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Seizure 19 (2010) 659–668

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Seizure

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Review Diverse perspectives on developments in surgery

Sarah J. Wilson a,b,*, Jerome Engel Jr.c

a Psychological Sciences, The University of Melbourne, Australia b Comprehensive Epilepsy Program, Austin Health, Melbourne, Australia c Department of Neurology, Neurobiology, and Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA

ARTICLE INFO ABSTRACT

Keywords: The objective of this article is to review the dramatic changes that have occurred in the field of History since the founding of Epilepsy Action in 1950. We have chosen to consider these Epilepsy surgery advances from the biomedical perspective (the physician and basic scientist), and the behavioral Seizure outcome perspective (the psychologist and the patient). Both these viewpoints are equally important in Cognition understanding the evolution of epilepsy surgery over the past 60 years, but may not always be well Psychosocial synchronized. Quality of life ß 2010 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.

1. Introduction greatly enhanced by development of in 191910 and cerebral in 1934.11 Also at this time, a To put this review in historical perspective, the modern era of revolutionary approach to monitoring both normal and abnormal surgical treatment for epilepsy was some 70 years old by the time brain function was being developed.12,13 The electroencephalo- of the founding of Epilepsy Action, with initial seminal work gram (EEG) allowed patterns associated with epilepsy to be having been already performed in the United Kingdom.1 In 1879, recognized,14 and the ability of EEG interictal spikes to localize Macewen2 of Glasgow reported the first resection of an epileptogenic tissue, including identification of mesial temporal ‘‘invisible’’ lesion to treat epilepsy based on localization derived structures as the site of onset of psychomotor seizures.15 Yet from the clinical seizure observations of John Hughlings Jackson,3 despite EEG later playing a critical role in epilepsy surgery, by followed by a report on a series of cases in 1881.4 Five years later, 1950 it played no role in the standard lesion-based approach to Victor Horsley published his seminal paper in Brain,5 combining epilepsy surgery. There were very few centers capable of clinical–pathological correlations by Jackson3 and electrical performing surgery as a treatment for epilepsy, and relatively stimulation studies carried out on monkeys by Ferrier6 to few patients underwent surgery at those centers; for many the confirm that localization of an epileptogenic region could be risks were high and the benefits relatively low compared to determined by the characterizing the onset today’s practice. of the habitual clinical seizures. Using this approach, localization was initially suspected by clinical observation of the seizure 2. The 1950s onset, and confirmed intraoperatively by identification of a structural abnormality, often accompanied by direct brain 2.1. The biomedical perspective stimulation. Subsequent work in the early 20th century, particularly from The decade following the founding of Epilepsy Action was a 7,8 9 Germany and Canada further confirmed the efficacy of surgery period of seminal advances in understanding the patho-anatomical as a treatment for epilepsy, but these procedures were limited to a basis of focal epilepsy and applying this information to surgical small number of patients with focal seizures for whom a structural treatment. Despite active research on EEG in epilepsy, epilepsy lesion could be demonstrated. Use of lesion-directed surgery was surgery continued to be lesion-directed based predominantly on evidence from angiography and pneumoencephalography of structural brain abnormalities. This changed with the landmark 16 * Corresponding author at: Psychological Sciences, The University of Melbourne, publication of Bailey and Gibbs (Figs. 1 and 2). They were the first Victoria 3010, Australia. Tel.: +61 3 8344 7391; fax: +61 3 9347 6618. to report a series of patients who underwent resection localized E-mail address: [email protected] (S.J. Wilson). exclusively by interictal EEG. These patients all had temporal lobe

1059-1311/$ – see front matter ß 2010 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.seizure.2010.10.028 660[()TD$FIG] S.J. Wilson, J. Engel Jr. / Seizure[()TD$FIG] 19 (2010) 659–668

Fig. 1. Percival Bailey (1892–1973).

