Sturge-weber syndrome (SWS) belongs to the spectrum of neurocutaneous disorders. In 1879, W. Allen Sturge was the first to describe a patient with a port-wine birthmark (PWB) and ipsilateral changes in the cerebral cortex.1 Since then, a somatic activating mutation in the GNAQ gene, causing disturbance in the development of vessels, has been shown to be the cause of SWS.2 Clinically, SWS presents with a PWB, ipsilateral leptomeningeal venous angioma (LVA), and glaucoma.3 Glaucoma is inconsistently described, occurring in up to 60% of the patients.4–6 Therefore, ophthalmological review is recommended in any patient with suggested SWS.7,8 Other hallmarks of SWS are cortical calcifications and cerebral atrophy, and more than 80% of all patients are affected by epilepsy.3,6,9,10 SWS is classified in three different stages according to the Roach scale. Type I is characterized by a facial nevus and LVA, type II by a facial nevus alone, and type III by a LVA alone.11 Stroke-like episodes due to assumed recurrent intracranial microthrombosis resulting in venous stasis have been described in SWS patients; therefore, prophylactic treatment with aspirin is controversially discussed.12
Because of the rarity of SWS, it is extremely difficult to predict the severity of the disease. However, the extent of cerebral involvement, early-onset seizure, and a high seizure frequency have been associated with a worse cognitive outcome.3,13–15 Hence, seizure control is of paramount importance in SWS. Currently, there is no causal therapy for SWS. Antiepileptic drugs (AEDs) are considered as first-line therapy. In cases of drug-resistant epilepsy, surgical treatment can be offered.5,6,16–23 Traditionally, hemispherectomy has been the surgery of choice for SWS; however, focal lesionectomy of the affected cortex is advocated as well.10
The aim of this case-based systematic review and meta-analysis was to provide an overview of the literature regarding focal lesionectomy as a surgical treatment option in SWS, with a focus on seizure outcome, motor and cognitive development, and morbidity.
Methods
Focal Lesionectomy for Drug-Resistant Epilepsy
We systematically searched the PubMed and Embase databases with a search string including the keywords“Sturge-Weber syndrome” and “surgery” and included studies from the inception of the databases until the beginning of December 2021 (Fig. 1). In addition to a case from our institution, reported within this paper, we included case reports, case series, retrospective and prospective cohort studies, and randomized controlled trials. Case reports were included due to the fact that studies on focal lesionectomy are sparse and these case reports as a whole could have statistical impact on the analyzed outcomes. Studies in the English language reporting on the outcome of seizure surgery (lesionectomy or comparison of lesionectomy with hemispherectomy) in pediatric and adult patients affected by SWS were included. Articles describing only hemispherectomy as the surgical treatment were excluded. Lesionectomy was defined as a focal resection of the affected cortex or a single lobectomy. For the systematic review, all studies describing the outcome of lesionectomy (including our presented case) were included. For the quantitative analysis, only studies comparing the outcomes of lesionectomy with those of hemispherectomy were included. Duplicates were removed and the studies assessed independently with the support of the web-based program Rayyan.24 Initially, all studies were analyzed according to their titles by two authors (N.A.F. and L.G.) independently. Thereafter, abstracts were reviewed, and a list of studies was generated, which underwent a full-text evaluation, whereafter a final list of studies to be included was generated. In case of a disagreement concerning a study’s inclusion or exclusion, the senior author (J.S.) made the final decision. Data from the included studies were extracted independently by two researchers (N.A.F. and L.G.) and compared with a final data set compiled for analysis. The primary outcome was the rate of seizure control, while secondary outcomes were postoperative complications, hemiparesis, and cognitive deficits. Complete seizure control was defined as Engel class I, while unfavorable seizure control was defined as Engel classes II–IV.25 Studies published before the inception of the Engel classification reported seizure outcome as complete or incomplete seizure control and were converted to the two groups of favorable or unfavorable seizure control accordingly. The total number of patients of each study and subgroup distribution was documented as well. Missing data sets for analysis, addressing the outcome, are denoted by “NA” in Table 1. Unequal units, such as year or month, were adapted.
