Cognitive dysfunctions associated with white matter damage due to cardiovascular burden – determinants and interpretations

• Authors: Paweł Krukow
• Languages of publication: EN

Abstracts

EN

Although considerable research has been devoted to cognitive functions deteriorating due to diseases of cardiovascular system, rather less attention has been paid to their theoretical background. Progressive vascular disorders as hypertension, atherosclerosis and carotid artery stenosis generate most of all pathological changes in the white matter, that cause specific cognitive disorder: disconnection syndromes, and disturbances in the dynamic aspect of information processing. These features made neuropsychological disorders secondary to cardiovascular diseases different than the effects of cerebral cortex damage, which may be interpreted modularly.

Keywords

EN

hypertension; atherosclerosis; white matter; cognitive processing speed; neural networks

• Publisher: Committee for Psychological Sciences, Polish Academy of Sciences
• Journal: Polish Psychological Bulletin
• Year: 2014
• Volume: 45
• Issue: 3
• Pages: 334-345

Dates

published

2014-09-01

online

2014-09-09

Contributors

author

Paweł Krukow

• Department of Clinical Neuropsychiatry, Chair and Department of Psychiatry, I Faculty of Medicine, Medical University of Lublin, ul. Głuska 1, 20-439 Lublin, Poland;

References

• Albert M. (1993). Neuropsychological and neurophysiological changes in healthy adult humans across the age range. Neurobiology of Aging, 14, 623-625.[Crossref]
• Albert M. (2005). Subcortical dementia: Historical review and personal view. Neurocase, 11, 243-245.[Crossref][PubMed]
• Albert M., Feldman R., Willis A. (1974). The ‘subcortical dementia’ of progressive supranuclear palsy. Journal of Neurology, Neurosurgery and Psychiatry, 37, 121-130.[Crossref]
• Armstrong C.L., Morrow L. (ed.). (2010). Handbook of Medical Neuropsychology. Applications of Cognitive Neuroscience. NY, Springer.
• Bartzokis G., Lu P.H., Mendez M.F., Richard A., Peters D.G., Oluwadara B., Barrall K.A., Finn J.P., Villablanca P., Thompson P.M., Mintz K. (2010). Lifespan trajectory of myelin integrity and maximum motor speed. Neurobiology of Aging, 31 (9), 1554-1562.[Crossref]
• Bartzokis, G., Cummings, J.L., Sultzer, D., Henderson, V.W., Nuechterlein, K.H., Mintz, J. (2003). White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Archives of Neurology, 60, 393-398.[Crossref]
• Bartzokis, G., Sultzer, D., Lu, P.H., Nuechterlein, K.H., Mintz, J., Cummings, J. (2004). Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical “Disconnection” in aging and Alzheimer’s disease. Neurobiology of Aging, 25, 843-851.[Crossref]
• Biechowska D., Harciarek M., Kurdelska M., Kozera G. (2007). Charakterystyka neuropsychologiczna osób z grupy podwyższonego ryzyka chorób naczyniowych mózgu (pp. 127-131). In: G. Chojnacka- Szawłowska, B. Pastwa-Wojciechowska (ed.), Kliniczne i sądowopenitencjarne aspekty funkcjonowania człowieka. Kraków, Oficyna Wydawnicza Impuls.
• Boatman D. (2004). Cortical bases of speech perception: evidence from functional lesion studies. Cognition, 92, 47-65.[PubMed][Crossref]
• Bowler J.V., Hachinski V.C. (1995). Vascular cognitive impairment: a new approach to vascular dementia (pp. 357-376). In: V.C. Hachinski (ed.), Cerebrovascular disease. Vol 4. London: Baillière Tindall.
• Brickman A.M., Zimmerman M.E., Paul R.H., Grieve S.M., Tate D.F., Cohen R.A., Williams L.M., Clark R., Gordon E.(2006). Regional white matter and neuropsychological functioning across the adult lifespan. Biological Psychiatry, 60, 444-453.[PubMed][Crossref]
