Neuropsychological and quality of life assessment in patients with Parkinson's disease submitted to bilateral deep brain stimulation in the subthalamic nucleus

Heluani, Alessandra Shenandoa; Porto, Fábio Henrique de Gobbi; Listik, Sergio; Campos, Alexandre Walter de; Machado, Alexandre Aluizio Costa; Cukiert, Arthur; Oliveira Jr, José Oswaldo de

doi:10.1590/S1980-57642012DN06040010

ABSTRACT

Deep brain stimulation (DBS) has been widely used to control motor symptoms and improve quality of life in patients with Parkinsons disease (PD). Recently, DBS in the subthalamic nucleus (STN) has become the preferred target for patients with mixed motor symptoms. Despite resultant motor and quality of life improvements, the procedure has been associated with cognitive decline, mainly in language skills, and also with psychiatric symptoms.

Objective:

To evaluate the influence of DBS in the STN on cognition, mood and quality of life.

Methods:

We studied 20 patients with PD submitted to DBS in the STN from May 2008 to June 2012 with an extensive battery of cognitive tests including memory, language, praxis, executive functions and attention assessments; the Parkinson's Disease Quality of Life Questionnaire (PDQ-39); and the Hospital Anxiety and Depression Scale (HAD), were applied both before and after the surgery. Data was analyzed using SPSS version 17.0 and results compared using the paired Student's t test.

Results:

A total of 20 patients with pre and post-operative assessments were included. A statistically significant improvement was found in total score and on subscales of mobility, activities of daily living and emotional well-being from the PDQ-39 (P=0.009, 0.025, 0.001 and 0.034, respectively). No significant difference was found on the cognitive battery or mood scale.

Conclusion:

DBS in the SNT improved quality of life in PD with no negative impact on cognitive skills and mood.

Key words:
deep brain stimulation; subthalamic nucleus; Parkinson's disease; cognitive assessment; quality of life

RESUMO

Estimulação cerebral profunda tem sido utilizada para controle das alterações motoras e melhorar qualidade de vida dos pacientes com Doença de Parkinson (DP). Mais recentemente, DBS em núcleo subtalâmico (STN) tem sido o alvo preferencialmente escolhido para sintomas mistos. Apesar da melhora motora e da qualidade de vida, o procedimento tem sido associado com declínio cognitivo, principalmente na linguagem e distúrbios psiquiátricos.

Objetivo:

Avaliar a influência do DBS em NST na cognição, humor e qualidade de vida.

Métodos:

Nós estudamos 20 pacientes submetidos a DBS em NST no período de Maio de 2008 a Junho de 2012, por meio de uma extensa avaliação neuropsicológica incluindo testes de memória, linguagem, praxia, funções executivas, funções atencionais, Parkinsons Disease Quality of Life Questionnaire (PDQ-39) e Escala Hospitalar de depressão e ansiedade (HAD) na fase pré e pós-operatória. Nós analisamos os dados usando o SPSS versão 17.0 e os resultados foram comparados através do teste pareado t-Student.

Resultados:

Houve melhora estatisticamente significativa no escore total e nas dimensões de mobilidade, atividades de vida diária e bem estar emocional do PDQ-39 (P=0,009, 0,025, 0,001 e 0,034, respectivamente). Diferenças significativas não foram encontradas na bateria cognitiva e nem na escala de humor.

Conclusão:

DBS em SNT melhorou a qualidade de vida nos pacientes com DP sem trazer impacto negativo nas funções cognitivas e humor.

