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Epileptic Syndrome and Cranioplasty: Implication of Reconstructions in the Electroencephalogram
Journal Pre-proof Epileptic syndrome and cranioplasty: Implication of reconstructions in the electroencephalogram Leandro Pelegrini de Almeida, Mateus Carvalho Casarin, Humberto Luiz Mosser, Paulo Valdeci Worm PII:
S1878-8750(20)30301-6
DOI:
https://doi.org/10.1016/j.wneu.2020.02.036
Reference:
WNEU 14311
To appear in:
World Neurosurgery
Received Date: 15 October 2019 Revised Date:
4 February 2020
Accepted Date: 5 February 2020
Please cite this article as: Pelegrini de Almeida L, Casarin MC, Mosser HL, Worm PV, Epileptic syndrome and cranioplasty: Implication of reconstructions in the electroencephalogram, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.02.036. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Epileptic syndrome and cranioplasty: Implication of reconstructions in the electroencephalogram
Leandro Pelegrini de Almeidaa a
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected] Mateus Carvalho Casarinb b
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected] Humberto Luiz Mosserc c
Department of Neurology. Nossa Senhora da Conceição Hospital, Porto Alegre,
Brazil. [email protected] Paulo Valdeci Wormd d
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected]
Corresponding Author: Leandro Pelegrini de Almeida, M.D. Corresponding Author's Institution: Department of Neurosurgery, Cristo Redentor Hospital, Rio Grande do Sul, Porto Alegre, Brazil; e-mail: [email protected]; Telephone 5551996049539.
Keywords:
Cranioplasty;
Electroencephalography
Epilepsy;
Decompressive
craniectomy;
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Abstract Background: It has been observed that, in the presence of a skull deformity following large decompressive craniectomy (DC), neurological deterioration manifesting as epileptic syndrome (ES) may occur independently of the primary disease or spontaneous improvement would be unduly impaired, and that such unfavorable outcomes have sometimes been reversed by cranioplasty. The objective of this study was to analyze the influence of cranioplasty on the presence of ES in patients who underwent DC. Methods: A prospective study was performed from October 2016 to October 2017 involving patients who underwent DC and subsequent cranioplasty. Electroencephalographic (EEG) status before and after cranioplasty was analyzed in the presence of seizures and was compared with results after DC. Results: The sample included 52 patients. Male sex (78.8%) and traumatic brain injury (82.7%) were common indications for DC. ES post-DC was verified in 26.9% and 50% of patients presented abnormal EEG. ES after cranioplasty was noted in 21.2% and 36.3% of patients followed by abnormal EEG. All patients with pre-cranioplasty epileptogenic paroxysms exhibited better EEG tracings after the procedure. Conclusion: In routine clinical practice, altered amplitudes were observed in the region of bone defects. Although cranioplasty reduced pathological EEG (epileptogenic paroxysms), it was not able to produce new EEG tracings that could predict changes in seizure discharge or reduce ES.
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Introduction Decompressive craniectomy (DC) is a lifesaving procedure involving removal of a portion of the skull to alleviate swelling in the treatment of medically refractory intracranial hypertension (1). Harvey Cushing was the first to describe this technique and, for decades (2-5), it has been most commonly used in the setting of trauma or large-vessel infarct, and less frequently for aneurysmal subarachnoid hemorrhage (SAH), intraoperative brain swelling, and encephalitis (6-7). The procedure is used to relieve the mass effect of a swollen hemisphere on the thalamus, brainstem, and/or network projections to the cortex, manifesting mainly as a decreased level of arousal (8). Once patients undergo DC, those who survive are obligated to undergo a second procedure for surgical cranial reconstruction―more specifically, cranioplasty. Cranioplasty is a surgical intervention used to repair cranial defects, both for cosmetic and functional purposes. Repair of a skull vault defect is usually performed by the
insertion
of
material
(bone
or
nonbiological
materials
such
as
polymethylmethacrylate (9). It provides relief of psychological sequelae, increases social performance, and is also important for restoring the dynamics of a closed cavity, which are disturbed when, in the absence of overlying bone, atmospheric pressure can exert an influence. Cranioplasty can prevent the recurrence of brain damage and relieve the “syndrome of trephined” (10) and mental syndrome(s). However, it is not clear whether the procedure can protect patients from cerebral seizures or whether it results in electroencephalographic (EEG) changes. Relatively few modern-day large clinical series have addressed the relationship between epileptic syndrome (ES) and cranioplasty after DC (11-14). In the current
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study, our goal was to provide a review addressing the value of EEG in predicting ES in patients undergoing DC and subsequent cranioplasty.
Methods Study design A prospective study of patients who underwent cranioplasty after DC from October 2016 to October 2017 at the Neurosurgery Department of the Cristo Redentor Hospital – Conceição Hospital Group – Porto Alegre/RS, Brazil, was performed.
Eligibility All patients underwent clinical and neurological examination, laboratory evaluation, computed tomography (CT), and routine EEG before and after cranioplasty. The inclusion criteria were as follows: surgery at the authors’ service due to trauma or stroke mechanisms and who underwent DC; clinical and neurological status, assessed using the Glasgow Coma Scale (GCS), and radiological status; available EEG data; and minimum 6 months follow-up to establish ES. The minimum diameter for DC was 12 cm to enable a potential gain in cranial volume. Patients in whom DC did not have the minimum diameter, individuals without EEG or medical records, and those lost to follow-up were excluded.
Surgical technique Surgery was performed using methyl-methacrylate (MM), a non-metal allograft that is the most extensively used cranioplasty material (15,16). Animal experiments have revealed that acrylic adheres to the dura mater with no reaction to underlying layers (15). Before the use of MM, the scalp adherent to the dura is gently removed and clean
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bone borders are achieved. MM is then formed with the appropriate curvature. After installation, the MM is washed with cool water to prevent heat damage to the adjacent brain tissue. After this step, the MM is placed in a cup filled with physiological serum to finish cooling and hardening. The material is fixed to the bone using miniplates. Once again, proper cooling is achieved using water.
Variables analyzed The variables analyzed included age, sex, mechanism of injury (trauma or stroke), neurological presentation (e.g., ES) before and after cranioplasty, location of the primary injury, and type of intracranial injury. Preoperative and postoperative electrocortical status was reported using EEG. Before cranioplasty, the EEG needles were placed only in the area where there is bone, outside the scalp flap, to avoid contamination from noise sources such as muscles (temporal, facial and eye) activities. Pre- and postoperative EEGs were stratified according to the following categories: normal; pseudo-normal (low voltage slow, fenda, and brecha); focal lesional (delta, theta, and interhemispheric asymmetry); and epileptogenic paroxysms (focal epileptogenic, generalized epileptogenic, and ictal activity). From these categories, patients were allocated into groups. ES was established according to the International League Against Epilepsy (17), in which epilepsy is defined as at least two unprovoked seizures > 24 h apart and can be considered to be present after one unprovoked seizure in individuals with other factors that are associated with a high likelihood of a persistently lowered seizure threshold and, therefore, a high risk for recurrence. Such risk should be equivalent to the recurrence risk of a third seizure in those with two unprovoked seizures (i.e., at least 60%). The latter risk level is associated with remote structural lesions, such as stroke, central nervous system infection, certain types of
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traumatic brain injury (TBI), diagnosis of a specific ES or, in some circumstances, the presence of other risk factors.
Statistical analysis Numerical results are expressed as mean and standard deviation (SD), median and 25th and 75th percentile, or minimal and maximal values. Categorical results are expressed as absolute and relative frequencies. Associations were assessed using chi-squared, equal proportion, and McNemar tests for paired proportions. Post-hoc analyses were performed using the Bonferroni test, and relative risk (RR) was calculated when necessary. Differences with p < 0.05 were considered to be statistically significant.
