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Biomechanics and Modeling in Mechanobiology

, Volume 17, Issue 2, pp 577–587 | Cite as

Local distribution of collagen fibers determines crack initiation site and its propagation direction during aortic rupture

  • Shukei SugitaEmail author
  • Takeo Matsumoto
Original Paper

Abstract

Although elucidation of the mechanism of aortic aneurysm rupture is important, the characteristics of crack initiation and propagation sites remain unknown. To determine the microscopic properties of these sites, the characteristics of local strains and constituents at crack initiation and propagation sites were investigated during biaxial stretching of porcine thoracic aortas (PTAs). PTAs were sliced into approximately 50-\(\upmu \hbox {m}\)-thick sections, and the center of the sections was made especially thin using our previously developed technique. Alpha-elastin and cell nuclei were fluorescently labeled as indices of local elastin density and as a strain marker, respectively. Birefringence and second harmonic generation (SHG) light images were used to determine local collagen distributions. The specimens were then stretched biaxially with a laboratory-made tensile tester under a fluorescent microscope equipped with a birefringence imaging system. Local strains were calculated from the local displacement of the cell nuclei. The degree of alignment and density of local collagen fibers were measured from retardance and SHG images. The strain distributions, specifically the first and second principal, and maximum shear strains, fluorescent intensity of \(\upalpha \)-elastin, and degree of alignment of collagen fibers, showed insignificant differences between the crack initiation sites and other sites. The retardance and intensity of SHG light at the crack initiation sites were significantly lower than those at other sites for all (\(n = 6\)) specimens. Cracks tended to propagate along the local direction of the collagen fibers. These results indicate that the local density and direction of collagen fibers play an important role in aorta rupture.

Keywords

Thoracic aorta Biaxial stretch rupture Local composition Second harmonic imaging microscopy Birefringence imaging microscopy 

Notes

Acknowledgements

This work was supported in part by Japan Society for the Promotion of Science KAKENHI (Nos. 26709002 and 15H02209) and AMED-CREST from Japan Agency for Medical Research and development, AMED (16gm0810005h0102). The authors acknowledge Dr. K. Nagayama for their help and discussion during experiments.

Compliance with ethical standards

Conflict of interest

There are no conflicts of interest.

Supplementary material

10237_2017_979_MOESM1_ESM.docx (14.4 mb)
Supplementary material 1 (docx 14777 KB)

