Skip to main content

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

  • Chapter
  • First Online:
Multi-scale Extracellular Matrix Mechanics and Mechanobiology

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.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Abrahams, M.: Mechanical behaviour of tendon in vitro; a preliminary report. Med. Biol. Engng. 5, 433–443 (1967)

    Article  Google Scholar 

  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.12027

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2011.05.009

    Article  Google Scholar 

  6. Morin, C., Krasny, W., Avril, S.: Multiscale mechanical behavior of large arteries. Encycl. Biomed. Eng. (2017) (Elsevier)

    Google Scholar 

  7. O’Rourke, M.: Mechanical principles in arterial disease. Hypertension 26, 2–9 (1995). https://doi.org/10.1161/01.HYP.26.1.2

    Article  Google Scholar 

  8. Brodsky, B., Eikenberry, E.F.: Characterization of fibrous forms of collagen. Methods Enzymol. 82, 127–174 (1982)

    Article  Google Scholar 

  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)70059-1

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2016.0620

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.5.1.19

    Article  Google Scholar 

  16. Ratz, P.H.: Mechanics of vascular smooth muscle. Compr. Physiol. (2014)

    Google Scholar 

  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.2011.11.021

    Article  Google Scholar 

  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)90409-6

    Article  Google Scholar 

  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-z

    Article  Google Scholar 

  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.2012.06.007

    Article  Google Scholar 

  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.2014.05.014

    Article  Google Scholar 

  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.2011.10.043

    Article  Google Scholar 

  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.00601.2013

    Article  Google Scholar 

  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.2011.11.016

    Article  Google Scholar 

  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/10.1114/1.1527047

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2012.11.015

    Article  Google Scholar 

  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.2013.08.001

    Article  Google Scholar 

  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/s41467-017-00801-3

    Article  Google Scholar 

  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-X

    Article  Google Scholar 

  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/JCI19028

    Article  Google Scholar 

  32. Humphrey, J.D.: Mechanisms of arterial remodeling in hypertension. Hypertension 52, 195–200 (2008)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2016.01.030

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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/s10439-006-9226-1

    Article  Google Scholar 

  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.14.5.400

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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. 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.200910024

    Article  Google Scholar 

  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. 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.0832308100

    Article  Google Scholar 

  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.104.047308

    Article  Google Scholar 

  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.104.042887

    Article  Google Scholar 

  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.2014.01.027

    Article  Google Scholar 

  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.Second

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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/BF00620308

    Article  Google Scholar 

  49. Semwogerere, D., Weeks, E.R.: Confocal microscopy. Encycl. Biomater. Biomed. Eng. 1–10 (2005). https://doi.org/10.1081/e-ebbe-120024153

  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.172368799

    Article  Google Scholar 

  51. Denk, W., Strickler, J., Webb, W.W.: Two-photon laser scanning fluorescence microscopy. Science (80) 248, 73–76 (1990)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2011.11.013

    Article  Google Scholar 

  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.2012.03.068

    Article  Google Scholar 

  55. Morin, C., Avril, S.: Inverse problems in the mechanical characterization of elastic arteries. MRS Bull. 40 (2015). https://doi.org/10.1557/mrs.2015.63

    Article  Google Scholar 

  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-y

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2010.04.007

    Article  Google Scholar 

  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.15-17129

    Article  Google Scholar 

  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/s12958-016-0204-7

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.7.003089

    Article  Google Scholar 

  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/jemt

    Article  Google Scholar 

  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/10.1117/1.3210768

    Article  Google Scholar 

  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)90003-7

    Article  Google Scholar 

  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.2017.08.014

    Article  Google Scholar 

  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.2017.04.033

    Article  Google Scholar 

  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.2017.07.022

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  70. Humphrey, J.D.D.: Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. Springer, New-York (2002)

    Book  Google Scholar 

  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/10.1115/1.4004495

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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/s12573-011-0027-2

    Article  Google Scholar 

  75. Jähne, B.: Spatio-Temporal Image Processing: Theory and Scientific Applications. Springer Science & Business Media (1993)

    Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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.2013.04.028

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  86. Morin, C., Krasny, W., Avril, S.: Multiscale mechanical behavior of large arteries. Encycl. Biomed. Eng. 2. Elsevier (2019)

    Google Scholar 

  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/s10439-012-0679-0

    Article  Google Scholar 

  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.2012.04.035

    Article  Google Scholar 

  89. Pourdeyhimi, B.: Imaging and Image Analysis Applications for Plastics. William Andrew (1999)

    Google Scholar 

  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.2012.10.012

    Article  Google Scholar 

  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.2012.1004

    Article  Google Scholar 

  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)05947-3

    Article  Google Scholar 

  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)90096-9

    Article  Google Scholar 

  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.12.9.1008

    Article  Google Scholar 

  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. 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.2016.06.028

    Article  Google Scholar 

  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/s10237-018-1073-0

    Article  Google Scholar 

  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.2005.05.003

    Article  Google Scholar 

  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/s10237-016-0851-9

    Article  Google Scholar 

  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.201700360

    Article  MathSciNet  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stéphane Avril .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Cavinato, C., Badel, P., Krasny, W., Avril, S., Morin, C. (2020). Experimental Characterization of Adventitial Collagen Fiber Kinematics Using Second-Harmonic Generation Imaging Microscopy: Similarities and Differences Across Arteries, Species and Testing Conditions. In: Zhang, Y. (eds) Multi-scale Extracellular Matrix Mechanics and Mechanobiology. Studies in Mechanobiology, Tissue Engineering and Biomaterials, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-030-20182-1_5

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-20182-1_5

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-20181-4

  • Online ISBN: 978-3-030-20182-1

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics