The Cognition and Affect after Stroke - a Prospective Evaluation of Risks (CASPER) study: rationale and design

Elles Douven, Syenna H J Schievink, Frans R J Verhey, Robert J van Oostenbrugge, Pauline Aalten, Julie Staals, Sebastian Köhler, Elles Douven, Syenna H J Schievink, Frans R J Verhey, Robert J van Oostenbrugge, Pauline Aalten, Julie Staals, Sebastian Köhler

Abstract

Background: Cognitive impairment and neuropsychiatric syndromes, like depression and apathy, are frequent residual consequences of stroke. These have a large impact on quality of life and long-term prognosis. Several factors are involved in the development of these residual syndromes, although their exact role and their interrelationships remain still rather unclear. The Cognition and Affect after Stroke: a Prospective Evaluation of Risks (CASPER) study has been primarily designed to examine whether stroke-specific (e.g. lesion location, volume, type, severity), cerebrovascular and neurodegenerative (e.g. white matter changes, atrophy, microbleeds, perivascular spaces), inflammatory, endothelial, and (epi)genetic markers are associated with cognitive impairment, post-stroke depression, and post-stroke apathy, and whether they predict their course over 12 months. The secondary aims are to investigate how the above-mentioned markers interact with each other, and to determine if patients with apathy and depression after stroke differ in pathogenesis, course, and outcome (e.g. functional outcome, neurocognitive performance, quality of life).

Methods/design: CASPER is a 1-year prospective clinical cohort follow-up study in 250 stroke patients recruited at the neurological in- and outpatient services at Maastricht University Medical Center (MUMC+, Maastricht, The Netherlands), and Zuyderland Medical Center (Sittard and Heerlen, The Netherlands). At baseline (3 months post-stroke), a neuropsychological assessment, neuropsychiatric interview, blood sample, and brain magnetic resonance imaging (MRI) scan are conducted. Assessment of neuropsychiatric and neurocognitive status are repeated 6 and 12 months later.

Discussion: The CASPER study investigates stroke-specific, vascular, neurodegenerative, inflammatory, and genetic markers of the development of vascular cognitive impairment, depression, and apathy after stroke. This creates the possibility to study not only the contribution of these individual markers but also their joint contribution, which differentiates this study from earlier stroke cohorts who lacked long-term follow-up data, a large sample size, an extensive MRI protocol, and markers from the blood. The knowledge we derive from this study might help in identifying markers that are associated with, or can predict the onset, maintenance, and progression of vascular cognitive impairment, depression, and apathy after stroke, and could provide new insights into possibilities for treatment and rehabilitation that result in better functional outcome after stroke.

Trial registration: ClinicalTrials.gov NCT02585349.

Keywords: Apathy; Cognition; Dementia; Depression; Design; Neuroimaging; Stroke.

References

    1. Feigin VL, Forouzanfar MH, Krishnamurthi R, Mensah GA, Connor M, Bennett DA, Moran AE, Sacco RL, Anderson L, Truelsen T. Global and regional burden of stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. Lancet. 2014;383(9913):245–255. doi: 10.1016/S0140-6736(13)61953-4.
    1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2013;380(9859):2095–2128. doi: 10.1016/S0140-6736(12)61728-0.
    1. Struijs JN, van Genugten ML, Evers SM, Ament AJ, Baan CA, van den Bos GA. Modeling the future burden of stroke in the Netherlands impact of aging, smoking, and hypertension. Stroke. 2005;36(8):1648–1655. doi: 10.1161/01.STR.0000173221.37568.d2.
    1. Jorge RE, Starkstein SE, Robinson RG. Apathy following stroke. Can J Psychiatr. 2010;55(6):350–354.
    1. van Dalen JW, van Charante EPM, Nederkoorn PJ, van Gool WA, Richard E. Poststroke apathy. Stroke. 2013;44(3):851–860. doi: 10.1161/STROKEAHA.112.674614.
