Skip to main content
SpringerLink
Log in

Characterizing the Collagen Fiber Orientation in Pericardial Leaflets Under Mechanical Loading Conditions

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

Abstract

When implanted inside the body, bioprosthetic heart valve leaflets experience a variety of cyclic mechanical stresses such as shear stress due to blood flow when the valve is open, flexural stress due to cyclic opening and closure of the valve, and tensile stress when the valve is closed. These types of stress lead to a variety of failure modes. In either a natural valve leaflet or a processed pericardial tissue leaflet, collagen fibers reinforce the tissue and provide structural integrity such that the very thin leaflet can stand enormous loads related to cyclic pressure changes. The mechanical response of the leaflet tissue greatly depends on collagen fiber concentration, characteristics, and orientation. Thus, understating the microstructure of pericardial tissue and its response to dynamic loading is crucial for the development of more durable heart valve, and computational models to predict heart valves' behavior. In this work, we have characterized the 3D collagen fiber arrangement of bovine pericardial tissue leaflets in response to a variety of different loading conditions under Second-Harmonic Generation Microscopy. This real-time visualization method assists in better understanding of the effect of cyclic load on collagen fiber orientation in time and space.

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

Access this article

Log in via an institution

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
Figure 8
Figure 9
Figure 10
Figure 11
Figure 12
Figure 13
Figure 14
Figure 15
Figure 16

Similar content being viewed by others

References

  1. Adamczyk, M. M., and I. Vesely. Biaxial strain distributions in explanted porcine bioprosthetic valves. J. Heart Valve Dis. 11:688–695, 2002.

    PubMed  Google Scholar 

  2. Alavi, S. H., W. F. Liu, and A. Kheradvar. Inflammatory response assessment of a hybrid tissue-engineered heart valve leaflet. Ann. Biomed. Eng. 2012 (in press).

  3. Ambekar Ramachandra Rao, R., M. R. Mehta, S. Leithem, and K. C. Toussaint, Jr. Fourier transform-second-harmonic generation imaging of collagen fibers in biological tissues. In Biomedical Optics. Optical Society of America, 2010.

  4. Bellhouse, B. Velocity and pressure distributions in the aortic valve. J. Fluid Mech. 37:587–600, 1969.

    Article  Google Scholar 

  5. Billiar, K. L., and M. S. Sacks. Biaxial mechanical properties of the native and glutaraldehyde-treated aortic valve cusp: part II—a structural constitutive model. J. Biomech. Eng. 122:327, 2000.

    Article  PubMed  CAS  Google Scholar 

  6. Boulesteix, T., A. M. Pena, N. Pages, G. Godeau, M. P. Sauviat, E. Beaurepaire, and M. C. Schanne-Klein. Micrometer scale ex vivo multiphoton imaging of unstained arterial wall structure. Cytometry Part A 69:20–26, 2006.

    Article  CAS  Google Scholar 

  7. Chen, J., A. Lee, J. Zhao, H. Wang, H. Lui, D. I. McLean, and H. Zeng. Spectroscopic characterization and microscopic imaging of extracted and in situ cutaneous collagen and elastic tissue components under two-photon excitation. Skin Res. Technol. 15:418–426, 2009.

    Article  PubMed  Google Scholar 

  8. Cox, G., E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell. 3-dimensional imaging of collagen using second harmonic generation. J. Struct. Biol. 141:53–62, 2003.

    Article  PubMed  CAS  Google Scholar 

  9. Driessen, N. J. B., C. V. C. Bouten, and F. P. T. Baaijens. Improved prediction of the collagen fiber architecture in the aortic heart valve. J. Biomech. Eng. 127:329–336, 2005.

    Article  PubMed  Google Scholar 

  10. Driessen, N., G. Peters, J. Huyghe, C. Bouten, and F. Baaijens. Remodelling of continuously distributed collagen fibres in soft connective tissues. J. Biomech. 36:1151–1158, 2003.

    Article  PubMed  CAS  Google Scholar 

  11. Engelmayr, Jr., G. C., G. D. Papworth, S. C. Watkins, J. E. Mayer, Jr., and M. S. Sacks. Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. J. Biomech. 39:1819–1831, 2006.

    Article  PubMed  Google Scholar 

  12. Farivar, R. S., and L. H. Cohn. Hypercholesterolemia is a risk factor for bioprosthetic valve calcification and explantation. J. Thorac. Cardiovasc. Surg. 126:969, 2003.

    Article  PubMed  Google Scholar 

  13. Georgiou, E., T. Theodossiou, V. Hovhannisyan, K. Politopoulos, G. S. Rapti, and D. Yova. Second and third optical harmonic generation in type I collagen, by nanosecond laser irradiation, over a broad spectral region. Opt. Commun. 176:253–260, 2000.

