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Normal variations in the caliber of the human cerebral aqueduct.

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NORMAL VARIATIONS I N T H E CALIBER O F T H E
HUMAN CEREBRAL AQUEDUCT
G. FLYGER AND U. HJELMQUIST'
Department of Histology, Earolinska Institutet and the Neurosurgical Clinic,
S6dersjukhuset, Stockholm, Sweden
ONE FIGURE
About 10 years ago Lelcsell elaborated a new surgical procedure for the relief of non-communicating hydrocephalus
due to obstruction at the aqueduct of Sylvius. Briefly, the
method consists of, through the usual suboccipital exposure,
easing a soft small rubber catheter up the aqueductal lumen
until it is insured, by suction, that the tip has entered the third
ventricle, when the catheter is removed. A spiral of metal
wire is threaded onto the tip of the catheter, which is then
reinserted. When the spiral is in correct position, the catheter
is removed leaving the spiral in situ. The catheter used was a
No. 7 or 8 CharriGre, i.e., with an outer area of 10 or 13 mm2.
The chief operative risk appears to be the infliction of
small lesions in this region. This is also pointed out by
Bailey in the 1949 Yearbook of Neurosurgery in a review of
Norlh's ('49) report of two cases in which the spiral was
used for inoperable tumor causing obstruction. Instead, the
methods of Torkildsen ('47) or Stookey and Scarff ('36) are
recommended in these cases. Both of these are anastomotic
operations. I n the former free communication is established
between the posterior horn of one lateral ventricle and the
cisterna magna by means of a rubber tube through a subgaleal
tunnel. I n the latter, communication between the third ventricle and the subarachnoid space is established by two openings: one through the lamina terminalis, connecting the third
'This study mas made possible by a grant from the Research Fund at
Sodersjukhuuet, Stockholm.
151
152
G . FLYGER AND U. HJELMQUIST
ventricle with the cisterna chiasmatis, and one through the
floor of the ventricle directly into the cisterna interpeduncularis. From the anatolmical standpoint, however, Leksell's
method seems more attractive, since it follows the natural
anatomical arrangement. Moreover, it has the advantage of
permitting inspection of the fourth ventricle and the posterior
surface of the aqueduct.
Leksell's operative procedure provides the point of departure f o r the present study of the normal variations in the
cross-sectional areas of the aqueduct at different ages.
The standard textbooks of Anatomy described only the
topography and approximate length of the aqueduct and state
that the cross-sectional area of the aqueduct varies at different
levels (Rauber-Kopsch, Gray, Villiger and others). These
descriptions appear to be taken from Gerlach (1858). This
author, however, carried out his investigations mainly on
infant brains which were fixed in 1%potassium bichromate
f o r a period of 5 to 6 weeks. A not inconsiderable amount of
distortion is inevitable from hardening in bichrotmate. He
made serial sections along the whole aqueduct. Each third
section was traced under magnification, and he then found
that the lumen of the aqueduct was not uniform throughout
the extent of the aqueduct, but that it varied at different levels.
No measurements of the aqueduct are given, but he published
a number of drawings together with the scale.
Turkewitsch ( '35, '36) has published anatomical studies on
the internal structure of the aqueduct based on plastic reconstructions, but no figures are given to indicate the variations in caliber encountered. On the other hand, they give a
good idea of variations in the shape of the aqueduct at different
levels which, however, are a t variance with those of Gerlach.
I n the normal encephalogram, in which the ventricular
system is filled with air, the aqueduct is visualized as a curvilinear streak of air, the radius of which varies from case to
case (Lindgren and di Chiro, '53). It is not possible, however,
to detect any variations in contour which might serve as a
153
V B K I A T I O N S OF SYLVISN AQUEDUCT
basis for a n anatomical division. Turkewitsch ( ’36) divided
the aqueduct into five parts : Pars Anterior, Ampulla, P a r s
Media, Gcnu and P a r s Posterior (fig. 1).
