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DOI: 10.1055/s-0043-1764415
Time course of hemispheric cerebral volume after decompressive craniectomy in malignant middle cerebral artery stroke
Evolução temporal do volume hemisférico cerebral após craniectomia descompressiva em infarto maligno de artéria cerebral médiaAbstract
Background Brain edema is the leading cause of death in patients with malignant middle cerebral artery (MCA) infarction. Midline shift (MLS) has been used as a monohemispheric brain edema marker in several studies; however, it does not precisely measure brain edema. It is now possible to directly measure hemisphere brain volume. Knowledge about the time course of brain edema after malignant middle cerebral artery infarction may contribute to the condition's management.
Objective Therefore, our goal was to evaluate the course of brain edema in patients with malignant MCA infarction treated with decompressive craniectomy (DC) using hemispheric volumetric measurements.
Methods Patients were selected consecutively from a single tertiary hospital between 2013 and 2019. All patients were diagnosed with malignant middle cerebral artery infarction and underwent a decompressive craniectomy (DC) to treat the ischemic event. All computed tomography (CT) exams performed during the clinical care of these patients were analyzed, and the whole ischemic hemisphere volume was calculated for each CT scan.
Results We analyzed 43 patients (197 CT exams). Patients' mean age at DC was 51.72 [range: 42–68] years. The mean time between the ischemic ictus and DC was 41.88 (range: 6–77) hours. The mean time between the ischemic event and the peak of hemisphere volume was 168.84 (95% confidence interval [142.08, 195.59]) hours.
Conclusion In conclusion, the peak of cerebral edema in malignant MCA infarction after DC occurred on the 7th day (168.84 h) after stroke symptoms onset. Further studies evaluating therapies for brain edema even after DC should be investigated.
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Resumo
Antecedentes O edema cerebral é a principal causa de morte em pacientes com infarto maligno de artéria cerebral média. O desvio da linha média tem sido utilizado como marcador de edema cerebral mono-hemisférico em alguns estudos; porém, ele não mede de forma precisa o edema cerebral. Atualmente é possível mensurar diretamente o volume do hemisfério cerebral. O conhecimento sobre a evolução temporal do edema cerebral após infartos malignos da artéria cerebral média pode contribuir para o cuidado clínico desta condição.
Objetivo Nosso objetivo é avaliar o edema hemisférico ao longo do tempo, em pacientes com infarto maligno da artéria cerebral média, tratados com craniectomia descompressiva.
Métodos Os pacientes foram selecionados de forma consecutiva, em um hospital terciário, entre 2013 e 2019. Todos os pacientes apresentavam diagnóstico de infarto maligno de artéria cerebral média e foram submetidos a craniectomia descompressiva. Todas as tomografias computadorizadas de crânio destes pacientes foram analizadas, e o volume do hemisfério cerebral infartado foi mensurado.
Resultados Analisamos 43 pacientes (197 tomografias de crânio). A idade média dos pacientes na craniectomia descompressiva foi 51,72 (42–68) anos. O tempo médio entre o ictus e a craniectomia descompressiva foi 41,88 (6–77) horas. O tempo médio entre o ictus e o pico do volume hemisférico foi 168,84 (142,08–195,59) horas.
Conclusão O pico do volume cerebral em pacientes com infarto maligno de artéria cerebral média submetidos a craniectomia descompressiva ocorreu no 7o dia (168,84 horas) após o infarto. Mais estudos avaliando terapêuticas direcionadas ao edema cerebral seriam úteis neste contexto.
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Palavras-chave
Craniectomia Descompressiva - Infarto de Artéria Cerebral Média - Pressão IntracranianaINTRODUCTION
Up to 10% of all stroke patients suffer from complete middle cerebral artery (MCA) infarction[1]; the leading cause of death is brain edema.[2] Swelling of the brain after ischemic insult has been described in numerous studies.[1] [3] [4] In an autopsy study, Shaw et al.[5] demonstrated that after an infarction in MCA territory, the midline shift (MLS) reaches its peak at day four. Silver et al.[4] found that the peak risk for death secondary to transtentorial herniation after a supratentorial infarction occurred 3 to 5 days (72–120 h) following the ischemic event. More recently, according to computed tomography (CT) exams, Dohmen et al.[3] showed that in 9 patients with a malignant course of an MCA infarction, MLS peaked after 54.7 h.
