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CLINICAL ARTICLE J Neurosurg 130:1203–1209, 2019

Seizure incidence in the acute postneurosurgical period diagnosed using continuous electroencephalography

Brin Freund, MD, John C. Probasco, MD, and Eva K. Ritzl, MD

Department of , Johns Hopkins Hospital, Baltimore, Maryland

OBJECTIVE Delay in diagnosis and subsequent treatment of nonconvulsive can lead to worsened outcomes. The gold standard in detecting nonconvulsive seizures is continuous video-electroencephalography (cEEG). Compared to routine, 30-minute EEG, the use of cEEG increases the likelihood of capturing intermittent nonconvulsive seizures. Studies of critically ill patients in intensive care units demonstrate a particularly high rate of nonconvulsive seizures. Some of these studies included postneurosurgical patients, but often subanalyses of specific populations were not done. In particular, few studies have specifically evaluated postneurosurgical patients by using cEEG in the acute postoperative setting. Therefore, the incidence and predictors of acute postneurosurgical seizures are unclear. METHODS In this study, the authors focused on patients who were admitted to the neurological critical care unit follow- ing and who underwent cEEG within 72 hours of surgery. RESULTS A total of 105 cEEG studies were performed in 102 patients. Twenty-nine patients demonstrated electro- graphic (subclinical) seizures, of whom 10 had clinical seizures clearly documented either before or during cEEG moni- toring. Twenty-two patients had subclinical seizures only detected on cEEG, 19 of whom did not have clinical activity at any point during hospitalization. Those with seizures were more likely to have had a history of (p = 0.006). The EEG studies of patients with seizures were more likely to show lateralized periodic discharges (p = 0.012) and lateralized rhythmic delta activity (p = 0.012). The underlying neuropathological disorders most associated with sei- zure risk were lobar tumor on presentation (p = 0.048), subdural hematoma (SDH) requiring for evacuation (p = 0.002), (SAH) (p = 0.026), and perioperative SAH (p = 0.019). In those undergoing cra- niotomy, the presence of SDH (p = 0.032), particularly if requiring evacuation (p = 0.003), increased the risk of seizures. In those without preoperative intracranial bleeding, perioperative SAH after craniotomy was associated with a higher incidence of seizures (p = 0.014). There was an additive effect on seizure incidence when perioperative SAH as well as concomitant intraparenchymal hemorrhage and/or were present. The clinical examination of the patient, including the presence or absence of altered mental status and the presence or absence of repetitive movements, was not predic- tive of subclinical seizures. CONCLUSIONS In postneurosurgical patients referred for cEEG monitoring, there is a high rate of both clinical and subclinical seizures in the early postoperative period. Seizures are particularly common in patients with SDH or lobar tumor and perioperative SAH. There was an additive effect on seizure incidence when more extensive injury was present. As expected, those with a history of epilepsy also demonstrated higher seizure rates. Further studies are needed to evaluate the time period of maximum seizure incidence after surgery, and the effects acute postneurosurgical seizures have on long-term outcomes. https://thejns.org/doi/abs/10.3171/2018.1.JNS171466 KEYWORDS continuous electroencephalography; neurosurgery; seizure; ; craniotomy; epilepsy

ontinuous video-electroencephalography (cEEG) up to 35% of patients.8,18,34 Typically, these studies listed monitoring is an important tool to evaluate acute the underlying conditions that were associated with sei- alteration of mental state in critically ill patients for zures, but they did not specifically analyze different sub- possibleC nonconvulsive seizures or nonconvulsive status groups. epilepticus.45,51 In the neurological critical care unit, stud- The association of postneurosurgical seizures with ies using cEEG have demonstrated subclinical seizures in worsened outcomes has been described previously, and

ABBREVIATIONS cEEG = continuous video-electroencephalography; GCS = Glasgow Scale; ICH = intracranial hemorrhage; LPD = lateralized periodic discharge; LRDA = lateralized rhythmic delta activity; SAH = subarachnoid hemorrhage; SDH = subdural hematoma. SUBMITTED June 15, 2017. ACCEPTED January 10, 2018. INCLUDE WHEN CITING Published online June 1, 2018; DOI: 10.3171/2018.1.JNS171466.

