A novel radiological classification of midbrain pilocytic astrocytomas and its implication for surgical management

J Neurosurg 140:1527–1539, 2024

Surgery for midbrain pilocytic astrocytoma (PA) remains a formidable challenge. To facilitate decisionmaking and achieve a better outcome in the management of patients with midbrain PA, the authors have proposed a novel radiological classification of midbrain PAs with long-term follow-up.

METHODS Fifty-seven midbrain PA patients who underwent surgery at Beijing Tiantan Hospital, Capital Medical University, from January 2008 to June 2021, were reviewed. Based on tumor location and the topological anatomical change identified on MRI, midbrain PAs were categorized into four types: crural (12/57, 21.1%), tegmental (25/57, 43.9%), aqueductal (5/57, 8.8%), and tectal (15/57, 26.3%) PAs. The relevant clinical, radiological, and pathological data; surgical procedures and results; and long-term outcomes were collected and analyzed.

RESULTS The 1-, 3-, and 5-year survival rates reached 98%, 96%, and 96%, respectively, with gross-total resection achieved in 66.7% of cases, followed by near-total resection in 17.5% cases. The clinical and radiological features, selection of surgical approaches, and long-term postoperative deficits were distinct among each type. Crural PAs were associated with younger age (median 9 years, IQR 5.0–12.8 years); the largest tumor volume (median 31.9 cm 3 , IQR 17.2–42.6 cm 3 ); the lowest preoperative Karnofsky Performance Scale (KPS) score (median 65, IQR 50–70); the most frequent preoperative motor deficit (91.7%); a mixed solid-cystic component (75%); occupation of the crural cistern; elevation and rotation of the thalamus (medial and/or lateral); displacement of the anterior third ventricle, uncus, and anterior commissure; the most diverse surgical approaches; more frequent use of multimodality image–guided surgery (58.3%); and the most remarkable improvement in KPS score at long-term follow-up. Tegmental PAs were associated with adolescents and young adults (median age 21 years, IQR 8–33 years); tumor volume (median 13.9 cm 3 , IQR 9.5–20.5 cm 3 ); a good preoperative KPS score (median 80, IQR 70–80); a mixed solid-cystic component (72%); occupation of the ambient cistern and cerebellomesencephalic fissure; a close relationship with the dorsal pons, superior cerebellar peduncle, and posterior inferior third ventricle; and a higher probability of permanent postoperative sensory deficits (40%). Aqueductal and tectal PAs were associated with small tumor volume (median 9.14 cm 3 , IQR 5.1–17.4 cm 3 and median 11.84 cm 3 , IQR 5.7–18.3 cm 3 , respectively), a higher percentage of hydrocephalus (80% and 86.7%, respectively), and a straightforward selection of limited surgical approaches.

CONCLUSIONS A novel and comprehensive radiological classification of midbrain PAs was established, which will serve as a valuable tool in patient management and promote uniform communication and comparison across different studies and publications.

Expanding the reach of the trans–middle cerebellar peduncle approach: pontine cavernous malformations, tissue transgression beyond the safe entry zone, and the invisible triangle

J Neurosurg 140:1344–1356, 2024

In the authors’ microsurgical experience, the trans–middle cerebellar peduncle (MCP) approach to the lateral and central pons has been the most common approach to brainstem cavernous malformations (BSCMs). This approach through a well-tolerated safe entry zone (SEZ) allows a wide vertical or posterior trajectory, reaching pontine lesions extending into the midbrain, medulla, and pontine tegmentum. Better understanding of the relationships among lesion location, surgical trajectory, and long-term clinical outcomes could determine areas of safe passage.

METHODS A single-surgeon cohort study of all primary trans-MCP BSCM resections was conducted from July 1, 2017, to June 30, 2021. Preoperative and postoperative MR images were independently reviewed by 3 investigators blinded to the intervention, using a standardized rubric to define BSCM regions of interest (ROIs) involved with a lesion or microsurgical tract. Statistical testing, including the chi-square test with the Bonferroni correction, logistic regression, and structural equation modeling, was performed to analyze relationships between ROIs and clinical outcomes.

