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.

Surgical Resection of Deep-Seated Arteriovenous Malformations Through Stereotactically Guided Tubular Retractor Systems

Operative Neurosurgery 24:499–506, 2023

Arteriovenous malformations (AVMs) in the subcortical and/or periventricular regions can cause significant intraventricular and intracranial hemorrhage. These AVMs can pose a unique surgical challenge because traditional, open approaches to the periventricular region require significant cortical/white matter retraction to establish sufficient operative corridors, which may result in risk of neurological injury. Minimally invasive tubular retractor systems represent a novel, feasible surgical option for treating deep-seated AVMs.

OBJECTIVE: To explore 5 cases of NICO BrainPath-assisted resection of subcortical/ periventricular AVMs.

METHODS: Five patients from a single institution were operated on for deep-seated AVMs using tubular retractor systems. Collected data included demographics, AVM specifications, preoperative neurological status, postoperative neurological status, and postoperative/intraoperative angiogram results.

RESULTS: Five patients, ranging from age 10 to 45 years, underwent mini-craniotomy for stereotactically guided tubular retractor-assisted AVM resection using neuronavigation for selecting a safe operative corridor. No preoperative embolization was necessary. Mean maximum AVM nidal diameter was 8.2 mm. All deep-seated AVMs were completely resected without complications. All AVMs demonstrated complete obliteration on intraoperative angiogram and on 6-month follow-up angiogram.

CONCLUSION: Minimally invasive tubular retractors are safe and present a promising surgical option for well-selected deep-seated AVMs. Furthermore, study may elucidate whether tubular retractors improve outcomes after microsurgical AVM resection secondary to mitigation of iatrogenic retraction injury risk.

Reappraisal of Intracerebral Hemorrhages and Intracerebral Hemorrhage Grading Scale Score in Surgically and Medically Managed Cerebellar Intracerebral Hemorrhage

 

Neurosurgery 92:1021–1028, 2023

As compared with supratentorial intracerebral hemorrhages (ICH), bleeds that occur within the cerebellum require special consideration given the nature of the posterior fossa.

OBJECTIVE: To validate ICH and ICH grading scale (ICH-GS) scores in patients with cerebellar hemorrhage and examine the outcomes of patients managed surgically as compared with those who underwent conservative treatment.

METHODS: This observational multicenter study included 475 patients with cerebellar hemorrhage from 9 different neurosurgical departments in Germany between 2005 and 2021. The prognostic accuracy of ICH and ICH-GS scores were calculated by the area under the curve of the receiver operating characteristic curves. Analyzed outcomes were the inhospital mortality, mortality at 6 months, in-hospital outcome, and outcome at 6 months.

RESULTS: Of 403 patients, 252 patients (62.5%) underwent surgical treatment and 151 patients (37.5%) conservative treatment. Both ICH and ICH-GS scores demonstrated good prognostic accuracy regarding both overall mortality and functional outcomes. In those patients presenting with severe cerebellar hemorrhages, ie, ICH score >3 and ICH-GS score >11, overall mortality was significantly lower in surgically treated patients. Mortality was significantly higher in those patients managed surgically who presented with ICH scores ≤3; in such patients, improved outcomes were noted when the hematoma was treated conservatively.

CONCLUSION: ICH and ICH scores are useful tools for prediction of survival and outcome in patients with cerebellar ICH. Surgical management may be beneficial for those who present with severe cerebellar ICH as reflected by ICH scores >3, while conservative management seems reasonable in patients with lower ICH scores.

Endoscopic clipping of an anterior communicating artery aneurysm

Acta Neurochirurgica (2023) 165:1227–1231

Anterior communicating artery aneurysms are most prone to rupture. Surgically, they are conventionally being managed by a pterional approach. Some neurosurgeons prefer a supraorbital keyhole approach in select cases. Fully endoscopic clipping of such aneurysms is seldom described.

Method We clipped an antero-inferiorly directed anterior communicating artery aneurysm endoscopically via a supraorbital keyhole approach. The intraoperative aneurysmal rupture was also managed endoscopically. The patient made an excellent postoperative recovery without any neurological deficits.

Conclusion Select cases of anterior communicating artery aneurysms can be clipped endoscopically using standard instruments and adhering to the basic principles of aneurysm clipping.

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.

The value of intraoperative indocyanine green angiography in microvascular decompression for hemifacial spasm to avoid brainstem ischemia

Acta Neurochirurgica (2023) 165:747–755

Despite being rarely reported, ischemic insults resulting from compromising small brainstem perforators following microvascular decompression (MVD) remain a potential devastating complication. To avoid this complication, we have been using indocyanine green (ICG) angiography intraoperatively to check the flow within the small brainstem perforators. We aim to evaluate the safety and usefulness of ICG videoangiography in MVD.

