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Conventional brain MRI features distinguishing limbic encephalitis from mesial temporal glioma

Neuroradiology volume 61, pages 853–860 (2019)Cite this article

Abstract

Purpose

Radiological hallmark of autoimmune limbic encephalitis (LE) is a hyperintense signal in MRI T2-weighted images of mesial temporal structures. We aimed to identify conventional magnetic resonance imaging (MRI) features that can help distinguish LE from temporal glioma.

Methods

Brain MRIs of 25 patients affected by antibody-positive autoimmune LE, 24 patients affected by temporal glioma (tumor group), and 5 negative controls were retrospectively blindly evaluated in random order.

Results

Ten brain MRIs from the LE group were correctly recognized; one additional patient with mesial temporal hyperintensity with anti-AK5 abs LE was wrongly diagnosed as having a tumor. The brain MRIs of the remaining 14 of the 25 patients with LE were judged negative or, in three cases, showed features not typical for LE. In the tumor group, all MRIs showed pathological alterations diagnosed as tumors in 22/24 cases and as LE in two (2/22, 9%). Unilateral lesions were more common in tumors than in neuroradiologically abnormal LE (96% vs. 18%, p < 0.001). T2/FLAIR hyperintensity of the parahippocampal gyrus was associated more with tumor than with LE (71% vs. 18%) (p = 0,009), as T2/FLAIR hyperintensity of extralimbic structures (p = 0.015), edema (p = 0.041), and mass effect (p = 0.015). Maintenance of gray/white matter distinction was strongly associated with LE (91% vs. 17%, p < 0.001).

Conclusion

Conventional brain MRI is a fundamental tool in the differential diagnosis between LE and glioma. Bilateral involvement and maintenance of gray/white matter distinction at the cortical/subcortical interface are highly suggestive of LE.

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References

  1. Demaerel P, Van Dessel W, Van Paesschen W et al (2011) Autoimmune-mediated encephalitis. Neuroradiology 53:837–851. https://doi.org/10.1007/s00234-010-0832-0

    Article  PubMed  Google Scholar 

  2. Graus F, Titulaer MJ, Balu R, et al (2016) A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol 15:391–404. https://doi.org/10.1016/S1474-4422(15)00401-9

  3. Vogrig A, Joubert B, Ducray F, Thomas L, Izquierdo C, Decaestecker K, Martinaud O, Gerardin E, Grand S, Honnorat J (2018) Glioblastoma as differential diagnosis of autoimmune encephalitis. J Neurol 265:669–677. https://doi.org/10.1007/s00415-018-8767-1

    Article  PubMed  Google Scholar 

  4. Hart IK, Waters C, Vincent A, Newland C, Beeson D, Pongs O, Morris C, Newsom-Davis J (1997) Autoantibodies detected to expressed K+ channels are implicated in neuromyotonia. Ann Neurol 41:238–246. https://doi.org/10.1002/ana.410410215

    Article  CAS  PubMed  Google Scholar 

  5. Saiz A, Blanco Y, Sabater L, González F, Bataller L, Casamitjana R, Ramió-Torrentà L, Graus F (2008) Spectrum of neurological syndromes associated with glutamic acid decarboxylase antibodies: diagnostic clues for this association. Brain 131:2553–2563. https://doi.org/10.1093/brain/awn183

    Article  PubMed  Google Scholar 

  6. Bernal F, Shams’ili S, Rojas I et al (2003) Anti-Tr antibodies as markers of paraneoplastic cerebellar degeneration and Hodgkin’s disease. Neurology. 60:230–234. https://doi.org/10.1212/01.WNL.0000041495.87539.98

    Article  CAS  PubMed  Google Scholar 

  7. van Sonderen A, Schreurs MWJ, de Bruijn MAAM, Boukhrissi S, Nagtzaam MMP, Hulsenboom ESP, Enting RH, Thijs RD, Wirtz PW, Sillevis Smitt PAE, Titulaer MJ (2016) The relevance of VGKC positivity in the absence of LGI1 and Caspr2 antibodies. Neurology 86:1692–1699. https://doi.org/10.1212/WNL.0000000000002637

