Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-18T22:43:10.834Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcaneal Tendon Collagen Fiber Morphometry and Aging

Published online by Cambridge University Press:  20 September 2017

Daniel Hadraba Open the ORCID record for Daniel Hadraba [Opens in a new window] ,
Jiri Janacek ,
Eva Filova ,
Frantisek Lopot ,
Rik Paesen ,
Ondrej Fanta ,
Anneliese Jarman ,
Alois Necas ,
Marcel Ameloot  and
Karel Jelen
Daniel Hadraba*
Affiliation:
Department of Biomathematics, Institute of Physiology, The Czech Academy of Sciences, Videnska 1083, Prague 4, 14220, Czech Republic Department of Anatomy and Biomechanics, Faculty of Physical Education and Sport, Charles University, Jose Martiho 31, Prague 6, 162 00, Czech Republic Department of Biophysics, Biomedical Research Institute, Hasselt University, Agoralaan building C, Diepenbeek, B-3590, Belgium
Jiri Janacek
Affiliation:
Department of Biomathematics, Institute of Physiology, The Czech Academy of Sciences, Videnska 1083, Prague 4, 14220, Czech Republic
Eva Filova
Affiliation:
Department of Tissue Engineering, Institute of Experimental Medicine, The Czech Academy of Sciences, Videnska 1083, Prague 4, 14220, Czech Republic
Frantisek Lopot
Affiliation:
Department of Anatomy and Biomechanics, Faculty of Physical Education and Sport, Charles University, Jose Martiho 31, Prague 6, 162 00, Czech Republic
Rik Paesen
Affiliation:
Department of Biophysics, Biomedical Research Institute, Hasselt University, Agoralaan building C, Diepenbeek, B-3590, Belgium
Ondrej Fanta
Affiliation:
Department of Anatomy and Biomechanics, Faculty of Physical Education and Sport, Charles University, Jose Martiho 31, Prague 6, 162 00, Czech Republic
Anneliese Jarman
Affiliation:
Department of Tissue Engineering & Biophotonics, King’s College London, Guy’s Campus, Great Maze Pond, London, SE1 9RT, UK
Alois Necas
Affiliation:
Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Palackeho tr. 1/3, Brno, 612 42, Czech Republic
Marcel Ameloot
Affiliation:
Department of Biophysics, Biomedical Research Institute, Hasselt University, Agoralaan building C, Diepenbeek, B-3590, Belgium
Karel Jelen
Affiliation:
Department of Biomathematics, Institute of Physiology, The Czech Academy of Sciences, Videnska 1083, Prague 4, 14220, Czech Republic
*
*Corresponding author. [email protected]
Get access

Abstract

Fibrillar collagen in tendons and its natural development in rabbits are discussed in this paper. Achilles tendons from newborn (~7 days) to elderly (~38 months) rabbits were monitored in intact (ntendons=24) and microtome sectioned (ntendons=11) states with label-free second harmonic generation microscopy. After sectioning, the collagen fiber pattern was irregular for the younger animals and remained oriented parallel to the load axis of the tendon for the older animals. In contrast, the collagen fiber pattern in the intact samples followed the load axis for all the age groups. However, there was a significant difference in the tendon crimp pattern appearance between the age groups. The crimp amplitude (A) and wavelength (Λ) started at very low values (A=2.0±0.6 µm, Λ=19±4 µm) for the newborn animals. Both parameters increased for the sexually mature animals (>5 months old). When the animals were fully mature the amplitude decreased but the wavelength kept increasing. The results revealed that the microtome sectioning artifacts depend on the age of animals and that the collagen crimp pattern reflects the physical growth and development.

