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The diameters of the cerebral arteries of the human fetus.

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The Diameters of the Cerebral Arteries
of the Human Fetus '
H. GUNTER SEYDEL
Departments of Anatomy and Radiology,
Wayne State University College of Medicine,
1401 Rivard Street, Detroit 7, Michigan
ABSTRACT
Ninety-eight fetal specimens of the circulus arteriosus cerebri and
adjacent arteries were injected with a mixture of latex and barium sulphate and
dissected after fixation in formalin. Measurements of the intracranial part of the
internal carotid artery were carried out and the measured diameters were compared
to those of the other arteries a t the base of the fetal brain. The diameters of the
internal carotid artery were symmetrical and increased approximately linearly with
fetal size from 0.7 m m for a fetus of 15.5 cm crown rump length to 2 m m i n a
specimen with 37.2cm crown rump length. In one specimen, the intracranial part
of the right internal carotid artery was smaller than the left. This was associated
with a n anomaly of the arterial circle. Twenty-one circles were symmetrical and
complete. The most significant differences between adult and fetal diameters were
in the posterior part of the circle, the circular part of the posterior cerebral artery
showing a relatively smaller average diameter (0.34 of the diameter of the internal
carotid artery) than that described for adult specimens (0.47) while the posterior
communicating arteries were of similar diameter (approximately 0.27) i n both adults
and fetuses. In three cases one posterior communicating artery was absent. No berry
aneurysms were found upon inspection with a hand lens.
Since Willis (1664) gave the first complete description of the anatomy of the arteries at the base of the human brain,
many studies of their relationships to each
other have been published. Summaries of
the studies which were made on adult
brains have been published by deVriese
( ' 0 5 ) , Padget ('47), Alpers, Berry and
Paddison ('59) and Gillilan ('59). The
relative sizes of the vessels were usually
described but specific measurements of
individual vessels are given only in the
papers by Lewis (1881), Hasebe ('28),
Alexander and Putnam ('38), Metz ('49),
Orlandini ('51 ), Neimanis ( ' 5 7 ) , and Pallie and Samarasinghe ('62). Reports of
anomalies of the circulus arteriosus of
Willis and of the adjacent arteries have
also been published recently by Priman
and Christie ('59), Kirgis, Llewellyn and
Pebbles ('60), McCullough ('62), and
Alpers and Berry ('63). Only one author
(devriese, '05) has reported on the arteries of newborns and fetuses but she gave
no measurements.
The purpose of the present study was to
measure the internal carotid arteries in human fetuses and to evaluate the diameter
of the other arteries for their relative size.
ANAT. REC., 150: 79-88.
Also, a search was made for berry aneurysms.
METHODS AND MATERIALS
Ninety-eight human fetuses and newborns ( 5 1 male and 47 female) were examined. They measured between 15.5 cm
and 37.2 cm in crown rump length with a
mean of 23.7 cm. According to Boyd ('41)
these measurements correspond to the
fiftieth percentile lengths at 18 post-menstrual weeks and at term, the mean being
25 weeks. The specimens were obtained
frozen from various hospitals in Detroit.
Premature and stillborn babies represented
the major portion of the material. Previously autopsied specimens were not used.
The fetuses were defrosted slowly, and
the common carotid arteries were exposed.
Glass cannulas were tied loosely into the
common carotid arteries and connected by
thin rubber tubing to a syringe which contained a mixture of liquid latex and barium sulphate suspension. The barium
sulphate suspension was prepared by dis1 Based upon a , thesis submitted in partial fulfillment of the requirements for the deeree Master of
Science, June, 1961. The author gratefully acknowledges the advice and encouragement given by Dr.
Ernest Gardner, Dr. Maurice Tatelman and Dr. Ronan
O'Rahilly.
79
80
H. GUNTER SEYDEL
solving 15 gm of a commercial barium
sulphate preparation in 25 ml of water.
One to two parts of this suspension were
mixed with one part of the liquid latex.
Injection was made by hand and the material was allowed to extravasate from the
common carotid artery at the point of insertion. This prevented extravasation of
contrast material from the intracerebral
arteries due to high pressure of injection.