Midline shift has been used as a marker of monohemispheric brain edema in several studies.[6] [7] However, it does not measure brain edema with the required volumetric quantitative precision. Instead, MLS more likely represents subfalcine herniation,[8] which occurs in advanced cases of monohemispheric brain edema. At the onset of brain edema in the cerebral hemisphere, compensatory mechanisms, including a reduction in hemispheric cerebrospinal fluid and blood volumes, occur before the establishment of MLS.[9]
Because of such compensatory mechanisms, intracranial pressure (ICP) monitoring in patients with malignant MCA infarction before decompressive craniectomy (DC) has limited use since patients with severe brain stem compression, and even pupillary asymmetry, can present normal ICP values.[10]
Therefore, in patients with malignant MCA infarction, cerebral edema's time course determines the therapeutic option and their timing. In this way, comprehensive knowledge regarding the time course of brain edema after DC could contribute to such patients' management.
Regarding this matter, cerebral whole-hemisphere volumetry, and its variation according to time from symptoms onset is an important factor to be considered. There are several free non-commercial tools used in neuroscience in order to measure brain volumes, including: FreeSurfer, volBrain and 3D-Slicer. Among these, 3D-Slicer is the unique option that allows CT analysis (the others are based on magnetic resonance imaging [MRI]).[11]
Studying patients with DC after malignant MCA infarction offers a unique opportunity to observe the time course of brain swelling after large ischemic strokes in patients that do not have a rigid covering of the brain. Therefore, our goal was to evaluate the course of brain edema in patients with malignant MCA infarction treated with decompressive craniectomy (DC) using hemispheric volumetric evaluations.
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METHODS
Patients' selection
This retrospective study was approved by an ethics committee and was performed following the declaration of Helsinki. During hospital admission, signed consent was obtained from patients or relatives, and all data were anonymized at the source. We selected consecutive patients from a single tertiary hospital between 2013 and 2019. All patients had been diagnosed with a malignant MCA infarction and were submitted to DC to treat the ischemic event. Patients with an intracerebral hematoma, either initially or after hemorrhagic transformation, were excluded. Patients with prolonged time between symptoms onset and DC (> 96 hours) were excluded as well, since this prolonged ischemic time in a hemisphere cover by bone could prevent hemisphere to expand.
Diagnosis of malignant MCA infarction was made through a comprehensive analysis of multiple factors, including infarction size, National Institutes of Health stroke scale (NIHSS) score, radiological signs of mass effect, age, and past medical history. Subsequently, a multidisciplinary team that included a neurologist, a neurosurgeon, and a critical care physician decided whether to apply DC or not. Under this diagnosis (malignant MCA infarction) we included patients with a large infarction in the vascular territory of the MCA, including or not impairment of other vascular territories (anterior cerebral artery or posterior cerebral artery).
Clinical and radiological data were collected from the electronic medical records and included: age, sex, side of infarction, time from onset of symptoms until DC, NIHSS score, pupillary status before DC, hemispheric volume time course variation, infarction vascular territory, past medical history, alteplase use, endovascular procedures before DC, and modified Rankin scale after 1 year.
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Surgical procedure
Neurosurgeons from our hospital department performed all procedures. Two types of skin flaps were made: a large, inverted question mark (Becker type) and the T-type skin flap. As a department rule, the craniectomy flap was planned to be as big as possible. After craniectomy, the dura was incised, and then an expansion duraplasty using pericranium was made.
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Image analysis
All CT exams performed during these patients' clinical care were analyzed and processed in the software 3D Slicer (v. 4.10 - www.slicer.org), a free, open-source software,[12] including CT exams before and after DC. After loading the CT scan image on 3D Slicer, we performed whole hemisphere segmentation and calculated the volume of the whole infarcted hemisphere, excluding the ventricular system ([Figure 1]). To do this, we made the following steps: In Segment Editor Module, we started using the threshold of Hounsfield units between 7 and 70 as a mask, to exclude the cerebrospinal fluid (CSF) in the intraventricular and subarachnoid spaces. Then, the whole hemisphere of interest was marked using the automated tool Grow from Seeds in the segment editor module. After that, we inspected the quality of segmentation, performing some manual corrections when necessary. Lastly, using the Segment Statistics Module, we obtained the volume of the segmented whole hemisphere.
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Statistical analysis
Categorical variables were described as numbers of cases and percentages, and quantitative variables were characterized as mean ± standard deviations (SDs) or means ± range.
In order to demonstrate the average time between the ischemic event and the peak of cerebral hemisphere volume, we used a Kaplan-Meyer survival curve, using the highest measure as the event. If the volumetric variation was seen as a curve (with the highest measure between two or more lower measures), we considered the event's occurrence. The event was censored if the volumetric variation did not show as a curve.