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Results Baseline characteristics During the period from October 2016 to October 2017, 52 patients who underwent DC evaluated by the Neurosurgical Service and underwent cranioplasty were eligible for the study. Patient demographic data and surgical indications are summarized in Table A. The mean (± SD) age of the patients was 32 ± 12.8 years, and 50% were between 20 and 39 years of age. The predominant sex was male (n = 41 [78.9%]). Patients with hypertension constituted 19.2% (n = 10) of the sample, while those with diabetes mellitus (DM) constituted 5.8% (n = 3). The proportion of smokers was 25% (n = 13), and no patient had ES. The most common indication for DC was TBI (n = 43 [82.7%]), followed by stroke (n = 9 [17.3%]). Mechanisms of trauma included: motorcycle accidents (n = 12 [23.1%]), gunshot wounds (n = 11 [21.1%]), fall accidents (n = 6 [11.5%]), altercations (n = 5 [9.6%]), motor vehicle accidents (n = 4 [7.7%]), and other causes (n = 5 [9.6%]). Considering stroke mechanisms, ischemic stroke was the most prevalent (n = 5 [9.6%]), followed by hemorrhage (n = 2 [3.8%]), and aneurysmal SAH (n = 2 [3.8%]). Neurological assessment before DC revealed 21 (40.4%) patients with a GCS score of 9–15, 22 (42.3%) with a GCS score of 6–8, and 9 (17.3%) with a GCS score of 3–5. Unilateral frontotemporoparietal hemicraniectomy was performed in 44 (84.6%) patients (40.4% right, 44.2% left) and 8 (15.4%) underwent bifrontal craniectomy at initial surgery. Most patients presented with normal EEG post-DC and post-cranioplasty.
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CT findings Individual CT scan features included 86.5% (n = 45) of patients with cortical lesions, 57.7% (n = 30) traumatic SAH, 40.4% (n = 21) subdural hemorrhage, 15.4% (n = 8) extradural hemorrhage, 15.4% (n=8) intraparenchymal hemorrhage, and 7.7% (n = 4) intraventricular hemorrhage. A midline shift > 5 mm was observed in 38 (73.1%) cases.
EEG study An EEG study was performed within 6 months before and after cranial repair. Precranioplasty EEG was normal in 19 (36.5%) patients and post-cranioplasty in 27 (51.9%).
Features of post-DC seizures Patients were followed-up for a mean of 6 months after the first surgery (i.e., DC) until the second surgery (i.e., cranioplasty), and evaluated for the presence of ES, which was detected in 14 (26.9%) patients, of whom 7 (50%) exhibited normal EEG, 6 (42.9%) pathological, and 1 (7.1%) pseudo-normal. None of the patients progressed to status epilepticus. The majority of seizures were focal impaired awareness seizures (complex partial seizure) (n = 6 [42.9%]), followed by bilateral tonic-clonic (n = 5 [35.7%]) and mixed (n = 3 [21.4%]) seizures. After acute seizure attack, all patients (n = 14) were treated with intravenous phenytoin as first-line medication, followed by oral antiepileptic drugs. Statistical analysis did not reveal significant inter-group differences with regard to clinical parameters (age, DM, hypertension, and smoking), or between seizure types and EEG post-DC, probably due to the small number of cases.
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Patients who developed ES after DC (n = 14) were affected in the left (n = 7), right (n = 6), and bifrontal (n = 1) sides. This fact did not reveal differences between the groups according to the development of ES (pre-cranioplasty) (p = 0.4), except for the correlation between bifrontal DC and posterior EEG normal (p = 0.013). Virtually all patients who presented with ES exhibited cortical lesions (n = 13 [92.9%]). Although cortical lesions were not correlated with pathological EEG changes (p = 0.43), the RR for the development of ES in patients with cortical lesions was higher than in those without (RR 2.02). Only one patient whose primary pathology was extradural hematoma (EDH) (n = 8 [15.4%]) exhibited ES. Compared with other primary pathologies, EDH was associated with a lower risk for ES (RR 0.4231); however, there was no difference between EDH and other pathologies according to EEG changes (p = 0.25). Patients with the worst GCS scores (i.e., 3–8) represented 57.1% (n = 8) of all those who followed with seizures. These associations, however, did not represent significant inter-group differences.
Features of post-cranioplasty seizures All patients underwent cranioplasty exclusively with MM, except one, in whom autologous bone partially used with MM association. The MM was modeled and placed at the skull defect (Fig A). Patients were followed up for a mean of 6 months after cranioplasty and evaluated for the presence of ES, which was detected in 11 (21.2%), among whom 54.5% (n = 6) developed impaired awareness seizures (complex partial seizure), followed by bilateral tonic-clonic seizures (n = 3 [27.3%]), and mixed seizures (n = 2 [18.2%]). None of the patients progressed to status epilepticus. After seizure attack, 3 were treated with
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phenytoin, 2 with phenobarbital, 2 with carbamazepine, 1 with valproic acid, 2 with phenytoin plus phenobarbital, and 1 with phenytoin and carbamazepine.
Features of pre- and post-cranioplasty ES Analyzing patients with pre-cranioplasty ES (n = 14 [26.9%]), 3 (21.4%) presented the syndrome post-cranioplasty; however, this reduction did not indicate that cranioplasty reduced the risk for ES (p = 0.65). Similarly, considering patients who followed the syndrome post-cranioplasty (n = 11 [21.2%]), 3 (27.3%) had the syndrome precranioplasty, and the association was also not significant. Considering patients with the syndrome post-cranioplasty, only 1 presented immediately after the procedure, while the others presented at 6 months after the procedure, and the association was not significant. The time-relationship between clinical seizure events and EEG, was variable, within 6 months before and after cranial repair.
Features of pre- and post-cranioplasty EEG The proportion of patients with normal EEG increased after cranioplasty, from 36% precranioplasty to 52% post-cranioplasty. Those who exhibited normal EEG precranioplasty (n = 19 [36.5%]), followed post-cranioplasty with normal EEG in 14 (73.7%) cases, pseudo-normal in 3 (15.8%), and pathological in 2 (10.5%). Patients who presented with pathological EEG pre-cranioplasty (n = 18 [34.6%]), followed postcranioplasty with less pathological EEG (n = 9 [50%]), increasing normal (n = 7 [38.9%]) , and pseudo-normal (n = 2 [11.1%]) EEG cases. Of these 18 patients, all who manifested with epileptogenic paroxysms (n = 4 [22.2%]) followed post-cranioplasty without this worst of EEG alterations (Table B).
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Features of ES correlated with EEG Patients who manifested ES post-cranioplasty (n = 11 [21.2%]), previously presented with normal and pathological EEG in 5 (45.5%) cases each, and pseudo-normal in 1 (9.1%) case. Post-cranioplasty, they followed normal EEG in 7 (63.6%) cases, pathological in 3 (27.3%), and pseudo-normal in 1 (9.1%) . Patients who presented improvement in their EEG after cranioplasty (n = 16 [30.8%]) did not exhibit improvement in their clinical seizure status because most of them followed without changes (n = 10 [62.5%]), 25% (n = 4) worsened, and only 2 (12.5%) stopped seizures. Similarly, patients who exhibited deterioration in EEG changes after cranioplasty did not follow the worst ES (Table C).
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Discussion Seizure(s) is a well-known potential sequela of TBI and malignant middle cerebral artery (MCA) infarcts after DC (18-22). In our case series, 26.9% of patients presented with seizures post-DC. Creutzfeldt (23) reported that 49% of patients developed seizures after DC for malignant MCA. For the same reason, Santamarina (24) observed seizures in 47.5% of all patients and in 53.7% of survivors, while Brondani (25) reported a prevalence of 61%. In the two randomized controlled multicenter trials of DC after malignant MCA stroke that were conducted, Decompressive Surgery for the Treatment of Malignant Infarction of the MCA (DESTINY) (26) and Hemicraniectomy after MCA infarction with life-threatening edema trial (HAMLET) (27), did not report risk factors for seizures. In the case of TBI, Ban et al. (28) reported that only approximately 3% developed seizures despite the use of anticonvulsants. Seizures disappeared in all patients after increasing the dosage or after adding other antiepileptic drugs, which is a reasonable approach to follow in the first 2 weeks post-injury. Considering each type of TBI, the incidence of ES in acute subdural hematoma (aSDH) has been reported to be approximately 22% and less in chronic subdural hematoma and EDH 10% (29,30). As a pathophysiological mechanism for the high epileptogenicity of an aSDH, it has been postulated that the hematoma itself irritates the cortical surface with blood compounds and, later, with its degradation products (31). The decomposition of hemoglobin on the cortical surface is highly epileptogenic (32,33). Thus, blood evacuation through craniotomy or craniectomy may reduce the risk for ES; however, intracranial surgery was found to be an independent predictor of ES (34,35,36).
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Englander (35) speculated that the correlation between surgery and ES may be explained by sudden decompression through craniotomy, which may cause an additional
intraparenchymal
injury
through
a
sudden
negative
deceleration.
