182 journals.sagepub.com/home/msj MULTIPLE SCLEROSIS MSJ JOURNAL Multiple Sclerosis Journal 2017, Vol. 23(2) 182–184 DOI: 10.1177/ 1352458516688352 © The Author(s), 2017. Reprints and permissions: http://www.sagepub.co.uk/ journalsPermissions.nav Although some of their characteristics overlap, neuro- myelitis optica spectrum disorder (NMOSD) is dis- tinct from multiple sclerosis (MS) in many clinical, laboratory, and neuroimaging features, including its strong association with a pathogenic autoantibody biomarker, AQP4-IgG. 1 The specificity of AQP4-IgG was leveraged by its incorporation into revised diag- nostic criteria in 2006. 2 Subsequently, a number of additional clinical phenotypes and magnetic reso- nance imaging (MRI) patterns were noted to occur in AQP4-IgG-seropositive neuromyelitis optica (NMO) patients who fulfilled 2006 criteria. These presenta- tions (notably, brain involvement and “NMO-typical” MRI lesion patterns) were proposed to be part of an umbrella term “NMO spectrum disorders” in 2007. 3 In 2015, the International Panel for Neuromyelitis Optica Diagnosis (IPND) proposed consensus diag- nostic criteria using the unified term NMOSD. 4 The 2015 criteria effectively merged the 2006 and 2007 definitions by including all AQP4-IgG-seropositive patients and further defined an expanded array of clinical and MRI phenotypes. A category of NMOSD without AQP4-IgG was retained to identify the roughly one-third of clinical cases that do not have detectable serum AQP4-IgG. Early and accurate NMOSD diagnosis is important for treatment deci- sion-making because AQP4-IgG-seropositive patients are at high risk for relapse (>60% in the first year) and MS disease-modifying therapies (especially inter- feron-beta and natalizumab) aggravate NMOSD regardless of AQP4-IgG serostatus. In this issue, Hamid et al. 5 present an analysis of the effects of diagnostic categorization by applying the 2006 NMO and 2015 NMOSD criteria to 176 subjects at an NMOSD specialty center in whom they diag- nosed an inflammatory demyelinating central nervous system (CNS) syndrome suggestive of NMOSD and atypical for MS. In all, 63 (35.8%; 42 AQP4-IgG seropositive) had characteristics fulfilling the 2006 criteria. When 2015 IPND criteria were applied to the same cohort, 111 (63.1%; 81 seropositive) met crite- ria. All but nine of the incremental patients were AQP4-IgG seropositive and failed to meet 2006 crite- ria because they had not experienced both optic neuri- tis and myelitis. Hamid et al. conclude that application of the 2015 rather than 2006 criteria increased the diagnostic yield (sensitivity) by 76%. Another study demonstrated a similar increase (85%). 6 Is the increase in sensitivity as impressive as it seems? Although not formally enshrined in diagnostic crite- ria, the 2007 concept of NMOSD had identified patients with recurrent optic neuritis, recurrent myeli- tis, and certain typical brain syndromes as NMOSD; such patients were treated with similar strategies as NMO patients who satisfied 2006 criteria. If one applies both the 2006 NMO definition and 2007 NMOSD concept (the latter includes only AQP4-IgG- seropositive cases), then 102 of 176 patients (58.0%) in Hamid et al.’s cohort would have been diagnosed NMO or NMOSD based on prevailing practice. The 2015 IPND criteria incrementally identified nine patients (all AQP4-IgG seronegative), an absolute increase in 5.1%; these cases experienced “combina- tions of clinical events” not satisfying 2006 criteria (brain stem plus either optic nerve or spinal cord or diencephalic plus spinal cord). A total of 50% of the AQP4-IgG-seronegative patients had myelin oligo- dendrocyte glycoprotein (MOG) autoantibodies. Diagnostic criteria identify a collection of symptoms, signs, and tests that are used in routine clinical practice to provide care for individual patients. In contrast, classification criteria are standardized definitions that are meant to identify relatively uniform groups of patients for the purpose of clinical research. Diagnostic criteria must be broad (highly sensitive) in order to reflect disease heterogeneity yet maintain reasonable specificity; classification criteria require high specific- ity. The differentiation of criteria type is particularly Neuromyelitis optica spectrum disorder diagnostic criteria: Sensitivity and specificity are both important Dean M Wingerchuk and Brian G Weinshenker Correspondence to: DM Wingerchuk Department of Neurology, Mayo Clinic, 13400 E. Shea Blvd, Scottsdale, AZ 85259, USA. wingerchuk.dean@mayo. edu Dean M Wingerchuk Department of Neurology, Mayo Clinic, Scottsdale, AZ, USA Brian G Weinshenker Department of Neurology, Mayo Clinic, Rochester, MN, USA 688352MSJ 0 0 10.1177/1352458516688352Multiple Sclerosis JournalDM Wingerchuk and BG Weinshenker editorial 2016 Editorial
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Neuromyelitis optica spectrum disorder diagnostic criteria: Sensitivity and specificity are both importantDOI: 10.1177/ 1352458516688352
© The Author(s), 2017. Reprints and permissions: http://www.sagepub.co.uk/ journalsPermissions.nav
Although some of their characteristics overlap, neuro- myelitis optica spectrum disorder (NMOSD) is dis- tinct from multiple sclerosis (MS) in many clinical, laboratory, and neuroimaging features, including its strong association with a pathogenic autoantibody biomarker, AQP4-IgG.1 The specificity of AQP4-IgG was leveraged by its incorporation into revised diag- nostic criteria in 2006.2 Subsequently, a number of additional clinical phenotypes and magnetic reso- nance imaging (MRI) patterns were noted to occur in AQP4-IgG-seropositive neuromyelitis optica (NMO) patients who fulfilled 2006 criteria. These presenta- tions (notably, brain involvement and “NMO-typical” MRI lesion patterns) were proposed to be part of an umbrella term “NMO spectrum disorders” in 2007.3
In 2015, the International Panel for Neuromyelitis Optica Diagnosis (IPND) proposed consensus diag- nostic criteria using the unified term NMOSD.4 The 2015 criteria effectively merged the 2006 and 2007 definitions by including all AQP4-IgG-seropositive patients and further defined an expanded array of clinical and MRI phenotypes. A category of NMOSD without AQP4-IgG was retained to identify the roughly one-third of clinical cases that do not have detectable serum AQP4-IgG. Early and accurate NMOSD diagnosis is important for treatment deci- sion-making because AQP4-IgG-seropositive patients are at high risk for relapse (>60% in the first year) and MS disease-modifying therapies (especially inter- feron-beta and natalizumab) aggravate NMOSD regardless of AQP4-IgG serostatus.
In this issue, Hamid et al.5 present an analysis of the effects of diagnostic categorization by applying the 2006 NMO and 2015 NMOSD criteria to 176 subjects at an NMOSD specialty center in whom they diag- nosed an inflammatory demyelinating central nervous system (CNS) syndrome suggestive of NMOSD and atypical for MS. In all, 63 (35.8%; 42 AQP4-IgG seropositive) had characteristics fulfilling the 2006
criteria. When 2015 IPND criteria were applied to the same cohort, 111 (63.1%; 81 seropositive) met crite- ria. All but nine of the incremental patients were AQP4-IgG seropositive and failed to meet 2006 crite- ria because they had not experienced both optic neuri- tis and myelitis. Hamid et al. conclude that application of the 2015 rather than 2006 criteria increased the diagnostic yield (sensitivity) by 76%. Another study demonstrated a similar increase (85%).6
Is the increase in sensitivity as impressive as it seems? Although not formally enshrined in diagnostic crite- ria, the 2007 concept of NMOSD had identified patients with recurrent optic neuritis, recurrent myeli- tis, and certain typical brain syndromes as NMOSD; such patients were treated with similar strategies as NMO patients who satisfied 2006 criteria. If one applies both the 2006 NMO definition and 2007 NMOSD concept (the latter includes only AQP4-IgG- seropositive cases), then 102 of 176 patients (58.0%) in Hamid et al.’s cohort would have been diagnosed NMO or NMOSD based on prevailing practice. The 2015 IPND criteria incrementally identified nine patients (all AQP4-IgG seronegative), an absolute increase in 5.1%; these cases experienced “combina- tions of clinical events” not satisfying 2006 criteria (brain stem plus either optic nerve or spinal cord or diencephalic plus spinal cord). A total of 50% of the AQP4-IgG-seronegative patients had myelin oligo- dendrocyte glycoprotein (MOG) autoantibodies.
