(Stroke. 2001;32:629.)
© 2001 American Heart Association, Inc.
Original Contribution |
Hemodynamic Consequences of Cerebral Vasospasm on Perforating Arteries
A Phantom Model Study
From the Department of Neurosurgery (J.F.S.), Rambam (Maimonides) Medical Center, Faculty of Medicine, The Technion–Israel Institute of Technology, Haifa, Israel; and Research Laboratory (E.L., R.B., S.L., D.M.), Biosonix Ltd, Kfar Malal, Israel.
Correspondence to Jean F. Soustiel, MD, Department of Neurosurgery, Rambam Medical Center, PO Box 9602, Haifa 31096, Israel. E-mail j_soustiel{at}rambam.health.gov.il
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Abstract |
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Background and Purpose—Hemodynamics of cerebral vasospasm after subarachnoid hemorrhage remain unclear, and the discrepancy between ultrasonographic or angiographic evidence of arterial narrowing and neurological ischemic deficit is still debated. Most blood flow studies have been involved with large arteries, and thus, very little is known regarding the hemodynamic behavior of small perforating vessels. Patients with symptomatic vasospasm, however, often present with neurological signs suggesting involvement of deep-sited areas of the brain supplied by perforating arteries.
Methods—A pulsatile pump was set to provide an outflow of 350 mL/min through a 10-mm-diameter C-flex tube at a perfusion pressure of 130/80 mm Hg. The perfusion fluid used was prepared to approximate blood viscosity. Perforating arteries were simulated by a 1-mm tube connected to the parent tube at a 90° angle. Cylindrical stenotic devices of decreasing diameters were then introduced into the parent tube at the level of the aperture of the secondary tube and 1.5 diameters upstream of it. Velocity profiles both proximal and distal to the stenosis in the parent tube were obtained with a newly developed ultrasonographic flowmeter that allows for high spatial resolution.
Results—Increasing stenosis resulted in decreased outflow in the main tube, although it was significant only with severe stenosis. Whenever the simulated stenosis was placed upstream of the secondary tube, flow reduction was associated with a progressive change in the velocity profile, which gradually changed from laminar conditions to a jet stream limited to the center of the lumen. Further diameter reduction was responsible for the occurrence of flow separation with retrograde flow velocities in the periphery of the lumen. In the secondary tube, flow reduction was much more pronounced and began at a lesser degree of stenosis. Increasing fluid viscosity and decreasing perfusion pressure enhanced flow separation and prominently affected the outflow in the secondary tube. Conversely, whenever the simulated stenosis involved the branching area of the secondary tube, there was a slightly progressive decrease in the relative flow in the main tube as the stenosis became tighter. When the stenosis equaled the diameter of the secondary tube, the relative contribution of the secondary tube increased markedly at the expense of the main tube outflow.
Conclusions—The present results show that local cerebral vasospasm induces changes in postvasospastic velocity profile affecting the shear rate and may eventually lead to flow separation. This phenomenon may, in turn, result in a venturi-like effect over the aperture of perforating arteries branching out of the postvasospastic portion of the affected parent artery. These alterations of cerebral hemodynamics may account for at least part of the vasospasm symptomatology, especially in the vertebrobasilar system, where vasospasm is commonly focal rather than diffuse. Furthermore, these changes proved to be affected significantly by manipulations of pressure and viscosity, supporting the use of hyperdynamic therapy in the management of cerebral vasospasm.
Key Words: blood flow velocity • cerebral blood flow • cerebral vasospasm • ultrasonography
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Introduction |
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Cerebral vasospasm has emerged as one of the most serious threats after subarachnoid hemorrhage (SAH). The introduction of the transcranial Doppler (TCD) by Aaslid et al1 has transfigured the diagnostic capabilities of neurosurgeons and enabled a broader investigation of this phenomenon. Consequently, numerous studies based on TCD have shown that the actual incidence of vasospasm is higher than previously thought,2 3 especially in traumatic SAH.4 5 6
Pioneers of aneurysmal surgery have pointed to the importance of perforating vessels for the blood supply of highly eloquent regions of the brain, such as the hypothalamus7 and the brain stem.8 Although these authors have stressed the clinical implications of surgical injury to these vessels, little is known about their hemodynamic response to vasospasm. Given the particular anatomy of perforating arteries, characterized by an abrupt decrease in lumen diameter and a right-angle bifurcation from the parent artery, it seems unlikely that those arteries would behave according to the same hemodynamic rules as for end arteries.