Fig. 3. Wilder Penfield (1891–1976) and Herbert H. Jasper (1906–1999). resections for psychomotor seizures. A year earlier, Penfield (Fig. 3) and Flanigan17 had published a larger series of patients who underwent temporal lobe resection for epilepsy based on lesion identification, and the following year Jasper et al.18 (Fig. 3) Talairach (Fig. 4) and Jean Bancaud (Fig. 5) in Paris in the late published the complete EEG findings on these patients. These three 1950s.23 The value of stereo EEG for three-dimensional localization papers confirmed that psychomotor seizures originated in the of epileptogenic tissue was rapidly appreciated; however, French temporal lobe, and that temporal lobe resections were beneficial in law at that time permitted electrodes to remain in place for only alleviating disabling seizures. As a result, there was a virtual several hours, so analysis was based on interictal spike activity, as explosion of surgical activity worldwide, almost exclusively well as ictal discharges induced by electrical stimulation and focused on temporal lobe resections.1 Interestingly, these initial convulsant drugs. resections were corticectomies for fear of possible deleterious An important contribution to research on the pathological consequences from hippocampal removal, and only approximately basis of temporal lobe epilepsy occurred in 1953. Murray Falconer one-third of patients achieved seizure freedom. Surgical results (Fig. 6) introduced a standardized en bloc anterior temporal improved greatly once surgeons realized that mesial temporal lobectomy procedure in London, which provided large intact structures could be safely resected.19–21 It might be argued, tissue specimens for pathological examination.24 As a result, therefore, that initial results largely represented a placebo effect clinical pathological correlations revealed that a high percentage and that temporal lobe surgery might never have been pursued of patients with temporal lobe epilepsy had hippocampal had it not been for this phenomenon. sclerosis. This development was essential for later detailed The 1950s were also a time of rapid advances in diagnostic EEG, pathophysiological research on epileptogenic , particularly as applied to localization for surgery. Various and elucidation of the prognostic importance of hippocampal noninvasive approaches using nasopharyngeal, tympanic, and sclerosis. sphenoidal electrodes were already in use by 1950, but direct intraoperative EEG recording, electrocorticography (ECoG), was [()TD$FIG] felt to be most important for localization of the epileptogenic region. Although Bickford and Kairns performed the first chronic depth electrode recordings by inserting multistranded insulated wires into a cerebral bullet track at Oxford in 1944,22 the modern approach to depth electrode recording was pioneered by Jean

[()TD$FIG]

Fig. 2. Erma L. (1904–1988) and Frederick A. Gibbs (1903–1992). Fig. 4. Jean Talairach (1911–2007). [()TD$FIG] S.J. Wilson, J. Engel Jr. / Seizure[()TD$FIG] 19 (2010) 659–668 661

Fig. 7. Brenda Milner (1918–). Fig. 5. Jean Bancaud (1921–1994).

2.2. The behavioral perspective systematic and scholarly evaluations of the surgical patients of Penfield and Scoville are widely recognized for identifying the In the 1950s, the practice of epilepsy surgery was not only being critical role of the mesial temporal region in recent advanced by significant electrophysiological and patho-anatomi- function.28 Her work also demonstrated the important dissociation cal discoveries, but also by seminal contributions from those between episodic and procedural memory, and gave rise to the committed to understanding brain–behavior relationships, such as modern day material-specific model of episodic memory that Brenda Milner (Fig. 7) and Juhn Wada (Fig. 8). A striking illustration ascribed learning and retention of verbal material to the left is the now famous case of H.M., who in 1954 underwent a bilateral temporal lobe.29,30 temporal lobectomy for medically intractable seizures that Wilder Penfield at the Montreal Neurological Institute (MNI) produced a dense postoperative amnesia.25 One year later, Milner first promoted the use of a multidisciplinary approach, including and Penfield26 described impaired recent memory function after routine neuropsychological examination, for the surgical evalua- unilateral temporal excision in the presence of bilateral mesial tion of epilepsy patients.31 Pre-surgery, neuropsychology played temporal pathology, again involving the hippocampi. While H.M. an increasing diagnostic role to (i) aid determination of the location was not the first case to undergo a bilateral procedure,27 Milner’s of cerebral abnormality, (ii) identify the risk for iatrogenic [()TD$FIG] [()TD$FIG]

