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| Journal of the New Zealand Medical Association,
30-October-2009, Vol 122 No 1305
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Temporal lobe resection for refractory temporal lobe
epilepsy at Auckland Hospital
Ravi Suppiah, Edward Mee, Elizabeth B Walker, Lynair
Roberts, Gregory Finucane, Peter S Bergin
Epilepsy is one of the most common neurological
disorders.1 Many patients who have epilepsy
have seizures that can be controlled relatively
easily.2,3 However, up to 30% of patients have
seizures that are resistant to currently available anti-epileptic
drugs.4,5 Many of these patients have their
lives greatly disrupted by their seizures.
A proportion of these patients can be rendered seizure-free
with surgery. Most elective surgery to cure epilepsy is performed in patients
with temporal lobe epilepsy6,7 Temporal lobe
epilepsy is the most common cause of refractory epilepsy in
adults,8 and experience has demonstrated that
surgery in this group of patients is more successful than surgery in patients
whose seizures arise elsewhere in the
brain.9–12 Most contemporary surgical
series suggest that 50–70% of individuals are seizure-free after temporal
lobectomy.7,9,12–21
Modern day surgical treatment for temporal lobe epilepsy was
first described by Penfield and Baldwin in
1952.22 Since then, temporal lobectomies have
been performed on thousands of patients throughout the world. A single
randomised controlled trial of epilepsy surgery has been
performed.18 Eighty patients who had undergone
a pre surgical assessment in London, Ontario, and who were deemed suitable for
surgery, were randomised to go onto the routine surgical waiting list, (which at
the time was over 1 year) or to have immediate surgery.
Forty patients were randomised to undergo immediate surgery;
on an intention to treat analysis, 58% were seizure-free after 1 year, versus 8%
of those who received medical treatment alone during the year.
Epilepsy surgery was first performed at Auckland Hospital in
1961. The first 26 patients were written up in this journal in
1987.23 Forty percent of those patients went
into long-term remission. We now describe the ongoing experience with temporal
lobectomy in Auckland since 1987.
The term ‘epilepsy surgery’ encompasses
operations that are performed specifically with the intention of curing
epilepsy. It does not include patients who have tumours or other lesions that
need surgery in their own right, even if they present with seizures. In this
paper we analyse patients who were assessed at Auckland Hospital by neurologists
with a special interest in epilepsy, and who subsequently underwent temporal
lobectomies with the specific intention of curing the epilepsy.
Patients and MethodsSince 1997 a prospective database of all patients who
undergo epilepsy surgery at Auckland Hospital has been maintained by the
epilepsy surgery unit. We reviewed neurology, neurophysiology and neurosurgical
records to identify patients who underwent surgery between 1987 (when the first
26 patients were reported) and 1997. Information has been reviewed for all
patients who underwent temporal lobectomies between 1987 and December 2007.
Nearly all patients were operated on by the same surgeon (EM).
As part of the work up for surgery, all patients have a
detailed clinical assessment by an epilepsy specialist, and undergo awake and
sleep interictal EEG recordings. The vast majority also undergo video-monitoring
to capture ictal EEG recordings. All patients undergo neuro-imaging; since 1994,
most individuals have had at least one MRI prior to surgery. Patients routinely
undergo pre and postoperative visual field testing and neuropsychological
testing. Wada tests (intracarotid sodium amytal injections) have been performed
when there has been concern that the patient may be at risk of postoperative
amnesia, though this test is seldom now performed.
All patients are seen in Auckland 1 year after surgery
by an epilepsy specialist (PB or EW) and a neuropsychiatrist (GF). A further
formal neuropsychological assessment and MR scan are also obtained at this time.
Most patients continue to be followed by a neurologist for several years, though
if they remain seizure-free they are eventually discharged from the clinic.
However, an attempt is made to maintain phone or e-mail contact with these
patients on an annual basis.
Seizure outcome following surgery has been determined
using Engel’s Classification.10 A class I
outcome means that patients have had no seizures resulting in loss of awareness
since surgery, or for at least 2 years. (Patients may continue to have auras,
and can have had a generalized seizure after antiepileptic drug withdrawal).
Class II comprises patients with rare but ongoing seizures. Class III is
considered a worthwhile improvement in seizures, while Class IV comprises
patients with no significant improvement in seizure control. Atypical seizures
occurring within 1 month of the time of surgery are disregarded.
