MRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines

doi:10.1016/S1474-4422(15)00393-2

The Lancet Neurology

Volume 15, Issue 3, March 2016, Pages 292-303

https://doi.org/10.1016/S1474-4422(15)00393-2 Get rights and content

Summary

In patients presenting with a clinically isolated syndrome, MRI can support and substitute clinical information in the diagnosis of multiple sclerosis by showing disease dissemination in space and time and by helping to exclude disorders that can mimic multiple sclerosis. MRI criteria were first included in the diagnostic work-up for multiple sclerosis in 2001, and since then several modifications to the criteria have been proposed in an attempt to simplify lesion-count models for showing disease dissemination in space, change the timing of MRI scanning to show dissemination in time, and increase the value of spinal cord imaging. Since the last update of these criteria, new data on the use of MRI to establish dissemination in space and time have become available, and MRI technology has improved. State-of-the-art MRI findings in these patients were discussed in a MAGNIMS workshop, the goal of which was to provide an evidence-based and expert-opinion consensus on proposed modifications to MRI criteria for the diagnosis of multiple sclerosis.

Introduction

MRI was formally included in the diagnostic work-up of patients presenting with a clinically isolated syndrome suggestive of multiple sclerosis in 2001 by an international panel of experts.¹ Diagnosis of multiple sclerosis relies on proof of disease dissemination in space and time and exclusion of other disorders that can mimic multiple sclerosis by their clinical and laboratory profile. MRI can support and substitute clinical information for multiple sclerosis diagnosis, enabling an early and accurate diagnosis and, as such, early treatment.

MRI criteria for multiple sclerosis are based on the presence of focal lesions in the white matter of the CNS, which are considered typical for this disorder in terms of distribution, morphology, evolution, and signal abnormalities on conventional MRI sequences (eg, T2-weighted and T2-weighted fluid-attenuated inversion recovery [FLAIR] scans, and pre-contrast and post-contrast T1-weighted scans).2, 3, 4 Several modifications of MRI diagnostic criteria have been proposed, but emphasis has consistently been that such criteria should be applied only in patients who present with a typical clinically isolated syndrome suggestive of multiple sclerosis or symptoms consistent with a CNS inflammatory demyelinating disease. These revisions have simplified lesion-count models for proof of dissemination in space, changed the timing of MRI scanning to show dissemination in time, and increased the value of spinal cord imaging.5, 6, 7, 8 In 2007, the European collaborative research network that studies MRI in multiple sclerosis (MAGNIMS) reviewed the findings of studies that addressed these issues and proposed new MRI criteria to be applied in multiple sclerosis.⁹ Those MAGNIMS criteria are included in the most recent diagnostic criteria for multiple sclerosis, known as the 2010 McDonald criteria.¹⁰ Consensus guidelines for clinicians to optimise planning, performance, and interpretation of brain and spinal cord MRI in the multiple sclerosis diagnostic process have also been published and are complementary to the recommendations in this Review.¹¹

Since 2011, new data on application of MRI to show dissemination in space and time have become available, and these data deserve consideration for future revisions of the multiple sclerosis diagnostic criteria. Additionally, many improvements in MRI technology have occurred, which have resulted in development of innovative acquisition sequences, identification of novel pathophysiological mechanisms that might help with differential diagnosis, and new insights into multiple sclerosis disease activity from studies using high-field and ultra-high-field scanners. The MAGNIMS members felt the need for timely review of these findings and consideration of how they should be used to modify the MRI criteria for diagnosis of multiple sclerosis. A summary of the main proposed revisions or clarifications to the MRI component of the 2010 McDonald criteria¹⁰ for multiple sclerosis is given in panel 1.

Section snippets

Methods

In March, 2015, an international workshop was held in Milan, Italy, under the auspices of MAGNIMS. The workshop involved clinical and imaging experts in diagnosis and management of patients with multiple sclerosis, including neurologists and neuroradiologists. Before the meeting, two co-chairs (M Filippi and F Barkhof) identified areas in which revision, clarification, or both might be necessary in future diagnostic criteria for multiple sclerosis. Experts for each topic were invited to provide

Dissemination in space

According to the 2010 McDonald criteria for multiple sclerosis,¹⁰ dissemination in space can be established with at least one T2 lesion in at least two of four locations characteristic for multiple sclerosis (juxtacortical, periventricular, infratentorial, and spinal cord). We propose an increase in the number of lesions necessary to confirm involvement of the periventricular area from one to three, and to add an additional cardinal CNS location, the optic nerve (panel 2). Together with a

Dissemination in time

According to the 2010 McDonald criteria,¹⁰ disease dissemination in time can be established by the following: presence of at least one new T2 or gadolinium-enhancing lesion on follow-up MRI, with reference to a baseline scan, irrespective of the timing of the baseline MRI; or the simultaneous presence of asymptomatic gadolinium-enhancing and non-enhancing lesions at any time.

Non-enhancing T1-hypointense lesions (black holes) are chronic lesions characterised by severe axonal damage.⁵⁸ In

Symptomatic lesions

In patients with a clinically isolated syndrome, symptomatic lesions that align with an acute clinical deficit do not contribute to the dissemination in time or space components of existing multiple sclerosis diagnostic criteria.¹⁰ Specifically, in patients with brainstem or spinal cord syndromes, lesions within the symptomatic region cannot be counted for dissemination in space. The simultaneous presence of asymptomatic gadolinium-enhancing and non-enhancing lesions at any time is a criterion

Spinal cord imaging

As set out in the 2010 McDonald criteria,¹⁰ clinically silent spinal cord lesions can contribute to assessment of dissemination in space and time, and on the basis of the available evidence, the expert panel recommends use of spinal cord MRI to establish dissemination in space. At symptom onset, spinal cord imaging is recommended in patients with clinical features suggestive of spinal cord involvement to exclude alternative cord pathology (eg, compression, spinal cord tumour, neuromyelitis

Primary progressive multiple sclerosis

In all formulations of the diagnostic criteria, diagnosis of primary progressive multiple sclerosis has been separated from that of the more common relapse-onset form of the disease. Since no evidence exists that imaging features differ substantially between patients with relapse-onset multiple sclerosis and patients with primary progressive multiple sclerosis, the expert group agreed that use of similar criteria would simplify the diagnostic work-up of patients with primary progressive

Paediatric populations

The 2010 consensus was that the proposed MRI criteria¹⁰ could be used for most paediatric patients with multiple sclerosis. An alert specified that use of the 2010 McDonald criteria for multiple sclerosis at baseline was not applicable for children with encephalopathy and multifocal neurological deficits meeting criteria for acute disseminated encephalomyelitis.¹⁰ Such children have many lesions, some of which might enhance; however, when defined with international consensus criteria for acute

Non-white populations

The 2010 McDonald criteria have been developed and tested mostly in adult white European and North American populations, and their formulation states that validation is needed in Asian and Latin American populations.¹⁰ Between 2011 and 2015, performance of MRI diagnostic criteria has been tested in Korean,²⁸ Taiwanese,²⁹ Argentinean (including a sub-analysis applied only to non-European descendants—ie, mestizos, natives, and zambos),³⁰ and Russian³¹ patients with clinically isolated syndromes,

Radiologically isolated syndromes

Availability of MRI assessment for indications unrelated to multiple sclerosis has led to increased recognition of individuals with incidental brain lesions consistent with multiple sclerosis. Criteria have been proposed to identify imaging features that are suggestive of a clinically asymptomatic demyelinating disorder, including fulfilment of at least three of four Barkhof criteria⁴ for dissemination in space.64, 65 The 2010 McDonald criteria¹⁰ concluded that “a firm diagnosis of [multiple

Differential diagnosis

Exclusion of alternative diagnoses that can mimic multiple sclerosis, including atypical demyelination and neuromyelitis optica, is imperative when applying the 2010 McDonald criteria.¹⁰ From an imaging perspective, many inherited and acquired disorders could manifest with evidence of dissemination in time or space, or both, and these disorders should be included in the differential diagnosis of multiple-sclerosis-like lesions. A timely recognition of imaging red flags in the work-up of

High-field scanners (3·0 T)

Compared with 1·5 T scanners, use of high-field-strength scanners (3·0 T) enables detection of a significantly higher number of lesions in patients with clinically isolated syndromes,76, 77 with improved recognition of lesions involving the cortical,⁷⁸ infratentorial, and periventricular regions.⁷⁶ Comparison of MRI criteria performance at 1·5 T versus 3·0 T in 40 patients with clinically isolated syndromes showed that one additional patient was diagnosed with dissemination in space at high

Future perspectives

The expert panel noted that some promising measures deserve further investigation before being moved (or not) to diagnostic criteria in the future.

For identification of the central vein, sequences capable of showing these features on 3·0 T and 1·5 T scanners need to be standardised, and standardised definitions need to be created for identification of central vessels. So far, central vessels have been identified if they could be visualised in at least two perpendicular planes, appeared linear

Conclusions

Assessment of MRI scans should be done in the appropriate clinical context. The premise of these guidelines and criteria is that we assume a basic knowledge of what constitutes a lesion. The largest linear measurement for lesion definition should be 3 mm or more in at least one plane. Therefore, lesion identification should be done by trained, expert personnel. Image quality should be of a high standard. A conservative approach to identification of lesions should be used.

