(Stroke. 1995;26:259-264.)
© 1995 American Heart Association, Inc.
Articles |
Decompressive Craniectomy for Cerebral Infarction
An Experimental Study in Rats
From the Departments of Neuroradiology and Neurology (W.H.), University of Heidelberg Medical School, Heidelberg, Germany.
Correspondence to Michael Forsting, MD, Department of Neuroradiology, University of Heidelberg Medical School, Im Neuenheimer Feld 400, D-69120 Heidelberg, Germany.
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Abstract |
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Background and Purpose Acute ischemia in the territory of the carotid artery can lead to massive cerebral edema with raised intracranial pressure and progression to coma and death due to uncal, cingulate, or tonsillar herniation. Thus far, only anecdotal experience with supratentorial ischemia treated by decompressive craniectomy has been reported, and there are no published experimental data dealing with this kind of therapy in acute supratentorial stroke. In this study, we present our results on the effect of decompressive craniectomy in an endovascular model of cerebral infarction in rats.
Methods Focal cerebral ischemia was induced in 50 rats using an endovascular occlusion technique of the middle cerebral artery. Decompressive craniectomy was performed in 30 animals: in 15 animals after 1 hour and in the remaining 15 animals 24 hours after vessel occlusion. Twenty animals were not treated by decompressive craniectomy (control group).
Results Mortality in the nontreated group was 35%, whereas none of the animals treated by decompressive craniectomy died. Neurological behavior, weight loss, and infarction size were all significantly better in the animals treated by decompressive craniectomy, regardless of whether they had been treated after 1 or 24 hours (P<.01).
Conclusions Our results suggest that decompressive craniectomy for cerebral ischemia not only reduces mortality but also significantly improves outcome and reduces infarction size, probably because of increased perfusion pressure through leptomeningeal collaterals. This experimental study suggests that a controlled study of decompressive craniectomy in patients with acute internal carotid or middle cerebral artery occlusion would be worthwhile. By performing decompressive craniectomy in a small, selected group of patients, neurosurgeons may play an important role in the management of these patients.
Key Words: carotid arteries • cerebral infarction • cerebral ischemia • craniectomy • middle cerebral artery • rats
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Introduction |
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Ischemic cerebrovascular disease is the most prevalent disease of the brain and also the most common cause of death among patients with such diseases. Acute ischemia in the territory of the carotid artery can lead to massive cerebral edema with raised intracranial pressure and progression to coma and death. This phenomenon has been well documented in clinical observations and autopsy studies.1 2 3 4 5 Although much has appeared in the recent literature on the experimental evaluation of various antiedema agents in the treatment of focal cerebral ischemia, no one regimen or combination of regimens has been shown to be consistently effective in clinical trials.6 Until today there has been no proven therapy for acute infarction, although restoration of cerebral blood flow by thrombolysis seems promising.7 In stroke victims with massive unilateral hemispheric edema, surgical decompression may be an effective therapeutic alternative. This kind of therapy is well established for large cerebellar strokes, where there is little discussion about the need for early surgical intervention.8 9 10 In supratentorial ischemia, however, there are only anecdotal case reports on patients treated by decompressive craniectomy.11 12 13 14 15 No experimental data have been published on the usefulness of decompressive craniectomy in acute stroke. The aim of this study, in which we used an endovascular model for occlusion of the middle cerebral artery (MCA) in rats, was to show the effects of decompressive craniectomy on mortality, infarct size, and neurological outcome.
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Materials and Methods |
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Animal Preparation
In 50 male Wistar rats weighing 270 to 320 g, focal cerebral ischemia was induced using the intraluminal suture occlusion method.16 The study was approved by the local animal protection committee. Animals were anesthetized with ketamine (4 mg/100 g) and xylazine (1.5 mg/100 g) by intramuscular injection and were allowed free access to food and water before the procedure. The right femoral artery was cannulated for measuring pH, PO2, and PCO2 levels before the induction of ischemia and for monitoring blood pressure during surgery. Rectal temperature was maintained at 37°C with a feedback-regulated heating pad during the operation.
