Selective Amygdalohippocampectomy
Selective Amygdalohippocampectomy
Amygdalohippocampectomy
Alastair T. Hoyt, MD, Kris A. Smith, MD*
KEYWORDS
Amygdalohippocampectomy Epilepsy Mesial temporal sclerosis Subtemporal
Temporal lobectomy Transcortical Transsylvian
KEY POINTS
Selective amygdalohippocampectomy effectively reduces seizure severity and frequency in pa-
tients with mesial temporal epilepsy.
Selective procedures seem to be as effective as anterior temporal lobectomy in patients whose dis-
ease is limited to the mesial temporal structures.
Although the evidence is inconclusive, it suggests that selective amygdalohippocampectomy may
preserve neurocognitive function better than anterior temporal lobectomy.
Multiple approaches are available to access the mesial temporal structures.
There is no definitive evidence for the superiority of a particular approach in terms of seizure control
or neurocognitive outcome.
Mandatory studies
PATIENT EVALUATION OVERVIEW
Indications Review of seizure history, semiology, and
symptoms
SAHC is reserved for patients with disabling,
Neuropsychological evaluation
medically intractable seizures that originate unilat-
erally in mesial temporal structures (Box 1).4,13–15 Video scalp EEG monitoring
The American Academy of Neurology recom- High-resolution MRI with coronal projections
mends that patients with drug-resistant MTLE re-
Complementary studies
sulting in disabling complex partial seizures be
referred for surgery5 because of a single random- PET with fludeoxyglucose F 18
ized controlled trial and a further 24 observational Ictal single-photon emission computed
studies.16 The International League Against Epi- tomography
lepsy (ILAE) defined drug resistance as failure of Magnetoencephalography
2 tolerated, appropriately chosen, and used anti-
Intracarotid amobarbital testing (Wada test)
epileptic drug schedules.15
Selective posterior cerebral artery amobar-
bital testing (selective Wada test)
Preoperative Evaluation
Intracranial EEG electrode monitoring
There are 2 key factors in selecting a patient for
Functional MRI
SAHC. First, localization of the epileptogenic zone
to the mesial temporal structures is paramount. Diffusion tensor imaging
Second, assessment of the risk for function decline Abbreviations: EEG, electroencephalography; MRI,
due to surgery is no less important. A full discussion magnetic resonance imaging; PET, positron emission
of seizure localization and risk assessment is tomography.
beyond the scope of this article, but most inves-
tigators2,16–20 agree that a thorough neurologic
examination, clear understanding of the seizure Complementary evaluation techniques can also
semiology, interictal electroencephalographic be of great value. However, a well-designed sys-
(EEG) evaluation, high-resolution magnetic reso- tematic review by Burch and colleagues21 of
nance imaging (MRI) of the brain, and neuropsycho- noninvasive presurgical evaluation other than
logical evaluation represent a minimum presurgical EEG and MRI identified no randomized trials or
investigation (Box 2). Indeed, the ILAE Subcommis- cohort studies, and minimal high-quality evidence
sion for Pediatric Epilepsy Surgery concluded that of effectiveness in any individual complementary
interictal EEG, neuropsychological assessment, study. The investigators opined that each of the
and high-resolution MRI were mandatory.19 complementary techniques may be useful in the
context of a comprehensive evaluation and rec-
Box 1 ommended thorough discussion of individual
Patient selection for SAHC cases in a multidisciplinary conference to provide
an optimal surgical plan. As elegantly described
Indications by Spencer and Burchiel,20 the selection of pa-
Disabling, drug-resistant, mesial temporal tients should depend on converging lines of
lobe epilepsy evidence.
