Electroencephalographic findings among inpatients with COVID-19 in a tertiary hospital from a middle-income country

ABSTRACT

Background: In 2019, the world witnessed the emergence of a new type of coronavirus - the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The spectrum of coronavirus disease 2019 (COVID-19) is variable, and amongst its manifestations are neurological implications. Objective: This report aimed to describe electroencephalographic findings in COVID-19 patients from a general tertiary hospital in São Paulo, Brazil. Methods: It was a retrospective, observational, and non-interventional study. Data were collected anonymously, comprising inpatients from Mar 1 to Jun 30, 2020, either confirmed (positive RT-PCR) or probable cases (CO-RADS 4/5) who had performed EEG during hospitalization. Results: Twenty-eight patients were enrolled, 17 (60.7%) women and 11 men, with a median age of 58 (minimum and maximum: 18-86; IQR 23.5). COVID-19 diagnosis was confirmed in 22 (78.5%). Twenty-one patients (75%) had severe disease, requiring mechanical ventilation due to acute respiratory distress syndrome (ARDS); 16 (57.1%) patients developed adjunct sepsis throughout hospitalization. There was no specific pattern found for COVID-19 in EEG. No patients presented with status epilepticus or electrographic events; most patients developed an encephalopathic pattern, as seen in most studies, with a high prevalence of altered mental status as an indication for EEG. Adjunct sepsis was associated with higher mortality. Conclusions: EEG presents as a useful tool in the context of COVID-19, as in other conditions, to differentiate nonconvulsive status epilepticus (NCSE) from encephalopathy and other causes of mental status alterations. Further studies are required to analyze whether there might be a specific EEG pattern to the disease.

RESUMO

Antecedentes: Em 2019, testemunhou-se o surgimento de um novo tipo de coronavírus - o coronavírus associado à síndrome da angústia respiratória tipo 2 (SARS-CoV-2). O espectro da doença associada ao novo coronavírus, a COVID-19, é variável e, dentre suas manifestações, há implicações neurológicas. Objetivos: O presente estudo objetivou descrever achados eletroencefalográficos em pacientes com COVID-19 internados em um hospital terciário em São Paulo. Métodos: Tratou-se de estudo observacional, retrospectivo e não-intervencionista, realizado por meio de coleta anônima e retrospectiva de dados de prontuário médico de pacientes com diagnóstico confirmado (RT-PCR positivo) ou provável (CO-RADS 4 ou 5), que realizaram eletroencefalograma durante internação hospitalar. Resultados: Vinte e oito pacientes foram elencados, 17 (60,7%) mulheres e 11 homens. O diagnóstico de COVID-19 foi confirmado em 22 (78,5%) dos casos. Dos pacientes, 21 (75%) apresentaram a doença, requerendo suporte ventilatório, e 16 (57,1%) desenvolveram sepse sobreposta. Não houve padrão específico de EEG para COVID-19, e nenhum paciente apresentou estado de mal epiléptico ou crise eletrográfica; a maioria desenvolveu padrão de encefalopatia, com alentecimento da atividade cerebral, sendo a alta prevalência de alteração de estado mental a indicação para o exame. A sepse sobreposta foi associada a um pior desfecho, com maior mortalidade. Conclusão: No contexto da COVID-19, o EEG figura como ferramenta importante, auxiliando, como em outras condições, na diferenciação entre estado de mal epiléptico, encefalopatia e outras causas de alteração do estado mental. Estudos adicionais são necessários para avaliar a existência de padrão específico de alteração eletroencefalográfica na COVID-19.

Keywords:

Electroencephalography - Betacoronavirus - Encephalopathy - Status Epilepticus

Palavras-chave:

Eletroencefalografia - Betacoronavírus - Encefalopatias - Estado Epiléptico

Authors’ contributions:

All authors contributed to text-proofreading and data collection. LAC: was responsible for database reviewing and main text writing. JFST: was responsible for graphics design and descriptive statistics. MAB and Mariana AB additionally reviewed electroencephalograms. SMDB, LAC, MSGR, and MAB were responsible for study conception.