In all animals, the right MCA was occluded using a transvascular approach as previously described in detail.17 18 For MCA occlusion, the right common carotid and the right external carotid arteries were exposed through a midline neck incision. The distal common and external carotid arteries were first ligated with a 4-0 suture. A 4-0 monofilament nylon suture (40 mm in length, its tip rounded by heat) was then inserted through an arteriotomy of the common carotid artery and gently advanced into the internal carotid artery to a point approximately 17 mm distal to the carotid bifurcation. Mild resistance to this advancement indicated that the suture had entered the anterior cerebral artery, thus occluding the origins of the MCA and the posterior communicating artery. To prevent bleeding, the common carotid artery was loosely ligated with a 4-0 silk suture just distal to the arteriotomy, after which the neck wound was rapidly closed.
In 20 animals, no therapy was performed after MCA occlusion (group A). In a total of 30 animals, the right cerebral hemisphere was surgically decompressed through a craniectomy. In 15 of these 30 animals, decompressive craniectomy was performed 1 hour after MCA occlusion (group B); in the remaining 15 animals, it was performed 24 hours after MCA occlusion (group C). A bone flap (0.9x0.5 cm) was created in the temporal bone, and additional bone was removed down to the floor of the middle fossa under microscopic control using microscissors. The dura covering the frontal, parietal, and temporal lobes was then opened in a large cruciate incision. No cortical resection of infarcted brain was attempted. At the end of the procedure, the temporalis muscle and skin flap were adapted and sutured in place.
During the next 5 days, all surviving rats were neurologically examined according to a protocol, using the scoring system of Menzies et al19 ; simultaneously their weight was measured. At the end of the fifth day, all animals were reanesthetized with ketamine and xylazine and then decapitated. In 5 animals out of each group, the brain was prepared for microangiography (see below). In the remaining animals, the brains were rapidly removed, and 2-mm brain slices were incubated for 30 minutes in a 4% solution of 2,3,5-triphenyltetrazolium chloride (TTC) at 37°C and fixed by immersion in 10% buffered formalin solution. TTC stains normal brain tissue (intact cellular membranes) red, whereas ischemic tissue turns pink and necrotic tissue turns grayish. Six brain sections per rat were stained with TTC and then photographed. In those animals from group A (without craniectomy) who died before day 5, neither TTC staining nor microangiography was performed because of the unknown point of death and to avoid any postmortem artifacts.
Neurological Evaluation
To evaluate abnormal postischemic motor behavior, we used an
established scoring system that was first introduced by Bedersen et
al20 and refined by Menzies et al19 (Table 1
).
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Microangiography
On the fifth day, 5 rats from each group were prepared for
microangiography. All animals were transcardially perfused with a
mixture of 20% barium sulfate (Micropaque) and gelatin
8:2.21 This mixture (100 mL total volume) was administered
over a 30-minute period using a water pressure of 50 in, after which
the brains were removed. Each brain was then cut into 2-mm-thick
coronal blocks using a rat brain matrix for a total of seven slices per
animal. After slices were dehydrated and embedded in paraffin, contact
radiographs were obtained with a microstructure x-ray device (Philips
x-ray generator PW 1720). Microangiograms were analyzed both
macroscopically and microscopically to correlate the ischemic area on
TTC staining with the vascular state.
Data Analysis
The TTC-stained brain slices were first photographed. After
digitization of the photographs, the area of infarction was quantified
using a public-domain software for Macintosh computers
(IMAGE 1.41, Wayne Rasband, National Institutes of
Health, Bethesda, Md). On each slice the nonstained area (ischemic
brain) was marked, and the infarct volume was calculated according to
the slice thickness of 2 mm per slice. Measurement and calculation of
the infarction size was done twice by two of the authors (S.H. and
M.F.), who were both blinded to the treatment group.
For statistical analysis of all results, commercial software (STATVIEW, Brain Power Inc) installed on a personal computer (Macintosh Quadra, Apple Computer Inc) was used. The Wilcoxon test was used, and a value of P<.05 was considered to be significant.
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Results |
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Mortality
Seven of the 20 animals of the control group A died, all between 24 and 48 hours after vessel occlusion; therefore, without craniectomy after MCA occlusion, mortality was 35%. None of the animals of groups B and C died; with craniectomy after MCA occlusion, mortality was 0%, regardless of whether it had been performed early (after 1 hour) or late (after 24 hours). This difference was statistically significant (P<.01).
