A taxonomy for deep cerebral cavernous malformations: subtypes of thalamic lesions

J Neurosurg 139:1681–1696, 2023

Anatomical taxonomy is a practical tool to successfully guide clinical decision-making for patients with brain arteriovenous malformations and brainstem cavernous malformations (CMs). Deep cerebral CMs are complex, difficult to access, and highly variable in size, shape, and position. The authors propose a novel taxonomic system for deep CMs in the thalamus based on clinical presentation (syndromes) and anatomical location (identified on MRI).

METHODS The taxonomic system was developed and applied to an extensive 2-surgeon experience from 2001 through 2019. Deep CMs involving the thalamus were identified. These CMs were subtyped on the basis of the predominant surface presentation identified on preoperative MRI. Six subtypes among 75 thalamic CMs were defined: anterior (7/75, 9%), medial (22/75, 29%), lateral (10/75, 13%), choroidal (9/75, 12%), pulvinar (19/75, 25%), and geniculate (8/75, 11%). Neurological outcomes were assessed using modified Rankin Scale (mRS) scores. A postoperative score ≤ 2 was defined as a favorable outcome and > 2 as a poor outcome. Clinical and surgical characteristics and neurological outcomes were compared among subtypes.

RESULTS Seventy-five patients underwent resection of thalamic CMs and had clinical and radiological data available. Their mean age was 40.9 (SD 15.2) years. Each thalamic CM subtype was associated with a recognizable constellation of neurological symptoms. The common symptoms were severe or worsening headaches (30/75, 40%), hemiparesis (27/75, 36%), hemianesthesia (21/75, 28%), blurred vision (14/75, 19%), and hydrocephalus (9/75, 12%). The thalamic CM subtype determined the selection of surgical approach. A single approach was associated with each subtype for most patients. The main exception to this paradigm was that in the surgeons’ early experience, pulvinar CMs were resected through a superior parietal lobule–transatrial approach (4/19, 21%), which later evolved to the paramedian supracerebellar-infratentorial approach (12/19, 63%). Relative outcomes implied by mRS scores were unchanged or improved in most patients (61/66, 92%) postoperatively.

CONCLUSIONS This study confirms the authors’ hypothesis that this taxonomy for thalamic CMs can meaningfully guide the selection of surgical approach and resection strategy. The proposed taxonomy can increase diagnostic acumen at the patient bedside, help identify optimal surgical approaches, enhance the clarity of clinical communications and publications, and improve patient outcomes.

Trends in the size of treated unruptured intracranial aneurysms over 35 years

J Neurosurg 139:1328–1338, 2023

In the absence of clear guidelines and consistent natural history data, the decision to treat unruptured intracranial aneurysms (UIAs) is a matter of some controversy. Currently, decisions are often guided by a consensus of cerebrovascular specialist teams and patient preferences. It is unclear how paradigm-shifting developments in the detection and treatment of UIAs have affected the size of the UIAs that are selected for treatment. Herein, the authors aimed to study potential changes in the average size of the UIAs that were treated over time. They hypothesized that the average size of UIAs that are treated is decreasing over time.

METHODS A systematic search of the literature was performed to identify all studies describing the size of UIAs that were treated using any modality. Scatter diagrams with trend lines were used to plot the size of the aneurysms treated over time and assess for the presence of a potentially significant trend via statistical correlation tests. Subgroup analyses based on type of treatment, country of study, and specialty of the authors were performed.

RESULTS A total of 240 studies including 35,150 UIAs treated between 1987 and 2021 met all eligibility criteria and were entered in the analysis. The mean age of patients was 55.5 years, and 70.7% of the patients were females. There was a significant decrease in the size of treated UIAs over time (Spearman’s r = −0.186, p < 0.001), with a 0.71-mm decrease in the average size of treated UIAs every 5 years since 1987 and an annual mean dropping below 7 mm in 2012. This decreasing trend was present in surgically and endovascularly treated UIAs (p < 0.001 for both), in more developed and developing countries (p < 0.001 for both), within neurosurgical and non-neurosurgical specialties (p < 0.001 for both), most prominently in the US (Spearman’s r = −0.482, p < 0.001), and less prominently in Europe (Spearman’s r = −0.221, p < 0.001) and was not detected in East Asia.

CONCLUSIONS The present study indicates that based on the treated UIA size data published in the literature over the past 35 years, smaller UIAs are being treated over time. This trend is likely driven by safer treatments. However, future studies should elucidate the cost-effectiveness of treating smaller UIAs as well as the possible real-world contribution of this trend in preventing aneurysmal subarachnoid hemorrhage.

Outcome of 107 conservatively managed unruptured brain arteriovenous malformations

J Neurosurg 139:1025–1035, 2023

Since the publication of A Randomized Trial of Unruptured Brain AVMs (ARUBA), the management of unruptured brain arteriovenous malformations (bAVMs) has been controversially discussed. Long-term follow-up data on the exclusively conservative management of unruptured bAVMs are scarce. The authors evaluated the long-term outcomes of patients with unruptured untreated bAVMs in a real-life cohort.

METHODS A retrospective observational cohort of 107 patients (of 897 bAVM patients referred to the authors’ institution) with a diagnosis of unruptured and conservatively managed bAVMs is presented. AVMs of all Spetzler-Martin grades were observed. The mean follow-up period was 84 months. In 44% of patients, a follow-up period of 5 years or longer was observed. A national death register comparison completed the outcome analysis.