Keywords

collagenagingcrimpfiber orientationtendon
Type
Biological Science Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 5 , October 2017 , pp. 1040 - 1047
Copyright
© Microscopy Society of America 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Avery, N.C. & Bailey, A.J. (2005). Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: Relevance to aging and exercise. Scand J Med Sci Sports 15(4), 231–240.Google Scholar
Bayan, C., Levitt, J.M., Miller, E., Kaplan, D. & Georgakoudi, I. (2009). Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels. J Appl Phys 105(10), 102042.Google Scholar
Carlo, C.N. & Stevens, C.F. (2011). Analysis of differential shrinkage in frozen brain sections and its implications for the use of guard zones in stereology. J Comp Neurol 519(14), 2803–2810.Google Scholar
Castellano, G., Bonilha, L., Li, L.M. & Cendes, F. (2004). Texture analysis of medical images. Clin Radiol 59(12), 1061–1069.Google Scholar
Chen, W.L., Hu, P.S., Ghazaryan, A., Chen, S.J., Tsai, T.H. & Dong, C.Y. (2012 a). Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis. Comput Med Imaging Graph 36(7), 519–526.CrossRefGoogle ScholarPubMed
Chen, X., Nadiarynkh, O., Plotnikov, S. & Campagnola, P.J. (2012 b). Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protocols 7(4), 654–669.CrossRefGoogle ScholarPubMed
Cicchi, R., Vogler, N., Kapsokalyvas, D., Dietzek, B., Popp, J. & Pavone, F.S. (2013). From molecular structure to tissue architecture: Collagen organization probed by SHG microscopy. J Biophotonics 6(2), 129–142.Google Scholar
Clemmer, J., Liao, J., Davis, D., Horstemeyer, M.F. & Williams, L.N. (2010). A mechanistic study for strain rate sensitivity of rabbit patellar tendon. J Biomech 43(14), 2785–2791.CrossRefGoogle ScholarPubMed
Courtney, T., Sacks, M.S., Stankus, J., Guan, J. & Wagner, W.R. (2006). Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy. Biomaterials 27(19), 3631–3638.Google ScholarPubMed
Deniset-Besseau, A., Duboisset, J., Benichou, E., Hache, F., Brevet, P.-F. & Schanne-Klein, M.-C. (2009). Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin. J Phys Chem B 113(40), 13437–13445.Google Scholar
Dickey, J.P., Hewlett, B.R., Dumas, G.A. & Bednar, D.A. (1998). Measuring collagen fiber orientation: A two-dimensional quantitative macroscopic technique. J Biomech Eng 120(4), 537–540.Google Scholar
Dorph-Petersen, K.A., Nyengaard, J.R. & Gundersen, H.J. (2001). Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204(Pt 3), 232–246.Google Scholar
Franchi, M., Fini, M., Quaranta, M., De Pasquale, V., Raspanti, M., Giavaresi, G., Ottani, V. & Ruggeri, A. (2007). Crimp morphology in relaxed and stretched rat Achilles tendon. J Anat 210(1), 1–7.Google Scholar
Franchi, M., Ottani, V., Stagni, R. & Ruggeri, A. (2010). Tendon and ligament fibrillar crimps give rise to left-handed helices of collagen fibrils in both planar and helical crimps. J Anat 216(3), 301–309.Google Scholar
Freed, A.D. & Doehring, T.C. (2005). Elastic model for crimped collagen fibrils. J Biomech Eng 127(4), 587–593.Google Scholar
Frisch, K.E., Duenwald-Kuehl, S.E., Lakes, R.S. & Vanderby, R. (2012). Quantification of collagen organization using fractal dimensions and Fourier transforms. Acta Histochem 114(2), 140–144.Google Scholar
Gillard, J.H., Waldman, A.D. & Barker, P.B. (2009). Clinical MR Neuroimaging: Physiological and Functional Techniques. New York, NY: Cambridge University Press.Google Scholar
Hansen, K.A., Weiss, J.A. & Barton, J.K. (2002). Recruitment of tendon crimp with applied tensile strain. J Biomech Eng 124(1), 72–77.Google Scholar
Haus, J.M., Carrithers, J.A., Trappe, S.W. & Trappe, T.A. (2007). Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 103(6), 2068–2076.Google Scholar
Herchenhan, A., Kalson, N.S., Holmes, D.F., Hill, P., Kadler, K.E. & Margetts, L. (2012). Tenocyte contraction induces crimp formation in tendon-like tissue. Biomech Model Mechanobiol 11(3–4), 449–459.Google Scholar
Holzapfel, G.A. (2008). Collagen in arterial walls: Biomechanical aspects. In Collagen, P. Fratzl (Ed.), pp. 285–324. New York: Springer.Google Scholar
Houdebine, L.M. & Fan, J. (2009). Rabbit Biotechnology: Rabbit Genomics, Transgenesis, Cloning and Models. Dordrecht: Springer.Google Scholar
Jähne, B. (2005). Digital Image Processing. Berlin, Heidelberg, New York: Springer.Google Scholar
Janacek, J., Kreft, M., Cebasek, V. & Erzen, I. (2012). Correcting the axial shrinkage of skeletal muscle thick sections visualized by confocal microscopy. J Microsc 246(2), 107–112.Google Scholar
Karlon, W.J., Covell, J.W., McCulloch, A.D., Hunter, J.J. & Omens, J.H. (1998). Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras. Anat Rec 252(4), 612–625.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Legerlotz, K., Dorn, J., Richter, J., Rausch, M. & Leupin, O. (2014). Age-dependent regulation of tendon crimp structure, cell length and gap width with strain. Acta Biomater 10(10), 4447–4455.Google Scholar
