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The spinal arachnoid villi of the monkeys Cercopithecus aethiops sabaeus and Macaca irus.

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The Spinal Arachnoid Villi of the Monkeys
Cercopithecus crethiops scrbcreus
and Mcrccrccr irus'
KEASLEY WELCH
AND
MICHAEL POLLAY
Division of Neurosurgery, University of Colorado Medical Center and
Veterans Administration Hospital, Denver, Colorado
The spinal arachnoid villi have been studied in the monkey by the
examination of serial sections of spinal nerve roots, particular attention being paid
to the relations of the arachnoid to the dura mater and to the veins which are regularly applied to the emerging roots. Although the roots vary in their content of specialized arachnoid formations, in many, columns and clusters of arachnoidal cells
occupy spaces between collagen bundles in the dura mater. In a few, leptomeningeal
tissue extends completely through the dura. In approximately one of each six roots
examined, arachnoidal tissue formed part of the wall of and projected into a vein associated with the root. This relationship to veins is considered an especially compelling
point in dispelling the doubt which has been cast upon the conception of spinal
arachnoid villi as specialized structures.
ABSTRACT
It is widely appreciated that at the sites
of exit of nerve roots from the spinal theca,
there are often found leptomeningeal proliferations which resemble the arachnoid
villi of the cerebral meninges. Whether
these are specialized structures as proposed by Elman ('23), who first described
them, or simply unspecific formations or
reactions of perhaps pathological significance, as implied by others, remains an
unresolved question.
The subject has been re-investigated by
study of the spinal nerve roots and related
meninges and blood vessels in two species
of monkey. In the African green monkey
(Cercopithecus aethiops sabaeus) and the
Cynamologus monkey (Macaca irus) the
evidence that there are indeed specialized
structures bearing a close resemblance to
arachnoid villi of the cerebral meninges is
unmistakable.
METHODS
Serial sections of 32 nerve roots, of
which 31 were lumbar and one cervical,
from 15 monkeys were studied. These
were cut at 5 LI from formalin fixed and
paraffin embedded material and stained
with hematoxylin and eosin.
In two anesthetized animals colored
latex was injected into the inferior vena
cava under pressure in order to outline
the venous plexuses in and surrounding
the nerve roots, and in four animals direct
observations of the vasculature of several
roots were made through a dissecting microscope during life.
OBSERVATIONS
Venous plexuses associated with spinal
nerve roots. A venous plexus is regularly
found to be associated with each spinal
nerve root and its sheath but the size and
extent of the plexus varies widely from one
root to the next. The plexus is in and attached to the dural sleeve of the nerve
root and the connective tissue covering
the spinal nerve root ganglion. Deeper
branches are entirely within the dura
mater; the more supeficial are applied
to the dura. There does not seem to be a
regular or characteristic pattern of distribution of the veins; in some roots, they
are more concentrated on the axillary side
and in others, toward the upper border.
The portions of the plexus which are
entirely within the dura are very thinwalled; often there is only endothelium applied directly to the connective tissue of
the dura. The more superficial veins have
walls of their own, especially on their external aspect, but these sometimes have
only an endothelial layer applied to dura
1 Aided by research g p n t (B-627)from the National
Institute of Neurqloglcal Ihseases and Blmdness,
United States Pubhc Health Servlce.
43
44
XEASLEY WELCH AND MICHAEL POLLAY
mater where vein and dura are apposed
(figs. 1, 2, 3).
The plexus receives blood from a segmental vein from within the subarachnoid
space and from veins of the dorsal root
ganglion. At levels where there is a particularly large segmental vein leaving the
subarachnoid space the plexus is likely to
be more rich than at other levels. Drainage
is through veins leaving the spinal canal
accompanying the spinal nerve root and
by numerous and irregular connections
with epidural veins. Direct observation
was made through a dissecting microscope
of a number of nerve roots during life and
no vein was ever observed to contain
clear fluid.
The leptomeninges associated with spinal nerve roots. Clusters of arachnoidal
cells are often found in the spinal leptomeninges and such nests are particularly
common at the very apex of the subarachnoid space where the arachnoid is reflected back along the nerve root. In this
situation, and sometimes more proximally,
these proliferated formations come to occupy the interstices of the dura mater of
the root sleeve and the connective tissue
capsule of the spinal root ganglion. Rarely,
there is complete penetration of the dura
mater so that the arachnoidal cells are
found in an epidural location. A thinwalled arachnoid diverticulum penetrating
the dura mater and coming into relation
with epidural fat, was observed on one
occasion (fig. 4).
Other arachnoidal formations consisting
of arachnoidal cells intermixed with fibers
come into relation with venous channels
of the plexus applied to the root, form
parts of the walls of such vessels and actually project into them (figs. 2, 5 ) .