Consequently, this may promote neuronal damage and lead to the creation of an epileptogenic focus (37). On the other hand, the high incidence of ES after craniotomy may also be explained by the simple fact that the craniotomy itself is a surrogate marker of the severity of a brain injury, which accompanies structural parenchymal damage, and known to be epileptogenic. Suggested mechanisms of postoperative epilepsy in patients who have undergone DC include graded increases in hyperexcitability and a reduced epileptogenic threshold (28,38). Identifying the key risk factors predisposing to seizures and their effect on clinical outcomes requires further prospective studies. In our series, we found a statistically significant correlation between the development of ES in patients with cortical lesions, which higher than in those without it. This correlation is consistent with the supposed physiopathology described above in TBI, which also explains the low presence of ES in patients with EDH, a pathology that usually tends to not cause additional intraparenchymal injury. Although the frequency of post-traumatic seizures for all types of head injuries varies, the literature agrees that increased severity of TBI appears to lead to an increased risk for seizures (30,39,40). Most of our patients who developed seizures after DC presented with the worst initial GCS score. Patients with preoperative seizure disorders are more likely to exhibit postcranioplasty seizure (41). In our study, ES can either be attributed to seizures arising after initial TBI or cranioplasty. The overall rate of post-cranioplasty ES in our study was 21.2% (n = 11), and was highest compared with other large studies that have reported the rate to be as high as 14.37%–14.81% (42,43). These studies found that TBI
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was significantly correlated with seizures, although cranioplasty has often been investigated for the treatment of stroke and tumors. On the other hand, the relatively high incidence may be due to the inclusion of patients who experienced seizures before cranioplasty, as well as studies by Zhang (44) (35.7%) and Shih (45) (30.3%), whereas other studies have excluded these patients. As a treatment of choice for post-traumatic seizures, early cranioplasty has been emphasized by many authors. The timing of cranioplasty after DC is a controversial topic in the literature. For example, Shih (45) reported that longer timing between DC and cranioplasty was an independent risk factor for postprocedural seizures. On the other hand, an earlier systematic review and meta-analysis by Yao (46) reported that early cranioplasty leads to more post-cranioplasty seizures than late cranioplasty. In our study, all patients underwent cranioplasty 6 months after DC, which can be considered early. However, no further analysis could be performed, especially because there was no control group. Regardless of the time after DC, in 1939, Grant (47) reported a decrease in the incidence and even complete disappearance of epileptic fits in 18 of 27 (67%) patients in whom cranioplasty was performed. Several other authors have reported similar findings, although mostly in studies with smaller numbers of patients (47-52). The improvements observed after cranioplasty were attributed to the removal of adhesions between the skin and the dura (53). However, this removal of adhesions can lead to a conflict: Why are some of these patients more vulnerable to early ES, mostly immediately, on the same day of cranioplasty? This is an important question that remains theoretically explained. We know that after cranioplasty, the post-traumatic contusion healing process can lead to scar formation. Alternatively, exposure of the temporalis muscle during cranioplasty may also cause scarring. This physical traction of
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the tissue at the original surgical site during scar formation causes abnormal electrical discharges, thus inducing early seizures. Seizures are believed to be triggered by surgical manipulation of the brain during cranial reconstruction, increasing its epileptogenic susceptibility and probably altering other factors in cerebrospinal fluid dynamics (54). Another consideration is that revascularization is observed between the autologous fascia and the cerebral cortex after DC, resulting in traction with subsequent cortical insult, which subsequently induces early seizures. Moreover, patients who postpone cranioplasty are more likely to experience immediate and early seizures rather than late seizures (41). Cerebral scars more easily induce abnormal electrical discharge after extended postponement of cranioplasty. In late-onset seizures, patients experiencing postoperative stress may be susceptible to a cascade of events. Free radical production and release, with peroxidation and cell death may result in damage to the cortex and the formation of epileptogenic foci (41). Should we use anticonvulsants routinely before a cranioplasty? Prevention of seizures using antiepileptic therapy before
cranial
reconstruction
remains
controversial.
However,
perioperative
prophylactic antiepileptic therapy should be carefully considered only in patients with a documented history of epilepsy (55). To decrease the risk for seizures after cranial reconstruction, it is recommended to avoid or reduce the manipulation of the dura mater as much as possible when preparing the skull edges of the cranial defect, also ensuring to not compress the brain by forcing placement of the prosthesis. Controversial views regarding the benefit of cranial repair in post-traumatic epilepsy, however, appeared later, especially after World War II (56). In reviewing postoperative course in a comparatively large population of patients, Erculei and Walker (57) found no conclusive evidence that cranial repair exerts a determining influence on post-traumatic epilepsy. Such doubts were also raised by other authors arguing that
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nearly always only cranial defects are repaired while the brain cicatrice and the adhesions between the dura and the brain surface remain (12,56). Despite the fact that patients experience a reduced incidence of seizures, the reason for this was assumed to be another independent factor. Along this line, repair surgery appeared to be justified only if cortical “epilepsy resection” could be performed (12,57). This pathophysiology may explain why patients in our study did not exhibit a statistically significant reduction in seizures after cranioplasty because our patients were not subjected to cortical resection. The fact that skull defects have a large effect on EEG has been known since the inception of EEG (58). Cobb et al. (59) used the phrase “breach rhythm” (BR) for the mu-like activity that can arise close to skull holes; they also reported an enhancement of the amplitude of alpha and frontal fast rhythms ‘over or near unilateral posterior and frontal defects, respectively’”. By itself, this is not indicative of brain dysfunction and may be considered to be an expected physiological consequence of a skull defect, unless associated with spikes or focal slowing. Differentiating between BR and epileptiform abnormalities occurring in the same area may be challenging because sharpening and irregular morphology of BR may lead to misinterpretations. In the presence of BR, it is advisable to adopt a “conservative” reading, having a high threshold for calling epileptiform abnormalities to avoid a misdiagnosis of epilepsy due to an overinterpretation of non-epileptic sharp patterns. In our data, none of the patients presented seizures before the first procedure and then, after DC, some of them followed with seizures and only 36.5% (n = 19) presented with normal EEG. Attention was devoted to not classifying irregular morphologies as epileptiform abnormalities. Aside from the classification “normal”, we described pseudo-normal, focal lesional, and epileptogenic paroxysms.
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EEG changes are not uniform across individuals due to differences in the severity of head injuries. Some individuals exhibit a clinically normal EEG as early as 15 min after sustaining a concussion (60). Immediately after TBI, epileptiform activity (high amplitude sharp waves or high frequency discharges), followed by diffuse suppression of cortical activity typically lasting 1–2 min, followed by diffuse slowing of the EEG, which returns to normal baseline within 10 min to 1 h (61-63). Weeks to months after TBI, there is a 1–2 Hz increase in the frequency of the posterior alpha rhythm, which has been explained as a return to the original baseline from post-traumatic slowing (64,65). The majority of the acute EEG abnormalities described above resolve by 3 months, and 90% resolve within 1 year of head trauma (65). Another study in which EEG examinations were performed before and after cranioplasty in 20 patients with cranial defects > 100 cm2 found that in 12 patients, pathological EEG recordings were not accompanied by overt epileptic fits. In 5 of 10 patients with craniocerebral injuries, EEG improved and 2 of 10 deteriorated (66), demonstrating better EEG improvement, although in a very small number of patients. Spencer (67) suggested that MM plates would be almost as resistant to EEG as a skull structure of the same thickness, and regarded the presence of epilepsy as one indication for cranioplasty. Reduction of pseudo normal abnormalities, pathological findings, and epileptogenic paroxysms were observed in our study after cranioplasty. Serial observation of EEG did not demonstrate evidence of a reversible mechanism in clinical seizure manifestation, or of the favorable effects of correction of deformities using cranioplasty. Using our method, electroencephalography cannot be used to predict clinical improvement.
Strengths and limitations of the study
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Strengths of the present study included the capacity to perform follow-up and the external applicability of the results. One particular limitation, however, the small number of patients. Another implication is that our patients may have had EEG alterations previous to DC. However, this fact is exceedingly difficult to reconcile because our study focused on patients who experienced an incidental event (i.e., TBI, malignant MCA infarcts). The current trend is to understand the specificity of each EEG alteration before and after cranioplasty to establish whether one could predict posterior seizures. Our study group is poised to start a prospective and multicenter study to evaluate patients who underwent cranioplasty to accurately predict seizures over time.
