Download Anatomy and pathology of the aging spine1

European Journal of Radiology 27 (1998) 181 – 195
Anatomy and pathology of the aging spine1
Andreas Prescher
Institut für Anatomie, Uni6ersitätsklinikum der RWTH Aachen, 52057 Aachen, Germany
Received 12 November 1997; accepted 14 November 1997
Abstract
The vertebral column is a complicated anatomical structure which is composed of the intervertebral discs and the vertebrae.
Both components develop special degenerative changes and morphologic features during life. This paper first reviews the
anatomical fundamentals and then describes the morphological features of the aging intervertebral disc and the subsequent
osseous changes of the vertebral bodies and the zygapophyseal joints. The aging intervertebral disc is characterised by processes
which are labeled as intervertebral chondrosis and intervertebral osteochondrosis. Often these processes are combined with typical
dislocations of intervertebral disc tissue in an anterior or dorsolateral direction. The well known Schmorl’s nodules must also be
mentioned in this context. Furthermore calcification and ossification of the intervertebral disc tissue can take place. More severe
processes lead to osseous changes of the vertebral bodies. In particular, an osteophytosis of the vertebral bodies can be
established. These sturdy osteophytes are able to stiffen the vertebral column. Furthermore the arthrotic changes of the
zygapophyseal joints are delineated in this paper. The special appearances of these changes are discussed according to the different
and specialised regions of the vertebral column. The advanced degenerative changes of the zygapophyseal and uncovertebral joints
of the cervical spine are of essential clinical interest because the compression of the vertebral artery or the narrowing of the
intervertebral foramina by these processes may cause severe neurological symptoms. The arthrotic changes of the medial
atlantoaxial joint, which lead to the crowned odontoid, and the pseudospondylolisthesis (so called M. Junghanns) of the lumbar
spine must also be mentioned. It is the aim of this paper, not only to explain and review the degenerative changes, but to illustrate
the anatomy and pathology of the aging spine on the basis of macerated osseous specimens in order to make radiological
investigations and pictures more understandable and clear. © 1998 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Degenerative changes; Spine; Spondylosis; Intervertebral disc
1. General anatomical fundamentals
The spine represents a movable column composed of
24 presacral vertebrae, disci intervertebrales and ligaments. Reflecting the increasing loads, the vertebrae
and intervertebral discs increase in a harmonic order
from the cranial end in the caudal direction.
For the changes in the structure and composition of
the spine with increasing age, the anatomy of the
intervertebral discs is of prime importance. An interver-
1
Dedicated to Professor Dr med D. Graf von Keyserlingk on the
occasion of his 60th birthday.
tebral disc consists basically of an external fibrous ring,
the anulus fibrosus, and a jelly-like center, the nucleus
pulposus. The anulus fibrosus can be subdivided into
an outer and an inner zone, which show different
histological structures. The outer zone is structured into
concentric lamellae of tight, collagenous fibers (Fig. 1a),
which in the inner zone are followed by fibrous-cartilaginous tissue. Without a distinct borderline, that tissue gradually exhibits a transition into the nucleus
pulposus (Fig. 1a). The fibers in the outer zone are
primarily type I collagen fibers, while the fibers of the
inner zone are mostly collagen fibers of type II. In the
individual lamellae of the outer zone, which are sequentially structured similar to the layers of an onion, the
fibers are arranged crossing each other clockwise and
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PII S0720-048X(97)00165-4
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
Fig. 1. (a) Horizontal section of a normal intervertebral disc, illustrating the concentric laminated anulus fibrosus and the eccentric located
nucleus pulposus with a brown degeneration forming. (b) Normal
osseous vertebral endplate exhibiting a porous surface structure and a
smooth ossified vertebral rim. A little step can be seen between these
two areas (36 years, female). (c) Structural changes of the osseous
vertebral endplate and the ossified vertebral rim due to osteochondrosis. Many little bony excrescences and irregularities are present (79
years, female).
counterclockwise in helical turns, connecting the
ossified vertebral rims of two adjacent vertebrae. In
these places the collagenous fibers penetrate into the
bony structure as Sharpey’s fibers. This special configuration of the fibers is particularly suitable for compensation of shear forces. The fibers additionally take care
of the forces transmitted from the nucleus pulposus as
a response on central as well as eccentric loads.
The nucleus pulposus, located eccentrically at the
transition between the central and the posterior part of
the intervertebral disc [1] contains glycosaminoglycanes,
which during youth and middle age comprise particularly chondroitine-4-sulphate, chondroitine-6-sulphate
and keratane-sulphate. However, in persons of advanced age, dermatane-sulphate is mainly found. The
high proportion of glycosaminoglycanes and the low
content of fibers result in a considerable capacity to
retain water. Accordingly, the nucleus pulposus has the
properties of a water-filled cushion.
The intervertebral discs exhibit a typical angioarchitecture which varies during the various periods of life
[2]. In foeti with a crown-rump length of 7 cm, blood
vessels can first be demonstrated between the lamellae
of the anulus fibrosus. However, these vessels never
reach the nucleus pulposus. Following the second year
of life, these blood vessels degenerate. Accordingly, the
moistness and hydration of the intervertebral discs decreases and the tendency towards changes characteristic
of advanced age is initiated. In healthy persons, the
system of vessels of the vertebral body is completely
separated from the corresponding system of the intervertebral disc by the cartilage endplates.