    Article  CAS  PubMed  Google Scholar 

  8. Louis DN, Ohgaki H, Wiestler ODCW (2016) World Health Organization histological classification of tumours of the central nervous system. International Agency for Research on Cancer, France

    Google Scholar 

  9. Athauda D, Delamont RS, De P-FE (2014) High grade glioma mimicking voltage gated potassium channel complex associated antibody limbic encephalitis. Case Rep Neurol Med 2014:1–4. https://doi.org/10.1155/2014/458790

    Article  Google Scholar 

  10. Cope TE, Breen DP, Chawda S, Cifelli A (2016) Anti-collapsin response mediator protein 5 encephalitis masquerading as a low-grade brain tumour. Pract Neurol 16:376–380. https://doi.org/10.1136/practneurol-2016-001379

    Article  PubMed  Google Scholar 

  11. Deramecourt V, Bombois S, Debette S, Delbeuck X, Ramirez C, Reyns N, Kerdraon O, Maurage CA, Pasquier F (2009) Bilateral temporal glioma presenting as a paraneoplastic limbic encephalitis with pure cognitive impairment. Neurologist. 15:208–211. https://doi.org/10.1097/NRL.0b013e31818fc022

    Article  PubMed  Google Scholar 

  12. Kerling F, Blümcke I, Stefan H (2008) Pitfalls in diagnosing limbic encephalitis—a case report. Acta Neurol Scand 118:339–342

    Article  CAS  PubMed  Google Scholar 

  13. Nagata R, Ikeda K, Nakamura Y, Ishikawa Y, Miura K, Sato R, Kawase Y, Kawabe K, Iwasaki Y (2010) A case of Gliomatosis Cerebri mimicking limbic encephalitis: malignant transformation to glioblastoma. Intern Med 49:1307–1310

    Article  PubMed  Google Scholar 

  14. Simo M, Dalmau J (2009) Cerebral gliomatosis simulating limbic encephalitis. Neurologia 24:500–501

    CAS  PubMed  Google Scholar 

  15. Schulz UG, Stewart W, Thomas SR (2009) A difficult case solved at autopsy: memory loss, behavioural change and seizures. Pract Neurol 9:90–95

    Article  CAS  PubMed  Google Scholar 

  16. Urbach H, Soeder BM, Jeub M, Klockgether T, Meyer B, Bien CG (2006) Serial MRI of limbic encephalitis. Neuroradiology 48:380–386. https://doi.org/10.1007/s00234-006-0069-0

    Article  PubMed  Google Scholar 

  17. Oyanguren B, Sánchez V, González FJ, de Felipe A, Esteban L, López-Sendón JL, Garcia-Barragán N, Martínez-San Millán J, Masjuán J, Corral I (2013) Limbic encephalitis: a clinical-radiological comparison between herpetic and autoimmune etiologies. Eur J Neurol 20:1566–1570. https://doi.org/10.1111/ene.12249

    Article  CAS  PubMed  Google Scholar 

  18. Kotsenas AL, Watson RE, Pittock SJ, Britton JW, Hoye SL, Quek AML, Shin C, Klein CJ (2014) MRI findings in autoimmune voltage-gated potassium channel complex encephalitis with seizures: one potential etiology for mesial temporal sclerosis. Am J Neuroradiol 35:84–89. https://doi.org/10.3174/ajnr.A3633

    Article  CAS  PubMed  Google Scholar 

  19. Chourmouzi D, Papadopoulou E, Marias K, Drevelegas A (2014) Imaging of brain tumors. Surg Oncol Clin N Am 23:629–684. https://doi.org/10.1016/j.soc.2014.07.004

    Article  PubMed  Google Scholar 

  20. Dean BL, Drayer BP, Bird CR, Flom RA, Hodak JA, Coons SW, Carey RG (1990) Gliomas: classification with MR imaging. Radiology 174:411–415. https://doi.org/10.1148/radiology.174.2.2153310

