Skip to main content

Flow in the Early Embryonic Human Heart

Abstract

Computational fluid dynamic (CFD) experimentation provides a unique medium for detailed examination of flow through complex embryonic heart structures. The purpose of this investigation was to demonstrate that streaming blood flow patterns exist in the early embryonic heart and that fluid surface stresses change significantly with anomalous alterations in fetal heart lumen shape. Stages 10 and 11 early human embryo hearts were digitized as calibrated two-dimensional (2D) cross-sectional sequential images. A 3D surface was constructed from the stacking of these 2D images. CFD flow solutions were obtained (steady and pulsatile flow). Particle traces were placed in the inlet and outlet portions of these two stages. Sections of the embryonic heart were artificially reshaped. CFD flow solutions were obtained and surface stress changes analyzed. Streaming was shown to exist, with particles released on one or the other side of the cardiac lumen tending not to cross over and mix with particles released from the opposite side of the cardiac lumen. Shear stress changes (stage 10) occur in the altered lumens. Streaming exists in steady and pulsatile flow scenarios in the embryonic heart models. There are differences in local shear stress distributions with surface shape anomalies of the fetal heart lumen. These observations may help shed light on the potential role of fluid dynamic factors in determining patterns of abnormal heart development.

This is a preview of subscription content, access via your institution.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

References

  1. HL Bergman JM Siegel JN Oshinski RI Pettigrew DN Ku (1996) ArticleTitleComputational simulation of magnetic resonance angiograms in stenotic vessels: effect of stenosis severity. Adv Bioeng 33 295–296

    Google Scholar 

  2. JL Bremer (1932) ArticleTitleThe presence and influence of two spiral streams in the heart of chick embryo. Am J Anat 49 409–440

    Google Scholar 

  3. KR Chein (2000) ArticleTitleMeeting Koch’s postulates for calcium signaling in cardiac hypertrophy. [Comment] J Clin Invest 105 1339–1342 Occurrence Handle10811840

    PubMed  Google Scholar 

  4. EB Clark N Hu (1982) ArticleTitleDevelopmental hemodynamic changes in the chick embryo from stage 18 to 27. Cir Res 51 810–815 Occurrence Handle1:STN:280:BiyD2M7jtlA%3D

    CAS  Google Scholar 

  5. EB Clark RR Markwald A Takao (1995) Developmental Mechanicisms of Heart Disease. Future Armonk, NY

    Google Scholar 

  6. PF Davies A Remuzzi EJ Gordon CF Dewey Jr MA Gimbrone (1986) ArticleTitleTurbulent fluid shear stress induces vascular endothelium cell turnover in utero. Proc Natl Acad Sci USA 83 2114–2117 Occurrence Handle1:STN:280:BimC2sjlsFM%3D Occurrence Handle3457378

    CAS  PubMed  Google Scholar 

  7. CG DeGroff AM Baptista DJ Sahn (1998) ArticleTitleInsights into the proximal flow convergence method using 2D finite elements. J Am Soc Echocardiogr 11 809–818 Occurrence Handle1:STN:280:DyaK1czotlGktw%3D%3D Occurrence Handle9719093

    CAS  PubMed  Google Scholar 

  8. CG DeGroff W Orlando R Shandas (2002) ArticleTitleInsights into the effect of aortic compliance on Doppler diastolic flow patterns seen in coarctation of the aorta: a numerical study. J Am Soc Echocardiogr Occurrence Handle11875394

    PubMed  Google Scholar 

  9. CG DeGroff R Shandas J Kwon L Valdes-Cruz (2000) ArticleTitleUtility of the proximal jet width in the assessment of regurgitant and stenotic orifices—effect of low velocity filter and comparison to actual vena contracta width: an in vitro and numerical study. Eur J Echocardiogr 1 42–54 Occurrence Handle10.1053/euje.1999.0005 Occurrence Handle1:STN:280:DC%2BD38zktlOnsw%3D%3D Occurrence Handle12086216