In adults, lateral fissures penetrating into the anulus
fibrosus and possibly subdividing the entire disc into
two halves, occur regularly in the area of the intervertebral discs of the cervical part of the spine. These
fissures were first described in 1858 by Hubert Luschka
[3] and designated as hemidiarthroses laterales. In 1893,
Trolard [4] called them articulationes uncovertebrales,
an expression presently still in use. The designations
‘Luschka-joints’ or ‘neurocentral joints’ are also frequently used. These fissures are not present in infants
and children of low age [2,5,6] and they can first be
observed in children at an age of 9 years [7]. This
author associates the development of these fissures with
the rising of the uncinate processes. Recently, the appearance of such a fissure was reported in a 1-monthold infant [8]. As far as this observation is concerned,
the presence of a true uncovertebral joint remains questionable however, as the fissures did not extend into the
anulus fibrosus. These fissures form in perfectly healthy
tissue of the intervertebral discs, and cannot be compared with the formation of fissures due to chondrosis
intervertebralis. After the formation of the fissures in
the anulus fibrosus, a joint-pseudocapsule develops, and
closes the fissure laterally. Within this capsule, vascular-
A. Prescher / European Journal of Radiology 27 (1998) 181–195
183
in shape, particularly in postmenopausal women in the
course of osteoporosis of the skeleton. As these changes
represent an entity of their own, they are not discussed
in more detail in this paper.
The chronic degenerative changes of the spine are
summarized as spondylopathia deformans (earlier synonyms: spondylitis deformans, polyspondylitis marginalis osteophytica or spondylchondrosis). As far as the
conditions for development of spondylopathia deformans are concerned, it was convincingly argued that a
degeneration of the intervertebral discs with a decrease
of their elasticity marks the onset of the disorder [10,11].
The subsequent inability to distribute loads equally in all
directions later causes the typical modifications at the
interface between the bones and the associated cartilage
in the spine and the minor joints of the spine (zygapophyseal joints).
The heading spondylopathia deformans can be subclassified, depending on the location of the degenerative
changes. In cases of spondylosis deformans the vertebral
bodies are affected while the term spondylarthrosis
deformans describes degenerative processes at the minor
joints of the spine.
Fig. 2. (a) Vertebra C6 and C7 completely fused due to synostosing
osteochondrosis (88 years, male). (b) Macerated cervical vertebral
column. Between C5 and C6 an isolated, heterotopic ossification
(arrow) lies in the region of the former anulus fibrosus (76 years,
male).
ized synovial folds have been observed. The details of
the formation of these fissures are presently still largely
unknown. The development of the cervical lordosis
results in a change of the configuration and the magnitude of the loads acting on the cervical spine. Therefore
the sections subsequently loaded are mostly located in
the region of C3 through C5. In that region, the lateral
fissures in the intervertebral discs also first appear. The
strong shear forces acting on the intervertebral discs,
particularly during rotational movements and lateral
inclinations, additionally increase the loads present in
this region. The formation of these fissures may therefore be assumed to be the consequence of large loads [9].
2. Degenerative disc disease
2.1. General features
During the human lifespan, the spinal column is
exposed to many continuously recurring loads, which
result in almost consequential changes in the morphological conditions. These changes can be described as
degenerative chronic processes on the intervertebral
discs, the zygapophyseal joints and the ligaments. Additionally the aging spine undergoes considerable changes
2.2. Chondrosis inter6ertebralis
As the age of a person increases, the quantity of water
present in the nucleus pulposus decreases and consequently the swelling by that water and the cushioning
effect previously present are reduced. In section, the
nucleus pulposus no longer bulges out, but has the
appearance of a dry, crumbling mass. The color has
likewise changed from a glassy greyish-blue to a yellowish color with a tendency towards brown. This change
in color is due to deposition of a brown coloring agent
belonging to the class of melanines [12,13] and resulted
in the designation of this change as ‘brown
degeneration’.
Additionally gaps and systems of fissures develop in
the intervertebral discs, which not are not only present
in the nucleus pulposus, but partly radiate also into the
anulus fibrosus. Occasionally these fissures appear in
roentgenograms brighter than the surrounding tissue, a
feature designated as ‘vacuum phenomenon’. Nitrogen
was demonstrated to be present in this system of fissures
[14]. All these changes, collectively described as ‘chondrosis intervertebralis’, result in considerable reduction
of the elasticity of the intervertebral disc, while the
height of the space occupied by the intervertebral disc
decreases only to a minor extent.
The variable anatomical manifestation of ‘chondrosis
intervertebralis’ as a gradual aging process and a decrease in water-content, is termed primary chondrosis
intervertebralis. In this context, chronic overloading
certainly represents an important factor. Identical morphological changes, which are however consequences of
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pathological changes outside the intervertebral discs,
e.g. following spondylolysis or abnormal deformation
of the spine, are designated as secondary chondrosis
intervertebralis [15].
If chondrosis intervertebralis has started, the degenerative destruction of the intervertebral disc continues
and experiences a transition into osteochondrosis intervertebralis. This stage is characterized by participation
of the cartilage endplates and gradual sclerosis of the
adjacent spongiosa of the vertebral body.
2.3. Osteochondrosis inter6ertebralis
Osteochondrosis intervertebralis has to be considered
as a process changing the structure of the intervertebral
disc into a condition prone to crumbling, accompanied
by a considerable reduction in the height of the space
occupied by the intervertebral disc. The material of the
former intervertebral disc presents as dry, crumbly,
grayish-white or brown-dark tissue between the vertebral bodies and frequently contains a cavity resulting
from the process of decomposition. Within such a
cavity, sequestra may be present as detached particles.
