Hippocampal atrophy and verbal episodic memory performance in amnestic mild cognitive impairment and mild Alzheimer's disease: A preliminary study

Marchiani, Nathalia Carollina Peruzza; Balthazar, Marcio Luiz Figueredo; Cendes, Fernando; Damasceno, Benito Pereira

doi:10.1590/S1980-57642009DN20100008

Abstract

To evaluate hippocampal volume in patients with AD and aMCI, and correlate its atrophy with verbal episodic memory performance. Methods: We studied 42 individuals older than 50 years, including 14 with amnestic mild cognitive impairment (aMCI), 14 with mild Alzheimer's disease (AD) and 14 normal controls. All individuals were submitted to the Rey auditory verbal learning test (RAVLT) to evaluate episodic memory. They were also submitted to the forward (FDS) and backward digit span (BDS) subtest of WAIS-R to evaluate working memory and attention, and to the Mini Mental State Examination (MMSE). Hippocampal volumetric measurements were performed according to anatomic guidelines from a standard protocol using high-resolution T1-inversion recovery 3-mm coronal MRI slices. Hippocampal volumes (HV) were corrected for the variation in total intracranial volume. There was no significant difference between the three groups concerning age and education. Results: On RAVLT, there was a continuum between the three groups, with AD recalling less words, controls more, and aMCI subjects showing an intermediate performance on all sub-items. We found an asymmetry between HVs, with smaller mean left HV for all groups. ANOVA and post hoc Tukey's test for comparisons of HV showed a significant difference among groups, with difference between controls and both AD and aMCI, although there was no significant difference between AD and aMCI groups. Conclusions: There was a significant correlation between hippocampal volumes and scores on RAVLT, confirming that medial temporal structures are closely associated with memory performance in normal ageing as well as in aMCI and AD.

Key words:
hippocampal atrophy; MRI; memory; Alzheimer's disease; mild cognitive impairment

Resumo

Avaliar os volumes hipocampais (VH) em pacientes com doença de Alzheimer (DA) leve e comprometimento cognitivo leve amnéstico (aCCL). Métodos: Estudamos 42 sujeitos maiores de 50 anos, incluindo 14 com DA leve, 14 com aCCL e 14 controles. Todos foram submetidos ao teste de aprendizado auditivo verbal de Rey (TAAVR) para avaliação de memória episódica, ao teste de extensão de dígitos direto e indireto do WAIS-R, para avaliação de memória operacional e atenção e ao Mini Exame do Estado Mental (MEEM). As medidas de volumetria hipocampal foram obtidas de acordo com as diretrizes anatômicas de um protocolo padrão usando imagens coronais ponderadas T1 inversion-recovery de 3 mm. Os VH foram corrigidos para a variação do volume intracraniano total. Não houve diferença significativa entre os 3 grupos quanto a idade e escolaridade. Resultados: No TAAVR houve um continuum no desempenho dos 3 grupos, com os pacientes com DA leve evocando menos palavras, os controles mais e os aCCL mostrando um desempenho intermediário em todos os subitens. Encontramos também uma assimetria entre os VH, com o lado esquerdo menor que o direito nos 3 grupos. O teste de análise de variância (ANOVA) seguido do teste post hoc de Tukey para comparações entre os VH dos grupos mostrou diferença significativa entre controles e DA e aCCL, mas não entre DA e aCCL. Encontramos também correlação estatística significativa entre os VH e o desempenho no TAAVR. Conclusões: As estruturas do lobo temporal medial estão intimamente ligadas ao desempenho de memória episódica tanto no envelhecimento normal quanto no aCCL e DA.