According to Tilling ('58), a similarly prepared barium sulphate contains particles
smaller than red cells but does not pass
through capillaries because of agglutination of the particles. Two to 5 ml of the
contrast material were used for each injection. When extravasation occurred, the
common carotid arteries were tied and
radiographs were obtained in the anteroposterior, lateral, and both posterior oblique positions, using Kodak non-screen
film and cardboard holders, and a portable
x-ray unit. Examples of the radiographs
are shown in figure 2. The specimens were
then immersed in 10% formalin solution
for at least six weeks.
Before dissection, the radiographs were
examined for obvious abnormalities of the
cerebral arteries and for aneurysms. No
aneurysms were encountered in the radiographic examinations. Dissection was
started with removal of the skull cap. The
brain and brain stem together with the
intracranial portions of the internal carotid
arteries and other blood vessels were then
carefully removed and the arteries dissected under water. A hand lens was used
to search for aneurysms.
Measurements of the dissected arterial
circles and attached vessels were then
made with a micrometer. The diameters
of the internal carotid arteries were measured 2 to 4 mm proximal to the origin of
the middle cerebral artery. Those of the
anterior cerebral, posterior cerebral, and
middle cerebral arteries were measured at
their origin. The diameters of the cerebral
arteries were expressed as a fraction of the
diameter of the left internal carotid artery.
Similar measurements and comparisons
were carried out for the anterior and posterior communicating and for the basilar
arteries, using their midpoints, and for the
vertebral arteries approximately 2 mm
from their junction to form the basilar
artery.
The accuracy of the measurements was
influenced by the accuracy of the micrometer, which could be read at 0.1 mm
markings. It is also evident that the arteries were near the limits of their elasticity. Metz ('49) examined dissected arteries from adults for elasticity, and found
that the distended arteries increased their
in sit= diameter up to one-fourth when
they were exposed to a pressure which
brought them close to rupture. The effect
of the elasticity of the arterial wall should
influence only the measurement of the internal carotid arteries because the diameters of the other arteries are expressed as
relative measurements.
Nomenclature
Figure 3 introduces the nomenclature
used in this study. For an accurate description of the portions of the circulus
arteriosus cerebri (of Willis) the nomenclature described in the Nomina Anatomica
('61) was extended by adding separate descriptions for the parts of the anterior and posterior cerebral arteries which
participate in the formation of the circulus arteriosus. Following a suggestion by
Mitterwallner ('55), the portion of the anterior cerebral artery which participates in
the formation of the circulus arteriosus is
called the circular part of the anterior cerebral artery, whereas the portion anterior
to the anterior communicating artery is
called antero-circular part of the anterior
cerebral artery. The posterior cerebral
artery is divided into two portions, the
circular part of the posterior cerebral artery being the part participating in the
formation of the circulus arteriosus, whereas the postero-circular part of the cerebral
artery is the portion distal to the posterior
communicating artery.
RESULTS
The results are reported in two parts.
The first is the description of the regular
configuration of the arteries at the base of
the fetal brain. The second is a descrip2 The
commercial barium sulphate preparation
Barotrast, generously supplied by Barnes-Hind Phar:
maceuticals, Inc., contains particles between 0.4 and
1.5 f i i n size, according to the manufacturer.
81
CEREBRAL ARTERIES O F THE FETUS
tion of the deviations from the regular disposition for the individual arteries.
The regular configurations of the
circulus arteriosus
According to the descriptions in current
textbooks of anatomy, the normal circulus
arteriosus is symmetrical and all arteries
participating in the formation of the circulus arteriosus are present. This configuration was found in 21 of 98 examined
specimens; 14 specimens were male and
seven female. The internal carotid artery
was symmetrical in 97 of 98 specimens.
Its diameter increased approximately linearly with fetal size from 0.7 mm for a
fetus of 15.5 cm crown rump length to
2 mm in a specimen with 37.2 cm crown
rump length. Plotting of the measured
data showed that there were only slight
differences between the diameters of the
intracranial portion of the internal carotid
arteries in the female and male fetuses
(fig. 1 ) .
Table 1 gives the diameter of all examined vessels expressed as fractions of the
diameters of the left internal carotid artery. The diameters for the 21 regular
circles are also listed separately.
Variants
Internal carotid artery, intracranial part.
