Age-Related Changes in the Spine


The spines of older individuals have both the changes of normal aging and the changes of “degeneration.” In the absence of accepted criteria to distinguish aging and degeneration, the features that characterize the majority of individuals at a specified age can be taken to represent normal aging rather than degeneration. The anatomic, chemical, and imaging features of the aging spine are discussed here, and the degenerative changes of the spine are reviewed elsewhere (see Chapter 7 ).

ANATOMY AND FUNCTIONAL ANATOMY OF THE INTERVERTEBRAL DISC

Specialized connective tissues give the intervertebral disc its biomechanical properties. For the purposes of description, the intervertebral disc can be divided into three components: outer annulus fibrosus, inner annulus fibrosus, and nucleus pulposus ( Fig. 6-1 ). The outer annulus fibrosus has thick lamellae of dense connective tissue, containing predominantly collagen. The inner annulus has cartilaginous matrix associated with the collagenous fibers. The nucleus pulposus has predominantly cartilagenous matrix with less structure than the annulus fibrosus.

FIGURE 6-1, Sagittal ( A) and axial ( B ) anatomic sections of a lumbar intervertebral disc. In the sagittal section, notice the well-defined, faintly colored lamellae in the peripheral annulus, especially in the anterior portion of the disc (to reader's left). The lamellae become less and less well defined toward the interior of the disc where the inner annulus fibrosus is located. The central portion of the disc has an amorphous tissue, the nucleus pulposus. In the central portion of the nucleus pulposus, some fibrous structure is evident. The pigments that give the nucleus pulposus a darker color are aging changes.

The outer annulus consists of multiple layers (lamellae), each containing dense collagenous fibers. Histologically it resembles tendinous structures such as the Achilles tendon. In each layer (lamella) of the annulus fibrosus, the fibers run parallel to each other at an angle of 60 degrees with respect to the vertebral end plate. These fibers originate and insert in bone, as do Sharpey's fibers in the anterior longitudinal ligament. The high concentration of collagen in the outer annulus fibrosus results in its low signal intensity on T1- and T2-weighted images ( Fig. 6-2 ). In successive lamellae the fibers alternate directions ( Fig. 6-3 ). These inelastic fibers running obliquely in the periphery of the disc resist axial rotatory torques but permit flexion and extension and lateral bending. The predominant cell type in the outer annulus fibrosus is the fibroblast, as its predominant constituent is collagen.

FIGURE 6-2, Sagittal anatomic and T2-weighted MR images of a cadaveric lumbar spine to illustrate the MR appearance of outer annulus, inner annulus, and nucleus pulposus. The most anterior portion of the disc, consisting of inner annulus fibrosus and nucleus pulposus, has a lamellated structure, which has low signal intensity on the MR image. The region in the nucleus with higher fiber content appears also as a horizontal band of low signal intensity, the central low signal intensity region of the disc.

FIGURE 6-3, Sketch showing the orientation of collagen fibers in the lamellae in the outer annulus fibrosus. In the most superficial layer the fibers are oriented at 60 degrees with respect to the adjacent end plate. This lamella has been delaminated from the disc to show the next adjacent lamella, which has fibers running also oriented 60 degrees with respect to the end plate, but alternating in direction with the outer lamella.

The inner annulus contains less well defined lamellae, together with collagenous matrix. Like the lamellae in the outer annulus, those in the inner annulus run obliquely. They insert and originate not in bone but in the thin layer of hyaline cartilage that covers the entire surface of each vertebral end plate except the ring apophysis. The transitions from outer annulus to inner annulus and from inner annulus to nucleus pulposus are indistinct. The glycosaminoglycans and water in the matrix give the inner annulus a higher T2 signal intensity than the outer annulus. The inner annulus contains fibroblasts and chondrocytes.

The nucleus pulposus also contains glycosaminoglycans, collagen, and chondrocytes, like the inner annulus fibrosus, but the structure of the nucleus pulposus is more amorphous and the fiber structure is less plentiful. The nucleus fibrosus has high signal intensity on T2-weighted images, reflecting the glycosaminoglycans and water content. A central region in the nucleus pulposus contains collagen, elastin, and reticulin fibers oriented horizontally ( Fig. 6-4 ). The fiber content of this region results in a lower signal intensity, visible on sagittal MR images of the lumbar and thoracic spine.

FIGURE 6-4, Sagittal anatomic ( A ), MR ( B ), desiccated slice ( C ), and H&E-stained section ( D ) of a lumbar disc. The desiccated section shows the fibrous content of the disc, which is most apparent in the peripheral annulus, but also in the central nucleus pulposus. The stained section shows fibrous tissue ( staining blue ) prominent in the annulus fibrosus and the central nucleus pulposus. Matrix in the nucleus pulposus and inner annulus fibrosus stains pink.