ResultsWe identified 242 patients who had undergone surgery for
epilepsy between 1987 and December 2007; There were 176 temporal lobe
resections, 39 lesionectomies, 8 corpus callosotomies, 8 hemispherectomies, 7
frontal lobe resections, 2 transcallosal resections of hypothalamic harmatomas,
and 2 brain biopsies.
We describe here the 176 patients who underwent temporal
lobe resections. All patients had seizures that were refractory to medical
therapy. We have at least 1 year of follow up for 174 patients. Patients
originated from all over the country (Table 1).
Table 1. Origin of patients by
district
There were 75 males and 101 females. Ages ranged from
10–61 years (mean 34 years). We had access to reports of video monitoring
for 84% of the patients; most patients had seizures recorded with scalp
electrodes only, though a small number had foramen ovale electrodes or subdural
electrodes inserted. Usually, all tests were congruent, and suggested that
seizures arose from one temporal lobe, though in a minority of cases one or more
of the tests gave discordant data. A decision to operate in these patients was
made on the basis of a balance of probabilities.
Left temporal lobe resection was performed in 83 patients,
and right temporal lobe resection in 93 patients.
Table 2. Patient characteristics
Seizure outcome (Table 3)—Overall 98
of 174 (56%) individuals were seizure-free 1 year after surgery (Engel Class I).
A further 61 (35%) had rare seizures (Engel Class II) or had significant
improvement in seizure frequency compared to preoperatively (Engel Class
III). There was no significant change in seizure outcomes between
follow up at 1 year and at the end of follow-up (average 4.3 years).
Table 3. Seizure outcome based on Engel
classification
Pathology—Histological analysis was
performed on all specimens. Results of the examination of the resected specimens
were available in 170 (96.5%) individuals. The most common finding was
hippocampal sclerosis, and this was present in 129 (73%) patients. The grade of
hippocampal sclerosis (Wyler score)24 was
determined in 90 (70%) of these specimens. The remainder had a variety of other
pathologies as listed in Table 4.
Table 4. Histopathology
Complications (Table 5)—There were 16
permanent complications directly attributable to surgery. This included 2
deaths. The first death occurred in a 30-year-old female who developed
Staphylococcus aureus meningitis a few days postoperatively, which
progressed to ventriculitis and death. The second death was a 32-year-old female
who had did not wake up postoperatively. Imaging showed bilateral thalamic
haemorrhages and diffuse brain oedema. She died soon afterwards.
There were two non-fatal strokes. A 13-year-old girl
developed a right hemiparesis, following left-sided temporal lobe resection.
Following rehabilitation, she made a good recovery. A 29-year-old female who had
a right temporal lobe resection developed infarction of the inferior and
posteromedial right temporal lobe and medial right occipital lobe, in keeping
with an occlusion of the right posterior cerebral artery. Her neurological
deficit was a permanent left homonymous hemianopia.
Six other patients had symptomatic visual field defects. One
patient had persistent gait problems, and four individuals developed troublesome
dysphasia. All of the individuals with dysphasia had left temporal lobe
resections. A single individual had persisting but unexplained urinary
incontinence postoperatively.
Thirteen individuals developed postoperative infections
(details listed in Table 5). All of these resolved with treatment. One patient
had a pulmonary embolus. A further four patients were diagnosed with aseptic
meningitis.
Results of detailed psychiatric assessments were available
on 114 of the 174 patients. Of these 66 had a lifetime prevalence of anxiety or
depression or another Axis I Disorder. A new episode of psychological symptoms
occurred in 52% of these 114 patients during the first year after surgery.
Depression was present in the first postoperative year in 50 patients, and 30
patients took antidepressant medication during that year; many of these patients
also had a prior history of depression. The postoperative depression had often
resolved by the time of the 1-year follow up. Anxiety disorders (most commonly
panic disorder) occurred in 15 patients, and 10 were prescribed anxiolytic /
hypnotics for this indication.
Thirty-eight patients had a lifetime prevalence of an Axis
II Disorder (personality disorder or intellectual impairment). New onset
psychosis occurred during the first postoperative year in two patients, though
both had previously had a psychotic episode.
Table 5. Surgical complications
*114 patients assessed.
There were 11 deaths over the duration of follow up. Six
individuals are thought to have died from sudden unexplained death in epilepsy
(SUDEP), one died during a witnessed seizure, one drowned, one committed
suicide, one died from a malignancy, and one died as a result of a head injury
(not related to his epilepsy).