Palavras-chave:
estimulação cerebral profunda; núcleo subtalâmico; doença de Parkinson; qualidade de vida

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REFERENCES

Barbosa ER, Melo LM. A cognição nos distúrbios do movimento. In: Miotto, EC, Lucia MC, Scaff M. Neuropsicologia Clínica. São Paulo: Editora. Roca; 2012.148:159.
Bueno OFA, Oliveira MGM. Doença de Parkinson - aspectos neuropsicológicos. In: Andrade, VM Santos, FH, Bueno, OFA. (Orgs). São Paulo: Artes Médicas; 2004:349-370.
Camargos ACR, Copio FC, Souza TRR, Goulart F. O impacto da doença de Parkinson na qualidade de vida: uma revisão de literatura. Rev Bras Fisioter 2004; 8:267-272.
Lana RC, Goulart FRP, Maia TA, Prudente C, Cardoso F. Estudo da confiabilidade do Questionário de Qualidade de Vida na Doença de Parkinson - 39 (PDQ-39). Anais do Encontro de Extensão da UFMG - Belo Horizonte; 2005.
Souza RG, Borges V, Silva SMCA, Ferraz HB. Quality of life scale in Parkinson's disease - PDQ-39 (Brazilian Portuguese version) to assess patients with and without levodopa motor flutuation. Arq Neuropsiquiatr 2007;65:787-791.
Ferraz FP, Aguiar PMC, Ferraz HB, Bidó JO, Bouza AA, Andrade LAF. Talamotomia e Palidotomia Estereotáxica com planejamento computadorizado no tratamento da Doença de Parkinson - avaliação do desempenho motor a curto prazo de 50 pacientes. Arq Neuropsiquiatr 1998;56:789-797.
Ribas GC. Das trepanações pré-históricas à neuronavegação: evolução histórica das contribuições da neuroanatomia e das técnicas de neuroimagem à prática neurocirúrgica. Arq Bras Neuroc 2006;25:166-175.
Benabid AL, Pollak P, Louveau A, et al. Combined (thalamotomy and stimulation) stereotatic surgery of the Vim Thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 1987;50:344-346.
Limousin P, Pollak P, Benazzouz A, et al. Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995; 345:91-95.
Smeding HMM, Speelman JD, Huizenga HM, Schuurman PR, Schmand B. Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson Disease. J Neurol Neurosurg Psychiatry 2011;82:754-760.
Caixeta L, Vieira RT. Demência na Doença de Parkinson - Revisão. Rev Bras Psiq 2008;30:375-383.
Caixeta L. Demência - abordagem multidisciplinar. São Paulo: Editora Atheneu; 2006:280-295
Castelli L, Rizzi L, Zibetti M, Angrisano S, Lanotte M, Lopiano L. Neuropsychological changes 1-year after subthalamic DBS in patients: A prospective controlled study. Parkinson Relat Disord 2010;16:115-118.
Fasano A, Romito LM, Daniele A, et al. Motor and cognitive outcome in patients with Parkinson's disease 8 years after subthalamic implants. Brain 2010;133:2664-2676
Halpern C, Rick JH Danish SF, Grossman M, Baltuch GH, Cognition following bilateral deep brain stimulation surgery of the subthalamic nucleus for Parkinson's disease. Int J Geriatr Psychiatry 2008;24: 443-451.
Heo JH, Lee KM, Paek SH, et al. The effects of bilateral Subthalamic Nucleus Deep Brain Stimulation (STN DBS) on cognition in Parkinson disease. J Neurol Sci 2008;273:19-24.
Kehagia AA, Barker RA, Robbins TW. Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's Disease. Lancet 2010; 9:1200-1213.
Parsons TD, Rogers SA, Braaten A, Woods SP, Troster AI. Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson's disease: a meta-analysis. Lancet Neurol 2006;5:578-588.
Benabid AL, Chabardes S, Mitropanis J, Pollak P. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's Disease. Lancet 2009;8:67-81.
Bronstein JM, Tagliati M, Alterman RL, et al. Deep Brain Stimulation for Parkinson Disease - An Expert Consensus and Review of Key Issues. (reprinted), Arch Neurol 2011;68:163-171.
Rodrigues-Oroz MC. Deep Brain Stimulation for Advanced Parkinson's Disease. Lancet 2010;29:558-559.
York MK, Dulay M, Macias A, et al. Cognitive declines following bilateral subthalamic nucleus deep brain stimulation for the treatment of Parkinson's disease. J Neurol Neurosurg Psychiatry 2008;79:789-795.
Svenningsson P, Westman E, Ballard C, Aarsland D. Cognitive impairment in patients with Parkinson's disease: diagnosis, biomarkers, and treatment. Lancet 2012; 11:697-707
Zangaglia R, Pacchetti C, Pasotti C, et al. Deep Brain Stimulation and cognitive function in Parkinson's Disease: A Three-Year Controlled Study. Mov Disord 2009;11:1621-1628.
