Experimental cerebral vasospasm. Part 2. Contractility of spastic arterial wall.
S Nagasawa, H Handa, Y Naruo, H Watanabe, K Moritake and K Hayashi
Stroke. 1983;14:579-584
doi: 10.1161/01.STR.14.4.579
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579
REGIONAL CBF IN HYPERTENSIVE RATS/Sadoshima & Heistad
10.
11.
12.
13.
14.
15.
16.
UG, Vorstrup S, Hemmingsen R, Bolwig TG: Cerebral blood flow
in rats with renal and spontaneous hypertension: Resetting of the
lower limit of autoregulation. J Cereb Blood Flow and Metabol 2:
347-353, 1982
Mueller SM, Heistad DD, Marcus ML: Total and regional cerebral
blood flow during hypotension, hypertension, and hypocapnia:
Effect of sympathetic denervation in dogs. Circ Res 41: 350-356,
1977
Sadoshima S, Thames M, Heistad D: Cerebral blood flow during
elevation of intracranial pressure: role of sympathetic nerves. Am J
Physiol 241: H78-H84, 1981
Edvinsson L, Owman C: Sympathetic innervation and adrenergic
receptors in intraparenchymal cerebral arterioles of baboon. Acta
Neurol Scand 56: 304-305, 1977
Tsuchiya M, Walsh GM, Frohlich ED: Systemic hemodynamic
effects of microspheres in conscious rats. Am J Physiol 2: H617H621, 1977
Buckberg GD, Luck JC, Payne DB, Hoffman JIE, Archie JP,
Fixler DE: Some sources of error in measuring regional blood flow
with radioactive microspheres. J App Physiol 31: 598-604, 1971
Steel RGD, Torrie JH: Principles and procedures of statistics. New
York, McGraw-Hill, pp 107-109, 1960
Heistad DD, Marcus ML: Evidence that neural mechanisms do not
have important effects on cerebral blood flow. Circ Res 42: 295302, 1978
17. Baumbach G, Heistad D: Cerebral microvascular pressure during
sympathetic stimulation. Fed Proc 41: 1610, 1982 (abstract)
18. Bill A, Linder J: Sympathetic control of cerebral blood flow in
acute arterial hypertension. Acta Physiol Scand 96: 114-121, 1976
19. Edvinsson L, Owman C, Siesjo B: Physiological role of cerebrovascular sympathetic nerves in the autoregulation of cerebral blood
flow. Brain Res 117: 519-523, 1976
20. Heistad DD, Marcus ML: Effect of sympathetic stimulation during
acute hypertension in cats. Circ Res 45: 331-338, 1979
21. MacKenzie ET, McGeorge AP, Graham DI, Fitch W, Edvinsson
L, Harper AM: Effects of increasing arterial pressure on cerebral
blood flow in the baboon: Influence of the sympathetic nervous
system. Pflugers Arch 378: 189-195, 1979
22. Fitch W, MacKenzie ET, Harper AM: Effects of decreasing arterial
blood pressure on cerebral blood flow in the baboon. Circ Res 37:
550-557, 1975
23. Marcus ML, Heistad DD: Effects of sympathetic nerves on cerebral
blood flow in awake dogs. Am J Physiol 238: H549-H553, 1979
24. Heistad DD, Gross PM, Busija DW, Marcus ML: Cerebral vascular response to loading and unloading of arterial baroreceptors. In
Arterial Baroreceptors and Hypertension (P. Sleight ed), New
York, Oxford Press, pp 210-217, 1980
25. Savaki HE, Macpherson H, McCulloch J: Alterations in local cerebral glucose utilization during hemorrhagic hypotension in the rat.
Circ Res 50: 633-644, 1982
Experimental Cerebral Vasospasm. Part 2.
Contractility of Spastic Arterial Wall
SHIRO NAGASAWA, M.D.,
HAJIME HANDA, M.D.,
YOSHITO NARUO,
M.D.,
HlDETOSHI WATANABE, M . D . , KOUZO MORITAKE, M . D . , AND KoZABURO HAYASHI, P H . D .
