Natural History of Spinal Cord Cavernous Malformations

Neurosurgery 90:390–398, 2022

The natural history of spinal cord cavernous malformations (SCCMs) remains relatively unclear.

OBJECTIVE: To investigate the natural history for hemorrhagic risks and neurological outcomes, as well as relevant predicting factors, of SCCMs.

METHODS: All patients between 2002 and 2019 with diagnosis of SCCMs were identified retrospectively. An observational study of patients with conservative management was performed to reveal the natural history of SCCMs.

RESULTS: We identified 305 patients in the full cohort, including 126 patients who were conservatively treated for at least 6 months (median observational period, 24.0 months). Forty-five hemorrhage events occurred during 527 person-years of follow-up, yielding an annual hemorrhage rate of 8.5% per person-year. The 1-, 2-, and 5-year cumulative risks of hemorrhage were 13.9%, 26.1%, and 35.1%, respectively. Prior hemorrhage (hazard ratio [HR] = 12.948, P = .012) and pediatric patients (HR = 2.841, P = .031) were independent predictors of hemorrhage in the long-term follow-up. Familial form (adjusted odds ratio [OR] = 30.695, P = .010) and subsequent hemorrhage events (adjusted OR = 16.333, P = .000) were independent risk factors for worsening of neurological function, and baseline neurological status (adjusted OR = 78.984, P = .000) and presence of subsequent hemorrhage (adjusted OR = 9.611, P = .001) were significantly associated with neurological outcomes.

CONCLUSION: The natural history of SCCMs varies. Baseline characteristics, such as pediatric patients, familial form, and baseline neurological status, as well as prior and subsequent hemorrhagic events, significantly affect the natural history of the SCCMs, which prompts a differentiated treatment strategy.

Surgical treatment of pontine cavernous malformations via subtemporal transtentorial and intradural anterior transpetrosal approaches

Neurosurgical Review (2020) 43:1179–1189

The aim of this study was to report our surgical experience on resection of the pontine cavernous malformations (CMs) via subtemporal transtentorial approach (STTA) and intradural anterior transpetrosal approach (ATPA).

Clinical data were retrospectively reviewed in 61 patients with pontine CMs that were surgically treated by the STTA and the intradural ATPA. The surgical procedures, complications, and outcomes were analyzed.

The study consists of 61 patients with a total of 61 pontine CMs. Other than 4 lesions located medially in the pons, all CMs were in the lateral pons with a left or right lateral epicenter (the left/right ratio was 22/35). Totally, 11 patients (18.0%) with lesions located in the upper pons were treated by the STTA, and 50 patients (82.0%) with lesions involving the lower pons were treated by the intradural ATPA. Postoperatively, the complete resection was achieved in 58 patients (95.1%) and incomplete resection in 3 patients (4.9%). Twenty-seven patients (44.3%) suffered from a new or worsened neurological deficit in the immediate postoperative period, and 8 patients (13.1%) encountered a non-neural complication, including rebleeding, cerebrospinal fluid leak, intracranial infection, and pulmonary infection, and 3 patients had contusion of temporal lobe. With a mean follow-up of 54.2 months, the patients’ neurological condition had improved in 43 cases (71.6%), not changed in 10 cases (16.7%), and worsened in 7 cases (11.7%), respectively. The Karnofsky Performance Scale (KPS) score evaluated at the last time for per patient was significantly better than their baseline status (t = 6.677, p < 0.001). However, 21 patients (35.0%) suffered from a new or worsened persistent postoperative deficit.

The lateral and anterolateral pons can be exposed well by the subtemporal transtentorial and intradural anterior transpetrosal approaches. Lesions of CMs located in the lateral pons, including ventrolateral and dorsolateral pons, could be totally removed by these two lateral approaches with an acceptable surgical morbidity.

Utility of a Quantitative Approach Using Diffusion Tensor Imaging for Prognostication Regarding Motor and Functional Outcomes in Patients With Surgically Resected Deep Intracranial Cavernous Malformations

Neurosurgery 86:665–675, 2020

Resection of deep intracranial cavernous malformations (CMs) is associated with a higher risk of neurological deterioration and uncertainty regarding clinical outcomes.

OBJECTIVE: To examine diffusion tractography imaging (DTI) data evaluating the corticospinal tract (CST) in relation to motor and functional outcomes in patients with surgically resected deep CMs.

METHODS: Perilesional CST was characterized as disrupted, displaced, or normal. Mean fractional anisotropy (FA) values were obtained for whole ipsilateral CST and in 3 regions: subcortical (proximal), perilesional, and distally. Mean FA values in anatomically equivalent regions in the contralateral CST were obtained. Clinical and radiological data were collected independently.Multivariable regression analysis was used for statistical analysis.