Diagnostic criteria identify a collection of symptoms, signs, and tests that are used in routine clinical practice to provide care for individual patients. In contrast, classification criteria are standardized definitions that are meant to identify relatively uniform groups of patients for the purpose of clinical research. Diagnostic criteria must be broad (highly sensitive) in order to reflect disease heterogeneity yet maintain reasonable specificity; classification criteria require high specific- ity. The differentiation of criteria type is particularly
Neuromyelitis optica spectrum disorder diagnostic criteria: Sensitivity and specificity are both important
Dean M Wingerchuk and Brian G Weinshenker
Correspondence to: DM Wingerchuk Department of Neurology, Mayo Clinic, 13400 E. Shea Blvd, Scottsdale, AZ 85259, USA. wingerchuk.dean@mayo. edu
Dean M Wingerchuk Department of Neurology, Mayo Clinic, Scottsdale, AZ, USA
Brian G Weinshenker Department of Neurology, Mayo Clinic, Rochester, MN, USA
688352MSJ0010.1177/1352458516688352Multiple Sclerosis JournalDM Wingerchuk and BG Weinshenker editorial2016
journals.sagepub.com/home/msj 183
important in the absence of a diagnostic standard, as is the case for most rheumatologic diseases.7
The distinction between criteria types is also relevant to MS and NMOSD. Although classification criteria are appropriate for MS because a single standard is lacking, AQP4-IgG may be a standard for NMOSD.8 Defining the disease based on AQP4-IgG seropositiv- ity would identify a homogeneous patient cohort suit- able for pathobiology studies and enhance the validity of therapeutic clinical trials at the expense of general- izability. However, restricting the diagnosis to AQP4- IgG-seropositive patients ignores the 30% of patients with otherwise typical NMOSD but who are AQP4- IgG seronegative. Such patients have a similar disease course and similar responses to preventive therapies as the seropositive patients.9 The Hamid report shows that a group of expert neurologists felt that 176 patients had a syndrome compatible with NMOSD (presuma- bly with no better explanation), but only 63% could be diagnosed by 2015 criteria. The other 37% remain an important, likely heterogeneous, group of patients who lack a firm diagnosis, as recognized by others.10 Hamid and colleagues mention the following caveats: (1) some patients were MOG-IgG seropositive, a con- dition that overlaps clinically, but is likely a myelinop- athy rather than an astrocytopathy,11 (2) some cases had suggestive clinical findings but lacked required “NMOSD-typical” MRI confirmation, (3) some had suggestive MRI findings without clinical correlate, and (4) AQP4-IgG-seronegative cases of recurrent iso- lated optic neuritis and recurrent longitudinal exten- sive transverse myelitis (LETM) are not included in the 2015 criteria, although many clinicians treat them as if they were AQP4 seropositive.
