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Experimental Characterization of Adventitial Collagen Fiber Kinematics Using Second-Harmonic Generation Imaging Microscopy: Similarities and Differences Across Arteries, Species and Testing Conditions

  • Cristina Cavinato
  • Pierre Badel
  • Witold Krasny
  • Stéphane AvrilEmail author
  • Claire Morin
Chapter
Part of the Studies in Mechanobiology, Tissue Engineering and Biomaterials book series (SMTEB, volume 23)

Abstract

Fibrous collagen networks are well known to play a central role in the passive biomechanical response of soft connective tissues to applied loads. In the current chapter we focus on vascular tissues and share our extensive experience in coupling mechanical loading and multi-photon imaging to investigate, across arteries, species and testing conditions, how collagen fibers move in response to mechanical loading. More specifically, we assess the deformations of collagen networks in rabbit, porcine or human arteries under different loading scenarios: uniaxial tension on flat samples, tension-inflation on tubular samples, bulge inflation on flat samples. We always observe that collagen fibers exhibit a wavy or crimped shape in load-free conditions, and tend to uncrimp when loads are applied, engaging sequentially to become the main load-bearing component. This sequential engagement, which is responsible for the nonlinear mechanical behaviour, is essential for an artery to function normally and appears to be less pronounced for arteries in elderly and aneurysmal patients. Although uncrimping of collagen fibers is a universal mechanism, we also observe large fiber rotations specific to tensile loading, with significant realignment along the loading axis. A unified approach is proposed to compare observations and quantitative analyses as the type of image processing may affect significantly the estimation of collagen fiber deformations. In summary, this chapter makes an important review of the basic roles of arterial microstructure and its deformations on the global mechanical response. Eventually, directions for future studies combining mechanical loading and multi-photon imaging are suggested, with the aim of addressing open questions related to tissue adaptation and rupture.

Keywords

Collagen fibers Artery Adventitia Extracellular matrix Uncrimping Biomechanics Multiphoton microscopy Second-harmonic generation Non-affine kinematics Aneurysm 

Notes

Acknowledgements

This research was supported by the European Research Council, Starting Grant No. 638804, AArteMIS, as well as by the ARC 2 “Bien-être et vieillissement” research program of the Auvergne-Rhône-Alpes region (FR). The authors thank Dr. Hélène Magoariec (Ecole Centrale Lyon, Université de Lyon, FR), Prof. Eric Viguier (VetAgro Sup, Université de Lyon, FR), Dr. Caroline Boulocher (VetAgro Sup, Université de Lyon, FR) and Mr. Fabrice Desplanches (Centre Lago, Vonnas, FR) for their help in the experimental studies on rabbit samples, as well as Dr. Ambroise Duprey for his help in provision of human arterial specimen. Authors also thank the IVTV (ANR-10-EQPX-06-01) team and the Hubert Curien laboratory (University Jean Monnet, Saint-Etienne, France) for their support during the imaging process.

References

  1. 1.
    Abrahams, M.: Mechanical behaviour of tendon in vitro; a preliminary report. Med. Biol. Engng. 5, 433–443 (1967)CrossRefGoogle Scholar
  2. 2.
    Thorpe, C.T., Birch, H.L., Clegg, P.D., Screen, H.R.C.: The role of the non-collagenous matrix in tendon function. Int. J. Exp. Pathol. 94, 248–259 (2013).  https://doi.org/10.1111/iep.12027CrossRefGoogle Scholar
  3. 3.
    Wells, S.M., Langille, B.L., Lee, J.M., Adamson, S.L.: Determinants of mechanical properties in the developing avine thoracic aorta. Am. J. Physiol. Heart Circ. Physiol. 277, H1385–H1391 (1999)CrossRefGoogle Scholar
  4. 4.
    Lynch, B., Bancelin, S., Bonod-Bidaud, C., Gueusquin, J.-B., Ruggiero, F., Schanne-Klein, M.-C., Allain, J.-M.: A novel microstructural interpretation for the biomechanics of mouse skin derived from multiscale characterization. Acta Biomater. 50, 302–311 (2017)CrossRefGoogle Scholar
  5. 5.
    Goulam Houssen, Y., Gusachenko, I., Schanne-Klein, M.-C., Allain, J.-M.: Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy. J. Biomech. 44, 2047–2052 (2011).  https://doi.org/10.1016/j.jbiomech.2011.05.009CrossRefGoogle Scholar
  6. 6.