Some investigators advocate reserving SAHC for
Contraindications
cases when imaging abnormalities are present on
Evidence that patients will have neurocogni- MRI.13 Other surgeons argue that if there is reason-
tive decline with surgery, which would able confidence of a mesial temporal seizure origin,
outweigh the benefit of seizure control
SAHC may be offered with the option of completing
Multifocal onset of seizures or bilateral inde- resection of the neocortical structures at a later
pendent mesial temporal lobe onset date if necessary. ATL with resection of the medial
Patients’ general medical inability to tolerate structures may be more appropriate if there are
surgery findings consistent with neocortical sources.22
Abbreviations: SAHC, selective amygdalohippocam-
The senior author’s current practice is to stereotac-
pectomy. tically implant depth electrodes into the hippocam-
pus and amygdala bilaterally in MRI-negative
Selective Amygdalohippocampectomy 3
fissure, and amygdala can be visualized on the described variations on the approach.2,49,50 This
medial inferior walls of the ventricle. approach takes advantage of the sylvian fissure
An opening is made in the ependyma at the ven- to access the mesial temporal region without
tricular sulcus at the junction of the hippocampus disruption of the lateral and anterior neocortex of
and the collateral eminence, and dissection is car- the white matter tracts surrounding the lateral
ried into the parahippocampal gyrus. With a com- ventricle. Yas‚argil and colleagues’ stated goal
bination of microdissection and ultrasonic was to perform a “pure lesionectomy.”11
aspiration, a subpial dissection of the parahippo-
campal gyrus in performed. The tentorial edge, Operative procedure
oculomotor nerve, posterior communicating ar- Patients are positioned in the supine position with
tery, posterior cerebral artery, and optic tract are the shoulder ipsilateral to the operative site sup-
typically visible through the pia; care should be ported. The head is fixated and rotated such that
taken to not violate the pia to preserve these the malar eminence is the highest point of the sur-
structures. Subpial dissection is carried forward gical field to bring the sylvian fissure into a roughly
into the tissue of the uncus. With traction from mi- vertical orientation. A semilunar incision is opened
crodissectors, the choroidal fissure can be similar to other pterional approaches. The tempo-
opened and the thin attachment of the fimbria ralis may be divided or dissected via an interfascial
hippocampi can be divided, allowing the hippo- technique. A craniotomy is fashioned overlying the
campus to be mobilized laterally and inferiorly. sylvian fissure. The craniotomy should extend su-
The vessels of the hippocampal arcade are coag- perior to the fissure by approximately 1.5 cm. A
ulated and divided as close as possible to the hip- drill is used to flatten the greater and lesser wings
pocampus to avoid injury to the parent vessels. of the sphenoid to the level of the superior orbital
The hippocampus is transected in the coronal fissure to facilitate exposure. The dura is opened
plane at the junction of the body and tail, providing and reflected over the remolded sphenoid and
an en bloc resection of the body and head of the orbit. Under microscopic magnification, the syl-
hippocampus. vian fissure is opened from the region of the ca-
Attention is turned to the residual parahippo- rotid bifurcation to about 2 cm distal to the MCA
campal gyrus and amygdala, which is resected bifurcation. The limen insulae, ascending M1
within the bounds of the medial and inferior pial branch, and anterior third of the insular cortex
margins. The amygdala may be as high as the hor- with its associated M2 branches can be visualized.
izontal segment of the middle cerebral artery The inferior circular sulcus, which separates the
(MCA). Additional subpial ultrasonic aspiration temporal operculum from the insula, is identified.
and microdissection of the tail of the hippocampus A 1- to 2-cm corticotomy is created in the tem-
is carried posteriorly from the site of the coronal poral stem at the level of the limen insulae, and
transection to at least the plane of the colliculi. dissection is carried down to the uncus parallel
The wound is irrigated and closed. to the M1 segment until the temporal horn of the
lateral ventricle is encountered. The tissue within
Special surgical considerations the uncus is resected by subpial dissection, taking
The location of the lateral temporal corticotomy care that the pia-arachnoid boundary is left intact.
can be varied, depending on the required angle The amygdala can be identified at the anterior
to approach the mesial structures on navigation.13 border of a line between the choroidal fissure
Some investigators37 advocate placing the inci- and the limen insulae. The amygdala and associ-
sion in a more posterior position (just anterior to ated entorhinal cortex in the anterior portion of
the plane of the central sulcus) in the nondominant the parahippocampal gyrus are resected. The
hemisphere and in a more anterior position (just opening into the ventricle is extended posteriorly
anterior to the plane of the precentral sulcus) in to better visualize the choroid emerging from the
the dominant hemisphere. The use of intraopera- choroidal fissure, which will mark the mesial
tive image-guided navigation can also be used to boundary of hippocampal dissection. An incision
tailor an entry site.45,47 is created in the floor of the lateral ventricle, lateral
to the hippocampus in the region of the collateral
Transsylvian Approach
eminence, and carried down to the collateral sul-
Overview cus. This incision defines the lateral boundary of
The transsylvian approach for SAHC (TS SAHC) the resection. Microdissectors and gentle traction
was introduced by Yas‚argil and colleagues in are used to define the superior medial border of
1973 and was first described by Wieser and Ya- the hippocampus along the choroidal fissure.