The villus depicted in figure 2 is, of
those we have examined, the largest, the
most complex and the most suitable for
detailed study. The vein which receives
this villus is thin-walled. That portion applied to the dura mater consists only of
an endothelial layer, while the portion
presenting to the epidural tissue shows a
thin layer of collagenous connective tissue external to the endothelium. The defect in the dura mater, through which the
arachnoidal tissue protrudes, measures
220 K. At the edges of the dura mater
bordering the defect the connective tissue
of the dura does not, at most points, end
abruptly. For a variable distance back
from the edge, perhaps 20 CI,looser arachnoidal tissue is intermingled with the connective tissue bundles of the dura and
some of the latter are extended for a
short distance into the villus or for a distance toward its dome. The structure protrudes 130 p into the vein. The villus itself is made up of mesothelial cells
applied to fibers outlining, between them,
many spaces. The largest of these spaces
measures approximately 16 II in diameter,
the average about one-fourth of this. From
the surface of the villus, several invaginations protrude deeply into the structure.
The covering is the same as the walls of
the spaces within.
The simplest formations associated with
veins were only a few cell layers deep occupying a portion of the wall of a vein.
The nerve roots are not equally endowed
with spinal arachnoid villi. In only 5 of
the 32 roots studied was arachnoidal tissue found to form a portion of the wall
of, or to project into a vein.
DISCUSSION
Elman (’23) studied the microscopic
anatomy of the meninges at the site of
exit of spinal nerve roots of the dog. He
discovered that at the distal extent of the
arachnoid, where it is obliquely reflected
from its position adjacent to the dura
mater back along the intradural portion
of the emerging nerve roots, there often
occurred clusters or columns of arachnoidal cells. These were attached to and
blended with the dura mater and even
penetrated into the interstices of the root
sleeve. Upon subarachnoid injection of
iron ammonium citrate and potassium ferrocyanide and subsequent acid fixation,
he showed granules of Prussian blue to
be precipitated amongst the mesothelial
cells of the clusters, in the dura mater in
that neighborhood, in the tissue surrounding the nerve roots and in some veins. He
did not describe a connection between the
spinal arachnoid “granulations” and the
adjacent veins but pointed out that large
veins are numerous in their neighborhood.
The rich venous plexuses associated
with the spinal theca at the sites of emerg-
SPINAL ARACHNOID VILLI
ence of nerve roots were later studied in
cats by Wislocki and Kubie (Wislocki, '32).
By the intravascular injection of India ink
or carmine gelatin, they outlined branches
of segmental arteries giving rise to a capillary network in the dura mater. This capillary bed was found to drain into veins
which accompany the segmental arteries,
but as they reached the dural sleeve of the
nerve root they enlarged and entered a
series of sinuses in the dural sheath.
These, in turn, were described to drain
into epidural veins. Wislocki thought it
probable that the veins of the plexus
might bear a functional relationship to
the leptomeninges similar to that borne by
the venous sinuses of the cranial dura although the spinal veins had not been described to receive arachnoid villi.
In the rat, Woollam and Millen ('58)
described massive venous plexuses associated with and intimately applied to the
emerging spinal nerve roots. These venous
plexuses they found to be supplied by
veins from the subarachnoid space and
from the spinal root and ganglion. They
described also some of these veins to receive arachnoid villi which had pierced
the dura mater and actually projected into the vascular lumen.
An issue with respect to the significance of the villi has been raised especially from the study of human material
where the emphasis has been largely upon
pathological change. Hassin ('30) found
overgrowth of arachnoid and the formation of arachnoidal protrusions, some of
which remained subdural while others
penetrated into the dura mater. These
formations he found to be exaggerated under certain pathological conditions. He
did not describe relationships of the proliferated arachnoid to veins. Unwilling to
ascribe to the structures any role in the
drainage of cerebrospinal fluid, he conceded their existence, albeit as a manifestation of some general propensity of
the leptomeninx to proliferate and invade
the dura. Rexed and Wennstrom ('59)
described proliferations of the spinal leptomeninges associated with nerve roots leading, in some cases, to cyst formation which
compressed nerve roots or occupied the
spinal root ganglion. Some of the arachnoidal proliferations actually penetrated
45
completely through the dura mater. No
relation between the arachnoid and the
adjacent veins was demonstrated. Rexed
and Wennstrom considered whether the
arachnoid penetrations of the dura might
represent spinal arachnoid villi but dismissed this possibility on the grounds that
such penetrations were not regularly seen
in the absence of other proliferative
change. Thus, they included the existence
of these formations with the other changes
they described as being reflections of
pathological response to an inflammatory
process in the meninges.