©AANS 2019, except where prohibited by US copyright law J Neurosurg Volume 130 • April 2019 1203

Unauthenticated | Downloaded 09/26/21 04:06 PM UTC B. Freund et al. seizures in this setting require prompt diagnosis and treat- occurring at nearly regular intervals and without evolution ment.6,16,​21,37 Importantly though, the incidence of postneu- into seizures (evolution in frequency or spread to adjacent rosurgical seizures may be greatest in the acute postoper- regions). Subclinical seizures were defined as events con- ative period.47 In those undergoing craniotomy, the acute sisting of rhythmic spiking showing intrinsic evolution, period is thought to be within 48–72 hours of surgery.42,43 often but not necessarily with a defined onset and reso- Although some studies have focused on the acute phase lution. Seizures were considered clinical if recorded as after surgery,2,3,9,​ 11,12,19,22–24,28,29,31,35,37–39,50​ they did not use facial or extremity “rhythmic movements,” “twitching,” cEEG monitoring, similar to others in which postneuro- “jerking,” or “tonic activity,” and intermittent or acute surgical seizures were studied in the subacute to chronic “gaze deviation” or “head turning,” “grand mal” or “gen- postoperative period.1,4,5,​ 15,​ 20,25,30,33,41,52​ cEEG is particularly eralized tonic-clonic” activity. If clinical seizure activity vital in patients who undergo anesthetic or sedative treat- was not well described, or if it was only mentioned when ment that can mask the neurological examination find- listed as the reason for ordering cEEG, it was not counted ings,22 and make abnormal, nonseizure-related rhythmic in the overall clinical seizure incidence. We recorded the movements difficult to differentiate from clinical seizures. presence of a clinical seizure correlate, as noted above, Although some studies evaluating seizures in neurosurgi- when electrographic (subclinical) seizures were detected cal patients did use cEEG,7,10,18,26,40,45,46,48 they were narrow on cEEG. in their focus, did not differentiate the acute time period, Statistical analyses were performed using SPSS, ver- included a small cohort, or omitted significant details re- sion 22 (IBM Corp.). Continuous data were analyzed us- garding the type of surgery or underlying neuropathology. ing the Mann-Whitney U-test, and categorical data were Therefore, further analysis of this subgroup of patients analyzed using Fisher’s exact t-test. All tests were 2-sided, with respect to seizure incidence is needed. and p < 0.05 was considered statistically significant. Post In this study we analyzed cEEG performed in the acute hoc Bonferroni testing was performed given the number postneurosurgical period, primarily after intracranial pro- of variables compared between groups regarding clinical cedures. Our goal was to better describe the incidence of features and EEG findings, with significance corrections seizures—including nonconvulsive seizures and noncon- to p < 0.005 for neuropathology, procedures, clinical ex- vulsive status epilepticus—in this population and to define amination, and EEG findings. We also performed linear those at most risk, to guide further study and use of cEEG regression for collinearity on data from those who under- in these patients. went a craniotomy or craniectomy with p values < 0.15, and also included demographic information (age, sex). We Methods then performed a logistic regression analysis to create a model predicting the likelihood of seizures. Our study design was approved by the institutional review board at Johns Hopkins University. We retrospec- tively identified patients consecutively admitted to the Results neurological critical care unit at the Johns Hopkins Hospi- Overall, 105 cEEG sessions were performed in 102 pa- tal between January 1, 2013, and December 31, 2015, who tients. Three patients had 2 