Abstract
Cortical superficial siderosis (cSS) is a pathologic and radiologic diagnosis of hemosiderin deposition in subpial brain layers. However, cSS has not been fully studied in patients with acute stroke. Here, we investigated the prevalence of cSS in patients with acute stroke and analyzed the relationship between cSS and different clinical and neuroimaging characteristics. From September 2014 through June 2016, consecutive patients with acute stroke who were admitted to our department were retrospectively investigated. We analyzed the prevalence of cSS and the associations between cSS and risk factors, the topographic distribution of cerebral microbleeds (CMBs), and the severity of white matter lesions (WMLs). In total, 739 patients (589 patients with ischemic stroke/transient ischemic stroke [IS/TIA] and 150 with intracerebral hemorrhage [ICH]; mean age, 71.4 years) were enrolled. We identified cSS in six (1.0%) patients with IS/TIA and seven (4.7%) patients with ICH. The presence of cSS was associated with ICH (P < 0.0001), WMLs (P = 0.0105), and lobar and non-lobar CMBs (both P < 0.0001); no associations between cSS and age, sex, cardiovascular risk factors, IS subtype classification, or antiplatelet and anticoagulant therapy were found. In a multivariable logistic regression analysis, high numbers of lobar CMBs (≥ 2; odds ratio, 11.03; 95% confidence interval, 2.03–205.40; P = 0.0029) were independently associated with cSS. Furthermore, cSS was often located near lobar CMBs. Our results suggest that cSS is prevalent in ICH and is independently associated with lobar CMBs; however, no associations between cSS and other risk factors or comorbidities were observed.
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Charidimou A, Linn J, Vernooij MW, Opherk C, Akoudad S, Baron JC, Greenberg SM, Jager HR, Werring DJ (2015) Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain 138:2126–2139
Feldman HH, Maia LF, Mackenzie IR, Forster BB, Martzke J, Woolfenden A (2008) Superficial siderosis: a potential diagnostic marker of cerebral amyloid angiopathy in Alzheimer disease. Stroke 39:2894–2897
Charidimou A, Peeters AP, Jager R, Fox Z, Vandermeeren Y, Laloux P, Baron JC, Werring DJ (2013) Cortical superficial siderosis and intracerebral hemorrhage risk in cerebral amyloid angiopathy. Neurology 81:1666–1673
Roongpiboonsopit D, Charidimou A, William CM, Lauer A, Falcone GJ, Martinez-Ramirez S, Biffi A, Ayres A, Vashkevich A, Awosika OO, Rosand J, Gurol ME, Silverman SB, Greenberg SM, Viswanathan A (2016) Cortical superficial siderosis predicts early recurrent lobar hemorrhage. Neurology 87:1863–1870
Takeda S, Yamazaki K, Miyakawa T, Onda K, Hinokuma K, Ikuta F, Arai H (2003) Subcortical hematoma caused by cerebral amyloid angiopathy: does the first evidence of hemorrhage occur in the subarachnoid space? Neuropathology 23:254–261
Linn J, Wollenweber FA, Lummel N, Bochmann K, Pfefferkorn T, Gschwendtner A, Bruckmann H, Dichgans M, Opherk C (2013) Superficial siderosis is a warning sign for future intracranial hemorrhage. J Neurol 260:176–181
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
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
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
Inoue Y, Nakajima M, Uetani H, Hirai T, Ueda M, Kitajima M, Utsunomiya D, Watanabe M, Hashimoto M, Ikeda M, Yamashita Y, Ando Y (2016) Diagnostic significance of cortical superficial siderosis for Alzheimer disease in patients with cognitive impairment. AJNR Am J Neuroradiol 37:223–227
Charidimou A, Ni J, Martinez-Ramirez S, Vashkevich A, Ayres A, Rosand J, Gurol EM, Greenberg SM, Viswanathan A (2016) Cortical superficial siderosis in memory clinic patients: further evidence for underlying cerebral amyloid angiopathy. Cerebrovasc Dis 41:156–162
Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in acute stroke treatment. Stroke 24:35–41
Shams S, Martola J, Charidimou A, Cavallin L, Granberg T, Shams M, Forslin Y, Aspelin P, Kristoffersen-Wiberg M, Wahlund LO (2016) Cortical superficial siderosis: prevalence and biomarker profile in a memory clinic population. Neurology 87:1110–1117
Moulin S, Labreuche J, Bombois S, Rossi C, Boulouis G, Hénon H, Duhamel A, Leys D, Cordonnier C (2016) Dementia risk after spontaneous intracerebral haemorrhage: a prospective cohort study. The Lancet Neurology 15:820–829
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356
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
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
Gattringer T, Eppinger S, Beitzke M, Wuensch G, Niederkorn K, Deutschmann H, Fazekas F, Enzinger C (2015) Cortical superficial siderosis and risk of bleeding after thrombolysis for ischemic stroke. Cerebrovasc Dis 40:191–197
Ni J, Auriel E, Jindal J, Ayres A, Schwab KM, Martinez-Ramirez S, Gurol EM, Greenberg SM, Viswanathan A (2015) The characteristics of superficial siderosis and convexity subarachnoid hemorrhage and clinical relevance in suspected cerebral amyloid angiopathy. Cerebrovasc Dis 39:278–286
Raposo N, Viguier A, Cuvinciuc V, Calviere L, Cognard C, Bonneville F, Larrue V (2011) Cortical subarachnoid haemorrhage in the elderly: a recurrent event probably related to cerebral amyloid angiopathy. Eur J Neurol 18:597–603
Kumar S, Goddeau RP Jr, Selim MH, Thomas A, Schlaug G, Alhazzani A, Searls DE, Caplan LR (2010) Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies. Neurology 74:893–899
De Reuck J, Deramecourt V, Cordonnier C, Auger F, Durieux N, Pasquier F, Bordet R, Defebvre L, Caparros-Lefebvre D, Maurage CA, Leys D (2013) Superficial siderosis of the central nervous system: a post-mortem 7.0-tesla magnetic resonance imaging study with neuropathological correlates. Cerebrovasc Dis 36:412–417
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
Arboix A, Vall-Llosera A, Garcia-Eroles L, Massons J, Oliveres M, Targa C (2002) Clinical features and functional outcome of intracerebral hemorrhage in patients aged 85 and older. J Am Geriatr Soc 50:449–454
Charidimou A, Baron JC, Werring DJ (2013) Transient focal neurological episodes, cerebral amyloid angiopathy, and intracerebral hemorrhage risk: looking beyond TIAs. Int J Stroke 8:105–108
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This study was conducted in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study protocol was approved by the ethics committee of Nippon Medical School and all participants or their family members provided written informed consent for participation.
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Suda, S., Shimoyama, T., Suzuki, S. et al. Prevalence and clinical characteristics of cortical superficial siderosis in patients with acute stroke. J Neurol 264, 2413–2419 (2017). https://doi.org/10.1007/s00415-017-8646-1
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DOI: https://doi.org/10.1007/s00415-017-8646-1