Skip to main content
Erschienen in: Clinical Neuroradiology 3/2015

01.09.2015 | Original Article

Diagnostic Efficacy of Conventional MRI Pulse Sequences in the Detection of Lesions Causing Internuclear Ophthalmoplegia in Multiple Sclerosis Patients

verfasst von: J. P. McNulty, R. Lonergan, P. C. Brennan, M. G. Evanoff, R. O’Laoide, J. T. Ryan, N. Tubridy

Erschienen in: Clinical Neuroradiology | Ausgabe 3/2015

Einloggen, um Zugang zu erhalten

Abstract

Purpose

The purpose of this study was to investigate the diagnostic efficacy of a range of conventional magnetic resonance imaging (MRI) pulse sequences in the identification of internuclear ophthalmoplegia (INO) caused by medial longitudinal fasciculus (MLF) lesions in multiple sclerosis patients using a receiver-operating characteristic (ROC) methodology.

Methods

A total of 15 clinically confirmed INO and 15 control subjects underwent conventional MRI at 1.5 T consisting of T2-weighted, proton density (PD)-weighted, and fluid-attenuated inversion recovery (FLAIR) sequences, following full institutional approval. A free-response, multiple-reader multiple-case design ROC study was used to evaluate the diagnostic efficacy of each sequence. All imaging sequences were evaluated by 10 board-certified neuroradiologists. Area under the curve (AUC), sensitivity, and specificity were analysed statistically for all three pulse sequences using repeated-measures analyses of variance and post-test analysis using Bonferroni’s multiple comparison test of differences.

Results

No significant AUC differences were found between the three sequences (p = 0.0697), with T2 recording the highest AUC (0.8346). Sensitivity differences between PD (0.7927) and FLAIR (0.6329) were significant (p < 0.05). Non-significant differences were also evident between T2 and FLAIR (p = 0.0511). The specificity analysis revealed an overall difference (p = 0.0005), with specific inter-sequence differences shown between T2 and PD (p < 0.05) and PD and FLAIR (p < 0.001) with the PD values being lower than those provided with the other two sequences.

