Dural arteriovenous fistulas without cortical venous drainage

J Neurosurg 136:942–950, 2022

Current evidence suggests that intracranial dural arteriovenous fistulas (dAVFs) without cortical venous drainage (CVD) have a benign clinical course. However, no large study has evaluated the safety and efficacy of current treatments and their impact over the natural history of dAVFs without CVD.

METHODS The authors conducted an analysis of the retrospectively collected multicenter Consortium for Dural Arteriovenous Fistula Outcomes Research (CONDOR) database. Patient demographics and presenting symptoms, angiographic features of the dAVFs, and treatment outcomes of patients with Borden type I dAVFs were reviewed. Clinical and radiological follow-up information was assessed to determine rates of new intracranial hemorrhage (ICH) or nonhemorrhagic neurological deficit (NHND), worsening of venous hyperdynamic symptoms (VHSs), angiographic recurrence, and progression or spontaneous regression of dAVFs over time.

RESULTS A total of 342 patients/Borden type I dAVFs were identified. The mean patient age was 58.1 ± 15.6 years, and 62% were women. The mean follow-up time was 37.7 ± 54.3 months. Of 230 (67.3%) treated dAVFs, 178 (77%) underwent mainly endovascular embolization, 11 (4.7%) radiosurgery alone, and 4 (1.7%) open surgery as the primary modality. After the first embolization, most dAVFs (47.2%) achieved only partial reduction in early venous filling. Multiple complementary interventions increased complete obliteration rates from 37.9% after first embolization to 46.7% after two or more embolizations, and 55.2% after combined radiosurgery and open surgery. Immediate postprocedural complications occurred in 35 dAVFs (15.2%) and 6 (2.6%) with permanent sequelae. Of 127 completely obliterated dAVFs by any therapeutic modality, 2 (1.6%) showed angiographic recurrence/recanalization at a mean of 34.2 months after treatment. Progression to Borden-Shucart type II or III was documented in 2.2% of patients and subsequent development of a new dAVF in 1.6%. Partial spontaneous regression was found in 22 (21.4%) of 103 nontreated dAVFs. Multivariate Cox regression analysis demonstrated that older age, NHND, or severe venous-hyperdynamic symptoms at presentation and infratentorial location were associated with worse prognosis. Kaplan-Meier curves showed no significant difference for stable/improved symptoms survival probability in treated versus nontreated dAVFs. However, estimated survival times showed better trends for treated dAVFs compared with nontreated dAVFs (288.1 months vs 151.1 months, log-rank p = 0.28). This difference was statistically significant for treated dAVFs with 100% occlusion (394 months, log-rank p < 0.001).

CONCLUSIONS Current therapeutic modalities for management of dAVFs without CVD may provide better symptom control when complete angiographic occlusion is achieved.

 

The influence of aneurysm morphology on the volume of hemorrhage after rupture

J Neurosurg 136:1015–1023, 2022

Factors determining the risk of rupture of intracranial aneurysms have been extensively studied; however, little attention is paid to variables influencing the volume of bleeding after rupture. In this study the authors aimed to evaluate the impact of aneurysm morphological variables on the amount of hemorrhage.

METHODS This was a retrospective cohort analysis of a prospectively collected data set of 116 patients presenting at a single center with subarachnoid hemorrhage due to aneurysmal rupture. A volumetric assessment of the total hemorrhage volume was performed from the initial noncontrast CT. Aneurysms were segmented and reproduced from the initial CT angiography study, and morphology indexes were calculated with a computer-assisted approach. Clinical and demographic characteristics of the patients were included in the study. Factors influencing the volume of hemorrhage were explored with univariate correlations, multiple linear regression analysis, and graphical probabilistic modeling.

RESULTS The univariate analysis demonstrated that several of the morphological variables but only the patient’s age from the clinical-demographic variables correlated (p < 0.05) with the volume of bleeding. Nine morphological variables correlated positively (absolute height, perpendicular height, maximum width, sac surface area, sac volume, size ratio, bottleneck factor, neck-to-vessel ratio, and width-to-vessel ratio) and two correlated negatively (parent vessel average diameter and the aneurysm angle). After multivariate analysis, only the aneurysm size ratio (p < 0.001) and the patient’s age (p = 0.023) remained statistically significant. The graphical probabilistic model confirmed the size ratio and the patient’s age as the variables most related to the total hemorrhage volume.

CONCLUSIONS A greater aneurysm size ratio and an older patient age are likely to entail a greater volume of bleeding after subarachnoid hemorrhage.

 

Intervention for unruptured high-grade intracranial dural arteriovenous fistulas: a multicenter study

J Neurosurg 136:962–970, 2022

The risk-to-benefit profile of treating an unruptured high-grade dural arteriovenous fistula (dAVF) is not clearly defined. The aim of this multicenter retrospective cohort study was to compare the outcomes of different interventions with observation for unruptured high-grade dAVFs.

METHODS The authors retrospectively reviewed dAVF patients from 12 institutions participating in the Consortium for Dural Arteriovenous Fistula Outcomes Research (CONDOR). Patients with unruptured high-grade (Borden type II or III) dAVFs were included and categorized into four groups (observation, embolization, surgery, and stereotactic radiosurgery [SRS]) based on the initial management. The primary outcome was defined as the modified Rankin Scale (mRS) score at final follow-up. Secondary outcomes were good outcome (mRS scores 0–2) at final follow-up, symptomatic improvement, all-cause mortality, and dAVF obliteration. The outcomes of each intervention group were compared against those of the observation group as a reference, with adjustment for differences in baseline characteristics.

