Status epilepticus after intracranial neurosurgery: incidence and risk stratification by perioperative clinical features

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  • 1 Departments of Neurosurgery and
  • | 2 Neurology, Stanford University School of Medicine, Stanford; and
  • | 3 Section of Neurosurgery, VA Palo Alto Healthcare System, Palo Alto, California
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OBJECTIVE

Status epilepticus (SE) is associated with significant mortality, cost, and risk of future seizures. In one of the first studies of SE after neurosurgery, the authors assess the incidence, risk factors, and outcome of postneurosurgical SE (PNSE).

METHODS

Neurosurgical admissions from the MarketScan Claims and Encounters database (2007 through 2015) were assessed in a longitudinal cross-sectional sample of privately insured patients who underwent qualifying cranial procedures in the US and were older than 18 years of age. The incidence of early (in-hospital) and late (postdischarge readmission) SE and associated mortality was assessed. Procedural, pathological, demographic, and anatomical covariates parameterized multivariable logistic regression and Cox models. Multivariable logistic regression and Cox proportional hazards models were used to study the incidence of early and late PNSE. A risk-stratification simulation was performed, combining individual predictors into singular risk estimates.

RESULTS

A total of 197,218 admissions (218,217 procedures) were identified. Early PNSE occurred during 637 (0.32%) of 197,218 admissions for cranial neurosurgical procedures. A total of 1045 (0.56%) cases of late PNSE were identified after 187,771 procedure admissions with nonhospice postdischarge follow-up. After correction for comorbidities, craniotomy for trauma, hematoma, or elevated intracranial pressure was associated with increased risk of early PNSE (adjusted OR [aOR] 1.538, 95% CI 1.183–1.999). Craniotomy for meningioma resection was associated with an increased risk of early PNSE compared with resection of metastases and parenchymal primary brain tumors (aOR 2.701, 95% CI 1.388–5.255). Craniotomies for infection or abscess (aHR 1.447, 95% CI 1.016–2.061) and CSF diversion (aHR 1.307, 95% CI 1.076–1.587) were associated with highest risk of late PNSE. Use of continuous electroencephalography in patients with early (p < 0.005) and late (p < 0.001) PNSE rose significantly over the study time period. The simulation regression model predicted that patients at high risk for early PNSE experienced a 1.10% event rate compared with those at low risk (0.07%). Similarly, patients predicted to be at highest risk for late PNSE were significantly more likely to eventually develop late PNSE than those at lowest risk (HR 54.16, 95% CI 24.99–104.80).

CONCLUSIONS

Occurrence of early and late PNSE was associated with discrete neurosurgical pathologies and increased mortality. These data provide a framework for prospective validation of clinical and perioperative risk factors and indicate patients for heightened diagnostic suspicion of PNSE.

ABBREVIATIONS

aHR = adjusted HR; aOR = adjusted OR; AUC = area under the receiver operating characteristic curve; cEEG = continuous EEG; CPT = Current Procedural Terminology; DBS = deep brain stimulation; EEG = electroencephalography; EVD = external ventricular drain; ICD = International Classification of Diseases; ICP = intracranial pressure; PNSE = postneurosurgical SE; SE = status epilepticus.

Supplementary Materials

    • Supplemental Methods and Tables (PDF 672 KB)

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Contributor Notes

Correspondence Jonathon J. Parker: Stanford University, Stanford, CA. parkerjo@stanford.edu.

INCLUDE WHEN CITING Published online May 14, 2021; DOI: 10.3171/2020.10.JNS202895.

Disclosures Dr. Li: support from and/or consultant for Novocure, Bristol Myers Squibb, NIH, Medtronic, Surgical Visions Technology, and Johnson and Johnson. Dr. Fisher: consultant for Medtronic and direct stock ownership in Avails Medical, Cerebral Therapeutics, Eyez, Irody, Smart Monitor, and Zeto.

M.C.J. and J.J.P. contributed equally to this work.

