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The vascular supply of vertebral structures. Gross anatomyRabbit and monkey

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The Vascular Supply of Vertebral Structures.
Gross Anatomy: Rabbit and Monkey'
DONALD L. STILWELL, JR.
Department o f A n a t o m y , S t a n f o r d University, California
Vascular supply and vascular tissue play
a prominent role in the function of bone,
and must be a basic consideration in its
health and disease. The present paper presents the initial results of an investigation
of blood supply, especially arterial, of vertebral structures in two laboratory mammals, rabbit and monkey, and in man.
Only the gross supply in lower animals
will be presented here, incident to studies
now being conducted on the relationship
between vascularity and growth in normal
and certain pathological conditions.
Previous studies of vertebral vessels have
been limited largely to man: Hanson
('26), Ubermuth ('29), Willis ('49), Ferguson ('SO), and Harris and Jones ('56).
Batson ('40, '55, '57) and Anderson ('51 ),
among several others, have studied the
vertebral venous system in man and
monkey.
MATERIALS AND METHODS
Six domestic albino rabbits (Oryctolagus cuniculus) between 4 and 6 months
of age, and 4 monkeys (Cynomolgus and
M. rhesus) about 18-36 months, were
used. A variety of vascular masses was
employed. Neoprene latex2j3 (Smith and
Henry, '45), vinyl plastic,z and acrylic
plastic4 (Batson, '55, '57).
Corrosion specimens were prepared by
immersion a variable period of time in
5-10 % potassium hydroxide, long enough
to remove most soft tissues, but before the
bones and intervertebral discs were attacked. After washing overnight in running tap water the connective tissues were
further dissolved in "Clorox," 50% in
water. Specimens were preserved in 5%
formaldehyde for study and photographing.
RESULTS
The blood vessels of vertebral structures
are illustrated by photographs in figures
1-16. Figures 1-6 summarize the locations of nutrient foramina.
1 . Cervical
Vertebrae, joints, ligaments, discs, and
deep muscles were supplied mainly by
branches of the vertebral artery, and to a
lesser extent by ascending cervical and
deep cervical arteries. The ascending cervical took origin from the inferior thyroid
artery, as in man, or the costocervical
trunk (fig. 7), coursing ventro-laterally
along transverse processes. Small twigs
connecting this artery with the vertebral or
its rami passed between the processes.
The deep cervical artery (fig. 8 ) usually
arose from the costocervical trunk or dorsal aspect of the subclavian artery, then
passed between transverse processes of the
first two thoracic vertebrae, or above the
neck of the first rib. Its upward course
lay near the laminae of neural arches, and
it often communicated with the descending portion of the occipital artery. In
their paths, ascending and deep cervical
arteries supplied adjacent muscles, Iigaments, joints, and periosteum.
Veins formed extensive longitudinal and
circumferential anastomoses external to
the arches and connecting ligaments,
draining into vertebrals and longitudinal
' Supported by a grant of the National Science
Foundation.
Ward's Natural Science Establishment, Inc.,
3000 Ridge Road, Rochester 9, New York.
3Rubber Chemicals Division, E. I. duPont de
Nemours and Co., Wilmington 98, Delaware.
H. D. Justi and Son Co., High Polymer Research Laboratory, 32nd and Spring Garden
Streets, Philadelphia 4, Pennsylvania.
169
170
DONALD L. STILWELL, JR.
which were directed laterally and dorsally,
arching somewhat upward (fig. 12). Before giving off dorsal rami lateral to the
bodies, small twigs were delivered to the
overlying pleura, to dorsal mediastinal
structures, and to vertebral periosteum.
Intercostal arteries, excepting branches of
their dorsal rami, were not otherwise concerned with the supply of spinal structures.
Opposite the intervertebral foramina
dorsal rami divided into ascending muscular, descending muscular, and spinal
rami (fig. 12). The first two directly entered deep dorsal muscles, breaking up
into numerous divisions. Overlapping
fields were supplied by muscular branches
of adjacent segments. The dorsal articulations (zygapophyses) were served by
twigs of a muscular artery as it passed
nearby.