    Article  CAS  PubMed  Google Scholar 

  21. Ng ASL, Kramer J, Centurion A, Dalmau J, Huang E, Cotter JA, Geschwind MD (2015) Clinico-pathological correlation in adenylate kinase 5 autoimmune limbic encephalitis. J Neuroimmunol 287:31–35. https://doi.org/10.1016/j.jneuroim.2015.08.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tüzün E, Rossi JE, Karner SF, Centurion AF, Dalmau J (2007) Adenylate kinase 5 autoimmunity in treatment refractory limbic encephalitis. J Neuroimmunol 186:177–180. https://doi.org/10.1016/j.jneuroim.2007.03.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Do LD, Chanson E, Desestret V, Joubert B, Ducray F, Brugière S, Couté Y, Formaglio M, Rogemond V, Thomas-Antérion C, Borrega L, Laurens B, Tison F, Curot J, de Brouker T, Lebrun-Frenay C, Delattre JY, Antoine JC, Honnorat J (2017) Characteristics in limbic encephalitis with anti-adenylate kinase 5 autoantibodies. Neurology 88:514–524. https://doi.org/10.1212/WNL.0000000000003586

    Article  CAS  PubMed  Google Scholar 

  24. Flanagan EP, Kotsenas AL, Britton JW, McKeon A, Watson RE, Klein CJ, Boeve BF, Lowe V, Ahlskog JE, Shin C, Boes CJ, Crum BA, Laughlin RS, Pittock SJ (2015) Basal ganglia T1 hyperintensity in LGI1-autoantibody faciobrachial dystonic seizures. Neurology 2. https://doi.org/10.1212/NXI.0000000000000161

  25. Tripathi M, Tripathi M, Roy SG, Parida GK, Ihtisham K, Dash D, Damle N, Shamim SA, Bal C (2018) Metabolic topography of autoimmune non-paraneoplastic encephalitis. Neuroradiology 60:189–198. https://doi.org/10.1007/s00234-017-1956-2

    Article  PubMed  Google Scholar 

  26. Urbach H, Rauer S, Mader I, Paus S, Wagner J, Malter MP, Prüss H, Lewerenz J, Kassubek J, Hegen H, Auer M, Deisenhammer F, Ufer F, Bien CG, Baumgartner A (2015) Supratentorial white matter blurring associated with voltage-gated potassium channel-complex limbic encephalitis. Neuroradiology 57:1203–1209. https://doi.org/10.1007/s00234-015-1581-x

    Article  CAS  PubMed  Google Scholar 

  27. Kim JA, Chung J, Ho Yoon P et al (2001) Transient MR signal changes in patients with generalized tonicoclonic seizure or status epilepticus: Periictal diffusion-weighted imaging. Am J Neuroradiol 22:1149–1160

    CAS  PubMed  Google Scholar 

  28. Gultekin SH, Rosenfeld MR, Voltz R et al (2000) Paraneoplastic limbic encephalitis: neurological symptoms, immunological findings and tumour association in 50 patients. Brain 123(Pt 7):1481–1494

    Article  PubMed  Google Scholar 

  29. van Sonderen A, Thijs RD, Coenders EC, Jiskoot LC, Sanchez E, de Bruijn MAAM, van Coevorden-Hameete MH, Wirtz PW, Schreurs MWJ, Sillevis Smitt PAE, Titulaer MJ (2016) Anti-LGI1 encephalitis: clinical syndrome and long-term follow-up. Neurology 87:1449–1456. https://doi.org/10.1212/WNL.0000000000003173

    Article  CAS  PubMed  Google Scholar 

  30. Finke C, Prüss H, Heine J, Reuter S, Kopp UA, Wegner F, Then Bergh F, Koch S, Jansen O, Münte T, Deuschl G, Ruprecht K, Stöcker W, Wandinger KP, Paul F, Bartsch T (2017) Evaluation of cognitive deficits and structural hippocampal damage in encephalitis with leucine-rich, glioma-inactivated 1 antibodies. JAMA Neurol 74:50–59. https://doi.org/10.1001/jamaneurol.2016.4226