    1. Carod-Artal J, Egido JA, González JL, De Seijas EV. Quality of life among stroke survivors evaluated 1 year after stroke: experience of a stroke unit. Stroke. 2000;31(12):2995–3000. doi: 10.1161/01.STR.31.12.2995.
    1. Ayerbe L, Ayis S, Wolfe CD, Rudd AG. Natural history, predictors and outcomes of depression after stroke: systematic review and meta-analysis. Br J Psychiatry. 2013;202(1):14–21. doi: 10.1192/bjp.bp.111.107664.
    1. O'Brien J, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, Bowler JV, Ballard C, DeCarli C, Gorelick PB. Vascular cognitive impairment. Lancet Neurol. 2003;2(2):89–98. doi: 10.1016/S1474-4422(03)00305-3.
    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(11):1006–1018. doi: 10.1016/S1474-4422(09)70236-4.
    1. Sachdev P, Brodaty H, Valenzuela M, Lorentz L, Looi J, Berman K, Ross A, Wen W, Zagami A. Clinical determinants of dementia and mild cognitive impairment following ischaemic stroke: the Sydney Stroke Study. Dement Geriatr Cogn Disord. 2006;21(5):275–283. doi: 10.1159/000091434.
    1. Pohjasvaara T, Mäntylä R, Salonen O, Aronen HJ, Ylikoski R, Hietanen M, Kaste M, Erkinjuntti T. How complex interactions of ischemic brain infarcts, white matter lesions, and atrophy relate to poststroke dementia. Arch Neurol. 2000;57(9):1295–1300. doi: 10.1001/archneur.57.9.1295.
    1. Kokmen E, Whisnant J, O'Fallon W, Chu C-P, Beard C. Dementia after ischemic stroke: a population-based study in Rochester, Minnesota (1960–1984) Neurology. 1996;46(1):154–159. doi: 10.1212/WNL.46.1.154.
    1. Richards M, Brayne C. What do we mean by Alzheimer’s disease? BMJ. 2010;341(7778):865–867.
    1. Spalletta G, Bossu P, Ciaramella A, Bria P, Caltagirone C, Robinson R. The etiology of poststroke depression: a review of the literature and a new hypothesis involving inflammatory cytokines. Mol Psychiatry. 2006;11(11):984–991. doi: 10.1038/sj.mp.4001879.
    1. Rothenburg LS, Herrmann N, Swardfager W, Black SE, Tennen G, Kiss A, Gladstone DJ, Ween J, Snaiderman A, Lanctôt KL. The relationship between inflammatory markers and post stroke cognitive impairment. J Geriatr Psychiatry Neurol. 2010;23(3):199–205. doi: 10.1177/0891988710373598.
    1. Di Napoli M, Schwaninger M, Cappelli R, Ceccarelli E, Di Gianfilippo G, Donati C, Emsley HC, Forconi S, Hopkins SJ, Masotti L. Evaluation of C-reactive protein measurement for assessing the risk and prognosis in ischemic stroke: a statement for health care professionals from the CRP pooling project members. Stroke. 2005;36(6):1316–1329. doi: 10.1161/01.STR.0000165929.78756.ed.
    1. Tzikas S, Schlak D, Sopova K, Gatsiou A, Stakos D, Stamatelopoulos K, Stellos K, Laske C. Increased myeloperoxidase plasma levels in patients with Alzheimer's disease. J Alzheimers Dis. 2014;39(3):557–564.
    1. Rajagopalan S, Brook R, Rubenfire M, Pitt E, Young E, Pitt B. Abnormal brachial artery flow-mediated vasodilation in young adults with major depression. Am J Cardiol. 2001;88(2):196–198. doi: 10.1016/S0002-9149(01)01623-X.
    1. Corsi MM, Licastro F, Porcellini E, Dogliotti G, Galliera E, Lamont JL, Innocenzi PJ, Fitzgerald SP. Reduced plasma levels of P-selectin and L-selectin in a pilot study from Alzheimer disease: relationship with neuro-degeneration. Biogerontology. 2011;12(5):451–454. doi: 10.1007/s10522-011-9335-6.