RESULTS The median age at diagnosis, sex distribution, neurological presentation, and modified Rankin Scale score were comparable to the patients in the medical management arm of the ARUBA study. Patients were mainly young, predominantly male, and in good clinical condition. Similar to the ARUBA cohort, 77% of this study’s cohort presented in an excellent clinical status at the time of last follow-up. However, 17% of patients had at least one hemorrhage, resulting in an overall annual hemorrhage risk of 2.7% in the observation period. Moreover, the cumulative 1-, 5-, and 10-year overall hemorrhage rates were 3.0%, 11.3%, and 15.3%, respectively. Consequently, the long-term follow-up AVM-related mortality rate amounted to 8%. The estimated median overall survival after AVM diagnosis was 19.3 years (95% CI 14.024.6 years). A multivariate Cox regression model revealed temporal and deep-seated localization as an independent risk factor for AVM hemorrhage, while the presence of seizures reached borderline significance as a risk factor.

CONCLUSIONS The authors’ results represent the long-term course of unruptured untreated bAVMs. Their data support the conclusion that even in the post-ARUBA era, tailored active treatment options may be offered to patients with unruptured bAVMs. For patient counseling, individual risk factors should be weighed against the center’s treatmentspecific risks.

HummingFlow: novel single twist-drill access for ventricular drainage, irrigation, monitoring, and automated local drug delivery in subarachnoid hemorrhage

J Neurosurg 139:1036–1041, 2023

The management of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage (aSAH) remains one of the most important targets for neurocritical care. Advances in monitoring technology have facilitated a more thorough understanding of the pathophysiology and therapeutic approaches, but interventions are generally limited to either systemic therapies or passive CSF drainage. The authors present a novel approach that combines a multimodal monitoring bolt-based system with an irrigating ventricular drain capable of delivering intrathecal medications and describe their early experience in patients with aSAH.

METHODS The authors performed a retrospective review of cases treated with the combined Hummingbird multimodal bolt system and the IRRAflow irrigating ventriculostomy.

RESULTS Nine patients were treated with the combined multimodal bolt system with irrigating ventriculostomy approach. The median number of days to clearance of the third and fourth ventricles was 3 days in patients with obstructive intraventricular hemorrhage. Two patients received intrathecal alteplase for intraventricular hemorrhage clearance, and 2 patients received intrathecal nicardipine as rescue therapy for severe symptomatic angiographic vasospasm.

CONCLUSIONS Combined CSF drainage, irrigation, multimodality monitoring, and automated local drug delivery are feasible using a single twist-drill hole device. Further investigation of irrigation settings and treatment approaches in high-risk cases is warranted.

Clinical and prognostic features of venous hypertensive myelopathy from craniocervical arteriovenous fistulas

J Neurosurg 139:687–697, 2023

Current knowledge about venous hypertensive myelopathy (VHM) is incomplete. This study was performed with the aim of clarifying the clinical features and outcomes of craniocervical VHM.

METHODS This retrospective, single-center cohort study included 65 patients with craniocervical junction arteriovenous fistulas resulting in VHM treated in Xuanwu Hospital from January 1, 2002, to December 30, 2020. All patients underwent microsurgery or endovascular treatment. The primary outcome was neurological function assessment using the Japanese Orthopaedic Association (JOA) scale, modified Aminoff-Logue Scale (mALS), and Venous Hypertensive Myelopathy Scale (VHMS). The secondary outcomes were recurrences and postoperative adverse events. Pearson linear regression and receiver operating characteristic curves were used to evaluate the relationships among the three scales. Kaplan-Meier and multivariate logistic regression analyses were performed to predict outcomes.

RESULTS The mean patient age was 57.4 ± 11.4 years, and 88% of patients were male. The 1-year follow-up rate was 83.1%, and the 5-year follow-up rate was 50.8%. The VHMS was correlated with the JOA (R 2 = 0.6722) and mALS (R 2 = 0.7399) and increased the assessment accuracy by approximately 20% when compared with the other two scales. Overall, 25.9% of patients experienced delayed neurological decline beyond the 1-year follow-up. Further logistic regression suggested that age > 65 years was an independent predictor (OR 7.831, 95% CI 1.090–56.266; p = 0.041). Embolic recanalization and new bilateral symmetry feeders were the major reasons for recurrence. Recurrence increased the risk of adverse events after the second surgery (OR 20.455, 95% CI 1.170–357.320; p = 0.039).

CONCLUSIONS CCJ AVFs resulting in VHM are a rare but deadly complication, and providers should be cautious of age-related delayed neurological decline and strive for a one-time anatomical cure.

Transforaminal Lumbar Interbody Fusion Versus Posterolateral Fusion Alone in the Treatment of Grade 1 Degenerative Spondylolisthesis

Neurosurgery 93:186–197, 2023

Transforaminal lumbar interbody fusion (TLIF) and posterolateral fusion (PLF) alone are two operations performed to treat degenerative lumbar spondylolisthesis. To date, it is unclear which operation leads to better outcomes.

OBJECTIVE: To compare TLIF vs PLF alone regarding long-term reoperation rates, complications, and patient-reported outcome measures (PROMs) in patients with degenerative grade 1 spondylolisthesis.

METHODS: A retrospective cohort study using prospectively collected data between October 2010 and May 2021 was undertaken. Inclusion criteria were patients aged 18 years or older with grade 1 degenerative spondylolisthesis undergoing elective, single-level, open posterior lumbar decompression and instrumented fusion with ≥1-year follow-up. The primary exposure was presence of TLIF vs PLF without interbody fusion. The primary outcome was reoperation. Secondary outcomes included complications, readmission, discharge disposition, return to work, and PROMs at 3 and 12 months postoperatively, including Numeric Rating Scale-Back/Leg and Oswestry Disability Index. Minimum clinically important difference of PROMs was set at 30% improvement from baseline.

