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Seizure: European Journal of Epilepsy: Review
Seizure: European Journal of Epilepsy: Review
Review
Keywords: Purpose: The purpose of our study is to compare seizure-free outcome and the incidence of visual field deficits
Temporal lobe epilepsy (VFD) between anterior temporal lobectomy (ATL) and selective amygdalohippocampectomy (SAH) among
Different surgical methods patients with intractable temporal lobe epilepsy (TLE).
Seizure freedom Methods: We searched MEDLINE, Embase and Cochrane databases using keywords related to ATL, SAH and VFD.
Postoperative complications
Previous studies that compared ATL and SAH with seizure-free outcome and the incidence of VFD were included.
Individualized treatment
A fixed-effect model was used to conduct meta-analysis. Risk ratio with 95% confidence intervals were pooled
and used to elucidate each outcome.
Results: Twenty-three retrospective and three prospective studies were recruited with a total of 2930 cases (1390
cases for SAH and 1540 cases for ATL). The meta-analysis showed no significant difference in seizure freedom
(SAH 63.5% vs ATL 63.8%) of these two procedures (RR 0.95, 95%CI 0.90-1.01, P = 0.102), but the odds of
seizure freedom in ATL was higher than transsylvian SAH approach (RR 0.89 95% CI 0.82-0.96, P = 0.004).
Comparing with ATL for TLE, SAH for TLE caused lower frequency of postoperative VFD. (RR 0.87, 95%CI 0.76-
0.99, P = 0.034).
Conclusions: There was no significant difference on seizure freedom between ATL and SAH procedures, while
subgroup analysis demonstrated that ATL was associated with higher opportunity to achieve seizure-free than
transsylvian SAH approach. Furthermore, the incidence of postoperative VFD was significantly lower in SAH
than ATL. Individualized treatment achieving balance between seizure free and collateral damage should be
considered in clinical practice. Well-designed randomized controlled clinical trials would be necessary to vali-
date our findings.
⁎
Corresponding author at: Department of Neurosurgery, Sanbo Brain Hospital, Capital Medical University, 50 Yikesong Road, Haidian District, Beijing, China.
E-mail address: sbnklgm@163.com (G. Luan).
https://doi.org/10.1016/j.seizure.2020.07.024
Received 31 May 2020; Received in revised form 21 July 2020; Accepted 23 July 2020
1059-1311/ © 2020 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
K. Xu, et al. Seizure: European Journal of Epilepsy 81 (2020) 228–235
different conclusions of these analyses was that the number of included and were included in our meta-analysis.
studies was varied. Moreover, no significant differences between these
two procedures were observed in a previous meta-analysis regarding 2.6. Data analysis
VFD differences. Therefore, we performed this systematic review and
meta-analysis, and included as many relevant studies as possible to Stata/SE V15.1 for Windows (Stata, College Station, TX, USA) was
evaluate the difference between SAH and ATL in both seizure freedom used for meta-analysis. Two meta-analyses were conducted to sepa-
and VFD. rately compare seizure freedom and the incidence of VFD after the
surgery for SAH versus ATL. Risk ratio with 95% confidence intervals
2. Methods were pooled and used to express each outcome, and P value < 0.05 was
considered statistically significant. Q statistic and I2 were used to test
2.1. Search strategy for between-study heterogeneity. If statistically significant hetero-
geneity was present (Q statistic P < 0.05 or I2 ≥ 50%) between stu-
A literature research of PubMed, EMBASE, and Cochrane dies, the random-effect model was applied; otherwise fixed-effect model
Collaboration Database was conducted to identify relevant studies. The was applied. Prespecified sensitivity analyses were performed to eval-
following search terms were used for this research: i) Temporal lobe uate the stability of the results as following: using the random-effects
epilepsy, ii) Selective amygdalohippocampectomy, iii) Anterior tem- model, excluding each article in turn, and analysing studies that solely
poral lobectomy, and iv) Visual field deficits. Results were restricted to focused on adults. Publication bias was examined with the application
English-language articles published up to 2019. We also reviewed the of Begg's correlation and Egger's regression (Begg & Mazumdar, 1994;
references of included articles to identify potential studies. Egger, Davey, Schneider, & Minder, 1997).
In subgroup analyses, the seizure-free outcome of ATL was com-
2.2. Inclusion and exclusion criteria pared with that of transsylvian and transcortical SAH. Furthermore, we
compared the seizure-free outcome of SAH and ATL for studies which
The following inclusion criteria were applied in this meta-analysis: exclusively focused on hippocampal sclerosis and studies reporting on
seizure-free outcome at 1-year, 2-year, and 5-year follow-ups.