The purpose of the present study was to investigate the impact of cerebral vasospasm on perforating vessels using a phantom model of cerebral vasospasm.
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Methods |
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Phantom Model
A pulsatile pump (Harvard Apparatus) was set to provide a physiological waveform and outflow of 350 mL/min through a 10-mm-internal-diameter C-flex tube (Cole Parmer) at a perfusion pressure of 130/80 mm Hg (Figure 1A
). Perfusion pressure was continuously monitored by
a 25-gauge needle introduced upstream of the stenosis device
and connected to a pressure transducer. The perfusion fluid was
prepared by mixing glycerol, salt, 20-µm cellulose particles
(Sigmacell), and distilled water. In all experiments except that
involving manipulation of fluid viscosity, the amount of glycerol used
was adjusted to approximate blood viscosity at
physiological hematocrit value (2.4 viscosity at
40% hematocrit), according to Holdsworth et
al.9 The C-flex tube was
immersed in a water aquarium, the temperature of which was maintained
at 30°C. Perforating vessels were simulated by a 1-mm-diameter
silicon tube connected to the parent tube at a 90° angle, reproducing
thereby the microvascular anatomy of the brain stem both in
general architecture and diameter ratio between parent and branching
arteries. For each phase of the study, experiments were repeated 3
times and the measured flows averaged for each tube. To improve the
reproducibility of flow measurements, digitally time-controlled valves
were used for system output. Furthermore, measurement accuracy was
double-checked by online monitoring of the system total outflow by
electromagnetic flowmeter. Consequently, because the model was based on
a steady-state pumping device that was continuously monitored for both
flow and pressures upstream of stenosis in the main tube and
that used digitally time-controlled valves for time-collected-flows,
measurement variations were limited only by reading error (2 to 4 mL).
Larger errors indicated improper manipulations, such as incomplete
removal of air bubbles after a tube replacement. In such an instance,
tubes were cleaned from air and experiments repeated until expected
steady results were obtained.
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Study Design
Phase 1: Poststenosis Perforating
Artery Model
The poststenosis perforating artery model is
shown in
Figure 1B
.
Increasing Stenosis
Cylindrical stenosis devices of 20-mm length
and decreasing diameters varying between 1 and 8 mm were
introduced into the parent tube 1.5 diameters upstream of the aperture
of the secondary tube. Upstream perfusion pressure was maintained at
130/80 mm Hg. Pressure measurements were performed downstream of
the stenosis both in the parent and secondary
tubes.
Increasing Perfusion Pressure
A 2-mm-diameter stenosis device (80%
stenosis) was selected and introduced into the parent tube as
previously described. Pump output was then set to produce gradually
increasing perfusion pressures from 90/40 to 190/90 mm Hg.
Time-collected flows in both parent and secondary tubes were
recorded.
Increasing Fluid Viscosity
A 3-mm-diameter stenosis device with a
constant perfusion pressure of 130/80 mm Hg was used to raise
absolute viscosity of the perfusion fluid from 2.1 to 2.9 by increasing
the amount of glycerol in the fluid mixture. These viscosity values
were chosen because they reproduce the changes in the blood viscosity
due to hematocrit elevation from 30% to 50%. Time-collected flows in
both tubes were recorded.
Phase 2: Intrastenosis Perforating
Artery Model
In this phase of the study, the secondary tube
was connected to the distal part of cylindrical stenosis
devices of 40-mm length and decreasing diameters varying between 1 and
8 mm previously introduced into the main tube. As in phase 1,
perfusion pressure was maintained at 130/80 mm Hg with a fluid
mixture viscosity of 2.4, and time-collected flows in both tubes were
recorded. (See
Figure 1C.)
Ultrasonographic Assessment
Velocity profiles across the tube cross-sectional
area were obtained with the high-resolution FlowGuard Doppler
ultrasound flow system (Biosonix Ltd, Israel). The system allows for
simultaneous spectrum determination at multiple sample
volumes along each ultrasound beam. Both flow velocities and velocity
profiles were assessed with the FlowGuard probe 10 parent-tube
diameters upstream and 1.5 parent-tube diameters downstream of the
stenosis only in the first phase of the study
(Figure 1B).