Palavras-chave:
atrofia hipocampal; MRI; memória; doença de Alzheimer; transtorno cognitivo leve

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References

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Markowitsch HJ. Memory and amnesia. In: Mesulam MM, editor. Principles of behavioral and cognitive neurology. New York, NY: Oxford University Press; 2000:257-293.
²
Economou A, Papageorgiou SG, Papanicolau AC. Amnesia associated with the dementias. In: Papanicolau AC, editor. The amnesias: a clinical textbook of memory disorders. New York, NY: Oxford University Press; 2006:75-110.
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Cummings JL. Cognitive and behavioral heterogeneity in Alzheimer's disease: seeking the neurobiological basis. Neurobiol Aging 2000;21:845-861.
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Lehéricy S, Baulac M, Chiras J, et al. Amygdalohippocampal MR volume measurement in the early stages of Alzheimer disease. AJNR Am J Neuroradiol 1994;15:927-937.
⁵
Visser PJ, Verhey FRJ, Hofman PAM, Scheltens P, Jolles J. Medial temporal lobe atrophy predicts Alzheimer's disease in patients with minor cognitive impairment. J Neurol Neurosurg Psychiatry 2002;72:491-497
⁶
Basso M, Yang J, Warren L , et al. Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease. Psychiatry Research: Neuroimaging 2006;146:251-261.
⁷
Petersen RC, Parisi JE, Dickson DW et al. Neuropathologic Features of Amnestic Mild Cognitive Impairment. Arch Neurol 2006;63:665-672.
⁸
Roth M, Huppert FA, Tym E, Mountjoy CQ. The Cambridge Examination for Mental Disorders of the Elderly (CAMDEX). Cambridge University Press; 1988.
⁹
Winblad B, Palmer K, Kivipelto M, et al. Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 2004;256:240-246.
¹⁰
Morris JC. The clinical dementia rating (CDR): Current version and scoring rules. Neurology 1993;43:2412-2414.
¹¹
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;34:939-944.
¹²
Rey A. L'examen clinique in psychologie. Paris: Press Universitaire de France, 1964.
¹³
Wechsler D. Wechsler Memory Scale-Revised: Manual. USA: The Psychological Corporation, Hartcourt Brace Jovanovich Inc., 1987.
¹⁴
Brucki SMD, Nitrini R, Caramelli P, Bertolucci PHF, Okamoto IH. Sugestões para o uso do mini-exame do estado mental no Brasil. Arq Neuropsiquiatr 2003;61:777-781.
¹⁵
Watson C, Jack CR, Cendes F. Volumetric MRI: Clinical applications and contributions to the understanding of temporal lobe epilepsy. Arch Neurol 1997; 54:1521-1531.
¹⁶
Modrego PJ. Predictors of conversion to dementia of probable Alzheimer type in patients with mild cognitive impairment. Curr Alzheimer Res 2006;3:161-170.
¹⁷
Mega SM, Small GW, Xu ML, et al. Hippocampal Atrophy in Persons With Age-Associated Memory Impairment: Volumetry Within a Common Space. Psychosomatic Medicine 2002;64:487-492.
¹⁸
Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, Jolesz F. Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer's disease. Arch Neurol 1993;50:949-954.
¹⁹
Soininen HS, Partanen K, Pitkänen A, et al. Volumetric MRI analysis of the amygdala and hippocampus in subjects with age-associated memory impairment: Correlation to visual and verbal memory. Neurology 1994;44:1660-1668.
²⁰
Mori E, Yoneda Y, Yamashita H, Hirono N, Ikeda M, Yamadori A. Medial temporal structures relate to memory impairment in Alzheimer's disease: an MRI volumetric study. J Neurol Neurosurg Psychiatry 1997;63:214-221.
²¹
Scher AI, Xu Y, Korf ES, et al. Hippocampal shape analysis in Alzheimer's disease: a population-based study. Neuroimage 2007;36:8-18.
²²
Fleisher AS, Sun S, Taylor C, et al. Volumetric MRI vs clinical predictors of Alzheimer disease in mild cognitive impairment. Neurology 2008;70:191-199.
²³
Devanand DP, Pradhaban G, Liu X, et al. Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 2007;68:828-836.

Publication Dates

Publication in this collection
Jan-Mar 2008

History

Received
25 Jan 2008
Reviewed
15 Feb 2008
Accepted
16 Feb 2008

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹
Markowitsch HJ. Memory and amnesia. In: Mesulam MM, editor. Principles of behavioral and cognitive neurology. New York, NY: Oxford University Press; 2000:257-293.

