Pre- and post-operative Wisconsin card sorting test performance in patients with temporal lobe epilepsy due to hippocampal sclerosis

Tisser, Luciana; Palmini, Andre; Paglioli, Eliseu; Portuguez, Mirna; Azambuja, Ney; Costa, Jaderson Costa da; Paglioli, Eduardo; Torres, Carolina; Martinez, Jose Victor

doi:10.1590/S1980-57642008DN10200010

Abstract

Patients with temporal lobe epilepsy due to hippocampal sclerosis (TLE/HS) have a distinct neuropsychological profile, but there is still debate on whether executive dysfunction is part of this profile and also whether temporal lobe surgery can modify this dysfunction.

Objective:

To study the presence and reversibility of executive dysfunction in patients with unilateral TLE/HS.

Methods:

Twenty-five patients with refractory seizures due to TLE/HS underwent presurgical evaluation which included the application of the Wiconsin Card Sorting Test (WCST). Nineteen were re-evaluated in follow up, at least 6 months after selective amygdalo-hippocampectomy (SAH). Twenty-two control subjects matched for age and education also performed the WCST.

Results:

Sixteen of the 25 patients (64%) completed fewer than four categories in the WCST whereas only 4 of the 22 controls (18%) did not complete at least four categories (p<0.005). In addition, the performance of the patients involved significantly more perseverative responses and errors compared to controls. The patient group demonstrated significant post-operative improvement in many measures of the WCST following SAH.

Conclusions:

These findings support the presence of executive dysfunction in patients with TLE/HS and suggest that such dysfunction can be partially reversed by selective resection of epileptogenic mesial temporal structures.

Key words:
temporal lobe epilepsy; hippocampal sclerosis; executive dysfunction; Wisconsin card sorting test; epilepsy surgery

Resumo

Pacientes com epilepsia de lobo temporal associada à esclerose hipocampal (ELT/EH) têm um perfil neuropsicológico em sua maior parte bem reconhecido, embora discuta-se se manifestações de disfunção executiva acompanham este perfil e se esta disfunção poderia ser modificada por cirurgia da epilepsia de lobo temporal.

Objetivo:

Estudar a presença e reversibilidade da disfunção executiva em pacientes com ELT/EH unilateral.

Métodos:

Vinte e cinco pacientes com crises refratárias associadas à ELT/EH foram submetidos à avaliação pré-cirúrgica que incluiu a aplicação do Teste de Seleção de Cartas de Wisconsin (TSCW). Dezenove foram reavaliados um mínimo de 6 meses após amígdalo-hipocampectomia seletiva (AHS). O TSCW foi também aplicado a 22 indivíduos controles pareados por idade e nível educacional.

Resultados:

Dezesseis dos 25 pacientes (64%) completaram menos de quatro categorias no TSCW, enquanto que apenas 4 dos 22 indivíduos do grupo controle (18%) tiveram este mesmo nível e disfunção (p<0.005). Além disto, a performance dos pacientes aresentava significativamente mais respostas e erros perseverativos do que os controles. Analisados como um grupo, os pacientes apresentaram melhoras significativas em várias medidas do TSCW após AHS.

Conclusão:

Estes achados apontam para a presença de disfunção executiva em pacientes com ELT/EH e sugerem que esta disfunção pode ser parcialmente revertida pela ressecção seletiva das estruturas temporais mesiais epileptogênicos.

Palavras-chave:
epilepsia do lobo temporal; escleroses hipocampal; disfunção executiva; Wisconsin card sorting test; cirurgia da epilepsia.

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Full text available only in PDF format.