Woollam and Millen ( ’ 5 3 ) coizsidcred this suhdivisiori
rather elaborate, and suggested a division into three parts :
Pars Anterior, Ampulla and Pars Posterior. They derive their.
points of division from the two natural constrictions of the
E’ig. 1 Normal appear:riice of the aqueduct of Rylvius as viewed
p h n e (reproduced from Turkewitsch, ’36).
ill
a sagittal
aqucductal luii1cii, one at the level of the rriiddle of the superior
colliculus and the other at the level of the intercollicular
sulcus.
Russel wrote in 1949: “As matters stand, therefore, \ye
do not Biiow either the normal range of variation in the caliber
of the aqueduct . . . .” Since then oiily two studies on tlie
dimensions of the aqueduct have becn published. Beckett,
Netsky and Zirrimei*rnan ( ’SO), whose study was based on 11
cases of steriosis of the aqueduct a i d 50 non-hyciroceplialic
cases, stated that the smallest cross-sectional area encountered
in the latter was 0.09 ern2. S o further details of this series are
154
0. PLYGEIL A N D U. HJELMQUlST
given. TVoollarri and lllillen ( ‘53) questioned the figure given
by Beckett et al., and on measurement of tlic lumen of the
appropriate aqueduct in their illustrations with tlie planimeter
found tlie area was 0.009 em2. Woollam arid Rlilleri’s results
were based on planimetric rneasureinent of the cross-sectional
a r e a in 14 normal human adult brains. The mean crosssectional area of the aqueduct i n their series ranged from
0.6 mm2 to 2 mm2. They stated that the shapc of the aqueducts
they examined approxiniated generally to the illustmtions
published by G erlach.
JIATERIAL
The present series consists of 2 1 brains removed from
individuals whose age at death ranged from 1 day to 75 years.
I n tlic majority of older persons - those over 50 years of
age -death was due to natural causes. Fourteen brains
mere from females and 10 from males. I n no case was the
cause of death related to disease of the central nervous system. Macroscopic sections of the brains revealed no abnorrnality a pa r t from moderate atrophy in the very oldest. Tlie
sex, age, arid roported cause of death are listed in table 1.
The irregular numhcring of the preparations is due to the
fact that after the comriiencement of the investigation a number of brains were rejected on the grounds that the causc of
death might have influenced the anatomical structure of the
brain.
MET HOD
The brains were removed at autopsy in thc usual rnariner
and fixed by suspension, by means of a string threaded under
the basilar artery, in a bath of 10% forcmalin for a period
of 2 to 4 weeks. Because of their softer consistency, tlie t,wo
infant brains required the longer period of hardening in order
to prevent distorting the enceplialon during removal. After
fixation the mesencephalic region was removed, passed successively through increasing concentrations of alcohol, and
The histcilogieal prcparations werc made by Mrs. Ulla Flyger, t o whoin n c
cxprcss our hcarty thanks.
155
VARIATIONS O F SYLVIAN AQUEDUCT
finally through methylbenzoate. Serial sections cut perpendicular to the long axis of the brain stem were made of the
entire mesencephalon. Two contiguous sections were cut at
intervals of 150 p, and one stained for cells and the other for
glia. I n preparations I to I11 the sections were cut 2 0 p in
thickness and in the remainder 7 p. It was found that sections
TABLE 3
Present series
PREPARATION
NO.
I
I1
I11
IV
VI
VIII
X
XI
XI1
XI11
xv
XVI
XVII
XVIII
XXI
XXII
XXIV
xxv
XXVII
XXIX
XXX
XL
XLI
XLII
AGE
76 yrs.
47
60
68
42
51
20
22
30
77
51
58
47
52
74
63
74
60
75
1 day
63 yrs.
