Multiple Sclerosis and Related Disorders 62 (2022) 103795

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Multiple Sclerosis and Related Disorders

journal homepage: www.elsevier.com/locate/msard

Review article

Autoimmune encephalitis associated with COVID-19: A systematic review

Fardin Nabizadeh a, Mohammad Balabandian a, Fatemeh Sodeifian b, Negin Rezaei c,
Mohammad Reza Rostami a, Abdorreza Naser Moghadasi d, *
a
Neuroscience Research Group (NRG), Universal Scientific Education and Research Network (USERN), Tehran, Iran
b
Student Research Committee, School of Medicine, Shahid Beheshti University of Medical Science, Tehran, Iran
c
Student Research Committee, Iran University of Medical Sciences, Tehran, Iran
d
Multiple Sclerosis Research Center, Neuroscience Institute, Tehran University of Medical Sciences, Tehran, Iran

A R T I C L E I N F O A B S T R A C T

Keywords: Introduction: There are increasing reports of COVID-19 related neurological complications which may be due to
COVID-19 direct viral invasion, or immune mediated inflammatory diseases such as autoimmune encephalitis and ADEM
Autoimmune encephalitis (acute demyelinating encephalomyelitis). In this study, a systematic review is presented of the reported cases
Systematic review
infected by the COVID-19 who were diagnosed with various forms of autoimmune encephalitis (AE).
Methods: The authors searched three databases including PubMed, Scopus, and Web of science for extracting
original articles on coronavirus/ COVID-19 and AE.
Results: Eighteen articles were considered in this study, including 15 case reports, and three case series with a
total of 81 patients. Among the studies, 19 cases were reported with AE including 7 (37%) cases of limbic en­
cephalitis, 5 (26%) patients with anti-N-methyl-D-aspartate (NMDA) receptor encephalitis, 2 (11%) with AE
presenting as new-onset refractory status epilepticus (NORSE), 1 (5%) case of steroid-responsive encephalitis,
and 4 (21%) cases with an unknown type of AE.
Conclusion: Our systematic review revealed evidence on AE development in patients infected with the COVID-19.
Clinicians should be aware of the possible diagnosis of AE when considering other neurological differential
diagnosis in SARS-CoV-2 infected patients.

1. Introduction including ischemic stroke and hemorrhage, ADEM, encephalopathy, and

myopathy (Liu et al., 2020a; Helms et al., 2020; Guilmot et al., 2021).
The novel coronavirus disease (COVID-19) appeared for the first time In the following, a systematic review can be found of the reported
in Wuhan of China in December 2019 (Lu et al., 2020). Caused by the cases who were infected by the COVID-19, and diagnosed with various
SARS-CoV-2 virus (severe acute respiratory syndrome coronavirus 2), it forms of autoimmune encephalitis (AE).
is a member of the family of coronaviruses infecting humans which is
responsible for lower respiratory infection and can cause acute respi­ 2. Methods
ratory distress syndrome (ARDS) (Zhou et al., 2020; Chen et al., 2020).
According to previous reports, there are confirmed cases with 2.1. Design
neurological manifestations who developed the disease either via direct
attack to the central nervous system (CNS) or via autoimmune processes This systematic review was conducted based on Preferred Reporting
(Sánchez-Morales et al., 2021a; Bhagat et al., 2021). New evidence has for Systematic Review and Meta-Analysis (PRISMA) (Moher et al.,
identified an association between the COVID-19 and systemic autoim­ 2009).
mune diseases like autoimmune hemolytic anemia or one-organ-specific
diseases like Guillain-Barre syndrome (Toscano et al., 2020; Lazarian
et al., 2020). Several neurological complications have now been 2.2. Search strategy
described: encephalitis, meningitis, and cerebrovascular diseases
We searched three databases of Pubmed, Scopus, and Web of science

* Corresponding author.
E-mail address: [email protected] (A. Naser Moghadasi).

https://doi.org/10.1016/j.msard.2022.103795
Received 27 April 2021; Received in revised form 17 January 2022; Accepted 31 March 2022
Available online 6 April 2022
2211-0348/© 2022 Elsevier B.V. All rights reserved.
F. Nabizadeh et al. Multiple Sclerosis and Related Disorders 62 (2022) 103795

Fig. 1. PRISMA flow diagram depicting the flow of information through the different phases of a systematic review.

