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SPINE Volume 24, Number 7, pp 619 – 628 ©1999, Lippincott Williams & Wilkins, Inc. The Ligaments and Anulus Fibrosus of Human Adult Cervical Intervertebral Discs Susan Mercer, B Phty (Hons), MSc, PhD,* and Nikolai Bogduk, MD, PhD, DSc, FAFRM Study Design. Descriptive, microdissection study. Objective. To determine the morphology of the human adult cervical intervertebral disc and its ligaments. Summary of Background Data. Some studies indicate that the cervical disc is distinctly different from the lumbar intervertebral disc, yet most clinical and anatomic texts appear content with extrapolating data from the lumbar spine. A detailed three-dimensional description of the cer- vical intervertebral disc and its surrounding ligaments is currently unavailable. Methods. Whole cervical spinal columns were freed from 12 human adult embalmed cadavers, and the pos- terior elements and soft tissues were removed. Using microdissection, the longitudinal ligaments and the fi- brous components of 59 cervical intervertebral discs were resected systematically. The orientation, location, and at- tachments of each stripped bundle of collagen were re- corded photographically and in sketches. Results. The cervical anulus fibrosus does not consist of concentric laminae of collagen fibers as in lumbar discs. Instead, it forms a crescentic mass of collagen thick anteriorly and tapering laterally toward the uncinate pro- cesses. It is essentially deficient posterolaterally and is represented posteriorly only by a thin layer of paramed- ian, vertically orientated fibers. The anterior longitudinal ligament covers the front of the disc, and the posterior longitudinal ligament reinforces the deficient posterior anulus fibrosus with longitudinal and alar fibers. Conclusions. The three-dimensional architecture of the cervical anulus fibrosus is more like a crescentic an- terior interosseous ligament than a ring of fibers sur- rounding the nucleus pulposus. [Key words: anulus fibro- sus, cervical intervertebral disc, longitudinal ligament, morphology] Spine 1999;24:619 – 628 The morphology and biochemistry of the lumbar inter- vertebral discs have been studied extensively, and several insights have emerged regarding the pathology of me- chanical disorders of the lumbar disc. However, when considering cervical intervertebral discs, most authors appear to be content with extrapolating data from the lumbar spine. Conspicuous in this regard is an article that appeared in a recent issue of an eminent journal dedicated to the cervical spine. In this article, five of six figures used to illustrate cervical motion segments actu- ally depicted lumbar motion segments. 4 It is clear that the pathology affecting cervical inter- vertebral discs is different from that affecting lumbar discs. In the lumbar disc, prolapse and its congeners are common. In the cervical spine, frank prolapse is uncom- mon, and degenerative changes are reported to occur typically in the form of endplate sclerosis, disintegration and collapse of the disc, bulging anulus fibrosus, devel- opment of osteophytes from the margins of the vertebral body, uncovertebral or zygapophysial joints, and nar- rowing of the intervertebral foramina or spinal canal by chondro-osseous spurs. 3,6,7,10,12,15,16,19,20,24,25 More recently, postmortem studies have found that after whiplash injuries, ligamentous injuries are ex- tremely common in the cervical spine and that herniation of the nucleus pulposus is a rare event. 13,14,23,28 –30,33 The lesions found in the cervical spine included bruising and hemorrhage of the uncinate region, so-called rim lesions or transections of the anterior anulus fibrosus, and avulsions of the vertebral endplate. 13,14,23,28 –30,33 Fundamental to any appreciation of the mechanism causing injury to the cervical intervertebral discs is a knowledge of their normal structure. It appears that little work has been reported concerning the morphology of the cervical intervertebral disc. One limited study de- scribed the structure of the cervical intervertebral disc in terms of disc height, cross-sectional area and shape, and fiber orientation of the anulus fibrosus. 21 Pooni et al, 22 using x-ray crystallography on the outer lamellae dis- sected from the anterior face of 13 C3–C4 discs, deter- mined that the fiber orientation was significantly less (65°) than the tilt of the fibers from the lumbar anulus fibrosus (70°). Other studies have addressed age changes in the cer- vical intervertebral discs, 1,18,21,26,32 but it is conspicuous that in all instances, observations were based on frontal, sagittal, or parasagittal sections of the intervertebral discs, yet no study illustrated a transverse section through a cervical disc. 1,8,18,21,26,31,32 Conspicuously missing in the literature is any description of the three- dimensional architecture of the cervical discs. Anatomy textbooks imply that all intervertebral discs conform to a generic pattern of a nucleus pulposus sur- rounded by concentric lamellae of obliquely orientated collagen fibers forming the anulus fibrosus. A small num- ber of studies, however, have indicated that the cervical discs are dissimilar to lumbar discs. 5,26,31 The develop- ment of cervical discs is distinctly different from that of the lumbar discs. The nucleus at birth constitutes no more than 25% of the entire disc, not 50% as in lumbar discs. 27 With aging, the nucleus pulposus rapidly under- From the *Department of Anatomy and Structural Biology, University of Otago, Dunedin, New Zealand, and the ²Newcastle Bone and Joint Institute, University of Newcastle, Newcastle, Australia. Supported in part by a grant from the Motor Accidents Authority of New South Wales. Acknowledgment date: February 19, 1998. Acceptance date: July 20, 1998. Device status category: 1. 619

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Page 1: SPINE Volume 24, Number 7, pp 619–628 ©1999, Lippincott Williams & Wilkins…soahs1.ttuhsc.edu/scdpt/6328/articles/6328-01-mercer... · 2003-08-28 · SPINE Volume 24, Number 7,

SPINE Volume 24, Number 7, pp 619–628©1999, Lippincott Williams & Wilkins, Inc.

