Antibodies in the Course of Autoimmune Encephalitis: History
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Contributor:
Michał Braczkowski
,
Dariusz Soszyński
,
Alicja Sierakowska
,
Ryszard Braczkowski
,
Klaudia Kufel
,
Beata Łabuz-Roszak

Encephalitis is a condition with a variety of etiologies, clinical presentations, and degrees of severity. The causes of these disorders include both neuroinfections and autoimmune diseases in which host antibodies are pathologically directed against self-antigens. In autoimmune encephalitis, autoantibodies are expressed in the central nervous system. The incidence of this disease is approximately 4% of all reported cases of encephalitis. Autoimmune encephalitis can be induced by antibodies against neuronal surface antigens such as N-methyl-D-aspartate-activated glutamate receptors (NMDAR), α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors (AMPAR) or gangliosides GQ1b, DPPX, CASPR2, LGI1, as well as by antibodies against neuronal intracellular antigens. 

  • autoimmune inflammation with antibodies
  • anti-NMDAR antibodies
  • anti-AMPAR antibodies

1. Introduction

Encephalitis is a severe disorder with many possible causes with varying clinical presentations and degrees of severity. The causes of these disorders include both neuroinfections and autoimmune diseases [1][2]. There are reports indicating that various inflammatory conditions may outnumber infectious diseases in the central nervous system [3].
Autoimmune encephalitis is a heterogeneous group of inflammatory diseases of the central nervous system of various etiologies, requiring complex differential diagnosis. It is a severe clinical condition in which there is a misdirected immune response and directing autoantibodies against self-antigens, with expression taking place in the central nervous system [3][4]. Autoimmune encephalitis is a heterogeneous group of diseases with central nervous system inflammation, characterized by a wide range of symptoms, both neurological and psychiatric. They can occur at any age, and it is characteristic that they develop as a rapidly progressive encephalopathy (usually in less than 6 weeks) caused by encephalitis [5][6]. According to Zuliani et al. [7], autoimmune encephalitis describes several types of different diseases with different pathophysiology, the understanding of which is necessary for the selection of appropriate therapy. In turn, this understanding requires diagnosis based on the identification of autoantibodies associated with this neurological disorder.
Autoimmune encephalitis is not uncommon these days. Initially, the incidence of this disease was a small proportion of all reported cases of encephalitis. However, the last two decades have seen a significant increase in the incidence of autoimmune encephalitis. This is related to the development of diagnostic methods and the discovery over this time of numerous autoantibodies directed against the extracellular domains of neuroglial proteins. Advances in autoimmune encephalitis research have led to the identification of new biomarkers that have allowed for an extended diagnostic approach to these disorders. Thus, there was a significant increase in the number of reported cases of autoimmune encephalitis. Due to the multitude of symptoms of autoimmune encephalitis, this disease is still underestimated. This makes it impossible to unequivocally determine the percentage of morbidity among the general population. Recent epidemiological studies even suggest that autoimmune encephalitis is probably as common as infectious encephalitis, with a prevalence estimated at 13.7/100,000 [5][6][7].
The factor that makes it difficult to make a diagnosis of autoimmune encephalitis is the time from the onset of the first symptoms. In the majority of reported cases, the median time to CSF antibody response ranges from a few days to a few weeks, with a peak frequency around the third week. However, the literature on the subject describes chronic cases, even from one to five years. Therefore, diagnostics based on differential tests of autoantibodies in the patient’s blood have become important [8][9].