for extracting original articles on coronavirus/ COVID-19 and autoim­ 2.5. Data extraction
mune encephalitis (AE) on the 1st of April. The search strategy consisted
of keywords including “Autoimmune encephalitis”, “Limbic encephali­ The same reviewers (M.B and M.R) independently extracted the
tis”, “Anti NMDA”, “Anti VGKC”, “Anti LGI1”, “Anti CASPR2”, “Anti following data manually: author, year, country, study design, number of
AMPA”, “Anti GAD65”, “Anti GABA”, “Anti GABAA”, “Anti GABAB”, patients, mean age, sex, number of AE cases, type of AE, and symptoms.
“Anti D2”, “Anti Dopamine-2′′ , “Anti DPPX”, “Anti Glycine”, “Anti
GlyR”, “Anti Glutamate”, “Anti mGluR1”, “Anti mGluR5”, “Anti 2.6. Data syntheses and analyses
amphiphysin”, “Anti Neuronal”, “Anti CV2”, “Anti Ta”, “Anti Purkinje”,
“COVID-19′′ , “Sars-Cov-2′′ , and “coronavirus”. The quantitative data was represented as percentage or mean ±
standard deviation. Studies and results were qualitatively compared.
2.3. Eligibility criteria
3. Results
We included the studies have reported the AE related to COVID-19
3.1. Eligible publications
infection. The studies with other types of encephalitis or unconfirmed
cases of autoimmune encephalitis were excluded.
Our comprehensive literature search yielded a total of 208 articles.
After removing duplicates and screening titles and abstracts, 22 reports
2.4. Study selection remained; however, after full text reviews, four studies did not meet the
inclusion criteria. Finally, qualitative synthesis was performed on18
Articles were independently selected by two investigators (M.B and studies (Fig. 1).
M.R) following two steps. First, the title and abstract were screened. In
the next step, the full texts of the selected studies were reviewed ac­ 3.2. Study characteristics
cording to eligibility criteria. At the end of each step, any disagreements
were resolved by discussing the issue with the third investigator (F.N). Among the included studies, there were 15 case report studies, two

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F. Nabizadeh et al. Multiple Sclerosis and Related Disorders 62 (2022) 103795

Table 1
Charcteristics and autoimmune encephaltis of included studies.
Author year country Study number age gender total number SARS-CoV-2 Encephalitis laboratory type of presenting signs
design of of laboratory results autoimmune
patients encephalitis results encephalitis
cases

Ayatollahi 2020 Iran, case 1 18 Female 1 SARS-CoV-2 MRI: normal, EEG: NM drowsiness,
Canada report rRT-PCR: showed moderate confusion, urinary
positive, SARS- intermittent retention,
CoV-2 CSF PCR: nonepileptiform generalized tonic-
negative, Lung abnormality over the clonic seizure
CT scan: normal frontocentrotemporal
regions
Zambreanu 2020 UK case 1 66 Female 1 SARS-CoV-2 MRI: symmetrical T2 Limbic confusion,
report rRT-PCR: and FLAIR encephalitis amnestic
positive, SARS- hyperintensities,
CoV-2 IgG: Diffusion MRI:
negative, SARS- punctate bright signal
CoV-2 CSF PCR: on the B1000 map in
negative the medial temporal
lobes, thalami and
fornices, Autoantibody
testing of
immunemediated
encephalitis: negative
Grimaldi 2020 France case 1 72 Male 1 Lung CT scan: EEG: symmetric diffuse NM action tremor,
report peripheral background, MRI: ataxia, dysarthria
bilateral ground- normal, F-FDG PET: and upper limbs
glass lesions and putaminal and dysmetria
consolidative cerebellum
opacities, SARS- hypermetabolism
CoV-2 rRT-PCR: associated with diffuse
positive first cortical
then turned to hypometabolism,
negative, SARS- serum IgG isotype
CoV-2 IgG and autoantibodies: High
IgM: negative
Manganotti 2021 Italy case 2 54 Male 1 SARS-CoV-2 EEG: generalized autoimmune convulsive status
report rRT-PCR: epileptic discharges encephalitis epilepticus,
positive with bilateral frontal presenting as generalized
high amplitude delta new-onset myoclonic jerks of
waves, MRI: normal refractory axial muscles and
status face
epilepticus
(NORSE)
Pilotto 2020 Italy case 25 65/ 15 2 RT PCR: positive NM Limbic altered mental
series 9 Male/ encephalitis status, aphasia,
10 seizure, focal
Female motor deficits
Khoo 2020 UK case 1 65 Female 1 SARS-CoV-2 MRI: normal, CSF white NM involuntary
report rRT-PCR: cell count: normal, movements, only
positive, Chest Autoantibody testing of speak in native
X-ray: bilateral immunemediated language,
peripheral encephalitis: negative, speaking
pulmonary EEG: normal, difficulties and
infiltrates increasing
confusion.
Pilotto 2020 Italy, case 1 60 Male 1 SARS-CoV-2 CSF: mild lymphocytic Steroid- severe akinetic
UK, report rRT-PCR: pleocytosis and responsive syndrome, unable
sweden positive, Chest moderate increase of encephalitis to carry out simple
X-ray: moderate CSF protein, EEG: orders,
bilateral generalized slowing palmomental and
interstitial with decreased glabella reflexes,
pneumonia, reactivity to acoustic nuchal rigidity,
SARS-CoV-2 CSF stimuli, MRI: normal,
PCR: negative Autoantibody testing of
immunemediated
encephalitis: negative
Wang 2020 China case 1 68 Male 1 Lung CT scan: Brain CT scan: lacunar NM unable to walk,
report groundglass lesions in the left basal uroclepsia,
shadows in both ganglia region coprolalia, and
lungs, PCR: persecution
negative, SARS- delusion.
CoV-2 IgG and
IgM: negative
and positive,
respectivly,
(continued on next page)