SUMMARY We studied the mechanical properties of canine basilar arteries subjected to experimental
subarachnoid hemorrhage (SAH). Smooth muscle contractility was determined from pressure-diameter
curves obtained after subjecting the basilar arteries to three different conditions: Krebs-Ringer solution
(KRS), Krebs-Ringer solution containing serotonin (5HT), and saline solution.
Pressure-diameter curves obtained in KRS and 5HT are biphasic and have sharp flexions that yield
flexion points. The pressure level at theflexionpoint increases as vasospasm increases. Strong constriction is
retained up to that pressure above which the constriction is released abruptly. These data suggest that
increasing the intraluminal pressure dilates the spastic artery nonlinearly and that induced hypertension
could relieve the cerebral ischemia caused by vasospasm if blood pressure were maintained above the flexion
point. The contractile response of spastic arterial wall to serotonin remains unchanged after SAH although
the spastic constriction increases progressively and becomes maximal seven days after SAH. The lesser the
arterial wall stiffness, the more efficiently it constricts. This means that the diminution of arterial stiffness
observed after SAH might be one of the factors promoting the development of vasospasm.
Stroke, Vol 14, No 4, 1983
ALTHOUGH THE PHENOMENON of cerebral vasospasm following the rupture of an aneurysm is well
recognized and has been described in many publications, there have been few studies on the mechanical
properties of arterial walls subjected to subarachnoid
hemorrhage (SAH). There is a controversy as to
From the Department of Neurosurgery, Kyoto University Medical
School, 54-Kawahara-cho, Sakyo-ku, Kyoto 606, Japan. *National
Cardiovascular Center Research Institute, 5-125 Fujishirodai, Suita,
Osaka 565, Japan.
Address correspondence to: Prof. Hajime Handa, Department of
Neurosurgery, Kyoto University Medical School, 54-Kawahara-cho,
Sakyo-ku, Kyoto 606, Japan.
Received July 12, 1982; revision accepted February 10, 1983.
whether the contractile response of a spastic arterial
wall to vasoconstrictors increases as compared to a
normal wall. 1,2 While it has been demonstrated in the
intracranial and extracranial arteries that the change in
connective tissue contents (collagen and elastin) produced in the processes of aging and systemic hypertension alters the contractility of walls, 3,4 there is little
information on the correlation that may exist between
the connective tissue contents and the contractility of
arterial walls subjected to SAH.
In a previous paper, we demonstrated that the vasospasm is attributable to the constriction of vascular
smooth muscle and hence is reversible, and that the
passive mechanical properties of vascular walls observed under the relaxed condition of the smooth mus-
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580
STROKE
cle correlate well with the ratio of collagen to elastin
contents.5
In this study, isobaric constriction and isometric
contraction induced by serotonin were measured in
canine basilar arteries subjected to experimental SAH
in order to determine the contractility of the spastic
cerebral vessel and the effects that the passive elastic
properties of the wall may have on cerebrovascular
contractility.
Materials and Methods
Experimental Procedures
A total of 35 adult mongrel dogs, weighing from 8 to
12 kg, were used in this study, and were divided into 6
groups: control group (10 dogs) with no treatment and
treated groups (25 dogs) in which 3 ml of autogenous
fresh arterial blood was injected into the cisterna magna with an exchange of the same amount of cerebrospinal fluid. After a certain period of time following the
blood injection, a clivectomy was performed under
anesthesia with sodium pentobarbital (25 mg/kg, i.v.)
to obtain segments of the basilar artery with the
branches ligated and severed. The treated dogs were
divided into five groups according to the periods of
time elapsed after the treatment: 2, 4, 7, 14 and 28
days. Each treated group was designated as 2-day, 4day, 7-day, 14-day and 28-day groups, respectively.
Each arterial segment was mounted horizontally at
its in vivo axial length in a tissue bath which contained
Krebs-Ringer solution (KRS) kept at 37°C and oxygenated with 95% 02-5% C0 2 . The segment was inflated with the solution from a reservoir under air pressure using the testing apparatus reported elsewhere.5'6
Intraluminal pressure and external diameter were
measured respectively, by a strain gauge manometer
and a specially designed displacement transducer.7
After incubating the segment in the KRS for 30
minutes at an intraluminal pressure of 100 mmHg, a
pressure-diameter curve was recorded during inflation
of the arterial segment from 0 mmHg to 250 mmHg.