cEEG recordings begun within underwent neurosurgery and were subsequently moni- the first 72 hours after surgery, 1 of whom had seizures de- tored using cEEG within 72 hours of the surgical proce- tected only on the second cEEG. All but 7 cEEG sessions dure, with concern for seizures. All patients were 18 years were recorded for at least 12 hours, the briefest being 4 of age or older. Patients with any neurosurgical procedure hours because the patient went for a procedure and needed were included. to be disconnected. This being a retrospective study, the Demographics and clinical data were obtained by cEEG recordings were ended at the discretion of the clini- detailed chart review, including medical history, labora- cian taking care of the patient at the time. However, none tory studies, medications, and imaging interpretations of those recorded for less than 12 hours demonstrated sei- by board-certified radiologists. Perioperative subarach- zure activity on cEEG, nor were they referred for a second noid hemorrhage (SAH) was defined by the presence of cEEG or described as having clinical seizures later in their subarachnoid blood products or hemorrhage noted in the hospitalization. radiologist’s interpretation on either CT or MRI studies. Thirty (29.4%) patients had either clinical or subclini- (GCS) score was calculated based cal seizures; 29 of these patients demonstrated electro- on the documented examination. Scalp EEG recordings graphic seizures during cEEG monitoring, with 15 diag- were performed using placed in accordance nosed as status epilepticus. One patient had a generalized with the 10–20 international system (Nihon Kohden sys- tonic-clonic seizure that was well documented prior to tem; Nihon Kohden Corp.). cEEG interpretations were cEEG, without any electrographic seizures detected while performed by expert encephalographers as part of clini- monitored. No other patient had well-documented clini- cal care. These reports were retrieved from the medical cal seizures without EEG correlation of epileptic activity. record system and, if seizures or status epilepticus were 22 (21.6%) patients had subclinical electrographic seizures noted, the EEG study was re-reviewed by an expert en- on cEEG, and 19 of these patients had no reported clini- cephalographer (E.K.R.) to confirm these findings and the cal motor seizures in the postoperative period, with their timing of onset in the recording. only clinical correlate being depressed mental state or un- Periodic discharges detected on cEEG were defined as responsiveness. repetitive sharp waves, spikes, or sharply contoured waves Table 1 describes demographic data and timing of

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TABLE 1. Demographic data and timing of cEEG TABLE 2. Seizure incidence and neuropathology or procedure Characteristic Szs No Szs p Value Szs in Szs in the Those w/ Rest of the p Age in yrs, mean 61.6 59.7 0.610 Neuropathology or History Variable Cohort Value Sex 10 M, 20 F 38 M, 37 F 0.131 Length of time on cEEG, mean 104.1 25.2 <0.001 History of Szs 12/22 18/83 0.006 hrs Lobar ICH 7/17 23/88 0.245 Time after op at which cEEG 35.3 (6–72) 32.5 (5–72) 0.749 Lobar tumor 12/27 18/78 0.048 was begun, mean hrs (range) Herniation (uncal or subfalcine) 1/7 29/98 0.670 Time to onset of Szs after 2.8 NA Midline shift 7/20 23/85 0.583 cEEG was begun, mean hrs Lobar stroke 12/27 21/78 0.622 NA = not applicable; Szs = seizures. SDH 10/20 20/85 0.056 SAH 14/63 16/42 0.026 SAH on presentation 4/14 26/91 >0.999 cEEG. Only 1 patient’s first seizure was detected more IVH 10/29 20/76 0.339 than 24 hours (52 hours) after cEEG was begun, and 26/29 Hydrocephalus 7/22 23/83 0.792 with electrographic seizures had seizures recorded within Periop SAH 13/28 17/77 0.019 the first hour. Periop SDH 2/8 28/97 >0.999 Data regarding history of seizures, underlying