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Subdural compartment in pigA morphologic study with blood and horseradish peroxidase infused subdurally.

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THE ANATOMICAL RECORD 230:22-37 (1991)
Subdural Compartment in Pig: A Morphologic
Study With Blood and Horseradish Peroxidase
Infused Subdurally
JAN R. ORLIN, KIRSTEN K. OSEN, AND TORSTEIN HOVIG
Division of Experimental Neurosurgery, Institute for Surgical Research (J.R.O.) and
Electron Microscope Laboratory, Institute of Pathology (T.H.), The National Hospital and
Anatomical Institute, University of Oslo (K.K.O.),
Oslo 1 , Norway
ABSTRACT
The dura-arachnoid junction is examined in normal animals and
in animals subjected to subdural infusion of blood immediately prior to death,
simulating acute subdural hemorrhages. The Norwegian landrace pig is used a s
the experimental animal. Horseradish peroxidase (HRP) has been added to the
injected blood to serve as a macromolecular tracer. The material is studied by light
and electron microscopy. Special attention is given to the level of the induced
subdural cleavage plane, the total distribution of the infused blood, and the natural sites of drainage.
The dura-arachnoid junction, identified here as the subdural compartment (the
dural border layer of others), consists of a n avascular tissue with flake-like, relatively electron-lucent cells stacked upon each other in several layers with narrow
intercellular clefts. Under normal conditions there is no evidence of a so-called
“subdural space.” When under the present experimental conditions bleeding takes
place into this cellular tissue, it splits without any particular, predestined cleavage
plane, although most often close to the fibrous matter of the dura. The bleeding
extends throughout the cerebral and spinal parts of the compartment and also
along the spinal nerve roots. Contamination of the subarachnoid space occurs only
in some cases subjected to large infusions and apparently only a t spinal levels. The
HRP diffuses into the dura, but does not traverse the arachnoid barrier layer.
The structure of the meninges has been described in
numerous studies of animals (Pease and Schultz, 1958;
Andres, 1967; Waggener and Beggs, 1967; Klika, 1967;
McCabe and Low, 1969; Himango and Low; 1971;
Akashi, 1972; Allen and Low, 1975; Fiedler and Drommer, 1976; Allen and DiDio, 1977; Nabeshima et al.,
1975; Oda and Nakanishi, 1984) and humans (Key and
Retzius, 1876; Anderson, 1969; Lopes and Mair, 1974;
Rascol and Izard, 1976; Schachenmayr and Friede,
1978; Alcolado et al., 1988). There is no general agreement, however, regarding definition, ultrastructure,
and function of the dura-arachnoid junction, i.e., the
meningeal layer referred to by Nabeshima e t al. (1975)
a s the “dural border layer,” but tentatively identified
here as the “subdural compartment” (SDC).
In spite of increasing evidence against the existence
of a preformed, so-called “subdural space” under normal conditions (Andres, 1967; Klika, 1967; Waggener
and Beggs, 1967; Anderson, 1969; Allen and Low, 1975;
Nabeshima et al., 1975; Rascol and Izard, 1976;
Schachenmayr and Friede, 1978; reviews by Haines,
1991; Haines and Frederickson, 19911, it is a fact that
a space easily occurs a t the level of the SDC, either as
a dissection artifact or as a result of pathological processes such a s subdural bleeding. There are, however,
no experimental data available concerning the fine
structure of the meninges immediately following such
bleedings, and conflicting opinions exist a s to the exact
0 1991 WILEY-LISS, INC.
level of the cleavage plane. The potentials for a n initial
flow of a subdural bleeding across the midline, a s indicated recently by magnetic resonance imaging (Makiyama et al., 1985; Polman et al., 19861, and to spinal
levels also need further anatomical investigation.
Experimental evidence for natural sites of drainage
of subdurally deposited blood is sparse (Mairova, 1965).
The cellular tissue forming what we call the SDC has
been shown electron microscopically to be directly contiguous with the stratified perineural sheaths of the
spinal nerve roots (Andres, 1967; McCabe and Low,
1969; Himango and Low, 1971; Fiedler and Drommer,
1976). Although a flow of cerebrospinal fluid from the
subarachnoid space (SAS) along the spinal nerves has
been documented (e.g., Klatzo et al., 1964), we have
found no paper testing the possibility of a drainage
from the SDC along this route.
In the present study these issues are investigated by
a novel combination of methods. These include light
microscopy and transmission and scanning electron
microscopy of the meninges under normal conditions
and immediately following subdural blood infusions
over one hemisphere. The infusions were performed so
Received July 16, 1990; accepted September 21, 1990.
Address reprint requests to Dr. J a n R. Orlin, Knapstadveien 12,
N-1823 Knapstad, Norway.
SUBDURAL COMPARTMENT I N PIG
23
a s to simulate acute venous and arterial subdural feeding tube No. 8 (inner diameter 1.6 mm) bent into
bleedings without concomitant brain contusion. In the 90” angle 2.5 cm from its tip. Under the dura a narrow
first case, horseradish peroxidase (HRP) was added to space appeared with a small amount of clear fluid
the injected blood as a tracer.
forming a meniscus. The tube was inserted into this
Previous animal experiments on subdural bleedings space with the tip pointing rostrally, and glued to the
have been performed in the cat (Cohn, 1948; Mairova, dura to prevent leakage.