The process in the direction of crumbling may spread
into the inner layers of the anulus fibrosus, with the
outer fibrous systems remaining, and appearing convexly arched towards the outside [16]. The cartilage
endplates of the vertebral bodies are likewise affected
by the degenerative changes or even destroyed completely. Frequently numerous irregular proliferations of
cartilage and ossifications within small foci are located
on the endplates of the vertebral bodies (Fig. 1b,c). The
adjacent spongiosa of the vertebral body shows reactive
sclerotization since the function of the disc equalizing
and distributing pressures and shocks has largely decreased. The processes described may basically develop
in all intervertebral discs, but take place predominantly
in the two lowest lumbar and less frequently in the
lower cervical intervertebral discs. Osteochondrosis intervertebralis may materialize in two special manifestations. In one, the brittle bony structure of the endplates
of the vertebral bodies and the sclerotized spongiosa
may break like the two wings of a door, resulting in
erosive osteochondrosis [17]. In the other manifestation,
blood vessels grow into the intervertebral discs and
trigger an ossification, which can result in a complete
ossification of the intervertebral disc (synostosing osteochondrosis) (Fig. 2a).
primary calcification is the consequence of degenerative
processes, while secondary calcification is the result of
earlier inflammation (e.g. tuberculosis). Another classification separates chronically degenerative manifestations from inflammatory-rheumatoid calcification [18].
Chronic degenerative calcification is predominantly
located in the central thoracic and the upper lumbar
vertebrae and may be localized in the nucleus pulposus
as well as in the anulus fibrosus. In the jelly-like part of
the nucleus pulposus it appears as small, crumbly, white
spots, mostly associated with the system of fissures of
the nucleus pulposus.
In the anulus fibrosus the calcification appears as
irregular particles in small foci, often associated with
tears and necroses; 71% of the calcification is located in
the anulus fibrosus and 6.5% in the nucleus pulposus
[19].
In this context, the deposits of bony structures within
the intervertebral disc, manifesting as a consequence of
degenerative changes, merit attention. These ossifications may manifest themselves in two different ways:
First as a consequence of the healing of a chondrosis or
2.4. Calcification and ossifications
In 1858, Luschka [3] mentioned small foci of calcification in the area of the nucleus pulposus. However,
Schmorl was the first to investigate this manifestation
in more detail and to classify it into primary and
secondary forms [15]. According to his opinion, the
Fig. 3. (a) Osseous top-plate of a thoracic vertebra exhibiting an
irregular cavity resulting from a cartilaginous nodule (Schmorl’s
nodule) (72 years, male). (b) Frontal section through a cavity resulting from a cartilaginous nodule (Schmorl’s nodule). The arrow points
to the sclerotising osseous reaction (85 years, male).
A. Prescher / European Journal of Radiology 27 (1998) 181–195
185
Fig. 4. (a) Macerated cervical vertebral column with moderate, caudally orientated osteophytes localised in the midline from C2 to C5 (91 years,
female). (b) Macerated cervical vertebral column with large osteophytes, blocking the last two cervical and the first thoracic vertebral bodies (91
years, female).
an osteochondrosis intervertebralis. In the course of the
process of healing, blood vessels sprout from the vertebral bodies through defects in the cartilage endplates
into the degeneratively damaged intervertebral disc and
induce the formation of bony structures. In most cases,
these structures result in the blockade of the respective
segment of motion. This course of the healing process
may be described as healing and amending of the
degenerative processes by rigidization.
The second manifestation is present in the anterior
parts of the anulus fibrosus. Here, blood vessels may
sprout into radial or concentric fissures between the
fibers and trigger formation of bony structures. A
small, spongious bony body results, located between the
bony margins of two adjacent vertebral bodies (Fig.
2b). These small ossicles should not be confused with
osteophytes, isolated osteophytes or intercalate bones
due to spondylosis deformans. These ossifications of
the anulus fibrosus definitely do not represent a disturbance in the ossification of the vertebral rim as was
assumed in literature [20].
3. Dislocations of intervertebral tissues
3.1. General features
In the aftermath of chronic degenerative changes in
the intervertebral disc, a dislocation of tissues of the
intervertebral disc (of the anulus fibrosus as well as of
the nucleus pulposus) may occur. Such a dislocation
may take place in two major modes: as a protrusion or
as a prolapse. Bulging of an intervertebral disc in a
dorsal, lateral or ventral direction is called a protrusion.
In most cases, a protrusion derives from a fissure in the
inner zone of the anulus fibrosus. The tissue of the
nucleus pulposus pushes outwards and bulges the fibers
of the outer zone outwards while no tissue of the
nucleus pulposus will prolapse or escape. If the fibers of
the outer zone tear however, the pressurized tissue of
the nucleus pulposus is pushed outwards and a prolapse
of the intervertebral disc results. Depending on the
topology, such a dislocation of tissue may be directed
cranially or caudally or in the dorsal, dorsolateral or
ventral direction.
3.2. Schmorl’s nodules
Schmorl’s nodules of cartilage represent a dislocation
of tissue of the nucleus pulposus through the cartilage
endplate into the vertebral body. Subsequently proliferation of cartilage and reactive ossification may develop
in the vicinity of the tissue dislocated from the nucleus
pulposus. This ossification encloses the dislocated tissue
like a shell and segregates it from the spongiosa of the
vertebral body (Fig. 3a,b and Fig. 4).