    Morin, C., Krasny, W., Avril, S.: Multiscale mechanical behavior of large arteries. Encycl. Biomed. Eng. (2017) (Elsevier)Google Scholar
  7. 7.
    O’Rourke, M.: Mechanical principles in arterial disease. Hypertension 26, 2–9 (1995).  https://doi.org/10.1161/01.HYP.26.1.2CrossRefGoogle Scholar
  8. 8.
    Brodsky, B., Eikenberry, E.F.: Characterization of fibrous forms of collagen. Methods Enzymol. 82, 127–174 (1982)CrossRefGoogle Scholar
  9. 9.
    Akhtar, R., Sherratt, M.J., Cruickshank, J.K., Derby, B.: Characterizing the elastic properties of tissues. Mater. Today 14, 96–105 (2011).  https://doi.org/10.1016/S1369-7021(11)70059-1CrossRefGoogle Scholar
  10. 10.
    Wagenseil, J.E., Mecham, R.P.: Vascular extracellular matrix and arterial mechanics. Physiol. Rev. 89, 957–989 (2010).  https://doi.org/10.1152/physrev.00041.2008.CrossRefGoogle Scholar
  11. 11.
    Gasser, T.C., Gallinetti, S., Xing, X., Forsell, C., Swedenborg, J., Roy, J.: Spatial orientation of collagen fibers in the abdominal aortic aneurysm’s wall and its relation to wall mechanics. Acta Biomater. 8, 3091–3103 (2012)CrossRefGoogle Scholar
  12. 12.
    Niestrawska, J.A., Viertler, C., Regitnig, P., Cohnert, T.U., Sommer, G., Holzapfel, G.A.: Microstructure and mechanics of healthy and aneurysmatic abdominal aortas: experimental analysis and modelling. J. R. Soc. Interface. 13 (2016).  https://doi.org/10.1098/rsif.2016.0620CrossRefGoogle Scholar
  13. 13.
    O’Connell, M.K., Murthy, S., Phan, S., Xu, C., Buchanan, J., Spilker, R., Dalman, R.L., Zarins, C.K., Denk, W., Taylor, C.A.: The three-dimensional micro- and nanostructure of the aortic medial lamellar unit measured using 3D confocal and electron microscopy imaging. Matrix Biol. 27, 171–181 (2008)CrossRefGoogle Scholar
  14. 14.
    Dingemans, K.P., Teeling, P., Lagendijk, J.H., Becker, A.E.: Extracellular matrix of the human aortic media: an ultrastructural histochemical and immunohistochemical study of the adult aortic media. Anat. Rec. 258, 1–14 (2000)CrossRefGoogle Scholar
  15. 15.
    Clark, J.M., Glagov, S.: Transmural organization of the arterial media. The lamellar unit revisited. Arterioscler. Thromb. Vasc. Biol. 5, 19–34 (1985).  https://doi.org/10.1161/01.atv.5.1.19CrossRefGoogle Scholar
  16. 16.
    Ratz, P.H.: Mechanics of vascular smooth muscle. Compr. Physiol. (2014)Google Scholar
  17. 17.
    Humphrey, J.D., Holzapfel, G.A.: Mechanics, mechanobiology, and modeling of human abdominal aorta and aneurysms. J. Biomech. 45, 805–814 (2012).  https://doi.org/10.1016/j.jbiomech.2011.11.021CrossRefGoogle Scholar
  18. 18.
    Rizzo, R.J., McCarthy, W.J., Dixit, S.N., Lilly, M.P., Shively, V.P., Flinn, W.R., Yao, J.S.T.: Collagen types and matrix protein content in human abdominal aortic aneurysms. J. Vasc. Surg. 10, 365–373 (1989).  https://doi.org/10.1016/0741-5214(89)90409-6CrossRefGoogle Scholar
  19. 19.
    Rezakhaniha, R., Agianniotis, A., Schrauwen, J.T.C., Griffa, A., Sage, D., Bouten, C.V.C., Van De Vosse, F.N., Unser, M., Stergiopulos, N.: Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech. Model. Mechanobiol. 11, 461–473 (2012).  https://doi.org/10.1007/s10237-011-0325-zCrossRefGoogle Scholar
  20. 20.