One of the 98 specimens showed asymmetry of the internal carotid arteries, the
right measuring 0.4 mm and the left
1.1 mm. There was an associated anomaly
of the circulus arteriosus with an absent
left posterior communicating artery and
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DIAMETER OF INTERNAL CAROTID ARTERY mm.
0.6
0.8
Fig. 1 Diameter of the left internal carotid artery plotted against the crown-rump length
of the fetus.
82
H. GUNTER SEYDEL
TABLE 1
Diameters of arteries a t the base of the fetal brain expressed as fractions of the diameter
of the left internal! carotid artery, with their standard deviations
Reeular circles
Anterior cerebral artery
Circular part
Antero-circular part
0.52f0.04
0.452 0.09
All circles
0.4920.23
0.42C 0.26
Anterior communicating artery
0.21 0.10
*
0.24f0.11
Middle cerebral artery
0.75f0.11
0.75-C0.08
Posterior communicating artery
0.2720.05
0.29f 0.18
Posterior cerebral artery
Circular part
Postero-circular part
0.402 0.12
0.39% 0.19
0.34f0.13
0.36& 0.13
Basilar artery
0.88 ‘-c 0.17
0.832 0.35
Right vertebral artery
0.61f0.35
0.58r 0.27
Left vertebral artery
0.652 0.27
0.602 0.25
Internal carotid artery
1.00
1.00
a small circular part of the right anterior
cerebral artery. Thus, the antero-circular
parts of both anterior cerebral arteries and
the left middle cerebral artery were supplied by the left internal carotid artery,
while the remainder of the anterior arterial
circle was supplied by the right internal
carotid and by the basilar arteries.
Middle cerebral arteries
The right middle cerebral artery was
larger than the left in five specimens (two
male and three female), and the left was
larger than the right in one female.
Circular part of the anterior
cerebral artery
This vessel was larger on the right in
seven specimens (five male and two female) and on the left in eight specimens
(one male and seven female).
Four cases deserve special mention. One
is an anomaly of the circulus described
above under “Internal carotid artery” in
which the circular part of the right anterior cerebral artery was very small (0.17).
In three specimens (two female and one
male), the diameter of the right vessel was
0.75 that of the internal carotid artery,
whereas the diameter of the left was only
0.33. The diameter of the anterior communicating artery was 0.33 that of the internal carotid artery, and the antero-cir-
cular parts of both anterior cerebral arteries measured 0.5.
In one other specimen, the left vessel
showed what has been called “island formation,” that is duplication of a part of
the vessel.
Antero-circular part of the anterior
cerebral artery
This vessel was larger on the left side in
six cases, (four male and two female) and
larger on the right in five cases (one male
and four female). In one male, the right
vessel divided into two branches of equal
size, 0.33 of the internal carotid artery,
while the left measured 0.5 and was single.
Anterior communicating artery
The artery was duplicated in 14 specimens (nine male and five female). Triplications were present in seven specimens
(four male and three female). Y configuration occurred in five cases (three male
and two female) and V configuration in
four cases (two male and two female).
The V configuration is not included in the
duplications.
A vessel termed “median artery of the
corpus calIosum” has been described by
deVriese (’05) and Luna (’14). This vessel, which is of variable length, originates
from the anterior communicating artery
and follows the longitudinal fissure. It
CEREBRAL ARTERIES OF THE FETUS
may be the only vessel forming the anterocircular part of the anterior cerebral arteries. In many instances, branches originate
from the anterior communicating artery in
the direction of the longitudinal fissure.
Minute branches, less than 0.12 of the
diameter of the internal carotid artery,
were present in 17 cases (nine male and
eight female). Small arteries, measuring
between 0.12 and 0.25 of the diameter of
the internal carotid artery, were present in
seven specimens (four male and three female). Larger arteries, 0.25 or more of the
diameter of the internal carotid artery were
found in one male and one female. There
were no cases in which the median artery
of the corpus callosum replaced the antero-circular parts of the anterior cerebral
arteries.
Posterior communicating artery
The right posterior communicating artery was larger than the left in 16 specimens (seven male and nine female),
whereas the left was larger in 16 specimens (eight female and eight male). The
right was missing in one male, and the
left was missing in one male and one female.