RESULTS Thirty-one patients underwent primary trans-MCP BSCM resection during the study period. The median age was 50 years (IQR 24–49 years); 19 (61%) patients were female, and 12 (39%) were male. Seven (23%) patients had familial cavernous malformation syndromes. The median follow-up was 9 months (range 6–37 months). At the last follow-up, composite neurological outcomes were favorable: 22 (71%) patients had 0 (n = 12, 39%) or 1 (n = 10, 32%) major persistent deficit, 5 patients (16%) had 2 deficits, 2 (7%) had 3 deficits, and 1 patient each (3%) had 4 or 6 deficits. Unfavorable composite outcomes were significantly associated with lesions (OR 7.14, p = 0.04) or surgical tracts (OR 12.18, p < 0.001) extending from the superior cerebellar peduncle (SCP) into the contralateral medial midbrain. The ipsilateral dorsal pons was the most frequently implicated ROI involving a surgical tract and the development of new postoperative deficits. This region involved the rhomboid pontine territory and transgression of the pontine tegmentum (OR 7.53, p < 0.001). Structural equation modeling supported medial midbrain and pontine tegmentum transgression as the primary drivers of morbidity.

CONCLUSIONS Trans-MCP resection is a safe and effective treatment for BSCMs, including lesions with marked superior or inferior ipsilateral extension. Two trajectories are associated with increased neurological risk: first, a superomedial trajectory to lesions extending into the midbrain that transgresses the SCP, its decussation, or both; and second, a posteromedial trajectory to lesions extending into the pontine tegmentum. The corticospinal tract, SCP, and pontine tegmentum form an invisible triangle within the pontine white matter tolerant of transgression. When the surgeon works within this triangle, most deep pontine BSCMs, including large lesions, those with contralateral or posterior extension, and others extending into the midbrain and medulla, can be resected safely with the trans-MCP approach.

Preserving the cerebellar hemispheric tentorial bridging veins through a novel tentorial cut technique for supracerebellar approaches

J Neurosurg 140:260–270, 2024

OBJECTIVE The objective of this study was to describe the distribution pattern of cerebellar hemispheric tentorial bridging (CHTB) veins on the tentorial surface in a case series of perimedian or paramedian supracerebellar approaches and to describe a novel technique to preserve these veins.

METHODS A series of 141 patients with various pathological processes in different locations was operated on via perimedian or paramedian supracerebellar approaches by the senior author from July 2006 through October 2022 and was retrospectively evaluated. During surgery, the number and locations of all CHTB veins were recorded to establish a distribution map on the tentorial surface, divided into nine zones. Patients were classified into four groups according to the surgical technique used to manage CHTB veins: 1) group 1 consisted of CHTB veins preserved without intervention during surgery or no CHTB veins found in the surgical route; 2) group 2 included CHTB veins coagulated during surgery; 3) group 3 included CHTB veins preserved with arachnoid and/or tentorial dissection from the cerebellar or tentorial surface, respectively; and 4) group 4 comprised CHTB veins preserved using a novel tentorial cut technique.

RESULTS Overall, 141 patients were included in the study. Of these 141 patients, 38 were in group 1 (27%), 32 in group 2 (22.7%), 47 in group 3 (33.3%), and 24 in group 4 (17%). The total number of CHTB veins encountered was 207 during surgeries on one side. According to the distribution zones of the tentorium, zone 5 had the highest density of CHTB veins, while zone 7 had the lowest. Of the patients in group 4, 6 underwent the perimedian supracerebellar approach and 18 had the paramedian supracerebellar approach. There were 39 CHTB veins on the surface of the 24 cerebellar hemispheres in group 4. The tentorial cut technique was performed for 27 of 39 CHTB veins. Twelve veins were not addressed because they did not present any obstacles during approaches. During surgery, no complications were observed due to the tentorial cut technique.

CONCLUSIONS Because there is no way to determine whether a CHTB vein can be sacrificed without complications, it is important to protect these veins in supracerebellar approaches. This new tentorial cut technique in perimedian or paramedian supracerebellar approaches makes it possible to preserve CHTB veins encountered during supracerebellar surgeries.

Microsurgical management of midbrain gliomas: surgical results and long-term outcome in a large, single-surgeon, consecutive series

J Neurosurg 140:104–115, 2024

The authors report on a large, consecutive, single-surgeon series of patients undergoing microsurgical removal of midbrain gliomas. Emphasis is put on surgical indications, technique, and results as well as long-term oncological follow-up.

