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CHAPTER 3/BIOMECHANICAL CONSIDERATIONS OF DISC DEGENERATION / 33
is subjected. The comple x recruitment patterns of the lumbar musculature are not well established. Howeve r, biomechanical and neurophysiologic evidence suggests that the
deep intrinsic muscles are recruited to control motions at
the intervertebral level, whereas the long multisegmental
muscles may be involved in a more “global” control of the
overall spinal orientation (18–20).
The innervation pattens of the active and passi v e structures of the lumbar spine have, for the most part, been
determined. The load-sensitive nerve endings, or mechanoreceptors, found in muscle (muscle spindles) and
tendon (Golgi tendon organs), provide proprioceptive
information regarding tension levels, essential for controlling muscle tone. Although the presence of nerve endings in the passive structures has been well documented
(21–28), their role has not been clearly established.
Regarding the articular structures, the outer annulus of
the intervertebral disc and the capsules of the facet joints
contain both free nerve endings and mechanoreceptors.
These structures act as proprioceptive transducers for
monitoring the position and movements of the motion
segment. The neurologic feedback from these passive
structures provides sensory information needed to regulate muscle tension, and hence the mobility and stability
of the lumbar spine. In addition to a regulatory function,
the presence of a nerve supply in the articular structures
makes these structures potential sources of pain (22).
BIOCHEMICAL AND STRUCTURAL CHANGES
ASSOCIATED WITH DISC DEGENERATION
Disc degeneration is the deterioration and remodeling
of the physical and chemical properties of the tissue—
whole or in part—with retrogressive pathologic changes
in the cells or macromolecules (14). The changes observed in degenerated discs are similar to those found in
normal aging (29,30), but they are more pronounced with
disc degeneration, may occur earlier in life and with more
severe changes, and are often associated with clinical
symptoms (31).
The principal biochemical sign of disc degeneration and
aging is the loss in proteoglycans and hence loss of water,
particularly in the nucleus (11,30,32,33). Cells in the
nucleus change their shape and begin to synthesize collagen types not found in normal intervertebral discs (34).
Structurally, the nucleus pulposus becomes progressively
more fibrous and opaque, with increased pigmentation
(34–37). The demarcation between the annulus-nucleus
boundary becomes less distinct and delamination of the
mid-to-outer annulus occurs, particularly in the anterior
annulus (38,39) (Fig. 3-2). Delamination is believed to be
a precursor stage for the development of concentric tears in
the annulus fibrosus (40). Abnormalities can be found in
the ultrastructural features of the collagen fibrils of the
annulus fibrous (e.g., widened fibrils or irregular fibril
cross-sectional diameters) (41). Radial fissures and cracks
in the annulus fibrosus can for m cavities within the disc
(42). There can be inward buckling of the inner annulus as
well as increased radial bulging of the annulus (43,44).
Radiographically identifiable pathology associated with
disc degeneration includes disc space narrowing, osteophyte formation around the margins of the vertebral bodies, and sclerosis of the vertebral end plates (45,46).
For describing the degree of degeneration according
to morphologically observed changes, Nachemson (47)
created an integer grading scale ranging from 0 (no
macroscopic signs of degeneration) to 4 (severely
degenerated). This grading scheme or versions similar
to it are commonly referred to when classifying the
degeneration status of specimens used in biomechanical studies. Kirkaldy-Willis (48) described the process
of degeneration as having three sequential phases: (a)
an early phase of dysfunction, where the motion segment does not function normally but the pathologic
changes are minimal (grade 1); (b) instability, an intermediate phase where there is increased joint laxity
which may be exemplified as abnormal segmental
motion (grade 2); and (c) the restabilization phase characterized by fibrosis in the posterior joints and osteophyte formations, which lead to decreased segmental
motion (grades 3 and 4).
MECHANICAL FACTORS AS POSSIBLE
PATHOMECHANISMS OF DISC
DEGENERATION
There are several theories about the possible pathomechanisms of disc degeneration. Mechanical, chemical,
age-related, autoimmune, hereditary, and genetic factors
have all been implicated (49). Considerable attention
has focused on trying to understand the etiologic role
mechanical loading plays in disc degeneration. This partially stems from the fact that back pain is the leading
cause of disability among the working population (50).