The Ligaments and Anulus Fibrosus of Human AdultCervical Intervertebral Discs

Susan Mercer, B Phty (Hons), MSc, PhD,* and Nikolai Bogduk, MD, PhD, DSc, FAFRM†

Study Design. Descriptive, microdissection study.Objective. To determine the morphology of the human

adult cervical intervertebral disc and its ligaments.Summary of Background Data. Some studies indicate

that the cervical disc is distinctly different from the lumbarintervertebral disc, yet most clinical and anatomic textsappear content with extrapolating data from the lumbarspine. A detailed three-dimensional description of the cer-vical intervertebral disc and its surrounding ligaments iscurrently unavailable.

Methods. Whole cervical spinal columns were freedfrom 12 human adult embalmed cadavers, and the pos-terior elements and soft tissues were removed. Usingmicrodissection, the longitudinal ligaments and the fi-brous components of 59 cervical intervertebral discs wereresected systematically. The orientation, location, and at-tachments of each stripped bundle of collagen were re-corded photographically and in sketches.

Results. The cervical anulus fibrosus does not consistof concentric laminae of collagen fibers as in lumbardiscs. Instead, it forms a crescentic mass of collagen thickanteriorly and tapering laterally toward the uncinate pro-cesses. It is essentially deficient posterolaterally and isrepresented posteriorly only by a thin layer of paramed-ian, vertically orientated fibers. The anterior longitudinalligament covers the front of the disc, and the posteriorlongitudinal ligament reinforces the deficient posterioranulus fibrosus with longitudinal and alar fibers.

Conclusions. The three-dimensional architecture ofthe cervical anulus fibrosus is more like a crescentic an-terior interosseous ligament than a ring of fibers sur-rounding the nucleus pulposus. [Key words: anulus fibro-sus, cervical intervertebral disc, longitudinal ligament,morphology] Spine 1999;24:619–628

The morphology and biochemistry of the lumbar inter-vertebral discs have been studied extensively, and severalinsights have emerged regarding the pathology of me-chanical disorders of the lumbar disc. However, whenconsidering cervical intervertebral discs, most authorsappear to be content with extrapolating data from thelumbar spine. Conspicuous in this regard is an articlethat appeared in a recent issue of an eminent journaldedicated to the cervical spine. In this article, five of sixfigures used to illustrate cervical motion segments actu-ally depicted lumbar motion segments.4

It is clear that the pathology affecting cervical inter-vertebral discs is different from that affecting lumbardiscs. In the lumbar disc, prolapse and its congeners arecommon. In the cervical spine, frank prolapse is uncom-mon, and degenerative changes are reported to occurtypically in the form of endplate sclerosis, disintegrationand collapse of the disc, bulging anulus fibrosus, devel-opment of osteophytes from the margins of the vertebralbody, uncovertebral or zygapophysial joints, and nar-rowing of the intervertebral foramina or spinal canal bychondro-osseous spurs.3,6,7,10,12,15,16,19,20,24,25

More recently, postmortem studies have found thatafter whiplash injuries, ligamentous injuries are ex-tremely common in the cervical spine and that herniationof the nucleus pulposus is a rare event.13,14,23,28–30,33

The lesions found in the cervical spine included bruisingand hemorrhage of the uncinate region, so-called rimlesions or transections of the anterior anulus fibrosus,and avulsions of the vertebral endplate.13,14,23,28–30,33

Fundamental to any appreciation of the mechanismcausing injury to the cervical intervertebral discs is aknowledge of their normal structure. It appears that littlework has been reported concerning the morphology ofthe cervical intervertebral disc. One limited study de-scribed the structure of the cervical intervertebral disc interms of disc height, cross-sectional area and shape, andfiber orientation of the anulus fibrosus.21 Pooni et al,22

using x-ray crystallography on the outer lamellae dis-sected from the anterior face of 13 C3–C4 discs, deter-mined that the fiber orientation was significantly less(65°) than the tilt of the fibers from the lumbar anulusfibrosus (70°).

Other studies have addressed age changes in the cer-vical intervertebral discs,1,18,21,26,32 but it is conspicuousthat in all instances, observations were based on frontal,sagittal, or parasagittal sections of the intervertebraldiscs, yet no study illustrated a transverse sectionthrough a cervical disc.1,8,18,21,26,31,32 Conspicuouslymissing in the literature is any description of the three-dimensional architecture of the cervical discs.

Anatomy textbooks imply that all intervertebral discsconform to a generic pattern of a nucleus pulposus sur-rounded by concentric lamellae of obliquely orientatedcollagen fibers forming the anulus fibrosus. A small num-ber of studies, however, have indicated that the cervicaldiscs are dissimilar to lumbar discs.5,26,31 The develop-ment of cervical discs is distinctly different from that ofthe lumbar discs. The nucleus at birth constitutes nomore than 25% of the entire disc, not 50% as in lumbardiscs.27 With aging, the nucleus pulposus rapidly under-

From the *Department of Anatomy and Structural Biology, Universityof Otago, Dunedin, New Zealand, and the †Newcastle Bone and JointInstitute, University of Newcastle, Newcastle, Australia.Supported in part by a grant from the Motor Accidents Authority ofNew South Wales.Acknowledgment date: February 19, 1998.Acceptance date: July 20, 1998.Device status category: 1.

