J Neurosurg 120:1428–1436, 2014 ©AANS, 2014
Transorbital endoscopic amygdalohippocampectomy: a feasibility investigation Laboratory investigation H. Isaac Chen, M.D.,1 Leif-Erik Bohman, M.D.,1 Laurie A. Loevner, M.D.,1,2 and Timothy H. Lucas, M.D., Ph.D.1 Department of Neurosurgery and 2Division of Neuroradiology, University of Pennsylvania, Philadelphia, Pennsylvania 1
Object. Resection of the hippocampus is the standard of care for medically intractable epilepsy in patients with mesial temporal sclerosis. Although temporal craniotomy in this setting is highly successful, the procedure carries certain immutable risks and may be associated with cognitive deficits related to cortical and white matter disruption. Alternative surgical approaches may reduce some of these risks by preserving the lateral temporal lobe. This study examined the feasibility of transorbital endoscopic amygdalohippocampectomy (TEA) as an alternative to open craniotomy in cadaveric specimens. Methods. TEA dissections were performed in 4 hemispheres from 2 injected cadaveric specimens fixed in alcohol. Quantitative predictions of the limits of exposure based on predissection imaging were compared with intradissection measurements. The extent of resection and angles of exposure during the dissection and on postdissection imaging were recorded. These measurements were validated with MRI studies from 10 epilepsy patients undergoing standard surgical evaluations. Results. The transorbital approach permitted direct access to the mesial temporal structures through the lateral orbital wall. Up to 97% of the hippocampal formation was resected with no brain retraction and minimal (mean 6.0 ± 1.4 mm) globe displacement. Lateral temporal lobe white matter tracts were preserved. Conclusions. TEA permits hippocampectomy comparable to standard surgical approaches without disrupting the lateral temporal cortex or white matter. This novel approach is feasible in cadaveric specimens and warrants clinical investigation in carefully selected cases. (http://thejns.org/doi/abs/10.3171/2014.2.JNS131060)
S
Key Words • amygdalohippocampectomy • endoscopy • epilepsy • temporal lobectomy • transorbital
urgical resection of the hippocampus is the standard of care for medically intractable temporal lobe epilepsy46 and significantly improves seizure control and quality of life.14,42 The 2 most common surgical approaches are anterior temporal lobectomy and selective amygdalohippocampectomy, both of which are performed through a standard temporal craniotomy. Despite the marked success of these approaches, craniotomy for the treatment of temporal lobe epilepsy is not without risk. Complications range from cosmetic disfigurement to permanent neurological and cognitive disability (Table 1). Though uncommon, these complications significantly diminish quality of life for affected patients. Alternative strategies that minimize these risks while still achieving an adequate hippocampectomy, the principle goal of surgery, could further improve patient outcomes.
Abbreviations used in this paper: IOF = inferior orbital fissure; SOF = superior orbital fissure; TEA = transorbital endoscopic amygdalohippocampectomy; TONES = transorbital neuroendoscopic surgery.
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Minimally invasive approaches have the potential to access the hippocampus with minimal disruption of the lateral temporal cortex and white matter pathways. For instance, stereotactic radiofrequency ablation permits hippocampal lesioning with 16–38 ablations through a single occipital bur hole.29,35 Likewise, endoscopic approaches may provide access to the hippocampus and permit resection under direct visualization. The present cadaveric study examines the feasibility of a transorbital approach to the mesial temporal lobe using endoscopic visualization and image guidance. Unlike the occipital approach, the transorbital route affords the surgeon a short working distance and early access to the anterior portion of the hippocampus. We present the quantitative metrics of transorbital endoscopic amygdalohippocampectomy (TEA) predicted by predissection neuroimaging in relation to the measurements taken during the dissections. These measurements are compared with scans from 10 patients with epilepsy for clinical validation of the angles of exposure. J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy TABLE 1: Neurological and cognitive complications of temporal craniotomies Complication
Authors & Year
No. of Incidence Patients (%)
visual field deficit
Wiebe et al., 2001 Egan et al., 2000 trochlear nerve palsy Cohen-Gadol et al., 2003 oculomotor nerve palsy Sindou et al., 2006 language deficit Acar et al., 2008 Jensen, 1975 memory deficit Acar et al., 2008 hemiparesis Wieser, 2006 Rydenhag & Silander, 2001 Behrens et al., 1997
40 29 47
55 76 19
100 39 858* 39 478 654
5 2.5 5 5 1 2.2
279*
1.4
* Temporal lobe procedures only.
Methods Cadaveric Specimens
Two adult cadaveric heads were obtained from the Maryland State Anatomy Board. These heads were fixed with a mixture of ethanol and glycerin and then injected with colored latex for vessel identification. The Operational Committee on Cadaver and Body Parts and the Institutional Review Board of the University of Pennsylvania approved the usage of cadaveric specimens in this study.
Predissection and Postdissection Imaging
Predissection CT and MRI scans were performed for dissection planning and intraoperative navigation. The CT studies of the head were performed on a Siemens Sensation 16 scanner, utilizing a BrainLAB protocol designed for operative navigation. The examinations included highresolution thin-section (1-mm) axial images in a medium smooth sinus window with a 300-mm field of view and reconstructed bone windows. Direct coronal images were also obtained using 3-mm sections in a medium smooth sinus window and were also reconstructed into bone windows. Predissection high-resolution MRI of the brain was performed on a 3.0-T unit (Siemens Magnetom Trio). Localizing images were obtained, followed by sagittal T1weighted and axial T2-weighted 5-mm-thick images, coronal high-resolution turbo spin echo T2-weighted 3-mm sections, and coronal T1-weighted true inversion recovery volumetric 4-mm-thick images. Then coronal oblique turbo spin echo T2-weighted 3-mm-thick sections were acquired from the ventral orbit through the temporal lobe angled to provide direct line of sight of the endoscopic trajectory through the lateral orbit to the medial temporal lobe (aligned with the long axis of the mesial temporal lobe). Following cadaveric dissections, CT and MRI studies utilizing the same preoperative sequences were repeated to assess the size of the craniectomy and the extent of temporal lobe resection.
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Dissection Equipment
The specimens were stabilized in a custom frame and then registered for frameless stereotactic navigation using the S7 StealthStation (Medtronic) running Synergy cranial planning and navigation software v2.1.5 (Medtronic). Anatomical measurements were obtained using superficial cranial landmarks. The initial soft-tissue dissection and bone work were performed with an operating microscope. Visualization of the intracranial space was obtained with a 0° and 30° Hopkins II 4-mm neuroendoscope and high-definition Storz endoscope system (Karl Storz). For each side, the distance from the midpupillary point to the midline was measured before orbital retraction and then again with the retractor in its final position. The distance between the lateral orbital rim and the lateral dural edge was recorded after dissection.
Dissection Technique
The heads were positioned supine with the surgeon seated above the head to simulate the standard operating position. A 2-cm curved skin incision was made lateral to the orbital rim (Fig. 1A). This lateral orbital incision was necessary due to the firmness of the fixed cadaveric skin and subcuticular tissue. In clinical practice, an eyelid/ eyebrow or retrocanthal incision would be used. The orbicularis oculi muscle was incised parallel to its fibers. The lateral orbital rim was exposed. A subperiosteal dissection was performed down to the level of the inferior orbital fissure (IOF). The orbit was gently retracted medially with a malleable retractor. The frontozygomatic suture, first identified on the lateral orbital rim, was a useful landmark for finding the IOF and defining the inferior-lateral extent of the craniectomy (Fig. 1B). A craniectomy was made superior to the IOF and lateral to the superior orbital fissure (SOF) with a high-speed electric drill. The dura was opened to reveal the temporal pole (Fig. 1C and D). The sylvian fissure was visualized at the superior extent of the craniotomy. Frameless stereotactic navigation was used to identify the desired trajectory to the hippocampus. In general, this angle was 10° superior to the canthomeatal line. Next, a 0° endoscope was introduced into the craniectomy. Simple suctioning facilitated the limited corticectomy, which measured approximately 1.5 cm in diameter. The anterior termination of the temporal horn of the lateral ventricle was readily identified. The anterior and inferior portions of the amygdala were resected. The pes of the hippocampus and the temporal horn was readily visualized (Fig. 1E). In 2 hemispheres, the hippocampectomy preceded the resection of the uncus and entorhinal cortex. In the other 2, the reverse order was employed. Securing the endoscope in place with a holding arm at the 12 o’clock position (the inferior aspect of the orbit) allowed for concurrent use of two instruments for the dissection. Resection of the amygdala and hippocampus was performed with gentle suction along the natural planes to a depth of up to 10 cm from the orbital rim (Fig. 1F). The anterior choroidal artery branches were clearly visualized throughout the dissection. Following amygdalohippocampectomy, resection of the uncus and entorhinal cortex was performed in subpial fashion, with careful preservation of the pial boundaries medially. The lateral brainstem, 1429
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Fig. 1. Dissection technique. Orientation: For A–F, left is medial, and bottom is cranial. For G, left is anterior, and bottom is cranial. A: A curvilinear incision (arrowhead) is made adjacent to the left lateral canthus. The horizontal line perpendicular to the incision is the canthomeatal line. The orientation lines designate superior (S), inferior (I), medial (M), and lateral (L) and apply to all images but G. B: The orbital contents are dissected in a subperiosteal manner and retracted medially with a malleable retractor. Along the lateral orbital wall, the frontozygomatic suture (arrowhead) leads to the inferior orbital fissure (probe tip). C: The planned region of the orbital craniectomy is outlined by the oval. D: After the craniectomy, removal of the dura reveals the temporal pole. E: Dissection through the temporal pole using frameless stereotactic navigation leads to the pes of the hippocampus (asterisk). F: Resection of the medial temporal lobe structures, including the head and body of the hippocampus and the inferior amygdala, is complete. The choroid plexus (arrowhead) and temporal lobe white matter (asterisk) remain laterally. Medially, the pia and vasculature in the ambient cistern are seen (arrow). G: With a 30° angled endoscope, the lateral brainstem and ambient cistern are readily visible. Superior to the tentorium cerebelli (asterisk), the posterior cerebral artery (arrowhead) wraps around the cerebral peduncle. The optic tract (arrow) is seen medial to the preserved choroidal vessels. Portions of the pia mater were preserved during the cadaveric dissection. For adoption in a clinical setting, the intent would be to preserve the entirety of the pia, as is done during open surgery.
