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Cognition and chronic hypoxia in pulmonary diseases

Cognição e hipóxia crônica em doenças pulmonares

Abstract

Lung disease with chronic hypoxia has been associated with cognitive impairment of the subcortical type. Objectives: To review the cognitive effects of chronic hypoxia in patients with lung disease and its pathophysiology in brain metabolism. Methods: A literature search of Pubmed data was performed. The words and expressions from the text subitems including "pathophysiology of brain hypoxia", "neuropsychology and hypoxia", "white matter injury and chronic hypoxia", for instance, were key words in a search of reports spanning from 1957 to 2009. Original articles were included. Results: According to national and international literature, patients with chronic obstructive pulmonary disease and sleep obstructive apnea syndrome perform worse on tests of attention, executive functions and mental speed. The severity of pulmonary disease correlates with degree of cognitive impairment. These findings support the diagnosis of subcortical type encephalopathy. Conclusion: Cognitive effects of clinical diseases are given limited importance in congresses and symposia about cognitive impairment and its etiology. Professionals that deal with patients presenting cognitive loss should be aware of the etiologies outlined above as a major cause or potential contributory factors, and of their implications for treatment adherence and quality of life.

Key words:
chronic hypoxia; brain; cognitive impairment; neuropsychological tests; encephalopathy of the subcortical type

Resumo

As doenças pulmonares que cursam com hipóxia crônica tem sido associadas à alteração cognitiva do tipo subcortical. Objetivo: Revisar os efeitos cognitivos da hipóxia crônica em pacientes com doenças pulmonar e sua fisiopatologia. Métodos: Foi utilizado o banco de dados do Pubmed. As palavras e expressões foram os temas dos subitens da revisão como, por exemplo, "fisiopatologia e hipóxia cerebral", "neuropsicologia e hipoxia", "lesões de substância branca e hipóxia crônica", variando de 1957 to 2009. Artigos originais foram incluídos. Resultados: De acordo com a literatura nacional e internacional, pacientes com doença pulmonar obstrutiva crônica e síndrome da apnéia obstrutiva do sono apresentam desempenho pior em testes neuropsicológicos que avaliam atenção, funções executivas e velocidade de processamento mental. Esses achados configuram uma encefalopatia do tipo subcortical. Conclusion: É dada importância limitada às conseqüências cognitivas das doenças clínicas em congressos e simpósios sobre cognição e suas etiologias. Profissionais que lidam com pacientes que apresentam perda cognitiva devem suspeitar das etiologias mencionadas acima com causa principal ou como co-fatores, assim com suas implicações na aderência ao tratamento e qualidade de vida.

Palavras-chave:
hipóxia crônica; cérebro; alteração cognitiva; testes neuropsicológicos; encefalopatia do tipo subcortical