    1. Togo T, Akiyama H, Kondo H, Ikeda K, Kato M, Iseki E, Kosaka K. Expression of CD40 in the brain of Alzheimer’s disease and other neurological diseases. Brain Res. 2000;885(1):117–121. doi: 10.1016/S0006-8993(00)02984-X.
    1. Engelhart MJ, Geerlings MI, Meijer J, Kiliaan A, Ruitenberg A, van Swieten JC, Stijnen T, Hofman A, Witteman JC, Breteler MM. Inflammatory proteins in plasma and the risk of dementia: the Rotterdam study. Arch Neurol. 2004;61(5):668–672. doi: 10.1001/archneur.61.5.668.
    1. Tarkowski E, Liljeroth A-M, Minthon L, Tarkowski A, Wallin A, Blennow K. Cerebral pattern of pro-and anti-inflammatory cytokines in dementias. Brain Res Bull. 2003;61(3):255–260. doi: 10.1016/S0361-9230(03)00088-1.
    1. Komulainen P, Lakka TA, Kivipelto M, Hassinen M, Penttilä IM, Helkala E-L, Gylling H, Nissinen A, Rauramaa R. Serum high sensitivity C-reactive protein and cognitive function in elderly women. Age Ageing. 2007;36(4):443–448. doi: 10.1093/ageing/afm051.
    1. Schrijvers EM, Schürmann B, Koudstaal PJ, van den Bussche H, Van Duijn CM, Hentschel F, Heun R, Hofman A, Jessen F, Kölsch H. Genome-wide association study of vascular dementia. Stroke. 2012;43(2):315–319. doi: 10.1161/STROKEAHA.111.628768.
    1. Chapman J, Wang N, Treves TA, Korczyn AD, Bornstein NM. ACE, MTHFR, factor V Leiden, and APOE polymorphisms in patients with vascular and Alzheimer’s dementia. Stroke. 1998;29(7):1401–1404. doi: 10.1161/01.STR.29.7.1401.
    1. Bertram L, Lill CM, Tanzi RE. The genetics of Alzheimer disease: back to the future. Neuron. 2010;68(2):270–281. doi: 10.1016/j.neuron.2010.10.013.
    1. Hackett ML, Yapa C, Parag V, Anderson CS. Frequency of depression after stroke: a systematic review of observational studies. Stroke. 2005;36(6):1330–1340. doi: 10.1161/01.STR.0000165928.19135.35.
    1. Hackett ML, Köhler S, T O'Brien J, Mead GE. Neuropsychiatric outcomes of stroke. Lancet Neurol. 2014;13(5):525–534. doi: 10.1016/S1474-4422(14)70016-X.
    1. Hama S, Yamashita H, Shigenobu M, Watanabe A, Hiramoto K, Kurisu K, Yamawaki S, Kitaoka T. Depression or apathy and functional recovery after stroke. Int J Geriatr Psychiatry. 2007;22(10):1046–1051. doi: 10.1002/gps.1866.
    1. Köhler S, Verhey F, Weyerer S, Wiese B, Heser K, Wagner M, Pentzek M, Fuchs A, Köhler M, Bachmann C. Depression, non-fatal stroke and all-cause mortality in old age: a prospective cohort study of primary care patients. J Affect Disord. 2013;150(1):63–69. doi: 10.1016/j.jad.2013.02.020.
    1. Bartoli F, Lillia N, Lax A, Crocamo C, Mantero V, Carrà G, Agostoni E, Clerici M. Depression after stroke and risk of mortality: a systematic review and meta-analysis. Stroke Res Treat. 2013;2013:862978–862988.
    1. Carson AJ, MacHale S, Allen K, Lawrie SM, Dennis M, House A, Sharpe M. Depression after stroke and lesion location: a systematic review. Lancet. 2000;356(9224):122–126. doi: 10.1016/S0140-6736(00)02448-X.