All statistical analyses were performed using SPSS Statistics for Windows, version 17.0 (SPSS Inc., Chicago, IL, USA).
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RESULTS
We identified 53 consecutive patients who underwent a DC after the diagnosis of a malignant MCA infarction in our hospital from 2013 to 2019. Six patients were excluded from the analysis, as we identified hemorrhagic transformation in the ischemic area, and four patients were excluded because of time from symptom onset to DC (higher than 96 hours).
Therefore, we analyzed data from 43 patients (20 female) and a total of 197 corresponding CT exams. The mean age at DC was 52.27 (SD, 11.18] years. The mean time between the ischemic ictus and DC was 41.88 (SD, 29.32) hours ([Table 1]).
Demographics |
|
---|---|
Men |
23 (53.5%) |
Mean age (years) |
52.27 (SD, 11.18] |
Mean time from symptom onset to DC (hours) |
41.88 (SD, 29.32) |
Neurological examination |
|
NIHSS score[12] (admission) |
18 (IQR 17-20) |
Ipsilateral mydriasis before DC |
12 (27.9%) |
ASPECTS[13] |
|
ASPECTS 0 |
12 (27.9%) |
ASPECTS 1 |
7 (16.3%) |
ASPECTS 2 |
14 (32.6%) |
ASPECTS 3-6 |
10 (23.2%) |
Stroke treatment used before DC |
|
Intravenous alteplase |
11 (25.6%) |
Intraarterial thrombolysis or thrombectomy |
7 (16.3%) |
Modified Rankin scale after one year |
|
mRS 3 |
16 (50%) |
mRS 4 |
9 (15%) |
mRS 5 |
2 (4.7%) |
mRS 6 (death) |
16 (37.2%) |
Infarction site restricted to ipsilateral MCA territory |
25 (58.1%) |
Infarction site in MCA territory plus ACA or PCA |
18 (41.9%) |
Abbreviations: ACA, anterior cerebral artery; ASPECTS, Alberta stroke program early CT score; DC, decompressive craniectomy; IQR, interquartile range; MCA, middle cerebral artery; NIHSS, National Institutes of Health stroke scale; PCA, posterior cerebral artery; SD, standard deviation.
The time course of the volumetric cerebral hemisphere variation in each patient is shown in [Figure 2].
The mean time between the ischemic event and the peak hemisphere volume was 168.84 (95% confidence interval [CI] [142.08, 195.59]) hours. All patients achieved peak ischemic hemisphere volume after DC.
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DISCUSSION
In this study, we evaluated a group of consecutive patients who underwent a DC after a malignant MCA infarction in our institution. The peak of hemispheric cerebral volume in our patients occurred 168.84 (7.03 days) hours after the initial presentation of malignant stroke symptoms. In all patients, peak hemispheric volume occurred after DC.
Understanding the timing at which ischemic hemisphere volume peaks in these patients is important in managing ICP after DC. Previous studies demonstrated that the ICP could be elevated in patients who underwent DC for malignant cerebral infarction in the postoperative period.[13] [14]
Dohmen et. al.[3] analyzed a series of 17 patients with MCA infarction and hypoattenuation exceeding 50% of the MCA territory in the early (< 12 h) CT scan. In this series, MLS peaked 62.4 hours after stroke in patients who did not develop malignant edema and 54.7 hours in patients who developed a malignant MCA syndrome. Only two patients underwent a DC in this series.
In our study, all patients underwent DC, and after DC, the MLS became an erratic hemispheric swelling indicator.[15] After DC, many factors could modify the relationship between MLS and hemispheric cerebral swelling, including the area of bone decompression, the adequacy of duraplasty, and the elasticity of the skin. These factors could explain the divergence between the peak of MLS (in previous studies) and the peak of hemispheric cerebral swelling that we identified in our study.
Previous studies have analyzed the volume of infarcted cerebral areas. Brott et al.[16] found a mean volume of infarcted brain tissue (visualized by CT exams performed within the first 48 hours after stroke onset, 7 to 10 days after stroke onset, and 3 months after stroke onset) of 14 cm3 (first 48 hours), 55 cm3 (7-10 days), and 41 cm3 (3 months). In a series of patients with a malignant MCA infarction who underwent DC, Freyschlag et al.[17] observed a mean volume of infarcted brain tissue of 250 cm3 (in the preoperative period), 315 cm3 (postoperative day one), and 349 cm3 (postoperative day three).
