Annals of Biomedical Engineering

, Volume 40, Issue 8, pp 1666–1678

Automated Estimation of Collagen Fibre Dispersion in the Dermis and its Contribution to the Anisotropic Behaviour of Skin

• Aisling Ní Annaidh
• Karine Bruyère
• Michael D. Gilchrist
• Melanie Otténio
• Giuseppe Saccomandi
Article

Abstract

Collagen fibres play an important role in the mechanical behaviour of many soft tissues. Modelling of such tissues now often incorporates a collagen fibre distribution. However, the availability of accurate structural data has so far lagged behind the progress of anisotropic constitutive modelling. Here, an automated process is developed to identify the orientation of collagen fibres using inexpensive and relatively simple techniques. The method uses established histological techniques and an algorithm implemented in the MATLAB image processing toolbox. It takes an average of 15 s to evaluate one image, compared to several hours if assessed visually. The technique was applied to histological sections of human skin with different Langer line orientations and a definite correlation between the orientation of Langer lines and the preferred orientation of collagen fibres in the dermis $$(p<0.001, R^{2}= 0.95)$$ was observed. The structural parameters of the Gasser–Ogden–Holzapfel (GOH) model were all successfully evaluated. The mean dispersion factor for the dermis was $$\kappa = 0.1404 \pm 0.0028.$$ The constitutive parameters μ, k 1 and k 2 were evaluated through physically-based, least squares curve-fitting of experimental test data. The values found for μ, k 1 and k 2 were 0.2014 MPa, 243.6 and 0.1327, respectively. Finally, the above model was implemented in ABAQUS/Standard and a finite element (FE) computation was performed of uniaxial extension tests on human skin. It is expected that the results of this study will assist those wishing to model skin, and that the algorithm described will be of benefit to those who wish to evaluate the collagen dispersion of other soft tissues.

Keywords

Fibre orientation Anisotropic Skin Collagen Fibres

Notes

Acknowledgments

The authors acknowledge gratefully the advice and assistance of Mr. Ciaran Driver, Dr. Michael Curtis and Prof. Marie Cassidy, of the Office of the State Pathologist (Ireland), in the area of histology. This research was supported by a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, awarded to MD; by the Irish Research Council for Science, Engineering and Technology; by the Office of the State Pathologist (Irish Department of Justice and Equality); and by the Ile-de-France region. G.S. is supported by the PRIN 2009 project “Matematica e meccanica dei sistemi biologici e dei tessuti molli”.