    1. Vataja R, Pohjasvaara T, Mäntylä R, Ylikoski R, Leskelä M, Kalska H, Hietanen M, Aronen HJ, Salonen O, Kaste M. Depression–executive dysfunction syndrome in stroke patients. Am J Geriatr Psychiatry. 2005;13(2):99–107.
    1. Taylor-Piliae RE, Hepworth JT, Coull BM. Predictors of depressive symptoms among community-dwelling stroke survivors. J Cardiovasc Nurs. 2013;28(5):460–467. doi: 10.1097/JCN.0b013e318258ad57.
    1. van Mierlo ML, van Heugten CM, Post MW, de Kort PL, Visser-Meily JM. Psychological factors determine depressive symptomatology after stroke. Arch Phys Med Rehabil. 2015;96(6):1064–70. doi: 10.1016/j.apmr.2015.01.022.
    1. Neubauer H, Petrak F, Zahn D, Pepinghege F, Hägele A-K, Pirkl P-A, Uhl I, Juckel G, Mügge A, Herpertz S. Newly diagnosed depression is associated with increased beta-thromboglobulin levels and increased expression of platelet activation markers and platelet derived CD40-CD40L. J Psychiatr Res. 2013;47(7):865–871. doi: 10.1016/j.jpsychires.2013.03.011.
    1. Howren MB, Lamkin DM, Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med. 2009;71(2):171–186. doi: 10.1097/PSY.0b013e3181907c1b.
    1. Tuglu C, Kara SH, Caliyurt O, Vardar E, Abay E. Increased serum tumor necrosis factor-alpha levels and treatment response in major depressive disorder. Psychopharmacology. 2003;170(4):429–433. doi: 10.1007/s00213-003-1566-z.
    1. Tang C-Z, Zhang Y-L, Wang W-S, Li W-G, Shi J-P: Elevated serum levels of neopterin at admission predicts depression after acute ischemic stroke: a 6-month follow-up study. Mol Neurobiol. 2015:1–11. doi:10.1007/s12035-015-9220-4.
    1. Lespérance F, Frasure-Smith N, Théroux P, Irwin M. The association between major depression and levels of soluble intercellular adhesion molecule 1, interleukin-6, and C-reactive protein in patients with recent acute coronary syndromes. Am J Psychiatr. 2004;161(2):271–277. doi: 10.1176/appi.ajp.161.2.271.
    1. Schaefer M, Horn M, Schmidt F, Schmid-Wendtner MH, Volkenandt M, Ackenheil M, Mueller N, Schwarz MJ. Correlation between sICAM-1 and depressive symptoms during adjuvant treatment of melanoma with interferon-α. Brain Behav Immun. 2004;18(6):555–562. doi: 10.1016/j.bbi.2004.02.002.
    1. Motivala SJ, Sarfatti A, Olmos L, Irwin MR. Inflammatory markers and sleep disturbance in major depression. Psychosom Med. 2005;67(2):187–194. doi: 10.1097/01.psy.0000149259.72488.09.
    1. Dimopoulos N, Piperi C, Salonicioti A, Mitsonis C, Liappas I, Lea RW, Kalofoutis A. Elevation of plasma concentration of adhesion molecules in late‐life depression. Int J Geriatr Psychiatry. 2006;21(10):965–971. doi: 10.1002/gps.1592.
    1. Zhan Y, Yang Y-T, You H-M, Cao D, Liu C-Y, Zhou C-J, Wang Z-Y, Bai S-J, Mu J, Wu B. Plasma-based proteomics reveals lipid metabolic and immunoregulatory dysregulation in post-stroke depression. Eur Psychiatry. 2014;29(5):307–315. doi: 10.1016/j.eurpsy.2014.03.004.
