The Surgery of Temporal Lobe Epilepsy I—Historical Development, Patient Selection, and Seizure Outcome

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Chapter 19 The Surgery of Temporal Lobe Epilepsy I—Historical Development, Patient Selection, and Seizure Outcome

Introduction

Surgery for temporal lobe epilepsy (TLE) is widely practiced in the developed world. Its efficacy in comparison to medical treatment for intractable epilepsy has not been seriously doubted by many workers and has now been confirmed in a randomized, controlled study of 80 patients, half with ongoing medical treatment versus half subjected to surgery. Fifty-eight percent in the surgical group and 8% in the medical group (P <0.001) had fewer seizures at 1 year.1 The current authors examined 72 papers on the outcome of surgery for TLE published between 1956 and 2000 (references not given). It was possible to reasonably amalgamate the outcome data in 26 papers (737 patients): 491 (67%) had excellent and 162 (22%) had good outcomes (excellent: UCLA classification I; good: UCLA classification II and III; for the UCLA classification see Vickrey et al., 19872).

This is an extensive and complex field encompassing many workers with varying approaches to preoperative assessment and operation types and encompassing the gamut of investigational modalities from the well established and widely available to the more cutting edge. For the purpose of orientation, therefore, we have divided this chapter into two sections. The first provides a brief summary of the historical development of epilepsy surgery and the second a summary of aspects of the outcome, in terms of seizure control, of temporal lobe surgery in contemporary practice. In the following chapter, we address the outcome in terms of adverse effects and complications.

History

From scarification to colectomy and nasal polypectomy, the list of physical treatments visited on patients with epilepsy appears, at least in retrospect, bizarre and misguided. Postauricular arteriotomy, first recorded in ancient Greece, was still used in the late 1800s, and in the following century, Charles Brown-Séquard advocated cauterization and William Gower circumcision; thumb amputation was performed as late as the 1920s.3,4

Some instances of prehistoric trephination (excision of a piece of the calvarium) may have been attempts to cure posttraumatic epilepsy.5 Otherwise, prior to the late nineteenth century, brain surgery was largely confined to the drainage, cleaning, and closure of open head injuries in a military setting. In Europe and the United States, trephination was sometimes performed at the site of head injuries to relieve seizures, but its popularity fluctuated.5,6 Success was limited, mortality high: “Nearly all the patients perished within the first week from inflammation of the brain and its envelopes” (Samuel Gross, 1872).7 There were also sporadic reports of trephination for cerebral abscess drainage, but the results were poor and, toward the end of the eighteenth century, many surgeons began to eschew it. Pierre Joseph Desault, a prominent French surgeon, “proscribed it entirely on the double reason of its danger and ordinary inutility.”8

As the development of modern general surgery flourished following the introduction of antisepsis and anaesthesia (ether and chloroform 1846 and 1847, respectively; antisepsis, 1867), brain surgery continued to be shunned.6 In 1886, Horsley remarked: “It is notorious that, for the last thirty or forty years … trephining has been in exceedingly evil repute, owing to the very high mortality which followed its practice.”9 The advent of modern neurosurgery required a third factor—the birth of modern neurology, with its emerging concepts of anatomical localization in the cerebral cortex.

Prominent landmarks included the identification of an expressive language area by Pierre Broca,10 the demonstration of the canine motor cortex by Gustav Fritsch and Eduard Hitzig,11 and the ethically reprehensible work of Robert Bartholow, a Cincinnati physician, on one unfortunate Mary Rafferty.12 A rodent ulcer had left much of her cerebral cortex exposed but “without any interruptions of its functions.” Bartholow, making use of an electrotherapeutics room that he had previously established at the Good Samaritan Hospital, subjected Mary Rafferty to repeated electrostimulatory experiments, clearly demonstrating contralateral movements with hemispheric stimulation. The final experiment induced status epilepticus that led to death within a few days. A full historical account has been given by Morgan.13

John Hughlings Jackson’s work was of particular importance. He began to use cerebral localization to explain the semiology of epileptic seizures, classically the “the Jacksonian march,” which he related to a lesion in the motor area.6,14 This was directly applied in 1884 when Rickman Godlee and Alexander Bennett found and excised a glioma from the right precentral gyrus based on an inference that the patient’s focal motor seizures arose there.15 This operation was observed by Horsley, Jackson, and David Ferrier.16 These workers, based at the National Hospital for Paralysis and Epilepsy, Queen Square in London, went on to make by far the greatest contribution to the early development of neurosurgery.