There is an underlying belief that pathology leading to
back symptoms can result from mechanical factors that
damage spinal structures (51–53). Farfan et al. (16), for
example, postulated that intervertebral disc degeneration
results from imposed torsional strains that cause impairment in the function of the facet joints. Although there is
no clear dose-response relation between occupational
loading exposure and degenerative findings, physical
workload has been found to predict spinal injury in truck
drivers (54). Suspected occupational risk factors for back
pain include the following physical demands: heavy
physical loading; materials handling including lifting,
bending, twisting, pulling or pushing; prolonged static
postures; and whole body vibration (52,55–57). However ,
there are discrepancies in the literature regarding which
physical factors are associated with an increased prevalence of low back pain. Marras et al. (58) assessed the
contribution of dynamic trunk motions to the risk for low
34 /SECTION I/BASIC SCIENCE
A B
C D
FIG. 3-2. Comparative photographs of cross-sectional and sagittal views of a degenerated disc (A, B)
and the adjacent disc (C, D) from an experimental model (end-plate injury) of disc degeneration, showing gross morphologic changes in both the annulus and nucleus structures. (From Kawchuk GN, Kaigle
AM, Holm SH, et al.The diagnostic performance of vertebral displacement measurements derived from
ultrasonic indentation in an in vivo model of degenerative disc disease. Spine 2001;26:1348–1355, with
permission.)
back disorders during occupational lifting in industry . An
increase in the magnitude of the following w orkplace factors significantly increased the risk for low back disorders: lifting frequently, load movement, trunk lateral
velocity, trunk twisting velocity, and trunk sagittal angle.
There is evidence to suggest that occupational exposures
have an ef fect on disc degeneration, specifically with regard
to lumbar disc degeneration; however, the contribution of
such risk factors appears to be modest, particularly when
compared to familial influences (52). A critical review of
the literature was recently made by Hansson and Westerholm (59) to assess whether or not existing scientific evidence substantiates relationships between low back problems and the following different physical work exposures:
patient handling and care, lifting of patients, materials handling, heavy physical work, heavy lifting, bent or twisted
work positions, standing or walking, prolonged sitting, and
exposure to whole body vibration. The review re v ealed that
there is strong evidence of an association between an
increased occurrence of low back problems and frequent
heavy lifting (greater than 15 kg) and twisted or bent working positions, whereas frequent lifting of less than 10 kg
shows a strong negative association. Moderate evidence
supports an association between whole body vibration and
an increased occurrence of low back problems. Limited
evidence yields an association between patient handling
and care, patient lifting, and heavy physical work and an
increased occurrence of low back problems. There is currently insufficient evidence for an association between low
back pain and standing, walking, or prolonged sitting.
Loading effects on the lumbar spine during physically
demanding tasks are not only dependent on the load magnitude, but also the loading rate and history (60,61). This is
partly because the intervertebral disc and ligaments are
viscoelastic structures. The viscoelastic behavior has been
well documented for the intervertebral disc, both normal
CHAPTER 3/BIOMECHANICAL CONSIDERATIONS OF DISC DEGENERATION / 35
and degenerated (62–70). The outflow of tissue fluid and
the stretching of the collagen fibers of the annulus fibrosus
under loading cause approximately a 20% reduction in the
height and volume of the disc (71). Intradiscal pressure has
also been shown to decrease with creep loading (72). Such
reductions make the tissue more elastic (73), less resistant
to bending (60) and shear loading (74), and causes greater
axial loading on the facet joints (75). When loading is
removed, the disc imbibes fluid and recovers from the
deformation, although complete recovery requires a considerable amount of time. With repetitive physical tasks,
even at relatively low physiologic loads, the spinal structures may suffer from fatigue. Mechanical fatiguing can
make the disc, as well as other viscoelastic spinal structures (e.g., ligaments, tendons, and fascia) more vulnerable
to microdamage. Considering the very low repair capacity
of the mature intervertebral disc, accumulative structural
damage is believed to be an underlying cause of disc
degeneration and low back pain (76).
Trying to establish cause and effect in disc degeneration
is extremely difficult. In a degenerated disc, structural disruption is accompanied by cell-meditated changes in composition. It is not clear as to whether progressive biochemical changes in the disc alter its structural integrity, or
whether mechanical disturbances precipitate biochemical
changes in disc cell metabolism (77). Adams and Dolan
(76) described how structural failure may cause biologic
degeneration of tissues by a number of mechanisms: by
altering the mechanical environment of the cells, by inter-
fering with metabolite transport to and from the cells, or by
breaking down barriers and allowing an inflammatory or
even autoimmune reaction to occur. Biochemical observations by Pearce et al. (78) support the hypothesis that low
proteoglycan concentrations in all the discs of a spine precede degeneration.