Body Weight
The body weight of the animals of the control group decreased by
an average of 23%. In contrast, animals treated by craniectomy had a
decline of body weight of only 9% to 10% (Table 2).
The weight differences at the end of the fifth day between animals of
group A and animals of groups B and C were statistically significant
(P<.05).
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Neurological Score
The average neurological score of the control group (A) was 3.1
after 120 hours. Animals with an early craniectomy (group B) had an
average score of 1.3, and those with a craniectomy after 24 hours
(group C) had a score of 1.8 (Table 3). The difference
between the treated and untreated animals was statistically
significant, but no significant difference was found when comparing
groups B and C.
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Volume of Infarction
The average volume of infarction in the animals of group A
(control group) was 161 mm3, whereas in group B
(early craniectomy) it was 26 mm3 and in group C (late
craniectomy) it was 59 mm3. The difference in infarct
volume of group A compared with groups B and C was statistically
significant, whereas the difference between groups B and C was not
significant (Table 4 and Figs 1 through 3). We found, however, a
trend toward larger and more cortically localized infarctions in group
C.
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Discussion |
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Massive unilateral infarctions that involve the entire MCA territory occur in 10% to 15% of supratentorial infarctions and can be associated with severe swelling and death due to brain herniation.22 23 24 Complete MCA infarction has a mortality rate of 5% to 33%.25 In some cases, potentially fatal herniation cannot be prevented with osmotic agents, diuretics, or hyperventilation. In the management of such cases, decompressive craniectomy has been recommended as an adequate lifesaving procedure.11 12 14 15 26 27 28
The treatment of surgical decompression for infarcted and swollen brain in general is not without precedent and is an old neurosurgical concept for posttraumatic brain swelling.29 In patients with massive supratentorial edema due to head trauma, however, decompressive craniectomy is known to be of limited value, since severe head trauma usually causes diffuse damage with bilateral edema and brain stem injury. An analogous situation in the posterior fossa that is due to ischemic necrosis of a cerebellar hemisphere is now widely recognized as a surgical emergency requiring surgical decompression with removal of infarcted brain.9 10 30 31 32 In anecdotal reports, decompressive craniectomy was found to be effective for treatment of massive edema related to supratentorial stroke.12 13 14 15 28 Before the age of computed tomographic scanning, swelling after cerebral infarction frequently masqueraded as brain tumor until surgery was performed.4 27 31 33 In 1956, Scarcella27 recommended resection of infarcted, necrotic brain in patients with encephalomalacia and mass effect. In contrast to the uniformly fatal outcome when biopsy alone was performed in these cases of suspected tumor, with resection two of three patients were alive 5 and 9 years after surgery. In their small series of five patients, Kondziolka and Faszl14 found craniectomy a lifesaving therapy in stroke patients. Rengachary and colleagues15 reported on three patients with large hemispheric infarctions who survived after craniectomy, but in two of them a severe focal neurological deficit persisted. Kalia and Yonas13 reported on four patients treated by decompressive craniectomy plus resection of nonviable brain, all of whom survived with a relatively good clinical outcome.
Thus far, there has been no experimental study or prospective randomized clinical study to evaluate the effectiveness of decompressive surgery in large, space-occupying supratentorial infarctions. The main reason for the lack of experimental studies is probably that the most commonly used model of focal cerebral ischemia, first described by Tamura et al,34 requires a craniectomy to occlude the MCA. Therefore, this model does not allow comparison of therapeutic effects of craniectomy with a control group because craniectomy has to be performed in all animals to occlude the vessel. Embolic models, on the other hand, do not require craniectomy, but infarction size is extremely variable and therapeutic effects are difficult to quantify unless large numbers of animals are used. The (photochemical) rose bengal model35 is characterized by an ischemic area that is small and without mass effect and does not simulate human cerebral ischemia at all.18 The lack of an appropriate model of focal cerebral ischemia thus prevented a systematic experimental study on the therapeutic effect of decompressive craniectomy in large cerebral infarction.
A model of endovascular occlusion, first described by Zea Longa et al16 and modified by different groups,36 37 38 nearly perfectly simulates MCA occlusion in humans and does not require any surgical manipulation of the skull. Therefore, this model allows evaluation of the effect of decompressive craniectomy in large supratentorial infarctions.