RESULTS The study included 415 dAVF patients, accounting for 29, 324, 43, and 19 in the observation, embolization, surgery, and SRS groups, respectively. The mean radiological and clinical follow-up durations were 21 and 25 months, respectively. Functional outcomes were similar for embolization, surgery, and SRS compared with observation. With observation as a reference, obliteration rates were higher after embolization (adjusted OR [aOR] 7.147, p = 0.010) and surgery (aOR 33.803, p < 0.001) and all-cause mortality was lower after embolization (imputed, aOR 0.171, p = 0.040). Hemorrhage rates per 1000 patient-years were 101 for observation versus 9, 22, and 0 for embolization (p = 0.022), surgery (p = 0.245), and SRS (p = 0.077), respectively. Nonhemorrhagic neurological deficit rates were similar between each intervention group versus observation.

CONCLUSIONS Embolization and surgery for unruptured high-grade dAVFs afforded a greater likelihood of obliteration than did observation. Embolization also reduced the risk of death and dAVF-associated hemorrhage compared with conservative management over a modest follow-up period. These findings support embolization as the first-line treatment of choice for appropriately selected unruptured Borden type II and III dAVFs.

Intermediate-grade brain arteriovenous malformations and the boundary of operability using the supplemented Spetzler-Martin grading system

J Neurosurg 136:125–133, 2022

Supplemented Spetzler-Martin grading (Supp-SM), which is the combination of Spetzler-Martin and Lawton-Young grades, was validated as being more accurate than stand-alone Spetzler-Martin grading, but an operability cutoff was not established. In this study, the authors surgically treated intermediate-grade AVMs to provide prognostic factors for neurological outcomes and to define AVMs at the boundary of operability.

METHODS Surgically treated Supp-SM intermediate-grade (5, 6, and 7) AVMs were analyzed from 2011 to 2018 at two medical centers. Worsened neurological outcomes were defined as increased modified Rankin Scale (mRS) scores on postoperative examinations. A second analysis of 2000–2011 data for Supp-SM grade 6 and 7 AVMs was performed to determine the subtypes with improved or unchanged outcomes. Patients were separated into three groups based on nidus size (S1: < 3 cm, S2: 3–6 cm, S3: > 6 cm) and age (A1: < 20 years, A2: 20–40 years, A3: > 40 years), followed by any combination of the combined supplemented grade: low risk (S1A1, S1A2, S2A1), intermediate risk (S2A2, S1A3, S3A1, or high risk (S3A3, S3A2, S2A3).

RESULTS Two hundred forty-six patients had intermediate Supp-SM grade AVMs. Of these patients, 102 had Supp-SM grade 5 (41.5%), 99 had Supp-SM grade 6 (40.2%), and 45 had Supp-SM grade 7 (18.3%). Significant differences in the proportions of patients with worse mRS scores at follow-up were found between the groups, with 24.5% (25/102) of patients in Supp-SM grade 5, 29.3% (29/99) in Supp-SM grade 6, and 57.8% (26/45) in Supp-SM grade 7 (p < 0.001). Patients with Supp-SM grade 7 AVMs had significantly increased odds of worse postoperative mRS scores (p < 0.001; OR 3.7, 95% CI 1.9–7.3). In the expanded cohort of 349 Supp-SM grade 6 AVM patients, a significantly higher proportion of older patients with larger Supp-SM grade 6 AVMs (grade 6+, 38.6%) had neurological deterioration than the others with Supp-SM grade 6 AVMs (22.9%, p = 0.02). Conversely, in an expanded cohort of 197 Supp-SM grade 7 AVM patients, a significantly lower proportion of younger patients with smaller Supp-SM grade 7 AVMs (grade 7–, 19%) had neurological deterioration than the others with Supp-SM grade 7 AVMs (44.9%, p = 0.01).

CONCLUSIONS Patients with Supp-SM grade 7 AVMs are at increased risk of worse postoperative neurological outcomes, making Supp-SM grade 6 an appropriate operability cutoff. However, young patients with small niduses in the low-risk Supp-SM grade 7 group (grade 7−) have favorable postoperative outcomes. Outcomes in Supp-SM grade 7 patients did not improve with surgeon experience, indicating that the operability boundary is a hard limit reflecting the complexity of high-grade AVMs.

Retrosigmoid transhorizontal fissure approach to lateral pontine cavernous malformation

J Neurosurg 136:205–214, 2022

The retrosigmoid (RS) approach is a classic route used to access deep-seated brainstem cavernous malformation (CM). The angle of access is limited, so alternatives such as the transpetrosal presigmoid retrolabyrinthine (TPPR) approach have been used to overcome this limitation. Here, the authors evaluated a modification to the RS approach, horizontal fissure dissection by using the RS transhorizontal (RSTH) approach.

METHODS Relevant clinical parameters were evaluated in 9 patients who underwent resection of lateral pontine CM. Cadaveric dissection was performed to compare the TPPR approach and the RSTH approach.