619

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goes fibrosis such that by the third decade there is barelyany nuclear material distinguishable.18,31

In view of these disparities and the lack of any formaldata on the structure of cervical discs, the current studywas undertaken. It used a microdissection approach todetermine the three-dimensional architecture of the cer-vical anulus fibrosus and its surrounding ligaments, withthe objective of providing an anatomic basis for biome-chanical models and studies of the cervical disc like thosedeveloped for the lumbar spine.9

Methods

Fifty-nine cervical intervertebral discs were obtained from 12embalmed cadavers of men and women with a mean age of65.4 years (range, 39–82 years) (Table 1). No specimen wasinvolved in trauma as a cause of death. Whole cervical spinalcolumns were removed from each cadaver by disarticulation ofthe atlas at the occipital condyles and disarticulation throughthe C7–T1 intervertebral disc and zygapophysial joints. Afterremoval of muscles and fascia, the posterior elements andtransverse processes were removed to reveal a column of ver-tebral bodies with attached longitudinal ligaments. Using a dis-secting microscope at 320 to 340 power, each disc was sys-tematically dissected by resecting its collagen fibers in bundlessmall enough to be grasped with sharpened jeweler’s forceps.As bundles were stripped and detached, their orientation, loca-tion, and attachments were recorded photographically and insketches. Each disc was dissected circumferentially and centrip-etally. Superficial layers of collagen were resected anteriorly,posteriorly. and laterally to reveal deeper layers, which werethen resected in a similar manner.

At each stage of dissection, photographs were taken andsketches drawn to illustrate the arrangement of collagen fibersin different sectors and at different depths of the disc. On com-pletion of the study, four additional specimens were dissectedin another manner to confirm and illustrate the three-dimensional architecture of the disc as determined by microdis-section. In these specimens, the perimeter of the disc wascleared of periosteum and all elements of the anterior and pos-terior longitudinal ligaments. Then the vertebra above the discwas resected with rongeurs and by drilling until only the infe-rior vertebral endplate remained. This then was scraped awaycarefully with a curette, with care taken not to damage any ofthe underlying tissues that attached to the endplate. Any re-maining island of bone was extracted by sharp dissection undera microscope. Once all osseous tissue had been removed, the

top surface of the disc was trimmed of any loose fibers toproduce a photogenic top view of an otherwise intact disc.

Results

On dissection of the cervical discs, four distinct struc-tures were encountered: 1) elements that could be as-signed to the anterior or posterior longitudinal ligamentswhose fibers were characterized by having attachmentsto the respective anterior or posterior surfaces of thevertebral bodies, 2) periosteofascial tissue overlying theuncovertebral area, 3) a structure interpreted as intrinsicfibers of the anulus fibrosus because the fibers were at-tached to the superior and inferior surfaces or edges ofthe vertebral bodies and did not extend onto the externalsurface of the bones, and 4) a deep core of undissectablefibrocartilaginous material.

Anterior Longitudinal LigamentThe anterior longitudinal ligament of the cervical verte-bral column was defined by fibers that attached to theanterior surfaces of the vertebral bodies. This ligamentcomprised four layers of fibers distinguished by their pat-terns of attachment.

The first (superficial) layer consisted of fibers that ranlongitudinally, crossing several segments, and that wereattached to the central areas of the anterior surfaces ofthe vertebral bodies (Figure 1). Rostrally, they were at-tached firmly to the anterior tubercle of the atlas. Belowthis level, they covered the middle two quarters of theanterior surfaces of the vertebral bodies. Densely aggre-gated from side to side in the upper cervical spine wherethe anterior longitudinal ligament is narrow, these fiberswere less densely packed at lower levels where the ante-rior longitudinal ligament expands laterally.

The fibers of the second (intermediate) layer also werelongitudinal, but distinctly shorter than the superficialfibers. They covered one intervertebral disc and insertedonto the anterior surfaces of the adjacent vertebral bod-ies, but never further than half way up or down thatsurface (Figure 1).

The third (deep) layer consisted of even shorter longi-tudinal fibers that spanned one disc but attached justcranial or caudal to the inferior or superior margins ofthe adjacent vertebral bodies (Figures 1 and 2).

The fourth layer consisted of fibers with an alar dis-position. They formed a thin curtain over each interver-tebral disc. Arising from the anterior surface of the ver-tebra above, close to its inferior margin, these fiberspassed inferiorly and laterally over the disc to insert intothe vertebra immediately below its superior margin. Themost lateral of these fibers reached the summit of theuncinate process and arose from the vertebra above at apoint where the lateral longitudinal ridges on the ante-rior surface of the vertebral body met the enchancrurefor the uncinate process (Figures 1 and 3). These fiberswere considered to be components of the anterior longi-tudinal ligament rather than components of the anulusfibrosus because they attached to the anterior surfaces of

Table 1. Specimens Studied by Age and Gender

Subject Discs Studied Age Gender

1 5 83 Female2 5 82 Male3 5 79 Male4 5 76 Male5 5 71 Male6 5 68 Male7 5 66 Male8 5 65 Male9 5 64 Male10 5 48 Male11 5 44 Male12 4 39 Female

620 Spine • Volume 24 • Number 7 • 1999

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the vertebral bodies rather than to their inferior and su-perior surfaces or edges.

