Top

Published in:

Open Access 01-02-2021 | Subarachnoid Hemorrhage | Original Communication

Seizures at the onset of aneurysmal SAH: epiphenomenon or valuable predictor?

Authors: Marvin Darkwah Oppong, Marcela Jara Bastias, Daniela Pierscianek, Leonie Droste, Thiemo F. Dinger, Yahya Ahmadipour, Laurèl Rauschenbach, Carlos Quesada, Mehdi Chihi, Philipp Dammann, Michael Forsting, Karsten H. Wrede, Ulrich Sure, Ramazan Jabbarli

Published in: Journal of Neurology | Issue 2/2021

Abstract

Objective

Seizures at the onset (SAO) of aneurysmal subarachnoid hemorrhage (aSAH) occur in up to one of every five cases. To date, there is no consensus on causal background and clinical value of these early bleeding-related seizures. This study aimed to analyze the predictors and the impact of SAO in aSAH.

Methods

All aSAH patients from the institutional observational cohort (01/2003–06/2016) were retrospectively reviewed. Patients’ charts and emergency protocols from first responders were screened for the occurrence of seizures in the first 24 h after aSAH. Patients’ baseline characteristics and occurrence of post-hemorrhagic complications were analyzed. Outcome endpoints included in-hospital mortality and poor outcome at 6-month follow-up (modified Rankin Scale > 3).

Results

Of 984 patients included in the final analysis, SAO occurred in 93 cases (9.5%) and were independently associated with younger age (< 51 years, p < 0.001), WFNS grade ≥ 4 (p < 0.001), aneurysm characteristics (location at the proximal branch of the anterior cerebral artery [p = 0.037] and irregular sac [p = 0.019]) and admission body temperature > 38.3 ℃ (p = 0.008). There was an association between SAO and early complications (early infarcts [p = 0.004] and primary decompressive craniectomy [p = 0.024]). Only in the subgroup analysis restricted to the younger individuals, SAO independently predicted poor outcome of aSAH (p = 0.002).

Significance

Onset seizures following aSAH are rare and most likely related to the severity of early brain injury. Particularly, younger individuals are not only at higher risk for SAO, but are also prone to poor outcome in case of aSAH accompanied with SAO.

Trial registration number

German clinical trial registry (DRKS, unique identifier: DRKS00008749, 06/09/2015)

Hart RG, Byer JA, Slaughter JR, Hewett JE, Easton JD (1981) Occurrence and implications of seizures in subarachnoid hemorrhage due to ruptured intracranial aneurysms. Neurosurgery 8(4):417–421. https://doi.org/10.1227/00006123-198104000-00002CrossRefPubMed

Pinto AN, Canhao P, Ferro JM (1996) Seizures at the onset of subarachnoid haemorrhage. J Neurol 243(2):161–164. https://doi.org/10.1007/bf02444009CrossRefPubMed

Butzkueven H, Evans AH, Pitman A, Leopold C, Jolley DJ, Kaye AH, Kilpatrick CJ, Davis SM (2000) Onset seizures independently predict poor outcome after subarachnoid hemorrhage. Neurology 55(9):1315–1320. https://doi.org/10.1212/wnl.55.9.1315CrossRefPubMed

Lin CL, Dumont AS, Lieu AS, Yen CP, Hwang SL, Kwan AL, Kassell NF, Howng SL (2003) Characterization of perioperative seizures and epilepsy following aneurysmal subarachnoid hemorrhage. J Neurosurg 99(6):978–985. https://doi.org/10.3171/jns.2003.99.6.0978CrossRefPubMed

Fung C, Balmer M, Murek M, Z'Graggen WJ, Abu-Isa J, Ozdoba C, Haenggi M, Jakob SM, Raabe A, Beck J (2015) Impact of early-onset seizures on grading and outcome in patients with subarachnoid hemorrhage. J Neurosurg 122(2):408–413. https://doi.org/10.3171/2014.10.jns14163CrossRefPubMed

Rose FC, Sarner M (1965) Epilepsy after ruptured intracranial aneurysm. BMJ 1(5426):18–21CrossRef

Teasdale GM, Drake CG, Hunt W, Kassell N, Sano K, Pertuiset B, De Villiers JC (1988) A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry 51(11):1457CrossRef

Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6(1):1–9CrossRef

Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J (1996) The ABCs of measuring intracerebral hemorrhage volumes. Stroke J Cereb Circ 27(8):1304–1305CrossRef

10.

Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison PB (1982) Computed tomographic diagnosis of intraventricular hemorrhage. Etiol Progn Radiol 143(1):91–96. https://doi.org/10.1148/radiology.143.1.6977795CrossRef

11.

Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, Macdonald RL, Diringer MN, Broderick JP, Dreier JP, Roos YB (2010) Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke J Cereb Circ 41(10):2391–2395. https://doi.org/10.1161/strokeaha.110.589275CrossRef

12.

Sarner M, Rose FC (1967) Clinical presentation of ruptured intracranial aneurysm. J Neurol Neurosurg Psychiatry 30(1):67–70CrossRef

13.

Biller J, Toffol GJ, Kassell NF, Adams HP Jr, Beck DW, Boarini DJ (1987) Spontaneous subarachnoid hemorrhage in young adults. Neurosurgery 21(5):664–667. https://doi.org/10.1227/00006123-198711000-00011CrossRefPubMed

14.

Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C (2003) Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci Off J Soc Neurosci 23(8):3295–3301. https://doi.org/10.1523/jneurosci.23-08-03295.2003CrossRef

15.

Cauley KA, Hu Y, Fielden SW (2020) Aging and the brain: a quantitative study of clinical ct images. AJNR Am J Neuroradiol 41(5):809–814. https://doi.org/10.3174/ajnr.A6510CrossRefPubMed

16.

Caldarelli M, Di Rocco C, Iannelli A (1980) Effects of artificially induced increases in intracranial pressure on epileptic activity. Epilepsia 21(6):587–596. https://doi.org/10.1111/j.1528-1157.1980.tb04312.xCrossRefPubMed

17.

Leach JP, Mohanraj R, Borland W (2012) Alcohol and drugs in epilepsy: pathophysiology, presentation, possibilities, and prevention. Epilepsia 53(Suppl 4):48–57. https://doi.org/10.1111/j.1528-1167.2012.03613.xCrossRefPubMed

18.

Chang TR, Kowalski RG, Carhuapoma JR, Tamargo RJ, Naval NS (2016) Cocaine use as an independent predictor of seizures after aneurysmal subarachnoid hemorrhage. J Neurosurg 124(3):730–735. https://doi.org/10.3171/2015.2.jns142856CrossRefPubMed

19.

Rousseaux P, Scherpereel B, Bernard MH, Graftieaux JP, Guyot JF (1980) Fever and cerebral vasospasm in ruptured intracranial aneurysms. Surg Neurol 14(6):459–465PubMed

20.

Oliveira-Filho J, Ezzeddine MA, Segal AZ, Buonanno FS, Chang Y, Ogilvy CS, Rordorf G, Schwamm LH, Koroshetz WJ, McDonald CT (2001) Fever in subarachnoid hemorrhage: relationship to vasospasm and outcome. Neurology 56(10):1299–1304. https://doi.org/10.1212/wnl.56.10.1299CrossRefPubMed

21.

Stevens RD, Nyquist PA (2007) The systemic implications of aneurysmal subarachnoid hemorrhage. J Neurol Sci 261(1–2):143–156. https://doi.org/10.1016/j.jns.2007.04.047CrossRefPubMed

22.

Zheng VZ, Wong GKC (2017) Neuroinflammation responses after subarachnoid hemorrhage: a review. J Clin Neurosci Off J Neurosurg Soc Australas 42:7–11. https://doi.org/10.1016/j.jocn.2017.02.001CrossRef

23.

Meier K, Lee K (2017) Neurogenic fever. J Intensiv Care Med 32(2):124–129. https://doi.org/10.1177/0885066615625194CrossRef

24.

Gowda R, Jaffa M, Badjatia N (2018) Thermoregulation in brain injury. Handb Clin Neurol 157:789–797. https://doi.org/10.1016/b978-0-444-64074-1.00049-5CrossRefPubMed

25.

Rabinstein AA, Sandhu K (2007) Non-infectious fever in the neurological intensive care unit: incidence, causes and predictors. J Neurol Neurosurg Psychiatry 78(11):1278–1280. https://doi.org/10.1136/jnnp.2006.112730CrossRefPubMedPubMedCentral

26.

Thompson HJ, Pinto-Martin J, Bullock MR (2003) Neurogenic fever after traumatic brain injury: an epidemiological study. J Neurol Neurosurg Psychiatry 74(5):614–619. https://doi.org/10.1136/jnnp.74.5.614CrossRefPubMedPubMedCentral

27.

