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Research Papers

Ageing Changes in the Tensile Properties of Tendons: Influence of Collagen Fibril Volume Fraction

[+] Author and Article Information
K. L. Goh1

Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore 639798, Singaporegohkl@ntu.edu.sg

D. F. Holmes, H.-Y. Lu, S. Richardson, K. E. Kadler

School of Biological Science, University of Manchester, Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK

P. P. Purslow

Department of Food Science, University of Guelph, Guelph, ON, N1G 2W1, Canada

T. J. Wess

Structural Biophysics Group, School of Optometry and Vision Sciences,  Cardiff University, Redwood Building, Cardiff, CF10 3NB, UK

1

Corresponding author.

J Biomech Eng 130(2), 021011 (Mar 31, 2008) (8 pages) doi:10.1115/1.2898732 History: Received May 31, 2006; Revised September 11, 2007; Published March 31, 2008

Connective tissues are biological composites comprising of collagen fibrils embedded in (and reinforcing) the hydrated proteoglycan-rich (PG) gel within the extracellular matrices (ECMs). Age-related changes to the mechanical properties of tissues are often associated with changes to the structure of the ECM, namely, fibril diameter. However, quantitative attempts to correlate fibril diameter to mechanical properties have yielded inconclusive evidence. Here, we described a novel approach that was based on the rule of mixtures for fiber composites to evaluate the dependence of age-related changes in tendon tensile strength (σ) and stiffness (E) on the collagen fibril cross-sectional area fraction (ρ), which is related to the fibril volume fraction. Tail tendons from C57BL6 mice from age groups 1.635.3months old were stretched to failure to determine σ and E. Parallel measurements of ρ as a function of age were made using transmission electron microscopy. Mathematical models (rule of mixtures) of fibrils reinforcing a PG gel in tendons were used to investigate the influence of ρ on ageing changes in σ and E. The magnitudes of σ, E, and ρ increased rapidly from 1.6monthsto4.0months (P-values <0.05) before reaching a constant (age independent) from 4.0monthsto29.0months (P-values >0.05); this trend continued for E and ρ (P-values >0.05) from 29.0monthsto35.3months, but not for σ, which decreased gradually (P-values <0.05). Linear regression analysis revealed that age-related changes in σ and E correlated positively to ρ (P-values <0.05). Collagen fibril cross-sectional area fraction ρ is a significant predictor of ageing changes in σ and E in the tail tendons of C57BL6 mice.

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Copyright © 2008 by American Society of Mechanical Engineers
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Figures

Grahic Jump Location
Figure 1

Plot of stress (MPa) versus strain obtained from loading a tail tendon in tension to failure. The tendons were from 1.6month and 4.0month old C57BL6 mice. The stress-strain data were fitted to a fifth order polynomial equation. The strength and stiffness of the tendon were determined from the maximum stress and the gradient at the point of inflexion, respectively.

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Figure 2

Transmission electron micrographs showing cross sections of collagen fibrils within a transverse section of tendons from the tail of C57BL6 mice corresponding to the following age classes (months): (a) 1.6, (b) 2.6, (c) 11.5, and (d) 29.0. Scale bar=350nm.

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Figure 3

Graphs of (a) strength σ and collagen cross-sectional area fraction ρ and (b) stiffness E and ρ versus age in months of tendons from the tail of C57BL6 mice. Diamonds ◆ are used to represent data points corresponding to σ and E; dots ● are used for ρ. The vertical bar at each data point indicates the SE of the mean value of σ, E, and ρ. Only data points from Robinson (9) are circled in order to distinguish them from the current work.

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Figure 4

Linear regression plots for (a) strength σ versus collagen cross-sectional area fraction ρ and (b) stiffness E versus ρ. Using data points from our work, the fitted continuous lines (trend line 1) were determined to be σ=114.21ρ−35.41(R‐squared=0.56) and E=921.05ρ−106.34(R‐squared=0.61). Statistical tables were used to obtain the critical F-ratio (Fcrit=5.99, α=0.05, and degree of freedoms ν1=1 and ν2=6). From ANOVA, the computed F-ratios for (a) and (b) were 7.68 and 9.41, respectively; the P-values were <0.05. When data points from Robinson (9) were considered together with those from the current work, the fitted dashed lines (trend line 2) were determined to be σ=166.96ρ−78.06(R‐squared=0.68) and E=1366.80ρ−463.14(R‐squared=0.69). The critical F-ratio, Fcrit=4.41 (α=0.05 and degree of freedoms ν1=1 and ν2=8). The computed F-ratios for (a) and (b) were 17.15 and 17.69, respectively; the P-values were <0.05.

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