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Published in: Journal of Neurology 10/2014

01-10-2014 | Original Communication

Gadolinium enhancement patterns of tumefactive demyelinating lesions: correlations with brain biopsy findings and pathophysiology

Authors: Masaki Kobayashi, Yuko Shimizu, Noriyuki Shibata, Shinichiro Uchiyama

Published in: Journal of Neurology | Issue 10/2014

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Abstract

Tumefactive demyelinating lesions (TDLs) can mimic brain tumors on radiological images. TDLs are often referred to as tumefactive multiple sclerosis (TMS), but the heterogeneous nature and monophasic course of TDLs do not fulfill clinical and magnetic resonance imaging (MRI) criteria for multiple sclerosis. Redefining TDLs, TMS and other inflammatory brain lesions is essential for the accurate clinical diagnosis of extensive demyelinating brain lesions. We retrospectively analyzed MRI from nine TDL cases that underwent brain biopsy. Patterns of gadolinium enhancement on MRI were categorized as homogenous, inhomogeneous, patchy and diffuse, open ring or irregular rim, and were compared with pathological hallmarks including demyelination, central necrosis, macrophage infiltration, angiogenesis and perivascular lymphocytic cuffing. All cases had coexistence of demyelinating features and axonal loss. Open-ring and irregular rim patterns of gadolinium enhancement were associated with macrophage infiltrations and angiogenesis at the inflammatory border. An inhomogeneous pattern of gadolinium enhancement was associated with perivascular lymphocytic cuffing. Central necrosis was seen in cases of severe multiple sclerosis and hemorrhagic leukoencephalopathy. These results suggest that the radiological features of TDLs may be related to different pathological processes, and indicate that MRI may be useful in understanding their pathophysiology. Further investigation is needed to determine the precise disease entity of these inflammatory demyelinating brain lesions.
Literature
1.
go back to reference Lucchinetti CF, Gavrilova RH, Metz I et al (2008) Clinical and radiographic spectrum of pathologically confirmed tumefactive multiple sclerosis. Brain 131:1759–1775PubMedCentralCrossRefPubMed Lucchinetti CF, Gavrilova RH, Metz I et al (2008) Clinical and radiographic spectrum of pathologically confirmed tumefactive multiple sclerosis. Brain 131:1759–1775PubMedCentralCrossRefPubMed
2.
go back to reference Siva A (2006) The spectrum of multiple sclerosis and treatment decisions. Clin Neurol Neurosurg 108:333–338CrossRefPubMed Siva A (2006) The spectrum of multiple sclerosis and treatment decisions. Clin Neurol Neurosurg 108:333–338CrossRefPubMed
3.
4.
go back to reference Kiriyama T, Kataoka H, Taoka T et al (2011) Characteristic neuroimaging in patients with tumefactive demyelinating lesions exceeding 30 mm. J Neuroimaging 21:e69–e77CrossRefPubMed Kiriyama T, Kataoka H, Taoka T et al (2011) Characteristic neuroimaging in patients with tumefactive demyelinating lesions exceeding 30 mm. J Neuroimaging 21:e69–e77CrossRefPubMed
5.
go back to reference Brück W, Bitsch A, Kolenda H et al (1997) Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 42:783–793CrossRefPubMed Brück W, Bitsch A, Kolenda H et al (1997) Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 42:783–793CrossRefPubMed
6.
go back to reference Nesbit GM, Forbes GS, Scheithauer BW et al (1991) Multiple sclerosis: histopathological and MR and/or CT correlation in 37 cases at biopsy and three cases at autopsy. Radiology 180:467–474CrossRefPubMed Nesbit GM, Forbes GS, Scheithauer BW et al (1991) Multiple sclerosis: histopathological and MR and/or CT correlation in 37 cases at biopsy and three cases at autopsy. Radiology 180:467–474CrossRefPubMed