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F. Nabizadeh et al. Multiple Sclerosis and Related Disorders 62 (2022) 103795

Table 1 (continued )
Author year country Study number age gender total number SARS-CoV-2 Encephalitis laboratory type of presenting signs
design of of laboratory results autoimmune
patients encephalitis results encephalitis
cases

SARS-CoV-2 CSF
IgG and IgM:
positive,
Burr 2020 USA case 1 2 Female 1 SARS-CoV-2 MRI: normal, serum Anti-NMDA fever, fussiness,
report PCR: positive, and CSF NMDA receptor poor sleep,
SARS-CoV-2 CSF receptor autoantibody: encephalitis constipation,
PCR: negative, positive decreased oral
SARS-CoV-2 IgG: intake, fussy, not
positive talking, constant
kicking and
thrashing
movements of
arms and legs.
Dhillon 2021 UK cohort 29 68/ 16 1 SARS-CoV-2 CSF MRI; Lesions in the Limbic acute-onset
9 Male/ PCR: negative limbic system, encephalitis delirium, altered
13 predominantly in the mental status,
Female left amygdala and status epilepticus,
hippocampus with cognitive
partial restricted impairment
diffusion,
Autoantibody testing of
immunemediated
encephalitis: negative
Sánchez- 2021 Mexico case 10 11/ 5 1 SARS-CoV-2 CSF NM Anti-NMDA Altered behavior
Morales series 8 Male/ PCR: positive, receptor and mental status,
5 Serum SARS- encephalitis seizures,
Female CoV-2 IgM and insomnia,
IgG: negative, orolingual
CSF antibodies dyskinesias
SARS-CoV-2 IgG:
positive
Dono 2020 Italy case 1 81 Male 1 Chest X-ray: EEG: normal, MRI: autoimmune drowsy with
report normal, Lung CT hyperintense lesions of encephalitis Glasgow coma
scan: ground- the bilateral parietal presenting as scale (GCS) of 5
glass pattern in cortex, left temporal new-onset (no eyes opening
both the inferior cortex, and right refractory both to verbal and
lobe segments, cingulate cortex, status pain stimulation,
SARS-CoV-2 Autoantibody testing of epilepticus no verbal
PCR: positive, immunemediated (NORSE) response, and
SARS-CoV-2 CSF encephalitis: negative flexion of the
PCR: negative upper limbs to
pain),
Contemporarily,
frequent jerky
myoclonic con-
tractions of the
abdomen and the
right lower limb
appeared.
Bhagat 2020 USA case 1 54 Male 1 SARS-CoV-2 MRI: hyperintensity on Limbic nonradiating
report rRT-PCR: right posterior medial encephalitis pressure type
positive, Chest temporal lobe, holocranial
X-ray: normal Autoantibody testing of headache,
immunemediated diaphoresis,
encephalitis: negative, palpitation,
EEG: right posterior nausea drowsy,
quadrant lateralized oriented to time,
periodic discharges place, and person
with intact
language, cranial
nerves, motor,
sensory, and
cerebellar
functions
Monti 2020 Italy case 1 50 Male 1 SARS-CoV-2 anti-NMDA receptors Anti-NMDA confabulations
report rRT-PCR: antibodies in CSF: receptor and delirious
positive, Lung positive, MRI: normal encephalitis ideas, focal motor
CT scan: normal seizures with
impaired
awareness and
oro-facial
dyskinesia/
automatisms,
(continued on next page)