• Brown J., Tomaszewski W. (2012). Microgenetic approach to thought and memory. Acta Neuropsychologica, 10 (1), 1 - 23.[Crossref]
• Burgmans S., Groneschild E.H.B.M., Fandakova Y., Shing Y.L., van Boxtel M.P.J., Vuurman E.F.P.M., Uylings H.B.M., Jollez J., Raz N. (2011). Age differences in speed of processing are partially mediated by differences in axonal integrity. NeuroImage, 55, 1287-1297.[Crossref][PubMed]
• Catani M., ffytche D.H. (2005). The rises and falls of disconnection syndromes. Brain, 128, 2224-2239.[PubMed][Crossref]
• Catani M., Thiebaut de Schotten M. (2012). Atlas of Human Brain Connections. New York, Oxford University Press.
• Cohen R.A. (2011). Neuroimaging of Cardiovascular Disease (pp. 215-256). In: R.A. Cohen, L.H. Sweets (ed.), Brain Imaging in Behavioral Medicine and Clinical Neuroscience. NY, Springer Science + Business Media.
• Cohen R.A., Paul R.H., Ott B.R. (2002). The relationship of subcortical MRI hyperintensities and brain volume to cognitive function in vascular dementia. Journal of INS, 8, 743-752.
• Cook I,A., Leuchter A.F., Morgan M. (2002). Cognitive and physiological correlates of subclinical structural brain disease in elderly healthy control subjects. Archives of Neurology, 59, 1612-1620.
• Cummings J.(1990). Subcortical dementia. New York, Oxford University Press.
• Cummings J., Benson F. (1984). Subcortical dementia: review of an emerging concept. Archives of Neurology, 41, 874-879.[Crossref]
• Cupples L.A., D’Agostino R.B., Kiely D. (1987). The Framingham Study. An Epidemiological Investigation of Cardiovascular Disease, Section 34. Some Risk Factors Related to the Annual Incidence of Cardiovascular Disease and Death Using Pooled Repeated Biennial Measurements Framingham Heart Study, 30 Year Follow-up. Bethesda, MD, National Heart, Lung, and Blood Institute.
• Damasio H., Tranel D., Grabowski T., Adolphs R., Damasio A. (2004). Neural systems behind word and concept retrieval. Cognition, 92, 179-229. de Groot J.C., de Leeuw F.E., Oudkerk M., van Gijn J., Hofman A., Jolles J., Breteler M.M. (2000). Cerebral white matter lesions and cognitive function: the Rotterdam Scan Study. Annuals of Neurology, 47, 145-51.[Crossref]
• Debette S., Markus H.S. (2010). The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ, 341, C3666.
• DeCarli C., Massaro J., Harvey D., Hald J., Tullberg M., Au R. (2005). Measures of brain morphology and infarction in the Framingham heart study: establishing what is normal. Neurobiology of Aging, 26, 491-510.[Crossref]
• Desmond D.W. (2004). The neuropsychology of vascular cognitive impairment: is there a specific cognitive deficit? Journal of the Neurological Sciences, 226, 3-7.
• Devasenapathy A., Hachinski V.C. (2000). Vascular Cognitive Impairment. Curr Treat Options Neurol, 2, 61-72.[PubMed]
• Dinnen R.A., Vilisaar J., Hlinka J., Bradshaw C.M., Morgan P.S., Constantinescu C.S., Auer D.P. (2008). Disconnection as mechanism for cognitive disfunction in multiple sclerosis. Brain, 132, 239-249.
• Duering M., Gonik M., Malik R., Zieren N., Reyes S., Jouvent E., Harve D., Gschwendtner A., Opherk C., Chabriat H., Dichgans M. (2013). Identification of a strategic brain network underlying processing speed deficits in vascular cognitive impairment. NeuroImage, 66, 177-183.[Crossref][PubMed]
• Duering M., Zieren N., Harve D., Jouvent E., Reyes S., Peters N., Pachai C., Opherk C., Chabriat H., Dichgans M. (2011). Strategic role of frontal white matter tracts in vascular cognitive impairment: a voxelbased lesion-symptom mapping study in CADASIL. Brain, 134, 2366-2375.
• Engel A.K., Fries P., Singer W. (2001). Dynamic predictions: oscillations and synchrony in top-down processing. Nature Reviews Neuroscience, 2, 704-716.[PubMed][Crossref]