Heit JJ, Ball RL, Telischak NA, Do HM, Dodd RL, Steinberg GK, Chang SD, Wintermark M, Marks MP (2017) Patient outcomes and cerebral infarction after ruptured anterior communicating artery aneurysm treatment. AJNR Am J Neuroradiol 38(11):2119–2125. https://doi.org/10.3174/ajnr.A5355CrossRefPubMed

28.

Bove-Fenderson E, Mannstadt M (2018) Hypocalcemic disorders. Best Pract Res Clin Endocrinol Metab 32(5):639–656. https://doi.org/10.1016/j.beem.2018.05.006CrossRefPubMed

29.

Manzanares W, Aramendi I, Langlois PL, Biestro A (2015) Hyponatremia in the neurocritical care patient: an approach based on current evidence. Medicina intensiva 39(4):234–243. https://doi.org/10.1016/j.medin.2014.11.004CrossRefPubMed

30.

Cuesta M, Hannon MJ, Thompson CJ (2016) Diagnosis and treatment of hyponatraemia in neurosurgical patients. Endocrinologia y nutricion organo de la Sociedad Espanola de Endocrinologia y Nutricion 63(5):230–238. https://doi.org/10.1016/j.endonu.2015.12.007CrossRefPubMed

31.

Andrew RD (1991) Seizure and acute osmotic change: clinical and neurophysiological aspects. J Neurol Sci 101(1):7–18. https://doi.org/10.1016/0022-510x(91)90013-wCrossRefPubMed

32.

Hanggi D, Winkler PA, Steiger HJ (2010) Primary epileptogenic unruptured intracranial aneurysms: incidence and effect of treatment on epilepsy. Neurosurgery 66(6):1161–1165. https://doi.org/10.1227/01.neu.0000369515.95351.2aCrossRefPubMed

33.

Lindgren AE, Koivisto T, Bjorkman J, von Und Zu, Fraunberg M, Helin K, Jaaskelainen JE, Frosen J (2016) Irregular shape of intracranial aneurysm indicates rupture risk irrespective of size in a population-based cohort. Stroke J Cereb Circu 47(5):1219–1226. https://doi.org/10.1161/strokeaha.115.012404CrossRef

34.

Bjorkman J, Frosen J, Tahtinen O, Backes D, Huttunen T, Harju J, Huttunen J, Kurki MI, von Und Zu, Fraunberg M, Koivisto T, Manninen H, Jaaskelainen JE, Lindgren AE (2017) Irregular shape identifies ruptured intracranial aneurysm in subarachnoid hemorrhage patients with multiple aneurysms. Stroke J Cereb Circu 48(7):1986–1989. https://doi.org/10.1161/strokeaha.117.017147CrossRef

35.

Mocco J, Brown RD Jr, Torner JC, Capuano AW, Fargen KM, Raghavan ML, Piepgras DG, Meissner I, Iii JH (2017) Aneurysm morphology and prediction of rupture: an international study of unruptured intracranial aneurysms analysis. Neurosurgery. https://doi.org/10.1093/neuros/nyx226CrossRefPubMedPubMedCentral

Title: Seizures at the onset of aneurysmal SAH: epiphenomenon or valuable predictor?
Authors: Marvin Darkwah Oppong
Marcela Jara Bastias
Daniela Pierscianek
Leonie Droste
Thiemo F. Dinger
Yahya Ahmadipour
Laurèl Rauschenbach
Carlos Quesada
Mehdi Chihi
Philipp Dammann
Michael Forsting
Karsten H. Wrede
Ulrich Sure
Ramazan Jabbarli
Publication date: 01-02-2021
Publisher: Springer Berlin Heidelberg
Keywords: Subarachnoid Hemorrhage
Aneurysm
Aneurysm
Intracranial Hypertension
Subarachnoid Hemorrhage
Published in: Journal of Neurology / Issue 2/2021
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-020-10173-2

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Seizures at the onset of aneurysmal SAH: epiphenomenon or valuable predictor?

Abstract

Objective

Methods

Results

Significance

Trial registration number

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Objective

Methods

Results

Significance

Trial registration number

Please log in to get access to this content

Other articles of this Issue 2/2021

Comment on “Stroke in patients with SARS‑CoV‑2 infection: case series” from a London hospital experience

COVID-19 and neurological disorders: are neurodegenerative or neuroimmunological diseases more vulnerable?

Inter-hospital transfer for mechanical thrombectomy within the supraregional stroke network NEVAS

Dangerous sweets: severe hypokalemia with rhabdomyolysis and tetraparesis from chronic consumption of licorice

Comorbidities contribute substantially to the severity of common multiple sclerosis symptoms

One-year survival of patients with high-grade glioma discharged alive from the intensive care unit