1965), the dog (Gardner, 1932; Watanabe et al., 1972),
and the monkey (Watanabe et al., 1972). We chose the Test injections
Four pigs were then turned to the supine position
Norwegian landrace pig, which has also been used in a
joint study (Orlin and Zwetnow, 1989) concerning the and prepared for perfusion by thoracotomy. Blood was
pathophysiological effects of subdural bleedings. The withdrawn from the femoral vein and mixed with hepig has become a common experimental animal in med- parine (130 i.u. per ml blood) and HRP (Sigma type 11,
ical research. Although a literature search, covering final concentration 0.1%).Between 7 and 15 ml of the
the last two decades, gave no examples of its use in mixture was injected through the subdural tube in 6-8
neurosurgical research, we have found the pig partic- min. In order to avoid reactive tissue changes and
ularly useful for our purpose because of its size. It is transport of HRP by phagocytosis (Nabeshima and
appropriate also from a technical, economical, and eth- Reese, 19721, the animals were perfusion-fixed, as
ical point of view. An ultrastructural examination of above, immediately after the infusion. The brain and
normal pigs, however, proved necessary because of the the spinal cord with surrounding meninges and about 8
shortage of reports on the structure of the meninges in mm of the spinal nerve roots, including the spinal ganthis species (Fiedler and Drommer, 1976; Klika and glia, were removed en bloc and kept in the same fixaRichter, 1989). Fifteen years after Nabeshima et al.’s tive for 2 hr, and overnight in 0.1 M phosphate buffer,
(1975) comprehensive electron microscopic study of the pH 7.4. The meninges usually remained intact except
meninges in smaller mammals, we take advantage of a t the base of the skull where the dura and the cranial
the “historical gain” and use their summary diagram nerve roots always ruptured during dissection.
a s a starting point in our results.
Blocks of the meninges and subjacent nervous tissue
were taken from the convexity of the hemispheres, cauMATERIALS AND METHODS
dal to the injection tube, and from the spinal cord, cut
Seven pigs with body weight 17-20 kg were anesthe- in 80 pm slices on a vibratome or in 20 pm sections on
tized by intraperitoneal injection of pentobarbital (20- a cryomicrotome, and reacted with diaminobenzidine
30 mg per kg), tracheotomized, artificially ventilated, (DAB)/H2O2(Graham and Karnovsky, 1966). The cryosections were counterstained with thionine and covand subjected to the procedures described below.
erslipped for light microscopy. The vibratome slices
Normal Specimens
were osmicated and prepared for transmission electron
Two pigs with intact meninges were perfused tran- microscopy. Because of poor penetration of the DAB, a
scardially with 1.0 liter phosphate-buffered saline, pH positive HRP reaction was found only in the most su7.4, followed by 4.5 liter of glutaraldehyde 2.5%, perficial ultrathin sections.
During blocking, the meninges tended to separate in
paraformaldehyde 1%, and calcium chloride 0.003% in
0.1 M phosphate buffer, pH 7.4. The skull was opened the blood-containing space. Segments of the deep and
and blocks of the meninges over the lateral part of the outer lining of the space were sampled for scanning
hemispheres with the subjacent cortex were removed electron microscopy.
for electron microscopy before further dissection.
Blocks for transmission electron microscopy were post- Arterial shunt bleedings
In one pig regular arterial blood was shunted difixed for 2 hr, treated with 1% osmium tetroxide in 0.1
M phosphate buffer, pH 7.4, for 1 hr, dehydrated in rectly from the abdominal aorta and through the subethanol and propyleneoxide, and embedded in Araldite dural tube with the animal in prone position. About 50
(TAAB). Semithin sections were stained with 1% tolu- ml of blood passed through the shunt before the animal
idine blue in 1% sodium borate. Ultrathin sections died after 15 min. The brain and the spinal cord with
were contrasted with uranyl acetate and lead citrate. the meninges were removed en bloc, as described
In blocks used for scanning electron microscopy the above, and immersion-fixed in 10% formalin. The dismeninges were split mechanically in the SDC imm.edi- tribution of the injected blood was examined by inspecately after the perfusion, whereby the leptomeninges tion and stereomicroscopy, a s well as by light microsbecame curled up like a carpet from the dura. The tis- copy of 20 pm cryostat sections of the spinal cord.
sue was postfixed and osmicated a s above, dried in a Before thionin staining, the sections were treated with
critical point dryer system, and sputtered with gold- DAB, as above, for visualisation of the erythrocytes
which react positively because of endogenous peroxipalladium.
dase. The meninges of 21 subdurally injected pigs from
Subdural Infusions
the pathophysiological experiments (Orlin and ZwetThese were performed either a s “test injections” of a now, 1989) were examined in the same way.
limited volume of HRP-containing blood or a s “arterial
shunt bleedings” leading to death. In both instances a Number of samples
Optimal fixation proved to be a problem, particularly
burr hole with a diameter of 15 mm was made over the
frontoparietal region of the left hemisphere. The dura after subdural injections which tended to impair the
was carefully lifted with a hook and a small hole was perfusion. The present figures were selected from 75
made, big enough to pass through it a Sherwood argyle electron micrographs from four samples of normal ma-
24
J.R. ORLIN ET AL.
with finely dispersed chromatin. The cytoplasm is rich
in organelles, particularly mitochondria, free ribosomes, and short profiles of rough endoplasmic reticulum (rER) (Figs. 2A, 3). Infoldings of the cell membrane, probably endo- or exocytotic pits, are seen
adjacent to the fibril-containing spaces (Fig. 3).
RESULTS
The subdural compartment, or “dural border layer,”
Normal Ultrastructure
varies in thickness, but is generally about 5 pm thick.
The structure of the meninges in normal pig con- It is composed of flattened, flake-like cells, referred to
forms, to a large extent, with Nabeshima et al.’s (1975) by us as “subdural cells” (after Akashi, 1972), stacked
electron microscopic study in rodents, cat, and monkey. upon each other in several layers parallel to the dura.
