Lateralising Value of Neuropsychological Protocols for Presurgical Assessment of Temporal Lobe Epilepsy
Nozomi Akanuma
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorGonzalo Alarcón
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorFrancis Lum
Department of Psychiatry, Chinese University of Hong Kong, Hong Kong, China; and
Search for more papers by this authorNajib Kissani
Department of Neurology, El Razi Universitary Hospital, Marrakech, Morocco
Search for more papers by this authorMichael Koutroumanidis
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorNaoto Adachi
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorColin D. Binnie
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorCharles E. Polkey
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorRobin G. Morris
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorNozomi Akanuma
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorGonzalo Alarcón
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorFrancis Lum
Department of Psychiatry, Chinese University of Hong Kong, Hong Kong, China; and
Search for more papers by this authorNajib Kissani
Department of Neurology, El Razi Universitary Hospital, Marrakech, Morocco
Search for more papers by this authorMichael Koutroumanidis
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorNaoto Adachi
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorColin D. Binnie
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorCharles E. Polkey
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorRobin G. Morris
Division of Neuroscience, Guy's, King's, and St Thomas' School of Medicine, King's College London, London, England;
Search for more papers by this authorAbstract
Summary: Purpose: To estimate the value of neuropsychological measurements in determining the side of seizure onset for presurgical assessment in patients with temporal lobe epilepsy. The lateralising value of neuropsychological protocols was evaluated for all patients and in subpopulations depending on surgical outcome with regard to seizure control, speech dominance, neuropathology, and need for intracranial EEG recordings.
Methods: A battery of neuropsychological procedures was carried out preoperatively in 125 patients who underwent left (n = 66) or right (n = 59) temporal lobectomies. Binary logistic regression analysis was performed to find sets of variables that allowed the best prediction of the side of seizure onset (assumed to be the operated-on side).
Results: Combinations of noninvasive neuropsychological tests and Wada subscores showed the highest lateralising values: 80.8% for all patients, 79.4% in seizure-free patients, 86.0% in patients not rendered seizure free, 85.7% in left speech patients, 77.8% in non–left speech patients, 89.3% in patients with mesial temporal sclerosis (MTS), 78.1% in non-MTS patients, 80.3% in patients who underwent intracranial EEG recordings, and 77.3% in those who did not.
Conclusions: The lateralising value (80-90%) of neuropsychological protocols appears similar to that of other tests widely accepted for lateralisation (ictal and interictal scalp EEG and neuroimaging). Attention should be paid to neuropsychological results, particularly from the Wada test, during presurgical assessment of temporal lobe epilepsy, as they can provide strong support for findings from other lateralising tests, particularly in patients with presumed MTS or in left-speech patients.
REFERENCES
- 1 Hermann BP, Wyler AR, Richey ET, et al. Memory function and verbal learning ability in patients with complex partial seizures of temporal lobe origin. Epilepsia 1987; 28: 547–54.
- 2 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: 781–7.
- 3 Sass KJ, Spencer DD, Kim JH, et al. Verbal memory impairment correlates with hippocampal pyramidal cell density. Neurology 1990; 40: 1694–7.
- 4 O'Rourke DM, Saykin AJ, Gilhool JJ, et al. Unilateral hemispheric memory and hippocampal neuronal density in temporal lobe epilepsy. Neurosurgery 1993; 32: 574–80.
- 5 Ferrier CH, Alarcón G, Glover A, et al. N-Acetylaspartate and creatine levels measured by 1H MRS relate to recognition memory. Neurology 2000; 55: 1874–83.
- 6 Aarts JH, Binnie CD, Smit AM, et al. Selective cognitive impairment during focal and generalized epileptiform EEG activity. Brain 1984; 107: 293–308.
- 7 Jones-Gotman M, Smith ML, Zatorre RJ. Neuropsychological testing for localizing and lateralizing the epileptogenic region. In: J Engel, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1993: 245–61.
- 8 Christianson SA, Saisa J, Silfvenius H. Hemisphere memory differences in sodium amytal testing of epileptic patients. J Clin Exp Neuropsychol 1990; 12: 681–94.
- 9 Perrine K, Gershengorn J, Brown ER, et al. Material-specific memory in the intracarotid amobarbital procedure. Neurology 1993; 43: 706–11.
- 10 Glosser G, Saykin AJ, Deutsch GK, et al. Neural organization of material-specific memory functions in temporal lobe epilepsy patients as assessed by the intracarotid amobarbital test. Neuropsychology 1995; 9: 449–56.
- 11 Roman DD, Beniak TE, Nugent S. Memory performance on the intracarotid amobarbital procedure as a predicator of seizure focus. Epilepsy Res 1996; 25: 243–8.
- 12 Kneebone AC, Chelune GJ, Luders HO. Individual patient prediction of seizure lateralization in temporal lobe epilepsy: a comparison between neuropsychological memory measures and the intracarotid amobarbital procedure. J Int Neuropsychol Soc 1997; 3: 159–68.
- 13 Loring DW, Hermann BP, Perrine K, et al. Effect of Wada memory stimulus type in discriminating lateralized temporal lobe impairment. Epilepsia 1997; 38: 219–24.
- 14 Glosser G, Deutsch GK, Cole LC, et al. Differential lateralization of memory discrimination and response bias in temporal lobe epilepsy patients. J Int Neuropsychol Soc 1998; 4: 502–11.
- 15 Wada JA, Rasmussen T. Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance: experimental and clinical observations. J Neurosurg 1960; 17: 266–82.
- 16 Milner B, Branch C, Rasmussen T. Study of short-term memory after intracarotid injection of sodium amytal. Trans Am Neurol Assoc 1962; 87: 224–6.