In patients with malignant hemispheric cerebral infarction, the whole hemisphere's volume is the main factor that determines the intracranial pressure. Therefore, therapeutic measures have to be based on the time course of the entire hemisphere volumetric variation. Our series demonstrated that the peak volume in the ischemic hemisphere occurred later than previously suspected. Secondary ischemic lesions that occur at the border of the DC area secondary to hemisphere ischemic expansion traction in axonal bundles, among other factors, could explain the delay of the peak hemispheric volume in patients who undergo DC. Furthermore, delayed involvement of PCA or anterior cerebral artery (ACA) territory could also contribute to explain our findings.
As previously expected, the peak ischemic hemisphere volume was after DC in all patients of this series. Preoperative measurements were made to obtain a volumetric baseline for each hemisphere.
Therefore, according to this study's data, after DC in patients with malignant MCA infarction, the critical care team should be vigilant in detecting intracranial hypertension even after the 5th day.
The present retrospective study has several limitations. First, it is based on a single institution case series. Second, the hemispheric volumetric calculations were made using a partial manual segmentation method, leading to measurement errors.
In conclusion, the peak of cerebral edema in malignant MCA infarction after DC occurred on the 7th day (168.84 h) after stroke symptoms onset. Further studies evaluating therapies for brain edema even after DC should be investigated.
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Conflict of Interest
The authors have no conflict of interests to declare.
Authors' Contributions
LFB: final revision; TPR, MASR: first draft and final revision; TPR, FECN, SC, EAJ, GSS, ICS, RSC: concept and discussion.
Support
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.
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References
- 1 Schwab S, Steiner T, Aschoff A. et al. Early hemicraniectomy in patients with complete middle cerebral artery infarction. Stroke 1998; 29 (09) 1888-1893
- 2 Hacke W, Schwab S, Horn M, Spranger M, De Georgia M, von Kummer R. ‘Malignant’ middle cerebral artery territory infarction: clinical course and prognostic signs. Arch Neurol 1996; 53 (04) 309-315
- 3 Dohmen C, Galldiks N, Bosche B, Kracht L, Graf R. The severity of ischemia determines and predicts malignant brain edema in patients with large middle cerebral artery infarction. Cerebrovasc Dis 2012; 33 (01) 1-7
- 4 Silver FL, Norris JW, Lewis AJ, Hachinski VC. Early mortality following stroke: a prospective review. Stroke 1984; 15 (03) 492-496
- 5 Shaw CM, Alvord Jr EC, Berry RG. Swelling of the brain following ischemic infarction with arterial occlusion. Arch Neurol 1959; 1: 161-177
- 6 Chen X, Huang Q, Deng Q. et al. A prediction model of brain edema after endovascular treatment in patients with acute ischemic stroke. J Neurol Sci 2019; 407: 116507
- 7 Schur S, Martel P, Marcoux J. Optimal Bone Flap Size for Decompressive Craniectomy for Refractory Increased Intracranial Pressure in Traumatic Brain Injury: Taking the Patient's Head Size into Account. World Neurosurg 2020; 137: e430-e436
- 8 Dhar R, Yuan K, Kulik T. et al. CSF Volumetric Analysis for Quantification of Cerebral Edema After Hemispheric Infarction. Neurocrit Care 2016; 24 (03) 420-427
- 9 Dhar R, Chen Y, Hamzehloo A. et al. Reduction in Cerebrospinal Fluid Volume as an Early Quantitative Biomarker of Cerebral Edema After Ischemic Stroke. Stroke 2020; 51 (02) 462-467
- 10 Poca MA, Benejam B, Sahuquillo J. et al. Monitoring intracranial pressure in patients with malignant middle cerebral artery infarction: is it useful?. J Neurosurg 2010; 112 (03) 648-657
- 11 Harkey T, Baker D, Hagen J, Scott H, Palys V. Practical methods for segmentation and calculation of brain volume and intracranial volume: a guide and comparison. Quant Imaging Med Surg 2022; 12 (07) 3748-3761
- 12 Fedorov A, Beichel R, Kalpathy-Cramer J. et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging 2012; 30 (09) 1323-1341