RESULTS Five patients underwent the TPPR approach, and 4 underwent the RSTH approach. Dissection of the horizontal fissure allowed for access to the infratrigeminal safe entry zone, with a direct trajectory to the middle cerebellar peduncle similar to that used in TPPR exposure. Operative time was longer in the TPPR group. All patients had a modified Rankin Scale score ≤ 2 at the last follow-up. Cadaveric dissection confirmed increased anteroposterior working angle and middle cerebellar peduncle exposure with the addition of horizontal fissure dissection.

CONCLUSIONS The RSTH approach leads to a direct lateral path to lateral pontine CM, with similar efficacy and shorter operative time compared with more extensive skull base exposure. The RSTH approach could be considered a valid alternative for resection of selected pontine CM.

Cost-effectiveness analysis in patients with an unruptured cerebral aneurysm treated with observation or surgery

J Neurosurg 135:1608–1616, 2021

The main goal of preventive treatment of unruptured intracranial aneurysms (UIAs) is to avoid the morbidity and mortality associated with aneurysmal subarachnoid hemorrhage. A comparison between the conservative approach and the surgical approach combining endovascular treatment and microsurgical clipping is currently lacking. This study aimed to conduct an updated evaluation of cost-effectiveness comparing the two approaches in patients with UIA.

METHODS A decision tree with a Markov model was developed. Quality-adjusted life-years (QALYs) associated with living with UIA before and after treatment were prospectively collected from a cohort of patients with UIA at a tertiary center. Other inputs were obtained from published literature. Using Monte Carlo simulation for patients aged 55, 65, and 75 years, the authors modeled the conservative management in comparison with preventive treatment. Different proportions of endovascular and microsurgical treatment were modeled to reflect existing practice variations between treatment centers. Outcomes were assessed in terms of QALYs. Sensitivity analyses to assess the model’s robustness and completed threshold analyses to examine the influence of input parameters were performed.

RESULTS Preventive treatment of UIAs consistently led to higher utility. Models using a higher proportion of endovascular therapy were more cost-effective. Models with older cohorts were less cost-effective than those with younger cohorts. Treatment was cost-effective (willingness to pay < 100,000 USD/QALY) if the annual rupture risk exceeded a threshold between 0.8% and 1.9% in various models based on the proportion of endovascular treatment and cohort age. A higher proportion of endovascular treatments and younger age lowered this threshold, making the treatment of aneurysms with a lower risk of rupture more cost-effective.

CONCLUSIONS Preventive treatment of aneurysms led to higher utility compared with conservative management. Models with a higher proportion of endovascular treatment and younger patient age were most cost-effective.

Basal ganglia cavernous malformations: case series and systematic review of surgical management and long-term outcomes

J Neurosurg 135:1113–1121, 2021

Reports on basal ganglia cavernous malformations (BGCMs) are rare. Here, the authors report on their experience in resecting these malformations to offer insight into this infrequent disease subtype.

METHODS The authors retrospectively reviewed a prospectively managed departmental database of all deep-seated cerebral cavernous malformations (CCMs) treated at Stanford between 1987 and 2019 and included for further analysis those with a radiographic diagnosis of BGCM. Moreover, a systematic literature review was undertaken using the PubMed and Web of Science databases.

RESULTS The departmental database search yielded 331 patients with deep-seated CCMs, 44 of whom had a BGCM (13.3%). Headache was the most common presenting sign (53.5%), followed by seizure (32.6%) and hemiparesis (27.9%). Lesion location involved the caudate nucleus in 21.4% of cases compared to 78.6% of cases within the lentiform nucleus. Caudate BGCMs were larger on presentation and were more likely to present to the ependymal surface (p < 0.001) with intraventricular hemorrhage and hydrocephalus (p = 0.005 and 0.007, respectively). Dizziness and diplopia were also more common with lesions involving the caudate. Because of their anatomical location, caudate BGCMs were preferentially treated via an interhemispheric approach and were less likely to be associated with worsening perioperative deficits than lentiform BGCMs (p = 0.006 and 0.045, respectively). Ten patients (25.6%) were clinically worse in the immediate postoperative period, 4 (10.2%) of whom continued to suffer permanent morbidity at the last follow-up. A longterm good outcome (modified Rankin Scale [mRS] score 0–1) was attained in 74.4% of cases compared to the 69.2% of patients who had presented with an mRS score 0–1. Relative to their presenting mRS score, 89.8% of patients had an improved or unchanged status at the last follow-up. The median postoperative follow-up was 11 months (range 1–252 months). Patient outcomes after resection did not differ among surgical approaches; however, patients presenting with hemiparesis and lesions involving the globus pallidus or posterior limb of the internal capsule were more likely to suffer neurological deficits during the immediate perioperative period. Patients who had undergone awake surgeries were more likely to suffer neurological decline at the early as well as the late follow-up. When adjusting for awake craniotomy as a potential confounder of lesion location, a BGCM involving the posterior limb was predictive of developing early postoperative deficits, but this finding did not persist at the long-term follow-up.

CONCLUSIONS Surgery is a safe and effective treatment modality for managing BGCMs, with an estimated long-term permanent morbidity rate of around 10%.

 

Microsurgical management of midbrain cavernous malformations: does lesion depth influence the outcome?

Acta Neurochirurgica (2021) 163:2739–2754

The purpose of this study was to clarify whether the intrinsic depth of midbrain cavernous malformations (MCMs) influenced the surgical outcome.

Methods The authors conducted a retrospective study of 76 consecutive patients who underwent microsurgical resection of a MCM. The vascular lesions were categorized into 4 distinct groups based on how these lesions had altered the brainstem surface. Additionally, it was verified whether the actual aspect of the brainstem surface could be predicted only by evaluating the pertinent preoperative MRI slices. Clinical outcome was assessed by determining the modified Rankin Scale Score (mRS) before and after surgery.

Results Twenty-three MCMs (30.3%) were located deeply within the midbrain. The overlying midbrain surface appeared to be normal (group nl). In 33 patients (43.4%), the midbrain surface showed only a yellowish discoloration (group yw). In another 14 individuals (18.4%), the midbrain surface was distorted by the underlying MCM and bulging out while the vascular lesion still remained covered by a thin parenchymal layer (group bg). In the smallest group comprising 6 patients (7.9%), the exophytic MCM had disrupted the midbrain surface and was clearly visible at microsurgical exposure (group ex). The mean mRS decreased in the group nl from 1.43 preoperatively to 0.61 at follow-up.

Conclusion This study demonstrates in a large patient population that a deep intrinsic MCM location is not necessarily associated with an unfavorable clinical outcome after microsurgical lesionectomy. Predicting the aspect of the midbrain surface by evaluating preoperative MR images alone was not sufficiently reliable.

Middle Meningeal Artery Embolization Versus Conventional Treatment of Chronic Subdural Hematomas

Neurosurgery 89:486–495, 2021

Middle meningeal artery (MMA) embolization is an emerging minimally invasive endovascular technique for chronic subdural hematoma (cSDH). Currently, limited literature exists on its safety and efficacy compared with conventional treatment (open- surgical-evacuation-only).

OBJECTIVE: To compare MMA embolization to conventional treatment.

METHODS: Retrospective analysis of patients with cSDHs treated with MMA embolization in a single center from 2018 to 2019 was performed. Comparisons were made with a historical conventional treatment cohort from 2006 to 2016. Propensity score matching analysis was used to assemble a balanced group of subjects.
RESULTS: A total of 357 conventionally treated cSDH and 45 with MMA embolization were included. After balancing with propensity score matching, a total of 25 pairs of cSDH were analyzed. Comparing the embolization with the conventional treatment group yielded no significant differences in complications (4% vs 4%; P > .99), clinical improvement (82.6% vs 83.3%; P = .95), cSDH recurrence (4.3% vs 21.7%; P = .08), overall re-intervention rates (12% vs 24%; P = .26), modified Rankin scale >2 on last follow-up (17.4% vs 32%; P = .24), as well as mortality (0% vs 12%; P = .09). Radiographic improvement at last follow-up was significantly higher in the open surgery cohort (73.9% vs 95.6%; P = .04). However, there was a trend for lengthier last follow-up for the historical cohort (72 vs 104 d; P = .07).

CONCLUSION: There was a trend for lower recurrence and mortality rates in the embolization era cohort. There were significantly higher radiological improvement rates on last follow-up in the surgical only cohort era. There were no significant differences in complications and clinical improvement.

Stereotactic radiosurgery with versus without prior Onyx embolization for brain arteriovenous malformations

J Neurosurg 135:742–750, 2021

Investigations of the combined effects of neoadjuvant Onyx embolization and stereotactic radiosurgery (SRS) on brain arteriovenous malformations (AVMs) have not accounted for initial angioarchitectural features prior to neuroendovascular intervention. The aim of this retrospective, multicenter matched cohort study is to compare the outcomes of SRS with versus without upfront Onyx embolization for AVMs using de novo characteristics of the preembolized nidus.

METHODS The International Radiosurgery Research Foundation AVM databases from 1987 to 2018 were retrospectively reviewed. Patients were categorized based on AVM treatment approach into Onyx embolization (OE) and SRS (OE+SRS) or SRS alone (SRS-only) cohorts and then propensity score matched in a 1:1 ratio. The primary outcome was AVM obliteration. Secondary outcomes were post-SRS hemorrhage, all-cause mortality, radiological and symptomatic radiation-induced changes (RICs), and cyst formation. Comparisons were analyzed using crude rates and cumulative probabilities adjusted for competing risk of death.

RESULTS The matched OE+SRS and SRS-only cohorts each comprised 53 patients. Crude rates (37.7% vs 47.2% for the OE+SRS vs SRS-only cohorts, respectively; OR 0.679, p = 0.327) and cumulative probabilities at 3, 4, 5, and 6 years (33.7%, 44.1%, 57.5%, and 65.7% for the OE+SRS cohort vs 34.8%, 45.5%, 59.0%, and 67.1% for the SRS-only cohort, respectively; subhazard ratio 0.961, p = 0.896) of AVM obliteration were similar between the matched cohorts. The secondary outcomes of the matched cohorts were also similar. Asymptomatic and symptomatic embolization-related complication rates in the matched OE+SRS cohort were 18.9% and 9.4%, respectively.

