Cognitive Impairment Before Intracerebral Hemorrhage Is Associated With Cerebral Amyloid Angiopathy

Gargi Banerjee, Duncan Wilson, Gareth Ambler, Karen Osei-Bonsu Appiah, Clare Shakeshaft, Surabhika Lunawat, Hannah Cohen, Tarek Yousry Dr, Gregory Y H Lip, Keith W Muir, Martin M Brown, Rustam Al-Shahi Salman, Hans Rolf Jäger, David J Werring, CROMIS-2 Collaborators, Gargi Banerjee, Duncan Wilson, Gareth Ambler, Karen Osei-Bonsu Appiah, Clare Shakeshaft, Surabhika Lunawat, Hannah Cohen, Tarek Yousry Dr, Gregory Y H Lip, Keith W Muir, Martin M Brown, Rustam Al-Shahi Salman, Hans Rolf Jäger, David J Werring, CROMIS-2 Collaborators

Abstract

Background and purpose: Although the association between cerebral amyloid angiopathy (CAA) and cognitive impairment is increasingly recognized, it is not clear whether this is because of the impact of recurrent intracerebral hemorrhage (ICH) events, disruptions caused by cerebral small vessel damage, or both. We investigated this by considering whether cognitive impairment before ICH was associated with neuroimaging features of CAA on magnetic resonance imaging.

Methods: We studied 166 patients with neuroimaging-confirmed ICH recruited to a prospective multicentre observational study. Preexisting cognitive impairment was determined using the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE). Magnetic resonance imaging markers of cerebral small vessel disease, including CAA, were rated by trained observers according to consensus guidelines.

Results: The prevalence of cognitive impairment before ICH was 24.7% (n=41) and, in adjusted analyses, was associated with fulfilling the modified Boston criteria for probable CAA at presentation (odds ratio, 4.01; 95% confidence interval, 1.53-10.51; P=0.005) and a higher composite CAA score (for each point increase, odds ratio, 1.42; 95% confidence interval, 1.03-1.97; P=0.033). We also found independent associations between pre-ICH cognitive decline and the presence of cortical superficial siderosis, strictly lobar microbleeds, and lobar ICH location, but not with other neuroimaging markers, or a composite small vessel disease score.

Conclusions: CAA (defined using magnetic resonance imaging markers) is associated with cognitive decline before symptomatic ICH. This provides evidence that small vessel disruption in CAA makes an independent contribution to cognitive impairment, in addition to effects due to brain injury caused directly by ICH.

Clinical trial registration: URL: https://www.clinicaltrials.gov. Unique identifier: NCT02513316.

Keywords: cerebral amyloid angiopathy; cerebral hemorrhage; cerebral small vessel diseases; cognitive dysfunction; prevalence; siderosis.

© 2017 The Authors.