METHODS A retrospective analysis was performed of prospectively collected data from a consecutive series of patients undergoing microneurosurgery for midbrain gliomas from March 2006 through June 2022 at the authors’ institution. According to the growth pattern and location of the lesion in the midbrain (tegmentum, central mesencephalic structures, and tectum), one of the following approaches was chosen: transsylvian (TS), extreme anterior interhemispheric transcallosal (eAIT), posterior interhemispheric transtentorial subsplenial (PITS), paramedian supracerebellar transtentorial (PST), perimedian supracerebellar (PeS), perimedian contralateral supracerebellar (PeCS), and transuvulotonsillar fissure (TUTF). Clinical and radiological data were gathered according to a standard protocol and reported according to common descriptive statistics. The main outcomes were rate of gross-total resection; extent of resection; occurrence of any complications; variation in Karnofsky Performance Status score at discharge, 3 months, and last follow-up; progression-free survival (PFS); and overall survival (OS).

RESULTS Fifty-four patients (28 of them pediatric) met the inclusion criteria (6 with high-grade and 48 with low-grade gliomas [LGGs]). Twenty-two tumors were in the tegmentum, 7 in the central mesencephalic structures, and 25 in the tectum. In no instance did the glioma originate in the cerebral peduncle. TS was performed in 2 patients, eAIT in 6, PITS in 23, PST in 16, PeS in 4, PeCS in 1, and TUTF in 2 patients. Gross-total resection was achieved in 39 patients (72%). The average extent of resection was 98.0% (median 100%, range 82%–100%). There were no deaths due to surgery. Nine patients experienced transient and 2 patients experienced permanent new neurological deficits. At a mean follow-up of 72 months (median 62, range 3–193 months), 49 of the 54 patients were still alive. All patients with LGGs (48/54) were alive with no decrease in their KPS score, whereas 42 showed improvement compared with their preoperative status.

CONCLUSIONS Microneurosurgical removal of midbrain gliomas is feasible with good surgical results and long-term clinical outcomes, particularly in patients with LGGs. As such, microneurosurgery should be considered as the first therapeutic option. Adequate microsurgical technique and anesthesiological management, along with an accurate preoperative understanding of the tumor’s exact topographic origin and growth pattern, is crucial for a good surgical outcome.

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.

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.

A taxonomy for brainstem cavernous malformations: subtypes of midbrain lesions

J Neurosurg 136:1667–1686, 2022

Anatomical taxonomy is a practical tool that has successfully guided clinical decision-making for patients with brain arteriovenous malformations. Brainstem cavernous malformations (BSCMs) are similarly complex lesions that are difficult to access and highly variable in size, shape, and position. The authors propose a novel taxonomy for midbrain cavernous malformations based on clinical presentation (syndromes) and anatomical location (identified with MRI).

METHODS The taxonomy system was developed and applied to an extensive 2-surgeon experience over a 30-year period (1990–2019). Of 551 patients with appropriate data who underwent microsurgical resection of BSCMs, 151 (27.4%) had midbrain lesions. These lesions were further subtyped on the basis of predominant surface presentation identified on preoperative MRI. Five distinct subtypes of midbrain BSCMs were defined: interpeduncular (7 lesions [4.6%]), peduncular (37 [24.5%]), tegmental (73 [48.3%]), quadrigeminal (27 [17.9%]), and periaqueductal (7 [4.6%]). Neurological outcomes were assessed using modified Rankin Scale (mRS) scores. A postoperative score ≤ 2 was defined as a favorable outcome; a score > 2 was defined as a poor outcome. Clinical and surgical characteristics and neurological outcomes were compared among subtypes.

RESULTS Each midbrain BSCM subtype was associated with a recognizable constellation of neurological symptoms. Patients with interpeduncular lesions commonly presented with ipsilateral oculomotor nerve palsy and contralateral cerebellar ataxia or dyscoordination. Peduncular lesions were associated with contralateral hemiparesis and ipsilateral oculomotor nerve palsy. Patients with tegmental lesions were the most likely to present with contralateral sensory deficits, whereas those with quadrigeminal lesions commonly presented with the features of Parinaud syndrome. Periaqueductal lesions were the most likely to cause obstructive hydrocephalus. A single surgical approach was preferred (> 90% of cases) for each midbrain subtype: interpeduncular (transsylvian-interpeduncular approach [7/7 lesions]), peduncular (transsylvian-transpeduncular [24/37]), tegmental (lateral supracerebellar-infratentorial [73/73]), quadrigeminal (midline or paramedian supracerebellar-infratentorial [27/27]), and periaqueductal (transcallosal-transchoroidal fissure [6/7]). Favorable outcomes (mRS score ≤ 2) were observed in most patients (110/136 [80.9%]) with follow-up data. No significant differences in outcomes were observed between subtypes (p = 0.92).