The anterior longitudinal ligament and posterior longitudinal ligament have close anatomic relationships to the disc. The anterior longitudinal ligament, containing predominantly collagen and contacting the anterior and lateral surfaces of the disc, cannot be distinguished in MR images from the outer annulus fibrosus ( Fig. 6-5 ). The posterior longitudinal ligament, which fuses to the posterior intervertebral disc margin, cannot be distinguished from the disc although it is a distinct structure posterior to the epidural venous plexus between intervertebral discs ( Fig. 6-6 ). Containing predominantly collagen, it is not distinguished from the disc on MR.

FIGURE 6-5, Axial MR image ( left ) and anatomic section ( right ) of a lumbar disc show the low signal intensity in the periphery of the disc (D). The anterior longitudinal ligament along the anterior and lateral surfaces of the disc cannot be distinguished.

FIGURE 6-6, Anatomic section in coronal plane through the spine along the posterior margin of the intervertebral disc. The section shows fibers in the posterior longitudinal ligament running horizontally along the posterior margin of the disc. The posterior longitudinal ligament runs superiorly and inferiorly out of the plane of section, where it lies posterior to the basivertebral veins, visible as the blood-containing structures above and below the disc.

The intervertebral disc has several thousand cells in each cubic milliliter ( Fig. 6-7 ). These cells produce collagen and glycosaminoglycan precursors. Due to the slow degradation of collagen and glycosaminoglycans in the disc, collagen and glycosaminoglycans are renewed approximately every 180 days by molecules synthesized within the disc.

FIGURE 6-7, Histologic section through the nucleus pulposus illustrating the plentiful chondroid matrix ( staining pink ) containing numerous chondrocytes, which appear as elliptical structures containing dark dots.

The cells in the intervertebral disc receive their nutrition via diffusion because the intervertebral disc has no arteries or capillaries, except in the fetus. Oxygen, glucose, sulfates, and other nutrients diffuse into the disc through the vertebral end plates and to a lesser extent through the outer annulus fibrosus, and carbon dioxide and other waste products diffuse out. Diffusion into the intervertebral disc can be measured as an increase in signal intensity in the disc after the intravenous administration of a paramagnetic contrast medium. Reduced diffusion into the intervertebral disc may contribute to disc degeneration by impeding the normal synthetic processes in the cell population of the disc.

The intervertebral disc is normally classified as nonenhancing. Disc fragments herniated into the spinal canal are usually observed to have no enhancement, in contrast to scar tissue, which does enhance. However, increase in signal intensity in normal discs can be detected after administration of contrast medium. Images obtained 40 minutes after intravenous contrast administration may have visible contrast enhancement, especially near the periphery ( Fig. 6-8 ).

FIGURE 6-8, Sagittal MR images of a dog spine before ( left ) and 40 minutes after ( right ) intravenous contrast medium injection, illustrating enhancement in normal intervertebral discs.

The intervertebral discs convey flexibility to the spine. Flexion and extension and lateral bending of the spine are possible mainly because of the flexibility of discs. In response to axial rotatory torques, the spine permits little rotation because of the oblique fibers in the annulus fibrosus. Properties of the disc also explain the diurnal variation in the height of the spinal column. When the human body is in the recumbent position, axial forces on the disc are minimized and as a result the disc absorbs additional water. With the body in upright position, the water is forced out of the disc, resulting in a loss of up to an inch of height in the spine.

The intervertebral disc does not have innervation. The anterior longitudinal ligament contains nerve endings. Nerve endings may be identified in the disc tissue immediately adjacent to the ligament but not more deeply in the disc. Therefore, the disc does not normally give rise to painful stimuli.

Disc morphology varies between the cervical, thoracic, and lumbar segments of the spine. The discs between the C2 through C7 vertebrae extend laterally between the uncinate process on the vertebra below and the demi-facet or echancrure on the vertebra above ( Fig. 6-9 ). This region is called the “uncovertebral joint” although it contains fibrocartilage typical of the disc, without synovium. With age, a bursa or cleft may develop in this region of the disc, suggesting a joint space. In the cervical region the uncinate process lies between the disc tissue and the exiting spinal nerve root. In the thoracic region, the discs are relatively rounded and thin ( Fig. 6-10 ). The outer annulus is distinguished on MR images. The lumbar discs, the thickest and largest in the spine, have a close relationship to the neural foramen.

FIGURE 6-9, Axial anatomic section through a cadaver cervical disc to illustrate the relationship of the disc centrally and the uncinate processes posterolaterally. The processes appear to buttress the lateral aspect of the disc. In the neural foramen, the ventral root and the dorsal root ganglion are evident.