EXPERIMENTAL MODELS OF DISC
DEGENERATION
In order to perform controlled investigations of the
etiology and progression of disc degeneration, animal
models are often used. Experimental models have the
advantage of allowing standardized evaluations of biomechanical, histochemical, and morphologic phenomena
of the degenerative process, directl y from initiation of the
process. There are several different ways in which experimental disc degeneration can be induced in vivo, either
chemically or mechanically. Injection of a matrix-degrading enzyme (e.g., chymopapain), into the disc can produce degenerative changes (79). A number of investigators have mechanically produced degeneration in vivo in
rat and mice tail discs chronically loaded with an external
compression device (80–82). Disc degeneration as a
result of torsional injuries has been demonstrated in vivo
in rabbit models (83,84). A scalpel stab incision into the
annulus fibrosus, with or without penetration into the
nucleus pulposus (Fig. 3-3), is a technique that has frequently been used to mechanically induce disc degenera-
A B
FIG. 3-3. Comparative photographs (sagittal view)
of motion segments from mechanically induced
porcine disc degeneration models showing the morphologic changes: (A) no intervention, (B) 3
months’ postscalpel stab incision into the annulus
fibrosus, and (C) 3 months’postscalpel stab incision
into the annulus fibrosus with penetration into the
nucleus pulposus. (From Kaigle AM, Holm SH,
Hansson TH. Kinematic behavior of the porcine
lumbar spine: a chronic lesion model. Spine 1997;
22:2796–2806, with permission.)
C
36 /SECTION I/BASIC SCIENCE
tion (85–94). In rabbit, sheep and pig, this model has
been shown to cause pro gressiv e de generation which biochemically and structurally resembles that in human disc
degeneration. A new injury model, involving penetration
of the end plate via the vertebral body, has been shown to
produce symmetrically widespread degenerative changes
in the disc that resemble human disc degeneration (i.e.,
declines in concentrations of water, cells, and proteoglycans as well as intradiscal pressure) (38). This is a model
in which the severity of the degenerative changes can
vary according to the penetration diameter or depth
(38,95). Loss in hydrostatic pressure in the nucleus and
disruption of nutritional pathways through the end plate
are believed to be tw o k e y mechanisms behind this model
of disc degeneration. Deficient metabolite transpor t has
been linked with degenerative changes (96). This model
mimics human degeneration caused by end-plate fractures or nucleus herniation through the end plate.
BIOMECHANICAL CONSEQUENCES OF DISC
DEGENERATION
In everyday life, the structures of the lumbar spine are
continuously subjected to pure as well as combined
physiologic loads (e.g., compressive, tensile, shear, torsional, and combinations thereof). Disc degeneration
affects both the geometry and material properties of the
motion segment. While geometric changes can be
expected to decrease flexibility, changes in material
properties may cause the opposite response. The extent
to which each of these factors affects the spinal behavior
is also dependent on the direction of loading. For these
reasons, along with the fact that the intervertebral disc is
an anisotropic structure, it is necessary to perform biomechanical testing which includes both simple and complex loading modes.
For several decades, numerous studies have been performed in order to assess how the biomechanical properties of the lumbar spine are affected by intervertebral
disc degeneration. Accurate knowledge of the intervertebral disc’s biomechanical properties in healthy,
injured, or diseased states is essential for performing
valid mathematical analyses of the intervertebral disc,
for refining injur y (failure) criteria, and for developing
artif icial disc replacements, as a few examples. Studies
have used various methodologies in order to quantify
the physical properties—elastic and viscoelastic—as
well as the kinematic behavior. Since the degenerative
status can be determined, the majority of studies of
intervertebral disc degeneration are conducted using
cadaveric material (isolated discs, motion segments,
or whole lumbar spines) or in vivo animal models.
Methodologies for performing such analyses have primarily employed servohydraulic-type material testing
devices or used similar techniques that can measure the
load-displacement behavior.
Elastic Behavior
With regard to biomechanical testing, axial compression has been a popular test mode for studying the intervertebral disc, perhaps due to physiologic as well as practical considerations; namely that the disc is a major
compression-carrying str ucture in the spine (97) and that
compression testing is a relatively straightforward experimental test mode that can provide considerable information about the disc’s physical properties. Early biomechanical studies from the 1950s by Brown et al. (98) and
Hirsch et al. (99–101) described the nonlinear mechanical characteristics of in vitro lumbar motion segments
under axial compression, as well as other test conditions.
Studies such as these were motivated by the fact that disc
degeneration was viewed as a possible pathologic anatomical explanation for low back pain, and although no
pain mechanisms were identifiable at the time, the importance of mechanical factors was strongly recognized.