2. Antibodies in the Course of Autoimmune Encephalitis

One of the essential elements of the diagnosis of autoimmune encephalitis is the detection and identification of specific antineuronal antibodies. This disease can be induced by antibodies directed against neuronal surface antigens, such as glutamate receptors activated by N-methyl-D-aspartate (NMDAR), α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors (AMPAR), and gangliosides GQ1b, DPPX, CASPR2, LGI1, as well as by antibodies directed against intracellular antigens of neurons. Identification of these antibodies determines the initiation of specific therapeutic actions [8][9][10].
Currently, numerous antibodies inducing the described autoimmune disease are distinguished. According to Wandinger et al. [10], newly identified forms of autoimmune encephalitis are often associated with antineuronal antibodies directed not only against intracellular antigens but, above all, against surface antigens.
As reported, with the highest frequency of 36%, a single anti-neuronal antibody directed against NMDAR antigens is identified. At the level of 9%, a single anti-neuronal antibody directed against AMPAR antigens is identified. At the level of 9%, a single antineuronal antibody directed against LGI1 antigens is identified. At the level of 9%, a single antineuronal antibody directed against CASPR2 antigens is identified. At the level of 8%, a single antineuronal antibody directed against Ri antigens is identified. At the level of 7%, a single antineuronal antibody directed against Yo antigens is identified. At the level of 5%, a single antineuronal antibody directed against Hu antigens is identified. At the level of 4%, a single anti-neuronal antibody directed against CV2 antigens is identified. At the level of 3%, a single antineuronal antibody directed against GABABR antigens is identified. At the 2% level, a single antineuronal antibody directed against the Ma2/Ta antigens is identified. At the 1% level, a single anti-neuronal antibody directed against PCA-2 antigens is identified. At the 1% level, a single anti-neuronal antibody directed against amphiphysin antigens is identified. 
Due to the frequency of occurrence, particular attention should be paid to antibodies against glutamate receptors induced by N-methyl-D-aspartate (NMDAR), antibodies to α-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPAR) receptors, and antibodies against gangliosides CASPR2, LGI1, as well as recently described GQ1b and DPPX [8][9].

2.1. Autoimmune Encephalitis with Anti-NMDAR Antibodies

Autoimmune encephalitis caused by antibodies directed against the NMDA (N-methyl-D-aspartate) receptor subtype was first described in 2007. It has since entered the mainstream of interest in neurology and psychiatry. Some patients with rapidly progressive psychiatric symptoms or cognitive impairment, seizures, abnormal movements, or coma of unknown cause have been observed to have a previously undiagnosed autoimmune disease.
Anti-NMDAR encephalitis is the most common form of autoimmune antibody-associated encephalitis. The prevalence of the disease was initially estimated at approximately 4% of all reported cases of encephalitis. In the study, the aim of which was to determine the cause of the first psychotic episode, in less than 4% of participants, the background was defined as non-psychiatric, of which anti-NMDAR antibodies were detected in as many as 75% [11][12]. The condition can affect people of all ages, but the highest incidence rates are in children and young adults. More than 37% of patients are under the age of 18 at the onset of the disease. The disease affects women more often than men. As many as 80% of patients are women, with an average age of onset of 21 years [12]. In more than half of cases, the disease is associated with cancer and responds to treatment but may recur. Ovarian teratoma was observed in 58% of women over 18 years of age. In addition to age, the presence of the tumor also depends on gender and ethnicity, being slightly more common in black women than in white women. Patients treated with tumor resection and immunotherapy (corticosteroids, intravenous immunoglobulins, or plasma exchange) respond more quickly to treatment and are less likely to require second-line immunotherapy (cyclophosphamide or rituximab or both) than patients without a tumor who receive similar initial immunotherapy. In over 75% of all patients, a significant recovery occurs, which occurs in the reverse order of the development of symptoms and is associated with a decrease in antibody titer [13].
In this disease, autoantibodies serve as a diagnostic marker and alter NMDAR-related synaptic transmission. N-methyl-d-aspartate receptor antibodies belong to the immunoglobulin G1 subclass and are capable of activating a complement on human embryonic kidney cells expressing the N-methyl-d-aspartate receptor. Patients’ antibodies cause a titer-dependent, reversible decrease in synaptic NMDAR through a mechanism of cross-linking and internalization. Based on models of pharmacological or genetic disruption of NMDARs, these antibody effects reveal a probable pathogenic link between receptor depletion and the clinical features of anti-NMDAR encephalitis [10]. The pathogenesis of autoimmune encephalitis with anti-NMDAR antibodies most likely has its origin in neoplastic lesions as well as in virus-infected neurons. They release antigens for NMDA receptors (NMDARs), which are taken up by antigen-presenting cells (APCs) after apoptosis. APCs migrate to local lymph nodes, where, as a result of cooperation with CD4+ T lymphocytes, naive B lymphocytes differentiate into plasma cells and memory cells. The anti-NMDAR antibodies produced by these plasma cells are transported with the blood to the regions of the brain and synaptic connections, where they compete with the GluN1 and RphB2 subunits and lead to neurotransmitter dysregulation. Thus, they become the cause of psychotic symptoms [13].
At the onset of symptoms, distinguishing autoimmune encephalitis from a primary psychiatric disorder is difficult. Autoimmune encephalitis with anti-NMDAR antibodies may begin with non-specific flu-like symptoms followed by fairly rapid (within days to six weeks) development of neuropsychiatric symptoms. The disease presents as a rapidly progressing encephalopathy with acute or subacute onset. The main symptom, which occurs in 90% of patients, is psychiatric disorders, usually of acute onset. The coexistence of a number of symptoms is significant, which is not characteristic of any mental illness. Most patients with anti-NMDAR encephalitis develop a multi-stage disease that progresses from psychosis and seizures to an unresponsive state with catatonic features often associated with autonomic and respiratory instability. In the cognitive sphere, abnormalities such as disorientation, confabulation, confusion, or memory deficits can be observed. The clinical picture is complemented by pathology noted in the motor sphere. Symptoms such as facial and tongue dyskinesia, chorea, stereotypia, athetosis, and dystonia, as well as epileptic seizures (mainly tonic-clonic morphology, focal seizures, and absence seizures), are not uncommon. The severity of symptoms often requires intensive care. Other than clinical evaluation, there are no specific prognostic biomarkers. The disease is characterized by an acute and aggressive course; however, in the case of correct diagnosis and promptly implemented treatment, most patients achieve permanent remission. Correctly defined criteria of diagnosis determine the period of occurrence of symptoms as not longer than 3 months. In addition to obtaining a positive result of anti-NMDAR antibodies, additional tests such as EEG or MRI should be performed to confirm symptoms associated with autoimmune encephalitis with anti-NMDAR antibodies, such as EEG or MRI [1][8][14][15][16][17].