(1) For seizure outcomes: (a) Observational studies aiming at temporal
lobe epilepsy; (b) original clinical research articles comparing sei- 3. Results
zure outcomes after SAH or ATL procedures; and (c) studies with at
least a 12 months follow-up period. A total of 535 articles were identified according to our searching
(2) For VFDs: (a) Visual field examined by kinetic Goldmann perimetry strategy. After screening duplicates, we identified 317 eligible studies.
or Humphrey static perimetry; (b) articles comparing number of Forty-four studies remained after reviewing the title and abstract
VFD patients after SAH or ATL procedure; and (c) patients tested (Fig. 1). Six studies were excluded for the following reasons: non-blind
more than 30 days after surgery to avoid temporary VFD caused by randomized trial [18], number of patients less than 20 [19,20], follow-
transient brain oedema. up for less than 1 year [21,22], and overlapping patient population
[23]. Twenty-six articles which included 2930 cases (1390 cases under
Studies were excluded under following criteria: (a) If the number of SAH and 1540 cases under ATL) met the inclusion criteria for meta-
patients was less than 20; (b) non-human studies, reviews and meta- analysis.
analyses, case reports and letters, and conference abstracts; and (c)
studies providing insufficient information. We also excluded multiple 3.1. Study characteristics
articles with overlapping patient populations from the same centre.
The characteristics of included studies are presented in Table 1.
2.3. Data extraction These studies were from Canada (6), Germany (6), USA (4), UK (3),
Australia (2), Japan (1), China (1), Brazil (1), and France (2). Of these
Two investigators independently extracted the first author’s name, 26 observational studies, three were prospective studies [24–26], and
year of publication, country of origin, institution of investigation, study the remaining ones were retrospective study designs. Among these 26
design, sample size, types of surgery, presurgical evaluation, age of articles, 22 compared seizure outcomes between SAH and ATL [3,5,7,
patients at the time of surgery, gender ratio, duration of epilepsy, [24–42], 4 compared the incidence of VFD between SAH and ATL
duration of follow-up, Engel classification of seizure outcome, pa- [11,43–45], and the other 2 included both the comparisons [27,32].
thology, and the number of VFD patients after surgery. Any discrepancy The average follow-up period of seizure outcomes was 12 to 104.4
was resolved through discussion. We contacted the corresponding au- months, and the testing time of visual field ranged from 1 to 9 months.
thor for further details when the relevant data were missing. In these studies, SAH was performed through transcortical (trans-su-
perior temporal gyrus [2 studies] [30,43], trans-middle temporal gyrus
2.4. Outcome evaluation [11 studies]7,12,26,28,31,33–36],42,45]), subtemporal (2 studies
[11,29]), transsylvian (13 studies [3,5,[11,[24,25,[27,29,
The Engel classification system [16] was used for seizure outcome [30,32,38,39,42,43]), and unmentioned (2 studies [40,41]) ap-
assessment, and Engel class I was considered when the patient was proaches. The type of procedure to be performed (ATL or SAH) was
seizure-free after the surgery. Seizure outcome at 5 years after the determined on the basis of the surgery timing, experience and tech-
surgery was used for meta-analysis if the seizure outcome was recorded nique of the surgeon, and results of presurgical evaluation. The char-
at multiple prespecified time points. The final numbers of the SAH and acteristics of the patients in studies included in the meta-analysis are
ATL patients incorporated into the research did not contain the patients presented in Table 2. There were 6 studies5,7,26,32,35,42]covering the
lost to follow-up. pathology of hippocampal sclerosis (HS) exclusively; the rest of the
studies included HS and other pathologies, such as tumour, dysplasia,
2.5. Quality assessment and gliosis.
Most of the included articles achieved 6 or more points on the
The methodological quality of these non-randomized studies was modified NOS; five retrospective articles [3,11,38,40,45] achieved 5
evaluated by the modified Newcastle-Ottawa Scale (NOS) [17]. Studies points because of low scores in the comparability category, and two of
that achieved 6 or more points were considered to be of high quality them11,45] were included in VFD meta-analysis. All of the studies
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K. Xu, et al. Seizure: European Journal of Epilepsy 81 (2020) 228–235
Fig. 1. PRISMA flow chart of study selection and reasons for exclusion. PRISMA: preferred Reporting Items for systematic Reviews and Meta-analyses.
showed complete follow-up time for seizure outcome and provided no significant heterogeneity between these studies was observed (Q
sufficient reasons for the patients lost to follow-up. statistic P = 0.321 and I2 = 12.7%). The subgroup analysis which
compared transsylvian SAH and transcortical SAH was not performed
3.2. Seizure freedom because there were only three studies29,30,42] comparing these two
approaches concurrently.
