Analysis of brief language tests in the detection of cognitive decline and dementia

Radanovic, Marcia; Carthery-Goulart, Maria Teresa; Charchat-Fichman, Helenice; Herrera Jr., Emílio; Lima, Edson Erasmo Pereira; Smid, Jerusa; Porto, Cláudia Sellitto; Nitrini, Ricardo

doi:10.1590/S1980-57642008DN10100007

Abstract

Lexical access difficulties are frequent in normal aging and initial stages of dementia. Verbal fluency tests are valuable to detect cognitive decline, evidencing lexico-semantic and executive dysfunction.

Objectives:

To establish which language tests can contribute in detecting dementia and to verify schooling influence on subject performance.

Method:

74 subjects: 33 controls, 17 Clinical Dementia Rating (CDR) 0.5 and 24 (Brief Cognitive Battery - BCB e Boston Naming Test - BNT) 1 were compared in tests of semantic verbal fluency (animal and fruit), picture naming (BCB and BNT) and the language items of Mini Mental State Examination (MMSE).

Results:

There were significant differences between the control group and both CDR 0.5 and CDR 1 in all tests. Cut-off scores were: 11 and 10 for animal fluency, 8 for fruit fluency (in both), 8 and 9 for BCB naming. The CDR 0.5 group performed better than the CDR 1 group only in animal fluency. Stepwise multiple regression revealed fruit fluency, animal fluency and BCB naming as the best discriminators between patients and controls (specificity: 93.8%; sensitivity: 91.3%). In controls, comparison between illiterates and literates evidenced schooling influence in all tests, except for fruit fluency and BCB naming. In patients with dementia, only fruit fluency was uninfluenced by schooling.

Conclusion:

The combination of verbal fluency tests in two semantic categories along with a simple picture naming test is highly sensitive in detecting cognitive decline. Comparison between literate and illiterate subjects shows a lesser degree of influence of schooling on the selected tests, thus improving discrimination between low performance and incipient cognitive decline.

Key words:
language tests; cognitive disorders; dementia; Alzheimer disease; education.

Resumo

Dificuldades de acesso lexical são freqüentes no envelhecimento normal e fases iniciais de demência. Testes de fluência verbal são úteis para detectar declínio cognitivo, evidenciando disfunções léxicosemânticas e executivas.

Objetivos:

Estabelecer quais testes de linguagem podem contribuir para detectar demência e verificar a influência da escolaridade no desempenho dos sujeitos.

Métodos:

74 indivíduos: 33 controles, 17 CDR 0,5 e 24 CDR 1, foram comparados quanto a fluência verbal semântica (animais e frutas), nomeação de figuras (BCB e TNB) e provas de linguagem do MEEM.

Resultados:

Houve diferenças significantes em todas as provas entre controles e os grupos CDR 0,5 e CDR 1. As notas de corte foram: 11 e 10 para animais, 8 (para ambos) para frutas, 8 e 9 para nomeação da BCB. O grupo CDR 0,5 teve desempenho superior ao CDR 1 apenas na fluência de animais. Fluência de frutas, de animais e nomeação da BCB foram as variáveis que melhor discriminaram pacientes e controles (especificidade: 93,8%; sensibilidade: 91,3%). Em controles, a comparação entre analfabetos e alfabetizados evidenciou influência da escolaridade em todas as provas, com exceção da fluência de frutas e nomeação da BCB. Em pacientes com demência só a fluência de frutas não sofreu influência da escolaridade.

Conclusão:

A combinação de testes de fluência verbal em duas categorias semânticas e nomeação de figuras simples é altamente sensível para detectar declínio cognitivo. A comparação entre alfabetizados e analfabetos mostrou menor influência da escolaridade nos testes selecionados, facilitando a discriminação entre baixo desempenho e declínio cognitivo incipiente.

Palavras-chave:
testes de linguagem; transtorno cognitivo; demência; doença de Alzheimer; escolaridade.

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References

¹
Faber-Langedoen K, Morris JC, Knevich JW, La Barge E,Miller JP, Berg L. Aphasia in senile dementia of the Alzheimer type. Ann Neurol 1988;23:365-370.
²
Bayles KA. Language function in senile dementia. BrainLang 1982;16:265-280.
³
Kempler D. Language changes in dementia of the Alzheimertype. In: Lubinski R, editor. Dementia and Communication. San Diego: Singular Publishing Group; 1995:98-114.
⁴
Caramelli P, Mansur LL, Nitrini R. Language and communication disorders in dementia of the Alzehimer type. In: Stemmer B, Whitaker HA, editors. Handbook of Neurolinguistics. San Diego: Academic Press; 1998:463-473.
⁵
Azuma R, Bayles KA. Memory impairments underlying language difficulties in dementia. Top Lang Dis 1997;18:58-71.
⁶
Reisberg B, Ferris SH, De Leon MJ, Crook T. The global deterioration scale (GDS):an instrument for the assessment of primary degenerative dementia (PDD).Am J Psychiatry 1982;139:1136-1139.
⁷
Bayles KA, Tomoeda CK, Cruz RF, Mahendra N. communication abilities of individuals with late-stage Alzheimer disease. Alzheimer Dis Assoc Disord 2000;14:176-181.
⁸
Chertkow H, Bub D. Semantic memory loss in dementia ofAlzheimer's type. What do various measures measure? Brain 1990;113:397-417.
⁹
Martin A, Fedio P. Word production and comprehension inAlzheimer's disease:the breakdown of semantic knowledge. Brain Lang 1983;19:124-141.
¹⁰
Huff FJ, Corkin S, Growdon JH. Semantic impairment andanomia in Alzheimer's disease. Brain Lang 1986;28:235-249.
¹¹
Nebes RD, Brady CB. Preserved organization of semantic attributes in Alzheimer's disease. Psychol Aging 1990;5:574-579.
¹²
Walker VG, Hardiman CJ, Hedrick DL, Holbrook A. Speechand language characteristics of an aging population. In: Norman JL, editor. Speech and Language: advances in basic research and practice. New York: Academic Press; 1981:143-202.
¹³
Lezak MD. Neuropsychological assessment, 3rd ed. NewYork: Oxford University Press; 1995.
¹⁴
Bryan J, Luszcz M. Measurement of executive function:considerations for detecting adult age differences. J Clin Exp Neuropsychol 2000;22:40-55.
¹⁵
Della Salla S, Lorenzi L, Spinnler H, Zuffi M. Componentsin the breakdown of verbal communication in Alzheimer's disease. Aphasiol 1993;7:285-300.
¹⁶
Caramelli P, Carthery MT, Porto CS, Charchat H, Nitrini R.Qualitative analysis of verbal fluency in normal aging and Alzheimer's disease: effects of educational background (Abstr). Neurology 2001; 56(Suupl 3):A183.
¹⁷
Pasquier F, Lebert F, Grymonprez L, Petit H. Verbal fluencyin dementia of frontal lobe and dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 1995;58:81-84.
¹⁸
Brucki SM, Malheiros SM, Okamoto IH, Bertolucci P. Normative data on the verbal fluency test in the animal category in our millieu. Arq Neuropsiquiatr 1997;55:56-61.
¹⁹
Savage CR. Neuropsychology of subcortical dementias. ThePsychiatric Clin North Am 1997;20:911-931.
²⁰
Haddad MS. Demências subcorticais. In: Forlenza OV,Caramelli P, editors. Neuropsiquiatria Geriátrica. São Paulo:Atheneu; 2000:243-251.
²¹
Jacobs DM, Stern Y, Mayeux R. Dementia in Parkinson disease, Huntington disease, and other degenerative conditions. In: Feinberg TE, Farah MJ, editors. Behavioral Neurology and Neuropsychology. New York:McGraw-Hill; 1997:579-588.
²²
Petersen RC, Stevens JC, Ganguli M, Tangalos EG, CummingsJL, DeKosky ST. Practice parameter:early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001;56:1133-1142.
²³
Lambon Ralph MA, Patterson K, Graham N, Dawson K,Hodges JR. Homogeneity and heterogeneity in mild cognitive impairment and Alzheimer's disease:a crosssectional and longitudinal study of 55 cases. Brain 2003; 126:2350-2362.
²⁴
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 1994.
²⁵
Pfeffer RI, Kurosaki TT, Harrah CH, et al. Measurement offunctional activities in older adults in the community. J Gerontol 1982;37:323-329.
²⁶
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;12:189-198.
²⁷
Brucki MD, 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.
²⁸
Bertolucci PH, Okamoto IH, Brucki SM, et al. Applicabilityof the CERAD neuropsychological battery to Brazilian elderly. Arq Neuropsiquiatr 2001; 59:532-536.
²⁹
Nitrini R, Lefèvre BH, Mathias SC, et al. Testes neuropsicológicos de aplicação simples para o diagnóstico de demência. Arquivos de Neuropsiquiatria 1994; 52:457-65.
³⁰
Kaplan E, Goodglass H, Weintraub S. The Boston NamingTest. Philadelphia: Lippincott Williams & Wilkins; 2001.
³¹
Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. Anew clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.
³²
Morris JC. The Clinical Dementia Rating (CDR):currentversion and scoring rules. Neurology 1993;43:2412-2414.
³³
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 the Department of Health an Human Services Task Force on Alzheimer's Disease. Neurology 1984;34:939-944.
³⁴
Román GC, Tatemichi TK, Erkinjuntti T et al. Vasculardementia: diagnostic criteria for research studies. Report of the NINDS-AIREN international workshop. Neurology 1993;43:250-260.
³⁵
Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease:a clinicopathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992; 55:181-184.
³⁶
Castro-Caldas A, Petersson KM, Reis A, Stone-Elander S,Ingvar M. The illiterate brain - Learning to read and write during childhood influences the functional organization of the adult brain. Brain 1998;121:1053-1063.
³⁷
Cerhan JH, Ivnik RJ, Smith GE, Tangalos EC, Petersen RC,Boeve BF. Diagnostic utility of letter fluency, category fluency, and fluency difference scores in Alzheimer's disease. Clin Neuropsychol 2002;16:35-42.
³⁸
Murphy KJ, Rich JB, Troyer AK. Verbal fluency patterns inamnestic mild cognitive impairment are characteristic of Alzheimer's type dementia. J Int Neuropsychol Soc 2006; 12:570-574.
³⁹
Vogel A, Gade A, Stokholm J, Waldemar G. Semantic memory impairment in the earliest phases of Alzheimer's disease. Dement Geriatr Cogn Disord 2005;19:75-81.
⁴⁰
Cooper DB, Lacritz LH, Weiner MF, Rosenberg RN, CullumCM. Category fluency in mild cognitive impairment: reduced effect of practice in test-retest conditions. Alzheimer Dis Assoc Disord 2004;18:120-122.
⁴¹
Jones S, Laukka EJ, Backman L. Differential verbal fluencydeficits in the preclinical stages of Alzheimer's disease and vascular dementia. Cortex 2006; 42:347-355.
⁴²
Sailor K, Antoine M, Diaz M, Kuslansky G, Kluger A. Theeffects of Alzheimer's disease on item output in verbal fluency tasks. Neuropsychology 2004;18:306-314.
⁴³
Forbes-McKay KE, Ellis AW, Shanks MF, Venneri A. The ageof acquisition of words produced in a semantic fluency task can reliably differentiate normal from pathological age related cognitive decline. Neuropsychologia 2005;43:1625-1632.
⁴⁴
Diaz M, Sailor K, Cheung D, Kuslansky G. Category sizeeffects in semantic and letter fluency in Alzheimer's patients. Brain Lang 2004;89:108-114.
⁴⁵
Fernandez T, Rios C, Santos S et al. "Household items": analternative task to "animals" in the assessment of semantic verbal fluency: a validation study. Rev Neurol (Spanish ) 2002;35:520-523.
⁴⁶
March EG, Pattison P. Semantic verbal fluency in Alzheimer's disease: approaches beyond the traditional scoring system. J Clin Exp Neuropsychol 2006;28:549-566.
⁴⁷
Rockwood K, Bowler J, Erkinjuntti T, Hachinski V, Wallin A.Subtypes of vascular dementia. Alzheimer Dis Assoc Disord 1999;13:59-65.
⁴⁸
Brucki SMD, Rocha MSG. Category fluency test: effects ofage, gender and education on total scores, clustering and switching in Brazilian Portuguese-speaking subjects. Braz J Med Biol Res 2004;37:1771-1777.
⁴⁹
Henry JD, Crawford JR, Phillips LH. Verbal fluency performance in dementia of the Alzheimer's type:a metaanalysis. Neuropsychologia 2004;42:1212-1222.
⁵⁰
Testa JA, Ivnik RJ, Boeve B et al. Confrontation naming doesnot add incremental diagnostic utility in MCI and Alzheimer's disease. J Int Neuropsychol Soc 2004;10:504-512.

Publication Dates

Publication in this collection
Jan-Mar 2007

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

[1] ¹
Faber-Langedoen K, Morris JC, Knevich JW, La Barge E,Miller JP, Berg L. Aphasia in senile dementia of the Alzheimer type. Ann Neurol 1988;23:365-370.

[2] ²
Bayles KA. Language function in senile dementia. BrainLang 1982;16:265-280.

[3] ³
Kempler D. Language changes in dementia of the Alzheimertype. In: Lubinski R, editor. Dementia and Communication. San Diego: Singular Publishing Group; 1995:98-114.

[4] ⁴
Caramelli P, Mansur LL, Nitrini R. Language and communication disorders in dementia of the Alzehimer type. In: Stemmer B, Whitaker HA, editors. Handbook of Neurolinguistics. San Diego: Academic Press; 1998:463-473.

[5] ⁵
Azuma R, Bayles KA. Memory impairments underlying language difficulties in dementia. Top Lang Dis 1997;18:58-71.

[6] ⁶
Reisberg B, Ferris SH, De Leon MJ, Crook T. The global deterioration scale (GDS):an instrument for the assessment of primary degenerative dementia (PDD).Am J Psychiatry 1982;139:1136-1139.

[7] ⁷
Bayles KA, Tomoeda CK, Cruz RF, Mahendra N. communication abilities of individuals with late-stage Alzheimer disease. Alzheimer Dis Assoc Disord 2000;14:176-181.

[8] ⁸
Chertkow H, Bub D. Semantic memory loss in dementia ofAlzheimer's type. What do various measures measure? Brain 1990;113:397-417.

[9] ⁹
Martin A, Fedio P. Word production and comprehension inAlzheimer's disease:the breakdown of semantic knowledge. Brain Lang 1983;19:124-141.

[10] ¹⁰
Huff FJ, Corkin S, Growdon JH. Semantic impairment andanomia in Alzheimer's disease. Brain Lang 1986;28:235-249.

[11] ¹¹
Nebes RD, Brady CB. Preserved organization of semantic attributes in Alzheimer's disease. Psychol Aging 1990;5:574-579.

[12] ¹²
Walker VG, Hardiman CJ, Hedrick DL, Holbrook A. Speechand language characteristics of an aging population. In: Norman JL, editor. Speech and Language: advances in basic research and practice. New York: Academic Press; 1981:143-202.

[13] ¹³
Lezak MD. Neuropsychological assessment, 3rd ed. NewYork: Oxford University Press; 1995.

[14] ¹⁴
Bryan J, Luszcz M. Measurement of executive function:considerations for detecting adult age differences. J Clin Exp Neuropsychol 2000;22:40-55.

[15] ¹⁵
Della Salla S, Lorenzi L, Spinnler H, Zuffi M. Componentsin the breakdown of verbal communication in Alzheimer's disease. Aphasiol 1993;7:285-300.

[16] ¹⁶
Caramelli P, Carthery MT, Porto CS, Charchat H, Nitrini R.Qualitative analysis of verbal fluency in normal aging and Alzheimer's disease: effects of educational background (Abstr). Neurology 2001; 56(Suupl 3):A183.

[17] ¹⁷
Pasquier F, Lebert F, Grymonprez L, Petit H. Verbal fluencyin dementia of frontal lobe and dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 1995;58:81-84.

[18] ¹⁸
Brucki SM, Malheiros SM, Okamoto IH, Bertolucci P. Normative data on the verbal fluency test in the animal category in our millieu. Arq Neuropsiquiatr 1997;55:56-61.

[19] ¹⁹
Savage CR. Neuropsychology of subcortical dementias. ThePsychiatric Clin North Am 1997;20:911-931.

[20] ²⁰
Haddad MS. Demências subcorticais. In: Forlenza OV,Caramelli P, editors. Neuropsiquiatria Geriátrica. São Paulo:Atheneu; 2000:243-251.

[21] ²¹
Jacobs DM, Stern Y, Mayeux R. Dementia in Parkinson disease, Huntington disease, and other degenerative conditions. In: Feinberg TE, Farah MJ, editors. Behavioral Neurology and Neuropsychology. New York:McGraw-Hill; 1997:579-588.

[22] ²²
Petersen RC, Stevens JC, Ganguli M, Tangalos EG, CummingsJL, DeKosky ST. Practice parameter:early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001;56:1133-1142.

[23] ²³
Lambon Ralph MA, Patterson K, Graham N, Dawson K,Hodges JR. Homogeneity and heterogeneity in mild cognitive impairment and Alzheimer's disease:a crosssectional and longitudinal study of 55 cases. Brain 2003; 126:2350-2362.

[24] ²⁴
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 1994.

[25] ²⁵
Pfeffer RI, Kurosaki TT, Harrah CH, et al. Measurement offunctional activities in older adults in the community. J Gerontol 1982;37:323-329.

[26] ²⁶
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;12:189-198.

[27] ²⁷
Brucki MD, 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.

[28] ²⁸
Bertolucci PH, Okamoto IH, Brucki SM, et al. Applicabilityof the CERAD neuropsychological battery to Brazilian elderly. Arq Neuropsiquiatr 2001; 59:532-536.

