Skip to main content
Log in

Engineering Analysis of Tricuspid Annular Dynamics in the Beating Ovine Heart

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

Abstract

Functional tricuspid regurgitation is a significant source of morbidity and mortality in the US. Furthermore, treatment of functional tricuspid regurgitation is suboptimal with significant recurrence rates, which may, at least in part, be due to our limited knowledge of the relationship between valvular shape and function. Here we study the dynamics of the healthy in vivo ovine tricuspid annulus to improve our understanding of normal annular deformations throughout the cardiac cycle. To this end, we determine both clinical as well as engineering metrics of in vivo annular dynamics based on sonomicrometry crystals surgically attached to the annulus. We confirm that the tricuspid annulus undergoes large dynamic changes in area, perimeter, height, and eccentricity throughout the cardiac cycle. This deformation may be described as asymmetric in-plane motion of the annulus with minor out-of-plane motion. In addition, we employ strain and curvature to provide mechanistic insight into the origin of this deformation. Specifically, we find that strain and curvature vary considerable across the annulus with highly localized minima and maxima resulting in aforementioned configurational changes throughout the cardiac cycle. It is our hope that these data provide valuable information for clinicians and engineers alike and ultimately help us improve treatment of functional tricuspid regurgitation.

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

Similar content being viewed by others

References

  1. Amini Khoiy, K., and R. Amini. On the biaxial mechanical response of porcine tricuspid valve leaflets. J. Biomech. Eng. 138:104504, 2016.

    Article  Google Scholar 

  2. Amini Khoiy, K., D. Biswas, T. N. Decker, K. T. Asgarian, F. Loth, and R. Amini. Surface strains of porcine tricuspid valve septal leaflets measured in ex vivo beating hearts. J. Biomech. Eng. 138:111006, 2016.

    Article  Google Scholar 

  3. Baillargeon, B., I. Costa, J. R. Leach, L. C. Lee, M. Genet, A. Toutain, J. F. Wenk, M. K. Rausch, N. Rebelo, G. Acevedo-Bolton, E. Kuhl, J. L. Navia, and J. M. Guccione. Human cardiac function simulator for the optimal design of a novel annuloplasty ring with a sub-valvular element for correction of ischemic mitral regurgitation. Cardiovasc. Eng. Technol. 6:105–116, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Basu, A., and Z. He. Annulus tension on the tricuspid valve: an in-vitro study. Cardiovasc. Eng. Technol. 7:270–279, 2016.

    Article  PubMed  Google Scholar 

  5. Bothe, W., E. Kuhl, J. P. E. Kvitting, M. K. Rausch, S. Göktepe, J. C. Swanson, S. Farahmandia, N. B. Ingels, and D. C. Miller. Rigid, complete annuloplasty rings increase anterior mitral leaflet strains in the normal beating ovine heart. Circulation 124:S81–S96, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bothe, W., M. K. Rausch, J. P. E. Kvitting, D. K. Echtner, M. Walther, N. B. Ingels, E. Kuhl, and D. Craig Miller. How do annuloplasty rings affect mitral annular strains in the normal beating ovine heart? Circulation 126:S231–S238, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chan, V., I. G. Burwash, B. K. Lam, T. Auyeung, A. Tran, T. G. Mesana, and M. Ruel. Clinical and echocardiographic impact of functional tricuspid regurgitation repair at the time of mitral valve replacement. Ann. Thorac. Surg. 88:1209–1215, 2009.

    Article  PubMed  Google Scholar 

  8. Eckert, C. E., B. Zubiate, M. Vergnat, J. H. Gorman, R. C. Gorman, and M. S. Sacks. In vivo dynamic deformation of the mitral valve annulus. Ann. Biomed. Eng. 37:1757–1771, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fawzy, H., K. Fukamachi, C. D. Mazer, A. Harrington, D. Latter, D. Bonneau, and L. Errett. Complete mapping of the tricuspid valve apparatus using three-dimensional sonomicrometry. J. Thorac. Cardiovasc. Surg. 141:1037–1043, 2011.

    Article  PubMed  Google Scholar 

  10. Fukuda, S., A. M. Gillinov, P. M. McCarthy, W. J. Stewart, J. M. Song, T. Kihara, M. Daimon, M. S. Shin, J. D. Thomas, and T. Shiota. Determinants of recurrent or residual functional tricuspid regurgitation after tricuspid annuloplasty. Circulation 114:I-582–I-587, 2006.

    Google Scholar 

  11. Fukuda, S., G. Saracino, Y. Matsumura, M. Daimon, H. Tran, N. L. Greenberg, T. Hozumi, J. Yoshikawa, J. D. Thomas, and T. Shiota. Three-dimensional geometry of the tricuspid annulus in healthy subjects and in patients with functional tricuspid regurgitation a real-time, 3-dimensional echocardiographic study. Circulation 2006. https://doiorg.10.1161/CIRCULATIONAHA.105.000257.