The right vessel was larger than the
right circular part of the posterior cerebral
artery in 29 cases (13 male and 16 female)
whereas the left vessel was larger than the
left circular part of the posterior cerebral
in 26 cases (11 male and 15 female). The
right vessel was equal to the circular part
of the posterior cerebral artery in 17 cases
(six male and nine female) and the left
was equal to the left circular part of the
posterior cerebral artery in 18 cases (ten
male and eight female).
Circular part of posterior
cerebral artery
The right vessel was larger than the left
in six specimens (three male and three
female) whereas the left was larger in five
specimens (three male and two female).
Postero-circular part of the posterior
cerebral artery
The right vessel was larger than the left
in seven cases, (three male and four female). The left was larger in six cases
(three male and three female).
83
Basilar artery
The basilar artery was considerably
smaller than average in four cases, all female. Three diameters measured 0.33,
and one 0.25 of the diameter of the internal carotid artery.
Vertebral arteries, intracranial part
The left vertebral artery was larger than
the right in 26 cases (13 male and 13 female) and the right larger than the left in
13 cases (six male and seven female).
DISCUSSION
The scarcity of published measurements
makes it difficult to compare the data reported here for the fetal arterial circle with
those reported for adult circles. According
to Padget (’47), the size of the posterior
communicating arteries relative to the circular part of the posterior cerebral arteries
is one of the main differences between the
fetal and adult types of the circulus arteriosus. She describes three configurations :
“normal,” in which the posterior communicating artery is smaller than the circular
part of the posterior cerebral artery, “transitional,” in which the diameters are equal,
and “primitive,” in which the circular part
of the posterior cerebral artery is smaller
than the posterior communicating artery.
The last two configurations also have been
called “transitional trifurcation” and “trifurcation of the internal carotid artery” respectively. DeVriese’s description suggests
that the posterior communicating arteries
are larger than usual more often in fetuses
than in adults, and therefore the term
“fetal trifurcation” has been used for “trifurcation of the internal carotid artery”
(Kirgis et al., ’60). If the normal diameter
of the posterior communicating artery is
considered to be one-half of that of the
circular part of the posterior cerebral,
deVriese finds that in the fetus 60% of the
right posterior communicating arteries and
58% of the left are larger than normal.
The respective values for the adult brains
examined by her are 30% and 24%. One
or both posterior communicating arteries
are larger than the circular part of the
posterior cerebral artery in 56% of the
fetal brains, but in only 14% of the adult
brains. The reverse is found in 66% of
fetal brains and 90% of adult brains. As
84
H. GUNTER SEYDEL
TABLE 2
Relative diameters of the posterior cerebral artery and of the posterior
Communicating artery. The figures are per cent of brains examined
Number
of brains
examined
Circular
Circular
part of
part
of
posterior
postemor
cerebral
Posterior
cerebral
artery
communicating
artery
smaller
artery
equal to
than
absent
posterior
posterior
communicating communicating
artery
artery
%
Alpers and Berry ('63)
Blackburn ('07)
Fawcett and Blachford ('06)
Fetterman and Moran ('41)
Hasebe ('28)
Kleiss ('41)
von Mitterwaher ('55)
Riggs and Griffith ('38)
Stopford ('15)
de Vriese, adults ('05)
de Vriese, fetuses ('05)
Windle (1888)
Seydel
194
220
700
200
83
325
360
566
150
50
100
100
98
table 2 shows, the present data indicate a
similar incidence of these configurations.
If a comparison of the diameters is applied to Hasebe's 83 illustrated cases for
adults in a manner comparable to that
used in this study, the average diameter of
posterior communicating arteries in his
studies is 0.27 of the diameter of internal
carotid artery, which is similar to the situation in fetuses. However the average
diameter of the circular part of the posterior cerebral artery in his studies is 0.47
which is considerably greater than the 0.34
found in the present series for the fetal
posterior cerebral arteries. Although Lewis
( 1881) did not include any measurements
of the adult posterior cerebral arteries in
his study, he described the circular part of
the posterior cerebral artery as being approximately two-thirds of the diameter of
the basilar artery, which in turn was nearly
equal to the internal carotid artery. This
is even higher than the above mentioned
values.
