(Stroke. 1999;30:1456-1463.)
© 1999 American Heart Association, Inc.
Original Contributions |
Decompressive Craniectomy, Reperfusion, or a Combination for Early Treatment of Acute "Malignant" Cerebral Hemispheric Stroke in Rats?
Potential Mechanisms Studied by MRI
From the Department of Radiology, Stanford University (Calif) (T.E., A.K., C.B., A. de C., M.E.M.), and the Department of Neuroradiology, University of Essen (Germany) (A.D., M.F.).
Correspondence to Arnd Doerfler, MD, Essen University School of Medicine, Department of Neuroradiology, Hufelandstrasse 55, D-45122 Essen, Germany. E-mail arnd.doerfler{at}uni-essen.de
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Abstract |
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Background and Purpose—Both early reperfusion and decompressive craniectomy have proved beneficial in the treatment of large space-occupying "malignant" hemispheric stroke. The aim of this study was to directly compare the benefit of reperfusion with that of craniectomy and to study the effects of combined treatment in a rat model of focal cerebral ischemia.
Methods—Cerebral ischemia was introduced in 28 rats. Four groups were investigated: (1) no treatment, (2) decompressive craniectomy, (3) reperfusion, and (4) reperfusion and craniectomy as treatment at 1 hour after middle cerebral artery occlusion. Perfusion- and diffusion-weighted MRI were performed serially from 0.5 to 6 hours after middle cerebral artery occlusion.
Results—The 6-hour DWI-derived hemispheric lesion volumes in the reperfusion group (10.2±3.9%), the craniectomy group (23.0±6.4%), and the combination group (21.8±12.4) were significantly smaller than that in the control group (44.1±5.4%) (P<0.05). Reperfusion, craniectomy, and combined treatment led to higher perfusion in the cortex compared with the control group, whereas only reperfused animals achieved significantly higher perfusion in the basal ganglia. In 5 animals, combined reperfusion and decompressive craniectomy resulted in an early contrast media enhancement.
Conclusions—Early reperfusion and craniectomy were shown to be effective in decreasing infarction volume by improving cerebral perfusion. Reperfusion remains the best therapy in malignant hemispheric stroke. Combined treatment yields no additional benefit compared with single treatment, probably because of early blood-brain barrier breakdown.
Key Words: cerebral infarction • craniectomy • magnetic resonance imaging • middle cerebral artery occlusion • reperfusion • rats
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferencesIntroduction |
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Acute occlusion of the carotid artery or the middle cerebral artery (MCA) can cause massive cerebral edema with raised intracranial pressure and progression to coma and death. This phenomenon, described as "malignant MCA infarction," has been well documented in clinical observations and in autopsy studies.1 2 3 Mortality rates for unselected groups of patients with MCA infarction are 30% to 66%.4 5 6 Hacke et al 2 reported a mortality rate of 78% in patients who developed a malignant hemispheric infarction.
In the management of such cases, decompressive craniectomy has been recommended and indeed may be an appropriate, lifesaving procedure.4 7 8 9 10 Thus far, few experimental data have been published on the usefulness of decompressive craniectomy in the treatment of acute stroke.11 12 Doerfler et al11 showed in an experimental study in rats that decompressive craniectomy for cerebral infarction significantly reduced mortality and improved clinical outcome in a time-dependent fashion.