The structure, which can now be demonstrated radiologically, represents the typical cartilaginous nodule
(Schmorl’s nodule) [21]. For compensation of a larger
Schmorl’s nodule, in juveniles an increased growth
opposite to the nodule may develop on the cartilage
endplate on the adjacent vertebral body and results in
an osseous projection resembling an exostosis (EdgrenVaino’s sign). If no cartilaginous or bony barrier is
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
established, more and more material of the nucleus
pulposus can enter into the vertebral body, resulting in
an extensive process, which should be termed a nucleus
pulposus prolapse or an intraspongious prolapse of the
nucleus pulposus [21]. Unfortunately, the actual
nomenclature reflects the conditions in an abbreviated
form only. Sometimes no distinction is therefore made
between the cartilaginous nodule and the intraspongious prolapse of the nucleus pulposus and both terms
are used synonymously.
Schmorl’s nodules are seen more frequently in men
than women, a condition attributed to larger spinal
loads in men [15]. Frequently the nodules are located in
the lower thoracic and in the lumbar region of the
spine. In most cases they are established in the center of
the vertebral body, since in that region the cartilage
endplate is thin because of the earlier passage of the
chorda dorsalis. The mechanical loads damage this
locus minoris resistentiae until it finally yields and the
pressurized tissue of the nucleus pulposus penetrates
into the spongiosa of the vertebral body. If the prolapsed tissue of the nucleus pulposus necrotizes, the
Fig. 6. (a) Anterolateral view of the macerated cervical vertebral
column (92 years, female). The intervertebral foramen between C3/4
is narrowed by an osteophyte of the zygapophyseal joint. (b) Anterolateral view of the macerated cervical column (65 years, male). The
intervertebral foramen between C3/4 is severe encroached by an
osteophyte of the zygapophyseal joint and an osteophytary structure
of the uncinate process.
Fig. 5. (a) Normally configured cervical vertebra, exhibiting the
typical morphology of the uncinate process (arrow). It is noticeable
that the lateral parts of the uncinate process are located medial to the
transverse foramen, whereas the dorsal parts lie anteromedial to the
intervertebral nerve sulcus (arrowhead) (36 years, female). (b) Cervical vertebra affected with severe degenerative changes. The uncinate
process (arrow) is bent outwards and narrows the intervertebral nerve
sulcus. Furthermore degenerative changes of the minor joint facets
can be seen (88 years, male).
cartilaginous nodule may become ‘resorbed’. If this rare
‘healing process’ does not take place, Schmorl’s nodules
may continue to exist throughout the remaining life of
the carrier.
3.3. Lateral or dorsolateral dislocation
In Schmorl’s autoptical series of investigations, a
dislocation of tissue of the nucleus pulposus in the
dorsal or dorsolateral direction takes place in 15.2% of
A. Prescher / European Journal of Radiology 27 (1998) 181–195
spines and shows a slight preference for the female sex
[15]. These prolapses are located in 95% of the cases
between L4 and L5, or between L5 and S1 [22].
In the cervical region such prolapses occur predominantly in the segments of motion C5/6 and C6/7 [23].
The dorsal prolapse is located between the dorsal side
of the intervertebral disc and the posterior longitudinal
ligament, in most cases slightly lateral to the ligament.
In the prolapsed tissue fine spots of calcification can be
demonstrated, which cannot be identified radiologically
however. Depending on the shape and morphology of
the dorsal or dorsolateral prolapse of the intervertebral
disc, various configurations can be distinguished: (1)
Dangling prolapse— in this case, tissue of the nucleus
pulposus issues from a fissure in the anulus fibrosus,
but may return into the initial place in the course of
particular motions. (2) Incarcerated prolapse — the prolapsed tissue is trapped in the fissure of the anulus
fibrosus in such a fashion that a return is impossible.
This configuration of a prolapse represents an early
stage of a sequestrated prolapse, in the course of which
the prolapsed material becomes detached and may subsequently be dislocated cranially or caudally. Such cases
are also described as ‘migrating prolapses’. If sequestrated material penetrates the dura mater and floats
subsequently in the liquor, an intradural prolapse exists, which only happens extremely rarely. In cases of a
dorsolateral prolapse, the displaced tissue is located in
the intervertebral foramen and causes a compression of
the spinal nerves. In the cervical region a compression
of the vertebral artery may also occur. The topographical location of the spinal nerves relative to the intervertebral disc is decisive for the efficiency of the
mechanism of compression. In the cervical and lumbar
region of the spine the intervertebral disc is located at
the same level as the spinal nerve in the intervertebral
foramen. For this reason a compression of the nerve
may occur easily in this region. In the thoracic region,
the spinal nerve is located cranially of the intervertebral
disc behind the vertebral body. Accordingly, the nerve
will rarely be contacted by the prolapse and the symptoms of nerve compression are seldom observed.
3.4. Ventral dislocation
Ventral dislocation of intervertebral disc tissue may
occur in two different ways: The anteriorly prolapsed
tissue rarely penetrates ventrally between the frontal
side of the spine and the anterior longitudinal ligament
cranially or caudally. Such cases are therefore of only
minor importance in practice [15].
Schmorl [21] drew the physician’s attention to a
second form of ventral dislocation of intravertebral disc
tissue. At the inner edge of the ossified vertebral rim a
stepwise transition exists from the smooth rim into the
porous endplate of the vertebral body (Fig. 1b) and
187
forms a locus minor resistentiae, into which tissue of
the nucleus pulposus may penetrate. If this should be
the case, the prolapsed tissue works its way in an
oblique direction outwards through the bone, finally
detaching the ventral edge of the vertebral body as a
triangular piece of bone [21]. The prolapsed tissue
subsequently becomes crushed by the now abnormally
mobile detached piece of bone and on the corresponding areas of the bones a fibrous-cartilaginous coating
develops as some kind of pseudoarthrosis. These manifestations are mainly observed at the upper edges of the
lumbar vertebrae and at the upper edge of the sacral
bone. Based on pathological investigations an incidence
of 5% was quoted [21]. In the course of a series of
radiological investigations an incidence of 1% was
found [24]. The difference was explained by the impossibility of identifying all pieces of detached bone radiologically.
