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Remission of Subacute Psychosis in a COVID-19 Patient With an Antineuronal Autoantibody After Treatment With Intravenous Immunoglobulin

Open AccessPublished:April 09, 2021DOI:https://doi.org/10.1016/j.biopsych.2021.03.033
      To the Editor:
      Patients with the COVID-19 coronavirus are at increased risk for developing new or recurrent psychosis (
      • Taquet M.
      • Luciano S.
      • Geddes J.R.
      • Harrison P.J.
      Bidirectional associations between COVID-19 and psychiatric disorder: Retrospective cohort studies of 62 354 COVID-19 cases in the USA.
      ). Viral infections—including SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) (
      • Panariello A.
      • Bassetti R.
      • Radice A.
      • Rossotti R.
      • Puoti M.
      • Corradin M.
      • et al.
      Anti-NMDA receptor encephalitis in a psychiatric Covid-19 patient: A case report.
      ,
      • Monti G.
      • Giovannini G.
      • Marudi A.
      • Bedin R.
      • Melegari A.
      • Simone A.M.
      • et al.
      Anti-NMDA receptor encephalitis presenting as new onset refractory status epilepticus in COVID-19.
      ,
      • Alvarez Bravo G.
      • Ramió i Torrentà L.
      Anti-NMDA receptor encephalitis secondary to SARS-CoV-2 infection Encefalitis anti-NMDA-R secundaria a infección por SARS-CoV-2.
      )—can cause psychosis in the context of autoimmune encephalitis (
      • Linnoila J.J.
      • Binnicker M.J.
      • Majed M.
      • Klein C.J.
      • McKeon A.
      CSF herpes virus and autoantibody profiles in the evaluation of encephalitis.
      ). However, some individuals with parainfectious psychosis do not meet criteria for autoimmune encephalitis, yet they respond to immunotherapy (
      • Gungor İ.
      • Derin S.
      • Tekturk P.
      • Tüzün E.
      • Bilgiç B.
      • Çakır S.
      First-episode psychotic disorder improving after immunotherapy.
      ,
      • Graus F.
      • Titulaer M.J.
      • Balu R.
      • Benseler S.
      • Bien C.G.
      • Cellucci T.
      • et al.
      A clinical approach to diagnosis of autoimmune encephalitis.
      ). We present a case of COVID-19–associated subacute psychosis that did not meet criteria for autoimmune encephalitis yet remitted after treatment with intravenous immunoglobulin (IVIg). We subsequently identified a novel IgG class antineuronal autoantibody in the patient’s cerebrospinal fluid (CSF).
      A 30-year-old man without medical, psychiatric, or substance use history developed fever and malaise. The following day, he developed a delusion that the “rapture” was imminent. On day 2, a nasopharyngeal swab was positive for SARS-CoV-2 by reverse transcriptase polymerase chain reaction. He began a 14-day isolation but maintained daily contact with family. He did not have anosmia, ageusia, or respiratory symptoms, nor did he receive treatment for COVID-19. He initially suffered from hypersomnia and slept 22 hours/day. He then developed insomnia, sleeping only 3 to 4 hours/day. During this time, he began pacing and rambling about “lights.” He worried that he was dying and said that he had been speaking to deceased relatives and God.
      On day 22, he kicked through a door and pushed his mother, prompting an emergency department evaluation. In the emergency department, he endorsed speaking with the dead, falsely claimed to be a veteran, and worried about being experimented on with “radiation.” He did not have suicidal ideation, homicidal ideation, or hallucinations. Noncontrast head computed tomography was normal, and urine toxicology was negative. He was started on haloperidol 5 mg by mouth twice daily with significant improvement of his agitation and delusions. After 48 hours he was discharged to outpatient follow-up. Outpatient magnetic resonance imaging of the brain with and without gadolinium was unremarkable.
      After discharge, his restlessness, insomnia, and cognitive slowing recurred, as did his fears that he would be experimented on “like a guinea pig.” On day 34, he punched through a wall and was hospitalized to be evaluated for autoimmune encephalitis. A detailed neurological exam was unremarkable. He had a flat affect, slowed speech, and akathisia, which resolved after decreasing haloperidol and starting benztropine and lorazepam. A 12-hour video electroencephalogram was normal. Blood studies were notable for an elevated ferritin and D-dimer, suggesting systemic inflammation (Table 1). CSF studies, including a clinical autoimmune encephalitis autoantibody panel, were only notable for an elevated IgG of 4.8 mg/dL (reference 1.0–3.0 mg/dL) with a normal IgG index (see Table 1).
      Table 1Clinical Studies
      SourceTestResult (Reference)
      Nasopharyngeal SwabSARS-CoV-2 RNA PCRDay 2: positive

      Day 34: negative
      Urine9-drug toxicology screenNegative
      SerumBasic metabolic panelWithin acceptable limits:

      Na 146 mmol/L (136–144 mmol/L)

      K 3.1 mmol/L (3.3–5.1 mmol/L)
      Prothrombin time11.5 s (9.6–12.3 s)
      International normalized ratio1.07
      Complete blood countDay 24 WBC: 6.9 × 1000/μL (4.0–10.0 × 1000/μL)

      Day 34 WBC: 5.4 × 1000/μL (4.0–10.0 × 1000/μL)

      MPV 11.6 fL (6.0–11.0 fL)
      Thyroid stimulating hormone2.520 uIU/mL (0.270–4.200 uIU/mL)
      D-dimer1.89 mg/L (≤0.50 mg/L)
      Liver enzymesAST 156 U/L (<35 U/L)

      ALT 372 U/L (<59 U/L)
      C-reactive protein1.7 mg/L (<1.0 mg/L)
      Ferritin1124 ng/mL (30–400 mg/mL)
      Ammonia27 μmol/L (11–35 μmol/L)
      Albumin4.2 g/dL (3.6–4.9 g/dL)
      IgG1230 mg/dL (700–1600 mg/dL)
      CSFCell count0 nucleated cells
      Protein41.2 mg/dL (15–45 mg/dL)
      Glucose60 mg/dL (40–70 mg/dL)
      CultureNo growth
      Oligoclonal bandingNone
      Albumin25.8 mg/dL (10–30 mg/dL)
      IgG4.8 mg/dL (1.0–3.0 mg/dL)
      IgG index0.67 (<0.7)
      Autoimmune encephalopathy panelNegative for AMPA Ab, amphiphysin Ab, antiglial nuclear Ab, neuronal nuclear Ab (types 1, 2, and 3), CASPR2, CRMP-5, DPPX, GABAB receptor, GAD65, GFAP, IgLON5, LGI1-IgG, mGluR1, NIF, NMDA receptor, Purkinje cell cytoplasmic Ab (types Tr, 1, and 2)
      ImagingCT head without contrastNo acute intracranial findings.
      MRI brain with contrastNo acute intracranial abnormality or definitive structural abnormality identified. Specifically, no imaging findings suggestive of encephalitis or acute demyelination.
      ElectroencephalographyNormal prolonged (>12 hours) awake and asleep inpatient video electroencephalogram.
      Ab, antibody; ALT, alanine aminotransferase; AST, aspartate aminotransferase; CSF, cerebrospinal fluid; CT; computed tomography; GABA, gamma-aminobutyric acid; IgG, immunoglobulin G; mGluR1, metabotropic glutamate receptor 1; MPV, mean platelet volume; MRI, magnetic resonance imaging; NIF, neuronal intermediate filament; PCR, polymerase chain reaction; WBC, white blood cell.
      Lacking focal neurologic symptoms, seizures, magnetic resonance imaging abnormalities, or CSF pleocytosis, his presentation did not meet consensus criteria for autoimmune encephalitis (
      • Graus F.
      • Titulaer M.J.
      • Balu R.
      • Benseler S.
      • Bien C.G.
      • Cellucci T.
      • et al.
      A clinical approach to diagnosis of autoimmune encephalitis.
      ). Nevertheless, his subacute psychosis, cognitive slowing, and recent SARS-CoV-2 infection raised concern for autoimmune-mediated psychosis. Therefore, starting on day 35, he received a total of 2 g/kg of IVIg over 3 days. His cognitive slowing and psychotic symptoms remitted after the first day of treatment. His sleep cycle normalized, and he was discharged without scheduled antipsychotics. He returned to work immediately after discharge and remained symptom-free 3 months later.
      Because his robust response to IVIg indicated an underlying autoimmune process, we tested his CSF for antineural autoantibodies using anatomic mouse brain tissue staining (
      • Ricken G.
      • Schwaiger C.
      • De Simoni D.
      • Pichler V.
      • Lang J.
      • Glatter S.
      • et al.
      Detection methods for autoantibodies in suspected autoimmune encephalitis.
      ), a validated and standard method performed by incubating rodent brain sections with CSF and counterstaining with a human IgG-specific antibody. At a 1:4 dilution, his CSF produced a novel immunostaining pattern that we have not observed in over 500 screens of CSF from other patients with neuroinflammatory disorders.