As indicated in Figure 1, we have adopted their strat- The extranuclear portion of each cell is about 1 pm
ification and terminology with a few modifications: We thick, and there are more cell layers (varying from a
introduce the term “subdural compartment” for their few up to 10-15) than expected from the number of
“dural border layer” a s a modification of the widely nuclei in semithin sections (compare Figs. 1B and 2A).
used term “subdural space,” to denote a soft tissue, but In electron micrographs the individual cells may be
not necessarily a cavity, enclosed between tougher traced over distances more than 50 pm (Fig. 2A). The
membranes. We emphasize the SDC as a structure dis- nucleus is usually flattened with finely dispersed chrotinct from the dura in order to make the term rational matin as in the fibrocytes of the dura. The cytoplasm is
and, hopefully, to end the fruitless discussion of more electron-lucent and contains fewer organelles
whether a process in this portion of the meninges than any other meningeal cells: scattered microfilashould be named intradural or subdural (for reviews, ments, a few mitochondria, and short profiles of rER.
see Leary, 1939, Loew and Kivelitz, 1976; Haines, The intercellular clefts are of about the same width
1991). Furthermore, we introduce the term “arachnoid (15-40 nm) as between the dural fibrocytes, but there
reticular layer” for the collagen-containing portion of are more dilatations filled with flocculent material
the arachnoid situated between the arachnoid barrier (Figs. 2-4). Scattered adhering (desmosome-like)junclayer and the SAS, to stress its existence and possible tions may be seen (Fig. 31, but there is no basement
role a s a mechanical reinforcement of the arachnoid. membrane and no fibrillar intercellular material reThe third portion of the arachnoid, i.e., the arachnoid lated to these cells. The cell borders are almost rectitrabeculae, and the pia are not further commented on linear. The innermost cells, however, have a more irregular deep surface accommodating the arachnoid
here.
Four meningeal layers are according to our defini- barrier layer. The corresponding intercellular cleft aption situated outside the SAS: the arachnoid reticular pears largely similar to the clefts between adjacent
layer, the arachnoid barrier layer, the SDC, and the subdural cells, but shorter stretches are narrower and
dura (Figs. 1-4). Although the cells of the four layers possess more numerous adhering junctions (Fig. 3).
are ultrastructurally distinct, the classification of in- Under these conditions a “subdural space” is definitely
dividual elements in the border zones may be difficult. lacking.
The three first-mentioned layers are composed of avasThe arachnoid barrier layer is about 5 pm thick. The
cular tissues, only traversed by the bridging veins near cells are less flattened than the subdural cells and form
the dural sinuses. The dura, on the contrary, contains
both blood vessels and lymphatics. The three layers
therefore must be nourished (or perfusion-fixed) either
via the cerebrospinal fluid or from the dura. In the
Abbreviations
following, the normal ultrastructure of each of the four AB
arachnoid barrier cell
layers is described separately, starting with the dura. ABL
arachnoid barrier layer
arachnoid reticular cell
Only cerebral levels are illustrated in this context, but AR
arachnoid reticular layer
from previous studies and our own observations only ARL
asa
anterior spinal artery
minor modifications are to be expected at spinal levels. c o
collagen
dural fibrocyte
Measurements are not corrected for shrinkage during D
E
elastin
preparation.
epineurium
The dura of pig is about 100 km thick over the hemi- EP
Er
erythrocyte
spheres, thicker (up to about 300 km) toward the mid- F
intercellular flocculent material
Golgi apparatus
line. It consists of a dense connective tissue (Fig. 1B). Go
horseradish peroxidase
As already shown by Key and Retzius (1876) by micro- HRP
lacuna
dissection of human and animal material, the dural LN
nucleus
fibrocytes are flattened parallel to the surface of the P1
plasma
perineurium
dura and have a few thin processes. Ultrastructurally Pn
rootlet
they are about 1 km thick and alternate with fibrillar r
rER
rough endoplasmic reticulum
intercellular material composed of relatively thick col- SAS
subarachnoid space
lagen fibrils (about 100 nm diameter), microfibrils, and SD
subdural cell
subdural compartment
elastin. In the deep part of the dura where the cells SDC
subdural hematoma
occur stacked upon each other, the intercellular clefts SDH
p.c
spinal cord
are electron-lucent and about 15-40 nm wide with few sSp.G
spinal ganglion
if any junctions, but with occasional dilatations con- Sp.NR
spinal nerve root
vessel
taining a flocculent material. The nucleus is flattened V
terial and 200 electron micrographs from 12 samples of
test-injected cases. The light micrographs are representative for about 100 tissue sections, including semithin
sections of numerous tissue blocks originally prepared
for electron microscopy.
SUBDURAL COMPARTMENT IN PIG
25
A
DURA
SAS
A and P
\
Fig. 1. A slightly modified version of Nabeshima et al.’s (1975, P1.
17, reproduced by courtesy of the authors) diagram of the mammalian
cerebral meninges in A is compared with a light photomicrographic
montage of a corresponding field of a toluidine blue-stained semithin
section from a normal pig in B. Corresponding borderlines in A and B
are connected by straight lines. The boldface letters between the lines
indicate the presently used terminology (see list of abbreviations),
slightly modified after that of Nabeshima et al. Our SDC is distinct
from the dura and corresponds to their dural border layer (Db). Our
ABL equals their arachnoid barrier layer (B). Our ARL corresponds to
the collagen-reinforced, sub-barrier part of the arachnoid, not specially named by them. In A the curved arrow, intended by Nabeshima
et al. to illustrate the artificial, dissection-induced “subdural space”
(SDS), also indicates the intended site of blood infusion in the present
study (which usually proved to be closer to the dura). Cell junctions:
desmosomes (d), hemidesmosomes (h), tight junctions (t), and gap
junctions (g). In B small arrows indicate dural fibrocytes, arrowheads
the dark intercellular line of the ABL (also illustrated in A), medium
arrows the deep lining of the ARL, open arrow perhaps a migrating
cell.