Twenty-two studies [3,5,7,24–42] comparing 2621 patients (1236 Six studies [5,7,26,32,35,42] which exclusively focused on hippo-
cases under SAH and 1385 cases under ATL) were included in the meta- campal sclerosis compared seizure freedom of SAH and ATL. The
analysis for seizure freedom. There was no significant difference be- probability of achieving seizure freedom revealed no difference in these
tween seizure freedom (SAH 63.5% vs ATL 63.8%) of the two proce- two procedures (RR 1.13, 95%CI 0.92-1.17, P = 0.528). There was no
dures (RR 0.95, 95%CI 0.90-1.01, P = 0.102) (Fig. 2). The random- heterogeneity between studies in this subgroup meta-analysis (Q sta-
effect model was used for meta-analysis because moderate hetero- tistic P = 0.446 and I2 =0.0%). Significant difference between these
geneity existed between the included studies (Q statistic P = 0.025 and two procedures was not observed with respect to seizure freedom at the
I2 = 40.7%). 1-year, 2-year, and 5-year follow-up.
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K. Xu, et al. Seizure: European Journal of Epilepsy 81 (2020) 228–235
Table 1
Characteristics of studies included in the meta-analysis.
No. Ref. Country Design No. (SAH/ATL) Approach of SAH Follow-up (mos) Analysis NOS scale
Abbreviations: retroretrospective; proprospective; TCtranscortical; TStranssylvian; 1sizure free outcomes; 2visual field deficits; 3neurophysiology; STGsuperior
temporal gyrus; MTGmiddle temporal gyrus; STsubtemporal; NAnot available; NOSNewcastle-Ottawa Scale.
3.5. Sensitivity analysis and publication bias analysis, and the result of seizure outcomes was not different with the
exclusion of low-quality studies (RR 0.96, 95%CI 0.90-1.02, P =
In the sensitivity analysis for seizure-free outcome, the result re- 0.220).
mained stable after we excluded each article in turn. Nineteen studies No significant publication bias was found in the meta-analysis ac-
achieving 6 or more points on the NOS were included to perform meta- cording to the reflection of P values from Begg’s correlation (SAH vs
Table 2
Characteristics of patients in studies included in the meta-analysis.
No. Ref. Gender male% Surgery side (left%) Age at surgery (yr, Mean) Duration of seizure (yr, Mean) Pathology
Abbreviations: DP: dual pathology; GWMA: gray-white matter abnormalities; HS: hippocampal sclerosis; MTS: mesial temporal sclerosis; NA: not available.
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Fig. 2. Forest plot and meta-analysis comparing selective amygdalohippocampectomy (SAH) and anterior temporal lobectomy (ATL) for seizure-free outcome. M-H,
Mantel-Haenszel.
ATL: P = 0.176; transsylvian SAH vs ATL: P = 0.876; transcortical SAH Within the subgroup analysis, it was observed that the seizure-free
vs ATL: P = 0.150) and Egger’s regression (SAH vs. ATL: P = 0.057; outcome of ATL was higher than that of the transsylvian SAH approach,
transsylvian SAH vs ATL: P = 0.413; transcortical SAH vs ATL: P = while no difference was found for the transcortical SAH approach. In
0.101). The shapes of the funnel plots did not show any strong evidence many cases, the actual epileptogenic zone may not merely be defined as
of asymmetry. the lesions identified on MRI. Besides, focal cortical dysplasia (FCD) is
the most common lesion accompanying hippocampal sclerosis, and
4. Discussion many FCD lesions cannot be detected clearly in MRI. In addition, some
seizures that originated in the temporal pole and quickly spread to the
After precise analysis of sufficient data, this systematic review has hippocampus can also mislead our diagnosis. Thus, all the situations
drawn the reliable conclusion that no significant difference exists be- mentioned above may cause poor seizure-free outcome after the
tween SAH and ATL procedures considering the odds of seizure transsylvian SAH approach.
