architecture of the human ventricular myocardium; technic for study using a modification of the Mall-MacCallum method. Lab Invest. 1956;5(5):396–409.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Grant RP. Notes on the muscular architecture of the left ventricle. Circulation. 1965;32(2):301–8.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Streeter DD Jr, Bassett DL. An engineering analysis of myocardial fiber orientation in pig’s left ventricle in systole. Anat Rec. 1966;155(4):503–11.CrossRefGoogle Scholar
  33. 33.
    Streeter DD Jr, et al. Fiber orientation in the canine left ventricle during diastole and systole. Circ Res. 1969;24(3):339–47.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Anderson RH, et al. The anatomical arrangement of the myocardial cells making up the ventricular mass. Eur J Cardiothorac Surg. 2005;28(4):517–25.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Hunter P, Smaill B. The analysis of cardiac function: a continuum approach. Prog Biophys Mol Biol. 1988;52(2):101.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Smerup M, et al. The three-dimensional arrangement of the myocytes aggregated together within the mammalian ventricular myocardium. Anat Rec. 2009;292(1):1–11.CrossRefGoogle Scholar
  37. 37.
    Stephenson RS, et al. The functional architecture of skeletal compared to cardiac musculature: Myocyte orientation, lamellar unit morphology, and the helical ventricular myocardial band. Clin Anat. 2016;29(3):316–32.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Sengupta PP, et al. Left ventricular form and function revisited: applied translational science to cardiovascular ultrasound imaging. J Am Soc Echocardiogr. 2007;20(5):539–51.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Rohen JW. Functional morphology: the dynamic wholeness of the human organism. Hillsdale: Adonis Press; 2007.Google Scholar
  40. 40.
    Kocica MJ, et al. The helical ventricular myocardial band: global, three-dimensional, functional architecture of the ventricular myocardium. Eur J Cardiothorac Surg. 2006;29(Suppl 1):S21–40.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Buckberg GD, et al. Ventricular structure–function relations in health and disease: part I. The normal heart. Eur J Cardiothorac Surg. 2014;47(4):587–601.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Pasipoularides A. Heart’s vortex: intracardiac blood flow phenomena. Shelton, CT: People’s Medical Publishing House-USA; 2010. p. 311–7.Google Scholar
  43. 43.
    Lunkenheimer P, et al. The forces generated within the musculature of the left ventricular wall. Heart. 2004;90(2):200–7.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Lunkenheimer PP, et al. Beta-blockade at low doses restoring the physiological balance in myocytic antagonism. Eur J Cardiothorac Surg. 2007;32(2):225–30.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Brecher GA. Venous return. New York: Grune & Stratton; 1956.Google Scholar
  46. 46.
    Brecher GA. Critical review of recent work on ventricular diastolic suction. Circ Res. 1958;6(5):554–66.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Coghlan HC, et al. ‘The electrical spiral of the heart’: its role in the helical continuum: the hypothesis of the anisotropic conducting matrix. Eur J Cardiothorac Surg. 2006;29(Suppl_1):S178–87.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Buckberg G, et al. Structure and function relationships of the helical ventricular myocardial band. J Thorac Cardiovasc Surg. 2008;136(3):578–589. e11.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Rushmer RF, Crystal DK, Wagner C. The functional anatomy of ventricular contraction. Circ Res. 1953;1(2):162–70.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Buckberg G, et al. Cardiac mechanics revisited. Circulation. 2008;118(24):2571–87.PubMedCrossRefGoogle Scholar
  51. 51.
    Hayabuchi Y, Sakata M, Kagami S. Assessment of the helical ventricular myocardial band using standard echocardiography. Echocardiography. 2015;32(2):310–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Batista RJ, et al. Partial left ventriculectomy to improve left ventricular function in end-stage heart disease. J Card Surg. 1996;11(2):96–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Buckberg G. Ventricular structure and surgical history. Heart Fail Rev. 2005;9(4):255–68.CrossRefGoogle Scholar
  54. 54.
    Lunkenheimer PP, et al. Three-dimensional architecture of the left ventricular myocardium. Anat Rec. 2006;288(6):565–78.CrossRefGoogle Scholar
  55. 55.
    Anderson RH, et al. How are the myocytes aggregated so as to make up the ventricular mass? In: Seminars in thoracic and cardiovascular surgery: Pediatric cardiac surgery annual. Amsterdam: Elsevier; 2007.Google Scholar
  56. 56.
    Borg T, Caulfield J. The collagen matrix of the heart. In: Federation proceedings; 1981;40(7):2037–41.Google Scholar
  57. 57.
    Kilner PJ, et al. Asymmetric redirection of flow through the heart. Nature. 2000;404:759–61.PubMedCrossRefGoogle Scholar
  58. 58.
    Fyrenius A, et al. Three dimensional flow in the human left atrium. Heart. 2001;86(4):448.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Domenichini F, et al. Combined experimental and numerical analysis of the flow structure into the left ventricle. J Biomech. 2007;40(9):1988–94.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Geiger J, et al. 4D-MR flow analysis in patients after repair for tetralogy of Fallot. Eur Radiol. 2011;21(8):1651–7.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Markl M, Kilner PJ, Ebbers T. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2011;13(1):1–22.CrossRefGoogle Scholar
  62. 62.
