Skip to main content
Log in

Affine kinematics in planar fibrous connective tissues: an experimental investigation

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

The affine transformation hypothesis is usually adopted in order to link the tissue scale with the fibers scale in structural constitutive models of fibrous tissues. Thanks to the recent advances in imaging techniques, such as multiphoton microscopy, the microstructural behavior and kinematics of fibrous tissues can now be monitored at different stretching within the same sample. Therefore, the validity of the affine hypothesis can be investigated. In this paper, the fiber reorientation predicted by the affine assumption is compared to experimental data obtained during mechanical tests on skin and liver capsule coupled with microstructural imaging using multiphoton microscopy. The values of local strains and the collagen fibers orientation measured at increasing loading levels are used to compute a theoretical estimation of the affine reorientation of collagen fibers. The experimentally measured reorientation of collagen fibers during loading could not be successfully reproduced with this simple affine model. It suggests that other phenomena occur in the stretching process of planar fibrous connective tissues, which should be included in structural constitutive modeling approaches.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Alavi SH, Sinha A, Steward E et al (2015) Load-dependent extracellular matrix organization in atrioventricular heart valves: differences and similarities. Am J Physiol Heart Circ Physiol 309:H276–84. doi:10.1152/ajpheart.00164.2015

    Article  Google Scholar 

  • Bancelin S, Lynch B, Bonod-Bidaud C et al (2015) Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy. Sci Rep 5:17635. doi:10.1038/srep17635

    Article  Google Scholar 

  • Benoit A, Latour G, Marie-Claire SK, Allain JM (2016) Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure. J Mech Behav Biomed Mater 60:93–105. doi:10.1016/j.jmbbm.2015.12.031

    Article  Google Scholar 

  • Billiar KL, Sacks MS (1997) A method to quantify the fiber kinematics of planar tissues under biaxial stretch. J Biomech 30:753–756. doi:10.1016/S0021-9290(97)00019-5

    Article  Google Scholar 

  • Butler DL, Goldstein Sa, Guilak F (2001) Functional tissue engineering: the role of biomechanics in articular cartilage repair. Clin Orthop Relat Res 122:S295–S305. doi:10.1115/1.1318906

    Google Scholar 

  • Chandran PL, Barocas VH (2005) Affine versus non-affine fibril kinematics in collagen networks: theoretical studies of network behavior. J Biomech Eng 128:259. doi:10.1115/1.2165699

    Article  Google Scholar 

  • Chauvet D, Carpentier A, Allain J-M et al (2010) Histological and biomechanical study of dura mater applied to the technique of dura splitting decompression in Chiari type I malformation. Neurosurg Rev 33:287–294. doi:10.1007/s10143-010-0261-x (discussion 295)

    Article  Google Scholar 

  • Deyl Z, Macek K, Adam M, Vancíková O (1980) Studies on the chemical nature of elastin fluorescence. Biochim Biophys Acta 625:248–54

    Article  Google Scholar 

  • Fan R, Sacks MS (2014) Simulation of planar soft tissues using a structural constitutive model: finite element implementation and validation. J Biomech 47:2043–2054. doi:10.1016/j.jbiomech.2014.03.014

    Article  Google Scholar 

  • Fung YC (1990) Biomechanics: motion, flow, stress, and growth. Springer, New York

    Book  MATH  Google Scholar 

  • Gasser TC (2011) An irreversible constitutive model for fibrous soft biological tissue: a 3-D microfiber approach with demonstrative application to abdominal aortic aneurysms. Acta Biomater 7:2457–66. doi:10.1016/j.actbio.2011.02.015

    Article  Google Scholar 

  • Gasser TC, Ogden RW, Ga Holzapfel (2006) Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface R Soc 3:15–35. doi:10.1098/rsif.2005.0073

    Article  Google Scholar 

  • Gelse K, Pöschl E, Aigner T (2003) Collagens—structure, function, and biosynthesis. Adv Drug Deliv Rev 55:1531–1546. doi:10.1016/j.addr.2003.08.002

    Article  Google Scholar 

  • Goulam Houssen Y, Gusachenko I, Schanne-Klein M-C, Allain J-M (2011) Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy. J Biomech 44:2047–2052. doi:10.1016/j.jbiomech.2011.05.009

    Article  Google Scholar 

  • Hannafin JA, Arnoczky SP (1994) Effect of cyclic and static tensile loading on water content and solute diffusion in canine flexor tendons: an in vitro study. J Orthop Res 12:350–6. doi:10.1002/jor.1100120307

    Article  Google Scholar 

  • Holzapfel GA, Stadler M, Schulze-Bauer CAJ (2002) A layer-specific three-dimensional model for the simulation of balloon angioplasty using magnetic resonance imaging and mechanical testing. Ann Biomed Eng 30:753–767. doi:10.1114/1.1492812

    Article  Google Scholar 

  • Humphrey JD (2003) Review paper: continuum biomechanics of soft biological tissues. Proc R Soc A Math Phys Eng Sci 459:3–46. doi:10.1098/rspa.2002.1060

    Article  MathSciNet  MATH  Google Scholar 

  • Jayyosi C (2015) Caractérisation mécanique et microstructurale du comportement à rupture de la capsule de Glisson pour la prédiction du risque de lésions des tissus hépatiques humains. Université Claude Bernard Lyon 1

  • Jayyosi C, Coret M, Bruyère-Garnier K (2016) Characterizing liver capsule microstructure via in situ bulge test coupled with multiphoton imaging. J Mech Behav Biomed Mater 54:229–243. doi:10.1016/j.jmbbm.2015.09.031