With the use of this endovascular model, mortality in our study was 0% for animals treated by craniectomy and 35% for the nontreated animals. These results corroborate the anecdotal clinical observation in patients with large supratentorial infarctions who were treated by decompressive craniectomy.11 12 13 14 15 Reduction of mortality (to zero) probably is due to a prevention of uncal herniation by converting the cranium from a "closed" cavity into an "open" one. Some may feel, however, that the saving of life may not be ethically appropriate if it is paid for with a severe functional neurological deficit. Our experimental results may provide an answer to this therapeutic problem as well, since neurological performance was significantly better, weight significantly higher, and infarction size significantly smaller in treated compared with untreated animals.
The most striking observation was reduced infarction size in the treated animals. For technical reasons, it was not possible to quantify the infarction size in those untreated animals of group A who died due to herniation before day 5 because TTC staining is not sufficient so many hours after death. Considering that these infarcts were the largest in the whole group, the real difference in infarction size between treated and untreated animals is even greater than was calculated. The same is probably true for body weight and neurological score. Dead animals were not scored; if they had been (with a score of 5), the difference between treated and untreated animals would have been larger. For all parts of our analysis in group A (body weight, neurological score, and infarction volume), our data analysis is more or less a "best-case" analysis: if data for animals that died early had been available, the differences between treated and untreated animals would have been larger.
What is the reason for the reduced infarction size in treated animals, resulting in improved neurological performance and less weight loss?
In this study, intracranial pressure, perfusion, and temperature were not measured to maintain a closed skull preparation. We cannot exclude the possibility that craniectomy did lower brain temperature. Low tissue temperature could have protected the brain from ischemic damage. However, there are several arguments in favor of a major role of intracranial pressure. Ischemic cerebral infarction associated with extensive edema and marked elevation of intracranial pressure may conceivably cause ischemia of neighboring brain tissue and thus lead to further infarction. Decompressive craniectomy interrupts this vicious cycle by decreasing the pressure of cerebrospinal fluid and brain tissue.39 This may increase cerebral perfusion pressure and optimize retrograde perfusion of MCA branches through leptomeningeal collaterals; functionally compromised but viable brain may thus be able to survive. The results of Valtysson et al40 lend further credence to this perfusion concept: They found that elevation of intracranial pressure increases the vulnerability of the border zones between the vascular territories. Decompressive craniectomy may better protect rat brain than the brains of humans because elevated perfusion pressure in humans may not uniformly lead to reactivation of the more regressed leptomeningeal vascular network. While vascular anatomy of rodents and primates is quite similar,41 42 a difference does exist in abundant collaterals between distal branches of the anterior, middle, and posterior cerebral arteries.41 Leptomeningeal vascular anastomoses undergo substantial structural changes with age leading to regression,43 a phenomenon that occurs to a lesser degree in rats than in humans.
Regardless of treatment, all rats suffered an ischemic infarction in the territory supplied by the lenticulostriate arteries, which are functional end arteries. This is also the area of the MCA territory where cerebral blood flow is most suppressed when the endovascular model of cerebral ischemia is used.37 In general, this is equivalent to M1 occlusions in humans: Those patients with excellent leptomeningeal collateral blood supply fare better, usually suffering only a subcortical striatocapsular infarction.44 45 This parallelism between human stroke and our animal model is a further argument that better perfused leptomeningeal collaterals are the main reason for reduced infarction size after decompressive craniectomy.
One problem facing the clinician is to determine the length of time to continue conservative therapy before considering decompressive craniectomy. Vasogenic edema after ischemic infarction in humans reaches a peak within 2 to 5 days.46 This time course does not exactly parallel that of rats, in which the peak of edema usually occurs within the first 24 to 48 hours. Our results (and those of experimental studies in general) cannot give the exact answer to the question of optimal timing of craniectomy in humans. First, we did not systematically perform craniectomy at times that differed from those used in our protocol, eg, at times other than 1 or 24 hours after vessel occlusion. The differences between both groups with craniectomy were not statistically significant, although there was a trend toward larger cortical infarcts in those animals in which we performed craniectomy after 24 hours. Second, the results obtained in rats cannot be directly transferred to humans, as the ratio of brain volume to skull volume in rats differs from that in humans, and (as mentioned above) the quality of leptomeningeal collateral also differs substantially. The exact time window for decompressive craniectomy as an alternative to medical therapy has to be evaluated in controlled patient studies. However, decompressive craniectomy should not be postponed so long that irreversible brain stem changes occur (eg, Duret hemorrhages). Integration of the clinical examination with early computed tomography findings and magnetic resonance perfusion imaging may allow the clinical significance of the infarction to be gauged and treatment options discussed before life-threatening brain swelling and herniation occur.47 48 49 50 The patient's age may be an important additional variable in that younger, less atrophic brains are less able to accommodate swelling than are older brains with generalized atrophy.
