The Clinical Neuropsychologist, 2014 Vol. 28, No. 8, 1321–1335, http://dx.doi.org/10.1080/13854046.2014.986198
Application of a Multidisciplinary Model to a Case Example of Presurgical Epilepsy Planning Nancy L. Nussbaum1, Deborah C. Potvin2, and Dave F. Clarke1 1 2
Dell Children’s Medical Center, The University of Texas at Austin, Austin, TX 78723, USA Children’s National Health System, Rockville, MD 20850, USA
This article presents a case example which illustrates the multidisciplinary model for presurgical assessment for epilepsy patients. Nearly three million people in the United States are diagnosed with epilepsy and more than one third of this population is refractory to pharmacological treatment. Poor seizure control is associated with additional impairment in quality of life and cognitive and social functioning, and even with premature death. In accordance with these concerns, surgical intervention is increasingly recognized as a viable treatment option, which should be considered soon after drug resistance becomes apparent. Despite the widespread evidence of effectiveness surgery is often delayed, in part because of the necessity, and difﬁculties, of correctly applying a multidisciplinary approach to presurgical assessment. And yet, a multidisciplinary team is crucial in the evaluation of risks and beneﬁts of possible surgical intervention and in guiding the surgical procedure to maximize seizure control and minimize risk to eloquent cortex. In the model and complex case presented, the neuropsychologist has a critical role in the presurgical evaluation, as well as in the postsurgical evaluation of outcome. Keywords: Neuropsychology; Epilepsy; Presurgical; Case; Multidisciplinary.
INTRODUCTION Epilepsy is one of the most common neurological conditions, estimated to affect 2.1 to 2.7 million people in the United State (Center for Disease Control and Prevention [CDC], 2012; Hirtz et al., 2007). While the majority of individuals with epilepsy achieve good seizure control through the use of anti-epileptic drugs (AEDs), more than one third continue to experience seizures despite AED treatment (CDC, 2013). After failure of two ﬁrst-line AEDs, the chance for seizure freedom with additional pharmacotherapy can be as low as 4% (Kwan & Brodie, 2000). Increasingly, clinicians are recognizing the dynamic nature of the disease and the association between periods of poor seizure control and additional impairment in quality of life and cognitive and social functioning, and even premature death (Kobau et al., 2008). Thus, seizure control through epilepsy surgery is increasingly being considered crucial to epilepsy treatment, especially for those patients with refractory epilepsy. A recently reported randomized trial of surgical treatment for temporal lobe epilepsy (Engel et al., 2012) has added support to previous research (Weibe, Blume, Girvin, Eliasziw, & Effectiveness and Efﬁciency of Surgery for Temporal Lobe Epilepsy Study Group, 2001) demonstrating
Address correspondence to: Nancy L. Nussbaum, Dell Children’s Medical Center, The University of Texas at Austin, 1301 Barbara Jordan Blvd., Suite 200, Austin, Texas 78723, USA. E-mail: [email protected]
(Received 16 March 2014; accepted 5 November 2014)
© 2014 Taylor & Francis
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the efﬁcacy of surgical intervention. Engel’s team found 11 of 15 (73%) participants in the surgical group and 0 of 23 (0%) in the AED-only group were seizure free during year 2 of the follow-up. Also, participants in the surgical group reported signiﬁcantly better quality of life. Similarly, in the pediatric population, epilepsy surgery has shown signiﬁcant reduction in seizure frequency in 40–80% of children, although outcomes vary by the location of seizure focus and the type of resection (Datta et al., 2011; Devlin et al., 2003; Freitag & Tuxhorn, 2005; Hamiwka et al., 2005). It has been noted in children and adults that the intelligence quotient typically is not affected by epilepsy surgery (Datta et al., 2011). Further evidence for the salutary effect of early surgical intervention is presented in Freitag and Tuxhorn’s 2005 study examining cognitive function in preschool children after epilepsy surgery. Given the low probability of achieving seizure freedom after the failure of two appropriately chosen AEDs, and the signiﬁcant negative consequences of intractable epilepsy, it has been proposed that criteria for eligibility to enter presurgical evaluation should be relatively liberal (Ryvlin & Rheims, 2008). These criteria include disabling seizures, which are intractable to appropriate AED treatment and have focal or localized onset that is amenable to surgical treatment. Despite the strength of this evidence, only a limited number of people with intractable epilepsy will have access to a comprehensive evaluation for possible surgical intervention. The average length of time before referral is 22 years of epilepsy duration, which is over 10 years after the failure of two AEDs (Haneef, Stern, Dewar, & Engel, 2010).
THE MULTIDISCIPLINARY MODEL The evaluation for possible surgical intervention necessarily involves multiple disciplines, including but not limited to neurology, neuroradiology, neuropsychology, and neurosurgery. Neurology is involved throughout the process from identiﬁcation of patients who have intractable seizures, characterizing seizure activity via video electroencephalogram (vEEG) monitoring, and assisting in subdural grid placement and intracranial monitoring. Neuroradiology participates through imaging studies for lesion identiﬁcation and characterization and through functional brain mapping. Neuropsychology provides data to help lateralize and localize the seizure focus, predict risk of postoperative cognitive impairment, establish a baseline, help predict postoperative seizure control, characterize psychosocial functioning, and participate in language and memory assessment via Wada, subdural grids, and imaging (Lee, 2010). Neurosurgery participates in patient selection, prediction of beneﬁt/risk, grid placement, selection of surgical procedure and surgical intervention. The presurgical assessment process and multidisciplinary model for this type of presurgical evaluation is presented below along with an illustrative case example (see Figure 1).