RESULTS: A total of 18 patients [brainstem (15) and thalamus/basal ganglia (3); median follow-up: 270 d] were identified over 2 yr. The CST was identified preoperatively as disrupted (6), displaced (8), and normal (4). Five of 6 patientswith disruption hadweakness. Higher preoperative mean FA values for distal ipsilateral CST segmentwere associated with better preoperative lower (P < .001), upper limb (P = .004), postoperative lower (P = .005), and upper limb (P < .001) motor examination. Preoperative mean FA values for distal ipsilateral CST segment (P = .001) and contralateral perilesional CST segment (P < .001) were negatively associated with postoperative modified Rankin scale scores.

CONCLUSION: Lower preoperative mean FA values for overall and defined CST segments corresponded to worse patient pre- and postoperative motor examination and/or functional status. FA value for the distal ipsilateral CST segment has prognostic potential with respect to clinical outcomes.

Brainstem Cavernous Malformations: Surgical Indications Based on Natural History and Surgical Outcomes

World Neurosurg. (2018) 110:55-63

Cavernous malformations (CMs) are uncommon lesions occurring in the central nervous system, with an incidence of approximately 0.5% in the general population and constituting 5%e10% of all intracranial vascular malformations. Among CMs, prevalence within the brainstem as reported in the literature has ranged from 4% to 35%. With their precarious location and potentially devastating clinical events, brainstem CMs have attracted attention from neurosurgeons, and with these surgeons’ unrelenting efforts, the microsurgical techniques to treat these lesions in the brainstem have greatly improved in recent decades. Although surgical outcomes reported in the literature have been satisfying, surgical intervention has become increasingly contraindicated because of the tendency for a benign clinical course in brainstem CMs, after weighing this fact against the high risk of surgical morbidity. Thus, it is advisable to operate on patients with symptomatic lesions abutting the pial or ependymal surface of the brainstem or where lesions are accessible to safe entry zones, which have caused more than 1 significantly symptomatic hemorrhage and can be defined as aggressive. However, treatment remains controversial for deep-seated lesions away from the surface of the brainstem or lesions that are inaccessible to safe entry zones. Other treatments, such as radiosurgery and medication, are still debatable, which might be as an alternative for lesions amenable to but at high risk with surgery.

Comparison of Outcome Between Surgical and Conservative Management of Symptomatic Spinal Cord Cavernous Malformations

Comparison of Outcome Between Surgical and Conservative Management of Symptomatic Spinal Cord Cavernous Malformations

Neurosurgery 78:552–561, 2016

Intramedullary cavernous malformations (CMs) are rare lesions with unclear natural history.

OBJECTIVE: To compare the functional outcomes of spinal CMs managed surgically and conservatively.

METHODS: We performed a retrospective study of patients diagnosed with intramedullary CMs seen at our institution from 2006 to 2013. Functional outcomes of patients were assessed by treatment modality with the Modified McCormick Scale and Karnofsky Performance Status.

RESULTS: We identified a total of 85 study-eligible patients; 51 (60.0%) were male. Mean age of patients was 40.5 years. Fifty-eight patients underwent microsurgical removal, and 27 patients underwent conservative management. All patients except 1 harbored a single symptomatic intramedullary CM. Mean follow-up time was 42.8 months. For the surgical group (n = 58), 51 CMs were completely resected. During the follow-up period, 40 patients (69.0%) within the surgical group had improvement in neurological state, 16 patients (27.6%) remained unchanged, and 2 patients (3.4%) experienced deteriorated functional status. In the conservative group, 4 patients (14.8%) had improvement of their symptoms, 19 patients (70.4%) remained in baseline, and 4 patients (14.8%) deteriorated. No significant statistical difference was observed in followup Karnofsky Performance Status assessment (odds ratio = 0.89; 95% confidence interval = 0.73-1.08; P = .15) or Modified McCormick Scale assessment (odds ratio = 0.90; 95% confidence interval = 0.74-1.10; P = .30) after adjustment for preoperative lesion size and location. Annual hemorrhagic risk was 3.9% in conservatively managed patients. In contrast, no patients experienced subsequent hemorrhages after surgical resection.

CONCLUSION: Surgical resection of intramedullary CMs eliminates the risk of subsequent hemorrhagic and may achieve satisfactory outcome when patients are carefully selected. Although conservative management is recommended in patients at high surgical risk, they should be closely monitored because of persistent hemorrhagic risk.

The utility of preoperative diffusion tensor imaging in the surgical management of brainstem cavernous malformations

The utility of preoperative diffusion tensor imaging in the surgical management of brainstem cavernous malformations

J Neurosurg 122:653–662, 2015

Resection of brainstem cavernous malformations (BSCMs) may reduce the risk of stepwise neurological deterioration secondary to hemorrhage, but the morbidity of surgery remains high. Diffusion tensor imaging (DTI) and diffusion tensor tractography (DTT) are neuroimaging techniques that may assist in the complex surgical planning necessary for these lesions. The authors evaluate the utility of preoperative DTI and DTT in the surgical management of BSCMs and their correlation with functional outcome.