- 13 Barber PA, Demchuk AM, Zhang J, Buchan AM. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group. Alberta Stroke Programme Early CT Score. Lancet 2000; 355 (9216): 1670-1674
- 14 Funchal BF, Alves MM, Suriano ÍC, Chaddad-Neto FE, Ferraz MEMR, Silva GS. Intracranial pressure following decompressive hemicraniectomy for malignant cerebral infarction: clinical and treatment correlations. Arq Neuropsiquiatr 2018; 76 (12) 812-815
- 15 Paldor I, Rosenthal G, Cohen JE. et al. Intracranial pressure monitoring following decompressive hemicraniectomy for malignant cerebral infarction. J Clin Neurosci 2015; 22 (01) 79-82
- 16 Brott T, Marler JR, Olinger CP. et al. Measurements of acute cerebral infarction: lesion size by computed tomography. Stroke 1989; 20 (07) 871-875
- 17 Freyschlag CF, Boehme C, Bauer M. et al. The Volume of Ischemic Brain Predicts Poor Outcome in Patients with Surgically Treated Malignant Stroke. World Neurosurg 2019; 123: e515 –e519
Address for correspondence
Publication History
Received: 17 May 2022
Accepted: 11 September 2022
Article published online:
09 May 2023
© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)
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References
- 1 Schwab S, Steiner T, Aschoff A. et al. Early hemicraniectomy in patients with complete middle cerebral artery infarction. Stroke 1998; 29 (09) 1888-1893
- 2 Hacke W, Schwab S, Horn M, Spranger M, De Georgia M, von Kummer R. ‘Malignant’ middle cerebral artery territory infarction: clinical course and prognostic signs. Arch Neurol 1996; 53 (04) 309-315
- 3 Dohmen C, Galldiks N, Bosche B, Kracht L, Graf R. The severity of ischemia determines and predicts malignant brain edema in patients with large middle cerebral artery infarction. Cerebrovasc Dis 2012; 33 (01) 1-7
- 4 Silver FL, Norris JW, Lewis AJ, Hachinski VC. Early mortality following stroke: a prospective review. Stroke 1984; 15 (03) 492-496
- 5 Shaw CM, Alvord Jr EC, Berry RG. Swelling of the brain following ischemic infarction with arterial occlusion. Arch Neurol 1959; 1: 161-177
- 6 Chen X, Huang Q, Deng Q. et al. A prediction model of brain edema after endovascular treatment in patients with acute ischemic stroke. J Neurol Sci 2019; 407: 116507
- 7 Schur S, Martel P, Marcoux J. Optimal Bone Flap Size for Decompressive Craniectomy for Refractory Increased Intracranial Pressure in Traumatic Brain Injury: Taking the Patient's Head Size into Account. World Neurosurg 2020; 137: e430-e436
- 8 Dhar R, Yuan K, Kulik T. et al. CSF Volumetric Analysis for Quantification of Cerebral Edema After Hemispheric Infarction. Neurocrit Care 2016; 24 (03) 420-427
- 9 Dhar R, Chen Y, Hamzehloo A. et al. Reduction in Cerebrospinal Fluid Volume as an Early Quantitative Biomarker of Cerebral Edema After Ischemic Stroke. Stroke 2020; 51 (02) 462-467
- 10 Poca MA, Benejam B, Sahuquillo J. et al. Monitoring intracranial pressure in patients with malignant middle cerebral artery infarction: is it useful?. J Neurosurg 2010; 112 (03) 648-657
- 11 Harkey T, Baker D, Hagen J, Scott H, Palys V. Practical methods for segmentation and calculation of brain volume and intracranial volume: a guide and comparison. Quant Imaging Med Surg 2022; 12 (07) 3748-3761
- 12 Fedorov A, Beichel R, Kalpathy-Cramer J. et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging 2012; 30 (09) 1323-1341
- 13 Barber PA, Demchuk AM, Zhang J, Buchan AM. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group. Alberta Stroke Programme Early CT Score. Lancet 2000; 355 (9216): 1670-1674
- 14 Funchal BF, Alves MM, Suriano ÍC, Chaddad-Neto FE, Ferraz MEMR, Silva GS. Intracranial pressure following decompressive hemicraniectomy for malignant cerebral infarction: clinical and treatment correlations. Arq Neuropsiquiatr 2018; 76 (12) 812-815
- 15 Paldor I, Rosenthal G, Cohen JE. et al. Intracranial pressure monitoring following decompressive hemicraniectomy for malignant cerebral infarction. J Clin Neurosci 2015; 22 (01) 79-82
- 16 Brott T, Marler JR, Olinger CP. et al. Measurements of acute cerebral infarction: lesion size by computed tomography. Stroke 1989; 20 (07) 871-875
- 17 Freyschlag CF, Boehme C, Bauer M. et al. The Volume of Ischemic Brain Predicts Poor Outcome in Patients with Surgically Treated Malignant Stroke. World Neurosurg 2019; 123: e515 –e519