Of the patients with presumed SUDEP, one patient was thought
to have been seizure-free until being found dead. (Engel Class 1) The other four
patients had had continuing seizures despite surgery (one patient in Engel Class
2, three patients in Engel Class 3, and one in Engel Class 4)
DiscussionThe goal of surgery in treating medically refractory
seizures is to eliminate seizures, and to improve quality of life. Clearly,
performing neurosurgery for epilepsy is a major undertaking. Not all patients
become seizure-free, and there are significant risks associated with the
surgery.
Overall, more than 90% of individuals who have undergone
surgery in Auckland have had improved seizure control, with 56% becoming
seizure-free. The outcome in our series is similar to that of other recently
published series.7, 11-13, 18, 19, 21 Being
seizure-free at 1 year was predictive of remaining seizure-free for the duration
of follow up in our series. This is consistent with other investigators who have
reported that seizure outcome 1 year postoperatively is a reasonable predictor
of long-term outcome.9, 13, 14,25
The impact of becoming seizure-free has often been dramatic.
Most of the patients who have stopped having seizures have obtained drivers
licences, and many of them have been able to markedly improve their work
circumstances. Nearly all those patients who became seizure-free have told us
that surgery has been enormously beneficial to them. Many of them have reported
that the surgery has transformed their lives. Even those who have not become
seizure-free generally state that they are pleased to have ‘given it a
go’.
There are well recognised risks of temporal lobectomies, and
these risks are discussed with patients in detail before a final decision
regarding surgery is made.21 Despite the
dramatic benefit that surgery often produces in a patient’s general
quality of life, there is often a temporary deterioration in psychiatric state.
Chronic epilepsy itself is associated with a high incidence of psychiatric
morbidity, and this is particularly common in patients whose seizures arise from
one or other temporal lobe.26, 27
It is clear that this can be temporarily exacerbated by
temporal lobectomy. Postoperative psychiatric depression may meet DSM-IV
criteria for Major Depression, while anxiety disorders, insomnia, irritability,
and even non epileptic attacks are all well
recognised.28 A Melbourne study suggests that
depression, anxiety and adjustment difficulties are at their most prominent 1
month after surgery and are improving by 3
months.29 It is often difficult to know whether
mental disorders arising in this population are true postoperative complications
or due to the stress of adapting to life without epilepsy, other epilepsy
related stressors, or medication changes.
Regardless of the cause, it is important that these
psychological problems are identified and treated to reduce the chances of
chronic morbidity.
It is estimated that a superior homonymous quadrantic field
defect can be detected on formal testing in 50% of patients, but is symptomatic
in only 8%.30 Only 3.4% of individuals in our
series complained of visual field problems.
Surgical complications are often not analysed in detail in
the epilepsy surgery literature, and psychiatric problems are often not
discussed. The reported complication rates range from
4-20%.13, 21, 30-32 Many series have ignored
reversible postoperative neurological disturbances that do not affect the
patients’ long-term outcome (e.g. aseptic meningitis), or have taken the
view that visual field defects are an unavoidable result of temporal lobe
surgery, and do not list these as postoperative complications.
A large series which specifically addressed the issue of
complications in epilepsy surgery reviewed 708 cases including 279 temporal
resections.30 Two per cent developed permanent
neurological deficits and 10% had temporary complications (including infections,
deep vein thrombosis and pulmonary embolus) following temporal lobe resection.
This series did not include mood disorders in its list of complications.
These surgical risks have to be weighed against the risk of
refractory epilepsy itself. The most important of these risks is sudden death in
epilepsy (SUDEP), which is as high as 0.9% per annum in some patient groups with
severe, drug resistant epilepsy.33 Successful
surgery appears to reduce this risk.34 Two of
our patients died as a result of the surgery, but a further seven patients died
during follow up as a result of uncontrolled epilepsy, despite the surgery.
One of these patients was thought to be seizure-free until
found dead, but surgery had not rendered the other six patients seizure-free. We
do not know the rate of SUDEP in New Zealand patients who have not been suitable
for surgery. However, Nilsson et al reported 6.3 cases of SUDEP per 1000 patient
years in 212 Swedish patients who were worked up for epilepsy surgery, but who
did not undergo an operation; this was in contrast to a rate of SUDEP of 2.4
cases per 1000 patient years in patients who underwent
surgery.35
Overall, temporal lobe resection has been very effective in
stopping or reducing seizures in the majority of our patients. In appropriate
patients it can be life changing. Many of the patients who have been rendered
seizure-free as a result of surgery have been able to lead much more productive
and satisfying lives, though in some of these there was a temporary exacerbation
of psychological problems during the first postoperative year.