Flowchart according to PRISMA guidelines for systematic review and meta-analysis. Data added to the PRISMA template [from Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 6(7):e1000097] under the terms of the Creative Commons Attribution License.
Baseline characteristics of the included studies
| Authors & Year | Study Type | No. of Pts | Focal Lesion* | Hemisphere* | Age at Epilepsy Onset, yrs† | Age at Op, yrs† | Postop FU, yrs‡ | Sz Outcome (no. undergoing focal lesion)* | NOS | |
|---|---|---|---|---|---|---|---|---|---|---|
| Favorable | Unfavorable | |||||||||
| Wang et al., 20214 | Retrospective | 90 | 44 | 46 | 1.11 ± 2.38 | 4.41 ± 5.6 | 2 (2) | 75 (35) | 15 (9) | 8 |
| Maton et al., 20105 | Retrospective | 8 | 4 | 4 | 0.92 ± 1.4 | 10.3 ± 6.5 | 4 (1–10)§ | 3 (1)¶ | 4 (2)¶ | 7 |
| Bourgeois et al., 20076 | Retrospective | 27 | 19 | 8 | 2.6 ± 3.5 | 6.1 ± 5.1 | 8.3 (0.75–17.3) | 20 (12) | 7 (7) | 8 |
| Arzimanoglou et al., 200016 | Retrospective | 19 | 14 | 5 | 4.37 ± 3.86 | 11.47 ± 9.64 | 9 (2–18.5)§ | 14 (8) | 5 (5) | 8 |
| Rosén et al., 198427 | Case report | 1 | 1 | NA | 0.58 | 1.41 | NA | 1 | 0 | NA |
| Bye et al., 198930 | Case report | 1 | 1 | NA | 4.5 | 13 | NA | 0 | 1 | NA |
| Hata et al., 199820 | Case report | 1 | 1 | NA | 0.25 | 1.6 | NA | 1 | 0 | NA |
| Shekhtman et al., 201319 | Case report | 1 | 1 | NA | 2 | 8 | NA | 1 | 0 | NA |
| Jiruska et al., 201129 | Case report | 1 | 1 | NA | 0.6 | 1.5 | NA | 1 | 0 | NA |
| Our case | Case report | 1 | 1 | NA | 0.6 | 2 | NA | 1 | 0 | NA |
FU = follow-up; Hemisphere = hemispherectomy; Lesion = lesionectomy; NA = not available; Pt = patient; Sz = seizure.
Values are given as number of patients.
Values are given as mean ± SD.
Values are given as median (range).
One patient was lost to follow-up.
Outcome information was not provided for 1 patient.
Qualitative Assessment
Quality assessment of the retrospective cohort studies was carried out using the Newcastle-Ottawa Scale (NOS) and was initially conducted by two authors (N.A.F. and L.G.) independently and then compared.
Statistical Analysis
Risk ratio (RR) was used as an effect measure for the pooled outcomes. Depending on the heterogeneity (I2 < 50%) of the studies, either the fixed-effects or random-effects model was applied. Forest plots were generated for all outcomes. All analyses were done using R statistical software (version 4.0.3, R Foundation for Statistical Computing) with the help of the dmetar package.26 A p value < 0.05 was considered as statistically significant. No sensitivity analysis (“leave-one-out method”) was performed due to the limited number of included studies.
This systematic review was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Fig. 1).
Case Description
A 1-year-old boy with a 4-month history of focal seizures was referred to University Children’s Hospital of Basel. His seizures presented as a left-sided clonus of the face and then propagated to the left extremities and subsequently resulted in Todd’s paresis of the left arm and leg. Clinical examination revealed slightly reduced cognitive development and slightly impaired fine motor movements of the left hand and fingers, indicating asymmetrical strength and tone. No PWB was present. MRI showed typical “tram-track signs” (Fig. 2). Combined PET-CT and MRI showed decreased metabolism in this area. He was diagnosed with SWS type III, with angiomatosis in the right parieto-occipital region of the brain.