This relation was considered to represent the active
elastic properties of the arterial wall in KRS. After the
intraluminal pressure was returned to 100 mmHg, serotonin (5HT) was added to the solution in a concentration of 10 ~5 M. When the peak contraction had been
reached, a second pressure-diameter curve was recorded from 0 mmHg to 250 mmHg and was assumed to
represent the active elastic properties of the segment in
5HT. After the intraluminal pressure was returned
again to 100 mmHg, the bath was drained and rinsed
with a saline solution and then incubated in the solution for at least 30 minutes. The pressure-diameter
curve obtained in this solution by the same procedures
as carried out previously represents the passive elastic
properties of the arterial segment. Our preliminary
study showed that at this concentration of serotonin the
maximum contraction can be obtained both in the control and the spastic basilar arteries. No difference was
observed between the curves obtained in the pure saline solution and in the saline solution mixed with a
metabolic inhibitor, which indicates that a blood vessel
VOL
14, No 4, 1983
has little smooth muscle tone in the pure saline solution. After these mechanical experiments, the segment
was removed from the bath, lightly blotted on filter
paper, and then weighed.
Data Analysis
For the evaluation of the mechanical properties of
blood vessels from their pressure-diameter curves, we
calculated tangential wall stress, a, and tangential
mid-wall strain, sm,6,8-9 to normalize the force-displacement relations of walls with different cross-sectional areas under different conditions of smooth muscle tone (fig. 1). These parameters are defined by the
following equations:
a = PiR/(R0 - R(),
(1)
and
8m = [(R0 + R ^ M O ; + r,)/2] - 1,
(2)
where P; is the intraluminal pressure, R0 the external
wall radius, Rj the internal wall radius, r0 and r{ the
external and internal radii at 0 mmHg under the passive
condition of smooth muscle, respectively. The internal
wall radius was calculated from the external wall radius, in vivo axial strain, and volume of the segment
assuming the wall density to be 1.06 g/cm3.10
Diameter response,3~5 (ADm/Dm)KRS and (ADm/
Dm)5HT, were calculated to express the isobaric constrictions of a blood vessel under the active conditions
in KRS and 5HT at a given pressure level, respectively, and were defined as:
Diameter Response ^Dm/Drr
(Dm)ss
WT
(Dm)ss
(Dm)5HT (Dm)l<RS (Dm)ss
Mid-V\fall Diameter Dm
Active Stress Ao
/
/
6
W^HT
^rt
P
•fc ORo
KRS
/
7
7*
•
ACT-
KRS = ° ' K R S - 0 &
/ /1
'5HT
/
°)ntm
/
Mid-Wall Strain
Sm
FIGURE 1. Schematic representation of the methods utilized
to evaluate the contractility of control and treated arteries from
their pressure-diameter curves. Pressure-mid-wall diameter
(Pi-Dm) and stress-mid-wall strain (c-sm) curves of a basilar
artery from the 7-day group depicted under different conditions
of smooth muscle in saline solution (SS), Krebs-Ringer solution
(KRS) and Krebs-Ringer solution containing serotonin (5HT)
are represented by solid, broken and dotted lines, respectively.
Diameter response, ADm/Dm, stands for isobaric constriction
at a given pressure and active stress, Acs, for isometric contraction at a given strain.
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CEREBRAL VASOSPASM/SPASTIC ARTERIAL WALL/Nagasawa et al.