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References

  • 1
    Blass JP, Gibson GE. Consequences of mild, graded hypoxia. Adv Neurol 1979;26:229-250.
  • 2
    Kirsch DB, Jozefowicz RF. Neurologic complications of respiratory disease. Neurol Clin 2002;20:247-264.
  • 3
    Freedmann BJ. Papilloedema, optic atrophy, and blindness due to emphysema and chronic bronchitis. Br J Ophthalmol 1963;47:290-294.
  • 4
    Tuder RM, Yun JH, Bhunia A, Fijalkowska I. Hypoxia and chronic lung disease. J Mol Med 2007;85:1317-1324.
  • 5
    Austen FK, Carmichael MW, Adams R. Neurologic manifestations of chronic pulmonary insufficiency. N Eng J Med 1957;257:579-90.
  • 6
    Kilburn K, Durham NC. Neurologic manifestations of respiratory failure. Arch Intern Med 1965;116:409-415.
  • 7
    Dulfano MJ, Ishikawa S. Hypercapnia: mental changes and extrapulmonary complications. An expanded concept of the "CO2 intoxication" syndrome. Ann Inter Med 1965;63:829-841.
  • 8
    Ackland GL, Noble R, Hanson MA. Red nucleus inhibits breathing during hypoxia in neonates. Respir Physiol 1997; 110:251-260.
  • 9
    Casanova C, Cote C, Marin JM, et al. Distance and oxygen desaturation during the 6-min walk test as predictors of long-term mortality in patients with COPD. Chest 2008; 134:746-752
  • 10
    Santos DB, Viegas CAA. Correlation of levels of obstruction in COPD with lactate and six-minute walk test. Rev Port Pneumol 2009;15:11-25.
  • 11
    Casanova C, Hernández MC, Sánchez A, et al. Twenty-four-hour ambulatory oximetry monitoring in COPD patients with moderate hypoxemia. Respir Care 2006;51:1416-1423.
  • 12
    Mueller P de T, Gomes MD, Viegas CA, Neder JA. Systemic effects of nocturnal hypoxemia in patients with chronic obstructive pulmonary disease without obstructive sleep apnea syndrome. J Bras Pneumol 2008;34:567-574
  • 13
    Zanchet RC, Viegas CA. Nocturnal desaturation: predictors and the effect on sleep patterns in patients with chronic obstructive pulmonary disease and concomitant mild daytime hypoxemia. J Bras Pneumol 2006;32:207-212.
  • 14
    Sum M-K, Reis DJ. Hypoxia selectively excites vasomotor neurons of rostral ventrolateral medulla in rats. Am J Physiol Regul Integr Comp Physiol 1994;266:245-256.
  • 15
    Horn EM, Waldrop TG. Oxygen-sensing neurons in the caudal hypothalamus and their role in cardiorespiratory control. Respir Physiol 1997;110:219-228.
  • 16
    Koos BJ, Chau A, Matsuura M, Punla O, and Kruger L. Thalamic locus mediates hypoxic inhibition of breathing in fetal sheep. J Neurophysiol 1998;79:2383-2393.
  • 17
    Solomon IC, Edelman NH, Neubauer JÁ. The pre-Botzinger complex functions as a central hypoxia chemoreceptor for respiration in vivo. J Neurophysiol 2000;83:2854-2868.
  • 18
    López-Barneo J, Pardal R, Ortega-Sáenz P. Cellular mechanism of oxygen sensing. Annu Rev Physiol 2001;63:259-287.
  • 19
    Neubauer JÁ. Physiological and pathophysiological responses to intermittent hypoxia. J Appl Physiol 2001;90:1593-1599.
  • 20
    Patel AJ, Honore E. Molecular physiology of oxygen-sensitive channels. Eur Respir J 2001;18:227-233.
  • 21
    Pollok JD, Kremplin M, Rudy B. Differential effects of NGF, FGH, EGF, c AMP and dexametasone on neurite outgrowth and sodium channel expression in PC12 cells. J Neurosci 1990;10:2626-2637.
  • 22
    Lesser SS, Lo DC. Regulation of voltage gated ion channels by NGF and cilliary neurotrophic factor in SK-N-SH75 neuroblastoma cells. J Neurosci 1995;15:153-161.
  • 23
