DOI: 10.14704/nq.2018.16.3.1179

Efficiency of Double Inversion Recovery (DIR) Sequence in the Evaluation of Supratentorial Cortical Lesions in Multiple Sclerosis

Gulhan Ertan, Ozge Arici, Sila Ulus, Baris Metin


The aim of this study is to investigate if the three–dimensional (3D) double inversion recovery (DIR) sequence is superior compared to the 3D fluid–attenuated inversion–recovery (FLAIR) sequence in detecting intracortical, mixed, juxtacortical (JX), and deep grey matter (GM) lesions in multiple sclerosis (MS) patients. The correlation between intracortical lesion load and disability status was also investigated. Magnetic resonance imaging examinations of 24 patients (9 males, 15 females; mean age 34.4±12.0 (16-69) were retrospectively evaluated from our database. Lesions were counted and classified according to anatomic regions as intracortical, mixed, JX, and deep GM on the 3D DIR and FLAIR sequences. The incidence of lesions on the two sequences were identified and compared. The relationship between the number of lesions and type of MS, patient age, gender, duration of the disease, disability, the mean number of attacks per year and Expanded Disability Status Scale (EDSS) score was also investigated. More lesions were detected by the DIR sequence compared to the FLAIR sequence in all regions except for thalamus (11/12). The lesion detection superiority of DIR was statistically significant for intracortical lesions (p<0.001) and GM lesions (intracortical +mixed) (p<0.001). Lesion load of the JX area in the DIR sequence decreased as the disease duration (r=-0.444; p=0.030) and age (r=-0.473; p=0.020) increased. JX lesion load in the DIR sequence decreased as the number of attacks increased (r=-0.602; p=0.002). More mixed lesion load on the DIR sequence were found in cerebral atrophy group than in no cerebral atrophy group (p=0.026). EDSS score increased as the disease duration and number of attacks increased (p=0.003, p<0.001). There was no correlation between lesion location and EDSS score. The DIR sequence is superior to the FLAIR sequence in the detection of intracortical and GM lesions. Also, the mixed lesion load on the DIR sequence is correlated with cerebral atrophy.


Multiple sclerosis; magnetic resonance imaging (MRI); Double inversion recovery (DIR) sequence; Fluid–attenuated inversion–recovery (FLAIR) sequence; cortical lesion.

Full Text:



Bakshi R, Ariyaratana S, Benedict RH, Jacobs L. Fluid-attenuated inversion recovery magnetic resonance imaging detects cortical and juxtacortical multiple sclerosis lesions. Archives of Neurology 2001; 58(5):742-48.

Bedell BJ, Narayana PA. Implementation and evaluation of a new pulse sequence for rapid acquisition of double inversion recovery images for simultaneous suppression of white matter and CSF. Journal of Magnetic Resonance Imaging 1998; 8(3):544-47.

Calabrese M, De Stefano N, Atzori M, Bernardi V, Mattisi I, Barachino L, Morra A, Rinaldi L, Romualdi C, Perini P, Battistin L, Gallo P. Detection of cortical inflammatory lesions by double inversion recovery magnetic resonance imaging in patients with multiple sclerosis. Archives of Neurology 2007; 64(10): 1416–22.

Calabrese M, Gallo P. Magnetic resonance evidence of cortical onset of multiple sclerosis. Multiple Sclerosis 2009; 15(8): 933–41.

Calabrese M, Rocca MA, Atzori M, Mattisi I, Favaretto A, Perini P, Gallo P, Filippi M. A 3‐year magnetic resonance imaging study of cortical lesions in relapse‐onset multiple sclerosis. Annals of Neurology 2010; 67(3):376-83.

Fisher E, Lee JC, Nakamura K, Rudick RA. Gray matter atrophy in multiple sclerosis: a longitudinal study. Annals of Neurology 2008; 64(3): 255–65.

Geurts JJ, Roosendaal SD, Calabrese M, Ciccarelli O, Agosta F, Chard DT, Gass A, Huerga E, Moraal B, Pareto D, Rocca MA. Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI. Neurology 2011; 76(5):418-24.

Geurts JJG, Pouwels PJW, Uitdehaag BMJ, Polman CH, Barkhof F, Castelijns JA. Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. Radiology 2005; 236(1):254–60.

Haider L, Simeonidou C, Steinberger G, Hametner S, Grigoriadis N, Deretzi G, Kovacs GG, Kutzelnigg A, Lassmann H, Frischer JM. Multiple sclerosis deep grey matter: the relation between demyelination, neurodegeneration, inflammation and iron. Journal of Neurology, Neurosurgery & Psychiatry 2014; 85(12): 1386-95.