Beyond these possible explanations, how should the remaining gap in diagnostic criteria sensitivity be definitively addressed for AQP4-IgG-seronegative patients? We believe that ultimate validation of AQP4-IgG-seronegative cases as NMOSD will depend on systematic, prospective, and longitudinal studies (or analysis of retrospectively obtained fol- low-up data of a fully ascertained population) that examine a broad group of patients in whom NMOSD is reasonably suspected.4 The ultimate reference standard is continuing conformity to an NMOSD diagnosis and failure to exhibit signs, symptoms, or other findings of an alternative “mimic” condition.4 Evolution of the clinical course and MRI findings may fulfill NMOSD criteria over time or identify alternative diagnoses; this will allow estimation of criteria specificity, which is not evaluable from the Hamid study design. AQP4-IgG seroconversion rates
should be examined. Immunopathological studies from biopsies or autopsies, when available, might arbitrate diagnosis in individual cases and serve to refine clinical and radiological disease patterns.12 The clinical spectrum, natural history, pathobiology, and response to treatment of MOG-IgG-associated NMOSD remains to be fully defined.
Future research may move us closer to an objective of biomarker-supported diagnosis that informs treatment decisions through understanding of underlying dis- ease mechanisms. The ultimate goal is to have diag- nostic criteria that individualize treatment yet account for all patients encountered in practice and that are both sensitive and specific. In the meantime, IPND consensus has achieved earlier, confident recognition of NMOSD diagnosis, so that early appropriate attack prevention is possible. Hamid and colleagues’ work highlights not only the utility of a more liberal and unified diagnostic criteria but also the work that remains to characterize AQP4-IgG-seronegative patients and assess the complete diagnostic properties of the 2015 IPND criteria.
Declaration of Conflicting Interests The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/ or publication of this article: D.M.W. receives research support paid to Mayo Clinic from Alexion Pharmaceuticals and Terumo BCT and serves on an adjudication committee for a NMO clinical trial con- ducted by MedImmune. B.G.W. receives royalties from RSR Ltd, Oxford University and MVZ Labor PD Dr. Volkmann und Kollegen GbR repatent for NMO- IgG as a diagnostic test for NMO and related disorders. He serves as a member of an adjudication committee for clinical trials in NMO being conducted by MedImmune and Alexion Pharmaceutical companies.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Lennon VA, Wingerchuk DM, Kryzer TJ, et al. A
serum autoantibody marker of neuromyelitis optica: Distinction from multiple sclerosis. Lancet 2004; 364: 2106–2112.
2. Wingerchuk DM, Lennon VA, Pittock SJ, et al. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006; 66: 1485–1489.
Multiple Sclerosis Journal 23(2)
184 journals.sagepub.com/home/msj
3. Wingerchuk DM, Lennon VA, Lucchinetti CF, et al. The spectrum of neuromyelitis optica. Lancet Neurol 2007; 6: 810–815.
4. Wingerchuk DM, Banwell B, Bennett JL, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85: 177–189.
5. Hamid SHM, Elsone L, Mutch K, et al. The impact of 2015 neuromyelitis optica spectrum disorders criteria on diagnostic rates. Mult Scler. Epub ahead of print 23 August 2016. DOI: 10.1177/1352458516663853.
6. Hyun JW, Jeong IH, Joung A, et al. Evaluation of the 2015 diagnostic criteria for neuromyelitis optica spectrum disorder. Neurology 2016; 86: 1772–1779.
7. Aggarwal R, Ringold S, Khanna D, et al. Distinctions between diagnostic and classification criteria. Arthritis Care Res 2015; 67: 891–897.
8. Zekeridou A and Lennon VA. Aquaporin-4 autoimmunity. Neurol Neuroimmunol Neuroinflamm 2015; 2(4): e110.
9. Sepúlveda M, Armangué T, Sola-Valls N, et al. Neuromyelitis optica spectrum disorders: Comparison according to the phenotype and serostatus. Neurol Neuroimmunol Neuroinflamm 2016; 3: e225.
10. Jurynczyk M, Weinshenker B, Akman-Demir G, et al. Status of diagnostic approaches to AQP4-IgG seronegative NMO and NMO/MS overlap syndromes. J Neurol 2016; 263: 140–149.