References

  1. Cambria RA, Gloviczki P, Stanson AW, Cherry KJ Jr, Bower TC, Hallett JW Jr, Pairolero PC (1995) Outcome and expansion rate of 57 thoracoabdominal aortic aneurysms managed nonoperatively. Am J Surg 170:213–217.  https://doi.org/10.1016/S0002-9610(99)80289-X CrossRefGoogle Scholar
  2. Coady MA, Rizzo JA, Hammond GL, Mandapati D, Darr U, Kopf GS, Elefteriades JA (1997) What is the appropriate size criterion for resection of thoracic aortic aneurysms? J Thorac Cardiovasc Surg 113:476–491.  https://doi.org/10.1016/S0022-5223(97)70360-X CrossRefGoogle Scholar
  3. Davis FM, Luo Y, Avril S, Duprey A, Lu J (2016) Local mechanical properties of human ascending thoracic aneurysms. J Mech Behav Biomed Mater 61:235–249.  https://doi.org/10.1016/j.jmbbm.2016.03.025 CrossRefGoogle Scholar
  4. Fung YC (1981) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  5. Garcia-Herrera CM, Atienza JM, Rojo FJ, Claes E, Guinea GV, Celentano DJ, Garcia-Montero C, Burgos RL (2012) Mechanical behaviour and rupture of normal and pathological human ascending aortic wall. Med Biol Eng Comput 50:559–566.  https://doi.org/10.1007/s11517-012-0876-x CrossRefGoogle Scholar
  6. Gasser TC, Ogden RW, Holzapfel GA (2006) Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface 3:15–35.  https://doi.org/10.1098/rsif.2005.0073 CrossRefGoogle Scholar
  7. Goh KL, Chen Y, Chou SM, Listrat A, Bechet D, Wess TJ (2010) Effects of frozen storage temperature on the elasticity of tendons from a small murine model. Animal 4:1613–1617.  https://doi.org/10.1017/S1751731110000698 CrossRefGoogle Scholar
  8. He CM, Roach MR (1994) The composition and mechanical properties of abdominal aortic aneurysms. J Vasc Surg 20:6–13.  https://doi.org/10.1016/0741-5214(94)90169-4 CrossRefGoogle Scholar
  9. Iliopoulos DC, Kritharis EP, Giagini AT, Papadodima SA, Sokolis DP (2009) Ascending thoracic aortic aneurysms are associated with compositional remodeling and vessel stiffening but not weakening in age-matched subjects. J Thorac Cardiovasc Surg 137:101–109.  https://doi.org/10.1016/j.jtcvs.2008.07.023 CrossRefGoogle Scholar
  10. Masson I, Fialaire-Legendre A, Godin C, Boutouyrie P, Bierling P, Zidi M (2009) Mechanical properties of arteries cryopreserved at -80 degrees C and -150 degrees C. Med Eng Phys 31:825–832.  https://doi.org/10.1016/j.medengphy.2009.03.009 CrossRefGoogle Scholar
  11. Ohashi T, Sugita S, Matsumoto T, Kumagai K, Akimoto H, Tabayashi K, Sato M (2003) Rupture properties of blood vessel walls measured by pressure-imposed test. JSME Int J Ser C 46:1290–1296.  https://doi.org/10.1299/jsmec.46.1290 CrossRefGoogle Scholar
  12. Oldenbourg R (1996) A new view on polarization microscopy. Nature 381:811–812.  https://doi.org/10.1038/381811a0 CrossRefGoogle Scholar
  13. Petroll WM, Cavanagh HD, Barry P, Andrews P, Jester JV (1993) Quantitative analysis of stress fiber orientation during corneal wound contraction. J Cell Sci 104:353–363Google Scholar
  14. Raghavan ML, Webster MW, Vorp DA (1996) Ex vivo biomechanical behavior of abdominal aortic aneurysm: assessment using a new mathematical model. Ann Biomed Eng 24:573–582CrossRefGoogle Scholar
  15. Raghavan ML, Kratzberg J, de Tolosa EMC, Hanaoka MM, Walker P, da Silva ES (2006) Regional distribution of wall thickness and failure properties of human abdominal aortic aneurysm. J Biomech 39:3010–3016.  https://doi.org/10.1016/j.jbiomech.2005.10.021 CrossRefGoogle Scholar
  16. Raghavan ML, Hanaoka MM, Kratzberg JA, de Lourdes Higuchi M, da Silva ES (2011) Biomechanical failure properties and microstructural content of ruptured and unruptured abdominal aortic aneurysms. J Biomech 44:2501–2507.  https://doi.org/10.1016/j.jbiomech.2011.06.004 CrossRefGoogle Scholar
  17. Sassani SG, Tsangaris S, Sokolis DP (2015) Layer- and region-specific material characterization of ascending thoracic aortic aneurysms by microstructure-based models. J Biomech 48:3757–3765.  https://doi.org/10.1016/j.jbiomech.2015.08.028 CrossRefGoogle Scholar
  18. Schriefl AJ, Zeindlinger G, Pierce DM, Regitnig P, Holzapfel GA (2011) Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries. J R Soc Interface 9:1275–1286.  https://doi.org/10.1098/rsif.2011.0727 CrossRefGoogle Scholar
  19. Sokolis DP, Kritharis EP, Giagini AT, Lampropoulos KM, Papadodima SA, Iliopoulos DC (2012) Biomechanical response of ascending thoracic aortic aneurysms: association with structural remodelling. Comput Methods Biomech Biomed Eng 15:231–248.  https://doi.org/10.1080/10255842.2010.522186
  20. Stemper BD, Yoganandan N, Stineman MR, Gennarelli TA, Baisden JL, Pintar FA (2007) Mechanics of fresh, refrigerated, and frozen arterial tissue. J Surg Res 139:236–242.  https://doi.org/10.1016/j.jss.2006.09.001 CrossRefGoogle Scholar
  21. Sugita S, Matsumoto T (2013a) Heterogeneity of deformation of aortic wall at the microscopic level: contribution of heterogeneous distribution of collagen fibers in the wall. Bio Med Mater Eng 23:447–461.  https://doi.org/10.3233/BME-130771 Google Scholar
  22. Sugita S, Matsumoto T (2013b) Novel biaxial tensile test for studying aortic failure phenomena at a microscopic level. Biomed Eng OnLine 12:3.  https://doi.org/10.1186/1475-925x-12-3 CrossRefGoogle Scholar
  23. Sugita S, Matsumoto T (2013c) Quantitative measurement of the distribution and alignment of collagen fibers in unfixed aortic tissues. J Biomech 46:1403–1407.  https://doi.org/10.1016/j.jbiomech.2013.02.003
  24. Sugita S, Matsumoto T (2017) Multiphoton microscopy observations of 3D elastin and collagen fiber microstructure changes during pressurization in aortic media. Biomech Model Mechanobiol 16:763–773.  https://doi.org/10.1007/s10237-016-0851-9 CrossRefGoogle Scholar
  25. Sugita S, Matsumoto T, Ohashi T, Kumagai K, Akimoto H, Tabayashi K, Sato M (2011) Evaluation of rupture properties of thoracic aortic aneurysms in a pressure-imposed test for rupture risk estimation. Cardiovasc Eng Technol 3:41–51.  https://doi.org/10.1007/s13239-011-0067-1 CrossRefGoogle Scholar
  26. Venkatasubramanian RT, Grassl ED, Barocas VH, Lafontaine D, Bischof JC (2006) Effects of freezing and cryopreservation on the mechanical properties of arteries. Ann Biomed Eng 34:823–832.  https://doi.org/10.1007/s10439-005-9044-x CrossRefGoogle Scholar
  27. Wan C, Hao Z, Wen S, Leng H (2014) A quantitative study of the relationship between the distribution of different types of collagen and the mechanical behavior of rabbit medial collateral ligaments. PLoS ONE 9:e103363.  https://doi.org/10.1371/journal.pone.0103363 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Biomechanics Laboratory, Department of Mechanical Engineering, Graduate School of EngineeringNagoya Institute of TechnologyNagoyaJapan
  2. 2.Department of Mechanical Systems Engineering, Graduate School of EngineeringNagoya UniversityNagoyaJapan

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