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F. Nabizadeh et al. Multiple Sclerosis and Related Disorders 62 (2022) 103795

Table 1 (continued )
Author year country Study number age gender total number SARS-CoV-2 Encephalitis laboratory type of presenting signs
design of of laboratory results autoimmune
patients encephalitis results encephalitis
cases

refractory status
epilepticus
Hosseini 2020 UK case 2 62/ Male 1 SARS-CoV-2 MRI: partial diffusion Limbic dysphasia and
report 5 rRT-PCR: restriction in limbic encephalitis impaired
positive, SARS- system orientation,
CoV-2 CSF PCR: attention and
negative, Lung memory.
CT scan:
bilateral pleural
effusion
Pizzanelli 2021 Italy case 1 74 Female 1 Lung CT scan: Brain CT scan: normal, Limbic mild confusion
report bilateral diffuse EEG: focal seizures encephalitis and a brief
areas of ground- with impaired episode of non-
glass pattern awareness and oral responsivity with
with subpleural automatisms, staring
parenchymal Autoantibody testing of
consolidations, immunemediated
SARS-CoV-2 encephalitis in CSF and
rRT-PCR: serum: negative, MRI:
positive, SARS- bilateral symmetric
CoV-2 CSF PCR: mesial temporal lobes
negative hyperintensity and
mild hippocampal
thickness
Moideen 2020 India, case 1 17 Male 1 NM MRI: normal, EEG: Anti-NMDA over-familiar
UK report normal, anti-NMDA receptor attitude, increased
receptors antibodies in encephalitis psychomotor
CSF: positive activity, and labile
affect
Panariello 2020 Italy case 1 23 Male 1 Chest X-ray: Brain CT scan: normal, Anti-NMDA psychomotor
report bilateral ground EEG: unstable non receptor agitation, anxiety,
glass opacities, reactive to visual encephalitis thought
Lung CT scan: stimuli, anti-NMDA disorganization,
patchy bi-basilar receptors antibodies in persecutory
consolidations CSF: positive delusions,
auditory
hallucinations,
and global
insomnia

NM: Not Mentioned; NMDA: N-Methyl-D aspartate, SARS-CoV-2: severe acute respiratory syndrome coronavirus 2, rRT-PCR: Real-time reverse-transcription poly­
merase chain reaction analysis, CT scan: Computed tomography, MRI: Magnetic resonance imaging, PET: Positron emission tomography, F-FDG: Fludeoxyglucose,
EEG: Electroencephalography.