  • 1

    Kapur J, Elm J, Chamberlain JM, et al. Randomized trial of three anticonvulsant medications for status epilepticus. N Engl J Med. 2019;381(22):21032113.

    • Search Google Scholar
    • Export Citation
  • 2

    Logroscino G, Hesdorffer DC, Cascino G, Hauser WA. Status epilepticus without an underlying cause and risk of death: a population-based study. Arch Neurol. 2008;65(2):221224.

    • Search Google Scholar
    • Export Citation
  • 3

    Sculier C, Gaínza-Lein M, Sánchez Fernández I, Loddenkemper T. Long-term outcomes of status epilepticus: a critical assessment. Epilepsia. 2018;59(suppl 2):155169.

    • Search Google Scholar
    • Export Citation
  • 4

    Towne AR, Pellock JM, Ko D, DeLorenzo RJ. Determinants of mortality in status epilepticus. Epilepsia. 1994;35(1):2734.

  • 5

    Tuppurainen KM, Ritvanen JG, Mustonen H, Kamppi LS. Predictors of mortality at one year after generalized convulsive status epilepticus. Epilepsy Behav. 2019;101(Pt B):106411.

    • Search Google Scholar
    • Export Citation
  • 6

    Kämppi L, Mustonen H, Kotisaari K, Soinila S. The essence of the first 2.5 h in the treatment of generalized convulsive status epilepticus. Seizure. 2018;55:916.

    • Search Google Scholar
    • Export Citation
  • 7

    Sutter R, Semmlack S, Kaplan PW, et al. Prolonged status epilepticus: early recognition and prediction of full recovery in a 12-year cohort. Epilepsia. 2019;60(1):4252.

    • Search Google Scholar
    • Export Citation
  • 8

    Betjemann JP, Josephson SA, Lowenstein DH, Burke JF. Trends in status epilepticus-related hospitalizations and mortality: redefined in US practice over time. JAMA Neurol. 2015;72(6):650655.

    • Search Google Scholar
    • Export Citation
  • 9

    Logroscino G, Hesdorffer DC, Cascino G, et al. Time trends in incidence, mortality, and case-fatality after first episode of status epilepticus. Epilepsia. 2001;42(8):10311035.

    • Search Google Scholar
    • Export Citation
  • 10

    Neligan A, Noyce AJ, Gosavi TD, et al. Change in mortality of generalized convulsive status epilepticus in high-income countries over time: a systematic review and meta-analysis. JAMA Neurol. 2019;76(8):897905.

    • Search Google Scholar
    • Export Citation
  • 11

    Cavaliere R, Farace E, Schiff D. Clinical implications of status epilepticus in patients with neoplasms. Arch Neurol. 2006;63(12):17461749.

    • Search Google Scholar
    • Export Citation
  • 12

    Claassen J, Bateman BT, Willey JZ, et al. Generalized convulsive status epilepticus after nontraumatic subarachnoid hemorrhage: the nationwide inpatient sample. Neurosurgery. 2007;61(1):6065.

    • Search Google Scholar
    • Export Citation
  • 13

    Giovannini G, Pasini F, Orlandi N, et al. Tumor-associated status epilepticus in patients with glioma: clinical characteristics and outcomes. Epilepsy Behav. 2019;101(Pt B):106370.

    • Search Google Scholar
    • Export Citation
  • 14

    Little AS, Kerrigan JF, McDougall CG, et al. Nonconvulsive status epilepticus in patients suffering spontaneous subarachnoid hemorrhage. J Neurosurg. 2007;106(5):805811.

    • Search Google Scholar
    • Export Citation
  • 15

    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.

    • Search Google Scholar
    • Export Citation
  • 16

    Al-Mefty O, Wrubel D, Haddad N. Postoperative nonconvulsive encephalopathic status: identification of a syndrome responsible for delayed progressive deterioration of neurological status after skull base surgery. Clinical article. J Neurosurg. 2009;111(5):10621068.

