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Variations in the circle of willis in Macaca mulatta.

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Variations in the Circle of Willis in Macaccr mulcrtta '
NEAL F. KASSELL AND THOMAS W. LANGFITT
Department of Neurosurgery, Pennsylvania Hospital
ABSTRACT
The circle of Willis was dissected in 75 Macaca mulatta monkeys, and
the anatomy is described and compared with several series of human specimens. The
principal difference between monkey and man is the presence of a single distal anterior
cerebral artery in the former, and the most common anomaly in the monkey is an
anterior communicating artery proximal to the junction of the anterior cerebral
arteries.
A large vessel joining the internal carotid arteries and a n accessory branch of
the anterior cerebral artery, probably communicating with the external carotid circulation, were found in a small number of our specimens. In man the posterior communicating is significantly reduced i n diameter far more frequently than the anterior
communicating artery, whereas the reverse situation obtains in the monkey.
In general, the intracranial distribution of blood i n the monkey is the same as
in man, because the similarities in the normal anatomy and variations i n the circle
of Willis outweigh their differences. However, physiological data on collateral cerebral
circulation will be more meaningful when it is based on the arterial anatomy in each
preparation.
There have been occasional descriptions
of the arterial supply of the brain in the
ape and monkey, but we have been unable
to find in the literature a detailed account
of the circle of Willis and its variations in
subhuman primates. Grunbaum and Sherrington dissected the circle of Willis and
its major branches in 11 chimpanzees and
one orangu-tan. Watts examined numerous primate species, including 53 Old
World monkeys, and described the normal
arterial anatomy at the base of the brain.
He noted the characteristic single distal
anterior cerebral artery but found in one
Macaca mulatta a n anterior communicating and two distal anterior cerebral
arteries, as i n man.
In recent years the monkey has been
used extensively in research in cerebrovascular physiology, primarily because
the extracranial cerebral circulation in
carnivora differs so much from man. Since
the interpretation of results is in part dependent upon the existence of collateral
channels of circulation similar to man,
the present study was undertaken to describe the anatomy of the circle of Willis
in a large series of monkeys and compare
the anomalies with those in the human.
MATERIALS AND METHODS
The material consisted of the brains
from 75 Macaca mulatta monkeys used
ANAT. REC.,152: 257-264.
primarily in a n investigation of the pathophysiology of acute and chronic increased
intracranial pressure. Following sacrifice
of each animal the brain was perfused
with normal saline and formalin through
the carotid arteries, followed by liquid
latex in 30 animals. The brain was removed, variations in the arterial anatomy
at the base were recorded, and the ventral
surface of the brain was photographed.
The circle of Willis was then removed,
marked appropriately, and preserved i n
formalin.
RESULTS
I. Normal circle of Willis
The normal human circle of Willis, as
defined by Padget is the familiar polygon
in which the anterior communicating artery is one-half to two-thirds the diameter
of the anterior cerebral artery, which is
half the diameter of the internal carotid
artery. Also, the posterior communicating
artery is one-half the size of the posterior
cerebral artery which is one-half the size
of the basilar artery. Using these criteria
the normal circle of Willis in the rhesus
monkey is essentially the same with the
following exceptions : the anterior communicating artery is absent, and the proximal anterior cerebral arteries fuse to form
1 Supported by a grant from the John A. Hartford
Foundation, Inc.
257
258
NEAL F. KASSELL AND THOMAS W. LANGFITT
Fig. 1 Normal circle of Willis. Single distal anterior cerebral artery and relatively small
size of posterior cerebral artery distinguished this from normal human specimen. An anterior
communicating artery was present in 46% of specimens, and one of these has been selected
for illustration.
a single vessel; the posterior communicating artery is one-third the diameter of
the posterior cerebral artery. Twenty-five
per cent of the circles of Willis in this
study were considered to be within normal
limits (fig. 1).
11. Abnormal circles of Willis
A. Absent vessels. All circles of Willis
examined in the monkey were complete.
B. Attenuated vessels. In the monkey
we have considered a component of the
circle of Willis to be significantly reduced
i n size when it is 50% or less the diameter
of its opposite number, and this occurred
i n 44% of the specimens (figs. 2 and 3 ) .
