Neuromyelitis optica
Neuromyelitis optica is a heterogeneous condition consisting of the inflammation and demyelination of the optic nerve and the spinal cord. It can be monophasic or recurrent. Currently at least three different kinds are proposed based on the presence of autoantibodies thought to produce the disease: anti-AQP4, anti-MOG and anti-NF. All the cases are considered autoimmune diseases.
Spinal cord lesions lead to varying degrees of weakness or paralysis in the legs or arms, loss of sensation, and/or bladder and bowel dysfunction.
Devic's disease is now studied along a collection of similar diseases called "Neuromyelitis optica spectrum diseases".
Signs and symptoms
The main symptoms of Devic's disease are loss of vision and spinal cord function. Optic neuritis may manifest as visual impairment with decreased visual acuity, although visual field defects, or loss of color vision may occur in isolation or prior to formal loss of acuity. Spinal cord dysfunction can lead to muscle weakness, reduced sensation, or loss of bladder and bowel control. The typical patient has an acute and severe spastic weakness of the legs or all four limbs with sensory signs, often accompanied by loss of bladder control.Causes
Devic's disease was associated in the past with many systemic diseases, based on anecdotal evidence. The discovery of NMO-IgG has opened a new way into the research for the causes. Currently, three principal causes are accepted:- A first subset of patients is anti-AQP4+. In them, the cause of the neuromyelitis optica is an autoimmune aquaporin-4 channelopathy, due to these specific autoantibodies. In these cases, astrocytes are the victims of the autoimmune attack.
- A second subset of patients is anti-MOG+. In them the cause is an anti-MOG associated encephalomyelitis,
- In a third subset of patients, NMO is due to the presence of anti-neurofascin auto-antibodies which damage the Ranvier nodes of the neurones. These antibodies are more related to the peripheral nervous demyelination, but they were also found in NMO.
anti-AQP4+ variants
In the AQP4+ cases, these auto-antibodies target the protein aquaporin 4 in the cell membranes of astrocytes which acts as a channel for the transport of water across the cell membrane. In any case, anti-AQP4 is produced mainly intrathecally.Aquaporin 4 is found in the astrocytes that surround the blood–brain barrier, a system responsible for preventing substances in the blood from crossing into the brain. The blood–brain barrier is weakened in Devic's disease, but it is currently unknown how the auto-antibodies cross the BBB. Some reports point to the metalloproteinase-2 and interleukin-6 as culprits for the BBB failure. There is broad consensus that AQP4/NMO-IgG initially enters the brain via BBB-deficient sites such as area postrema, where access to CSF occurs.
There are "normal appearing areas" in NMO but compared to patients with MS, NAWM damage is less extensive.
Most research into the pathology of Devic's disease has focused on the spinal cord. The damage can range from inflammatory demyelination to necrotic damage of the white and grey matters. The inflammatory lesions in Devic's disease have been classified as type II lesions, but they differ from MS pattern II lesions in their prominent perivascular distribution. Therefore, the pattern of inflammation is often quite distinct from that seen in MS.
About the presence of anti-AQP4 autoantibodies, some researchers have pointed out that some other cases could be paraneoplastic. It seems also clear that lupus can produce NMO-IgG autoantibodies sometimes, leading to some cases of lupus-derived NMO.
AQP4+ NMO is the most common and is considered an autoimmune astrocytopathy or autoimmune astrocytic channelopathy) in which a person's own immune system attacks the astrocytes of the optic nerves and spinal cord.
In Anti-AQP4 positive variants, CNS astrocytes, which are the basis for the glymphatic system are the target of the autoimmune attack. NMO-IgG-negative cases are less understood. It seems currently that astrocytes are spared in these IgG negative cases.
anti-MOG+ variants
Currently, the second most documented auto-antibody in NMO is anti-MOG autoantibody.MOG antibodies are currently considered mostly absent in similar diseases like multiple sclerosis. Therefore, it can be said that anti-MOG is a group contained inside AQP-Negative NMO.
Together with the anti-AQP4 they form the wider part of the NMO spectrum. They classify the NMO cases in four classes, according to the presence or absence of any of these two main auto-antibodies.
The clinical course and the response to therapy is different for these groups, showing a better prognosis for those in the NMO-Ab/MOG-Ab group, and a worse prognosis for those in the NMO-Ab/MOG-Ab group. The MOG-related neuromyelitis optica can be radiologically identified by the conus involvement. Myelin-oligodendrocyte glycoprotein antibody–positive patients were more likely to have conus involvement on spinal magnetic resonance imaging.