    • Search Google Scholar
    • Export Citation
  • 17

    Devarajan J, Siyam AM, Alexopoulos AV, et al. Non-convulsive status epilepticus in the postanesthesia care unit following meningioma excision. Can J Anaesth. 2011;58(1):6873.

    • Search Google Scholar
    • Export Citation
  • 18

    Morioka T, Sayama T, Mukae N, et al. Nonconvulsive status epilepticus during perioperative period of cerebrovascular surgery. Neurol Med Chir (Tokyo). 2011;51(3):171179.

    • Search Google Scholar
    • Export Citation
  • 19

    Zeiler FA, Kaufmann AM, Gillman LM, et al. Ketamine for medically refractory status epilepticus after elective aneurysm clipping. Neurocrit Care. 2013;19(1):119124.

    • Search Google Scholar
    • Export Citation
  • 20

    Kortland LM, Alfter A, Bähr O, et al. Costs and cost-driving factors for acute treatment of adults with status epilepticus: a multicenter cohort study from Germany. Epilepsia. 2016;57(12):20562066.

    • Search Google Scholar
    • Export Citation
  • 21

    Sánchez Fernández I, Amengual-Gual M, Barcia Aguilar C, Loddenkemper T. Estimating the cost of status epilepticus admissions in the United States of America using ICD-10 codes. Seizure. 2019;71:295303.

    • Search Google Scholar
    • Export Citation
  • 22

    Sánchez Fernández I, Loddenkemper T. Estimating the cost of admissions related to convulsive status epilepticus in the United States of America. Seizure. 2018;61:186198.

    • Search Google Scholar
    • Export Citation
  • 23

    Medress Z, Ugiliweneza B, Parker J, et al. Simulating episode-based bundled payments for cranial neurosurgical procedures. Neurosurgery. 2020;87(1):8695.

    • Search Google Scholar
    • Export Citation
  • 24

    Azad TD, Zhang Y, Stienen MN, et al. Patterns of opioid and benzodiazepine use in opioid-naïve patients with newly diagnosed low back and lower extremity pain. J Gen Intern Med. 2020;35(1):291297.

    • Search Google Scholar
    • Export Citation
  • 25

    Jin MC, Wu A, Azad TD, et al. Evaluating shunt survival following ventriculoperitoneal shunting with and without stereotactic navigation in previously shunt-naïve patients. World Neurosurg. 2020;136:e671e682.

    • Search Google Scholar
    • Export Citation
  • 26

    Fatemi P, Zhang Y, Ho A, et al. Opioid use in adults with low back or lower extremity pain who undergo spine surgical treatment within one year of diagnosis. Spine (Phila Pa 1976). 2020;45(24):17251735.

    • Search Google Scholar
    • Export Citation
  • 27

    Whetzel PL, Noy NF, Shah NH, et al. BioPortal: enhanced functionality via new Web services from the National Center for Biomedical Ontology to access and use ontologies in software applications. Nucleic Acids Res. 2011;39(Suppl_2):W541W545.

    • Search Google Scholar
    • Export Citation
  • 28

    Elixhauser A, Steiner C, Harris DR, Coffey RM. Comorbidity measures for use with administrative data. Med Care. 1998;36(1):827.

  • 29

    Quan H, Sundararajan V, Halfon P, et al. Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med Care. 2005;43(11):11301139.

    • Search Google Scholar
    • Export Citation
  • 30

    Hoerl AE, Kennard RW. Ridge regression: biased estimation for nonorthogonal problems. Technometrics. 1970;12(1):5567.

  • 31

    Friedman J, Hastie T, Tibshirani R. Regularization paths for generalized linear models via coordinate descent. J Stat Softw. 2010;33(1):122.

    • Search Google Scholar
    • Export Citation
  • 32

    Robin X, Turck N, Hainard A, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12(1):77.

