Impact of Clinically Relevant Elliptical Deformations on the Damage Patterns of Sagging and Stretched Leaflets in a Bioprosthetic Heart Valve

Abstract

After implantation of a transcatheter bioprosthetic heart valve its original circular circumference may become distorted, which can lead to changes in leaflet coaptation and leaflets that are stretched or sagging. This may lead to early structural deterioration of the valve as seen in some explanted transcatheter heart valves. Our in vitro study evaluates the effect of leaflet deformations seen in elliptical configurations on the damage patterns of the leaflets, with circular valve deformation as the control. Bovine pericardial tissue heart valves were subjected to accelerated wear testing under both circular (N = 2) and elliptical (N = 4) configurations. The elliptical configurations were created by placing the valve inside custom-made elliptical holders, which caused the leaflets to sag or stretch. The hydrodynamic performance of the valves was monitored and high resolution images were acquired to evaluate leaflet damage patterns over time. In the elliptically deformed valves, sagging leaflets experienced more damage from wear compared to stretched leaflets; the undistorted leaflets of the circular valves experienced the least leaflet damage. Free-edge thinning and tearing were the primary modes of damage in the sagging leaflets. Belly region thinning was seen in the undistorted and stretched leaflets. Leaflet and fabric tears at the commissures were seen in all valve configurations. Free-edge tearing and commissure tears were the leading cause of valve hydrodynamic incompetence. Our study shows that mechanical wear affects heart valve pericardial leaflets differently based on whether they are undistorted, stretched, or sagging in a valve configuration. Sagging leaflets are more likely to be subjected to free-edge tear than stretched or undistorted leaflets. Reducing leaflet stress at the free edge of non-circular valve configurations should be an important factor to consider in the design and/or deployment of transcatheter bioprosthetic heart valves to improve their long-term performance.

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

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

Abbreviations

CE:

Commissure exposure

CT:

Commissure tear

FE:

Free-edge exposure

FT:

Free-edge tear

FTh:

Free-edge thinning

BTh:

Belly region thinning

Circ:

Circular

Emin:

Ellipse minor

Emaj:

Ellipse major

AWT:

Accelerated wear testing

THV:

Transcatheter heart valve

Nm:

Nominal

Sg:

Sagging

St:

Stretched

M:

Millions

References

  1. 1.

    Aguiari, P., M. Fiorese, L. Iop, G. Gerosa, and A. Bagno. Mechanical testing of pericardium for manufacturing prosthetic heart valves. Interact. Cardiovasc. Thorac. Surg. 2015. https://doi.org/10.1093/icvts/ivv282.

    Article  Google Scholar 

  2. 2.

    Alavi, S. Hamed, E. M. Groves, and A. Kheradvar. The effects of transcatheter valve crimping on pericardial leaflets. Ann. Thorac. Surg. 97(4):1260–1266, 2014. https://doi.org/10.1016/j.athoracsur.2013.11.009.

    Article  Google Scholar 

  3. 3.

    Bapat, V. N., R. Attia, and M. Thomas. Effect of valve design on the stent internal diameter of a bioprosthetic valve. JACC 7(2):115–127, 2014. https://doi.org/10.1016/j.jcin.2013.10.012.

    Article  Google Scholar 

  4. 4.

    Benjamin, E. J., M. J. Blaha, S. E. Chiuve, M. Cushman, S. R. Das, R. Deo, S. D. de Ferranti, et al. Heart disease and stroke statistics—2017 update: a report from the american heart association. Circulation 2017. https://doi.org/10.1161/cir.0000000000000485.

    Article  Google Scholar 

  5. 5.

    Broom, N. D. The stress/strain and fatigue behaviour of glutaraldehyde preserved heart-valve tissue. J. Biomech. 10(11):707–724, 1977. https://doi.org/10.1016/0021-9290(77)90086-0.

    Article  Google Scholar 

  6. 6.