RESULTS: Of 546 patients, 373 (68.3%) underwent TLIF and 173 underwent (31.7%) PLF. Median follow-up was 6.1 years (IQR = 3.6-9.0), with 339 (62.1%) >5-year follow-up. Multivariable logistic regression showed that patients undergoing TLIF had a lower odds of reoperation compared with PLF alone (odds ratio = 0.23, 95% CI = 0.54-0.99, P = .048). Among patients with >5-year follow-up, the same trend was seen (odds ratio = 0.15, 95% CI = 0.03-0.95, P = .045). No differences were observed in 90-day complications (P = .487) and readmission rates (P = .230) or minimum clinically important difference PROMs.

CONCLUSION: In a retrospective cohort study from a prospectively maintained registry, patients with grade 1 degenerative spondylolisthesis undergoing TLIF had significantly lower long-term reoperation rates than those undergoing PLF.

Safety of brainstem safe entry zones: comparison of microsurgical outcomes associated with superficial, exophytic, and deep brainstem cavernous malformations

J Neurosurg 139:113–123, 2023

Safe entry zones (SEZs) enable safe tissue transgression to lesions beneath the brainstem surface. However, evidence for the safety of SEZs is scarce and is based on anatomical studies, case reports, and small series.

METHODS A cohort of 154 patients who underwent microsurgical brainstem cavernous malformation (BSCM) treatment during a 23-year period and who had preoperative MR images and intraoperative photographs or videos was retrospectively examined. This study assessed the safety of SEZs for access to deep BSCMs, preoperative MRI to predict BSCM surface proximity, and the relationships between BSCM subtype, surgical approach, and SEZs. Lesions were characterized as exophytic, superficial, or deep on the basis of preoperative MRI and intraoperative inspection. Outcomes were scored as good (modified Rankin Scale [mRS] score ≤ 2) or poor (mRS score > 2) and relative outcomes as stable/ improved or worse relative to baseline (± 1 point).

RESULTS Resections included 34 (22%) in the midbrain, 102 (66%) in the pons, and 18 (12%) in the medulla. Of those, 23 (15%) were exophytic, 57 (37%) were superficial, and 74 (48%) were deep. Established SEZs were used for 97% (n = 72) of deep lesions; the preferred SEZ associated with its subtype was used for 91% (n = 67). MR images accurately depicted exophytic BSCMs that did not require SEZ approaches (sensitivity, 96%) but overestimated the proximity of lesions superficial to brainstem surfaces (specificity, 67%), resulting in unanticipated SEZ use. Final neurological outcomes were good in 80% of patients with follow-up data (119/149), and relative outcomes were stable/improved in 93% (139/149). Outcomes for patients with brainstem transgression through an SEZ did not differ from outcomes for patients with superficial or exophytic lesions that did not require SEZ use (final mRS score ≤ 2 in 72% of all patients with deep lesions vs 82% of all patients with superficial or exophytic lesions [p = 0.10]). Among patients with follow-up, the rates of permanent new cranial nerve deficits in patients with deep BSCMs and superficial or exophytic BSCMs were 21% and 20%, respectively (p = 0.81), with no significant change in overall cranial nerve deficit (0 and −1, p = 0.65).

CONCLUSIONS Neurological outcomes for patients with deep BSCMs were equivalent to those for superficial or exophytic BSCMs, validating the safety of SEZs for deep BSCMs. Preoperative T1-weighted MR images overestimated the lesion’s surface proximity, necessitating detailed knowledge of SEZs and readiness to use them in cases of radiologicalmicrosurgical discordance. Most patients achieved favorable outcomes despite the transgression of eloquent brainstem tissue in and around SEZs.

Rehemorrhage of brainstem cavernous malformations: a benchmark approach to individualized risk and severity assessment

J Neurosurg 139:94–105, 2023

Brainstem cavernous malformations (BSCMs) represent a unique subgroup of cavernous malformations with more hemorrhagic presentation and technical challenges. This study aimed to provide individualized assessment of the rehemorrhage clustering risk of BSCMs after the first symptomatic hemorrhage and to identify patients at higher risk of neurological deterioration after new hemorrhage, which would help in clinical decision-making.

METHODS A total of 123 consecutive BSCM patients with symptomatic hemorrhage were identified between 2015 and 2022, with untreated follow-up > 12 months or subsequent hemorrhage during the untreated follow-up. Nomograms were proposed to individualize the assessment of subsequent hemorrhage risk and neurological status (determined by the modified Rankin Scale [mRS] score) after future hemorrhage. The least absolute shrinkage and selector operation (LASSO) regression was used for feature screening. The calibration curve and concordance index (C-index) were used to assess the internal calibration and discrimination performance of the nomograms. Cross-validation was further performed to validate the accuracy of the nomograms.

RESULTS Prior hemorrhage times (adjusted OR [aOR] 6.78 per ictus increase) and Zabramski type I or V (OR 11.04) were associated with rehemorrhage within 1 year. A lower mRS score after previous hemorrhage (aOR 0.38 for a shift to a higher mRS score), Zabramski type I or V (OR 3.41), medulla or midbrain location (aOR 2.77), and multiple cerebral cavernous malformations (aOR 11.76) were associated with worsened neurological status at subsequent hemorrhage. The nomograms showed good accuracy and discrimination, with a C-index of 0.80 for predicting subsequent hemorrhage within 1 year and 0.71 for predicting neurological status after subsequent hemorrhage, which were maintained in cross-validation.

CONCLUSIONS An individualized approach to risk and severity assessment of BSCM rehemorrhage was feasible with clinical and imaging features.