    • Search Google Scholar
    • Export Citation
  • 33

    Harrell FE Jr. Regression Modeling Strategies: With Applications to Linear Models, Logistic and Ordinal Regression, and Survival Analysis. Springer; 2015.

    • Search Google Scholar
    • Export Citation
  • 34

    Grill MF, Treiman DM, Maganti RK. Status epilepticus associated with subtentorial posterior fossa lesions. Arch Neurol. 2009;66(12):15001504.

    • Search Google Scholar
    • Export Citation
  • 35

    Oushy S, Sillau SH, Ney DE, et al. New-onset seizure during and after brain tumor excision: a risk assessment analysis. J Neurosurg. 2018;128(6):17131718.

    • Search Google Scholar
    • Export Citation
  • 36

    Dewan MC, Thompson RC, Kalkanis SN, et al. Prophylactic antiepileptic drug administration following brain tumor resection: results of a recent AANS/CNS Section on Tumors survey. J Neurosurg. 2017;126(6):17721778.

    • Search Google Scholar
    • Export Citation
  • 37

    Lv RJ, Wang Q, Cui T, et al. Status epilepticus-related etiology, incidence and mortality: a meta-analysis. Epilepsy Res. 2017;136:1217.

  • 38

    Gaspard N, Foreman BP, Alvarez V, et al. New-onset refractory status epilepticus: Etiology, clinical features, and outcome. Neurology. 2015;85(18):16041613.

    • Search Google Scholar
    • Export Citation
  • 39

    Strzelczyk A, Ansorge S, Hapfelmeier J, et al. Costs, length of stay, and mortality of super-refractory status epilepticus: a population-based study from Germany. Epilepsia. 2017;58(9):15331541.

    • Search Google Scholar
    • Export Citation
  • 40

    Eskioglou E, Stähli C, Rossetti AO, Novy J. Extended EEG and non-convulsive status epilepticus: benefit over routine EEG? Acta Neurol Scand. 2017;136(3):272276.

    • Search Google Scholar
    • Export Citation
  • 41

    Jongeling AC, Bazil CW, Claassen J. Status epilepticus: redefined or increasingly detected? JAMA Neurol. 2015;72(6):631633.

  • 42

    Hill CE, Blank LJ, Thibault D, et al. Continuous EEG is associated with favorable hospitalization outcomes for critically ill patients. Neurology. 2019;92(1):e9e18.

    • Search Google Scholar
    • Export Citation
  • 43

    Koffman L, Rincon F, Gomes J, et al. Continuous electroencephalographic monitoring in the intensive care unit: a cross-sectional study. J Intensive Care Med. 2020;35(11):12351240.

    • Search Google Scholar
    • Export Citation
  • 44

    Trinka E, Cock H, Hesdorffer D, et al. A definition and classification of status epilepticus—report of the ILAE Task Force on classification of status epilepticus. Epilepsia. 2015;56(10):15151523.

    • Search Google Scholar
    • Export Citation
  • 45

    Lowenstein DH, Bleck T, Macdonald RL. It’s time to revise the definition of status epilepticus. Epilepsia. 1999;40(1):120122.

  • 46

    Rolston JD, Han SJ, Chang EF. Systemic inaccuracies in the National Surgical Quality Improvement Program database: implications for accuracy and validity for neurosurgery outcomes research. J Clin Neurosci. 2017;37:4447.

    • Search Google Scholar
    • Export Citation
  • 47

    Sapkota S, Kobau R, Pastula DM, Zack MM. People with epilepsy are diagnosed most often with unspecified epilepsy, followed by focal epilepsy, generalized convulsive epilepsy, and generalized nonconvulsive epilepsy—US MarketScan data, 2010-2015. Epilepsy Behav. 2018;79:244246.

    • Search Google Scholar
    • Export Citation
  • 48

    Jetté N, Reid AY, Quan H, et al. How accurate is ICD coding for epilepsy? Epilepsia. 2010;51(1):6269.

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