Methods We extracted retrospective data of patients who received ICG videoangiography from our prospectively maintained database for microvascular decompression. We noted relevant data including demographics, offending vessels, operative technique, outcome, and complications.

Results Out of the 438 patients, 15 patients with a mean age (SD) of 53 ± 10.5 years underwent intraoperative ICG angiography. Male:female was 1:1.14. The mean disease duration prior to surgery was 7.7 ± 5.3 years. The mean follow-up (SD) was 50.7 ± 42.0 months. In 14 patients, the offending vessel was an artery, and in one patient, a vein. Intraoperative readjustment of the Teflon pledget or sling was required in 20% (3/15) of the cases. No patient had any sort of brainstem ischemia. Eighty percent of the patients (12/15) experienced complete resolution of the spasms. 86.7% (13/15) of the patients reported a satisfactory outcome with marked improvement of the spasms. Three patients experienced slight hearing affection after surgery, which improved in two patients later. There was no facial or lower cranial nerve affection.

Conclusion Intraoperative ICG is a safe tool for evaluating the flow within the brain stem perforators and avoiding brainstem ischemia in MVD for hemifacial spasm.

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.

Helsinki style mini‑pterional craniotomy for clipping of middle cerebral artery bifurcation aneurysms

Acta Neurochirurgica (2023) 165:489–493

Different versions of the mini-pterional (MPT) approach have been described often with the idea the smaller the better. Attempts to reduce incision and craniotomy size for better cosmetic results should not be performed at the expense of safety.

Method We present our take on the MPT as a balance between size and safety which can be adopted by vascular neurosurgeons in training. The craniotomy stays within the confines of the superior temporal line and is completely covered by temporal muscle after closure.

Conclusion This approach is cosmetically superior while still offering anatomical familiarity and sufficient instrument maneuverability.

Association of Preoperative Vascular Wall Imaging Patterns and Surgical Outcomes in Patients With Unruptured Intracranial Saccular Aneurysms

Neurosurgery 92:421–430, 2023

MR vascular wall imaging (VWI) may have prognostic value in patients with unruptured intracranial aneurysms (UIAs).

OBJECTIVE: To evaluate the value of VWI as a predictor of surgical outcome in patients with UIAs.

METHODS: This prospective cohort study evaluated surgical outcomes in consecutive patients with UIAs who underwent surgical clipping at a single center. All participants underwent high-resolution VWI and were followed for at least 6 months. The primary clinical outcome was modified Rankin scale (mRS) score 6 months after surgery.

RESULTS: The number of patients in the no wall enhancement, uniformwall enhancement (UWE), and focal wall enhancement (FWE) groups was 37, 145, and 154, respectively. Incidence of postoperative complications was 15.5% in the FWE group, 12.4% in the UWE group, and 5.4% in the no wall enhancement group. The proportion of patients with mRS score >2 at the 6-month follow-up was significantly higher in the FWE group than in the UWE group (14.3% vs 6.9%; P = .0389). In the multivariate analysis, FWE (odds ratio, 2.573; 95% CI 1.001-6.612) and positive proximal artery remodeling (odds ratio, 10.56; 95% CI 2.237-49.83) were independent predictors of mRS score >2 at the 6-month follow-up.

CONCLUSION: Preoperative VWI can improve the surgeon’s understanding of aneurysm pathological structure. Type of aneurysmal wall enhancement on VWI is associated with clinical outcome and incidence of salvage anastomosis and surgical complications.

The risk factors of postoperative infarction after surgical clipping of unruptured anterior communicating artery aneurysms

Acta Neurochirurgica (2023) 165:501–515

An anterior communicating artery is a common location for both ruptured and unruptured intracranial aneurysms, and microsurgery is sometimes necessary for their successful treatment. However, postoperative infarction should be considered during clipping due to the complex surrounding structures of anterior communicating artery aneurysms. This study aimed to evaluate the risk factors of postoperative infarction after surgical clipping of unruptured anterior communicating artery aneurysms and its clinical outcomes.

Methods The data of patients who underwent microsurgical clipping of an unruptured anterior communicating artery aneurysm in our hospital between January 2008 and December 2020 were retrospectively analyzed. The patients’ demographic data, anatomical features of the anterior communicating artery complex and aneurysm, surgical technique, characteristics of postoperative infarction, and its clinical course were evaluated.