    1. Folstein M, Liu T, Peter I, Buel J, Arsenault L, Scott T, Qiu WW. The homocysteine hypothesis of depression. Am J Psychiatr. 2007;164(6):861–867. doi: 10.1176/ajp.2007.164.6.861.
    1. Bottiglieri T, Laundy M, Crellin R, Toone BK, Carney MW, Reynolds EH. Homocysteine, folate, methylation, and monoamine metabolism in depression. J Neurol Neurosurg Psychiatry. 2000;69(2):228–232. doi: 10.1136/jnnp.69.2.228.
    1. Marin RS. Differential diagnosis and classification of apathy. Am J Psychiatry. 1990;147(1):22–30. doi: 10.1176/ajp.147.1.22.
    1. Roth RM, Flashman LA, McAllister TW. Apathy and its treatment. Curr Treat Options Neurol. 2007;9(5):363–370. doi: 10.1007/s11940-007-0022-5.
    1. Withall A, Brodaty H, Altendorf A, Sachdev PS. A longitudinal study examining the independence of apathy and depression after stroke: the Sydney Stroke Study. Int Psychogeriatr. 2011;23(02):264–273. doi: 10.1017/S1041610209991116.
    1. Marin RS. Apathy: a neuropsychiatric syndrome. J Neuropsychiatry Clin Neurosci. 1991;3(3):243–254. doi: 10.1176/jnp.3.3.243.
    1. Brodaty H, Sachdev P, Withall A, Altendorf A, Valenzuela M, Lorentz L. Frequency and clinical, neuropsychological and neuroimaging correlates of apathy following stroke: the Sydney Stroke Study. Psychol Med. 2005;35(12):1707–1716. doi: 10.1017/S0033291705006173.
    1. Hama S, Yamashita H, Shigenobu M, Watanabe A, Kurisu K, Yamawaki S, Kitaoka T. Post-stroke affective or apathetic depression and lesion location: left frontal lobe and bilateral basal ganglia. Eur Arch Psychiatry Clin Neurosci. 2007;257(3):149–152. doi: 10.1007/s00406-006-0698-7.
    1. Caeiro L, Ferro J, Figueira M. Apathy in acute stroke patients. Eur J Neurol. 2012;19(2):291–297. doi: 10.1111/j.1468-1331.2011.03508.x.
    1. Andersson S, Krogstad J, Finset A. Apathy and depressed mood in acquired brain damage: relationship to lesion localization and psychophysiological reactivity. Psychol Med. 1999;29(2):447–456. doi: 10.1017/S0033291798008046.
    1. Okada K, Kobayashi S, Yamagata S, Takahashi K, Yamaguchi S. Poststroke apathy and regional cerebral blood flow. Stroke. 1997;28(12):2437–2441. doi: 10.1161/01.STR.28.12.2437.
    1. Mayo NE, Fellows LK, Scott SC, Cameron J, Wood-Dauphinee S. A longitudinal view of apathy and its impact after stroke. Stroke. 2009;40(10):3299–3307. doi: 10.1161/STROKEAHA.109.554410.
    1. APA . Diagnostic and Statistical Manual of Mental Disorders. 5. Arlington: American Psychiatric Publishing; 2013.
    1. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease Report of the NINCDS‐ADRDA Work Group* under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34(7):939–939. doi: 10.1212/WNL.34.7.939.
    1. Román GC, Tatemichi TK, Erkinjuntti T, Cummings J, Masdeu J, Garcia J, Amaducci L, Orgogozo J-M, Brun A, Hofman A, et al. Vascular dementia Diagnostic criteria for research studies: Report of the NINDS‐AIREN International Workshop*. Neurology. 1993;43(2):250–250. doi: 10.1212/WNL.43.2.250.
    1. Jorm A. A short form of the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): development and cross-validation. Psychol Med. 1994;24(1):145–153. doi: 10.1017/S003329170002691X.
