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Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract

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Abstract

Heart morphogenesis and growth are influenced by hemodynamic forces (wall shear stress and blood pressure) acting on the walls of the heart. Mechanisms by which hemodynamic forces affect heart development are not well understood, in part because of difficulties involved in measuring these forces in vivo. In this paper, we show how wall shear stress in the heart outflow tract (OFT) of chick embryos at an early developmental stage (HH18) are affected by changes in the geometry and motion of the OFT wall. In particular, we were interested in the effects of cardiac cushions, which are protrusions of the OFT wall toward the lumen and that are located where valves will later form. We developed idealized finite element models (FEM) of the chick OFT with and without cardiac cushions. Geometrical parameters used in these models were estimated from in vivo images obtained using optical coherence tomography (OCT) techniques. The FEMs showed significant reverse blood flow (backflow) in the OFT, consistent with experimental observations in the chick heart at HH18, and revealed that cardiac cushions decrease backflow. In addition, our FEMs showed that the spatial distribution of wall shear stress is affected by cardiac cushions, with larger absolute peak values observed at the cushions. Differences in mechanical stimuli (wall shear stress) that the cells in the cardiac cushions and elsewhere are subjected to may affect valve formation and heart development.

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References

  1. Bartman T, Hove J (2005) Mechanics and function in heart morphogenesis. Dev Dyn 233:373–381

    Article  Google Scholar 

  2. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE (1997) Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ Res 80:473–481

    Google Scholar 

  3. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE (1999) Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41:87–99

    Article  Google Scholar 

  4. Hove JR, Köster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–177

    Article  Google Scholar 

  5. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, Mericko P, Stadtfeld M, Zhou D, Cheng L, Graf T, MacRae CA, Lepore JJ, Lo CW, Kahn ML (2006) Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell 11:845–857

    Article  Google Scholar 

  6. Hoffman JIE (1995) Incidence of congenital heart disease. II. Prenatal incidence. Pediatr Cardiol 16:155–165

    Article  Google Scholar 

  7. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, Zheng ZJ, Flegal K, O’Donnell C, Kittner S, Lloyd-Jones D, Goff DJ Jr, Hong Y, Adams R, Friday G, Furie K, Gorelick P, Kissela B, Marler J, Meigs J, Roger V, Sidney S, Sorlie P, Steinberger J, Wasserthiel-Smoller S, Wilson M, Wolf P (2006) Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circ 113:85–151

    Article  Google Scholar 

  8. Fisher AB, Chien S, Barakat AI, Nerem RM (2001) Endothelial cellular response to altered shear stress. Am J of Physiol Lung Cell Mol Physiol 281:529–533

    Google Scholar 

  9. Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75:519–560

    Google Scholar 

  10. Li YS, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:1949–1971

    Article  Google Scholar 

  11. Miller CE, Donlon KJ, Toia L, Wong CL, Chess PR (2000) Cyclic strain induces proliferation of cultured embryonic heart cells. In Vitro Cell Dev Biol-Animal 36:633–639

    Article  Google Scholar 

  12. Clark EB, Hu N, Frommelt P, Vandekieft GK, Dummett JL, Tomanek RJ (1989) Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol 257 (Heart Circ. Physiol. 26): 55–61

    Google Scholar 

  13. Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB (1999) Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254:238–252

    Article  Google Scholar 

  14. Groenendijk BC, Hierck BP, Vrolijk J, Baiker M, Pourquie MJ, Gittenberger-de Groot AC, Poelmann RE (2005) Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo. Circ Res 96:1291–1298

    Article  Google Scholar 

  15. Lucitti JL, Tobita K, Keller BB (2005) Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. J Exp Biol 208:1877–1885

    Article  Google Scholar 

  16. Hu N, Keller BB (1995) Relationship of simultaneous atrial and ventricular pressures in stage 16–27 chick embryos. Heart Circ Physiol 38:1359–1362

    Google Scholar 

  17. Vennemann P, Kiger KT, Lindken R, Groenendijk BC, Stekelenburg-de Vos S, ten Hagen TL, Ursem NT, Poelmann RE, Westerweel J, Hierck BP (2006) In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J Biomech 39:1191–1200

    Article  Google Scholar 

  18. Hove JR (2006) Quantifying cardiovascular flow dynamics during early development. Pediatr Res 60:6–13

    Article  Google Scholar 

  19. DeGroff CG, Thornburg BL, Pentecost JO, Thornburg KL, Gharib M, Sahn DJ, Baptista A (2003) Flow in the early embryonic human heart: a numerical study. Pediatr Cardiol 24:375–380

    Article  Google Scholar 

  20. Loots E, Hillen B, Veldman AEP (2003) The role of hemodynamics in the development of the outflow tract of the heart. J Eng Math 45:91–104