T1-weighted MR images with gadolinium showing the characteristic enhancement of pathologic vessels as a leptomeningeal angiomatosis (tram tracks) in the parietooccipital lobe on the right side in the coronal (A), sagittal (B), and axial (C) views. Furthermore, a noticeable asymmetry between both hemispheres is visible as a typical sign of SWS (A and C).
AED therapy with levetiracetam was initiated, and valproic acid and oxcarbazepinum were added. Despite triple-AED treatment, the patient did not remain seizure free and showed persistent reduced cognitive development and mild motoric dysfunction in the left hand and fingers. Therefore, a phase I epileptic evaluation for epilepsy surgery was undertaken, identifying the affected right occipital lobe as the most probable epileptogenic origin of the seizures. After a multidisciplinary case discussion, as well as a discussion of the risk and benefits with the child’s parents, who gave informed consent, the patient, at the age of 2 years, underwent surgery. We conducted a right-sided fronto-parieto-occipital craniotomy and cortical resection of the cerebral angiomatosis with the help of neuronavigation (Brainlab AG) and intraoperative neurophysiological and EEG monitoring (inomed Medizintechnik GmbH).
Phase reversal using a strip electrode to define the precentral and postcentral area as well as the central sulcus was difficult and had no clear results, probably due to cortical alteration caused by the LVA. The precentral and postcentral gyri (Fig. 3), more specifically the hand and face area, were successfully identified by direct cortical stimulation. We started with preparation of the postcentral sulcus to its bottom and removed the angiomatosis completely in a subcortical level with respect to the postcentral gyrus from bottom up. Cortical stimulation remained stable with insignificant reduction of motor evoked potentials after resection. The postcentral gyrus (sensory strip), showing LVA, was not resected, to avoid further neurological deterioration (Fig. 4). On the 1st postoperative day, the boy experienced a single, self-limiting seizure, and he was discharged from the hospital to neurological rehabilitation 5 days after surgery in good health, without any new neurological deficits and improving fine motor skills of the left hand, and with antiepileptic triple therapy maintained. No complication occurred during follow-up. A postoperative assessment showed that the patient’s psychomotor development was adequate for his age, while a preference of his right hand persisted. MRI of the brain 5 months after surgery showed an expected enhancement in the postcentral gyrus. Clinically and on follow-up, no increased epileptic activity was seen; therefore, antiepileptic medication was stepwise reduced. Two years after surgery, the boy showed normal development in his psychomotor milestones, with very slight restricted mobility of his left hand. He is treated with two AEDs and has remained seizure free (Engel class I).
Left: Presurgical MR image with visible affected central region with angiomatosis in the central and postcentral sulci. Right: Intraoperative photograph of the cortical angiomatosis obtained prior to resection with a strip electrode placed on the pre- and postcentral gyri (white arrows) for neurophysiological monitoring during surgery.
Intraoperative photograph showing the partial cortical resection of the angiomatosis. The postcentral gyrus is left intact to avoid neurological deficits.
Results
After removal of duplicates, we screened 439 studies, of which 9 articles were included in the qualitative analysis and 4 studies in the quantitative meta-analysis (Fig. 1, Table 1). Four of these were retrospective cohort studies and 6 (including the case in this paper) were case reports, while no prospective trial was identified.4–6,16,19,20,27–30 In total, we included 150 patients, 87 (58%) of whom underwent focal lesionectomy. For qualitative analysis, we compared 81 (54%) patients who underwent a lesionectomy to 63 (42%) patients who were treated by hemispherectomy.4–6,16,19,20,27,29,30
Clinical Presentation and Diagnosis
In the included studies, more than half of the patients presented with a PWB.4–6,16 Bilateral cerebral manifestation is rare and has only been described in 1 case of all the included studies.4 Seizure onset occurred prior to a mean age of 5 years in all studies.4–6,16,19,20,27,29,30 The most common (56/60 patients, 93%) seizure semiology was partial seizure,5,6,16,20,27,29,30 with a secondary transformation to generalized tonic-clonic seizure in 53%.6,16 Wang et al., in their cohort, did not give detailed information on the distribution of the seizure type, but documented a majority with partial seizure at onset.4 Atonic seizures are rarely described in SWS, and only 3 (2%) patients in all the included studies presented with this semiology.16,19 The interval from seizure onset to surgery ranged from 1.5 to 33 years.16 All patients underwent presurgical EEG studies.4–6,16,19,20,27,29,30 Intraoperative electrocorticography was only conducted in 4 studies and in our case.16,20,27,30 Follow-up time was available in 4 (100%) of the included studies, with a median follow-up of 6.15 years (range 0.75–18.5 years);4–6,16 2 (1.4%) patients were lost to follow-up5,16 (Table 1).
Seizure Control
Of 87 patients, 22 (25%) had a complete lesionectomy,5,6,16,19,20,27,29,30 while 21 (24%) underwent a partial lesionectomy due to proximity to eloquent cortex.5,6,16 There was no detailed information about the distribution of complete and partial resection in the cohort of Wang et al. (44 patients) for focal lesionectomy.4 Postoperative seizure control was determined using the Engel scale in all included studies4–6,19,29 except in those by Arzimanoglou et al.,16 Bye et al.,30 Hata et al.,20 and Rosén et al.,27 since the Engel scale was only published in 2001 and was therefore not available at the time of their publication.25 In 25 of 42 (59%) of the cases with a complete resection, a favorable outcome (Engel class I) was described.5,6,16,19,20,27,29,30 While in the case report of Bye et al.30 an improvement after complete resection was described, 1 (11%) patient in the series by Bourgeois et al.6 showed a worsening in seizure activity after complete lesionectomy, while 6 (66%) improved and 2 (22%) remained stable. Most incomplete lesionectomies (8/21, 38%) showed an improvement in seizure control;5,6,16 our described patient showed a significant improvement after incomplete lesionectomy, since he became seizure free.
The overall pooled outcome analysis for postoperative favorable Engel class (class I) showed a nonsignificant lower rate for lesionectomy compared with hemispherectomy (69.2% vs 87.3%; RR 0.73, 95% CI 0.50–1.08; t = −2.56, p = 0.08) (Fig. 5A).
Forest plots of favorable seizure outcome (A), postoperative hemiparesis (B), and postoperative developmental delay (C). HS = hemispherectomy; FL = focal lesionectomy.
Complications
Six studies reported postoperative complications for lesionectomies.4,6,16,27,29,30 These included hemianopia (3%, n = 5), cerebral hemorrhage (0.7%, n = 1), hemiparesis (0.7%, n = 1), and infection (1.3%, n = 2: 1 superficial, 1 deep intracranial). No significant difference in the pooled outcome analysis regarding complications was observed between lesionectomy and hemispherectomy (10.3% vs 5.8%; RR 1.4, 95% CI 0.29–6.35; z = 0.41, p = 0.68). However, all patients undergoing a hemispherectomy developed a postoperative hemiparesis compared with 18.1% after lesionectomies. This resulted in a significantly lower pooled rate of postoperative hemiparesis after lesionectomy (18.1% vs 100%; RR 0.11, 95% CI 0.06–0.21; z = −6.58, p < 0.0001) (Fig. 5B). Moreover, after lesionectomy a significantly lower rate of postoperative developmental delay compared with hemispherectomy was seen (29.8% vs 76.3%; RR 0.41, 95% CI 0.28–0.59; z = −4.77, p < 0.0001) (Fig. 5C).
Qualitative Assessment
The qualitative assessment for the 4 retrospective cohort studies showed a mean NOS rating of 7.5 ± 0.5 (Table 1).
Discussion
To our knowledge, this is the first systematic review and meta-analysis regarding focal lesionectomy for SWS patients. This analysis showed that patients undergoing lesionectomy compared with hemispherectomy had a nonsignificant lower rate of favorable seizure outcome. However, lesionectomy had a significantly lower rate of postoperative hemiparesis and cognitive decline compared with hemispherectomy, while the overall postoperative complication rate was comparable in both groups.