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Conclusion In routine clinical practice, altered amplitudes were observed in the region of bone defects and cranioplasty can reduce pathological EEG (epileptogenic paroxysms), but is not able to produce new EEG tracings that can predict change(s) in seizure discharge and cannot reduce ES.
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Appendices Figure A - (1) Patient and cranial CT before performing cranioplasty; (2) after cranioplasty
Table A - Characteristics of patients who underwent cranioplasty Table B - Changes in each EEG abnormally following cranioplasty Table C - EEG and seizure changes following cranioplasty
Acknowledgements The authors would like to thanks all staffs and professors of the Department of Neurosurgery of the Cristo Redentor Hospital for the encouragement to develop this important research. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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21. Najafi MR, Tabesh H, Hosseini H, et al. Early and late posttraumatic seizures following traumatic brain injury: a five-year follow-up survival study. Adv Biomed Res. 2015;4:82. 22. Wang H, Xin T, Sun X, et al. Post-traumatic seizures—a prospective, multicenter, large case study after head injury in China. Epilepsy Res. 2013;107:272– 278. 23. Creutzfeldt CJ, Tirschwell DL, Kim LJ, Schubert GB, Longstreth WT, Becker KJ. Seizures after decompressive hemicraniectomy for ischaemic stroke. J Neurol Neurosurg Psychiatry. 2014;85:721–5. 24. Santamarina E, Sueiras M, Toledo M, Guzman L, Torné R, Riveiro M, et al. Epilepsy in patients with malignant middle cerebral artery infarcts and decompressive craniectomies. Epilepsy Res. 2015;112:130–136. 25. Brondani R, Garcia de Almeida A, Abrahim Cherubini P, Mandelli Mota S, de Alencastro LC, Antunes ACM, et al. High risk of seizures and epilepsy after decompressive
hemicraniectomy
for
malignant
middle
cerebral
artery
stroke. Cerebrovasc Dis Extra. 2017;7:51–61. 26. Juttler E, Schwab S, Schmiedek P, Unterberg A, Hennerici M, Woitzik J, Witte S, Jenetzky E, Hacke W; DESTINY Study Group: Decompressive Surgery for the Treatment of Malignant Infarction of the Middle Cerebral Artery (DESTINY): a randomized, controlled trial. Stroke. 2007;38: 2518–2525. 27. Hofmeijer J, Kappelle LJ, Algra A, Amelink GJ, van Gijn J, van der Worp HB; HAMLET Investigators: Surgical decompression for space-occupying cerebral infarction (the Hemicraniectomy After Middle Cerebral Artery infarction with Lifethreatening Edema Trial [HAMLET]): a multicentre, open, randomised trial. Lancet Neurol. 2009;8: 326–333.
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28. Ban SP, Son Y-J, Yang H-J, Chung YS, Lee SH, Han DH. Analysis of complications following decompressive craniectomy for traumatic brain injury. J Korean Neurosurg Soc. 2010;48:244–50. 29. Hamasaki T, Yamada K, Kuratsu J. Seizures as a presenting symptom in neurosurgical patients: a retrospective single-institution analysis. Clin Neurol Neurosurg. 2013;115:2336–40. 30.Annegers JF, Hauser WA, Coan SP, et al. A population-based study of seizures after traumatic brain injuries. N Engl J Med. 1998;338:20–4. 31. Frey LC. Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 2003;44(Suppl. 10):11–7. 32. Haltiner AM, Temkin NR, Dikmen SS. Risk of seizure recurrence after the first late posttraumatic seizure. Arch Phys Med Rehabil. 1997;78:835–40. 33. Hammond EJ, Ramsay RE, Villarreal HJ, et al. Effects of intracortical injection of blood and blood components on the electrocorticogram. Epilepsia. 1980;21 (February (1)):3–14. 34. Rabinstein AA, Chung SY, Rudzinski LA, et al. Seizures after evacuation of subdural hematomas: incidence, risk factors, and functional impact. J Neurosurg. 2010;112:455–60. 35. Englander J, Bushnik T, Duong TT, et al. Analyzing risk factors for late posttraumatic seizures: a prospective, multicenter investigation. Arch Phys Med Rehabil. 2003;84:365–73. 36. Hirakawa K, Hashizume K, Fuchinoue T, et al. Statistical analysis of chronic subdural hematoma in 309 adult cases. Neurol Med Chir. 1972;12:71–83.
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37. Seifi A, Asadi-Pooya AA, Carr K, et al. The epidemiology, risk factors, and impact on hospital mortality of status epilepticus after subdural hematoma in the United States. Springerplus. 2014;3:332. 38. Chen JWY, Ruff RL, Eavey R, Wasterlain CG. Posttraumatic epilepsy and treatment. J Rehabil Res Dev. 2009;46:685. 39. Annegers JF, Coan SP. The risks of epilepsy after traumatic brain injury. Seizure. 2000;9:453–7. 40. Ferguson PL, Smith GM, Wannamaker BB, Thurman DJ, Pickelsimer EE, Selassie AW. A population-based study of risk of epilepsy after hospitalization for traumatic brain injury. Epilepsia. 2010;51:891–8. 41. Haifeng W, Kewei Z, Hongshi C, et al. Seizure after cranioplasty: incidence and risk factors. The Journal of Craniofacial Surgery. Brief Clinical Studies. 2017. 42. Lee L, Ker J, Quah BL, et al. A retrospective analysis and review of an institution’s experience with the complications of cranioplasty. Br J Neurosurg. 2013;27:629–635. 43. Zanaty M, Chalouhi N, Starke RM, et al. Complications following cranioplasty: incidence and predictors in 348 cases. J Neurosurg. 2015;123:182–188. 44. Zhang, J., Liu, X., Zhou, J., Zhang, Z., Fu, M., Guo, Y., & Li, G. Seizures Following Cranioplasty. Journal of Craniofacial Surgery. 2019;30(2),e170e175. 45. Shih F-Yuan, Lin C-Cheng, Wang H-Chen, Ho J-Tsun, Lin C-Hsiang, Lu YTing, Chen W-Fu, Tsai M-Han. Risk Factors for Seizures after Cranioplasty. Seizure: European Journal of Epilepsy. 2018;66:15-21. 46. Yao Z, Hu X, You C. The incidence and treatment of seizures after cranioplasty: a systematic review and meta-analysis. Br J Neurosurg. 2018;32(5):489494.
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47. Grant, FC, Nacross, NC. Repair of Cranial Defects by Cranioplasty. Ann. Surg. 1939;110, 488-512. 48. Eiselberg, A. Zur Behandlung von erworbenen Schadelknochendefekten. Zbl. Chir. 1895;22,27-44. 49. Gardner, WJ. Tantal in the Immediate Repair of Traumatic Skull Defects. Method of Immobilizing the Wounded Brain. Nav. med. Bull. 1944;43,1100-1106. 50. Gardner, WJ. Closure of Defect of the Skull with Tantalum. Surg. Gynec. Obstet. 1975;80, 303-312. 51. Konig, F. Der knocherne Ersatz groBer Schiideldefekte. Zbl. Chir. Leipzig. 1890;17, 497-501. 52. Rasmussen, P, Husby, J. Proceedings of the 28th Annual Meeting of the Nordisk Neurokirurgisk Forening. Acta Neurochir. 1977;37, 304-305. 53. Glowacki, J, Murray, JE, Kaban, LB, Folkman, J, Mulliken, JB. Application of the Biological Principle of Induced Osteogenesis for Craniofacial Defects. The Lancet. 1981;May 2. 54. Walcott BP, Kwon C-S, Sheth S, Fehnel CR, Koffie RM, Asaad WF, et al. Predictors of cranioplasty complications in stroke and trauma patients. J Neurosurg. 2013;118:757–762. 55. Deutschman CS, Haines SJ. Anticonvulsant Prophylaxis in Neurological Surgery. Neurosurgery. 1985;17:510-7. 56. Walkter, AE, Jablon, S. A Follow-Up Study of Head Wounds in World War II, p. 202. Washington, D. c.: U.S. Government Printing Office. 1961. 57. Erculei, F, Walker, AE. Posttraumatic Epilepsy and Early Cranioplasty. J. Neurosurg. 1963;1085-1089.