References

¹
Engel J Jr. Surgery for seizures. N Engl J Med 1996;334:647-652.
²
Wiebe S, Blume WT, Girvin JP, et al. A randomized controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 2001;345:311-318.
³
Semah F, Picot MC, Adam MD et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence ? Neurology 1998;51:1256-1262.
⁴
Briellmann RS, Kalnins RM, Berkovic SF, Jackson GD. Hippocampal pathology in refractory temporal lobe epilepsy: T2-weighted signal change reflects dentate gliosis. Neurology 2002;58:265-271.
⁵
Williamson P, French JA, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results and pathology. Ann Neurol 1993;34:781-787.
⁶
Paglioli E, Palmini A, Paglioli E, et al. Survival Analysis of the surgical outcome of temporal lobe epilepsy due to hippocampal sclerosis. Epilepsia 2004;45:1383-1391.
⁷
Paglioli E, Palmini A, Portuguez M, et al. Seizure and memory outcome following temporal lobe surgery: selective compared with nonselective approaches for hippocampal sclerosis. J Neurosurg 2006;104:70-78.
⁸
McLachlan RS, Rose KJ, Derry PA, et al. Health-related quality of life and seizure control in temporal lobe epilepsy. Ann Neurol 1997;41:482-489.
⁹
Mikati MA, Comair YG, Rahi A. Normalization of quality of life trhee years afther temporal lobectomy: a controlled study. Epilepsia 2006;47:928-933.
¹⁰
Dupont S, Tanguy ML, Clemenceau S, Adam C, Hazemann P, Baulac M. Long-term prognosis and psychosocial outcomes afther surgery for MTLE. Epilepsia 2006;47:2115-2124.
¹¹
Baker GA, Gagnon D, McNulty P. The relationship between seizure frequency, seizure type, and quality of life: findings from three European countries. Epilepsy Res 1998;31: 231-240.
¹²
Jones-Gotman M. Commentary: Psychological evaluation. Testing hippocampal function. In: Engel J Jr, editor. Surgical Treatment of the Epilepsies. New York: Raven Press; 1987: 203-211.
¹³
Hermann BP, Seidenberg M, Schoenfeld J, Davis MD. Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Arch Neurol 1997;54:369-376.
¹⁴
Helmstaedter C. Neuropsychological aspects of epilepsy surgery. Epilepsy & Behavior 2004;5(suppl 1):S45-S55.
¹⁵
Kier EL, Staib LH, Davis LM, Bronen RA. Dissection tractography of the uncinate fasciculus, inferior occipital fasciculus, and Meyer's loop of the optic radiation. AJNR 2004;25:677-691.
¹⁶
Giovagnoli AR. Relation of sorting impairment to hippocampal damage in temporal lobe epilepsy. Neuropsychologia. 2001;39:140-150.
¹⁷
Drake M, Allegri RF, Thomson A. Alteracion cognitiva ejecutiva de tipo prefrontal en pacientes con epilepsia del lobulo temporal mesial. Medicina 2000;60:453-456.
¹⁸
Martin RC, Sawrie SM, Gilliam FG, Palmer CA, Faught E. Winsconsin card Sorting performance in patients with temporal lobe epilepsy: clinical and neuroanatomical correlates. Epilepsia 2000;41:1626-1632.
¹⁹
Hermann B, Seidenberg M. Executive system dysfunction in temporal lobe epilepsy: effects of nociferous cortex versus hippocampal pathology. J Clin Exp Neuropsychol 1995;17:809-819.
²⁰
Sheehan D, Lecrubeier Y, Sheehan KH, et al. The Mini International Neuropsychiatric Interview (MINI): The Dvelopment and Validation of a Structured Diagnostic Psychiatric Interview for DSM- IV and CID-10. J Clin Psychiatry 1998;59(suppl 20):22-33.
²¹