Predicting the growth of middle cerebral artery bifurcation aneurysms using differences in the bifurcation angle and inflow coefficient

J Neurosurg 138:1357–1365, 2023

Growing intracranial aneurysms (IAs) are prone to rupture. Previous cross-sectional studies using postrupture morphology have shown the morphological or hemodynamic features related to IA rupture. Yet, which morphological or hemodynamic differences of the prerupture status can predict the growth and rupture of smaller IAs remains unknown. The purpose of this longitudinal study was to investigate the effects of morphological features and the hemodynamic environment on the growth of IAs at middle cerebral artery (MCA) bifurcations during the follow-up period.

METHODS One hundred two patients with MCA M1–2 bifurcation saccular IAs who underwent follow-up for more than 2 years at the authors’ institutions between 2011 and 2019 were retrospectively identified. During the follow-up period, cases involving growth of MCA IAs were assigned to the event group, and those with MCA IAs unchanged in size were assigned to the control group. The morphological parameters examined were aneurysmal neck length, dome height, aspect ratio and volume, M1 and M2 diameters and their ratio, and angle configurations among M1, M2, and the aneurysm. Hemodynamic parameters were flow rate and wall shear stress in M1, M2, and the aneurysm, including the aneurysmal inflow rate coefficient (AIRC), defined as the ratio of the aneurysmal inflow rate to the M1 flow rate. Those parameters were compared statistically between the two groups. Correlations between morphological and hemodynamic parameters were also examined.

RESULTS Eighty-three of 102 patients were included: 25 with growing MCA IAs (event group) and 58 with stable MCA IAs (control group). The median patient age at initial diagnosis was 66.9 (IQR 59.8–72.3) years. The median follow-up period was 48.5 (IQR 36.5–65.6) months. Both patient age and the AIRC were significant independent predictors of the growth of MCA IAs. Moreover, the AIRC was strongly correlated with sharper bifurcation and inflow angles, as well as wider inclination angles between the M1 and M2 arteries.

CONCLUSIONS The AIRC was a significant independent predictor of the growth of MCA IAs. Sharper bifurcation and inflow angles and wider inclination angles between the M1 and M2 arteries were correlated with the AIRC. MCA IAs with such a bifurcation configuration are more prone to grow and rupture.

Endovascular treatment of brain arteriovenous malformations: clinical outcomes of patients included in the registry of a pragmatic randomized trial

J Neurosurg 138:1393–1402, 2023

The role of endovascular treatment in the management of patients with brain arteriovenous malformations (AVMs) remains uncertain. AVM embolization can be offered as stand-alone curative therapy or prior to surgery or stereotactic radiosurgery (SRS) (pre-embolization). The Treatment of Brain AVMs Study (TOBAS) is an all-inclusive pragmatic study that comprises two randomized trials and multiple registries.

METHODS Results from the TOBAS curative and pre-embolization registries are reported. The primary outcome for this report is death or dependency (modified Rankin Scale [mRS] score > 2) at last follow-up. Secondary outcomes include angiographic results, perioperative serious adverse events (SAEs), and permanent treatment-related complications leading to an mRS score > 2.

RESULTS From June 2014 to May 2021, 1010 patients were recruited in TOBAS. Embolization was chosen as the primary curative treatment for 116 patients and pre-embolization prior to surgery or SRS for 92 patients. Clinical and angiographic outcomes were available in 106 (91%) of 116 and 77 (84%) of 92 patients, respectively. In the curative embolization registry, 70% of AVMs were ruptured, and 62% were low-grade AVMs (Spetzler-Martin grade I or II), while the pre-embolization registry had 70% ruptured AVMs and 58% low-grade AVMs. The primary outcome of death or disability (mRS score > 2) occurred in 15 (14%, 95% CI 8%–22%) of the 106 patients in the curative embolization registry (4 [12%, 95% CI 5%–28%] of 32 unruptured AVMs and 11 [15%, 95% CI 8%–25%] of 74 ruptured AVMs) and 9 (12%, 95% CI 6%–21%) of the 77 patients in the pre-embolization registry (4 [17%, 95% CI 7%–37%] of 23 unruptured AVMs and 5 [9%, 95% CI 4%–20%] of 54 ruptured AVMs) at 2 years. Embolization alone was confirmed to occlude the AVM in 32 (30%, 95% CI 21%–40%) of the 106 curative attempts and in 9 (12%, 95% CI 6%–21%) of 77 patients in the pre-embolization registry. SAEs occurred in 28 of the 106 attempted curative patients (26%, 95% CI 18%–35%, including 21 new symptomatic hemorrhages [20%, 95% CI 13%–29%]). Five of the new hemorrhages were in previously unruptured AVMs (n = 32; 16%, 95% CI 5%–33%). Of the 77 pre-embolization patients, 18 had SAEs (23%, 95% CI 15%–34%), including 12 new symptomatic hemorrhages [16%, 95% CI 9%–26%]). Three of the hemorrhages were in previously unruptured AVMs (3/23; 13%, 95% CI 3%–34%).

CONCLUSIONS Embolization as a curative treatment for brain AVMs was often incomplete. Hemorrhagic complications were frequent, even when the specified intent was pre-embolization before surgery or SRS. Because the role of endovascular treatment remains uncertain, it should preferably, when possible, be offered in the context of a randomized trial.

Nomogram for predicting an individual prospective hemorrhage risk in untreated brainstem cavernous malformations

J Neurosurg 138:910–921, 2023

In this study, the authors aimed to create a nomogram for precisely predicting the 5-year prospective hemorrhage risk in brainstem cavernous malformations (BSCMs).