Following
the
same
principle
of
materialization, lateral or infrequently even dorsal
pieces of bone may break off the edges of the vertebral
bodies [25]. The triangular bony elements resulting
from these detachments from the edges of the vertebrae
were formerly considered as persistent epiphyses of the
vertebral bodies [20,26], an opinion which has been
disproved by extensive investigations [21,24,27–29].
The anterior detachment of bone from the edge of the
vertebral body has to be distinguished unambiguously
from pieces of bone torn from the edge of the vertebra
traumatically [30]. Degenerative detachments of the
anterior edge of the vertebral bodies are only of minor
clinical importance [24].
4. Spondylosis deformans
4.1. General features
In cases of spondylosis deformans, bony osteophytes
and excrescences develop in the region of the vertebral
bodies. These manifestations represent chronic degenerative changes, which are predominantly located in the
cervical, lower thoracic and lumbar region of the spine.
The incidence increases with advanced age. In
Schmorl’s series of 4253 specimens of the spine collected in the course of autopsies, at an age of 49 years,
60% of female and 80% of male spines showed osteophytes of the vertebral bodies. At an age of 79 years,
both sexes were equally affected in approximately 95%
of cases [15]. The results of a large-scale investigation of
spondylosis deformans in the cervical region of the
spine were published by Aufdermaur (1960) [23] who
also added comments on the interpretation of the statistically determined incidences during various periods of
life. A connection between the manifestation and the
extent of this disorder and the occupational loads and
stresses seems to be questionable and is discussed con-
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
troversially in the literature [31,32]. Concerning the
initiation of spondylosis, two different pathogenetic
concepts are currently discussed: the first hypothesis is
based on the extensive investigations by Schmorl and
has been discussed exhaustively [15]. In his opinion, the
formation of fissures in the outer zone of the anulus
fibrosus (the ‘Randleistenanulus’ according to Schmorl)
is the cause of subsequent changes. The anatomical
conditions at the ‘Randleistenanulus’ are characterized
by the prominent fibers of Sharpey, which extend into
the bony structure of the ossified vertebral rim of the
vertebral body. If this fixation is reduced or torn as a
consequence of the formation of a fissure, or even
suspended, the intervertebral disc maintains less connection with the adjacent vertebral bodies and may
engage in unphysiological movements. These circumstances may cause excessive loading of the anterior
longitudinal ligament and result in the formation of
bony peaks at the insertions of the ligament. If the
nucleus pulposus has not yet been degenerated, pressure
exerted against the anterior longitudinal ligament
causes additional pulling forces on the points of ligament-insertion. This concept explains the observation
of particularly large osteophytes predominantly in persons in which the nucleus pulposus has not degenerated
and the height of the spaces occupied by the intervertebral discs has dropped only to a minor extent. This
interpretation of the processes involved clearly confirms
the earlier opinions [10,11] of the cause for spondylosis
deformans to be located in the intervertebral discs and
not in the vertebral bodies.
A second concept addressing the development of
spondylosis deformans has been presented by Collins
[33], who also confirms the degeneration of the intervertebral disc to mark the early stage of the disorder and
believes the special anatomical conditions in the region
of the anterior longitudinal ligament to be responsible
for the development of the osteophytes. He claims this
ligament retains tissue from the intervertebral disc expanding as a consequence of the formation of fissures
and the detachment of the ‘Randleistenanulus’. Laterally, where the anterior longitudinal ligament ends comparatively sharply and abruptly, changing to a weak
membrane of connective tissue, such a dislocation of
tissue is not stopped, but results in detachment of the
periost from the vertebral body. Consequently, periosteal development of bone starts, resulting in the
formation of osteophytes.
A unilateral partisanship for the first or second concept does not appear to be advisable, since the typical
manifestations of spondylosis deformans very likely
develop both ways, in a combined action [30].
Evidence supporting the concept of Collins [33] is the
ossifications histologically frequently to be found below
the anterior longitudinal ligament and showing no connection or at most a secondary extension to the anterior
longitudinal ligament only. Details observed at the
cervical region of the spine, such as the osteophytes
located ventrally (Fig. 4a) in most cases also favor the
concept of Collins. As the anterior longitudinal ligament of the cervical region of the spine is much weaker
than in the thoracic or lumbar region, pressing back of
the tissue of the intervertebral disc will be much less
effective. This condition may be advantageous for the
formation of ventral osteophytes, as this has been
observed.
4.2. Spondylosis cer6icalis and spondylosis
unco6ertebralis
The degenerative changes in the cervical region of the
spine have to be subdivided into the actual spondylosis
cervicalis and the spondylosis uncovertebralis.
The capacity for motion is most pronounced in the
region of the segment of motion C5/C6 and continuously decreases cranially. This anatomical condition
correlates with the observation that spondylosis deformans manifests mostly in the region of the segments
C5/C6 and C6/C7 and seldom occurs cranially [23].
Fig. 7. (a) Cervical vertebra exhibiting a typical, dorsal located
accessory transverse foramen on both sides (arrows) (72 years, male).
(b) Cervical vertebra exhibiting a medial located, pseudoaccessory
transverse foramen (arrow) in an osteophytary addition of the vertebral body (92 years, female).