Posterior Longitudinal LigamentThe posterior longitudinal ligament covered the entirefloor of the cervical vertebral canal and consisted of dis-tinct superficial, intermediate, and deep layers. The su-perficial layer contained two elements: 1) central, longi-tudinally directed fibers that spanned a variable numberof segments, and 2) lateral extensions that swept out

from the central band to cross an intervertebral disc andattach to the base of the pedicle one or two segmentsbelow (Figures 4 and 5). Centrally, all fibers of the su-perficial layer were attached to the central posterior sur-faces of the vertebral bodies. Resection of these fibersrevealed longitudinally disposed tubercles on the central,posterior surface of the vertebral bodies to which they at-tached.

The intermediate layer of the posterior longitudinalligament consisted of longitudinal fibers that spannedonly one intervertebral disc. These fibers, restricted to a

Figure 1. A schematic sketch of the components of the anteriorlongitudinal ligament. At different levels, more superficial fibershave been transected and removed to reveal deeper fibers. 1 5superficial longitudinal fibers; 2 5 intermediate longitudinal fibers;3 5 deep longitudinal fibers; 4 5 alar fibers; pf, periosteofascialtissue covering the uncovertebral cleft.

Figure 2. A photograph showing the deepest longitudinal fibers ofthe anterior longitudinal ligament (f).

Figure 3. A photograph showing the alar fibers of the anteriorlongitudinal ligament (a).

Figure 4. A schematic sketch of the components of the posteriorlongitudinal ligament. At different levels, more superficial fibershave been transected and removed to reveal deeper fibers. s 5superficial fibers and their lateral extensions (e) to the bases ofthe pedicles (p); i 5 intermediate fibers; d 5 deep fibers and theirthin alar extensions (a) toward the uncinate process (u); t 5tubercles that receive the superficial fibers.

621Ligaments and Anulus Fibrosus of Cervical Discs • Mercer and Bogduk

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position close to the median plane, were attached to theposterior surfaces of the adjacent vertebral bodies justcaudally or cranially to the tubercles on the posteriorsurfaces of the vertebral bodies (Figures 4 and 6).

The deep layer of the posterior longitudinal ligamentconsisted of short fibers that spanned each intervertebraldisc. These fibers arose from the posterior surface of theupper vertebra just above its inferior border and passedinferiorly and somewhat laterally to reach the vertebrabelow, immediately below its superior margin. Laterally,the fibers of this layer extended in an alar fashion as faras the posterior end of the base of the uncinate process(Figures 4 and 6). The deep layer was considered to be acomponent of the posterior longitudinal ligament ratherthan a component of the anulus fibrosus because its fi-bers attached to the posterior surfaces of the vertebralbodies rather than to their inferior and superior surfacesor edges.

Periosteofascial TissuePeriosteofascial tissue covered the area of the lateralclefts in the uncovertebral region. This tissue was so

named because it was continuous with the periosteumover the posterior lateral aspect of the vertebral body andpedicles but became distinctly fascial as it left the bone. Itconsisted of unorganized fibrous connective tissue em-bedded with fat and a large number of blood vessels.Posteriorly, having covered the uncovertebral cleft, thefascia disappeared deep to the free, lateral edge of thealar portion of the posterior longitudinal ligament thatcovered the cartilaginous core of the underlying disc.Anteriorly, the fascia disappeared deep to the alar por-tion of the anterior longitudinal ligament to interweavewith the outer fibers of the anterolateral portion of theanulus fibrosus (Figure 7).

Anulus FibrosusThe structure of the anulus fibrosus was different in itsanterior and posterior parts. The anterior part was thicktoward the median plane, but progressively thinner whentraced to the uncinate processes, such that in a top view,the anterior anulus was crescentic in form (Figure 8). Theposterior part consisted of only a thin layer of colla-gen fibers.

Covering the anterior aspect of the anulus fibrosuswas a thin layer of collagen fibers that was transitionalbetween the deepest fibers of the anterior longitudinal

Figure 5. A photograph showing the intermediate (i) and superfi-cial lateral (s) fibers of the posterior longitudinal ligament.

Figure 6. A photograph showing the short, longitudinal fibers (s)of the posterior longitudinal ligament and its alar fibers (a). Notethe disc bulge (b) and the herniation (h), each below their respec-tive alar fibers.

Figure 7. Periosteofascial tissue (pt) covering the uncovertebralregion. A, posterior lateral view. B, anterior view.

622 Spine • Volume 24 • Number 7 • 1999

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ligament and the most superficial layers of the anulus(Figures 9A and 10A). Their orientation was like that ofthe deepest fibers of the anterior longitudinal ligament,in that in the paramedian region they passed inferiorlybut diverged laterally, whereas more laterally the fibersassumed an alar disposition passing inferiorly and later-ally. However, unlike the definitive fibers of the anteriorlongitudinal ligament, their attachments were to theedges of the vertebral bodies, not to their ante-rior surfaces.