Hirsch and Nachemson (101) demonstrated differences in
the mechanical behavior between cadaveric motion segments with normal and degenerated discs, noting that for
the same applied axial load, degenerated discs deformed
more easily than healthy discs, particularly at higher
loads. Nachemson et al. (102) reported differences in
stiffness between less degenerated discs [grades 0 to 2 on
a total 5-point scale of 0 (normal) to 4] and grossly
degenerated discs (grades 3 and 4) that were dependent
on the loading configuration. In axial compression, less
degenerated discs were stiffer than grossly degenerated
discs. However, in flexion and extension modes, more
degenerated discs were found to be less flexible, while in
lateral bending and torsion, there were no significant differences. Fibrosis in the posterior joints of the grossly
degenerated discs may explain the observed increase in
stiffness in the flexion and extension loading modes
observed in the degenerated discs. Keller et al. (68) also
reported a decrease in axial compressive stiffness with
increasing grades of degeneration [1 to 3 on a total 4point scale of 1 (normal) to 4]. In a recent in vitro study,
Brown et al. (103) examined lumbar motion segment
stiffness under flexion-traction loading. A nonlinear
trend, which coincided with the degenerative process
described by Kirkaldy-Willis (48), dysfunction-instability-restabilization, was observed between motion segment stiffness and degeneration grade; reduced stiffness
was found in discs with early stages of degeneration
whereas discs with more severe degenerative changes
showed a tendency toward increased stiffness.
Viscoelastic Behavior
Using static and dynamic axial compression test
modes, it has been shown that degeneration alters the viscoelastic (time-dependent) behavior of the intervertebral
disc. Virgin (70) was the first to demonstrate that the hys-
CHAPTER 3/BIOMECHANICAL CONSIDERATIONS OF DISC DEGENERATION / 37
teresis behavior was greater in discs that showed actual
signs of degeneration than in middle-aged or older discs
that did not show an y degenerati ve signs. This means that,
in the degenerate state, there is greater energy loss during
loading-unloading cycles, which can be of considerable
importance with regard to repetitive axial vibration.
Koeller et al. (69) studied the effects of age and degeneration on the creep response of the intervertebral disc
under dynamic axial compression. From the middle of
the third to the beginning of the sixth decade, only slight
alterations in the biomechanical properties were found,
whereas later in life, where there was a greater occurrence of disc degeneration, increased creep was observed
in the lumbar spine. Kazarian (65) performed static axial
compression tests on older cadaveric lumbar motion segments with various degrees of degeneration. The creep
behavior was found to correlate with the degree of degeneration; the degenerate discs exhibited greater initial
deformation and approached equilibrium at a more rapid
rate compared with the nondegenerate discs. Similar
behavior has been confirmed by Keller et al. (68).
Internal Disc Mechanics
With the intervertebral disc being an inhomogeneous
structure, there are regional material property differences, particularly in the annulus fibrosus, which reflect
the variations in structural and biochemical composition. Such regional properties will affect the manner in
which the intervertebral disc responds to loading and
must be taken into consideration when performing analytical representations. Brown et al. (98) were perhaps
the first g roup to map the regional tensile strengths of
the intervertebral disc. Rectangular vertebra-disc-vertebra sections from different locations of the disc were
axially stretched to failure. In this normal material, the
strongest areas were found to be in the anterior and posterior portions of the disc, while the central portion was
the weakest.
More recent studies of the radial and circumferential
variations in the tensile properties of nondegenerate lumbar disc specimens have reported that, when loaded along
the plane of the lamella, the anterior annulus is stiffer and
stronger than the posterolateral regions, and the outer
annulus is stiffer and stronger than the inner regions
(10,104). Ebara et al. (104) speculated as to how load distribution would benefit from a lower tensile modulus in
the inner annulus fibrosus. They stated that the lower values for the tensile modulus and the larger values for strain
suggest that the inner annulus fibrosus is likely to be
more deformable, and thus be more successful at distributing applied loads in a uniform manner across the inner
annulus fibrosus, as compared to the more restrictive
outer annulus. Therefore, the more deformable inner
annulus fibrosus may provide for significant energy dissipation within the tissue. Acaroglu et al. (105), using
multiple-layer annulus specimens, evaluated the effects
of aging and degeneration on the regional tensile properties when loaded along the plane of the lamellae. Degeneration was found to be accompanied by significant
decreases in the failure properties (i.e., failure stress and
strain energy density), indicating that degenerated annulus fibrosus will fail at lower stresses and require less
energy to fail. Also, a significant decrease in the Poisson
ratio, which is a ratio of the transverse and axial strains in
the tissue, was found. This indicates structural changes in
the annulus lamellae, which will affect the internal
stresses in the disc and thus the overall manner in which
the disc bears loads. Fujita et al. (106) studied in vitro the
radial tensile properties of normal and degenerated lumbar annulus fibrosus, when loading per pendicular to the
plane of the lamellae. The radial tensile behavior of the
annulus was highly nonlinear and showed region-dependent behavior that was likely due to radial variations in
interlaminar weaving. Compared to specimens from both
the inner and outer annulus of normal discs, specimens
from the middle layers were stiffer and failed at smaller
strain magnitudes with radial tensile loading. Differences
due to degeneration were noted; moderately degenerated
discs showed a 30% decrease in yield and ultimate stress
compared with normal discs.