References

1. 1.
Bischoff, J. E., E. M. Arruda, and K. Grosh. Finite element modeling of human skin using an isotropic, nonlinear elastic constitutive model. J. Biomech. 33:645–652, 2000.
2. 2.
Bischoff, J. E., E. M. Arruda, and K. Grosh. A rheological network model for the continuum anisotropic and viscoelastic behaviour of soft tissue. Biomech. Model. Mechanobiol. 3:56–65, 2004.
3. 3.
Cortes, D. H., S. P. Lake, J. A. Kadlowec, and L. J. Soslowsky, and D. M. Elliott. Characterizing the mechanical contribution of fiber angular distribution in connective tissue: comparison of two modeling approaches. Biomech. Model. Mechanobiol. 9:651–658, 2010.
4. 4.
Elbischger, P., H. Bischof, P. Regitnig, and G. Holzapfel. Automatic analysis of collagen fiber orientation in the outermost layer of human arteries. Pattern Anal. Appl. 7:269–284, 2004.Google Scholar
5. 5.
Evans, S. L. On the implementation of a wrinkling, hyperelastic membrane model for skin and other materials. Comput. Meth. Biomech. Biomed. Eng. 12:319–332, 2009.
6. 6.
Flamini, V., C. Kerskens, K. M. Moerman, C. K. Simms, and C. Lally. Imaging arterial fibres using diffusion tensor imaging—feasability study and preliminary results. EURASIP J. Adv. Signal. Process. 2010.Google Scholar
7. 7.
Flynn, C., and A. Taberner, P. Modeling the mechanical response of in vivo human skin under a rich set of deformations. Ann. Biomed. Eng. 39:1935–1946, 2011.
8. 8.
Gamage, T. P., V. Rajagopal, M. Ehrgott, M. P. Nash, and P. M. F. Nielsen. Identification of mechanical properties of heterogeneous soft bodies using gravity loading. Int. J. Numer. Methods Biomed. Eng. 27:391–407, 2011.
9. 9.
Gasser, T., R. W. Ogden, and G. Holzapfel. Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J. R. Soc. Interface 3:15–35, 2006.
10. 10.
Haralick, R. M., and L. G. Shapiro. Computer and Robot Vision, vol. 1. Boston: Addison-Wesley, 1992.Google Scholar
11. 11.
Holzapfel, G. A. Handbook of Materials Behavior Models: Biomechanics of Soft Tissue, edited by J. Lemaitre. Academic Press, 2001, pp. 1057–1071.Google Scholar
12. 12.
Holzapfel, G. A. Determination of material models for arterial walls from uniaxial extension tests and histological structure. J. Theor. Biol. 238:290–302, 2006.
13. 13.
Holzapfel, G. A., and R. W. Ogden. On planar biaxial tests for anisotropic nonlinearly elastic solids: a continuum mechanical framework. Math. Mech. Solids 14:474–489, 2009.
14. 14.
Jones, T. A. MATLAB functions to analyze directional (azimuthal) data–I: single-sample inference. Comput. Geosci. 32:166–175, 2006.
15. 15.
Jor, J. W. Y., P. M. F. Nielsen, M. P. Nash, and P. J. Hunter. Modelling collagen fibre orientation in porcine skin based upon confocal laser scanning microscopy. Skin Res. Technol. 17:149–159, 2011.
16. 16.
Jor, J. W. Y., M. P. Nash, P. M. F. Nielsen, and P. J. Hunter. Estimating material parameters of a structurally based constitutive relation for skin mechanics. Biomech. Model. Mechanobiol. 10:767–778, 2011.
17. 17.
Langer, K. On the anatomy and physiology of the skin. The Imperial Academy of Science, Vienna (1861). Reprinted in (1978): Br. J. Plast. Surg. 17:93–106, 1978. Google Scholar
18. 18.
Lanir, Y. Constitutive equations for fibrous connective tissues. J. Biomech. 16:1–12, 1983.
19. 19.
Lanir, Y., O. Lichtenstein, and O. Imanuel Optimal design of biaxial tests for structural material characterization of flat tissues. J. Biomech. Eng. 118:41–46, 1996.
20. 20.
Ní Annaidh, A., K. Bruyère, M. Destrade, M. Gilchrist, and M. Otténio. Characterising the anisotropic mechanical properties of excised human skin. J. Mech. Behav. Biomed. Mater. 5:139–148, 2012.
21. 21.
Noorlander, M. L., P. Melis, A. Jonker, and C. J. Van Noorden. A quantitative method to determine the orientation of collagen fibers in the dermis. J. Histochem. Cytochem. 50:1469–1474, 2002.
22. 22.
Ogden, R. W., G. Saccomandi, and I. Sgura. Fitting hyperelastic models to experimental data. Comput. Mech. 34:484–502, 2004.
23. 23.
Otsu, N. A threshold selection method from grey-level histograms. IEEE Trans. Syst. Man Cybern. 9:62–66, 1979.
24. 24.
Ridge, M., and V. Wright. Mechanical properties of skin: a bioengineering study of skin structure. J. Appl. Physiol. 21:1602–1606, 1966.
25. 25.
Ruvolo, E. C., Jr., G. N. Stamatas, and N. Kollias. Skin viscoelasticity displays site- and age-dependent angular anisotropy. Skin Pharmacol. Physiol. 20:313–321, 2007.
26. 26.
Van Zuijlen, P. P. M., H. J. de Vries, E. N. Lamme, J. E. Coppens, J. Van Marle, R. W. Kries, and E. Middelkoop. Morphometry of dermal collagen orientation by Fourier analysis is superior to multi-observer assessment. J. Pathol. 198:284–291, 2002.
27. 27.
Verhaegen, P. D. H. M., E. M. Res, A. Van Engelen, E. Middelkoop, and P. P. M. Van Zuijlen. A reliable, non-invasive measurement tool for anisotropy in normal skin and scar tissue. Skin Res. Technol. 16(3):325–331, 2010.
28. 28.
Wu, J., B. Ragwa, D. Filmer, C. Hoffmann, B. Yuan, C. Chiang, J. Sturgis, and J. Robison. Automated quantification and reconstruction of collagen matrix from 3D confocal datasets. J. Microscopy 210:158–165, 2003.
29. 29.
Yasui, T., Y. Tohno, and T. Araki. Characterization of collagen orientation in human dermis by two-dimensional second-harmonic-generation polarimetry. J. Biomed. Opt. 9:259–264, 2004.

Authors and Affiliations

• Aisling Ní Annaidh
• 1
• 2
• 3
Email author
• Karine Bruyère
• 4
• 5
• 6
• 1
• 7
• Michael D. Gilchrist
• 1
• 2
• 3
• Melanie Otténio
• 4
• 5
• 6
• Giuseppe Saccomandi
• 8
1. 1.School of Mechanical and Materials EngineeringUniversity College DublinDublin 4Ireland
2. 2.UPMC, Univ Paris 6, UMR 7190, Institut Jean Le Rond d’AlembertParisFrance
3. 3.CNRS, UMR 7190, Institut Jean Le Rond d’AlembertParisFrance
4. 4.Université de LyonLyonFrance
5. 5.IFSTTAR, LBMC, UMR_T9406BronFrance
6. 6.Université Lyon 1VilleurbanneFrance
7. 7.School of Mathematics, Statistics and Applied MathematicsNational University of Ireland GalwayGalwayIreland
8. 8.Dipartimento di Ingegneria IndustrialeUniversità degli Studi di PerugiaPerugiaItaly
{"extraction_info": {"found_math": true, "script_math_tex": 0, "script_math_asciimath": 0, "math_annotations": 0, "math_alttext": 0, "mathml": 0, "mathjax_tag": 0, "mathjax_inline_tex": 0, "mathjax_display_tex": 1, "mathjax_asciimath": 0, "img_math": 0, "codecogs_latex": 0, "wp_latex": 0, "mimetex.cgi": 0, "/images/math/codecogs": 0, "mathtex.cgi": 0, "katex": 0, "math-container": 0, "wp-katex-eq": 0, "align": 0, "equation": 0, "x-ck12": 0, "texerror": 0, "math_score": 0.5761894583702087, "perplexity": 18988.59300342038}, "config": {"markdown_headings": false, "markdown_code": true, "boilerplate_config": {"ratio_threshold": 0.18, "absolute_threshold": 10, "end_threshold": 15, "enable": true}, "remove_buttons": true, "remove_image_figures": true, "remove_link_clusters": true, "table_config": {"min_rows": 2, "min_cols": 3, "format": "plain"}, "remove_chinese": true, "remove_edit_buttons": true, "extract_latex": true}, "warc_path": "s3://commoncrawl/crawl-data/CC-MAIN-2019-13/segments/1552912202924.93/warc/CC-MAIN-20190323181713-20190323203713-00495.warc.gz"}