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Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study.
Lancet Neurol 2018; 17(2):133-142LN

Abstract

BACKGROUND

In 2016, the Magnetic Resonance Imaging in Multiple Sclerosis (MAGNIMS) network proposed modifications to the MRI criteria to define dissemination in space (DIS) and time (DIT) for the diagnosis of multiple sclerosis in patients with clinically isolated syndrome (CIS). Changes to the DIS definition included removal of the distinction between symptomatic and asymptomatic lesions, increasing the number of lesions needed to define periventricular involvement to three, combining cortical and juxtacortical lesions, and inclusion of optic nerve evaluation. For DIT, removal of the distinction between symptomatic and asymptomatic lesions was suggested. We compared the performance of the 2010 McDonald and 2016 MAGNIMS criteria for multiple sclerosis diagnosis in a large multicentre cohort of patients with CIS to provide evidence to guide revisions of multiple sclerosis diagnostic criteria.

METHODS

Brain and spinal cord MRI and optic nerve assessments from patients with typical CIS suggestive of multiple sclerosis done less than 3 months from clinical onset in eight European multiple sclerosis centres were included in this retrospective study. Eligible patients were 16-60 years, and had a first CIS suggestive of CNS demyelination and typical of relapsing-remitting multiple sclerosis, a complete neurological examination, a baseline brain and spinal cord MRI scan obtained less than 3 months from clinical onset, and a follow-up brain scan obtained less than 12 months from CIS onset. We recorded occurrence of a second clinical attack (clinically definite multiple sclerosis) at months 36 and 60. We evaluated MRI criteria performance for DIS, DIT, and DIS plus DIT with a time-dependent receiver operating characteristic curve analysis.

FINDINGS

Between June 16, 1995, and Jan 27, 2017, 571 patients with CIS were screened, of whom 368 met all study inclusion criteria. At the last evaluation (median 50·0 months [IQR 27·0-78·4]), 189 (51%) of 368 patients developed clinically definite multiple sclerosis. At 36 months, the two DIS criteria showed high sensitivity (2010 McDonald 0·91 [95% CI 0·85-0·94] and 2016 MAGNIMS 0·93 [0·88-0·96]), similar specificity (0·33 [0·25-0·42] and 0·32 [0·24-0·41]), and similar area under the curve values (AUC; 0·62 [0·57-0·67] and 0·63 [0·58-0·67]). Performance was not affected by inclusion of symptomatic lesions (sensitivity 0·92 [0·87-0·96], specificity 0·31 [0·23-0·40], AUC 0·62 [0·57-0·66]) or cortical lesions (sensitivity 0·92 [0·87-0·95], specificity 0·32 [0·24-0·41], AUC 0·62 [0·57-0·67]). Requirement of three periventricular lesions resulted in slightly lower sensitivity (0·85 [0·78-0·90], slightly higher specificity (0·40 [0·32-0·50], and similar AUC (0·63 [0·57-0·68]). Inclusion of optic nerve evaluation resulted in similar sensitivity (0·92 [0·87-0·96]), and slightly lower specificity (0·26 [0·18-0·34]) and AUC (0·59 [0·55-0·64]). AUC values were also similar for DIT (2010 McDonald 0·61 [0·55-0·67] and 2016 MAGNIMS 0·61 [0·55-0·66]) and DIS plus DIT (0·62 [0·56-0·67] and 0·64 [0·58-0·69]).

INTERPRETATION

The 2016 MAGNIMS criteria showed similar accuracy to the 2010 McDonald criteria in predicting the development of clinically definite multiple sclerosis. Inclusion of symptomatic lesions is expected to simplify the clinical use of MRI criteria without reducing accuracy, and our findings suggest that needing three lesions to define periventricular involvement might slightly increase specificity, suggesting that these two factors could be considered during further revisions of multiple sclerosis diagnostic criteria.

FUNDING

UK MS Society, National Institute for Health Research University College London Hospitals Biomedical Research Centre, Dutch MS Research Foundation.