Clinical Presentation and Diagnosis
The clinical presentation of SWS can vary among patients. Most patients are diagnosed at birth due to a PWB, which is present in more than 90% of all patients.19,31 If PWB is not apparent, diagnosis is made by intracranial imaging after seizures commence. The imaging method of choice is MRI, including T1 postcontrast, T2, and fluid-attenuated inversion recovery (FLAIR) sequences.4,8,32 The calcifications result in the classic tram-track sign in a postcontrast T1 scan or CT scan.8 Moreover, perfusion MRI studies show abnormal white matter hypoperfusion in the affected areas and a PET scan confirms an abnormally low glucose metabolism in the affected areas that are in correlation with EEG origins for seizure.33 Apart from 13 patients in the study by Arzimanoglou et al. who only underwent CT, all patients included in this analysis were investigated with MRI preoperatively.4–6,16,19,20,27–30
Although most patients present neurologically with seizures, at times, other neurological deficits might be present. In the study by Arzimanoglou et al.,16 6 of 20 (30%) patients undergoing hemispherectomy experienced preoperative hemiparesis with different degrees of severity that persisted postoperatively, while only 1 (5%) patient had a hemiparesis after focal lesionectomy. In the study by Wang et al., nearly all patients undergoing hemispherectomy had a previous motor deficit compared with only a few before undergoing focal lesionectomy.4 The cause of hemiparesis in SWS might be due to the anatomical attribute of LVA, while it has been hypothesized that stroke-like episodes due to microthrombosis might be an additional cause of hemiparesis in SWS.33
Seizure Control and Management
There is no causal therapy for SWS, and therefore the focus remains on seizure control, since the extent and onset (especially under the age of 1 year) of seizures have a significantly negative impact on the neurological outcome.15 In 75% of the patients, epilepsy manifests itself within the 1st year of life and more than 85% of all patients are affected by epilepsy by the age of 2 years.3,4,10,34 Especially in infants, it can be challenging to detect seizure because in SWS seizures are mostly focal and not generalized.5,6 First-line seizure treatment remains AED therapy. However, especially in SWS, approximately 20%–25% of all patients develop drug-resistant epilepsy.31,34 In cases of drug-resistant epilepsy, surgery should be considered, and early surgery should be pursued in order to reduce seizure-induced neuronal damage leading to cognitive decline and increase the chances of good postoperative neurological outcome.16,29,35–37 The decision for surgery is mostly based on the discussion and recommendation of a multidisciplinary team including pediatricians, pediatric neurosurgeons, pediatric neuroradiologists, and pediatric neurologists.4 EEG findings usually correlate with the MRI findings, although, at times, radiologically noninvolved areas might show pathological changes on EEG as well.38 Moreover, most authors recommend obtaining a preoperative neuropsychological evaluation for their patients4–6,16,19,27,29,30 because in most patients with SWS an impairment in development, attention span, or motor deficits was observed.4–6,16,19,20,27,29 The main aim of any epilepsy surgery is to remove the epileptogenic focus, namely the LVA in SWS.4 The two main surgical approaches in SWS are lesionectomy and hemispherectomy.4,36,37
To date, no consensus exists regarding the type of epilepsy surgery in SWS, and the chosen surgical approach is often dependent on the standard of the treating department and their experience. Generally, hemispherectomy is chosen in patients with a widespread or hemispheric defect, while focal lesionectomy can be selected if a clear focal seizure focus is seen, ideally correlating with the radiological location of the lesion as indicated by Wang et al.4 and Bourgeois et al.6 As shown in our meta-analysis, hemispherectomy was associated with a 100% rate of postoperative hemiparesis, and therefore it might be preferable at an early age since brain plasticity seems to be better in younger children, leading to potentially better outcomes in motor function.39,40 It should be noted that many patients present with a hemiparesis before hemispherectomy due to diffuse distribution of LVA.4–6,16 This might explain the high rate of hemiparesis seen postoperatively in the hemispherectomy group.