Spinal rami of the dorsal ramus usually were two in number: ( a ) an ascending (radicular) spinal ramus, commonly
from the proximal portion of the dorsal
ramus, which entered the foramen at its
cranial end; ( b ) a slightly larger descending (osseous) spinal ramus arising near
the terminus of a dorsal ramus. The latter
entered the caudal part of an intervertebra1 foramen, descending mediaIward to
enter a vascular foramen of the body (fig.
13). Dorsal arteries of the epiphysis in
the rabbit usually were branches of the
osseous (descending) artery. Epiphyseal
vessels were lacking in the vertebral body
of the monkey, as will be remarked on
later.
3 . Lumbar
Segmental branches of the aorta divided
into pairs of lumbar arteries which encircled the vertebrae. Figures 14 and 15
show their course and branchings. The
most caudal lumbar artery arose from the
median sacral. Anterior to their point of
division into dorsal and ventral rami, muscular and periosteal twigs were delivered
to psoas muscles and vertebral bodies.
2. Thoracic
The ventral ramus was directed to muscles
Figures 12 and 13 summarize the plan on either surface of a transverse process,
of distribution of arteries to the thoracic while the dorsal ramus branched opposite
spine. The costocervical trunk served as intervertebral foramina into spinal and
the source of intercostal arteries to the muscular rami, following the Dattern at
upper two to four thoracic segments. Be- thoracic levels. Overlap of adjacent seglow this the aorta gave off pairs of (poste- ments again was observed. A nutrient forrior) intercostal and subcostal arteries, amen often seen in the rabbit at the base
venous channels in the spinal canal. The
last have been adequately reviewed in the
excellent papers by Batson ('40, '55, '57).
Much the same conditions held in both
rabbit and monkey. Figures 9-11 show
details of the arterial supply of cervical
structures of the rabbit. Bodies (centra)
were supplied with arterial twigs which
entered at three distinct areas. Two of
these were at their ventro-lateral aspects
(fig. 9 ) ; the other lay dorsally and centrally, where large vascular foramina constantly occurred (fig. 11). Ventral rami
of the vertebral artery were directed between transverse processes, variably to
divide into ascending and descending
branches, which were directed to the
ventro-lateral nutritive foramina, epiphyses, deep ventral muscles, longitudinal ligaments, periosteum and ventral aspect of
the joint capsules (fig. 9).
Spinal rami to structures within the vertebral canal arose dorsally from the vertebral artery (figs. 10, 11). External to
intervertebral foramina they divided into
ascending and descending spinal rami.
As can be seen, the ascending vessel usually redivided to form radicular, meningeal, and osseous vessels, while the descending branch, somewhat smaller, often
communicated with an ascending spinal
ramus of the segment below. Radicular
arteries followed ventral roots to the spinal
cord, forming a longitudinally continuous
anterior (ventral) spinal artery. Vessels
from the basilar junction of vertebral arteries contributed to, or drained the cephalic end of the spinal artery (fig. 10, top).
Anastomosis between the basilar artery
and several spinal rami of the vertebral
was thus established via the anterior spinal
artery. It is possible that circulation to
the spinal cord and medulla, as well as to
other vertebral structures, remains uninterrupted, despite obstruction of one vertebral artery or its segmental branches.
VESSELS O F VERTEBRAL C O L U M N
of mammillary processes was penetrated
by a small artery (fig. 14).
Spinal rami were duplicated, as at thoracic and cervical levels (fig. 16). Considerable variation was observed.
Vertebrae were supplied by osseous arteries entering dorsally into the body, on
the arch near mammillary processes and at
the ventral base of transverse processes.
Except for those to periosteum no arterial
vessels in the rabbit appeared to enter
lumbar bodies on their ventral aspect,
as they did in cervical, and variably in
thoracic vertebrae.