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Results |
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Phase 1: Poststenosis Perforating Model
Arterial Stenosis Simulation
Effect on Velocity Profiles
Increasing stenosis of the parent tube resulted in a progressive change in the poststenotic velocity profile, which gradually turned into a thin jet limited to the center of the lumen (Figure 2
). At normal or minimally decreased parent-tube
diameter (
20% stenosis), the distal velocity profile
exhibited a smooth parabolic profile indicative of laminar, undisturbed
steady-state flow
(Figure 2). As stenosis severity increased, a gradual
decrease in the poststenotic shear rate was noticed, indicated
by flattening of the velocity profile near the walls (ie, decrease in
flow velocity at the walls). At 80% stenosis, the velocity
profile became completely flat (zero shear rate) in the periphery of
the lumen, and no flow could be detected near the tube walls. The
poststenotic laminar-like profile was corrupted, and the
velocity in the center on the tube lumen began to increase and turned
into a sharp velocity jet. Extreme stenosis (90%) eventually
caused separation of flow in the periphery of the lumen with a plug
flow profile characterized by clear retrograde velocities near the wall
boundaries. Surprisingly, these changes in the poststenotic
velocity profile, which were clearly noticed even at moderate
stenosis levels of 40%, were not coupled with a corresponding
effect on the parent-tube flow
(Figure 3). It is interesting to note that the laminar
proximal velocity profiles became rather flat with increasing
stenosis severity. This effect, however, became significant
only with stenosis of 
80%
severity.
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Effect on Outflow
As expected, increases in stenosis of the
parent tube correlated with a gradual decrease in both the parent- and
secondary-tube outflows
(Figure 3). Unlike changes in velocity profile, however, this
decrease in outflow became significant only with stenosis of
70%. Quite remarkably, this decrease in outflow was not symmetrical
in the parent and secondary tubes, starting at earlier stages of
stenosis and being much more emphasized in the secondary tube,
whereas it occurred at a 60% reduction in the main-tube
diameter
(Figure 3). Furthermore, flow reduction was significantly
deeper in the secondary tube, reaching an almost 90% flow decrease at
90% stenosis, whereas flow reduction was less than half the
initial value in the parent tube in the same condition. Such a flow
reduction in the secondary tube implies a significant change in flow
distribution, where the relative percentage of the flow in the
secondary tube compared with total system flow dropped from 18.5% to
4.5%.
Effect on Intraluminal Pressures
Stenosis of 70% induced a central lumen
pressure drop from 125/80 mm Hg upstream of the stenosis
to 80/45 mm Hg at the center of the lumen, 1.5 tube diameters
downstream of the stenosis. However, as the recording
needle was pulled out from the center of the lumen toward the tube
walls, the pressure dropped abruptly to 35/20 mm Hg near the
parent-tube wall. Intraluminal pressure recording from within
the secondary tube in the same conditions yielded a pressure of
25/20 mm Hg.
Pump Output and Perfusion Pressure
Increasing perfusion pressures through an extremely
narrowed main tube (80% diameter reduction) induced a gradual increase
in the total system outflow. Flow distribution between the parent and
secondary tubes, however, was markedly affected by the changes in
perfusion pressure
(Figure 4). As perfusion pressure was elevated, the relative
part of secondary-tube flow compared with total system flow increased
progressively from 8% to 14%.
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Fluid Viscosity
Effects on Velocity Profile
Increases in the viscosity of the perfusion mixture
from 2.1 to 2.9 were associated with marked changes in velocity
profiles that became gradually narrower, with a sharp velocity jet in
the center of the tube lumen. With a 70% parent-tube stenosis,
even a slight increase in the viscosity of the mixture led to
poststenotic flow separation, with notable retrograde flow
velocities near the vessel walls at viscosity levels exceeding 2.3
(Figure 5).
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Effects on Volume Flow
As expected, increased mixture viscosity was
responsible for a gradual and significant decrease in the system
outflow. This decrease in outflow, however, was much more prominent in
the secondary tube, whose relative flow contribution to the total
system flow dropped from 22% at a viscosity level of 2.1 to 15% at a
viscosity level of 2.9
(Figure 6).