[29] ²⁹
Nitrini R, Lefèvre BH, Mathias SC, et al. Testes neuropsicológicos de aplicação simples para o diagnóstico de demência. Arquivos de Neuropsiquiatria 1994; 52:457-65.

[30] ³⁰
Kaplan E, Goodglass H, Weintraub S. The Boston NamingTest. Philadelphia: Lippincott Williams & Wilkins; 2001.

[31] ³¹
Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. Anew clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-572.

[32] ³²
Morris JC. The Clinical Dementia Rating (CDR):currentversion and scoring rules. Neurology 1993;43:2412-2414.

[33] ³³
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 the Department of Health an Human Services Task Force on Alzheimer's Disease. Neurology 1984;34:939-944.

[34] ³⁴
Román GC, Tatemichi TK, Erkinjuntti T et al. Vasculardementia: diagnostic criteria for research studies. Report of the NINDS-AIREN international workshop. Neurology 1993;43:250-260.

[35] ³⁵
Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease:a clinicopathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992; 55:181-184.

[36] ³⁶
Castro-Caldas A, Petersson KM, Reis A, Stone-Elander S,Ingvar M. The illiterate brain - Learning to read and write during childhood influences the functional organization of the adult brain. Brain 1998;121:1053-1063.

[37] ³⁷
Cerhan JH, Ivnik RJ, Smith GE, Tangalos EC, Petersen RC,Boeve BF. Diagnostic utility of letter fluency, category fluency, and fluency difference scores in Alzheimer's disease. Clin Neuropsychol 2002;16:35-42.

[38] ³⁸
Murphy KJ, Rich JB, Troyer AK. Verbal fluency patterns inamnestic mild cognitive impairment are characteristic of Alzheimer's type dementia. J Int Neuropsychol Soc 2006; 12:570-574.

[39] ³⁹
Vogel A, Gade A, Stokholm J, Waldemar G. Semantic memory impairment in the earliest phases of Alzheimer's disease. Dement Geriatr Cogn Disord 2005;19:75-81.

[40] ⁴⁰
Cooper DB, Lacritz LH, Weiner MF, Rosenberg RN, CullumCM. Category fluency in mild cognitive impairment: reduced effect of practice in test-retest conditions. Alzheimer Dis Assoc Disord 2004;18:120-122.

[41] ⁴¹
Jones S, Laukka EJ, Backman L. Differential verbal fluencydeficits in the preclinical stages of Alzheimer's disease and vascular dementia. Cortex 2006; 42:347-355.

[42] ⁴²
Sailor K, Antoine M, Diaz M, Kuslansky G, Kluger A. Theeffects of Alzheimer's disease on item output in verbal fluency tasks. Neuropsychology 2004;18:306-314.

[43] ⁴³
Forbes-McKay KE, Ellis AW, Shanks MF, Venneri A. The ageof acquisition of words produced in a semantic fluency task can reliably differentiate normal from pathological age related cognitive decline. Neuropsychologia 2005;43:1625-1632.

[44] ⁴⁴
Diaz M, Sailor K, Cheung D, Kuslansky G. Category sizeeffects in semantic and letter fluency in Alzheimer's patients. Brain Lang 2004;89:108-114.

[45] ⁴⁵
Fernandez T, Rios C, Santos S et al. "Household items": analternative task to "animals" in the assessment of semantic verbal fluency: a validation study. Rev Neurol (Spanish ) 2002;35:520-523.

[46] ⁴⁶
March EG, Pattison P. Semantic verbal fluency in Alzheimer's disease: approaches beyond the traditional scoring system. J Clin Exp Neuropsychol 2006;28:549-566.

[47] ⁴⁷
Rockwood K, Bowler J, Erkinjuntti T, Hachinski V, Wallin A.Subtypes of vascular dementia. Alzheimer Dis Assoc Disord 1999;13:59-65.

[48] ⁴⁸
Brucki SMD, Rocha MSG. Category fluency test: effects ofage, gender and education on total scores, clustering and switching in Brazilian Portuguese-speaking subjects. Braz J Med Biol Res 2004;37:1771-1777.

[49] ⁴⁹
Henry JD, Crawford JR, Phillips LH. Verbal fluency performance in dementia of the Alzheimer's type:a metaanalysis. Neuropsychologia 2004;42:1212-1222.

[50] ⁵⁰
Testa JA, Ivnik RJ, Boeve B et al. Confrontation naming doesnot add incremental diagnostic utility in MCI and Alzheimer's disease. J Int Neuropsychol Soc 2004;10:504-512.

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