Authors+Show Affiliations

Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy; Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy. Electronic address: filippi.massimo@hsr.it.Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy; Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, University College London, London, UK; National Institute for Health Research University College London Hospitals Biomedical Research Centre, London, UK.Clinic of Neurology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.Section of Neuroradiology, Department of Radiology, Hospital Universitari Vall d'Hebron, Barcelona, Spain.Clinic of Optic Neuritis and Clinic of Multiple Sclerosis, Department of Neurology, Rigshospitalet Glostrup, University of Copenhagen, Copenhagen, Denmark.Department of Neurology, Medical University of Graz, Graz, Austria.Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, University College London, London, UK; National Institute for Health Research University College London Hospitals Biomedical Research Centre, London, UK; Department of Radiology and Nuclear Medicine, MS Center Amsterdam, VU University Medical Center, Amsterdam, Netherlands.Department of Neurosciences, San Camillo Forlanini Hospital, Rome, Italy.Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, University College London, London, UK; National Institute for Health Research University College London Hospitals Biomedical Research Centre, London, UK.Clinic of Neurology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.Unitat de Neuroimmunologia Clinica, Centre d'Esclerosi Múltiple de Catalunya (CEM-Cat), Hospital Universitari Vall d'Hebron, Barcelona, Spain.Functional Imaging Unit, Department of Clinical Physiology, Nuclear Medicine and PET, Rigshospitalet, Copenhagen, Denmark.Department of Neurology, Medical University of Graz, Graz, Austria.Department of Neurology, MS Center Amsterdam, VU University Medical Center, Amsterdam, Netherlands.Department of Neurosciences, San Camillo Forlanini Hospital, Rome, Italy.Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, University College London, London, UK; National Institute for Health Research University College London Hospitals Biomedical Research Centre, London, UK.Unitat de Neuroimmunologia Clinica, Centre d'Esclerosi Múltiple de Catalunya (CEM-Cat), Hospital Universitari Vall d'Hebron, Barcelona, Spain.Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.Department of Radiology and Nuclear Medicine, MS Center Amsterdam, VU University Medical Center, Amsterdam, Netherlands; Department of Neurology, MS Center Amsterdam, VU University Medical Center, Amsterdam, Netherlands.Department of Neurology, MS Center Amsterdam, VU University Medical Center, Amsterdam, Netherlands.Clinic of Neurology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy; Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.

Pub Type(s)

Journal Article
Multicenter Study
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29275979