4 . Intervertebrul discs, joints, muscles
The anulus fibrosus appeared not to be
supplied by vessels of a size demonstrable
in these studies. A later paper will show
that arterioles and venules form a rather
definitely oriented vascular plexus at the
surface of the disc. These vessels appeared to be continuous with those of the
adjacent periosteum.
Joints and deep dorsal vertebral muscles were usually supplied by terminal
muscular branches of the dorsal rami
(figs. 8, 12, 1 4 ) . Longitudinal, interspinous, and flaval ligaments were supplied by
twigs of vessels supplying nearby periosteum and muscle. Since these vessels were
often of arteriolar size they were not satisfactorily demonstrated by the gross
methods employed.
5. Differences between rabbit
and monkey
Only minor differences were observed.
Vessels to bodies, arches, meninges, joints,
and muscles had a pattern common to both
animals, and arose from similar sources.
Corresponding terminology was applied.
In these young rabbits well developed
discoid epiphyses were present on cranial
and caudal surfaces of the vertebral bodies. They were supplied by epiphyseal
branches of the spinal rami (fig. 1 3 ) .
These secondary centers of ossification do
not appear in the calcified epiphyseal cartilages of man and monkey until near
puberty. Separate epiphyseal nutritive vessels were therefore not observed in the immature monkeys.
Schmorl (’29) and Bick (’51) have described these peripherally placed, ring-like
171
epiphyseal ossifications in man, and have
called them respectively “Randleisten” and
“ring apophyses.” The time of their initial
appearance in the monkey, the sources of
their blood supply, and fusion with the
vertebral body await further investigation.
Deficiencies in the cartilage plates,
shown in figures 5 and 6, do not represent
patent vascular canals, but probably are
empty remnants of fetal cartilage canals.
Finer details of vessels to the growth cartilage, the epiphyses of rabbit vertebral
bodies, and the anulus fibrosus will be discussed and illustrated in a later paper,
devoted to microscopic aspects of spinal
vessels.
DISCUSSION A N D SUMMARY
Corrosion specimens of intravascularlyinjected colored acrylic or vinyl plastic,
and Neoprene latex were used to demonstrate the gross sources and distribution of
vessels to vertebral structures in young
rabbits and monkeys. Major attention was
paid to arteries. At thoracic and lumbar,
levels these vessels arose from segmental
branches of the aorta, and in the cervical
region from the vertebral, ascending, and
deep cervical arteries.
The bodies (centra) were supplied by
small arteries which entered through (variable) foramina placed ventro-laterally and
dorsally. The vertebral arches usually had
a small nutritive foramen located dorsally
on a lamina or near the base of a mammillary process (lumbar and lower thoracic). Another foramen usually was located
ventrally at the base of the transverse
process.
Joints and deep dorsal muscles were
supplied by ascending and descending
muscular branches of the dorsal rami.
Ligaments received twigs of arteriolar size
from vessels of overlying muscles.
Spinal rami, which supplied structures
within the vertebral canal, arose in the
cervical region directly from the vertebral
artery, and at thoracic and lumbar levels
from segmental arteries, near the origins
of dorsal primary rami. As a rule spinal
rami were duplicated, consisting of ascending and descending arteries, which
entered cranial and caudal ends of the
intervertebral foramina, to supply meninges, spinal cord, and body. These last
172
DONALD L. STILWELL, JR.
vessels are referred to respectively as meningeal, radicular, and osseous branches of
spinal rami. Some variability in their
mode of branching was observed, but a
similar pattern of distribution was recognized at all vertebral levels, as will be
seen in the accompanying photographs.
Small twigs to the dorsal aspect of epiphyses of the bodies of the rabbit arose from
radicular or osseous arteries. These were
not observed in monkeys, since cranial and
caudal body epiphyses had not yet made
their appearance.
Overlap and communication of arteries
of adjacent spinal segments were observed
in the continuity of anterior spinal arteries, and in anastomosis and imbrication
of ascending and descending branches of
spinal and muscular branches of the dorsal rami.