Palmini A, Gloor P. The localizing value of auras in partial seizures: a prospective and retrospective study. Neurology 1992;42:801-808.
²²
French JA, Williamson P, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann Neurol 1993;34:774-780.
²³
Williamson PD, French JA, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results and pathology. Ann Neurol 1993;34:781-787.
²⁴
Wechsler D. Teste de inteligência para adultos WAIS-III. Adaptação e Padronização Brasileira. São Paulo: Casa do Psicólogo; 2005.
²⁵
Wescheler D. Weschler Memory Scale-revised. San Antonio: The Psychological Corporation; 1987.
²⁶
Cunha JA, Trentini CM, Argimon IL, et al. Wisconsin de Classificação de Cartas. Manual revisado e ampliado. Adaptação e Padronização Brasileira. São Paulo: Casa do Psicólogo; 2005.
²⁷
Cunha JA. Manual da versão em português das Escalas Beck. São Paulo: Casa do Psicólogo; 2001.
²⁸
Chelune GJ, Baer RA. Developmental norms for the Wisconsin Card Sorting test. J Clin Exp Neuropsychol 1986;8:219-228.
²⁹
Niemeyer P. The transventricular amygdalohippocampectomy in temporal lobe epilepsy. In: Baldwin M, Bailey P, editors. Temporal Lobe Epilepsy. Springfield, Il: Charles C. Thomas; 1958:461-482.
³⁰
Martin RC, Sarwrie SM, Edwards R, et al. Investigation of executive function change following anterior temporal lobectomy: selective normalization of verbal fluency. Neuropsychology 2000;14:501-508.
³¹
Lieb JP, Dasheiff RM, Engel JJr. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia. 1991;32:822-837.
³²
Savic I, Altshuler L, Baxter L, Engel JJr. Pattern of interictal hypometabolism in PET scans with fludeoxyglucose F 18 reflects prior seizure types in patients with mesial temporal lobe seizures. Arch Neurol 1997;54:129-136.
³³
Van Paesschen W, Dupont P, Van Driel G, Van Billoen H, Maes A. SPECT perfusion changes during complex partial seizures in patients with hippocampal sclerosis. Brain 2003;126:1103-1111.
³⁴
Nelissen N, Van Paesschen W, Baete K, et al. Correlations of interictal FDG-PET metabolism and ictal SPECT perfusion changes in human temporal lobe epilepsy with hippocampal sclerosis. Neuroimage 2006;32:684-695.
³⁵
Takaya S, Hanakawa T, Hashikawa K, et al. Prefontral hypofunction in patients with intractable mesial temporal lobe epilepsy. Neurology 2006;67:1674-1676.
³⁶
Getz K, Hermann BP, Bell B, et al. Negative symptoms in temporal lobe epilepsy. Am J Psychiatry 2002;59:644-651.
³⁷
Getz K, Hermann B, Seidenberg M, et al. Negative symptoms and psychosocial status in temporal lobe epilepsy. Epilepsy Res 2003;53:240-244.
³⁸
Baddeley A. The episodic buffer: a new component of working memory? Trends Cogn Sci 2000;4:417-423.
³⁹
Palmini A, Haase VG. 'To do or not to do'? The neurobiology of decision-making in daily life: I: Getting the basics. Dement Neuropsychol 2007;1:10-17.
⁴⁰
Hermann BP, Wyler AR, Ritchie ET. Wisconsin Card Sorting Test performance in patients with complex partial seizures of temporal lobe origin. J Clin Exp Neuropsychology 1988;10:467-476.
⁴¹
Kim CH, Lee AS, Yoo HJ, Kang JK, Lee JK. Executive performance on the wisconsin card sorting test in temporal lobe epilepsy. Eur Neurol 2007;57:39-46
⁴²
Ingram F, Greve KW, Ingram PTF, Soukup VM. Temporal stability of the Wisconsin Card Sorting Test in an untreated patient sample. Br J Clin Psychol 1999;38:209-211.