    Schrauwen, J.T.C., Vilanova, A., Rezakhaniha, R., Stergiopulos, N., van de Vosse, F.N., Bovendeerd, P.H.M.: A method for the quantification of the pressure dependent 3D collagen configuration in the arterial adventitia. J. Struct. Biol. 180, 335–342 (2012).  https://doi.org/10.1016/j.jsb.2012.06.007CrossRefGoogle Scholar
  21. 21.
    Chow, M.-J., Turcotte, R., Lin, C.P., Zhang, Y.: Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen. Biophys. J. 106, 2684–2692 (2014).  https://doi.org/10.1016/j.bpj.2014.05.014CrossRefGoogle Scholar
  22. 22.
    Chen, H., Liu, Y., Slipchenko, M.N., Zhao, X., Cheng, J.-X.X., Kassab, G.S.: The layered structure of coronary adventitia under mechanical load. Biophys. J. 101, 2555–2562 (2011).  https://doi.org/10.1016/j.bpj.2011.10.043CrossRefGoogle Scholar
  23. 23.
    Chen, H., Slipchenko, M.N., Liu, Y., Zhao, X., Cheng, J.-X., Lanir, Y., Kassab, G.S.: Biaxial deformation of collagen and elastin fibers in coronary adventitia. J. Appl. Physiol. 115, 1683–1693 (2013).  https://doi.org/10.1152/japplphysiol.00601.2013CrossRefGoogle Scholar
  24. 24.
    Hill, M.R., Duan, X., Gibson, G.A., Watkins, S., Robertson, A.M.: A theoretical and non-destructive experimental approach for direct inclusion of measured collagen orientation and recruitment into mechanical models of the artery wall. J. Biomech. 45, 762–771 (2012).  https://doi.org/10.1016/j.jbiomech.2011.11.016CrossRefGoogle Scholar
  25. 25.
    Tower, T.T., Neidert, M.R., Tranquillo, R.T.: Fiber alignment imaging during mechanical testing of soft tissues. Ann. Biomed. Eng. 30, 1221–1233 (2002).  https://doi.org/10.1114/1.1527047CrossRefGoogle Scholar
  26. 26.
    Sutton, M.A., Ke, X., Lessner, S.M., Goldbach, M., Yost, M., Zhao, F., Schreier, H.W.: Strain field measurements on mouse carotid arteries using microscopic three-dimensional digital image correlation. J. Biomed. Mater. Res., Part A 84, 178–190 (2008)CrossRefGoogle Scholar
  27. 27.
    Genovese, K., Lee, Y.-U., Lee, A.Y., Humphrey, J.D.: An improved panoramic digital image correlation method for vascular strain analysis and material characterization. J. Mech. Behav. Biomed. Mater. 27, 132–142 (2013).  https://doi.org/10.1016/j.jmbbm.2012.11.015CrossRefGoogle Scholar
  28. 28.
    Wang, R., Brewster, L.P., Gleason Jr., R.L.: In-situ characterization of the uncrimping process of arterial collagen fibers using two-photon confocal microscopy and digital image correlation. J. Biomech. 46, 2726–2729 (2013).  https://doi.org/10.1016/j.jbiomech.2013.08.001CrossRefGoogle Scholar
  29. 29.
    Ehret, A.E., Bircher, K., Stracuzzi, A., Marina, V., Zündel, M., Mazza, E.: Inverse poroelasticity as a fundamental mechanism in biomechanics and mechanobiology. Nat. Commun. 8, 1002 (2017).  https://doi.org/10.1038/s41467-017-00801-3CrossRefGoogle Scholar
  30. 30.
    Faury, G.: Function–structure relationship of elastic arteries in evolution: from microfibrils to elastin and elastic fibres. Pathol. Biol. 49, 310–325 (2001).  https://doi.org/10.1016/S0369-8114(01)00147-XCrossRefGoogle Scholar
  31. 31.
    Faury, G., Pezet, M., Knutsen, R.H., Boyle, W.A., Heximer, S.P., McLean, S.E., Minkes, R.K., Blumer, K.J., Kovacs, A., Kelly, D.P., Li, D.Y., Starcher, B., Mecham, R.P.: Developmental adaptation of the mouse cardiovascular system to elastin haploinsufficiency. J. Clin. Invest. 112, 1419–1428 (2003).  https://doi.org/10.1172/JCI19028CrossRefGoogle Scholar
  32. 32.
    Humphrey, J.D.: Mechanisms of arterial remodeling in hypertension. Hypertension 52, 195–200 (2008)CrossRefGoogle Scholar
  33. 33.