Considering the anterior portion of the
circulus arteriosus, the incidence of abnormalities is charted in table 3. Comparable
data of other authors are included. Padget
('47) describes the circular part of the
anterior cerebral artery in the adult as normally one-half of the diameter of the internal carotid artery, and the anterior com-
28
21.5
36
15
10.2
35.7
20
41
35
%
%
14.6
30
1.5
0.6
1
3.6
3.5
1.2
0.3
0.3
25.7
16.8
18
26.7
10
14
56
12
56
7
12.5
3
municating artery as one-half to two-thirds
of this diameter. These estimates can be
supported by an evaluation of Hasebe's
circles. The occurrence of a very thin unilateral circular part of the anterior cerebral artery leads to so called "anterior trifurcation" (Kirgis et al., '60) with a large
opposite artery supplying both antero-circular parts of the anterior cerebral artery.
This variant occurs in approximately 4%
of the brains examined by deVriese, both
in adults and fetuses, and in 3% in the
present study. It is therefore evident that
significant differences in caliber are more
frequent in the posterior part of the circle
than in the anterior part.
CONCLUSIONS
The study confirmed the previously described findings that the symmetrical, regular configuration of the circulus arteriosus
cerebri is present in only about one-fifth of
cases (20.6% ). The differences in diameters of the posterior communicating artery
and the circular part of the posterior cerebral artery are the main distinction between the fetal and adult disposition. In
the fetus, the posterior communicating artery is more likely to be larger than or
equal to the circular part of the posterior
cerebral artery, whereas in the adult the
posterior communicating artery is usually
85
CEREBRAL ARTERIES O F THE FETUS
TABLE 3
Anomalies of the anterior part of the Circle of Willis. The figures are
per cent of brains examined
Anomalies
artery
%
Alpers and Berry ('63)
Blackburn ('07)
Fawcett and Blachford ('06)
Hasebe ('28)
Kleiss ('41)
von Mitterwallner ('55)
Riggs and Griffith ('38)
Stopford ('15)
de Vriese adults ('05)
de Vriese fetuses ('05)
Windle (1888)
Seydel
194
220
700
83
325
360
566
150
50
100
100
98
smaller. Otherwise, the incidence of anomalies of the fetal arteries does not seem
to be significantly different from that in
the adult brain.
LITERATURE CITED
Alexander, Leo, and J. Putnam 1938 Pathological Alterations of the Cerebral Vascular Pattern. Association for Research in Nervous and
Mental Diseases, Research Publications, Vol.
VIII, The Circulation of the Brain and Spinal
Cord, Baltimore, Williams and Wilkins Co., pp.
471-543.
Alpers, Bernard J., and Richard G. Berry 1963
The Circle of Willis in cerebral vascular disorders. Archives of Neurology, 8: 398402.
Alpers, Bernard J., Richard G. Berry and Richard
M. Paddison 1959 Anatomical studies of the
Circle of Willis i n normal brain. AMA
Archives of Neurology and Psychiatry, 81:
409418.
Blackburn, I. W. 1907 Anomalies of the encephalic arteries among the insane. J. Comp.
Neur., 17: 493-509.
Boyd, Edith 1941 Outline of Physical Growth
and Development, Minneapolis, Burgess Publ.
Co., Plate 9.
Fawcett, F., and J. V. Blachford 1906 The
Circle of Willis, a n examination of 700 specimens. Journal. of Anatomy and Physiology,
40: 63-70.
Fettermann, George, and Thomas Moran 1941
Anomalies of the Circle of Willis in relation to
cerebral softening. Archives of Pathology, 32:
251-257.
Gillilan, Lois A. 1959 Significant superficial
anastomosis of the arterial blood supply to the
human brain. J. Comp. Neur., 112: 55-74.
Hasebe, J. 1928 In: Adachi, Buntaro, Das Arteriensystem der Japaner. Kyoto, Maruzen Co.,
Bd. 1, pp. 111 ff.
11
10
8
63.3
56.4
24.8
47.9
14
48
58
14.5
31
%
%
0
15
49.3
10
27.3
44.3
1.2
0.6
3.3
6
4
0
4
5
1
15
0
Kleiss, Ekkehard 1941 Die verschiedenen Formen des circulus arteriosus cerebri Willisii.
Anatomischer Anzeiger, 92: 216-230.