Publication Dates

Publication in this collection
Apr-Jun 2007

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

[1] ¹
Engel J Jr. Surgery for seizures. N Engl J Med 1996;334:647-652.

[2] ²
Wiebe S, Blume WT, Girvin JP, et al. A randomized controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 2001;345:311-318.

[3] ³
Semah F, Picot MC, Adam MD et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence ? Neurology 1998;51:1256-1262.

[4] ⁴
Briellmann RS, Kalnins RM, Berkovic SF, Jackson GD. Hippocampal pathology in refractory temporal lobe epilepsy: T2-weighted signal change reflects dentate gliosis. Neurology 2002;58:265-271.

[5] ⁵
Williamson P, French JA, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results and pathology. Ann Neurol 1993;34:781-787.

[6] ⁶
Paglioli E, Palmini A, Paglioli E, et al. Survival Analysis of the surgical outcome of temporal lobe epilepsy due to hippocampal sclerosis. Epilepsia 2004;45:1383-1391.

[7] ⁷
Paglioli E, Palmini A, Portuguez M, et al. Seizure and memory outcome following temporal lobe surgery: selective compared with nonselective approaches for hippocampal sclerosis. J Neurosurg 2006;104:70-78.

[8] ⁸
McLachlan RS, Rose KJ, Derry PA, et al. Health-related quality of life and seizure control in temporal lobe epilepsy. Ann Neurol 1997;41:482-489.

[9] ⁹
Mikati MA, Comair YG, Rahi A. Normalization of quality of life trhee years afther temporal lobectomy: a controlled study. Epilepsia 2006;47:928-933.

[10] ¹⁰
Dupont S, Tanguy ML, Clemenceau S, Adam C, Hazemann P, Baulac M. Long-term prognosis and psychosocial outcomes afther surgery for MTLE. Epilepsia 2006;47:2115-2124.

[11] ¹¹
Baker GA, Gagnon D, McNulty P. The relationship between seizure frequency, seizure type, and quality of life: findings from three European countries. Epilepsy Res 1998;31: 231-240.

[12] ¹²
Jones-Gotman M. Commentary: Psychological evaluation. Testing hippocampal function. In: Engel J Jr, editor. Surgical Treatment of the Epilepsies. New York: Raven Press; 1987: 203-211.

[13] ¹³
Hermann BP, Seidenberg M, Schoenfeld J, Davis MD. Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Arch Neurol 1997;54:369-376.

[14] ¹⁴
Helmstaedter C. Neuropsychological aspects of epilepsy surgery. Epilepsy & Behavior 2004;5(suppl 1):S45-S55.

[15] ¹⁵
Kier EL, Staib LH, Davis LM, Bronen RA. Dissection tractography of the uncinate fasciculus, inferior occipital fasciculus, and Meyer's loop of the optic radiation. AJNR 2004;25:677-691.

[16] ¹⁶
Giovagnoli AR. Relation of sorting impairment to hippocampal damage in temporal lobe epilepsy. Neuropsychologia. 2001;39:140-150.

[17] ¹⁷
Drake M, Allegri RF, Thomson A. Alteracion cognitiva ejecutiva de tipo prefrontal en pacientes con epilepsia del lobulo temporal mesial. Medicina 2000;60:453-456.

[18] ¹⁸
Martin RC, Sawrie SM, Gilliam FG, Palmer CA, Faught E. Winsconsin card Sorting performance in patients with temporal lobe epilepsy: clinical and neuroanatomical correlates. Epilepsia 2000;41:1626-1632.

[19] ¹⁹
Hermann B, Seidenberg M. Executive system dysfunction in temporal lobe epilepsy: effects of nociferous cortex versus hippocampal pathology. J Clin Exp Neuropsychol 1995;17:809-819.

[20] ²⁰
Sheehan D, Lecrubeier Y, Sheehan KH, et al. The Mini International Neuropsychiatric Interview (MINI): The Dvelopment and Validation of a Structured Diagnostic Psychiatric Interview for DSM- IV and CID-10. J Clin Psychiatry 1998;59(suppl 20):22-33.

[21] ²¹
Palmini A, Gloor P. The localizing value of auras in partial seizures: a prospective and retrospective study. Neurology 1992;42:801-808.

[22] ²²
French JA, Williamson P, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann Neurol 1993;34:774-780.

