Download PDF
CC BY-NC-ND 4.0 · Arquivos Brasileiros de Neurocirurgia: Brazilian Neurosurgery 2018; 37(03): 206-212
DOI: 10.1055/s-0038-1672202
Review Article | Artigo de Revisão
Thieme Revinter Publicações Ltda Rio de Janeiro, Brazil

Seizures and Epilepsy following Subarachnoid Hemorrhage: A Review on Incidence, Risk Factors, Outcome and Treatment

Crises convulsivas e epilepsia após hemorragia subaracnoide: uma revisão sobre incidência, fatores de risco, desfecho e tratamento
Miguel Bertelli Ramos
1   School of Medicine, Universidade de Caxias do Sul, Caxias do Sul, RS, Brazil
,
Manoel Jacobsen Teixeira
2   School of Medicine, Universidade de São Paulo, SP, Brazil
,
Eberval Gadelha Figueiredo
2   School of Medicine, Universidade de São Paulo, SP, Brazil
› Author Affiliations
Further Information

Publication History

06 June 2018

10 July 2018

Publication Date:
18 October 2018 (online)

   Permissions and Reprints

Abstract

The mortality rates of subarachnoid hemorrhage (SAH) average 51%, and survivors frequently experience acute and long-term neurological conditions, including seizures and epilepsy. The incidence of post SAH-related seizures and epilepsy, its risk factors, outcomes and management are controversial. The present paper aims to discuss these aspects, to provide the pros and cons of different management options of this condition. A review on PubMed was performed encompassing the incidence of seizures and epilepsy following SAH, the risk factors for its occurrence, its related outcomes, and treatment. The incidence of seizures and epilepsy following SAH varies widely in the literature (from 6 to 26%). Some possible risk factors were identified, such as middle cerebral artery (MCA) aneurysm, Hunt and Hess grade III, aneurysm clipping, thick subarachnoid clot, intracerebral hemorrhage, rebleeding, ischemic brain infarction, Fisher grade III or IV, acute hydrocephalus, hypertension history and poor World Federation of Neurosurgical Societies (WFNS) grade. Nevertheless, these relations are frequently uncertain. Also, it appears that the outcome of patients who suffered SAH is worsened by seizures. Given these uncertainties, the need for antiepileptic drug (AED) prophylaxis, the choice of the best drug and dose, as well as the duration of the treatment are controversial topics. However, some recommendations based on low quality evidence are reasonable to be adopted. These include considering AED prophylaxis when a seizure occur after SAH, considering routine long-term AED prophylaxis in specific populations, considering electroencephalogram (EEG) monitoring, and avoiding phenytoin prescription. That is, an individualized approach appears to be the best option, since there is no high-quality evidence.

Resumo

As taxas de mortalidade da hemorragia subaracnoide (HSA) são de 51%, e os sobreviventes frequentemente sofrem condições neurológicas agudas e em longo prazo, incluindo convulsões e epilepsia. A incidência de convulsões e epilepsia após HSA, seus fatores de risco, desfecho e tratamento são controversos. O presente artigo pretende discutir esses aspectos para fornecer os prós e os contras de diferentes opções de manejo dessa condição. Realizou-se uma revisão no PubMed, englobando a incidência de convulsões e epilepsia após HSA, os fatores de risco para a sua ocorrência, seu desfecho e tratamento. A incidência de convulsões e epilepsia após HSA varia amplamente na literatura (de 6 a 26%). Alguns possíveis fatores de risco foram identificados, como aneurisma da artéria cerebral média (ACM), Hunt e Hess grau III, clipagem do aneurisma, coágulo subaracnoide espesso, hemorragia intracerebral, ressangramento, isquemia cerebral, Fisher grau III ou IV, hidrocefalia aguda, história de hipertensão e uma pontuação desfavorável na escala da Federação Mundial de Sociedades de Neurocirurgia (WFNS, na sigla em inglês). Entretanto, essas relações frequentemente são incertas. Além disso, os pacientes que apresentam convulsões após HSA parecem ter pior desfecho. Devido a essas incertezas, a necessidade de profilaxia com anticonvulsivantes, a escolha do melhor fármaco e posologia, e a duração do tratamento são controversos. Contudo, algumas recomendações baseadas em evidências de baixa qualidade podem ser adotadas. Elas incluem considerar profilaxia com anticonvulsivantes para convulsões pós HSA, considerar profilaxia rotineira em longo prazo em populações específicas após HSA, considerar monitoramento com eletroencefalograma (EEG), e evitar a prescrição de fenitoína. Ou seja, uma abordagem individual parece a melhor opção até que haja evidências de alta qualidade.