CONCLUSIONS The study confirmed the authors’ hypothesis that taxonomy for midbrain BSCMs 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 consistency of clinical communications and publications, and improve patient outcomes.

 

 

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

Acta Neurochirurgica (2021) 163:2739–2754

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

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

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

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

The Aqueduct of Sylvius: Applied 3-T Magnetic Resonance Imaging Anatomy and Morphometry With Neuroendoscopic Relevance

Aqueduct of Sylvius MRI morphometry

Neurosurgery 73[ONS Suppl 2]:ons132–ons140, 2013

The aqueduct of Sylvius (AqSylv) is a structure of increasing importance in neuroendoscopic procedures. However, there is currently no clear and adequate description of the normal anatomy of the AqSylv.

OBJECTIVE: To study in detail hitherto unavailable normal magnetic resonance imaging morphometry and anatomic variants of the AqSylv.

METHODS: We retrospectively studied normal midsagittal T1-weighted 3-T magnetic resonance images in 100 patients. We measured widths of the AqSylv pars anterior, ampulla, and pars posterior; its narrowest point; and its length. We recorded angulation of the AqSylv relative to the third ventricle as multiple deviations of the long axis of the AqSylv from the Talairach bicommissural line. We statistically determined age- and sexrelated changes in AqSylv morphometry using the Pearson correlation coefficient. We measured angulation of the AqSylv relative to the fourth ventricle and correlated this to the cervicomedullary angle (a surrogate for head position).

RESULTS: Patients were 13 to 83 years of age (45% male, 55% female). Mean morphometrics were as follows: pars anterior width, 1.1 mm; ampulla width, 1.2 mm; pars posterior width, 1.4 mm; length, 14.1 mm; narrowest point, 0.9 mm; and angulation in relation to the third and fourth ventricles, 26 and 18, respectively. Age correlated positively with width and negatively with length of the AqSylv. There was no correlation between AqSylv alignment relative to the foramen magnum and the cervicomedullary angle.

CONCLUSION: Normative dimensions of the AqSylv in vivo are at variance with published cadaveric morphometrics. The AqSylv widens and shortens with cerebral involution. Awareness of these normal morphometrics is highly useful when stent placement is an option during aqueductoplasty. Reported data are valuable in guiding neuroendoscopic management of hydrocephalus and aqueductal stenosis.

Cavernous Malformations of the Brainstem Presenting in Childhood: Surgical Experience in 40 Patients

Neurosurgery 67:1589–1599, 2010 DOI: 10.1227/NEU.0b013e3181f8d1b2

Brainstem cavernous malformations (BSCMs) are believed to compose 9% to 35% of all cerebral cavernous malformations, but these lesions have been reported in children in very limited numbers.

OBJECTIVE: To review surgical outcomes of pediatric patients with BSCMs treated at 1 institution.

METHODS: We retrospectively analyzed the course of 40 pediatric patients (19 males, 21 females; age range, 10 months to 18.9 years; mean, 12.3 years) who underwent surgery between 1984 and 2009. Age, sex, presenting symptoms, location of lesion, surgical approach, new postoperative deficits, Glasgow Outcome Scale score, recurrences, and resolution of baseline symptoms were recorded.

RESULTS: Thirty-nine patients experienced hemorrhage before surgery. Lesion locations included the pons (n = 22), midbrain (n = 4), midbrain and thalamus (n = 4), pontomesencephalic junction (n = 3), medulla (n = 3), pontomedullary junction (n = 3), and cervicomedullary junction (n = 1). Mean lesion size was 2.3 cm. Mean length of hospital stay was 10.7 days. The average clinical follow-up was 31.9 months in 36 patients with follow-up after discharge. At last follow-up, 5 patients had experienced symptoms and/ or imaging consistent with rehemorrhage, either from a residual that enlarged or true recurrence (5.25% annual rebleed risk per patient after surgery); 2 required reoperation for further resection of cavernoma. Mean Glasgow Outcome Scale score was 4.2 on admission, 4.05 at discharge, and 4.5 at latest follow-up. Preoperative symptoms and deficits improved in 16 patients (40%). New neurological deficits developed in 19 patients (48%) and resolved in 9, leaving 10 patients (25%) with new permanent deficit.

CONCLUSION: Compared with adults, pediatric patients with BCSMs tend to have larger lesions and higher rates of recurrence (regrowth of residual lesion). Given the greater life expectancy of children, surgical treatment seems warranted in those with surgically accessible lesions that have bled. Outcomes were similar to those in our adult series of patients with BSCMs.