neuro- , surgical procedure, and associated incidence of Periop IVH 5/15 25/90 0.536 seizures are described in Table 2. A majority of patients Procedure (79) underwent craniotomy or craniectomy, of which 4 Aneurysm coiling 3/8 27/97 0.686 were suboccipital craniectomies and the rest were supra- Aneurysm clipping 5/25 25/80 0.321 tentorial surgeries. Other procedures included angiogra- Tumor resection (craniotomy or 12/35 18/70 0.369 phy, extraventricular drain placement, and placement of endoscopy) burr holes. In those undergoing craniotomy or craniecto- Craniotomy for SDH evacuation 8/11 22/94 0.002 my, when excluding those with preoperative intracranial bleeding on CT or MRI, perioperative SAH was a risk IVC or EVD 6/20 24/85 >0.999 factor for clinical and subclinical seizures (p = 0.014). Craniotomy or craniectomy 25/79 5/26 0.318 There was a trend toward a further increase in seizure risk EVD = extraventricular drain; IVC = intraventricular catheter; IVH = intraven- when perioperative SAH occurred concurrent with stroke tricular hemorrhage. and/or lobar intracranial hemorrhage (ICH); this can be concluded based on the fact that there was a nonsignifi- cant difference in seizure incidence when SAH patients Direct logistic regression performed using data from with coexisting stroke and/or ICH were excluded from the those in the craniotomy or craniectomy group produced subanalysis (p = 0.054). Other conditions that significantly a model containing the following factors: continuous increased the risk of seizure in those undergoing craniot- variables including GCS score and age; and categorical omy or craniectomy were a preexisting history of seizure variables including sex (0 = male, 1 = female); history of disorder (p = 0.004) and subdural hematoma (SDH) (p = seizures (0 = no, 1 = yes); lobar tumor (0 = no, 1 = yes); 0.032), particularly if requiring craniotomy for evacuation SAH (0 = no, 1 = yes); and craniotomy or craniectomy for (p = 0.003). SDH evacuation (0 = no, 1 = yes). The model was statisti- Indications for cEEG and neurological examination cally significant, with c2 = 34.23 (7 variables, n = 79; p < findings are noted in Table 3, which demonstrates that 0.001), indicating that it was able to distinguish between these factors had no association with the presence of elec- those with and without seizures. The model as a whole trographic seizures. explained between 35.2% and 49.3% of the variance in Table 4 lists EEG patterns other than seizures found in seizure incidence, and correctly classified 85% of cases. our patients. Of these the only EEG findings that predict- As shown in Table 5, 4/7 independent variables (history ed seizure incidence were lateralized periodic discharges of seizures, lobar tumor, SAH, and craniotomy for SDH (LPDs) (p = 0.012) and lateralized rhythmic delta activity evacuation) made a unique statistically significant contri- (LRDA) (p = 0.012). bution to the model. The strongest predictors of seizure With respect to outcomes, 4/30 patients with clinical or incidence were a history of seizures and undergoing a cra- subclinical seizures and 11/75 without seizures died prior niotomy for SDH evacuation. SAH and lobar tumor were to discharge (p > 0.05). There was no difference in mortal- moderately strong predictors of seizure incidence, where- ity at discharge between those who had status epilepticus as sex, age, and GCS score did not significantly factor into and the rest of the cohort (3/15 vs 12/90, p > 0.05) for all the model. surgical procedures taken together. In those undergoing craniotomy or craniectomy, mortality at discharge was greater in those with status epilepticus (p = 0.052). Long- Discussion term follow-up was not documented for the majority of Our study elucidates the incidence of early clinical patients. and subclinical seizures after neurosurgical procedures.