69
62
1 day
SEX
F
F
M
F
F
M
F
F
F
F
M
F
M
M
M
F
F
M
M
F
M
?if
F
F
CAUSE O F DEATH
Chronic endocarditis
Barbiturate poisoning
Cancer of the tongue
Gastric carcinoma
Uterocervical carcinoma
Gastric ulcer (operated)
Cardiac defect
Chronic hepatitis
Chronic endocarditis
Syphilitic aortitis
Nephrosclerosis
Hypertonia
Gastric ulcer (operated]
Addison’s disease
Duodenal ulcer
pneumonia
Chronic endocarditis
Ovarian carcinoma
Hydronephrosis
Laryngopharyngeal carcinoma
Asphyxia
Cardiac arteriosclerosis
Cardiac infarction
Cholangitis
Asphyxia
+
cut at 20 ~1 were too thick for a study of the ependyma upon
which the present authors are engaged.
Ehrlich’s eosin was used for staining cells. All measurements are based on these sections. For the staining of glia
were used Haggqvist ’s modification of Alzheimer-Mann ’s
method in preparations I to X, and Ranke’s method in preparations XI to XIJII.
156
G. FLYGER AND U. HJELMQUIST
The only definition of the boundaries of the aqueduct available in the literature is that given by Woollam and Millen.
Like those of these workers, our sections begin first caudal
to the posterior commissure and continual to a point immediately caudal to the inferior colliculus.
It may justifiably be argued that the cross-sectional appearance of the aqueduct in our investigations does not correspond exactly with that encountered in vivo, since the
fixatives which we used might have caused shrinkage or other
distortion of the brains. Casts of the ventricles made with
the brain in situ might be expected to produce more satisfactory results. Such casts have been made by, among others,
Torkildsen ('33) using melted wax, and Woollam ('52) who
employed Neoprene, a plastic mass for the purpose. These
methods, however, are also subject to errors, since the amount
of pressure used in the injection can affect the final size of
parts distended by the injected material and thus produce
erroneous values. From a practical standpoint, therefore, it
seemed 'more valuable to fix the brains by a well-recognized
pathologic-anatomic technique.
The sections were magnified X 50 and the area of each
section of the lumen of the aqueduct was measured with a
planimeter. Each eosin-stained section was measured 3 to 5
times and the mean determined. The small number of measurements on each section did not warrant the calculation of the
mean error. The differences encountered, however, never
exceeded 5 units, and hence the figures are exceedingly exact.
According to Romeis ( '48) considerably more reliable values
are obtained by planimetric measurelment than, e.g., by excision and weighing. If correctly carried out, the exactitude
attained is between 1,400 and 1,600 of the area measured.
The statistical calculations of the variations in the crosssectional areas of the aqueduct are based on the formula:
ds2:-PF,
n-1
where n = the total values, M = the mean and
x = the variable.
The statistical tabulations were made by Mr. Torkel Westling.
157
VARIATIONS O F SYLVIAN AQUEDUCT
RESULTS
The cross-sectional areas of the aqueduct in the present
series are shown in table 2. All measurements are expressed
in square millimeters. The beginning and the end of the
aqueduct indicate the cross-sectional areas immediately caudal
TABLE 2
T h e cross-sectional area of the normal cerebral aqueduct ( i n mmz)
at various levels at different ages
PREP.
NO.
I
I1
I11
IV
VI
VIII
x
XI
XI1
XI11
XV
XVI
XVII
XVIII
XXI
XXII
XXIV
XXV
XXVII
XXIX
XXX
XL
XLI
XLII
BEGINNING
AGE
76 yrs.
47
60
68
42
51
20
22
30
77
51
58
47
52
74
63
74
60
75
1 day
63 yrs.
69
62
1 day
SEX
F
F
M
F
F
M
F
F
F
F
M
F
M
M
M
F
F
M
M
F
M
M
F
F
END
o~
n p U ~ ~ U c TAQUEDUCT
2.53
2.91
5.50
2.94
1.76
1.48
2.28
0.71
1.68
3.12
2.27
1.86
5.22
1.53
2.40
0.98
1.24
1.24
2.69
1.12
7.22
3.34
0.75
1.55
6.98
3.40
3.28
2.84
2.02
5.20
4.26
1.50
1.38
2.74
1.92
5.15
5.88
4.07
3.59
1.16
4.45
3.87
2.29
1.46
9.84
5.92
1.10
0.83
MAXIMUM
AREA
MINIMUM
AREA
DIFFERENCE
BETWEEN
MAX.AND
MIN.