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58. Berger H. Hans Berger on the electroencephalogram of man (translated by P. Gloor). Electroenceph clin Neurophysiol 1930(Suppl 28):48. van den Broek SP, Reinders F, Donderwinkel M, Peters MJ. Volume conduction effects in EEG and MEG. Electroenceph clin Neurophysiol 1998;106:522–534. van Burik MJ, Peters MJ. EEG and implanted sources in the brain. Arch Physiol Biochem 2000a;107:367–375. van Burik MJ, Peters MJ. Estimation of the electric conductivity from scalp measurements: feasibility and application to source localization. Clin Neurophysiol. 2000b;111:1514– 1521. 59. Cobb WA, Guiloff EJ, Cast J. Breach rhythm: the EEG related to skull defects. Electroenceph clin Neurophysiol. 1979;47:251–271. 60. Dow RS, Ulett G, Raaf J. Electroencephalographic studies immediately following head injury. Am J Psychiatry. 1944;101:174-83. 61. Walker AE, Kollros JJ, Case TJ. The physiological basis of cerebral concussion. J Neurosurg. 1944;1:103-16. 62. Meyer JS, Denny-Brown D. Studies of cerebral circulation in brain injury. II. Cerebral concussion. Electroencephalogr Clin Neurophysiol. 1955;7:529-44. 63. Hayes RL, Katayama Y, Young HF, Dunbar JG. Coma associated with flaccidity produced by fluid-percussion concussion in the cat. I: Is it due to depression of activity within the brainstem reticular formation? Brain Inj. 1988;2:31-49. 64. Koufen H, Dichgans J. Frequency and course of posttraumatic EEGabnormalities and their correlations with clinical symptoms: a systematic follow up study in 344 adults. Fortschr Neurol Psychiat Grenzgeb. 1978;46:165-77. 65. Nuwer MR, Hovda DA, Schrader LM, Vespa PM. Routine and quantitative EEG in mild traumatic brain injury. Clin Neurophysiol. 2005;116:2001-25.
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66. Stula, D. Cranioplasty: indications, techniques, and results. SpringerVerlag/Wien. 1984;1º edition. 67. Spence, WT. Form-fitting plastic cranioplasty. J. Neurosurg. 1954;11:219225.
27
Variable Age at operation, y Median > 50 ≤50 Sex Male Female Smoking Diabetes Mellitus Hypertension Location Right Left Bifrontal GCS at decompressive craniectomy 3-5 6-8 9-15 Indication for DC TBI Stroke
No
%
32 5 47
9.6% 90.4%
41 11 13 3 10
78.9 21.1 25 5.8 19.2
21 23 8
40.4 44.2 15.4
9 22 21
17.3 42.3 40.4
43 9
82.7 17.3
Preoperative abnormality
Post cranioplasty (number of patients) Improved No Changes Deteriorated
Pseudonormal Low voltage slow (n=8) Fenda (n=6) Brecha (n=1)
2 3 0
4 2 1
2 1 0
1 2 4
0 1 3
0 2 1
4 0 0
0 0 0
0 0 0
Focal lesional Theta (n=1) Delta (n=5) Interhemispheric asymmetry (8)
Epileptogenic paroxysms Focal epileptogenic (n=4) Generalized epileptogenic (n=0) Ictal activity (n=0)
EEG changes following cranioplasty Improved (n=16) No changes (n=25) Deteriorated (n=11)
Seizures (number of patients) Stoped No changes Deteriorated 2 10 4 6 16 3 3 7 1
p Value 0.66 0.81 0.072
Abbreviations List aSDH – Acute Subdural Hematoma BR – Breach Rhythm CI – Confidence Interval CT - Computed Tomography DC – Decompressive Craniectomy DM – Diabetes Mellitus EDH - Extradural Hematoma EEG – Electroencephalography ES – Epileptic Syndrome GCS – Glasgow Coma Scale GW - Gunshot Wounds MCA – Middle Cerebral Artery MM – Methyl-Methacrilate N - Number of cases RR - Relative Risk SAH - Aneurysmal Subarachnoid Hemorrhage SD – Standard Deviation TBI - Traumatic Brain Injury
Leandro Pelegrini de Almeida, MD, corresponding author
Disclosure-Conflict of Interest
The authors have no conflicts or disclosures to identify, and ethical standards have been utilized during the preparation of this manuscript. We also have no financial disclosures to identify.
Leandro Pelegrini de Almeida, MD, corresponding author
Credit Author Statement
Leandro Pelegrini de Almeida - Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Project administration; Resources; Software; Validation; Visualization; Roles/Writing - original draft; Writing - review & editing.
Mateus Carvalho Casarin - Investigation; Methodology; Software; Visualization; Roles/Writing - original draft.
Humberto Luiz Mosser - Investigation; Methodology; Software; Validation; Visualization.
Paulo Valdeci Worm - Conceptualization; Data curation; Methodology; Project administration; Resources; Supervision; Roles/Writing - original draft; Writing - review & editing.
Leandro Pelegrini de Almeida, MD, corresponding author
S1878-8750(20)30301-6
DOI:
https://doi.org/10.1016/j.wneu.2020.02.036
Reference:
WNEU 14311
To appear in:
World Neurosurgery
Received Date: 15 October 2019 Revised Date:
4 February 2020
Accepted Date: 5 February 2020
Please cite this article as: Pelegrini de Almeida L, Casarin MC, Mosser HL, Worm PV, Epileptic syndrome and cranioplasty: Implication of reconstructions in the electroencephalogram, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.02.036. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Epileptic syndrome and cranioplasty: Implication of reconstructions in the electroencephalogram
Leandro Pelegrini de Almeidaa a
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected] Mateus Carvalho Casarinb b
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected] Humberto Luiz Mosserc c
Department of Neurology. Nossa Senhora da Conceição Hospital, Porto Alegre,
Brazil. [email protected] Paulo Valdeci Wormd d
Department of Neurosurgery. Cristo Redentor Hospital, Porto Alegre, Brazil.
[email protected]
Corresponding Author: Leandro Pelegrini de Almeida, M.D. Corresponding Author's Institution: Department of Neurosurgery, Cristo Redentor Hospital, Rio Grande do Sul, Porto Alegre, Brazil; e-mail: [email protected]; Telephone 5551996049539.
Keywords:
Cranioplasty;
Electroencephalography
Epilepsy;
Decompressive
craniectomy;
Almeida
Abstract Background: It has been observed that, in the presence of a skull deformity following large decompressive craniectomy (DC), neurological deterioration manifesting as epileptic syndrome (ES) may occur independently of the primary disease or spontaneous improvement would be unduly impaired, and that such unfavorable outcomes have sometimes been reversed by cranioplasty. The objective of this study was to analyze the influence of cranioplasty on the presence of ES in patients who underwent DC. Methods: A prospective study was performed from October 2016 to October 2017 involving patients who underwent DC and subsequent cranioplasty. Electroencephalographic (EEG) status before and after cranioplasty was analyzed in the presence of seizures and was compared with results after DC. Results: The sample included 52 patients. Male sex (78.8%) and traumatic brain injury (82.7%) were common indications for DC. ES post-DC was verified in 26.9% and 50% of patients presented abnormal EEG. ES after cranioplasty was noted in 21.2% and 36.3% of patients followed by abnormal EEG. All patients with pre-cranioplasty epileptogenic paroxysms exhibited better EEG tracings after the procedure. Conclusion: In routine clinical practice, altered amplitudes were observed in the region of bone defects. Although cranioplasty reduced pathological EEG (epileptogenic paroxysms), it was not able to produce new EEG tracings that could predict changes in seizure discharge or reduce ES.