    Article  PubMed  Google Scholar 

  31. van Sonderen A, Ariño H, Petit-Pedrol M, Leypoldt F, Körtvélyessy P, Wandinger KP, Lancaster E, Wirtz PW, Schreurs MWJ, Sillevis Smitt PAE, Graus F, Dalmau J, Titulaer MJ (2016) The clinical spectrum of Caspr2 antibody-associated disease. Neurology 87:521–528. https://doi.org/10.1212/WNL.0000000000002917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hirai T, Korogi Y, Yoshizumi K, Shigematsu Y, Sugahara T, Takahashi M (2000) Limbic lobe of the human brain: evaluation with turbo fluid-attenuated inversion-recovery MR imaging. Radiology 215:470–475. https://doi.org/10.1148/radiology.215.2.r00ma06470

    Article  CAS  PubMed  Google Scholar 

  33. Coan AC, Kubota B, Bergo FPG, Campos BM, Cendes F (2014) 3T MRI quantification of hippocampal volume and signal in mesial temporal lobe epilepsy improves detection of hippocampal sclerosis. Am J Neuroradiol 35:77–83. https://doi.org/10.3174/ajnr.A3640

    Article  CAS  PubMed  Google Scholar 

  34. Wagner J, Schoene-Bake JC, Malter MP, Urbach H, Huppertz HJ, Elger CE, Weber B (2013) Quantitative FLAIR analysis indicates predominant affection of the amygdala in antibody-associated limbic encephalitis. Epilepsia 54:1679–1687. https://doi.org/10.1111/epi.12320

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Francesc Graus (Barcelona, Spain) for providing cell-based assay for AK5 antibody and Angela Vincent (Oxford, UK) for VGKC radioimmunoassay, and Joanne Fleming for reviewing the manuscript.

Funding

No funding was received for this study.

Author information

Authors and Affiliations

  1. Neurology Unit, AULSS 6 Euganea, Padua, Italy

    Marco Zoccarato & Silvia Valeggia

  2. Neuroimmunology Group, Istituto di Ricerca Pediatrica, Padua, Italy

    Marco Zoccarato, Luigi Zuliani & Piera De Gaspari

  3. Department of Neurology, Ospedale San Bortolo, AULSS 8 Berica, Vicenza, Italy

    Luigi Zuliani

  4. Neuroimmunology Laboratory, IRCSS Mondino Foundation, Pavia, Italy

    Matteo Gastaldi & Diego Franciotta

  5. Neurology Unit, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy

    Sara Mariotto & Sergio Ferrari

  6. Department of Oncology, Oncology 1, Veneto Institute of Oncology IOV-IRCCS, Padua, Italy

    Giuseppe Lombardi & Vittorina Zagonel

  7. Department of Neurosciences (DNS), Statistic and Informatics Unit, School of Medicine, University of Padua, Padua, Italy

    Mario Ermani

  8. Department of Health Sciences, University of Genoa, Genoa, Italy

    Alessio Signori

  9. Department of Neuroradiology, IRCSS Mondino Foundation, Pavia, Italy

    Anna Pichiecchio

  10. Department of Neurology, Ospedale Santa Chiara, Trento, Italy

    Bruno Giometto

  11. Neuroradiology, Department of Medicine and Surgery, Sezione di Neuroscienze, University of Salerno, Salerno, Italy

    Renzo Manara

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  1. Marco Zoccarato
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Correspondence to Marco Zoccarato.

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Zoccarato, M., Valeggia, S., Zuliani, L. et al. Conventional brain MRI features distinguishing limbic encephalitis from mesial temporal glioma. Neuroradiology 61, 853–860 (2019). https://doi.org/10.1007/s00234-019-02212-1

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