C . Accessory vessels. Accessory vessels
were present i n the form of duplication or
triplication of one of the component vessels in 60% of monkeys. Two accessory
MONKEY CIRCLE O F WILLIS
259
Fig. 2 Attenuated right posterior communicating artery. Anterior communicating artery
also present in this specimen and figure 4.
vessels were found in a small number of
specimens which are interesting in terms
of potential collateral circulation, although
not a part of the circle of Willis. A rather
large artery joining the internal carotids
above the cavernous sinus was present in
9% (fig. 4 ) , and arteries arising from the
medial portion of the anterior cerebral
artery and entering foramina posterolatera1 to the optic foramen were identified
in 5% of animals. An attempt was made
to follow the course of these latter vessels
in the latex injected preparations. Although the distribution was extracranial,
we could not be certain if they perforated
the base of the skull in the region of the
anterior portion of the sphenoid sinus or
entered the orbit.
D. Anomalous origin of vessels. None
of the specimens had an embryonic origin
of the posterior cerebral from the internal
carotid artery.
260
NEAL F. KASSELL AND THOMAS W. LANGFITT
Y
Fig. 3
Attenuated proximal right anterior cerebral artery.
E. Fusion of the anterior cerebral arteries. In 96% of the monkeys there was
fusion of the proximal anterior cerebral
arteries to form a single distal anterior
cerebral supplying both hemispheres.
F. Multiple variations. Combinations of
the above variations of the circles of Willis
occurred in 24% of the specimens.
In table 1 our findings are summarized
and compared to a large human series.
DISCUSSION
The incidence of normal circles of Willis
depends on the criteria employed, and in
human studies it has vaned from 11%
(Fawcett and Blanchford) to 73% (Hasbe).
In the study by Alpers et al. 52% of the
circles of Willis were normal by Padget’s
definition. Hodes et al. found the circle
complete in more than 1,600 consecutive
autopsies in contrast to Windle who de-
MONKEY CIRCLE O F WILLIS
26 1
Fig. 4 Large vessel joining internal carotid arteries at the level of the hypophyseal stalk.
Black marker has been inserted between the vessel and brain for contrast.
scribed absent vessels in 27 of 200 speci- present. Of the attenuated vessels 7%
mens. Alpers et al. found absence of the were posterior communicating and 24%
Posterior communicating artery in 0.6% anterior communicating arteries. Among
and the anterior communicating artery in the human
4 to 46% contained at2% Of the specimens they examined' In tenuated vessels. Alpers found attenuation
the present series the circle of Willis was
of a posterior communicating artery in
complete in all specimens.
Attenuated vessels were observed in 22% and an anterior cerebral artery in
~ ~ a m i n were
e d Patent,
44% of the monkeys, but irrespective of 396, but all v&%ds
the size of the artery a lumen was always as in the monkey.
2
9
3
0.6
0.6
5
E. Fusion of anterior cerebral
2
5
5
1 0.3
0 0
0 0
29
10
2
2
16
16
F. Multiple variations
2.6
0.6
33 9.6
28 8
3 1
2 0.6
7
2
5
1. Posterior cerebral
D. Anomalous origin
C. Accessory vessels
1. Anterior communicating
2. Anterior cerebral
a. Proximal duplication
b. Distal duplication
c. Distal triplication
3. Posterior communicating
4. Primitive olfactory artery
5. Artery joining internal carotids
1. Posterior communicating
2. Anterior communicating
3. Anterior cerebral
B. Attenuated vessels
I. Normal
11. Abnormal
A. Absent vessels
1. Posterior communicating
2. Anterior communicating
4.2
0
0
13 4
13 4
0
0
14
1 0.3
1 0.3
0
0
0
0
6
6
0
0
21
21
0
0
______
No. %
No. 7'0
Bilateral
47
1
22
22
14
1
0
0
37
20
4
4
42
29
7
6
1
0
1
No'
13
0.3
7
7
4.2
0.3
0
0
11
6
1
1
13
9
2
2
0.3
0
0.3
o9'
Combined
variations
Human
Alpers et al.
(350)
96
47
6
51
51
67
30
7
7
345
28
2
0
0
96
78
10
8
13
2
15
15
19
9
2
2
98
8
1
0
0
27
22
3
3
183 52
167 48
8
3
2
0.6
6
2
No'
Total
0
0
%
19
0
0
0
1
5
28
20
2
2
25
0
0
0
1
7
37
27
3
3
21 28
2
3
13 17
6
8
0
0
No.
