Advertisement

The Onset of Circulation

  • Branko Furst
Chapter

Abstract

It is generally assumed that the blood begins to move as soon as the heart begins its contractile activity. Evidence suggests that there is a marked variability between the first heartbeat and the movement of blood amongst the early vertebrate embryos. This points to a complex relation which exists between the first movement of plasma and the red blood cells. In order to further elucidate this intricate phenomenon, the onset of circulation in chick, mouse, and zebrafish embryos will be examined. The reviewed evidence suggests the existence of plasma flow either before, or at the beginning of contractions of the tubular heart. This primary flow or “progenitor circulation” is essentially of low-pressure type and can be compared with lymphatic flow in higher vertebrates. Its possible function is transport and distribution of erythroid progenitors produced in the yolk sac into the embryo. The timing of this event does not appear to be linked with the onset of cardiac contractions. The combination of a valveless heart and immature vessels, with incomplete endothelial lining, speak against the principle of pressure propulsion. The primary streaming should be differentiated from the secondary, oxygen-carrying circulation which assumes the role of delivering oxygen to the tissues only after a considerable delay.

Keywords

Primary circulation Secondary circulation Primary myocardium Working myocardium Hemodynamic forces Chick embryo heart Mouse embryo heart Zebrafish embryo heart Flow-driven plasticity Plasma circulation 

References

  1. 1.
    Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88(1):49–92.CrossRefGoogle Scholar
  2. 2.
    Hirota A, et al. Early events in development of electrical activity and contraction in embryonic rat heart assessed by optical recording. J Physiol. 1985;369(1):209–27.CrossRefGoogle Scholar
  3. 3.
    Kamino K. Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev. 1991;71(1):53–91.CrossRefGoogle Scholar
  4. 4.
    Sakai T, Hirota A, Kamino K. Video-imaging assessment of initial beating patterns of the early embryonic chick heart. Jpn J Physiol. 1996;46(6):465–72.CrossRefGoogle Scholar
  5. 5.
    Patten BM, Kramer TC. The initiation of contraction in the embryonic chick heart. Am J Anat. 1933;53(3):349–75.CrossRefGoogle Scholar
  6. 6.
    Patten BM. The first heart beats and the beginning of the embryonic circulation. Am Sci. 1951;39(2):224–43.Google Scholar
  7. 7.
    Sissman NJ. Developmental landmarks in cardiac morphogenesis: comparative chronology. Am J Cardiol. 1970;25(2):141–8.CrossRefGoogle Scholar
  8. 8.
    Hogers B, et al. Intracardiac blood flow patterns related to the yolk sac circulation of the chick embryo. Circ Res. 1995;76(5):871–7.CrossRefGoogle Scholar
  9. 9.
    le Noble F, et al. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development. 2004;131(2):361–75.CrossRefGoogle Scholar
  10. 10.
    Romanoff AL, Romanoff AJ. Pathogenesis of the avian embryo: an analysis of causes of malformations and prenatal death. Hoboken: Wiley; 1972.Google Scholar
  11. 11.
    Carlson BM. Patten’s foundations of embryology. New York: McGraw-Hill; 1988.Google Scholar
  12. 12.
    Hirota A, et al. Initial development of conduction pattern of spontaneous action potential in early embryonic precontractile chick heart. Dev Biol. 1983;99(2):517–23.CrossRefGoogle Scholar
  13. 13.
    Christoffels VM, Burch JBE, Moorman AFM. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc Med. 2004;14(8):301–7.CrossRefGoogle Scholar
  14. 14.
    Sedmera D, et al. Developmental transitions in electrical activation patterns in chick embryonic heart. Anat Rec A Discov Mol Cell Evol Biol. 2004;280(2):1001–9.CrossRefGoogle Scholar
  15. 15.
    Houweling AC, et al. Developmental pattern of ANF gene expression reveals a strict localization of cardiac chamber formation in chicken. Anat Rec. 2002;266(2):93–102.CrossRefGoogle Scholar
  16. 16.
    Chapman W. The effect of the heart-beat upon the development of the vascular system in the chick. Am J Anat. 1918;23(1):175–203.CrossRefGoogle Scholar
  17. 17.
    Buschmann I, et al. Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development. 2010;137(13):2187–96.CrossRefGoogle Scholar
  18. 18.
    Burggren WW. What is the purpose of the embryonic heart beat? Or how facts can ultimately prevail over physiological dogma. Physiol Biochem Zool. 2004;77(3):333–45.CrossRefGoogle Scholar
  19. 19.
    Burggren WW, Warburton SJ, Slivkoff MD. Interruption of cardiac output does not affect short-term growth and metabolic rate in day 3 and 4 chick embryos. J Exp Biol. 2000;203(24):3831–8.PubMedGoogle Scholar
  20. 20.
    Cirotto C, Arangi I. Chick embryo survival under acute carbon monoxide challenges. Comp Biochem Physiol A Physiol. 1989;94(1):117–23.CrossRefGoogle Scholar
  21. 21.
    Theiler K, Westphal H. The house mouse: atlas of embryonic development. New York: Springer-Verlag; 1989.CrossRefGoogle Scholar
  22. 22.
    Phoon CKL. Circulatory physiology in the developing embryo. Curr Opin Pediatr. 2001;13(5):456–64.CrossRefGoogle Scholar
  23. 23.
    McGrath KE, et al. Circulation is established in a stepwise pattern in the mammalian embryo. Blood. 2003;101(5):1669–76.CrossRefGoogle Scholar
  24. 24.
    Lucitti JL, et al. Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development. 2007;134(18):3317–26.CrossRefGoogle Scholar
  25. 25.
    Phoon CKL, Turnbull DH. Ultrasound biomicroscopy-Doppler in mouse cardiovascular development. Physiol Genomics. 2003;14(1):3–15.CrossRefGoogle Scholar
  26. 26.
    Ji RP, et al. Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res. 2003;92(2):133–5.CrossRefGoogle Scholar
  27. 27.
    Iida A, et al. Metalloprotease-dependent onset of blood circulation in zebrafish. Curr Biol. 2010;20(12):1110–6.CrossRefGoogle Scholar
  28. 28.
    North TE, et al. Hematopoietic stem cell development is dependent on blood flow. Cell. 2009;137(4):736–48.CrossRefGoogle Scholar
  29. 29.
    Palis J. Ontogeny of erythropoiesis. Curr Opin Hematol. 2008;15(3):155–61.CrossRefGoogle Scholar
  30. 30.
    Goss CM. The physiology of the embryonic mammalian heart before circulation. Am J Physiol. 1942;137(1):146–52.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

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

Personalised recommendations