- 17 Wyllie E, Naugle R, Chelune G, et al. Intracarotid amobarbital procedure, II: lateralizing value in evaluation for temporal lobectomy. Epilepsia 1991; 32: 865–9.
- 18 Perrine K, Westerveld M, Sass KJ, et al. Wada memory disparities predict seizure laterality and postoperative seizure control. Epilepsia 1995; 36: 851–6.
- 19 Breier JI, Thomas AB, Plenger PM, et al. Asymmetries in the effect of side of seizure onset on recognition memory following intracarotid amobarbital injection. Epilepsia 1997; 38: 1209–15.
- 20 Spencer DC, Morrell MJ, Risinger MW. The role of the intracarotid amobarbital procedure in evaluation of patients for epilepsy surgery. Epilepsia 2000; 41: 320–5.
- 21 Morris RG, Polkey CE, Cox T. Independent recovery of memory and language functioning during the intracarotid sodium amytal test. J Clin Exp Neuropsychol 1998; 20: 433–44.
- 22 Rausch R, Walsh GO. Right-hemisphere language dominance in right-handed epileptic patients. Arch Neurol 1984; 41: 1077–80.
- 23 Powell GE, Polkey CE, Canavan AG. Lateralisation of memory functions in epileptic patients by use of the sodium amytal (Wada) technique. J Neurol Neurosurg Psychiatry 1987; 50: 665–72.
- 24 Wechsler D. The Wechsler Adult Intelligence Scale–Revised. New York: The Psychological Corporation, 1987.
- 25 Canavan AG, Dunn G, McMillan TM. Principal components of the WAIS-R. Br J Clin Psychol 1986; 25: 81–5.
- 26 Wechsler D. The Wechsler Memory Scale manual. New York: The Psychological Corporation, 1945.
- 27 Goldstein LH, Polkey CE. Short-term cognitive changes after unilateral temporal lobectomy or unilateral amygdalo-hippocampectomy for the relief of temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 1993; 56: 135–40.
- 28 Morton N, Polkey CE, Cox T, et al. Episodic memory dysfunction during sodium amytal testing of epileptic patients in relation to posterior cerebral artery perfusion. J Clin Exp Neuropsychol 1996; 18: 24–37.
- 29 Engel J Jr, Van Ness PC, Rasmussen TB, et al. Outcome with respect to epileptic seizures. In: J Engel, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1993: 609–21.
- 30 SPSS. SPSS regression models 9.0. Chicago: SPSS Inc., 1999.
- 31 Haberman SJ. The analysis of residuals in cross-classified tables. Biometrics 1973; 29: 205–20.
- 32 Hamberger MJ, Walczak TS, Goodman RR. Intracarotid amobarbital procedure memory performance and age at first risk for seizures distinguish between lateral neocortical and mesial temporal lobe epilepsy. Epilepsia 1996; 37: 1088–92.
- 33 Davies KG, Bell BD, Dohan FC, et al. Prediction of presence of hippocampal sclerosis from intracarotid amobarbital procedure memory asymmetry scores and epilepsy on set age. Epilepsy Res 1999; 33: 117–23.
- 34 Hennessy MJ, Elwes RD, Binnie CD, et al. Failed surgery for epilepsy: a study of persistence and recurrence of seizures following temporal resection. Brain 2000; 123: 2445–66.
- 35 Strauss E, Hunter M, Hermann BP, et al. Differential rates of age of seizure onset between sexes and between hemispheres? J Int Neuropsychol Soc 1997; 3: 428–34.
- 36 Loring DW, Strauss E, Hermann BP, et al. Effects of anomalous language representation on neuropsychological performance in temporal lobe epilepsy. Neurology 1999; 53: 260–4.
- 37 Alpherts WC, Vermeulen J, Van Veelen CW. The Wada test: prediction of focus lateralization by asymmetric and symmetric recall. Epilepsy Res 2000; 39: 239–49.
- 38 Adachi N, Alarcón G, Binnie CD, et al. Predictive value of interictal epileptiform discharges during non-REM sleep on scalp EEG recordings for the lateralization of epileptogenesis. Epilepsia 1998; 39: 628–32.
- 39 Serles W, Caramanos Z, Lindinger G, et al. Combining ictal surface-electroencephalography and seizure semiology improves patient lateralization in temporal lobe epilepsy. Epilepsia 2000; 41: 1567–73.
- 40 Alarcon G, Kissani N, Dad M, et al. Lateralizing and localizing values of ictal onset recorded on the scalp: evidence from simultaneous recordings with intracranial foramen ovale electrodes. Epilepsia 2001; 42: 1426–37.
- 41 Menzel C, Hufnagel A, Grunwald F, et al. The relevance of interictal rCBF brain SPECT in temporal lobe epilepsy: diagnostic value and effects of spatial resolution. Ann Nucl Med 1995; 9: 215–23.
- 42 Newton MR, Berkovic SF, Austin MC, et al. Ictal postictal and interictal single-photon emission tomography in the lateralization of temporal lobe epilepsy. Eur J Nucl Med 1994; 21: 1067–71.
- 43 Ho SS, Berkovic SF, Berlangieri SU, et al. Comparison of ictal SPECT and interictal PET in the presurgical evaluation of temporal lobe epilepsy. Ann Neurol 1995; 37: 738–45.
- 44 Henry TR, Chugani HT, Abou-Khalil BW, et al. Positron emission tomography. In: J Engel, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1993: 211–32.
- 45 Kuzniecky R, Suggs S, Gaudier J, et al. Lateralization of epileptic foci by magnetic resonance imaging in temporal lobe epilepsy. J Neuroimaging 1991; 1: 163–7.
- 46 Lee DH, Gao FQ, Rogers JM, et al. MR in temporal lobe epilepsy: analysis with pathologic confirmation. AJNR Am J Neuroradiol 1998; 19: 19–27.