The Auckland Epilepsy Group have offered surgery to patients
throughout the country, although the programme is not formally recognised or
funded as a national programme. However, there is an imbalance in rates of
operations performed for patients from different areas; this appears to be due
to a difference in referral patterns. Similar discrepancies in surgical rates
have also been noted in other countries, particularly Great
Britain.36 In the past, we understand that some
patients—particularly from the South Island—were sent to Australia
for epilepsy surgery.
It is possible that some operations may have also been
performed at other New Zealand centres, in which case our figures may not
reflect the true rate of surgery for the different regions. However, we doubt if
many temporal lobectomies will have been performed in other New Zealand
hospitals, since the Neurological Association of New Zealand decided some years
ago that a single New Zealand centre should undertake epilepsy surgery.
This is because a large team of health professionals is
involved in the workup towards surgery, and a certain minimum number of cases
need to be undertaken on a regular basis to maintain expertise. Guidelines
published by the National Association of Epilepsy centres in the USA recommended
that surgery should be performed in centres where an average of 20 epilepsy
operations per year could be undertaken.37
The work up for surgery is time consuming and can be
emotionally draining. In the recent past, there have been significant delays at
each step of the process, and a wait of 2 years from referral to surgery is
clearly too long. It is possible that this delay has deterred some referrers and
patients. Fortunately, the process is now more streamlined and many recent
patients have had surgery within a year of referral. Some of the delay is
sometimes a result of patients themselves wanting time to consider the pros and
cons. Patients are informed that a minority of patients are left worse off
following temporal lobe resection, and surgery is not to be undertaken lightly.
We give patients as much time as they wish to make a
decision, and we regularly put patients in touch with others who have previously
gone through the process, so that they can get another patient’s
perspective. Delay sometimes also occurs for other reasons; some patients have
needed treatment for depression or other psychiatric issues before they have
been considered suitable for temporal lobectomy.
We believe that surgery is being under utilised in New
Zealand, as we continue to meet patients who ask us why they weren’t
offered surgery earlier. New Zealand is not unusual in this regard; experts in
many countries have reported that temporal lobectomies should be performed more
frequently.21,36,38,39 Follow up of large
groups of patients suggest that patients who are going to be resistant to drug
treatment can often be identified relatively
early;40 one report found that only 1% of
patients who had failed to respond to two different antiepileptic drugs in
adequate dosage gained control of their seizures with a third
drug.41
Another study found that if a child with temporal lobe
epilepsy failed to respond to the first antiepileptic drug, there was a 90%
chance that the epilepsy would be uncontrolled at 2
years.42 Reviews have not found any evidence
that age at seizure onset or time of surgery play a significant role in
determining the likelihood of a successful
outcome.39 It is sometimes appropriate to
operate on children when it is clear that their epilepsy is resistant to drug
treatment, and MR scanning shows mesial temporal sclerosis or another structural
lesion in the brain. Paediatric neurologists and neurosurgeons with a special
interest in epilepsy are now working in Auckland, alongside the adult
neurologists and surgeons, and we are now undertaking increasing numbers of
operations for epilepsy in children.
We would contend, therefore, that patients who have temporal
lobe epilepsy and who have used two antiepileptic drugs in appropriate doses,
yet who still have uncontrolled seizures 2 years after diagnosis, should be
referred for consideration of possible surgery, whether adults or
children.39 Not all patients will want surgery,
but we believe that the options should be presented to them.
Competing interests: None known.
Author information: Ravi Suppiah, Neurology
Registrar, Department of Neurology, Auckland City Hospital, Auckland; Edward
Mee, Neurosurgeon, Surgical Director of the Epilepsy Surgery Programme,
Department of Neurosurgery, Auckland City Hospital, Auckland; Elizabeth Walker,
Neurologist and Neurophysiologist, Department of Neurology, Auckland City
Hospital, Auckland; Lynair Roberts, Epilepsy Nurse, Department of Neurology,
Auckland City Hospital, Auckland; Gregory Finucane, Neuropsychiatrist,
Department of Psychiatry, Auckland City Hospital, Auckland; Peter Bergin,
Neurologist and Neurophysiologist, Medical Director of the Epilepsy Surgery
Programme, Department of Neurology, Auckland City Hospital, Auckland
Correspondence: Dr Peter Bergin, Neurology
Department, Auckland City Hospital, Park Rd, Grafton, Auckland, New Zealand.
Fax: +64 (0)9 3078912; email: pbergin@adhb.govt.nz
References:
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