Keywords

subarachnoid hemorrhage - epilepsy - incidence - risk factors - anticonvulsants - prognosis

Palavras-chave

hemorragia subaracnoidea - epilepsia - incidência - fatores de risco - anticonvulsivantes - prognóstico
 

  • References

  • 1 Tidswell P, Dias PS, Sagar HJ, Mayes AR, Battersby RD. Cognitive outcome after aneurysm rupture: relationship to aneurysm site and perioperative complications. Neurology 1995; 45 (05) 875-882
    PubMedGoogle Scholar
  • 2 Stegmayr B, Eriksson M, Asplund K. Declining mortality from subarachnoid hemorrhage: changes in incidence and case fatality from 1985 through 2000. Stroke 2004; 35 (09) 2059-2063
    CrossrefPubMedGoogle Scholar
  • 3 Ingall TJ, Whisnant JP, Wiebers DO, O'Fallon WM. Has there been a decline in subarachnoid hemorrhage mortality?. Stroke 1989; 20 (06) 718-724
    CrossrefPubMedGoogle Scholar
  • 4 van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001; 124 (Pt 2): 249-278
    CrossrefPubMedGoogle Scholar
  • 5 Truelsen T, Bonita R, Duncan J, Anderson NE, Mee E. Changes in subarachnoid hemorrhage mortality, incidence, and case fatality in New Zealand between 1981-1983 and 1991-1993. Stroke 1998; 29 (11) 2298-2303
    CrossrefPubMedGoogle Scholar
  • 6 Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010; 41 (08) e519-e536
    CrossrefPubMedGoogle Scholar
  • 7 Buczacki SJ, Kirkpatrick PJ, Seeley HM, Hutchinson PJ. Late epilepsy following open surgery for aneurysmal subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 2004; 75 (11) 1620-1622
    CrossrefPubMedGoogle Scholar
  • 8 Rhoney DH, Tipps LB, Murry KR, Basham MC, Michael DB, Coplin WM. Anticonvulsant prophylaxis and timing of seizures after aneurysmal subarachnoid hemorrhage. Neurology 2000; 55 (02) 258-265
    CrossrefPubMedGoogle Scholar
  • 9 Lin C-L, Dumont AS, Lieu A-S. , et al. Characterization of perioperative seizures and epilepsy following aneurysmal subarachnoid hemorrhage. J Neurosurg 2003; 99 (06) 978-985
    CrossrefPubMedGoogle Scholar
  • 10 Choi KS, Chun HJ, Yi HJ, Ko Y, Kim YS, Kim JM. Seizures and Epilepsy following Aneurysmal Subarachnoid Hemorrhage : Incidence and Risk Factors. J Korean Neurosurg Soc 2009; 46 (02) 93-98
    CrossrefPubMedGoogle Scholar
  • 11 Sundaram MB, Chow F. Seizures associated with spontaneous subarachnoid hemorrhage. Can J Neurol Sci 1986; 13 (03) 229-231
    PubMedGoogle Scholar
  • 12 Hart RG, Byer JA, Slaughter JR, Hewett JE, Easton JD. Occurrence and implications of seizures in subarachnoid hemorrhage due to ruptured intracranial aneurysms. Neurosurgery 1981; 8 (04) 417-421
    CrossrefPubMedGoogle Scholar
  • 13 Gilmore E, Choi HA, Hirsch LJ, Claassen J. Seizures and CNS hemorrhage: spontaneous intracerebral and aneurysmal subarachnoid hemorrhage. Neurologist 2010; 16 (03) 165-175
    CrossrefPubMedGoogle Scholar
  • 14 Butzkueven H, Evans AH, Pitman A. , et al. Onset seizures independently predict poor outcome after subarachnoid hemorrhage. Neurology 2000; 55 (09) 1315-1320
    CrossrefPubMedGoogle Scholar
  • 15 Little AS, Kerrigan JF, McDougall CG. , et al. Nonconvulsive status epilepticus in patients suffering spontaneous subarachnoid hemorrhage. J Neurosurg 2007; 106 (05) 805-811
    CrossrefPubMedGoogle Scholar
  • 16 Lindgren C, Nordh E, Naredi S, Olivecrona M. Frequency of non-convulsive seizures and non-convulsive status epilepticus in subarachnoid hemorrhage patients in need of controlled ventilation and sedation. Neurocrit Care 2012; 17 (03) 367-373
    CrossrefPubMedGoogle Scholar
  • 17 Ohman J. Hypertension as a risk factor for epilepsy after aneurysmal subarachnoid hemorrhage and surgery. Neurosurgery 1990; 27 (04) 578-581
    CrossrefPubMedGoogle Scholar
  • 18 Claassen J, Peery S, Kreiter KT. , et al. Predictors and clinical impact of epilepsy after subarachnoid hemorrhage. Neurology 2003; 60 (02) 208-214