    Canham, P.B., Finlay, H.M., Dixon, J.A.N.G., Boughner, D.R., Chen, A.: Measurements from light and polarised light microscopy of human coronary arteries fixed at distending pressure. Cardiovasc. Res. 23, 973–982 (1989)CrossRefGoogle Scholar
  34. 34.
    Sáez, P., García, A., Peña, E., Gasser, T.C., Martínez, M.A.: Microstructural quantification of collagen fiber orientations and its integration in constitutive modeling of the porcine carotid artery. Acta Biomater. 33, 183–193 (2016).  https://doi.org/10.1016/j.actbio.2016.01.030CrossRefGoogle Scholar
  35. 35.
    Schriefl, A.J., Reinisch, A.J., Sankaran, S., Pierce, D.M., Holzapfel, G.A.: Quantitative assessment of collagen fibre orientations from two-dimensional images of soft biological tissues. J. R. Soc. Interface. 9, 3081–3093 (2012)CrossRefGoogle Scholar
  36. 36.
    Dahl, S.L.M., Rhim, C., Song, Y.C., Niklason, L.E.: Mechanical properties and compositions of tissue engineered and native arteries. Ann. Biomed. Eng. 35, 348–355 (2007).  https://doi.org/10.1007/s10439-006-9226-1CrossRefGoogle Scholar
  37. 37.
    Wolinsky, H., Glagov, S.: Structural basis for the static mechanical properties of the aortic media. Circ. Res. 14, 400–413 (1964).  https://doi.org/10.1161/01.RES.14.5.400CrossRefGoogle Scholar
  38. 38.
    Fujimoto, J.G., Boppart, S.A., Tearney, G.J., Bouma, B.E., Pitris, C., Brezinski, M.E.: High resolution in vivo intra-arterial imaging with optical coherence tomography. Heart 82, 128–133 (1999)CrossRefGoogle Scholar
  39. 39.
    Acosta, V., Flechas Garcia, M., Molimard, J., Avril, S.: Three-dimensional full-field strain measurements across a whole porcine aorta subjected to tensile loading using optical coherence tomography–digital volume correlation. Front. Mech. Eng. (2018). https://doi.org/10.3389/fmech.2018.00003
  40. 40.
    Campagnola, P.J., Dong, C.Y.: Second harmonic generation microscopy: principles and applications to disease diagnosis. Laser Photonics Rev. 5, 13–26 (2011).  https://doi.org/10.1002/lpor.200910024CrossRefGoogle Scholar
  41. 41.
    Rouède, D., Schaub, E., Bellanger, J.J., Ezan, F., Scimeca, J.C., Baffet, G., Tiaho, F.: Determination of extracellular matrix collagen fibril architectures and pathological remodeling by polarization dependent second harmonic microscopy. Sci. Rep. 7 (2017).  https://doi.org/10.1038/s41598-017-12398-0
  42. 42.
    Zipfel, W.R., Williams, R.M., Christie, R., Nikitin, A.Y., Hyman, B.T., Webb, W.W.: Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. 100, 7075–7080 (2003).  https://doi.org/10.1073/pnas.0832308100CrossRefGoogle Scholar
  43. 43.
    Williams, R.M., Zipfel, W.R., Webb, W.W.: Interpreting second-harmonic generation images of collagen I fibrils. Biophys. J. 88, 1377–1386 (2005).  https://doi.org/10.1529/biophysj.104.047308CrossRefGoogle Scholar
  44. 44.
    Zoumi, A., Lu, X., Kassab, G.S., Tromberg, B.J.: Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. Biophys. J. 87, 2778–2786 (2004).  https://doi.org/10.1529/biophysj.104.042887CrossRefGoogle Scholar
  45. 45.
    Koch, R.G., Tsamis, A., D’Amore, A., Wagner, W.R., Watkins, S.C., Gleason, T.G., Vorp, D.A.: A custom image-based analysis tool for quantifying elastin and collagen micro-architecture in the wall of the human aorta from multi-photon microscopy. J. Biomech. 47, 935–943 (2014).  https://doi.org/10.1016/j.jbiomech.2014.01.027CrossRefGoogle Scholar
  46. 46.
    Chen, X., Nadiarynkh, O., Plotnikov, S., Campagnola, P.J.: Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat. Protoc. 7, 654–669 (2015).  https://doi.org/10.1038/nprot.2012.009.SecondCrossRefGoogle Scholar
  47. 47.
    Freund, I., Deutsch, M., Sprecher, A.: Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon. Biophys. J. 50, 693–712 (1986)CrossRefGoogle Scholar
  48. 48.
    Gannaway, J.N., Sheppard, C.J.R.: Second-harmonic imaging in the scanning optical microscope. Opt. Quantum Electron. 10, 435–439 (1978).  https://doi.org/10.1007/BF00620308CrossRefGoogle Scholar
  49. 49.
    Semwogerere, D., Weeks, E.R.: Confocal microscopy. Encycl. Biomater. Biomed. Eng. 1–10 (2005).  https://doi.org/10.1081/e-ebbe-120024153
  50. 50.
    Zoumi, A., Yeh, A., Tromberg, B.J.: Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence. Proc. Natl. Acad. Sci. 99, 11014–11019 (2002).  https://doi.org/10.1073/pnas.172368799CrossRefGoogle Scholar
  51. 51.
    Denk, W., Strickler, J., Webb, W.W.: Two-photon laser scanning fluorescence microscopy. Science (80) 248, 73–76 (1990)CrossRefGoogle Scholar
  52. 52.
    Bancelin, S., Lynch, B., Bonod-Bidaud, C., Ducourthial, G., Psilodimitrakopoulos, S., Dokládal, P., Allain, J.-M., Schanne-Klein, M.-C., Ruggiero, F.: Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy. Sci. Rep. 5, 17635 (2015)CrossRefGoogle Scholar
  53. 53.
    Ambekar, R., Chittenden, M., Jasiuk, I., Toussaint, K.C.: Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes. Bone 50, 643–650 (2012).  https://doi.org/10.1016/j.bone.2011.11.013CrossRefGoogle Scholar
  54. 54.
    Gusachenko, I., Tran, V., Goulam Houssen, Y., Allain, J.-M., Schanne-Klein, M.-C.: Polarization-resolved second-harmonic generation in tendon upon mechanical stretching. Biophys. J. 102, 2220–2229 (2012).  https://doi.org/10.1016/j.bpj.2012.03.068CrossRefGoogle Scholar
  55. 55.
    Morin, C., Avril, S.: Inverse problems in the mechanical characterization of elastic arteries. MRS Bull. 40 (2015).  https://doi.org/10.1557/mrs.2015.63CrossRefGoogle Scholar
  56. 56.
    Zeinali-Davarani, S., Chow, M.-J., Turcotte, R., Zhang, Y.: Characterization of biaxial mechanical behavior of porcine aorta under gradual elastin degradation. Ann. Biomed. Eng. 41, 1528–1538 (2013).  https://doi.org/10.1007/s10439-012-0733-yCrossRefGoogle Scholar
  57. 57.
    Zeinali-Davarani, S., Wang, Y., Chow, M.-J., Turcotte, R., Zhang, Y.: Contribution of collagen fiber undulation to regional biomechanical properties along porcine thoracic aorta. J. Biomech. Eng. 137, 51001 (2015)CrossRefGoogle Scholar
  58. 58.
    Chow, M.-J., Zhang, Y.: Changes in the mechanical and biochemical properties of aortic tissue due to cold storage. J. Surg. Res. 171, 434–442 (2011).  https://doi.org/10.1016/j.jss.2010.04.007CrossRefGoogle Scholar
  59. 59.
    Park, C.Y., Lee, J.K., Chuck, R.S.: Second harmonic generation imaging analysis of collagen arrangement in human cornea. Investig. Ophthalmol. Vis. Sci. 56, 5622–5629 (2015).  https://doi.org/10.1167/iovs.15-17129CrossRefGoogle Scholar
  60. 60.
    Narice, B.F., Green, N.H., Macneil, S., Anumba, D.: Second Harmonic Generation microscopy reveals collagen fibres are more organised in the cervix of postmenopausal women. Reprod. Biol. Endocrinol. 14, 70–78 (2016).  https://doi.org/10.1186/s12958-016-0204-7CrossRefGoogle Scholar
  61. 61.
    Jayyosi, C., Coret, M., Bruyere-Garnier, K.: Characterizing liver capsule microstructure via in situ bulge test coupled with multiphoton imaging. J. Mech. Behav. Biomed. Mater. 54, 229–243 (2016)CrossRefGoogle Scholar
  62. 62.
