Data on the distribution of collagen fibril diameters in various connective tissues have been collected and analysed for common features. The diameter distributions of the collagen fibrils at birth and in the foetal stages of development are unimodal, whereas at maturity the mass-average diameter of the collagen fibrils is generally larger than at birth and the distributions of fibril sizes may be either unimodal or bimodal depending on the tissue. At senescence, few data are available but in most instances both the mean and mass-average diameters of the collagen fibrils are smaller than those at maturity and the fibril distributions are mainly bimodal. The division between tissues showing unimodal or bimodal fibril distributions at maturity does not simply relate to the type I collagen/type II collagen classification, to the distinction between orientated and unorientated material or indeed directly to the levels of stress and strain encountered by the tissue. However, there may prove to be a relation between a bimodal fibril diameter distribution at maturity and the maintenance over long periods of time of either high stress in stretched tissues or low stress in compressed tissues. It has also been noted that the width of the collagen fibril diameter distribution at birth differs between altricious and precocious animals. The ultimate tensile strength of a connective tissue and the mass-average diameter of the constituent collagen fibrils have been shown to have a positive correlation. Further, the form of the collagen fibril diameter distribution can be directly related to the mechanical properties of the tissue. In particular, it is postulated that the size distribution of the collagen fibrils is largely determined by two factors. First, if the tissue is primarily designed to have high tensile strength, then an increase in the diameter of the collagen fibrils will parallel an increase in the potential density of intrafibrillar covalent crosslinks. Consequently large collagen fibrils are predicted to have a greater tensile strength than small fibrils. Secondly, if the tissue is designed to be elastic and hence withstand creep, then a reduction in the diameter of the collagen fibrils will effectively increase the surface area per unit mass of the fibrils thus enhancing the probability of interfibrillar non-covalent crosslinks between the collagen fibrils and the components of the matrix. The idealized description given may indicate how the mechanical properties of a tissue may be interpreted in terms of the collagen fibril diameter distribution.
SynopsisAn electron microscope study of collagen fibrils from fixed tail tendons of rats has revealed that from some time shortly after birth until maturity, the fibril diameters have a bimodal distribution. The "two" types of fibril are indistinguishable in both transverse and longitudinal section. Unfixed specimens of eight-week-old-tail tendon showed a similar bimodal distribution of diameters though the positions of the peak values compared to fixed specimens of an eight-week-old-tail tendon were shifted upwards by about 30%. It has also been shown quantitatively that the polar collagen fibrils are directed randomly "up" and "down" with respect to their neighbors. Whilst it has been suggested by others that anastomosis is a feature of collagen structure, the results presented here do not support this hypothesis. Fibrillar units -140 A in diameter have been observed and the possibilities that these are elastic fibers or the breakdown products of collagen fibrils have been considered.
A theoretical expression has been derived for the mean collagen fibril length in tendon based on the assumption that collagen fibrils originate in cell surface invaginations and terminate either at some remote cell surface or another collagen fibril bundle. The expression thus determined requires knowledge of the effective lengths of the fibrocytes (or fibrocyte assemblies) and the cellular content of the tendon. Both of these parameters have been measured experimentally as a function of age for rat-tail tendon using a combined light microscope and electron microscope approach. The results obtained for immature tendon suggest that the mean collagen fibril length is at least equal to the critical length required to maintain the appropriate tensile properties. In the most mature tissue studied, however, the mean-collagen fibril length is in excess of 100 times the critical length.
Samples of anatomically and functionally distinct regions of the skin of a variety of altricial and precocial animals were taken at various stages of development from birth to beyond maturity. The glycosaminoglycan (GAG) content and composition of the tissues were determined by chemical analysis and the collagen fibril diameters measured by transmission electron microscopy. The fibril diameters of the skins of two fish and a bird were also assessed for comparison. Analysis and comparison of the data collected show that there was a significant correlation between collagen fibril diameter distribution, GAG type and amount, and functional load-bearing of the various skins, and that the variations in the biochemical and physical composition of the tissues at different stages of development could be related to both their post-conceptual maturity and their prospective functional loading.
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