Deep to these transitional fibers, the fibers of the anu-lus fibrosus proper arose from the superior surface of thelower vertebra. The most lateral fibers arose from theapex and anterior surface of the uncinate process andpassed upward and medially to insert into the inferiorsurface of the vertebral body above, opposite where theipsilateral anterior longitudinal ridge meets the anteriormargin (Figures 9B and 10B). Progressively, more medialfibers arose from the upper surface of the lower vertebralbody and passed upward and medially into the inferiorsurface of the vertebra above. Toward the midline, these

fibers interwove with the corresponding fibers of the op-posite side. These fibers did not pass one another in sep-arate laminae, but were distinctly and tightly interwo-ven, as in a decussation (Figures 9B and 10B).

Deeper into the anterior anulus, fibers in successivelayers repeated this pattern of central interweaving, butindividual fibers became difficult to trace within andthrough the weave. However, progressively deeper fiberswere increasingly restricted to attachments closer to themidline (i.e., fewer fibers in successive layers arose fromregions toward the uncinate processes on each side. Thisfeature produced the crescentic appearance of the anuluswhen viewed from above (Figure 8).

Beyond 2 to 3 mm from the surface of the anterioranulus, collagen fibers were increasingly embedded withwhat was assumed to be proteoglycans to form a homo-geneous fibrocartilaginous mass that had a pearly ap-pearance and the consistency of soap (Figure 9D and10C). These fibers defied microdissection. However,when the vertebral bodies were separated by blunt dis-section, it was apparent that this mass consisted of la-

Figure 8. Top views of a cervical disc. A, Sketch showing how the anterior anulus (a) is crescentic, thick anteriorly, but tapering towardthe uncinate region (u). It surrounds a central fibrocartilaginous core (fc). The posterior anulus (p) is limited to paramedian longitudinalfibers. B, Sketch showing how the anulus is surrounded anteriorly by the three longitudinal layers of the anterior longitudinal ligament(a), laterally by the alar fibers (aa) of the anterior longitudinal ligament, posteriorly by the two longitudinal layers of the posteriorlongitudinal ligament (p) and its alar fibers (pa). The posterior lateral corner of the fibrocartilaginous core is covered only byperiosteofascial tissue (pf). The thickness of the layers is not drawn to scale. C, Photograph showing a top view of a 39-year-old disc fromwhich all elements of the anterior and posterior longitudinal ligaments have been removed. The anulus fibrosus (af) is relatively thick andfibrous anteriorly, but tapers posteriorly toward the uncinate region (ur). It covers the uncinate region on the right but is deficient on theleft. Deep to the fibrous anulus is a fibrocartilaginous layer (fc, and arrows) that surrounds the large nucleus pulposus (np). Posteriorly,there is only a thin posterior anulus fibrosus (p) whose thickness is indicated by the brackets.

Figure 9. The anterior anulus fibrosus. A, Transitional fibers. B, Superficial fibers. C, Deeper fibers. D, The fibrocartilaginous core of thedisc deep to the anterior anulus.

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mellae that could not be dissected because the dominanttissue was a proteoglycan matrix. Deeper still, the fibro-cartilage became more homogeneous and less laminated,forming what was interpreted to be the nucleus ofthe disc.

The posterior anulus was different in character fromthe anterior anulus. It extended between the bases of theuncinate processes on each side and consisted of one setof vertically orientated collagen fibers that ran betweenthe facing surfaces of opposing vertebral bodies (Figures

8, 11, and 12). This layer was not more than 1 mm thick,and deep to it lay the homogeneous fibrocartilagi-nous core.

In this context it should be noted that anterior to eachuncus the fibrocartilaginous core was covered by themost peripheral fibers of the anterior anulus. The poste-rior anulus covered only the posteromedial aspect of the

Figure 10. Photographs showing three depths of the anterior anu-lus fibrosus. A, Transitional layer. B, Deeper layer. C, The fibro-cartilaginous core of the disc (fc).

Figure 11. The posterior anulus fibrosus. A, The longitudinal fibersof the anulus fibrosus. B, The fibrocartilaginous core of the discdeep to the posterior anulus.

Figure 12. A, Photograph showing the posterior anulus fibrosus(af). Deep to it lies the fibrocartilaginous core of the disc (fc). B,The fibrocartilaginous core fully revealed by resection of theposterior anulus.

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fibrocartilaginous core. Superoposteriorly to the uncus,no anulus fibers covered the core, which was coveredonly by the periosteofascial tissue described earlier (Fig-ure 8).

Fibrocartilaginous CoreIn the uncovertebral region, clefts extended into the fi-brocartilaginous core. The clefts opened under the peri-osteofascial tissue covering the uncovertebral region andpenetrated the core to different extents. In younger spec-imens, the clefts extended only partially into the core,whereas in older specimens, the clefts totally transectedthe posterior two thirds of the disc, occasionally leavingan isolated posterior central plug of fibrocartilage deepto the posterior anulus (Figure 13).

Discussion

Readers may be as startled as the investigators were bythe results of this study: the structure of the cervical discsdoes not match the descriptions they currently have re-ceived in the literature. The cervical discs are not likelumbar discs. The cervical anulus fibrosus does not con-sist of concentric lamellae of collagen fibers that uni-formly surround the nucleus pulposus, and that exhibitalternating oblique orientations. Rather, the cervicalanulus is crescentic, being thick anteriorly but tapering inthickness laterally as it approaches the uncoverte-bral region.