A. Prescher / European Journal of Radiology 27 (1998) 181–195
189
Fig. 8. (a) Macerated thoracic vertebral column (88 years, male) exhibiting strong, fused osteophytes predominantly on the right side. (b) Frontal
section through two thoracic vertebral bodies with marked osteophytes on the right side. It is clearly seen that the osteophytes are located
somewhat below or above the vertebral limbus (72 years, male).
Spondylosis deformans in the cervical region is characterized by osteophytes primarily developed in the
ventral direction (Fig. 4a), because of the weakly developed anterior longitudinal ligament. Osteophytes developed in the dorsal direction also occur but are often
only of minor size. The configurations of the osteophytes are very diversified, and they can merge,
blocking the respective segment of motion (Fig. 4b).
Osteophytes never start at the edges of a vertebral
body, but only slightly below [23]. They are composed
of lamellar bone structure and contain a more or less
compact spongiosa, the marrow spaces of which are
connected to the marrow spaces of the vertebral bodies.
Osteophytes on the uncinate processes characterize
the spondylosis uncovertebralis [30]. The various
configurations of spondylosis uncovertebralis can also
be observed in the region C3 – C7. Distinct manifestations are however found predominantly on the lower
segments C5/C6 and C6/C7 [30,34]. The regular uncinate processes are positioned higher and steeper in the
cranial region of the cervical spine than in the caudal
region. Additionally, in most cases they are dorsolateral, i.e. where they assume a topographical connection
to the intervertebral canal, and with a flatter shape than
in the lateral region, where they are located next to the
transverse foramen (Fig. 5a). A flat uncinate process is
a preferred place for the development of osteophytes
[30]. Fully developed osteophytosis however results in
brimming of the uncinate process into a shape similar
to a console. Such a console may have a height of 2–3
mm and accordingly almost define a horizontal plateau
on which the next vertebral body above rests with a
corresponding lateral trough.
In cases in which the lateral brimming of the uncinate processes is located in the dorsal region, a narrowing of the intervertebral foramen results (Fig. 5b),
causing a corresponding compression of the spinal
nerve. A simultaneous spondylarthrosis will worsen the
situation, since in such a configuration, osteophytes
also grow from the dorsal direction into the intervertebral foramen and the spinal nerve will partly be trapped
by these projections like the jaws of pliers (Fig. 6b).
If the console-shaped brimming also takes place in
the opposite region of the uncinate process at the
adjacent higher vertebral body, such an arthrotic osteophyte can project into the transverse foramen. A
perforation and formation of a hole may develop in the
osteophyte, simulating a partitioned transverse foramen
(Fig. 7b). The true partitioned transverse foramen is an
insignificant anatomical variety, observed frequently,
particularly in the caudal cervical vertebrae for the
passage of veins. This accessory transverse foramen is
regularly located dorsal of the transverse foramen (Fig.
7a) while the pseudoaccessory transverse foramen is
located medial. Furthermore it is closed by connective
tissue or fibrous cartilage. The osteophytes developed at
the anterior section of the uncinate processes may
compress the vertebral artery from the medial direction.
Such a configuration has quite some significance, as
chiropractical manipulations may result in dissection of
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
Fig. 9. (a) Thoracic vertebra (Th9) exhibiting a typical dorsal osteophyte (arrow). This osteophyte is shaped like the flame of a candle and arises
somewhat below the ossified vertebral limbus (76 years, male). (b) Dorsal aspect of two thoracic vertebral bodies (Th11 – 12) exhibiting osseous
changes due to a dorsal cartilaginous nodule (Schmorl’s nodule). The arrow points to an irregular cavity, surrounded by an irregular, prominent,
osseous margin. The ossified vertebral rim is destroyed (68 years, male).
the vertebral artery on the osteophytes of the uncinate processes with serious consequences for the
blood supply to the vertebro-basilar region [35].
4.3. Spondylosis thoracalis
Inspection of a macerated preparation will be more
instructive for the characteristic details of pronounced
spondylosis thoracalis than any description (Fig. 8a).
The osteophytes always arise slightly below or above
the ossified rim of the vertebral body (Fig. 8b). They
may contact each other, interlock mutually and
finally fuse together. They are frequently located below the anterior longitudinal ligament and ossification
of this ligament will be a secondary phenomenon
only. The large thoracic osteophytes will cause a
blockage of the respective segments of motion (Fig.
8a).
The formation of osteophytes in the region of the
thoracic part of the spine occurs predominantly ventrolaterally, but also dorsally (Fig. 9a). However,
these dorsal osteophytes are small in size, shaped like
the flame of a candle and are mostly located paramedian. The low extent of the dorsal osteophytosis is
based on the anatomical conditions determined by the
posterior longitudinal ligament. This ligament inserts
primarily at the rear of the intervertebral disc and
with only a few fibers at the vertebral body. The
vertebral body is not available for insertion of a ligament across a large area, as it shows the basivertebral
foramen offering passage for voluminous veins. The
typical dorsal osteophytes (Fig. 9a) must be differentiated from calcification and ossification forming
around the ‘posterior Schmorl’s nodules’. These bony
objects are located in an irregular pattern at the back
edge of the vertebral body and are frequently associated with depressions harboring these nodules (Fig.
9b).
4.4. Spondylosis lumbalis
The manifestations of spondylosis lumbalis are similar to the configurations in spondylosis thoracalis,
except for their substantially larger size, which may
reach grotesque dimensions, and the higher incidence
of isolated bony elements located as intercalate bones
between the osteophytes. In cases of pronounced decrease in the height of the intervertebral discs, the
spinous processes of adjacent vertebra may contact
each other. Between the grinding bony parts sclerotization, grinding-facets and also pseudoarthroses may
develop (Fig. 10a–c). These manifestations are known
as osteoarthrosis interspinosa [36], kissing spines or
Baastrup’s disease.
