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Collagen Morphology of the Collagen Framework

The pattern of collagen fibrils within articular cartilage is well suited to the functional requirements of the tissue. The air-tent analogy described earlier requires that a pressurized internal medium be constrained from expansion by a membrane. A matted surface layer of collagen fibrils provides this membranelike function.

The collagen pattern in the deeper layers of the cartilage surface is morphologically quite different from the surface pattern. In 1925, Benninghoff  described an arcade pattern of organization for articular cartilage collage.

This pattern has subsequently been challenged with respect to the precise accuracy of the proposed scheme. The concept is at least partially correct, however, and it is useful in understanding the function of cartilage.

The surface fibrillar pattern clearly differs from that of fibers in deeper layers . The surface collagen fibrils are smaller (diameter, 30–32 nm) and more closely packed than in the middle and deeper layers. The surface pattern of the collagen framework as described has been recognized implicitly for decades by the term “armor plate” layer, referring to the tough, resilient, skinlike cartilage surface. The collagen concentration is greatest at the surface, where the small fibrils are compacted tangentially.

This arrangement creates a small pore size, which has been calculated by McCutchen to be approximately 6 nm. The largest molecule that can traverse a pore of this dimension is hemoglobin. Small ions and glucose, for example, easily traverse these pores, but larger molecules, such as most proteins and hyaluronan (hyaluronic acid), do not enter cartilage in significant amounts under normal conditions.

Collagen fibers in the intermediate layers are no longer oriented tangentially to the surface but, rather, are directed obliquely or randomly. They are larger than the surface fibrils, with most ranging between 40 and 100 nm. The deepest fibrils are the largest in cartilage.

They are disposed perpendicularly relative to the joint surface, and they perforate the calcified basal layers of cartilage through the tidemark regions and, eventually, enter the subchondral bone layer, where they are firmly attached, much as in the attachment of the Sharpey fibers of ligament to cortical bone. This feature is crucial for cartilage to be able to resist shearing forces, which otherwise would tend to peel the cartilage away from the subchondral surface.

It has been well demonstrated clinically that loss of the densely packed collagen mat at the surface of cartilage in weight-bearing regions is the prelude to fibrillation, accelerated wear, and degenerative arthritis. This seems completely logical, because the coarse, widely spaced fibrils in deeper layers that are principally oriented vertically are poorly suited for constraining the swelling forces that are generated by the matrix proteoglycans.

The term fibrillation describes the tendency of these fibrils to be split vertically all the way to their subchondral attachment, much as wood splits along the grain of its fibers.

The villuslike strands so exposed collectively resemble a shag rug, and the individual strands are prone to tear off at the base when mechanically loaded and exposed to shear stresses.

Clearly, the description of an “armor plate” applies well to the normal surface mat of collagen fibrils, and loss of this layer no longer permits the cartilage to function as a pressurized unit suited to weight-bearing.

Evidence supporting the fibril pattern of collagen orientation derives from several types of observation, including routine histology, transmission-electron microscopy, scanning-electron microscopy, and the demonstration of Hultkrantz lines .

Hultkrantz lines typically are observed on the surface of cartilage and are analogous to the Langer lines of skin. These lines become visible when the surface of cartilage is pricked with a pin. Coating the cartilage surface with India ink and then wiping it dry best demonstrates the puncture defects. Hultkrantz noted many years ago that the puncture holes appeared as slits rather than round holes.

Furthermore,these slits have axes that generally are perpendicular to the principal axis of movement of the joint. Hultkrantz lines therefore are different for each joint of the body.

Mechanical tensile tests have confirmed that the Hultkrantz lines indicate the preferred orientation of the collagen fibrils at the surface of the joint resists tensile forces.

Bullough and Goodfellow have shown this characteristic of joint surfaces in polarized-light experiments. For interested readers, the pattern of matrix and cellular organization of articular cartilage has been described in greater detail by Wong and Hunziker.

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