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Phase 2: Intrastenosis Perforating
Artery Model
At a moderate level of stenosis, there was no
significant change in flow distribution between the main and secondary
tubes, which was similar to that observed in the same conditions with a
poststenosis perforating artery model. Whenever the main tube
diameter was reduced beneath 60%, however, there was a progressive
although moderate increase in the flow in the secondary tube at the
expense of the main tube. At an extreme level of stenosis
(90%), although the system outflow was globally reduced, the
respective flow in the secondary tube was markedly increased
(Figure 7).
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Discussion |
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Despite considerable improvement in its understanding and management, cerebral vasospasm after aneurysmal SAH remains a source of etiopathogenic controversies and is still responsible for 10% to 20% of death and disability.10 11 12 One of the most debated controversies is the contribution of arterial narrowing, as demonstrated by TCD or angiographic studies, to delayed neurological morbidity.3 This may be even more challenging in head injury, where neurological outcome is influenced by multiple factors.5 6 In this ongoing debate, most authors have stressed that arterial narrowing, as evidenced by TCD or angiographic studies, is significantly more common than the incidence of delayed brain ischemia and should therefore be distinguished from hemodynamically significant vasospasm.6 13 Moreover, the incidence of brain infarction in those patients suffering from symptomatic vasospasm is even lower, ranging from 3% to 17% in different CT studies of SAH patients.14 15 16 A generally accepted assumption for this discrepancy between anatomic and clinical findings is that arterial narrowing does not necessarily result in blood flow reduction below a critical threshold. Clinical and laboratory studies have indeed demonstrated that brain function can be sustained until blood flow remains above a critical threshold of 20 mL/100 g of brain per minute, whereas cell death occurs with blood flow levels <15 mL/100 g of brain per minute.17 18 19 This assumption is well supported by our results showing that flow in the main tube remained almost unaffected by stenosis <70%. Our results are in close accordance with early observations made by Moore and Malone20 in carotid stenosis and similar to the findings recently reported by Aaslid21 in a similar phantom model of arterial stenosis. Yet, all those studies, including ours, involved models based on short stenosis, so that the impact of the length of the stenosis was not taken into consideration. This may affect their validity in case of diffuse vasospasm involving large segments of cerebral arteries.
Most of the available information relates to large-vessel vasospasm, and CT scan studies usually refer to hypodense regions in vascular territories of major cerebral arteries. Clinical deterioration due to vasospasm, however, is seldom limited to the motor consequences of anterior or middle cerebral artery constriction. On the contrary, confusion and consciousness impairment most often initiate the clinical picture, whether or not focal deficit eventually develops.13 These signs suggest the involvement of hypothalamic perforating branches of the anterior cerebral artery. This assumption is in accordance with the anterior location of 85% of all saccular aneurysms and has been supported by pathological studies.22 23
In the present study, a phantom model was designed to simulate the anatomy of the perforating arteries characterized both by a right-angle bifurcation with the parent artery as well as an abrupt decrease in lumen diameter. Although the diameter of the tubes used in the model was significantly larger than that of cerebral arteries, the relative proportions between main cerebral and perforating arteries was respected. As expected, increasing stenosis induced a progressive decrease in the outflow in both tubes. The pattern of this decrease, however, appeared to depend on the relative location of the secondary tube with respect to the stenosis. Whenever the secondary tube emerged from the stenosis itself, its relative contribution to the system outflow increased moderately up to 80% stenosis and then increased abruptly. This phenomenon is likely to be the consequence of the progressive increase in the main-stem peripheral resistance caused by the stenosis, whereas resistance within the secondary tube remained unchanged. As the stenosis worsens or extends in length, the resistance ratio between the main and secondary tubes further increases, with a subsequent and prominent decrease in the main-tube outflow. This cumulative increase of peripheral resistance is probably responsible for the occurrence of brain infarction in territories supplied by end arteries rather than in deep-sited regions in patients suffering from diffuse spasm involving the branching zone of perforating arteries. This assumption is further supported by relatively higher flow rates in the secondary tube at each level of stenosis compared with the poststenotic model, which used a stenosis device half as long as that used in the intrastenosis model.