581
(ADm/Dm)^ = [(Dm)ss - (Dm)KRS]/(Dm)ss, (3)
and
i i
(ADm/Dm)5
[(Dm)s
(Dm)5HT]/(Dm)ss. (4)
(Dm)KRS, (Dm)5HT and (Dm)ss are the mid-wall diameters under the active conditions in KRS and 5HT, and
under the passive condition in the saline solution, respectively. Active stress,3-5 ArjKRS and ACT5HT, were calculated to express the isometric contractions of a blood
vessel at a given strain level and were defined as:
A(7„
— — 5HT
•
• KRS
(5)
and
(6)
where G , ^ , a,5HT and a ss are the wall stresses developed
at a given strain under three different conditions. The
details of the experimental procedures and data analysis employed in this study have been described previously.5, 6-8
Arj 5HT =
-
Control
CTC
Results
Pressure-diameter Curve and Flexion Point
Examples of pressure-diameter curves of a basilar
artery are shown in figure 2. The solid curve of each
group obtained in the saline solution is convex toward
the diameter axis, indicating that the arterial wall becomes stiffer with elevation of pressure when the
smooth muscle is relaxed. The activation of smooth
muscle caused constriction and made the pressure-diameter curves shift toward the pressure axis. The
curves of 4-day and 7-day groups obtained in KRS are
biphasic and have sharp flexions at intraluminal pressures of 40 and 20 mmHg, respectively. The wall is
fairly stiff below theflexionpoint and becomes distensible after the intraluminal pressure exceeds the flexion
point. The curve of each group observed in 5HT has a
flexion point at higher intraluminal pressure than that
in KRS, below which pressure the wall manifests very
little distension with the increase in pressure.
2
4
7
14
28
Days after Treatment
FIGURE 3. Change in the pressure at flexion point, expressed
as mean ± SE.
The pressure levels at which the flexion points appear in KRS and 5HT are summarized infigure3. This
pressure observed in 5HT increases with time, reaches
the maximum value of 220 mmHg on the 7th day after
treatment, and then falls to around the control value on
the 14th and 28th days. In the case of KRS, flexion
points appear just in the 4-day and 7-day groups and
their pressure levels are much lower than in the case of
5HT.
Diameter Response and Active Stress
Figure 4 summarizes the relations between the diameter response caused by 5HT and intraluminal pressure in the control and treated groups. Pressure
dependence of the diameter response observed in the
control, 2-day, 14-day and 28-day groups is somewhat
different from that in the 4-day and 7-day groups. The
diameter responses in the former 4 groups are maximal
below 100 mmHg and decrease monotonously with the
QQ4
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Control
2-day
4 -day
7-day
u 14-day
0 28-day
IQI
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b
1.5
1.0
1.5
External Diameter H(mm)
0
100
200 240
Intraluminal Pressure Pi (mmHg)
FIGURE 4. Pressure dependence of diameter response caused
FIGURE 2. Examples ofpressure-diameter curves of a basilar
artery obtained from control and treated groups. Arrows indiby serotonin, expressed as mean ± SE at every 20 mmHg. Each
cate flexion points.
arrow indicates the pressure at flexion point.
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582
STROKE
0.4r
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VOL 14, No 4, 1983
04
"""CaDm/DnOSHT
i——o—i
4
7
14
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Days after Treatment
FIGURE 5. Change in the diameter response at 100 mmHg
obtained in Krebs-Ringer solution (KRS) and Krebs-Ringer solution containing serotonin (5HT), expressed as mean ± SE.
pressure elevation. The 4-day and 7-day arteries, on
the other hand, retain their strong constriction up to a
pressure level of approximately 200 mmHg, since they
have their flexion points in such high pressure range.
After exceeding these points, their diameter responses
decrease rather rapidly.
Figure 5 shows the changes in diameter response at
100 mmHg developed by KRS and 5HT. Each diameter response first increases with time and reaches a
maximum value on the 7th day and then decreases
rapidly, recovering to the control value on the 28th day
after the treatment. The changes in the diameter response with time are rather paralleled to each other.
Figure 6 exhibits the maximum active stress induced
by 5HT and the active stress by KRS at the same strain
as the former is developed. These two stresses change
with time in a manner similar to the diameter response,
being maximum in the 7-day group and returning to the
control values in the 14-day and/or 28-day groups.
The maximum active stresses developed by 5HT are
plotted against maximum diameter responses in figure
7. The 7-day artery has the highest maximum active
stress and maximum diameter response. Although
there is no significant difference in the maximum ac-
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em=Q25 £^0.25
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em=Q20
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a
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0.1
Control
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Maximum Active Stress A O ^ T flcfdynes/cm2)
FIGURE 7. Maximum diameter response versus maximum active stress developed by serotonin, expressed as mean ± SE.
tive stresses in the control, 2-day, 14-day and 28-day
groups, the 2-day artery yields a significantly greater
maximum diameter response than those in the other 3
groups.