Umehara et al. (107) studied variations in the disc’s
axial compressive properties as a function of location in
the disc and degeneration. Using an indentation technique on whole disc specimens, the axial compressive
elastic modulus was assessed in lumbar discs with various degrees of degeneration. In normal discs, the elastic
moduli were lowest in the nucleus as well as the lateral
portions of the annulus, whereas the values were significantly greater in the posterior and anterior annulus, being
greatest in the anterior portion. This normal distribution
pattern, which correlated with the distributions of tensile
strengths reported in earlier studies, was affected by disc
degeneration. In normal discs, the distribution was symmetrical about the midsagittal plane, whereas the more
severely degenerated discs showed asymmetrical and
irregular profiles and higher nucleus moduli. In the
slightly degenerated discs, the lowest values of the elastic
moduli were found in the posterolateral portions of the
disc, which is also the region where disc disruption is
clinically found to occur most frequently (108). Farfan et
al. (16) found that the location of maximum stress under
torsional loading was at the posterolateral angles of the
intervertebral disc, again coinciding with the common
site of clinical disc protrusion.
Annular lesions of the radial, circumferential, or rimlesion type compromise the disc’s internal mechanical
integrity. Such lesions appear to evolve independent of
age or each other (40), and may be the result of fatigue
failure or part of a degeneration process. A study has
examined how the type and severity of such lesions in
lumbar intervertebral discs alter the biomechanical prop-
38 /SECTION I/BASIC SCIENCE
erties (109). Flexion-extension stiffness increased with
greater tear severity, which was believed to be partly due
to the accompanied loss in disc height. Increasing severity of circumferential tears and rim lesions correlated
with decreasing joint axial torsional stiffness. With a circumferential tear, interlamellar bonding is absent in a
portion of the annulus; thus the disc’s ability to transfer
shear forces induced by torsional loading is reduced. It
has been suggested that interlaminar separation and
matrix failure between the lamellae might be a more clinically relevant injury mechanism than tensile failure of
the collagen fibers within a lamella (106). It is believed
that with loss of cohesion between the annulus lamellae,
other structures of the motion segment, particularly the
facet joints, have to provide a greater portion of torsional
resistance, and that this could play a major role in early
degenerative changes (16). With a rim lesion, there is a
defect in the annulus attachment close to the bone of the
vertebral rim, which compromises the transferring of torsional loads across the motion segment. Thompson et al.
(109) reported that radial tears showed little or no effect
on the axial torsional stiffness. Schmidt et al. (110) compared the stiffness (flexion-extension, axial rotation, lateral bending) in cadaveric motion segments with and
without high intensity zones (i.e., radial tears, in the
annulus fibrosus viewed on magnetic resonance images).
In this study, the presence of a radial tear was associated
with a significant reduction in stiffness in the motion segment in axial rotation.
A direct means for measuring loading on the spine is
with intradiscal pressure measurement techniques. In a
healthy disc, the pressurized gelatinous nucleus pulposus
acts as a hydraulic cushion that generates tensile stresses
in the annulus, permitting applied loads and pressures to
be evenly distributed over multiple spinal segments. The
lamellae of the annulus fibrosus are believed to primarily
bulge radially outward due to the hydrostatic pressure
in the nucleus. However, with aging and degenerative
processes, the reduction in water content and increased
fibrosis in the nucleus result in reduced hydrostatic
behavior, and there are structural disruptions in the annulus lamellae and end-plate regions. In degenerated discs,
there have been reported observations of inward bulging
of the inner lamellae (43,44,77), and that such bulging is
associated with pressure loss in the nucleus (81). Under
loading, such changes alter the internal disc mechanics,
producing high stress concentrations that may cause pain
or even further disc disruption. Since the nucleus of a
severely degenerated disc does not always exhibit hydrostatic behavior, discometric studies of such material must
be interpreted with caution.
In a number of pioneering in vivo human studies,
Nachemson et al. (111–116) measured intradiscal pressure in lumbar intervertebral discs during various activities. From these and the later studies by Andersson et
al. (117,118) and Schultz et al. (119), intradiscal pres-
sure measurements, electromyo graphic data, and biomechanical modeling have altogether provided vital information that has been used to establish workplace recommendations as well as clinical treatment strategies
for disc diseases. Recent in vivo investigation (120,121)
using modern pressure transducer technology has substantiated the findings of the intradiscal pressure studies
from the 1960s and 1970s. In a healthy male volunteer,
Wilke et al. (121) measured the intradiscal pressure
in the L4-L5 disc and found good correlation with
Nachemson’s data, with two exceptions. First, intradiscal pressure was found to be lower in relaxed sitting
than in relaxed standing, and second, the pressures
while lying supine and lying on the side were essentially
the same, whereas Nachemson found a threefold pressure increase in side lying. Ho w ever, in a larger group of
subjects (8 healthy volunteers and 28 patients with low
back pain), Sato et al. (120) measured L4-L5 intradiscal
pressures during various postures that corroborated the
earlier findings of Nachemson et al.