11. Kaneko K, Sato D, Nakashima I, et al. Myelin injury without astrocytopathy in neuroinflammatory disorders with MOG antibodies. J Neurol Neurosurg Psychiatry 2016; 87: 1257–1259.
12. Popescu BF, Guo Y, Jentoft ME, et al. Diagnostic utility of aquaporin-4 in the analysis of active demyelinating lesions. Neurology 2015; 84: 148–158.
Visit SAGE journals online http://journals.sagepub.com/ home/msj
SAGE journals
© The Author(s), 2017. Reprints and permissions: http://www.sagepub.co.uk/ journalsPermissions.nav
Although some of their characteristics overlap, neuro- myelitis optica spectrum disorder (NMOSD) is dis- tinct from multiple sclerosis (MS) in many clinical, laboratory, and neuroimaging features, including its strong association with a pathogenic autoantibody biomarker, AQP4-IgG.1 The specificity of AQP4-IgG was leveraged by its incorporation into revised diag- nostic criteria in 2006.2 Subsequently, a number of additional clinical phenotypes and magnetic reso- nance imaging (MRI) patterns were noted to occur in AQP4-IgG-seropositive neuromyelitis optica (NMO) patients who fulfilled 2006 criteria. These presenta- tions (notably, brain involvement and “NMO-typical” MRI lesion patterns) were proposed to be part of an umbrella term “NMO spectrum disorders” in 2007.3
In 2015, the International Panel for Neuromyelitis Optica Diagnosis (IPND) proposed consensus diag- nostic criteria using the unified term NMOSD.4 The 2015 criteria effectively merged the 2006 and 2007 definitions by including all AQP4-IgG-seropositive patients and further defined an expanded array of clinical and MRI phenotypes. A category of NMOSD without AQP4-IgG was retained to identify the roughly one-third of clinical cases that do not have detectable serum AQP4-IgG. Early and accurate NMOSD diagnosis is important for treatment deci- sion-making because AQP4-IgG-seropositive patients are at high risk for relapse (>60% in the first year) and MS disease-modifying therapies (especially inter- feron-beta and natalizumab) aggravate NMOSD regardless of AQP4-IgG serostatus.
In this issue, Hamid et al.5 present an analysis of the effects of diagnostic categorization by applying the 2006 NMO and 2015 NMOSD criteria to 176 subjects at an NMOSD specialty center in whom they diag- nosed an inflammatory demyelinating central nervous system (CNS) syndrome suggestive of NMOSD and atypical for MS. In all, 63 (35.8%; 42 AQP4-IgG seropositive) had characteristics fulfilling the 2006
criteria. When 2015 IPND criteria were applied to the same cohort, 111 (63.1%; 81 seropositive) met crite- ria. All but nine of the incremental patients were AQP4-IgG seropositive and failed to meet 2006 crite- ria because they had not experienced both optic neuri- tis and myelitis. Hamid et al. conclude that application of the 2015 rather than 2006 criteria increased the diagnostic yield (sensitivity) by 76%. Another study demonstrated a similar increase (85%).6
Is the increase in sensitivity as impressive as it seems? Although not formally enshrined in diagnostic crite- ria, the 2007 concept of NMOSD had identified patients with recurrent optic neuritis, recurrent myeli- tis, and certain typical brain syndromes as NMOSD; such patients were treated with similar strategies as NMO patients who satisfied 2006 criteria. If one applies both the 2006 NMO definition and 2007 NMOSD concept (the latter includes only AQP4-IgG- seropositive cases), then 102 of 176 patients (58.0%) in Hamid et al.’s cohort would have been diagnosed NMO or NMOSD based on prevailing practice. The 2015 IPND criteria incrementally identified nine patients (all AQP4-IgG seronegative), an absolute increase in 5.1%; these cases experienced “combina- tions of clinical events” not satisfying 2006 criteria (brain stem plus either optic nerve or spinal cord or diencephalic plus spinal cord). A total of 50% of the AQP4-IgG-seronegative patients had myelin oligo- dendrocyte glycoprotein (MOG) autoantibodies.