7.
go back to reference Takahashi T, Fujihara K, Nakashima I et al (2006) Establishment of a new sensitive assay for anti-human aquaporin-4 antibody in neuromyelitis optica. Tohoku J Exp Med 210:307–313CrossRefPubMed Takahashi T, Fujihara K, Nakashima I et al (2006) Establishment of a new sensitive assay for anti-human aquaporin-4 antibody in neuromyelitis optica. Tohoku J Exp Med 210:307–313CrossRefPubMed
8.
go back to reference Noseworthy JH, Lucchinetti C, Rodrequez M et al (2000) Multiple sclerosis. N Engl J Med 343:938–952CrossRefPubMed Noseworthy JH, Lucchinetti C, Rodrequez M et al (2000) Multiple sclerosis. N Engl J Med 343:938–952CrossRefPubMed
9.
go back to reference Wingerchuk DM, Lennon VA, Lucchinetti CF et al (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6:805–815CrossRefPubMed Wingerchuk DM, Lennon VA, Lucchinetti CF et al (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6:805–815CrossRefPubMed
10.
go back to reference Wingerchuk DM, Hogancamp WF, O’Brien PC et al (1999) The clinical course of neuromyelitis optica (Devic’s syndrome). Neurology 53:1107–1114CrossRefPubMed Wingerchuk DM, Hogancamp WF, O’Brien PC et al (1999) The clinical course of neuromyelitis optica (Devic’s syndrome). Neurology 53:1107–1114CrossRefPubMed
11.
go back to reference Tintore M, Rovira A, Rio J et al (2003) New diagnostic criteria for multiple sclerosis: application in first demyelinating episode. Neurology 60:27–30CrossRefPubMed Tintore M, Rovira A, Rio J et al (2003) New diagnostic criteria for multiple sclerosis: application in first demyelinating episode. Neurology 60:27–30CrossRefPubMed
12.
go back to reference Van Waesberghe JH, Kamphorst W, De Groot CJ et al (1999) Axonal loss in MS lesions: MR insight into substrate of disability. Ann Neurol 46:1289–1293 Van Waesberghe JH, Kamphorst W, De Groot CJ et al (1999) Axonal loss in MS lesions: MR insight into substrate of disability. Ann Neurol 46:1289–1293
13.
go back to reference Given CA 2nd, Stevens CS, Lee C (2004) The MRI appearance of tumefactive demyelinating lesions. Am J Radiol 182:195–199 Given CA 2nd, Stevens CS, Lee C (2004) The MRI appearance of tumefactive demyelinating lesions. Am J Radiol 182:195–199
14.
go back to reference Walner-Blazek M, Rovira A, Filippi M et al (2013) Atypical idiopathic inflammatory demyelinating lesions: prognostic implications and relation to multiple sclerosis. J Neurol 260:2016–2022CrossRef Walner-Blazek M, Rovira A, Filippi M et al (2013) Atypical idiopathic inflammatory demyelinating lesions: prognostic implications and relation to multiple sclerosis. J Neurol 260:2016–2022CrossRef
15.
go back to reference Rossi A (2008) Imaging of acute disseminated encephalomyelitis. Neuroimaging Clin N Am 18:149–161CrossRefPubMed Rossi A (2008) Imaging of acute disseminated encephalomyelitis. Neuroimaging Clin N Am 18:149–161CrossRefPubMed
16.
go back to reference Young NP, Weinshenker BG, Parisi JE et al (2010) Perivenous demyelination: association with clinically defined acute disseminated encephalomyelitis and comparison with pathologically confirmed multiple sclerosis. Brain 133:333–348PubMedCentralCrossRefPubMed Young NP, Weinshenker BG, Parisi JE et al (2010) Perivenous demyelination: association with clinically defined acute disseminated encephalomyelitis and comparison with pathologically confirmed multiple sclerosis. Brain 133:333–348PubMedCentralCrossRefPubMed
17.
go back to reference Gibbs WN, Kreidie MA, Kim RC et al (2005) Acute hemorrhagic leukoencephalitis neuroimaging features and neuropathologic diagnosis. J Comput Assist Tomogr 29:689–693CrossRefPubMed Gibbs WN, Kreidie MA, Kim RC et al (2005) Acute hemorrhagic leukoencephalitis neuroimaging features and neuropathologic diagnosis. J Comput Assist Tomogr 29:689–693CrossRefPubMed