Several investigators have examined how the internal
disc mechanics are altered by disc degeneration. In
moderately degenerated human discs, the intradiscal
pressure has been shown to be approximately 30% less
than in nondegenerate discs (111,114). Using an in vivo
porcine model, Ekström et al. (122,123) and Holm et al.
(38) measured the intradiscal pressure in normal lumbar
discs and discs with experimentally induced degeneration, as well as the disc adjacent to the degenerated
level. The intradiscal pressure in the disc adjacent to the
degenerated level, which did not show morphologic
signs of degeneration, was found to be slightly higher
than in normal discs. This increase can be expected due
to the redistribution in mobility demands and alignment
of the segments adjacent to those with increased stiffness (i.e., degenerated or fused) (124). Intradiscal pressure has been shown to be highly dependent on the
angle of the motion segment (120). Similar to the in
vivo human studies discussed previously, the intradiscal
pressure in the degenerated disc was significantly lower
(more than 50%) compared to the pressures in the adjacent and normal discs. Sato et al. (120) reported a progressive decline in intradiscal pressure with increasing
disc degeneration grade. Using stress profilometry,
age-related degenerative changes in cadaveric lumbar
motion segments have been shown to reduce the sagittal
diameter of the central hydrostatic region (nucleus and
inner annulus) of the disc by approximatel y 50% and the
pressure by 30%, and increase the width of the “functional” annulus by 80% (125) (Fig. 3-4). Structural disruptions, such as radial f issures or fractures in the end
plate, increase the space available to nucleus material,
thus reducing the central intradiscal pressure (77).
Stress profilometry has shown that compressive stresses
are transferred from the nucleus to the annulus, particularly the posterior region where increases in peak
CHAPTER 3/BIOMECHANICAL CONSIDERATIONS OF DISC DEGENERATION / 39
stresses by 160% have been reported (125). Similar
effects in the stress redistribution (i.e., reduced nucleus
pressure and increased peak compressive stresses in the
posterior annulus) have been observed with sustained
(creep) loading (72).
Spinal Kinematics
Several biomechanical investigations, both in vitro
and in vivo, have looked at the effects of disc degenera-
tion on spinal kinematics. Mimura et al. (126) performed a comprehensive investigation into the relationship between multidirectional flexibility of whole
cadaveric lumbar spines and disc de generation. Fle xionextension, lateral bending, and axial rotation pure mov ements were applied and the motion parameters used to
describe the nonlinear spinal behavior were neutral
zone, range of motion, and neutral zone ratio. The neutral zone is an absolute measure of the joint laxity
around the neutral position, where little resistance is
offered by the passive spinal column (127). In an in
vitro study, the neutral zone has been shown to increase
with disc degeneration, particularly in axial rotation and
anteroposterior shear motions, and is considered to be a
more sensitive parameter than range of motion in relating to disc degeneration (128). The neutral zone ratio, a
quotient of the neutral zone and the range of motion,
increases in value with greater joint laxity. In the presence of increasing disc degeneration, Mimura et al.
(126) reported an increase in intervertebral joint laxity
around the neutral position, believed to be due to lax
collagenous tissues, as demonstrated by an increase in
the neutral zone ratio for all three types of loading
modes. With regard to range of motion, a significant
decrease in lateral bending was found, perhaps resulting
from facet hypertrophy. Tendencies toward decreased
flexion-extension and increased axial rotation ranges of
motion were observed. In a clinical study, a reduction in
disc height was found to be significantly associated
with reduced flexion-extension range of motion (129).
The finding of an increase in axial rotation with higher
degrees of disc degeneration has been corroborated in
other studies (128,130–132), presumably due to fissure
formations in the annulus fibrosus and a reduction in
disc height. While segmental motion has been shown to
increase with increasing severity of degeneration, a
decrease has been found at the highest grade of degeneration (126,131). This is in accordance with the final
phase of degeneration, as reported by Kirkaldy-Willis
(48), where there is a restabilization due to osteochondrotic changes.