    1. Nys G, Van Zandvoort M, De Kort P, Jansen B, De Haan E, Kappelle L. Cognitive disorders in acute stroke: prevalence and clinical determinants. Cerebrovasc Dis. 2007;23(5–6):408–416. doi: 10.1159/000101464.
    1. Overbeek I, Schruers K, Griez E. Mini international neuropsychiatric interview: Nederlandse versie 5.0.0. DSM-IV [Dutch version] Maastricht. The Netherlands: Universiteit Maastricht; 1999.
    1. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134(4):382–389. doi: 10.1192/bjp.134.4.382.
    1. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–370. doi: 10.1111/j.1600-0447.1983.tb09716.x.
    1. Kang H-J, Stewart R, Kim J-M, Jang J-E, Kim S-Y, Bae K-Y, Kim S-W, Shin I-S, Park M-S, Cho K-H, et al. Comparative validity of depression assessment scales for screening poststroke depression. J Affect Disord. 2013;147(1–3):186–191. doi: 10.1016/j.jad.2012.10.035.
    1. Marin RS, Biedrzycki RC, Firinciogullari S. Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res. 1991;38(2):143–162. doi: 10.1016/0165-1781(91)90040-V.
    1. Clarke DE, Ko JY, Kuhl EA, van Reekum R, Salvador R, Marin RS. Are the available apathy measures reliable and valid? A review of the psychometric evidence. J Psychosom Res. 2011;70(1):73–97. doi: 10.1016/j.jpsychores.2010.01.012.
    1. Cummings JL. The Neuropsychiatric Inventory Assessing psychopathology in dementia patients. Neurology. 1997;48(5 Suppl 6):10S–16S. doi: 10.1212/WNL.48.5_Suppl_6.10S.
    1. Aalten P, de Vugt ME, Jaspers N, Jolles J, Verhey FR. The course of neuropsychiatric symptoms in dementia. Part I: findings from the two-year longitudinal Maasbed study. Int J Geriatr Psychiatry. 2005;20(6):523–530. doi: 10.1002/gps.1316.
    1. Kat MG, De Jonghe JF, Aalten P, Kalisvaart C, Dröes R-M, Verhey FR. Neuropsychiatric symptoms of dementia: psychometric aspects of the Dutch version of the Neuropsychiatric Inventory (NPI) Tijdschift voor Gerontologie en Geriatrie. 2002;33:150–155.
    1. Cummings J, McPherson S. Neuropsychiatric assessment of Alzheimer’s disease and related dementias. Aging Clin Exp Res. 2001;13(3):240–246. doi: 10.1007/BF03351482.
    1. Herlofson K, Larsen JP. Measuring fatigue in patients with Parkinson's disease: the fatigue severity scale. Eur J Neurol. 2002;9(6):595–600. doi: 10.1046/j.1468-1331.2002.00444.x.
    1. Mahoney FI. Functional evaluation: the Barthel index. Md State Med J. 1965;14:61–65.
    1. Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179–186. doi: 10.1093/geront/9.3_Part_1.179.
    1. Post MW, Boosman H, Van Zandvoort MM, Passier PE, Rinkel GJ, Visser-Meily JM. Development and validation of a short version of the Stroke Specific Quality of Life Scale. J Neurol Neurosurg Psychiatry. 2011;82(3):283–286. doi: 10.1136/jnnp.2009.196394.
    1. Costa PT, McCrae RR. The NEO personality inventory: manual, form S and form R. Odessa: Psychological Assessment Resources; 1985.
    1. Aalten P, Ramakers IH, Biessels GJ, de Deyn PP, Koek HL, OldeRikkert MG, Oleksik AM, Richard E, Smits LL, van Swieten JC. The Dutch Parelsnoer Institute-Neurodegenerative diseases; methods, design and baseline results. BMC Neurol. 2014;14(1):254–261. doi: 10.1186/s12883-014-0254-4.
    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. Am J Neuroradiol. 1987;8(3):421–426.