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Introduction Decompressive craniectomy (DC) is a lifesaving procedure involving removal of a portion of the skull to alleviate swelling in the treatment of medically refractory intracranial hypertension (1). Harvey Cushing was the first to describe this technique and, for decades (2-5), it has been most commonly used in the setting of trauma or large-vessel infarct, and less frequently for aneurysmal subarachnoid hemorrhage (SAH), intraoperative brain swelling, and encephalitis (6-7). The procedure is used to relieve the mass effect of a swollen hemisphere on the thalamus, brainstem, and/or network projections to the cortex, manifesting mainly as a decreased level of arousal (8). Once patients undergo DC, those who survive are obligated to undergo a second procedure for surgical cranial reconstruction―more specifically, cranioplasty. Cranioplasty is a surgical intervention used to repair cranial defects, both for cosmetic and functional purposes. Repair of a skull vault defect is usually performed by the
insertion
of
material
(bone
or
nonbiological
materials
such
as
polymethylmethacrylate (9). It provides relief of psychological sequelae, increases social performance, and is also important for restoring the dynamics of a closed cavity, which are disturbed when, in the absence of overlying bone, atmospheric pressure can exert an influence. Cranioplasty can prevent the recurrence of brain damage and relieve the “syndrome of trephined” (10) and mental syndrome(s). However, it is not clear whether the procedure can protect patients from cerebral seizures or whether it results in electroencephalographic (EEG) changes. Relatively few modern-day large clinical series have addressed the relationship between epileptic syndrome (ES) and cranioplasty after DC (11-14). In the current
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study, our goal was to provide a review addressing the value of EEG in predicting ES in patients undergoing DC and subsequent cranioplasty.
Methods Study design A prospective study of patients who underwent cranioplasty after DC from October 2016 to October 2017 at the Neurosurgery Department of the Cristo Redentor Hospital – Conceição Hospital Group – Porto Alegre/RS, Brazil, was performed.
Eligibility All patients underwent clinical and neurological examination, laboratory evaluation, computed tomography (CT), and routine EEG before and after cranioplasty. The inclusion criteria were as follows: surgery at the authors’ service due to trauma or stroke mechanisms and who underwent DC; clinical and neurological status, assessed using the Glasgow Coma Scale (GCS), and radiological status; available EEG data; and minimum 6 months follow-up to establish ES. The minimum diameter for DC was 12 cm to enable a potential gain in cranial volume. Patients in whom DC did not have the minimum diameter, individuals without EEG or medical records, and those lost to follow-up were excluded.
Surgical technique Surgery was performed using methyl-methacrylate (MM), a non-metal allograft that is the most extensively used cranioplasty material (15,16). Animal experiments have revealed that acrylic adheres to the dura mater with no reaction to underlying layers (15). Before the use of MM, the scalp adherent to the dura is gently removed and clean
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bone borders are achieved. MM is then formed with the appropriate curvature. After installation, the MM is washed with cool water to prevent heat damage to the adjacent brain tissue. After this step, the MM is placed in a cup filled with physiological serum to finish cooling and hardening. The material is fixed to the bone using miniplates. Once again, proper cooling is achieved using water.
Variables analyzed The variables analyzed included age, sex, mechanism of injury (trauma or stroke), neurological presentation (e.g., ES) before and after cranioplasty, location of the primary injury, and type of intracranial injury. Preoperative and postoperative electrocortical status was reported using EEG. Before cranioplasty, the EEG needles were placed only in the area where there is bone, outside the scalp flap, to avoid contamination from noise sources such as muscles (temporal, facial and eye) activities. Pre- and postoperative EEGs were stratified according to the following categories: normal; pseudo-normal (low voltage slow, fenda, and brecha); focal lesional (delta, theta, and interhemispheric asymmetry); and epileptogenic paroxysms (focal epileptogenic, generalized epileptogenic, and ictal activity). From these categories, patients were allocated into groups. ES was established according to the International League Against Epilepsy (17), in which epilepsy is defined as at least two unprovoked seizures > 24 h apart and can be considered to be present after one unprovoked seizure in individuals with other factors that are associated with a high likelihood of a persistently lowered seizure threshold and, therefore, a high risk for recurrence. Such risk should be equivalent to the recurrence risk of a third seizure in those with two unprovoked seizures (i.e., at least 60%). The latter risk level is associated with remote structural lesions, such as stroke, central nervous system infection, certain types of
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traumatic brain injury (TBI), diagnosis of a specific ES or, in some circumstances, the presence of other risk factors.
Statistical analysis Numerical results are expressed as mean and standard deviation (SD), median and 25th and 75th percentile, or minimal and maximal values. Categorical results are expressed as absolute and relative frequencies. Associations were assessed using chi-squared, equal proportion, and McNemar tests for paired proportions. Post-hoc analyses were performed using the Bonferroni test, and relative risk (RR) was calculated when necessary. Differences with p < 0.05 were considered to be statistically significant.
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Results Baseline characteristics During the period from October 2016 to October 2017, 52 patients who underwent DC evaluated by the Neurosurgical Service and underwent cranioplasty were eligible for the study. Patient demographic data and surgical indications are summarized in Table A. The mean (± SD) age of the patients was 32 ± 12.8 years, and 50% were between 20 and 39 years of age. The predominant sex was male (n = 41 [78.9%]). Patients with hypertension constituted 19.2% (n = 10) of the sample, while those with diabetes mellitus (DM) constituted 5.8% (n = 3). The proportion of smokers was 25% (n = 13), and no patient had ES. The most common indication for DC was TBI (n = 43 [82.7%]), followed by stroke (n = 9 [17.3%]). Mechanisms of trauma included: motorcycle accidents (n = 12 [23.1%]), gunshot wounds (n = 11 [21.1%]), fall accidents (n = 6 [11.5%]), altercations (n = 5 [9.6%]), motor vehicle accidents (n = 4 [7.7%]), and other causes (n = 5 [9.6%]). Considering stroke mechanisms, ischemic stroke was the most prevalent (n = 5 [9.6%]), followed by hemorrhage (n = 2 [3.8%]), and aneurysmal SAH (n = 2 [3.8%]). Neurological assessment before DC revealed 21 (40.4%) patients with a GCS score of 9–15, 22 (42.3%) with a GCS score of 6–8, and 9 (17.3%) with a GCS score of 3–5. Unilateral frontotemporoparietal hemicraniectomy was performed in 44 (84.6%) patients (40.4% right, 44.2% left) and 8 (15.4%) underwent bifrontal craniectomy at initial surgery. Most patients presented with normal EEG post-DC and post-cranioplasty.
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CT findings Individual CT scan features included 86.5% (n = 45) of patients with cortical lesions, 57.7% (n = 30) traumatic SAH, 40.4% (n = 21) subdural hemorrhage, 15.4% (n = 8) extradural hemorrhage, 15.4% (n=8) intraparenchymal hemorrhage, and 7.7% (n = 4) intraventricular hemorrhage. A midline shift > 5 mm was observed in 38 (73.1%) cases.
EEG study An EEG study was performed within 6 months before and after cranial repair. Precranioplasty EEG was normal in 19 (36.5%) patients and post-cranioplasty in 27 (51.9%).
Features of post-DC seizures Patients were followed-up for a mean of 6 months after the first surgery (i.e., DC) until the second surgery (i.e., cranioplasty), and evaluated for the presence of ES, which was detected in 14 (26.9%) patients, of whom 7 (50%) exhibited normal EEG, 6 (42.9%) pathological, and 1 (7.1%) pseudo-normal. None of the patients progressed to status epilepticus. The majority of seizures were focal impaired awareness seizures (complex partial seizure) (n = 6 [42.9%]), followed by bilateral tonic-clonic (n = 5 [35.7%]) and mixed (n = 3 [21.4%]) seizures. After acute seizure attack, all patients (n = 14) were treated with intravenous phenytoin as first-line medication, followed by oral antiepileptic drugs. Statistical analysis did not reveal significant inter-group differences with regard to clinical parameters (age, DM, hypertension, and smoking), or between seizure types and EEG post-DC, probably due to the small number of cases.
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Patients who developed ES after DC (n = 14) were affected in the left (n = 7), right (n = 6), and bifrontal (n = 1) sides. This fact did not reveal differences between the groups according to the development of ES (pre-cranioplasty) (p = 0.4), except for the correlation between bifrontal DC and posterior EEG normal (p = 0.013). Virtually all patients who presented with ES exhibited cortical lesions (n = 13 [92.9%]). Although cortical lesions were not correlated with pathological EEG changes (p = 0.43), the RR for the development of ES in patients with cortical lesions was higher than in those without (RR 2.02). Only one patient whose primary pathology was extradural hematoma (EDH) (n = 8 [15.4%]) exhibited ES. Compared with other primary pathologies, EDH was associated with a lower risk for ES (RR 0.4231); however, there was no difference between EDH and other pathologies according to EEG changes (p = 0.25). Patients with the worst GCS scores (i.e., 3–8) represented 57.1% (n = 8) of all those who followed with seizures. These associations, however, did not represent significant inter-group differences.