In the diagnostic

Search strategy and selection criteria

References for this Review were identified through searches of PubMed with the search terms “clinically isolated syndrome”, “multiple sclerosis”, “McDonald criteria”, “diagnosis”, “differential diagnosis”, “cortical lesions”, “white matter”, “lesions”, “cortical lesions”, “brain”, “spinal cord”, “MRI”, “optic nerve”, “disease dissemination in space”, “disease dissemination in time”, “radiologically isolated syndromes”, “pediatric MS”, “T1-hypointense lesions”, “symptomatic lesions”, “primary

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Estos cambios han motivado la presente actualización del consenso mediante metodología Delphi, con el objetivo de reflejar el nuevo paradigma de manejo del paciente con EM basándose en la evidencia científica y la experiencia clínica de los participantes.
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The last consensus statement of the Spanish Society of Neurology's Demyelinating Diseases Study Group on the treatment of multiple sclerosis (MS) was issued in 2016. Although many of the positions taken remain valid, there have been significant changes in the management and treatment of MS, both due to the approval of new drugs with different action mechanisms and due to the evolution of previously fixed concepts. This has enabled new approaches to specific situations such as pregnancy and vaccination, and the inclusion of new variables in clinical decision-making, such as the early use of high-efficacy disease-modifying therapies (DMT), consideration of the patient's perspective, and the use of such novel technologies as remote monitoring.
In the light of these changes, this updated consensus statement, developed according to the Delphi method, seeks to reflect the new paradigm in the management of patients with MS, based on the available scientific evidence and the clinical expertise of the participants.
The most significant recommendations are that immunomodulatory DMT be started in patients with radiologically isolated syndrome with persistent radiological activity, that patient perspectives be considered, and that the term “lines of therapy” no longer be used in the classification of DMTs (> 90% consensus). Following diagnosis of MS, the first DMT should be selected according to the presence/absence of factors of poor prognosis (whether epidemiological, clinical, radiological, or biomarkers) for the occurrence of new relapses or progression of disability; high-efficacy DMTs may be considered from disease onset.
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Clinical magnetic resonance images (MRIs) lack a standard intensity scale due to differences in scanner hardware and the pulse sequences used to acquire the images. When MRIs are used for quantification, as in the evaluation of white matter lesions (WMLs) in multiple sclerosis, this lack of intensity standardization becomes a critical problem affecting both the staging and tracking of the disease and its treatment. This paper presents a study of harmonization on WML segmentation consistency, which is evaluated using an object detection classification scheme that incorporates manual delineations from both the original and harmonized MRIs. A cohort of ten people scanned on two different imaging platforms was studied. An expert rater, blinded to the image source, manually delineated WMLs on images from both scanners before and after harmonization. It was found that there is closer agreement in both global and per-lesion WML volume and spatial distribution after harmonization, demonstrating the importance of image harmonization prior to the creation of manual delineations. These results could lead to better truth models in both the development and evaluation of automated lesion segmentation algorithms.
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We examined the clinical course, neuroimaging, cerebrospinal fluid (CSF), treatment and outcomes of patients with recurrent tumefactive demyelinating lesions (TDLs).
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We identified 18 cases (11F, 7 M). The median age at onset of the index TDL was 37 years (range 12–72) and most were solitary lesions 72 % (13/18). CSF-restricted oligoclonal bands (OCBs) were detected in 25 % (4/16). Only one of those tested (n = 13) was positive for AQP4-IgG. A moderate-to-marked treatment response (high dose corticosteroid with or without additional plasmapheresis, IVIg or disease modifying therapies) was evident in 89 % of treated patients. Median EDSS at the median follow-up of 36 months (range 6–144) was 2 (range 1–10). Most remained ambulatory (EDSS < 4 in 13/18), but 1 patient died.
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Intracranial volume (ICV) represents the maximal brain volume for an individual, attained prior to late adolescence and remaining constant throughout life after. Thus, ICV serves as a surrogate marker for brain growth integrity. To assess the potential impact of adult-onset multiple sclerosis (MS) and its preceding prodromal subclinical changes on ICV in a large cohort of monozygotic twins clinically discordant for MS.
FSL software was used to derive ICV estimates from 3D-T1-weighted-3 T-MRI images by using an atlas scaling factor method. ICV were compared between clinically affected and healthy co-twins. All twins were compared to a large healthy reference cohort using standardized ICV z-scores. Mixed models assessed the impact of age at MS diagnosis on ICV.
54 twin-pairs (108 individuals/80female/42.45 ± 11.98 years), 731 individuals (375 non-twins, 109/69 monozygotic/dizygotic twin-pairs; 398female/29.18 ± 0.13 years) and 35 healthy local individuals (20male/31.34 ± 1.53 years). In 45/54 (83 %) twin-pairs, both clinically affected and healthy co-twins showed negative ICV z-scores, i.e., ICVs lower than the average of the healthy reference cohort (M = -1.53 ± 0.11, P<10⁻⁵). Younger age at MS diagnosis was strongly associated with lower ICVs (t = 3.76, P = 0.0003). Stratification of twin-pairs by age at MS diagnosis of the affected co-twin (≤30 versus > 30 years) yielded lower ICVs in those twin pairs with younger age at diagnosis (P = 0.01). Comparison within individual twin-pairs identified lower ICVs in the MS-affected co-twins with younger age at diagnosis compared to their corresponding healthy co-twins (P = 0.003).
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^†: MAGNIMS Steering Committee members are listed at the end of the paper

