Neck Solutions

Biomechanical Implications of Degenerative Joint Disease in the Apophyseal Joints of Human Thoracic and Lumbar Vertebrae

From: Am J of Physical Anthrop. 136:318–326 (2008) The extent to which degenerative joint disease in bone may be seen as an indicator of mechanical or occupational stress has long been a focus of debate within osteoarchaeology. While some studies of paleopathology continue to use degenerative joint disease as a predictor of specific activity patterns, most urge caution. Clinical studies have failed to demonstrate a simple relationship between degenerative joint disease and specific patterns of movement or activity. Certain aspects of degenerative joint disease appear to be related to age, whereas others appear to be related to sex, genetic inheritance, or body weight. degenerative joint disease is probably best thought of as resulting from a combination of ‘‘systemic’’ risk factors (which can lead to degenerative changes to many joints within an individual) and localized factors which may be more closely related to the mechanical loading experienced at a particular joint. An additional complication is that skeletal tissues are able to strengthen in response to mechanical loading which does not damage them, so that moderate loading appears to be better for the joints than either low or high loading. Not surprisingly, this complexity has tended to discourage consideration of the biomechanical implications of degenerative joint disease, even where the presence and pattern of such pathology is well documented.

The vertebral column is one region of the skeleton that has become a focus of interest for paleopathological study into degenerative joint disease. Comparative studies between species have suggested that modern humans suffer vertebral osteophytosis and osteoarthritis more commonly and more severely than any other living primate, which might support the view that bipedal posture and locomotion generate localized mechanical factors affecting the spine that differ from those of other primate species. Detailed study of the morphology and distribution of degenerative changes in the human spine suggest that complex interacting factors are involved. For example, postmortem studies indicate that traumatic flexion or torsion injury to the lumbar spine can damage the articular surfaces of the apophyseal joints, possibly precipitating degenerative joint disease, and the pattern of cartilage damage may be indicative of the type of mechanical overload involved. Palaeopathological studies have suggested that degenerative joint disease occurs in the apophyseal joints of the cervical spine, which is subjected to relatively wide range of motion and also in the lower lumbar spine, which is heavily loaded. It is not clear if degenerative joint disease reflects excessive movements, or loading, or both.

The situation can be further complicated by the adjacent intervertebral discs. Disc degeneration and narrowing increase compressive load-bearing by the apophyseal joints, especially when specimens are loaded to simulate a lordotic posture, and clinical studies confirm that lumbar disc degeneration increases the risk of degenerative joint disease in the apophyseal joints. Evidence from postmortem studies has led to speculation that patterns of cartilage wear on the apophyseal joint surfaces may reflect focal loading of these surfaces in certain individuals and postures. However, there is little firm evidence to support this suggestion.

Given this complex background, it is perhaps not surprising that degenerative joint disease in the apophyseal joints is of uncertain biomechanical relevance to palaeopathology. There has recently been a call for experimentally tested and validated biomechanical models to enable skeletal function to be inferred from skeletal morphology. The present study responds to this call by combining experimental biomechanics and quantitative osteoarchaeology in order to investigate the mechanical implications of degenerative changes in human apophyseal joints. Direct quantification of the compressive load transmitted by the apophyseal joints is difficult, even in cadaveric specimens, but it can be achieved indirectly, by calculating the compressive force transmitted by the adjacent intervertebral disc. Here this technique will be used to compare load-bearing in the apophyseal joints of elderly cadavers with direct evidence of degenerative joint disease in the same joints, assessed from morphological changes in cartilage and bone.

Apophyseal joints evidently play a major, but variable, role in resisting compressive forces acting on the human thoracolumbar spine. On average, they resisted 45% of this force, but in particular specimens it could be as much as 96% or as little as 5%. This wide variation in levels of compressive load may be explained by the degree of disc degeneration. In a previous study that included the specimens described here, it was shown that disc degeneration transfers compressive load bearing from the anterior vertebral body to the neural arch in upright postures, but that this effect does not depend on spinal level or sex. In the present study, the results of the mixed ANOVA examining within-subject factors suggest that apophyseal joint loadbearing and degeneration were not systematically influenced by the spinal level. However, distribution of apophyseal joint degeneration with spinal level across the whole data set appears to reveal a pattern of peaks and troughs, which may mask any systematic trend within a single individual. The peaks of severity across the whole group lie between T10-T11 and L2-L5. This finding is consistent with previous work.

The compressive force that may underlie this finding is defined as the force acting down the long axis of the spine, perpendicular to the mid-plane of the intervertebral disc at each spinal level. Compression dominates spinal loading during vigorous activities, and arises primarily from tension in the paraspinal muscles which tend to follow the curvature of the spine. Even in simple standing postures, the need to stabilize the upright spine leads to high antagonistic activity of trunk muscles, and considerable spinal compression. Shear loading of the spine acts in a direction perpendicular to the compressive force (i.e. parallel to the mid-plane of the disc) and is resisted mainly by the articular surfaces of the apophyseal joints. Shear loading arises mainly from superincumbent body weight, and so tends to be greatest in the lower lumbar spine, where the discs are most inclined to the vertical. This may explain the relatively large size of the lower lumbar apophyseal joints. Lumbar apophyseal joints also resist axial rotation, and they couple axial rotation with lateral bending in a posture-dependent manner. Nevertheless, it is compressive loading that acts on the apophyseal joints for most of the time in upright posture, and which is applied to all spinal levels, and this is why compressive loading is the focus of the present study.