Using an in vivo porcine model, Kaigle et al. (133)
studied dynamically the alterations in segmental kinematics during flexion-extension as a result of acute
interventions to the passive stabilizing components of
the lumbar spine and to the musculature. Acute injury to
the intervertebral disc resulted in greater axial joint laxity during flexion-extension maneuvers, while acute
injury to the facet joints caused greater segmental sagittal plane rotation. A facetectomy resulted in considerable destabilization of the motion segment, particularly
in the neutral region, where erratic behavior was exhibited during flexion-extension. Although increasing the
flexion-extension range of motion, activation of the
lumbar paraspinal muscles was shown to have a stabilizing effect on the segmental patterns of motion in the
FIG. 3-4. Stress profiles (posterior-anterior). Left: Grade 1 disc, female, 27 years old, L1-L2. Right:
Grade 4 disc, female, 82 years old, L4-L5. (Redrawn from Adams MA, McNally DS, Dolan P. Stress distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br
1996;78:965–972, with permission.)
40 /SECTION I/BASIC SCIENCE
acutely injured porcine motion segment by reducing the
abrupt kinematic behavior in the neutral region. Similar
findings were reported in an in vitro study by Panjabi et
al. (134), where it was demonstrated that the application
of simulated intersegmental muscle forces maintained
or decreased intervertebral motions (i.e., maintained or
decreased neutral zone) for intact and injured motion
segments, except the range of motion in flexion which
increased with muscle force. In a chronic lesion model,
however, the musculature was overall less efficient at
providing stability when the interver tebral disc or facet
joints were degenerated (87). This may have been due to
altered mechanisms in the neuromuscular feedback system in the degenerated motion segments and consequently, the lumbar spine as a whole.
In the clinical situation, there are some important
aspects to consider regarding increased joint laxity.
Daily activities involve movements across the neutral
position (e.g., right-to-left lateral bending, forward flexion to extension, etc.). This transition requires wellcoordinated activation/deactivation of various different
muscles. With increased joint laxity, there may be insufficient tension in the spinal ligaments and annulus
fibers, both of which are known to contain nerve endings that allow them to act as proprioceptive transducers. Lack of sufficient tension may delay or even prevent the detection and delivery of sensory information
needed to regulate muscle tension. Stability becomes
compromised when the recruitment of the appropriate
sequence of muscles needed to overcome the loading
demands is too slow, too late, or insuff icient.
In a clinical study, in vivo segmental motion, overall
trunk bending, and myoelectric activity of the lumbar
erector spinae muscles were continuously measured
during flexion-extension maneuvers in patients with
suspected degenerative instability and in healthy volunteers (135). Segmental motion as well as trunk mobility
was significantly less in the patients during flexionextension. Reduced range of motion on functional radiographs has previously been found in patients with low
back pain and degenerative changes in the lumbar spine
(136–138). The patterns of motion in flexion were also
significantly different from the controls. Using videofluoroscopy, Okawa et al. (139) found that, compared to
a control group, patients with lumbar degenerative
spondylolisthesis showed disordered patterns of motion
in forward flexion and a tendency toward smaller ranges
of motion, however, the degree of disc degeneration
alone did not correlate with the disordered motion
patterns. In contrast, in patients with degenerative disorders in the lumbar spine, it has been reported that
anterior translatory instability as measured on flexionextension radiographs is positively associated with disc
degeneration and facet joint osteoarthritis, while other
forms of sagittal plane instability (rotatory, posterior)
have shown no association (140).
In a clinical study, McGregor et al. (141) were unable
to find a relationship between degenerative disc disease
as seen on plain lateral radiographs and the overall lumbar range of motion. Altogether, the findings suggest
that degenerative changes in the lumbar spine and the
accompanying aberrant kinematic behavior are associated with alterations in the neuromuscular system. Analyzing the muscular behavior during flexion-extension,
Kaigle et al. (135) found that flexion relaxation (i.e.,
decreased myoelectric activity with extreme trunk flexion) was demonstrated in healthy volunteers but not in
the group of chronic low back pain patients with suspected degenerative instability (Fig. 3-5). The restricted
segmental mobility found in these patients was believed
to be due to the persistent activation of the musculature.
It is conceivable that the activated muscles behaved
more as stabilizers rather than mobilizers, compensating
for the laxity in the diseased motion segment. Such activation would also allow loads to be transferred via the
muscles instead of the diseased passive structures, perhaps as a means for avoiding pain. Pain is one factor
that has been shown to inhibit flexion relaxation
(142,143). Ahern et al. (144) showed that pain behavior,
particularly guarded movement, was significantly
related to flexion relaxation. Wolf et al. (145) suggested
that chronic low back pain patients develop postural
abnormalities, such as guarded movement and splinting,
in order to compensate for actual or anticipated pain,
and that over time, these postural adjustments could
alter the normal neuromuscular function.