Massano J, Garret C. Deep brain stimulation and cognitive decline in Parkinson's disease: a clinical review. Front Neurol 2012;3:1-13.
Ostergaard K, Sunde NA. Evolution of Parkinson's Disease During 4 years of Bilateral Deep Brain Stimulation of the Subtalamic Nucleus. Moviment Disorders 2006;21:624-631.
Brucki SMD, Nitrini R, Caramelli P, Bertolucci PHF, Okamoto IH. Sugestão para o uso do mini-exame do estado mental no Brasil. Arq Neuropsiquiatr 2003;61:777-781.
Botega NJ, Bio MR, Zogminani MA, Garcia JC, Pereira WAB. Transtorno do humor em enfermaria da clínica médica e validação da escala de medida (HAD) de ansiedade e depressão. Rev Saúde Pública 1995; 29:355-363.
Ringe WK, Saine KC, Laura HL, Linda SH, Munro CC. Dyadic Short Forms of the Wechsler Adult Intelligence Scale-III. Assessment 2002;9: 254-259.
Nascimento E. WAIS-III: Escala de Inteligência Wechsler para Adultos: Manual David Wechsler; Adaptação e padronização de uma amostra brasileira, 1ºed. São Paulo: Casa do Psicólogo; 2004
Brandt J, Benedict RHB. Hopkins Verbal Learning Test-Revised. Odessa: Psychological Assessment Resourse; 2001.
Benedict RHB. Brief Visuoespatial Memory Test-Revised. Odessa: Psychological Assessment Resourse; 1997.
Spreen O, Strauss E. A compendium of Neuropsychological Tests - Administration, norms, and commentary (2nd ed.). Oxford University Press; 1998.
Brucki SMD, Malheiros SMF, Okamoto IH, Bertolucci PHF. Dados Normativos para o teste de fluência verbal categoria animais em nosso meio. Arq Neuropsiquiatr 1997;55:56-61.
Nelson HE. A modified card sorting test sensitive to frontal lobe deficits. Cortex 1976;12:313-324.
Smith A. Symbol Digit Modalities Test. University of Michigan; 2000.
Mansur, LL, Radanovic, M, Araújo, GC. Taquemori, LY, Greco, LL. Teste de Nomeação de Boston: desempenho de uma população de São Paulo. Pró-Fono Revista de Atualização Científica 2006;18:13-20
Spreen, O, Sherman, EMS, Strauss, E. A compendium of Neuropsychological Tests - Administration, norms, and commentary . 3rd ed. Oxford University Press; 2006.
Nitrini R, Caramelli P, Bottino CMC, Damasceno BP, Brucki SMD, Anghinah R. Diagnóstico de doença de Alzheimer no Brasil - Avaliação Cognitiva e Funcional - Recomendações do Departamento Científico de Neurologia Cognitiva e do Envelhecimento da Academia Brasileira de Neurologia. Arq Neuropsiquiatr 2005; 63:720-727
Bôer AGEM, Wijker W, Speelman JD, Haes JCJM. Quality of life in patients with Parkinson's disease: development of a questionnaire. J Neurol Neurosurg Psychiatry 1996;61:70-74.
Carod-Artal FJ, Martinez-Martin P, Vargas AP. Independent validation of Scopa-psychosocial and metric properties of the PDQ-39 Brazilian version. Mov Disord 2007;22:91-98.
Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N. The Parkinson's disease questionnaire (PDQ-39): development and validation of a Parkinson's disease summary index score. Age Ageing 1997;26:353-357.
Jenkinson C, Hefferman C, Doll H. Fitzpatrick R. The Parkinson's Disease Questionnaire (PDQ-39): evidence for a method of imputing missing data. Age Aging 2006;35:497-502.
Goulart F, Pereira LX. Uso de escalas para avaliação da doença de Parkinson em fisioterapia. Fisioter Pesq 2004;2:49-56.
Lana RC, Álvares LMRS, Nasciutti-Prudente C, Goulart FRP. Teixeira-Salmeça LF, Cardoso FE. Percepção da qualidade de vida de indivíduos com Doença de Parkinson através do PDQ-39. Rev Bras Fisioter 2007;11:397-402.
Rito, M. Doença de Parkinson: Instrumentos Avaliativos. Arquivos de Fisioterapia a Revista Portuguesa de Fisioterapia 2006;1:27-45.
Contarino MF, Daniele A, Sibilia AH, et al. Cognitive outcome 5 years after bilateral chronic stimulation of subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 2007;78:248-252.
Guridi J, Rodriguez-Oros MC, Clavero P, Manrique M, Revisión Crítica de La stimulación subtalámica em la enfermidad de Parkinson. Neurocirurgia 2009; 20:521-532
Erola T, Karinen P, Heikkinen E, et. al. Bilateral subthalamic nucleus stimulation improves health-related quality of life in Parkinsonian patients. Parkinson Relat disord 2005;11:89-94.
Nazarro JM, Pahwa R, Lyons KE. The impact of bilateral subthalamic stimulation on non-motor symptoms of Parkinson's disease. Parkinson Relat disord 2011;17:606-609.