Our results suggest that decompressive craniectomy for cerebral ischemia not only may reduce mortality but may also significantly improve outcome and reduce infarction size. The next step in the evaluation of the benefit of craniectomy in large MCA infarction complicated by edema should be a controlled study in patients with acute internal carotid or MCA occlusion.
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Acknowledgments |
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This study was supported in part by a grant of the Deutsche Forschungsgemeinschaft (DFG; Ku 294/18-1). This work contains parts of the thesis of Dr W.-R. Schäbitz.
Received September 6, 1994; accepted October 21, 1994.
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T. Gerriets, E. Stolz, S. Konig, S. Babacan, I. Fiss, M. Jauss, and M. Kaps Sonographic Monitoring of Midline Shift in Space-Occupying Stroke : An Early Outcome Predictor Stroke, February 1, 2001; 32(2): 442 - 447. [Abstract] [Full Text] [PDF]
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C. Oppenheim, Y. Samson, R. Manai, T. Lalam, X. Vandamme, S. Crozier, A. Srour, P. Cornu, D. Dormont, G. Rancurel, et al. Prediction of Malignant Middle Cerebral Artery Infarction by Diffusion-Weighted Imaging Stroke, September 1, 2000; 31(9): 2175 - 2181. [Abstract] [Full Text] [PDF]
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T. Engelhorn, A. Doerfler, A. Kastrup, C. Beaulieu, Alexander de Crespigny, M. Forsting, M. E. Moseley, and F. M. Faraci Decompressive Craniectomy, Reperfusion, or a Combination for Early Treatment of Acute "Malignant" Cerebral Hemispheric Stroke in Rats? : Potential Mechanisms Studied by MRI • Editorial Comment: Potential Mechanisms Studied by MRI Stroke, July 1, 1999; 30(7): 1456 - 1463. [Abstract] [Full Text] [PDF]
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H.-P. Haring, E. Dilitz, A. Pallua, G. Hessenberger, A. Kampfl, B. Pfausler, and E. Schmutzhard Attenuated Corticomedullary Contrast: An Early Cerebral Computed Tomography Sign Indicating Malignant Middle Cerebral Artery Infarction : A Case-Control Study Stroke, May 1, 1999; 30(5): 1076 - 1082. [Abstract] [Full Text] [PDF]
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S. Schwab, T. Steiner, A. Aschoff, S. Schwarz, H. H. Steiner, O. Jansen, and W. Hacke Early Hemicraniectomy in Patients With Complete Middle Cerebral Artery Infarction Stroke, September 1, 1998; 29(9): 1888 - 1893. [Abstract] [Full Text] [PDF]
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S. Liachenko, P. Tang, R. L. Hamilton, Y. Xu, and L. Litt A Reproducible Model of Circulatory Arrest and Remote Resuscitation in Rats for NMR Investigation • Editorial Comment Stroke, June 1, 1998; 29(6): 1229 - 1239. [Abstract] [Full Text] [PDF]
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Y. Morimoto, Y. Morimoto, D. S. Warner, R. D. Pearlstein, and J. P. Muizelaar Acute Changes in Intracranial Pressure and Pressure-Volume Index After Forebrain Ischemia in Normoglycemic and Hyperglycemic Rats Stroke, August 1, 1996; 27(8): 1405 - 1410. [Abstract] [Full Text]
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J.C. Baron, R. von Kummer, and G.J. del Zoppo Treatment of Acute Ischemic Stroke : Challenging the Concept of a Rigid and Universal Time Window Stroke, December 1, 1995; 26(12): 2219 - 2221. [Full Text]
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