    CrossrefPubMedGoogle Scholar
  • 19 Giroud M, Gras P, Fayolle H, André N, Soichot P, Dumas R. Early seizures after acute stroke: a study of 1,640 cases. Epilepsia 1994; 35 (05) 959-964
    CrossrefPubMedGoogle Scholar
  • 20 Hasan D, Schonck RSM, Avezaat CJJ, Tanghe HLJ, van Gijn J, van der Lugt PJ. Epileptic seizures after subarachnoid hemorrhage. Ann Neurol 1993; 33 (03) 286-291
    PubMedGoogle Scholar
  • 21 Ukkola V, Heikkinen ER. Epilepsy after operative treatment of ruptured cerebral aneurysms. Acta Neurochir (Wien) 1990; 106 (3-4): 115-118
    CrossrefPubMedGoogle Scholar
  • 22 Keränen T, Tapaninaho A, Hernesniemi J, Vapalahti M. Late epilepsy after aneurysm operations. Neurosurgery 1985; 17 (06) 897-900
    CrossrefPubMedGoogle Scholar
  • 23 Olafsson E, Gudmundsson G, Hauser WA. Risk of epilepsy in long-term survivors of surgery for aneurysmal subarachnoid hemorrhage: a population-based study in Iceland. Epilepsia 2000; 41 (09) 1201-1205
    CrossrefPubMedGoogle Scholar
  • 24 Bidziński J, Marchel A, Sherif A. Risk of epilepsy after aneurysm operations. Acta Neurochir (Wien) 1992; 119 (1–4): 49-52
    CrossrefPubMedGoogle Scholar
  • 25 Kotila M, Waltimo O. Epilepsy after stroke. Epilepsia 1992; 33 (03) 495-498
    CrossrefPubMedGoogle Scholar
  • 26 Cabral NL, Gonçalves AR, Longo AL. , et al. Incidence of stroke subtypes, prognosis and prevalence of risk factors in Joinville, Brazil: a 2 year community based study. J Neurol Neurosurg Psychiatry 2009; 80 (07) 755-761
    CrossrefPubMedGoogle Scholar
  • 27 Matthew E, Sherwin AL, Welner SA, Odusote K, Stratford JG. Seizures following intracranial surgery: incidence in the first post-operative week. Can J Neurol Sci 1980; 7 (04) 285-290
    CrossrefPubMedGoogle Scholar
  • 28 Kvam DA, Loftus CM, Copeland B, Quest DO. Seizures during the immediate postoperative period. Neurosurgery 1983; 12 (01) 14-17
    CrossrefPubMedGoogle Scholar
  • 29 Raper DMS, Starke RM, Komotar RJ, Allan R, Connolly Jr ES. Seizures after aneurysmal subarachnoid hemorrhage: a systematic review of outcomes. World Neurosurg 2013; 79 (5-6): 682-690
    CrossrefPubMedGoogle Scholar
  • 30 Dennis LJ, Claassen J, Hirsch LJ, Emerson RG, Connolly ES, Mayer SA. Nonconvulsive status epilepticus after subarachnoid hemorrhage. Neurosurgery 2002; 51 (05) 1136-1143 , discussion 1144
    CrossrefPubMedGoogle Scholar
  • 31 Fisher RS, Acevedo C, Arzimanoglou A. , et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014; 55 (04) 475-482
    CrossrefPubMedGoogle Scholar
  • 32 Connolly Jr ES, Rabinstein AA, Carhuapoma JR. , et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke 2012; 43 (06) 1711-1737
    CrossrefPubMedGoogle Scholar
  • 33 Diringer MN, Bleck TP, Claude Hemphill III J. , et al; Neurocritical Care Society. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society's Multidisciplinary Consensus Conference. Neurocrit Care 2011; 15 (02) 211-240
    CrossrefPubMedGoogle Scholar
  • 34 Molyneux AJ, Kerr RSC, Yu L-M. , et al; International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005; 366 (9488): 809-817
    CrossrefPubMedGoogle Scholar
  • 35 Raper DMS, Kokabi N, McGee-Collett M. The efficacy of antiepileptic drug prophylaxis in the prevention of early and late seizures following repair of intracranial aneurysms. J Clin Neurosci 2011; 18 (09) 1174-1179
    CrossrefPubMedGoogle Scholar
  • 36 Johansson M, Cesarini KG, Contant CF, Persson L, Enblad P. Changes in intervention and outcome in elderly patients with subarachnoid hemorrhage. Stroke 2001; 32 (12) 2845-2949
    CrossrefPubMedGoogle Scholar
  • 37 Scott RB, Eccles F, Molyneux AJ, Kerr RSC, Rothwell PM, Carpenter K. Improved cognitive outcomes with endovascular coiling of ruptured intracranial aneurysms: neuropsychological outcomes from the International Subarachnoid Aneurysm Trial (ISAT). Stroke 2010; 41 (08) 1743-1747 (ISAT)