Conclusion

T2-weighted axial imaging through the MLF region resulted in the greatest overall diagnostic efficacy when viewing a combination of mean AUC, sensitivity, and specificity, in terms of the identification of INO-causing lesions.
Literatur
1.
Zurück zum Zitat Matthews B. Symptoms and signs of multiple sclerosis. In: Compston A, Ebers G, Lassmann H, McDonald I, Matthews B, Wekerle H, editors. McAlpine’s multiple sclerosis. 3rd ed. London: Churchill Liveingstone; 1998. pp. 157–62. Matthews B. Symptoms and signs of multiple sclerosis. In: Compston A, Ebers G, Lassmann H, McDonald I, Matthews B, Wekerle H, editors. McAlpine’s multiple sclerosis. 3rd ed. London: Churchill Liveingstone; 1998. pp. 157–62.
2.
Zurück zum Zitat Poser CM, Brinar VV. Diagnostic criteria for multiple sclerosis. Clin Neurol Neurosurg. 2001;103:1–11.CrossRefPubMed Poser CM, Brinar VV. Diagnostic criteria for multiple sclerosis. Clin Neurol Neurosurg. 2001;103:1–11.CrossRefPubMed
3.
Zurück zum Zitat Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.PubMedCentralCrossRefPubMed Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.PubMedCentralCrossRefPubMed
4.
Zurück zum Zitat Frohman EM, Goodin DS, Calabresi PA, Corboy JR, Coyle PK, Filippi M, et al. The utility of MRI in suspected MS: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology. 2003;61:602–11.CrossRefPubMed Frohman EM, Goodin DS, Calabresi PA, Corboy JR, Coyle PK, Filippi M, et al. The utility of MRI in suspected MS: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology. 2003;61:602–11.CrossRefPubMed
6.
Zurück zum Zitat Comi G, Filippi M, Barkhof F, Durelli L, Edan G, Fernández O, et al. Effect of early interferon treatment on conversion to definite multiple sclerosis. Lancet. 2001;357:1576–82.CrossRefPubMed Comi G, Filippi M, Barkhof F, Durelli L, Edan G, Fernández O, et al. Effect of early interferon treatment on conversion to definite multiple sclerosis. Lancet. 2001;357:1576–82.CrossRefPubMed
7.
Zurück zum Zitat Miller DH, Grossmann RI, Reingold SC, McFarland HF. The role of magnetic resonance techniques in understanding and managing multiple sclerosis. Brain. 1998;121:3–24.CrossRefPubMed Miller DH, Grossmann RI, Reingold SC, McFarland HF. The role of magnetic resonance techniques in understanding and managing multiple sclerosis. Brain. 1998;121:3–24.CrossRefPubMed
8.
Zurück zum Zitat Pelidou SH, Giannopoulos S, Tzavidid S, Lagos G, Kyritsis AP. Multiple sclerosis presented as clinically isolated syndrome: the need for early diagnosis and treatment. Ther Clin Risk Manag. 2008;4(3):627–30.PubMedCentralPubMed Pelidou SH, Giannopoulos S, Tzavidid S, Lagos G, Kyritsis AP. Multiple sclerosis presented as clinically isolated syndrome: the need for early diagnosis and treatment. Ther Clin Risk Manag. 2008;4(3):627–30.PubMedCentralPubMed
9.
Zurück zum Zitat Frohman EM, Zhang H, Kramer PD, Fleckenstein J, Hawker K, Racke MK, et al. MRI characteristics of the MLF in MS patients with chronic internuclear ophthalmoparesis. Neurology. 2001;57:762–8.CrossRefPubMed Frohman EM, Zhang H, Kramer PD, Fleckenstein J, Hawker K, Racke MK, et al. MRI characteristics of the MLF in MS patients with chronic internuclear ophthalmoparesis. Neurology. 2001;57:762–8.CrossRefPubMed
10.
Zurück zum Zitat Miller D, Barkhof F, Montalban X, Thompson A, Filippi M. Clinically isolated syndrome suggestive of multiple sclerosis, part I: natural history, pathogenesis, diagnosis, and prognosis. Lancet Neurol. 2005;4:281–8.CrossRefPubMed Miller D, Barkhof F, Montalban X, Thompson A, Filippi M. Clinically isolated syndrome suggestive of multiple sclerosis, part I: natural history, pathogenesis, diagnosis, and prognosis. Lancet Neurol. 2005;4:281–8.CrossRefPubMed
