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

Abstract

OBJECTIVE 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 radiological-microsurgical discordance. Most patients achieved favorable outcomes despite the transgression of eloquent brainstem tissue in and around SEZs.

Treatment Modalities and Outcomes in Brainstem Cavernous Malformations: A Large Multicenter Observational Cohort Study

“…Most existing research on BSCM might be explorations on microsurgical treatment and a compilation of neurosurgeons' personal experiences. 24,[33][34][35][36] A universally recognized treatment protocol is currently lacking. According to the current CCM guidelines, 6 asymptomatic CCMs, particularly those within the brainstem, are not recommended for surgical resection due to potential higher risks of early postoperative mortality, morbidity, and quality-of-life implications.…”

Association of hemorrhage-to-treatment time with outcomes in patients with brainstem cavernous malformations: a nationwide cohort study

“…In recent years, the extensive publications by Professor Lawton detailing the surgical experience with BSCMs, particularly emphasizing the nuances of surgical approach selection, have played a pivotal role in advancing neurosurgical techniques across various centres 26 – 30 . A notable development addressing a longstanding challenge in brainstem surgery is the introduction of the Surgical Entry Zone (SEZ) concept 13 . In contrast to lesions in more superficial locations, the removal of deep-seated lesions carries an elevated risk of compromising brainstem nuclei and fibre tracts, potentially resulting in residual neurological impairments.…”

“…Covariates that affect the prognosis of BSCM and time to treatment were selected from the literatures and clinical experience 13 – 16 . One index of severity based on first in-hospital assessments conducted before any procedures were performed included the modified Rankin Scale (mRS) score.…”

“…Despite previous studies attempting to assess the role of various factors on outcomes, such as patient age, disease severity, lesion features, and complications, there is still a lack of robust evidence regarding the optimal timing of surgery 13 – 16 . Expert opinions suggest that performing surgical resection early yields better results than delayed intervention; however, this concept and the precise timing have not been definitively established through a comprehensive analysis of real-world data 8 .…”

Hemorrhagic Outcome of Brainstem Cavernous Malformations following Radiosurgery: Dose-Response Relationship

“…The 5-year hemorrhage risk has been estimated to range from 18.4% to over 40% [2]. Surgical excision is effective for treating symptomatic hemorrhagic brainstem CMs, but it comes with a notable postoperative hemorrhage rate (ranging from 5.9% [3] to 7.7% [4] per year) and a high surgical morbidity (ranging from 32.5% [ n = 154] [5] to 52.7% [ n = 260] [4]), even when performed by experienced teams. According to the Lawton brainstem CMs grading, a recent study recommended observation as the only treatment for high-grade brainstem CMs to prevent future hemorrhages [6].…”