6.98
3.40
3.50
2.94
2.02
5.20
4.68
2.29
1.38
3.12
2.37
5.19
5.88
4.07
3.59
1.25
4.86
3.87
3.25
1.46
9.84
7.06
2.09
1.76
1.70
1.08
2.60
1.78
1.15
1.18
2.12
0.71
0.69
1.49
1.26
0.95
2.07
0.71
1.62
0.40
0.44
1.21
1.74
0.84
7.22
2.67
0.52
0.54
5.28
1.32
2.90
1.16
0.87
4.02
2.56
2.58
0.69
1.63
1.11
4.24
3.81
3.36
1.97
. 0.85
4.22
2.66
1.51
0.62
2.62
4.59
1.57
1.22
to the posterior comrnissure and immediately caudal to the
inferior colliculus, respectively. I n the next two columns are
given the maximum and minimum areas encountered, and in
the last column the difference between the maximum and
minimum values.
158
G. FLYGER A N D U. HJELMQUIST
What. strikes one most is the wide range of variation in
area, from 0.4mm2 to 9.84mm2. It might be expected that
comparable levels from preparations of approximately the
same age would show some agreement, but such is not the
case. For example, in preparations I and XI11 the maximum
area of cross-section was 6.98 mm2 and 3,12 mm2, respectively,
and in preparations XXI and XXIV the difference between
the maximum and minimum areas was 1.97 mm2 and 4.22 mm2,
respectively. Neither does sex appear to play any part. Accordingly, as the table shows, the size of the aqueductal lumen
is highly individual.
I n 17 of the 24 preparations the lufmen of the aqueduct
was larger at the caudal end than at the cranial end, in 8 of
them as much as 2 mm2, a very high figure, when one considers
the minute size of the aqueductal lumen. In 8 preparations
the cranial and caudal lumina were approximately the same
size ; in none of these 8 cases did the difference exceed 0.4 mm2.
I n three preparations the lumen was more than 0.4 mm2 larger
at the cranial end than at the caudal end.
Table 3 shows the mean cross-sectional areas of the aqueduct and the standard deviation.
The minute size of the aqueductal lumen is remarkable,
and it is difficult to believe that this canal provides the sole
means of transit for the cerebrospinal fluid from the third
to the fourth ventricle. This has also been pointed out by
Woollam and Millen ('53) and Hassin ( '48). The possibility
of other means of exit must be taken into consideration.
DISCUSSION
As Broman ( '27), Bickers and Adams ( '49) and others
noted, an absolute as well as a relative decrease in the size of
the aqueductal lumen occurs progressively from the second
foetal nionth to the time of birth. This is attributed to the
influence of the nuclear masses and fiber tracts surrounding
the aqueduct. This explanation would lead one to expect a
progressive decrease in the aqueductal lumen up to time of
159
VARIATIONS O F SYLVIAN AQUEDUCT
onset of those degenerative changes which usually accompany
aging and result in atrophy of adjacent parts of the brain.
The normal variations with increase in age are not known
with certainty. Spiller ('16) introduced the hypothesis that
the aqueductal lumen decreased with age much like the central
canal of the spinal cord. To test this theory, the material
was grouped according to age (table 4).
TABLE 3
Mean cross-sectional area of the aqueduct ( i n mmZ) b t different
levels and standard deviation
MEAN
STANDARD
DEVIATION
Beginning of aqueduct
2.4
& 1.6
End of aqueduct
3.5
2 2.2
Maximum area
3.9
2 2.1
Minimum area
1.5
zk 1.4
Difference between
maximum and minimum
2.4
r+ 1.4
~
TABLE 4
Mean cross-sectional area of the aqueduct [in mmz) in different age groups
AGE GROUP
BEGINNING
OF
AOUXDUCT
END O F
AQUEDUCT
MAXIMUM
AREA
MINIMUM
AREA
0-30
31 - 50
50
1.6
3.3
2.6
1.9
3.7
4.0
2.3
3.7
4.1
1.0
1.4
1.7
The table shows the mean cross-sectional areas of the
aqueduct in each age group. Except at the cranial end of the
aqueduct, there is a definite although not, perhaps, a statistically significant increase in area with increase in age.