Features of post-cranioplasty seizures All patients underwent cranioplasty exclusively with MM, except one, in whom autologous bone partially used with MM association. The MM was modeled and placed at the skull defect (Fig A). Patients were followed up for a mean of 6 months after cranioplasty and evaluated for the presence of ES, which was detected in 11 (21.2%), among whom 54.5% (n = 6) developed impaired awareness seizures (complex partial seizure), followed by bilateral tonic-clonic seizures (n = 3 [27.3%]), and mixed seizures (n = 2 [18.2%]). None of the patients progressed to status epilepticus. After seizure attack, 3 were treated with
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phenytoin, 2 with phenobarbital, 2 with carbamazepine, 1 with valproic acid, 2 with phenytoin plus phenobarbital, and 1 with phenytoin and carbamazepine.
Features of pre- and post-cranioplasty ES Analyzing patients with pre-cranioplasty ES (n = 14 [26.9%]), 3 (21.4%) presented the syndrome post-cranioplasty; however, this reduction did not indicate that cranioplasty reduced the risk for ES (p = 0.65). Similarly, considering patients who followed the syndrome post-cranioplasty (n = 11 [21.2%]), 3 (27.3%) had the syndrome precranioplasty, and the association was also not significant. Considering patients with the syndrome post-cranioplasty, only 1 presented immediately after the procedure, while the others presented at 6 months after the procedure, and the association was not significant. The time-relationship between clinical seizure events and EEG, was variable, within 6 months before and after cranial repair.
Features of pre- and post-cranioplasty EEG The proportion of patients with normal EEG increased after cranioplasty, from 36% precranioplasty to 52% post-cranioplasty. Those who exhibited normal EEG precranioplasty (n = 19 [36.5%]), followed post-cranioplasty with normal EEG in 14 (73.7%) cases, pseudo-normal in 3 (15.8%), and pathological in 2 (10.5%). Patients who presented with pathological EEG pre-cranioplasty (n = 18 [34.6%]), followed postcranioplasty with less pathological EEG (n = 9 [50%]), increasing normal (n = 7 [38.9%]) , and pseudo-normal (n = 2 [11.1%]) EEG cases. Of these 18 patients, all who manifested with epileptogenic paroxysms (n = 4 [22.2%]) followed post-cranioplasty without this worst of EEG alterations (Table B).
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Features of ES correlated with EEG Patients who manifested ES post-cranioplasty (n = 11 [21.2%]), previously presented with normal and pathological EEG in 5 (45.5%) cases each, and pseudo-normal in 1 (9.1%) case. Post-cranioplasty, they followed normal EEG in 7 (63.6%) cases, pathological in 3 (27.3%), and pseudo-normal in 1 (9.1%) . Patients who presented improvement in their EEG after cranioplasty (n = 16 [30.8%]) did not exhibit improvement in their clinical seizure status because most of them followed without changes (n = 10 [62.5%]), 25% (n = 4) worsened, and only 2 (12.5%) stopped seizures. Similarly, patients who exhibited deterioration in EEG changes after cranioplasty did not follow the worst ES (Table C).
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Discussion Seizure(s) is a well-known potential sequela of TBI and malignant middle cerebral artery (MCA) infarcts after DC (18-22). In our case series, 26.9% of patients presented with seizures post-DC. Creutzfeldt (23) reported that 49% of patients developed seizures after DC for malignant MCA. For the same reason, Santamarina (24) observed seizures in 47.5% of all patients and in 53.7% of survivors, while Brondani (25) reported a prevalence of 61%. In the two randomized controlled multicenter trials of DC after malignant MCA stroke that were conducted, Decompressive Surgery for the Treatment of Malignant Infarction of the MCA (DESTINY) (26) and Hemicraniectomy after MCA infarction with life-threatening edema trial (HAMLET) (27), did not report risk factors for seizures. In the case of TBI, Ban et al. (28) reported that only approximately 3% developed seizures despite the use of anticonvulsants. Seizures disappeared in all patients after increasing the dosage or after adding other antiepileptic drugs, which is a reasonable approach to follow in the first 2 weeks post-injury. Considering each type of TBI, the incidence of ES in acute subdural hematoma (aSDH) has been reported to be approximately 22% and less in chronic subdural hematoma and EDH 10% (29,30). As a pathophysiological mechanism for the high epileptogenicity of an aSDH, it has been postulated that the hematoma itself irritates the cortical surface with blood compounds and, later, with its degradation products (31). The decomposition of hemoglobin on the cortical surface is highly epileptogenic (32,33). Thus, blood evacuation through craniotomy or craniectomy may reduce the risk for ES; however, intracranial surgery was found to be an independent predictor of ES (34,35,36).
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Englander (35) speculated that the correlation between surgery and ES may be explained by sudden decompression through craniotomy, which may cause an additional
intraparenchymal
injury
through
a
sudden
negative
deceleration.
Consequently, this may promote neuronal damage and lead to the creation of an epileptogenic focus (37). On the other hand, the high incidence of ES after craniotomy may also be explained by the simple fact that the craniotomy itself is a surrogate marker of the severity of a brain injury, which accompanies structural parenchymal damage, and known to be epileptogenic. Suggested mechanisms of postoperative epilepsy in patients who have undergone DC include graded increases in hyperexcitability and a reduced epileptogenic threshold (28,38). Identifying the key risk factors predisposing to seizures and their effect on clinical outcomes requires further prospective studies. In our series, we found a statistically significant correlation between the development of ES in patients with cortical lesions, which higher than in those without it. This correlation is consistent with the supposed physiopathology described above in TBI, which also explains the low presence of ES in patients with EDH, a pathology that usually tends to not cause additional intraparenchymal injury. Although the frequency of post-traumatic seizures for all types of head injuries varies, the literature agrees that increased severity of TBI appears to lead to an increased risk for seizures (30,39,40). Most of our patients who developed seizures after DC presented with the worst initial GCS score. Patients with preoperative seizure disorders are more likely to exhibit postcranioplasty seizure (41). In our study, ES can either be attributed to seizures arising after initial TBI or cranioplasty. The overall rate of post-cranioplasty ES in our study was 21.2% (n = 11), and was highest compared with other large studies that have reported the rate to be as high as 14.37%–14.81% (42,43). These studies found that TBI
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was significantly correlated with seizures, although cranioplasty has often been investigated for the treatment of stroke and tumors. On the other hand, the relatively high incidence may be due to the inclusion of patients who experienced seizures before cranioplasty, as well as studies by Zhang (44) (35.7%) and Shih (45) (30.3%), whereas other studies have excluded these patients. As a treatment of choice for post-traumatic seizures, early cranioplasty has been emphasized by many authors. The timing of cranioplasty after DC is a controversial topic in the literature. For example, Shih (45) reported that longer timing between DC and cranioplasty was an independent risk factor for postprocedural seizures. On the other hand, an earlier systematic review and meta-analysis by Yao (46) reported that early cranioplasty leads to more post-cranioplasty seizures than late cranioplasty. In our study, all patients underwent cranioplasty 6 months after DC, which can be considered early. However, no further analysis could be performed, especially because there was no control group. Regardless of the time after DC, in 1939, Grant (47) reported a decrease in the incidence and even complete disappearance of epileptic fits in 18 of 27 (67%) patients in whom cranioplasty was performed. Several other authors have reported similar findings, although mostly in studies with smaller numbers of patients (47-52). The improvements observed after cranioplasty were attributed to the removal of adhesions between the skin and the dura (53). However, this removal of adhesions can lead to a conflict: Why are some of these patients more vulnerable to early ES, mostly immediately, on the same day of cranioplasty? This is an important question that remains theoretically explained. We know that after cranioplasty, the post-traumatic contusion healing process can lead to scar formation. Alternatively, exposure of the temporalis muscle during cranioplasty may also cause scarring. This physical traction of
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the tissue at the original surgical site during scar formation causes abnormal electrical discharges, thus inducing early seizures. Seizures are believed to be triggered by surgical manipulation of the brain during cranial reconstruction, increasing its epileptogenic susceptibility and probably altering other factors in cerebrospinal fluid dynamics (54). Another consideration is that revascularization is observed between the autologous fascia and the cerebral cortex after DC, resulting in traction with subsequent cortical insult, which subsequently induces early seizures. Moreover, patients who postpone cranioplasty are more likely to experience immediate and early seizures rather than late seizures (41). Cerebral scars more easily induce abnormal electrical discharge after extended postponement of cranioplasty. In late-onset seizures, patients experiencing postoperative stress may be susceptible to a cascade of events. Free radical production and release, with peroxidation and cell death may result in damage to the cortex and the formation of epileptogenic foci (41). Should we use anticonvulsants routinely before a cranioplasty? Prevention of seizures using antiepileptic therapy before
cranial
reconstruction
remains
controversial.
