Skip to main content

Advertisement

Log in

Peristaltic-Like Motion of the Human Fetal Right Ventricle and its Effects on Fluid Dynamics and Energy Dynamics

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

In both adult human and canine, the cardiac right ventricle (RV) is known to exhibit a peristaltic-like motion, where RV sinus (inflow region) contracts first and the infundibulum (outflow region) later, in a wave-like contraction motion. The delay in contraction between the sinus and infundibulum averaged at 15% of the cardiac cycle and was estimated to produce an intra-ventricular pressure difference of 15 mmHg. However, whether such a contractile motion occurs in human fetuses as well, its effects on hemodynamics remains unknown, and are the subject of the current study. Hemodynamic studies of fetal hearts are important as previous works showed that healthy cardiac development is sensitive to fluid mechanical forces. We performed 4D clinical ultrasound imaging on eight 20-weeks old human fetuses. In five fetal RVs, peristaltic-like contractile motion from the sinus to infundibulum (“forward peristaltic-like motion”) was observed, but in one RV, peristaltic-like motion was observed from the infundibulum to sinus (“reversed peristaltic-like motion”), and two RVs contraction delay could not be determined due to poor regression fit. Next, we performed dynamic-mesh computational fluid dynamics simulations with varying extents of peristaltic-like motions for three of the eight RVs. Results showed that the peristaltic-like motion did not affect flow patterns significantly, but had significant influence on energy dynamics: increasing extent of forward peristaltic-like motion reduced the energy required for movement of fluid out of the heart during systolic ejection, while increasing extent of reversed peristaltic-like motion increased the required energy. It is currently unclear whether the peristaltic-like motion is an adaptation to reduce physiological energy expenditure, or merely an artefact of the cardiac developmental process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Allan, L., S. K. Chita, W. Al-Ghazali, D. Crawford, and M. Tynan. Doppler echocardiographic evaluation of the normal human fetal heart. Br. Heart J. 57:528–533, 1987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Armour, J., J. Pace, and W. Randall. Interrelationship of architecture and function of the right ventricle. Am. J. Physiol.-Leg. Content 218:174–179, 2016.

    Google Scholar 

  3. Geva, T., A. J. Powell, E. C. Crawford, T. Chung, and S. D. Colan. Evaluation of regional differences in right ventricular systolic function by acoustic quantification echocardiography and cine magnetic resonance imaging. Circulation 98:339–345, 1998.

    Article  CAS  PubMed  Google Scholar 

  4. Harada, K., M. J. Rice, T. Shiota, M. Ishii, R. W. McDonald, M. D. Reller, and D. J. Sahn. Gestational age-and growth-related alterations in fetal right and left ventricular diastolic filling patterns. Am. J. Cardiol. 79:173–177, 1997.

    Article  CAS  PubMed  Google Scholar 

  5. Hove, J. R., R. W. Koster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–177, 2003.

    Article  CAS  PubMed  Google Scholar 

  6. Kenny, J. F., T. Plappert, P. Doubilet, D. H. Saltzman, M. Cartier, L. Zollars, G. Leatherman, and M. S. J. Sutton. Changes in intracardiac blood flow velocities and right and left ventricular stroke volumes with gestational age in the normal human fetus: a prospective Doppler echocardiographic study. Circulation 74:1208–1216, 1986.

    Article  CAS  PubMed  Google Scholar 

  7. Lai, C. Q., G. L. Lim, M. Jamil, C. N. Z. Mattar, A. Biswas, and C. H. Yap. Fluid mechanics of blood flow in human fetal left ventricles based on patient-specific 4D ultrasound scans. Biomech. Modeling Mechanobiol. 15:1159–1172, 2016.

    Article  Google Scholar 

  8. Li, Y., J. Sun, C. K. Tang, and I. Y. Shum. Lazy snapping. Acm Trans. Graph. 23:303–308, 2004.

    Article  Google Scholar 

  9. Molina, F., C. Faro, A. Sotiriadis, T. Dagklis, and K. Nicolaides. Heart stroke volume and cardiac output by four-dimensional ultrasound in normal fetuses. Ultrasound Obstet. Gynecol. 32:181–187, 2008.

    Article  CAS  PubMed  Google Scholar 

  10. Moorman, A. F., F. De Jong, M. M. Denyn, and W. H. Lamers. Development of the cardiac conduction system. Circu. Res. 82:629–644, 1998.

    Article  CAS  Google Scholar 

  11. Moss, A. J., and F. H. Adams. Heart Disease in Infants, Children, and Adolescents. Baltimore: Williams & Wilkins Company, 1968.

    Google Scholar 

  12. Paladini, D., M. Vassallo, G. Sglavo, C. Lapadula, and P. Martinelli. The role of spatio-temporal image correlation (STIC) with tomographic ultrasound imaging (TUI) in the sequential analysis of fetal congenital heart disease. Ultrasound Obstet. Gynecol. 27:555–561, 2006.

    Article  CAS  PubMed  Google Scholar 

  13. Raines, R., M. LeWinter, and J. Covell. Regional shortening patterns in canine right ventricle. Am. J. Physiol.-Leg. Content 231:1395–1400, 1976.

    CAS  Google Scholar 

  14. Ramanathan, C., P. Jia, R. Ghanem, K. Ryu, and Y. Rudy. Activation and repolarization of the normal human heart under complete physiological conditions. Proc. Natl. Acad. Sci. 103:6309–6314, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Steinman D. and L. Antiga. VMTK-Vascular Modeling Toolkit. Webpage, 2008.

  16. Tobita, K., and B. B. Keller. Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am. J. Physiol. Heart Circ. Physiol. 279:H959–H969, 2000.

    CAS  PubMed  Google Scholar 

  17. Tworetzky, W., L. Wilkins-Haug, R. W. Jennings, M. E. van der Velde, A. C. Marshall, G. R. Marx, S. D. Colan, C. B. Benson, J. E. Lock, and S. B. Perry. Balloon dilation of severe aortic stenosis in the fetus potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation 110:2125–2131, 2004.

    Article  PubMed  Google Scholar 

  18. Wiputra, H., C. Q. Lai, G. L. Lim, J. J. W. Heng, L. Guo, S. M. Soomar, H. L. Leo, A. Biwas, C. N. Z. Mattar, and C. H. Yap. Fluid mechanics of human fetal right ventricles from image-based computational fluid dynamics using 4D clinical ultrasound scans. Am. J. Physiol.-Heart Circ. Physiol. 311:H1498–H1508, 2016.

    Article  PubMed  Google Scholar 

  19. Wiputra, H., G. L. Lim, D. A. K. Chia, C. N. Z. Mattar, A. Biswas, and C. H. Yap. Methods for fluid dynamics simulations of human fetal cardiac chambers based on patient-specific 4D ultrasound scans. J. Biomech. Sci. Eng. 11:15, 2016.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the National University of Singapore Young Investigator Award, grant entitled “Fluid Mechanics and Mechanobiology of Congenital Cardiac Outflow Tract Malformations” (PI: Yap) for funding, and the National University of Singapore Graduate School of Integrated Sciences and Engineering Scholarship for funding support for the lead author, Hadi Wiputra.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Choon Hwai Yap.

Additional information

Associate Editor Dan Elson oversaw the review of this article.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wiputra, H., Lim, G.L., Chua, K.C. et al. Peristaltic-Like Motion of the Human Fetal Right Ventricle and its Effects on Fluid Dynamics and Energy Dynamics. Ann Biomed Eng 45, 2335–2347 (2017). https://doi.org/10.1007/s10439-017-1886-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-017-1886-5

Keywords

Navigation