Conversely, whenever the secondary tube was connected in the poststenotic portion of the main tube, a decrease in the lumen of the parent tube resulted in a gradual change in the poststenotic velocity profile that progressively turned into a sharp and narrow velocity jet limited to the very center of the lumen. Further increases in the degree of the stenosis proved to be responsible for the occurrence of flow separation, with retrograde flow velocities observed in the periphery of the lumen. Yet, arterial tone of large vessels has proved to be reduced by increased shear rate induced by higher velocities.24 Therefore, in this situation, a vasodilatory response mediated by the endothelium of the affected artery might have modified the results in vivo. Nevertheless, our results are in close accordance with the findings of Hutchinson,25 who showed that partial ligation of the common carotid artery in dogs induced significant changes in velocity profile downstream of the carotid stenosis, leading to flow separation. Flow separation, in turn, may produce a venturi-like effect responsible for pressure collapse at the aperture of the secondary tube and partial rerouting of the flow into the main tube. The abrupt decrease in intraluminal pressure from the center of the tube toward its boundaries distally to the stenosis reported here supports this hypothesis. This pressure decrease, secondary to the changes in velocity profiles, most likely accounts for the much more profound reduction in secondary-tube outflow compared with that of the parent tube. Indeed, flow reduction in the secondary tube reached 90% of its initial value in a 90% stenosis model, whereas flow in the parent tube was reduced by only 40% in the same conditions. These results suggest that deep-sited regions of the brain supplied by perforating arteries are particularly vulnerable to changes in velocity profile such as those induced by focal cerebral vasospasm located proximally to such perforating vessels. This assumption is further supported by postmortem studies after SAH showing small brain infarction in cerebral territories supplied by perforating arteries.22 23 26 This clinical situation, however, is more likely to be relevant to the vertebrobasilar system, where vasospasm is most commonly focal and therefore exposes those perforators that branch out of the postvasospastic portion of the parent vessel.27 These results may also explain the occurrence of severe and prolonged consciousness impairment due to local cerebral vasospasm even in those patients who do not present with motor deficit or crude brain infarction on CT scan. Flow reduction in perforating arteries due to vasospasm has been also advocated to explain upper brain stem ischemia after SAH.28 29 More recently, Ritter et al30 reported on reduced brain stem blood flow in head-injured patients with papillary dilation. They showed that blood flow reduction did not correlate with brain stem lesion on CT scan or with elevated intracranial pressure. Although they did not measure blood flow velocities in the basilar artery, it may be hypothesized that posttraumatic basilar vasospasm may account in part for this blood flow reduction, at least in some of their patients. This hypothesis is supported by the blood supply architecture of the brain stem based mainly on perforating arteries on one hand and on the other hand by recent studies that showed that basilar artery vasospasm was significantly more frequent in posttraumatic hemorrhage than previously thought and could affect neurological outcome.6 31
Interestingly, our results suggest that triple H therapy (hyperdilution, hypervolemia, and hypertension), which is often used in the management of cerebral vasospasm, prominently affects perforating arteries. In the present model, increasing viscosity within physiological limits resulted in significant exacerbation of shear rates and flow separation downstream of a severe stenosis. As viscosity was elevated, thinning of the poststenotic jet wash and subsequent thickening of the turbulent surrounding zone induced a progressive redistribution of the flow at the expense of the secondary tube. This observation suggests that hemoconcentration is therefore more likely to impair flow in perforating vessels. However, several substantial differences between the present model and physiological facts in vivo should be considered, because they might affect the validity of our results. First, the present methodology did not include the complex and dynamic relationships between viscosity, shear rate, and vascular resistance. In large arteries, decreasing viscosity by means of hemodilution has yielded controversial results. As mentioned above, Merkumyants and Balashov24 showed that the femoral artery of anesthetized cats responds to increase blood flow by endothelium-mediated vasodilation. Such a vasodilation of large arteries was also speculated by Hudack et al to explain elevation of blood flow secondary to hemodilution32 despite associated arteriolar constriction.33 Conversely, Muizelaar et al34 challenged this hypothesis and proved that hemodilution was in fact accompanied by moderate vasoconstriction of large arteries in vivo, probably acting as a compensatory measure to disproportionate viscosity reduction at the microcirculatory level. They assumed, however, that the vascular bed was not affected by hemodilution and that there was no vascular recruitment. Our results may challenge this assumption by showing that decreased viscosity causes a relative redistribution of the blood flow in favor of perforating arteries, probably by reducing the phenomenon of flow separation. Conversely, increasing viscosity lead to an exacerbation of flow separation that may eventually lead to partial hemodynamic exclusion of at least some of the perforating arteries directly involved by intense negative flow-velocity vectors. This hypothesis, however, is obviously limited by the fact that specific rheological properties of the blood, such as variable erythrocyte aggregation in small vessels, could not be incorporated in the model. In addition, our model could not technically take into consideration complex physiological vascular properties such as autoregulatory vasodilation that might have otherwise influenced our results. Nevertheless, because changes in viscosity induced by hemodilution and hemoconcentration are more pronounced in the microcirculation, they are even more likely to enhance perturbations induced by changes in velocity profile.