Anti-Neurofascin variants
NF auto antibodies can also appear in NMO cases. These antibodies are more related to the peripheral nervous demyelination, but they were also found in NMO.Diagnosis
The Mayo Clinic proposed a revised set of criteria for diagnosis of Devic's disease in 2006. Those new guidelines require two absolute criteria plus at least two of three supportive criteria. In 2015 a new review was published by an international panel refining the previous clinical case definition but leaving the main criteria unmodified:Absolute criteria:
- Optic neuritis
- Acute myelitis
- Brain MRI not meeting criteria for MS at disease onset
- Spinal cord MRI with continuous T2-weighted signal abnormality extending over three or more vertebral segments, indicating a relatively large lesion in the spinal cord
- NMO-IgG seropositive status
Neuromyelitis optica spectrum disorders
The term NMOSD has been designed to allow incorporation of cases associated a non-AQP4 biomarkers. Therefore, it includes all the clinical variants due to anti-AQP4 plus other non-related but clinically similar syndromes like antiMOG associated encephalomyelitis. Some cases with MOG+ and AQP4+ antibodies have been found.
The collection of these condition has been named "neuromyelitis optica spectrum disorders" and they are expected to respond to the same treatments as standard NMO. Some authors propose to use the name "autoimmune aquaporin-4 channelopathy" for these diseases, while others prefer a more generic term "AQP4-astrocytopathy" that includes also problems in AQP4 with a non-autoimmune origin.
Variants
After the development of the NMO-IgG test, the spectrum of disorders comprising Devic's disease was expanded. The spectrum is now believed to consist of:- Standard Devic's disease, according to the diagnostic criteria described above
- Limited forms of Devic's disease, such as single or recurrent events of longitudinally extensive myelitis, and bilateral simultaneous or recurrent optic neuritis
- Asian optic-spinal MS, or AQP4+ OSMS. This variant can present brain lesions like MS, but it should not be confused with an AQP4-negative form of inflammatory demyelinating diseases of the central nervous system spectrum, sometimes called optic-spinal MS.
- Longitudinally extensive myelitis or optic neuritis associated with systemic autoimmune disease
- Optic neuritis or myelitis associated with lesions in specific brain areas such as the hypothalamus, periventricular nucleus, and brainstem
- NMO-IgG negative NMO: AQP4 antibody-seronegative NMO poses a diagnostic challenge. Some cases could be related to anti-myelin oligodendrocyte glycoprotein autoantibodies.
Recently, AQP4 has been found to distinguish standard multiple sclerosis from neuromyelitis optica, but as MS is a heterogeneous condition, and some MS cases are reported to be Kir4.1 channelopathies it is still possible to consider NMO as part of the MS spectrum. Besides, some NMO-AQP variants are not astrocytopathic, but demyelinating.
Overlaps
in NMO are not usual, but they have been reported to appear in several cases mistakenly treated with interferon beta.Also an overlap with the Sjögren syndrome has been reported.
Differential diagnosis
AQP4-Ab-negative NMO presents problems for diagnosis. The behavior of the oligoclonal bands respect MS can help to establish a more accurate diagnosis. Oligoclonal bands in NMO are rare and they tend to disappear after the attacks, while in MS they are nearly always present and persistent.It is important to notice for differential diagnosis that, though uncommon, it is possible to have longitudinal lesions in MS.
Other problem for diagnosis is that AQP4ab in MOGab levels can be too low to be detected. Some additional biomarkers have been proposed.
Treatment
Currently, there is no cure for Devic's disease, but symptoms can be treated. Some patients recover, but many are left with impairment of vision and limbs, which can be severe.Attacks
Attacks are treated with short courses of high dosage intravenous corticosteroids, such as methylprednisolone IV.Plasmapheresis can be an effective treatment when attacks progress or do not respond to corticosteroids. Clinical trials for corticosteroids contain very small numbers, and most are uncontrolled, though some report high success percentage.
Secondary prevention
Treatment, in order to prevent relapses, for neuromyelitis optica is generally employed but the exact duration of prophylaxis is still debated. In 2019, Eculizumab became the first medication to be approved by the FDA for the treatment of neuromyelitis optica spectrum disorder in adults who are AQP4 antibody positive. In June 2020, Inebilizumab received approval from the FDA, making it the second available treatment for NMOSD. Other immunosuppressant treatments that are used include: azathioprine with prednisone; mycophenolate mofetil with prednisone; mitoxantrone; intravenous immunoglobulin ; and cyclophosphamide.B-cell depletion has been tested with the monoclonal antibody medication, rituximab, indirectly reducing the antibody levels, showing good results.
Several other disease modifying therapies are being tested. In 2007, Devic's disease was reported to be responsive to glatiramer acetate and to low-dose corticosteroids. Use of Mycophenolate mofetil is also currently under research.
Hematopoietic stem cell transplantation can be used in severe cases of NMO. Currently available data suggests that this procedure can reduce inflammatory activity in the short term, but a clear majority of the patients will relapse within 5 years.
Prognosis
Normally, some measure of improvement appears in a few weeks, but residual signs and disability may persist, sometimes severely.The disease can be monophasic, i.e. a single episode with permanent remission. However, at least 85% of patients have a relapsing form of the disease with repeated attacks of transverse myelitis and/or optic neuritis. In patients with the monophasic form, the transverse myelitis and optic neuritis occur simultaneously or within days of each other. On the other hand, patients with the relapsing form are more likely to have weeks or months between the initial attacks, and to have better motor recovery after the initial transverse myelitis event. Relapses usually occur early, with about 55% of patients having a relapse in the first year and 90% in the first five years.