Publication History

Received: 27 November 2020

Accepted: 16 February 2021

Article published online:
01 June 2023

• REFERENCES

• 1 Hepburn M, Mullaguri N, George P, Hantus S, Punia V, Bhimraj A, et al. acute symptomatic seizures in critically ill patients with COVID-19: is there an association? Neurocrit Care. 2021 Feb;34(1):139-43. https://doi.org/10.1007/s12028-020-01006-1
• 2 Chaumont H, Etienne P, Roze E, Couratier C, Roger PM, Lannuzel A. Acute meningoencephalitis in a patient with COVID-19. Rev Neurol (Paris). 2020 Jun;176(6):519-21. https://doi.org/10.1016/j.neurol.2020.04.014
• 3 Brucki S, Corazza L, Queiroz A, Barros M, Tatsch J, Riso I, et al. Neurological complications in COVID-19 patients from Latin America. Brain. 2020 Dec;awaa440. https://doi.org/10.1093/brain/awaa440
• 4 Prokop M, van Everdingen W, van Rees Vellinga T, Quarles van Ufford J, Stöger L, Beenen L, et al. CO-RADS-A categorical CT assessment scheme for patients with suspected COVID-19: definition and evaluation. Radiology. 2020 Aug;296(2):E97-104. https://doi.org/10.1148/radiol.2020201473
• 5 Rábano-Suárez P, Bermejo-Guerrero L, Méndez-Guerrero A, Parra-Serrano J, Toledo-Alfocea D, Sánchez-Tejerina D, et al. Generalized myoclonus in COVID-19. Neurology. 2020 Aug 11;95(6):e767-72. https://doi.org/10.1212/WNL.20200555202005559829
• 6 Mao L, Jin H, Wang M, Hu Y, Shengcai C, Quanwei H, et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Jun;77(6): 1-9. https://doi.org/10.1001/jamaneurol.2020.1127
• 7 Parsons T, Banks S, Bae C, Gelber J, Alahmadi H, Tichauer M. COVID-19-associated acute disseminated encephalomyelitis (ADEM). J Neurol. 2020 May:1-4. https://doi.org/10.1007/s00415-020-09951-9
• 8 Pasini E, Bisulli F, Volpi L, Minardi I, Tappatà M, Muccioli L, et al. EEG findings in COVID-19 related encephalopathy. Clin Neurophysiol. 2020 Sep;131(9):2265-7. https://doi.org/10.1016/j.clinph.2020.07.003
• 9 Ellul MA, Benjamin L, Singh B, Lant S, Daniel Michael B, Easton A, et al. Neurological associations of COVID-19. Lancet Neurol. 2020 Sep;19(9):767-783.. https://doi.org/10.1016/S1474-4422(20)30221-0
• 10 Canham LJW, Staniaszek LE, Mortimer AM, Nouri LF, Kane NM. Electroencephalographic (EEG) features of encephalopathy in the setting of COVID-19: a case series. Clin Neurophysiol Pract. 2020;5:199-205. https://doi.org/10.1016/j.cnp.2020.06.001
• 11 Koutroumanidis M, Gratwicke J, Sharma S, Whelan A, Tan SV, Glover G. Alpha coma EEG pattern in patients with severe COVID-19 related encephalopathy. Clin Neurophysiol. 2021 Jan;132(1):218-25. https://doi.org/10.1016/j.clinph.2020.09.008
• 12 Pilotto A, Maschiocchi S, Volonghi I, del Zotto E, Magni E, De Giuli V, et al. The clinical spectrum of encephalitis in COVID-19 disease: the ENCOVID multicentre study. medRxiv. 2020. 2020.06.19.20133991. https://doi.org/10.1101/2020.06.19.20133991
• 13 Duong L, Xu P, Liu A. Meningoencephalitis without respiratory failure in a young female patient with COVID-19 infection in Downtown Los Angeles, early April 2020. Brain Behav Immun. 2020 Jul;87:33. https://doi.org/10.1016/j.bbi.2020.04.024
• 14 Espinosa PS, Rizvi Z, Sharma P, Hindi F, Filatov A. Neurological Complications of Coronavirus Disease (COVID-19): Encephalopathy, MRI Brain and Cerebrospinal Fluid Findings: Case 2. Cureus. 2020 May;12(5):e7930. https://doi.org/10.7759/cureus.7930
• 15 Farhadian S, Glick LR, Vogels CBF, Thomas J, Chiarella J, Casanovas-Massana A, et al. Acute encephalopathy with elevated CSF inflammatory markers as the initial presentation of COVID-19. BMC Neurol. 2020 Jun;20(1):248. https://doi.org/10.21203/rs.3.rs-28583/v1
• 16 Galanopoulou AS, Ferastraoaru V, Correa DJ, Cherian K, Duberstein S, Gursky J, et al. EEG findings in acutely ill patients investigated for SARS-CoV-2/COVID-19: asmall case series preliminary report. Epilepsia Open. 2020 May;5(2):314-24. https://doi.org/10.1002/epi4.12399
• 17 Virhammar J, Kumlien E, Fällmar D, Frithiof R, Jackmann S, Sköld MK, et al. Acute necrotizing encephalopathy with SARS-CoV-2 RNA confirmed in cerebrospinal fluid. Neurology. 2020 Sep;95(10):445-9. https://doi.org/10.1212/WNL.202005550000010250
• 18 Ashraf M, Sajed S. Seizures related to coronavirus disease (COVID-19): case series and literature review. Cureus. 2020 Jul;12(7):e9378. https://doi.org/10.7759/cureus.9378
• 19 Narula N, Joseph R, Katyal N, Daouk A, Acharya S, Avula A, et al. Seizure and COVID-19: association and review of potential mechanism. Neurol Psychiatry Brain Res. 2020 Dec;38:49-53. https://doi.org/10.1016/j.npbr.2020.10.001
• 20 Helms J, Kremer S, Merdji H, Schenck M, Severac F, Clere-Jehl R, et al. Delirium and encephalopathy in severe COVID-19: a cohort analysis of ICU patients. Crit Care. 2020 Aug;24:491. https://doi.org/10.1186/s13054-020-03200-1
• 21 Ayub N, Cohen J, Jing J, Jain A, Tesh R, Mukerji SS, et al. Clinical electroencephalography findings and considerations in hospitalized patients with coronavirus SARS-CoV-2. medRxiv. 2020 Jul;2020.07.13.20152207. https://doi.org/10.1101/2020.07.13.20152207
• 22 Louis S, Dhawan A, Newey C, Nair D, Jehi L, Hantus S, et al. Continuous electroencephalography characteristics and acute symptomatic seizures in COVID-19 patients. Clin Neurophysiol 2020 Nov;131(11):2651-56. https://doi.org/10.1016/j.clinph.2020.08.003
• 23 Pastor J, Vega-Zelaya L, Martín Abad E. Specific EEG encephalopathy pattern in SARS-CoV-2 patients. J Clin Med. 2020 May;9:1545. https://doi.org/10.3390/jcm9051545
• 24 Antony A, Zulfi H. Systematic review of EEG findings in 617 patients diagnosed with COVID-19. Seizure. 2020 Dec;83:234-41. https://doi.org/10.1016/j.seizure.2020.10.014
• 25 Pellinen J, Carroll E, Friedman D, Boffa M, Dugan P, Friedman DE, et al. Continuous EEG findings in patients with COVID-19 infection admitted to a New York academic hospital system. Epilepsia. 2020 Oct;61(10):2097-105. https://doi.org/10.1111/epi.16667
• 26 Cecchetti G, Vabanesi M, Chieffo R, Fanelli G, Minicucci F, Agosta F, et al. Cerebral involvement in COVID-19 is associated with metabolic and coagulation derangements: an EEG study. J Neurol. 2020 Nov;267(11):3130-4. https://doi.org/10.1007/s00415-020-09958-2
• 27 Cani I, Barone V, D'Angelo R, Pisani L, Allegri V, Spinardi L, et al. Frontal encephalopathy related to hyperinflammation in COVID-19. J Neurol. 2020 Jul:1-4. https://doi.org/10.1007/s00415-020-10057-5
• 28 Chen W, Toprani S, Werbaneth K, Falco-Walter J. Status epilepticus and other EEG findings in patients with COVID-19: a case series. Seizure. 2020 Oct;81:198-200. https://doi.org/10.1016/j.seizure.2020.08.022
• 29 Flamand M, Perron A, Buron Y, Szurhaj W. Pay more attention to EEG in COVID-19 pandemic. Clin Neurophysiol. 2020 Aug;131(8):2062-4. https://doi.org/10.1016/j.clinph.2020.05.011
• 30 Rodrigo-Armenteros P, Uterga-Valiente JM, Zabala-Del-Arco J, Taramundi-Argüeso S, Erburu-Iriarte M, Antón-Méndez L, et al. Non-convulsive status epilepticus in a patient with COVID-19 infection. Clin Neurophysiol. 2020 Nov;131(11):2588-90. https://doi.org/10.1016/j.clinph.2020.08.005
• 31 Somani S, Pati S, Gaston T, Chitlangia A, Agnihotri S. De Novo Status Epilepticus in patients with COVID-19. Ann Clin Transl Neurol. 2020 Jul;7(7):1240-4. https://doi.org/10.1002/acn3.51071
• 32 Vellieux G, Rouvel-Tallec A, Jaquet P, Grinea A, Sonneville R, d'Ortho MP. COVID-19 associated encephalopathy: is there a specific EEG pattern? Clinical Neurophysiology. 2020 Aug;131(8):1928-30. https://doi.org/10.1016/j.clinph.2020.06.005.
• 33 Vespignani H, Colas D, Lavin BS, Soufflet C, Maillard L, Pourcher V, et al. Report on Electroencephalographic Findings in Critically Ill Patients with COVID-19. Ann Neurol. 2020 Sep;88(3):626-30. https://doi.org/10.1002/ana.25814
• 34 Petrescu AM, Taussig D, Bouilleret V. Electroencephalogram (EEG) in COVID-19: a systematic retrospective study. Neurophysiol Clin. 2020 Jul;50(3):155-65. https://doi.org/10.1016/j.neucli.2020.06.001
• 35 Elgamasy S, Kamel MG, Ghozy S, Khalil A, Morra ME, Islam SMS. First case of focal epilepsy associated with SARS-coronavirus-2. J Med Virol. 2020 Oct;92(10):2238-42. https://doi.org/10.1002/jmv.26113.
• 36 Vollono C, Rollo E, Romozzi M, Frisullo G, Servidei S, Borghetti A, et al. Focal status epilepticus as unique clinical feature of COVID-19: a case report. Seizure. 2020 May;78:109-12. https://doi.org/10.1016/j.seizure.2020.04.009
• 37 Skorin I, Carrillo R, Perez CP, Sanchez N, Parra J, Troncoso P, et al. EEG findings and clinical prognostic factors associated with mortality in a prospective cohort of inpatients with COVID-19. Seizure. 2020 Dec;83:1-4. https://doi.org/10.1016/j.seizure.2020.10.007