As a peculiarity, a helmet-shaped sclerotization of
the spongiosa on top of an intervertebral disc may
develop, in most cases in the two lower lumbar vertebral bodies. This manifestation, in most cases seen
against a generally degenerative background, is designated spondylosis hemisphaerica or Dihlmann’s syndrome [37,38].
A. Prescher / European Journal of Radiology 27 (1998) 181–195
191
5. Spondylarthrosis
5.1. General features
The term ‘spondylarthrosis’ describes degenerative
changes in the zygapophyseal joints. Unfortunately, in
some careless generalizations this terminology is also
used in the current literature for changes in the intervertebral discs and vertebral bodies. This practice
should be discontinued to maintain a clearly defined
nomenclature without ambiguities. A continuously increasing incidence of degenerative changes in the minor
joints of the vertebrae, particularly in the cervical and
lumbar region of the spine, is seen in patients of more
than 30 years of age, as these joints are substantially
loaded by the large range and frequency of motion [39].
Changes in the intervertebral discs (chondrosis intervertebralis and osteochondrosis intervertebralis) resulting in a decrease in the height of the intervertebral disc,
are assumed to be responsible for the pathogenesis of
spondylarthrosis. Such a decrease in height results in
loosening of the segment of motion and in unphysiolog-
Fig. 10. (a) Lateral aspect of two lumbar vertebra (L2–3), exhibiting
typical ‘kissing spines’ (86 years, female). (b) Cranial aspect of the
surface of the spinous process of L4. Irregular osteophytary additions, grinding facets, cysts and eburnisations can easily be seen. (c)
Caudal aspect of the surface of the spinous process of L3. Corresponding changes, as described in (b) are visible.
Fig. 11. (a) Anterior aspect of the atlas (89 years, male). A semilunarshaped arthrotic coulisse (arrows) is located on the anterior arch. (b)
Posterolateral aspect of a ‘crowned odontoid’ (87 years, male). The
arrow points to the typical osteophytary addition, which exhibits
cysts and trabeculae at its dorsal side.
ical loading of the minor joints of the vertebral column.
The decrease in height also causes a caudal dislocation
of the inferior articular processes and stressing of the
capsules of the joints. Additionally a dorsal dislocation
of a vertebra (retrolisthesis) may develop. All three
factors mentioned contribute to the degenerative
changes in the zygapophyseal joints. In this context
however, the simple pathogenic concept ‘decrease in the
height of the intervertebral discs and subsequent irregular loading of the minor joints of the vertebral column’
only partially represents the whole truth, for time and
again, cases with manifest osteochondrosis intervertebralis are seen in which no spondylarthrosis of the
associated minor joints of the vertebrae is present at all.
On the other hand, cases with considerable degenerative changes of the zygapophyseal joints without simultaneous damage to the intervertebral discs are known.
Within these inconsistencies, the observation must be
mentioned that the spondylarthrosis develops most frequently in the segment Th 4/5 [39]. However, this
segment of motion exhibits the lowest degree of mobility of the entire spine. Other, unknown factors, must
therefore be considered contributing to the pathological
concept just presented. The morphological manifestations of spondylarthrosis do not differ from the manifestations in cases of arthrosis deformans of the large
joints. Progredient damage of the cartilage, showing
fissures, grinding-facets and eburnizations have been
observed. The subchondral lamella also show strong
sclerotization and cysts may develop. Furthermore typi-
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
cally osteophytes may be formed at the joint facets. The
meniscoid folds of the minor joints of the vertebral
column are much less delicate and show fibrozation and
hyalinization. Frequently detritus, consisting of fragments detached from the cartilage, rests in the joints.
The articular capsule shows ribbon-like fibrozations
causing isolation of the joint from the surrounding
structures [30]. Since spondylarthrosis exhibits special
peculiarities in the various parts of the spine resulting
from the anatomical conditions typical for the respective section of the spine, the characteristic details are
presented separately below.
5.2. Spondylarthrosis cer6icalis and arthrosis of the
median atlantoaxial joint
In the cervical region of the spine some peculiarities
result from the special morphology of the two upper
cervical vertebrae. In this context, the expression
‘spondylarthrosis cervicalis’ not only covers the degenerative processes in the minor joints of the vertebrae,
but also the degenerative processes of the atlantooccipital joints, of the median atlantoaxial joint and the
Fig. 13. (a) Inferior articular processes of a lumbar vertebra (L4)
showing severe degenerative changes. Not only are osteophytary
additions, grinding facets, cysts and eburnisations visible, but also a
grotesque deformation is present (82 years, female). (b) Superior
articular processes of L5 corresponding to the inferior articular
processes shown in (a). A grotesque deformation and all signs of
degenerative changes document a severe spondylarthrosis lumbalis.
Fig. 12. (a) Cranial aspect of a cervical vertebra, showing normally
figured articular facets (36 years, female). (b) Cranial aspect of a
cervical vertebra exhibiting serious degenerative changes of the articular facets. Osteophytary additions, cysts, grinding facets and enlargement of the facets are present and document a severe
spondylarthrosis cervicalis (88 years, male).
lateral atlantoaxial joints. Only in the median atlantoaxial joint do the degenerative changes represent a
major disorder however, resulting in extensive and
characteristic morphological changes. According to radiological investigations, persons above 61 years of age
show degenerative alterations of this joint in 88% of the
cases [40]. The morphological changes in the median
atlantoaxial joint are on the one hand characterized by
the typical joint-changes seen in degenerative disorders.