cranial nerves, and vessels within the CSF cisterns were readily apparent with application of the 30° endoscope. The removal of the remaining medial temporal lobe was performed in a subpial fashion. The 30° endoscope enabled further inspection of the lateral ventricle and temporal lobe white matter laterally and the brainstem and other neurovascular structures medially once the pia had been opened (Fig. 1G). Analysis of Exposure
The limits of the surgical exposure were predicted on CT and MRI using the boundaries of the orbit, measurements of the globe diameter, and measurements of the extraglobe soft tissues within the orbit. Angles of exposure were predicted with reference to the apex of the orbit lateral to the insertion of the annulus of Zinn and the SOF. During the dissection, measured angles of exposure were obtained anatomically and again using the frameless stereotactic probe. Coordinates for each stage of the dissection were digitally recorded in the Synergy cranial application. We used OsiriX v5.5.1 (www.osirix-viewer.com) to analyze the pre- and postdissection imaging studies. The size of the orbital craniectomy, angles of exposure afforded by the craniectomy, and extent of hippocampal resection were measured. Values for the maximal medial-lateral and superior-inferior dimensions of the approach were measured on axial and sagittal CT sections, respectively.
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We created 3D reconstructions with reformatted images from the CT data to delineate the relationship between the craniectomy and the orbital bony anatomy. Intradissection coordinates of the surgical exposure boundaries were mapped onto the predissection MR images to determine the surgical angles of exposure. We predicted the horizontal and vertical angles of exposure using the midpupillary axial T2-weighted section and the sagittal T1-weighted section approximately 3 mm lateral to the midpupillary point, respectively. Readily identifiable anatomical landmarks were used to define the sides of the angular measurements. The extent of the lateral orbital exposure determined the medial limits of intracranial access, and vice versa. Similarly, the superior and inferior orbital boundaries determined the inferior and superior limits of intracranial access. In the axial plane, the medial border was defined by a line connecting the lateral orbital rim to the lateral edge of the SOF. The lateral border was defined by a line connecting a point 6 mm medial to the lateral edge of the orbit at the level of the pupil, mimicking orbital retraction, to the point on the sphenoid bone adjacent to the temporalis muscle laterally and the temporal pole inferomedially. In the sagittal plane, the superior border was defined by a line connecting the inferior orbital rim to the sphenoid bone adjacent to the sylvian fissure. The inferior border was defined by a line connecting the superior orbital rim to the floor of the middle cranial fossa. The actual and predicted angles of exposure were J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy compared using the Mann-Whitney U-test for nonparametric variables, with a p value of 0.05 as the threshold for significance. Finally, the hippocampal volume on pre- and postdissection MR images was manually segmented. We defined the extent of hippocampal resection as a simple ratio of the 2 calculated volumes. To validate cadaveric predictions with patients seen in clinical practice, we measured the predicted limits of exposure for 10 consecutive patients undergoing standard evaluation for epilepsy surgery. The method for analyzing the predicted transorbital approach was identical to that in the cadaveric specimens. Institutional review board approval was obtained for this aspect of the study separately.
Results
In all 4 cadaveric hemispheres, we successfully performed an amygdalohippocampectomy and resection of mesial structures (Fig. 2). The extent of hippocampal resection was 97% (volume 2.42 cm3 predissection vs 0.07 cm3 postdissection). This resection was achieved through a mean orbital opening of 10.2 × 12.2 mm (Fig. 3; Table 2). The maximum globe displacement was 7 mm. This maximum was within the range of the measured periorbital tissue thickness. The duration of each dissection was approximately 90 minutes. The approach described above yielded a wide range of intracranial access (Fig. 4). In the axial plane, access to the brainstem medially and the lateral temporal white matter was possible. In the sagittal plane, it was possible to reach the inferior frontal lobe superiorly and the middle cranial fossa floor inferiorly. The depth of resection reached the level of the quadrigeminal cistern. There was no significant difference between the observed angles of exposure, derived from intradissection neuronavigation coordinates, and the predicted angles of exposure measured from the predissection MRI study (medial-lateral, p = 0.85; superior-lateral, p = 0.56). We also measured predicted angles of exposure from preoperative MR images in 10 patients with seizure disorders undergoing evaluation for epilepsy surgery (medial-lateral, 42° ± 4°; superior-inferior, 64° ± 5°; Table 3). There were no significant differences between the actual cadaveric and predicted patient angles of exposure (medial-lateral, p = 0.85; superior-lateral, p = 0.21), suggesting that our cadaveric angle of exposure data can be generalized to patients.
Discussion
In cadaveric heads, the transorbital endoscopic approach enables near-total resection of the amygdala, hippocampus, uncus, and perirhinal and entorhinal cortex. Lateral orbital craniectomy affords access to the anterior temporal pole aligned with the long axis of the mesial temporal lobe (Fig. 4). Endoscopy permits panoramic visualization and illumination of the mesial structures, the mesencephalon, and the ambient and crural cisterns with minimal retraction upon the globe and no retraction of the temporal lobe. It remains to be seen how well these findings translate into the clinical arena and how the risk/benefit profile of J Neurosurg / Volume 120 / June 2014
Fig. 2. Extent of hippocampal resection. A: Predissection axial T2-weighted MR image demonstrating the anatomical relationship of the orbit relative to the temporal lobe. The posterolateral orbital wall (blue line) lies immediately anterior to the temporal pole (arrowhead). Medial retraction of the globe and orbital craniectomy provide access to the temporal pole and the medial temporal lobe, including the hippocampus (arrow). B: Postdissection axial T2-weighted MR image showing near-complete resection of the hippocampal head and body to the level of the quadrigeminal cistern posterior to the collicular plate. C: Serial coronal sections from anterior (left) to posterior (right) illustrating the extent of resection and preservation of lateral temporal cortex, lateral wall of the temporal horn of the ventricle, and temporal white matter. D: Sagittal plane key.
this procedure compares to the current standard-of-care and other minimally invasive therapies for temporal lobe epilepsy. Because seizure control is directly correlated with the extent of hippocampal resection,48 one might expect TEA to have seizure outcomes comparable to the gold-standard procedures (anterior temporal lobectomy and selective amygdalohippocampectomy). However, detailed clinical studies are necessary before any definitive statements can be made. We enumerate the benefits and anticipated clinical challenges of TEA below. 1431
H. I. Chen et al. TABLE 2: Anatomical measurements for the transorbital approach* Measurement
Fig. 3. Orbital craniectomy. 3D reconstructions of the predissection (A) and postdissection (B) CT scans. An orbital view of the skull demonstrates the orbital craniectomy lateral to the superior orbital fissure, with preservation of a rim of bone. Estimates of intracranial access did not require unroofing the SOF.
Potential Benefits of TEA Reduction of Neurological Deficits Associated With Standard Approaches. Craniotomy for the treatment of
temporal lobe epilepsy is associated with well-described risks to neurological function (Table 1). TEA may reduce the incidence of these neurological sequelae. We consider below the major complications of hemiparesis, diplopia, and visual field deficits. Hemiparesis is among the most profound deficits associated with epilepsy surgery, occurring even in expert hands.47 This complication has been described following violation of the temporal stem or injury to the anterior choroidal artery, which results in ischemia to the posterior limb of the internal capsule.39 Traction upon the anterior choroidal artery may result in ischemia that is not apparent at the time of surgery. Retraction can cause primary tissue damage or secondary injury from direct compression and subsequent hypoperfusion in as little as 15 minutes.6 Clinically significant postoperative deficits attributable to retraction have been reported in 3%–10% of intracranial cases, depending on the approach and the experience of the operative team.2,43,50 Diplopia following temporal lobe surgery affects up to 19% of patients.10,40 Direct manipulation and thermal injury may result in demyelination, microischemia, and postoperative edema to the oculomotor and trochlear nerves.10 These nerves lie at the deep margin of the resection cavity and are veiled by the arachnoid during uncal resection. Although postoperative diplopia typically resolves within 6 months, cranial nerve dysfunction constitutes a significant morbidity. Visual field deficits are the most common complications associated with anterior temporal lobectomy and selective amygdalohippocampectomy, occurring in 55%–76% of cases.12,46 In a quarter of affected patients, the extent of the visual field loss may be sufficient to prevent them from obtaining a driver’s license.30 Visual field deficit results from division of optic radiations coursing along the tapetum in the lateral wall of the temporal horn of the lateral ventricle.36 They project from the lateral geniculate nucleus anterolaterally along the temporal horn27 and are commonly encountered during the intraventricular exposure of the hippocampus. The extent of division of the fibers along the tapetum predicts the extent of visual field loss. 1432
globe displacement midpupillary line to midline—pre-retraction midpupillary line to midline—w/ retraction estimated globe displacement periorbital tissue thickness medial lateral lateral orbital rim to dura craniectomy dimensions medial-lateral superior-inferior
Mean Value (mm) 33.5 ± 3.1 27.5 ± 3.7 6.0 ± 1.4 5.7 ± 1.0 4.9 ± 0.9 25 ± 2.9 10.2 ± 3.3 12.2 ± 1.5
* Mean values are presented with ± SDs.