    Article  CAS  Google Scholar 

  14. Gloeckner, D. C., K. L. Billiar, and M. S. Sacks. Effects of mechanical fatigue on the bending properties of the porcine bioprosthetic heart valve. ASAIO J. 45:59–63, 1999.

    Article  PubMed  CAS  Google Scholar 

  15. Grande, K. J., R. P. Cochran, P. G. Reinhall, and K. S. Kunzelman. Stress variations in the human aortic root and valve: the role of anatomic asymmetry. Ann. Biomed. Eng. 26:534–545, 1998.

    Article  PubMed  CAS  Google Scholar 

  16. Human, P., and P. Zilla. The possible role of immune responses in bioprosthetic heart valve failure. J. Heart Valve Dis. 10:460–466, 2001.

    PubMed  CAS  Google Scholar 

  17. Kheradvar, A., and A. Falahatpisheh. The effects of dynamic saddle annulus and leaflet length on transmitral flow pattern and leaflet stress of a bileaflet bioprosthetic mitral valve. J. Heart Valve Dis. 21:225–233, 2012.

    PubMed  Google Scholar 

  18. Lawford, P. V., M. M. Black, and P. J. Drupy. The in vivo durability of bioprosthetic heart valves: mores of failure observed in explanted valves. Eng. Med. 16:95–103, 1987.

    Article  PubMed  CAS  Google Scholar 

  19. Manji, R. A., L. F. Zhu, N. K. Nijjar, D. C. Rayner, G. S. Korbutt, T. A. Churchill, R. V. Rajotte, A. Koshal, and D. B. Ross. Glutaraldehyde-fixed bioprosthetic heart valve conduits calcify and fail from xenograft rejection. Circulation 114:318–327, 2006.

    Article  PubMed  CAS  Google Scholar 

  20. May-Newman, K., C. Lam, and F. C. P. Yin. A hyperelastic constitutive law for aortic valve tissue. J. Biomech. Eng. 131, 2009.

  21. Mol, A., N. J. B. Driessen, M. C. M. Rutten, S. P. Hoerstrup, C. V. C. Bouten, and F. P. T. Baaijens. Tissue engineering of human heart valve leaflets: a novel bioreactor for a strain-based conditioning approach. Ann. Biomed. Eng. 33:1778–1788, 2005.

    Article  PubMed  Google Scholar 

  22. Nollert, G., J. Miksch, E. Kreuzer, and B. Reichart. Risk factors for atherosclerosis and the degeneration of pericardial valves after aortic valve replacement. J. Thorac. Cardiovasc. Surg. 126:965, 2003.

    Article  PubMed  Google Scholar 

  23. Pibarot, P., and J. G. Dumesnil. Prosthetic heart valves. Circulation 119:1034–1048, 2009.

    Article  PubMed  Google Scholar 

  24. Rao, R. A., M. R. Mehta, and K. C. Toussaint, Jr. Fourier transform-second-harmonic generation imaging of biological tissues. Opt. Express 17:14534–14542, 2009.

    Article  PubMed  CAS  Google Scholar 

  25. Ruel, M., A. Kulik, F. D. Rubens, P. Bédard, R. G. Masters, A. L. Pipe, and T. G. Mesana. Late incidence and determinants of reoperation in patients with prosthetic heart valves. Eur. J. Cardiothorac. Surg. 25:364–370, 2004.

    Article  PubMed  Google Scholar 

  26. Sacks, M. S., C. J. Chuong, and R. More. Collagen fiber architecture of bovine pericardium. ASAIO J. 40:PM632–PM637, 1994.

    Article  Google Scholar 

  27. Sacks, M. S., D. B. Smith, and E. D. Hiester. A small angle light scattering device for planar connective tissue microstructural analysis. Ann. Biomed. Eng. 25:678–689, 1997.

    Article  PubMed  CAS  Google Scholar 

  28. Sacks, M. S., and A. P. Yoganathan. Heart valve function: a biomechanical perspective. Philos. Trans. R. Soc. B Biol. Sci. 362:1369–1391, 2007.

    Article  Google Scholar 

  29. Schenke-Layland, K. Non-invasive multiphoton imaging of extracellular matrix structures. J. Biophotonics 1:451–462, 2008.

    Article  PubMed  CAS  Google Scholar 

  30. Schenke-Layland, K., N. Madershahian, I. Riemann, B. Starcher, K. J. Halbhuber, K. Konig, and U. A. Stock. Impact of cryopreservation on extracellular matrix structures of heart valve leaflets. Ann. Thorac. Surg. 81:918–926, 2006.