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TABLE 3. Indication for cEEG, clinical examination findings, and TABLE 4. EEG findings and seizure incidence seizure incidence Szs in Those Szs in the Rest p Szs in Those w/ Szs in the Finding w/ EEG Finding of the Cohort Value cEEG Indication Rest of the p Main background alpha 1/4 29/101 >0.999 Factor or Exam Finding Cohort Value Main background theta 4/11 26/94 0.506 Indication for cEEG Main background delta 3/9 27/96 0.713 Not following commands 1/7 29/98 0.670 Generalized slowing 21/73 9/32 >0.999 Clinical Sz 16/46 14/59 0.277 LPDs 7/11 23/94 0.012 Fluctuating mental state 1/12 29/93 0.101 BIPDs 1/5 29/100 >0.999 Intermittent or fluctuating 1/6 29/99 0.671 GPDs 1/3 29/102 >0.999 hemiparesis SIRPIDs 2/4 28/101 0.322 AMS or 12/46 18/59 0.678 LRDA 7/11 23/94 0.012 Clinical exam findings Reactive background 19/71 11/34 0.645 Aphasia 2/2 28/103 0.080 Comatose 10/26 20/79 0.218 BIPDs = bilateral independent periodic discharges; GPDs = generalized periodic discharges; SIRPIDs = stimulus-induced, rhythmic, periodic, or ictal Hemiplegia or hemiparesis 4/24 26/81 0.199 discharges. Gaze preference or devia- 1/9 29/96 0.441 tion Cranial nerve deficits 2/6 28/99 >0.999 the lack of increased seizure risk in those with SAH on Normal exam 1/4 29/101 >0.999 presentation. Other mechanisms suggested in the literature for early GCS score (mean) 9.2 10 0.145 postneurosurgical seizures after craniotomy or craniecto- 3–8 15/40 15/65 0.125 my are manipulation and traction of brain tissue; forma- 9–12 7/36 23/69 0.174 tion of edema; hematoma; and pneumocephalus—with 13–15 8/29 22/76 >0.999 subsequent brain injury due to ischemia or hypoxia. These mechanical changes can, in turn, lead to free-radical gen- AMS = altered mental status. eration, with an ensuing lack of cell membrane stabil- ity.13,23,27,32,36 All of these changes may contribute to the association of seizure incidence with the extent of brain In prior studies focusing on seizure incidence within the injury that we observed in our study. first 1–2 weeks after neurosurgery the incidence has been Those patients with lobar tumors who underwent resec- reported as ranging widely, from 1% to 42%, depending tion demonstrated a higher rate of postoperative seizures on the underlying neuropathology and surgical proce- when compared to the rest of the cohort in this study. Pa- dure.1–5,9,​ 11,​ 12,​ 19,​ 20,22–24,28–31,33,35,37–39,41,49,50,52​ Notably, however, tients with supratentorial brain tumors are known to have cEEG was not universally obtained. Some investigators an increased risk of seizure postcraniotomy.12,25 However, used brief EEG recordings in an attempt to correlate clini- studies have shown mixed results with respect to using cal signs with seizure activity, but most relied on clinical antiseizure drug prophylaxis perioperatively to prevent manifestations of seizures alone. We have shown that a seizures early after surgery.1,9,12,20,29,38,39,41,50,52 Furthermore, significant proportion of postneurosurgical patients re- most studies in those undergoing tumor resection focused ferred for EEG monitoring have subclinical seizures, and more on subacute or chronic seizure incidence. This study without cEEG most if not all of these seizures would have is unique in the characterization of seizure incidence eluded detection due to their intermittent nature. There- acutely after tumor resection using cEEG. fore, studies reporting the seizure incidence in the post- The presence of SDH as the indication for undergoing neurosurgical patient population as much below 30% may craniotomy was associated with increased risk of seizures underestimate this important surgical complication. following surgery in our study. A high rate of seizures fol- In our study, patients undergoing craniotomy who de- lowing acute SDH evacuation has been described, particu- veloped SAH as noted on after surgery had larly in patients who remain less responsive after sedatives a higher rate of seizures compared to the rest of the cohort, are wearing off.37 Interestingly, undergoing craniotomy including those with SAH on admission. This was par- for SDH evacuation was one of the largest contributors to ticularly true and statistically