Citation

Filippi, Massimo, et al. "Prediction of a Multiple Sclerosis Diagnosis in Patients With Clinically Isolated Syndrome Using the 2016 MAGNIMS and 2010 McDonald Criteria: a Retrospective Study." The Lancet. Neurology, vol. 17, no. 2, 2018, pp. 133-142.
Filippi M, Preziosa P, Meani A, et al. Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study. Lancet Neurol. 2018;17(2):133-142.
Filippi, M., Preziosa, P., Meani, A., Ciccarelli, O., Mesaros, S., Rovira, A., ... Rocca, M. A. (2018). Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study. The Lancet. Neurology, 17(2), pp. 133-142. doi:10.1016/S1474-4422(17)30469-6.
Filippi M, et al. Prediction of a Multiple Sclerosis Diagnosis in Patients With Clinically Isolated Syndrome Using the 2016 MAGNIMS and 2010 McDonald Criteria: a Retrospective Study. Lancet Neurol. 2018;17(2):133-142. PubMed PMID: 29275979.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study. AU - Filippi,Massimo, AU - Preziosa,Paolo, AU - Meani,Alessandro, AU - Ciccarelli,Olga, AU - Mesaros,Sarlota, AU - Rovira,Alex, AU - Frederiksen,Jette, AU - Enzinger,Christian, AU - Barkhof,Frederik, AU - Gasperini,Claudio, AU - Brownlee,Wallace, AU - Drulovic,Jelena, AU - Montalban,Xavier, AU - Cramer,Stig P, AU - Pichler,Alexander, AU - Hagens,Marloes, AU - Ruggieri,Serena, AU - Martinelli,Vittorio, AU - Miszkiel,Katherine, AU - Tintorè,Mar, AU - Comi,Giancarlo, AU - Dekker,Iris, AU - Uitdehaag,Bernard, AU - Dujmovic-Basuroski,Irena, AU - Rocca,Maria A, Y1 - 2017/12/21/ PY - 2017/08/17/received PY - 2017/11/02/revised PY - 2017/11/13/accepted PY - 2017/12/26/pubmed PY - 2019/1/25/medline PY - 2017/12/26/entrez SP - 133 EP - 142 JF - The Lancet. Neurology JO - Lancet Neurol VL - 17 IS - 2 N2 - BACKGROUND: In 2016, the Magnetic Resonance Imaging in Multiple Sclerosis (MAGNIMS) network proposed modifications to the MRI criteria to define dissemination in space (DIS) and time (DIT) for the diagnosis of multiple sclerosis in patients with clinically isolated syndrome (CIS). Changes to the DIS definition included removal of the distinction between symptomatic and asymptomatic lesions, increasing the number of lesions needed to define periventricular involvement to three, combining cortical and juxtacortical lesions, and inclusion of optic nerve evaluation. For DIT, removal of the distinction between symptomatic and asymptomatic lesions was suggested. We compared the performance of the 2010 McDonald and 2016 MAGNIMS criteria for multiple sclerosis diagnosis in a large multicentre cohort of patients with CIS to provide evidence to guide revisions of multiple sclerosis diagnostic criteria. METHODS: Brain and spinal cord MRI and optic nerve assessments from patients with typical CIS suggestive of multiple sclerosis done less than 3 months from clinical onset in eight European multiple sclerosis centres were included in this retrospective study. Eligible patients were 16-60 years, and had a first CIS suggestive of CNS demyelination and typical of relapsing-remitting multiple sclerosis, a complete neurological examination, a baseline brain and spinal cord MRI scan obtained less than 3 months from clinical onset, and a follow-up brain scan obtained less than 12 months from CIS onset. We recorded occurrence of a second clinical attack (clinically definite multiple sclerosis) at months 36 and 60. We evaluated MRI criteria performance for DIS, DIT, and DIS plus DIT with a time-dependent receiver operating characteristic curve analysis. FINDINGS: Between June 16, 1995, and Jan 27, 2017, 571 patients with CIS were screened, of whom 368 met all study inclusion criteria. At the last evaluation (median 50·0 months [IQR 27·0-78·4]), 189 (51%) of 368 patients developed clinically definite multiple sclerosis. At 36 months, the two DIS criteria showed high sensitivity (2010 McDonald 0·91 [95% CI 0·85-0·94] and 2016 MAGNIMS 0·93 [0·88-0·96]), similar specificity (0·33 [0·25-0·42] and 0·32 [0·24-0·41]), and similar area under the curve values (AUC; 0·62 [0·57-0·67] and 0·63 [0·58-0·67]). Performance was not affected by inclusion of symptomatic lesions (sensitivity 0·92 [0·87-0·96], specificity 0·31 [0·23-0·40], AUC 0·62 [0·57-0·66]) or cortical lesions (sensitivity 0·92 [0·87-0·95], specificity 0·32 [0·24-0·41], AUC 0·62 [0·57-0·67]). Requirement of three periventricular lesions resulted in slightly lower sensitivity (0·85 [0·78-0·90], slightly higher specificity (0·40 [0·32-0·50], and similar AUC (0·63 [0·57-0·68]). Inclusion of optic nerve evaluation resulted in similar sensitivity (0·92 [0·87-0·96]), and slightly lower specificity (0·26 [0·18-0·34]) and AUC (0·59 [0·55-0·64]). AUC values were also similar for DIT (2010 McDonald 0·61 [0·55-0·67] and 2016 MAGNIMS 0·61 [0·55-0·66]) and DIS plus DIT (0·62 [0·56-0·67] and 0·64 [0·58-0·69]). INTERPRETATION: The 2016 MAGNIMS criteria showed similar accuracy to the 2010 McDonald criteria in predicting the development of clinically definite multiple sclerosis. Inclusion of symptomatic lesions is expected to simplify the clinical use of MRI criteria without reducing accuracy, and our findings suggest that needing three lesions to define periventricular involvement might slightly increase specificity, suggesting that these two factors could be considered during further revisions of multiple sclerosis diagnostic criteria. FUNDING: UK MS Society, National Institute for Health Research University College London Hospitals Biomedical Research Centre, Dutch MS Research Foundation. SN - 1474-4465 UR - https://www.unboundmedicine.com/medline/citation/29275979/Prediction_of_a_multiple_sclerosis_diagnosis_in_patients_with_clinically_isolated_syndrome_using_the_2016_MAGNIMS_and_2010_McDonald_criteria:_a_retrospective_study_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1474-4422(17)30469-6 DB - PRIME DP - Unbound Medicine ER -