    Nolan PC, Waldrop TG. In vitro responses of VLM neurons to hypoxia after normobaric hypoxic acclimatization. Respir Physiol 1996;105:23-33.
  • 24
    Xu K, LaManna JC. Chronic hypoxia and cerebral circulation. J Appl Physiol 2006;100:725-730.
  • 25
    Severinghaus JW, Chiodi H, Eger EL, Brandstater B, Hornbein TF. Cerebral blood flow in man at high altitude. Circ Res 1966;19:274-282.
  • 26
    Bongstrom L, Johansson H, Siesjo BK. The relationship between arterial PO2 and cerebral blood flow in hypoxic hypoxia. Acta Physioll Scand 1975;93:423-432.
  • 27
    Beck T, Krieglstein J. Cerebral circulation, metabolism and blood-brain barrier in rats in hypocapnic hypoxia. Am J Psysiol Heart Circ Physiol 1987;252:504-512.
  • 28
    Kissen I, Weiss HR. Cervical sympathectomy and cerebral microvascuular and blood flow responses to hypocapnic hypoxia. Am J Physiol Heart Circ Physiol 1989;256:460-467.
  • 29
    Dahlgren N. Local cerebral blood flow in spontaneously breathing rats subjected to graded isobaric hypoxia. Acta Anesthesiol Scand 1990;34:463-467.
  • 30
    Nakai M, Iadecola C, Ruggiero DA, Tucker LW, Reis DJ. Electrical stimulation of cerebellar fastigial nucleus increases cerebral cortical blood flow without change in local metabolism: evidence for an intrinsic system in brain for primary vasodilation. Brain Res 1983;260:35-49.
  • 31
    Phillips JW. Adenosine and adenine nucleotides as regulators of cerebral blood flow: roll of acidosis, cell swelling, and KATP channels. Crit Rev Neurobiol 2004;16:237-277.
  • 32
    Underwood MD, Iadecola C, Resis DJ. Lesions of the rostral ventrolateral medulla reduce to hypoxia. Brain Res 1994; 635:217-233.
  • 33
    Golanov EV, Reis DJ. Contribution of oxygen-sensitive neurons of the rostral ventrolateral medulla to hypoxic cerebral vasodilation in the rat. J Psysiol 1996;495:201-216.
  • 34
    Golanov EV, Christensen JR, Reis DJ. Neurons of a limited subthalamic area mediate elevations in a cortical cerebral flow evoked by hypoxia and excitation of neurons of the rostral ventrolateral medulla. J Neurosci 2001;21:4031-4041.
  • 35
    Brown MM, Wade JPH, Marshall J. Fundamental importance of arterial oxygen content in the regulation of cerebral blood flow in man. Brain 1985;108:81-93.
  • 36
    Hudak ML, Koehler RC, Rosenberg AA, Traystman RJ, Jones MD. Effect of hematocrit on cerebral blood flow. Am J Physiol Heart Circ Physiol 1986;251:H63-H70.
  • 37
    LaManna JC, Vendel LM, Farrel RM. Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 1992;72: 2238-2243.
  • 38
    Xu K, Puchowicz MA, LaManna JC. Renormalization of regional brain blood flow during prolonged mild hypoxic exposure in rats. Brain Res 2004;1027:188-191.
  • 39
    Lenfant C, Sullivan K. Adaptation to high altitude. N Eng J Med 1971;284:1298-1309.
  • 40
    Patt S, Sampaolo S, Theallier-Janko A, Tschairkin I, Cervos-Navarro J. Cerebral angiogenesis triggered by severe chronic hypoxia displays regional differences. J Cereb Blood Flow Metab 1997;17:801-806.
  • 41
    Boero JÁ, Ascher J, Arregui A, Rovainen C, Woolsey TA. Increased brain capillaries in chronic hypoxia. J Appl Physiol 1999;86:1211-1219.
  • 42
    Pichiule P, LaManna JC. Angiopietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J Appl Physiol 2002;93:1131-1139.
  • 43
    Pichiule P, Chavez JC, LaManna JC. Hypoxic regulation of angiopoietin-2 expression in endothelial cells. J Biol Chem 2004;279:12171-12180.
  • 44
    Sick TJ, Lutz PL, LaManna JC, Rosenthal M. Comparative brain oxygenation and mitochondrial redox activity in turtles and rats. J Appl Physiol 1982;53:1354-1359.