CONCLUSIONS Pre-SRS AVM embolization with Onyx does not appear to negatively influence outcomes after SRS. These analyses, based on de novo nidal characteristics, thereby refute previous studies that found detrimental effects of Onyx embolization on SRS-induced AVM obliteration. However, given the risks incurred by nidal embolization using Onyx, this neoadjuvant intervention should be used judiciously in multimodal treatment strategies involving SRS for appropriately selected large-volume or angioarchitecturally high-risk AVMs.

Outcomes of stereotactic radiosurgery for hemorrhagic arteriovenous malformations with or without prior resection or embolization

J Neurosurg 135:733–741, 2021

The major concern about ruptured arteriovenous malformations (rAVMs) is recurrent hemorrhage, which tends to preclude stereotactic radiosurgery (SRS) as a therapeutic modality for these brain malformations. In this study, the authors aimed to clarify the role of SRS for rAVM as a stand-alone modality and an adjunct for a remnant nidus after surgery or embolization.

METHODS Data on 410 consecutive patients with rAVMs treated with SRS were analyzed. The patients were classified into groups, according to prior interventions: SRS-alone, surgery and SRS (Surg-SRS), and embolization and SRS (Embol- SRS) groups. The outcomes of the SRS-alone group were analyzed in comparison with those of the other two groups.

RESULTS The obliteration rate was higher in the Surg-SRS group than in the SRS-alone group (5-year cumulative rate 97% vs 79%, p < 0.001), whereas no significant difference was observed between the Embol-SRS and SRS-alone groups. Prior resection (HR 1.78, 95% CI 1.30–2.43, p < 0.001), a maximum AVM diameter ≤ 20 mm (HR 1.81, 95% CI 1.43–2.30, p < 0.001), and a prescription dose ≥ 20 Gy (HR 2.04, 95% CI 1.28–3.27, p = 0.003) were associated with a better obliteration rate, as demonstrated by multivariate Cox proportional hazards analyses. In the SRS-alone group, the annual post-SRS hemorrhage rates were 1.5% within 5 years and 0.2% thereafter and the 10-year significant neurological event–free rate was 95%; no intergroup difference was observed in either outcome. The exclusive performance of SRS (SRS alone) was not a risk for post-SRS hemorrhage or for significant neurological events based on multivariate analyses. These results were also confirmed with propensity score–matched analyses.

CONCLUSIONS The treatment strategy for rAVMs should be tailored with due consideration of multiple factors associated with the patients. Stand-alone SRS is effective for hemorrhagic AVMs, and the risk of post-SRS hemorrhage was low. SRS can also be favorably used for residual AVMs after initial interventions, especially after failed resection.

Functional DTI tractography in brainstem cavernoma surgery

J Neurosurg 135:712–721, 2021

Surgical resection of brainstem cavernomas is associated with high postoperative morbidity due to the density of local vulnerable structures. Classical mapping of pathways by diffusion tensor imaging (DTI) has proven to be unspecific and confusing in many cases. In the current study, the authors aimed to establish a more reliable, specific, and objective method for somatotopic visualization of the descending motor pathways with navigated transcranial magnetic stimulation (nTMS)–based DTI fiber tracking.

METHODS Twenty-one patients with brainstem cavernomas were examined with nTMS prior to surgery. The resting motor threshold (RMT) and cortical representation areas of hand, leg, and facial function were determined on both hemispheres. Motor evoked potential (MEP)–positive stimulation spots were then set as seed points for tractography. Somatotopic fiber tracking was performed at a fractional anisotropy (FA) value of 75% of the individual FA threshold.

RESULTS Mapping of the motor cortex and tract reconstruction for hand, leg, and facial function was successful in all patients. The somatotopy of corticospinal and corticonuclear tracts was also clearly depicted on the brainstem level. Higher preoperative RMT values were associated with a postoperative motor deficit (p < 0.05) and correlated with a lower FA threshold (p < 0.05), revealing structural impairment of the corticospinal tract (CST) prior to surgery. In patients with a new deficit, the distance between the lesion and CST was below 1 mm.

CONCLUSIONS nTMS-based fiber tracking enables objective somatotopic tract visualization on the brainstem level and provides a valuable instrument for preoperative planning, intraoperative orientation, and individual risk stratification. nTMS may thus increase the safety of surgical resection of brainstem cavernomas.

 

Recurrent brainstem cavernous malformations following primary resection

J Neurosurg 135:671–682, 2021

Proximity of brainstem cavernous malformations (BSCMs) to tracts and cranial nerve nuclei make it costly to transgress normal tissue in accessing the lesion or disrupting normal tissue adjacent to the lesion in the separation plane. This interplay between tissue sensitivity and extreme eloquence makes it difficult to avoid leaving a remnant on occasion. Recurrences require operative intervention, which may increase morbidity, lengthen recovery, and add to overall costs. An approximately 20-year experience with patients with recurrent BSCM lesions following primary microsurgical resection was reviewed.

METHODS A prospectively maintained database of 802 patients who underwent microsurgical resection of cerebral cavernous malformations during 1997–2018 was queried to identify 213 patients with BSCMs. A retrospective chart review was conducted for patients with recurrent BSCM after primary resection who required a second surgery.