FIGURE 6-10, Sagittal anatomic section through the thoracic spine. The intervertebral discs have a dense fibrous outer annulus fibrosus, as do the lumbar discs. The inner annulus fibrousus and nucleus pulposus contain cartilagenous matrix. The pigments in the inner disc represent aging changes.

AGE-RELATED CHANGES OF THE INTERVERTEBRAL DISC

Neonate

The neonatal disc lies between partially ossified vertebral bodies ( Fig. 6-11A ). In anatomic sections, the nucleus pulposus and inner annulus fibrosus appear together as a colorless, translucent structure. The peripheral (outer) annulus fibrosus displays a darker color due to its collagen content. Thin streaks that contain remnants of the primitive notochord stretch across the equator (center) of the disc from anterior to posterior. In anatomic sections, the unossified cartilage of the vertebral end plates resembles the cartilage of the disc itself. In the neonate, large blood vessels are present in the unossified vertebral cartilage. The neonatal disc is graded as stage I in the Thompson system for staging intervertebral disc degeneration.

FIGURE 6-11, Normal newborn lumbar intervertebral disc. A , Sagittal anatomic section. The newborn nucleus pulposus ( short arrows ) appears as a light gray translucent ovoid within the center of the interspace. Hyaline cartilage of the inner annulus fibrosus and the unossified portions of the adjacent vertebral bodies ( long arrows ) form a ring around the nucleus pulposus. Anteriorly and posteriorly the peripheral annulus fibrosus ( crossed arrows ) shows as a brown color and laminar structure. Small blood vessels are evident within the hyaline cartilage of the vertebral end plate ( arrowheads ). B , Sagittal T2W MR image of the specimen illustrated in A . The nucleus pulposus ( short arrows ) has high signal intensity. The hyaline cartilage in the inner annulus fibrosus and the unossified portions of the vertebral body ( long arrows ) have slightly lower signal intensity. The peripheral annulus fibrosus ( crossed arrows ) shows appreciably lower signal intensity.

In T2-weighted (T2W) MR images, the neonatal intervertebral disc shows uniformly high signal intensity in the nucleus pulposus and inner annulus fibrosus and low signal intensity in the more collagenous outer annulus fibrosus (see Fig. 6-11B ). No boundary is perceptible between the nucleus pulposus and the inner annulus. However, a sharp boundary is present between the inner annulus fibrosus and the outer annulus, which contains collagen. Unossified cartilage in the adjacent vertebra has the same signal intensity as the cartilage in the disc. These MRI characteristics are considered stage I in the Pfirrmann system for classifying intervertebral disc degeneration.

Second Decade

In anatomic sections, the intervertebral disc in the second decade of life appears white and opaque ( Fig. 6-12A ), owing in part to an increase in collagen content. During this decade, the disc appears less and less homogeneous. The nucleus pulposus now has a greater concentration of collagen and elastin fibers, especially in the equator, where the syncytial notochordal cells have disappeared. The fibers of the annulus fibrosus are more distinct than in the first decade of life. The outer annulus fibrosus contains as many as 80 lamellae and has greater width than in the first decade of life. The collagenous fibers of the lamellae course in parallel within each lamella, but their orientation differs by about 60 degrees from lamella to lamella. The vertebral end plates adjacent to the disc ossify by the end of the second decade of life. No blood vessels are now present in the disc or in the end plate. Water content in the disc does not decrease between the first and second decades of life. Intervertebral discs in the second decade of life usually meet criteria for stage II by the Thompson grading system.

FIGURE 6-12, Normal lumbar intervertebral disc of a 12-year-old. A , Sagittal anatomic section. The nucleus pulposus ( short arrows ) now appears inhomogeneous and semi-opaque with slightly reddish tissue and small foci of translucent material. Hyaline cartilage persists in the unossified end plates of the adjacent vertebrae ( long arrows ). The boundary between the inner annulus fibrosus and nucleus pulposus is indistinct. The peripheral annulus fibrosus ( crossed arrows ) has greater thickness and a more lamellar structure than in the newborn. No blood vessels are evident in the hyaline cartilage. B , Sagittal T2W MR image of the specimen illustrated in A . The nucleus pulposus and inner annulus fibrosus ( short arrows ) show nearly the same high signal intensity. The peripheral portion of the annulus fibrosus ( crossed arrows ) exhibits very low signal intensity.

T2W MR images of lumbar discs now show increased thickness of the peripheral region of low signal intensity (see Fig. 6-12B ). The central region of the disc maintains a relatively uniform high signal intensity. The boundary between the low and high signal intensity regions is less distinct than in the neonate. Between the ages of 4 and 20 years, the T2 relaxation time of the disc lengthens, suggesting an increase in free water content. Because the boundary between the low and high signal intensity regions is less distinct than in the neonate, the adolescent disc is graded as stage II in the Pfirrmann scale.

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