Whether this is due to general old age atrophy or to a reduction in the size of the surrounding nuclear masses and fiber
tracts has not been studied in this investigation.
It may seem peculiar that the size of the aqueductal lumen
does not, like the central canal, diminish with age. The chief
160
G. FLYGER AND U. HJELMQUIST
reason is doubtless the cerebrospinal fluid pressure, which
does not permit any shrinkage.
Now, how do our results compare with those of others?
As f a r as we are aware, the only similar investigations are
those of Beckett and co-workers ( '50) and Woollam and Millen
( '53). Our technique was almost identical with theirs. Beckett
and his co-workers, however, reported only the smallest crosssectional area they encountered in their non-hydrocephalic
series, 0.9 mmZ (corrected by Woollam and Millen), which is
at variance with that encountered in this investigation 0.4mm2. It is impossible to be sure that the difference between Becliett's findings and ours are as they appear, since
his paper does not describe the exact method of fixation used
or the details of the technique employed in measuring the
cross-sectional areas. I n this procedure, the slightest deviation in the transverse plane from the perpendicular to the
long axis of the brain stem is sufficient to produce an appreciable difference from the true value.
A comparison of our results with those of Woollam and
Millcn must be limited to only the cross-sectional area of the
aqueduchl lumen at the cranial and caudal ends and the maximum and minimum area of cross-section. All our values are
considerably higher (see table 3 ) . I n their series the mean
area of cross-section at the crainal end was 1.7mm2, and at
the caudal end 2.5mm2. What this diffcrence is due to is
difficult to say. As stated earlier, differences in the crosssection technique are a factor to be taken into consideration.
Another not unessential difference lies in the fact that Woollam and Millen employed 5% formalin t o fix the brains while
we used 10%. The latter concentration is stated by Hansen
('07) to be that which produces a minimum of distortion.
There rema.ins, however, the fact that the size of the aqueductal lumen is so minute that one is justified in questioning
whether this canal is actually the sole outlet f o r the cerebrospinal fluid. Sjoqvist ( '36) estimated that cerebrospinal fluid
is formed at the rate of about 500cm3 per day.
VARIATIONS O F SYLVIAN AQUEDUCT
161
A further object of this investigation has been, on the basis
of the normal variations in the size of the aqueductal lumen,
to try to decide what attitude should be adopted towards
Leksell’s operative method for the relief of noncolmmunicating
hydrocephalus. Our results would seem t o indicate that
catheterization of an aqueduct which normally has such a
small lumen cannot be performed without considerable
risk. Furtherlmore, the aqueduct is not a straight tube, but
bow-shaped, and surrounded by very soft tissues which may
easily be damaged by the passage of a catheter. It is to be
noted that the operation comes into question only in cases
of stenosis of the aqueduct where, accordingly, the lumen is
smaller than normal. From the anatomical standpoint, therefore, this operative procedure seems to us to be extremely
dangerous. No extensive postoperakive follow-up study has
been published, but we hope to be able to do so at a future date.
SUMMARY
The normal variations in the size of the lumen of the cerebral aqueduct have been studied by means of sections in a
series of 24 normal human brains. The cross-sectional areas
of the aqueduct were measured with the planimeter.
Variations in area ranged from 0.40 mm2 to 9.84 mm2. The
large individual variations are pointed out.
The advisability of catheterization in cases of noncommucating hydrocephalus is discussed.
LITERATURE CITED
BAILEY, P. 1949 I n : Yearbook of Pieurosurgery: 454-455. The Year-Book
Publishers, Inc., Chicago, Ill.
BECITETT,R., M. NETSKP AND H. M. ZIMNERNAN 1950 Developmental stenosis
of the aqueduct of Sylvius. Am. J. Path., 26: 755-787.