Kirgiss, Homer D., Raeburn C. Llewellyn and
Edward McC. Pebbles 1960 Functional trifurcation of the internal carotid artery and it's
potential clinical significance. Journal of Neurosurgery, 17: 1062-1072.
Lewis, Bevan 1881 On methods of preparing,
demonstrating, and examining cerebral structure i n health and disease. Brain, 3: 314-336
and 502-515.
Luna, E. 1914 Studie nella morfologia delle
arterie dell' encefalo. I. Morfologia e morfogenesi delle arterie della superficie del bulbo
e del ponte. Richerche del Laboratorio Anatomico Roma, 18: 117, (quoted by Mazzella in
Richerche anatomo-radiografiche sulla morfogenesi delle arterie dell' encefalo. Ateneo
Parmense, 26: 580-603, 1955).
McCullough, A. W. 1962 Some anomalies of
the cerebral arterial Circle (of Willis) and related vessels. Anat. Rec., 142: 537-543.
Metz, Ulrich 1949 Physikalisch-morphologische
Untersuchungen ueber Festigkeit und Dehnbarkeit der basalen Hirngefaesse. Virchow's
Archiv., 317: 385-413.
von Mitterwallner, F. 1955 Variationsstatistische Untersuchungen a n den basalen Hirngefaessen. Acta anatomica, 2 4 : 51-87.
Neimanis, G. 1956 Ueber Kaliberschwankungen
und Verlaufsanomalien des intrakraniellen Abschnittes der arteria vertebralis. Frankfurter
Zeitschrift fuer Pathologie, 67: 461484.
Nomina
Anatomica 1961 Excerpta Medica
Foundation, Amsterdam.
Orlandini, I. 1951 I1 sistema arterioso della
testa e del collo. Atlante Anatomo-radiografiche. Cappelli, Bologna.
Padget, D. 1947 Embryology and Anatomy of
the Circle of Willis. I n : Dandy, W., Intracranial Arterial Aneurysms. Ithaca, New York,
Comstock Publ. Co., chapter 111.
86
H. GUNTER SEYDEL
Pallie, W., and D. D. Samarasinghe 1962 A
study in the quantitation of the Circle of Willis.
Brain, 85: 569-578.
Priman, Jacob, and Dorothy H. Christie 1959
A case of abnormal internal carotid artery and
associated vascular anomalies. Anat. Rec., 134:
87-95.
Riggs, Helena, and John 0. Griffith 1938 Anomalies of the Circle of Willis in persons with
nervous and mental disorders. Archives of Neurology and Psychiatry, 39: 1353-1356.
Stopford, J. S. B. 1915-1916 The arteries of
the pons and medulla oblongata. Journal of
anatomy and physiology, 50: 131-164 and 255280.
Tilling, Gunnar 1958 The Vascular Anatomy
of Long Bones. Acta radiologica, Suppl. 161, p.
18.
devriese, Bertha 1905 Sur la signscation morphologiques des arteres cerebrales. Archives de
biologie, 21: 357457.
Willis, T. 1664 Cerebri Anatome, London, J.
Fleshner .
Windle, Bertram C. 1888 On the arteries forming the Circle of Willis. Journal of Anatomy
and Physiology, 22: 289-293.
PLATE 3
EXPLANATION OF FIGURES
2
Radiographs of normal cerebral arteries after injection of both common carotid arteries.
L e f t Upper: Antero-posterior position.
Right Upper: Right lateral position.
L e f t Lower: Right posterior oblique position.
Right Lower: Left posterior oblique position.
CEREBRAL ARTERIES OF THE FETUS
H. Gunter Sevdel
PLATE 1
a7
CEREBRAL ARTERIES OF THE FETUS
H. Gunter Seydel
3
Injected specimen of the circulus arteriosus (approximately actual size) and nomenclature of the vessels a t the base of the brain.
A, Median artery of the corpus callosum
B, Anterior cerebral artery, antero-circular part
C , Anterior communicating artery (Double)
D, Anterior cerebral artery, circular part
E, Middle cerebral artery
F, Internal carotid artery
G , Posterior communicating artery
H, Posterior cerebral artery, circular part
I, Posterior cerebral artery, postero-circular part
J, Basilar artery
K, Vertebral artery
88
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