    Google Scholar 

  12. Gorman, J. H., R. C. Gorman, B. M. Jackson, Y. Enomoto, M. G. St. John-Sutton, and L. H. Edmunds. Annuloplasty ring selection for chronic ischemic mitral regurgitation: lessons from the ovine model. Ann. Thorac. Surg. 76:1556–1563, 2003.

    Article  PubMed  Google Scholar 

  13. Gorman, J. H., R. C. Gorman, T. Plappert, B. M. Jackson, Y. Hiramatsu, M. G. St. John-Sutton, and L. H. Edmunds, Jr. Infarct size and location determine development of mitral regurgitation in the sheep model. J. Thorac. Cardiovasc. Surg. 115:615–622, 1998.

    Article  PubMed  Google Scholar 

  14. Hiro, M. E., J. Jouan, M. R. Pagel, E. Lansac, K. H. Lim, H.-S. Lim, and C. M. Duran. Sonometric study of the normal tricuspid valve annulus in sheep. J. Heart Valve Dis. 13:452–460, 2004.

    PubMed  Google Scholar 

  15. Jouan, J., M. R. Pagel, M. E. Hiro, K. H. Lim, E. Lansac, and C. M. G. Duran. Further information from a sonometric study of the normal tricuspid valve annulus in sheep: geometric changes during the cardiac cycle. J. Heart Valve Dis. 16:511–518, 2007.

    PubMed  Google Scholar 

  16. Leng, S., M. Jiang, X. D. Zhao, J. C. Allen, G. S. Kassab, R. Z. Ouyang, J. Le Tan, B. He, R. S. Tan, and L. Zhong. Three-dimensional tricuspid annular motion analysis from cardiac magnetic resonance feature-tracking. Ann. Biomed. Eng. 44:3522–3538, 2016.

    Article  PubMed  Google Scholar 

  17. Malinowski, M., A. G. Proudfoot, D. Langholz, L. Eberhart, M. Brown, H. Schubert, J. Wodarek, and T. A. Timek. Large animal model of functional tricuspid regurgitation in pacing induced end-stage heart failure. Interact. Cardiovasc. Thorac. Surg. 24:905–910, 2017.

    Article  PubMed  Google Scholar 

  18. Malinowski, M., P. Wilton, A. Khaghani, M. Brown, D. Langholz, V. Hooker, L. Eberhart, R. L. Hooker, and T. A. Timek. The effect of acute mechanical left ventricular unloading on ovine tricuspid annular size and geometry. Interact. Cardiovasc. Thorac. Surg. 23:391–396, 2016.

    Article  PubMed  Google Scholar 

  19. Malinowski, M., P. Wilton, A. Khaghani, D. Langholz, V. Hooker, L. Eberhart, R. L. Hooker, and T. A. Timek. The effect of pulmonary hypertension on ovine tricuspid annular dynamics. Eur. J. Cardio-thorac. Surg. 49:40–45, 2016.

    Article  Google Scholar 

  20. Mutlak, D., D. Aronson, J. Lessick, S. A. Reisner, S. Dabbah, and Y. Agmon. Functional tricuspid regurgitation in patients with pulmonary hypertension: is pulmonary artery pressure the only determinant of regurgitation severity? Chest 135:115–121, 2009.

    Article  PubMed  Google Scholar 

  21. Nishi, H., K. Toda, S. Miyagawa, Y. Yoshikawa, S. Fukushima, M. Kawamura, D. Yoshioka, T. Saito, T. Ueno, T. Kuratani, and Y. Sawa. Tricuspid annular dynamics before and after tricuspid annuloplasty- three-dimensional transesophageal echocardiography. Circ. J. 79:873–879, 2015.

    Article  PubMed  Google Scholar 

  22. Onoda, K., F. Yasuda, M. Takao, T. Shimono, K. Tanaka, H. Shimpo, and I. Yada. Long-term follow-up after Carpentier-Edwards ring annuloplasty for tricuspid regurgitation. Ann. Thorac. Surg. 70:796–799, 2000.

    Article  CAS  PubMed  Google Scholar 

  23. Oren, M., O. Oren, A. Feldman, L. Bloch, and Y. Turgeman. Permanent lone atrial fibrillation and atrioventricular valve regurgitation: may the former lead to the latter? J. Heart Valve Dis. 23:759–764, 2014.

    PubMed  Google Scholar 

  24. Rausch, M. K., W. Bothe, J. P. E. Kvitting, S. Göktepe, D. Craig Miller, and E. Kuhl. In vivo dynamic strains of the ovine anterior mitral valve leaflet. J. Biomech. 44:1149–1157, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Rausch, M. K., W. Bothe, J. P. E. Kvitting, J. C. Swanson, N. B. Ingels, D. C. Miller, and E. Kuhl. Characterization of mitral valve annular dynamics in the beating heart. Ann. Biomed. Eng. 39:1690–1702, 2011.