11.
Zurück zum Zitat Muri RM, Meienberg O. The clinical spectrum of internuclear ophthalmoplegia in multiple sclerosis. Arch Neurol. 1985;42:851–5.CrossRefPubMed Muri RM, Meienberg O. The clinical spectrum of internuclear ophthalmoplegia in multiple sclerosis. Arch Neurol. 1985;42:851–5.CrossRefPubMed
12.
Zurück zum Zitat Savino PJ. Neuro-ophthalmology. In: Tasman W, Jaeger EA, editors. The Wills Eye Hospital atlas of clinical ophthalmology. 1st ed. Philadelphia: Lippincott-Raven; 1996. pp. 310–1. Savino PJ. Neuro-ophthalmology. In: Tasman W, Jaeger EA, editors. The Wills Eye Hospital atlas of clinical ophthalmology. 1st ed. Philadelphia: Lippincott-Raven; 1996. pp. 310–1.
13.
Zurück zum Zitat Lavin PJM, Donahue SP. Disorders of supranuclear control of ocular motility. In: Yanoff M, Duker JS, editors. Ophthalmology. 2nd ed. St. Louis: Mosby; 2004. p. 1310. Lavin PJM, Donahue SP. Disorders of supranuclear control of ocular motility. In: Yanoff M, Duker JS, editors. Ophthalmology. 2nd ed. St. Louis: Mosby; 2004. p. 1310.
14.
Zurück zum Zitat Atlas SW, Grossman RI, Savino PJ, Schatz NJ, Sergott RC, Bosley TM, et al. Internuclear ophthalmoplegia: MR-anatomic correlation. AJNR Am J Neuroradiol. 1987;8:243–7.PubMed Atlas SW, Grossman RI, Savino PJ, Schatz NJ, Sergott RC, Bosley TM, et al. Internuclear ophthalmoplegia: MR-anatomic correlation. AJNR Am J Neuroradiol. 1987;8:243–7.PubMed
15.
Zurück zum Zitat Barnes D, McDonald WI. The ocular manifestations of multiple sclerosis. 2. Abnormalities of eye movements. J Neurol Neurosurg Psychiatry. 1992;55(10):863–8.PubMedCentralCrossRefPubMed Barnes D, McDonald WI. The ocular manifestations of multiple sclerosis. 2. Abnormalities of eye movements. J Neurol Neurosurg Psychiatry. 1992;55(10):863–8.PubMedCentralCrossRefPubMed
16.
Zurück zum Zitat Marx JJ, Thoemke F, Fitzek S, Vucurevic G, Fitzek C, Mika-Gruettner A, et al. A new method to investigate brain stem structural–functional correlations using digital post-processing MRI—reliability in ischemic internuclear ophthalmology. Eur J Neurol. 2001;8:489–93.CrossRefPubMed Marx JJ, Thoemke F, Fitzek S, Vucurevic G, Fitzek C, Mika-Gruettner A, et al. A new method to investigate brain stem structural–functional correlations using digital post-processing MRI—reliability in ischemic internuclear ophthalmology. Eur J Neurol. 2001;8:489–93.CrossRefPubMed
17.
Zurück zum Zitat Flipse JP, Straathof CSM, Van der Steen J, Van Leeuwen AF, Van Doorn PA, Van der Meché, et al. Binocular saccadic eye movements in multiple sclerosis. J Neurol Sci. 1997;148:53–65. Flipse JP, Straathof CSM, Van der Steen J, Van Leeuwen AF, Van Doorn PA, Van der Meché, et al. Binocular saccadic eye movements in multiple sclerosis. J Neurol Sci. 1997;148:53–65.
18.
Zurück zum Zitat Frohman EM, Frohman TC, O’Suilleabhain P, Zhang H, Hawker K, Racke M, et al. Quantitative oculographic characterization of internuclear ophthalmoparesis in multiple sclerosis: the versional dysconjugacy index Z score. J Neurol Neurosurg Psychiatry. 2002;73:51–5.PubMedCentralCrossRefPubMed Frohman EM, Frohman TC, O’Suilleabhain P, Zhang H, Hawker K, Racke M, et al. Quantitative oculographic characterization of internuclear ophthalmoparesis in multiple sclerosis: the versional dysconjugacy index Z score. J Neurol Neurosurg Psychiatry. 2002;73:51–5.PubMedCentralCrossRefPubMed
19.
Zurück zum Zitat Ventre J, Vighetto A, Bailly G, Prablanc C. Saccade metrics in multiple sclerosis: versional velocity disconjugacy as the best clue? J Neurol Sci. 1991;102:144–9.CrossRefPubMed Ventre J, Vighetto A, Bailly G, Prablanc C. Saccade metrics in multiple sclerosis: versional velocity disconjugacy as the best clue? J Neurol Sci. 1991;102:144–9.CrossRefPubMed
20.
Zurück zum Zitat Alexander JA, Castillo M, Hoffman JC. Magnetic resonance findings in a patient with internuclear ophthalmoplegia. J Clin Neuroophthalmol. 1991;11:58–61. Alexander JA, Castillo M, Hoffman JC. Magnetic resonance findings in a patient with internuclear ophthalmoplegia. J Clin Neuroophthalmol. 1991;11:58–61.
21.
Zurück zum Zitat Balanos I, Lozano D, Cantú C. Internuclear ophthalmoplegia: causes and long-term follow-up in 65 patients. Acta Neurol Scand. 2004;110:161–5.CrossRef Balanos I, Lozano D, Cantú C. Internuclear ophthalmoplegia: causes and long-term follow-up in 65 patients. Acta Neurol Scand. 2004;110:161–5.CrossRef
22.
Zurück zum Zitat De Seze J, Lucas C, Leclerc X, Sahli A, Vermersch P, Leys D. One-and-a-half syndrome in pontine infarcts: MRI correlates. Neuroradiology. 1999;41:666–9.CrossRefPubMed De Seze J, Lucas C, Leclerc X, Sahli A, Vermersch P, Leys D. One-and-a-half syndrome in pontine infarcts: MRI correlates. Neuroradiology. 1999;41:666–9.CrossRefPubMed
23.
Zurück zum Zitat Eggenberger E, Golnik K, Lee A, Santos R, Suntay A, Satana B, et al. Prognosis of ischaemic internuclear ophthalmoplegia. Ophthalmology. 2002;109:1676–8.CrossRefPubMed Eggenberger E, Golnik K, Lee A, Santos R, Suntay A, Satana B, et al. Prognosis of ischaemic internuclear ophthalmoplegia. Ophthalmology. 2002;109:1676–8.CrossRefPubMed
24.
Zurück zum Zitat Korteweg T, Tintoré M, Uitdehaag B, Rovira A, Frederiksen J, Miller D, et al. MRI criteria for dissemination in space in patients with clinically isolated syndromes: a multicentre follow-up study. Lancet Neurol. 2006;5:221–7.CrossRefPubMed Korteweg T, Tintoré M, Uitdehaag B, Rovira A, Frederiksen J, Miller D, et al. MRI criteria for dissemination in space in patients with clinically isolated syndromes: a multicentre follow-up study. Lancet Neurol. 2006;5:221–7.CrossRefPubMed
25.
Zurück zum Zitat Simon JH, Li D, Traboulsee A, Coyle PK, Arnold DL, Barkhof F, et al. Standardized MR imaging protocol for multiple sclerosis: consortium of MS centers consensus guidelines. AJNR Am J Neuroradiol. 2006;27:455–61.PubMed Simon JH, Li D, Traboulsee A, Coyle PK, Arnold DL, Barkhof F, et al. Standardized MR imaging protocol for multiple sclerosis: consortium of MS centers consensus guidelines. AJNR Am J Neuroradiol. 2006;27:455–61.PubMed
27.
Zurück zum Zitat Filippi M, Yousry T, Baratti C, Horsfield MA, Mammi S, Becker C, et al. Quantitative assessment of MRI lesion load in multiple sclerosis. A comparison of conventional spin-echo with fast fluid attenuation inversion recovery. Brain. 1996;119:1349–55.CrossRefPubMed Filippi M, Yousry T, Baratti C, Horsfield MA, Mammi S, Becker C, et al. Quantitative assessment of MRI lesion load in multiple sclerosis. A comparison of conventional spin-echo with fast fluid attenuation inversion recovery. Brain. 1996;119:1349–55.CrossRefPubMed
28.
Zurück zum Zitat Yousry TA, Filippi M, Becker C, Horsfield MA, Voltz R. Comparison of MR pulse sequences in the detection of multiple sclerosis lesions. AJNR Am J Neuroradiol. 1997;18:959–63.PubMed Yousry TA, Filippi M, Becker C, Horsfield MA, Voltz R. Comparison of MR pulse sequences in the detection of multiple sclerosis lesions. AJNR Am J Neuroradiol. 1997;18:959–63.PubMed