Recently, thrombolysis proved to be beneficial in acute ischemic stroke.13 14 Experimental studies suggest that there is a limited time window within the first 2 hours for successful reperfusion after vessel occlusion in rodents.15 16 An increased risk for intracerebral hemorrhage has been reported as a dangerous side effect of thrombolytic therapy.17 18
The aim of this study was to directly compare the benefits of reperfusion with those of decompressive craniectomy and to study the effects of a combined treatment of reperfusion and craniectomy in an animal model of hemispheric infarction. The techniques of diffusion- and perfusion-weighted MRI (DWI and PWI, respectively) were used to follow the progression of the ischemic lesion and the perfusion deficit, respectively.16 19
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Materials and Methods |
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Animal Model and Protocol
Focal cerebral ischemia was introduced in 28 male Sprague-Dawley rats (weight, 290 to 340 g) with the use of an intraluminal suture occlusion model. All animals were anesthetized initially with 3% halothane in a mixture of air (80%) supplemented with oxygen (20%). The rats were intubated and ventilated to keep blood gases within the physiological range. Anesthesia was maintained with 0.75% to 1.5% halothane throughout surgery and imaging. Body temperature was controlled with circulation of thermostated air. The femoral artery and vein were catheterized to monitor blood pressure and blood gases and to administer contrast agent. The study was approved by the Stanford Institutional Review Board.
In all animals, the right MCA was occluded by a transvascular approach as previously described in detail.20 21 Immediately after the advancement of the silicone-coated suture, all animals were transferred to the MRI scanner and were removed from the magnet at 1 hour after MCA occlusion (MCAO) for withdrawal of the suture and/or to perform a craniectomy. All animals were held in a plastic headholder with ear bars, and surgery was done without removing animals from the headholder. Before removal from the magnet after the first time point, the position of the headholder inside the probe and the position of the probe within the magnet were marked so that repositioning of the animal only involved realigning the alignment marks. Control animals received no additional treatment but were also removed from the magnet. To calculate infarction volume, all animals were killed at 24 hours after MCAO, and coronal brain sections (2 mm thick) were stained with 2,3,5-triphenyltetrazolium chloride (TTC) to obtain an MRI-independent measure of the ischemic injury.22
The study protocol consisted of 4 groups (n=7 per group): control group with no additional therapy (ie, no craniectomy or reperfusion) (group A), decompressive craniectomy (group B), reperfusion (group C), and reperfusion and decompressive craniectomy (group D) as treatment at 1 hour after MCAO.
In 14 of the 28 animals, decompressive craniectomy was performed as described recently.11 12 A bone flap (10x5 mm) was created in the parietal and temporal bone, and additional bone was removed down to the floor of the middle cerebral fossa. The dura covering the frontal, parietal, and temporal lobes was then opened by a large incision.
Magnetic Resonance Imaging
To follow the progression of the ischemic lesion, MRI
was performed at 6 time points: approximately 0.5 (before treatment),
1.5, 2.5, 3.5, 4.5, and 6 hours after MCAO. All imaging was performed
on a 2-T Bruker Omega CSI spectrometer equipped with shielded gradients
capable of producing 20 G/cm.
Isotropic diffusion-weighted spin-echo imaging was used for delineation of the ischemic region since it can depict the region of ischemia more accurately than single-axis DWI by removing the confounding effects of anisotropic diffusion on signal intensity.23 24 25 Each set of diffusion-sensitizing gradients before and after the radiofrequency pulse had a duration of 25 ms. A high gradient factor (b value) of 1300 s/mm2 was used for a diffusion-weighted image, and a low b value of 20 s/mm2 was used for a primarily T2-weighted image with a repetition time of 2.5 seconds and an echo time of 80 ms. The images were acquired with a 128x128 matrix, field of view of 50 mm, 1 average, 8 coronal slices, slice thickness of 1.5 mm, interslice gap of 0.2 mm, and an acquisition time of approximately 5.5 minutes.
PWI was performed after the DWI acquisition using a spin-echo, echo-planar imaging sequence to follow the passage of a bolus application of 0.3 mmol/kg Gd-DTPA (Magnevist, Schering).26 The echo-planar images were acquired with a 64x64 matrix, field of view of 40 mm, repetition time of 1 second, echo time of 88 ms, 1 average, 4 coronal slices, slice thickness of 2.5 mm, and an interslice gap of 0.2 mm. Forty sets of 3 slices were acquired continuously for 40 seconds.