Little, T.D. (2013). The Oxford Handbook of Quantitative Methods, Vol. 2: Statistical Analysis. Oxford, New York: Oxford University Press.Google Scholar
Maeda, E., Shelton, J.C., Bader, D.L. & Lee, D.A. (2007). Time dependence of cyclic tensile strain on collagen production in tendon fascicles. Biochem Biophys Res Commun 362(2), 399–404.Google Scholar
Melvin, N.R. & Sutherland, R.J. (2010). Quantitative caveats of standard immunohistochemical procedures: Implications for optical disector-based designs. J Histochem Cytochem 58(7), 577–584.Google Scholar
Myllyharju, J. & Kivirikko, K.I. (2004). Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20(1), 33–43.Google Scholar
Ntziachristos, V. (2010). Going deeper than microscopy: The optical imaging frontier in biology. Nat Method 7(8), 603–614.Google Scholar
Osman, O.S., Selway, J.L., Harikumar, P.E., Stocker, C.J., Wargent, E.T., Cawthorne, M.A., Jassim, S. & Langlands, K. (2013). A novel method to assess collagen architecture in skin. BMC Bioinform 14(1), 1–10.Google Scholar
Park, C.Y., Lee, J.K. & Chuck, R.S. (2015). Second harmonic generation imaging analysis of collagen arrangement in human cornea. Invest Ophthalmol Vis Sci 56(9), 5622–5629.Google Scholar
Patterson-Kane, J.C., Firth, E.C., Goodship, A.E. & Parry, D.A. (1997). Age-related differences in collagen crimp patterns in the superficial digital flexor tendon core region of untrained horses. Aust Vet J 75(1), 39–44.Google Scholar
Pavone, F.S. & Campagnola, P.J. (2013). Second Harmonic Generation Imaging. Boca Raton, London, New York: CRC Press.Google Scholar
Peeters, T., Vilanova, A., Strijkers, G. & ter Haar Romeny, B. (2006). Visualization of the fibrous structure of the heart. In Vision, Modeling and Visualization, Leif Kobbelt (Ed.), pp. 309–316. Amsterdam, The Netherlands: IOS Press.Google Scholar
Provenzano, P.P. & Vanderby, R. Jr (2006). Collagen fibril morphology and organization: Implications for force transmission in ligament and tendon. Matrix Biol 25(2), 71–84.Google Scholar
Raspanti, M., Manelli, A., Franchi, M. & Ruggeri, A. (2005). The 3D structure of crimps in the rat Achilles tendon. Matrix Biol 24(7), 503–507.Google Scholar
Raspanti, M., Reguzzoni, M., Protasoni, M. & Congiu, T. (2015). Mineralization-related modifications in the calcifying tendons of turkey (Meleagris gallopavo). Micron 71, 46–50.Google Scholar
Rocha-Mendoza, I., Yankelevich, D.R., Wang, M., Reiser, K.M., Frank, C.W. & Knoesen, A. (2007). Sum frequency vibrational spectroscopy: The molecular origins of the optical second-order nonlinearity of collagen. Biophys J 93(12), 4433–4444.Google Scholar
Sivaguru, M., Durgam, S., Ambekar, R., Luedtke, D., Fried, G., Stewart, A. & Toussaint, K.C. (2010). Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging. Opt Express 18(24), 24983–24993.Google Scholar
Soille, P. (2013). Morphological Image Analysis: Principles and Applications. Berlin, Heidelberg: Springer.Google Scholar
Stoller, P., Reiser, K.M., Celliers, P.M. & Rubenchik, A.M. (2002). Polarization-modulated second harmonic generation in collagen. Biophys J 82(6), 3330–3342.Google Scholar
Su, P.J., Chen, W.L., Chen, Y.F. & Dong, C.Y. (2011). Determination of collagen nanostructure from second-order susceptibility tensor analysis. Biophys J 100(8), 2053–2062.Google Scholar
Svensson, R.B., Mulder, H., Kovanen, V. & Magnusson, S.P. (2013). Fracture mechanics of collagen fibrils: Influence of natural cross-links. Biophys J 104(11), 2476–2484.Google Scholar
Thomason, D.B., Anderson, O. & Menon, V. (1996). Fractal analysis of cytoskeleton rearrangement in cardiac muscle during head-down tilt. J Appl Physiol 81(4), 1522–1527.Google Scholar
Thomopoulos, S., Marquez, J.P., Weinberger, B., Birman, V. & Genin, G.M. (2006). Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J Biomech 39(10), 1842–1851.Google Scholar
Varga, M. (2013). Textbook of Rabbit Medicine. 2nd ed. Cheshire, UK: Elsevier Health Sciences.Google Scholar
Vidal, B.D.C. (2003). Image analysis of tendon helical superstructure using interference and polarized light microscopy. Micron 34(8), 423–432.Google Scholar
Wang, J.H.C. (2006). Mechanobiology of tendon. J Biomech 39(9), 1563–1582.Google Scholar
Wang, J.H.C., Guo, Q. & Li, B. (2012). Tendon biomechanics and mechanobiology—A minireview of basic concepts and recent advancements. J Hand Therapy 25(2), 133–141.Google Scholar
Zhao, L., Thambyah, A. & Broom, N. (2015). Crimp morphology in the ovine anterior cruciate ligament. J Anat 226(3), 278–288.Google Scholar
Zhuo, S., Chen, J., Luo, T., Chen, H. & Zhao, J. (2007). High-contrast multimodel nonlinear optical imaging of collagen and elastin. In Journal of Physics: Conference Series, Vol. 48, T. Jiubin (Ed), p. 1476. Bristol, UK: IOP Publishing.Google Scholar