26
J.R. ORLIN ET AL.
Fig. 2. Electron micrographs of the cerebral meninges of a normal
pig. A shows part of the dura with dural fibrocytes (D), the SDC
(between large arrows) with subdural cells, the layer of arachnoid
barrier cells, and part of the arachnoid reticular layer with arachnoid
reticular cells and lacunae. The thicker collagen fibrils of the dura are
indicated by small arrows, the thinner of the arachnoid by double
arrows. Each SD-cell spans almost the entire field of the picture (SD,
labeled by asterisks). The same is the case for the deepest D-cell (D,).
Thus, both SD- and D-cells seem more sheet-like than AB-cells that
are thicker with thin, interdigitating cell processes (isolated profiles
indicated by dots). Of the cell types present, the SD-cells are most
electron-lucent, the AR-cells most electron-dense. The narrow, electron-dense intercellular clefts between AB-cells are indicated by arrowheads, a possible migrating cell by open arrow. B shows part of an
AB-cell connected by a triple-adhering junction (curved arrow) to adjacent AR-cells.
SUBDURAL COMPARTMENT IN PIG
Fig. 3. Electron micrograph with details from Figure 2, showing the
innermost part of the dura (top) with D-cells, the SDC (between large
arrows) with SD-cells, arachnoid barrier layer with AB-cells, and the
outermost part of the arachnoid reticular layer with AR-cells (bottom). The dura contains collagen fibrils, microfibrils (small arrows),
and elastin. The electron-lucent intercellular clefts between the Dcells and between the SD-cells show dilatations with a flocculent material. The large vesicles with flocculent material in SD1 may repre-
27
sent infoldings of the cell membrane. SD1 abuts upon the subjacent
AB-cells and has a more irregular deep surface than the other SDcells. The narrow intercellular clefts of the interdigitating AB-cells
show several adhering junctions (curved arrows) and a possible gap
junction (double-crossed arrow). The AR-cells are darker and have
larger mitochondria than the other cells. The lacunae (L) contain thin
collagen fibrils and microfibrils (small arrows). Hemidesmosomes are
attached to remnants of a basement membrane (arrowheads).
28
J.R. ORLIN ET AL.
Fig. 4. Electron micrograph from the cerebral arachnoid barrier
layer flanked by SD-cells to the left and AR-cells to the right. The
AB-cell in the center of the field shows a Golgi apparatus, short profiles of rER, a few microtubules (small arrows), and microfilaments.
The wide intercellular cleft (indicated by large arrows) toward the
adjacent subdural cell (SD1) shows a dilatation with a flocculent ma-
terial (F). The SD-cells show scattered microfilaments in their electron-lucent cytoplasm. The intercellular clefts (arrowheads) between
AB-cells show adhering junctions (curved arrows) and tight junctions
(crossed arrow). The arachnoid lacunae (L) contain collagen and microfibrils.
29
SUBDURAL COMPARTMENT IN PIG
a n epithelium-like tissue with only one row of nuclei,
but with 1-4 layers of highly interdigitating cell processes (Figs. 2-4). The intercellular clefts are narrower
(about 10 n m wide) and filled with a n electron-dense
material. The cells are interconnected by adhering
junctions (Figs. 3,4,curved arrows), occluding (tight)
junctions (Fig. 4, crossed arrow), and communication
(gap) junctions (Fig. 3, double-crossed arrow), a s described by Nabeshima et al. (1975; see our Fig. 1A).
The nucleus is oval with coarser chromatin than in the
subdural cells. The cytoplasm is slightly darker with
more organelles, notably rER, free ribosomes, scattered
dark bodies, and groups of small vesicles, probably
Golgi apparatuses. The cells also contain a few microtubules and many filaments, some evidently being
tonofilaments related to the adhering junctions (Fig.
4).Vesicles and surface pits speak in favor of endo- or
exocytotic activities.
The arachnoid reticular layer, as defined here, is
about 10-20 pm thick and composed of irregularly
branched cells which form a loose network with intercellular “lacunae” (“cisterns” in Nabeshima et al.’s terminology) of irregular shape and size. These lacunae
contain microfibrils and bundles of thin collagen fibrils
(diameter about 50 nm) oriented in a crisscross pattern
parallel to the brain surface (Figs. 2, 3). The lacunae
appear partly shut off from the SAS by sheet-like cell
processes (Fig. 1B). Between the lacunae, the interdigitating cell processes are separated by a regular, 20 nm
wide electron-lucent space (Fig. 2B). The cell nucleus is
irregularly shaped with relatively coarse chromatin.
The cytoplasm is more electron-dense with numerous
microfilaments (Fig. 4),and the mitochondria appear
larger than in the barrier cells (Fig. 2A). Scattered
rER, quite a few polyribosomes, and possible endo- or
exocytotic vesicles are usually present (Fig. 3). Adhering junctions are scattered both between the arachnoid
reticular cells and between these and the barrier cells
(Fig. 2B). Hemidesmosomes occur toward the lacunae,
and near the barrier layer short pieces of a basement
membrane adjoin both kinds of cell (Fig. 3). When only
parts of cells are present in the micrographs, a distinction between arachnoid barrier and reticular cells is
not always possible (Fig. 4).
infiltrated by erythrocytes (Fig. 6B), and a blood-containing space, probably continuous with that of the
SDC, was found within the perineural sheaths (Fig.
6C). Occasionally the endoneurium was also infiltrated. Because the dura ruptured a t the base of the
skull during the dissection, the basal part of the cerebral SAS and the cranial nerve roots could not be examined.