References

    1. Pendlebury ST, Rothwell PM. Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis. Lancet Neurol. 2009;8:1006–1018. doi: 10.1016/S1474-4422(09)70236-4.
    1. Moulin S, Labreuche J, Bombois S, Rossi C, Boulouis G, Hénon H, et al. Dementia risk after spontaneous intracerebral haemorrhage: a prospective cohort study. Lancet Neurol. 2016;15:820–829. doi: 10.1016/S1474-4422(16)00130-7.
    1. Poon MT, Fonville AF, Al-Shahi Salman R. Long-term prognosis after intracerebral haemorrhage: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2014;85:660–667. doi: 10.1136/jnnp-2013-306476.
    1. Xiong L, Reijmer YD, Charidimou A, Cordonnier C, Viswanathan A. Intracerebral hemorrhage and cognitive impairment. Biochim Biophys Acta. 2016;1862:939–944. doi: 10.1016/j.bbadis.2015.12.011.
    1. Biffi A, Bailey D, Anderson CD, Ayres AM, Gurol EM, Greenberg SM, et al. Risk factors associated with early vs delayed dementia after intracerebral hemorrhage. JAMA Neurol. 2016;73:969–976. doi: 10.1001/jamaneurol.2016.0955.
    1. Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74:1346–1350. doi: 10.1212/WNL.0b013e3181dad605.
    1. Charidimou A, Martinez-Ramirez S, Reijmer YD, Oliveira-Filho J, Lauer A, Roongpiboonsopit D, et al. Total magnetic resonance imaging burden of small vessel disease in cerebral amyloid angiopathy: an imaging-pathologic study of concept validation. JAMA Neurol. 2016;73:994–1001. doi: 10.1001/jamaneurol.2016.0832.
    1. Charidimou A, Wilson D, Shakeshaft C, Ambler G, White M, Cohen H, et al. The Clinical Relevance of Microbleeds in Stroke study (CROMIS-2): rationale, design, and methods. Int J Stroke. 2015;10(suppl A100):155–161. doi: 10.1111/ijs.12569.
    1. McGovern A, Pendlebury ST, Mishra NK, Fan Y, Quinn TJ. Test accuracy of informant-based cognitive screening tests for diagnosis of dementia and multidomain cognitive impairment in stroke. Stroke. 2016;47:329–335. doi: 10.1161/STROKEAHA.115.011218.
    1. Harrison JK, Fearon P, Noel-Storr AH, McShane R, Stott DJ, Quinn TJ. Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE) for the diagnosis of dementia within a secondary care setting. Cochrane Database Syst Rev. 2015;3:CD010772.
    1. Jorm AF. A short form of the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): development and cross-validation. Psychol Med. 1994;24:145–153.
    1. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, et al. STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12:822–838. doi: 10.1016/S1474-4422(13)70124-8.
    1. Gregoire SM, Chaudhary UJ, Brown MM, Yousry TA, Kallis C, Jäger HR, et al. The Microbleed Anatomical Rating Scale (MARS): reliability of a tool to map brain microbleeds. Neurology. 2009;73:1759–1766. doi: 10.1212/WNL.0b013e3181c34a7d.
    1. Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41:450–454. doi: 10.1161/STROKEAHA.109.564914.
    1. Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75:1519–1523. doi: 10.1136/jnnp.2003.030858.
    1. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149:351–356. doi: 10.2214/ajr.149.2.351.
    1. Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, et al. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology. 1993;43:1683–1689.
    1. Charidimou A, Linn J, Vernooij MW, Opherk C, Akoudad S, Baron JC, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015;138(pt 8):2126–2139. doi: 10.1093/brain/awv162.
    1. Harper L, Barkhof F, Fox NC, Schott JM. Using visual rating to diagnose dementia: a critical evaluation of MRI atrophy scales. J Neurol Neurosurg Psychiatry. 2015;86:1225–1233. doi: 10.1136/jnnp-2014-310090.
    1. Kebets V, Gregoire SM, Charidimou A, Barnes J, Rantell K, Brown MM, et al. Prevalence and cognitive impact of medial temporal atrophy in a hospital stroke service: retrospective cohort study. Int J Stroke. 2015;10:861–867. doi: 10.1111/ijs.12544.
    1. Volbers B, Staykov D, Wagner I, Dörfler A, Saake M, Schwab S, et al. Semi-automatic volumetric assessment of perihemorrhagic edema with computed tomography. Eur J Neurol. 2011;18:1323–1328. doi: 10.1111/j.1468-1331.2011.03395.x.
    1. Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 2014;83:1228–1234. doi: 10.1212/WNL.0000000000000837.
    1. Staals J, Booth T, Morris Z, Bastin ME, Gow AJ, Corley J, et al. Total MRI load of cerebral small vessel disease and cognitive ability in older people. Neurobiol Aging. 2015;36:2806–2811. doi: 10.1016/j.neurobiolaging.2015.06.024.
    1. Cordonnier C, Leys D, Dumont F, Deramecourt V, Bordet R, Pasquier F, et al. What are the causes of pre-existing dementia in patients with intracerebral haemorrhages? Brain. 2010;133:3281–3289. doi: 10.1093/brain/awq246.
    1. Reijmer YD, Fotiadis P, Martinez-Ramirez S, Salat DH, Schultz A, Shoamanesh A, et al. Structural network alterations and neurological dysfunction in cerebral amyloid angiopathy. Brain. 2015;138(p)(t 1):179–188. doi: 10.1093/brain/awu316.
    1. Reijmer YD, Fotiadis P, Riley GA, Xiong L, Charidimou A, Boulouis G, et al. Progression of brain network alterations in cerebral amyloid angiopathy. Stroke. 2016;47:2470–2475. doi: 10.1161/STROKEAHA.116.014337.
    1. Arvanitakis Z, Leurgans SE, Wang Z, Wilson RS, Bennett DA, Schneider JA. Cerebral amyloid angiopathy pathology and cognitive domains in older persons. Ann Neurol. 2011;69:320–327. doi: 10.1002/ana.22112.
    1. Case NF, Charlton A, Zwiers A, Batool S, McCreary CR, Hogan DB, et al. Cerebral amyloid angiopathy is associated with executive dysfunction and mild cognitive impairment. Stroke. 2016;47:2010–2016. doi: 10.1161/STROKEAHA.116.012999.
    1. Xiong L, Davidsdottir S, Reijmer YD, Shoamanesh A, Roongpiboonsopit D, Thanprasertsuk S, et al. Cognitive profile and its association with neuroimaging markers of non-demented cerebral amyloid angiopathy patients in a stroke unit. J Alzheimers Dis. 2016;52:171–178. doi: 10.3233/JAD-150890.
    1. Boyle PA, Yu L, Nag S, Leurgans S, Wilson RS, Bennett DA, et al. Cerebral amyloid angiopathy and cognitive outcomes in community-based older persons. Neurology. 2015;85:1930–1936. doi: 10.1212/WNL.0000000000002175.
    1. Harper L, Barkhof F, Scheltens P, Schott JM, Fox NC. An algorithmic approach to structural imaging in dementia. J Neurol Neurosurg Psychiatry. 2014;85:692–698. doi: 10.1136/jnnp-2013-306285.

Source: PubMed

3
订阅