Harrison DM, Roy S, Oh J, Izbudak I, Pham D, Courtney S, Caffo B, Jones CK, Van Zijl P, Calabresi PA. Association of cortical lesion burden on 7-T magnetic resonance imaging with cognition and disability in multiple sclerosis. JAMA Neurology 2015; 72(9):1004-12.

Honce JM. Gray matter pathology in MS: neuroimaging and clinical correlations. Multiple Sclerosis İnternational 2013; 627870.

Kolber P, Montag S, Fleischer V, Luessi F, Wilting J, Gawehn J, Gröger A, Zipp F. Identification of cortical lesions using DIR and FLAIR in early stages of multiple sclerosis. Journal of Neurology 2015; 262(6):1473-82.

Lazeron RH, Langdon DW, Filippi M, van Waesberghe JH, Stevenson VL, Boringa JB, Origgi D, Thompson AJ, Falautano M, Polman C, Barkhof F. Neuropsychological impairment in multiple sclerosis patients: the role of (juxta) cortical lesion on FLAIR. Multiple Sclerosis Journal 2000; 6(4):280-85.

Mainero C, Louapre C, Govindarajan ST, Giannì C, Nielsen AS, Cohen-Adad J, Sloane J, Kinkel RP. A gradient in cortical pathology in multiple sclerosis by in vivo quantitative 7 T imaging. Brain 2015; 138(4):932-45.

Moraal B, Roosendaal SD, Pouwels PJ, Vrenken H, Van Schijndel RA, Meier DS, Guttmann CR, Geurts JJ, Barkhof F. Multi-contrast, isotropic, single-slab 3D MR imaging in multiple sclerosis. European Radiology 2008; 18(10):2311-20.

Moriarty DM, Blackshaw AJ, Talbot PR, Griffiths HL, Snowden JS, Hillier VF, Capener S, Laitt RD, Jackson A. Memory dysfunction in multiple sclerosis corresponds to juxtacortical lesion load on fast fluid-attenuated inversion-recovery MR images. American Journal of Neuroradiology 1999; 20(10):1956-62.

Popescu BFG, Bunyan RF, Parisi JE, Ransohoff RM, Lucchinetti CF. A case of multiple sclerosis presenting with inflammatory cortical demyelination. Neurology 2011; 76 (20): 1705–10.

Rudick RA, Lee JC, Nakamura K, Fisher E. Gray matter atrophy correlates with MS disability progression measured with MSFC but not EDSS. Journal of the Neurological Sciences 2009; 282(1):106-11.

Seewann A, Kooi E-J, Roosendaal SD, Roosendaal SD, Pouwels PJ, Wattjes MP, van der Valk P, Barkhof F, Polman CH, Geurts JJ. Postmortem verification of MS cortical lesion detection with 3D DIR. Neurology 2012; 78(5): 302-08.

Seewann A, Vrenken H, Kooi EJ, van der Valk P, Knol DL, Polman CH, Pouwels PJ, Barkhof F, Geurts JJ. Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis. Multiple Sclerosis Journal 2011; 17(10):1202-10.

Sethi V, Muhlert N, Ron M, Golay X, Wheeler-Kingshott CA, Miller DH, Chard DT, Yousry TA. MS cortical lesions on DIR: not quite what they seem? PLoS One 2013; 8(11): e78879.

Tan I, Pouwels P, van Schijndel R, Adèr H, Manoliu R, Barkhof F. Isotropic 3D fast FLAIR imaging of the brain in multiple sclerosis patients: initial experience. European Radiology 2002; 12(3):559-67.

Tubridy N, Barker GJ, Macmanus DG, Moseley IF, Miller DH. Three-dimensional fast fluid attenuated inversion recovery (3D fast FLAIR): a new MRI sequence which increases the detectable cerebral lesion load in multiple sclerosis. The British Journal of Radiology 1998; 71(848):840-45.

Vural G, Keklikoğlu HD, Temel Ş, Deniz O, Ercan K. Comparison of double inversion recovery and conventional magnetic resonance brain imaging in patients with multiple sclerosis and relations with disease disability. The Neuroradiology Journal 2013; 26(2):133-42.

Wattjes MP, Lutterbey GG, Gieseke J, Träber F, Klotz L, Schmidt S, Schild HH. Double inversion recovery brain imaging at 3T: diagnostic value in the detection of multiple sclerosis lesions. American Journal of Neuroradiology 2007;28(1):54-59.

Supporting Agencies

| NeuroScience + QuantumPhysics> NeuroQuantology :: Copyright 2001-2019