case series, and one cohort article with a total of 81 patients. 62.6% of encephalitis were reported in four case reports (Bhagat et al., 2021;
these patients were men. Three studies were multicenter (Ayatollahi Pizzanelli et al., 2021; Hosseini et al., 2020). The patients were more
et al., 2020; Pilotto et al., 2020a; Moideen et al., 2020), six from Italy likely to develop acute-onset delirium, altered mental status, status
(Manganotti et al., 2021; Pilotto et al., 2021; Dono et al., 2021; Monti epilepticus, cognitive impairment, aphasia, seizure, focal motor deficits,
et al., 2020; Pizzanelli et al., 2021; Panariello et al., 2020), four from UK headache, diaphoresis, palpitation, nausea drowsy, mild confusion, and
(Zambreanu et al., 2020a; Khoo et al., 2020a; Dhillon et al., 2021; a brief episode of non-responsivity (Table 1). In limbic encephalitis,
Hosseini et al., 2020), two from USA (Bhagat et al., 2021; Burr et al., when measured, no cases of LGI1 or CASPR2 antibodies were found.
2021), one from Mexico (Sánchez-Morales et al., 2021a), one from Five studies reported cases of Anti-NMDA receptor encephalitis.
China (Wang et al., 2020a), and one from France (Grimaldi et al., Among the cases, there was a two-year-old girl with symptoms such as
2020a). fever, poor sleep, constipation, decreased oral intake, not talking, con­
stant kicking, and thrashing movements of arms and legs (Burr et al.,
2021). Furthermore, three other cases were patients aged 17, 23, and 50
3.3. Autoimmune encephalitis
years old with Anti-NMDA receptor encephalitis (Sánchez-Morales et al.,
2021a; Moideen et al., 2020; Monti et al., 2020). It seems that this type
Findings from the studies on the AE are summarized in Table 1.
of AE affects younger individuals infected with COVID-19. These pa­
Among the included studies, 19 cases were reported with AE, including 7
tients were reported with altered behavior and mental status, seizures,
(37%) cases of limbic encephalitis, 5 (26%) patients with anti-N-methyl-
insomnia, dyskinesia, refractory status epilepticus, over-familiar atti­
D-aspartate (NMDA) receptor encephalitis, 2 (11%) with AE presenting
tude, increased psychomotor activity, anxiety, and labile affect
as new-onset refractory status epilepticus (NORSE), 1 (5%) case of
(Table 1).
steroid-responsive encephalitis, and 4 (21%) cases with unknown type
Moreover, there were two cases with AE presenting as new-onset
of AE (Table 1, Fig. 2).
refractory status epilepticus (NORSE), both from Italy (Manganotti
A cohort study from UK reported one case of limbic encephalitis out
et al., 2021; Dono et al., 2021). The clinical symptoms including
of 29 COVID-19 cases (Dhillon et al., 2021). Also, there was a case series
convulsive status epilepticus, and generalized myoclonic jerks of axial
study reporting two patients with limbic encephalitis among 25
muscles and face were reported in these patients (Table 1).
COVID-19 patients (Pilotto et al., 2021). The other cases of limbic

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Fig. 2. Types of autoimmune encephalitis expressed as percentage.

A case report also described a patient with steroid responsive en­ Based on the reviewed articles in this study, limbic encephalitis is the
cephalitis after COVID 19 infection (Pilotto et al., 2020a). The case was most frequent type of encephalitis among patients with AE, followed by
unable to carry out simple orders and presented severe akinetic syn­ anti-NMDA receptor encephalitis. This type of encephalitis is caused by
drome, palmomental and glabella reflexes, and nuchal rigidity. autoantibodies that target NMDA receptors located in CNS. Infection-
Also, seven other studies reported AE in COVID-19 the patients induced anti-NMDA-R encephalitis has been reported after herpes sim­
without mentioning the exact type (Ayatollahi et al., 2020; Khoo et al., plex virus (HSV1) infection (Monti et al., 2020). In a prospective study,
2020a; Wang et al., 2020a; Grimaldi et al., 2020a). All the clinical AE was observed in about 27% of patients with HSV1 infection
symptoms of encephalitis in reported cases are detailed in Table 1. (Armangue et al., 2018). Among patients who developed AE after the
COVID-19, only one case was reported with positive CSF PCR and there
4. Discussion was one positive case for IgG and IgM in CSF for SARS-CoV-2 (Table 1).
Based on this finding, the presence of undetectable virus in the CSF of
Different theories have been postulated to explain the pathophysi­ COVID-19 patients with AE maybe due to transient presence of the virus
ology of SARS-CoV-2 CNS invasion. SARS-CoV-2 reaches to CNS through in cerebrospinal fluid (CSF) or immunological response-induced CSF
systemic circulating system. The virus cannot easily cross the blood injury (Ayatollahi et al., 2020; Zambreanu et al., 2020b). Moreover, the
brain barrier (BBB) and invade the CNS (Achar and Ghosh, 2020). absence of virus RNA is not associated with the severity of neurological
However, virus recruits three main strategies to cross the BBB. These disorders (Matschke et al., 2020). Positive autoimmune antibody and
mechanisms include transcellular migration, paracellular migration, high level of proteins in CSF are applied as diagnostic criteria for AE
and Trojan horse (Dahm et al., 2016). (Wang et al., 2020b). However, antibody test could be negative in some
There is another important mechanism explaining the development patients (Khoo et al., 2020b). Studies have reported that corticosteroids
of AE in the COVID-19 infection. It has been demonstrated that cytokine- and intravenous immunoglobulin are considered as first-line therapies
mediated neuroinflammation in response to SARS-CoV-2 infection plays for AE treatment (Manganotti et al., 2021; Khoo et al., 2020b; Pilotto
an important role in the pathogenesis of AE (Dhillon et al., 2021). Severe et al., 2020b; Grimaldi et al., 2020b).
case of COVID-19 infection induces overproduction of inflammatory
cytokines, known as cytokine storm (Achar and Ghosh, 2020). Sup­ 5. Conclusion
portably, patients with a severe condition of COVID-19 show higher
levels of inflammatory cytokines such as IL-2R, IL-6, IL-8, IL-10, and Our systematic review revealed evidence on the probability of
TNF-α compared to cases with non-severe COVID-19 condition (Liu developing AE in patients infected with the COVID-19. Clinicians should
et al., 2020b). Elevated IL-6 which is known as a common feature of the be aware of the possible diagnosis of AE when considering other
disease during the inflammatory phase can be a linking factor due to its neurological differential diagnosis in SARS-CoV-2 infected patients.
role in facilitating autoantibody production in anti-NMDA-R encepha­
litis (Byun et al., 2016). Overproduction of inflammatory cytokines Declaration of Competing Interest
seems to affect BBB integrity, increase its permeability, and lead to viral
transmission through BBB (Achar and Ghosh, 2020). Furthermore, it has The authors declare there is no conflict of interest
been shown that SARS-CoV-2 induces production of anti-NMDA-R au­
toantibodies and causes AE (Sánchez-Morales et al., 2021b). Based on Supplementary materials
the reviewed articles in this study, hyperinflammation syndrome is a
leading cause for the development of AE in the majority of COVID-19 Supplementary material associated with this article can be found, in
patients. Moreover, the results indicate that the AE is mostly pre­ the online version, at doi:10.1016/j.msard.2022.103795.
sented several days after respiratory symptoms, suggesting a trigger role
for COVID-19 infection in autoimmune induced CNS disorders.

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References Lu, H., Stratton, C.W., Tang, Y.W., 2020. Outbreak of pneumonia of unknown etiology in
Wuhan, China: the mystery and the miracle. J. Med. Virol. 92 (4), 401–402.
Manganotti, P., Furlanis, G., Ajčević, M., Moras, C., Bonzi, L., Pesavento, V., et al., 2021.
Achar, A., Ghosh, C., 2020. COVID-19-associated neurological disorders: the potential
Intravenous immunoglobulin response in new-onset refractory status epilepticus
route of CNS invasion and blood-brain relevance. Cells 9 (11), 2360.
(NORSE) COVID-19 adult patients. J. Neurol. 268 (10), 3569–3573.
Armangue, T., Spatola, M., Vlagea, A., Mattozzi, S., Cárceles-Cordon, M., Martinez-
Matschke, J., Lütgehetmann, M., Hagel, C., Sperhake, J.P., Schröder, A.S., Edler, C.,
Heras, E., et al., 2018. Frequency, symptoms, risk factors, and outcomes of
et al., 2020. Neuropathology of patients with COVID-19 in Germany: a post-mortem
autoimmune encephalitis after herpes simplex encephalitis: a prospective
case series. Lancet Neurol. 19 (11), 919–929.
observational study and retrospective analysis. Lancet Neurol. 17 (9), 760–772.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., 2009. Preferred reporting items for
Ayatollahi, P., Tarazi, A., Wennberg, R., 2020a. Possible autoimmune encephalitis with
systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6 (7),
claustrum sign in case of acute SARS-CoV-2 infection. Can. J. Neurol. Sci. 48 (3),
e1000097.
430–432.
Moideen, S., Thomas, R., Suresh Kumar, P.N., Uvais, N.A., Ul Haq Katshu, M.Z., 2020.
Bhagat, R., Kwiecinska, B., Smith, N., Peters, M., Shafer, C., Palade, A., et al., 2021. New-
Psychosis in a patient with anti-NMDA-receptor antibodies experiencing significant
onset seizure with possible limbic encephalitis in a patient With COVID-19 infection:
stress related to COVID-19. Brain Behav. Immun. Health 7, 100125.
a case report and review. J. Investig. Med. High Impact Case Rep. 9,
Monti, G., Giovannini, G., Marudi, A., Bedin, R., Melegari, A., Simone, A.M., et al., 2020.
2324709620986302.
Anti-NMDA receptor encephalitis presenting as new onset refractory status
Burr, T., Barton, C., Doll, E., Lakhotia, A., Sweeney, M., 2021. N-methyl-D-aspartate
epilepticus in COVID-19. Seizure 81, 18–20.
receptor encephalitis associated with COVID-19 infection in a toddler. Pediatr.
Panariello, A., Bassetti, R., Radice, A., Rossotti, R., Puoti, M., Corradin, M., et al., 2020.
Neurol. 114, 75–76.
Anti-NMDA receptor encephalitis in a psychiatric COVID-19 patient: a case report.
Byun, J.I., Lee, S.T., Moon, J., Jung, K.H., Sunwoo, J.S., Lim, J.A., et al., 2016. Distinct
Brain Behav. Immun. 87, 179–181.
intrathecal interleukin-17/interleukin-6 activation in anti-N-methyl-D-aspartate
Pilotto, A., Odolini, S., Masciocchi, S., Comelli, A., Volonghi, I., Gazzina, S., et al., 2020a.
receptor encephalitis. J. Neuroimmunol. 297, 141–147.
Steroid-responsive encephalitis in coronavirus disease 2019. Ann. Neurol. 88 (2),
Chen, Y., Liu, Q., Guo, D., 2020. Emerging coronaviruses: genome structure, replication,
423–427.
and pathogenesis. J. Med. Virol 92 (4), 418–423.
Pilotto, A., Odolini, S., Masciocchi, S., Comelli, A., Volonghi, I., Gazzina, S., et al., 2020b.
Dahm, T., Rudolph, H., Schwerk, C., Schroten, H., Tenenbaum, T., 2016. Neuroinvasion
Steroid-responsive encephalitis in coronavirus disease 2019. Ann. Neurol. 88 (2),
and inflammation in viral central nervous system infections. Med. Inflamm. 2016.
423–427.
Dhillon, P.S., Dineen, R.A., Morris, H., Tanasescu, R., Nikfekr, E., Evans, J., et al., 2021.
Pilotto, A., Masciocchi, S., Volonghi, I., Crabbio, M., Magni, E., De Giuli, V., et al., 2021.
Neurological disorders associated with COVID-19 hospital admissions: experience of
Clinical presentation and outcomes of severe acute respiratory syndrome
a single tertiary healthcare center. Front. Neurol. 12, 640017.
coronavirus 2-related encephalitis: the ENCOVID multicenter study. J. Infect. Dis.
Dono, F., Carrarini, C., Russo, M., De Angelis, M.V., Anzellotti, F., Onofrj, M., et al., 2021.
223 (1), 28–37.
New-onset refractory status epilepticus (NORSE) in post SARS-CoV-2 autoimmune
Pizzanelli, C., Milano, C., Canovetti, S., Tagliaferri, E., Turco, F., Verdenelli, S., et al.,
encephalitis: a case report. Neurol. Sci. Off. J. Ital. Neurol. Soc. Ital. Soc. Clin.
2021. Autoimmune limbic encephalitis related to SARS-CoV-2 infection: case-report
Neurophysiol. 42 (1), 35–38.
and review of the literature. Brain behav. Immun. Health 12, 100210.
Grimaldi, S., Lagarde, S., Harlé, J.R., Boucraut, J., Guedj, E., 2020a. Autoimmune
Sánchez-Morales, A.E., Urrutia-Osorio, M., Camacho-Mendoza, E., et al., 2021a.
encephalitis concomitant with SARS-CoV-2 infection: insight from (18)F-FDG PET
Neurological manifestations temporally associated with SARS-CoV-2 infection in
imaging and neuronal autoantibodies. J. Nucl. Med. 61 (12), 1726–1729.
pediatric patients in Mexico. Childs Nerv. Syst. 37 (7), 2305–2312.
Grimaldi, S., Lagarde, S., Harlé, J.R., Boucraut, J., Guedj, E., 2020b. Autoimmune
Sánchez-Morales, A.E., Urrutia-Osorio, M., Camacho-Mendoza, E., Rosales-Pedraza, G.,
encephalitis concomitant with SARS-CoV-2 infection: insight from 18F-FDG PET
Dávila-Maldonado, L., González-Duarte, A., et al., 2021b. Neurological
imaging and neuronal autoantibodies. J. Nucl. Med. 61 (12), 1726–1729.
manifestations temporally associated with SARS-CoV-2 infection in pediatric
Guilmot, A., Maldonado Slootjes, S., Sellimi, A., Bronchain, M., Hanseeuw, B., Belkhir, L.,
patients in Mexico. Child’s Nerv. Syst. 1–8.
et al., 2021. Immune-mediated neurological syndromes in SARS-CoV-2-infected
Toscano, G., Palmerini, F., Ravaglia, S., Ruiz, L., Invernizzi, P., Cuzzoni, M.G., et al.,
patients. J. Neurol. 268 (3), 751–757.
2020. Guillain–barré syndrome associated with SARS-CoV-2. N. Engl. J. Med. 382
Helms, J., Kremer, S., Merdji, H., Clere-Jehl, R., Schenck, M., Kummerlen, C., et al.,
(26), 2574–2576.
2020. Neurologic features in severe SARS-CoV-2 infection. N. Engl. J. Med. 382 (23),
Wang, M., Li, T., Qiao, F., Wang, L., Li, C., Gong, Y., 2020a. Coronavirus disease 2019
2268–2270.
associated with aggressive neurological and mental abnormalities confirmed based
Hosseini, A.A., Shetty, A.K., Sprigg, N., Auer, D.P., Constantinescu, C.S., 2020. Delirium
on cerebrospinal fluid antibodies: a case report. Medicine 99 (36), e21428
as a presenting feature in COVID-19: neuroinvasive infection or autoimmune
(Baltimore).
encephalopathy? Brain Behav. Immun. 88, 68–70.
Wang, M., Li, T., Qiao, F., Wang, L., Li, C., Gong, Y., 2020b. Coronavirus disease 2019
Khoo, A., McLoughlin, B., Cheema, S., Weil, R.S., Lambert, C., Manji, H., et al., 2020a.
associated with aggressive neurological and mental abnormalities confirmed based
Postinfectious brainstem encephalitis associated with SARS-CoV-2. J. Neurolo.
on cerebrospinal fluid antibodies: a case report. Medicine 99 (36) (Baltimore).
Neurosurg. Psychiatry. 91 (9), 1013.
Zambreanu, L., Lightbody, S., Bhandari, M., Hoskote, C., Kandil, H., Houlihan, C.F.,
Khoo, A., McLoughlin, B., Cheema, S., Weil, R.S., Lambert, C., Manji, H., et al., 2020b.
et al., 2020a. A case of limbic encephalitis associated with asymptomatic COVID-19
Postinfectious brainstem encephalitis associated with SARS-CoV-2. J. Neurol.
infection. J. Neurol. Neurosurg. Psychiatr. 91 (11), 1229–1230.
Neurosurg. Psychiatry 91 (9), 1013–1014.
Zambreanu, L., Lightbody, S., Bhandari, M., Hoskote, C., Kandil, H., Houlihan, C.F.,
Lazarian, G., Quinquenel, A., Bellal, M., Siavellis, J., Jacquy, C., Re, D., et al., 2020.
et al., 2020b. A case of limbic encephalitis associated with asymptomatic COVID-19
Autoimmune haemolytic anaemia associated with COVID-19 infection. Br. J.
infection. J. Neurol. Neurosurg. Psychiatry 91 (11), 1229–1230.
Haematol. 190 (1), 29–31.
Zhou, P., Yang, X.L., Wang, X.G., Hu, B., Zhang, L., Zhang, W., et al., 2020. A pneumonia
Liu, K., Pan, M., Xiao, Z., Xu, X., 2020a. Neurological manifestations of the coronavirus
outbreak associated with a new coronavirus of probable bat origin. Nature 579
(SARS-CoV-2) pandemic 2019-2020. J. Neurol. Neurosurg. Psychiatr. 91 (6),
(7798), 270–273.
669–670.
Liu, J., Li, S., Liu, J., Liang, B., Wang, X., Wang, H., et al., 2020b. Longitudinal
characteristics of lymphocyte responses and cytokine profiles in the peripheral blood
of SARS-CoV-2 infected patients. EBioMedicine 55, 102763.