Test Injections
Arterial Shunt Bleedings
After injections of a smaller amount of HRPcontaining, heparinized venous blood, the distribution
of the blood was largely the same a s after the shunt
bleedings although the diastasis of the dura and arachnoid was smaller (Fig. 7). There was no contamination
of the SAS, not even at spinal levels (Fig. 7C,D).
At the outer lining of the blood-containing space,
blood cells appeared either in direct contact with the
collagen fibrils and small vessels of the dura or separated from these structures by some flat cells that
could be fibrocytes and/or subdural cells (Fig. 7B,E).
The blood corpuscles could also be seen squeezed in
between such cells (Fig. 7E).
At the inner lining of the space, erythrocytes and
platelet aggregates were sometimes found close to, and
perhaps in contact with, the arachnoid barrier layer
(not illustrated). More often the blood cells were separated from the arachnoid by several layers of subdural
cells (Fig. 8). These appeared thinner and more irregularly shaped than normally and had increased electron density of the cytoplasm. The intercellular spaces
were widened with a flocculent content, some of which
undoubtedly represents plasma proteins (Fig. 8B).
HRP reaction product occurred throughout the dura,
but not in the arachnoid or subjacent structures (Fig.
7A,D). In superficial ultrathin sections from the DABreacted slices, the HRP appeared to have diffused with
the plasma in between the subdural cells and a certain
distance in between the arachnoid barrier cells, but not
deep to the latter (Fig. 8A).
As after the shunt bleedings, erythrocyte infiltration
occurred in the epineurium and perineurium of the spinal nerve roots. In the latter location rows of erythrocytes appeared squeezed in between the perineural
lamellae (Fig. 6D).
Shunt bleedings from the abdominal aorta led to
flow of blood bilaterally throughout the entire SDC,
spinal as well as cerebral. On dissection of the fixed
specimen a cap-like subdural blood clot was found over
both cerebral hemispheres. The cisterna magna, itself
free of blood, was compressed by a thick dorsal “collar”
of blood (Fig. 5A). The spinal cord was surrounded by
blood all the way down to the dural sac (Fig. 5B). Usually more blood was located dorsally than ventrally
(Fig. 6B), which cannot be explained by gravitation
because of the animal’s prone position during the infusion. Blood often filled the “pocket” of the SDC between
the dorsal and ventral roots (Fig. 6B). The SAS was
clearly compressed by the distended SDC. Blood was
occasionally present in the lateral part of the spinal
SAS, among the emerging rootlets, despite the absence of blood in the cisterna magna (Figs. 5B, 6A).
On gross inspection the spinal nerve roots were discolored by blood (Fig. 5B). In sections the epineurium was
The tendency for the SDC to split close to the dura is
supported also by scanning electron microscopy of the
cleaved SDC in the normal pig and in test-injected
specimens. In normal animals the deep surface of the
cleavage space, i.e., on the arachnoid side, was covered
by a continuous, smooth cell layer that could represent
subdural cells and/or arachnoid barrier cells (Fig. 9A).
The fibrillar network of the arachnoid reticular layer
could be seen through ruptures in the surface lining.
The outer surface of the space, i.e., on the dural side,
showed coarse fibers only partially covered by sheetlike cells that could be dural fibrocytes and/or subdural
cells (Fig. 9B). In the injected specimens erythrocytes
occurred on both surfaces of the blood-containing space.
In areas not completely concealed by erythrocytes, the
deep surface appeared covered by a continuous layer of
flat cells, as in normal cases, but with the nuclear sites
Scanning Electron Microscopy
30
J.R. ORLIN ET AL.
Fig. 5. Color photographs from the central nervous system of a pig
with arterial shunt bleeding. A shows the empty cisterna magna in a
dorsolateral view, covered by a partly removed subdural hematoma.
The originally infolded arachnoid is artificially stretched. B shows the
cranial surface of a slice of the cervical spinal cord with the nerve
roots and spinal ganglia. The pia is marked by black arrows, the
arachnoid by white arrows. Blood is present in the SDC as well as in
between the rootlets in the lateral part of the SAS, and in the roots.
There is no blood around the anterior spinal artery.
protruding slightly above the surroundings (Fig. 9C,
compare with 9A). The latter feature may correspond
to the shrinkage of the cytoplasm observed by transmission electron microscopy in such cases (Fig. $). The
outer surface also had a n appearance corresponding to
the normal pattern, with erythrocytes adhering either
to the naked collagen fibrils of the dura or to a cover of
flat cells (Fig. 9D).
we call the SDC, conforms with the general mammalian pattern. By subdural infusions the blood immediately spreads throughout the SDC, including spinal
levels. In contrast to serous cavities, the cleavage plane
of the SDC is not predestined. The stacks of flattened
cells split randomly, although most often close to the
fibrous matter of the dura. The injected blood immediately infiltrates the epineural and perineural sheaths
of the nerve roots. Leakage into the SAS appears limited to some cases with arterial shunt bleeding. The
two latter findings may be restricted to spinal levels,
although reservations have to be made for the base of
DISCUSSION
According to the present study, the normal ultrastructure of the meninges in pig, including that portion
SUBDURAL COMPARTMENT IN PIG
31
Flg. 6. Light photomicrographs of the spinal meninges. A-C are
from DAB-reacted, Nissl-stained cryosections of two cases with arterial shunt bleedings. The arachnoid is indicated by arrowheads. The
empty spaces in the blood-containing SDC are due partly to sectioning
artifacts, partly to contraction of the coagulum. A is from the same
case a s Figure 5 with blood both in the distended SDC and the compressed SAS. B and C are from a case with only traces of blood in the
SAS (at arrow), but with bleeding into the nerve roots. On the right
hand side is discoloring of the epineurium. On the left hand side,
enlarged in C, is bleeding into the perineural sheaths (arrows), in one
fascicle (asterisk) also into the endoneurium. The lateral pocket of the
blood-containing SDC is indicated by a white asterisk, the dentate
ligament by an open star. D is from a toluidine blue-stained semithin
section of a spinal nerve root fascicle of a test-injected case with erythrocytes (arrows) squeezed in between the membranes of the perineural sheath (some myelinated fibers marked by asterisks). Magn.: A,C
x80;B x 6 ; D ~ 7 5 0 .
