Download Carotid Arterial Supply of the Feline Brain

Carotid Arterial Supply of the Feline Brain
APPLICATIONS TO THE STUDY OF REGIONAL CEREBRAL ISCHEMIA
BY YOSHINARI KAMIJYO, M.D., AND JULIO H. GARCIA, M.D.
Abstract:
Carotid
Arterial
Supply
of the
Feline
Brain
• A study of the supply to the feline brain by the carotid-middle cerebral arteries was conducted using in vivo transcardiac injection with a mixture of micropaque and carbon black.
Modifications in the filling pattern of the arterial vessels were visualized following short-term
occlusion of a middle cerebral artery. A modified surgical method to induce occlusion of the M1 segment of the middle cerebral artery is also described.
Additional Key Words
cat MCA occlusion
anatomy
modified transorbital approach
arterial anastomoses
Introduction
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• The consequences of occluding a middle cerebral
artery (MCA) in the cat have been widely studied
through dynamic and structural methods in several
models of regional cerebral ischemia, or arterial infarction.1"4 The variability in the size and location of
the lesions obtained with this model is probably
dependent upon the individual variations in the
anatomy of the cerebral arteries, caliber and pattern
of the anastomotic channels,5 and changes in perfusion
pressure;6 the last factor may or may not be dependent
upon the previous two.7
The purpose of this communication is to describe
and illustrate in detail the carotid arterial system of
the cat. Special reference is made to the anastomoses
that exist among leptomeningeal arteries and between
them and the dural arteries. The anatomy of the M-l
segment of the MCA is carefully described and illustrated, as a background for previous and subsequent studies involving experimental occlusion of this
vessel. Finally, some significant modifications to
previously described methods of surgical occlusion of
the MCA are detailed.2-8
Methods
Seven adult cats weighing 2.7 kg to 3.5 kg were anesthetized
with pentobarbital (30 mg per kilogram of body weight, intraperitoneally) and subjected to transcardiac perfusion with
a solution of colloidal micropaque mixed with carbon black
(40°C),* after prewashing with a sodium chloride solution
(37°C). The injection was performed at a pressure
equivalent to the systolic blood pressure of the animal and
while the descending thoracic aorta was being clamped.
Two animals were infused with this colloidal microFrom the Departments of Pathology and Neurology, University of
Maryland School of Medicine, 22 South Greene Street, Baltimore,
Maryland 21201.
Financial support from the National Institute of Neurological
Diseases and Stroke, Grant NS 06779.
Reprint requests to Dr. Garcia.
*240 gm micropaque, 30 gm gelatin, 1.5 gm NaCl, 1.5 capfuls
"Dish Dri," 329 cc warm distilled water, and 30 ml carbon black;
keep in a refrigerator and heat it at the time of use.
Stroke. Vol. 6. July-August 1975
middle cerebral artery
microangiography
paque solution without any preliminary preparation, except
for the anesthesia, and two others were injected through the
heart with a solution of 4% formaldehyde (10% formalin)
before injecting the contrast medium mixture. Five to ten
minutes before the transcardiac perfusion, three cats had the
right MCA occluded using a modified transorbital
approach, as described below.
For a right-handed surgeon, the animal was placed in a
supine position on a headholder and the right eye was exposed. The skin incision began at the midnasal portion, at
the level of the inner palpebral angle, and extended 2.5 cm
cranially. The inner end of the incision was connected with
the inner palpebral angle to form a skin flap that included
the upper eyelid. The nictitating membrane was cut and
enucleation of the eyeball was completed without resecting
the intraorbital soft tissues. Then, the head was slightly
rotated to the left and the optic nerve was approached subperiosteally with the soft tissues being retracted inferolaterally. Once the optic nerve was sectioned at the level
of the optic canal, the illumination from the operating
microscope was placed on the inferior medial part of the
orbit while the surgical instruments were directed through
the superior lateral portion of the orbit. In this manner, the
direction of the illumination and the surgical approach were
convergent rather than parallel. The optic canal was
enlarged with a dental drill and the dura was opened; this incision started at the superior edge of the bony fenestration.
Once the previous steps were completed, the entire
carotid arterial system was dissected with the aid of the
microscope. The brain was sectioned coronally at 3 mm and
soft tissue x-rays were obtained with a Faxitron machine.