CASE STUDY The patient (BA) is a left-handed, 21-year-old young man. Pregnancy was complicated by ﬁrst trimester bleeding with no further complications. Spontaneous vaginal delivery occurred at 36 weeks with no birth complications. BA was noted to have a
APPLICATION OF MULTIDISCIPLINARY MODEL
Localization of Seizure Focus
Localization of Eloquent Cortex
Figure 1. Multidisciplinary model of presurgical evaluation involving neurology, neuropsychology, neuroradiology, anesthesiology, and neurosurgery. Electroencephalogram (EEG), Vagus nerve stimulator (VNS), magnetic resonance imaging (MRI), single photon emission computed tomography (SPECT), positron emission tomography (PET), magnetoencephalography (MEG)/magnetic source imaging (MSI), subtraction ictal SPECT co-registered to MRI (SISCOM), functional MRI (fMRI), responsive neurostimulation (RNS), deep brain stimulation (dbs), corpus callosotomy (cc), multiple subpial transections (mst), ketogenic diet (KD).
large head size at birth and he was subsequently diagnosed with spina biﬁda occulta, congenital brain malformation characterized by partial absence of the corpus callosum, hydrocephalus requiring a ventriculoperitoneal (VP) shunt, and spastic cerebral palsy primarily in the lower extremities and right arm, with related motor delays, with walking beginning at age 5. VP shunt catheter placement was through the right parieto-occipital region with the tip resting in the lateral ventricle. No other contributory medical history was reported in his records. Epilepsy-related history and presurgical evaluation results are presented below.
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Epilepsy history BA’s history of cerebral palsy signiﬁcantly increased his risk for seizures, and seizure activity was recognized at age 2. His seizures initially presented as febrile evolving to complex partial seizures. He was successfully treated with an AED until age 15. Unfortunately, after age 15, BA’s seizures became intractable, and he continued to have spontaneous unprovoked events despite treatment with multiple AEDs without seizure control, including in order of treatment, phenytoin, carbamazepine, zonisamide, topirimate, levetiracetam, lacosamide, and lamotrigine. Seizure semiology included a vaguely described aura, with BA indicating only that he could predict a seizure. His typical ictal behavior was characterized by freezing in place, left arm posturing, tightening of hands and lip smacking with duration lasting less than 1 minute, and seizures occurring both nocturnally and diurnally. When awake, he demonstrated altered consciousness but did maintain some awareness and sometimes spoke slowly during an event. More speciﬁc information about seizure semiology was gathered while BA was in the epilepsy monitoring unit (EMU). BA was admitted to the EMU for 3 days, his medications were lowered, and he had 14 similar electroclinical events. During video EEG monitoring it was observed that while asleep BA would have eye opening and elevation of his head. He would occasionally appear to motion as if trying to alert someone but this was rapidly followed by unresponsiveness, orobuccal automatisms, and dystonic/tonic posturing of his left upper extremity, with evolution to versive head and eye deviation towards the left. With more prolonged seizures, clonic activity was observed on the left with or without secondary generalization. When BA was presented verbal questions and commands during several seizures, he attempted to sit up utilizing his hand his right upper extremity. He attempted to respond to questions and commands but he responded in a confused, incoherent manner. Immediately after most seizures captured in the EMU, BA was able to speak, although not always coherently, and his memory for the events was unclear. It also was noted after most seizures that he was able to raise his right hand but had difﬁculty raising his left hand to command, suggesting occult paresis. Video EEG monitoring identiﬁed localization-related seizure activity with interictal activity primarily showing right temporal spikes and ictal onset identiﬁed in the right temporoparietal occipital region. More speciﬁcally, consistent with prior EEG documentation, vEEG/EMU monitoring revealed interictal epileptiform discharges predominantly coming from the right temporal region with maximal phase reversal at F8, T4, and T6. These discharges often had a wider ﬁeld involving the perirolandic region and central parietal regions (C4 and P4). Ictal electroencephalographic semiology revealed initial overall rhythmic slowing of the right mid to posterior temporal region (T4, T6) with a ﬁeld also involving the right parietal region (P4>Pz) and contiguous spread to the occipital region (O2) as well as bilateral posterior hemispheres. Secondary bilateral synchronous mode diffuse rhythmicity was often seen with more prolonged events. Magnetic resonance imaging (MRI) data were signiﬁcant for an abnormality in the right occipital lobe, showing a deep sulcus and slight thickening of the cortical ribbon, suggesting a subtle neuronal migrational anomaly. The MRI also was signiﬁcant for dysgenesis of the posterior corpus callosum with remnants of the anterior corpus callosum noted. There was no evidence of mesial temporal sclerosis reported. Also,
APPLICATION OF MULTIDISCIPLINARY MODEL
Figure 2. Axial T1 weighted image showing prominent right lateral occipital sulcus with thickening of the cortical ribbon.
after careful examination, there was no explanation in imaging studies for the lateralized cerebral palsy ﬁndings (greater right side upper extremity involvement; see Figure 2). Multidisciplinary evaluation After over 5 years of suffering intractable epilepsy, BA’s history, vEEG, and MRI data were presented to a multidisciplinary epilepsy team at a regional comprehensive epilepsy center. This team included professionals from the disciplines of neurology, neuropsychology, neuroradiology, and neurosurgery. At the conclusion of the ﬁrst epilepsy conference, it was the recommendation of the team that BA proceed to the next stage of evaluation, which would include gathering neuropsychological, subtraction single-photon emission computed tomography (SPECT), and functional MRI (fMRI) data. This information was reviewed at a second epilepsy conference and the decision was made to recommend subdural grid mapping (vEEG and functional mapping). Of note, it was decided that Wada testing was not viable given behavioral and cognitive limitations. Figure 1 illustrates the decisional ﬂow chart for BA. Neuropsychological findings: Baseline/presurgical. A tailored neuropsychological test battery was chosen to answer the multidisciplinary team’s questions regarding overall cognitive functioning, lateralization and localization of impairment, and lateralization of language functioning. Neuropsychological results are presented
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below in a narrative format more typical to presentation at epilepsy conference. See Table 1 for a quantitative data summary of neuropsychological results. General ﬁndings. BA exhibited a left hand, foot, and eye preference. The only family history of left-handedness is in one second degree relative. Results from the neuropsychological evaluation revealed generalized impairment in all areas: intellectual, language, memory, attention, and motor functioning. Intellectual functioning was found to be in the mild to moderate range of intellectual disability on the Wechsler Abbreviated Scale of Intelligence (WASI) with consistency noted between verbal and nonverbal abilities. A relative strength was noted in basic auditory processing of language on the SCAN-A Test of Auditory Processing Disorders with performance in the average range. Suggestion of bilateral language. BA’s raw scores indicated no clear ear advantage on tasks from the SCAN-A. However, he did show a slightly greater left ear advantage on the two dichotic listening subtests (Competing Words and Competing Sentences). These ﬁndings were particularly remarkable given research showing that patients with disorders compromising the corpus callosum typically exhibit a more pronounced right ear advantage on dichotic listening tasks (Musiek & Weihing, 2011). Suggestion of left hemisphere dysfunction. On a clinical motor exam BA demonstrated spastic cerebral palsy primarily in the lower extremities and right arm. His strength of grip was below average bilaterally with greater strength noted with the left hand. There was bilateral ﬁne motor impairment with slower performance observed with the right hand on the Lafayette Pegboard. Suggestion of non-dominant (right?) hemisphere dysfunction. BA demonstrated severe constructional dyspraxia on the copy portion of the Rey, although this ﬁnding must be interpreted cautiously given BA’s level of generalized neurocognitive impairment (Figure 3). Suggestions of possible cognitive decline. There was a suggestion of a possible decline in verbal abilities from a previous childhood assessment on the Wechsler Intelligence Scale for Children-III (FSIQ = 69) to the current assessment on the WASI (FSIQ = 52). In addition, reading vocabulary (SS = 67) on the Woodcock Johnson – III was found to be somewhat better than verbal abilities on the WASI (SS = 55). Functional MRI (fMRI). The neuropsychologist assisted with the fMRI paradigm selection, training, and administration. Functional imaging data were acquired on a 1.5 Tesla scanner using word generation, verb generation, and auditory word listening paradigms. Via image processing using the Dynasuite Neuro Program the neuroradiologist carried out a clinical interpretation of the data. The results from BA’s fMRI were interpreted by the neuroradiologist as indicative of bilateral language representation with somewhat greater left hemisphere activation. More speciﬁcally, the word generation task was noted to produce symmetrical activity in the superolateral frontal region bilaterally. Mildly increased bilateral activity also was noted in the posterior temporal region. The verb generation task produced increased activity involving left posterior frontal lobe (Broca’s area). Finally, the auditory word listening task produced fairly symmetrical activity in the superior temporal lobe bilaterally. Subtraction single-photon emission computed tomography (SPECT). A subtraction SPECT was acquired using a process whereby interictal images were
APPLICATION OF MULTIDISCIPLINARY MODEL
Table 1. Pre- and post-surgical assessment results Pre-surgical Test
Raw score a
WASI : FSIQ Verbal Comprehension Similarities Vocabulary Perceptual Reasoning Block Design Matrix Reasoning Grip Strength: Right Grip Strength: Left Lafayette Pegboard – 1 row: Right Lafayette Pegboard – 2 rows: Left COWAb RCFTc: Copy Immediate Recall Delayed Recall SCAN-Ad: Auditory FigureGround
14 14 4 8 24/kg 26/kg 166” 148” 5 15 10 2
SS/(T) score 52 55 (20) (20) 56 (23) (20) 65 65