Neuromyelitis optica (NMO) is characterized as a
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1 Neuromyelitis optica (NMO) is characterized as a severe, relapsing inflammatory disease resulting in vision loss and impaired mobility. As with multiple sclerosis, clinical symptoms result from demyelination within the central nervous system Also similar to MS, the presenting symptoms, degree of severity and longitudinal course are variable among individual patients. However, the observation that patients with NMO preferentially develop optic neuritis and myelitis (with relative sparing of the brain) has resulted in the impression that NMO is a separate disease, distinct from other idiopathic demyelinating conditions of the CNS. Despite periodic revisions to the diagnostic criteria, each incorporating putative clinical features, MRI findings and diagnostic laboratory testing to distinguish it from MS, NMO remains a controversial entity. Most recently, the detection of an autoantibody, neuromyelitis optica immunoglobulin G (NMO-IgG), has been proposed as a method to differentiate NMO from multiple sclerosis. 1 Proponents support this assertion by citing the fact that no specific biomarker for MS has yet been identified. 2 Nonetheless, debate remains as to whether the NMO-IgG autoantibody is a universal indicator of a distinct disease, or merely represents an epiphenomenon of the demyelinating process. For the practicing clinician, the ability to recognize the manifestations of NMO has important implications. Vision 32 Practical Neurology December 2007
2 Is neuromyelitis optica a distinct entity, or simply a manifestation of multiple sclerosis? Two neuro-ophthalmologists review the evidence and say it isn t as clear as black and white. By Christopher C. Glisson, DO and Steven L. Galetta, MD loss in NMO may be bilateral and severe, and the potential for longitudinally-extensive spinal cord involvement can result in significant disability. While the scientific rigor of determining the place of NMO within the framework of demyelinating disease is underway, an understanding of the clinical characteristics and the diagnostic studies available, including their reasonable use in the appropriate clinical setting, can improve individual patient care and assist in defining a therapeutic strategy for patients presenting with optic neuritis or myelitis. The Evolution Of Devic s Disease Over a century ago, the clinical syndrome now known as NMO was described by Devic and Gault as an acute disease characterized by bilateral (or rapidly sequential) optic neuritis and myelitis. 3,4 Patient s suspected of having Devic s disease were identified based on a monophasic course, with demyelination limited to the optic nerve and spinal cord; the resulting disability was severe. In contrast, patients with relapsing disease were considered to have multiple sclerosis. Over time, observers have documented marked variability in the presenting features, clinical course, and accumulated disability in patients with presumed NMO In contrast to the previously held precept that simultaneous clinical symptoms were a hallmark of the diagnosis, it is now recognized that patients diagnosed with NMO often present with either acute optic neuritis (more commonly unilateral) or myelitis. In contrast to typical optic neuritis, vision loss associated with NMO is often severe, and retro-orbital pain is not as common. 11 Paraparesis or paraplegia, often with bladder dysfunction and sensory loss below the level of the lesion, results from spinal cord demyelination. 12 Importantly, these symptoms do not need to occur simultaneously at the time of presentation, and in fact attacks may be separated by years. 10,13 In addition, a relapsing course in patients with NMO is now accepted, and a subset of patients will manifest cerebellar and brainstem disease, and have MS-like brain lesions. 14 Based on accumulating evidence, the initial diagnostic criteria for NMO 15 were later revised, with the intent of further defining NMO as a nosologic entity distinct from MS. The revised criteria address the shortcomings of the first version, most notably that patients with otherwise typical NMO do demonstrate brain involvement at MRI, and that longitudinally-extensive spinal cord lesions are often present in patients with NMO. The Clinical Diagnosis As in any inflammatory demyelinating syndrome, the diagnosis rests on a careful history and physical examination. Attention to onset, associated features (including orbital or retro-orbital pain in the setting of optic neuritis), time course of progression, and potential provocative factors is of tantamount importance. Other causative entities, such as vascular, infectious, metabolic, and structural abnormalities, must be excluded. The presenting symptoms of NMO are optic neuritis and/or myelitis. Rarely, the patient may present with medullary or extensive brainstem lesions. The resultant neurological deficits are severe, and in contrast to MS typically do not involve the brain. 15 While infection or vaccination has preceded onset in some patients with NMO, 16,17 no specific cause has been identified. The current diagnostic criteria for NMO were proposed in 2006 by the Mayo Clinic. 14 (see Table 1). Based on longitudinal evaluation of 96 patients with relapsing NMO, and 33 patients with MS of an optic-spinal phenotype, it was determined that longitudinally-extensive spinal cord lesions (sensitivity 76 percent and specificity 83 percent) and the presence of the NMO- IgG autoantibody (sensitivity 76 percent and specificity 83 percent) were the most useful features in making the diagnosis. In this diagnostic scheme, NMO requires both optic neuritis and acute myelitis, as well as two of three supportive criteria: longitudinally-extensive spinal cord lesions extending over three or more vertebral segments; MRI of the brain not meeting the diagnostic criteria for MS; and, NMO-IgG seropositivity. Based on the understanding that optic neuritis need not be bilateral, and that optic neuritis and myelitis need not occur simultaneously, many have heralded the NMO-IgG autoantibody test as a clinically useful tool in detecting patients with NMO, and thus those patients at risk for severe disability in future. Despite this presumed biological marker, however, there remains significant clinical overlap between NMO and other December 2007 Practical Neurology 33
3 NMO & MS Table 1: Mayo Clinic Proposed Diagnostic Criteria for NMO Definite NMO Optic neuritis Acute myelitis At least two of three supportive criteria: 1. Contiguous spinal cord MRI lesions extending over >3 vertebral segments 2. Brain MRI not meeting diagnostic criteria for multiple sclerosis 3. NMO-IgG seropositive status idiopathic inflammatory demyelinating disorders. A review of the collected literature to date yields evidence for, and against, the classification of NMO as a separate entity. Table 2: Clinical Features of NMO versus Multiple Sclerosis Neuromyelitis Optica Severe myelopathy, visual loss unilateral early in course, often bilateral late Attacks more severe with less complete remission Secondary progressive course is uncommon Patients may not respond to conventional MS therapy, often require immunosuppression Epidemiology Based on published analyses, 10,13,14,18 general observations regarding the population of patients meeting the widely accepted criteria for NMO have been offered. NMO occurs in women up to nine times more often than men, with a median age at onset of 39 years. MS preferentially affects women with a range of to 1, 19 and has a median age of onset at 29 years. 20 Characteristic features of NMO have been reported on the basis of geographic locale. While MS occurs more frequently in white populations in the Northern hemisphere, clinical features consistent with NMO appear to be more prevalent in non- Caucasian populations. 14 Indeed, African and Asian populations appear to be more predominantly affected. In Japan, percent of patients with recurrent demyelinating disease demonstrate an opticospinal course, characterized by selective involvement of the optic nerve and spinal cord, older age at onset, greater female prevalence, minimal lesions at brain MRI, and longitudinally-extensive spinal cord lesions. 21 Opinions differ as to whether this entity is distinct from NMO, or represents a continuum of the same disease process. Additional race-based variation has been described. Papais- Alvarenga and colleagues 22 reported the clinical characteristics and longitudinal course of optic neuritis in relapsing neuromyelitis optica (RNMO), based on a large cohort of patients from Rio de Janeiro, Brazil. Optic neuritis was most often unilateral, and resulted in severe vision loss. While most patients improved with time or after treatment with corticosteroids, significant vision loss due to relapses was common: over 50 percent of the patients had bilateral visual impairment, and 63 percent were legally blind in at least one eye. Severe vision loss and death related to cervical spine disease was more common in patients of Afro-Brazilian descent than in white patients. These and other studies suggest that an immune-mediated mechanism may underlie the development of idiopathic demyelinating disease, and work is ongoing to determine