No difference in overall postoperative complications was seen between the two groups. In the study by Wang et al., hemispherectomy had more serious complications, such as hemorrhage and cerebral infarction, which required subsequent surgeries.4 It has been shown that patients undergoing hemispherectomy more often require a CSF diversion due to hydrocephalus.6 The potential reason might be the opening of the temporal horn in hemispherectomy procedures, which can usually be avoided for lesionectomies. Lesionectomies are conducted either as focal cortical resections or as partial lobectomies of the affected lobe depending on the anatomical location and the individual epilepsy spread on EEG.4–6,16,19,20 For lesionectomies, intraoperative electrocorticography is often obtained to define the extent of resection, since preoperative EEG changes do not always respect the extent of LVA.16,19 Partial lesionectomies were undertaken in 3 included studies as well as in our presented case and were mostly performed because of neighboring eloquent cortex, which could not be resected without risking neurological deficits.5,6,16 In these cases, an individual, patient-tailored risk-benefit analysis is important, weighing the risks of neurological deficits against achieving maximal seizure control. In our presented case, the patient did not present with severe neurological deficits preoperatively. Therefore, partial lesionectomy was performed, preserving the affected eloquent cortex. Although, in our case, partial lesionectomy showed complete seizure control, in general, the available literature shows that the level of seizure control is dependent on the extent of resection or disconnection of highly epileptogenic regions.4,6,16 In case of insufficient seizure control caused by persisting epileptogenic brain tissue, repeat lesionectomy was also shown to be effective and seems feasible.21 However, the potential perioperative complications of every surgery and general anesthesia, as well as the psychological burden of an additional surgery and hospitalization, have to be explained to patients and their families.
Because of the scarce literature available, the surgical philosophy and preference of the treating neurosurgeon have a vast impact on the surgical technique chosen, and the decisions remain mostly case-by-case decisions. Owing to the complexity of this disease, SWS patients should only be treated in specialized and experienced centers, where a multidisciplinary team is present.
Limitations
Despite our conducting a systematic review and meta-analysis, several limitations are present in this study. First, we only searched two databases (PubMed and Embase) and only the English-language literature, which carries a risk of omitting important data published elsewhere. Second, epilepsy surgery in SWS is a rare topic and the included studies are very heterogeneous, which carries a risk of bias. For the quantitative meta-analysis, only 4 retrospective cohort studies could be included. Although the quality of the studies was overall good according to the NOS, the small number of studies and the small number of patients within the studies possibly limit the results. Third, no prospective or randomized trials are available on the topic, and this systematic review contains only retrospective analyses or case reports and thus has all the limitations associated with them. Fourth, the year of publication of the included studies ranged from 1984 until 2021, which induces a certain bias due to the technical developments and improved surgical tools over the last few decades, such as imaging and intraoperative neuromonitoring. Fifth, even though we assessed for publication bias, we cannot exclude a general publication bias, due to unpublished negative studies, which are not included in our meta-analysis. Last, the cohort studies of Arzimanoglou et al.16 and Bourgeois et al.6 were conducted at the same institution, which could lead to a certain overlap of their patient data.
Conclusions
Lesionectomy has a nonsignificant lower rate of favorable seizure outcome and a significantly lower rate of postoperative hemiparesis and cognitive deficits compared with hemispherectomy. Lesionectomy can be considered a valid treatment option for circumscribed LVAs, while hemispherectomy is warranted in diffuse cerebral disease and patients with a preexisting hemiparesis. Even partial lesionectomy, sparing affected neighboring eloquent cortex regions, can improve seizure control, leading to a favorable outcome. Because of the limited data available, an individual case-based approach, discussed by a specialized multidisciplinary team, is strongly advised.
Disclosures
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Author Contributions
Conception and design: Frank, Greuter, Soleman. Acquisition of data: Frank, Greuter, Soleman. Analysis and interpretation of data: Frank, Greuter. Drafting the article: Frank, Greuter. 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: Frank. Statistical analysis: Greuter. Administrative/technical/material support: Dill. Study supervision: Soleman.