Results Notably, among 848 patients, 66 (7.8%) and 34 (4%) patients had radiologic and symptomatic infarctions, respectively. Univariate and multivariate logistic regression analyses showed that hypertension (odds ratio (OR), 1.99; p = 0.022), previous stroke (OR, 3.89; p = 0.009), posterior projection (OR, 5.58; p < 0.001), aneurysm size (OR, 1.17; optimal cut-off value, 6.14 mm; p = 0.002), and skull base-to-aneurysm distance (OR, 1.15; optimal cut-off value, 11.09 mm; p < 0.001) were associated with postoperative infarction. In the pterional approach, a closed A2 plane was an additional risk factor (OR, 1.88; p = 0.041). Infarction of the subcallosal and hypothalamic branches was significantly associated with symptomatic infarction ( p = 0.001).

Conclusion Hypertension, previous stroke, posteriorly projecting aneurysms, aneurysm size, and highly positioned aneurysms are independent risk factors for postoperative infarction during surgical clipping of an unruptured anterior communicating artery aneurysm. Additionally, a closed A2 plane is an additional risk factor of postoperative infarction in patients undergoing clipping via the pterional approach.

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.

The positive impact of cisternostomy with cisternal drainage on delayed hydrocephalus after aneurysmal subarachnoid hemorrhage

Acta Neurochirurgica (2023) 165:187–195

Hydrocephalus is one of the major complications of aneurysmal subarachnoid haemorrhage (aSAH). In the acute setting, an external ventricular drain (EVD) is used for early management. A cisternal drain (CD) coupled with the micro-surgical opening of basal cisterns can be an alternative when the aneurysm is clipped. Chronic hydrocephalus after aSAH is managed with ventriculo-peritoneal (VP) shunt, a procedure associated with a wide range of complications. The aim of this study is to analyse the impact of microsurgical opening of basal cisterns coupled with CD on the incidence of VP shunt, compared to patients treated with EVD.

Methods The authors conducted a retrospective review of 89 consecutive cases of patients with aSAH treated surgically and endovascularly with either EVD or CD between January 2009 and September 2021. Patients were stratified into two groups: Group 1 included patients with EVD, Group 2 included patients with CD. Subgroup analysis with only patients treated surgically was also performed. We compared their baseline characteristics, clinical outcomes and shunting rates.

Results There were no statistically significant differences between the two groups in terms of epidemiological characteristics, WFNS score, Fisher scale, presence of intraventricular hemorrhage (IVH), acute hydrocephalus, postoperative meningitis or of clinical outcomes at last follow-up. Cisternostomy with CD (Group 2) was associated with a statistically significant reduction in VP-shunt compared with the use of an EVD (Group 1) (9.09% vs 53.78%; p < 0.001). This finding was confirmed in our subgroup analysis, as among patients with a surgical clipping, the rate of VP shunt was 43.7% for the EVD group and 9.5% for the CD group (p = 0.02).

Conclusions Cisternostomy with CD may reduce the rate of shunt-dependent hydrocephalus. Cisternostomy allows the removal of subarachnoid blood, thereby reducing arachnoid inflammation and fibrosis. CD may enhance this effect, thus resulting in lower rates of chronic hydrocephalus.

Keywords Cisternostomy · Cisternal drain · External ventricular drain · Aneurysmal subarachnoid haemorrhage · Hydrocephalus · Ventriculo-peritoneal shunt

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.

Chronic Encapsulated Expanding Hematomas After Stereotactic Radiosurgery for Intracranial Arteriovenous Malformations

Neurosurgery 92:195–204, 2023

Stereotactic radiosurgery (SRS) offers a minimally invasive treatment modality for appropriately selected intracranial arteriovenous malformations (AVMs). Recent reports have described the development of rare, delayed chronic encapsulated expanding hematomas (CEEHs) at the site of an angiographically confirmed obliterated AVM.

OBJECTIVE: To elucidate the incidence, characteristics, and management of CEEH in patients with AVM after SRS.

METHODS: The records of all patients who underwent SRS for an intracranial AVM at 4 institutions participating in the International Radiosurgery Research Foundation between 1987 and 2021 were retrospectively reviewed. Data regarding characteristics of the AVM, SRS treatment parameters, CEEH presentation, management, and outcomes were collected and analyzed.

RESULTS: Among 5430 patients, 15 developed a CEEH at a crude incidence of 0.28%. Nine patients were female, and the mean age was 43 ± 14.6 years. Nine patients underwent surgical evacuation, while 6 were managed conservatively. The median CEEH development latency was 106 months after SRS. The patients were followed for a median of 32 months, and 9 patients improved clinically, while 6 patients remained stable. No intraoperative complications were reported after CEEH resection, although 1 patient recovered from postoperative meningitis requiring intravenous antibiotics.

CONCLUSION: CEEH is a rare, late complication of AVM SRS with an incidence of 0.28% and a median latency of 106 months. In the presence of a delayed and symptomatic expanding hematoma in the bed of an angiographically obliterated AVM, surgical resection resulted in clinical improvement in most patients. Conservative management is possible in asymptomatic patients with stable, small-sized hematomas in deeply seated locations.