Previous studies have suggested that mechanical loading may underlie the development of degenerative joint disease in the lower spine, and the results presented here provide more detailed evidence which helps to explain how this occurs, at least in relatively elderly individuals. The loess curve in this figure presents a locally weighted regression, and at any particular point on the x axis it is determined only by the points in that vicinity. Figure 2 suggests that specimens in which less than 50% of the experimental compressive load was resisted by the apophyseal joints did not show a strong relationship between increasing load and increasing degeneration of the apophyseal joints. However, where the apophyseal joints resisted more than 50% of the compressive load, bone changes in the apophyseal joints were much more severe. This may imply that there is a compressive force threshold under which the apophyseal joints can accommodate the force transmission, but over which degeneration of cartilage and (especially) bone becomes more likely. There is experimental evidence that disc degeneration and narrowing can cause the apophyseal joints to transmit compressive load by extra-articular impingement between the bony tips of the inferior articular processes and the laminae below. Such load-transmission would largely by-pass the articular surfaces, and may explain why high neural arch loadbearing in the present study was marginally more closely associated with degenerative changes in the bone than cartilage. Another factor involved in the development of degenerative joint disease is age. Previous studies using a large number of specimens dispersed over a wide age range (19– 92years) showed that the compressive force resisted by the apophyseal joints increased significantly with age. However, there was a large variation in the force resisted by the apophyseal joints at any particular age (for example, at 79 years the force resisted varied between 20 and 65%). The lack of correlation between apophyseal joint loading and age found in the present study may be due to the narrower age range, combined with this variation in loading at any particular age. However, while age and load-bearing by the apophyseal joints are not significantly correlated, markers of joint degeneration such as cartilage loss and bone change clearly are. It is possible that, with advancing years, senescent chondrocytes are less likely to activate so that cartilage damage is more likely to accumulate, subsequently causing lesions and other changes in the underlying bone. Three categories of bone change— pitting, the presence of marginal osteophytes, and eburnation— appear to be particularly good predictors of this cartilage loss.

The results of the present study probably depend on the manner in which mechanical loading was applied to the cadaveric specimens. Each motion segment was creep-loaded to reduce disc water content and height by an amount similar to the normal diurnal variation seen in life, and this height loss is known to increase compressive load-bearing by the apophyseal joints. Also, specimens were tested in 28 of extension to simulate the erect standing posture in which the ‘‘normal’’ lordosis (i.e. the lordosis of an excised unloaded cadaveric lumbar spine) is slightly increased. In moderately flexed postures, the apophyseal joints resist very little compressive force, even when the discs are narrowed. In this way, the relationship between degenerative joint disease and spinal loading can be seen to depend on posture, and the time of day. Load-sharing in the spine is sensitive to small variations in posture and disc height: for example, just 28 of backwards bending of a motion segment increases stress concentrations within the intervertebral discs by 16%, reduces pressure in the nucleus pulposus by 10%, and approximately doubles load-bearing by the apophyseal joints.

The results of this present experiment suggest that degenerative joint disease in the apophyseal joints of the elderly human thoracolumbar spine can be strongly suggestive of biomechanical environment in life. Even the observation of mild degenerative joint disease in this region is a good indicator of cartilage loss on the articular surface, and therefore joint space narrowing, and increased interfacet forces. Observation of severe bone change in the spine of an archaeological skeleton of similar age at death to those included in this study may suggest that the apophyseal joints were bearing much of the compressive load on the vertebra, probably in a lordotic posture. This situation is known to arise when intervertebral disc degeneration is severe, and it is associated with a reduction in bone density in the anterior vertebral body, and high bone density in the apophyseal joints relative to the vertebral body. Other factors, such as variations in apophyseal joint morphology within and between spines may also be important. Together, these results indicate a change in vertebral function and show how bone (in particular) responds to a changing mechanical environment.

This study has demonstrated how pathological and biomechanical data can be combined to reveal new insights into a skeletal condition of interest to palaeopathology. This approach is relatively uncommon, as comparative cadaveric or clinical studies involving collaborative efforts across discipline boundaries may be difficult to establish. It is also the case that for some aspects of palaeopathological study clinical comparison may not hold the key to archaeological interpretation. For studies of degenerative joint disease, however, such an approach provides an essential grounding. Not only is the relationship between cartilage and bone change exposed, but also the experimental framework permits testing of specific biomechanical hypotheses related to human movement, posture, and activity widely discussed in more general terms. This may be of significance to the study of human remains from archaeological contexts in a number of ways. It provides support for the palaeopathological investigation of sex or age related differences in the participation of activities that involve significant compressive loading on the vertebrae, both within populations and between them. Similarly, there may also be implications for the assessment of vertebral pathology in extinct hominin populations. For example, degenerative changes have been observed on some of the Hadar australopithecine vertebrae, particularly in the thoracolumbar region. The relatively large size of the neural arch in australopithecines, coupled with the patterning of degenerative joint disease described, could be an indication that the apophyseal joints played a significant role in resisting compressive forces acting on the australopithecine thoracolumbar spine, which in turn suggests intervertebral disc degeneration or lordotic posture, or both. This possibility requires further investigation, but it is encouraging that while it may not be possible to isolate a particular behavior or activity that most stressed peoples’ bodies in life, the comparative, experimental approach presented here can nevertheless yield insights into human biomechanics in archaeological populations.

Previous work has shown that human apophyseal joints have a variable load-bearing function, which increases following degeneration and narrowing of the intervertebral discs, and in lordotic postures. The present study shows that in elderly individuals, when loadbearing exceeds 50% of the compressive force acting on the spine, then degenerative changes are to be expected in the apophyseal joints, particularly in the subchondral bone. This suggests that load transmission is largely extra-articular, between the tips of the inferior articular processes and the laminae. The variables describing bone change (pitting, marginal osteophytes, bony contour change and eburnation) are positively and significantly correlated with degree of cartilage loss, and therefore may be seen as good palaeopathological predictors of such soft tissue degeneration in elderly individuals.