[2] ²
Economou A, Papageorgiou SG, Papanicolau AC. Amnesia associated with the dementias. In: Papanicolau AC, editor. The amnesias: a clinical textbook of memory disorders. New York, NY: Oxford University Press; 2006:75-110.

[3] ³
Cummings JL. Cognitive and behavioral heterogeneity in Alzheimer's disease: seeking the neurobiological basis. Neurobiol Aging 2000;21:845-861.

[4] ⁴
Lehéricy S, Baulac M, Chiras J, et al. Amygdalohippocampal MR volume measurement in the early stages of Alzheimer disease. AJNR Am J Neuroradiol 1994;15:927-937.

[5] ⁵
Visser PJ, Verhey FRJ, Hofman PAM, Scheltens P, Jolles J. Medial temporal lobe atrophy predicts Alzheimer's disease in patients with minor cognitive impairment. J Neurol Neurosurg Psychiatry 2002;72:491-497

[6] ⁶
Basso M, Yang J, Warren L , et al. Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease. Psychiatry Research: Neuroimaging 2006;146:251-261.

[7] ⁷
Petersen RC, Parisi JE, Dickson DW et al. Neuropathologic Features of Amnestic Mild Cognitive Impairment. Arch Neurol 2006;63:665-672.

[8] ⁸
Roth M, Huppert FA, Tym E, Mountjoy CQ. The Cambridge Examination for Mental Disorders of the Elderly (CAMDEX). Cambridge University Press; 1988.

[9] ⁹
Winblad B, Palmer K, Kivipelto M, et al. Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 2004;256:240-246.

[10] ¹⁰
Morris JC. The clinical dementia rating (CDR): Current version and scoring rules. Neurology 1993;43:2412-2414.

[11] ¹¹
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;34:939-944.

[12] ¹²
Rey A. L'examen clinique in psychologie. Paris: Press Universitaire de France, 1964.

[13] ¹³
Wechsler D. Wechsler Memory Scale-Revised: Manual. USA: The Psychological Corporation, Hartcourt Brace Jovanovich Inc., 1987.

[14] ¹⁴
Brucki SMD, Nitrini R, Caramelli P, Bertolucci PHF, Okamoto IH. Sugestões para o uso do mini-exame do estado mental no Brasil. Arq Neuropsiquiatr 2003;61:777-781.

[15] ¹⁵
Watson C, Jack CR, Cendes F. Volumetric MRI: Clinical applications and contributions to the understanding of temporal lobe epilepsy. Arch Neurol 1997; 54:1521-1531.

[16] ¹⁶
Modrego PJ. Predictors of conversion to dementia of probable Alzheimer type in patients with mild cognitive impairment. Curr Alzheimer Res 2006;3:161-170.

[17] ¹⁷
Mega SM, Small GW, Xu ML, et al. Hippocampal Atrophy in Persons With Age-Associated Memory Impairment: Volumetry Within a Common Space. Psychosomatic Medicine 2002;64:487-492.

[18] ¹⁸
Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, Jolesz F. Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer's disease. Arch Neurol 1993;50:949-954.

[19] ¹⁹
Soininen HS, Partanen K, Pitkänen A, et al. Volumetric MRI analysis of the amygdala and hippocampus in subjects with age-associated memory impairment: Correlation to visual and verbal memory. Neurology 1994;44:1660-1668.

[20] ²⁰
Mori E, Yoneda Y, Yamashita H, Hirono N, Ikeda M, Yamadori A. Medial temporal structures relate to memory impairment in Alzheimer's disease: an MRI volumetric study. J Neurol Neurosurg Psychiatry 1997;63:214-221.

[21] ²¹
Scher AI, Xu Y, Korf ES, et al. Hippocampal shape analysis in Alzheimer's disease: a population-based study. Neuroimage 2007;36:8-18.

[22] ²²
Fleisher AS, Sun S, Taylor C, et al. Volumetric MRI vs clinical predictors of Alzheimer disease in mild cognitive impairment. Neurology 2008;70:191-199.

[23] ²³
Devanand DP, Pradhaban G, Liu X, et al. Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 2007;68:828-836.

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