METHODS Patients with confirmed BSCMs in a single-center prospective observational series from January 2012 to December 2016 were included in the present study for nomogram building and validation. The concordance index (C-index), calibration curves, and decision curve analysis were used to evaluate the predictive accuracy, discriminative ability, and clinical usefulness of the nomogram. Then, a nomogram-based risk stratification model for untreated BSCMs was developed.

RESULTS In total, 600 patients were included in the study; 417 patients who had been enrolled before July 2015 were divided into the training and validation cohorts, and 183 subsequently enrolled patients were used as the external validation cohort. By applying a backward stepwise procedure in the multivariable Cox model, variables, including prior hemorrhage (HR 1.69), hemorrhage on admission (HR 3.33), lesion size > 1.5 cm (HR 1.84), lesion depth (HR 2.35), crossing the axial midpoint (HR 1.94), and developmental venous anomaly (HR 2.62), were incorporated to develop a nomogram. The Harrell C-index values for a 5-year prospective hemorrhage were 0.752 (95% CI 0.687–0.816), 0.801 (95% CI 0.665–0.936), and 0.758 (95% CI 0.674–0.842) in the training, internal validation, and external validation cohorts, respectively. The nomogram performed well in terms of consistency between prediction and actual observation according to the calibration curve. The patients could be classified into three distinct (low, medium, and high) risk groups using the final score of this nomogram.

CONCLUSIONS Independent predictors of the 5-year hemorrhage risk in untreated BSCMs were selected to create the first nomogram for predicting individual prospective hemorrhage. The nomogram was able to stratify patients into different risk groups and assist in clinical decision-making.

Microsurgical clipping and endovascular management of unruptured anterior circulation aneurysms: how age, frailty, and comorbidity indexes influence outcomes

J Neurosurg 138:922–932, 2023

Frailty is one of the important factors in predicting the outcomes of surgery. Many surgical specialties have adopted a frailty assessment in the preoperative period for prognostication; however, there are limited data on the effects of frailty on the outcomes of cerebral aneurysms. The object of this study was to find the effect of frailty on the surgical outcomes of anterior circulation unruptured intracranial aneurysms (UIAs) and compare the frailty index with other comorbidity indexes.

METHODS A retrospective study was performed utilizing the National Inpatient Sample (NIS) database (2016–2018). The Hospital Frailty Risk Score (HFRS) was used to assess frailty. On the basis of the HFRS, the whole cohort was divided into low-risk (0–5), intermediate-risk (> 5 to 15), and high-risk (> 15) frailty groups. The analyzed outcomes were nonhome discharge, complication rate, extended length of stay, and in-hospital mortality.

RESULTS In total, 37,685 patients were included in the analysis, 5820 of whom had undergone open surgical clipping and 31,865 of whom had undergone endovascular management. Mean age was higher in the high-risk frailty group than in the low-risk group for both clipping (63 vs 55.4 years) and coiling (64.6 vs 57.9 years). The complication rate for open surgical clipping in the high-risk frailty group was 56.1% compared to 0.8% in the low-risk group. Similarly, for endovascular management, the complication rate was 60.6% in the high-risk group compared to 0.3% in the low-risk group. Nonhome discharges were more common in the high-risk group than in the low-risk group for both open clipping (87.8% vs 19.7%) and endovascular management (73.1% vs 4.4%). Mean hospital charges for clipping were $341,379 in the high-risk group compared to $116,892 in the low-risk group. Mean hospital charges for coiling were $392,861 in the high-risk frailty group and $125,336 in the low-risk group. Extended length of stay occurred more frequently in the highrisk frailty group than in the low-risk group for both clipping (82.9% vs 10.7%) and coiling (94.2% vs 12.7%). Frailty had higher area under the receiver operating characteristic curve values than those for other comorbidity indexes and age in predicting outcomes.

CONCLUSIONS Frailty affects surgical outcomes significantly and outperforms age and other comorbidity indexes in predicting outcome. It is imperative to include frailty assessment in preoperative planning.

Surgical treatment of brain arteriovenous malformations: clinical outcomes of patients included in the registry of a pragmatic randomized trial

The Treatment of Brain Arteriovenous Malformations Study (TOBAS) is a pragmatic study that includes 2 randomized trials and registries of treated or conservatively managed patients. The authors report the results of the surgical registry.

METHODS TOBAS patients are managed according to an algorithm that combines clinical judgment and randomized allocation. For patients considered for curative treatment, clinicians selected from surgery, endovascular therapy, or radiation therapy as the primary curative method, and whether observation was a reasonable alternative. When surgery was selected and observation was deemed unreasonable, the patient was not included in the randomized controlled trial but placed in the surgical registry. The primary outcome of the trial was mRS score > 2 at 10 years (at last follow-up for the current report). Secondary outcomes include angiographic results, perioperative serious adverse events, and permanent treatment-related complications leading to mRS score > 2.

RESULTS From June 2014 to May 2021, 1010 patients were recruited at 30 TOBAS centers. Surgery was selected for 229/512 patients (44%) considered for curative treatment; 77 (34%) were included in the surgery versus observation randomized trial and 152 (66%) were placed in the surgical registry. Surgical registry patients had 124/152 (82%) ruptured and 28/152 (18%) unruptured arteriovenous malformations (AVMs), with the majority categorized as low-grade SpetzlerMartin grade I–II AVM (118/152 [78%]). Thirteen patients were excluded, leaving 139 patients for analysis. Embolization was performed prior to surgery in 78/139 (56%) patients. Surgical angiographic cure was obtained in 123/139 all-grade (89%, 95% CI 82%–93%) and 105/110 low-grade (95%, 95% CI 90%–98%) AVM patients. At the mean follow-up of 18.1 months, 16 patients (12%, 95% CI 7%–18%) had reached the primary safety outcome of mRS score > 2, including 11/16 who had a baseline mRS score ≥ 3 due to previous AVM rupture. Serious adverse events occurred in 29 patients (21%, 95% CI 15%–28%). Permanent treatment-related complications leading to mRS score > 2 occurred in 6/139 patients (4%, 95% CI 2%–9%), 5 (83%) of whom had complications due to preoperative embolization.