if this may play a role in observed differences among diverse patient populations. The Course Of NMO It is important to emphasize that all of the clinical features of neuromyelitis optica may not be evident at the initial presentation. The overwhelming majority of patients with NMO have a relapsing course, 23 and severe neurological disability accumulates over time. The long-term prognosis is poor; however, a certain subset of patients will have a relatively benign course, maintain- Multiple Sclerosis Mild to moderate myelopathy, visual loss is usually unilateral Attacks mild to moderate with initially good recovery Secondary progressive course is common Patients often respond to conventional MS therapy, immunosuppressive drugs often not needed Table 3: Radiographic Features of NMO versus Multiple Sclerosis Neuromyelitis Optica Brain MRI: often normal, particularly early in the disease course. Cord MRI: long, central lesions (> 3 vertebral segments), hypointensity on T1 images Lesions involving cental medulla, hypothalamus and diencephalon Multiple Sclerosis Brain MRI: typically show periventricular and subcortical lesions Cord MRI: peripheral lesions, usually short in length (2 vertebral segments or less) Brainstem lesions involve the medial longitudinal fasciculus or peripheral brainstem 34 Practical Neurology December 2007
4 FIG.1a ing a good measure of visual acuity and mobility (unpublished observations) even without treatment. The diagnostic dilemma involves distinguishing the patients in which an index event portends the spectrum of NMO, which may not become manifest for years. Common clinical characteristics of NMO, in contradistinction to typical features of MS, are presented in Table 2. Monophasic NMO, of the type first described by Devic, can be recognized by the presence of bilateral optic neuritis and myelitis, occurring simultaneously or in rapid succession. In relapsing disease, 60 percent of patients develop a second clinical event within one year, and 90 percent within three years. 13 In distinction from MS, recovery from attacks is incomplete, but a secondary progressive course in NMO is uncommon: a comparison of 96 patients with NMO showed only two demonstrated conversion to a secondary progressive phase at a median follow-up of 6.1 years. 24 A hallmark clinical feature of NMO is its severity, providing yet another argument for its clinical and phenomenological separation from other forms of demyelinating disease. Wingerchuk and colleagues have reported that within five years of disease onset, fully 50 percent of patients are blind in at least one eye and require assistance with ambulation. Diencephalic and brainstem lesions (Figure 1) may occur in NMO, resulting in numerous symptoms ranging from hiccup and nausea 25 to acute neurogenic respiratory failure. 26 In contrast, brainstem lesions (either focal or as extensions of cervical myelitis), are known to be rare in MS. A series of patients collected by Pittock and colleagues has indicated that, in comparison to MS, patients with NMO and brainstem involvement have a shorter time from disease onset to ventilatory support, require a longer duration of mechanical ventilation, and have a worse prognosis for independent ventilation. 26 While distinct differences have suggested the plausibility of defining NMO as an independent entity, in practice there is considerable variation in the rich tapestry of clinical phenotypes. As each new case series emerges in the literature, it is clear that no single characteristic is adequate to define the broad scope of NMO. Each individual case needs to be considered individually, and it is the constellation of clinical features that allows the best differentiation of NMO from other demyelinating disorders. Neuroimaging Common MRI features of neuromyelitis optica and multiple sclerosis are listed in Table 3. Brain lesions have been considered rare in patients with typical NMO, and in the past were regarded as evidence against the diagnosis. More recently, however, a study conducted by Pittock and colleagues 27 found that 60 percent of patients with NMO demonstrated abnormalities at brain MRI. Neuroimaging is required in all patients with suspected demyelinating disease, even if the NMO phenotype is present, to exclude other potential causes of optic neuritis (see above). Figure 1. (a) T2 weighted and (b) T1 post-contrast MRI in a patient with NMO, demonstrating a lesion in the medulla (arrows), centrally located and adjacent to the fourth ventricle. FIG.1b Figure 2. Saggital T2-weighted MRI, with longitudinally extensive, centrallylocated demyelinating lesion involving the cervical spine.