• Felts P.A., Baker T.A., Smith K.J. (1997). Conduction in Segmentally Demyelinated Mammalian Central Axons. Journal of Neuroscience, 17 (19), 7267-77.
• Filley C.M. (2001). The Behavioral Neurology of White Matter. New York, Oxford University Press.
• Filley C.M. (2010). White Matter : Organization and Functional Relevance. Neuropsychology Review, 20, 158-173.[Crossref][PubMed]
• Filley C.M., Franklin G.M., Heaton R.K., Rosenberg N.L. (1988). White matter dementia. Clinical disorders and implications. Neuropsychiatry Neuropsychol Behav Neurol, 1, 239-254.
• Fowkes F.G.R., Housley E., Riemersma R.A. (1992). Smoking, lipids, glucose-intolerance, and blood pressure as risk factors for peripheral atherosclerosis compared with ischemic heart disease in the Edinburgh Artery Study. American Journal of Epidemiology, 135, 331-340.
• Geschwind N. (1965a). Disconnection syndromes in animals and man. I. Brain, 88, 237-294.[Crossref]
• Geschwind N. (1965b). Disconnection syndromes in animals and man. II. Brain, 88, 585-644.[Crossref]
• Graham I., Atar D., Borch-Johnsen K., Boysen G., Burell G., Cifkova R., Dallongeville J., de Backer G., Ebrahim S., Gjelsvik B., Herrmann- Lingen C., Hoes A., Humphries S., Knapton M., Perk J., Priori S.G., Pyorala K., Reiner Z., Ruilope L., Sans-Menendez S., Opreimer W.S., Weissberg P., Wood D., Yarnell J., Zamorano J.L. (2007). European guidelines on cardiovascular disease prevention in clinical practice: executive summary. Atherosclerosis, 194, 1-45.
• Gutierrez R., Boison D., Heinemann U., Stoffel W. (2005). Decompaction of CNS myelin leads to a reduction of the conduction velocity of action potentials in optic nerve. Neuroscience Letters, 195, 93-96.
• Hachinski V.C. (1994). Vascular Dementia: A radical redefinition. Dementia, 5, 130-132.[PubMed]
• Haines D.E. (2002). Neuroanatomy: An atlas of structures, sections, and systems. NY / Philadelphia, Lippincott Williams & Wilkins.
• Harciarek M., Biedunkiewicz B., Lichodziejewska-Niemierko M., DębskaŚlizień A., Rutkowski B. (2011). Cognition one year following a successful Kidney transplant: A longitudinal comparison with adequately dialyzed patients and matched controls without chronic kidney disease. Kidney International, 79, 1353-1360.[Crossref]
• Herzyk A. (1996). Nieświadomość zaburzeń zachowania w uszkodzeniach mózgu (pp. 175-204). In: A. Herzyk, D. Kądzielawa (ed.), Zaburzenia w funkcjonowaniu człowieka z perspektywy neuropsychologii klinicznej. Lublin, Wyd. UMCS.
• Herzyk A. (1999). Anozognozja. Mechanizmy mózgowe i objawy. Przegląd Psychologiczny, 42, 99-110.
• Herzyk A. (2002). Dysocjacja wiedzy świadomej i nieświadomej w różnych formach zaburzeń neuropsychologicznych (pp. 61-87). In: A. Herzyk, D. Kądzielawa (ed.), Zaburzenia w funkcjonowaniu człowieka z perspektywy neuropsychologii klinicznej. Lublin, Wyd.
• UMCS Herzyk A. (2011). Neuropsychologia kliniczna wobec zjawisk świadomości i nieświadomości. Warszawa, Wyd. PWN.
• Iskra T. (2007). Unaczynienie mózgowia (pp. 3-25). In: A. Szczudlik, A. Członkowska, H. Kwieciński, A. Słowik (ed.), Udar mózgu. Kraków, Wyd. UJ.
• Jodzio K. (2008). Problemy neuropsychologiczne w praktyce kardiologicznej i kardiochirurgicznej. In: K. Jodzio, W. Nyka (ed.), Neuropsychologia medyczna. Wybrane zagadnienia. Wyd. Arche, Sopot.
• Jodzio K. (2011). Diagnostyka neuropsychologiczna w praktyce klinicznej. Warszawa, Wyd. Difin.
• Jodzio K., Drumm D.A. (2001). Cognitive disorders subsequent to ischemic heart disease from the physiotherapeutic perspective. Fizjoterapia Polska, 1, 117-122.