      His IgG prominently immunostained Satb2-expressing upper-layer (layer II/III) pyramidal neurons in the anteromedial cortex (Figure 1A), a population of excitatory callosal projection neurons necessary for the integration of intercortical information (
      • Alcamo E.A.
      • Chirivella L.
      • Dautzenberg M.
      • Dobreva G.
      • Fariñas I.
      • Grosschedl R.
      • et al.
      Satb2 regulates callosal projection neuron identity in the developing cerebral cortex.
      ). We also observed relatively uniform puncta in the corpus callosum (Figure 1B), consistent with immunostaining of callosal projections. In the olfactory bulb, mitral cell bodies and the external plexiform neuropil were immunostained (Figure 1C). In the dentate gyrus, linearly organized puncta resembling axonal transport vesicles and oblong neurons were apparent in the hilus (Figure 1D). In the thalamus, linear and less organized punctate staining was observed (Figure 1E). In the cerebellum, Purkinje cell bodies were modestly stained, while the overlying molecular layer was densely stained with variably size puncta (Figure 1F).
      Figure thumbnail gr1
      Figure 1Characterization of antineuronal antibody staining. Mice were perfused with 4% paraformaldehyde; 12-μm frozen sagittal brain sections were immunostained with cerebrospinal fluid at a 1:4 dilution and counterstained with an antihuman IgG secondary antibody (green) (Jackson #709-545-149 at 2 μg/mL). Nuclei were labeled with DAPI (blue). Scale bars = 10 μm. (A) Cortical immunostaining of pyramidal neuron cell bodies and proximal processes in layer II of the anteromedial cortex. Staining of neuropil was also observed. (Inset) Cerebrospinal fluid immunostains Satb2-expressing (red) neurons (filled arrowheads) but not surrounding Satb2-negative cells (unfilled arrowhead) (Abcam #ab51502 at 1 μg/mL). (B) Relatively uniform punctate staining along the ventricular wall (filled arrowheads) and overlying corpus callosum. (C) Olfactory bulb immunostaining of mitral cell bodies (filled arrowheads) and neuropil of the external plexiform layer (ep). (D) Hippocampal immunostaining of an axon-like process in the hilus (h) of the dentate gyrus (filled arrowheads) and a subset of hilar cell bodies (unfilled arrowheads). (E) Thalamic axon-like (filled arrowhead) and scattered (unfilled arrowhead) punctate immunostaining. (F) Immunostaining of cerebellar Purkinje cell bodies (filled arrowheads) and neuropil of the molecular layer (m). bv, blood vessel; gc, granule cell layer; ip, internal plexiform layer; mc, mitral cell layer; pc, Purkinje cell layer; v, ventricle.
      In this case we identified a candidate novel neuronal autoantibody in the CSF of a COVID-19 patient with antipsychotic-refractory subacute psychosis, whose symptoms rapidly and completely remitted after treatment with IVIg. This autoantibody primarily localized to layer II/III callosal cortical neurons, which have been implicated in schizophrenia (
      • Kolluri N.
      • Sun Z.
      • Sampson A.R.
      • Lewis D.A.
      Lamina-specific reductions in dendritic spine density in the prefrontal cortex of subjects with schizophrenia.
      ). Although antineural autoantibodies are present in some neurologically impaired COVID-19 patients (
      • Song E.
      • Bartley C.M.
      • Chow R.D.
      • Ngo T.
      • Jiang R.
      • Zamecnik C.R.
      • et al.