Methods A retrospective review was conducted to identify patients who underwent resection of a BSCM between 2007 and 2012. All patients had preoperative DTI/DTT studies and a minimum of 6 months of clinical and radiographic follow-up. Five major fiber tracts were evaluated preoperatively using the DTI/DTT protocol: 1) corticospinal tract, 2) medial lemniscus and medial longitudinal fasciculus, 3) inferior cerebellar peduncle, 4) middle cerebellar peduncle, and 5) superior cerebellar peduncle. Scores were applied according to the degree of distortion seen, and the sum of scores was used for analysis. Functional outcomes were measured at hospital admission, discharge, and last clinic visit using modified Rankin Scale (mRS) scores.

Results Eleven patients who underwent resection of a BSCM and preoperative DTI were identified. The mean age at presentation was 49 years, with a male-to-female ratio of 1.75:1. Cranial nerve deficit was the most common presenting symptom (81.8%), followed by cerebellar signs or gait/balance difficulties (54.5%) and hemibody anesthesia (27.2%). The majority of the lesions were located within the pons (54.5%). The mean diameter and estimated volume of lesions were 1.21 cm and 1.93 cm3, respectively. Using DTI and DTT, 9 patients (82%) were found to have involvement of 2 or more major fiber tracts; the corticospinal tract and medial lemniscus/medial longitudinal fasciculus were the most commonly affected. In 2 patients with BSCMs without pial presentation, DTI/DTT findings were important in the selection of the surgical approach. In 2 other patients, the results from preoperative DTI/DTT were important for selection of brainstem entry zones. All 11 patients underwent gross-total resection of their BSCMs. After a mean postoperative follow-up duration of 32.04 months, all 11 patients had excellent or good outcome (mRS Score 0–3) at the time of last outpatient clinic evaluation. DTI score did not correlate with long-term outcome.

Conclusions Preoperative DTI and DTT should be considered in the resection of symptomatic BSCMs. These imaging studies may influence the selection of surgical approach or brainstem entry zones, especially in deep-seated lesions without pial or ependymal presentation. DTI/DTT findings may allow for more aggressive management of lesions previously considered surgically inaccessible. Preoperative DTI/DTT changes do not appear to correlate with functional postoperative outcome in long-term follow-up.

Contralateral Interhemispheric Approach to Deep-Seated Cavernous Malformations

Contralateral Interhemispheric Approach to Deep-Seated Cavernous Malformations (1)

Neurosurgery 75:80–86, 2014

Deep-seated periventricular cavernous malformations of the basal ganglia or thalamus can be approached via an interhemispheric craniotomy. OBJECTIVE: To determine surgical efficacy and clinical outcomes of the contralateral interhemispheric approach.

METHODS: Retrospective chart review was performed on patients undergoing an interhemispheric approach for the resection of deep-seated cavernous malformation by the senior author (R.F.S.) between 2005 and 2013. Demographic data and clinical outcomes were reviewed. Pre- and postoperative imaging were analyzed for lesion location, size, associated venous anomaly, proximity to ventricle, and presence of residual.

RESULTS: Twenty-one patients underwent a contralateral interhemispheric-transventricular approach, 7 patients had a contralateral interhemispheric-transcingulate approach and 3 patients had a contralateral interhemispheric-transchoroidal approach. Mean age was 40.1 years, and the majority were female (58.1%). Mean maximum cavernoma diameter was 1.97 cm, and 43.8% reached the surface of the ventricle. Average follow-up was 8.9 months, with complete resection achieved in 96.8% of patients. At last follow-up, 61.3% of patients remained stable and 29.0% had improved. Of the patients, 6.5% experienced transient weakness that resolved at last follow-up, and 1 patient (3.2%) had short-term memory problems. There were no surgical mortalities.

CONCLUSION: The contralateral interhemispheric approach is a safe, clinically well tolerated, and surgically efficacious approach to deep-seated cavernomas.

Flexible Omnidirectional Carbon Dioxide Laser as an Effective Tool for Resection of Brainstem, Supratentorial, and Intramedullary Cavernous Malformations

Ponto-mesencephalic cavernoma

Operative Neurosurgery 10:34–45, 2014

Lasers have a long history in neurosurgery, yet bulky designs and difficult ergonomics limit their use. With its ease of manipulation and multiple applications, the OmniGuide CO2 laser has reintroduced laser technology to the microsurgical resection of brain and spine lesions. This laser, delivered through a hollow-core fiber lined with a unidirectional mirror, minimizes energy loss and allows precise targeting.