  • 45
    Lübbers DW e Baumgärt H. Heterogeneities and profiles of oxygen pressure in brain and kidney as examples of the PO2 distribution in living tissue. Kidney Int 1997;51:372-380.
  • 46
    Chávez JC, Agani F, Pichiule P, LaManna JC. Expression of hypoxic inducible factor 1alfa in the brain of rats during chronic hypoxia. J Appl Physiol 2000;89:1937-1942.
  • 47
    Harik SL, Behmand RA, LaManna JC. Hypoxia increases glucose transport at blood-brain barrier in rats. J Appl Physiol 1994;77:896-901.
  • 48
    Gilbert RD, Pearce WJ, Longo LD. Fetal cardiac and cerebrovascular acclimatization responses to high altitude, long term hypoxia. High Alt Med Biol 2003;4:203-213.
  • 49
    Huppert F. Memory impairment associated with chronic hypoxia. Thorax 1982;37:858-860.
  • 50
    Grant I, Heaton RK, McSweeny AJ, Adams KM, Timms RM. Neuropsychologic findings in hypoxemic chronic obstructive pulmonary disease. Arch Intern Med 1982;142:1470-1476.
  • 51
    Prigatano GP, Parsons O, Levin DC, Wright E, Hawryluk G. Neuropsychological test performance in midly hypoxemic patients with chronic obstructive pulmonary disease. J Consul Clin Psychol 1983;51:108-116.
  • 52
    Fix AJ, Daughton D, Kass I, Bell CW, Golden CJ. Cognitive function and survival among patients with chronic obstructive pulmonary disease. Inter J Neuroscience 1985;27:13-17.
  • 53
    Incalzi RA, Gemma A, Marra C, Muzzolon R, Capparella O, Carbonin P. Chronic obstructive pulmonary disease. An original model of cognitive decline. Am Rev Respir Dis 1993;148:418-424.
  • 54
    Vos PJE, Folgering TM, van Herwaarden. Visual attention in patients with chronic OCDP. Biol Psychol 1995;41:295-305.
  • 55
    Fioravanti M, Nacca D, Amati S, Buckley AE, Bisetti A. Chronic obstructive pulmonary disease and associated patterns of memory decline. Dementia 1995;6:39-48.
  • 56
    Incalzi RA, Gemma A, Marra C, Capparella O, Fuso L, Carbonin PI. Verbal memory impairment in COPD. Its mechanisms and clinical relevance. Chest 1997;112:1506-1513.
  • 57
    Incalzi RA, Chiappini F, Fuso L, Torrice MP, Gemma A, Pistelli R. Predicting cognitive decline in patients with COPD. Respir Med 1998;92:527-533.
  • 58
    Etnier J, Johnston R, Dagenbach D, Pollard RJ, Reseski J, Berry M. The relationship among pulmonary function, aerobic fitness and cognitive functioning in older COPD patients. Chest 1999;116:953-960.
  • 59
    Stuss DT, Peterkin I, Guzman DA, Guzman C, Troyer AK. Chronic obstructive pulmonary disease: effects of hypoxia on neurological and neuropsychological measures. J Clin Exp Neuropsychol 1999;19:515-524.
  • 60
    Hjalmarsen A, Waterloo K, Dahl A, Jorde R, Viitanen M. Effect of long-term oxygen therapy on cognitive and neurological dysfunction in chronic obstructive pulmonary disease. Eur Neurol 1999;42:27-35.
  • 61
    Kozora E, Filley CM, Julian LJ, Cullum CM. Cognitive functioning in patients with chronic obstructive pulmonary disease and mild hypoxemia compared with patients with mild Alzheimer disease and normal controls. Neuropsychiatry Neuropsychol Behav Neurol 1999;12:178-183.
  • 62
    Antonelli Incalzi R, Marra C, Giordano A, et al. Cognitive impairment in chronic obstructive pulmonary disease--a neuropsychological and spect study. J Neurol 2003;250:325-332.
  • 63
    Liesker JJ, Postma DS, Beukema RJ, et al. Cognitive performance in patients with COPD. Respir Med 2004;98:351-356.
  • 64