29.
Zurück zum Zitat Pikus L, Woo JH, Wolf RL, Herskovits EH, Moonis G, Jawad AF, et al. Artificial multiple sclerosis lesions on simulated FLAIR brain MR images: echo time and observer performance in detection. Radiology. 2006;239:238–45.CrossRefPubMed Pikus L, Woo JH, Wolf RL, Herskovits EH, Moonis G, Jawad AF, et al. Artificial multiple sclerosis lesions on simulated FLAIR brain MR images: echo time and observer performance in detection. Radiology. 2006;239:238–45.CrossRefPubMed
30.
Zurück zum Zitat Woo JH, Henry LP, Krejza J, Melhem ER. Detection of simulated multiple sclerosis lesions on T2-weighted and FLAIR images of the brain: observer performance. Radiology. 2006;241:206–12.CrossRefPubMed Woo JH, Henry LP, Krejza J, Melhem ER. Detection of simulated multiple sclerosis lesions on T2-weighted and FLAIR images of the brain: observer performance. Radiology. 2006;241:206–12.CrossRefPubMed
31.
Zurück zum Zitat Wattjes MP, Lutterbey GG, Harzheim M, Gieseke J, Traber F, Klotz L, et al. Imaging of inflammatory lesions at 3.0 Tesla in patients with clinically isolated syndromes suggestive of multiple sclerosis: a comparison of fluid-attenuated inversion recovery with T2 turbo spin-echo. Eur Radiol. 2006;16:1494–500.CrossRefPubMed Wattjes MP, Lutterbey GG, Harzheim M, Gieseke J, Traber F, Klotz L, et al. Imaging of inflammatory lesions at 3.0 Tesla in patients with clinically isolated syndromes suggestive of multiple sclerosis: a comparison of fluid-attenuated inversion recovery with T2 turbo spin-echo. Eur Radiol. 2006;16:1494–500.CrossRefPubMed
32.
Zurück zum Zitat Metz CE. Receiver operating characteristic analysis: a tool for the quantitative evaluation of observer performance and imaging systems. J Am Coll Radiol. 2006;3:413–22.CrossRefPubMed Metz CE. Receiver operating characteristic analysis: a tool for the quantitative evaluation of observer performance and imaging systems. J Am Coll Radiol. 2006;3:413–22.CrossRefPubMed
33.
Zurück zum Zitat Stevenson VL, Parker GJM, Barker GJ, Birnie K, Tofts PS, Miller DH, et al. Variations in T1 and T2 relaxation times of normal appearing white matter and lesions in multiple sclerosis. J Neurol Sci. 2000;178:81–7.CrossRefPubMed Stevenson VL, Parker GJM, Barker GJ, Birnie K, Tofts PS, Miller DH, et al. Variations in T1 and T2 relaxation times of normal appearing white matter and lesions in multiple sclerosis. J Neurol Sci. 2000;178:81–7.CrossRefPubMed
34.
Zurück zum Zitat Simon B, Schmidt S, Lukas C, Gieseke J, Traber F, Knol DL, et al. Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla. Eur Radiol. 2010;20:1675–83.PubMedCentralCrossRefPubMed Simon B, Schmidt S, Lukas C, Gieseke J, Traber F, Knol DL, et al. Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla. Eur Radiol. 2010;20:1675–83.PubMedCentralCrossRefPubMed
Metadaten
Titel
Diagnostic Efficacy of Conventional MRI Pulse Sequences in the Detection of Lesions Causing Internuclear Ophthalmoplegia in Multiple Sclerosis Patients
verfasst von
J. P. McNulty
R. Lonergan
P. C. Brennan
M. G. Evanoff
R. O’Laoide
J. T. Ryan
N. Tubridy
Publikationsdatum
01.09.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Neuroradiology / Ausgabe 3/2015
Print ISSN: 1869-1439
Elektronische ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-014-0295-5

Weitere Artikel der Ausgabe 3/2015

Clinical Neuroradiology 3/2015 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.