      Exploratory neuroimmune profiling identifies CNS-specific alterations in COVID-19 patients with neurological involvement.
      ,
      • Franke C.
      • Ferse C.
      • Kreye J.
      • Momsen Reincke S.
      • Sanchez-Sendin E.
      • Rocco A.
      • et al.
      High frequency of cerebrospinal fluid autoantibodies in COVID-19 patients with neurological symptoms.
      ,
      • Severance E.G.
      • Dickerson F.B.
      • Viscidi R.P.
      • Bossis I.
      • Stallings C.R.
      • Origoni A.E.
      • et al.
      Coronavirus immunoreactivity in individuals with a recent onset of psychotic symptoms.
      ), autoantibody studies are rarely performed in cases of COVID-19–associated psychosis (
      • Parra A.
      • Juanes A.
      • Losada C.P.
      • Álvarez-Sesmero S.
      • Santana V.D.
      • Martí I.
      • et al.
      Psychotic symptoms in COVID-19 patients. A retrospective descriptive study.
      ,
      • Smith C.M.
      • Komisar J.R.
      • Mourad A.
      • Kincaid B.R.
      COVID-19-associated brief psychotic disorder.
      ,
      • Ferrando S.J.
      • Klepacz L.
      • Lynch S.
      • Tavakkoli M.
      • Dornbush R.
      • Baharani R.
      • et al.
      COVID-19 psychosis: A potential new neuropsychiatric condition triggered by novel coronavirus infection and the inflammatory response?.
      ,
      • DeLisi L.E.
      A commentary revisiting the viral hypothesis of schizophrenia: Onset of a schizophreniform disorder subsequent to SARS CoV-2 infection.
      ,
      • Lanier C.G.
      • Lewis S.A.
      • Patel P.D.
      • Ahmed A.M.
      • Lewis P.O.
      An unusual case of COVID-19 presenting as acute psychosis [published online ahead of print Dec 7].
      ,
      • Majadas S.
      • Pérez J.
      • Casado-Espada N.M.
      • Zambrana A.
      • Bullón A.
      • Roncero C.
      Case with psychotic disorder as a clinical presentation of COVID-19.
      ,
      • Clouden T.A.
      Persistent hallucinations in a 46-year-old woman after COVID-19 infection: A case report.
      ,
      • Chacko M.
      • Job A.
      • Caston 3rd, F.
      • George P.
      • Yacoub A.
      • Cáceda R.
      COVID-19-induced psychosis and suicidal behavior: Case report [published online ahead of print Sep 26].
      ,
      • Gillett G.
      • Jordan I.
      Severe psychiatric disturbance and attempted suicide in a patient with COVID-19 and no psychiatric history.
      ).
      Importantly, early initiation of immunotherapy for autoimmune disorders of the central nervous system significantly improves outcomes (
      • Nosadini M.
      • Mohammad S.S.
      • Ramanathan S.
      • Brilot F.
      • Dale R.C.
      Immune therapy in autoimmune encephalitis: A systematic review.
      ). Although autoimmune encephalitis can be established on clinical grounds, the diagnosis requires neurologic, magnetic resonance imaging, and/or CSF abnormalities (
      • Graus F.
      • Titulaer M.J.
      • Balu R.
      • Benseler S.
      • Bien C.G.
      • Cellucci T.
      • et al.
      A clinical approach to diagnosis of autoimmune encephalitis.
      ). To identify individuals with potentially immune-responsive acute psychosis without neurological impairment, Pollak et al. (
      • Pollak T.A.
      • Lennox B.R.
      • Müller S.
      • Benros M.E.
      • Prüss H.
      • Tebartz van Elst L.
      • et al.
      Autoimmune psychosis: An international consensus on an approach to the diagnosis and management of psychosis of suspected autoimmune origin.
