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Clinical spectrum, underlying etiologies and radiological characteristics of cortical superficial siderosis

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Abstract

Cortical superficial siderosis (cSS) is an increasingly recognized MR-imaging marker most probably caused by focal convexity subarachnoid hemorrhage (SAH). There is accumulating evidence that cSS represents an important risk factor for subsequent intracranial hemorrhages. Here, we aimed to determine clinical symptoms, underlying etiologies, and radiological characteristics of cSS in a large patient cohort. We performed an electronic database search on all patients who presented between 2002 and 2013 to the university hospital Munich with non-traumatic and non-aneurysmal cSS. T2*-weighted gradient-echo sequences were analyzed regarding localization and extent of cSS as well as of acute SAH, intracerebral hemorrhages (ICH) and microbleeds. Besides, all available clinical, laboratory, imaging and histological data were analyzed. 113 subjects matched the inclusion criteria. The following etiologies for cSS were identified: definite (n = 6; 5 %), probable (n = 75; 66 %), and possible (n = 28; 25 %) cerebral amyloid angiopathy (CAA); reversible cerebral vasoconstriction syndrome: 2 (2 %); central nervous system vasculitis: 1; and hyperperfusion syndrome: 1. Acute ICH was evident in 55 (49 %) cases. Other clinical manifestations were: transient focal neurological episodes (TFNE): 38 (34 %); cognitive impairment: 14 (12 %); generalized seizure: 4 (4 %); and headache: 2 (2 %). Adjusting for age and gender, cognitive impairment was more frequent in disseminated cSS, while TFNE was more often found in focal cSS (p = 0.042). Our data indicate CAA to be the most common etiology of cSS. In absence of symptomatic ICH, patients with focal cSS frequently present with TFNE, while those with disseminated cSS commonly manifest with cognitive impairment.

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References

  1. Charidimou A, Jager RH, Fox Z, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Werring DJ (2013) Prevalence and mechanisms of cortical superficial siderosis in cerebral amyloid angiopathy. Neurology 81:626–632. doi:10.1212/WNL.0b013e3182a08f2c

    Article  PubMed  Google Scholar 

  2. Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, van Buchem MA, Bruckmann H, Greenberg SM (2010) Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 74:1346–1350. doi:10.1212/WNL.0b013e3181dad605

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Linn J, Wollenweber FA, Lummel N, Bochmann K, Pfefferkorn T, Gschwendtner A, Bruckmann H, Dichgans M, Opherk C (2012) Superficial siderosis is a warning sign for future intracranial hemorrhage. J Neurol 260:176–181. doi:10.1007/s00415-012-6610-7

    Article  PubMed  Google Scholar 

  4. Kumar N, Cohen-Gadol AA, Wright RA, Miller GM, Piepgras DG, Ahlskog JE (2006) Superficial siderosis. Neurology 66:1144–1152. doi:10.1212/01.wnl.0000208510.76323.5b

    Article  CAS  PubMed  Google Scholar 

  5. Kumar N (2010) Neuroimaging in superficial siderosis: an in-depth look. AJNR Am J Neuroradiol 31:5–14. doi:10.3174/ajnr.A1628

    Article  CAS  PubMed  Google Scholar 

  6. Linn J, Herms J, Dichgans M, Bruckmann H, Fesl G, Freilinger T, Wiesmann M (2008) Subarachnoid hemosiderosis and superficial cortical hemosiderosis in cerebral amyloid angiopathy. AJNR Am J Neuroradiol 29:184–186. doi:10.3174/ajnr.A0783

    Article  CAS  PubMed  Google Scholar 

  7. Cuvinciuc V, Viguier A, Calviere L, Raposo N, Larrue V, Cognard C, Bonneville F (2010) Isolated acute nontraumatic cortical subarachnoid hemorrhage. AJNR Am J Neuroradiol 31:1355–1362. doi:10.3174/ajnr.A1986

    Article  CAS  PubMed  Google Scholar 

  8. Charidimou A, Peeters A, Fox Z, Gregoire SM, Vandermeeren Y, Laloux P, Jager HR, Baron JC, Werring DJ (2012) Spectrum of transient focal neurological episodes in cerebral amyloid angiopathy: multicentre magnetic resonance imaging cohort study and meta-analysis. Stroke 43:2324–2330. doi:10.1161/STROKEAHA.112.657759

    Article  PubMed  Google Scholar 

  9. Wollenweber FA, Buerger K, Mueller C, Ertl-Wagner B, Malik R, Dichgans M, Linn J, Opherk C (2014) Prevalence of cortical superficial siderosis in patients with cognitive impairment. J Neurol 261:277–282. doi:10.1007/s00415-013-7181-y

    Article  PubMed  Google Scholar 

  10. Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjogren M, Wallin A, Ader H, Leys D, Pantoni L, Pasquier F, Erkinjuntti T, Scheltens P, European task force on age-related white matter C (2001) A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke 32:1318–1322. doi:10.1161/01.STR.32.6.1318

    Article  CAS  PubMed  Google Scholar 

  11. Knudsen KA, Rosand J, Karluk D, Greenberg SM (2001) Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 56:537–539. doi:10.1212/WNL.56.4.537

    Article  CAS  PubMed  Google Scholar 

  12. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194. doi:10.1111/j.1365-2796.2004.01388.x