5 NMO & MS In patients with acute myelitis, spinal cord evaluation by MRI demonstrates the presence of enhancing lesions. A contiguous lesion extending for three or more vertebral segments is correlated with NMO (Figure 2), but a similar appearance may be seen in conventional MS. CEREBROSPINAL FLUID TESTING Cerebrospinal fluid (CSF) analysis has been advocated as an additional means of differentiating NMO from MS.13,18 The presence of CSF pleocytosis (white blood cell count >50 x 10 3 /ml), and the absence of oligoclonal banding both may be useful indicators in the appropriate setting. Once again, however, significant variation exists among published NMO cohorts. Oligoclonal banding is detected in approximately 70 to 90 percent of patients with multiple sclerosis, but may also be present in 20 to 35 percent of patients with NMO. 13,18 Likewise, while pleocytosis (>50 white blood cells, often with neutrophils) is very rare in MS, it is an inconsistent finding in NMO, with a reported range of 13 to 35 percent. NMO-IgG Testing In 2004, a serum autoantibody (NMO-IgG) was identified as a potential specific biomarker for NMO. 28 The autoantibody is detected by indirect immunofluorescence on a substrate of mouse CNS tissues. This serum marker was reported to be 73 percent sensitive and 91 percent specific for NMO in patients with an initial optic-spinal syndrome, and was not commonly found in patients with conventional MS. 28,29 Subsequently, NMO-IgG seropositivity has been incorporated into the most recent diagnostic criteria for NMO. 14 The NMO-IgG autoantibody selectively binds to aquaporin- 4 (AQP4); 29 the autoantibody cannot be detected in AQP4 knockout mice. Aquaporin-4 is a predominant water channel in the central nervous system that is principally expressed in astroglial foot processes in the blood-brain barrier. Recent data 30 have been proposed to support the theory that a targeted process of humoral autoimmunity may underlie the pathogenesis of NMO. NMO-IgG selectively binds to microvessels, pia, subpia and Virchow-Robin spaces; 1 this correlates with observed sites of immune complex deposition in the lesions of NMO. 31 Interestingly, this preferential binding of NMO-IgG may suggest an explanation for some of the MS-like lesions seen at MRI, as the hypothalamus and brainstem are known to be high in aquaporin-4 expression. 32 However, detection of the autoantibody in patients with brain lesions but without the other typical features of NMO calls into question whether this antibody represents an aquaporin-4 channelopathy, or is an epiphenomenon of longitudinally-extensive transverse myelitis. A recent study 33 by Scott and colleagues investigated the rate of NMO-IgG seropositivity in patients with acute partial transverse myelitis (APTM) and unremarkable brain MRI. They concluded that patients with lesions extending two vertebral segments or less harbored the NMO-IgG autoantibody only five percent of the time. In contrast, the rate of antibody positivity in patients with typical NMO spinal cord lesions was 75 percent, a higher percentage than in patients with MS and predominantly spinal-optic symptoms. This finding led the authors to suggest that lesion length in patients with TM could have important clinical implications, supporting separation of TM into distinct diagnostic and pathogenetic categories. Seropositivity for NMO-IgG has been described in Asian optic-spinal multiple sclerosis (OSMS). 34 A cohort of 19 patients with OSMS were tested for presence of the autoantibody, compared against three patients with MS involving the spinal cord and 13 patients with conventional MS. Fourteen of the patients with OSMS were found to harbor the antibody (73 percent); moreover, OSMS patients with a positive test were more likely to have longitudinally-extensive spinal cord lesions and severe visual deficits than those without NMO-IgG. More work remains ahead to determine whether longitudinal involvement of the spinal cord can reliably distinguish NMO. It is important to note that some patients with conventional MS may also demonstrate similar cord findings. Along these same lines, it remains to be proven that the presence of the autoantibody reflects a distinct disease process, and is not merely a consequence of extensive transverse myelitis. Furthermore, the NMO IgG antibody may be observed in other connective tissue disorders such as systemic lupus erythematosus or Sjögren s syndrome, particularly those with evidence of neuro-myelitis optica. A survey of patients with relapsing transverse myelitis and positive NMO antibody tests indicated that about 50 percent also had positive test results for antinuclear antibodies, and approximately 75 percent of patients with recurrent demyelination demonstrated the presence of autoimmune antibodies. 35 These other autoimmune conditions such as lupus are most reliably distinguished from NMO when there are clinical and biopsy features that suggest a systemic inflammatory process. However, some patients with the NMO phenotype will just have other autoimmune antibodies without evidence of a systemic inflammatory condition. 36 Further study of these patients will help elucidate the autoimmune overlap that may exist between these conditions. Treatment Strategies In NMO To date, there have been no rigorous therapeutic trials investigating potential therapies for NMO. During an acute attack of optic neuritis or myelitis, most practitioners offer treatment with intravenous (IV) methylprednisolone, 1g/day for three days followed by oral taper, based on the protocol established in the Optic Neuritis Treatment Trial (ONTT). 37 The rapid anti- 36 Practical Neurology December 2007