the brain where the meninges and nerves ruptured
during dissection. The arachnoid forms a n effective
barrier against HRP, while the dura is leaky.
as in the meninges of other animals (Pease and
Schultz, 1958, rat; Andres, 1967, dog, cat; Waggener
and Beggs, 1967, rat, guinea pig; Himango and Low,
1971, rat; Akashi, 1972, rabbit; Nabeshima et al., 1975,
mouse, rat, chinchilla, rabbit, cat, monkey; Oda and
Nakanishi, 1984, mouse) and humans (Anderson, 1969;
Lopes and Mair, 1974; Rascol and Izard, 1976;
Schachenmayr and Friede, 1978; Alcolado et al., 1988).
It may correspond to the spongy-looking “intermediate
leptomeningeal layer” shown by scanning electron microscopy a t spinal levels in humans (Nicholas and
Weller, 1988).
Normal Features, Comparative Aspects
The arachnoid reticular layer, in our terminology,
has been described by others (e.g., Alcolado et al., 1988)
as the “inner layer of the arachnoid membrane.” In pig
it is regularly distinguishable deep to the arachnoid
barrier layer of the cerebral meninges. Judged by previously published illustrations i t is present also at spinal levels in pig (Fiedler and Drommer, 1976) a s well
32
J.R. ORLIN ET AL.
Fig. 7. Light photomicrographs from the meninges following test
injections of heparin- and HRP-containing blood. The arachnoid is
marked by arrowheads. A shows a DAB-reacted cryosection of the
cerebral meninges with the subjacent cortex. The HRP reaction is
restricted to the blood-containing SDC and the dura. B is a toluidine
blue-stained semithin section from the outer lining of the SDC showing erythrocytes in direct contact with the collagen fibers of the dura.
C and D are from a DAB-reacted cryosection from the spinal
meninges showing blood in the SDC and HRP reaction in the dura.
The boxed area in C is shown at higher magnification in D. E is from
a corresponding part of the meninges as shown in D, but from a toluidine blue-stained semithin section of another animal. Erythrocytes
and platelets in the SDC are in part situated between layers of sheetlike cells (arrows) which may be subdural cells and/or dural fibrocytes. Magn.: A,D x 104; B x 1,500;C x 8; E x 750.
Although we have done no systematic sampling from
the brain surface, the arachnoid reticular layer in our
opinion may not merely constitute a layer of compressed arachnoid trabeculae. The arachnoid lacunae,
although probably traversed by cerebrospinal fluid,
are, a s described also by others (e.g., Nabeshima et al.,
1975), partly shut off from the main part of the SAS.
The collagen fibrils in the lacunae are oriented parallel
to the brain surface (Allen and DiDio, 1977; Alcolado et
al., 1988),and obviously serve to strengthen the arachnoid mechanically. As shown by Key and Retzius
(1876) by microdissection and Alcolado et al. (1988) by
scanning electron microscopy, the fibrils converge toward the arachnoid trabeculae and apparently also
serve to anchor the arachnoid to the pia.
The arachnoid barrier layer in pig conforms with
Nabeshima e t al.’s (1975) description based on transmission electron microscopy and freeze fracture in rodents, cat, and monkey. The typical interdigitation of
the cells, the many junctions, and the narrow intercellular clefts filled with electron-dense material have
been illustrated in most of the animal studies referred
to above, as well a s in human biopsies obtained during
surgery (Rascol and Izard, 1976; Alcolado et al., 1988).
The dark intercellular clefts appear less conspicuous in
Schachenmayr and Friede’s (1978) autopsy material of
human. When appearing as a continuous line, many
authors tend to misinterprete this a s the border between the barrier layer and the SDC.
The many adhering junctions, the cellular microfil-
SUBDURAL COMPARTMENT IN PIG
Fig. 8. Electron micrographs from DAB-reacted slices of the cerebral
meninges following test injections of heparin- and HRP-containing
blood. The SDC-ABL border is indicated by large arrows. A is from a
superficial section of a slice with strong HRP reaction in the injected
plasma (P1+ HRP). Electron-lucent platelets (Tr)are seen between
shrunken SD-cells (also marked by asterisks). A thin layer of reaction
product (arrowheads) is seen between the AB-cells, but not deep to
them. B is from a deep section without HRP reaction products. The
33
SD-cells are more electron-dense than normal, shrunken and irregularly shaped, and widely separated from each other by a flocculent
material, some of which is probably plasma. Also in the outer part of
the arachnoid barrier layer the intercellular clefts are slightly wider
than normal and here the adhering junctions (curved arrows) and
occluding junctions (crossed arrow) are clearly seen. A communication
junction (double-crossed arrow) is seen between AR-cells.
34
J.R. ORLIN ET AL.