    Olson, E., Levene, M.J., Torres, R.: Multiphoton microscopy with clearing for three dimensional histology of kidney biopsies. Biomed. Opt. Express. 7, 3089 (2016).  https://doi.org/10.1364/BOE.7.003089CrossRefGoogle Scholar
  63. 63.
    Pena, A.-M., Fabre, A., Débarre, D., Marchal-Somme, J., Crestani, B., Martin, J.-L., Beaurepaire, E., Schanne-Klein, M.-C.: Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy. Microsc. Res. Tech. 70, 162–170 (2007).  https://doi.org/10.1002/jemtCrossRefGoogle Scholar
  64. 64.
    Wang, C.-C., Li, F.-C., Wu, R.-J., Hovhannisyan, V.A., Lin, W.-C., Lin, S.-J., So, P.T.C., Dong, C.-Y.: Differentiation of normal and cancerous lung tissues by multiphoton imaging. J. Biomed. Opt. 14, 044034 (2009).  https://doi.org/10.1117/1.3210768CrossRefGoogle Scholar
  65. 65.
    Campa, J.S., Greenhalgh, R.M., Powell, J.T.: Elastin degradation in abdominal aortic aneurysms. Atherosclerosis 65, 13–21 (1987).  https://doi.org/10.1016/0021-9150(87)90003-7CrossRefGoogle Scholar
  66. 66.
    Krasny, W., Magoariec, H., Morin, C., Avril, S.: Kinematics of collagen fibers in carotid arteries under tension-inflation loading. J. Mech. Behav. Biomed. Mater. 77, 718–726 (2018).  https://doi.org/10.1016/j.jmbbm.2017.08.014CrossRefGoogle Scholar
  67. 67.
    Krasny, W., Morin, C., Magoariec, H., Avril, S.: A comprehensive study of layer-specific morphological changes in the microstructure of carotid arteries under uniaxial load. Acta Biomater. 57, 342–351 (2017).  https://doi.org/10.1016/j.actbio.2017.04.033CrossRefGoogle Scholar
  68. 68.
    Cavinato, C., Helfenstein-Didier, C., Olivier, T., du Roscoat, S.R., Laroche, N., Badel, P.: Biaxial loading of arterial tissues with 3D in situ observations of adventitia fibrous microstructure: a method coupling multi-photon confocal microscopy and bulge inflation test. J. Mech. Behav. Biomed. Mater. 74, 488–498 (2017).  https://doi.org/10.1016/j.jmbbm.2017.07.022CrossRefGoogle Scholar
  69. 69.
    Jayyosi, C., Affagard, J.-S., Ducourthial, G., Bonod-Bidaud, C., Lynch, B., Bancelin, S., Ruggiero, F., Schanne-Klein, M.-C., Allain, J.-M., Bruyère-Garnier, K., et al.: Affine kinematics in planar fibrous connective tissues: an experimental investigation. Biomech. Model. Mechanobiol. 16(4), 1459–1473 (2017)CrossRefGoogle Scholar
  70. 70.
    Humphrey, J.D.D.: Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. Springer, New-York (2002)CrossRefGoogle Scholar
  71. 71.
    Keyes, J.T., Haskett, D.G., Utzinger, U., Azhar, M., Vande Geest, J.P.: Adaptation of a planar microbiaxial optomechanical device for the tubular biaxial microstructural and macroscopic characterization of small vascular tissues. J. Biomech. Eng. 133, 075001 (2011).  https://doi.org/10.1115/1.4004495CrossRefGoogle Scholar
  72. 72.
    Länne, T., Sonesson, B., Bergqvist, D., Bengtsson, H., Gustafsson, D.: Diameter and compliance in the male human abdominal aorta: influence of age and aortic aneurysm. Eur. J. Vasc. Endovasc. Surg. 6, 178–184 (1992)CrossRefGoogle Scholar
  73. 73.
    Romo, A., Badel, P., Duprey, A., Favre, J.-P., Avril, S.: In vitro analysis of localized aneurysm rupture. J. Biomech. 47, 607–616 (2014)CrossRefGoogle Scholar
  74. 74.
    Roy, S., Boss, C., Rezakhaniha, R., Stergiopulos, N.: Experimental characterization of the distribution of collagen fiber recruitment. J. Biorheol. 24, 84–93 (2010).  https://doi.org/10.1007/s12573-011-0027-2CrossRefGoogle Scholar
  75. 75.
