Cartilage collagen matrix reorientation and displacement in response to surface loading.
Abstract: An investigation of collagen fiber reorientation, as well as fluid and matrix movement of equine articular cartilage and subchondral bone under compressive mechanical loads, was undertaken using small angle X-ray scattering measurements and optical microscopy. Small angle X-ray scattering measurements were made on healthy and diseased samples of equine articular cartilage and subchondral bone mounted in a mechanical testing apparatus on station ID18F of ESRF, Grenoble, together with fiber orientation analysis using polarized light and displacement measurements of the cartilage matrix and fluid using tracers. At surface pressures of up to approximately 1.5 MPa, there was reversible compression of the tangential surface fibers and immediately subjacent zone. As load increased, deformation in these zones reached a maximum and then reorientation propagated to the radial deep zone. Between surface pressures of 4.8 MPa and 6.0 MPa, fiber orientation above the tide mark rotated 10 deg from the radial direction, with an overall loss of alignment. With further increase in load, the fibers "crimped" as shown by the appearance of subsidiary peaks approximately +/-10 deg either side of the principal fiber orientation direction. Failure at higher loads was characterized by a radial split in the deep cartilage, which propagated along the tide mark while the surface zone remained intact. In lesions, the fiber organization was disrupted and the initial response to load was consistent with early rupture of fibers, but the matrix relaxed to an organization very similar to that of the unloaded tissue. Tracer measurements revealed anisotropic solid and fluid displacement, which depended strongly on depth within the tissue.
Publication Date: 2009-01-22 PubMed ID: 19154067DOI: 10.1115/1.3049478Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research study investigates the changes in collagen fiber arrangement, as well as the fluid and matrix movement, in horse joint cartilage and the bone below it when subjected to pressure, using X-ray scattering measurements and light microscopy.
Research Method
- Small angle X-ray scattering measurements were used to observe the physical characteristics and behavior of the cartilage and subchondral bone taken from both healthy and diseased equine samples, which were subjected to mechanical pressure.
- Their orientation was studied using polarized light and any displacement in their matrix and fluid was observed through the use of trackers.
Findings and Revelations
- Under surface pressure of about 1.5 MPa, the surface fibers and immediately adjacent zone exhibited reversible compression.
- As the load increased, the deformation in these areas also increased to its limit, before the change in orientation travelled to the deep radial zone.
- When the surface pressure was between 4.8 MPa and 6.0 MPa, fibers above the tide mark moved 10 degrees from the radial direction, leading to a loss of overall alignment.
- With further load, the fibers exhibited a ‘crimped’ appearance, highlighted by secondary peaks around +/- 10 degrees either side of the main fiber orientation direction.
- Failure at higher loads was characterized by a split in the deep cartilage in radial direction, spreading along the tide mark while the surface zone remained intact.
- In lesions, the organization of the fibers was disrupted with the initial loading response resembling early fiber ruptures, but the matrix eventually relaxed to an arrangement similar to that of unloaded tissue.
- The measurements showed non-uniform displacement of solid and fluid within the tissue, which was strongly dependent on the depth.
Conclusion
- The study provides insights into the way the cartilage matrix and collagen fibers reorient and displace under mechanical stress, which can contribute to the understanding and treatment of collagen-related ailments such as arthritis.
Cite This Article
APA
Moger CJ, Arkill KP, Barrett R, Bleuet P, Ellis RE, Green EM, Winlove CP.
(2009).
Cartilage collagen matrix reorientation and displacement in response to surface loading.
J Biomech Eng, 131(3), 031008.
https://doi.org/10.1115/1.3049478 Publication
Researcher Affiliations
- School of Physics, University of Exeter, Stocker Road, Exeter, Devon EX4 4QL, UK. c.j.moger@ex.ac.uk
MeSH Terms
- Animals
- Anisotropy
- Cartilage, Articular / physiology
- Collagen / physiology
- Coloring Agents / metabolism
- Compressive Strength
- Equipment Design
- Evans Blue / metabolism
- Extracellular Matrix / physiology
- Fluorescent Dyes / metabolism
- Horses / physiology
- Microinjections
- Microscopy, Polarization
- Models, Biological
- Osteoarthritis / physiopathology
- Pressure
- Rhodamines / metabolism
- Scattering, Small Angle
- Stress, Mechanical
- Weight-Bearing
- X-Ray Diffraction
Citations
This article has been cited 14 times.- Inamdar SR, Prévost S, Terrill NJ, Knight MM, Gupta HS. Reversible changes in the 3D collagen fibril architecture during cyclic loading of healthy and degraded cartilage.. Acta Biomater 2021 Dec;136:314-326.
- Huynh RN, Pesante B, Nehmetallah G, Raub CB. Polarized reflectance from articular cartilage depends upon superficial zone collagen network microstructure.. Biomed Opt Express 2019 Nov 1;10(11):5518-5534.
- Ravanfar M, Yao G. Simultaneous tractography and elastography imaging of the zone-specific structural and mechanical responses in articular cartilage under compressive loading.. Biomed Opt Express 2019 Jul 1;10(7):3241-3256.
- Inamdar SR, Barbieri E, Terrill NJ, Knight MM, Gupta HS. Proteoglycan degradation mimics static compression by altering the natural gradients in fibrillar organisation in cartilage.. Acta Biomater 2019 Oct 1;97:437-450.
- Mansfield JC, Mandalia V, Toms A, Winlove CP, Brasselet S. Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy.. J R Soc Interface 2019 Jan 31;16(150):20180611.
- Wang N, Badar F, Xia Y. Experimental Influences in the Accurate Measurement of Cartilage Thickness in MRI.. Cartilage 2019 Jul;10(3):278-287.
- Wang N, Badar F, Xia Y. MRI properties of a unique hypo-intense layer in degraded articular cartilage.. Phys Med Biol 2015 Nov 21;60(22):8709-21.
- Nagai M, Aoyama T, Ito A, Tajino J, Iijima H, Yamaguchi S, Zhang X, Kuroki H. Alteration of cartilage surface collagen fibers differs locally after immobilization of knee joints in rats.. J Anat 2015 May;226(5):447-57.
- Wang N, Kahn D, Badar F, Xia Y. Molecular origin of a loading-induced black layer in the deep region of articular cartilage at the magic angle.. J Magn Reson Imaging 2015 May;41(5):1281-90.
- Raub CB, Hsu SC, Chan EF, Shirazi R, Chen AC, Chnari E, Semler EJ, Sah RL. Microstructural remodeling of articular cartilage following defect repair by osteochondral autograft transfer.. Osteoarthritis Cartilage 2013 Jun;21(6):860-8.
- Hadi MF, Sander EA, Barocas VH. Multiscale model predicts tissue-level failure from collagen fiber-level damage.. J Biomech Eng 2012 Sep;134(9):091005.
- Han EH, Chen SS, Klisch SM, Sah RL. Contribution of proteoglycan osmotic swelling pressure to the compressive properties of articular cartilage.. Biophys J 2011 Aug 17;101(4):916-24.
- Xu J, Zhu P, Morris MD, Ramamoorthy A. Solid-state NMR spectroscopy provides atomic-level insights into the dehydration of cartilage.. J Phys Chem B 2011 Aug 25;115(33):9948-54.
- Rolauffs B, Muehleman C, Li J, Kurz B, Kuettner KE, Frank E, Grodzinsky AJ. Vulnerability of the superficial zone of immature articular cartilage to compressive injury.. Arthritis Rheum 2010 Oct;62(10):3016-27.
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