    Gharib M, et al. Optimal vortex formation as an index of cardiac health. Proc Natl Acad Sci. 2006;103(16):6305–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Hong GR, et al. Characterization and quantification of vortex flow in the human left ventricle by contrast echocardiography using vector particle image velocimetry. JACC Cardiovasc Imaging. 2008;1(6):705–17.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Pasipoularides A. Heart’s vortex: intracardiac blood flow phenomena. Shelton: People’s Medical Publishing House-USA; 2010. p. 735–807.Google Scholar
  65. 65.
    Sengupta PP, et al. Left ventricular isovolumic flow sequence during sinus and paced rhythms: new insights from use of high-resolution Doppler and ultrasonic digital particle imaging velocimetry. J Am Coll Cardiol. 2007;49(8):899–908.PubMedCrossRefGoogle Scholar
  66. 66.
    Pasipoularides A, et al. Diastolic right ventricular filling vortex in normal and volume overload states. Am J Physiol Heart Circ Physiol. 2003;284(4):H1064–72.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Taylor T, Yamaguchi T. Flow patterns in three-dimensional left ventricular systolic and diastolic flows determined from computational fluid dynamics. Biorheology. 1995;32(1):61.PubMedCrossRefGoogle Scholar
  68. 68.
    Sengupta PP, et al. Twist mechanics of the left ventricle: principles and application. JACC Cardiovasc Imaging. 2008;1(3):366–76.PubMedCrossRefGoogle Scholar
  69. 69.
    Faludi R, et al. Left ventricular flow patterns in healthy subjects and patients with prosthetic mitral valves: an in vivo study using echocardiographic particle image velocimetry. J Thorac Cardiovasc Surg. 2010;139(6):1501–10.PubMedCrossRefGoogle Scholar
  70. 70.
    Maire R, et al. Abnormalities of left ventricular flow following mitral valve replacement: a colour flow Doppler study. Eur Heart J. 1994;15(3):293–302.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Pasipoularides A, et al. RV instantaneous intraventricular diastolic pressure and velocity distributions in normal and volume overload awake dog disease models. Am J Physiol Heart Circ Physiol. 2003;285(5):H1956–65.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Watanabe H, Sugiura S, Hisada T. The looped heart does not save energy by maintaining the momentum of blood flowing in the ventricle. Am J Physiol Heart Circ Physiol. 2008;294(5):H2191–6.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Pasipoularides A. Heart’s vortex: intracardiac blood flow phenomena. Shelton: People’s Medical Publishing House-USA; 2010. p. 791.Google Scholar
  74. 74.
    Kilner P, et al. Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation. 1993;88(5):2235–47.PubMedCrossRefGoogle Scholar
  75. 75.
    Marinelli R, et al. Rotary motion in the heart and blood vessels: a review. J Appl Cardiol. 1991;6(6):421–31.Google Scholar
  76. 76.
    Motomiya M, Karino T. Flow patterns in the human carotid artery bifurcation. Stroke. 1984;15(1):50–6.PubMedCrossRefGoogle Scholar
  77. 77.
    Karino T, et al. Flow patterns in vessels of simple and complex geometriesa. Ann N Y Acad Sci. 1987;516(1):422–41.PubMedCrossRefGoogle Scholar
  78. 78.
    Noble MI. The contribution of blood momentum to left ventricular ejection in the dog. Circ Res. 1968;23(5):663–70.PubMedCrossRefGoogle Scholar
  79. 79.
    Ambrosi C, Starr I. Incoordination of the cardiac contraction, as judged by the force ballistocardiogram and the carotid pulse derivative. Am Heart J. 1965;70(6):761–74.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Parker KH, et al. What stops the flow of blood from the heart? Heart Vessels. 1988;4(4):241–5.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Sugawara M, et al. Aortic blood momentum–the more the better for the ejecting heart in vivo? Cardiovasc Res. 1997;33(2):433–46.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Ohte N, et al. The mechanism of emergence and clinical significance of apically directed intraventricular flow during isovolumic relaxation. J Am Soc Echocardiogr. 2002;15(7):715–22.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Rushmer RF, Crystal DK. Changes in configuration of the ventricular chambers during the cardiac cycle. Circulation. 1951;4(2):211–8.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Katz AM. Physiology of the heart. New York: Raven Press; 1992. p. 196–218.Google Scholar
  85. 85.
    Hansford RG, Lakatta EG. Ryanodine releases calcium from sarcoplasmic reticulum in calcium-tolerant rat cardiac myocytes. J Physiol. 1987;390(1):453–67.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Lipp P, Niggli E. Microscopic spiral waves reveal positive feedback in subcellular calcium signaling. Biophys J. 1993;65(6):2272–6.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Granzier HL, Labeit S. The giant protein titin. Circ Res. 2004;94(3):284–95.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Sengupta PP, Narula J. RV form and function a piston pump, vortex impeller, or hydraulic ram? JACC Cardiovasc Imaging. 2013;6(5):636–9.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Hammond HK, et al. Heart size and maximal cardiac output are limited by the pericardium. Am J Physiol Heart Circ Physiol. 1992;263(6):H1675–81.CrossRefGoogle Scholar
  90. 90.
    Stray-Gundersen J, et al. The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circ Res. 1986;58(4):523–30.PubMedCrossRefGoogle Scholar
  91. 91.
    Forrest P. Anaesthesia and right ventricular failure. Anaesth Intensive Care. 2009;37(3):370.PubMedCrossRefGoogle Scholar
  92. 92.
    Ryan JJ, Tedford RJ. Diagnosing and treating the failing right heart. Curr Opin Cardiol. 2015;30(3):292.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Branko Furst
    • 1
  1. 1.Professor of AnesthesiologyAlbany Medical CollegeAlbanyUSA

Personalised recommendations