BICKERS,
D., AND R. ADANS 1949 Hereditary stenosis of the aqueduct of Sylvius.
J. Neuropath. Exp. Neuro., 8 ; 104-105.
1949 Hereditary stenosis of the aqueduct of SyIvius as a cause of
congenital hydrocephalus. Brain, 78 ; 246-262.
BROMAN,
I. 1927 Manniskans utveckling fore fodelsen. C. W. K. Gleerups
forlag, Lund.
GERLACH,J. 1858 Mikroskopische Studien aus dem Gebiete der menschlischen
Morphologie. Verlag von Ferd. Enke, Leipzig.
162
GRAY,H.
G . FLYGER AND U. HJELMQUIST
1954 Textbook of Anatomy (ed. 3 1 ) : 988. Longmans, Green Company, London.
HANSEN,F. C. C. 1907 Om efterfixering af formolpreparater. Saertryk ur
Hospitalstidende, 21. 3-10. Kobenhavn.
HASSIN,Q. B. 1948 Cerebrospinal fluid ( i t s origin, nature and iorrnation). J.
Neuropath. Exp. Neurol., 7 : 172-187.
HAGGQVIS’P, G. 1936 Analyse der Faserverteilung i n eineni Riickenmarkquerschnitt (Th. 3 ) . Ztschr. f. mikr. anat. Forsch., 39: 1-34.
LEKSELL,
L. 1949 A surgical procedure f o r atresia of the aqueduct of Sylvius.
Acta Psych. e t Neur., 2 4 : 559-568.
LINDGREN,E., A N D G. DI CHIRO 1953 The roentgenologic appearance of the
aqueduct of Sylvius. Acta Radiologica, X X I X : 117-125.
N O R L ~ NG.
, 1949 Surgical treatment of iiioperablc tumors causing obstruction of Sylvius aqueduct. Yearbook of Neurosurgery: 454-456.
RAUBER-KOPSCH
1955 Lehrbuch uiid Atlas der Anatomie des Menschen (ed.
1 9 ) , I I : 342-343. Verlag von Georg Thieme, Leipzig.
ROMEIS,I). 1948 Mikroskopische Technik (ed. 15). Leibnitz Verlag, Miinchen.
RUSSEL, D. 1949 Observations on the pathology of hydrocephalus. Medical
Research Council, no. 265.
SJOQVIST,
0. 1937 Beobachtungen iiber die Liqvorsekrption beim Menschen.
Zbl. Neurochir., 1: 8-18.
SPILLER,
W. G. 1916 Syringomyelia. Syringoencephalomyelia. J. Nerv. Ment.
Dis., 4 4 : 395-414.
STOOKEY,
B., AND J. E. S C A R F F 1936 Occhsion of aqueduct of sylvius by
neoplastic and nou-neoplastic processes with rational surgical treatment f o r relief of resulting obstructive hydrocephalus, €3~11.Neuro.
Iiist. h’ew Pork, 5 : 348-377.
TURKETYITSCH,
N. 1935 Die Entwicklung des Aqueductus cerebri bei Menschen.
Morph. Jahrhuch, 76: 421-477.
- 1936 La constitution anatomique d e I’aqucductus cerebri cle
l’honime. Arch. Anat. Strasbourg, 21 : 323-358.
TORXILDSE:N,
A. 1933 Cit. from Woollam.
- 1947 Ventriculoristernostomy. A palliative operation i n different
types of non-communicating hydrocephalus. Johan Grundt Tanuni
Forlag, Oslo.
VILLIGER,E. 1922 Gehirn und Ruckenmark. Verlag von Wilhelm Engelmann,
Leipzig.
WOOLLAM,
D. 1952 Casts of the ventricles of the brain. Brain, 7 5 : 259-267.
WOOLLAM,
D., AND J. MILLEN 1953 Anatomical considerations i n the pathology
of the stenosis of the cerebral aqueduct. Brain, 7’6: 104-112.
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