[23] ²³
Williamson PD, French JA, Thadani VM, et al. Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results and pathology. Ann Neurol 1993;34:781-787.

[24] ²⁴
Wechsler D. Teste de inteligência para adultos WAIS-III. Adaptação e Padronização Brasileira. São Paulo: Casa do Psicólogo; 2005.

[25] ²⁵
Wescheler D. Weschler Memory Scale-revised. San Antonio: The Psychological Corporation; 1987.

[26] ²⁶
Cunha JA, Trentini CM, Argimon IL, et al. Wisconsin de Classificação de Cartas. Manual revisado e ampliado. Adaptação e Padronização Brasileira. São Paulo: Casa do Psicólogo; 2005.

[27] ²⁷
Cunha JA. Manual da versão em português das Escalas Beck. São Paulo: Casa do Psicólogo; 2001.

[28] ²⁸
Chelune GJ, Baer RA. Developmental norms for the Wisconsin Card Sorting test. J Clin Exp Neuropsychol 1986;8:219-228.

[29] ²⁹
Niemeyer P. The transventricular amygdalohippocampectomy in temporal lobe epilepsy. In: Baldwin M, Bailey P, editors. Temporal Lobe Epilepsy. Springfield, Il: Charles C. Thomas; 1958:461-482.

[30] ³⁰
Martin RC, Sarwrie SM, Edwards R, et al. Investigation of executive function change following anterior temporal lobectomy: selective normalization of verbal fluency. Neuropsychology 2000;14:501-508.

[31] ³¹
Lieb JP, Dasheiff RM, Engel JJr. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia. 1991;32:822-837.

[32] ³²
Savic I, Altshuler L, Baxter L, Engel JJr. Pattern of interictal hypometabolism in PET scans with fludeoxyglucose F 18 reflects prior seizure types in patients with mesial temporal lobe seizures. Arch Neurol 1997;54:129-136.

[33] ³³
Van Paesschen W, Dupont P, Van Driel G, Van Billoen H, Maes A. SPECT perfusion changes during complex partial seizures in patients with hippocampal sclerosis. Brain 2003;126:1103-1111.

[34] ³⁴
Nelissen N, Van Paesschen W, Baete K, et al. Correlations of interictal FDG-PET metabolism and ictal SPECT perfusion changes in human temporal lobe epilepsy with hippocampal sclerosis. Neuroimage 2006;32:684-695.

[35] ³⁵
Takaya S, Hanakawa T, Hashikawa K, et al. Prefontral hypofunction in patients with intractable mesial temporal lobe epilepsy. Neurology 2006;67:1674-1676.

[36] ³⁶
Getz K, Hermann BP, Bell B, et al. Negative symptoms in temporal lobe epilepsy. Am J Psychiatry 2002;59:644-651.

[37] ³⁷
Getz K, Hermann B, Seidenberg M, et al. Negative symptoms and psychosocial status in temporal lobe epilepsy. Epilepsy Res 2003;53:240-244.

[38] ³⁸
Baddeley A. The episodic buffer: a new component of working memory? Trends Cogn Sci 2000;4:417-423.

[39] ³⁹
Palmini A, Haase VG. 'To do or not to do'? The neurobiology of decision-making in daily life: I: Getting the basics. Dement Neuropsychol 2007;1:10-17.

[40] ⁴⁰
Hermann BP, Wyler AR, Ritchie ET. Wisconsin Card Sorting Test performance in patients with complex partial seizures of temporal lobe origin. J Clin Exp Neuropsychology 1988;10:467-476.

[41] ⁴¹
Kim CH, Lee AS, Yoo HJ, Kang JK, Lee JK. Executive performance on the wisconsin card sorting test in temporal lobe epilepsy. Eur Neurol 2007;57:39-46

[42] ⁴²
Ingram F, Greve KW, Ingram PTF, Soukup VM. Temporal stability of the Wisconsin Card Sorting Test in an untreated patient sample. Br J Clin Psychol 1999;38:209-211.

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