    Article  MATH  MathSciNet  Google Scholar 

  21. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88(1):49–92

    Article  Google Scholar 

  22. Clark EB, Hu N (1982) Developmental hemodynamic changes in the chick embryo from stage 18 to 27. Circ Res 51:810–815

    Google Scholar 

  23. Martinsen BJ (2005) Reference guide to the stages of chick heart embryology. Dev Dyn 233:1217–1237

    Article  Google Scholar 

  24. Rothenberg F, Fisher SA, Watanabe M (2003) Sculpting the cardiac outflow tract. Birth Defects Res C Embryo Today 69:38–45

    Article  Google Scholar 

  25. Clark EB (1984) Functional aspects of cardiac development. In: Zak R (ed) Growth of the Heart in Health and Disease. Raven Press, New York, pp 81–103

    Google Scholar 

  26. de Jong F, Opthof T, Wilde AA, Janse MJ, Charles R, Lamers WH, Moorman AF (1992) Persisting zones of slow impulse conduction in developing chicken hearts. Circ Res 71:240–250

    Google Scholar 

  27. Männer J (2000) Cardiac looping in the chick embryo: a morphological review with special reference to terminological and biomechanical aspects of the looping process. Anat Rec 259:248–262

    Article  Google Scholar 

  28. Qayyum SR, Webb S, Anderson RH, Verbeek FJ, Brown NA, Richardson MK (2001) Septation and valve formation in the outflow tract of the embryonic chick heart. Anat Rec 264:273–283

    Article  Google Scholar 

  29. Keller BB, Hu N, Clark EB (1990) Correlation of ventricular area, perimeter and conotruncal diameter with ventricular mass and function in the chick embryo from stages 12 to 24. Circ Res 66:109–114

    Google Scholar 

  30. Hu N, Clark EB (1989) Hemodynamics of the stage 12 to stage 29 chick embryo. Circ Res 65:1665–1670

    Google Scholar 

  31. Davies PF, Zilberberg J, Helmke BP (2003) Spatial microstimuli in endothelial mechanosignaling. Circ Res 92:359–370

    Article  Google Scholar 

  32. White CR, Haidekker M, Bao X, Frangos JA (2001) Temporal gradients in shear, but not spatial gradients stimulate endothelial cell proliferation. Circ 103:2508–2513

    Google Scholar 

  33. Liu A, Rugonyi S, Pentecost JO, Thornburg KL (2007) Finite element modeling of blood flow-induced mechanical forces in the outflow tract of chick embryonic hearts. Comput Struct 85:727–738

    Article  Google Scholar 

  34. Wang RK, Ma ZH (2006) A practical approach to eliminate autocorrelation artifacts for volume-rate spectral domain optical coherence tomography. Phys Med Biol 51:3231–3239

    Article  MathSciNet  Google Scholar 

  35. Wang RK (2007) In vivo full range complex Fourier Domain optical coherence tomography. Appl Phys Lett 90:1–3

    Google Scholar 

  36. Wang RK, Ma ZH (2006) Real time flow imaging by removing texture pattern artifacts in spectral domain optical Doppler tomography. Opt Lett 31:3001–3003

    Article  Google Scholar 

  37. Donea J (1983) Arbitrary Lagrangian–Eulerian finite element methods. In: Belytschko T, Hughes T (eds) Computational methods for transient analysis. Elsevier, Amsterdam, pp 474–515

    Google Scholar 

  38. Rugonyi S, Bathe KJ (2001) On finite element analysis of fluids flows fully coupled with structural interactions. CMES 2:195–212

    Google Scholar 

  39. Chadwick P (1976) Continuum Mechanics: Concise Theory and Problems. Dover Publications Inc, New York

    Google Scholar 

  40. Hogers B, DeRuiter MC, Baasten AM, Gittenberger-de Groot AC, Poelmann RE (1995) Intracardiac blood flow patterns related to the yolk sac circulation of the chick embryo. Circ Res 76:871–877

    Google Scholar 

  41. ADINA R&D (2006) Adina System Online Manuals. Adina R&D Inc, Massachusetts, USA

  42. Bathe KJ, Zhang H (2002) A flow-condition-based interpolation finite element procedure for incompressible fluid flows. Comput Struct 80:1267–1277

    Article  MathSciNet  Google Scholar 

  43. White FM (2006) Viscous Fluid Flow. McGraw-Hill, New York

    Google Scholar 

  44. Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation: positive correlation between the plaque location and low oscillating shear stress. Arterioscl 5:293–302

    Google Scholar 

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Acknowledgments

This work was partially supported by a Beginning Grant-in-Aid from the Pacific Mountain Affiliate of the American Heart Association (0760063Z).

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Correspondence to Sandra Rugonyi.

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Liu, A., Wang, R.K., Thornburg, K.L. et al. Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract. Engineering with Computers 25, 73–86 (2009). https://doi.org/10.1007/s00366-008-0107-0

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  • DOI: https://doi.org/10.1007/s00366-008-0107-0

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