T1-weighted imaging was performed 10 minutes after bolus injection of contrast media to examine disturbance of the blood-brain barrier (BBB). The T1-weighted images were acquired with a 128x128 matrix, field of view of 50 mm, repetition time of 500 ms, echo time of 14 ms, 2 averages, 8 coronal slices, and slice thickness of 1.5 mm.
Data Analysis
Data from DWI, PWI, and TTC studies were analyzed by 2
observers blinded to the treatment groups using the image processing
software MRVision (MRVision Co).
The evolution of the ischemic injury was followed by
calculating lesion volumes from diffusion-weighted images. Gray-scale
maps corresponding to actual signal intensity on a pixel-by-pixel basis
were displayed on the computer monitor. On all slices, the infarcted
and contralateral hemispheres were delineated by eyeballing.
Ischemic brain tissue was defined (computer assisted) as
regions with hyperintensity >1 SD (consistently 
18%)
compared with the normal contralateral side on the diffusion-weighted
images. This threshold is comparable to signal increases of 15% and
20% used in other DWI studies27 28 and correlates with
decrease in apparent diffusion coefficient (ADC) of
20%.29
The areas of DWI hyperintensity were summed over the central 6 MR images, and the lesion volume was expressed as a percentage of the hemispheric volume (%HLV). Lesion volumes at 24 hours after MCAO were measured by summing the unstained areas on TTC sections. To avoid overestimation of the infarction volume, as described by Lin et al,30 the corrected infarction volume (CIV) is given by the equation CIV=[LT-(RT-RI)]xd, where LT is the area of the left hemisphere (in mm2), RT is the area of the right hemisphere (in mm2), RI is the infarcted area (in mm2), and d is the thickness of the slices (1.7 mm).
As a semiquantitative measure of cerebral perfusion in the ischemic hemisphere, the time to peak (TTP) and the bolus-peak ratio (BPR) in the bolus-tracking curves were measured in the basal ganglia as well as in the MCA-supplied cortex and were normalized relative to the corresponding regions in the nonischemic hemisphere.16 TTP and BPR in the stroked ipsilateral hemisphere compared with the contralateral side are given by the following equations: TTP=(Time to Maximum Signal Loss, Ipsilateral)-(Time to Maximum Signal Loss, Contralateral) and BPR=[(Maximum Signal Loss, Ipsilateral)/(Maximum Signal Loss, Contralateral)]x100.
Since the signal loss in the ipsilateral hemisphere must be normalized with respect to the contralateral hemisphere, which presumably has normal perfusion, a BPR of 100% would imply normal perfusion in the ipsilateral hemisphere and 0% would indicate no perfusion. Perfusion changes were analyzed on the central slice at the level of the caudoputamen, and relative values compared with the contralateral nonischemic hemisphere were calculated.
Statistical Analysis
Statistical analysis between groups was performed by
1-way ANOVA with the use of commercial software (StatView; Brain
Power). To confirm that 2 given groups were significantly different,
the Fisher least significant difference test was performed when the
overall differences between the 4 groups were significant according to
ANOVA. A P value <0.05 for an overall difference between
the groups was considered to indicate statistical significance. Means
and SDs are presented for the various groups.
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Results |
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Physiology
Body temperature, pH, PO2, PCO2, and mean arterial blood pressure were within physiological range for all groups (Table
). None of the animals
experienced subarachnoid hemorrhage. Twenty-six of 28
animals survived until the 24-hour time point, and therefore infarct
volumes at 24 hours after MCAO were calculated from TTC-stained brain
sections for these animals.
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Mortality
Two of 7 animals of the control group died between 18 and 24 hours
after MCAO (mortality rate, 29%). None of the animals in the treated
groups died. This difference was significant (P<0.05).
TTC-Derived Lesion Volume
The TTC-derived hemispheric lesion volume (%HLV) at 24 hours
after MCAO is shown in Figure 1.
The final %HLV values on the TTC-stained brain sections at 24 hours
after MCAO in the craniectomy group (19.4±5.2%), reperfusion group
(8.8±3.5%), and combination group (18.7±9.7%) were significantly
smaller than in the control group (43.6±4.0%;
P<0.001).