significant in the presence seizure risk in our model. of stroke or intraparenchymal blood products. In general, Not surprisingly, those with a prior seizure disorder SAH with or without surgical intervention is a risk fac- were very likely to have postoperative seizures. This has tor for seizures.10 Stroke after SAH due to vasospasm has been noted previously regarding postneurosurgical pa- been noted to increase this risk further, and vasospasm tients36 and others in critical care settings.8 This is consis- can occur up to 2 weeks after SAH.15 We monitored our tent with the strong influence a history of seizures had on patients for a relatively short period of time, and so those the likelihood of seizures in our model. presenting with SAH may have had seizures later in their Preoperative neurological deficits found on examina- course from subsequent vasospasm and parenchymal in- tion have been described as a risk factor for postneuro- jury not yet present in the study period. This may explain surgical seizures.23 We were unable to find a correlation

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TABLE 5. Logistic regression predicting likelihood of seizures in 95% of seizures are captured within the first 24 hours.8 In those undergoing craniotomy or craniectomy our study 90% of patients demonstrating seizures on cEEG 95% CI p had their first event within 24 hours of the start of cEEG Variable OR Lower Upper Value monitoring, and a significant proportion had their first seizure within the first hour. However, this may be con- Age 1.030 0.976 1.088 0.280 founded by the fact that monitoring was begun on average Sex 4.344 1.003 18.792 0.050 more than 30 hours after surgery. Therefore, it is unclear Lobar tumor* 5.538 1.206 25.426 0.030 at what point patients are most susceptible to the onset of History of Szs* 20.938 3.014 145.463 0.002 subclinical seizures postneurosurgery. It is quite possible that monitoring patients earlier after neurosurgery may GCS score 3–8 2.302 0.624 8.500 0.210 lead to improved outcomes. Our study is unable to assess Craniotomy for SDH* 25.550 3.330 196.029 0.002 this. Future studies are necessary to determine whether SAH* 7.187 1.584 32.624 0.010 earlier seizure monitoring and treatment is warranted. 14 * Significant contribution to model. Previous studies have noted LRDA and epileptiform activity or LPDs as predictive of seizure activity during prolonged monitoring in critically ill patients,40,46,48 where- between neurological examination or clinical seizure-like as generalized slowing forecasts lower seizure incidence.46 movements—occurring both during and before video-EEG Our results confirm these findings for our study popula- recording—and the incidence of seizures. The observation tion. that reported clinical seizure activity may not predict sub- Our model for predicting seizure incidence in those un- sequent detection of electrographic seizures on EEG has dergoing craniotomy or craniectomy who are referred for not been described previously. Yet, it highlights the fact cEEG due to concern for seizures showed very high speci- that attempting to diagnose seizures clinically and without ficity and high negative and positive predictive values. an EEG, particularly in critically ill postneurosurgical pa- Therefore, in patients with any of the 4 variables showing tients, is unreliable and potentially harmful. This may be significant contribution to the model, cEEG should not be especially true if the reliability of the clinical neurologi- delayed. In those undergoing craniotomy without these cal examination is confounded by the use of anesthetics in clinical factors present, liberal use of cEEG monitoring the operating room and postoperative sedatives to permit is still warranted. This model should be evaluated pro- ventilator support. The lack of EEG correlation with re- spectively in patients undergoing craniotomy acutely after ported seizure-like movements may also be muddled by surgery to validate its use. It is also important to keep in aggressive antiseizure treatment on an empirical basis in a the fact that the model was developed for a selected vulnerable patient population prior to EEG. patient population and may therefore not be applicable to In this cohort