    Article  Google Scholar 

  • Jayyosi C, Fargier G, Coret M, Bruyère-Garnier K (2014) Photobleaching as a tool to measure the local strain field in fibrous membranes of connective tissues. Acta Biomater 10:2591–601. doi:10.1016/j.actbio.2014.02.031

    Article  Google Scholar 

  • Keyes JT, Lockwood DR, Simon BR, Vande Geest JP (2013) Deformationally dependent fluid transport properties of porcine coronary arteries based on location in the coronary vasculature. J Mech Behav Biomed Mater 17:296–306. doi:10.1016/j.jmbbm.2012.10.002

    Article  Google Scholar 

  • Lanir Y, Salant EL, Foux A (1988) Physico-chemical and microstructural changes in collagen fiber bundles following stretch in-vitro. Biorheology 25:591–603

    Google Scholar 

  • Loerakker S, Ristori T, Baaijens FPT (2016) A computational analysis of cell-mediated compaction and collagen remodeling in tissue-engineered heart valves. J Mech Behav Biomed Mater 58:173–187. doi:10.1016/j.jmbbm.2015.10.001

    Article  Google Scholar 

  • Lynch B, Bancelin S, Bonod-Bidaud C et al (2016) A novel microstructural interpretation for the biomechanics of mouse skin derived from multiscale characterization. Acta Biomater. doi:10.1016/j.actbio.2016.12.051

    Google Scholar 

  • Mauri a, Perrini M, Mateos JM (2013) Second harmonic generation microscopy of fetal membranes under deformation: normal and altered morphology. Placenta 34:1020–1026. doi:10.1016/j.placenta.2013.09.002

    Article  Google Scholar 

  • Mauri A, Ehret AE, Perrini M et al (2015) Deformation mechanisms of Human amnion: quantitative studies based on second harmonic generation microscopy. J Biomech. doi:10.1016/j.jbiomech.2015.01.045

  • Obbink-Huizer C, Oomens CWJ, Loerakker S et al (2014) Computational model predicts cell orientation in response to a range of mechanical stimuli. Biomech Model Mechanobiol 13:227–236. doi:10.1007/s10237-013-0501-4

    Article  Google Scholar 

  • Puxkandl R, Zizak I, Paris O et al (2002) Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc Lond B Biol Sci 357:191–197. doi:10.1098/rstb.2001.1033

    Article  Google Scholar 

  • Ramanujan S (1914) Modular equations and approximations to pi. Q J Math 45:350–372

    MATH  Google Scholar 

  • Raub CB, Unruh J, Suresh V et al (2008) Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties. Biophys J 94:2361–2373. doi:10.1529/biophysj.107.120006

    Article  Google Scholar 

  • Rezakhaniha R, Agianniotis a, Schrauwen JTC et al (2012) Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11:461–473. doi:10.1007/s10237-011-0325-z

    Article  Google Scholar 

  • Robert L (2002) Elastin, past, present and future. Pathol Biol 50:503–511. doi:10.1016/S0369-8114(02)00336-X

    Article  Google Scholar 

  • Sacks MS (2003) Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. J Biomech Eng 125:280. doi:10.1115/1.1544508

    Article  Google Scholar 

  • Screen HRC, Evans SL (2009) Measuring strain distributions in tendon using confocal microscopy and finite elements. J Strain Anal Eng Des 44:327–335. doi:10.1243/03093247JSA491

    Article  Google Scholar 

  • Tang T, Ebacher V, Cripton P et al (2015) Shear deformation and fracture of human cortical bone. Bone 71:25–35. doi:10.1016/j.bone.2014.10.001

    Article  Google Scholar 

  • Vijayaraghavan S, Huq R, Hausman MR (2014) Methods of peripheral nerve tissue preparation for second harmonic generation imaging of collagen fibers. Methods 66:246–255. doi:10.1016/j.ymeth.2013.08.012

    Article  Google Scholar 

  • Voss B, Rauterberg J, Allam S, Pott G (1980) Distribution of collagen type I and type III and of two collagenous components of basement membranes in the human liver. Pathol Res Pract 170:50–60. doi:10.1016/S0344-0338(80)80155-5

    Article  Google Scholar 

  • Zoumi A, Lu X, Kassab GS, Tromberg BJ (2004) Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. Biophys J 87:2778–2786. doi:10.1529/biophysj.104.042887

    Article  Google Scholar 

  • Zoumi A, Yeh A, Tromberg BJ (2002) Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence. Proc Natl Acad Sci USA 99:11014–11019. doi:10.1073/pnas.172368799

    Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Pr Mathias Brieu for useful discussions. This work was supported by the Programme Avenir Lyon Saint-Etienne (ANR-11-IDEX-0007) of Université de Lyon, within the program “Investissements d’Avenir” operated by the French National Research Agency (ANR), and by grants from Ecole Polytechnique (interdisciplinary project) and from Agence Nationale de la Recherche (ANR-13-BS09-0004-02 and ANR-10-INBS-04).

Conflict of interest

None of the authors have any professional or financial conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. Bruyère-Garnier.

Additional information

J-M. Allain, K. Bruyère-Garnier and M. Coret have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 360 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jayyosi, C., Affagard, JS., Ducourthial, G. et al. Affine kinematics in planar fibrous connective tissues: an experimental investigation. Biomech Model Mechanobiol 16, 1459–1473 (2017). https://doi.org/10.1007/s10237-017-0899-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-017-0899-1

Keywords

Navigation