    Article  CAS  PubMed  Google Scholar 

  13. Ducros A, Boukobza M, Porcher R, Sarov M, Valade D, Bousser MG (2007) The clinical and radiological spectrum of reversible cerebral vasoconstriction syndrome. A prospective series of 67 patients. Brain 130:3091–3101. doi:10.1093/brain/awm256

    Article  PubMed  Google Scholar 

  14. Khurram A, Kleinig T, Leyden J (2014) Clinical associations and causes of convexity subarachnoid hemorrhage. Stroke 45:1151–1153. doi:10.1161/STROKEAHA.113.004298

    Article  CAS  PubMed  Google Scholar 

  15. Brunot S, Osseby GV, Rouaud O, Kazemi A, Ricolfi F, Couvreur G, Catteau A, Hervieu M, Moreau T, Giroud M, Bejot Y (2010) Transient ischaemic attack mimics revealing focal subarachnoid haemorrhage. Cerebrovasc Dis 30:597–601. doi:10.1159/000319780

    Article  PubMed  Google Scholar 

  16. Izenberg A, Aviv RI, Demaerschalk BM, Dodick DW, Hopyan J, Black SE, Gladstone DJ (2009) Crescendo transient Aura attacks: a transient ischemic attack mimic caused by focal subarachnoid hemorrhage. Stroke 40:3725–3729. doi:10.1161/STROKEAHA.109.557009

    Article  PubMed  Google Scholar 

  17. Kleinig TJ, Kiley M, Thompson PD (2008) Acute convexity subarachnoid haemorrhage: a cause of aura-like symptoms in the elderly. Cephalalgia 28:658–663. doi:10.1111/j.1468-2982.2008.01570.x

    Article  CAS  PubMed  Google Scholar 

  18. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ (2006) Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 129:3224–3237. doi:10.1093/brain/awl297

    Article  PubMed  Google Scholar 

  19. Vernooij MW, Ikram MA, Hofman A, Krestin GP, Breteler MM, van der Lugt A (2009) Superficial siderosis in the general population. Neurology 73:202–205. doi:10.1212/WNL.0b013e3181ae7c5e

    Article  CAS  PubMed  Google Scholar 

  20. Zonneveld HI, Goos JD, Wattjes MP, Prins ND, Scheltens P, van der Flier WM, Kuijer JP, Muller M, Barkhof F (2014) Prevalence of cortical superficial siderosis in a memory clinic population. Neurology 82:698–704. doi:10.1212/WNL.0000000000000150

    Article  PubMed  Google Scholar 

  21. Arvanitakis Z, Leurgans SE, Wang Z, Wilson RS, Bennett DA, Schneider JA (2011) Cerebral amyloid angiopathy pathology and cognitive domains in older persons. Ann Neurol 69:320–327. doi:10.1002/ana.22112

    Article  PubMed Central  PubMed  Google Scholar 

  22. Shoamanesh A, Martinez-Ramirez S, Oliveira-Filho J, Reijmer Y, Falcone GJ, Ayres A, Schwab K, Goldstein JN, Rosand J, Gurol ME, Viswanathan A, Greenberg SM (2014) Interrelationship of superficial siderosis and microbleeds in cerebral amyloid angiopathy. Neurology 83:1838–1843. doi:10.1212/WNL.0000000000000984

    Article  PubMed  Google Scholar 

  23. Na HK, Park JH, Kim JH, Kim HJ, Kim ST, Werring DJ, Seo SW, Na DL (2015) Cortical superficial siderosis: a marker of vascular amyloid in patients with cognitive impairment. Neurology 84:849–855. doi:10.1212/WNL.0000000000001288

    Article  CAS  PubMed  Google Scholar 

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Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical standards statement

We hereby state, that the study has been approved by our institutional ethics committee and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All patients or their guardians gave their informed consent prior to their inclusion in the study.

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    Authors and Affiliations

    1. Department of Neuroradiology, University Hospital Munich, Munich, Germany

      Nina Lummel & Katja Bochmann

    2. Department of Neurology, University Hospital Munich, Munich, Germany

      Frank Arne Wollenweber

    3. Institute for Stroke and Dementia Research, University Hospital Munich, Munich, Germany

      Frank Arne Wollenweber, Rainer Malik & Christian Opherk

    4. Department of Radiology, University Hospital K. U. Leuven, Louvain, Belgium

      Philippe Demaerel

    5. Department of Neurology, SLK-Kliniken Heilbronn GmbH, Heilbronn, Germany

      Christian Opherk

    6. Institute for Diagnostic and Interventional Neuroradiology, University Hospital Carl Gustav Carus, Fetscherstr. 74, 01307, Dresden, Germany

      Jennifer Linn

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    1. Nina Lummel
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    Correspondence to Jennifer Linn.

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    N. Lummel and F. A. Wollenweber contributed equally.

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    Lummel, N., Wollenweber, F.A., Demaerel, P. et al. Clinical spectrum, underlying etiologies and radiological characteristics of cortical superficial siderosis. J Neurol 262, 1455–1462 (2015). https://doi.org/10.1007/s00415-015-7736-1

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    • DOI: https://doi.org/10.1007/s00415-015-7736-1

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