Diagnostic criteria identify a collection of symptoms, signs, and tests that are used in routine clinical practice to provide care for individual patients. In contrast, classification criteria are standardized definitions that are meant to identify relatively uniform groups of patients for the purpose of clinical research. Diagnostic criteria must be broad (highly sensitive) in order to reflect disease heterogeneity yet maintain reasonable specificity; classification criteria require high specific- ity. The differentiation of criteria type is particularly
Neuromyelitis optica spectrum disorder diagnostic criteria: Sensitivity and specificity are both important
Dean M Wingerchuk and Brian G Weinshenker
Correspondence to: DM Wingerchuk Department of Neurology, Mayo Clinic, 13400 E. Shea Blvd, Scottsdale, AZ 85259, USA. wingerchuk.dean@mayo. edu
Dean M Wingerchuk Department of Neurology, Mayo Clinic, Scottsdale, AZ, USA
Brian G Weinshenker Department of Neurology, Mayo Clinic, Rochester, MN, USA
688352MSJ0010.1177/1352458516688352Multiple Sclerosis JournalDM Wingerchuk and BG Weinshenker editorial2016
journals.sagepub.com/home/msj 183
important in the absence of a diagnostic standard, as is the case for most rheumatologic diseases.7
The distinction between criteria types is also relevant to MS and NMOSD. Although classification criteria are appropriate for MS because a single standard is lacking, AQP4-IgG may be a standard for NMOSD.8 Defining the disease based on AQP4-IgG seropositiv- ity would identify a homogeneous patient cohort suit- able for pathobiology studies and enhance the validity of therapeutic clinical trials at the expense of general- izability. However, restricting the diagnosis to AQP4- IgG-seropositive patients ignores the 30% of patients with otherwise typical NMOSD but who are AQP4- IgG seronegative. Such patients have a similar disease course and similar responses to preventive therapies as the seropositive patients.9 The Hamid report shows that a group of expert neurologists felt that 176 patients had a syndrome compatible with NMOSD (presuma- bly with no better explanation), but only 63% could be diagnosed by 2015 criteria. The other 37% remain an important, likely heterogeneous, group of patients who lack a firm diagnosis, as recognized by others.10 Hamid and colleagues mention the following caveats: (1) some patients were MOG-IgG seropositive, a con- dition that overlaps clinically, but is likely a myelinop- athy rather than an astrocytopathy,11 (2) some cases had suggestive clinical findings but lacked required “NMOSD-typical” MRI confirmation, (3) some had suggestive MRI findings without clinical correlate, and (4) AQP4-IgG-seronegative cases of recurrent iso- lated optic neuritis and recurrent longitudinal exten- sive transverse myelitis (LETM) are not included in the 2015 criteria, although many clinicians treat them as if they were AQP4 seropositive.
Beyond these possible explanations, how should the remaining gap in diagnostic criteria sensitivity be definitively addressed for AQP4-IgG-seronegative patients? We believe that ultimate validation of AQP4-IgG-seronegative cases as NMOSD will depend on systematic, prospective, and longitudinal studies (or analysis of retrospectively obtained fol- low-up data of a fully ascertained population) that examine a broad group of patients in whom NMOSD is reasonably suspected.4 The ultimate reference standard is continuing conformity to an NMOSD diagnosis and failure to exhibit signs, symptoms, or other findings of an alternative “mimic” condition.4 Evolution of the clinical course and MRI findings may fulfill NMOSD criteria over time or identify alternative diagnoses; this will allow estimation of criteria specificity, which is not evaluable from the Hamid study design. AQP4-IgG seroconversion rates
should be examined. Immunopathological studies from biopsies or autopsies, when available, might arbitrate diagnosis in individual cases and serve to refine clinical and radiological disease patterns.12 The clinical spectrum, natural history, pathobiology, and response to treatment of MOG-IgG-associated NMOSD remains to be fully defined.