Portions of these brain slices were frozen and sectioned at
200 n for evaluation of the filling pattern of the smaller intraparenchymal arteries and arterioles. Photography was
obtained with a micro-Nikkor lens to which an M-2 ring had
been adapted.
Results
The carotid rete in the cat has two components: (1) extracranial (external), and (2) intracranial (fig. 1). The
external part of the rete extends from the foramen
rotundum to the optic foramen and receives its blood
supply from the internal maxillary artery (IM).
Several large-caliber anastomotic arteries arising
from the medial side of the external rete pass through
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KAMIJYO, GARCIA
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Soft tissue x-ray of the extradural part of the carotid arterial system of the cat at the skull base. AP:
ascending pharyngeal artery, ECR: external carotid rete, EB: eyeball, EE: external ethmoidal artery, IC:
internal carotid artery (cut end of the intradural part), IE: internal ethmoidal artery, IH: inferior
hypophyseal artery, IM: internal maxillary artery, M: meningeal branch, PIC: primitive internal carotid
artery. *Cut end of the superior hypophyseal artery anastomosing with the IE.
the orbital fissure into the cavernous sinus, where they
unite to form a major trunk which is joined by the distal end of the primitive internal carotid artery (PIC)
whose original cervical portion is vestigial in adult
cats. The convergence of these vessels forms the
relatively large-sized intracranial internal carotid
artery (ICA) (fig. 1). A meningeal arterial branch (M)
and the inferior hypophyseal (IH) artery originate
from the rete before die main trunk of the ICA is
formed. A superior hypophyseal artery originates
from the ICA either inside the cavernous sinus or immediately after the ICA pierces the dura. The superior
hypophyseal (SH) artery establishes an anastomosis
with the internal ethmoidal artery (IE) at the
chiasmatic region (figs. 1 and 2a and b). This
meningeal anastomotic branch of the SH is usually
unilateral but two out of seven cats showed bilateral
branching. After giving off a large posterior communicating artery, the ICA courses around the optic
362
chiasm giving origin to an anterior choroidal artery
and a few small branches that supply the anteromedial
portion of the pyriform lobe. Then, the ophthalmic
artery originates; its size varies from a trace to 100 \i
in outer diameter. In one-half of the animals studied
by us, the ophthalmic artery was not visible. Near its
bifurcation, the ICA gives rise to several branches that
supply the anterior hypothalamic region (figs. 2a and
b).
Usually, as a first branch, the anterior cerebral
artery (ACA) gives off a perforating (striate) branch
that corresponds to the Heubner artery of the human
brain (figs. 2a and b). The anterior communicating
artery, as it exists in humans, was absent in the
animals studied but an anastomosis between the ACA
and a branch of the contralateral ICA was seen in
some animals. A large anastomotic vessel between the
ACA and the internal ethmoidal artery was observed
on the medial surface of the olfactory bulb (figs. 1 and
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CAROTID ARTERIAL SUPPLY OF THE FELINE BRAIN
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3). Such anastomosis is usually unilateral but some
small branches establish a bilateral connection. The
ACA gives off a major branch that supplies the falx
and the dura covering the frontal convexity. In
addition, the ACA has a group of branches that connect it with the ethmoidal plexus (fig. 3).
The site of the ICA bifurcation varies from 0.9 to
2.1 mm from the midline (average distance: 1.5 mm).
The midline was drawn at the midpoint of a straight
line connecting the lateral angles of the right and left
anterior perforated substances (figs. 2a and b).
The initial portion of the MCA courses
horizontally in a slightly caudal direction (figs. 2a and
b). The external diameter of the first segment of the
MCA varies from 0.70 to 0.75 mm in the pre-fixed
material. The position of the perforators' branching
point varies considerably. The site of origin of the first
perforator is found anywhere between 3.3 mm and 7.8
mm (average 5.1 mm) from the midline (figs. 2a and
b). The medial striate group in most animals
originates from the ACA (equivalent to the Heubner
artery). When these are small, one finds that the
medial striate group of perforators originates from the
MCA proper. The number of main perforators
(defined as those more than 80 n in external diameter)
that originates from the MCA varies between two and
five. The last ones originate either from the main
trunk of the MCA (M-l) or from an MCA branch
(M-2), distal to the anterior perforated substance;
therefore, in order to reach their point of entrance into
the parenchyma, these branches turn back sharply
forming a narrow angle with the parent vessel (figs. 2a
and b). After branching several times, the majority of
these vessels penetrate the cerebral parenchyma
through the lateral corner of the anterior perforated
substance to form the lateral striate arteries. In the M1 segment of the MCA one constantly finds only one
small cortical branch that supplies the anterolateral
part of the pyriform lobe (figs. 2a and b). The origin of
this branch is found anywhere between 3.6 mm and 7.5
mm (average: 6 mm) from the midline. In one case we
found a branch originating from the ICA and giving
off cortical branches that supply the medial and lateral
pyriform area and the posterior sylvian gyrus.