Over the anterior end of the uncovertebral regionthere is only a single layer of obliquely orientated fiberscovering the fibrocartilaginous core of the disc. Laterallyover the uncovertebral region there is no substantiveanulus. Only a flimsy layer of periosteofascial tissue cov-ers the fibrocartilaginous core, disappearing deep to thealar portions of the anterior and posterior longitudinalligaments. Posteriorly, the anulus fibrosus is not multi-laminated like the anterior anulus of cervical discs or the

posterior anulus of lumbar discs, nor does it consist ofobliquely orientated fibers. It is represented only by athin set of vertically running fibers.

In no region of the cervical anulus fibrosus do succes-sive lamellae exhibit alternating orientations. A cruciatepattern occurs only in the anterior portion of the anuluswhere obliquely orientated fibers, upward and medially,interweave with one another. This weave is what mayhave been regarded in x-ray crystallography studies22 asalternating layers, but it is not produced by alter-nate lamellae.

Skeptical individuals might argue that the currentstudy was confounded by the use of elderly cadavers andthat the features observed were the consequence of de-generative or age-related changes. However, all the spec-imens exhibited the same morphology including the sam-ples taken from the 39-year-old individual and the twoother individuals younger than 50 years of age. More-over, even though age changes might be expected tocause desiccation and fibrosis of the disc, and perhapsdisruption and attrition of collagen fibers, they cannot beexpected to alter the orientation and attachments of col-lagen fibers.

Therefore, although it might be conceded that agechanges could result in thinning of the anulus fibrosus byabsorption of deeper layers of collagen into the nucleus,they cannot alter the geometry of those anulus elementsthat remain. Accordingly, the cervical discs are rendereddifferent from the lumbar discs by certain key features:Anteriorly, the cervical anulus consists of interwoven,alar fibers, whereas posteriorly, the anulus lacks anyoblique fibers and consists exclusively of vertically ori-entated fibers. In essence, the cervical anulus has thestructure of a dense, anterior interosseous ligament withfew fibers to contain the nucleus pulposus posteriorly.That role is subserved by the overlying posterior longi-tudinal ligament. Posterolaterally, the nucleus is con-tained only by the alar fibers of the posterior longitudinalligament, under which or through which nuclear mate-rial must pass if it is to herniate (Figure 6).

The vertical orientation of the posterior anulus of cer-vical discs has not been reported before, but a similarobservation has been made for thoracic discs.34 The ab-sence of an anulus over the uncovertebral region is not anew observation because previous studies have shownthat in this region collagen fibers are torn by 15 years,10

or as early as 932 or 7 years,11 leaving clefts that progres-sively extend across the back of the disc.10 Rather thanan incidental age change, this disruption has been inter-preted either as enabling2 or resulting from21 rotatorymovements of the cervical vertebrae. Axial rotation of atypical cervical vertebra occurs around an oblique axisperpendicular to the plane of its facets.21 The uncover-tebral clefts are necessary to allow the posterior cornersof the vertebral body to swing laterally as they pivotaround the dense, interosseous portion of the ante-rior anulus.

Figure 13. A photograph of a cervical disc viewed from behindshowing uncovertebral clefts (vc) penetrating medially through thefibrocartilaginous core but leaving a central, posterior plug offibrocartilage (fc) covered by some undissected vertical fibers ofthe posterior anulus (a).

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The results of the current study have biomechanicaland clinical ramifications. For biomechanists, the differ-ent anatomy of the cervical anulus fibrosus means thatthe model devised for lumbar discs9 cannot be applied tothe neck. A separate and new model must be devised forthe cervical discs. For clinicians, a question can be raisedabout the etiology and mechanism of cervical discogenicpain. Such pain cannot be ascribed to posterolateral fis-sures in the anulus fibrosus, as it is in the lumbar spine,17

because in cervical discs the posterolateral anulus is lack-ing. Considering the structure of the cervical anulus, thepossibilities that emerge for mechanisms of discogenicpain are strain or tears of the anterior anulus, particu-larly after hyperextension trauma, and strain of the alarportions of the posterior longitudinal ligament whenstretched by a bulging disc.

Even though the current study was based largely onelderly specimens, the results are sufficiently striking tocall for an immediate revision of prevailing notionsabout the structure of cervical discs. What remains to beexplored is whether this distinctive structure is evident atall ages or whether younger discs have components dif-ferent from or additional to those seen in the elderly. Inparticular, if a posterior anulus is lacking only in elderlydiscs, when does the attrition of the posterior anuluscommence, and why?