This cadaveric study suggests that TEA may reduce the incidence of disabling neurological deficits by avoiding exposure of the temporal stem, permitting early identification of the branches of the anterior choroidal artery, and minimizing the need for brain retraction. TEA may also be expected to minimize oculomotor and trochlear nerve dysfunction because the mesial structures (for example, uncus, entorhinal cortex, perirhinal cortex, and cranial nerves) are visualized early during the course of the dissection. Additionally, the dissection trajectory proceeds away from the ambient cistern instead of toward the cistern. Finally, TEA may reduce the occurrence of visual field loss because the hippocampus is resected with preservation of the lateral tapetum and underlying optic radiations.
Reduction of Neurocognitive Complications. Tradition al approaches to the mesial temporal lobe necessitate disruption of the lateral temporal cortex and temporal white matter. Neurocognitive deficits are known to follow temporal lobe resections. TEA may reduce neurocognitive sequelae by preserving lateral temporal lobe cortex and white matter pathways important for language and memory. Language deficits following temporal lobe surgery are reliably documented when standard aphasia batteries are employed.20–22,31 These findings are particularly pronounced in patients with late age of seizure onset5 or in patients lacking a history of early neurological insults.44 The precise etiology of these language deficits is unknown. After selective amygdalohippocampectomy, language deficits correlate with the extent of cortical disruption.19 White matter pathways connecting distant cortical regions are critically important for language processing.11 Increasingly, it is appreciated that pathways beyond the superior longitudinal fasciculus/arcuate fasciculus are engaged in elements of language processing, such as phonological processing and semantic-lexical associations. Additional connectivity investigations may shed light on this anatomical-physiological relationship and refine which cortical regions and white matter pathways must be spared J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy
Fig. 4. Angles of exposure. The boundaries of exposure were recorded during the dissection and compared with the predictions based on preoperative T1-weighted MR images. The green lines represent the maximum medial-lateral (A) and superiorinferior (B) extent of access via the orbital craniectomy to a depth of 9 cm from the orbital rim.
during temporal lobe surgery. TEA preserves the temporal cortex with the exception of a 1.5-cm2 corticectomy at the anterior temporal pole. Memory decline also may occur after temporal lobe surgery. While the role of the hippocampus and entorhinal cortex in memory is well established, these structures are not the sole regions involved in memory function. The resection of lateral temporal cortical sites can lead to significant postoperative verbal memory decline.34 Additional evidence for the role of the lateral cortex in working memory is the higher rate of memory decline following anterior temporal lobectomy compared with selective amygdalohippocampectomy.18 The perirhinal cortex and temporal lobe white matter tracts are involved in semantic memory processing,23 as are the middle and inferior temporal gyri.9 Traditional surgical approaches can compromise the cortex and fiber tracts subserving memory function, resulting in progressive white matter atrophy up to a year following surgery16 and impeding cognitive recovery. TEA would not prevent memory deficits associated with hippocampal or mesial structure resection. However, memory functions supported by the lateral temporal lobe may be expected to remain intact if that region is preserved during TEA. Cosmetic Considerations. Traditional craniotomies require a scalp incision and surgical manipulation of the temporalis muscle. Temporalis muscle atrophy, as measured by volumetrics and electromyography, is observed in more than half of patients undergoing temporal lobe epilepsy surgery, even when the fascia is dissected care-
fully.49 Unilateral temporal hollowing results in obvious facial asymmetry. The cosmetic defect may become sufficiently pronounced to drive patients to pursue surgical reconstruction. Additionally, up to 10% of patients undergoing pterional craniotomies experience frontalis muscle palsy from injury to the frontotemporal branch of the facial nerve.1,41 TEA would not affect either temporalis or frontalis muscle function. In this cadaveric feasibility study, we approached the lateral orbital wall via a lateral orbital incision. This incision was necessary due to the stiffness of the fixed cadaveric tissue. For patients, an eyelid,37 eyebrow, or conjunctival33 incision would be preferred. Similar incisions for cosmetic “face-lifts” leave minimal scars. Nevertheless, a facial incision could be objectionable to some patients on cosmetic grounds, given the potential for periorbital scarring. Patients would have to be fully informed about this risk should TEA be applied clinically.
Considerations of Endoscopic Surgery. Cranial approaches have been adapted successfully for surgery of the anterior skull base25 and posterior fossa.28 Similar techniques pioneered by Moe and colleagues (transorbital neuroendoscopic surgery, or TONES)3,33 have been employed to treat CSF leaks, skull base fractures, and cavernous sinus and orbital apex lesions. Generally, endoscopic surgery is associated with shorter hospital stays7 and leads to an improved quality of life in the early postoperative period,32 although selection bias may confound these observations.
TABLE 3: Mean values of actual and predicted angles of exposure* Variable
Actual
Predicted (cadaver)
p-Value (actual vs predicted [cadaver])
Predicted (patients)
p-Value (actual vs predicted [patients])
no. of hemispheres medial-lateral angle superior-inferior angle
4 43° ± 5° 72° ± 10°
4 45° ± 2° 69° ± 7°
0.85 0.56
20 42° ± 4° 64° ± 5°
0.85 0.21
* Means are presented ± SDs.
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H. I. Chen et al. Anticipated Challenges to TEA
TEA is not a panacea for epilepsy surgery. As with any new surgical approach, a steep learning curve is expected. More important, TEA introduces risks that are not present with traditional surgical approaches. Whether these risks are outweighed by the potential benefits remains to be seen. We discuss some of the anticipated challenges to TEA and how they may be overcome.
Ophthalmological Considerations. Orbital surgery includes the potential for injury to the orbital contents: the globe, extraocular muscles, and neurovascular structures. Therefore, an experienced oculoplastic surgeon would be a valuable partner in performing a TEA. The primary ophthalmological consideration is preservation of visual acuity. In this investigation, 4–7 mm of globe retraction was required to permit access to the posterior lateral orbital wall. To determine whether this degree of retraction would deform the globe, we measured the periorbital space on both sides of the globe. The combined periorbital tissue thickness was greater than the maximum required globe displacement, suggesting that there is adequate space for such displacement within the orbit. Oculoplastic surgeons routinely apply retraction upon the globe to this degree and more without compromising vision. The initial description of the TONES approach found no postoperative ophthalmological complications in 20 consecutive patients.33 The authors monitored the integrity of the visual system by serially testing the pupillary reflex. In addition, the surgeons released globe retraction every 20–30 minutes. Tonometry also could be used during the initial implementation of TEA to quantitatively monitor the status of the globe. More likely than visual acuity changes is postoperative diplopia. Any manipulation of the intraorbital contents may cause diplopia as a result of edema in the periorbital fat and extraocular muscles or direct injury to the cranial nerves. No data yet exist for the rate of postoperative diplopia after TEA. In the setting of orbital trauma, 13% of patients experience diplopia after a TONES repair,3 which may be partially attributed to the nature of the orbital injury (traumatic fracture) necessitating surgical intervention. This rate is comparable to the rate of diplopia (5%–19%) in patients undergoing standard temporal lobectomy.10,40 Moving forward, a key factor in assessing the risk/benefit ratio for TEA would be determining the incidence and duration of postoperative diplopia or visual changes.
Cerebrospinal Fluid Leak. TEA requires a dural opening through a small orbitotomy. Therefore, a critical step in the successful clinical translation of this technique will be the creation of a watertight closure to prevent CSF leakage. This risk is impossible to accurately estimate in cadaveric specimens, in which the intracranial pressure is equivalent to atmospheric pressure. Instead, we can draw insights from the collective experience of endoscopic anterior skull base surgery. In this setting, the rate of CSF leaks has fallen to 1%–8%, depending on the extent of skull base resection.8,13,15,17,26,45 There are several reasons why the rate of CSF leak after TEA could be lower than after transsphenoidal sur-
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gery. Because the sella turcica is a bony depression within the air-filled sphenoid sinus, grafts used for dural repair are not naturally buttressed in any way. Moreover, the sella resides in a gravity-dependent position that puts increased fluid pressure on the dural repair. In contrast, the orbital contents could provide physical support to the dural repair, and the lateral orbit does not reside in a gravitydependent position. Of course, TEA introduces elements that may increase the risk of CSF leak relative to transsphenoidal approaches. In particular, hippocampectomy requires intraventricular access, which may change CSF flow dynamics and predispose patients to CSF leakage. Methods that may help minimize this risk include dural reconstruction and augmentation with synthetic or autologous grafts, graft buttressing with orbital wall reconstructive implants, polymer sealants, and lumbar drainage. As with the evolution of endoscopic anterior skull base surgery over the past decades, a learning curve would be expected.