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Evolution of Diffusion-Weighted Images
Diffusion-weighted MR images demonstrating the developing
ischemic lesion over 6 hours after MCAO in
representative animals of the 4 groups are shown in
Figure 2. The evolution of the %HLV in
the 4 groups is shown in Figure 1
. The %HLV for all groups did
not differ before treatment at 1 hour after MCAO, but then the lesion
volumes diverged and rapidly became different as soon as 1.5 hours
after MCAO. Both the combination group and the reperfusion group had
significantly smaller lesion volumes at 1.5 hours than at 0.5 hours
after MCAO and compared with the control group (P<0.01).
The lesion volume in the craniectomy group was significantly smaller at
2.5 hours after MCAO (P<0.05). At 2.5 to 6 hours after
MCAO, all 3 treated groups showed a significantly smaller DWI-derived
lesion volume.
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Perfusion Alterations
The BPR time course in the 4 groups during 6 hours after MCAO is
shown in Figures 3 and 4 for the ipsilateral basal ganglia and
cortex, respectively. The BPR before any treatment was reduced to
values from 35% to 39% in the cortex and from 61% to 63% in the
basal ganglia. These results are not significantly different between
the groups for either the basal ganglia or the cortex before treatment.
Importantly, there were no distinct indications of significant changes
in BPR between 30 minutes and 6 hours after MCAO in the cortex of
control animals (40% to 36%).
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After the suture was withdrawn, the area with a bolus delay (TTP) >2 seconds decreased from 48% to 66% to approximately 8% to 20%. The lack of a significant bolus delay after withdrawal of the suture signified that the origin of the MCA had been reopened properly in reperfused animals. As expected during the reperfusion phase, the BPR increased immediately after withdrawal of the occluding suture in all cases: 84.5±6.2% and 77.5±12.9% for the basal ganglia and the cortex, respectively, in the reperfusion group and 82.5±10.9% and 72.3±10.2% in the combination group. Compared with the control group and the craniectomy group, these values were significantly higher (P<0.01).
At 1.5 hours after MCAO, animals that underwent craniectomy showed a significantly higher BPR in the MCA-supplied cortex (54.1±9.9%), whereas BPR in the basal ganglia was not significantly better compared with control animals.
Contrast-Enhanced T1-Weighted Imaging
Postcontrast T1-weighted MR images demonstrating disruption of the
BBB in the ischemic area at 1.5 to 6 hours after MCAO are shown
in Figure 5 for
representative animals of all groups. All animals
undergoing decompressive craniectomy showed a slight contrast
enhancement at the cortex underlying the trepanation defect. At 1.5
hours after MCAO, 2 of 7 animals (29%) and at 2.5 hours 5 of 7 animals
(71%) that underwent reperfusion and craniectomy showed enhancement in
the MCA territory. The average BPR in these 5 animals was lower than in
the 2 animals without contrast media enhancement. In contrast, none of
the animals in the reperfusion group and only 2 animals (29%) in the
control group showed enhancement at 1.5 to 2.5 hours after MCAO.
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Discussion |
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The prognosis of complete MCAO is very poor.1 2 3 4 5 6 In the clinical management of patients with MCAO, early thrombolysis proved to be beneficial.13 14 However, thrombolysis increases the risk for intracranial hemorrhage.17 18 Decompressive craniectomy has shown to be a lifesaving procedure for malignant MCA infarction.4 7 8 9 10
This experimental study directly compared the benefits of early reperfusion with those of decompressive craniectomy and evaluated the effects of combined treatment on infarction size and cerebral perfusion. To maximize reperfusion effects, we chose 60 minutes of permanent MCAO. We used DWI and PWI to follow the progression of the ischemic lesion and the perfusion deficit in an animal model of hemispheric stroke.