CONCLUSIONS The surgical treatment of brain AVMs in the TOBAS registry was curative in 88% of patients. The participation of more patients, surgeons, and centers in randomized trials is needed to definitively establish the role of surgery in the treatment of unruptured brain AVMs.

Long-term outcomes after surgery for brainstem cavernous malformations: analysis of 46 consecutive cases

J Neurosurg 138:900–909, 2023

The objective of this study was to evaluate the long-term outcomes after resection of brainstem cavernous malformations (BSCMs) and to assess the usefulness of the Lawton grading system in these cases.

METHODS This retrospective study analyzed 46 consecutive patients with BSCMs operated on between July 1990 and December 2020. Outcomes at the last follow-up were defined as favorable (modified Rankin Scale [mRS] score 0–2) or unfavorable (mRS score > 2).

RESULTS The study cohort comprised 24 men (52%) and 22 women (48%), ranging in age from 8 to 78 years old (median 37 years). In 19 patients (41%), the preoperative mRS score was > 2. All patients had hemorrhagic BSCM. There were 12 (26%) mesencephalic, 19 (41%) pontine, 7 (15%) medullary, and 8 (17%) cerebellar peduncle lesions, with a maximal diameter ranging from 5 to 40 mm (median 15 mm). In total, 24 BSCMs (52%) had bilateral extension crossing the brainstem midline. Lawton grades of 0, I, II, III, IV, V, and VI were defined in 3 (7%), 2 (4%), 10 (22%), 11 (24%), 8 (17%), 7 (15%), and 5 (11%) cases, respectively. Total resection of BSCMs was attained in 43 patients (93%). There were no perioperative deaths. Excluding the 3 most recent cases, the length of follow-up ranged from 56 to 365 months. The majority of patients demonstrated good functional recovery, but regress of the preexisting oculomotor nerve deficit was usually incomplete. No new hemorrhagic events were noted after total resection of BSCMs. In 42 patients (91%), the mRS score at the time of last follow-up was ≤ 2 (favorable outcome), and in 18 (39%), it was 0 (absence of neurological symptoms). Forty-four patients (96%) demonstrated clinical improvement and 2 (4%) had no changes compared with the preoperative period. Multivariate analysis revealed that only lower Lawton grade had a statistically significant independent association (p = 0.0280) with favorable long-term outcome. The area under the receiver operating characteristic curve for prediction of favorable outcome with 7 available Lawton grades of BSCM was 0.93.

CONCLUSIONS Resection of hemorrhagic BSCMs by an experienced neurosurgeon may be performed safely and effectively, even in severely disabled patients. In the authors’ experience, preexisting oculomotor nerve palsy represents the main cause of permanent postoperative neurological morbidity. The Lawton grading system effectively predicts longterm outcome after surgery.

Seven bypasses simulation set: description and validity assessment of novel models for microneurosurgical training

J Neurosurg 138:732–739, 2023

Microsurgical training remains indispensable to master cerebrovascular bypass procedures, but simulation models for training that accurately replicate microanastomosis in narrow, deep-operating corridors are lacking. Seven simulation bypass scenarios were developed that included head models in various surgical positions with premade approaches, simulating the restrictions of the surgical corridors and hand positions for microvascular bypass training. This study describes these models and assesses their validity.

METHODS Simulation models were created using 3D printing of the skull with a designed craniotomy. Brain and external soft tissues were cast using a silicone molding technique from the clay-sculptured prototypes. The 7 simulation scenarios included: 1) temporal craniotomy for a superficial temporal artery (STA)–middle cerebral artery (MCA) bypass using the M4 branch of the MCA; 2) pterional craniotomy and transsylvian approach for STA-M2 bypass; 3) bifrontal craniotomy and interhemispheric approach for side-to-side bypass using the A3 branches of the anterior cerebral artery; 4) far lateral craniotomy and transcerebellomedullary approach for a posterior inferior cerebellar artery (PICA)–PICA bypass or 5) PICA reanastomosis; 6) orbitozygomatic craniotomy and transsylvian-subtemporal approach for a posterior cerebral artery bypass; and 7) extended retrosigmoid craniotomy and transcerebellopontine approach for an occipital artery–anterior inferior cerebellar artery bypass. Experienced neurosurgeons evaluated each model by practicing the aforementioned bypasses on the models. Face and content validities were assessed using the bypass participant survey.

RESULTS A workflow for model production was developed, and these models were used during microsurgical courses at 2 neurosurgical institutions. Each model is accompanied by a corresponding prototypical case and surgical video, creating a simulation scenario. Seven experienced cerebrovascular neurosurgeons practiced microvascular anastomoses on each of the models and completed surveys. They reported that actual anastomosis within a specific approach was well replicated by the models, and difficulty was comparable to that for real surgery, which confirms the face validity of the models. All experts stated that practice using these models may improve bypass technique, instrument handling, and surgical technique when applied to patients, confirming the content validity of the models.

CONCLUSIONS The 7 bypasses simulation set includes novel models that effectively simulate surgical scenarios of a bypass within distinct deep anatomical corridors, as well as hand and operator positions. These models use artificial materials, are reusable, and can be implemented for personal training and during microsurgical courses.