References

1. Bland JH, Boushey DR. Anatomy and physiology of the cervical spine. SeminArthritis Rheum 1990;20:1–20.2. Bogduk N. Biomechanics of the cervical spine. In: Grant R, ed. Physical

Therapy of the Cervical and Thoracic Spine. 2nd ed. New York: Churchill Liv-ingstone, 1994:27–45.3. Brooker AEW, Barter RW. Cervical spondylosis: A clinical study with com-

parative radiology. Brain 1965;88:925–36.4. Connell MD, Wiesel SW. Natural history and pathogenesis of cervical disk

disease. Orthop Clin North Am 1992;23:369–80.5. Ecklin U. Die Altersveranderungen der Halswirbelsaule. Berlin:

Springer, 1960.6. Goodman BW. Neck pain. Prim Care 1988;15:689–707.7. Gore DR, Sepic SB, Gardner GM, Murray MP. Neck pain: A long-term

follow-up of 205 patients. Spine 1987;12:1–5.8. Hall MC. Luschka’s Joint. Springfield, IL: Charles C Thomas, 1965.9. Hickey DS, Hukins DWL. Relation between the structure of the annulus

fibrosus and the function and failure of the intervertebral disc. Spine 1980;5:106–16.10. Hirsch C. Some morphological changes in the cervical spine during ageing.In: Hirsch C, Zotterman Y, eds. Cervical Pain. Oxford: Pergamon, 1971.11. Hirsch C, Schajowicz F, Galante J. Structural changes in the cervical spine: Astudy on autopsy specimens in different age groups. Acta Orthop Scand 1967;Suppl 109.

12. Holt S, Yates PO. Cervical spondylosis and nerve root lesions: Incidence atroutine necropsy. J Bone Joint Surg [Br] 1966;48:407–23.13. Jonsson H, Cesarini K, Sahlstedt B, Rauschning W. Findings and outcome inwhiplash-type neck distortions. Spine 1994;19:2733–43.14. Jonsson H, Bring G, Rauschning W, Sahlstedt B. 1991 Hidden cervical spineinjuries in traffic accident victims with skull fractures. J Spinal Disord 1991;4:251–63.15. Lestini WF, Wiesel SW. The pathogenesis of cervical spondylosis. Clin Or-thop 1989;239:69–93.16. McNab I. Cervical spondylosis. Clin Orthop 1975;109:69–77.17. Moneta GB, Videman T, Kaivanto K, et al. Reported pain during lumbardiscography as a function of anular ruptures and disc degeneration. A re-analysisof 833 discograms. Spine 1994;17:1968–74.18. Oda J, Tanaka H, Tsuzuki N. Intervertebral disc changes with aging ofhuman cervical vertebra: From neonate to the eighties. Spine 1988;13:1205–11.19. Pallis C, Jones AM, Spillane JD. Cervical spondylosis: Incidence and impli-cations. Brain 1954;77:274–89.20. Payne EE, Spillane JD. The cervical spine: An anatomic–pathological studyof 70 specimens. Brain 1957;80:571–96.21. Penning L. Differences in anatomy, motion, development, and ageing of theupper and lower cervical disk segments. Clin Biomech 1988;3:37–47.22. Pooni JS, Hukins DWL, Harris PF, Hilton RC, Davies KE. Comparison ofthe structure of human intervertebral discs in the cervical, thoracic, and lumbarregions of the spine. Surg Radiol Anat 1986:8:175–82.23. Rauschning W, McAfee PC, Jonsson H. Pathoanatomical and surgical find-ings in cervical spinal injuries. J Spinal Disord 1989;2:213–22.24. Robinson RA, Afeiche N, Dunn EJ, Northup BE. Cervical spondylotic my-elopathy: Etiology and treatment concepts. Spine 1977;2:89–99.25. Scoville WB. Types of cervical disk lesions and their surgical approaches.JAMA 1966;196:479–81.26. Taylor JR. Growth and Development of the Human Intervertebral Disc(Thesis). University of Edinburgh, 1974.27. Taylor JR. Regional variation in the development and position of the noto-chordal segments of the human nucleus pulposus. J Anat 1971;110:131–2.28. Taylor JR, Kakulas BA. Neck injuries. Lancet 1991;338:1343.29. Taylor JR, Twomey LT. Disc injuries in cervical trauma. Lancet 1990;44:1318.30. Taylor JR, Twomey LT. Acute injuries to cervical joints. Spine 1993;18:1115–22.31. Tondury G. Entwicklungsgeschichte und Fehlbildungen der Halswirbel-saule. Stuttgart: Hippokrates, 1958.32. Tondury G. The behaviour of the cervical discs during life. In: Hirsch C,Zotterman Y, eds. Cervical Pain. Oxford: Pergamon, 1971.33. Twomey LT, Taylor JR. The whiplash syndrome: Pathology and physicaltreatment. J Manual Manipulative Ther 1993;1:26–9.34. Zaki W. Aspect morphologique et fonctionnel de l’ annulus fibrosus dudisque intervertebrale de la colonne dorsale. Arch Anat Path 1973;21:401–3.