2.2. Autoimmune Encephalitis with Anti-AMPAR Antibodies

Autoimmune encephalitis can be induced by antibodies directed against α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors (AMPAR), which are neuronal surface antigens. The disease is a rare type of autoimmune encephalitis, which was first described by Lai et al. [18]. α-Amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors are expressed throughout the central nervous system, particularly in the hippocampus and other limbic regions. Anti-AMPAR antibodies are directed against extracellular epitopes of the GluA1 or GluA2 subunits of this receptor. Anti-AMPAR encephalitis is most common in middle-aged women, and most patients have an acute or subacute onset. As with anti-NMDAR autoimmune encephalitis, suspected anti-AMPAR autoimmune encephalitis often shows inflammatory changes in the cerebrospinal fluid in laboratory tests. Therefore, it can be expected that in patients with anti-NMDAR and anti-AMPAR encephalitis, tests will show inflammatory changes in the cerebrospinal fluid in most cases. This is important in the diagnosis of this autoimmune disease, as it allows for making appropriate and quick therapeutic decisions. Encephalitis caused by anti-AMPAR antibodies is a neurological disease that is often accompanied by the presence of tumors and, therefore, may cover the entire spectrum of the paraneoplastic syndrome [8][18].
The thymus is the central organ of the immune system, and it is believed that tumors of the thymus may be the initiators of many neurological disorders. Recently, there has been increasing evidence that thymomas are associated with autoimmune encephalitis. Omi et al. [19] were the first to describe a case of encephalitis directed against the α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor, whose clinical recurrence coincided with thymoma recurrence. Clinical recurrence of anti-AMPAR encephalitis after recurrence of the initially detected tumor has not been previously reported. The patient had been in remission for 34 months and showed clinical relapse 3 months after the thymoma recurrence was detected. This case highlights the pathogenic importance of specific tumor antigens as a trigger for anti-AMPAR antibody production and disease induction. In turn, Song et al. [20] tracked data from 1 January 2011 to 1 October 2021 from PubMed, Web of Science, Ovid, and CNKI platforms to analyze general demographic characteristics, frequency of symptoms and associations, and prognosis results in the treatment of 68 patients with naty-AMPAR autoimmune encephalitis in combination with thymoma. Clinical manifestations were mainly cognitive changes (70.6%), psychiatric disorders (57.4%), and epilepsy (50.0%). Treatment included immunotherapy and thymoma therapy, with 79.7% of patients improving post-treatment. In comparison, 20.3% of patients had a poor prognosis. Relapse occurred in 14.8% of patients. According to these authors, thymoma-associated autoimmune encephalitis is a disease entity that absolutely requires long-term follow-up of chest CT results. Zhang et al. [21] report that inflammation of the limbic system of the brain is very often accompanied by antibodies against AMPAR receptors. Autoimmune encephalitis in this form is clinically characterized by a subacute disorder consisting of short-term memory loss, confusion, abnormal behavior, and seizures. According to these authors, most patients with anti-AMPAR encephalitis had malignant complications such as thymoma, small cell lung cancer, breast cancer, and ovarian cancer. Most patients with anti-AMPAR encephalitis showed a partial neurological response to immunotherapy. McCombe et al. [22] confirmed the occurrence of thymoma as the most common tumor accompanying autoimmune encephalitis with anti-AMPAR antibodies. In addition, these authors report that in anti-AMPAR encephalitis, the concomitant antibodies predict a different clinical picture than encephalitis and thymoma. In isolated cases, anti-AMPAR autoimmune encephalitis is accompanied by unexpected disease entities. Despite not fully understanding the connections between its co-diagnosis with thymoma and myasthenia gravis, Li et al. [23] were the first to describe the autoimmune profile and clinical picture of a patient with α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and myasthenia gravis. This points to the extraordinary complexity of thymoma-associated autoimmune networks. Joubert et al. [24] report that the clinical picture of autoimmune encephalitis with anti-AMPAR antibodies is variable. Most patients present with symptoms suggestive of autoimmune limbic encephalitis. They may also show no symptoms or may manifest as severe encephalitis that evolves to a state of minimal consciousness and diffuse cerebral atrophy. Contrary to other reports, in the group of seven patients analyzed, these authors observed only one patient with epileptic seizures and only two patients with cancer—one with lung cancer and one with thymus cancer. These authors clearly emphasize that due to poorly understood clinical features, patients with suspected autoimmune encephalitis associated with the presence of antibodies to the α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor should be screened for the presence of anti-AMPR antibodies both in the serum and in the cerebrospinal fluid [18][19][20][21][22][23][24][25].