• Johnstone S.C., O’Meara E.S. Manolio T.A., Lefkowitz D., O’Leary D., Goldstein S., Carlson M.C., Fried L.P., Longstreth W.T. (2004). Cognitive impairment and decline are associated with carotid artery disease in patients without clinically evident cerebrovascular disease. Annual of Internal Medicine,140, 237-247.
• Kadykov A.S., Manvelov L.S., Shahparonova N.V. (2006). Хронические сосудистые заболевания головного мозга [Chronic vascular brain diseases]. Москва [Moscow], ГЭОТАР-Медиа.
• Kaźmierski R. (2011). Badanie ultrasonograficzne tętnic szyjnych w odcinku zewnątrzczaszkowym (pp. 45-105). In: R. Kaźmierski (ed.), Podręcznik diagnostyki ultrasonograficznej w neurologii. Lublin, Wyd. Czelej.
• Kearney P.M, Whelton M., Reynolds K., Muntner P., Whelton P.K., He J. (2005). Global burden of hypertension: analysis of worldwide data. Lancet, 365, 217-223.
• Kim J.E., Lee B.R., Chun J.E., Lee S.J., Lee B.H., Yu I.K., Kim SY. (2007). Cognitive dysfunction in 16 patients with carotid stenosis: Detailed neuropsychological findings. Journal of Clinical Neurology, 3, 9-17.[Crossref]
• Konorski J. (1967). Integracyjna działalność mózgu. Warszawa, PWN.
• Kropotov Y.,Mueller A. (2012). Neurophysiological basis of microgenesis theory: stages of visual information flow as reflected in functionally defined components of event related potentials in man. Acta Neuropsychologica, 10 (1), 25-33. Leuchter A.F., Cook I.A., [Crossref]
• Lufkin R.B., Dunkin J., Newton T.F., Cummings J.L., Mackey J.K., Walter D.O. (1994). Cordance: a new method for assessment of cerebral perfusion and metabolism using quantitative electroencephalography. NeuroImage, 1, 208-219.[PubMed]
• Liang M., Zhou Y., Jiang T., Liu Z., Tian L., Liu H., Hao Y. (2006). Widespread functional disconnectivity in schizophrenia with restingstate functional magnetic resonance imaging. NeuroReport, 17, 209-213.[Crossref]
• Liao D., Cooper L., Cai J., Toole J.F., Bryan N.R., Hutchinson R.G., Tyroler H.A. (1996). Presence and severity of cerebral white matter lesions and hypertension, its treatment, and its control. Atherosclerosis Risk in Communities Study. Stroke, 27, 2262-2270.[Crossref][PubMed]
• Libon D.J., Barker W.W., Loewenstein D.A., Crum T.A. (2004). Conversion to dementia among two groups with cognitive impairment. Dementia and Geriatric Cognitive Disorders, 20, 45-51.
• Libon D.J., Bogdanoff B., Cloud B.S., Skalina S., Carew T.G., Gitlin H.L. (1998). Motor learning and qualitative measures of the hippocampus and subcortical white alternetions in Alzheimer’s disease and ischemic vascular dementia. Journal of Clinical and Experimental Neuropsychology, 20, 30-41.[Crossref]
• Libon D.J., Price C.C., Swenson R.A., Penney D., Haake B., Pennisi A. (2009). Vascular Cognitive Impairment (pp. 75-86). In: J.R. Festa, R.M. Lazar (ed.), Neurovascular Neuropsychology. NY, Springer Science + Business Media.
• Lim Ch., Alexander M. (2009). Cardiac Arrest (pp. 135-156). In: J.R. Festa, R.M. Lazar (ed.), Neurovascular Neuropsychology. NY, Springer Science + Business Media.
• Longstreth W. Jr, Manolio T.A., Arnold A. (1996). Clinical correlates of white matter findings on cranial magnetic resonanceimaging of 3301 elderly people. The Cardiovascular Health Study. Stroke, 27, 1274-1282.[PubMed][Crossref]
• Markowitsch H.J. (1995). Which brain regions are critically involved in the retrieval of old episodic memory? Brain Res Rev, 21, 117-127.[Crossref]
• Marquine M.J., Attix D.K., Goldstein L.B., Samsa G.P., Payne M.E., Chelune G.J., Steffens D.C. (2010). Differential patterns of cognitive decline in anterior and posterior white matter hyperintensity progression. Stroke, 41, 1946-1950.[PubMed][Crossref]