    Antonelli-Incalzi R, Corsonello A, Pedone C, et al. Drawing impairment predicts mortality in severe COPD. Chest 2006;130:1687-1694.
  • 65
    Orth M, Kotterba S, Duchna K, et al. Cognitive deficits in patients with chronic obstructive pulmonary disease (COPD). Pneumologie 2006;60:593-599.
  • 66
    Ozge C, Ozge A, Unal O. Cognitive and functional deterioration in patients with severe COPD. Behav Neurol 2006;17: 121-130.
  • 67
    Ortapamuk H, Naldoken S. Brain perfusion abnormalities in chronic obstructive pulmonary disease: comparison with cognitive impairment. Ann Nucl Med 2006;20:99-106.
  • 68
    Goldstein PC. Drawing impairment predicts mortality in severe COPD: a naive approach to COPD mortality prediction. Chest 2007;132:141.
  • 69
    Lima OM, Oliveira-Souza R, Santos Oda R, Moraes PA, Sá LF, Nascimento OJ. Subclinical encephalopathy in chronic obstructive pulmonary disease. Arq Neuropsiquiatr 2007;65: 1154-1157.
  • 70
    Kirkil G, Tug T, Ozel E, Bulut S, Tekatas A, Muz MH. The evaluation of cognitive functions with P300 test for chronic obstructive pulmonary disease patients in attack and stable period. Clin Neurol Neurosurg 2007;109:553-560.
  • 71
    Antonelli-Incalzi R, Corsonello A, Trojano L, Acanfora D, Spada A, Izzo O, Rengo F. Correlation between cognitive impairment and dependence in hypoxemic COPD. J Clin Exp Neuropsychol 2007;21:1-10.
  • 72
    Antonelli-Incalzi R, Corsonello A, Trojano L, Pedone C, Acanfora D, Spada A, Izzo O, Rengo F. Screening of cognitive impairment in chronic obstructive pulmonary disease. Dement Geriatr Cogn Disord 2007;23:264-270.
  • 73
    Antonelli-Incalzi R, Corsonello A, Trojano L, et al. Correlation between cognitive impairment and dependence in hypoxemic COPD. J Clin Exp Neuropsychol 2008;30:141-150.
  • 74
    Zheng GQ, Wang Y, Wang XT. Chronic hypoxia-hypercapnia influences cognitive function: a possible new model of cognitive dysfunction in chronic obstructive pulmonary disease. Med Hypotheses 2008;71:111-113.
  • 75
    Favalli A, Miozzo A, Cossi S, Marengoni A. Differences in neuropsychological profile between healthy and COPD older persons. Int J Geriatr Psychiatry 2008;23:220-221.
  • 76
    Foley DJ, Monjan AA, Masaki KH, Enright PL, Quan SF, White LR. Associations of symptoms of sleep apnea with cardiovascular disease, cognitive impairment, and mortality among older Japanese-American men. J Am Geriatr Soc 1999;47:524-528.
  • 77
    Beebe DW, Groesz L, Wells C, Nichols A, McGee K. The neuropsychological effects of obstructive sleep apnea: a meta-analysis of norm-referenced and case-controlled data. Sleep 2003;26:298-307.
  • 78
    Sateia MJ. Neuropsychological impairment and quality of life in obstructive sleep apnea. Clin Chest Med 2003;24:249-259.
  • 79
    Antonelli Incalzi R, Marra C, Salvigni BL, et al. Does cognitive dysfunction conform to a distinctive pattern in obstructive sleep apnea syndrome? J Sleep Res 2004;13:79-86.
  • 80
    Verstraeten E, Cluydts R, Pevernagie D, Hoffmann G. Executive function in sleep apnea: controlling for attentional capacity in assessing executive attention. Sleep 2004;27:685-693.
  • 81
    Morrell MJ, Twigg G. Neural consequences of sleep disordered breathing: the role of intermittent hypoxia. Adv Exp Med Biol 2006;588:75-88.
  • 82
    Quan SF, Wright R, Baldwin CM, et al. Obstructive sleep apnea-hypopnea and neurocognitive functioning in the Sleep Heart Health Study. Sleep Med 2006;7:498-507.
  • 83
    Spira AP, Blackwell T, Stone KL, et al. Sleep-disordered breathing and cognition in older women. J Am Geriatr Soc 2008;56:45-50.