CONCLUDING REMARKS
The behavior of the lumbar spine is dependent upon
the characteristics of its passive, active, and neural subsystems, any of which can become injured or diseased,
and all of which undergo the aging process. The neuromuscular system controls the movements and stability in
the lumbar spine and can compensate, to a certain degree,
for loss in function of one or more of the structures. As
conceptually described by P anjabi (1), dysfunction in any
of the subsystems may lead to one or more of the following responses in the other subsystems: (a) an immediate,
compensatory response, which would result in normal
function; (b) a long-term adaptation response, which
would result in normal function but with an altered spinal
stabilizing system; and (c) an injury which would lead to
overall system dysfunction, producing, for example, low
back pain.
Numerous investigations have demonstrated that disc
degeneration alters the biomechanical behavior of the
lumbar spine in a number of ways. However, discrepancies in the literature exist regarding the exact manner in
which a disc’s biomechanical properties are affected by
degeneration. Although grouping of in vitro disc specimens according to degeneration grade facilitates compar-
CHAPTER 3/BIOMECHANICAL CONSIDERATIONS OF DISC DEGENERATION / 41
FIG. 3-5. Segmental kinematic (sagittal rotation) and myoelectric [right-side erector spinae surface
Root Mean Square electromyography (RMS EMG)] experimental data as a function of the overall trunk
flexion-extension angle during a flexion-extension cycle from the L4-L5 motion segment of a control
subject (top) and a patient with degenerative instability (bottom).Note the absence of flexion-relaxation
in patient myoelectric data.
isons, averaging results in groups of motion segments
with diverse degenerative changes may obscure the
effects of degeneration on the biomechanical response.
This may be a factor contributing to the disparities
reported in the literature. Additionally, it has also been
pointed out by Vernon-Rober ts et al. (40) that to properly
classify disc disease, it is essential to examine disc slices
at multiple levels within a disc since abnormalities are
three-dimensionally complex. However, very few studies
have reported employing such procedures. It should also
be noted that the majority of in vitro studies have been
performed on lumbar motion segments obtained from
cadaveric specimens be yond the sixth decade in age, suggesting that the degenerative changes were age-related.
Although biochemical and biomechanical changes due to
normal aging are similar to those found in degeneration,
it would be more appropriate to perform biomechanical
studies on degenerate discs from specimens in the middle
decades of life, which is the time in life where there is a
maximal incidence of disc-related back problems (146).
Since disc degeneration is a process, the biomechanical properties will undergo changes throughout this
process. An observed increase in flexion-extension stiffness, for example, during one stage of the degenerative
process may not necessarily be present at a later point in
time. Even at a similar point in time, while changes in
the material properties may increase the flexibility of the
motion segment, geometric changes may produce an
opposite affect, thus producing no net effect on the overall behavior. Clinically, patients suspected of having
degenerative se gmental instability display vertebral misalignment on functional radiographs, accompanied by
42 /SECTION I/BASIC SCIENCE
morphologic changes in the intervertebral disc, vertebrae, and possibly facet joints. However, clinical studies
as a whole have been unable to demonstrate segmental
hypermobility (i.e., greater range of motion), which correlates with the pathologic signs and symptoms. On the
contrary, the majority of studies have found hypomobility in the suspected ‘unstable’ motion segment. This
raises an important issue regarding the ability of the
neuromuscular feedback system to compensate for joint
laxity or abnormal movements in a lumbar motion segment. To better understand the mechanisms by which the
passive, active, and neural structures interact, refer to
Chapter 11.
In summary, the overall findings reported in the literature indicate that with disc degeneration, the biochemical and structural changes compromise the disc’s structural integrity, regionally and subsequently as a whole.
The effects of disc degeneration on the motion segment
stiffness are a function of the loading mode. When
loaded in axial compression or torsion, degenerated
discs display a reduction in stiffness, whereas in flexionextension and lateral bending, a stiffening effect has
generally been found. Disc degeneration alters the normal stress distribution patterns. The failure properties of
the annulus lamellae are reduced along with the intradiscal pressure in the nucleus. This produces high stress
concentrations in the posterior annulus, the region where
disc disruption is clinically found to occur most frequently. Such alterations in the internal disc mechanics
may cause pain or precipitate further disc disruption.
Degenerative changes in the lumbar spine cause aberrant
kinematic behavior, particularly around the neutral position. Although increased intervertebral laxity around the
neutral position has been associated with disc degeneration, the majority of in vivo studies have found reduced
ranges of motion. Persistent muscle activation is believed to be a mechanism by which the neuromuscular
system provides stabilization in order to guard diseased
passive structures from abnormal motion, which may
cause pain or further tissue damage.
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