• Mathiasen E.B., Waterloo K., Joakimsen O., Bakke S.J., Jacobsen E.A., Bonaa K.H. (2004). Reduced neuropsychological test performance in asymptomatic carotid stenosis - The Tromso Study. Neurology, 62, 695-701.[Crossref]
• Mesulam M.M. (1998). From sensation to cognition. Brain, 121, 1013-1052.
• Mesulam M.M. (1999). Neuroplasticity failure in Alzheimer’s disease: Bridging the gap between plaques and tangles. Neuron, 24, 521-529.[Crossref][PubMed]
• Monolio T.A., Olson J., Longstreth W.T. (2003). Hypertension and Cognitive Function: Pathophysiologic Effects of Hypertension on the Brain. Current Hypertension Reports, 5, 255-261.[Crossref]
• Naruszewicz M. (2003). Patogeneza miażdżycy, nowe koncepcje w świetle badań podstawowych i klinicznych (pp. 26-37). In: M. Dłużniewski, A. Mamcarz, P. Krzyżak (ed.), Kardiologia praktyczna. T. III: Choroba niedokrwienna serca. Warszawa, Wyd. AM.
• Ojeda N., Peña J., SchretlenD.J., Sánchez P., Aretouli E., Elizagárate E., Ezcurra J., Gutiérrez M. (2012). Hierarchical structure of the cognitive processes in schizophrenia: the fundamental role of processing speed. Schizophrenia Research, 135, 72-78.
• Pantoni L., Garcia J.H. (1995). The Significance of Cerebral White Matter Abnormalities 100 Years After Binswanger’s Report. A review. Stroke, 26, 1293-1301.[Crossref]
• Pantoni L., Garcia J.K. (1997). Pathogenesis of leukoaraiosis: A review. Stroke, 28, 652-659.[PubMed][Crossref]
• Plaut D.C. (1996). Relearning after damage in connectionist networks: Toward a theory of rehabilitation. Physiology and Behavior, 79, 487-493.
• Price C.C., Jefferson A.L., Merino J.G. (2005). Subcortical vascular dementia: integrating neuropsychological and neuroradiologic data. Neurology, 65, 376-382.[Crossref][PubMed]
• Rao R. (2002). The role of carotid stenosis in vascular cognitive impairment. Journal of Neurological Science, 15, 103-107.[Crossref]
• Raz N., Gunning F.M, Head D., Dupuis J.H., McQuain J., Briggs S.D. (1997). Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cerebral Cortex, 7, 268-282.[Crossref]
• Reed B.R., Eberling J.L., Mungas D., Weiner M., Kramer J.H., Jagust W.J. (2004). Effects of white matter lesions and lacunes on cortical function. Archives of Neurology, 61,1545-1550.[Crossref]
• Reijmer Y.D., Brundel M., Bresser J., Kappelle J., Leemans A., Biessels G.J. (2013). Microstructural White Matter Abnormalities and Cognitive Functioning in Type 2 Diabetes. A Diffusion Tensor Imaging Study. Diabetes Care, 36, 137-144.[PubMed]
• Romero J.R., Beiser A., Seshadri S., Benjamin E.J., Polak J.F., Vasan R.S., Au R., DeCarli C., Wolf P.A. (2009). Carotid artery stherostenosis, MRI indices of brain ischemia, aging, and cognitive impairment: the Framingham study. Stroke, 40, 1590-1596.[PubMed][Crossref]
• Rosamond W., Flegal K., Furie K., Go A., Greenlund K., Haase N., Hailpern S.M., Ho M., Howard V., Kissela B., Kittner S., Lloyd-Jones D., McDermott M., Meigs J., Moy C., Nichol G., O’Donnell C., Roger V., Sorlie P., Steinberger J., Thom T., Wilson M., Hong Y., American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2008). Heart disease and stroke statistics--2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation, 117, 25-146
• Ross R. (1999). Atherosclerosis: an inflammatory disease. New England Journal of Medicine, 340, 115-126.
• Salat D.H., Buckner R.L., Snyder A.Z., Greve D.N., Desikan R.S., Busa E. (2004). Thinning of the cerebral cortex in aging. Cerebral Cortex, 14, 721-730.[Crossref]
• Sasson E., Doniger G.M., Pasternak O., Tarrasch R., Assaf Y. (2012).
• Structural correlates of cognitive domains in normal aging with diffusion tensor imaging. Brain Structures and Functions, 217, 503-515.