Risk of intracranial aneurysm recurrence after microsurgical clipping based on 3D digital subtraction angiography

J Neurosurg 138:717–723, 2023

Current knowledge of recurrence rates after intracranial aneurysm (IA) surgery relies on 2D digital subtraction angiography (DSA), which fails to detect more than 75% of small aneurysm remnants. Accordingly, the discrimination between recurrence and growth of a remnant remains challenging, and actual assessment of recurrence risk of clipped IAs could be inaccurate. The authors report, for the first time, 3D-DSA–based long-term durability and risk factor data of IA recurrence and remnant growth after microsurgical clipping.

METHODS Prospectively collected data for 305 patients, with a total of 329 clipped IAs that underwent baseline 3DDSA, were evaluated. The incidence of recurrent IA was described by Kaplan-Meier curves. Risk factors for IA recurrence were analyzed by multivariable Cox proportional hazards and logistic regression models.

RESULTS The overall observed proportion of IA recurrence after clipping was 2.7% (9 of 329 IAs) at a mean followup of 46 months (0.7% per year). While completely obliterated IAs did not recur during follow-up, incompletely clipped aneurysms (76 of 329) demonstrated remnant growth in 11.8% (3.4% per year). Young age and large initial IA size significantly increased the risk of IA recurrence.

CONCLUSIONS The findings support those in previous studies that hypothesized that completely clipped IAs have an extremely low risk of recurrence. Conversely, the results highlight the significant risk posed by incompletely clipped IAs. Young patients with initial large IAs and incomplete obliteration have an especially high risk for IA recurrence and therefore should be monitored more closely.

A system of anatomical triangles defining dissection routes to brainstem cavernous malformations

J Neurosurg 138:768–784, 2023

Anatomical triangles defined by intersecting neurovascular structures delineate surgical routes to pathological targets and guide neurosurgeons during dissection steps. Collections or systems of anatomical triangles have been integrated into skull base surgery to help surgeons navigate complex regions such as the cavernous sinus. The authors present a system of triangles specifically intended for resection of brainstem cavernous malformations (BSCMs). This system of triangles is complementary to the authors’ BSCM taxonomy that defines dissection routes to these lesions.

METHODS The anatomical triangle through which a BSCM was resected microsurgically was determined for the patients treated during a 23-year period who had both brain MRI and intraoperative photographs or videos available for review.

RESULTS Of 183 patients who met the inclusion criteria, 50 had midbrain lesions (27%), 102 had pontine lesions (56%), and 31 had medullary lesions (17%). The craniotomies used to resect these BSCMs included the extended retrosigmoid (66 [36.1%]), midline suboccipital (46 [25.1%]), far lateral (30 [16.4%]), pterional/orbitozygomatic (17 [9.3%]), torcular (8 [4.4%]), and lateral suboccipital (8 [4.4%]) approaches. The anatomical triangles through which the BSCMs were most frequently resected were the interlobular (37 [20.2%]), vallecular (32 [17.5%]), vagoaccessory (30 [16.4%]), supracerebellar-infratrochlear (16 [8.7%]), subtonsillar (14 [7.7%]), oculomotor-tentorial (11 [6.0%]), infragalenic (8 [4.4%]), and supracerebellar-supratrochlear (8 [4.4%]) triangles. New but infrequently used triangles included the vertebrobasilar junctional (1 [0.5%]), supratrigeminal (3 [1.6%]), and infratrigeminal (5 [2.7%]) triangles. Overall, 15 BSCM subtypes were exposed through 6 craniotomies, and the approach was redirected to the BSCM by one of the 14 triangles paired with the BSCM subtype.

CONCLUSIONS A system of BSCM triangles, including 9 newly defined triangles, was introduced to guide dissection to these lesions. The use of an anatomical triangle better defines the pathway taken through the craniotomy to the lesion and refines the conceptualization of surgical approaches. The triangle concept and the BSCM triangle system increase the precision of dissection through subarachnoid corridors, enhance microsurgical execution, and potentially improve patient outcomes.

Long-term functional independence after minimally invasive endoscopic intracerebral hemorrhage evacuation

J Neurosurg 138:154–164, 2023

Intracerebral hemorrhage (ICH) is a devastating form of stroke with no proven treatment. However, minimally invasive endoscopic evacuation is a promising potential therapeutic option for ICH. Herein, the authors examine factors associated with long-term functional independence (modified Rankin Scale [mRS] score ≤ 2) in patients with spontaneous ICH who underwent minimally invasive endoscopic evacuation.

METHODS Patients with spontaneous supratentorial ICH who had presented to a large urban healthcare system from December 2015 to October 2018 were triaged to a central hospital for minimally invasive endoscopic evacuation. Inclusion criteria for this study included age ≥ 18 years, hematoma volume ≥ 15 ml, National Institutes of Health Stroke Scale (NIHSS) score ≥ 6, premorbid mRS score ≤ 3, and time from ictus ≤ 72 hours. Demographic, clinical, and radiographic factors previously shown to impact functional outcome in ICH were included in a retrospective univariate analysis with patients dichotomized into independent (mRS score ≤ 2) and dependent (mRS score ≥ 3) outcome groups, according to 6-month mRS scores. Factors that reached a threshold of p < 0.05 in a univariate analysis were included in a multivariate logistic regression.