    Article  CAS  PubMed  Google Scholar 

  10. CG DeGroff R Shandas LM Valdes-Cruz (1998) ArticleTitleAnalysis of the effect of flow rate on the Doppler continuity equation for stenotic orifice area calculations: a numerical study. Circulation 97 1597–1605 Occurrence Handle1:STN:280:DyaK1c3lsVeqtQ%3D%3D Occurrence Handle9593565

    CAS  PubMed  Google Scholar 

  11. CG DeGroff R Shandas L Valdes-Cruz (2000) ArticleTitleAccuracy of the Bernoulli equation for estimate of pressure gradient across BT shunts: an in vitro and numerical study. Pediatr Cardiol 21 439–447 Occurrence Handle10.1007/s002460010104 Occurrence Handle1:STN:280:DC%2BD3M%2Fnt1WisQ%3D%3D Occurrence Handle10982702

    Article  CAS  PubMed  Google Scholar 

  12. G Ekman (1925) ArticleTitleExperimentelle Beitrage zur Herzentwidklung der Amphibien. Rous Arch Entwiski-Mech Org 106 320

    Google Scholar 

  13. K Goerttler (1954) ArticleTitleDurchstromungsversuche an Glasmodellen Ebryonaler Herzanlagen. Ver Disch Ges Pathol 38 220

    Google Scholar 

  14. K Goerttler (1970) Glass model experiments of embryonic human hearts. OC Jaffee (Eds) Cardiac Development with Special Reference to Human Heart Disease Dayton Press Dayton, CH 29–43

    Google Scholar 

  15. TM Griffith DH Edwards RL Davies TJ Harrison KT Evans (1987) ArticleTitleEDRF coordinates the behaviour of vascular resistance vessels. Nature 329 442–445 Occurrence Handle10.1038/329442a0 Occurrence Handle1:CAS:528:DyaL2sXlvFWktbk%3D Occurrence Handle3498901

    Article  CAS  PubMed  Google Scholar 

  16. B Hogers MC DeRuiter AC Gittenberger-de Groot RE Poelman (1999) ArticleTitleExtraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41 87–99 Occurrence Handle10.1016/S0008-6363(98)00218-1 Occurrence Handle1:CAS:528:DyaK1MXmtVKmtw%3D%3D Occurrence Handle10325956

    Article  CAS  PubMed  Google Scholar 

  17. O Hudlicka (1985) Development of microcirculation: capillary growth and adaptation. N Resnick (Eds) Handbook of Physiology, Section 2: The Cardiovascular System, Vol, 4 Williams & Wilkins Baltimore 165–216

    Google Scholar 

  18. A Kamiya T Togawa (1980) ArticleTitleAdaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol 239 H14–H21 Occurrence Handle1:STN:280:Bi%2BB3sbntFc%3D Occurrence Handle7396013

    CAS  PubMed  Google Scholar 

  19. BB Keller MJ MacLennan JP Tinney M Yoshigi (1996) ArticleTitleIn vivo assessment of embryonic cardiovascular dimensions and function in day 10.5 to 14.5 mouse embryos. Circ Res 79 247–255 Occurrence Handle1:CAS:528:DyaK28XkslyiurY%3D Occurrence Handle8756001

    CAS  PubMed  Google Scholar 

  20. BL Langille F O’Donnell (1986) ArticleTitleReductions in arterial diameter produced by chronic descreases in blood flow are endothelium-dependent. Science 231 405–407 Occurrence Handle1:STN:280:BimD1MnnvVU%3D Occurrence Handle3941904

    CAS  PubMed  Google Scholar 

  21. L Leatherbury DM Connuck HE Gauldin ML Kirby (1991) ArticleTitleHemodynamic changes and compensatory mechanisms during early cardiogenesis after neural crest ablation in chick embryos. Pediatr Res 30 509–512 Occurrence Handle1:STN:280:By2B3M3mtVY%3D Occurrence Handle1805144

    CAS  PubMed  Google Scholar 

  22. VB Makhijani JM Siegel NC Hwang (1996) ArticleTitleNumerical analysis of squeeze-flow in tilting disc mechanical heart valves. J Heart Valve Dis 5 97–103 Occurrence Handle1:STN:280:BymH3s7msFQ%3D Occurrence Handle8834732