    Caudron, J., J. Fares, C. Hauville, A. Cribier, J.-N. Dacher, C. Tron, F. Bauer, P.-Y. Litzler, J.-P. Bessou, and H. Eltchaninoff. Evaluation of multislice computed tomography early after transcatheter aortic valve implantation with the Edwards SAPIEN bioprosthesis. Am. J. Cardiol. 108(6):873–881, 2011. https://doi.org/10.1016/j.amjcard.2011.05.014.

    Article  Google Scholar 

  7. 7.

    Côté, N., P. Pibarot, and M.-A. Clavel. Incidence, risk factors, clinical impact, and management of bioprosthesis structural valve degeneration. Curr. Opin. Cardiol. 2017. https://doi.org/10.1097/HCO.0000000000000372.

    Article  Google Scholar 

  8. 8.

    Delgado, V., A. C. T. Ng, N. R. van de Veire, F. van der Kley, J. D. Schuijf, L. F. Tops, A. de Weger, et al. Transcatheter aortic valve implantation: role of multi-detector row computed tomography to evaluate prosthesis positioning and deployment in relation to valve function. Eur. Heart J. 2010. https://doi.org/10.1093/eurheartj/ehq018.

    Article  Google Scholar 

  9. 9.

    Duraiswamy, N., J. D. Weaver, Y. Ekrami, S. M. Retta, and W. Changfu. A parametric computational study of the impact of non-circular configurations on bioprosthetic heart valve leaflet deformations and stresses: possible implications for transcatheter heart valves. Cardiovasc. Eng. Technol. 7(2):126–138, 2016. https://doi.org/10.1007/s13239-016-0259-9.

    Article  Google Scholar 

  10. 10.

    Fanning, J. P., D. G. Platts, D. L. Walters, and J. F. Fraser. Transcatheter aortic valve implantation (TAVI): valve design and evolution. Int. J. Cardiol. 168(3):1822–1831, 2013. https://doi.org/10.1016/j.ijcard.2013.07.117.

    Article  Google Scholar 

  11. 11.

    Fleisher, A. G., R. J. Lafaro, and R. A. Moggio. Immediate structural valve deterioration of 27-mm Carpentier-Edwards aortic pericardial bioprosthesis. Ann. Thorac. Surg. 77(4):1443–1445, 2004. https://doi.org/10.1016/S0003-4975(03)01253-0.

    Article  Google Scholar 

  12. 12.

    Grubitzsch, H., M. Galloni, and V. Falk. Wrinkles, folds and calcifications: reduced durability after transcatheter aortic valve-in-valve replacement. J. Thorac. Cardiovasc. Surg. 2017. https://doi.org/10.1016/j.jtcvs.2016.08.018.

    Article  Google Scholar 

  13. 13.

    Haziza, F., G. Papouin, B. Barratt-Boyes, G. Christie, and R. Whitlock. Tears in bioprosthetic heart valve leaflets without calcific degeneration. J. Heart Valve Dis. 5(1):35–39, 1996.

    Google Scholar 

  14. 14.

    Herrmann, H. C., and F. Maisano. Transcatheter therapy of mitral regurgitation. Circulation 130(19):1712–1722, 2014. https://doi.org/10.1161/CIRCULATIONAHA.114.009881.

    Article  Google Scholar 

  15. 15.

    Hilbert, S. L., V. J. Ferrans, H. A. McAllister, and D. A. Cooley. Ionescu-Shiley bovine pericardial bioprostheses. Histologic and ultrastructural studies. Am. J. Pathol. 140(5):1195–1204, 1992.

    Google Scholar 

  16. 16.

    Ishihara, T., V. J. Ferrans, S. W. Boyce, M. Jones, and W. C. Roberts. Structure and classification of cuspal tears and perforations in porcine bioprosthetic cardiac valves implanted in patients. Am. J. Cardiol. 48(4):665–678, 1981. https://doi.org/10.1016/0002-9149(81)90145-4.

    Article  Google Scholar 

  17. 17.

    Jang, W., S. Choi, S. H. Kim, E. Yoon, H. G. Lim, and Y. J. Kim. A comparative study on mechanical and biochemical properties of bovine pericardium after single or double crosslinking treatment. Korean Circ J. 42(3):154–163, 2012. https://doi.org/10.4070/kcj.2012.42.3.154.

    Article  Google Scholar 

  18. 18.

    Khoffi, F., and F. Heim. Mechanical degradation of biological heart valve tissue induced by low diameter crimping: an early assessment. J. Mech. Behav. Biomed. Mater. 44(April):71–75, 2015. https://doi.org/10.1016/j.jmbbm.2015.01.005.

    Article  Google Scholar 

  19. 19.

    Kiefer, P., F. Gruenwald, J. Kempfert, H. Aupperle, J. Seeburger, F. W. Mohr, and T. Walther. Crimping may affect the durability of transcatheter valves: an experimental analysis. Ann. Thorac. Surg. 92(1):155–160, 2011. https://doi.org/10.1016/j.athoracsur.2011.03.020.

    Article  Google Scholar 

  20. 20.

    Kim, E. K., S. H. Choi, P. S. Song, and S.-J. Park. Valve prosthesis distortion after cardiac compression in a patient who underwent transcatheter aortic valve implantation (TAVI). Catheter. Cardiovasc. Interv. 83(3):E165–E167, 2014. https://doi.org/10.1002/ccd.24412.

    Article  Google Scholar 

  21. 21.

    Kosek, M., A. Witkowski, M. Dąbrowski, J. Jastrzębski, I. Michałowska, Z. Chmielak, M. Demkow, et al. Transcatheter aortic valve implantation in patients with bicuspid aortic valve: a series of cases. Kardiol. Polska 73(8):627–636, 2015. https://doi.org/10.5603/KP.a2015.0068.

    Article  Google Scholar 

  22. 22.

    Lee, M. C., Y. C. Fung, R. Shabetai, and M. M. LeWinter. Biaxial mechanical properties of human pericardium and canine comparisons. Am. J. Physiol. 253(1 Pt 2):H75–H82, 1987.

    Google Scholar 

  23. 23.

    Maeno, Y., Y. Abramowitz, S.-H. Yoon, H. Jilaihawi, S. Raul, S. Israr, M. Miyasaka, et al. Transcatheter aortic valve replacement with different valve types in elliptic aortic annuli. Circ. J. 81(7):1036–1042, 2017. https://doi.org/10.1253/circj.CJ-16-1240.

    Article  Google Scholar 

  24. 24.

    Martin, C., and W. Sun. Comparison of transcatheter aortic valve and surgical bioprosthetic valve durability: a fatigue simulation study. J. Biomech. 48(12):3026–3034, 2015. https://doi.org/10.1016/j.jbiomech.2015.07.031.

    Article  Google Scholar 

  25. 25.

    Midha, P. A., V. Raghav, J. F. Condado, I. U. Okafor, S. Lerakis, V. H. Thourani, V. Babaliaros, and A. P. Yoganathan. Valve type, size, and deployment location affect hemodynamics in an in vitro valve-in-valve model. JACC 9(15):1618–1628, 2016. https://doi.org/10.1016/j.jcin.2016.05.030.

    Article  Google Scholar 

  26. 26.

    Raghav, V., I. Okafor, M. Quach, L. Dang, S. Marquez, and A. P. Yoganathan. Long-term durability of carpentier-edwards magna ease valve: a one billion cycle in vitro study. Ann. Thorac. Surg. 101(5):1759–1765, 2016. https://doi.org/10.1016/j.athoracsur.2015.10.069.

    Article  Google Scholar 

  27. 27.

    Sacks, M. S. The biomechanical effects of fatigue on the porcine bioprosthetic heart valve. J. Long Term Eff. Med. Implants 2001. https://doi.org/10.1615/JLongTermEffMedImplants.v11.i34.100.