Clinical Translation. Cadaveric specimens are useful models to investigate surgical approaches, but they do not fully replicate the clinical environment. Thus, there are challenges faced in the clinical environment that are not encountered in cadaveric studies. One of the clear differences between cadaveric and live brain tissue is tissue character. In this study, the intraaxial dissection likely was assisted by the stiffness of the fixed tissue, which prevented the surrounding brain from collapsing in on the resection cavity. In patients, the more supple brain may fall into the surgical cavity, thereby impairing visualization. A tube retraction system might be helpful in this case. Another issue not encountered in cadavers is bleeding. Important in all surgical cases, adequate hemostasis is especially vital in minimally invasive approaches, in which maneuverability is limited. The clinical translation of TEA would greatly benefit from the availability of a robust endoscopic bipolar electrocautery system. Lastly, the amount of globe retraction that can be tolerated in clinical practice may be less than the median of 6 mm used in this study. Less globe retraction would translate into reduced access. Intraoperative globe tonometry might be useful to determine the maximal safe degree of globe retraction. Alternatively, intermittent relaxation of retraction could be employed to protect the globe when more aggressive retraction is necessary.
Conclusions
Transorbital endoscopic amygdalohippocampectomy permits near-total resection of the mesial temporal structures through a minimal access corridor in cadaveric specimens. This feasibility study documented the angles of exposure and limits of resection predicted on predissection imaging studies and measured during the dissections themselves. These values were compared with MR images from epilepsy patients undergoing surgical evaluation for preclinical validation of the angles of exposure. While TEA has theoretical benefits compared with open craniotomy approaches, it has unique potential complicaJ Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy tions as well. Further study in patients is warranted to critically evaluate whether the anticipated benefits outweigh the potential complications of TEA. Acknowledgments We would like to thank Dr. Daqing Li (Department of Otorhinolaryngology, University of Pennsylvania) for access to dissection laboratory space. We would also like to thank Robin Armstrong and Dwayne Hallman for assistance with acquiring and managing the cadaveric specimens. Disclosure This work was supported by unrestricted educational grants (to H.I.C., L.E.B., and T.H.L.) and loan of equipment from Karl Storz. The study sponsor did not have any editorial input into study design, data analysis, or manuscript preparation. Author contributions to the study and manuscript preparation include the following. Conception and design: Chen, Lucas. Acquisition of data: all authors. Analysis and interpretation of data: Chen, Bohman, Lucas. Drafting the article: Chen. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Chen. Statistical analysis: Chen, Bohman. Study supervision: Lucas. References 1. Acar G, Acar F, Miller J, Spencer DC, Burchiel KJ: Seizure outcome following transcortical selective amygdalohippocampectomy in mesial temporal lobe epilepsy. Stereotact Funct Neurosurg 86:314–319, 2008 2. Andrews RJ, Bringas JR: A review of brain retraction and recommendations for minimizing intraoperative brain injury. Neurosurgery 33:1052–1064, 1993 3. Balakrishnan K, Moe KS: Applications and outcomes of orbital and transorbital endoscopic surgery. Otolaryngol Head Neck Surg 144:815–820, 2011 4. Behrens E, Schramm J, Zentner J, König R: Surgical and neurological complications in a series of 708 epilepsy surgery procedures. Neurosurgery 41:1–10, 1997 5. Bell BD, Davies KG, Hermann BP, Walters G: Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names. Neuropsychologia 38:83–92, 2000 6. Bennett MH, Albin MS, Bunegin L, Dujovny M, Hellstrom H, Jannetta PJ: Evoked potential changes during brain retraction in dogs. Stroke 8:487–492, 1977 7. Cappabianca P, Alfieri A, Colao A, Ferone D, Lombardi G, de Divitiis E: Endoscopic endonasal transsphenoidal approach: an additional reason in support of surgery in the management of pituitary lesions. Skull Base Surg 9:109–117, 1999 8. Cappabianca P, Cavallo LM, Esposito F, Valente V, De Divitiis E: Sellar repair in endoscopic endonasal transsphenoidal surgery: results of 170 cases. Neurosurgery 51:1365–1372, 2002 9. Chan D, Fox NC, Scahill RI, Crum WR, Whitwell JL, Leschziner G, et al: Patterns of temporal lobe atrophy in semantic dementia and Alzheimer’s disease. Ann Neurol 49:433– 442, 2001 10. Cohen-Gadol AA, Leavitt JA, Lynch JJ, Marsh WR, Cascino GD: Prospective analysis of diplopia after anterior temporal lobectomy for mesial temporal lobe sclerosis. J Neurosurg 99:496–499, 2003 11. Dick AS, Tremblay P: Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain 135:3529–3550, 2012 12. Egan RA, Shults WT, So N, Burchiel K, Kellogg JX, Salinsky M: Visual field deficits in conventional anterior temporal lo-
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bectomy versus amygdalohippocampectomy. Neurology 55: 1818–1822, 2000 13. Eloy JA, Choudhry OJ, Shukla PA, Kuperan AB, Friedel ME, Liu JK: Nasoseptal flap repair after endoscopic transsellar versus expanded endonasal approaches: is there an increased risk of postoperative cerebrospinal fluid leak? Laryngoscope 122:1219–1225, 2012 14. Engel J Jr: The timing of surgical intervention for mesial temporal lobe epilepsy: a plan for a randomized clinical trial. Arch Neurol 56:1338–1341, 1999 15. Esposito F, Dusick JR, Fatemi N, Kelly DF: Graded repair of cranial base defects and cerebrospinal fluid leaks in transsphenoidal surgery. Neurosurgery 60 (4 Suppl 2):295–304, 2007 16. Faber J, Schoene-Bake JC, Trautner P, von Lehe M, Elger CE, Weber B: Progressive fiber tract affections after temporal lobe surgery. Epilepsia 54:e53–e57, 2013 17. Hadad G, Bassagasteguy L, Carrau RL, Mataza JC, Kassam A, Snyderman CH, et al: A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap. Laryngoscope 116:1882–1886, 2006 18. Helmstaedter C, Grunwald T, Lehnertz K, Gleissner U, Elger CE: Differential involvement of left temporolateral and temporomesial structures in verbal declarative learning and memory: evidence from temporal lobe epilepsy. Brain Cogn 35:110–131, 1997 19. Helmstaedter C, Van Roost D, Clusmann H, Urbach H, Elger CE, Schramm J: Collateral brain damage, a potential source of cognitive impairment after selective surgery for control of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 75:323–326, 2004 20. Hermann B, Davies K, Foley K, Bell B: Visual confrontation naming outcome after standard left anterior temporal lobectomy with sparing versus resection of the superior temporal gyrus: a randomized prospective clinical trial. Epilepsia 40: 1070–1076, 1999 21. Hermann BP, Perrine K, Chelune GJ, Barr W, Loring DW, Strauss E, et al: Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches. Neuropsychology 13:3–9, 1999 22. Hermann BP, Wyler AR, Somes G, Clement L: Dysnomia after left anterior temporal lobectomy without functional mapping: frequency and correlates. Neurosurgery 35:52–57, 1994 23. Hirni DI, Kivisaari SL, Monsch AU, Taylor KI: Distinct neuroanatomical bases of episodic and semantic memory performance in Alzheimer’s disease. Neuropsychologia 51:930– 937, 2013 24. Jensen I: Temporal lobe surgery around the world. Results, complications, and mortality. Acta Neurol Scand 52:354– 373, 1975 25. Jho HD, Carrau RL: Endoscopy assisted transsphenoidal surgery for pituitary adenoma. Technical note. Acta Neurochir (Wien) 138:1416–1425, 1996 26. Kaptain GJ, Kanter AS, Hamilton DK, Laws ER: Management and implications of intraoperative cerebrospinal fluid leak in transnasoseptal transsphenoidal microsurgery. Neurosurgery 68 (1 Suppl Operative):144–151, 2011 27. Kier EL, Staib LH, Davis LM, Bronen RA: MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. AJNR Am J Neuroradiol 25:677–691, 2004 28. Lang SS, Chen HI, Lee JY: Endoscopic microvascular decompression: a stepwise operative technique. ORL J Otorhinolaryngol Relat Spec 74:293–298, 2012 29. Liscak R, Malikova H, Kalina M, Vojtech Z, Prochazka T, Marusic P, et al: Stereotactic radiofrequency amygdalohippocampectomy in the treatment of mesial temporal lobe epilepsy. Acta Neurochir (Wien) 152:1291–1298, 2010
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H. I. Chen et al. 30. Manji H: Epilepsy surgery, visual fields, and driving: a study of the visual field criteria for driving in patients after temporal lobe epilepsy surgery with a comparison of Goldmann and Esterman perimetry. Am J Ophthalmol 129:704, 2000 (Abstract) 31. Martin RC, Sawrie SM, Roth DL, Gilliam FG, Faught E, Morawetz RB, et al: Individual memory change after anterior temporal lobectomy: a base rate analysis using regressionbased outcome methodology. Epilepsia 39:1075–1082, 1998 32. McCoul ED, Anand VK, Schwartz TH: Improvements in site-specific quality of life 6 months after endoscopic anterior skull base surgery: a prospective study. Clinical article. J Neurosurg 117:498–506, 2012 33. Moe KS, Bergeron CM, Ellenbogen RG: Transorbital neuroendoscopic surgery. Neurosurgery 67 (3 Suppl Operative): ons16–ons28, 2010 34. Ojemann GA, Dodrill CB: Verbal memory deficits after left temporal lobectomy for epilepsy. Mechanism and intraoperative prediction. J Neurosurg 62:101–107, 1985 35. Parrent AG, Blume WT: Stereotactic amygdalohippocampotomy for the treatment of medial temporal lobe epilepsy. Epilepsia 40:1408–1416, 1999 36. Peltier J, Travers N, Destrieux C, Velut S: Optic radiations: a microsurgical anatomical study. J Neurosurg 105:294–300, 2006 37. Pelton RW: The anterior eyelid crease approach to the orbit. Curr Opin Ophthalmol 20:401–405, 2009 38. Rydenhag B, Silander HC: Complications of epilepsy surgery after 654 procedures in Sweden, September 1990-1995: a multicenter study based on the Swedish National Epilepsy Surgery Registrar. Neurosurgery 49:51–57, 2001 39. Sasaki-Adams D, Hadar EJ: Temporal lobe epilepsy surgery: surgical complications, in Luders HO (ed): Textbook of Epilepsy Surgery. London: Informa, 2008, pp 1288–1299 40. Sindou M, Guenot M, Isnard J, Ryvlin P, Fischer C, Mauguière F: Temporo-mesial epilepsy surgery: outcome and complications in 100 consecutive adult patients. Acta Neurochir (Wien) 148:39–45, 2006 41. Song J, Kim MH, Kim SH, Shin KM, Lee HK: The usefulness of subfascial temporalis dissection method in pterional craniotomy. J Korean Neurosurg Soc 26:235–240, 1997 42. Sperling MR, O’Connor MJ, Saykin AJ, Plummer C: Temporal lobectomy for refractory epilepsy. JAMA 276:470–475, 1996