6 inflammatory effect of high dose steroids may increase the rate of recovery, as in multiple sclerosis. If the patient does not respond or worsens, anecdotal reports suggest that intravenous immunoglobulin (IVIg) or plasmapheresis may be useful, presumably through the removal of pathogenic or humoral factors underlying the acute process. A proposed method of plasma exchange involves a total of seven exchanges, performed everyother-day, at 1.0 to 1.5 plasma volume per exchange. 38 Early treatment is recommended in suspected cases of NMO, given the potential for debilitating bilateral vision loss or mobility impairment. Similarly, maintenance therapy is indicated to forestall worsening disability due to relapses, as the neurologic effects of NMO often do not resolve completely after an acute attack, and deficits can accumulate over time. Case reports and small case series have investigated the use of immunosuppressive agents. A study of azathioprine in combination with prednisone demonstrated a mean improvement in EDSS from 9 to 3 in seven patients over an 18 month period. 39 Additional experience with mitoxantrone and mycophenolate mofetil has been successful in individual patients. Monthly IVIG therapy remains a consideration, and a report of two patients 40 suggested that relapses may be minimized by this approach. 40 Finally, a study by Cree and colleagues 41 investigated the use of rituximab in neuromyelitis optica. A total of eight patients with NMO were given weekly IV infusions for a one month period, at a dose of 375mg/m 2. B cell counts were followed bimonthly, and re-treatment was offered when B cells again became detectable; re-treatment consisted of two infusions of 1000mg, administered two weeks apart. Although the cohort was small, results indicated a significant decrease in the anticipated relapse rate. Although preliminary data suggests that these immunosuppressive strategies may be more effective than conventional MS therapies in NMO, 41,42 randomized prospective studies are needed for confirmation. Conclusion Both neuromyelitis optica and multiple sclerosis are inflammatory demyelinating disorders that can result in neurologic impairment. Despite accumulating evidence hinting at clinical, epidemiologic, radiologic and pathologic differences between these conditions, there remains sufficient overlap between NMO and MS to support the contention that the observed spectrum of disease represents a continuum of a single but multifaceted entity. Two versions of diagnostic criteria for NMO have been required since 1999, with the most recent incorporating a biomarker that has been purported to characterize a unique pathophysiologic mechanism. However, until a gold standard for diagnosis is aligned with careful prospective analyses, separating NMO from MS will remain a diagnostic and therapeutic challenge to the clinician. PN Christopher C. Glisson, DO is Assistant Professor of Neurology and Ophthalmology at Michigan State University College of Human Medicine s Neuro-Ophthalmology Unit in East Lansing, MI. Steven L. Galetta, MD is Ruth Wagner Van Meter and J. Ray Van Meter Professor of Neurology and Director of Neuro-Ophthalmology at the University of Pennsylvania School of Medicine in Philadelphia. Disclosure: Dr. Galetta has received research support from Genentech and Biogen Idec, and speaking honoraria from Biogen Idec. 1. Lennon VA, Wingerchuk DM, Kryzer TJ, et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004; 364: Frohman EM, Racke MK, Raine CS. Multiple sclerosis the plaque and its pathogenesis. N Engl J Med 2006; 354: Devic E. 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Neurology 2003;60: Wingerchuk DM, Pittock SJ, Lucchinetti CF, Lennon VA, Weinshenker BG. A secondary progressive clinical course is uncommon in neuromyelitis optica. Neurology 2007;68: Misu T, Fujihara K, Nakashima I, Sato S, Itoyama Y. Intractable hiccup and nausea with periaqueductal lesions in neuromyelitis optica. Neurology 2005;65: Pittock SJ, Weinshenker BG, Wijdicks EF. Mechanical ventilation and tracheostomy in multiple sclerosis. J Neurol Neurosurg Psychiatry 2004;75: Pittock SJ, Lennon VA, Krecke K, Wingerchuk DM, Lucchinetti CF, Weinshenker BG. Brain abnormalities in neuromyelitis optica. Arch Neurol 2006;63: Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, Nakashima I and Weinshenker BG. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004;364: Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005;202: Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W, Mandler RN, Weinshenker BG, Pittock SJ, Wingerchuk DM, Lucchinetti CF. Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 2007 (in press). 31. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM, Trebst C, Weinshenker B, Wingerchuk D, Parisi JE, Lassmann H. The role for humoral mechanisms in the pathogenesis of Devic s neuromyelitis optica. Brain 2002;125: Pittock SJ, Weinshenker BG, Lucchinetti CF, et al. Neuromyelitis optica brain lesions localized at sites of high aquaporin 4 expression. Arch Neurol 2006; 63: Scott TF, Kassab SL, Pittock SJ. Neuromyelitis optica IgG status in acute partial transverse myelitis. Archives of Neurology 2006;63: Nakashima I, Fujihara K, Miyazawa I, et al. Clinical and MRI features of Japanese patients with multiple sclerosis positive for NMO-IgG. 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