Fig. 9. Scanning electron micrographs from the cleaved SDC. A, B
From a normal animal. C, D From a subdural test injection. In the
latter case the lining of the blood-containing space is represented only
by sites incompletely covered by erythrocytes. A and C are from the
arachnoid side, B and D from the dural side of the space. A shows a
continuous, smooth cell lining with an artificial rupture (arrowheads)
exposing the fibrillar network of the subjacent arachnoid reticular
layer. B shows the coarse fiber bundles of the dura, partially covered
by flattened cells (asterisks). C shows a cellular lining reminiscent of
that in A, but with protruding nuclear sites (N) and scattered adherent erythrocytes. D is similar to B apart from the presence of erythrocytes.
aments, and the basement membrane toward the subjacent lacunae may serve to strengthen the barrier
layer mechanically. The numerous occluding junctions
are evidently responsible for the barrier function, as
demonstrated by injections of macromolecular tracers
into the SAS (Key and Retzius, 1876; Weed, 1923;
Nabeshima and Reese, 1972) and the SDC (Key and
Retzius, 1876; present study). The function of the electron-dense material in the intercellular clefts remains
to the explained.
The subdural compartment, as defined here, corresponds to the “dural border layer” of Waggener and
Beggs (1967) and Nabeshima et al. (1975). The more
common term “subdural space” denotes a pathological
condition and therefore is a misnomer in the context of
normal anatomy (for reviews, see Haines, 1991; Haines
and Frederickson, 1991). Its persistent use may be as-
cribed to the topographically important keyword “subdural,” as opposed to “epidural” and “subarachnoid.”
Our terminology retains this word and makes it rational by defining the SDC a s a unique structure that is
histologically distinct from both the dura and the
arachnoid. The term SDC simply replaces “space” with
“compartment,” which goes with many languages and
is used also elsewhere for soft tissues enveloped by
membranes, e.g., “muscle compartments.”
Although there seems to be general agreement regarding the fundamental cellular composition of this
portion of the meninges, opinions differ with respect to
the electron density of the cells and the size of the
intercellular clefts. As discussed below, the discrepancies are probably due to difficulties with the fixation of
this avascular, not easily accessible tissue, rather than
to species characteristics.
SUBDURAL COMPARTMENT IN PIG
In well-preserved, perfusion-fixed material, obtainable only in experimental animals, the subdural cells
appear densely packed and more electron-lucent than
the arachnoid cells (Fiedler and Drommer, 1976; Andres, 1967; Himango and Low, 1971; Oda and Nakanishi, 1984; present study). They are darker in animals
perfused with high concentrations of glutaraldehyde
(Waggener and Beggs, 1967,6.2%) known to cause tissue shrinkage. In Nabeshima et al.’s (1975) material
the “dural border cells” were darker than the barrier
cells following glutaraldehyde fixation (concentration
not given), while with osmium as first fixative no such
difference was found. They invariably appear thin and
electron-dense with wide intercellular clefts in
necropsy material (Schachenmayr and Friede, 1978)
and biopsies (Lopes and Mair, 1974; Rascol and Izard,
1976; Alcolado et al., 1988) of human, as well a s in
sections from improperly fixed animals (Pease and
Schultz, 1958). I n pig we found both varieties: electronlucent subdural cells with narrow clefts in normal animals, and shrunken, electron-dense cells with wide
clefts in infused cases. As also emphasized by Andres
(1967), the cells in question appear to vary in fluid
content during anoxic, osmotic, and mechanical stress.
The shrunken and electron-dense subdural cells observed under such circumstances are reminiscent of the
“dark neurons” following manipulation of improperly
fixed brain tissue (Cammermeyer, 1962).
The classification of the subdural cells is unclear. The
name “subdural cell” was introduced by Akashi (1972)
who in contrast to us, but in agreement with general
practice as mentioned above, included in this term also
the arachnoid barrier cells outside the dark intercellular cleft. Key and Retzius (1876) and Mallory (1920)
described the cells as a “subdural endothelium” lining
the “subdural space.” More common terms are “subdural neurothelium” (Andres, 1967; Rascol and Izard,
19761, “subdural mesothelium” (Pease and Schultz,
1958; Tripathi, 1973; Alcolado et al., 19881, and “dural
border cells” (Waggener and Beggs, 1967; Nabeshima
et al., 1975; Schachenmayr and Friede, 1978; Yamashima and Yamamoto, 1985).
The terms endo-, neuro-, and mesothelium point to
certain epithelial features of the subdural cells, i.e., the
lack of fibrillary intercellular substance and the presence of adhesion junctions. The cells are, however, less
densely packed and show fewer junctions than usual
for epithelia. The layer also lacks a basement membrane toward the connective tissue of the dura. According to Nabeshima et al. (19751, the subdural cells (their
“dural border cells”) are not significantly different
from the dural fibroblasts. Also in the present material
these two cell types have many features in common,
but in our opinion the differences in electron density
and amount of organelles justify a distinction.
In support of the fibroblast nature of the subdural
cells, it has been claimed that these cells contribute to
the formation of the neomembranes encapsulating
chronic subdural hematoma (Friede and Schachenmayr, 1978; Yamashima and Yamamoto, 1985; for a
review, see Haines, 1991). Since the SDC and the
arachnoid barrier layer are both avascular, the numerous blood vessels of the neomembranes (Voris, 1946;
Watanabe et al., 1972; Apfelbaum et al., 1974; Loew
and Kivelitz, 1976) must originate from the dura. Fi-
35
brocytes from this source could grow into the neomembranes along with the vessels. In a situation with reactive changes, the subdural cells and dural fibrocytes
may be even more difficult to distinguish than under
normal conditions.
The subdural cells have also been considered a subtype of arachnoid cells (Klika, 1967; Alcolado et al.,
1988). Schachenmayr and Friede (1978) proposed to
pool them with the arachnoid barrier cells into one
common “interface layer.” In our opinion that would
represent a step backward in the search for a specific
role of the various cell types in meningeal function.