A similar distribution and overlap was
noted previously in the sensory innervation
of these vertebral structures (Pedersen et
al., '56; Stilwell, '56). Transverse and
longitudinal communications were seen
on both anterior and posterior aspects of
the centra (figs. 1, 4, 5, 9, 12, and 1 3 ) .
It is clear that bony and soft tissues associated with the vertebral column are
supplied bilaterally and bisegmentally.
LITERATURE CITED
Anderson, R. 1951 Diodrast studies of the
vertebral and cranial venous systems. J. Neurosurg., 8: 411-422.
Batson, 0. V. 1940 Function of vertebral veins
and their role i n spread of metastases. Ann.
Surg., 112: 138-149.
1955 Corrosion specimens prepared
with a new material. Anat. Rec., 121: 425
(abstract).
1957 The vertebral vein system. Am.
J. Radiol. Rad. Ther. Nuc. Med., 78: 195-212.
Beadle, 0. A. 1931 The intervertebral discs:
etc. Medical Res. Council, Special Report Series,
161: 1-79. His Majesty's Stationary Office,
London.
Bick, E. M. 1951 The ring apophysis of the
' human vertebra.
J. Bone Jt. Surg., 33A: 783787.
Ferguson, W. R. 1950 Some observations on
the circulation in foetal and infant spines.
Ibid., 32A: 640-648.
Hanson, R. 1926 Some anomalies, deformities
and diseased conditions of the vertebrae during
their different stages of development, etc. Acta
Chir. Scand., 60: 309-368.
Harris, R. S., and D. M. Jones 1956 The arterial supply to the adult cervical vertebral
bodies. J. Bone. Jt. Surg., 38B: 922-927.
Pedersen, H. E., C. F. J. Blunck and E. Gardner
1956 The anatomy of lumbosacral posterior
rami and meningeal branches of spinal nerves
(sinu-vertebral nerves). Ibid., 38A: 377-391.
Schmorl, G. 1929 Zur pathologischen Anatomie
der Wirbelsaule. Klin. Wochenschr., 8: 12431249.
Smith, J. R., and M. J. Henry 1945 Demonstration of the coronary arterial system with Neoprene latex. J. Lab. Clin. Med., 30: 462466.
Stilwell, D. L. 1956 The nerve supply of the
vertebral column and its associated structures
i n the monkey. Anat. Rec., 125: 139-170.
Ubermuth, H. 1929 Die Bedeutung der Altersveranderungen der menschlichen Bandscheiben fur die Pathologie der Wirbelsaule. Arch,
f. Klin. Chir., 156: 567-577.
Willis, T. A. 1949 Nutrient arteries of the vertebral bodies. J. Bone Jt. Surg., 31A: 538-540.
PLATES
Sacral.
4a, 4b
5a, 5b, 6 Deficiencies of the calcified cartilage plate. Apposed surfaces of lumbar body
and plate displayed in 5a, 5b. These are probably openings of vascular cartilage canals
remaining from the fetal stage.
Lumbar.
3a, 3b
2a, 2b Mid-thoracic, dorsal and ventral. In latter, arrows indicate nutritive foramen
ventrally a t base of transverse process.
1 Axis.
Vertebrae of monkey about two years old. Nutritive foramina are seen, usually two on
ventro-lateral surface of body, one or more dorso-central. Smaller, satellite openings and
minute cortical deficiencies transmit periosteal venules. Main nutrient arteries and veins
enter the large foramina exclusively. X 2.5-3.
EXPLANATION O F FIGURES
PLATE 1
VESSELS OF VERTEBRAL COLUMN
Donald L. Stilwell, Jr.
PLATE 1
Dorso-lateral. Veins from regions of spines, arches, ligamenta flava drain left toward
vertebrals in transverse foramina. Note circumferential and longitudinal venous communications. Veins of dorsal muscles draining into these have been removed to show
vessels related to spine. Deep cervical artery and vein arise from subclavian, pass between ribs 1 and 2, lie near laminae. Inosculation with descending branches of occipital
vessels is indicated. Note communication of occipital and vertebral between atlas and
axis, as well as between C.3 and C.4. X 2.