s‚argil48 in 1982, with several subsequent descrip- This incision provides access to the hippocampal
tions.10,11,39 Various investigators have now vessels entering the hippocampal fissure, which
Selective Amygdalohippocampectomy 5
Fig. 3. (A) Postoperative coronal T2-weighted magnetic resonance imaging (MRI) showing that the hippocampus
was resected with preservation of all lateral temporal lobe structures. The approach does not disrupt the tempo-
ral stem (arrow). (B) Postoperative axial T2-weighted MRI obtained at different levels showing selective resection
of the mesial temporal structures. The hippocampus was resected posteriorly just beyond the level of the collic-
ular plate. (From Little AS, Smith KA, Kirlin K, et al. Modifications to the subtemporal selective amygdalohippo-
campectomy using a minimal-access technique: seizure and neuropsychological outcomes. J Neurosurg
2009;111(6):1269; with permission.)
Table 1
Theoretical advantages of various approaches to SAHC
Fig. 4. The different approaches to the hippocampus. Note that the transsylvian approach involves some transec-
tion of the temporal stem in order to gain access to the temporal horn and visualize the hippocampus. The trans-
sulcal and trans-T2–gyral approaches are technically easiest to perform; however, they result in injury and some
disconnection of the lateral temporal white matter in order to access the mesial structures. The subtemporal
approach, by entering into the collateral sulcus between the fusiform and parahippocampal gyrus, spares all
of the lateral temporal structures and the frontotemporal connections of the temporal stem and, therefore,
should theoretically have potentially the best chance of preserving cognitive functions related to the lateral tem-
poral lobe. (Courtesy of Barrow Neurological Institute, Phoenix, AZ; with permission.)
Table 2
Select publications detailing surgical complications after SAHC
Abbreviations: CN, cranial nerve; SAHC, selective amygdalohippocampectomy; ST SAHC, subtemporal SAHC; TC SAHC,
transcortical SAHC; TS SAHC, transsylvian SAHC; VFD, visual field defect.
Data from Refs.9,11,28,62,101,106–108
EVALUATION OF OUTCOME AND LONG- suggest that selective procedures have a superior
TERM RECOMMENDATIONS functional outcome.75,76
Seizure Control A single controlled trial77 comparing the memory
outcomes of surgically and medically treated pa-
Control of seizures is the primary measure of suc-
tients with temporal lobe epilepsy revealed that
cess after SAHC. Two prospective randomized
both groups had cognitive decline after 10 years,
clinical trials have demonstrated the superiority
although seizure-free patients showed significant
of surgical treatment of MTLE over medical man-
recovery of nonmemory function after surgery. Ev-
agement, with 58% to 73% of surgical patients
idence from structured reviews and meta-ana-
achieving seizure freedom versus 0% to 8% in
lyses78–82 suggests that intelligence is not
the medical group.3,4 An analysis by Jobst and
affected by temporal lobe surgery. Verbal decline
Cascino52 of 9 systematic reviews and 2 large
is the most common adverse event following tem-
case studies identified rates of seizure freedom
poral lobe resection, with 44% of patients with left-
following temporal lobe surgery of 34% to 73%
sided surgery and 20% with right-sided surgery
(median 62.4%). However, no randomized clinical
showing a decline in verbal memory.80 Nondomi-
trials comparing SAHC with medical management
nant resections do not seem to be associated
alone have been performed to date. Therefore,
with substantial nonverbal memory decline.79,82
rates of seizure control after SAHC are frequently
Naming deficits were present in 34% of dominant
compared with those following ATL.
temporal lobe resections.78,80 Evidence is accu-
Reported outcomes vary considerably, with
mulating that postoperative memory preservation
most large series reporting that 50% to 90% of pa-
after ATL depends on reorganization within the
tients with MTLE are seizure free 1 year after
ipsilateral temporal lobe, including the posterior
SAHC.11,16,26,52,62–70 For example, Mackenzie
hippocampus, anterior cingulum, orbitofrontal cor-
and colleagues64 reported only 21% seizure
tex, and insula.83
freedom at 1 year after SAHC, whereas Tanriverdi
and Olivier68 reported 100% seizure freedom at
the same interval. Several factors contribute to Comparison of Anterior Temporal Lobectomy
the variability of reported outcomes. First, and Selective Amygdalohippocampectomy
although outcomes are frequently reported using
Although selective procedures were developed in
the scale proposed by Engel and colleagues,71
an effort to preserve function, no prospective, ran-
there is no clear consensus of what constitutes a
domized controlled trials demonstrate superiority
satisfactory outcome. Second, MTLE is the com-
of SAHC or ATL. Two meta-analyses have sup-
mon pathologic expression of a highly heteroge-
ported a moderate advantage to seizure control
neous group of patients. Third, the technique,
with ATL for a 5% to 8% greater likelihood of
approach, and experience of the surgeon vary.