It is possible that the relapsing form is related to the antiAQP4+ seropositive status and the monophasic form related to its absence Unlike multiple sclerosis, Devic's disease rarely has a secondary progressive phase in which patients have increasing neurologic decline between attacks without remission. Instead, disabilities arise from the acute attacks.
Approximately 20% of patients with monophasic Devic's disease have permanent visual loss, and 30% have permanent paralysis in one or both legs. Among patients with relapsing Devic's disease, 50% have paralysis or blindness within five years. In some patients, transverse myelitis in the cervical spinal cord resulted in respiratory failure and subsequent death. However, the spectrum of Devic's disease has widened due to improved diagnostic criteria, and the options for treatment have improved; as a result, researchers believe these estimates will be lowered.
Epidemiology
The prevalence and incidence of Devic's disease has not been established, partly because the disease is underrecognized and often confused with MS. Devic's disease is more common in women than men, with women comprising over two-thirds of patients and more than 80% of those with the relapsing form of the disease.A retrospective study found that prevalence of [|NMOsd] was 1.5% inside a random sample of neurological patients, with a MS:NMOsd ratio of 42.7. Among 13 NMOsd patients, 77% had long spinal cord lesions, 38% had severe optic neuritis and 23% had brain or brainstem lesions. Only 56% had clinically definite NMO at follow-up.
According to the Walton Centre in England, "NMO seems to be present across the world unlike MS, which has a higher incidence in temperate climates and white races. Africans and Asians especially in Far East may have a higher risk of NMO, although the exact incidence of this disease is unknown, making specific conclusions difficult". Although many people who have Devic's disease were initially misdiagnosed with MS, 35% of African Americans are often misdiagnosed with MS when they really have NMO.
Devic's disease is more common in Asians than Caucasians. In fact, Asian optic-spinal MS has been suggested to be identical to Devic's disease. In the indigenous populations of tropical and subtropical regions, MS is rare, but when it appears, it often takes the form of optic-spinal MS.
The majority of Devic's disease patients have no affected relatives, and it is generally regarded as a nonfamilial condition.
History
First reports on an association of spinal cord and optic nerve disorders date back to the late 18th and early 19th century. However, only an 1870 report by Sir Thomas Clifford Allbutt created sustained interest of neurologists and ophthalmologists in this rare syndrome. In 1894, Eugène Devic and his PhD student Fernand Gault described 16 patients who had lost vision in one or both eyes and within weeks developed severe spastic weakness of the limbs, loss of sensation and often bladder control. They recognized these symptoms were the result of inflammation of the optic nerve and spinal cord, respectively.Similar instances of optic neuritis and myelitis were reported, and many believed it constituted a distinct clinical entity. However, some patients had pathology in other parts of the brain, a feature which was more suggestive of acute disseminated encephalomyelitis or MS.
In 2002, Mayo Clinic researchers identified an humoral mechanism, targeting a perivascular protein, as the culprit for NMO and in 2004 an unknown specific autoantibody was found. In 2005 they identified the aquaporin 4 protein as the target of the disease, and developed a test to aid in the diagnosis of Devic's disease by detection of an antibody, AQP4-IgG, in the blood.
Later some other auto-antibodies have been found in NMO AQP4-negative cases, like anti-MOG IgG, but some NMO Anti-AQP4-negative cases still remain idiopathic.
Research directions
Since the discovery of AQP-4 involvement, some research studies have focused on targeted treatment aimed at anti-aquaporin 4 antibodies. The most established method for antibody removal is plasmapheresis. A number of drugs are being studied: aquaporumab, sivelestat, and eculizumab.There is little research into the primary causes of the Anti-AQP4 auto-antibodies. It has been noticed that some cases could be paraneoplastic.
In addition, several NMO variants have been discovered with antibodies other than those for AQP4, turning NMO into a heterogeneous disease. Six different patterns of damage have been reported in NMO, raising the possibility of six different types of auto-antibodies. As of 2019 only three of them are known.
Research into new auto-antibodies
A new auto-antibody was found in 2016 in transverse myelitis and atypical NMO, leading to the concept of Autoimmune GFAP Astrocytopathy.Other auto-antibody under research is flotillin. It has been found in seronegative NMO and some MS patients
Finally, other proteins under study are Connexin 43 and anti-AQP1though, as of 2015, there are only initial reports about the involvement of these proteins
The group AQP+/MOG+ is very small and it can be considered a coincidence of two independent problems in the same person. Assuming these cases could be verified, currently five different kinds of NMO are being considered:
- NMO derived from an autoimmune channelopathy, around 80% of the cases
- NMO derived from an antiMOG associated encephalomyelitis, around 10% of the cases
- Connexin-43 NMO
- Aquaporin-1 associated NMO which could be related to pattern III MS
- Idiopatic NMO, defined by the absence of all previous antibodies
Antibody negative NMO