2.3. Autoimmune Encephalitis with Anti-GQ1b, Anti-DPPX, Anti-CASPR2, and Anti-LGI1 Antibodies

Autoimmune encephalitis can also be induced by antibodies directed against gangliosides GQ1b, DPPX, CASPR2, and LGI1 [8][26][27][28][29][30].
In the 1950s, Bickerstaff and Fisher independently reported cases with the unique symptom of ophthalmoplegia and ataxia. Neurological symptoms were usually preceded by a previous infection, and most patients recovered spontaneously. However, both authors saw some similarities with Guillain–Barré syndrome, such as the presence of peripheral neuropathy and albuminocytological dissociation of the cerebrospinal fluid. The discovery of anti-GQ1b antibodies in patients with Fisher’s syndrome and later Bickerstaff’s encephalitis was crucial in providing the necessary evidence to conclude that both conditions were, in fact, part of the same spectrum of diseases due to their common clinical and immunological characteristics. The occurrence of anti-GQ-1b antibodies is associated with a variety of disorders. According to Yoshikawa et al. [27], confirmation of the presence of anti-GQ1b antibodies may affect vision disorders. Only recently have these antibodies been associated with autoimmune encephalitis [26][27].
Autoimmune encephalitis caused by autoantibodies directed against the dipeptidyl peptidase-like protein (DPPX), a potassium channel subunit, is rare. In autoimmune encephalitis with antibodies against DPPX receptors, the cerebrospinal fluid is often characterized by inflammation. The disease is typically characterized by a triad of symptoms that include weight loss, central nervous system hyperactivity, and cognitive deficits. However, recent reports suggest that the clinical picture may be more heterogeneous. Although blood and cerebrospinal fluid analyses often show normal cell counts, high titers of DPPX antibodies in the blood and cerebrospinal fluid confirm autoimmune encephalitis with anti-DPPX antibodies. Piepgras et al. [28] confirmed the pathogenic role of anti-DPPX antibodies in anti-DPPX encephalitis in studies on the hyperexcitability of neurons of the enteric nervous system and the reduction of the level of DPPX from the membranes of hippocampal neurons. Xiao et al. [29] conducted a retrospective analysis of nine patients with anti-DPPX encephalitis to expand the clinical and imaging phenotypes of anti-DPPX encephalitis. Nine patients (median age 51 years; range 14–65 years) were identified with symptoms of prodromal fever, diarrhea, or weight loss, followed by rapidly progressive encephalopathy characterized by cognitive impairment. They described three patients with anti-DPPX encephalitis who had sleep disturbance with abnormal sleep behavior with rapid eye movements, limb paralysis, and severe pleocytosis. One patient who received methylprednisolone therapy and a trial of tacrolimus showed significant improvement and had no recurrence during the 6-month follow-up. 

This entry is adapted from the peer-reviewed paper 10.3390/diagnostics13152589

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