seizure freedom.84,85 A comparison study at 2
Most importantly, accuracy of seizure localization
separate centers also suggested that ATL was
and patient selection can vary independently
slightly more effective in seizure control than
from the technical success of surgery and exerts
SAHC, but the difference did not reach statistical
perhaps the highest influence on outcome.
significance.86 However, SAHC led to significantly
There is evidence that seizures recur in patients
better results in visual encoding, verbal and short-
who are initially seizure free.16,62,72,73 Conversely,
term memory, and visual working memory. Many
some studies suggest the effect of surgery is
retrospective studies are available (see Table 3).
more durable. Wasade and colleagues74 reported
Most studies suggest that, in appropriately
long-term outcomes of 253 patients up to 15 years
selected patients, seizure control after surgery is
after surgery, with a mean just more than 10 years.
similar for SAHC or ATL,51,68,86–90 whereas others
Among patients who had undergone temporal
suggest ATL provides superior seizure control.26,66
resection, 78% reported favorable (Engel class I
There is evidence to suggest that neuropsycho-
and II) outcomes after more than 15 years.
logical outcomes are improved after selective pro-
cedures,49,88,91–93 although some investigators
found no significant differences.94,95 Helmstaedter
Neuropsychological Outcomes
and colleagues91 performed a detailed prospec-
Although seizure control following surgery is of tive study suggesting that, in surgery on the domi-
utmost concern, preservation of function is equally nant side, ATL was less impactful on measures of
important. There is a paucity of high-quality data verbal learning than SAHC, whereas on the
specific to SAHC,52 and comparison is often nondominant side, selective surgery was less
made to the better-characterized risks following impactful. Interestingly, a study of category-
ATL (Table 3). Converging lines of evidence related naming and object recognition found no
Table 3
Select publications comparing temporal lobe resection surgeries
Duration of
Study Number of Follow- Classification of
Author, Year Comparing Design Patients up (mo) Favorable Outcome Seizure Outcome Cognitive Outcome
Helmstaedter et al,65 ATL vs TS SAHC vs Retro 59 3 Seizure free No difference Favors ALT
1996 lesionectomy
Mackenzie et al,64 ATL vs SAHC Retro 100 12 Engel III or better Favors ATL No difference
1997
Clusmann et al,87 2002 ATL vs TS SAHC vs Retro 321 38 Engel II or better No difference Favors SAHC
lesionectomy
Clusmann et al,26 2004 ATL vs TS SAHC Retro 89 (peds) 46 Engel II or better Favors ATL No difference on
right, favors ATL on
left
Hader et al,109 2005 ATL vs TC SAHC Retro 72 Not specified Engel II or better No difference No difference
Paglioli et al,88 2006 ATL vs TC SAHC Pro 161 70 Engel I No difference Favors SAHC
Morino et al,49 2006 ATL vs TS SAHC Retro 49 12 Seizure free No difference Favors SAHC
Bate et al,66 2007 CAH vs SAHC Retro 114 12 Engel II or better Favors ATL Not reported
Tanriverdi and CAH vs TC SAHC Retro 72 12 Engel II or better No difference No difference
Selective Amygdalohippocampectomy
Olivier68 2007
Helmstaedter et al,91 Modified ATL vs Pro 97 12 Only Engel I included Only Engel I included ATL better verbal
2008 TS SAHC learning, SAHC
better figural
learning
Tanriverdi et al,62 2008 CAH vs TC SAHC Retro 100 60 Engel II or better No difference Not examined
Tanriverdi et al,89 2010 CAH vs TC SAHC Retro 256 12 Engel II or better No difference No difference
Sagher et al,86 2012 ATL vs TC SAHC Retro 96 44 Engel I No difference No difference
Bujarski et al,72 2013 ATL vs TC SAHC Retro 69 81 Engel II or better No difference No difference
Wendling et al,90 2013 ATL vs TS SAHC Retro 95 102 Seizure free No difference Favors SAHC
Mansouri et al,110 ATL vs TC SAHC Retro 54 40 Seizure free No difference No difference
2014
Abbreviations: ATL, anterior temporal lobectomy; CAH, corticoamygdalohippocampectomy; peds, pediatric patients; Pro, prospective; Retro, retrospective; SAHC, selective amygda-
lohippocampectomy; TC SAHC, transcortical SAHC; TS SAHC, transsylvian SAHC.