    Jähne, B.: Spatio-Temporal Image Processing: Theory and Scientific Applications. Springer Science & Business Media (1993)Google Scholar
  76. 76.
    Bigun, J., Bigun, T., Nilsson, K.: Recognition by symmetry derivatives and the generalized structure tensor. IEEE Trans. Pattern Anal. Mach. Intell. 26, 1590–1605 (2004)CrossRefGoogle Scholar
  77. 77.
    Ayres, C., Jha, B.S., Meredith, H., Bowman, J.R., Bowlin, G.L., Henderson, S.C., Simpson, D.G.: Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D Fast Fourier Transform approach. J. Biomater. Sci. Polym. Ed. 19, 603–621 (2008)CrossRefGoogle Scholar
  78. 78.
    Phillippi, J.A., Green, B.R., Eskay, M.A., Kotlarczyk, M.P., Hill, M.R., Robertson, A.M., Watkins, S.C., Vorp, D.A., Gleason, T.G.: Mechanism of aortic medial matrix remodeling is distinct in patients with bicuspid aortic valve. J. Thorac. Cardiovasc. Surg. 147, 1056–1064 (2014).  https://doi.org/10.1016/j.jtcvs.2013.04.028CrossRefGoogle Scholar
  79. 79.
    D’Amore, A., Stella, J.A., Wagner, W.R., Sacks, M.S., D’Amore, A., Stella, J.A., Wagner, W.R., Sacks, M.S.: Characterization of the complete fiber network topology of planar fibrous tissues and scaffolds. Biomaterials 31, 5345–5354 (2010)CrossRefGoogle Scholar
  80. 80.
    Tonar, Z., Nemecek, S., Holota, R., Kocova, J., Treska, V., Molacek, J., Kohoutek, T., Hadravska, S.: Microscopic image analysis of elastin network in samples of normal, atherosclerotic and aneurysmatic abdominal aorta and its biomechanical implications. J. Appl. Biomed. 1, 149–160 (2003)CrossRefGoogle Scholar
  81. 81.
    Schriefl, A.J., Wolinski, H., Regitnig, P., Kohlwein, S.D., Holzapfel, G.A.: An automated approach for three-dimensional quantification of fibrillar structures in optically cleared soft biological tissues. J. R. Soc. Interface. 10, 20120760 (2013)CrossRefGoogle Scholar
  82. 82.
    Polzer, S., Gasser, T.C., Forsell, C., Druckmüllerova, H., Tichy, M., Staffa, R., Vlachovsky, R., Bursa, J.: Automatic identification and validation of planar collagen organization in the aorta wall with application to abdominal aortic aneurysm. Microsc. Microanal. 19, 1395–1404 (2013)CrossRefGoogle Scholar
  83. 83.
    Ayres, C., Bowlin, G.L., Henderson, S.C., Taylor, L., Shultz, J., Alexander, J., Telemeco, T.A., Simpson, D.G.: Modulation of anisotropy in electrospun tissue-engineering scaffolds: analysis of fiber alignment by the fast Fourier transform. Biomaterials 27, 5524–5534 (2006)CrossRefGoogle Scholar
  84. 84.
    Morrill, E.E., Tulepbergenov, A.N., Stender, C.J., Lamichhane, R., Brown, R.J., Lujan, T.J.: A validated software application to measure fiber organization in soft tissue. Biomech. Model. Mechanobiol. 15, 1467–1478 (2016)CrossRefGoogle Scholar
  85. 85.
    Sander, E.A., Barocas, V.H.: Comparison of 2D fiber network orientation measurement methods. J. Biomed. Mater. Res. Part A. 88, 322–331 (2009)CrossRefGoogle Scholar
  86. 86.
    Morin, C., Krasny, W., Avril, S.: Multiscale mechanical behavior of large arteries. Encycl. Biomed. Eng. 2. Elsevier (2019)Google Scholar
  87. 87.
    Keyes, J.T., Lockwood, D.R., Utzinger, U., Montilla, L.G., Witte, R.S., Vande Vande Geest, J.P., Geest, J.P.: Comparisons of planar and tubular biaxial tensile testing protocols of the same porcine coronary arteries. Ann. Biomed. Eng. 41, 1579–1591 (2013).  https://doi.org/10.1007/s10439-012-0679-0CrossRefGoogle Scholar
  88. 88.