References
- 1↑
Sturge WA. A Case of Partial Epilepsy, Apparently Due to a Lesion of One of the Vasomotor Centres of the Brain. Spottiswoode & Co;1879.
- 2↑
Shirley MD, Tang H, Gallione CJ, et al. Sturge-Weber syndrome and port-wine stains caused by somatic mutation in GNAQ. N Engl J Med. 2013;368(21):1971–1979.
- 3↑
De la Torre AJ, Luat AF, Juhász C, et al. A multidisciplinary consensus for clinical care and research needs for Sturge-Weber syndrome. Pediatr Neurol. 2018;84:11–20.
- 4↑
Wang S, Pan J, Zhao M, et al. Characteristics, surgical outcomes, and influential factors of epilepsy in Sturge-Weber syndrome. Brain. 2021;139(4):16–17.
- 5↑
Maton B, Kršek P, Jayakar P, et al. Medically intractable epilepsy in Sturge-Weber syndrome is associated with cortical malformation: implications for surgical therapy. Epilepsia. 2010;51(2):257–267.
- 6↑
Bourgeois M, Crimmins DW, de Oliveira RS, et al. Surgical treatment of epilepsy in Sturge-Weber syndrome in children. J Neurosurg. 2007;106(1)(suppl):20–28.
- 7↑
Benedikt RA, Brown DC, Walker R, Ghaed VN, Mitchell M, Geyer CA. Sturge-Weber syndrome: cranial MR imaging with Gd-DTPA. AJNR Am J Neuroradiol. 1993;14(2):409–415.
- 9↑
Sujansky E, Conradi S. Sturge-Weber syndrome: age of onset of seizures and glaucoma and the prognosis for affected children. J Child Neurol. 1995;10(1):49–58.
- 11↑
Roach ES, Riela AR, Chugani HT, Shinnar S, Bodensteiner JB, Freeman J. Sturge-Weber syndrome: recommendations for surgery. J Child Neurol. 1994;9(2):190–192.
- 12↑
Lance EI, Sreenivasan AK, Zabel TA, Kossoff EH, Comi AM. Aspirin use in Sturge-Weber syndrome: side effects and clinical outcomes. J Child Neurol. 2013;28(2):213–218.
- 13↑
Pearl PL, Pinto A, Sahin M. Epileptogenesis in neurocutaneous disorders with focus in Sturge Weber syndrome. F1000Res. 2016;5:370.
- 14
Lo W, Marchuk DA, Ball KL, et al. Updates and future horizons on the understanding, diagnosis, and treatment of Sturge-Weber syndrome brain involvement. Dev Med Child Neurol. 2012;54(3):214–223.
- 15↑
Luat AF, Behen ME, Chugani HT, Juhász C. Cognitive and motor outcomes in children with unilateral Sturge-Weber syndrome: effect of age at seizure onset and side of brain involvement. Epilepsy Behav. 2018;80:202–207.
- 16↑
Arzimanoglou AA, Andermann F, Aicardi J, et al. Sturge-Weber syndrome: indications and results of surgery in 20 patients. Neurology. 2000;55(10):1472–1479.
- 17
Schramm J, Kuczaty S, Sassen R, Elger CE, von Lehe M. Pediatric functional hemispherectomy: outcome in 92 patients. Acta Neurochir (Wien). 2012;154(11):2017–2028.
- 18
Liang C, Liu N, Wu J, et al. Surgery can get favorable outcome in atypical Sturge-Weber syndrome with intractable epilepsy. J Craniofac Surg. 2015;26(2):597–599.
- 19↑
Shekhtman Y, Kim I, Riviello JJJ Jr, Milla SS, Weiner HL. Focal resection of leptomeningeal angioma in a rare case of Sturge-Weber syndrome without facial nevus. Pediatr Neurosurg. 2013;49(2):99–104.
- 20↑
Hata D, Isu T, Nakanishi M, Tanaka T. Intraoperative electrocorticography and successful focus resection in a case of Sturge-Weber syndrome. Seizure. 1998;7(6):505–508.