there was no association between early all postneurosurgical patients. postoperative seizures and by the time of discharge. Our study had certain limitations. We included only There was a trend toward an increased risk of death in those patients in whom cEEG was requested due to concern for who underwent craniotomy and subsequently developed seizures (based on poor mental status and/or abnormal acute-onset electrographic status epilepticus. Although movements), and we did not monitor all postoperative pa- most patients were not followed past discharge, it has been tients. We were also limited by the retrospective nature noted previously that the effects of postoperative seizures of our review of medical records, which described clini- may impact outcomes prior to discharge more than in the cal seizure activity, medical history, and examinations. It long term.36 Some have questioned the utility of aggres- should also be noted that for those patients we categorized sive antiseizure treatment in critically ill patients who de- as “without seizures,” seizures might simply have been velop seizures.44 The difficulty in determining outcomes missed if they occurred outside of the monitoring period. is that critical-care patients who develop seizures tend to Furthermore, we were unable to collect detailed long-term be sicker, and therefore worsened outcomes may be due to outcome data. Although our sample size is comparable to the underlying disease itself rather than being related to others in this field of study, larger-sized analyses could seizures. Based on this, aggressive antiseizure treatment yield additional information. may not provide much benefit, and it may prolong admis- sion and leave patients prone to complications of hospital- ization and intensive care.50,51 On the other hand, an inde- Conclusions pendent effect of seizures on outcomes in some critically In this study we found a high rate of seizures in the ill populations has been described.17 Whether or not acute acute postneurosurgical period, most of which were sub- postneurosurgical seizures independently contribute to an clinical and would have gone undetected without cEEG. unfavorable outcome has not been addressed specifically A history of seizures and the presence of SAH, periopera- and should be evaluated in future studies. tive SAH, undergoing craniotomy for SDH evacuation, or It is unclear how long cEEG monitoring should be per- the presence of lobar tumor heralded an increased risk of formed before the presence of subclinical seizures can be seizures when evaluating the cohort as a whole. Although ruled out with appropriate certainty, and it may depend on the surgical procedure itself did not predict the likelihood the population being evaluated. Studies have shown that in of seizures, the following variables were associated with comatose patients 87% of seizures are detected within the a higher incidence of seizures: those undergoing crani- first 48 hours of monitoring, and in noncomatose patients otomy, history of seizures, SAH, lobar tumor, and SDH

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Unauthenticated | Downloaded 09/26/21 04:06 PM UTC B. Freund et al. requiring evacuation. Nearly all of those who had seizures 14. Gaspard N, Manganas L, Rampal N, Petroff OA, Hirsch LJ: did not require more than 24 hours of monitoring to detect Similarity of lateralized rhythmic delta activity to periodic them, and seizures often occurred within the first hour. lateralized epileptiform discharges in critically ill patients. JAMA Neurol 70:1288–1295, 2013 However, cEEG monitoring was begun on average more 15. Hart Y, Sneade M, Birks J, Rischmiller J, Kerr R, Molyneux than 30 hours after surgery, and so seizure activity prior to A: Epilepsy after subarachnoid hemorrhage: the frequency cEEG monitoring may have gone undetected. No clinical of seizures after clip occlusion or coil embolization of a examination features were helpful in determining those at ruptured cerebral aneurysm: results from the International greater risk of seizures. 