Reperfusion at 1 hour after MCAO significantly reduced the size of the ischemic lesion compared with animals without treatment. After the suture was withdrawn, the area with a bolus delay >2 seconds decreased from 50% to 65% to approximately 10% to 20% of the hemisphere (data not shown). The lack of a significant bolus delay after withdrawal of the suture signified that the origin of the MCA had been reopened properly in the reperfused animals. As expected during the reperfusion phase, the BPR increases immediately after withdrawal of the occluding suture in all cases. Perfusion in the ischemic basal ganglia does not rebound to the values of the normal contralateral side (the BPRs remained <1), whereas the cortex was hyperperfused at 1.5 and 2.5 hours after reperfusion (103±7% and 109±20%, respectively). In agreement with other reports,31 32 the areas of T2-weighted abnormality were less conspicuous and underestimated the size of the ischemic lesion compared with that seen in DWI. However, most animals in the reperfusion group did show significant T2-weighted hyperintensities. The T2-weighted intensity, when present within the lesion, generally increased throughout the remainder of the reperfusion period in parallel with the development of vasogenic edema.
While clinical data suggest benefit for patients undergoing decompressive surgery, few data about the effect of decompressive craniectomy on experimental ischemia are available.11 12 Like early reperfusion, decompressive craniectomy performed at 1 hour after MCAO significantly reduces infarction size compared with untreated animals. The hemispheric lesion volume (%HLV) at 24 hours after MCAO was approximately 55% smaller compared with the control group. In these animals PWI provides insight into the marked decrease of underperfused brain tissue within the ischemic lesion. This group demonstrated significantly larger BPR in the cortex and hence better perfusion than the control group. This observation suggests that perfusion was improved probably via leptomeningeal collaterals as a result of decompressive craniectomy and that this improved perfusion may be directly responsible, at least in part, for the reduced size of the ensuing infarction volume in this group. However, although BPR in the basal ganglia increased after craniectomy, it was not significantly better compared with control animals. All animals undergoing decompressive craniectomy suffered an infarction of the basal ganglia. Compared with animals undergoing early reperfusion, craniectomy resulted in a less reduced infarction volume and less improved cerebral perfusion.
The measured ADCs for the normal and the infarcted contralateral hemispheres were similar for all 4 groups, as were the ADCs in the ischemic regions (data not shown). Since the ADC is a function of temperature, this result implies that brain temperature was not influenced by treatment,33 indicating that the results in the craniectomy group are not based on a simple cooling effect of the brain.
Interestingly, DWI-derived infarction volume was less reduced and cerebral perfusion less improved in animals that underwent a combined treatment of craniectomy and reperfusion compared with animals that underwent reperfusion only. Cortical areas in these animals showed a significant drop in BPR. However, BPR in the basal ganglia remained in the ranges of the reperfusion animals. TTC-derived HLV at 24 hours after MCAO was significantly larger (18.7±9.7%) than that of the reperfusion group (8.8±3.5%) and nearly in the same range as in the craniectomy group (19.4±5.2%).
Why does a combined treatment of reperfusion and decompressive craniectomy have no additional effects on infarction volume and cerebral perfusion compared with reperfusion as single treatment? Cooper at al34 showed that bony decompression results in apparent exacerbation of edema in a cold lesion model in dogs. Mean edema volume was 7 times larger in the craniectomized animals. The driving force for the formation of edema is the pressure gradient across the injured capillaries. This gradient is the difference between intravascular and interstitial fluid pressure. In the presence of edema, there is a hydrostatic gradient with highest interstitial pressure in the area adjacent to the lesion and decreasing pressures along the edema pathway toward normal tissue.35 36 Decompression of the brain probably results in decreased interstitial fluid pressure and subsequent enhancement of edema.