Ventral view. Vertebral arteries surrounded by network of small veins, many of which
enter from laterally and ventrally. Vessels on ventral body surfaces enter and leave
nutritive foramina, anastornose both longitudinally and transversely. Ascending cervical
artery from costocervical trunk communicates with vertebral between transverse processes in its upward course. x 2.
Cervical, monkey. Double injection of vinyl plastic.
EXPLANATION OF FIGURES
PLATE 2
VESSELS OF VERTEBRAL COLUMN
Donald L. Stilwell, Jr.
PLATE 2
PLATE 3
Ventral view. Ventral rami of vertebral arteries issue between transverse processes,
ascending and descending to supply bodies (centra), joints, deep muscles. Muscular
branches removed for clarity. Foramina of bodies on ventro-lateral aspect and at base
of transverse processes are penetrated by osseous vessels. x 2.8.
Dorsal view. Spinal rami of vertebrals enter intervertebral foramina. Median longitudinal vessel is the anterior (ventral) spinal artery. It drains (top) into basilar junction
of vertebral arteries, via 4-5 small vessels. X 2.5.
Dorsal view. Ascending spinal rami entering the vertebral canal divide variably to form
meningeal, osseous, and radicular branches. Anterior spinal artery, placed in midline
of photograph, is contributed to by several radiculars, mainly of the right of photo.
Meningeal vessels are laterally placed, forming a longitudinal chain which complements
the continuous anterior spinal artery. Descending spinal rami are small or absent, and
vary in distribution. The right ascending ramus at (2.4 first gives off a meningeal, then
a n osseous branch, and continues to the spinal cord as a radicular artery. At right
C.5 the osseous artery is a branch of the meningeal. Note anastomoses across midline.
x 4.
9
10
11
Cervical, rabbit. Arterial acrylic plastic.
EXPLANATION O F FIGURES
VESSELS OF VERTEBRAL COLUMN
Donald L. Stilwell, Jr.
PLATE 3
0
co
Y
13
Dorsal, arches removed. Intercostal arteries directed laterally. Origins of dorsal and
spinal rami seen. Descending spinal rami form epiphyseal and osseous branches. Ascending rami smaller, usually radicular in distribution. X 4.
12 Intercostal arteries arise i n pairs from aorta; note narrowing a t their origins. Dorsal
ramus given off ahead of transverse process, then proceeds dorsalward to divide opposite
intervertebral foramen into spinal rami, which enter foramen, and terminal muscular
rami, which ascend and descend. Fields of adjacent muscular rami overlap. Continuations of cut intercostals beyond origins of dorsal rami retouched for clarity. X 2.5.
Lateral and dorsal views of thoracic spine of rabbit. Acrylic plastic, arteries.
EXPLANATION O F FIGURES
PLATE 4
181
16 Dorsal lumbar, monkey. Arterial Neoprene. Ascending and descending spinal rami each
give off multiple small meningeal and larger osseous branches. The latter enter central
deficiencies in the dorsal body cortex. X 3.
15 Same specimen, ventro-lateral view. Single lumbar artery gives off psoas branches,
divides ventral to body, then issues periosteal, osseous, and smaller psoas branches.
14 Lumbar, rabbit, lateral. Arterial acrylic. Ventral rami follow elongated transverse
processes to muscular terminations. Dorsal ramus, best seen between L6 and L7, divides
opposite intervertebral foramen into spinal and two terminal muscular rami. At the
base of each mammillary process a small artery (arrow) supplies the dorsal portion of
arch. The lowest lumbar artery is a branch of median sacral. x 1.8.
E X P L A N A T I O N O F FIGURES
PLATE 5
w
c
00
Donald L. Stilwell, Jr.
VESSELS OF VERTEBRAL COLUMN
PLATE 5
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