    CrossrefPubMedGoogle Scholar
  • 38 Hesdorffer DC, Benn EKT, Cascino GD, Hauser WA. Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia 2009; 50 (05) 1102-1108
    CrossrefPubMedGoogle Scholar
  • 39 Marigold R, Günther A, Tiwari D, Kwan J. Antiepileptic drugs for the primary and secondary prevention of seizures after subarachnoid haemorrhage. Cochrane Database Syst Rev 2013; (06) CD008710
    PubMedGoogle Scholar
  • 40 Sakowitz OW, Raabe A, Vucak D, Kiening KL, Unterberg AW. Contemporary management of aneurysmal subarachnoid hemorrhage in germany: results of a survey among 100 neurosurgical departments. Neurosurgery 2006; 58 (01) 137-145 , discussion 137–145
    CrossrefPubMedGoogle Scholar
  • 41 Naidech AM, Kreiter KT, Janjua N. , et al. Phenytoin exposure is associated with functional and cognitive disability after subarachnoid hemorrhage. Stroke 2005; 36 (03) 583-587
    CrossrefPubMedGoogle Scholar
  • 42 Rosengart AJ, Huo JD, Tolentino J. , et al. Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg 2007; 107 (02) 253-260
    CrossrefPubMedGoogle Scholar
  • 43 Chumnanvej S, Dunn IF, Kim DH. Three-day phenytoin prophylaxis is adequate after subarachnoid hemorrhage. Neurosurgery 2007; 60 (01) 99-102 , discussion 102–103
    CrossrefPubMedGoogle Scholar
  • 44 Silverman IE, Restrepo L, Mathews GC. Poststroke seizures. Arch Neurol 2002; 59 (02) 195-201
    CrossrefPubMedGoogle Scholar
  • 45 Krumholz A, Wiebe S, Gronseth GS. , et al. Evidence-based guideline: Management of an unprovoked first seizure in adults: Report of the Guideline Development Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Neurology 2015; 84 (16) 1705-1713
    CrossrefPubMedGoogle Scholar
  • 46 Hauser WA, Rich SS, Lee JR-J, Annegers JF, Anderson VE. Risk of recurrent seizures after two unprovoked seizures. N Engl J Med 1998; 338 (07) 429-434
    CrossrefPubMedGoogle Scholar
  • 47 Kim LG, Johnson TL, Marson AG, Chadwick DW. ; MRC MESS Study group. Prediction of risk of seizure recurrence after a single seizure and early epilepsy: further results from the MESS trial. Lancet Neurol 2006; 5 (04) 317-322
    CrossrefPubMedGoogle Scholar
  • 48 French JA, Kanner AM, Bautista J. , et al; Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology; Quality Standards Subcommittee of the American Academy of Neurology; American Epilepsy Society. Efficacy and tolerability of the new antiepileptic drugs I: treatment of new onset epilepsy: report of the Therapeutics and Technology Assessment Subcommittee and Quality Standards Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Neurology 2004; 62 (08) 1252-1260
    CrossrefPubMedGoogle Scholar
  • 49 Glauser T, Ben-Menachem E, Bourgeois B. , et al; ILAE Subcommission on AED Guidelines. Updated ILAE evidence review of antiepileptic drug efficacy and effectiveness as initial monotherapy for epileptic seizures and syndromes. Epilepsia 2013; 54 (03) 551-563
    CrossrefPubMedGoogle Scholar
  • 50 Marson AG, Al-Kharusi AM, Alwaidh M. , et al; SANAD Study group. The SANAD study of effectiveness of carbamazepine, gabapentin, lamotrigine, oxcarbazepine, or topiramate for treatment of partial epilepsy: an unblinded randomised controlled trial. Lancet 2007; 369 (9566): 1000-1015
    CrossrefPubMedGoogle Scholar
  • 51 Marson AG, Al-Kharusi AM, Alwaidh M. , et al; SANAD Study group. The SANAD study of effectiveness of valproate, lamotrigine, or topiramate for generalised and unclassifiable epilepsy: an unblinded randomised controlled trial. Lancet 2007; 369 (9566): 1016-1026
    CrossrefPubMedGoogle Scholar
  • 52 Marson AG, Appleton R, Baker GA. , et al. A randomised controlled trial examining the longer-term outcomes of standard versus new antiepileptic drugs. The SANAD trial. Health Technol Assess 2007; 11 (37) iii-iv , ix–x, 1–134
    CrossrefPubMedGoogle Scholar