Publication Dates

Publication in this collection
Oct-Dec 2012

History

Received
10 Sept 2012
Accepted
13 Nov 2012

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

[1] Barbosa ER, Melo LM. A cognição nos distúrbios do movimento. In: Miotto, EC, Lucia MC, Scaff M. Neuropsicologia Clínica. São Paulo: Editora. Roca; 2012.148:159.

[2] Bueno OFA, Oliveira MGM. Doença de Parkinson - aspectos neuropsicológicos. In: Andrade, VM Santos, FH, Bueno, OFA. (Orgs). São Paulo: Artes Médicas; 2004:349-370.

[3] Camargos ACR, Copio FC, Souza TRR, Goulart F. O impacto da doença de Parkinson na qualidade de vida: uma revisão de literatura. Rev Bras Fisioter 2004; 8:267-272.

[4] Lana RC, Goulart FRP, Maia TA, Prudente C, Cardoso F. Estudo da confiabilidade do Questionário de Qualidade de Vida na Doença de Parkinson - 39 (PDQ-39). Anais do Encontro de Extensão da UFMG - Belo Horizonte; 2005.

[5] Souza RG, Borges V, Silva SMCA, Ferraz HB. Quality of life scale in Parkinson's disease - PDQ-39 (Brazilian Portuguese version) to assess patients with and without levodopa motor flutuation. Arq Neuropsiquiatr 2007;65:787-791.

[6] Ferraz FP, Aguiar PMC, Ferraz HB, Bidó JO, Bouza AA, Andrade LAF. Talamotomia e Palidotomia Estereotáxica com planejamento computadorizado no tratamento da Doença de Parkinson - avaliação do desempenho motor a curto prazo de 50 pacientes. Arq Neuropsiquiatr 1998;56:789-797.

[7] Ribas GC. Das trepanações pré-históricas à neuronavegação: evolução histórica das contribuições da neuroanatomia e das técnicas de neuroimagem à prática neurocirúrgica. Arq Bras Neuroc 2006;25:166-175.

[8] Benabid AL, Pollak P, Louveau A, et al. Combined (thalamotomy and stimulation) stereotatic surgery of the Vim Thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 1987;50:344-346.

[9] Limousin P, Pollak P, Benazzouz A, et al. Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995; 345:91-95.