0
0
0
0
1
0
1
0
0
1
1
0
1
0
0
1
0
0
3
2
1 1
2 3
1 1
0
0
No. 3' %
Unilateral Bilateral
0
71
0
0
18 24
53
0
0
18 24
96
0
0
72
0
0
53 69
35 46
6
8
3
4
3
4
0
0
1
1
4
5
7
9
53
23 31
15 20
3
4
1
1
2
3
0
0
1
1
2
3
2
3
40
0
19 25
56 75
0
0
No'
33 44
5
7
18 24
1013
0
0
%
Total
-
13
3
7
4
10
2
5
3
0
0
No'
variations
Combined
Monkey
Kassell and Langfitt
(75)
Single variation
anomalies of t h e circle of Willis in m a n and m o n k e y
Single variation
of
Unilateral
Comparison
TABLE 1
H
r
r
B
v)
&
w
w
E3
MONKEY CIRCLE OF WILLIS
Accessory vessels occurred in 69% of
the monkeys. In 46% an anterior communicating artery was present immediately proximal to the junction of the anterior cerebral arteries. Because of this
high incidence it might be equally valid
to consider an anterior communicating
artery as part of the normal circle of Willis
in the monkey. In Watts analysis of 56
Macaca mulatta monkeys an anterior communicating artery was not mentioned.
Alpers et al. found duplication or triplication of component vessels in 19% of the
human specimens. In 4% of our specimens there was duplication of one proximal anterior cerebral artery and in 4%
duplication of the distal anterior cerebral
was present, analogous to the normal human anatomy.
The artery joining the internal carotids
at the level of the hypophysis, observed in
9% of our specimens, has also been described by Padget in human embryological
studies, and recently Hayes demonstrated
communication between the internal carotids through two inferior hypophyseal and
one meningeal artery in adult man. The
vessels which take origin from the medial
portion of the proximal anterior cerebral
arteries and enter the base of the skull
beneath the optic foramina may be analogous to primitive olfactory arteries described by Padget and are indicated as
such in table 1.
Embryonic origin of the posterior cerebral artery from the posterior communicating artery occurred in 15% of the human circles of Willis examined by Alpers
et al., but this variation was not observed
in the monkey.
Fusion of the anterior cerebral arteries
was present in 2% of the human circles of
Willis examined by Alpers et al. while this
occurred in 96% of the specimens examined in the present study.
The normal anatomy of the circle of
Willis in the monkey is quite similar to
man, and though numerous anomalies occur in both species, it is unlikely that they
create significant differences in cerebral
263
hemodynamics. The major difference is a
single anterior cerebral artery in the monkey, but the anterior communicating artery
in man permits irrigation of both frontal
lobes from either side of the circle of Willis,
SO physiologically the circulation is essentially the same. The incidence of attenuated posterior communicating arteries in
man is three times that in the monkey
which may be of some significance in terms
of the contribution of the vertebral-basilar
circulation to the blood supply of the cerebral hemisphere. The accessory branch
of the anterior cerebra1 artery, probably
communicating with the external carotid
circulation, provides a collateral channel
for the anterior circle of Willis which is
apparently not present in man. However,
this was identified in only a few specimens.
A large and important accessory vessel between the internal carotid arteries was
found in one of ten monkeys, but as noted,
similar vessels have now been described
in human material.
LITERATURE CITED
Alpers, J. B., R. G. Berry and R. M. Paddison
1959 Anatomical studies of the circle of Willis
in normal brain. Arch. Neurol. Psychiat., 81:
409-418.
Fawcett, E., and J. V. Blanchford 1905-1906
The circle of Willis: An examination of 700
specimens. J. Anat. Physiol., 40: 63-70.
Grunbaum, A. S. F., and C. S. Sherrington 1902
Notes on the arterial supply of the brain in
anthropoid apes. Brain, 25: 270-273.
Hasbe, K. 1928 In das arteiensystem der Japaner, Kyoto, B. Adachii.
Hayes, G. J. 1963 External carotid-cavernous
sinus fistulas. J. Neurosurg., 20: 692-700.
Hodes, P. J., F. Campoy, H. E. Riggs and P. Bly
1953 Cerebral angiography: Fundamentals in
anatomy and physiology. Amer. 3. Roentgend.,
70: 61-81.
Padget, D. H. 1945 The circle of Willis: Its
embryology and anatomy. In: Intracranial
Arterial Aneurysms. Ed. W. E. Dandy, New
York, Comstock Publishing Co., Chapt. 111.
Watts, J. W. 1933-1934 A comparative study
of the anterior cerebral artery and the circle
of Willis in primates. Am. J. Anatomy, 68:
534-550.
Windle, B. C. A. 1888 On the arteries forming
the circle of Willis. J. Anat. Physiol., 22: 289293.
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