    Article  Google Scholar 

  28. 28.

    Sacks, M. S., A. Mirnajafi, W. Sun, and P. Schmidt. Bioprosthetic heart valve heterograft biomaterials: structure, mechanical behavior and computational simulation. Expert Rev. Med. Devices 3(6):817–834, 2006. https://doi.org/10.1586/17434440.3.6.817.

    Article  Google Scholar 

  29. 29.

    Sacks, M. S., and F. J. Schoen. Collagen fiber disruption occurs independent of calcification in clinically explanted bioprosthetic heart valves. J. Biomed. Mater. Res. 62(3):359–371, 2002. https://doi.org/10.1002/jbm.10293.

    Article  Google Scholar 

  30. 30.

    Sacks, M. S., and D. B. Smith. Effects of accelerated testing on porcine bioprosthetic heart valve fiber architecture. Biomaterials 19(11–12):1027–1036, 1998.

    Article  Google Scholar 

  31. 31.

    Scharfschwerdt, M., R. Meyer-Saraei, C. Schmidtke, and H.-H. Sievers. Hemodynamics of the Edwards Sapien XT transcatheter heart valve in noncircular aortic annuli. J. Thorac. Cardiovasc. Surg. 148(1):126–132, 2014. https://doi.org/10.1016/j.jtcvs.2013.07.057.

    Article  Google Scholar 

  32. 32.

    Schoen, F. J., and R. J. Levy. Tissue heart valves: current challenges and future research perspectives. J. Biomed. Mater. Res. 47(4):439–465, 1999.

    Article  Google Scholar 

  33. 33.

    Schoen, F. J., and R. J. Levy. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann. Thorac. Surg. 79(3):1072–1080, 2005. https://doi.org/10.1016/j.athoracsur.2004.06.033.

    Article  Google Scholar 

  34. 34.

    Schultz, C. J., A. Weustink, N. Piazza, A. Otten, N. Mollet, G. Krestin, R. J. van Geuns, P. de Feyter, Patrick W. J. Serruys, and P. de Jaegere. Geometry and degree of apposition of the corevalve revalving system with multislice computed tomography after implantation in patients with aortic stenosis. J. Am. Coll. Cardiol. 54(10):911–918, 2009. https://doi.org/10.1016/j.jacc.2009.04.075.

    Article  Google Scholar 

  35. 35.

    Seeburger, J., G. Weiss, M. A. Borger, and F. W. Mohr. Structural valve deterioration of a corevalve prosthesis 9 months after implantation. Eur. Heart J. 34(21):1607, 2013. https://doi.org/10.1093/eurheartj/ehs422.

    Article  Google Scholar 

  36. 36.

    Shabetai, R. The Pericardium. Berlin: Springer, 2012.

    Google Scholar 

  37. 37.

    Souteyrand, G., K. Wilczek, A. Innorta, L. Camilleri, P. Chodor, J.-R. Lusson, P. Motreff, J.-C. Laborde, P. Chabrot, and N. Durel. Distortion of the corevalve during transcatheter aortic valve-in-valve implantation due to valve dislocation. Cardiovasc. Revasc. Med. 14(5):294–298, 2013. https://doi.org/10.1016/j.carrev.2013.05.004.

    Article  Google Scholar 

  38. 38.

    Sun, W., K. Li, and E. Sirois. Simulated elliptical bioprosthetic valve deformation: implications for asymmetric transcatheter valve deployment. J. Biomech. 43(16):3085–3090, 2010. https://doi.org/10.1016/j.jbiomech.2010.08.010.

    Article  Google Scholar 

  39. 39.

    Sun, W., M. Sacks, G. Fulchiero, J. Lovekamp, N. Vyavahare, and M. Scott. Response of heterograft heart valve biomaterials to moderate cyclic loading. J. Biomed. Mater. Res. A. 69(4):658–669, 2004.

    Article  Google Scholar 

  40. 40.