OBJECTIVE: To analyze resections performed by the senior author from April 2009 to March 2013 of 58 cavernous malformations (CMs) in the brain and spine with the use of the OmniGuide CO2 laser, to reflect on lessons learned from laser use in eloquent areas, and to share data on comparisons of laser power calibration and histopathology.

METHODS: Data were collected from electronic medical records, radiology reports, operative room records, OmniGuide CO2 laser case logs, and pathology records.

RESULTS: Of 58 CMs, approximately 50% were in the brainstem (30) and the rest were in supratentorial (26) and intramedullary spinal locations (2). Fifty-seven, ranging from 5 to 45 mm, were resected, with a subtotal resection in 1. Laser power ranged from 2 to 10 W. Pathology specimens showed minimal thermal damage compared with traditionally resected specimens with bipolar coagulation.

CONCLUSION: The OmniGuide CO2 laser is safe and has excellent precision for the resection of supratentorial, brainstem, and spinal intramedullary CMs. No laser-associated complications occurred, and very low energy was used to dissect malformations from their surrounding hemosiderin-stained parenchymas. The authors recommend its use for deep-seated and critically located CMs, along with traditional tools.

Cavernous Malformation of Brainstem, Thalamus, and Basal Ganglia: A Series of 176 Patients


Neurosurgery 72:573–589, 2013

Cavernous malformations (CMs) in deep locations account for 9% to 35% of brain malformations and are surgically challenging.

OBJECTIVE: To study the clinical features and outcomes following surgery for deep CMs and the complication of hypertrophic olivary degeneration (HOD).

METHODS: Clinical records, radiological findings, operative details, and complications of 176 patients with deep CMs were reviewed retrospectively.

RESULTS: Of 176 patients with 179 CMs, 136 CMs were in the brainstem, 27 in the basal ganglia, and 16 in the thalamus. Cranial nerve deficits (51.1%), hemiparesis (40.9%), numbness (34.7%), and cerebellar symptoms (38.6%) presented most commonly. Hemorrhage presented in 172 patients (70 single, 102 multiple). The annual retrospective hemorrhage rate was 5.1% (assuming CMs are congenital with uniform hemorrhage risk throughout life); the rebleed rate was 31.5%/patient per year. Surgical approach depended on the proximity of the CM to the pial or ependymal surface. Postoperatively, 121 patients (68.8%) had no new neurological deficits. Follow-up occurred in 170 patients. Delayed postoperative HOD developed in 9/134 (6.7%) patients with brainstem CMs. HOD occurred predominantly following surgery for pontine CMs (9/10 patients). Three patients with HOD had palatal myoclonus, nystagmus, and oscillopsia, whereas 1 patient each had limb tremor and hemiballismus. At follow-up, 105 patients (61.8%) improved, 44 (25.9%) were unchanged, and 19 (11.2%) worsened neurologically. Good preoperative modified Rankin Score (98.2% vs 54.5%, P = .001) and single hemorrhage (89% vs 77.3%, P , .05) were predictive of good longterm outcome.

CONCLUSION: Symptomatic deep CMs can be resected with acceptable morbidity and outcomes. Good preoperative modified Rankin Score and single hemorrhage are predictors of good long-term outcome.

Supracerebellar Infratentorial Approach to Cavernous Malformations of the Brainstem: Surgical Variants and Clinical Experience With 45 Patients

Neurosurgery 66:389-399, 2010. DOI: 10.1227/01.NEU.0000363702.67016.5D

OBJECTIVE: The supracerebellar infratentorial (SCIT) approach can be performed at the midline (median variant), lateral to the midline (paramedian variant), or at the level of the angle formed by the transverse and sigmoid sinuses (extreme lateral variant). We analyzed our experience with SCIT approaches for the surgical treatment of cavernous malformations of the brainstem (CMBs).

METHODS: Demographic, clinical, radiologic, and surgical data from 45 patients (20 males and 25 females; mean age, 36.2 years) with CMBs surgically removed through SCIT approaches were reviewed retrospectively. Anatomic information was explored using cadaver head dissection.

RESULTS: Twenty-three lesions were in the midbrain, 3 were at the midbrain and extended to the thalamus, 9 were at the pontomesencephalic junction, and 10 were in the upper pons. All patients presented with hemorrhage. The median variant was used in 13 patients, the paramedian variant in 9, and the extreme lateral variant in 23. Intraoperatively, all CMBs were associated with a developmental venous anomaly. At last follow-up, 88% of the patients were the same or better. After a mean follow-up of 20 months, their mean Glasgow Outcome Scale score was 4.1.

CONCLUSION: SCIT approaches provide excellent exposure to CMBs located at the posterior incisural space, not only in the midline but also in the posterolateral surface of the upper pons and midbrain. Careful preoperative planning and neuronavigational assistance are needed to determine the best angle of attack and trajectory for SCIT approaches. Refined microsurgical techniques are paramount to achieve safe surgical removal of CMBs with good outcomes.