On the other hand, manifestations specific for this
location are also seen. At the upper edge of the anterior
arch of the atlas, bony excrescences are established in a
semilunar shape, resembling a coulisse (Fig. 11a), which
manifest on a.p. roentgenograms as a peridental aureole. These bony appositions may isolate themselves,
and subsequently form independent accessory elements
[41], located between the anterior rim of the occipital
foramen and the anterior arch of the atlas. This
‘coulisse of the atlas’ may also extend substantially in
the cranial direction, resulting in physical contact with
the anterior border of the occipital foramen. The
A. Prescher / European Journal of Radiology 27 (1998) 181–195
coulisse of the atlas resulting from arthrosis can also
get bent in the dorsal direction and be placed over the
apex dentis like a roof. This configuration was termed a
‘Processus opercularis atlantis’ [42]. Recently a picture
of a typical specimen was published [41]. The degenerative changes in the median atlantoaxial joint cause
typical manifestations on the dens axis itself. Here the
anterior articular facet is partly dislocated in the cranial
direction by rolling action, resulting in a bony addition
in the shape of a coulisse at the anterior edge of the
apex dentis (Fig. 11b). In the literature, this configuration is designated as ‘crowned odontoid process’,
‘crowned dens’, ‘peridental aureole’ or ‘arthrotic
coulisse of the dens’ [43 – 46]. This coulisse of the dens
is characterized by the smooth structure of the frontal
area (possibly forming an articulation with a coulisse of
the atlas) and by numerous cysts on the back area and
structures similar to trabeculae (Fig. 11b). Parts may
break away from the coulisse and turn into independent
bony elements [43] which in the course of differential
diagnosis must not be mixed up with isolated ossicles of
phylogenetic origin.
The typically degenerative changes of the ‘crowned
odontoid’ and in the coulisse of the atlas should not be
193
mixed up with calcination (tendinitis calcarea) or ossification of the ligaments. Spondylarthrosis cervicalis also
manifests at the zygapophyseal joints of the cervical
region of the spine, resulting in a grotesque deformation and enlarging of the joint surfaces due to osteophytary additions (Fig. 12a,b). As the anterior parts
of the zygapophyseal joints approach the intervertebral
foramen directly from the rear, such osteophytes result
in considerable reduction of this narrow passage (Fig.
6a) and in compression of the spinal nerve. In cases
with simultaneous spondylosis uncovertebralis, the
compression of the spinal nerve, which, figuratively
speaking, is caught by the osteophytes partly ‘between
the jaws of pliers’ (Fig. 6b), represents a particularly
serious condition. Narrowing of the intervertebral foramen is caused most frequently solely by spondylosis
uncovertebralis, less frequently by a combination of
spondylosis uncovertebralis and spondylarthrosis, and
least frequently solely by spondylarthrosis [23,34].
5.3. Spondylarthrosis thoracalis
Spondylarthrosis thoracalis shows no significant deviations from the common arthrosis deformans. The
descension of the inferior articular processes, initiating
formation of bulges similar to consoles in the arcus
vertebrae of the next vertebra below and thus limiting
the degree of descension, is noteworthy however. If the
spaces occupied by the intervertebral discs experience
further reduction in height, the vertebral bodies tilt
forwards to some extent and increased kyphozation
takes place. Because even in cases of pronounced
spondylarthrosis thoracalis, major osteophytes will
rarely grow into the intervertebral foramen, compression of the spinal nerves is only observed infrequently.
Other conditions reducing the incidence of compression
of the nerves by prolapses of intervertebral discs from a
ventral direction are the protected cranial location of
the spinal nerves and the comparatively large dimensions of the intervertebral foramina.
5.4. Spondylarthrosis lumbalis
Fig. 14. Median-sagittal section of the lumbar vertebral column (82
years, female). The arrow points to the typical cavity of a cartilaginous nodule (Schmorl’s nodule). Furthermore a remarkable anterior
dislocation of L4 can be seen and represents a typical pseudospondylolisthesis (M. Junghanns).
The degenerative changes developing in the course of
this disorder are distinctly serious and result in
grotesque deformation of the zygapophyseal joints (Fig.
13a,b). All manifestations of arthrosis deformans, such
as cysts, porozation, grinding-facets, eburnizations and
joint-deformations may simultaneously be seen in a
great variety of combinations. In cases of advanced
spondylarthrosis lumbalis, a vertebra may slide forwards (Fig. 14), predominantly in females. In most
cases the vertebra L4 is involved. This anterior dislocation takes place while the arch of the vertebra is intact.
No relationship with spondylolisthesis exists therefore.
Junghanns [47,48] noticed this phenomenon and termed
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A. Prescher / European Journal of Radiology 27 (1998) 181–195
it ‘Pseudospondylolisthesis.’ Cases of pseudospondylolisthesis show pronounced spondylarthrosis of the
minor joints of the affected section of motion, which is
usually less severe in the adjacent joints. Based on this
observation, a hypoplastic or excessively flat development of the articular facets between L4 and L5 triggering this anterior sliding dislocation has therefore been
assumed. The resulting unphysiologic distribution of
the loads then causes the development of substantial
spondylarthrosis in this segment of motion. This pseudospondylolisthesis (M. Junghanns) has however to be
strictly set apart from spondylolisthesis in cases of
spondylolysis, mostly affecting L5 and predominantly
occurring in men. At the present time, no final rating of
the role of the inherent factors in the manifestation of
pseudospondylolisthesis is possible however [49,50].
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