  • 84
    Mathieu A, Mazza S, Décary A, et al. Effects of obstructive sleep apnea on cognitive function: a comparison between younger and older OSAS patients. Sleep Med 2008;9:112-120.
  • 85
    van der Post J, Noordzij LAW, Kam ML, Blauw GJ, Cohen AF, van Gerven JMA. Evaluation of tests of central nervous system performance after hypoxaemia for a model for cognitive impairment. J Psychopharmachol 2002;16:337-343.
  • 86
    Zhang JX, Lu XJ, Wang XC, Li W, Du JZ. Intermittent hypoxia impairs performance of adult mice in the two-way shuttle box but not in the Morris water maze. J Neurosci Res 2006;84:228-235.
  • 87
    Kida M, Imai A. Cognitive performance and event-related brain potentials under simulated high altitudes. J Appl Physiol 1993;74:1735-1741.
  • 88
    Virués-Ortega J, Buela-Casal G, Garrido E, Alcázar B. Neuropsychological functioning associated with high-altitude exposure. Neuropsychol Rev 2004;14:197-224.
  • 89
    Titus AD, Shankaranarayana Rao BS, Harsha HN, Ramkumar K, Srikumar BN, Singh SB, Chattarji S, Raju TR. Hypobaric hypoxia-induced dendritic atrophy of hippocampal neurons is associated with cognitive impairment in adult rats. Neuroscience 2007;145:265-78.
  • 90
    Lezak MD. Neuropsychological assessment. Terceira Ed. Nova York: Oxford University Press, 1995.
  • 91
    Cummings JL. Subcortical dementia: neuropsychology, neuropsychiatry and pathophysiology. Brit J Psychiatr 1986; 149:682-697.
  • 92
    Bondi MW, Salmon DP, Kaszniak AW. The neuropsychology of dementia. Em: Grant I e Adams KM (Eds.) The neuropsychological assessment of neuropsychiatric disorders. Segunda Edição. New York: Oxford University press. 1996.
  • 93
    Mega MS, Cummings JL. Frontal-subcortical circuits and neuropsychiatric disorders. J Neuropsychiatry Clin Neurosci 1994;6:358-70.
  • 94
    Duke LM, Kaszniak AW. Executive control functions in degenerative dementias: a comparative review. Neuropsychol Rev 2000;10:75-99.
  • 95
    Shimada M. Alteration in acetylcholine synthesis in mouse brain cortex in mild hypoxia. J Neural Transm 1981;50:233-45.
  • 96
    Gibson GE, Peterson C, Sansone J. Decreases in amino acids and acetylcholine metabolism during hypoxia. J Neuchem 1981;37:192-201.
  • 97
    Dinger LHB, Fidone S. Effect of chronic hypoxia on cholinergic transmission in rat carotic body. J Appl Physiol 2005; 614-619.
  • 98
    Santos MS, Moreno AJ, Carvalho AP. Relationship between ATP depletion, membrane potential, and the release of neurotransmitters in rat nerve terminals. In vitro study under conditions that mimic anoxia, hypoglycemia and ischemia. Stroke 1996;27:941-950.
  • 99
    Wolfe R, Worrall-Carter L, Foister K, Keks N, Howe V. Assessment of cognitive function in heart failure patients. Eur J Cardiovasc Nurs 2006;5:158-164.
  • 100
    Krieger S, Jauss M, Jansen O, Theilmann L, Geissler M, Krieger D. Neuropsychiatric profile and hyperintense globus pallidus on T1-weighted magnetic resonance images in liver cirrhosis. Gastroenterology 1996;111:147-155.
  • 101
    Vogels RL, Scheltens P, Schroeder-Tanka JM, Weinstein HC. Cognitive impairment in heart failure: a systematic review of the literature. Eur J Heart Fail 2007;9:440-449.
  • 102
    Vogels RL, Oosterman JM, van Harten B, et al. Profile of cognitive impairment in chronic heart failure. J Am Geriatr Soc 2007;55:1764-1770.
  • 103
    Schear JM, Sato SD. Effects of visual acuity and visual motor speed and dexterity on cognitive performance. Arch Clin Neuropsychol 1989;4:25-32.