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43. Spetzler RF, Daspit CP, Pappas CT: The combined supra- and infratentorial approach for lesions of the petrous and clival regions: experience with 46 cases. J Neurosurg 76:588–599, 1992 44. Stafiniak P, Saykin AJ, Sperling MR, Kester DB, Robinson LJ, O’Connor MJ, et al: Acute naming deficits following dominant temporal lobectomy: prediction by age at 1st risk for seizures. Neurology 40:1509–1512, 1990 45. Tabaee A, Anand VK, Brown SM, Lin JW, Schwartz TH: Algorithm for reconstruction after endoscopic pituitary and skull base surgery. Laryngoscope 117:1133–1137, 2007 46. Wiebe S, Blume WT, Girvin JP, Eliasziw M: A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:311–318, 2001 47. Wieser HG: Selective amygdalohippocampectomy has major advantages, in Miller JW, Silbergeld DL (eds): Epilepsy Surgery: Principles and Controversies. New York: Taylor & Francis, 2006, pp 465–478 48. Wyler AR, Hermann BP, Somes G: Extent of medial temporal resection on outcome from anterior temporal lobectomy: a randomized prospective study. Neurosurgery 37:982–991, 1995 49. Yasuda CL, Costa AL, Franca M Jr, Pereira FR, Tedeschi H, de Oliveira E, et al: Postcraniotomy temporalis muscle atrophy: a clinical, magnetic resonance imaging volumetry and electromyographic investigation. J Orofac Pain 24:391–397, 2010 50. Zhong J, Dujovny M, Perlin AR, Perez-Arjona E, Park HK, Diaz FG: Brain retraction injury. Neurol Res 25:831–838, 2003
Manuscript submitted June 7, 2013. Accepted February 24, 2014. A subset of the data from this manuscript was presented in abstract form at the Congress of Neurological Surgeons Annual Meeting, October 19–23, 2013, San Francisco, California. Please include this information when citing this paper: published online April 4, 2014; DOI: 10.3171/2014.2.JNS131060. Address correspondence to: H. Isaac Chen, M.D., 3rd Floor, Silverstein Pavilion, 3400 Spruce St., Philadelphia, PA 19104. email: [email protected].
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Transorbital endoscopic amygdalohippocampectomy: a feasibility investigation Laboratory investigation H. Isaac Chen, M.D.,1 Leif-Erik Bohman, M.D.,1 Laurie A. Loevner, M.D.,1,2 and Timothy H. Lucas, M.D., Ph.D.1 Department of Neurosurgery and 2Division of Neuroradiology, University of Pennsylvania, Philadelphia, Pennsylvania 1
Object. Resection of the hippocampus is the standard of care for medically intractable epilepsy in patients with mesial temporal sclerosis. Although temporal craniotomy in this setting is highly successful, the procedure carries certain immutable risks and may be associated with cognitive deficits related to cortical and white matter disruption. Alternative surgical approaches may reduce some of these risks by preserving the lateral temporal lobe. This study examined the feasibility of transorbital endoscopic amygdalohippocampectomy (TEA) as an alternative to open craniotomy in cadaveric specimens. Methods. TEA dissections were performed in 4 hemispheres from 2 injected cadaveric specimens fixed in alcohol. Quantitative predictions of the limits of exposure based on predissection imaging were compared with intradissection measurements. The extent of resection and angles of exposure during the dissection and on postdissection imaging were recorded. These measurements were validated with MRI studies from 10 epilepsy patients undergoing standard surgical evaluations. Results. The transorbital approach permitted direct access to the mesial temporal structures through the lateral orbital wall. Up to 97% of the hippocampal formation was resected with no brain retraction and minimal (mean 6.0 ± 1.4 mm) globe displacement. Lateral temporal lobe white matter tracts were preserved. Conclusions. TEA permits hippocampectomy comparable to standard surgical approaches without disrupting the lateral temporal cortex or white matter. This novel approach is feasible in cadaveric specimens and warrants clinical investigation in carefully selected cases. (http://thejns.org/doi/abs/10.3171/2014.2.JNS131060)
S
Key Words • amygdalohippocampectomy • endoscopy • epilepsy • temporal lobectomy • transorbital
urgical resection of the hippocampus is the standard of care for medically intractable temporal lobe epilepsy46 and significantly improves seizure control and quality of life.14,42 The 2 most common surgical approaches are anterior temporal lobectomy and selective amygdalohippocampectomy, both of which are performed through a standard temporal craniotomy. Despite the marked success of these approaches, craniotomy for the treatment of temporal lobe epilepsy is not without risk. Complications range from cosmetic disfigurement to permanent neurological and cognitive disability (Table 1). Though uncommon, these complications significantly diminish quality of life for affected patients. Alternative strategies that minimize these risks while still achieving an adequate hippocampectomy, the principle goal of surgery, could further improve patient outcomes.
Abbreviations used in this paper: IOF = inferior orbital fissure; SOF = superior orbital fissure; TEA = transorbital endoscopic amygdalohippocampectomy; TONES = transorbital neuroendoscopic surgery.
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Minimally invasive approaches have the potential to access the hippocampus with minimal disruption of the lateral temporal cortex and white matter pathways. For instance, stereotactic radiofrequency ablation permits hippocampal lesioning with 16–38 ablations through a single occipital bur hole.29,35 Likewise, endoscopic approaches may provide access to the hippocampus and permit resection under direct visualization. The present cadaveric study examines the feasibility of a transorbital approach to the mesial temporal lobe using endoscopic visualization and image guidance. Unlike the occipital approach, the transorbital route affords the surgeon a short working distance and early access to the anterior portion of the hippocampus. We present the quantitative metrics of transorbital endoscopic amygdalohippocampectomy (TEA) predicted by predissection neuroimaging in relation to the measurements taken during the dissections. These measurements are compared with scans from 10 patients with epilepsy for clinical validation of the angles of exposure. J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy TABLE 1: Neurological and cognitive complications of temporal craniotomies Complication
Authors & Year
No. of Incidence Patients (%)
visual field deficit
Wiebe et al., 2001 Egan et al., 2000 trochlear nerve palsy Cohen-Gadol et al., 2003 oculomotor nerve palsy Sindou et al., 2006 language deficit Acar et al., 2008 Jensen, 1975 memory deficit Acar et al., 2008 hemiparesis Wieser, 2006 Rydenhag & Silander, 2001 Behrens et al., 1997
40 29 47
55 76 19
100 39 858* 39 478 654
5 2.5 5 5 1 2.2
279*
1.4
* Temporal lobe procedures only.
Methods Cadaveric Specimens
Two adult cadaveric heads were obtained from the Maryland State Anatomy Board. These heads were fixed with a mixture of ethanol and glycerin and then injected with colored latex for vessel identification. The Operational Committee on Cadaver and Body Parts and the Institutional Review Board of the University of Pennsylvania approved the usage of cadaveric specimens in this study.
Predissection and Postdissection Imaging
Predissection CT and MRI scans were performed for dissection planning and intraoperative navigation. The CT studies of the head were performed on a Siemens Sensation 16 scanner, utilizing a BrainLAB protocol designed for operative navigation. The examinations included highresolution thin-section (1-mm) axial images in a medium smooth sinus window with a 300-mm field of view and reconstructed bone windows. Direct coronal images were also obtained using 3-mm sections in a medium smooth sinus window and were also reconstructed into bone windows. Predissection high-resolution MRI of the brain was performed on a 3.0-T unit (Siemens Magnetom Trio). Localizing images were obtained, followed by sagittal T1weighted and axial T2-weighted 5-mm-thick images, coronal high-resolution turbo spin echo T2-weighted 3-mm sections, and coronal T1-weighted true inversion recovery volumetric 4-mm-thick images. Then coronal oblique turbo spin echo T2-weighted 3-mm-thick sections were acquired from the ventral orbit through the temporal lobe angled to provide direct line of sight of the endoscopic trajectory through the lateral orbit to the medial temporal lobe (aligned with the long axis of the mesial temporal lobe). Following cadaveric dissections, CT and MRI studies utilizing the same preoperative sequences were repeated to assess the size of the craniectomy and the extent of temporal lobe resection.
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Dissection Equipment
The specimens were stabilized in a custom frame and then registered for frameless stereotactic navigation using the S7 StealthStation (Medtronic) running Synergy cranial planning and navigation software v2.1.5 (Medtronic). Anatomical measurements were obtained using superficial cranial landmarks. The initial soft-tissue dissection and bone work were performed with an operating microscope. Visualization of the intracranial space was obtained with a 0° and 30° Hopkins II 4-mm neuroendoscope and high-definition Storz endoscope system (Karl Storz). For each side, the distance from the midpupillary point to the midline was measured before orbital retraction and then again with the retractor in its final position. The distance between the lateral orbital rim and the lateral dural edge was recorded after dissection.
Dissection Technique
The heads were positioned supine with the surgeon seated above the head to simulate the standard operating position. A 2-cm curved skin incision was made lateral to the orbital rim (Fig. 1A). This lateral orbital incision was necessary due to the firmness of the fixed cadaveric skin and subcuticular tissue. In clinical practice, an eyelid/ eyebrow or retrocanthal incision would be used. The orbicularis oculi muscle was incised parallel to its fibers. The lateral orbital rim was exposed. A subperiosteal dissection was performed down to the level of the inferior orbital fissure (IOF). The orbit was gently retracted medially with a malleable retractor. The frontozygomatic suture, first identified on the lateral orbital rim, was a useful landmark for finding the IOF and defining the inferior-lateral extent of the craniectomy (Fig. 1B). A craniectomy was made superior to the IOF and lateral to the superior orbital fissure (SOF) with a high-speed electric drill. The dura was opened to reveal the temporal pole (Fig. 1C and D). The sylvian fissure was visualized at the superior extent of the craniotomy. Frameless stereotactic navigation was used to identify the desired trajectory to the hippocampus. In general, this angle was 10° superior to the canthomeatal line. Next, a 0° endoscope was introduced into the craniectomy. Simple suctioning facilitated the limited corticectomy, which measured approximately 1.5 cm in diameter. The anterior termination of the temporal horn of the lateral ventricle was readily identified. The anterior and inferior portions of the amygdala were resected. The pes of the hippocampus and the temporal horn was readily visualized (Fig. 1E). In 2 hemispheres, the hippocampectomy preceded the resection of the uncus and entorhinal cortex. In the other 2, the reverse order was employed. Securing the endoscope in place with a holding arm at the 12 o’clock position (the inferior aspect of the orbit) allowed for concurrent use of two instruments for the dissection. Resection of the amygdala and hippocampus was performed with gentle suction along the natural planes to a depth of up to 10 cm from the orbital rim (Fig. 1F). The anterior choroidal artery branches were clearly visualized throughout the dissection. Following amygdalohippocampectomy, resection of the uncus and entorhinal cortex was performed in subpial fashion, with careful preservation of the pial boundaries medially. The lateral brainstem, 1429
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Fig. 1. Dissection technique. Orientation: For A–F, left is medial, and bottom is cranial. For G, left is anterior, and bottom is cranial. A: A curvilinear incision (arrowhead) is made adjacent to the left lateral canthus. The horizontal line perpendicular to the incision is the canthomeatal line. The orientation lines designate superior (S), inferior (I), medial (M), and lateral (L) and apply to all images but G. B: The orbital contents are dissected in a subperiosteal manner and retracted medially with a malleable retractor. Along the lateral orbital wall, the frontozygomatic suture (arrowhead) leads to the inferior orbital fissure (probe tip). C: The planned region of the orbital craniectomy is outlined by the oval. D: After the craniectomy, removal of the dura reveals the temporal pole. E: Dissection through the temporal pole using frameless stereotactic navigation leads to the pes of the hippocampus (asterisk). F: Resection of the medial temporal lobe structures, including the head and body of the hippocampus and the inferior amygdala, is complete. The choroid plexus (arrowhead) and temporal lobe white matter (asterisk) remain laterally. Medially, the pia and vasculature in the ambient cistern are seen (arrow). G: With a 30° angled endoscope, the lateral brainstem and ambient cistern are readily visible. Superior to the tentorium cerebelli (asterisk), the posterior cerebral artery (arrowhead) wraps around the cerebral peduncle. The optic tract (arrow) is seen medial to the preserved choroidal vessels. Portions of the pia mater were preserved during the cadaveric dissection. For adoption in a clinical setting, the intent would be to preserve the entirety of the pia, as is done during open surgery.
cranial nerves, and vessels within the CSF cisterns were readily apparent with application of the 30° endoscope. The removal of the remaining medial temporal lobe was performed in a subpial fashion. The 30° endoscope enabled further inspection of the lateral ventricle and temporal lobe white matter laterally and the brainstem and other neurovascular structures medially once the pia had been opened (Fig. 1G). Analysis of Exposure
The limits of the surgical exposure were predicted on CT and MRI using the boundaries of the orbit, measurements of the globe diameter, and measurements of the extraglobe soft tissues within the orbit. Angles of exposure were predicted with reference to the apex of the orbit lateral to the insertion of the annulus of Zinn and the SOF. During the dissection, measured angles of exposure were obtained anatomically and again using the frameless stereotactic probe. Coordinates for each stage of the dissection were digitally recorded in the Synergy cranial application. We used OsiriX v5.5.1 (www.osirix-viewer.com) to analyze the pre- and postdissection imaging studies. The size of the orbital craniectomy, angles of exposure afforded by the craniectomy, and extent of hippocampal resection were measured. Values for the maximal medial-lateral and superior-inferior dimensions of the approach were measured on axial and sagittal CT sections, respectively.
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We created 3D reconstructions with reformatted images from the CT data to delineate the relationship between the craniectomy and the orbital bony anatomy. Intradissection coordinates of the surgical exposure boundaries were mapped onto the predissection MR images to determine the surgical angles of exposure. We predicted the horizontal and vertical angles of exposure using the midpupillary axial T2-weighted section and the sagittal T1-weighted section approximately 3 mm lateral to the midpupillary point, respectively. Readily identifiable anatomical landmarks were used to define the sides of the angular measurements. The extent of the lateral orbital exposure determined the medial limits of intracranial access, and vice versa. Similarly, the superior and inferior orbital boundaries determined the inferior and superior limits of intracranial access. In the axial plane, the medial border was defined by a line connecting the lateral orbital rim to the lateral edge of the SOF. The lateral border was defined by a line connecting a point 6 mm medial to the lateral edge of the orbit at the level of the pupil, mimicking orbital retraction, to the point on the sphenoid bone adjacent to the temporalis muscle laterally and the temporal pole inferomedially. In the sagittal plane, the superior border was defined by a line connecting the inferior orbital rim to the sphenoid bone adjacent to the sylvian fissure. The inferior border was defined by a line connecting the superior orbital rim to the floor of the middle cranial fossa. The actual and predicted angles of exposure were J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy compared using the Mann-Whitney U-test for nonparametric variables, with a p value of 0.05 as the threshold for significance. Finally, the hippocampal volume on pre- and postdissection MR images was manually segmented. We defined the extent of hippocampal resection as a simple ratio of the 2 calculated volumes. To validate cadaveric predictions with patients seen in clinical practice, we measured the predicted limits of exposure for 10 consecutive patients undergoing standard evaluation for epilepsy surgery. The method for analyzing the predicted transorbital approach was identical to that in the cadaveric specimens. Institutional review board approval was obtained for this aspect of the study separately.
Results
In all 4 cadaveric hemispheres, we successfully performed an amygdalohippocampectomy and resection of mesial structures (Fig. 2). The extent of hippocampal resection was 97% (volume 2.42 cm3 predissection vs 0.07 cm3 postdissection). This resection was achieved through a mean orbital opening of 10.2 × 12.2 mm (Fig. 3; Table 2). The maximum globe displacement was 7 mm. This maximum was within the range of the measured periorbital tissue thickness. The duration of each dissection was approximately 90 minutes. The approach described above yielded a wide range of intracranial access (Fig. 4). In the axial plane, access to the brainstem medially and the lateral temporal white matter was possible. In the sagittal plane, it was possible to reach the inferior frontal lobe superiorly and the middle cranial fossa floor inferiorly. The depth of resection reached the level of the quadrigeminal cistern. There was no significant difference between the observed angles of exposure, derived from intradissection neuronavigation coordinates, and the predicted angles of exposure measured from the predissection MRI study (medial-lateral, p = 0.85; superior-lateral, p = 0.56). We also measured predicted angles of exposure from preoperative MR images in 10 patients with seizure disorders undergoing evaluation for epilepsy surgery (medial-lateral, 42° ± 4°; superior-inferior, 64° ± 5°; Table 3). There were no significant differences between the actual cadaveric and predicted patient angles of exposure (medial-lateral, p = 0.85; superior-lateral, p = 0.21), suggesting that our cadaveric angle of exposure data can be generalized to patients.
Discussion
In cadaveric heads, the transorbital endoscopic approach enables near-total resection of the amygdala, hippocampus, uncus, and perirhinal and entorhinal cortex. Lateral orbital craniectomy affords access to the anterior temporal pole aligned with the long axis of the mesial temporal lobe (Fig. 4). Endoscopy permits panoramic visualization and illumination of the mesial structures, the mesencephalon, and the ambient and crural cisterns with minimal retraction upon the globe and no retraction of the temporal lobe. It remains to be seen how well these findings translate into the clinical arena and how the risk/benefit profile of J Neurosurg / Volume 120 / June 2014
Fig. 2. Extent of hippocampal resection. A: Predissection axial T2-weighted MR image demonstrating the anatomical relationship of the orbit relative to the temporal lobe. The posterolateral orbital wall (blue line) lies immediately anterior to the temporal pole (arrowhead). Medial retraction of the globe and orbital craniectomy provide access to the temporal pole and the medial temporal lobe, including the hippocampus (arrow). B: Postdissection axial T2-weighted MR image showing near-complete resection of the hippocampal head and body to the level of the quadrigeminal cistern posterior to the collicular plate. C: Serial coronal sections from anterior (left) to posterior (right) illustrating the extent of resection and preservation of lateral temporal cortex, lateral wall of the temporal horn of the ventricle, and temporal white matter. D: Sagittal plane key.
this procedure compares to the current standard-of-care and other minimally invasive therapies for temporal lobe epilepsy. Because seizure control is directly correlated with the extent of hippocampal resection,48 one might expect TEA to have seizure outcomes comparable to the gold-standard procedures (anterior temporal lobectomy and selective amygdalohippocampectomy). However, detailed clinical studies are necessary before any definitive statements can be made. We enumerate the benefits and anticipated clinical challenges of TEA below. 1431
H. I. Chen et al. TABLE 2: Anatomical measurements for the transorbital approach* Measurement
Fig. 3. Orbital craniectomy. 3D reconstructions of the predissection (A) and postdissection (B) CT scans. An orbital view of the skull demonstrates the orbital craniectomy lateral to the superior orbital fissure, with preservation of a rim of bone. Estimates of intracranial access did not require unroofing the SOF.
Potential Benefits of TEA Reduction of Neurological Deficits Associated With Standard Approaches. Craniotomy for the treatment of
temporal lobe epilepsy is associated with well-described risks to neurological function (Table 1). TEA may reduce the incidence of these neurological sequelae. We consider below the major complications of hemiparesis, diplopia, and visual field deficits. Hemiparesis is among the most profound deficits associated with epilepsy surgery, occurring even in expert hands.47 This complication has been described following violation of the temporal stem or injury to the anterior choroidal artery, which results in ischemia to the posterior limb of the internal capsule.39 Traction upon the anterior choroidal artery may result in ischemia that is not apparent at the time of surgery. Retraction can cause primary tissue damage or secondary injury from direct compression and subsequent hypoperfusion in as little as 15 minutes.6 Clinically significant postoperative deficits attributable to retraction have been reported in 3%–10% of intracranial cases, depending on the approach and the experience of the operative team.2,43,50 Diplopia following temporal lobe surgery affects up to 19% of patients.10,40 Direct manipulation and thermal injury may result in demyelination, microischemia, and postoperative edema to the oculomotor and trochlear nerves.10 These nerves lie at the deep margin of the resection cavity and are veiled by the arachnoid during uncal resection. Although postoperative diplopia typically resolves within 6 months, cranial nerve dysfunction constitutes a significant morbidity. Visual field deficits are the most common complications associated with anterior temporal lobectomy and selective amygdalohippocampectomy, occurring in 55%–76% of cases.12,46 In a quarter of affected patients, the extent of the visual field loss may be sufficient to prevent them from obtaining a driver’s license.30 Visual field deficit results from division of optic radiations coursing along the tapetum in the lateral wall of the temporal horn of the lateral ventricle.36 They project from the lateral geniculate nucleus anterolaterally along the temporal horn27 and are commonly encountered during the intraventricular exposure of the hippocampus. The extent of division of the fibers along the tapetum predicts the extent of visual field loss. 1432
globe displacement midpupillary line to midline—pre-retraction midpupillary line to midline—w/ retraction estimated globe displacement periorbital tissue thickness medial lateral lateral orbital rim to dura craniectomy dimensions medial-lateral superior-inferior
Mean Value (mm) 33.5 ± 3.1 27.5 ± 3.7 6.0 ± 1.4 5.7 ± 1.0 4.9 ± 0.9 25 ± 2.9 10.2 ± 3.3 12.2 ± 1.5
* Mean values are presented with ± SDs.
This cadaveric study suggests that TEA may reduce the incidence of disabling neurological deficits by avoiding exposure of the temporal stem, permitting early identification of the branches of the anterior choroidal artery, and minimizing the need for brain retraction. TEA may also be expected to minimize oculomotor and trochlear nerve dysfunction because the mesial structures (for example, uncus, entorhinal cortex, perirhinal cortex, and cranial nerves) are visualized early during the course of the dissection. Additionally, the dissection trajectory proceeds away from the ambient cistern instead of toward the cistern. Finally, TEA may reduce the occurrence of visual field loss because the hippocampus is resected with preservation of the lateral tapetum and underlying optic radiations.
Reduction of Neurocognitive Complications. Tradition al approaches to the mesial temporal lobe necessitate disruption of the lateral temporal cortex and temporal white matter. Neurocognitive deficits are known to follow temporal lobe resections. TEA may reduce neurocognitive sequelae by preserving lateral temporal lobe cortex and white matter pathways important for language and memory. Language deficits following temporal lobe surgery are reliably documented when standard aphasia batteries are employed.20–22,31 These findings are particularly pronounced in patients with late age of seizure onset5 or in patients lacking a history of early neurological insults.44 The precise etiology of these language deficits is unknown. After selective amygdalohippocampectomy, language deficits correlate with the extent of cortical disruption.19 White matter pathways connecting distant cortical regions are critically important for language processing.11 Increasingly, it is appreciated that pathways beyond the superior longitudinal fasciculus/arcuate fasciculus are engaged in elements of language processing, such as phonological processing and semantic-lexical associations. Additional connectivity investigations may shed light on this anatomical-physiological relationship and refine which cortical regions and white matter pathways must be spared J Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy
Fig. 4. Angles of exposure. The boundaries of exposure were recorded during the dissection and compared with the predictions based on preoperative T1-weighted MR images. The green lines represent the maximum medial-lateral (A) and superiorinferior (B) extent of access via the orbital craniectomy to a depth of 9 cm from the orbital rim.
during temporal lobe surgery. TEA preserves the temporal cortex with the exception of a 1.5-cm2 corticectomy at the anterior temporal pole. Memory decline also may occur after temporal lobe surgery. While the role of the hippocampus and entorhinal cortex in memory is well established, these structures are not the sole regions involved in memory function. The resection of lateral temporal cortical sites can lead to significant postoperative verbal memory decline.34 Additional evidence for the role of the lateral cortex in working memory is the higher rate of memory decline following anterior temporal lobectomy compared with selective amygdalohippocampectomy.18 The perirhinal cortex and temporal lobe white matter tracts are involved in semantic memory processing,23 as are the middle and inferior temporal gyri.9 Traditional surgical approaches can compromise the cortex and fiber tracts subserving memory function, resulting in progressive white matter atrophy up to a year following surgery16 and impeding cognitive recovery. TEA would not prevent memory deficits associated with hippocampal or mesial structure resection. However, memory functions supported by the lateral temporal lobe may be expected to remain intact if that region is preserved during TEA. Cosmetic Considerations. Traditional craniotomies require a scalp incision and surgical manipulation of the temporalis muscle. Temporalis muscle atrophy, as measured by volumetrics and electromyography, is observed in more than half of patients undergoing temporal lobe epilepsy surgery, even when the fascia is dissected care-
fully.49 Unilateral temporal hollowing results in obvious facial asymmetry. The cosmetic defect may become sufficiently pronounced to drive patients to pursue surgical reconstruction. Additionally, up to 10% of patients undergoing pterional craniotomies experience frontalis muscle palsy from injury to the frontotemporal branch of the facial nerve.1,41 TEA would not affect either temporalis or frontalis muscle function. In this cadaveric feasibility study, we approached the lateral orbital wall via a lateral orbital incision. This incision was necessary due to the stiffness of the fixed cadaveric tissue. For patients, an eyelid,37 eyebrow, or conjunctival33 incision would be preferred. Similar incisions for cosmetic “face-lifts” leave minimal scars. Nevertheless, a facial incision could be objectionable to some patients on cosmetic grounds, given the potential for periorbital scarring. Patients would have to be fully informed about this risk should TEA be applied clinically.
Considerations of Endoscopic Surgery. Cranial approaches have been adapted successfully for surgery of the anterior skull base25 and posterior fossa.28 Similar techniques pioneered by Moe and colleagues (transorbital neuroendoscopic surgery, or TONES)3,33 have been employed to treat CSF leaks, skull base fractures, and cavernous sinus and orbital apex lesions. Generally, endoscopic surgery is associated with shorter hospital stays7 and leads to an improved quality of life in the early postoperative period,32 although selection bias may confound these observations.
TABLE 3: Mean values of actual and predicted angles of exposure* Variable
Actual
Predicted (cadaver)
p-Value (actual vs predicted [cadaver])
Predicted (patients)
p-Value (actual vs predicted [patients])
no. of hemispheres medial-lateral angle superior-inferior angle
4 43° ± 5° 72° ± 10°
4 45° ± 2° 69° ± 7°
0.85 0.56
20 42° ± 4° 64° ± 5°
0.85 0.21
* Means are presented ± SDs.
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H. I. Chen et al. Anticipated Challenges to TEA
TEA is not a panacea for epilepsy surgery. As with any new surgical approach, a steep learning curve is expected. More important, TEA introduces risks that are not present with traditional surgical approaches. Whether these risks are outweighed by the potential benefits remains to be seen. We discuss some of the anticipated challenges to TEA and how they may be overcome.
Ophthalmological Considerations. Orbital surgery includes the potential for injury to the orbital contents: the globe, extraocular muscles, and neurovascular structures. Therefore, an experienced oculoplastic surgeon would be a valuable partner in performing a TEA. The primary ophthalmological consideration is preservation of visual acuity. In this investigation, 4–7 mm of globe retraction was required to permit access to the posterior lateral orbital wall. To determine whether this degree of retraction would deform the globe, we measured the periorbital space on both sides of the globe. The combined periorbital tissue thickness was greater than the maximum required globe displacement, suggesting that there is adequate space for such displacement within the orbit. Oculoplastic surgeons routinely apply retraction upon the globe to this degree and more without compromising vision. The initial description of the TONES approach found no postoperative ophthalmological complications in 20 consecutive patients.33 The authors monitored the integrity of the visual system by serially testing the pupillary reflex. In addition, the surgeons released globe retraction every 20–30 minutes. Tonometry also could be used during the initial implementation of TEA to quantitatively monitor the status of the globe. More likely than visual acuity changes is postoperative diplopia. Any manipulation of the intraorbital contents may cause diplopia as a result of edema in the periorbital fat and extraocular muscles or direct injury to the cranial nerves. No data yet exist for the rate of postoperative diplopia after TEA. In the setting of orbital trauma, 13% of patients experience diplopia after a TONES repair,3 which may be partially attributed to the nature of the orbital injury (traumatic fracture) necessitating surgical intervention. This rate is comparable to the rate of diplopia (5%–19%) in patients undergoing standard temporal lobectomy.10,40 Moving forward, a key factor in assessing the risk/benefit ratio for TEA would be determining the incidence and duration of postoperative diplopia or visual changes.
Cerebrospinal Fluid Leak. TEA requires a dural opening through a small orbitotomy. Therefore, a critical step in the successful clinical translation of this technique will be the creation of a watertight closure to prevent CSF leakage. This risk is impossible to accurately estimate in cadaveric specimens, in which the intracranial pressure is equivalent to atmospheric pressure. Instead, we can draw insights from the collective experience of endoscopic anterior skull base surgery. In this setting, the rate of CSF leaks has fallen to 1%–8%, depending on the extent of skull base resection.8,13,15,17,26,45 There are several reasons why the rate of CSF leak after TEA could be lower than after transsphenoidal sur-
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gery. Because the sella turcica is a bony depression within the air-filled sphenoid sinus, grafts used for dural repair are not naturally buttressed in any way. Moreover, the sella resides in a gravity-dependent position that puts increased fluid pressure on the dural repair. In contrast, the orbital contents could provide physical support to the dural repair, and the lateral orbit does not reside in a gravitydependent position. Of course, TEA introduces elements that may increase the risk of CSF leak relative to transsphenoidal approaches. In particular, hippocampectomy requires intraventricular access, which may change CSF flow dynamics and predispose patients to CSF leakage. Methods that may help minimize this risk include dural reconstruction and augmentation with synthetic or autologous grafts, graft buttressing with orbital wall reconstructive implants, polymer sealants, and lumbar drainage. As with the evolution of endoscopic anterior skull base surgery over the past decades, a learning curve would be expected.
Clinical Translation. Cadaveric specimens are useful models to investigate surgical approaches, but they do not fully replicate the clinical environment. Thus, there are challenges faced in the clinical environment that are not encountered in cadaveric studies. One of the clear differences between cadaveric and live brain tissue is tissue character. In this study, the intraaxial dissection likely was assisted by the stiffness of the fixed tissue, which prevented the surrounding brain from collapsing in on the resection cavity. In patients, the more supple brain may fall into the surgical cavity, thereby impairing visualization. A tube retraction system might be helpful in this case. Another issue not encountered in cadavers is bleeding. Important in all surgical cases, adequate hemostasis is especially vital in minimally invasive approaches, in which maneuverability is limited. The clinical translation of TEA would greatly benefit from the availability of a robust endoscopic bipolar electrocautery system. Lastly, the amount of globe retraction that can be tolerated in clinical practice may be less than the median of 6 mm used in this study. Less globe retraction would translate into reduced access. Intraoperative globe tonometry might be useful to determine the maximal safe degree of globe retraction. Alternatively, intermittent relaxation of retraction could be employed to protect the globe when more aggressive retraction is necessary.
Conclusions
Transorbital endoscopic amygdalohippocampectomy permits near-total resection of the mesial temporal structures through a minimal access corridor in cadaveric specimens. This feasibility study documented the angles of exposure and limits of resection predicted on predissection imaging studies and measured during the dissections themselves. These values were compared with MR images from epilepsy patients undergoing surgical evaluation for preclinical validation of the angles of exposure. While TEA has theoretical benefits compared with open craniotomy approaches, it has unique potential complicaJ Neurosurg / Volume 120 / June 2014
Transorbital hippocampectomy tions as well. Further study in patients is warranted to critically evaluate whether the anticipated benefits outweigh the potential complications of TEA. Acknowledgments We would like to thank Dr. Daqing Li (Department of Otorhinolaryngology, University of Pennsylvania) for access to dissection laboratory space. We would also like to thank Robin Armstrong and Dwayne Hallman for assistance with acquiring and managing the cadaveric specimens. Disclosure This work was supported by unrestricted educational grants (to H.I.C., L.E.B., and T.H.L.) and loan of equipment from Karl Storz. The study sponsor did not have any editorial input into study design, data analysis, or manuscript preparation. Author contributions to the study and manuscript preparation include the following. Conception and design: Chen, Lucas. Acquisition of data: all authors. Analysis and interpretation of data: Chen, Bohman, Lucas. Drafting the article: Chen. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Chen. Statistical analysis: Chen, Bohman. Study supervision: Lucas. References 1. Acar G, Acar F, Miller J, Spencer DC, Burchiel KJ: Seizure outcome following transcortical selective amygdalohippocampectomy in mesial temporal lobe epilepsy. Stereotact Funct Neurosurg 86:314–319, 2008 2. Andrews RJ, Bringas JR: A review of brain retraction and recommendations for minimizing intraoperative brain injury. Neurosurgery 33:1052–1064, 1993 3. Balakrishnan K, Moe KS: Applications and outcomes of orbital and transorbital endoscopic surgery. Otolaryngol Head Neck Surg 144:815–820, 2011 4. Behrens E, Schramm J, Zentner J, König R: Surgical and neurological complications in a series of 708 epilepsy surgery procedures. Neurosurgery 41:1–10, 1997 5. Bell BD, Davies KG, Hermann BP, Walters G: Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names. Neuropsychologia 38:83–92, 2000 6. Bennett MH, Albin MS, Bunegin L, Dujovny M, Hellstrom H, Jannetta PJ: Evoked potential changes during brain retraction in dogs. Stroke 8:487–492, 1977 7. Cappabianca P, Alfieri A, Colao A, Ferone D, Lombardi G, de Divitiis E: Endoscopic endonasal transsphenoidal approach: an additional reason in support of surgery in the management of pituitary lesions. Skull Base Surg 9:109–117, 1999 8. Cappabianca P, Cavallo LM, Esposito F, Valente V, De Divitiis E: Sellar repair in endoscopic endonasal transsphenoidal surgery: results of 170 cases. Neurosurgery 51:1365–1372, 2002 9. Chan D, Fox NC, Scahill RI, Crum WR, Whitwell JL, Leschziner G, et al: Patterns of temporal lobe atrophy in semantic dementia and Alzheimer’s disease. Ann Neurol 49:433– 442, 2001 10. Cohen-Gadol AA, Leavitt JA, Lynch JJ, Marsh WR, Cascino GD: Prospective analysis of diplopia after anterior temporal lobectomy for mesial temporal lobe sclerosis. J Neurosurg 99:496–499, 2003 11. Dick AS, Tremblay P: Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain 135:3529–3550, 2012 12. Egan RA, Shults WT, So N, Burchiel K, Kellogg JX, Salinsky M: Visual field deficits in conventional anterior temporal lo-
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Manuscript submitted June 7, 2013. Accepted February 24, 2014. A subset of the data from this manuscript was presented in abstract form at the Congress of Neurological Surgeons Annual Meeting, October 19–23, 2013, San Francisco, California. Please include this information when citing this paper: published online April 4, 2014; DOI: 10.3171/2014.2.JNS131060. Address correspondence to: H. Isaac Chen, M.D., 3rd Floor, Silverstein Pavilion, 3400 Spruce St., Philadelphia, PA 19104. email: [email protected].
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