In the cat, the MCA irrigates the entire lateral
surface of the cerebral hemispheres and the orbital
surface lateral to the olfactory tract with the exception
of the sigmoid gyrus, the marginal gyrus and the
posterior composite gyrus (figs. 4 and 5) where the
MCA anastomoses with several branches of the ACA
and the PCA. The nomenclature used to designate the
feline cerebral gyri is based on that of Crouch's.9 The
size of the leptomeningeal anastomoses may be up to
130 n when measured on the outer surface (fig. 5). In
addition, numerous smaller connections form a
network among individual branches. From this
network the cortical penetrating branches originate.
Anastomoses between the MCA and dural
arteries were not observed, except for one animal in
Stroke, Vol. 6. July-August 1975
which a dural artery was seen; this originated from a
cortical branch of the MCA over the anterior frontal
convexity and measured 100 n in external diameter.
Following unilateral occlusion of the MCA with
a ground Heifetz clip* there was good filling by contrast medium of the main striate branches and the
circumferential branches over the hemispheric surfaces (figs. 4 to 6b). The differences in density between
the two hemispheres are explained on the basis of poor
filling of the fine branches corresponding to the cortical perforators. The long subcortical perforating
arteries show essentially the same filling pattern in
both hemispheres (fig. 6b). In the material studied by
us it was not clear whether distal anastomoses between
the medial and lateral group of striated arteries existed.
Discussion
In lower vertebrates, the designation of carotid rete
(rete mirabile) is applied primarily to a compact
network of freely anastomosing arteries, interlaced
with a venous plexus, that are associated with a
vestigial or hypoplastic internal carotid artery, such as
is found in the cat, sheep, goat, ox and pig.1015 A true
rete mirabile means a network of fine arterial twigs interlaced with venous plexus supplying the circle of
Willis from the external carotid artery, as mentioned
above. Frequently, the term rete mirabile has been
used in a broader sense to designate anastomotic
channels between the external carotid artery branches
and the leptomeningeal arteries on the surface of the
brain.16
The so-called circle of Willis of the arterial tree,
which is located at the base of the brain in humans,
differs from the feline one in the following aspects.
In the cat, the ophthalmic artery originates from
the distal end of the ICA (Cl) and supplies the frontoorbital meninges, establishing anastomoses with the
ciliary artery. The size of the ophthalmic artery varies
considerably and sometimes is completely absent.
The anterior communicating artery does not exist
in the cat, and this is in agreement with Hiirlimann,
although others have described one.10-12
There are several varieties of anastomoses
between the intradural vessels and the meningeal
vessels. (1) The falx and the dura over the frontal convexity are supplied by branches of the ACA, which
anastomose directly with the internal ethmoidal artery
and indirectly with the external ethmoidal artery, via
the ethmoidal plexus. At the latter, the right and left
ACA join one another, although in some cats both
ACAs are connected directly via the internal
ethmoidal artery. (2) Anastomoses between the internal ethmoidal and the superior hypophyseal artery
are found constantly. (3) There is an inconstant dural
branch which originates in MCA branches. Such was
*The tip of the Heifetz clip was ground triangularly to make its
application easy and safe.
363
KAMUYO, GARCIA
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NOUHSloANOb
Ventral view of the cat brain. Arterial system is filled with colloidal micropaque solution mixed with carbon
black through the heart IC: internal carotid artery, IE: internal ethmoidal artery, LS: lateral striale
arteries, MC: middle cerebral artery, MS: medial striate arteries (Heubner's artery), SH: superior
hypophyseal artery. *Cut end of the SH connecting with the IE at * mark in figure I.
364
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CAROTID ARTERIAL SUPPLY OF THE FELINE BRAIN
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Slrokt, Vol. 6, July-August 1975
365
KAMIJYO, GARCIA
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found in one animal, although its caliber was small.