Future research may move us closer to an objective of biomarker-supported diagnosis that informs treatment decisions through understanding of underlying dis- ease mechanisms. The ultimate goal is to have diag- nostic criteria that individualize treatment yet account for all patients encountered in practice and that are both sensitive and specific. In the meantime, IPND consensus has achieved earlier, confident recognition of NMOSD diagnosis, so that early appropriate attack prevention is possible. Hamid and colleagues’ work highlights not only the utility of a more liberal and unified diagnostic criteria but also the work that remains to characterize AQP4-IgG-seronegative patients and assess the complete diagnostic properties of the 2015 IPND criteria.
Declaration of Conflicting Interests The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/ or publication of this article: D.M.W. receives research support paid to Mayo Clinic from Alexion Pharmaceuticals and Terumo BCT and serves on an adjudication committee for a NMO clinical trial con- ducted by MedImmune. B.G.W. receives royalties from RSR Ltd, Oxford University and MVZ Labor PD Dr. Volkmann und Kollegen GbR repatent for NMO- IgG as a diagnostic test for NMO and related disorders. He serves as a member of an adjudication committee for clinical trials in NMO being conducted by MedImmune and Alexion Pharmaceutical companies.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Lennon VA, Wingerchuk DM, Kryzer TJ, et al. A
serum autoantibody marker of neuromyelitis optica: Distinction from multiple sclerosis. Lancet 2004; 364: 2106–2112.
2. Wingerchuk DM, Lennon VA, Pittock SJ, et al. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006; 66: 1485–1489.
Multiple Sclerosis Journal 23(2)
184 journals.sagepub.com/home/msj
3. Wingerchuk DM, Lennon VA, Lucchinetti CF, et al. The spectrum of neuromyelitis optica. Lancet Neurol 2007; 6: 810–815.
4. Wingerchuk DM, Banwell B, Bennett JL, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85: 177–189.
5. Hamid SHM, Elsone L, Mutch K, et al. The impact of 2015 neuromyelitis optica spectrum disorders criteria on diagnostic rates. Mult Scler. Epub ahead of print 23 August 2016. DOI: 10.1177/1352458516663853.
6. Hyun JW, Jeong IH, Joung A, et al. Evaluation of the 2015 diagnostic criteria for neuromyelitis optica spectrum disorder. Neurology 2016; 86: 1772–1779.
7. Aggarwal R, Ringold S, Khanna D, et al. Distinctions between diagnostic and classification criteria. Arthritis Care Res 2015; 67: 891–897.
8. Zekeridou A and Lennon VA. Aquaporin-4 autoimmunity. Neurol Neuroimmunol Neuroinflamm 2015; 2(4): e110.
9. Sepúlveda M, Armangué T, Sola-Valls N, et al. Neuromyelitis optica spectrum disorders: Comparison according to the phenotype and serostatus. Neurol Neuroimmunol Neuroinflamm 2016; 3: e225.
10. Jurynczyk M, Weinshenker B, Akman-Demir G, et al. Status of diagnostic approaches to AQP4-IgG seronegative NMO and NMO/MS overlap syndromes. J Neurol 2016; 263: 140–149.
11. Kaneko K, Sato D, Nakashima I, et al. Myelin injury without astrocytopathy in neuroinflammatory disorders with MOG antibodies. J Neurol Neurosurg Psychiatry 2016; 87: 1257–1259.
12. Popescu BF, Guo Y, Jentoft ME, et al. Diagnostic utility of aquaporin-4 in the analysis of active demyelinating lesions. Neurology 2015; 84: 148–158.
Visit SAGE journals online http://journals.sagepub.com/ home/msj
SAGE journals
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