    Article  PubMed  Google Scholar 

  31. Schoen, F., and R. Levy. Pathology of substitute heart valves. J. Cardiac Surg. 9:222–227, 1994.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  33. Senthilnathan, V., T. Treasure, G. Grunkemeier, and A. Starr. Heart valves: which is the best choice? Cardiovasc. Surg. 7:393–397, 1999.

    Article  PubMed  CAS  Google Scholar 

  34. Sivaguru, M., S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint, Jr. Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging. Opt. Express 18:24983–24993, 2010.

    Article  PubMed  CAS  Google Scholar 

  35. Thubrikar, M., J. Deck, J. Aouad, and S. Nolan. Role of mechanical stress in calcification of aortic bioprosthetic valves. J. Thorac. Cardiovasc. Surg. 86:115–125, 1983.

    Google Scholar 

  36. Timmins, L. H., Q. Wu, A. T. Yeh, J. E. Moore, and S. E. Greenwald. Structural inhomogeneity and fiber orientation in the inner arterial media. Am J Physiol Heart Circ Physiol 298:H1537–H1545, 2010.

    Article  PubMed  CAS  Google Scholar 

  37. 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. 10:471–477, 2001.

    PubMed  CAS  Google Scholar 

  38. Vesely, I., D. Bougher, and T. Song. Tissue buckling as a mechanism of bioprosthetic valve failure. Ann. Thorac. Surg. 46:302–308, 1988.

    Article  PubMed  CAS  Google Scholar 

  39. Voytik-Harbin, S. L., B. A. Roeder, J. E. Sturgis, K. Kokini, and J. P. Robinson. Simultaneous mechanical loading and confocal reflection microscopy for three-dimensional microbiomechanical analysis of biomaterials and tissue constructs. Microsc. Microanal. 9:74–85, 2003.

    Article  PubMed  CAS  Google Scholar 

  40. Vyavahare, N., M. Ogle, F. J. Schoen, R. Zand, D. C. Gloeckner, M. S. Sacks, and R. J. Levy. Mechanisms of bioprosthetic heart valve failure: fatigue causes collagen denaturation and glycosaminoglycan loss. J. Biomed. Mater. Res. 46:44–50, 1999.

    Article  PubMed  CAS  Google Scholar 

  41. Weinberg, E. J., and M. R. Kaazempur Mofrad. A finite shell element for heart mitral valve leaflet mechanics, with large deformations and 3D constitutive material model. J. Biomech. 40:705–711, 2007.

    Article  PubMed  Google Scholar 

  42. Wheatly D. H., J. Fisher, I. J. Reece, T. Spyt, and P. Breeze. Primary tissue failure in pericardial heart valves. J. Thorac. Cardiovasc. Surg. 94:367, 1999.

    Google Scholar 

  43. Yasui, T., Y. Tohno, and T. Araki. Determination of collagen fiber orientation in human tissue by use of polarization measurement of molecular second-harmonic-generation light. Appl. Opt. 43:2861–2867, 2004.

    Article  PubMed  Google Scholar 

  44. Yoganathan, A. Cardiac valve prostheses. In: The Biomedical Engineering Handbook. Boca Raton: CRC Press, 1995.

Download references

Acknowledgments

This work is supported by a Coulter Translational Research Award (CTRA) by the Wallace H. Coulter Foundation that was provided to Dr. Kheradvar. This research was also made possible in part through access to the Laser Microbeam and Medical Program (LAMMP), an NIH/NIBIB Biomedical Technology Center, P41EB05890.

Author information

Authors and Affiliations

  1. The Edwards Lifesciences Center for Advanced Cardiovascular Technology, Department of Biomedical Engineering, University of California, Irvine, Irvine, CA, 92697, USA

    S. Hamed Alavi, Elliot L. Botvinick & Arash Kheradvar

  2. Department of Mechanical and Aerospace Engineering, University of California, San Diego, San Diego, CA, USA

    Victor Ruiz

  3. Beckman Laser Institute, University of California, Irvine, Irvine, CA, USA

    Tatiana Krasieva & Elliot L. Botvinick

Authors
  1. S. Hamed Alavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Victor Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiana Krasieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elliot L. Botvinick
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arash Kheradvar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arash Kheradvar.

Additional information

Associate Editor Jane Grande-Allen oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alavi, S.H., Ruiz, V., Krasieva, T. et al. Characterizing the Collagen Fiber Orientation in Pericardial Leaflets Under Mechanical Loading Conditions. Ann Biomed Eng 41, 547–561 (2013). https://doi.org/10.1007/s10439-012-0696-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-012-0696-z

Keywords

Search

Navigation