Hatashita and Hoff37 reported a significant drop in tissue pressure in the cortical gray matter after craniectomy in cats. The reduction of tissue pressure in the cortex was significantly larger than in the underlying white matter and the basal ganglia. These authors speculated that decompressive craniectomy may have adverse effects on severe cerebral edema and ischemic brain swelling after an increase of the intravascular blood volume. They demonstrated an extensive increase in vasogenic brain edema caused by BBB breakdown when arterial hypertension was combined with a decompressive craniectomy.38
Venes and Collins39 observed a worse outcome after spontaneous reperfusion in a patient undergoing a bifrontal decompressive craniectomy after head damage and brain infarction caused by traumatic vessel occlusion. An increase in transmural hydrostatic pressure gradient across the brain capillary bed produced by craniectomy (ie, decrease in tissue pressure) and increased intravascular blood volume (ie, increase in intravascular pressure) may be the underlying pathogenic factors.
We demonstrated in this study that at 1.5 hours after MCAO 2 of 7 animals (29%) and at 2.5 hours after MCAO 5 of 7 animals (71%) that underwent combined reperfusion and craniectomy had contrast media enhancement in the MCA territory. The average BPR values in these 5 animals were lower than in the 2 animals without early enhancement. In contrast, none of the animals in the reperfusion group and only 2 animals (29%) in the control group showed contrast media enhancement at 1.5 or 2.5 hours. Animals that underwent craniectomy showed no contrast media enhancement in the MCA territory at this time apart from subtle enhancement in the cortex underlying the opened dura, probably caused by extravasation from dural vessels. In addition to this significant increase in BBB breakdown, enhancement of the ventricular system, indicating a breakdown of the blood–cerebrospinal fluid barrier, was observed in 4 animals treated by reperfusion and craniectomy. Therefore, we presume that early BBB breakdown and the subsequent increase in brain edema (visible in the T2-weighted MR images) caused the worse outcome of animals in the combination group compared with the reperfusion group. Probably the extensive raised intracranial pressure decreased the perfusion of MCA branches and leptomeningeal collateral vessels, leading to the observed drop in BPR.
Our results suggest that early reperfusion should be the goal in the treatment of large hemispheric ischemia. Infarction volume was significantly reduced and cerebral perfusion was significantly improved in these animals compared with untreated animals. Interestingly, early decompressive craniectomy also significantly reduced infarction size compared with untreated animals without the increased risk of hemorrhage of thrombolytic therapy. The combination of reperfusion and decompressive craniectomy (although reducing infarction size) caused an extensive increase in BBB breakdown and brain edema in 5 of 7 animals, and such treatment should be considered carefully in the treatment of massive brain swelling caused by cerebral ischemia.
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Acknowledgments |
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This study was supported by the Deutscher Akademischer Austauschdienst (Dr Engelhorn), the Deutsche Forschungsgemeinschaft (Drs Kastrup and Engelhorn), the Alberta Heritage Foundation for Medical Research (Dr Beaulieu), the Center for Advanced MR Technology at Stanford, and the Lucas Foundation. We thank Maj Hedehus and Kim Butts for the isotropic diffusion pulse sequence.
Received February 22, 1999; accepted March 31, 1999.
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Editorial Comment
Potential Mechanisms Studied by MRI
Department of Internal Medicine, Cardiovascular Center, University of Iowa College of Medicine, Iowa City, Iowa
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Early reperfusion or a decompressive craniotomy may provide benefit by reducing brain injury during some forms of cerebral ischemia. In this study, the authors examined the effect of a craniotomy to reduce intracranial pressure, the effect of reperfusion, and a combination of the 2 treatments on brain injury in a rat model of focal cerebral ischemia. MRI was used to follow relative reductions in blood flow and the progression of ischemic injury.
The results of the study suggest that both reperfusion and craniotomy are effective in improving cerebral blood flow and reducing brain injury. Combined treatment with both these interventions produced no additional benefit compared with single treatment and may have enhanced disruption of the blood-brain barrier and edema formation. Thus, these findings support the concept that single interventions that increase cerebral perfusion are protective in this experimental model of cerebral ischemia.
Received February 22, 1999; accepted March 31, 1999.
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