    Tang, Gilbert H. L., S. L. Lansman, M. Cohen, D. Spielvogel, L. Cuomo, H. Ahmad, and T. Dutta. Transcatheter aortic valve replacement: current developments, ongoing issues, future outlook. Cardiol. Rev. 21(2):55–76, 2013. https://doi.org/10.1097/CRD.0b013e318283bb3d.

    Article  Google Scholar 

  41. 41.

    Trowbridge, E. A., P. V. Lawford, and C. E. Crofts. Pericardial heterografts: a comparative study of suture pull-out and tissue strength. J. Biomed. Eng. 11(4):311–314, 1989.

    Article  Google Scholar 

  42. 42.

    Vesely, I. The evolution of bioprosthetic heart valve design and its impact on durability. Cardiovasc. Pathol. 12(5):277–286, 2003. https://doi.org/10.1016/S1054-8807(03)00075-9.

    Article  Google Scholar 

  43. 43.

    Vesely, I., J. E. Barber, and N. B. Ratliff. Tissue damage and calcification may be independent mechanisms of bioprosthetic heart valve failure. J. Heart Valve Dis. 10(4):471–477, 2001.

    Google Scholar 

  44. 44.

    Vesely, I., D. R. Boughner, and J. Leeson-Dietrich. Bioprosthetic valve tissue viscoelasticity: implications on accelerated pulse duplicator testing. Ann. Thorac. Surg. 60(2 Suppl):S379–S382, 1995.

    Article  Google Scholar 

  45. 45.

    Wiegner, A. W., O. H. Bing, T. K. Borg, and J. B. Caulfield. Mechanical and structural correlates of canine pericardium. Circ. Res. 49(3):807–814, 1981. https://doi.org/10.1161/01.RES.49.3.807.

    Article  Google Scholar 

  46. 46.

    Ye, J., A. Cheung, M. Yamashita, D. Wood, D. Peng, M. Gao, C. R. Thompson, et al. Transcatheter aortic and mitral valve-in-valve implantation for failed surgical bioprosthetic valves: an 8-year single-center experience. JACC 8(13):1735–1744, 2015. https://doi.org/10.1016/j.jcin.2015.08.012.

    Article  Google Scholar 

  47. 47.

    Young, E., J. F. Chen, O. Dong, S. Gao, A. Massiello, and K. Fukamachi. Transcatheter heart valve with variable geometric configuration. In vitro evaluation. Artif. Organs 35(12):1151–1159, 2011. https://doi.org/10.1111/j.1525-1594.2011.01331.x.

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the FDA’s Office of Women’s Health grants and in part by an appointment to the ORISE Research Participation Program at the FDA/CDRH, administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and FDA/CDRH. We are thankful to Edwards Lifesciences, for assisting with purchase of the surgical valves for this study. We appreciate help from our colleagues, Jon Casamento, Terry Woods, and Shiril Sivan, and our interns Lena Karkar, Nick Lane, and Robyn Hall.

Disclaimer

The mention of commercial products, their sources, or their use in connection with materials reported herein is not to be construed as either an actual or implied endorsement of such products by the Department of Health and Human Services. This material is declared a work of the U.S. Government and is not subject to copyright protection in the United Stated. Approved for public release; distribution is unlimited.

Conflict of interest

There are no conflicts of interest.

Statement of Human and Animal Studies

None/not applicable.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nandini Duraiswamy.

Additional information

Associate Editors Michael S. Sacks and Ajit P. Yoganathan oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 1588 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sritharan, D., Fathi, P., Weaver, J.D. et al. Impact of Clinically Relevant Elliptical Deformations on the Damage Patterns of Sagging and Stretched Leaflets in a Bioprosthetic Heart Valve. Cardiovasc Eng Tech 9, 351–364 (2018). https://doi.org/10.1007/s13239-018-0366-x

Download citation

Keywords

  • Bioprosthetic heart valve
  • Pericardial tissue
  • Leaflet durability
  • Non-circular deformation
  • Valve fatigue