Observations on morphologic changes in the aging and degenerating human disc: secondary collagen alterations

Abstract

Background: In the annulus, collagen fibers that make up the lamellae have a wavy, planar crimped pattern. This crimping plays a role in disc biomechanical function by allowing collagen fibers to stretch during compression. The relationship between morphologic changes in the aging/degenerating disc and collagen crimping have not been explored.

Methods: Ultrastructural studies were performed on annulus tissue from 29 control (normal) donors (aged newborn to 79 years) and surgical specimens from 49 patients (aged 16 to 77 years). Light microscopy and specialized image analysis to visualize crimping was performed on additional control and surgical specimens. Human intervertebral disc tissue from the annulus was obtained in a prospective morphologic study of the annulus. Studies were approved by the authors' Human Subjects Institutional Review Board.

Results: Three types of morphologic changes were found to alter the crimping morphology of collagen: 1) encircling layers of unusual matrix disrupted the lamellar collagen architecture; 2) collagen fibers were reduced in amount, and 3) collagen was absent in regions with focal matrix loss.

Conclusions: Although proteoglycan loss is well recognized as playing a role in the decreased shock absorber function of the aging/degenerating disc, collagen changes have received little attention. This study suggests that important stretch responses of collagen made possible by collagen crimping may be markedly altered by morphologic changes during aging/degeneration and may contribute to the early tissue changes involved in annular tears.

Figure 1

Diagrammatic illustration of the organization of the intervertebral disc with attention to lamellar structure in the annulus and crimping in the collagen fibers. (Reproduced with permission [3].

Figure 2

Figs. 2A and 2B: Photomicrographs of light microscopic features of the annulus in a disc from a three month old infant (A) and a control disc from a 68 year old female (B and C). Arrows in A mark regions of prominent collagen crimping. In B note the presence of abnormal matrix encircling disc cells and decreased matrix in intraterritorial regions. In Fig. 2C a region of prominent focal loss of matrix is present near encapsulated cells. (A, glycol methacrylate embedment, Goldner's stain; B and C, paraffin with Masson-trichrome; X 980).

Figure 3

Electron micrographs showing regions of collagen fibers in a wavy pattern in a region of annulus (Fig. 3A) which contrasts with sparser collagen in a region with more prominent matrix loss (Fig. 3B). (Surgical specimen from a 35 year old female. (Fig. 3A, X 5,900; Fig. 3B, X 13, 940).

Figure 4

Photomicrographs of disc tissue from the annulus in a region of healthy matrix (Fig. 4B, surgical specimen from a 46 year old female) and from a region with marked matrix changes (Fig. 4D, surgical specimen from a 54 year old male). In Figures 4A and 4C, collagen crimping patterns throughout the same microscopic fields shown in Figs. 4B and 4D are converted to graphic images with three-dimensional intensity images using BioScan^® OPTIMAS™ using the following settings for both images: rotation: x, 25.000; y, 1.000; sampling, x: 45, y:45, and viewpoint Z: 3000.0 . White arrows in Fig. 4D mark small regions showing collagen crimping, but degenerative changes in the tissue disrupt crimping in the adjacent regions. (Figs. 4B and 4D, polarized light, picrosirius red/alcian blue, X 102).