RESULTS Fourteen of 213 patients (6.6%) underwent repeat resection for recurrent BSCM. Thirty-four hemorrhagic events were observed among these 14 patients over 576 patient-years (recurrent hemorrhage rate, 5.9% per year; median discrete hemorrhagic events, 2; median time to rehemorrhage, 897 days). BSCM occurred in the pons in 10 cases, midbrain in 2 cases, and medulla in 2 cases. A blind spot in the operative corridor was the most common cause of residual BSCM (9 patients). All recurrent BSCMs were removed completely, although 2 patients each required 2 operations to treat recurrence. Twelve patients had unchanged or improved modified Rankin Scale scores at last clinical evaluation compared with admission, and 2 patients had worse scores. Recurrence was more common among patients who were operated on in the first versus the second half of the series (8.5% vs 4.7%).

CONCLUSIONS The 6.6% rate of BSCM recurrence requiring reoperation reflects the fine lines between complete resection and recurrence and between safe and harmful surgery. The detection of remnants is difficult postoperatively and remains so even at 6 months when the resection bed has healed. The 5.9% annual hemorrhage risk associated with recurrent BSCM in this experience is consistent with that reported for unoperated BSCMs. The right-angle method helps to anticipate blind spots and meticulously inspect the resection cavity for residual BSCM during surgery. A low percentage of recurrent BSCM (5%–10%) ensures ongoing effort toward an acceptable balance of safety and completeness.

Optimal access route for pontine cavernous malformation resection with preservation of abducens and facial nerve function

J Neurosurg 135:683–692, 2021

The aim of this study was to analyze the differences between posterolateral and posteromedial approaches to pontine cavernous malformations (PCMs) in order to verify the hypothesis that a posterolateral approach is more favorable with regard to preservation of abducens and facial nerve function.

METHODS The authors conducted a retrospective analysis of 135 consecutive patients who underwent microsurgical resection of a PCM. The vascular lesions were first classified in a blinded fashion into 4 categories according to the possible or only reasonable surgical access route. In a second step, the lesions were assessed according to which approach was performed and different patient groups and subgroups were determined. In a third step, the modified Rankin Scale score and the rates of permanent postoperative abducens and facial nerve palsies were assessed.

RESULTS The largest group in this series comprised 77 patients. Their pontine lesion was eligible for resection from either a posterolateral or posteromedial approach, in contrast to the remaining 3 patient groups in which the lesion location already had dictated a specific surgical approach. Fifty-four of these 77 individuals underwent surgery via a posterolateral approach and 23 via a posteromedial approach. When comparing these 2 patient subgroups, there was a statistically significant difference between postoperative rates of permanent abducens (3.7% vs 21.7%) and facial (1.9% vs 21.7%) nerve palsies. In the entire patient population, the abducens and facial nerve deficit rates were 5.9% and 5.2%, respectively, and the modified Rankin Scale score significantly decreased from 1.6 ± 1.1 preoperatively to 1.0 ± 1.1 at follow-up.

CONCLUSIONS The authors’ results suggest favoring a posterolateral over a posteromedial access route to PCMs in patients in whom a lesion is encountered that can be removed via either surgical approach. In the present series, the authors have found such a constellation in 57% of all patients. This retrospective analysis confirms their hypothesis in a large patient cohort. Additionally, the authors demonstrated that 4 types of PCMs can be distinguished by preoperatively evaluating whether only one reasonable or two alternative surgical approaches are available to access a specific lesion. The rates of postoperative sixth and seventh nerve palsies in this series are substantially lower than those in the majority of other published reports.

Cerebral venous drainage in patients with dural arteriovenous fistulas: correlation with clinical presentation

J Neurosurg 135:440–448, 2021

Dural arteriovenous fistulas (DAVFs) are abnormal, acquired arteriovenous connections within the dural leaflets. Their associated symptoms may be mild or severe and are related to the patient’s venous anatomy. With the hypothesis that the patient’s venous anatomy determines the development of symptoms, the authors aimed to identify which venous anatomy elements are important in the development of major symptoms in patients with a DAVF.

METHODS A multicenter study was performed based on the retrospective analysis of cerebral angiographies with systematic assessment of brain drainage pathways (including fistula drainage) in patients over 18 years of age with a single DAVF. The patients were divided into two groups: those with minor (group 1, n = 112) and those with major (group 2, n = 89) symptoms. Group 2 was subdivided into two groups: patients with hemorrhage (group 2a, n = 47) and patients with severe nonhemorrhagic symptoms (group 2b, n = 42).

RESULTS The prevalence of stenosis in DAVF venous drainage and the identification of tiny anastomoses between venous territories were significantly higher in group 2 (32.6% and 19.1%, respectively) compared with group 1 (2.68% and 5.36%, respectively). Stenosis of DAVF venous drainage was significantly more frequent in group 2a than in group 2b (51.1% vs 11.9%, p < 0.001). Group 2b patients had increased prevalence of shared use of the cerebral main drainage pathway (85.0% vs 53.2%, p = 0.002), the absence of an alternative route (45.0% vs 17.0%, p = 0.004), and the presence of contrast stagnation (62.5% vs 29.8%, p = 0.002) compared with group 2a patients. In patients with high-grade fistulas, the group with major symptoms had increased prevalence of a single draining direction (31.3% vs 8.33%, p = 0.003), stenosis in the draining vein (35.0% vs 6.25%, p = 0.000), the absence of an alternative pathway for brain drainage (31.3% vs 12.5%, p = 0.017), and the presence of contrast stagnation (48.8% vs 22.9%, p = 0.004).

