Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study

Massimo Filippi; Paolo Preziosa; Alessandro Meani; Olga Ciccarelli; Sarlota Mesaros; Alex Rovira; Jette Frederiksen; Christian Enzinger; Frederik Barkhof; Claudio Gasperini; Wallace Brownlee; Jelena Drulovic; Xavier Montalban; Stig P Cramer; Alexander Pichler; Marloes Hagens; Serena Ruggieri; Vittorio Martinelli; Katherine Miszkiel; Mar Tintorè; Giancarlo Comi; Iris Dekker; Bernard Uitdehaag; Irena Dujmovic-Basuroski; Maria A Rocca

doi:10.1016/S1474-4422(17)30469-6

Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study

Massimo Filippi, Paolo Preziosa, Alessandro Meani, Olga Ciccarelli, Sarlota Mesaros, Alex Rovira, Jette Frederiksen, Christian Enzinger, Frederik Barkhof, Claudio Gasperini, Wallace Brownlee, Jelena Drulovic, Xavier Montalban, Stig P Cramer, Alexander Pichler, Marloes Hagens, Serena Ruggieri, Vittorio Martinelli, Katherine Miszkiel, Mar TintorèGiancarlo Comi, Iris Dekker, Bernard Uitdehaag, Irena Dujmovic-Basuroski, Maria A Rocca

Department of Clinical Medicine

56 Citations (Scopus)

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.

Original language	English
Journal	Lancet Neurology
Volume	17
Issue number	2
Pages (from-to)	133-142
ISSN	1474-4422
DOIs	https://doi.org/10.1016/S1474-4422(17)30469-6
Publication status	Published - Feb 2018

Keywords

Adult
Brain/diagnostic imaging
Brain Stem/diagnostic imaging
Cerebellar Diseases/diagnostic imaging
Cerebral Ventricles/diagnostic imaging
Cohort Studies
Demyelinating Diseases/diagnostic imaging
Diagnosis, Differential
Female
Follow-Up Studies
Humans
Kaplan-Meier Estimate
Magnetic Resonance Imaging
Male
Multiple Sclerosis/diagnostic imaging
Neurologic Examination
Optic Nerve/diagnostic imaging
Optic Neuritis/diagnostic imaging
Spinal Cord/diagnostic imaging

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10.1016/S1474-4422(17)30469-6

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Filippi, M., Preziosa, P., Meani, A., Ciccarelli, O., Mesaros, S., Rovira, A., Frederiksen, J., Enzinger, C., Barkhof, F., Gasperini, C., Brownlee, W., Drulovic, J., Montalban, X., Cramer, S. P., Pichler, A., Hagens, M., Ruggieri, S., Martinelli, V., Miszkiel, K., ... 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. Lancet Neurology, 17(2), 133-142. https://doi.org/10.1016/S1474-4422(17)30469-6

Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria : a retrospective study. / Filippi, Massimo; Preziosa, Paolo; Meani, Alessandro et al.

In: Lancet Neurology, Vol. 17, No. 2, 02.2018, p. 133-142.

Research output: Contribution to journal › Journal article › Research › peer-review

Filippi, M, Preziosa, P, Meani, A, Ciccarelli, O, Mesaros, S, Rovira, A, Frederiksen, J, Enzinger, C, Barkhof, F, Gasperini, C, Brownlee, W, Drulovic, J, Montalban, X, Cramer, SP, Pichler, A, Hagens, M, Ruggieri, S, Martinelli, V, Miszkiel, K, Tintorè, M, Comi, G, Dekker, I, Uitdehaag, B, Dujmovic-Basuroski, I & Rocca, MA 2018, 'Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study', Lancet Neurology, vol. 17, no. 2, pp. 133-142. https://doi.org/10.1016/S1474-4422(17)30469-6

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title = "Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study",

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.",

keywords = "Adult, Brain/diagnostic imaging, Brain Stem/diagnostic imaging, Cerebellar Diseases/diagnostic imaging, Cerebral Ventricles/diagnostic imaging, Cohort Studies, Demyelinating Diseases/diagnostic imaging, Diagnosis, Differential, Female, Follow-Up Studies, Humans, Kaplan-Meier Estimate, Magnetic Resonance Imaging, Male, Multiple Sclerosis/diagnostic imaging, Neurologic Examination, Optic Nerve/diagnostic imaging, Optic Neuritis/diagnostic imaging, Spinal Cord/diagnostic imaging",

author = "Massimo Filippi and Paolo Preziosa and Alessandro Meani and Olga Ciccarelli and Sarlota Mesaros and Alex Rovira and Jette Frederiksen and Christian Enzinger and Frederik Barkhof and Claudio Gasperini and Wallace Brownlee and Jelena Drulovic and Xavier Montalban and Cramer, {Stig P} and Alexander Pichler and Marloes Hagens and Serena Ruggieri and Vittorio Martinelli and Katherine Miszkiel and Mar Tintor{\`e} and Giancarlo Comi and Iris Dekker and Bernard Uitdehaag and Irena Dujmovic-Basuroski and Rocca, {Maria A}",

year = "2018",

month = feb,

doi = "10.1016/S1474-4422(17)30469-6",

language = "English",

volume = "17",

pages = "133--142",

journal = "The Lancet Neurology",

issn = "1474-4422",

publisher = "TheLancet Publishing Group",

number = "2",

}

TY - JOUR

T1 - Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria

T2 - 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

PY - 2018/2

Y1 - 2018/2

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.

AB - 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.

KW - Adult

KW - Brain/diagnostic imaging

KW - Brain Stem/diagnostic imaging

KW - Cerebellar Diseases/diagnostic imaging

KW - Cerebral Ventricles/diagnostic imaging

KW - Cohort Studies

KW - Demyelinating Diseases/diagnostic imaging

KW - Diagnosis, Differential

KW - Female

KW - Follow-Up Studies

KW - Humans

KW - Kaplan-Meier Estimate

KW - Magnetic Resonance Imaging

KW - Male

KW - Multiple Sclerosis/diagnostic imaging

KW - Neurologic Examination

KW - Optic Nerve/diagnostic imaging

KW - Optic Neuritis/diagnostic imaging

KW - Spinal Cord/diagnostic imaging

U2 - 10.1016/S1474-4422(17)30469-6

DO - 10.1016/S1474-4422(17)30469-6

M3 - Journal article

C2 - 29275979

SN - 1474-4422

VL - 17

SP - 133

EP - 142

JO - The Lancet Neurology

JF - The Lancet Neurology

IS - 2

ER -

Prediction of a multiple sclerosis diagnosis in patients with clinically isolated syndrome using the 2016 MAGNIMS and 2010 McDonald criteria: a retrospective study

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Keywords

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