      ) proposed criteria for autoimmune psychosis. While “possible” autoimmune psychosis relies solely on clinical factors, “probable” and “definite” require abnormal imaging or laboratory studies.
      Our patient’s subacute psychosis and cognitive dysfunction qualified him for possible autoimmune psychosis. However, he had several red flags for probable autoimmune psychosis: infectious prodrome, rapid progression, and insufficient response to antipsychotics (
      • Pollak T.A.
      • Lennox B.R.
      • Müller S.
      • Benros M.E.
      • Prüss H.
      • Tebartz van Elst L.
      • et al.
      Autoimmune psychosis: An international consensus on an approach to the diagnosis and management of psychosis of suspected autoimmune origin.
      ). Moreover, his mood dysregulation, cognitive slowing, and hypersomnia were evocative of the mixed symptomatology more typical of autoimmune encephalitis (
      • Muñoz-Lopetegi A.
      • Graus F.
      • Dalmau J.
      • Santamaria J.
      Sleep disorders in autoimmune encephalitis.
      ,
      • Al-Diwani A.
      • Handel A.
      • Townsend L.
      • Pollak T.
      • Leite M.I.
      • Harrison P.J.
      • et al.
      The psychopathology of NMDAR-antibody encephalitis in adults: A systematic review and phenotypic analysis of individual patient data.
      ). Given his overall clinical picture, we administered IVIg with apparent clinical response. Although our patient might have later developed autoimmune encephalitis, consideration of autoimmune psychosis can prompt earlier immunotherapy and potentially improve outcomes. Only by relying on ancillary criteria were we able to justify immunotherapy for our patient, suggesting that re-evaluating the criteria for autoimmune psychosis may improve its sensitivity (
      • Franke C.
      • Prüss H.
      Letter to the Editor: Comment on Mulder J et al. (2021) Indirect immunofluorescence for detecting anti-neuronal autoimmunity in CSF after COVID-19—Possibilities and pitfalls.
      ).
      Even so, this case should be interpreted with caution. Psychotic disorders are protean by nature, mixed symptomatology does occur, and most psychotic presentations are unlikely to be immune mediated. However, given the scale of the COVID-19 pandemic, psychiatric practitioners should consider autoimmune psychosis in patients with COVID-19–associated psychosis.

      Acknowledgments and Disclosures

      This work was supported by National Institute of Mental Health Grant Nos. R01MH122471 (to SJP, MRW), R01MH125396 (to SS), R21MH118109 (to SS), and R01AI157488 (to SFF); National Institute of Neurological Disorders and Stroke Grant No. R01NS118995-14S (to SJP); a Scientific Innovations Award from the Brain Research Foundation (to SJP); the National Institute of Allergy and Infectious Diseases Grant No. K23MH118999 (to SFF); the Hanna H. Gray Fellowship from the Howard Hughes Medical Institute (to CMB); the President’s Postdoctoral Fellowship Program from the University of California (to CMB); and the John A. Watson Scholar Program of the University of California, San Francisco (to CMB).
      We thank Trung Huynh and Anne Wapniarski for laboratory assistance.
      During the course of treatment, we obtained surrogate consent to use surplus cerebrospinal fluid for research. After regaining capacity, the patient provided written informed consent for this case report. This work has not previously been published in any form.
      MRW has received a research grant from Roche/Genentech. All other authors report no biomedical financial interests or potential conflicts of interest.

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