freedom, while the subgroup analysis demonstrated that ATL has higher The reported rate of VFD following anterior temporal resection
odds of seizure freedom than the transsylvian SAH approach. Moreover, varies widely from 0% to 100%, predominantly occurring in the su-
the results remained stable after sensitivity analysis with exclusion of perior quadrantanopia. Studies recruited in this analysis describe con-
each study. In addition, SAH has lower risk of VFD than ATL, which is troversial views on the results while comparing the VFD rate of SAH
concordant with the results of several previous articles [10–12]. and ATL. Schmeiser et al. [11] found fewer VFD in subtemporal SAH,
Previous meta-analyses drew discordant conclusions after com- whereas, Mengesha et al. [44] reported that the incidence of VFD after
paring seizure-free outcome in ATL and SAH. The reasons for these SAH was lower than that after ATL. On the other hand, Egan et al. [45],
inconsistent conclusions can be summarized as following: different in- Mathon et al. [43], and Wang et al. [27] found no difference in the
clusion criteria (especially, how strict were the exclusion criteria ap- incidence of VFD between SAH and ATL. This meta-analysis shows that
plied for temporal-plus epilepsy), and the different time points selected SAH has a lower risk of VFD. ATL may cause contralateral superior
for analysis. A randomized comparative trial [18] also found no dif- homonymous quadrantanopia by disruption of the Meyer’s loop and
ference between SAH and ATL procedures on seizure-free outcome. The anterior bundle of the optic radiations that traverse through the tem-
studies by Hu et al. [9] and Josephson et al. [15] found that ATL can poral lobe. Subtemporal SAH was reported with a lower incidence of
achieve better seizure freedom than SAH, which seems to be logically VFD than other approaches since it involves approaching the temporal
accepted because of broader resection in ATL. Kuang et al. [13] did not horn through its floor [46]. Another rare randomized study also de-
find significant difference regarding seizure control between the two monstrated that subtemporal SAH shows significantly fewer VFDs than
approaches. More than 10 recently published studies were transsylvian SAH. Additionally, the occurrence of VFD in the sub-
[24,27–31,33,34,39,40], included in our meta-analysis compared to temporal group was associated with closer distance of the optic radia-
theirs. Three of the studies 24,29,30 with large sample size could influ- tion to the temporal base [47]. However, comparison between sub-
ence the weight distribution of the result. The study by Jain et al. did temporal SAH and other approaches was not performed in our meta-
not identify any difference in seizure-free outcome of ATL versus that of analysis because of the limited number of recruited articles [11,29].
SAH [14], which is concordant with our finding. However, comparison Preoperative visualization of the optic radiation and sparing tissue
between different approaches of ATL and SAH was not performed in posterosuperior to the temporal horn [48] are recommended to help in
their study. reducing the opportunity of optic radiation injury.
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K. Xu, et al. Seizure: European Journal of Epilepsy 81 (2020) 228–235
Fig. 3. Forest plot and meta-analysis comparing seizure-free outcome of transsylvian or transcortical SAH and ATL. M-H, Mantel-Haenszel.
Our meta-analysis can help in better evaluation of operative risks in with the following factors: demographics, criteria for selection, ex-
clinical practice, thereby, providing individualized treatment. While perience and technique of the surgeon, aetiology, use of antiepileptic
selecting the type of surgical approach, a balance between seizure drugs after surgery, methodology, and follow-up duration. To provide
freedom and collateral damage should be considered. Patients with better evidence regarding the efficacy and complications of ATL and
severe epileptic symptomatology and long epilepsy duration could have SAH, RCTs comprehensively comparing the differences of SAH and ATL
a higher demand for postoperative seizure control, while in individuals, procedures are definitely necessary.
such as drivers, whose primary concern is visual field function, pre-
operative evaluation and intraoperative protection of relevant tissues
5. Conclusion
are particularly essential.
Several limitations reduce the scientific value of this meta-analysis;
Discordant results from previous studies may create confusion for
these need to be explored further. All the recruited studies were ob-
clinical physicians. According to this meta-analysis, no significant dif-
servational studies, which implies that the current absence of RCTs may
ference exists between SAH and ATL procedures considering the
have increased the influence of confounders on the research outcome,
probability of seizure freedom, while the subgroup analysis demon-
and the risk of selection bias. In this study, the neuropsychological
strated that ATL is associated with higher odds of seizure-free outcome
outcomes between SAH and ATL were compared. However, the mean
than transsylvian SAH. On the other hand, the probability of VFD is
changes in full-scale IQ, verbal IQ, and performance IQ scores before
significantly lower in SAH than ATL. Well-designed RCTs are needed to
and after surgery were not mentioned in the recruited articles.
validate our findings. In different disorders, like malignant tumours,
Moreover, the method of neuropsychological testing is not unified,
with definite surgical indication, treatment of epilepsy should be highly
making it impossible to be analysed in this meta-analysis.
individualized based on a balance between the disease characteristics
Heterogeneity and inconsistency in the meta-analysis was associated
and patient’s demands.
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K. Xu, et al. Seizure: European Journal of Epilepsy 81 (2020) 228–235
Fig. 4. Forest plot and meta-analysis comparing VFD of SAH and ATL. M-H, Mantel-Haenszel.
Disclosure References
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