Anastomoses between the anterior cerebral
artery and the middle cerebral artery as well as
between the middle cerebral artery and the posterior
cerebral artery are abundant over the sigmoid gyrus,
the marginal gyrus, and the posterior composite
gyrus, but they are less abundant between the MCA
and the ICA branches over the pyriform lobe. The
potential for efficient collateral circulation, in the
presence of large artery occlusion, is limited to the
larger leptomeningeal arteries. In the cat, these are
considered to be more than 70 /x in external diameter.
The fine leptomeningeal network is inefficient for such
a purpose, as previously described in humans by
Vander Eecken.6- »•18
When one uses the transorbital approach to the
MCA, with the modifications described herein, the
proximal portion of the MCA is surgically inaccessible due to the near-midline location of the ICA
point of bifurcation. The lateral edge of the optic
OB
366
Anterior portion of medial surface of the cat brain. AC anterior
cerebral artery, IE: internal ethmoidal artery, MB: meningeal
branch of AC, OB: olfactory bulb branch.
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CAROTID ARTERIAL SUPPLY OF THE FELINE BRAIN
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'
FIGUII3
Dorsal view of the same brain as figure 4; note the size and number of the leptomemngeal collateral channels
between A CA and MCA. PC A and MCA. Basic filling pattern of leptomemngeal arterial networks is same
on both hemispheres, although the background is pale on the clipped side.
canal is located approximately 5 mm from the
midline, which thus becomes the most proximal site
where the MCA could be clipped, using the modified
technique previously described. With O'Brien and
Waltz's approach, 2 the most proximal site at which
the artery can be clipped is 4 mm from the midline, as
measured from their illustrations. The presence of a
paranasal sinus (ethmoidal sinus) close to the medial
FIGURI 4
Lateral view of the cat brain. Colloidal micropaque solution is perfused through the heart with clip placed
on MCA on the side shown. The MCA territory is filled retrogradely via leplomeningeal collateral
channels. AS: anterior sylvian gyrus, C: coronal gyrus, ES: eclosylvian gyrus, M: marginal gyrus. PC:
posterior composite gyrus, PS. posterior sylvian gyrus, S: sigmoid gyrus, SS: suprasylvian gyrus.
Slrokt, Vol. 6, Juty -Augvil
1975
367
KAMIJYO, GARCIA
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6b
FIGURES 6a AND b
Coronal sections of the same specimen as in figures 4 and 5, illustrating in 6a pallor of the cortex on the
right hemisphere. The site of the clip is indicated by an arrow. In 6b. which is a soft tissue x-ray of the
specimen, filling of the MCA branches distal to the point of occlusion occurs in a retrograde fashion. The
differences in the color density of the two hemispheres are due to lack of filling in some of the short cortical
perforators. Note the slight pallor in the lateral half of the caudate nucleus which thus becomes the most
peripheral arterial field after occluding the main trunk of the MCA.
368
Stroke, Vol. 6. July-August 1975
CAROTID ARTERIAL SUPPLY OF THE FELINE BRAIN
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half of the optic canal constitutes one more
anatomical reason for failing to have access to the initial millimeters of the MCA in the cat, when one uses
the transorbital approach. In older cats (over 3.6 kg of
body weight) this paranasal sinus extends even more
laterally than in younger animals and surrounds the
optic canal completely, thus making it impossible to
reach the MCA without entering the sinus and increasing the possibility of postoperative infectious
complications.
In chronic experiments in which temporary
clipping of the MCA is desirable, we have determined
that the modifications to the transorbital approach
described herein are advantageous, primarily at the
time when the clip is to be removed, which is the most
difficult part of the surgical procedure. During this
maneuver, direct visualization of the blade of the
Heifetz clip is essential, in order to avoid damage to
the arterial wall and the surrounding structures. The
convergent direction of the illumination axis and that
of the clip applicator, as previously described,
facilitate this maneuver immensely.
Acknowledgments
The authors acknowledge with gratitude the technical help of Mr.
Harold Bell, and the secretarial assistance of Mrs. Debra Haines.
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369
Carotid Arterial Supply of the Feline Brain: Applications to the Study of Regional Cerebral
Ischemia
YOSHINARI KAMIJYO and JULIO H. GARCIA
Stroke. 1975;6:361-369
doi: 10.1161/01.STR.6.4.361
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