    CAS  PubMed  Google Scholar 

  23. VB Makhijani HQ Yang PJ Dionne MJ Thubrikar (1997) ArticleTitleThree-dimensional coupled fluid-structure simulation of pericardial bioprosthetic aortic valve function. ASAIO 43 5–7

    Google Scholar 

  24. VB Makhijani HQ Yang AK Singhal NC Hwang (1994) ArticleTitleAn experimental–numerical analysis of MHV cavitation: effects of leaflet squeezing and rebound. J Heart Valve Dis 1) 35–48

    Google Scholar 

  25. FJ Manasek RG Monroe (1972) ArticleTitleEarly cardiac morphogenesis is independent of function. Dev Biol 27 584–588 Occurrence Handle1:STN:280:CS2C1M3lsFA%3D Occurrence Handle5029499

    CAS  PubMed  Google Scholar 

  26. MJ Mulvany (1992) ArticleTitleDeterminants of vascular structure. J Cardiovasc Pharmacol 19 S1–S6

    Google Scholar 

  27. SP Olsen DE Claphan PF Davies (1988) ArticleTitleHaemodynamic shear stress activates K+ current in vascular endothelial cells. Nature 331 168–170 Occurrence Handle10.1038/331168a0 Occurrence Handle2448637

    Article  PubMed  Google Scholar 

  28. F Pourageaud JG DeMey (1997) ArticleTitleStructural properties of rat mesenteric small arteries after 4-wk exposure to elevated or reduced blood flow. Am J Physiol 273 H1699–H1706 Occurrence Handle1:CAS:528:DyaK2sXnt1Srurk%3D Occurrence Handle9362233

    CAS  PubMed  Google Scholar 

  29. DJ Sahn KL Thornburg BL Thornburg et al. (2000) ArticleTitleStudies of flow in accurate models of early embryonic human heart. [Abstract] J Am Coll Cardiol 35 517A

    Google Scholar 

  30. A Spitzer (1951) ArticleTitleUber den Bauplan des Normalen und Missbildeten Herzens. Versuch Einer Phylogenetischen Theorie. Virchows Arch Pathol Anat 243 81–272

    Google Scholar 

  31. P Stohr Jr (1924) ArticleTitleExperimentelle studien an embryoanalen amphibienherzen: I Uber explanation embyonaler amphibienherzen. Rouz Arch Entwiski Mech Ork 102 426–451

    Google Scholar 

  32. R Sukumar MM Athavale VB Makhijani AJ Przekwas (1996) ArticleTitleApplication of computational fluid dynamics techniques to blood pumps. Artif Organs 20 529–533 Occurrence Handle1:STN:280:BymH3MvpsV0%3D Occurrence Handle8817950

    CAS  PubMed  Google Scholar 

  33. H Yoshida F Manasek RA Arcilla (1983) ArticleTitleIntracardiac flow patterns in early embryonic life. A reexamination. Circ Res 53 363–371 Occurrence Handle1:STN:280:BiyB1crns1M%3D Occurrence Handle6883655

    CAS  PubMed  Google Scholar 

  34. CK Zarins MA Zatina DP Giddens DN Ku S Glagov (1987) ArticleTitleShear stress regulation of artery lumen diameter in experimental atherogenesis. J Vasc Surg 5 413–420 Occurrence Handle10.1067/mva.1987.avs0050413 Occurrence Handle1:STN:280:BiaA283ntFA%3D Occurrence Handle3509594

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to C. G. DeGroff.

Appendix

Appendix

Strain rate is proportional to surface shear stress imposed on the wall by flow. Strain rate is derived from the strain rate tensor (ε ij ), which is defined as

where u i is the velocity component in the ith direction. The magnitude of strain rate (γ) is defined as

Rights and permissions

Reprints and Permissions

About this article

Cite this article

DeGroff, C., Thornburg, B., Pentecost, J. et al. Flow in the Early Embryonic Human Heart . Pediatr Cardiol 24, 375–380 (2003). https://doi.org/10.1007/s00246-002-0343-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00246-002-0343-9

Keywords

  • Computational fluid dynamics
  • Congenital heart disease
  • Embryology
  • Fetal heart