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ReviewMRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines

Summary

Introduction

Section snippets

Methods

Dissemination in space

Dissemination in time

Symptomatic lesions

Spinal cord imaging

Primary progressive multiple sclerosis

Paediatric populations

Non-white populations

Radiologically isolated syndromes

Differential diagnosis

High-field scanners (3·0 T)

Future perspectives

Conclusions

Search strategy and selection criteria

Lancet Neurol

Pediatr Neurol

Lancet Neurol

J Neurol Sci

Mult Scler

Lancet Neurol

Lancet Neurol

Lancet Neurol

Handb Clin Neurol

Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis

Ann Neurol

MRI in the diagnosis of MS: a prospective study with comparison of clinical evaluation, evoked potentials, oligoclonal banding, and CT

Neurology

Criteria for an increased specificity of MRI interpretation in elderly subjects with suspected multiple sclerosis

Neurology

Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis

Brain

Modification of MRI criteria for multiple sclerosis in patients with clinically isolated syndromes

J Neurol Neurosurg Psychiatry

A single, early magnetic resonance imaging study in the diagnosis of multiple sclerosis

Arch Neurol

Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”

Ann Neurol

MRI criteria for MS in patients with clinically isolated syndromes

Neurology

Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria

Ann Neurol

Evidence-based guidelines: MAGNIMS consensus guidelines on the use of MRI in multiple sclerosis-clinical implementation in the diagnostic process

Nat Rev Neurol

Factors that determine disease course: the symptomatic lesion matters. 1000 CIS subgroup analysis

Mult Scler

Criteria improving multiple sclerosis diagnosis at the first MRI

J Neurol

Should we include lesions in the symptomatic site in dissemination in space in patients with clinically isolated syndromes?

Mult Scler

Application and a proposed modification of the 2010 McDonald criteria for the diagnosis of multiple sclerosis in a Canadian cohort of patients with clinically isolated syndromes

Mult Scler

Spinal cord lesions in patients with clinically isolated syndrome: a powerful tool in diagnosis and prognosis

Neurology

Spinal cord abnormalities in recently diagnosed MS patients: added value of spinal MRI examination

Neurology

Biplanar MRI for the assessment of the spinal cord in multiple sclerosis

Mult Scler

Optimized T1-MPRAGE sequence for better visualization of spinal cord multiple sclerosis lesions at 3T

AJNR Am J Neuroradiol

A proposed modification to the McDonald 2010 criteria for the diagnosis of primary progressive multiple sclerosis

Mult Scler

2010 McDonald criteria in a pediatric cohort: is positivity at onset associated with a more aggressive multiple sclerosis course?

Mult Scler

Pediatric onset multiple sclerosis: McDonald criteria 2010 and the contribution of spinal cord MRI

Mult Scler

2010 McDonald criteria for diagnosing pediatric multiple sclerosis

Ann Neurol

Risk of multiple sclerosis after a first demyelinating syndrome in an Australian Paediatric cohort: clinical, radiological features and application of the McDonald 2010 MRI criteria

Mult Scler

Evaluation of the 2010 McDonald multiple sclerosis criteria in children with a clinically isolated syndrome

Mult Scler

Evaluation of McDonald MRI criteria for dissemination in space in Korean patients with clinically isolated syndromes

Mult Scler

Application of the McDonald 2010 criteria for the diagnosis of multiple sclerosis in an Argentinean cohort of patients with clinically isolated syndromes

Mult Scler

Revised McDonald criteria for multiple sclerosis diagnostics in central Russia: sensitivity and specificity

Review
MRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines