key: cord-0958369-vgo0p8i5
authors: Asadi-Pooya, Ali A.; Simani, Leila; Shahisavandi, Mina; Barzegar, Zohreh
title: COVID-19, de novo seizures, and epilepsy: a systematic review
date: 2020-11-25
journal: Neurol Sci
DOI: 10.1007/s10072-020-04932-2
sha: cfe7e62ef41344e39ef1f436b05486e682313479
doc_id: 958369
cord_uid: vgo0p8i5

OBJECTIVE: We discuss the evidence on the occurrence of de novo seizures in patients with COVID-19, the consequences of this catastrophic disease in people with epilepsy (PWE), and the electroencephalographic (EEG) findings in patients with COVID-19. METHODS: This systematic review was prepared according to the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement. MEDLINE, Scopus, and Embase from inception to August 15, 2020 were systematically searched. These key words were used: “COVID” AND “seizure” OR “epilepsy” OR “EEG” OR “status epilepticus” OR “electroencephalography”. RESULTS: We could identify 62 related manuscripts. Many studies were case reports or case series of patients with COVID-19 and seizures. PWE showed more psychological distress than healthy controls. Many cases with new-onset focal seizures, serial seizures, and status epilepticus have been reported in the literature. EEG studies have been significantly ignored and underused globally. CONCLUSION: Many PWE perceived significant disruption in the quality of care to them, and some people reported increase in their seizure frequency since the onset of the pandemic. Telemedicine is a helpful technology that may improve access to the needed care for PWE in these difficult times. De novo seizures may occur in people with COVID-19 and they may happen in a variety of forms. In addition to prolonged EEG monitoring, performing a through metabolic investigation, electrocardiogram, brain imaging, and a careful review of all medications are necessary steps. The susceptibility of PWE to contracting COVID-19 should be investigated further.

Since late 2019, the world has been experiencing a catastrophic pandemic of a new coronavirus disease (COVID-19) caused by SARS-CoV2 . [1] . Previous outbreaks of coronaviruses consist of the severe acute respiratory syndrome (SARS) in 2002 and the Middle East respiratory syndrome (MERS) in 2012 . [2] Coronaviruses primarily target the human respiratory system. However, they have also been associated with neurological manifestations (e.g., seizures, change in mental status, and encephalitis) . [2, 3] . Neurotropic and neuroinvasive capabilities of coronaviruses have been described before . [4] .

The signs and symptoms of COVID-19 infection often appear after an incubation period of about five days [1] . The most frequent manifestations at the onset of COVID-19 illness are fever, cough, loss of smell and taste, and fatigue; other manifestations may include headache, hemoptysis, diarrhea, and dyspnea. In patients with severe disease, pneumonia, acute respiratory distress syndrome, organ failure, metabolic derangements, and acute cardiac injury may happen [1] . It is reasonable to expect that some patients with COVID-19 develop seizures as a consequence of hypoxemia, organ failure, metabolic derangements, drug-drug interactions, or even brain damage that may occur in patients with COVID-19 [2, 3, 5] .

On the other hand, information on the susceptibility of people with epilepsy (PWE) to contracting COVID-19 and the consequences and challenges of this catastrophic disease in PWE are scarce.

In the current systematic review, we will discuss the evidence on the occurrence of de novo seizures in patients with COVID-19 (the types of seizures and the etiology), the consequences, and challenges of this catastrophic disease in PWE (e.g., access to care and seizure control), and finally, the electroencephalographic (EEG) findings in patients with COVID-19. We will also provide suggestions to tackle the abovementioned issues based on the best available evidence.

This manuscript was prepared according to the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [6, 7] (Fig. 1 and Table 1 ). MEDLINE (accessed from PubMed), Scopus, and Embase from inception to August 15, 2020 were systematically searched for related published articles. In all electronic databases, the following search strategy was implemented and these key words (in the title/abstract) were used: "COVID" AND "seizure" OR "epilepsy" OR "EEG" OR "status epilepticus" OR "electroencephalography". Articles written in English were all included. To ensure literature saturation, the authors scanned the reference lists of the included studies or relevant articles identified through the search. All authors participated through each phase of the review independently (screening, eligibility, and inclusion). They obtained full reports for all titles that appeared to meet the inclusion criteria or where there was any uncertainty. They resolved any disagreement through discussions. Neither of the authors were blind to the journal titles nor the study authors or institutions.

The following data were extracted from the included studies: study authors, study location, study designs, main results, and limitations. The methodological quality of the included studies was assessed by the authors. The class of evidence was defined following the American Academy of Neurology criteria for classification of evidence in studies of causation (Appendix, Table 5 ) [8] .

The Shiraz University of Medical Sciences Institutional Review Board approved this study and systematic review.

Through the search strategy, we could identify 62 related manuscripts (Tables 2, 3 , and 4) . Only one paper provided class 2 evidence and 11 papers provided class 3 evidence; the rest of the publications provided class 4 evidence. Many studies were case reports or case series of patients with COVID-19 and seizures. The rest of the publications were surveys or observational studies (Tables 2, 3, and 4 ). Below, we summarize the results of this systematic review:

1.1. Epilepsy related papers (Table 2) : One cross-sectional study of 21 patients with active epilepsy and COVID-19 out of 1537 patients (1.4%) with level 2 of evidence showed that the cumulative incidence of COVID-19 in people with epilepsy was higher compared with the population without epilepsy (1.2% vs. 0.5%) [9] . Furthermore, the total case fatality rate was higher in PWE compared to patients without active epilepsy (23.8% vs. 3.6%; p < 0.001) [9] . However, these results were obtained based on a small number of PWE (21 persons) and should be interpreted with caution.

In addition, in another study, among 5700 PWE, who were managed at the studied centers, only 14 people tested positive for SARS-CoV-2, without obvious impacts on their epilepsy [18] . Six surveys of PWE showed that many people perceived significant disruption in the quality and availability of care to them (31 to 95%), as well as increased stress and social isolation, and increase in seizure frequency (6 to 35%) since the onset of the pandemic [11, 12, [14] [15] [16] [17] . One observational comparative study confirmed that PWE showed more psychological distress than healthy controls, and they spent significantly more time following the COVID-19 outbreak news [13] . Finally, four studies showed that telemedicine may improve access to specialized care for PWE in these difficult times [10, [20] [21] [22] . The development of an epilepsy electronic patient portal may promote improved patient-clinician partnerships and facilitate patient self-management [23] 1.2. Seizure-related papers (Table 3) : While one retrospective study reported no seizures in 304 patients with COVID-19 [25] , multiple studies refuted that finding [24, [26] [27] [28] [29] . Furthermore, many cases with new-onset focal seizures, serial seizures, and status epilepticus have been reported in the literature [30-49, 51, 63] . The etiology of seizure(s) in the reported patients was most likely multifactorial, as many of them had comorbidities (e.g., diabetes and kidney disease), multiorgan failure, metabolic derangements, hypoxemia, etc. In addition, all these patients received many medications [33] [34] [35] [36] [37] [38] [39] [40] [41] [42] [43] [44] [45] [46] [47] . However, some of the patients had specific neurological problems (e.g., encephalitis [33, 40, 70] and cerebrovascular events [38, 42, 43, 51, 59] ). SARS-CoV-2 RNA was detected in the cerebrospinal fluid (CSF) in two patients [40, 53] ; however, many other studies that tested for this had negative results [36, 42, 44, 46, 52, 59, 60, 64, 67, 70] . It should be emphasized that many centers did not investigate the patients with COVID-19, who had seizures, thoroughly. For example, many patients did not have EEG exams, and in a significant number of them CSF analysis and even brain imaging studies were not performed. 1.3. EEG-related papers ( Table 4 ): While change in mental status has frequently been reported in patients with COVID-19 [26, 27, 55, 60, 65, 66, 70] , and while there are many reports on clinical and subclinical seizures and status epilepticus in these patients [33-47, 63, 66] , EEG studies have been significantly ignored and underused in these patients globally. Three studies showed that EEG services have been significantly disrupted by the pandemic of COVID-19 [18, 19, 57] . Three other studies showed that many of the patients with COVID-19 and encephalopathy/seizures had epileptiform discharges/seizures in their EEG [29, 54, 55] . One study of two patients with COVID-19 and encephalopathy suggested a unique EEG pattern with continuous, slightly asymmetric, monomorphic, diphasic, delta slow waves with greater amplitude over both frontal areas and with a periodic organization [58] . Finally, two studies suggested that quantitative EEG (QEEG) features may be useful for diagnosis and prognostication of the neurological outcome in critically ill patients with COVID-19 [61, 62] . While studies investigating EEG in patients with COVID-19 did not find a consistent and specific neurophysiological pattern in critically ill patients, the authors should describe the EEG findings more appropriately, adhering to the standardized terminologies, in future studies [71] .

The evidence on the susceptibility of PWE to contracting COVID-19 and the consequences of this catastrophic disease in PWE is scarce. A recent systematic review suggested that patients with pre-existing neurological disorders (including epilepsy) and COVID-19 may develop exacerbation of their neurological problems and also severe COVID-19 [72] . This significant concern should be addressed in the future through well-designed prospective cohort studies with all relevant confounders controlled. However, evidence showed that many PWE perceived significant disruption in the quality and availability of care to them, and some people reported increase in their seizure frequency since the onset of the pandemic [11, 12, 14, 16, 17] . Previous global experiences confirm this piece of evidence. A study of 227 PWE during the SARS outbreak in 2003 in Taiwan demonstrated that 22% of them did not receive their medications due to loss of contact with their healthcare providers; 12% of them experienced seizure control status worsening [73] . In addition, many PWE may have increased stress and social isolation, even more than that in others, during such circumstances as COVID-19 pandemic [12] [13] [14] [15] . During pandemics and other difficult and catastrophic circumstances (e.g., wars and mass displacements), healthcare workers should focus not only on seizure control status of their patients, but also on the mental health of PWE [13] . In such times, stress is associated with increased seizures in PWE [11] , and stress management strategies may play a significant role in helping these patients cope with their ongoing problems more successfully. Research shows that people who follow COVID-19 news the most, experience more anxiety and stress [74, 75] . Healthcare providers should advise their patients to avoid following COVID-19 news frequently. In addition, it might be helpful to use digital communication methods such as social networks to prevent social isolation [75] . Similarly, many patients with epilepsy may have depressive symptoms, particularly during such difficult times, and several factors related to epilepsy (e.g., seizure frequency and quality of life) are significantly correlated with depressive symptoms [76] . Therefore, it is helpful to screen all PWE for anxiety, stress, and depression, and treat any psychological problems that patients may have, particularly during a pandemic or other difficult circumstances. Telemedicine is a viable and helpful technology that may improve access to the needed care for PWE in these difficult times [10, 20, 22] . During a pandemic such as what we are experiencing now, telemedicine, particularly video consultations, ought to be promoted in order to reduce the risk of disease transmission [77] . Telemedicine has been shown to improve access to care for PWE in difficult circumstances (e.g., people living in rural areas) [78] . However, many countries do not have the infrastructure or the regulatory frameworks to authorize, integrate, and reimburse telemedicine services [77] .

Another important issue is the occurrence of new-onset seizures in people with COVID-19. While seizure is not a common manifestation of COVID-19, it may happen in a variety of forms (e.g., focal motor, tonic-clonic, convulsive status epilepticus, and nonconvulsive status epilepticus) [28, [30] [31] [32] [33] [34] [35] [36] [37] [38] [39] [40] [41] [42] [43] [44] [45] [46] [47] . On the other hand, many patients with severe COVID-19 may have changes in their mental status [26, 27] . When visiting a patient who is in a critical medical condition and has a change in mental status, the treating healthcare professional should make sure that nonconvulsive status epilepticus is not a part of the clinical scenario. Prolonged EEG monitoring is required in these circumstances [3] . Electroencephalography is probably one of the most useful tests to help identify the etiology of seizures and/or change in mental status in critically ill patients, including those with COVID-19; and at the same time, it is probably the most neglected test so far in the management process of these patients globally. It is helpful to describe the EEG findings in a systematic and consistent manner in order to characterize any possible distinguishing and/or prognosticating EEG patterns in patients with COVID-19. Finally, quantitative EEG may also be useful for diagnosis and prognostication of the neurological outcome in critically ill patients with COVID-19 [61, 62] .

Seizures may happen as a consequence of hypoxia, metabolic derangements, organ failure, medications, or brain damage that could happen in people with COVID-19 [3, 5] . If a patient with COVID-19 develops a seizure, one should try to Self-report design IV Asadi-Pooya/Iran [12] Survey of 100 patients 31% expressed hardship obtaining their drugs; 6% expressed worsening of their seizure control status in the past 4 weeks.

Self-report design IV Hao/China [13] Cross-sectional study of 252 patients with epilepsy and 252 controls Patients with epilepsy showed more psychological distress than healthy controls and spent significantly more time following the COVID-19 outbreak.

Self-report design IV Miller/USA [14] Survey of 94 patients Significant disruption in epilepsy self-management was reported. Lack of ability to obtain medications or see epilepsy providers, as well as increased stress, and social isolation were reported; 35% reported an increase in seizure frequency since the onset of the pandemic.

Self-report design IV Aledo-Serrano/Spain [15] Survey of 227 patients Three patients with Dravet syndrome had confirmed COVID-19. All of them had mild symptoms, and none needed hospitalization or showed either seizure or behavioral worsening. However, 14% of the whole cohort reported seizure frequency increase and 30% reported behavioral deterioration during the lockdown.

The main variables associated with seizure increase were age and difficulties finding antiseizure medications.

Self-report design IV Assenza/Italy [16] Survey of 456 patients and 472 controls Disruption in epilepsy management was reported in 95%; 18% reported seizure worsening. People with epilepsy had worse depressive and anxiety symptoms.

Self-report design IV Alkhotani/ Saudi Arabia [17] Survey of 156 patients 29.5% reported an increase in seizure frequency. 59% had an increase in self-reported stress. The development of an epilepsy electronic patient portal The system can promote improved patient-clinician partnerships and facilitate patient self-management.

- - A case report of a seizure (67-year-old man)

Tests were not done. The patient died.

-

A case report of tonic-clonic seizure (a 20-year-old man) CSF analysis demonstrated a lymphocytic pleocystosis (21 cells/mm 3 , 99% mononuclear, 1% polymorphs). Brain imaging was normal. The patient remained well and was discharged home. Follow-up EEG was normal.

-

A case report of focal motor seizures (a 73-year-old woman)

CSF analysis was normal. Brain imaging had nonspecific findings. EEG was normal. The patient was discharged home in a good condition.

-

Kadono/Japan [35] A case report of focal motor seizure (a 44-year-old man with known focal epilepsy)

Brain CT scan showed severe brain swelling of the right temporal lobe. CSF analysis was not done. EEG was not done. The patient was discharged home in a good condition.

-

Farhadian/USA [36] A case report of seizure (a 78-year-old woman with kidney transplant) CSF analysis was normal. Levels of IL-6, IL-8, and IP-10 were elevated in both CSF and plasma. EEG showed mild generalized slowing. Brain imaging had nonspecific findings. CSF SARS-CoV-2 was negative.

The patient was discharged home in a good condition.

-IV Kabashneh/USA [37] A case report of seizure (a 54-year-old man with diabetes) CSF analysis was normal. EEG showed mild generalized slowing.

Brain imaging was normal. The patient had diabetic ketoacidosis, acute kidney injury, hypovolemic shock, and hyperammonemia. The patient was discharged home in a good condition.

-IV Efe/Turkey [38] A case report of seizures (a 35-year-old woman)

Brain MRI showed hyperintense signal in the left temporal lobe (an encephalitis mimicking a glial tumor after surgery and pathology examination). CSF analysis was not done. EEG was not done.

- A case report (a 32-year-old man with convulsive status epilepticus)

Brain CT scan was normal. CSF analysis showed elevated protein (2212 mg/L). EEG was not done.

The patient was discharged home in a good condition.

-

Bolaji/UK [51] A case report (a 63-year-old man with status epilepticus)

Brain CT scan showed extensive cerebral venous sinus thrombosis with bilateral venous cortical infarcts and acute cortical hemorrhage. CSF analysis was not done. EEG was not done. The patient was discharged to a rehabilitation center.

-

Monti/Italy [52] A case report (a 50-year-old man with acute onset of psychiatric symptoms and refractory status epilepticus)

EEG showed a delta brush pattern. CSF study showed pleocytosis and anti-NMDA receptors antibodies. CSF SARS-CoV2

PCR was negative. Brain MRI was unremarkable. Four months after the onset, the patient was discharged home in good condition.

-IV CNS, central nervous system; CSF, cerebrospinal fluid; EEG, electroencephalography;

ICU, intensive care unit; CT, computerized tomography; MRI, magnetic resonance imaging;

HIV, human immunodeficiency virus;

PCR, polymerase chain reaction was not detected in the CSF in any case.

Small sample size III Abenza-Abildúa/Spain [68] A case report (a 56-year-old woman with change in mental status) EEG showed generalized slowing. CSF analysis was normal.

Brain MRI was uneventful. The patient remained well.

-

Roy-Gash/France [69] A case report (a 63-year-old woman with status epilepticus) EEG showed focal status epilepticus. CSF analysis was not done.

Brain CT scan showed left temporal hemorrhage with venous thrombosis. The patient died.

-

Pilotto/Italy [70] A case report (a 60-year-old man with change in mental status) EEG showed generalized slowing. CSF analysis showed lymphocytic pleocytosis (18/μL). CSF PCR for SARS-CoV-2 was negative. Brain MRI was normal. The patient was discharged home in a good condition.

-IV CSF, cerebrospinal fluid; EEG, electroencephalography; CT, computerized tomography; MRI, magnetic resonance imaging;

PCR, polymerase chain reaction;

QEEG, quantitative EEG determine the etiology of the seizure and manage the cause (e.g., hypoxia and metabolic derangements) immediately. In addition to prolonged EEG monitoring, performing a thorough metabolic investigation, electrocardiogram, brain imaging, and a careful review of all medications (for adverse drug reactions and also drug-drug interactions) are necessary steps. CSF analysis is also necessary, at least to investigate other causes for acute symptomatic seizures that may happen concomitantly or that may mimic the clinical picture of COVID-19 (e.g., herpes simplex virus-1 encephalitis) [79] . In addition, it is often necessary to start an antiseizure medication (ASM) for a patient with COVID-19 and seizure(s); this is to abort prolonged seizures and also to prevent further seizures from happening [3] . It should be emphasized that patients with acute symptomatic seizures do not need long-term ASM therapy after the period of acute illness, unless a subsequent seizure happens [80] . For a comprehensive review on these issues, please refer to the references [3, 5, 81] .

What we know and should pay more attention to

Many PWE perceived significant disruption in the quality and availability of care to them, and some people reported increase in their seizure frequency since the onset of the pandemic. In addition, many PWE may have increased stress and anxiety.

During pandemics and other difficult and catastrophic circumstances, healthcare workers should focus not only on seizure control status of their patients, but also on the mental health of PWE.

Telemedicine is a viable and helpful technology that may improve access to the needed care for PWE in these difficult times. The current COVID-19 pandemic is a strong call to develop the required infrastructure and to adopt the appropriate regulatory frameworks for implementation of telemedicine services globally [77] .

De novo seizures may occur in people with COVID-19, and they may happen in a variety of forms (e.g., focal motor, tonic-clonic, convulsive status epilepticus, nonconvulsive status epilepticus, and post SARS-CoV2 autoimmune encephalitis associated with new-onset refractory status epilepticus (NORSE) [82, 83] ). Furthermore, many patients with severe COVID-19 may have change in mental status. If a patient with COVID-19 develops a seizure or change in mental status, one should try to determine the etiology and manage the cause immediately. In addition to prolonged EEG monitoring, performing a thorough metabolic investigation, electrocardiogram, brain imaging, CSF analysis, and a careful review of all medications are necessary steps.

The evidence on the susceptibility of PWE to contracting COVID-19 and the consequences of this catastrophic disease in PWE is scarce. This significant concern should be addressed in the future through well-designed prospective cohort studies with all relevant confounders controlled.

SARS-CoV-2 RNA was detected in the CSF in two patients, but many other studies that tested for this had negative results. This is important to clarify the role of neurtropism and neuroinvasiveness of this virus in causing seizures in future studies.

It is not clear whether there is a unique EEG pattern for COVID-19 encephalopathy. It is helpful to describe the EEG findings in a systematic and consistent manner in order to characterize any possible distinguishing and/or prognosticating EEG patterns in patients with COVID-19.

Contributions Ali A. Asadi-Pooya: Designed and conceptualized the study; collected the data; analyzed the data; drafted and revised the manuscript.

Leila Simani, Mina Shahisavandi, Zohreh Barzegar: Collected the data; revised the manuscript.

Funding This study is supported by Shiraz University of Medical Sciences.

Data availability Data sharing is not applicable to this article.

Conflict of interest Ali A. Asadi-Pooya, M.D.: Honoraria from Cobel Daruo, RaymandRad and Tekaje; Royalty: Oxford University Press (book publication). Others: none.

Ethical approval The Shiraz University of Medical Sciences Institutional Review Board approved this study and systematic review.

Research involving human participants and/or animals Not applicable.

Informed consent Not applicable.

Role of the funding source Shiraz University of Medical Sciences had no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

None of the authors listed on the manuscript are employed by a government agency. All are academicians. None of the authors are submitting this manuscript as an official representative or on behalf of the government. 

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