    1. de Boer R, Vrooman HA, van der Lijn F, Vernooij MW, Ikram MA, van der Lugt A, Breteler MM, Niessen WJ. White matter lesion extension to automatic brain tissue segmentation on MRI. Neuroimage. 2009;45(4):1151–1161. doi: 10.1016/j.neuroimage.2009.01.011.
    1. Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein H, Vermersch P, Kuiper M, Steinling M, Wolters EC, Valk J. Atrophy of medial temporal lobes on MRI in “probable” Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry. 1992;55(10):967–972. doi: 10.1136/jnnp.55.10.967.
    1. Wolz R, Aljabar P, Hajnal JV, Hammers A, Rueckert D. LEAP: learning embeddings for atlas propagation. NeuroImage. 2010;49(2):1316–1325. doi: 10.1016/j.neuroimage.2009.09.069.
    1. Wolz R, Schwarz AJ, Yu P, Cole PE, Rueckert D, Jack CR, Raunig D, Hill D. Robustness of automated hippocampal volumetry across magnetic resonance field strengths and repeat images. Alzheimers Dement. 2014;10(4):430–438. doi: 10.1016/j.jalz.2013.09.014.
    1. Carmena R, Duriez P, Fruchart J-C. Atherogenic lipoprotein particles in atherosclerosis. Circulation. 2004;109(23):III-2–III-7.
    1. Antonios N, Angiolillo DJ, Silliman S. Hypertriglyceridemia and ischemic stroke. Eur Neurol. 2008;60(6):269–278. doi: 10.1159/000157880.
    1. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA. 2002;287(19):2570–2581. doi: 10.1001/jama.287.19.2570.
    1. Rasquin S, Verhey F, Van Oostenbrugge R, Lousberg R, Lodder J. Demographic and CT scan features related to cognitive impairment in the first year after stroke. J Neurol Neurosurg Psychiatry. 2004;75(11):1562–1567. doi: 10.1136/jnnp.2003.024190.
    1. Bour A, Rasquin S, Aben I, Boreas A, Limburg M, Verhey F. A one-year follow-up study into the course of depression after stroke. J Nutr Health Aging. 2010;14(6):488–493. doi: 10.1007/s12603-010-0033-x.
    1. Arauz A, Rodríguez-Agudelo Y, Sosa AL, Chávez M, Paz F, González M, Coral J, Díaz-Olavarrieta C, Román GC. Vascular cognitive disorders and depression after first-ever stroke: the fogarty-Mexico stroke cohort. Cerebrovasc Dis. 2014;38(4):284–289. doi: 10.1159/000366471.
    1. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–198. doi: 10.1016/0022-3956(75)90026-6.
    1. Rey A. L'examen clinique en psychologie. Oxford England: Presses Universitaries De France; 1958.
    1. Wechsler D. Wechsler Memory Scale - 3rd edition: Administration and Scoring Manual. San Antonio: The Psychological Corporation; 1997.
    1. Reitan RM. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills. 1958;8(3):271–276. doi: 10.2466/pms.1958.8.3.271.
    1. Wilson BA, Alderman N, Burgess PW, Emslie H, Evans JJ. Behavioural assessment of the dysexecutive syndrome (BADS) J Occup Psychol Employ Disabil. 2003;5(2):33–37.
    1. Lezak MD. Neuropsychological assessment. 3. New York: Oxford University Press; 1995.
    1. Halligan P, Marshall J, Wade D. Visuospatial neglect: underlying factors and test sensitivity. Lancet. 1989;334(8668):908–911. doi: 10.1016/S0140-6736(89)91561-4.
    1. Schmand BA, Bakker D, Saan RJ, Louman J: De Nederlandse Leestest voor Volwassenen: een maat voor het premorbide intelligentieniveau. Tijdschr Gerontol Geriatr. 1991:127–138.
    1. Kaplan E, Goodglass H, Weintraub S. The Boston naming test. 2. Philadelphia: Lea & Febiger; 1983.

Source: PubMed

3
Abonnere