Discussion
Kuwayama et al." and White et al. 12 have reported
successful production of the cerebral vasospasm in the
dog by the same method used in this study. Pressurediameter curves obtained in the KRS, 5HT and saline
solution were considered to represent the elastic properties of an arterial wall under three different conditions of smooth muscle contraction, that is, under the
vasospastic, maximally contracted, and fully relaxed
conditions. Although vasospasm was detected in KRS
in the present in vitro experiment, the diameter response observed, i.e. isobaric constriction, was smaller than that measured angiographically by Kuwayama.
The reason for this difference has been discussed previously. 5
Significant increases in the diameter response and
active stress developed by 5HT were observed 7 days
after experimental SAH (fig. 5 and 6). To evaluate the
contractility of treated arterial walls, the differences in
the active stress as well as in the diameter response
between two conditions in the KRS and 5HT are plotted against the period after the treatment in figure 8.
No significant change with time can be detected in
these two values. These results imply that the contractile response of spastic arterial walls to serotonin remains unchanged after SAH although the contractile
capacity of the wall itself increases with the advance of
cerebral vasospasm shown in figures 5 and 6. Toda et
al.' and Lobato et al. 2 have measured isometric tension
to investigate the contractility of spastic arterial walls.
Toda demonstrated the decreased contractility of walls
and attributed the result to their impaired metabolism,
while Lobato documented the increased contractility
and ascribed the hypersensitivity of walls to vasoconstrictors. In those studies they did not consider the
contraction retained in the spastic arterial wall before
FIGURE 6. Change in the maximum active stress induced by
serotonin and active stress produced in Krebs-Ringer solution
(KRS) at the same strain as the former is developed, shown with
the strain and expressed as mean ± SE.
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CEREBRAL VASOSPASM/SPASTIC ARTERIAL WALL/Nagasawa et al.
1= 20 r
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OAO
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g Q3r
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3°
Pi= 100 mmHg
C
2
4
7
14
28
Days after Treatment
FIGURE 8. Differences in active stress, Aa, as well as in diameter response, M)mlDm, between two conditions in KrebsRinger solution (KRS) and Krebs-Ringer solution containing
serotonin (5HT).
the administration of vasoconstrictors, and this limits
the significance of their findings.
Under active smooth muscle condition in KRS or
5HT, pressure-diameter curves have flexion points,
and shift toward the pressure axis compared with those
obtained under passive smooth muscle condition in
saline solution (figs. 2 and 3). The strong vasoconstriction, accompanied by little change in the vascular diameter with pressure elevation, is retained up to the
pressure level at the flexion point, above which the
constriction is released abruptly (fig. 4). Although
there have been many studies on the mechanical properties of arterial walls, the existence of flexion point
over the intraluminal pressure of 100 mmHg is documented only in canine saphenous and rabbit ear arteries13-15 as well as human vertebral artery subjected to
SAH.8 To explain the mode and mechanism of vasospasm from biomechanical viewpoints, we attach great
importance to the flexion point, and explained its appearance by a possible mechanical interaction between
connective tissue and contracted smooth muscle.8
Under physiological conditions it is generally accepted that arterioles reduce their lumen caliber and
hence increase the peripheral resistance greatly with an
increase in intraluminal pressure, while the larger
arteries are hardly or only slightly contracted by that
stimulus.1617 With cerebral vasospasm, it has been
suggested that it is the spastic main trunk of the cere-
583
bral artery that determines the regional cerebral blood
flow. An increase in blood pressure not only accelerates the flow velocity through the constricted vessel18
but also expands it and hence improves the ischemic
deficit both in humans1920 and experimental animals.21, 22 The results obtained in this study imply that
increasing the intraluminal pressure dilates a spastic
artery nonlinearly (fig. 2), and that induced hypertension could improve the cerebral ischemia of vasospasm
if the blood pressure were maintained above the flexion point.