RESULTS A total of 90 patients met the study inclusion criteria. The median preoperative hematoma volume was 41 (IQR 27–65) ml and the median postoperative volume was 1.2 (0.3–7.5) ml, resulting in a median evacuation percentage of 97% (85%–99%). The median hospital length of stay was 17 (IQR 9–25) days, and 8 (9%) patients died within 30 days of surgery. Twenty-four (27%) patients had attained functional independence by 6 months. Factors independently associated with long-term functional independence included lower NIHSS score at presentation (OR per point 0.78, 95% CI 0.67–0.91, p = 0.002), lack of intraventricular hemorrhage (IVH; OR 0.20, 95% CI 0.05–0.77, p = 0.02), and shorter time to evacuation (OR per hour 0.95, 95% CI 0.91–0.99, p = 0.007). Specifically, patients who had undergone evacuation within 24 hours of ictus demonstrated an mRS score ≤ 2 rate of 36% and were associated with an increased likelihood of long-term independence (OR 17.7, 95% CI 1.90–164, p = 0.01) as compared to those who had undergone evacuation after 48 hours.

CONCLUSIONS In a single-center minimally invasive endoscopic ICH evacuation cohort, NIHSS score on presentation, lack of IVH, and shorter time to evacuation were independently associated with functional independence at 6 months. Factors associated with functional independence may help to better predict populations suitable for minimally invasive endoscopic evacuation and guide protocols for future clinical trials.

A quantitative model to differentiate nonaneurysmal perimesencephalic subarachnoid hemorrhage from aneurysmal etiology

J Neurosurg 138:165–172, 2023

OBJECTIVE Nonaneurysmal perimesencephalic subarachnoid hemorrhage (pmSAH) is considered to have a lower-risk pattern than other types of subarachnoid hemorrhage (SAH). However, a minority of patients with pmSAH may harbor a causative posterior circulation aneurysm. To exclude this possibility, many institutions pursue exhaustive imaging. In this study the authors aimed to develop a novel predictive model based on initial noncontrast head CT (NCHCT) features to differentiate pmSAH from aneurysmal causes.

METHODS The authors retrospectively reviewed patients admitted to an academic center for treatment of a suspected aneurysmal SAH (aSAH) during the period from 2016 to 2021. Patients with a final diagnosis of pmSAH or posterior circulation aSAH were included. Using NCHCT, the thickness (continuous variable) and location of blood in basal cisterns and sylvian fissures (categorical variables) were compared between groups. A scoring system was created using features that were significantly different between groups. Receiver operating characteristic curve analysis was used to measure the accuracy of this model in predicting aneurysmal etiology. A separate patient cohort was used for external validation of this model.

RESULTS Of 420 SAH cases, 48 patients with pmSAH and 37 with posterior circulation aSAH were identified. Blood thickness measurements in the crural and ambient cisterns and interhemispheric and sylvian fissures and degree of extension into the sylvian fissure were all significantly different between groups (all p < 0.001). The authors developed a 10-point scoring model to predict aneurysmal causes with high accuracy (area under the curve [AUC] 0.99; 95% CI 0.98–1.00; OR per point increase 10; 95% CI 2.18–46.4). External validation resulted in persistently high accuracy (AUC 0.97; 95% CI 0.92–1.00) of this model.

CONCLUSIONS A risk stratification score using initial blood clot burden may accurately differentiate between aneurysmal and nonaneurysmal pmSAH. Larger prospective studies are encouraged to further validate this quantitative tool.

A taxonomy for brainstem cavernous malformations: subtypes of medullary lesions

J Neurosurg 138:128–146, 2023

Medullary cavernous malformations are the least common of the brainstem cavernous malformations (BSCMs), accounting for only 14% of lesions in the authors’ surgical experience. In this article, a novel taxonomy for these lesions is proposed based on clinical presentation and anatomical location.

METHODS The taxonomy system was applied to a large 2-surgeon experience over a 30-year period (1990–2019). Of 601 patients who underwent microsurgical resection of BSCMs, 551 were identified who had the clinical and radiological information needed for inclusion. These 551 patients were classified by lesion location: midbrain (151 [27%]), pons (323 [59%]), and medulla (77 [14%]). Medullary lesions were subtyped on the basis of their predominant surface presentation. Neurological outcomes were assessed according to the modified Rankin Scale (mRS), with an mRS score ≤ 2 defined as favorable.

RESULTS Five distinct subtypes were defined for the 77 medullary BSCMs: pyramidal (3 [3.9%]), olivary (35 [46%]), cuneate (24 [31%]), gracile (5 [6.5%]), and trigonal (10 [13%]). Pyramidal lesions are located in the anterior medulla and were associated with hemiparesis and hypoglossal nerve palsy. Olivary lesions are found in the anterolateral medulla and were associated with ataxia. Cuneate lesions are located in the posterolateral medulla and were associated with ipsilateral upper-extremity sensory deficits. Gracile lesions are located outside the fourth ventricle in the posteroinferior medulla and were associated with ipsilateral lower-extremity sensory deficits. Trigonal lesions in the ventricular floor were associated with nausea, vomiting, and diplopia. A single surgical approach was preferred (> 90% of cases) for each medullary subtype: the far lateral approach for pyramidal and olivary lesions, the suboccipital-telovelar approach for cuneate lesions, the suboccipital-transcisterna magna approach for gracile lesions, and the suboccipital-transventricular approach for trigonal lesions. Of these 77 patients for whom follow-up data were available (n = 73), 63 (86%) had favorable outcomes and 67 (92%) had unchanged or improved functional status.

CONCLUSIONS This study confirms that the constellation of neurological signs and symptoms associated with a hemorrhagic medullary BSCM subtype is useful for defining the BSCM clinically according to a neurologically recognizable syndrome at the bedside. The proposed taxonomical classifications may be used to guide the selection of surgical approaches, which may enhance the consistency of clinical communications and help improve patient outcomes.

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