    Article  PubMed  Google Scholar 

  26. Rausch, M. K., W. Bothe, J. P. E. Kvitting, J. C. Swanson, D. C. Miller, and E. Kuhl. Mitral valve annuloplasty: a quantitative clinical and mechanical comparison of different annuloplasty devices. Ann. Biomed. Eng. 40:750–761, 2012.

    Article  PubMed  Google Scholar 

  27. Rausch, M. K., F. A. Tibayan, N. B. Ingels, D. C. Miller, and E. Kuhl. Mechanics of the mitral annulus in chronic ischemic cardiomyopathy. Ann. Biomed. Eng. 41:2171–2180, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Rausch, M. K., A. M. Zöllner, M. Genet, B. Baillargeon, W. Bothe, and E. Kuhl. A virtual sizing tool for mitral valve annuloplasty. Int. J. Numer. Method Biomed. Eng. 2017. https://doiorg.10.1002/cnm.2788.

    PubMed  Google Scholar 

  29. Ring, L., B. S. Rana, A. Kydd, J. Boyd, K. Parker, and R. A. Rusk. Dynamics of the tricuspid valve annulus in normal and dilated right hearts: a three-dimensional transoesophageal echocardiography study. Eur. Heart J. Cardiovasc. Imaging 13:756–762, 2012.

    Article  PubMed  Google Scholar 

  30. Saeed, D., T. Kidambi, S. Shalli, B. Lapin, S. C. Malaisrie, R. Lee, W. G. Cotts, and E. C. McGee. Tricuspid valve repair with left ventricular assist device implantation: is it warranted? J. Heart Lung Transplant. 30:530–535, 2011.

    Article  PubMed  Google Scholar 

  31. Salgo, I. S., J. H. Gorman, R. C. Gorman, B. M. Jackson, F. W. Bowen, T. Plappert, M. G. St John Sutton, and L. H. Edmunds. Effect of annular shape on leaflet curvature in reducing mitral leaflet stress. Circulation 106:711–717, 2002.

    Article  PubMed  Google Scholar 

  32. Smith, D. Annulus Tension in the Tricuspid Valve: The Effects of Annulus Dilation and Papillary Muscle Movement. Thesis. 2012.

  33. Spinner, E. M., D. Buice, C. H. Yap, and A. P. Yoganathan. The effects of a three-dimensional, saddle-shaped annulus on anterior and posterior leaflet stretch and regurgitation of the tricuspid valve. Ann. Biomed. Eng. 40:996–1005, 2012.

    Article  PubMed  Google Scholar 

  34. Spinner, E. M., S. Lerakis, J. Higginson, M. Pernetz, S. Howell, E. Veledar, and A. P. Yoganathan. Erratum: correlates of tricuspid regurgitation as determined by 3d echocardiography: pulmonary arterial pressure, ventricle geometry, annular dilatation, and papillary muscle displacement. Circulation 5:43–45, 2012.

    PubMed  Google Scholar 

  35. Tei, C., J. P. Pilgrim, P. M. Shah, J. A. Ormiston, and M. Wong. The tricuspid valve annulus: study of size and motion in normal subjects and in patients with tricuspid regurgitation. Circulation 66:665–672, 1982.

    Article  CAS  PubMed  Google Scholar 

  36. Ton-Nu, T.-T., R. A. Levine, M. D. Handschumacher, D. J. Dorer, C. Yosefy, D. Fan, L. Hua, L. Jiang, and J. Hung. Geometric determinants of functional tricuspid regurgitation. Circulation 114:143–149, 2006.

    Article  PubMed  Google Scholar 

  37. Zhou, X., Y. Otsuji, S. Yoshifuku, T. Yuasa, H. Zhang, K. Takasaki, K. Matsukida, A. Kisanuki, S. Minagoe, and C. Tei. Impact of atrial fibrillation on tricuspid and mitral annular dilatation and valvular regurgitation. Circ. J. 66:913–916, 2002.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by an internal Grant from the Meijer Heart and Vascular Institute at Spectrum Health.

Conflict of interest

None of the authors have conflict of interest to report.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manuel K. Rausch.

Additional information

Associate Editor Ender A. Finol oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 3319 kb)

Supplementary material 2 (MP4 3005 kb)

Supplementary material 3 (MP4 3433 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rausch, M.K., Malinowski, M., Wilton, P. et al. Engineering Analysis of Tricuspid Annular Dynamics in the Beating Ovine Heart. Ann Biomed Eng 46, 443–451 (2018). https://doi.org/10.1007/s10439-017-1961-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-017-1961-y

Keywords

Navigation