    Wan, W., Dixon, J.B., Gleason Jr., R.L.: Constitutive modeling of mouse carotid arteries using experimentally measured microstructural parameters. Biophys. J. 102, 2916–2925 (2012).  https://doi.org/10.1016/j.bpj.2012.04.035CrossRefGoogle Scholar
  89. 89.
    Pourdeyhimi, B.: Imaging and Image Analysis Applications for Plastics. William Andrew (1999)Google Scholar
  90. 90.
    Chen, Q., Pugno, N.M.: Bio-mimetic mechanisms of natural hierarchical materials: a review. J. Mech. Behav. Biomed. Mater. 19, 3–33 (2013).  https://doi.org/10.1016/j.jmbbm.2012.10.012CrossRefGoogle Scholar
  91. 91.
    Tsamis, A., Krawiec, J.T., Vorp, D.A.: Elastin and collagen fibre microstructure of the human aorta in ageing and disease: a review. J. R. Soc. Interface. 10 (2013).  https://doi.org/10.1098/rsif.2012.1004CrossRefGoogle Scholar
  92. 92.
    Brüel, A., Oxlund, H.: Changes in biomechanical properties, composition of collagen and elastin, and advanced glycation endproducts of the rat aorta in relation to age. Atherosclerosis 127, 155–165 (1996).  https://doi.org/10.1016/S0021-9150(96)05947-3CrossRefGoogle Scholar
  93. 93.
    Cox, R.H.: Age-related changes in arterial wall mechanics and composition of NIA Fischer rats. Mech. Ageing Dev. 23, 21–36 (1983).  https://doi.org/10.1016/0047-6374(83)90096-9CrossRefGoogle Scholar
  94. 94.
    Fornieri, C., Quaglino, D., Mori, G.: Role of the extracellular matrix in age-related modifications of the rat aorta. Ultrastructural, morphometric, and enzymatic evaluations. Arterioscler. Thromb. Vasc. Biol. 12, 1008–1016 (1992).  https://doi.org/10.1161/01.atv.12.9.1008CrossRefGoogle Scholar
  95. 95.
    Valenta, J., Vitek, K., Cihak, R., Konvickova, S., Sochor, M., Horny, L.: Age related constitutive laws and stress distribution in human main coronary arteries with reference to residual strain. Biomed. Mater. Eng. 12, 121–134 (2002)Google Scholar
  96. 96.
    Duprey, A., Trabelsi, O., Vola, M., Favre, J.P., Avril, S.: Biaxial rupture properties of ascending thoracic aortic aneurysms. Acta Biomater. 42, 273–285 (2016).  https://doi.org/10.1016/j.actbio.2016.06.028CrossRefGoogle Scholar
  97. 97.
    Farzaneh, S., Trabelsi, O., Avril, S.: Inverse identification of local stiffness across ascending thoracic aortic aneurysms. Biomech. Model. Mechanobiol. 18(1), 137–153 (2019).  https://doi.org/10.1007/s10237-018-1073-0CrossRefGoogle Scholar
  98. 98.
    Sokolis, D.P., Kefaloyannis, E.M., Kouloukoussa, M., Marinos, E., Boudoulas, H., Karayannacos, P.E.: A structural basis for the aortic stress-strain relation in uniaxial tension. J. Biomech. 39, 1651–1662 (2006).  https://doi.org/10.1016/j.jbiomech.2005.05.003CrossRefGoogle Scholar
  99. 99.
    Sugita, S., Matsumoto, T.: Multiphoton microscopy observations of 3D elastin and collagen fiber microstructure changes during pressurization in aortic media. Biomech. Model. Mechanobiol. 1–11 (2016).  https://doi.org/10.1007/s10237-016-0851-9CrossRefGoogle Scholar
  100. 100.
    Morin, C., Avril, S., Hellmich, C.: Non-affine fiber kinematics in arterial mechanics: a continuum micromechanical investigation. ZAMM - J. Appl. Math. Mech. / Zeitschrift für Angew. Math. und Mech. 1–21 (2018).  https://doi.org/10.1002/zamm.201700360MathSciNetCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Cristina Cavinato
    • 1
  • Pierre Badel
    • 1
  • Witold Krasny
    • 1
  • Stéphane Avril
    • 1
    Email author
  • Claire Morin
    • 1
  1. 1.Mines Saint-EtienneUniv Lyon, Univ Jean Monnet, INSERMSaint-EtienneFrance

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