- 21↑
Jacobs J, Levan P, Olivier A, Andermann F, Dubeau F. Late-onset epilepsy in a surgically-treated Sturge-Weber patient. Epileptic Disord. 2008;10(4):312–318.
- 22
Tuxhorn IEB, Pannek HW. Epilepsy surgery in bilateral Sturge-Weber syndrome. Pediatr Neurol. 2002;26(5):394–397.
- 23↑
Liu X, Otsuki T, Takahashi A, Kaido T. Vertical parasagittal hemispherotomy for Sturge-Weber syndrome in early infancy: case report and literature review. Springerplus. 2016;5(1):1434.
- 25↑
Engel J Jr. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia. 2001;42(6):796–803.
- 26↑
Harrer M, Cuijpers P, Furukawa TA, Ebert DD. Doing Meta-Analysis With R: A Hands-On Guide. Chapman & Hall;2021.
- 27↑
Rosén I, Salford L, Starck L. Sturge-Weber disease—neurophysiological evaluation of a case with secondary epileptogenesis, successfully treated with lobe-ectomy. Neuropediatrics. 1984;15(2):95–98.
- 28
Ito M, Sato K, Maruki C, Nitta T, Ohnuki A, Ishii S. Surgical treatment of Sturge-Weber syndrome—case report. Neurol Med Chir (Tokyo). 1989;29(1):60–64.
- 29↑
Jiruska P, Marusic P, Jefferys JGR, et al. Sturge-Weber syndrome: a favourable surgical outcome in a case with contralateral seizure onset and myoclonic-astatic seizures. Epileptic Disord. 2011;13(1):76–81.
- 30↑
Bye AM, Matheson JM, Mackenzie RA. Epilepsy surgery in Sturge-Weber syndrome. Aust Paediatr J. 1989;25(2):103–105.
- 31↑
Jagtap S, Srinivas G, Harsha KJ, Radhakrishnan N, Radhakrishnan A. Sturge-Weber syndrome: clinical spectrum, disease course, and outcome of 30 patients. J Child Neurol. 2013;28(6):725–731.
- 32↑
Griffiths PD, Coley SC, Romanowski CAJ, Hodgson T, Wilkinson ID. Contrast-enhanced fluid-attenuated inversion recovery imaging for leptomeningeal disease in children. AJNR Am J Neuroradiol. 2003;24(4):719–723.
- 33↑
Alkonyi B, Miao Y, Wu J, et al. A perfusion-metabolic mismatch in Sturge-Weber syndrome: a multimodality imaging study. Brain Dev. 2012;34(7):553–562.
- 34↑
Powell S, Fosi T, Sloneem J, Hawkins C, Richardson H, Aylett S. Neurological presentations and cognitive outcome in Sturge-Weber syndrome. Eur J Paediatr Neurol. 2021;34:21–32.
- 35↑
Kossoff EH, Buck C, Freeman JM. Outcomes of 32 hemispherectomies for Sturge-Weber syndrome worldwide. Neurology. 2002;59(11):1735–1738.
- 36↑
Kan P, Van Orman C, Kestle JRW. Outcomes after surgery for focal epilepsy in children. Childs Nerv Syst. 2008;24(5):587–591.
- 37↑
Bianchi F, Auricchio AM, Battaglia DI, Chieffo DRP, Massimi L. Sturge-Weber syndrome: an update on the relevant issues for neurosurgeons. Childs Nerv Syst. 2020;36(10):2553–2570.
- 38↑
Chevrie JJ, Specola N, Aicardi J. Secondary bilateral synchrony in unilateral pial angiomatosis: successful surgical treatment. J Neurol Neurosurg Psychiatry. 1988;51(5):663–670.
- 39↑
Hoffman HJ, Hendrick EB, Dennis M, Armstrong D. Hemispherectomy for Sturge-Weber syndrome. Childs Brain. 1979;5(3):233–248.
- 40↑
Ogunmekan AO, Hwang PA, Hoffman HJ. Sturge-Weber-Dimitri disease: role of hemispherectomy in prognosis. Can J Neurol Sci. 1989;16(1):78–80.