CONCLUSIONS Major symptoms were observed when normal brain tissue venous drainage was impaired by competition with DAVF (predominance in group 2b) or when DAVF venous drainage had anatomical characteristics that hindered drainage, with consequent venous hypertension on the venous side of the DAVF (predominance in group 2a). The same findings were observed when comparing two groups of patients with high-grade lesions: those with major versus those with minor symptoms.

Assessment and validation of proposed classification tools for brainstem cavernous malformations

J Neurosurg 135:410–416, 2021

Treatment indications for patients with brainstem cavernous malformations (BSCMs) remain difficult and controversial. Some authors have tried to establish classification tools to identify eligible candidates for surgery. Authors of this study aimed to validate the performance and replicability of two proposed BSCM grading systems, the Lawton- Garcia (LG) and the Dammann-Sure (DS) systems.

METHODS For this cross-sectional study, a database was screened for patients with BSCM treated surgically between 2003 and 2019 in the authors’ department. Complete clinical records, preoperative contrast-enhanced MRI, and a postoperative follow-up ≥ 6 months were mandatory for study inclusion. The modified Rankin Scale (mRS) score was determined to quantify neurological function and outcome. Three observers independently determined the LG and the DS score for each patient.

RESULTS A total of 67 patients met selection criteria. Univariate and multivariate analyses identified multiple bleedings (p = 0.02, OR 5.59), lesion diameter (> 20 mm, p = 0.007, OR 5.43), and patient age (> 50 years, p = 0.019, OR 4.26) as predictors of an unfavorable postoperative functional outcome. Both the LG (AUC = 0.72, p = 0.01) and the DS (AUC = 0.78, p < 0.01) scores were robust tools to estimate patient outcome. Subgroup analyses confirmed this observation for both grading systems (LG: p = 0.005, OR 6; DS: p = 0.026, OR 4.5), but the combined use of the two scales enhanced the test performance significantly (p = 0.001, OR 22.5).

CONCLUSIONS Currently available classification systems are appropriate tools to estimate the neurological outcome after BSCM surgery. Future studies are needed to design an advanced scoring system, incorporating items from the LG and the DS score systems.

 

The middle communicating artery: a novel fourth-generation bypass for revascularizing trapped middle cerebral artery bifurcation aneurysms

J Neurosurg 134:1879–1886, 2021

The anterior and posterior communicating arteries are natural connections between arteries that enable different adjacent circulations to redistribute blood flow instantly in response to changing supply and demand. An analogous communication does not exist in the middle cerebral circulation. A middle communicating artery (MCoA) can be created microsurgically between separate middle cerebral artery (MCA) trunks, enabling flow to redistribute in response to changing supply and demand. The MCoA would draw blood flow from an adjacent circulation such as the external carotid circulation. The MCoA requires the application of fourth-generation techniques to reconstruct bi- and trifurcations after occluding complex MCA trunk aneurysms.

In this report, the authors describe two recent cases of complex MCA biand trifurcation aneurysms in which the occluded efferent trunks were revascularized by creating an MCoA. The first MCoA was created with a “double-barrel” superficial temporal artery–M2 segment bypass and end-to-end reimplantation of the middle and inferior MCA trunks. The second MCoA was created with an external carotid artery–radial artery graft–M2 segment interpositional bypass and end-to-side reimplantation of the inferior trunk onto the superior trunk. Both aneurysms were occluded, and both patients experienced good outcomes.

This report introduces the concept of the MCoA and demonstrates two variations. Angioarchitectural and technical elements include the donation of flow from an adjacent circulation, a communicating bypass, the application of fourth-generation bypass techniques, and a minimized ischemia time. The MCoA construct is ideally suited for rebuilding bi- and trifurcated anatomy after trapping or distally occluding complex MCA aneurysms.

Intradural spinal cord arteriovenous shunts in a personal series of 210 patients

J Neurosurg Spine 34:920–930, 2021

Few classifications of intradural spinal arteriovenous shunts (ID-SAVSs) have considered their anatomical localization in relation to their phenotype and angioarchitectonics. The authors propose another vision of ID-SAVSs allowing a reappraised classification based on analysis of the anatomical disposition, angioarchitecture, and histogenetic location of these vascular malformations.

METHODS The radiological and clinical records of 210 patients with ID-SAVSs were retrospectively reviewed, considering their localization, vascular architectonics, and correlation with the 5 histogenetic units of the spinal cord. Among these, 183 files with complete data allowed precise analysis of the ID-SAVSs.