[10] Smeding HMM, Speelman JD, Huizenga HM, Schuurman PR, Schmand B. Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson Disease. J Neurol Neurosurg Psychiatry 2011;82:754-760.

[11] Caixeta L, Vieira RT. Demência na Doença de Parkinson - Revisão. Rev Bras Psiq 2008;30:375-383.

[12] Caixeta L. Demência - abordagem multidisciplinar. São Paulo: Editora Atheneu; 2006:280-295

[13] Castelli L, Rizzi L, Zibetti M, Angrisano S, Lanotte M, Lopiano L. Neuropsychological changes 1-year after subthalamic DBS in patients: A prospective controlled study. Parkinson Relat Disord 2010;16:115-118.

[14] Fasano A, Romito LM, Daniele A, et al. Motor and cognitive outcome in patients with Parkinson's disease 8 years after subthalamic implants. Brain 2010;133:2664-2676

[15] Halpern C, Rick JH Danish SF, Grossman M, Baltuch GH, Cognition following bilateral deep brain stimulation surgery of the subthalamic nucleus for Parkinson's disease. Int J Geriatr Psychiatry 2008;24: 443-451.

[16] Heo JH, Lee KM, Paek SH, et al. The effects of bilateral Subthalamic Nucleus Deep Brain Stimulation (STN DBS) on cognition in Parkinson disease. J Neurol Sci 2008;273:19-24.

[17] Kehagia AA, Barker RA, Robbins TW. Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's Disease. Lancet 2010; 9:1200-1213.

[18] Parsons TD, Rogers SA, Braaten A, Woods SP, Troster AI. Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson's disease: a meta-analysis. Lancet Neurol 2006;5:578-588.

[19] Benabid AL, Chabardes S, Mitropanis J, Pollak P. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's Disease. Lancet 2009;8:67-81.

[20] Bronstein JM, Tagliati M, Alterman RL, et al. Deep Brain Stimulation for Parkinson Disease - An Expert Consensus and Review of Key Issues. (reprinted), Arch Neurol 2011;68:163-171.

[21] Rodrigues-Oroz MC. Deep Brain Stimulation for Advanced Parkinson's Disease. Lancet 2010;29:558-559.

[22] York MK, Dulay M, Macias A, et al. Cognitive declines following bilateral subthalamic nucleus deep brain stimulation for the treatment of Parkinson's disease. J Neurol Neurosurg Psychiatry 2008;79:789-795.

[23] Svenningsson P, Westman E, Ballard C, Aarsland D. Cognitive impairment in patients with Parkinson's disease: diagnosis, biomarkers, and treatment. Lancet 2012; 11:697-707

[24] Zangaglia R, Pacchetti C, Pasotti C, et al. Deep Brain Stimulation and cognitive function in Parkinson's Disease: A Three-Year Controlled Study. Mov Disord 2009;11:1621-1628.

[25] Massano J, Garret C. Deep brain stimulation and cognitive decline in Parkinson's disease: a clinical review. Front Neurol 2012;3:1-13.

[26] Ostergaard K, Sunde NA. Evolution of Parkinson's Disease During 4 years of Bilateral Deep Brain Stimulation of the Subtalamic Nucleus. Moviment Disorders 2006;21:624-631.

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

[28] Botega NJ, Bio MR, Zogminani MA, Garcia JC, Pereira WAB. Transtorno do humor em enfermaria da clínica médica e validação da escala de medida (HAD) de ansiedade e depressão. Rev Saúde Pública 1995; 29:355-363.

[29] Ringe WK, Saine KC, Laura HL, Linda SH, Munro CC. Dyadic Short Forms of the Wechsler Adult Intelligence Scale-III. Assessment 2002;9: 254-259.

[30] Nascimento E. WAIS-III: Escala de Inteligência Wechsler para Adultos: Manual David Wechsler; Adaptação e padronização de uma amostra brasileira, 1ºed. São Paulo: Casa do Psicólogo; 2004

[31] Brandt J, Benedict RHB. Hopkins Verbal Learning Test-Revised. Odessa: Psychological Assessment Resourse; 2001.