Both isobaric constriction (diameter response) and
isometric contraction (active stress) caused by serotonin were measured in this study. Figure 7 shows that
there is not a good correlation between the maximum
values of these two parameters. Similar results have
been observed in aged and hypertensive rats by Cox,
who ascribed them to changes in the passive elastic
properties of walls which are eventually determined by
the quality and/or quantity of connective tissues.3,4 We
measured the incremental elastic modulus of the canine basilar arteries subjected to experimental SAH
under the fully relaxed condition of smooth muscle in
saline solution to evaluate the passive elastic properties
inherent to their wall materials.5 The passive elastic
cC30
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7-day
14-day
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Q
O
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8
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c
. •
•
-
-
.
i
.
. . .
i
. . . .
i
5
10
15
20
Incremental Bast jc Modulus Einc
(^dynes/cm2)
FIGURE 9. Ratio of maximum diameter response to maximum
active stress versus incremental elastic modulus, Einc, at 100
mmHg obtained under the relaxed condition of smooth muscle.
Downloaded from http://stroke.ahajournals.org/ by guest on April 24, 2014
584
STROKE
properties are changed greatly by SAH and the treated
arterial walls have significantly lower moduli than the
control ones, having a minimum value in the 2-day
group. The elastic modulus correlated well with the
ratio of collagen to elastin contents through the posttreated period. The ratios of maximum diameter responses to maximum active stresses were calculated to
express the efficacy of constriction of arterial walls
since diameter change is a primary consideration with
respect to vasospasm. They were plotted against the
incremental elastic moduli to establish the effects of
passive elastic properties on the contractility of walls
subjected to SAH (fig. 9). A rather good correlation
was obtained between these two parameters, indicating that the lesser the stiffness of arterial wall, the more
efficiently it constricts. These results indicate that the
decreased stiffness of arterial wall subjected to SAH
might be one of the factors promoting vasospasm.
References
1. Toda N, Ozaki T, Ohta T: Cerebrovascular sensitivity to vasoconstricting agents induced by subarachnoid hemorrhage and vasospasm in dogs. J Neurosurg 46: 296-303, 1977
2. Lobato RD, Marin J, Salaices M, et al: Cerebrovascular reactivity
to noradrenaline and serotonin following experimental subarachnoid hemorrhage. J Neurosurg 53: 480-485, 1980
3. Cox RH: Effects of age on the mechanical properties of rat carotid
artery. Am J Physiol 233: H256-H263, 1977
4. Cox RH: Comparison of arterial wall mechanics in normotensive
and spontaneously hypertensive rats. Am J Physiol 237: H159H167, 1979
5. Nagasawa S, Handa H, Naruo Y, et al: Experimental cerebral
vasospasm. Arterial wall mechanics and connective tissue composition. Stroke 13: 595-600, 1982
6. Hayashi K, Handa H, Nagasawa S, et al: Stiffness and elastic
behavior of human intracranial and extracranial arteries. J Biomechanics 13: 175-184, 1980
VOL
14, No 4, 1983
7. Nagasawa S, Okumura A, Naruo Y, et al: Displacement transducer
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397-460, 1978
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158-163, 1979
13. Cox RH: Differences in mechanics of arterial smooth muscle from
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18. Price TR, Nelson E: Cerebrovascular diseases. Eleventh Princeton
Conference, Raven Press, 269-338, 1979
19. DeAraujo LC, Zappulla RA, Yang WC, et al: Angiographic
changes to induced hypertension in cerebral vasospasm. J Neurosurg 49: 312-315, 1978
20. Shibata K, Miyake S, Tanikawa M, et al: Effects of dopamineinduced hypertension on cerebral vasospasm. Neurol Med Chir 20
(Suppl): 31-32, 1980
21. Boisvert DP, Overton TR, Weir B, et al: Cerebral arterial responses to induced hypertension following subarachnoid hemorrhage in the monkey. J Neurosurg 49: 75-83, 1978
22. Ritchie WL, Weir B, Overton TR: Experimental subarachnoid
hemorrhage in the cynomolgus monkey. Neurosurg 6:57-62, 1980
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