Our own observations in the monkey
are compatible with those described in
other species with the exception that we
have not encountered changes which could
be considered pathological. The existence
of groups of arachnoidal cells occupying
tissue spaces of the dura mater and capsule of the ganglion seem not dissimilar
to the observations originally made by
Elman ('23) for the dog and by Hassin
('30) in human tissue, while the extension
of these arachnoidal formations all the
way through the dura was also seen in
human material by Rexed and Wennstrom
('59). The relationship to veins, seen by
Woollam and Millen ('58) in the rat and
shown also in our own material, appears
to be of crucial importance in any consideration of the significance of arachnoid
villi of the spinal meninges. Simple proliferation of tissue in response to a pathological agent would not be expected to lead
to invasion of venous walls.
The establishment of relationships between these structures and the lumina of
veins confirms the suspicion expressed
long ago by Wislocki ('32) and, although
direct evidence cannot be offered, there is
sufficient resemblance between some of
these and the villi of the cerebral meninges
(Welch and Friedman, '60) to suggest a
similar function. In this connection, it
may be pointed out that the spinal arachnoid villi are so situated that they might
conduct, to the sites where they have been
found, the various tracer particles which
have been employed in the study of cerebrospinal fluid pathways. The studies
made before 1948were reviewed by Brierly
and Field ('48). Introduced into the subarachnoid space of rabbits, particles of
46
KEASLEY WELCH AND MICHAEL POLLAY
DURA MATER
DORSAL NERVE ROOT
E
Fig. 1 Diagrammatic representation of the kinds of meningeal and vascular relationships
found in spinal nerve roots. At A growth of arachnoidal cells within the dura mater is
represented. B represents complete penetration of dura mater by leptomeninx and C protrusion of arachnoidal tissue into a vein. At D and E arachnoidal proliferations are shown.
India ink reached the epidural connective
tissue and regional lymphatics (Brierly and
Field, ’48). They were also found within
spinal arachnoid villi of the rat by Woollam and Millen (‘58). A pathway into the
blood was shown for colloidal palladium
by Howarth ( ’ 5 2 )and Howarth and Cooper
(’55) in cats, and, although the authors
believed the passage to be directly through
vascular walls, the spinal arachnoid villi
were not studied.
LITERATURE CITED
Brierley, J. B., and E. J. Field 1948 The connexions of the spinal subarachnoid space with
the lymphatic system. J. Anat., 82: 153-166.
Elman, R. 1923 Spinal arachnoid granulations
with especial reference to the cerebrospinal
fluid. Bull. Johns Hopkins Hosp., 34: 99-104.
Hassin, G. B. 1930 Villi (Pacchionian bodies)
of the spinal arachnoid. A.M.A. Arch. Neurol.
Psychiat., 23: 65-78.
Howarth, F. 1952 Observations on the passage
of a colloid from cerebrospinal fluid to blood
and tissues. Brit. J. Pharmacol., 7: 573-580.
Howarth, F., and E. R. A. Cooper 1955 The
fate of certain foreign colIoids and crystalloids
after subarachnoid injection. Acta Anat., 25:
112-140.
Rexed, B. A., and K. G. Wennstrom 1959
Arachnoidal proliferation and cystic formation
in the spinal nerve root pouches of man. J.
Neurosurg., 16: 73-84.
Welch, K., and V. Friedman 1960 The cerebrospinal fluid valves. Brain., 83.454-469.
Wislocki, G. B. 1932 in “Special Cytology.”
Ed. by Edmund V. Cowdry, 2nd edition, New
York, Paul B. Hoeber, Vol. 3, p. 1483.
Woollam, D. H. M., and J. W. Millen 1958 Observations on the production and circulation
of the cerebrospinal fluid in Ciba Foundation
Symposium on the Cerebrospinal Fluid. G. E.
W. Wolstenholme, editor, Boston, Little Brown
and Company, pp. 124-146.
SPINAL ARACHNOID VILLI
PLATE 1
Keasley Welch and Michael Pollay
2
3
An arachnoid villus protruding into a venous channel associated with a nerve root
sleeve is shown. H & E X 200. AV, arachnoid villus; V, vein; DM, dura mater; NR,
nerve root.
Higher power view of a portion of the villus shown in figure 2. H & E x 640.
47
SPINAL ARACHNOID VILLI
Keasley Welch and Michael Pollay
4
5
48
PLATE 2
A diverticulum of arachnoid (arrow) completely penetrates the dura mater and comes
into relation with epidural fat. H & E X 200. NR, nerve root; DM, dura mater.
A villus composed of both compact and loose arachnoidal tissue forms a wall of a
space which in serial sections is connected with epidural veins. H & E X 200. V, vein;
DM, dura mater; NR, nerve root.
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