RESULTS Among these 183 files (162 and 21 cases with single and multiple lesions, respectively), different entities were identified: 13 pial macro arteriovenous fistulas (MAVFs), 92 pial micro arteriovenous fistulas (mAVFs), 33 superficial pial niduses, and 69 intramedullary niduses. Thirteen sulcal shunts (either fistulas or niduses) were considered subtypes of pial lesions. Among the 21 multiple cases, 11 were monomyelomeric while 10 were multimyelomeric. Pial lesions, either fistulas or niduses, were dominantly vascularized by pial arteries (anterior or posterior depending on the localization of the shunt) and occasionally (except for MAVFs) by transmedullary arteries. Pial niduses occasionally extended into the funiculus by recruiting intrinsic veins or by extension of the nidus itself inside the white matter. Intramedullary niduses were always vascularized by both centrifugal and centripetal feeders, respectively, from sulcal arteries (SAs) and pial arteries. Sulcal lesions are pial lesions located within the ventral median sulcus and vascularized by SAs and veins. Single or multiple ID-SAVSs can be part of various syndromes such as hereditary hemorrhagic telangiectasia, Parkes-Weber, RASA1, CLOVES, and spinal arteriovenous metameric syndromes. Histogenetic analyses revealed a specific distribution of each ID-SAVS in the 5 histogenetic units of the spinal cord: intramedullary niduses were found almost equally from cervical to thoracic units, while MAVFs and mAVFs were mostly found from thoracic to postcrural ones. Pial niduses showed intermediate features between intramedullary and fistulous lesions and were mostly distributed from brachial to crural segments.

CONCLUSIONS Precise analysis of the anatomical disposition of ID-SAVSs in relation to functional histogenetic units allows a better understanding of these lesions and improved therapeutic management.

 

Subclinical imaging changes in cerebral cavernous angiomas during prospective surveillance

J Neurosurg 134:1147–1154, 2021

The purpose of this study was to systematically assess asymptomatic changes (ACs), including subclinical hemorrhage, growth, or new lesion formation (NLF) during longitudinal follow-up of cerebral cavernous angiomas (CAs), and to correlate these with symptomatic hemorrhage (SH) during the same period and with clinical features of the disease.

METHODS One hundred ninety-two patients were included in this study, among 327 consecutive patients with CA, prospectively identified between September 2009 and February 2019. Included patients had undergone clinical and MRI follow-up, in conjunction with institutional review board–approved biomarker studies, and harbored ≥ 1 CA with a maximum diameter of ≥ 5 mm on T2-weighted MRI. Rates of AC and SH per lesion-year and patient-year were assessed using prospectively articulated criteria. In multifocal/familial cases, rates of NLF were also assessed.

RESULTS There were no differences in demographic or disease features among cases included or excluded in the study cohort, except for a higher proportion of included patients with CCM3 mutation. Follow-up was 411 patient-years (2503 lesion-years). The rate of AC was higher than the rate of SH (12.9% vs 7.5% per patient-year, and 2.1% vs 1.2% per lesion-year, both p = 0.02). Patients presenting with a prior history of SH had a higher rate of AC than those with other forms of presentation (19.7% and 8.2% per patient-year, respectively; p = 0.003). A higher rate of NLF on T2-weighted MRI (p = 0.03) was observed in patients with prior SH. Three of 6 solitary/sporadic and 2 of 28 multifocal/familial patients underwent resection of the lesion after AC.

CONCLUSIONS Rates of AC are greater than SH during prospective follow-up of CAs, and greater in cases with prior SH. AC may be a more sensitive biomarker of lesional activity, and a more efficient surrogate outcome in clinical trials than SH. Patients experiencing an AC are more likely to undergo a surgical intervention when CAs are solitary/sporadic than when they are multifocal/familial.

 

Sphenoparietal sinus transposition technique: optimization of the surgical corridor with preservation of prominent bridging veins between the brain and the cranial base during aneurysm clipping via the pterional approach

J Neurosurg 134:999–1005, 2021

The sylvian bridging veins between the brain and the dura on the inner surface of the sphenoid wing can restrict brain retraction for widening of the lateral retrocarotid space during clipping surgery for internal carotid artery (ICA)–posterior communicating artery (PCoA) and basilar apex (BX) aneurysms. In such cases, the authors perform extradural anterior clinoidectomy with peeling of the temporal dura propria from the periosteal dura and inner cavernous membrane around the superior orbital fissure, with the incision of the dura mater stretching from the base of the temporal side to just before the distal dural ring of the ICA (termed by the authors as the sphenoparietal sinus transposition [SPST] technique). This technique displaces the bridging segment of the sylvian vein posteriorly and enables widening of the surgical space without venous injury. In this study, the authors observed the operative nuances and investigated the usefulness of this technique.

METHODS The authors retrospectively reviewed the medical charts of 66 consecutive patients with ICA-PCoA and BX aneurysms between January 2016 and July 2018. This technique was performed in 8 patients (5 patients with PCoA aneurysms and 3 with BX aneurysms) in whom the bridging segments of the sylvian veins between the brain and the skull base restricted brain retraction for widening of the surgical space. The surface areas of the lateral retrocarotid space and the aneurysm were measured at the most visible working angle before and after the SPST technique was performed.

RESULTS With the use of the SPST technique, an adequate surgical space for aneurysm clipping was obtained with preservation of the bridging veins in all patients. The mean surface areas of the lateral retrocarotid space (p = 0.002) and aneurysm (p = 0.001) were significantly increased from 18.3 ± 18.8 and 2.8 ± 2.5 cm2 before to 64.2 ± 21.1 and 20.9 ± 20.6 cm2, respectively, after the SPST technique was performed.

CONCLUSIONS The SPST technique enables displacement of the bridging segments of the sylvian veins without venous injury and enables widening of the surgical space around the lateral retrocarotid area.