Address reprint requests to

Nikolai Bogduk, MDNewcastle Bone and Joint Institute

Royal Newcastle HospitalNewcastle, NSW 2300

Australia

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Point of View

James R. Taylor, MD, PhDVisiting Professor, Australian Neuromuscular Research InstituteQEII Medical CentreNedlands, Western Australia

This detailed study of cervical discs from 12 adult cadav-ers (aged 39 to 83 years) comes from two institutions,both highly respected for anatomic study and research. Itdeals with a topic much neglected in recent years, theunique structure of adult cervical discs. Radiologists andsurgeons dealing with the cervical spine and anatomistswho teach this subject in should be aware of its uniquestructure. This article contains new information on thedetailed structure of adult cervical discs and their liga-ments, but I doubt that well-informed radiologists willbe as “startled” as the authors about the main findings,the absence of an intact posterior anulus fibrosus, andthe presence of transverse fissuring from the uncoverte-bral clefts through the “central core.” Cervical discogra-phy has fallen into disfavor in many quarters, but thosewho still practice it often see a posterior fissure systemoutlined by centrally injected contrast, showing a “bi-partite disc,” except for the anterior anulus (McCormickCC, personal communication). This commentator, withLT Twomey, has been describing and illustrating theposterior transverse fissures in bipartite middle aged andelderly cervical discs at scientific conferences and in bookchapters for the past 10 years.1–4 Before that, Tonduryand Penning (cited by the authors) gave good descrip-tions of the age-related anatomy of cervical discs, basedon Tondury’s series of 150 spines aged from 20 to 90years.5 He showed that cervical discs are often bipartitein older subjects, even those as young as 33 years—though he emphasized the age-related variation—in hislarge series. Despite this, it would still be true that manyscientists and clinicians still regard the cervical disc as asmaller copy of the lumbar disc, and, as the authors pointout, clinical texts and texts on anatomy are content toregard them as essentially similar.

This study confirms that adult cervical discs are verydifferent from lumbar discs. This was evident in our au-topsy studies of cervical spines, which included histo-logic studies of 32 spines6 and a sagittal sectioning studyof 180 spines ranging from infancy to old age,7 but ourstudies are not directly comparable with the detailed,dissection-based study of the “three-dimensional archi-tecture” of the discs and ligaments by Mercer and Bog-duk. The authors confirm that only the crescentic ante-rior anulus of adult discs persists as an intact structure,with age-related variability of penetration of the trans-verse clefts into the original posterior anulus and thenucleus or “core.” They go further and suggest that thestructure of the anulus is likely to be unique at all stagesof development—a doubtful conclusion in a study that

excludes immature discs. Their descriptions of the longi-tudinal ligaments are interesting and informative. Thestrength and structure of these ligaments are importantfor a number of reasons, e.g., in relation to the contain-ment of some posterior herniations by the layered, pos-terior longitudinal ligament (they do not mention its re-lation to the anterior internal vertebral venous plexus)and in relation to the order of failure of anterior struc-tures in neck extension injuries. The anterior anulus failsbefore the anterior longitudinal ligament.6 The longerfibers of the anterior longitudinal ligament would bemore compliant than the shorter fibers of the anterioranulus. The first and second layers discussed by the au-thors correspond to the anterior longitudinal ligament asI have regarded it, with superficial fibers spanning severalsegments and shorter fibers spanning one full segment;both can be traced into the anterior periosteum. I alsohave observed the interchange of fibers with the anterioranulus (the authors’ transitional fibers). I have regardedlayers 3 and 4 as superficial parts of the anulus, but I notethat the authors distinguish layer 4 from the anuluspartly by the particular orientation of its fibers.

Mercer and Bogduk have described the unique anat-omy of the adult cervical disc in more detail than haveauthors of previous studies. To be fair to the (false) ac-counts of cervical discs in anatomy texts, many anato-mists approach anatomy from a developmental perspec-tive. This also has its merits, because in fetuses, infants,children, adolescents, and even in many young adults,freshly cut cervical discs, viewed in midsagittal section,show central swelling of a nucleus or central core, sur-rounded by an anulus, much like lumbar discs. The un-covertebral clefts are not true joints, as they do not ap-pear posterolaterally until adolescence. As described byTondury,5 from the third or fourth decade onwards, fis-sures penetrate medially from these clefts in response tothe shearing forces of cervical movements, with attritionof the posterior anulus and central core, producing thedramatic contrasts with lumbar discs described in thisarticle. The preservation of the posterior longitudinalligament from this attrition is probably related to thegreater compliance of its longer fibers; I would maintainthat the connective tissue geometry in the disc can changein adults, just as bones remodel in response to alteredloading.

References

1. Twomey L, Taylor JR. Cervical and lumbar spines: Contrasting age changesand injury. Proceedings of the Australian Physiotherapy Association Pelvic Sym-

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posium. Melbourne, Australia: Australian Physiotherapy Association 1993: 91–92.2. Taylor JR, Twomey L. Functional and applied anatomy of the cervical spine.In: Grant R, ed. Physical Therapy of the Cervical and Thoracic Spine. 2nd ed.New York: Churchill Livingstone, 1994:1–25.3. Taylor JR, Twomey LT. The effects of aging on the intervertebral discs. In:Boyling JD, Palastanga N, eds. Grieve’s Manual Therapy of the Vertebral Col-umn. 2nd ed. Edinburgh: Churchill Livingstone, 1994:177–88.

4. Twomey LT, Taylor JR. Development and growth of the cervical and lumbarspine. In: White AH, Schofferman JA, eds. Spine Care. Vol. 2: Operative Treat-ment. St. Louis, Mosby, 1995:792–808.5. Tondury G. La colonne cervicale: son developpement et ses modificationsdurant la vie. Acta Orthop Belge 25:602–26.6. Taylor JR, Twomey L. Acute injuries to cervical joints. Spine 1993;18:1115–22.7. Taylor JR, Taylor M. Cervical spinal injuries: An autopsy study of 109 bluntinjuries. J Musculoskeletal Pain 1996;4:61–80.

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