18.
go back to reference Xia L, Lin S, Wang ZC et al (2009) Tumefactive demyelinating lesions: nine cases and a review of the literature. Neurosurg Rev 32:171–179CrossRefPubMed Xia L, Lin S, Wang ZC et al (2009) Tumefactive demyelinating lesions: nine cases and a review of the literature. Neurosurg Rev 32:171–179CrossRefPubMed
19.
go back to reference Morrissey SP, Stodal H, Zettl U et al (1996) In vivo MRI and its histological correlations in acute adoptive transfer experimental allergic encephalomyelitis. Quantification of inflammation and edema. Brain 119:239–248CrossRefPubMed Morrissey SP, Stodal H, Zettl U et al (1996) In vivo MRI and its histological correlations in acute adoptive transfer experimental allergic encephalomyelitis. Quantification of inflammation and edema. Brain 119:239–248CrossRefPubMed
20.
go back to reference Schwartz KM, Erickson BJ, Lucchinetti CF (2006) Pattern of T2 hypointensity associated with ring-enhancing brain lesions can help to differentiate pathology. Neuroradiology 48:143–149CrossRefPubMed Schwartz KM, Erickson BJ, Lucchinetti CF (2006) Pattern of T2 hypointensity associated with ring-enhancing brain lesions can help to differentiate pathology. Neuroradiology 48:143–149CrossRefPubMed
21.
go back to reference Kirk SL, Karlik SJ (2003) VEGF and vascular changes in chronic neuroinflammation. J Autoimmune 21:353–363CrossRef Kirk SL, Karlik SJ (2003) VEGF and vascular changes in chronic neuroinflammation. J Autoimmune 21:353–363CrossRef
22.
go back to reference Su JJ, Osoegawa M, Matsuoka T et al (2006) Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings. J Neurol Sci 243:21–30CrossRefPubMed Su JJ, Osoegawa M, Matsuoka T et al (2006) Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings. J Neurol Sci 243:21–30CrossRefPubMed
23.
go back to reference Proesholdt MA, Jacobson S, Tresser N et al (2002) Vascular endothelial growth factor is expressed in multiple sclerosis plaque and can induce inflammatory lesions in experimental allergic encephalomyelitis rats. J Neuropathol Exp Neurol 61:914–925 Proesholdt MA, Jacobson S, Tresser N et al (2002) Vascular endothelial growth factor is expressed in multiple sclerosis plaque and can induce inflammatory lesions in experimental allergic encephalomyelitis rats. J Neuropathol Exp Neurol 61:914–925
24.
go back to reference Sorensen TL, Ransohoff RM, Strieter RM et al (2004) Chemokine CCL2 and chemokine receptor CCR2 in early active multiple sclerosis. Eur J Neurol 11:445–449CrossRefPubMed Sorensen TL, Ransohoff RM, Strieter RM et al (2004) Chemokine CCL2 and chemokine receptor CCR2 in early active multiple sclerosis. Eur J Neurol 11:445–449CrossRefPubMed
25.
go back to reference Kobayashi M, Ono Y, Shibata N et al (2009) Correlation between magnetic resonance imaging findings and pathological observations in tumefactive multiple sclerosis. Neuroradiol J 22:155–163CrossRefPubMed Kobayashi M, Ono Y, Shibata N et al (2009) Correlation between magnetic resonance imaging findings and pathological observations in tumefactive multiple sclerosis. Neuroradiol J 22:155–163CrossRefPubMed
Metadata
Title
Gadolinium enhancement patterns of tumefactive demyelinating lesions: correlations with brain biopsy findings and pathophysiology
Authors
Masaki Kobayashi
Yuko Shimizu
Noriyuki Shibata
Shinichiro Uchiyama
Publication date
01-10-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 10/2014
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-014-7437-1

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