Data from Refs.26,49,62,64–66,72,86–91,109,110
11
12 Hoyt & Smith
differences in patients undergoing ATL or selective neuropsychological outcomes among the 80 pa-
procedures but superior outcomes following tients studied. Other investigators have reported
SAHC using laser interstitial thermal ablation.96 similar equality of seizure control between the
Although psychiatric outcomes are infrequently two methods.70,99 Inconsistency in testing tech-
reported, Bujarski and colleagues72 found no dif- niques between studies, particularly in regard to
ference in depression or anxiety between ATL neuropsychological function, make high-quality
and SAHC. However, measures of paranoia in- comparisons difficult, if not impossible (Table 4).
creased overall with ATL and decreased overall Von Rhein and colleagues100 evaluated neuro-
with selective surgery. Taking this evidence to- psychological outcomes in matched cohorts of
gether, SAHC seems to be as effective as ALT in patients who underwent transsylvian and subtem-
patients with disease limited to the mesial tempo- poral approaches. Although the study design did
ral structures. Although not conclusive, the not allow a comparison of seizure control, the in-
converging evidence suggests that selective vestigators found more decline in verbal recogni-
resection likely offers better neurocognitive out- tion memory in left TS SAHC and more decline in
comes. More esoteric functions attributed to the figural memory and verbal fluency with ST SAHC.
anterolateral temporal lobe, such as semantic Very positive outcomes were reported in several
memory and relating conceptual understanding studies of subtemporal approaches.9,41,101–103 Ta-
to social norms, are difficult to assess with stan- kaya and colleagues41 demonstrated postopera-
dard neuropsychiatric paradigms but would theo- tive improvement in glucose metabolism, verbal
retically be preserved by SAHC and be impaired memory, attention, and delayed recall following a
after ATL.97 subtemporal approach in a limited number of
patients without a control group. In a detailed anal-
ysis of 47 patients, Hill and colleagues104 demon-
Comparison of Approaches to Selective
strated decline in memory, verbal intellect, and
Amygdalohippocampectomy
naming in 29% to 38% of patients undergoing
Data supporting the use of a particular surgical dominant hemisphere surgery, and declines in
approach for SAHC are even more limited than memory in 36% of patients undergoing nondomi-
data comparing SAHC with ATL. Lutz and col- nant hemisphere surgery using the minimal access
leagues98 published a rare, prospective random- approach described by the senior author. Current
ized trial comparing transsylvian and transcortical investigations are under way to determine if
approaches. With the exception of phonemic preoperative factors, such as hippocampal vol-
fluency, which improved after transcortical proce- ume on MRI, can identify patients at higher risk
dures, there was no difference in seizure or for developing deficits after ST SAHC. Some
Table 4
Select publications comparing approaches to SAHC
Duration of
Number of Follow-up Seizure Cognitive
Author, Year Comparing Study Design Patients (mo) Outcome Outcome
Renowden TC SAHC vs Retrospective 17 24 No No difference
et al,60 TS SAHC difference
1995
Lutz et al,98 TC SAHC vs Randomized 80 7 No Slightly better
2004 TS SAHC prospective difference phonemic
fluency
in TC SAHC
von Rhein ST SAHC vs Prospective 26 12 Could not No difference
et al,100 TS SAHC cohort report
2011
Drane et al,96 TC SAHC vs Nonrandomized 58 6 No Favored SLAHC in
2015 ATL vs prospective difference naming and
SLAHC recognition of
famous faces
surgeons,98,105 in an effort to preserve cognitive results in the partial disconnection or injury to the
function, have begun to explore other ablation spared lateral cortex. ST SAHC is the authors’
techniques, such as laser thermal ablation. Early favored approach because of the minimal access
reports of these techniques suggest positive re- needed and because of the theoretical lack of
sults with respect to preservation of function but disconnection or damage from the approach itself,
with likely diminished long-term seizure control although admittedly ventral visual pathway injury
compared with complete mesial resections. Clin- may contribute to memory decline beyond what
ical trials comparing laser ablation with SAHC would occur from hippocampectomy alone. Expe-
have been initiated to accurately quantify the po- rience and skill on the part of the treating surgeon
tential disparity. are necessities for the safe and efficacious execu-
tion of all the discussed approaches. Specialized
Long-term Follow-up training in a high-volume center is strongly recom-
mended before attempting these techniques
The authors advocate follow-up of patients who
independently.
have undergone SAHC for at least 1 year after sur-
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