Fig. 6. Murray A. Falconer (1910–1977). Fig. 8. Juhn Wada (1924–). 662 S.J. Wilson, J. Engel Jr. / Seizure 19 (2010) 659–668 cognitive impairments, particularly in language and memory London that promoted a comprehensive review of patient change (including intra-operative mapping), and (iii) assess the presence pre- to post-surgery across a range of domains, including of cortical reorganization of cognitive functions, notably right psychological, psychiatric, family, socio-economic, and sexual hemisphere dominance for speech in left-handed patients.32 functioning.49–51 Relevant to this third issue, Juhn Wada pioneered the intracarotid amobarbital procedure (also known as the ‘Wada test’) that 3. The latter part of the 20th century became the method for determining hemispheric specialization for speech and language functions pre-surgery.33,34 Introduction of 3.1. The biomedical perspective the technique to the MNI in 1955 demonstrated that early onset of seizures was associated with greater prevalence of atypical Bouchet and Cazauvieilh first described hippocampal sclerosis language organization, and it was subsequently used to assess in the brains of patients with epilepsy in the early nineteenth lateralized contributions of mesiotemporal structures to memory century,52 but by the 1960s it was still being debated whether this function.35,36 was a result, or a cause, of epilepsy. Falconer’s en bloc temporal Alongside these advances, Ward Halstead developed a battery resection made it possible to demonstrate that the presence of of neuropsychological measures that when applied to epilepsy hippocampal sclerosis predicted an excellent postoperative surgery, showed that surgery did not produce generalized outcome,46,53 indicating that this pathological abnormality was cognitive decline, and that post-operative improvement was epileptogenic. Not only was this conclusion ultimately important observable on some tasks.37 In London, Meyer and Yates also for selection of surgical candidates and determining prognosis, it reported minimal impact of temporal lobectomy on IQ scores, but identified brain tissue that would become valuable for basic selectively identified the task of paired-associate learning as research into the fundamental mechanisms of epilepsy. having increased sensitivity to hippocampal dysfunction.38 Their In 1963, Paul Crandall et al. (Fig. 10) at UCLA were the first to work supported the material-specific model of memory, and report the use of chronic stereotactically implanted depth distinguished recovery of language disturbance from auditory- electrodes to record EEG changes occurring at the onset of verbal learning impairments post-surgery. This was an important spontaneous seizures.54 Crandall then combined these chronic precursor to contemporary theories of the role of the hippocampus electrophysiological recordings with Falconer’s standardized en in ‘binding’ associations,30 and later identification of arbitrary bloc anterior temporal resection, which permitted detailed relational learning as a neurocognitive marker of mesial temporal electroclinical–pathological correlations. This approach became epileptogenesis.39 the basis for innovative multidisciplinary collaborative investiga- From the patient’s perspective, epilepsy surgery is an elective tions into fundamental mechanisms of human epilepsy that are procedure meaning that understanding its effects on cognition and now pursued at epilepsy surgery centers worldwide.55–57 behavior are central to making an informed decision.40 In the At the same time, Ross Adey at UCLA was devising EEG 1950s, outcome studies initially measured the efficacy of surgery telemetry technology for the National Aeronautics and Space in terms of post-operative seizure frequency,16,17,19 however soon Administration to record from chimpanzees orbiting the earth.58 after psychological functioning was considered mainly due to the Crandall and coworkers enlisted the collaboration of Adey to referral of patients from psychiatric sources and the then current develop the first epilepsy EEG telemetry unit,59 which permitted opinion associating temporal lobe epilepsy with psychological artifact-free continuous EEG recordings from depth electrodes over problems.41,42 The results generally indicated that psychiatric long periods of time. During the 1970s, this advance was improvement followed seizure relief or improvement, despite a accompanied by simultaneous cinemagraphic, and then video time lag of 12–24 months between the two.43–46 During this monitoring, of ictal behavior, in order to obtain second-by-second period, a transient worsening in patient mood or behavior could electroclinical correlations of ictal onset and propagation. Over occur, that Ferguson and Rayport47 attributed to a process of the next decade, EEG artifact rejection became sufficiently psychological adjustment. This process stemmed from the [()TD$FIG] patient’s pre-operative psychosocial situation, where ‘illness’ behaviors and enmeshed family dynamics often engendered a need for the patient to learn to become ‘well’ after surgery.47–49 In recognition[()TD$FIG] of this, Taylor (Fig. 9) spearheaded a series of studies in

Fig. 9. David C. Taylor (1933–). Fig. 10. Paul Crandall (1923–). S.J. Wilson, J. Engel Jr. / Seizure 19 (2010) 659–668 663 sophisticated to permit long-term video and EEG monitoring using Table 1 scalp and sphenoidal electrodes.60,61 Outcomes before 1985 and from 1986 to 1990. The advent of X-ray computed tomography (CT) in the 1970s Number of patients (%) made it possible to visualize the entire brain in three dimensions, Seizure-free Improved Not improved Total to identify localized structural lesions in many patients with focal Limbic resections epilepsy whose seizures had been diagnosed as cryptogenic.62 This Before 1985 1296 (55.5) 648 (27.7) 392 (16.8) 2336 (100) marked the beginning of modern , which has 1986–1990 ATL 2429 (67.9) 860 (24.0) 290 (8.1) 3579 (100) gradually moved us back to a lesion-directed approach to epilepsy AH 284 (68.8) 92 (22.3) 37 (9.0) 413 (100) surgery. Neuroimaging has not replaced EEG, however, which Neocortical resections remains essential for demonstrating that an identified lesion is Before 1985 356 (43.2) 229 (27.8) 240 (29.1) 825 (100) epileptogenic. With the later advent of magnetic resonance 1986–1990 ETR 363 (45.1) 283 (35.2) 159 (19.8) 805 (100) imaging (MRI), which has higher resolution than CT, MRI rapidly L 195 (66.6) 63 (21.5) 35 (11.9) 293 (100) replaced CT for localizing structural lesions in epilepsy. Hemispherectomies The next neuroimaging technique to play a critical role in Before 1985 68 (77.3) 16 (18.2) 4 (4.5) 88 (100) presurgical evaluation was functional, not structural. In the early 1986–1990 H 128 (67.4) 40 (21.1) 22 (11.6) 190 (100) 1980s, positron emission tomography (PET) with 18F-fluorodox- MR 75 (45.2) 59 (35.5) 32 (19.3) 166 (100) yglucose (FDG) revealed unilateral temporal hypometabolism in Corpus callosotomies patients with hippocampal sclerosis and other mesial temporal Before 1985 10 (5.0) 140 (71.0) 47 (23.9) 197 (100) 1986–1990 43 (7.6) 343 (60.9) 177 (31.4) 563 (100) lesions not visible on CT or MRI.60,63 Combining scalp and sphenoidal video-EEG monitoring with FDG–PET and neuropsy- ATL, anterior temporal lobectomy; AH, ; ETR, extra- chological testing obviated the need for invasive electrophysiolog- temporal resection; L, lesionectomy; H, ; MR, large multilobar 60 resection. ical investigations in many patients. Subsequently, FDG–PET From Reference,113 with permission. became useful in identifying large unilateral areas of cortical dysplasia in infants and small children with secondary generalized epilepsy64 who were candidates for hemispherectomy and multi- based on noninvasive data, and carrying out a variety of surgical lobar resections. procedures for different epilepsy conditions.72 During the inter- By 1990, improvement in MRI resolution permitted convincing vening six years there was also a tremendous increase in demonstration of hippocampal sclerosis,65 and is now able to publications on epilepsy surgery, a doubling of epilepsy surgery demonstrate cortical dysplasia66 and a variety of other subtle centers worldwide, and improvement in seizure outcomes of lesions in patients with epilepsy who were previously diagnosed as surgical treatment specifically for anterior temporal lobe resec- cryptogenic. Consequently, a significant percentage of patients tions (Table 1). who undergo surgery have hippocampal sclerosis and cortical By the time of the second Palm Desert conference, the dysplasia that is identified noninvasively, many of whom might tremendous increase in available antiepileptic drugs had become not have been considered surgical candidates a decade or so an obstacle to timely surgical intervention because neurologists earlier. Additional PET tracers, such as flumazenil (a benzodiaze- could almost always find another drug to try. In fact, the term pine receptor ligand), and a-methyl-tryptophane (AMT), have also ‘‘medically refractory epilepsy’’ lost its practical usefulness when it become useful in identifying potentially epileptogenic abnormali- would literally take a lifetime to try every available antiepileptic ties in patients with normal MRI.67 drug in every conceivable combination in each individual patient. During this time, single photon emission computed tomography A seminal conceptual advance introduced at the Palm Desert (SPECT) was applied to reveal decreased cerebral perfusion in conference, therefore, was the definition of surgically remediable epileptogenic temporal lobes but with a somewhat lower spatial syndromes as conditions with a known etiology and a predictable resolution than PET. SPECT became particularly useful, however, natural history of pharmacoresistance after failure of a few when interictal hypoperfused regions became hyperperfused appropriate antiepileptic drugs at maximal doses.73 Surgical ictally.68,69 Consequently, by the end of the 20th century, a variety treatment for these conditions is cost-effective because presurgical of functional and structural neuroimaging approaches had become evaluation can usually be performed noninvasively and a high indispensable in presurgical evaluation. These technologies also percentage of patients, by definition, will become free of disabling made it possible for neuroscientists interested in basic mechanisms seizures postoperatively. Mesial temporal lobe epilepsy with or of epilepsy to noninvasively identify the neuroanatomical substrates without hippocampal sclerosis is the prototype of a surgically of a variety of ictal behaviors and to begin to develop concepts of remediable syndrome, but patients with demonstrable structural neuronal networks underlying different epilepsy syndromes. lesions that can be surgically resected also have surgically The last decade of the 20th century was a time of major remediable epilepsy, as do infants and small children with conceptual change in the practice of epilepsy surgery. In the 1980s, secondary generalized due to diffuse structural lesions most epilepsy surgery teams pursued only one particular surgical limited to one hemisphere. It is important to note that many approach, depending on where they were trained.1 The first Palm patients with pharmacoresistant epilepsy who do not have a Desert Conference on Surgical Treatment of the Epilepsies was held surgically remediable epilepsy syndrome as defined here, might in California in 1986, where virtually all of the epilepsy surgery still benefit from surgical treatment and could even become programs in the world at the time convened to compare strategies seizure free. Such patients, however, usually require invasive and outcomes.70 Prior to this there had been only one textbook on evaluation, and thus the risks are higher and the benefits lower epilepsy surgery,71 and very few centers published their work, so than for patients with well-defined surgically remediable epilepsy this was a novel opportunity for sharing experiences and syndromes. Reducing the risks and increasing the benefits of developing standardized approaches. Over the next five years surgery for such patients remains a major challenge for the future. most epilepsy surgery programs tried approaches used at other centers, and adopted different approaches for different types of 3.2. The behavioral perspective epilepsy. A follow-up Palm Desert conference in 1992 confirmed that most centers were now performing depth electrode and By the latter part of the 20th century, the Wada test had become subdural grid recordings selectively, operating on many patients a key tool in the neuropsychologist’s diagnostic armamentarium in 664 S.J. Wilson, J. Engel Jr. / Seizure 19 (2010) 659–668 epilepsy surgery centers worldwide. This was despite a range of seizure frequency.84,86 Soon after, the importance of other methodological concerns arising in the late 1960s and early 1970s predictors of post-operative HRQOL was recognized, including about possible widespread diffusion of the barbituate, individual mood (particularly depression), cognition (perceived memory), differences in arterial distribution, imprecise determination of the employment, driving, and anticonvulsant cessation.87,88 In the case duration of maximal drug effect, and the use of different stimuli of low mood, a strong negative linear relationship with HRQOL was and criteria for assessing language and memory across centers. described by Gilliam et al.,89 likely reflecting that a sense of well- Initially progress to address these concerns was slow, likely being is a basic component of human existence maintained by reflecting that the majority of clinicians using the Wada test had adaptive psychological processes that are essential for species been trained at, or followed the published protocols of one surgical survival.90 Around the same time, work by Trimble and coworkers center.32 Although these concerns remain relevant today, by the in London,91 Blumer et al. in Memphis,92 and subsequently Wilson 1990s considerable progress had been made, with work by Jones- and coworkers in Melbourne93 demonstrated the greater risk for Gotman et al. at the MNI,74,75 and Loring and colleagues in early mood disturbance following resection of the temporal lobe Georgia30 contributing to a range of studies focusing on the compared to resection outside this region, including increased risk reliability and validity of the procedure, accompanied by efforts to for de novo depression.92,93 These findings support a broader, define and standardize an optimal approach.76 emerging idea that shared pathogenic mechanisms may underpin In 1990, the National Institutes of Health (NIH) ‘Consensus mesial temporal epileptogenesis and mood disturbance,94 and Conference on Surgery for Epilepsy’ declared neuropsychological possibly impaired episodic associative memory function. examination a necessary diagnostic procedure in the surgical While HRQOL research has principally focused on improve- evaluation of epilepsy patients.77 The material-specific model had ments in well-being after surgery, by the last decade of the 20th become the cornerstone of the field, guiding both presurgical century progress had also been made in characterizing the nature decision making and dominating the approach to the assessment of the adjustment process reported by patients, particularly within and interpretation of cognitive outcomes.39,40 Rausch and Babb at the first 24 months after efficacious surgery. Bladin and Wilson UCLA had demonstrated that subfield neuronal loss in the left likened this process to being ‘burdened with normality’, as patients hippocampus specifically predicted impaired learning of arbitrari- face new challenges and refashion their psychosocial milieu as ly related words (the ‘hard’ pairs) of the paired-associate learning they undergo a psychological and social transition from chronically task, but not semantically rich prose.78 Around the same time, ill to well.90,95 Characterization of this commonly reported Saling et al. in Melbourne reported mildly impaired story recall in adjustment process concurred with an increasing emphasis in patients with well characterised left or right mesial temporal foci, the literature on the need for post-operative rehabilitation but selectively impaired learning of arbitrarily related words in programs that routinely address all aspects of a patient’s patients with left mesial temporal foci.79 Notably, this led them to functioning to maximize the ‘real life’ benefits of seizure freedom consider task-specificity, rather than material-specificity, as the and decrease the significant risk of adjustment difficulties and more relevant factor in verbal memory outcomes, that distin- mood disturbance post-surgery.96 In preparing patients for the guishes medial versus lateral specialization (or arbitrary versus vicissitudes of post-operative life, the importance of addressing semantic forms of learning) within the temporal lobe.38 pre-surgical expectations of both patients and family members Consistent with this notion of task-specificity, Hermann et al.80 was also recognized,97,98 including the impact of expectations on had reported that retroactive interference in word list learning the patient’s view of the success of epilepsy surgery.99 might provide the most ‘pure’ indicator of memory functioning of the left temporal lobe, as it is unrelated to language adequacy. 4. The 21st century Following this, Helmstaedter et al. showed that memory tasks with a semantic component decline from pre-operative levels following The past decade has seen continued advances in diagnostic en bloc temporal resections, whereas this is not evident after testing and microsurgical techniques. This has increased the selective amygdalohippocampectomy. This provided further sup- accuracy of localization of the epileptogenic region and the safety port for the notion of specialization of memory functions within of surgery, as well as expanding the number of patients considered the temporal lobe, again fractionating the roles of mesial and surgical candidates to include those with no demonstrated lesions lateral temporal cortical structures.81 on MRI, or diffuse or multifocal structural abnormalities, only one Perhaps most salient at the NIH Consensus Conference in 1990, of which might be responsible for generating habitual seizures. a new way of assessing surgical outcome was conceived ‘‘...that Technologies that were still considered experimental at the would take advantage of validated and quantitative methods to end of the 20th century have now become available for general assess the quality of life and health status of individuals.’’77 This use, including (MEG), functional MRI was, in part, anticipated by Carl Dodrill’s work on quantifying the (fMRI), and simultaneous EEG–fMRI recordings with the capabili- psychosocial aspects of living with epilepsy through development ty of localizing alterations in blood flow associated with interictal of the Washington Psychosocial Seizure Inventory.82 The health spikes and ictal EEG discharges. Additional useful approaches related quality of life approach (HRQOL), however, extended this include MR spectroscopy (MRS), to localize metabolic alterations work by utilizing a general measure, to allow comparison with associated with the epileptogenic region, diffusion tensor imaging other chronic conditions, supplemented by epilepsy specific (DTI) to map alterations in fiber tracks that may indicate the items.77 While a large number of HRQOL measures have now presence of an epileptogenic lesion, and statistical parametric been established for people with epilepsy across cultures, Vickrey mapping (SPM) of structural MRI, which provides high-resolution et al. at UCLA first responded to the NIH recommendation by definition of localized abnormalities that are not visible on developing the Epilepsy Surgery Inventory-55,83 followed by a standard MRI. measure established by Baker and coworkers in Liverpool.84,85 fMRI now also provides a noninvasive means of mapping These subjective measures of quality of life were designed to essential neocortical functions, permitting the boundaries of reflect the patient’s perception of daily functioning and experience localized corticectomies adjacent to eloquent cortex to be of health and well-being across a range of dimensions, including determined noninvasively prior to surgery. This has generally general, physical, mental, and social functioning. been accompanied by a shift to validate less invasive techniques Initial studies employing HRQOL measures demonstrated that for assessing language and memory functions, using the Wada test improvements after surgery were linearly related to a reduction in as a benchmark. In conjunction with a worldwide shortage of S.J. Wilson, J. Engel Jr. / Seizure 19 (2010) 659–668 665 amobarbital, this has led to re-evaluation of the clinical indications surface of the brain. To be most useful, noninvasive approaches to for the Wada test.76 Recent surveys of a large number of epilepsy recording pHFOs are needed, and perhaps will be provided by MEG surgery programs have indicated that the Wada test is no longer or EEG–fMRI. If the accuracy of these putative biomarkers is routinely used in every patient. This has prompted a call for the confirmed, even when invasive recording is required this could development of a set of guiding principles for use of the Wada, to greatly reduce the cost and increase the efficacy of resective ensure the risk–benefit ratio is justified.76 surgical treatment. As pHFOs are frequent interictal events, the The epilepsy surgery setting has provided fertile ground for invasive recording could be completed in a few hours, without the basic scientists interested in understanding fundamental neuro- need for long-term chronic recording to capture spontaneous nal mechanisms of epilepsy.100 For several decades, hippocampal seizures. sclerosis has been the primary focus of attention, but in recent The concept of identifying new markers of outcome has also years other common epileptogenic lesions, particularly focal emerged in current behavioral research.40 Moving away from the cortical dysplasia, have been the subject of investigation. Not material-specific model, neurocognitive markers of mesial tempo- only is resected epileptogenic tissue available for molecular ral dysfunction have been proposed, with arbitrary relational biological, microanatomical, and electrophysiological in vitro learning providing a candidate endophenotype of disruption of the investigations, but several epilepsy centers have developed the rhinal–hippocampal interface.39 Progress has also been made in capability of chronic in vivo microelectrode techniques to record identifying neurobiological and psychological markers of risk for localized field potentials and single unit activity, as well as mood disturbance after surgery,104,105 with reduced contralateral microdialysis for evaluating neurotransmitter release. While the hippocampal volume pre-surgery recently being identified as a ultimate objective of this research is to identify primary marker for increased risk of depression post-surgery.106 This epileptogenic abnormalities that could be the target for novel approach requires an understanding of the complex interaction of pharmacotherapy and other treatments, it has also identified biological, cognitive, psychological, and social factors at play in a disturbances that could lead to the development of reliable given individual, that combined, create the framework for an biomarkers of epileptogenicity. individual’s trajectory from seizure onset to chronicity and There is still no single diagnostic approach that can identify not subsequent response to surgical treatment. For example, prelimi- only the location but the extent of the epileptogenic region, that is nary work linking the process of post-operative adjustment with the area necessary and sufficient for generation of spontaneous HRQOL outcomes indicates that patients with early onset of seizures, and thus the minimal area that needs to be resected in seizures (before or during adolescence) are more likely to order to produce a seizure free outcome. The location and extent of experience a greater sense of self-change after surgery, that while the epileptogenic region remains approximated based on a variety tumultuous, ultimately concurs more beneficial effects for of diagnostic information, including EEG, sophisticated neuroim- HRQOL.107 In contrast, work linking HRQOL with cognitive aging, and neuropsychological testing, as well as observation outcomes shows that the ‘‘double whammy’’ of seizure recurrence of seizure semiologies. The identification of a biomarker that and memory decline has a highly detrimental effect on HRQOL.108 would reliably localize uniquely to epileptogenic tissue would be a Greater understanding of these interactions and their individual major advance for epilepsy surgery. Such a biomarker could differences lies at the heart of identifying markers of risk for, and greatly decrease the cost and risk of presurgical evaluation, resilience to, poor post-operative outcomes. This is directly improve surgical results, and increase the number of patients who relevant to the ongoing development of models of post-surgical might be considered surgical candidates. Basic research in the rehabilitation that can target treatment interventions to an epilepsy surgery setting, along with parallel reiterative research individual’s specific phase and needs in post-operative recovery, using experimental animal models of human surgically remedia- to facilitate improvements in day-to-day functioning over the ble epilepsy syndromes, have revealed a number of disturbances long-term. that could become targets for effective biomarkers (Table 2). Access to epilepsy surgery remains a major obstacle to be At present, there are two potential biomarkers under active overcome. Epilepsy surgery is arguably the most underutilized of investigation. all therapeutic approaches that are generally accepted as effective. There is evidence that AMT, on PET, localizes to epileptogenic Perhaps only 1% of potential surgical candidates are ever referred tissue, particularly when there are multiple potential epileptogen- to an epilepsy surgery center in industrialized countries, and at the ic lesions, as in the case of tuberous sclerosis.101 More recent beginning of this century very few individuals with epilepsy living interest, however, has been in pathological high-frequency in the developing world had access to surgical treatment. Several oscillations (pHFOs), brief 100–600 Hz EEG events often associated important advances have been made in the past decade in an with interictal spikes which are believed to be summated action attempt to improve this situation. Reluctance on the part of potentials of the synchronously bursting neurons characteristic of physicians and patients to consider surgical intervention has been epileptogenic tissue.102 Although reports from several centers attributed to several factors. Fear of surgery is understandable, suggest that pHFOs could more reliably identify epileptogenic although the risk of morbidity and mortality is much greater with tissue than interictal EEG spikes and even ictal onset,103 these uncontrolled disabling seizures than it is with surgery. We events can only be recorded from electrodes within or on the obviously have not done as good a job as we could in educating the general public and the medical community, despite the significant increase in publications since the first Palm Desert Table 2 conference, that all support the safety and efficacy of surgical Target mechanisms for biomarkers of epileptogenicity and epileptogenesis. treatment for epilepsy. Cell loss One criticism at the end of the last century was that there had Axonal sprouting never been a randomized controlled trial (RCT) of epilepsy surgery Synaptic reorganization that clearly confirmed the safety and efficacy that is reported in Altered neuronal function (gene expression profiles, protein products) Neurogenesis published uncontrolled series. This concern was overcome in 2001 Altered glial function and gliosis with the publication of a RCT of epilepsy surgery at the University Inflammatory changes of Western Ontario109 that clearly demonstrated the superiority of Angiogenesis surgical treatment over continued pharmacotherapy in patients Altered excitability and synchrony with temporal lobe epilepsy. Based on this, in 2003, the American 666 S.J. Wilson, J. Engel Jr. / Seizure 19 (2010) 659–668

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