However,
perioperative
prophylactic antiepileptic therapy should be carefully considered only in patients with a documented history of epilepsy (55). To decrease the risk for seizures after cranial reconstruction, it is recommended to avoid or reduce the manipulation of the dura mater as much as possible when preparing the skull edges of the cranial defect, also ensuring to not compress the brain by forcing placement of the prosthesis. Controversial views regarding the benefit of cranial repair in post-traumatic epilepsy, however, appeared later, especially after World War II (56). In reviewing postoperative course in a comparatively large population of patients, Erculei and Walker (57) found no conclusive evidence that cranial repair exerts a determining influence on post-traumatic epilepsy. Such doubts were also raised by other authors arguing that
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nearly always only cranial defects are repaired while the brain cicatrice and the adhesions between the dura and the brain surface remain (12,56). Despite the fact that patients experience a reduced incidence of seizures, the reason for this was assumed to be another independent factor. Along this line, repair surgery appeared to be justified only if cortical “epilepsy resection” could be performed (12,57). This pathophysiology may explain why patients in our study did not exhibit a statistically significant reduction in seizures after cranioplasty because our patients were not subjected to cortical resection. The fact that skull defects have a large effect on EEG has been known since the inception of EEG (58). Cobb et al. (59) used the phrase “breach rhythm” (BR) for the mu-like activity that can arise close to skull holes; they also reported an enhancement of the amplitude of alpha and frontal fast rhythms ‘over or near unilateral posterior and frontal defects, respectively’”. By itself, this is not indicative of brain dysfunction and may be considered to be an expected physiological consequence of a skull defect, unless associated with spikes or focal slowing. Differentiating between BR and epileptiform abnormalities occurring in the same area may be challenging because sharpening and irregular morphology of BR may lead to misinterpretations. In the presence of BR, it is advisable to adopt a “conservative” reading, having a high threshold for calling epileptiform abnormalities to avoid a misdiagnosis of epilepsy due to an overinterpretation of non-epileptic sharp patterns. In our data, none of the patients presented seizures before the first procedure and then, after DC, some of them followed with seizures and only 36.5% (n = 19) presented with normal EEG. Attention was devoted to not classifying irregular morphologies as epileptiform abnormalities. Aside from the classification “normal”, we described pseudo-normal, focal lesional, and epileptogenic paroxysms.
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EEG changes are not uniform across individuals due to differences in the severity of head injuries. Some individuals exhibit a clinically normal EEG as early as 15 min after sustaining a concussion (60). Immediately after TBI, epileptiform activity (high amplitude sharp waves or high frequency discharges), followed by diffuse suppression of cortical activity typically lasting 1–2 min, followed by diffuse slowing of the EEG, which returns to normal baseline within 10 min to 1 h (61-63). Weeks to months after TBI, there is a 1–2 Hz increase in the frequency of the posterior alpha rhythm, which has been explained as a return to the original baseline from post-traumatic slowing (64,65). The majority of the acute EEG abnormalities described above resolve by 3 months, and 90% resolve within 1 year of head trauma (65). Another study in which EEG examinations were performed before and after cranioplasty in 20 patients with cranial defects > 100 cm2 found that in 12 patients, pathological EEG recordings were not accompanied by overt epileptic fits. In 5 of 10 patients with craniocerebral injuries, EEG improved and 2 of 10 deteriorated (66), demonstrating better EEG improvement, although in a very small number of patients. Spencer (67) suggested that MM plates would be almost as resistant to EEG as a skull structure of the same thickness, and regarded the presence of epilepsy as one indication for cranioplasty. Reduction of pseudo normal abnormalities, pathological findings, and epileptogenic paroxysms were observed in our study after cranioplasty. Serial observation of EEG did not demonstrate evidence of a reversible mechanism in clinical seizure manifestation, or of the favorable effects of correction of deformities using cranioplasty. Using our method, electroencephalography cannot be used to predict clinical improvement.
Strengths and limitations of the study
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Strengths of the present study included the capacity to perform follow-up and the external applicability of the results. One particular limitation, however, the small number of patients. Another implication is that our patients may have had EEG alterations previous to DC. However, this fact is exceedingly difficult to reconcile because our study focused on patients who experienced an incidental event (i.e., TBI, malignant MCA infarcts). The current trend is to understand the specificity of each EEG alteration before and after cranioplasty to establish whether one could predict posterior seizures. Our study group is poised to start a prospective and multicenter study to evaluate patients who underwent cranioplasty to accurately predict seizures over time.
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Conclusion In routine clinical practice, altered amplitudes were observed in the region of bone defects and cranioplasty can reduce pathological EEG (epileptogenic paroxysms), but is not able to produce new EEG tracings that can predict change(s) in seizure discharge and cannot reduce ES.
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Appendices Figure A - (1) Patient and cranial CT before performing cranioplasty; (2) after cranioplasty
Table A - Characteristics of patients who underwent cranioplasty Table B - Changes in each EEG abnormally following cranioplasty Table C - EEG and seizure changes following cranioplasty
Acknowledgements The authors would like to thanks all staffs and professors of the Department of Neurosurgery of the Cristo Redentor Hospital for the encouragement to develop this important research. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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27
Variable Age at operation, y Median > 50 ≤50 Sex Male Female Smoking Diabetes Mellitus Hypertension Location Right Left Bifrontal GCS at decompressive craniectomy 3-5 6-8 9-15 Indication for DC TBI Stroke
No
%
32 5 47
9.6% 90.4%
41 11 13 3 10
78.9 21.1 25 5.8 19.2
21 23 8
40.4 44.2 15.4
9 22 21
17.3 42.3 40.4
43 9
82.7 17.3
Preoperative abnormality
Post cranioplasty (number of patients) Improved No Changes Deteriorated
Pseudonormal Low voltage slow (n=8) Fenda (n=6) Brecha (n=1)
2 3 0
4 2 1
2 1 0
1 2 4
0 1 3
0 2 1
4 0 0
0 0 0
0 0 0
Focal lesional Theta (n=1) Delta (n=5) Interhemispheric asymmetry (8)
Epileptogenic paroxysms Focal epileptogenic (n=4) Generalized epileptogenic (n=0) Ictal activity (n=0)
EEG changes following cranioplasty Improved (n=16) No changes (n=25) Deteriorated (n=11)
Seizures (number of patients) Stoped No changes Deteriorated 2 10 4 6 16 3 3 7 1
p Value 0.66 0.81 0.072
Abbreviations List aSDH – Acute Subdural Hematoma BR – Breach Rhythm CI – Confidence Interval CT - Computed Tomography DC – Decompressive Craniectomy DM – Diabetes Mellitus EDH - Extradural Hematoma EEG – Electroencephalography ES – Epileptic Syndrome GCS – Glasgow Coma Scale GW - Gunshot Wounds MCA – Middle Cerebral Artery MM – Methyl-Methacrilate N - Number of cases RR - Relative Risk SAH - Aneurysmal Subarachnoid Hemorrhage SD – Standard Deviation TBI - Traumatic Brain Injury
Leandro Pelegrini de Almeida, MD, corresponding author
Disclosure-Conflict of Interest
The authors have no conflicts or disclosures to identify, and ethical standards have been utilized during the preparation of this manuscript. We also have no financial disclosures to identify.
Leandro Pelegrini de Almeida, MD, corresponding author
Credit Author Statement
Leandro Pelegrini de Almeida - Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Project administration; Resources; Software; Validation; Visualization; Roles/Writing - original draft; Writing - review & editing.
Mateus Carvalho Casarin - Investigation; Methodology; Software; Visualization; Roles/Writing - original draft.
Humberto Luiz Mosser - Investigation; Methodology; Software; Validation; Visualization.
Paulo Valdeci Worm - Conceptualization; Data curation; Methodology; Project administration; Resources; Supervision; Roles/Writing - original draft; Writing - review & editing.
Leandro Pelegrini de Almeida, MD, corresponding author