The same limitations exist for the present model of elevation of perfusion pressure. Changes in perfusion pressure in this study had a more significant effect on secondary-tube outflow, probably as a result of an increase in the poststenotic pressure in the periphery of the lumen in the main tube despite further increase in shear stress.
In conclusion, the results of this study suggest that changes in velocity profile induced by cerebral vasospasm may lead to flow separation across the vascular cross-sectional area, resulting in pressure collapse at the aperture of small perforating vessels. These alterations of cerebral hemodynamics may account for at least part of the vasospasm symptomatology. Furthermore, these changes proved to be affected significantly by manipulations of pressure and viscosity, supporting the use of triple H therapy in the management of cerebral vasospasm.
Received September 7, 2000; revision received November 29, 2000; accepted December 11, 2000.
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G. E. Sviri, D. W. Newell, D. H. Lewis, C. Douville, B. Ghodke, M. Chowdhary, A. M. Lam, D. Haynor, M. Zaaroor, and G. W. Britz Impact of Basilar Artery Vasospasm on Outcome in Patients With Severe Cerebral Vasospasm After Aneurysmal Subarachnoid Hemorrhage Stroke, November 1, 2006; 37(11): 2738 - 2743. [Abstract] [Full Text] [PDF]
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 D. Goldsher, R. Shreiber, V. Shik, Y. Tavor, and J. F. Soustiel Role of Multisection CT Angiography in the Evaluation of Vertebrobasilar Vasospasm in Patients with Subarachnoid Hemorrhage AJNR Am. J. Neuroradiol., October 1, 2004; 25(9): 1493 - 1498. [Abstract] [Full Text] [PDF]
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G. E. Sviri, D. H. Lewis, R. Correa, G. W. Britz, C. M. Douville, and D. W. Newell Basilar Artery Vasospasm and Delayed Posterior Circulation Ischemia After Aneurysmal Subarachnoid Hemorrhage Stroke, August 1, 2004; 35(8): 1867 - 1872. [Abstract] [Full Text] [PDF]
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J.F. Soustiel, T.C. Glenn, P. Vespa, B. Rinsky, C. Hanuscin, and N.A. Martin Assessment of Cerebral Blood Flow by Means of Blood-Flow-Volume Measurement in the Internal Carotid Artery: Comparative Study With a 133Xenon Clearance Technique Stroke, August 1, 2003; 34(8): 1876 - 1880. [Abstract] [Full Text] [PDF]
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 J. F. Soustiel, E. Levy, M. Zaaroor, R. Bibi, S. Lukaschuk, and D. Manor A New Angle-Independent Doppler Ultrasonic Device for Assessment of Blood Flow Volume in the Extracranial Internal Carotid Artery J. Ultrasound Med., December 1, 2002; 21(12): 1405 - 1412. [Abstract] [Full Text] [PDF]
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J. F. Soustiel, V. Shik, R. Shreiber, Y. Tavor, D. Goldsher, and J. P. Muizelaar Basilar Vasospasm Diagnosis: Investigation of a Modified "Lindegaard Index" Based on Imaging Studies and Blood Velocity Measurements of the Basilar Artery * Editorial Comment: Investigation of a Modified "Lindegaard Index" Based on Imaging Studies and Blood Velocity Measurements of the Basilar Artery Stroke, January 1, 2002; 33(1): 72 - 78. [Abstract] [Full Text] [PDF]
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