Distribution of the Infused Blood
The free flow of blood throughout the SDC in the pig,
although unexpected, may not be unique for this species. The possibility of a flow across the midline in
human is supported by the frequent occurrence of bilateral subdural hematomas, 15-50% in adults
(Kaump and Love, 1938; Leary, 1939)and up to 78% in
infants (Gutkelch, 1971), and the successful treatment
of such cases by unilateral subdural-peritoneal shunting (Aoki et al., 1985; Aoki and Masuzawa, 1988). Recent investigations with magnetic resonance imaging
have also demonstrated a bilateral dissipation of acute
unilateral bleeding (Makiyama et al., 1985; Polman et
al., 1986).
A volume competition obviously exists between the
SDC and the SAS within the rigid framework of the
dura. Since the spinal compartment of the SAS may
accommodate up to 70% of fluid injected into the cisterna magna (Lofgren and Zwetnow, 1973), i t is reasonable that most of the blood infused subdurally tends
to accumulate outside the cisterna magna and at spinal
levels. As far a s we know, involvement of the spinal
meninges has not been reported following subdural infusions in animals (Cohn, 1948; Gardner, 1932, Watanabe e t al., 1972) or in connection with subdural hematomas in humans. A negative evidence in this
regard, however, may not be conclusive because spinal
levels are seldom examined.
On the other hand, the larger brain surface, the
deeper falx cerebri (about 5 cm against 0.5 cm in the
pig), and the connective tissue strands between the cervical dura and arachnoid (Key and Retzius, 1876) in
human could perhaps contribute to a more restricted
distribution of subdural hematoma. The different
modes of bleeding, as well as possible concomitant
brain contusion, are other decisive factors.
The Subdural Cleavage Plane
Although a “subdural space” does not exist normally
(Andres, 1967; Klika, 1967; Waggener and Beggs, 1967;
Anderson, 1969; Allen and Low, 1975; Nabeshima et al.,
1975; Rascol and Izard, 1976; Schachenmayr and
Friede, 1978; Haines, 1991; Haines and Frederickson,
1991; present study), i t is a fact that a cleavage of the
SDC easily occurs either a s a dissection artifact or a s a
result of pathological processes. The tendency for the
meninges to split in the SDC was also directly demonstrated in the present study during the insertion of the
infusion cannula. The small amount of fluid encountered in the artificial “subdural space” under the lifted
and perforated dura may have been generated by leakage from the subdural cells or by pressure-generated
36
J.R. ORLIN ET AL.
a role in shearing (sliding) movements between the
brain and the skull. Judged by shape and orientation,
the subdural cells should be able to slide sideward, both
with respect to each other and to the adjacent
meninges, especially the dura. The need for such movements may become particularly urgent a t the hemispheres where the arachnoid is tightly anchored to the
pia over the gyri (Key and Retzius, 1876; Allen and
Low, 1975). That such movements really occur under
extreme conditions has been demonstrated in monkeys
whose calvarium had been replaced by a transparent
material (Pudenz and Shelden, 1946).
Subdural bleedings may originate from dural capillaries, bridging veins, and arteries of adjacent tissues
(break through bleedings). Rupture of the bridging
veins may be caused by shearing movements in the
SDC during acceleration or deceleration traumas, even
without direct impact to the head (Gennarelli and
Thibault, 19821, for example, subdural hematoma in
infants caused by violent shaking (Gutkelch, 1971;
Aoki and Masuzawa, 1986). If the SDC is expanded due
to cerebral atrophy and the veins are stretched in adDrainage of the SDC
vance (Doherty, 19881, shearing movements may be
The diffusion of erythrocytes into the sheaths of the assumed to cause subdural bleeding even after otherspinal nerve roots may be explained by the normal ul- wise negligible traumas.
trastructure of the transitional zone between the nerve
Questions might be raised about whether the locaroot sheaths and the meninges (Andres, 1967; McCabe tion of the cannula tip during infusions corresponds to
and Low, 1969; Himango and Low, 1971; Fiedler and the sites at which bleeding occurs as a result of trauma.
Drommer, 1976). The root epineurium coalesces with This uncertainty is inherent in the experimental dethe dura while the perineurium splits, the outer layers sign used. However, the correspondence between the
merge with the SDC and the inner layer with the experimental results and the pathology of traumatic
sheath of the rootlets. Evidently the blood dissects its subdural hemorrhages suggests that the experimental
way along these routes. In live individuals perhaps this data have clear relevance to this common neurosurgical problem.
could cause root symptoms.
The explanation for the contamination of the SAS in
ACKNOWLEDGMENTS
some cases of shunt bleeding is unclear. Since both the
SDC and the SAS (Klatzo et al., 1964) drain along the
The authors wish to thank K.M. Gujord, J.J. Knutspinal nerve roots, erythrocytes originating from the sen, T.A. Slyngstad, and R. Odegbrd for technical asSDC could perhaps pass centrally into the SAS along sistance, L. Schjerven and his staff for animal care, E.
the root sheaths. The absence of a typical arachnoid Buntz and her staff for library service, C. Ingebrigtsen,
barrier layer in the subarachnoid angle, where the G.F. Lothe, B. Onstad, and E. Aarseth for phototechniarachnoid reflects from the deep aspect of the dura onto cal work, K. Skullerud and N.N. Zwetnow for advice on
the rootlets (Andres, 1967; McCabe and Low, 1969; Hi- the project design, and O.P. Ottersen and D.E. Haines
mango and Low, 1971; Fiedler and Drommer, 1976), for constructive criticism. Finally we want to thank R.
could perhaps also allow a migration of erythrocytes Raaken for typing the manuscript.
directly from the SDC into the SAS. Mairova (1965)
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