  • 104
    Secretaria de Estado da Saúde - Guia do usuário de oxigenoterapia domiciliar. Florianópolis, 2004. http://www.saude.sc.gov.br/gestores/oxigenoterapia/guia%20do%20
    » http://www.saude.sc.gov.br/gestores/oxigenoterapia/guia%20do%20
  • 105
    Sociedade Brasileira de Pneumologia e Tisiologia. Oxigenoterapia domiciliar prolongada. J Pneumol 2000;26:341-350.
  • 106
    Allen SC. Competence thresholds for the use of inhalers in people with dementia. Age Ageing 1997;26:83-86
  • 107
    Allen SC, Jain M, Ragab S, Malik N. Acquisition and short-term retention of inhaler techniques require intact executive function in elderly subjects. Age Ageing 2003;32:299-302
  • 108
    Board M, Allen SC. A simple drawing test to identify patients who are unlikely to be able to learn to use an inhaler. Int J Clin Pract 2006;60:510-513
  • 109
    Allen SC, Ragab S. Ability to learn inhaler technique in relation to cognitive scores and tests of praxis in old age. Postgrad Med J 2002;78:37-39.
  • 110
    Fix AJ, Daughton D, Kass I, Bell CW, Golden CJ. Cognitive functioning and survival among patients with chronic obstructive pulmonary disease. Int J Neurosci 1985;272:13-17.
  • 111
    Jokinen H, Kalska H, Ylikoski R, et al. LADIS group. Longitudinal cognitive decline in subcortical ischemic vascular disease: the LADIS Study. Cerebrovasc Dis 2009;27:384-391.
  • 112
    Targosz-Gajniak M, Siuda J, Ochudło S, Opala G. Cerebral white matter lesions in patients with dementia - from MCI to severe Alzheimer's disease. J Neurol Sci 2009;283:79-82.
  • 113
    Jokinen H, Kalska H, Ylikoski R, et al. LADIS group. MRI-defined subcortical ischemic vascular disease: baseline clinical and neuropsychological findings. The LADIS Study. Cerebrovasc Dis 2009;27:336-344.
  • 114
    Erkinjuntti T, Gauthier S. The concept of vascular cognitive impairment. Front Neurol Neurosci 2009;24:79-85.
  • 115
    Schmahmann JD, Smith EE, Eichler FS, Filley CM. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. Ann N Y Acad Sci 2008;1142:266-309.
  • 116
    Black S, Gao F, Bilbao J. Understanding white matter disease: imaging-pathological correlations in vascular cognitive impairment. Stroke 2009;40:S48-S52.
  • 117
    Jagust WJ, Zheng L, Harvey DJ, et al. Neuropathological basis of magnetic resonance images in aging and dementia. Ann Neurol 2008;63:72-80.
  • 118
    Jellinger KA. Pathology and pathophysiology of vascular cognitive impairment. A critical update. Panminerva Med 2004;46:217-226.
  • 119
    Udaka F, Sawada H, Kameyama M. White matter lesions and dementia: MRI-pathological correlation. Ann N Y Acad Sci 2002;977:411-415.
  • 120
    van Dijk EJ, Vermeer SE, de Groot JC, et al. Arterial oxygen saturation, COPD, and cerebral small vessel disease. J Neurol Neurosurg Psychiatry 2004;75:733-736.
  • 121
    Guo X, Pantoni L, Simoni M, et al. Midlife respiratory function related to white matter lesions and lacunar infarcts in late life: the Prospective Population Study of Women in Gothenburg, Sweden. Stroke 2006;37:1658-1662.

Publication Dates

  • Publication in this collection
    Jan-Mar 2010

History

  • Received
    06 Nov 2009
  • Accepted
    17 Jan 2010
Academia Brasileira de Neurologia, Departamento de Neurologia Cognitiva e Envelhecimento R. Vergueiro, 1353 sl.1404 - Ed. Top Towers Offices, Torre Norte, São Paulo, SP, Brazil, CEP 04101-000, Tel.: +55 11 5084-9463 | +55 11 5083-3876 - São Paulo - SP - Brazil
E-mail: revistadementia@abneuro.org.br | demneuropsy@uol.com.br