Horsley initiated brain surgery at the National Hospital in 1886 and, within 1 year, published a case series of 10 operations. These cases were mostly similar in concept to Godlee and Bennett’s operation (i.e., clinical localization was used to identify and pursue a structural lesion). However, one case (O.S.H.), a “moral imbecile” with “seizures beginning at the left angle of the mouth” stands out. Finding no cortical abnormality, Horsley used electrical faradic cortical stimulation to map out the “facial center,” which he excised.17 This appears to be the first instance of a stimulation-guided corticectomy (some have, incorrectly, attributed it to Fedor Krause6). The contribution of William Macewan in Glasgow should also be remembered, although of less direct relevance to epilepsy surgery rather than general neurosurgery. In 1888, William Macewan published a series of 21, mostly successful, operations for brain abscesses.18

Horsley had demonstrated the technical feasibility of brain operations, firmly basing his surgical technique on animal experiment and anatomical observation. In addition to the application of neurological localization, he greatly developed surgical technique. Horsley’s advocacy of brain surgery was evidently emboldened, rebutting opponents’ “vague statements which one sees paraded on our journals … even were the language in which they are couched worthy of notice”; urging that “no one … need hesitate to follow the dictates of reason and common sense, and proceed to operate.”9 In Germany, Krause took up focal anterior cortical excisions for Jacksonian epilepsy in 1893 and, in 1910, reported on 29 patients, 8 with a marked improvement in seizures (although with a mortality of 10%).6 Some cases lacked surgical pathology, and corticectomies were based on stimulation (galvanic and, later, safer monopolar faradic).

Thus, neurosurgery became increasingly accepted: in 1899, Otto Binswanger identified 50 reports and seven theses on epilepsy surgery between 1894–1898.3 However, surgery in this period was almost entirely restricted to the vicinity of the primary motor area of the frontal lobe. The importance of the temporal lobe in epilepsy had not been appreciated.

In the first few decades of the 20th century, epilepsy surgery largely centered on the excision of cortical scars, fueled by the First World War. In Breslau, Otfrid Förster, neurologist turned neurosurgeon, ventured beyond the motor strip, performing excisions in all lobes. He developed the use of simulation and was the first to use intraoperative electrocorticography (ECoG).7 Following on from Förster, Wilder Penfield initiated the epilepsy surgery program at the Royal Victoria Hospital (and then the Montreal Neurological Institute), Canada, in 1928.19 Penfield’s program was chiefly concerned with the excision of, mostly extratemporal, cortical scars in addition to expanding, in collaboration with Jaspers, work on cortical localization.19 Penfield emphasized the importance of surgical pathology—structural lesions and gyral atrophy—in determining resections. However, ECoG and cortical stimulation were usually employed and, whereas Penfield, on the one hand, counseled against the resection of normal appearing cortex, he did also describe extending resections into surrounding normal cortex based on the ECoG findings. In addition, electrodes were used to locate areas of potentially abnormal cortex not visible without dissection or manipulation (“the diviner’s rod”). Later, Penfield increasingly performed temporal lobe operations, but mainly on the neocortex. Of 68 cases between 1939 and 1949, the excisions were focused on the anterior and lateral temporal lobe, the uncus being excised in ten cases (15%) and the hippocampus in only two (3%).20,21 Only following the work of Morris, Bailey, and Gibbs (see later discussion) did his attention turn to the mesial structure.

The most important development underpinning the further development of epilepsy surgery arose from the electroencephalographic work of Herbert Jaspers and then Pearce Bailey and Frederick Gibbs that, in the 1940s, crystallized the concept of psychomotor seizures arising from the temporal lobe.22,23 Previously, the importance of the temporal lobe in epilepsy had not been widely emphasized, even though macroscopic and microscopic descriptions of sclerosis of the mesial temporal lobe in association with epilepsy had been published in 1825 and 1880, respectivley,24 and Jackson had essentially characterized psychomotor seizures (“the uncinate group of fits”) and localized them to the medial temporal lobe.25 However, the primary nature of mesial temporal sclerosis was opposed by prominent clinicians and neuropathologists, and it was widely held that the pathological changes were the consequence rather than the cause of epilepsy.

Bailey and Gibbs quickly translated their findings into surgical practice, initiating temporal lobe operations at the Illinois College of Medicine in 1947.26 Their first 19 operations were limited excisions determined by ECoG, but the success rate was low, prompting more radical excisions, “radical lobectomy”: all tissue between the Sylvian fissure and the occipitotemporal sulcus, extending posteriorly at least to the level of the central sulcus and, in some cases, depending on the ECoG findings, up to one centimeter posterior to it. The hippocampus and insula were spared for fear of producing the neuropsychological deficits reported in primates following bilateral ablation of the medial temporal lobe. The results of the radical procedure were superior (“… very good to date”), and Bailey and Gibbs urged its adoption in all cases.

Simultaneously, although with much less acclaim, Morris at Georgetown University School of Medicine developed a similar radical resection but, remarkably, including the uncus, amygdala, and 2 to 4 cm of the anterior end of the hippocampus. Morris invariably observed diffuse temporal lobe epileptiform activity on ECoG (as Bailey and Gibbs did), and consequently, he took the bold step of abandoning intraoperative electrophysiological studies, simply performing “standard temporal lobectomy” in all patients—with good results.27

In the 3 years subsequent to 1949, Penfield performed 81 temporal lobe operations in contrast to 68 in the preceding 10 years. Furthermore, the uncus, amygdala, and hippocampus were routinely removed as well as the anterolateral temporal lobe anterior to the vein of Labbé. Penfield ascribed this development in his practice to the recognition of incisural sclerosis (i.e., hippocampal sclerosis, henceforth referred to as mesial temporal sclerosis [MTS] in this chapter) as the commonest cause of TLE arising from his earlier work.19 Additionally, Penfield reoperated on “a number” of his earlier temporal lobe patients to excise the hippocampus, sometimes with conversion of failure to success.28

Murray Falconer at the Maudsley Hospital, London, perused the approach of removal of the lateral and media structures, developing the technique of “anterior temporal lobectomy,” using an en bloc excision. In addition to the medial structures, the whole temporal lobe was amputated 5.5 to 8 cm (most commonly 6 cm) posterior to its tip, although sparing the superior temporal gyrus other than its anterior 1 to 2 cm; this modification was introduced to avoid dysphasia.29 The en bloc method allowed pathological study and revealed, in many cases, gliosis and atrophy in the hippocampus. As these abnormalities often extended into the contiguous gray matter, the term “mesial temporal sclerosis” was coined.30 Falconer’s finding that seizure outcome was superior in cases where the resection included definitely pathological tissue, particularly MTS, as opposed to no or nonspecific abnormalities, led him to the belief that “the removal of diseased brain tissue rather than the interruption of neuronal circuits” was essential to successful outcome.29,31

To summarize, by the 1950s, epilepsy surgery had expanded from a practice mainly concerned with the excision of tumors related to the motor strip and cortical scars in posttraumatic epilepsy to one centered around TLE identified by the clinical history, seizure semiology, and surface electroencephalogram (EEG). Although most workers continued to carry out intraoperative neurophysiological studies, they nevertheless performed a standard temporal resection regardless of these and the gross surgical pathology. It was recognized that the mesial temporal structures, particularly the hippocampus, were central to TLE and that resections should include these structures.

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