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Anti-N-methyl-D-aspartate (NMDA) receptor encephalitis (ANMDARE) is an autoimmune disease caused by reversible internalization of NMDA receptors by immune-triggered autoantibodies.
Epidemiology has documented a wide age range (2 months to 85 years) of affected patients, with a median age of approximately 21 years. In young women, the prevalence is higher than in men (4:1); this gender gap gradually disappears after age 45.
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It is often described as a paraneoplastic disorder, as it is often associated with ovarian teratomas; however, this is not always the case, as viral causes and undetermined causes have been documented. This article reviews the latest literature on the pathophysiology of ANMDAREs and provides a brief overview of their clinical features, diagnostic imaging findings, and treatment.
The first reported cases of ANMDARE involved 4 women who were diagnosed with comorbid ovarian teratomas and a characteristic symptom pattern was identified. Thus, the clinical features of ANMDARE can be described progressively in three phases (Figure 1).
1. Prodromal period. The first stage shows flu-like symptoms such as headache, fatigue and low-grade fever.
2. The psychotic stage. Primary positive and negative symptoms indistinguishable from schizophrenia (eg, hallucinations, delusions, disorganized behavior, and paranoia) are associated with the second stage.
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3. Nervous system. In the third stage, more neurologic symptoms develop, such as focal or generalized seizures, movement disturbances, and autonomic instability. Other neuropsychiatric symptoms include restlessness, irritability, catatonia, depression, speech disturbances, and memory loss.
These steps represent a general progression, but other differences can also be observed. The following describes cases discussed in the literature that exemplify this diversity, followed by a brief review of pathology and laboratory findings, imaging, and treatment as we understand it today.
A 27-year-old woman with no overt psychiatric or systemic medical history presented to the emergency department with a 15-day history of confusion, hypochondriatic hallucinations, auditory hallucinations, insomnia, and short-term memory loss. Current medical history does not reveal headache, fever, seizures, dyskinesia, or autonomic instability. Over time, mental status testing revealed disorientation, lack of abstract thinking, inattention, speech delays, verbal exertion, and auditory hallucinations. Initial laboratory tests and imaging studies were normal; she was admitted to the inpatient psychiatric unit with a first episode of psychosis.
During his stay in the psychiatric ward, the patient showed refusal to eat, decreased speech, and alternating periods of inactivity and hyperactivity. The initial regimen was titrated to aripiprazole 30 mg/day and lorazepam 3 mg/day. Although her psychiatric and behavioral symptoms improved, her short-term memory symptoms worsened, prompting further neurologic examination.
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Brain MRI showed diffuse enlargement of the cerebellar vermis. Electroencephalogram (EEG) showed independent bilateral slow-time activity without strong triangular brushing patterns. A complete blood count was unremarkable. Urine toxicology was negative.
Due to the bizarre appearance, anti-NMDA receptor antibodies were detected in serum and cerebrospinal fluid (CSF); the results of both assays were positive. All other autoimmune antibodies were negative. CSF also showed mild lymphocytosis with a predominance of lymphocytes. An intravaginal ultrasound revealed a mass in her right ovary, which was later diagnosed as ovarian teratoma.
Further treatment consisting of intravenous (IV) immunoglobulin 0.4 mg/kg/day and methylprednisolone 1 g/day for 5 days successfully improved her episodic and visuospatial memory, fluency and attention, and relieved her psychotic symptoms. Repeat brain MRI and EEG revealed no specific findings. She was treated with aripiprazole 30 mg/day, prednisolone 60 mg/day, and monthly IV immune globulin 0.4 mg/kg/day for 5 days. Psychiatric and neurological follow-up showed significant improvement in all symptoms.
A 23-year-old woman with no psychiatric or general medical history presented with an approximately 10-minute seizure at home, followed by several brief focal seizures with oral spasms. She then develops mood swings, irritability, and unreasonable and inappropriate laughter and crying. She was sent to a mental hospital for inpatient treatment. Brain MRI T2 and Diffusion Weighted Imaging-Hypertension (DWI-Hypertension) showed right temporal lobe lesion. The initial regimen consisted of valproic acid 500 mg twice daily and olanzapine (dose not specified).
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On admission, despite treatment with valproic acid, she developed a fever of 37.8°C and tonic-clonic convulsions. During the seizure, vital signs were stable and responsive; however, she was lost in time and place. Neurologic examination revealed decreased muscle tone but normal strength in her upper and lower extremities. She will be transferred to a general hospital for further treatment. A spinal tap was positive for herpes simplex virus 1 (HSV-1) polymerase chain reaction, immunoglobulin M (IgM), and IgG. Both serum and cerebrospinal fluid tested positive for anti-NMDA receptor antibody IgG. Serum was positive for glutamic acid decarboxylase (GAD) antibodies. Contrast-enhanced MRI T2, fluid-attenuated inversion recovery (FLAIR) imaging, and DWI revealed a hyperintense lesion in the right temporal lobe. EEG showed diffuse slow waves in the right temporal lobe. Pelvic ultrasound was negative.
Treatment consists of intravenous acyclovir 10 mg/kg. Methylprednisolone 1000 mg/d i.v. and valproic acid 500 mg every 8 hours. After 7 days, symptoms were not under control, so intravenous immunoglobulin 0.4 mg/kg/d was added to her regimen. After a second round of intravenous immunoglobulin therapy, her physical and cognitive symptoms improved sufficiently and she was discharged. Subsequent MRI showed resolution of the hyperintense lesion.
They are a complex of 4 subunits – 2 GluN1 subunits and 2 GluN2 subunits – each with a similar structure. These subunits serve as targets for autoantibodies produced by ANMDARE (Figure 2).
NMDA receptors are ionotropic glutamate receptors that regulate a variety of neurological functions. It is a heterodimer composed of 2 NR1 subunits that bind glycine and 2 NR2 subunits that bind glutamate.
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These subunits serve as targets for anti-NMDA receptor antibodies. Binding of each subunit’s respective ligand activates the receptor and opens an ion channel that is more permeable to calcium, allowing the receptor to function.
ANMDARE is ultimately caused by autoantibodies that promote reversible internalization of NMDA receptors. This internalization creates the NMDA hypofunctioning state described in the NMDA psychosis hypothesis.
It is a possible cause of major positive and negative psychotic symptoms. It is widely believed that the specific site of autoantibody action is on the GluN1 subunit. These autoantibodies cause cross-linking of NMDA receptors and alter their ability to interact properly, leading to their internalization and trafficking through endosomes and lysosomes.
The production of these autoantibodies can be roughly divided into 3 categories: paraneoplastic processes, viral infections, and unknown. The most common paraneoplastic trigger is ovarian teratoma.
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Neuronal tissue expressing NMDA receptors is hypothesized to be associated with certain teratomas. These tumor cells undergo apoptosis and release antigen to antigen-presenting cells (APCs), which engulf free antigen and present it to regional lymph nodes. Since antigens on tumor cells are usually intracellular and not accessible to APCs, cytotoxic T cells are suspected.
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