[32] Benedict RHB. Brief Visuoespatial Memory Test-Revised. Odessa: Psychological Assessment Resourse; 1997.

[33] Spreen O, Strauss E. A compendium of Neuropsychological Tests - Administration, norms, and commentary (2nd ed.). Oxford University Press; 1998.

[34] Brucki SMD, Malheiros SMF, Okamoto IH, Bertolucci PHF. Dados Normativos para o teste de fluência verbal categoria animais em nosso meio. Arq Neuropsiquiatr 1997;55:56-61.

[35] Nelson HE. A modified card sorting test sensitive to frontal lobe deficits. Cortex 1976;12:313-324.

[36] Smith A. Symbol Digit Modalities Test. University of Michigan; 2000.

[37] Mansur, LL, Radanovic, M, Araújo, GC. Taquemori, LY, Greco, LL. Teste de Nomeação de Boston: desempenho de uma população de São Paulo. Pró-Fono Revista de Atualização Científica 2006;18:13-20

[38] Spreen, O, Sherman, EMS, Strauss, E. A compendium of Neuropsychological Tests - Administration, norms, and commentary . 3rd ed. Oxford University Press; 2006.

[39] Nitrini R, Caramelli P, Bottino CMC, Damasceno BP, Brucki SMD, Anghinah R. Diagnóstico de doença de Alzheimer no Brasil - Avaliação Cognitiva e Funcional - Recomendações do Departamento Científico de Neurologia Cognitiva e do Envelhecimento da Academia Brasileira de Neurologia. Arq Neuropsiquiatr 2005; 63:720-727

[40] Bôer AGEM, Wijker W, Speelman JD, Haes JCJM. Quality of life in patients with Parkinson's disease: development of a questionnaire. J Neurol Neurosurg Psychiatry 1996;61:70-74.

[41] Carod-Artal FJ, Martinez-Martin P, Vargas AP. Independent validation of Scopa-psychosocial and metric properties of the PDQ-39 Brazilian version. Mov Disord 2007;22:91-98.

[42] Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N. The Parkinson's disease questionnaire (PDQ-39): development and validation of a Parkinson's disease summary index score. Age Ageing 1997;26:353-357.

[43] Jenkinson C, Hefferman C, Doll H. Fitzpatrick R. The Parkinson's Disease Questionnaire (PDQ-39): evidence for a method of imputing missing data. Age Aging 2006;35:497-502.

[44] Goulart F, Pereira LX. Uso de escalas para avaliação da doença de Parkinson em fisioterapia. Fisioter Pesq 2004;2:49-56.

[45] Lana RC, Álvares LMRS, Nasciutti-Prudente C, Goulart FRP. Teixeira-Salmeça LF, Cardoso FE. Percepção da qualidade de vida de indivíduos com Doença de Parkinson através do PDQ-39. Rev Bras Fisioter 2007;11:397-402.

[46] Rito, M. Doença de Parkinson: Instrumentos Avaliativos. Arquivos de Fisioterapia a Revista Portuguesa de Fisioterapia 2006;1:27-45.

[47] Contarino MF, Daniele A, Sibilia AH, et al. Cognitive outcome 5 years after bilateral chronic stimulation of subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 2007;78:248-252.

[48] Guridi J, Rodriguez-Oros MC, Clavero P, Manrique M, Revisión Crítica de La stimulación subtalámica em la enfermidad de Parkinson. Neurocirurgia 2009; 20:521-532

[49] Erola T, Karinen P, Heikkinen E, et. al. Bilateral subthalamic nucleus stimulation improves health-related quality of life in Parkinsonian patients. Parkinson Relat disord 2005;11:89-94.

[50] Nazarro JM, Pahwa R, Lyons KE. The impact of bilateral subthalamic stimulation on non-motor symptoms of Parkinson's disease. Parkinson Relat disord 2011;17:606-609.

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