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32. Nishizawa Y: Glutamate release and neuronal damage in is- 46. Swisher CB, Shah D, Sinha SR, Husain AM: Baseline EEG chemia. Life Sci 69:369–381, 2001 pattern on continuous ICU EEG monitoring and incidence of 33. North JB, Penhall RK, Hanieh A, Frewin DB, Taylor WB: seizures. J Clin Neurophysiol 32:147–151, 2015 Phenytoin and postoperative epilepsy. A double-blind study. 47. Weiss N, Post KD: Avoidance of complications in neurosur- J Neurosurg 58:672–677, 1983 gery, in Winn HR (ed): Youmans Neurological Surgery, ed 34. Pandian JD, Cascino GD, So EL, Manno E, Fulgham JR: 6. Philadelphia: Elsevier, 2011 Digital video-electroencephalographic monitoring in the 48. Westover MB, Shafi MM, Bianchi MT, Moura LM, O’Rourke neurological-neurosurgical intensive care unit: clinical fea- D, Rosenthal ES, et al: The probability of seizures during tures and outcome. Arch Neurol 61:1090–1094, 2004 EEG monitoring in critically ill adults. Clin Neurophysiol 35. Pouratian N, Reames DL, Frysinger R, Elias WJ: Compre- 126:463–471, 2015 hensive analysis of risk factors for seizures after deep brain 49. Wong JM, Ziewacz JE, Ho AL, Panchmatia JR, Kim AH, stimulation surgery. Clinical article. J Neurosurg 115:310– Bader AM, et al: Patterns in neurosurgical adverse events: 315, 2011 open cerebrovascular neurosurgery. Neurosurg Focus 36. Pulman J, Greenhalgh J, Marson AG: Antiepileptic drugs as 33(5):E15, 2012 prophylaxis for post-craniotomy seizures. Cochrane Data- 50. Wu AS, Trinh VT, Suki D, Graham S, Forman A, Weinberg base Syst Rev (3):CD007286, 2015 JS, et al: A prospective randomized trial of perioperative 37. Rabinstein AA, Chung SY, Rudzinski LA, Lanzino G: Sei- seizure prophylaxis in patients with intraparenchymal brain zures after evacuation of subdural hematomas: incidence, risk tumors. J Neurosurg 118:873–883, 2013 factors, and functional impact. J Neurosurg 112:455–460, 51. Young GB, Jordan KG, Doig GS: An assessment of noncon- 2010 vulsive seizures in the intensive care unit using continuous 38. Rowe AS, Goodwin H, Brophy GM, Bushwitz J, Castle A, EEG monitoring: an investigation of variables associated Deen D, et al: Seizure prophylaxis in neurocritical care: with mortality. Neurology 47:83–89, 1996 a review of evidence-based support. Pharmacotherapy 52. Zachenhofer I, Donat M, Oberndorfer S, Roessler K: Periop- 34:396–409, 2014 erative levetiracetam for prevention of seizures in supratento- 39. Sbeih I, Tamas LB, O’Laoire SA: Epilepsy after operation for rial brain tumor surgery. J Neurooncol 101:101–106, 2011 aneurysms. Neurosurgery 19:784–788, 1986 40. Shafi MM, Westover MB, Cole AJ, Kilbride RD, Hoch DB, Cash SS: Absence of early epileptiform abnormalities predicts lack of seizures on continuous EEG. Neurology Disclosures 79:1796–1801, 2012 The authors report no conflict of interest concerning the materi- 41. Shaw MDM, Foy P, Chadwick D: The effectiveness of pro- als or methods used in this study or the findings specified in this phylactic anticonvulsants following neurosurgery. Acta Neu- paper. rochir (Wien) 69:253–258, 1983 42. Sughrue ME, Rutkowski MJ, Chang EF, Shangari G, Kane Author Contributions AJ, McDermott MW, et al: Postoperative seizures following the resection of convexity meningiomas: are prophylactic Conception and design: Freund, Ritzl. Acquisition of data: anticonvulsants indicated? Clinical article. J Neurosurg Freund, Ritzl. Analysis and interpretation of data: all authors. 114:705–709, 2011 Drafting the article: all authors. Critically revising the article: all 43. Suri A, Mahapatra AK, Bithal P: Seizures following poste- authors. Reviewed submitted version of manuscript: all authors. rior fossa surgery. Br J Neurosurg 12:41–44, 1998 Approved the final version of the manuscript on behalf of all 44. Sutter R, Marsch S, Fuhr P, Kaplan PW, Rüegg S: Anesthetic authors: Freund. Statistical analysis: all authors. Administrative/ drugs in status epilepticus: risk or rescue? A 6-year cohort technical/material support: Freund, Ritzl. Study supervision: study. Neurology 82:656–664, 2014 Freund, Ritzl. 45. Sutter R, Stevens RD, Kaplan PW: Continuous electroen- cephalographic monitoring in critically ill patients: indica- Correspondence tions, limitations, and strategies. Crit Care Med 41:1124– Brin Freund: Johns Hopkins School of , Baltimore, MD. 1132, 2013 [email protected].

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