• Schmidt R., Fazekas F., Offenbacher H., (1993). Neuropsychologic correlates of MRI white matter hyperintensities: a study of 150 normal volunteers. Neurology, 43, 2490-2494.[Crossref]
• Schmitt A., Hasan A., Gruber O., Falkai P. (2011). Schizophrenia as a disorder of disconnectivity. Eur Arch Psychiatry Clin Neurosci, 261 (suppl), 150-154.
• Shallice T. (1988). From neuropsychology to mental structure. Cambridge, Cambridge University Press.
• Sierra C., Domenech M., Coca A. (2009). Brain damage in hypertension. Arch Med Sci, 5, 254-266.
• Silverstein A. (1959). Occlusive disease of the carotid arteries. Circulation, 20, 4-16.[PubMed][Crossref]
• Sinha K., Karimi-Abdolrezaee S., Velumian A.A., Fehlings M.G. (2006). Functional changes in genetically dysmyelinated spinal cord axons of shiverer mice: role of juxtaparanodal Kv1 family K+ channels. Journal of Neurophysiology, 95,1683-1695.
• Sporns O. (2012). Discovering the Human Connectcome. Cambridge, Massachusetts, The MIT Press.
• Stockert, F.G. (1932). Subcorticale demenz. Archives of Psychiatry, 97, 77-100.[Crossref]
• Tandon O.P., Joon M.K. (1997). Event related evoked potentials in hypertensive subjects. Indian J Physiol Pharrnacol, 41(1), 79-82.
• Tapp P.D., Siwak C.T., Gao F.Q., Chiou J.Y., Black S.E., Head E. (2004). Frontal lobe volume, function and beta-amyloid pathology in a canine model of aging. Journal of Neuroscience, 24, 8205-8213.[Crossref]
• Tarter R.E., Butters M., Beers S.R. (2001). Medical Neuropsychology. Second Edition. NY, Boston, Dordrecht, London, Moscow, Kluver Academic Press.
• Tolhurst D.J., Lewis P.R. (1992). Effect of myelination on the conduction velocity of optic nerve fibres. Ophthalmic Physiol Opt, 12, 241-243.
• Turken A.U., Whitfield-Gabrieli S., Bammer R., Baldo J., Dronkers N.F., Gabrieli J.D.E. (2008). Cognitive processing speed and the structure of white matter pathways: Convergent evidence from normal variation and lesion studies. NeuroImage, 42, 1032-1044.[Crossref][PubMed]
• Van den Heuvel D.M., ten Dam V.H., de Craen A.J. (2006). Increase in periventricular white matter hyperintensities parallels decline in mental processing speed in a non-demented elderly population. Journal of Neurology Neurosurgery and Psychiatry, 77, 149-153.
• Van Dijk K.R.A., Van Gerven P.W.M., Van Boxtel M.P.J., Van der Elst W., Jolles J. (2008). No Protective Effects of Education during Normal Cognitive Aging: Results from the 6-year follow-up of the Maastricht Aging Study (MAAS). Psychology and Aging, 23, 119-30.
• Waldstein S.R., Wendell C.R., Hosey M.M., Seliger S.L., Katzel L.I. (2010). Cardiovascular Disease and Neurocognitive Function (pp. 69-99). In: by C.L. Armstrong, L. Morrow (ed.), Handbook of Medical Neuropsychology. Ny, Springer Science + Business Media.
• Walecki J., Bulski T. (2007). Diagnostyka neuroradiologiczna zmian naczyniowych ośrodkowego układu nerwowego (pp. 119-174). In: A. Szczudlik, A. Członkowska, H. Kwieciński, A. Słowik (ed.), Udar mózgu. Kraków, Wyd. UJ.
• Wen W., Sachdev P. (2004). The topography of white matter hyperintensities on brain MRI in middle-aged individuals. NeuroImage, 22, 144-154.[PubMed][Crossref]
• Wojczal J. (2011). Badanie ultrasonograficzne tętnic wewnątrzczaszkowych metodą dupleks z kodowaniem przepływu w kolorze (pp. 197-213). In: R. Kaźmierski (ed.), Podręcznik diagnostyki ultrasonograficznej w neurologii. Lublin, Wyd. Czelej.
• Yoshita M., Fletcher E., DeCarli Ch. (2005). Current Concepts of Analysis of Cerebral White Matter Hyperintensities on Magnetic Resonance Imaging. Tomography and Magnetic Resonance Imaging, 16, 399-407.

Identifiers

DOI

10.2478/ppb-2014-0041