Surgical Resection of Cavernous Malformations of the Brainstem: Evolution of a Minimally Invasive Technique
Jeffrey C. Mai, Dinesh Ramanathan, Louis J. Kim, Laligam N. Sekhar

Key words Ⅲ Brainstem Ⅲ Cavernoma Ⅲ Cavernous malformation Ⅲ Skull base Abbreviations and Acronyms CMB: Cavernous malformation of the brainstem Gd: Gadolinium mRS: Modified Rankin scale MR: Magnetic resonance
Department of Neurosurgery, University of Washington School of Medicine, Seattle, Washington, USA To whom correspondence should be addressed: Laligam N. Sekhar, M.D. [E-mail:] Citation: World Neurosurg. (2013) 79, 5/6:691-703. Supplementary digital content available online. Journal homepage: Available online: 1878-8750/$ - see front matter © 2013 Published by Elsevier Inc.

Ⅲ OBJECTIVE: The purpose of this study is to provide an institutional retrospective review of surgically treated brainstem cavernous malformations. Ⅲ METHODS: Between 2005 and 2010, 22 consecutive patients with brainstem cavernous malformations (15 female and 7 male) with a mean age of 43 years underwent surgical treatment. Mean volume of the resected cavernous malformations was 0.65 cm3. A minimally invasive resection technique was used for these cases, in conjunction with skull base approaches. Ⅲ RESULTS: The mean follow-up period was 26.6 months (range, 4-68 months). Of the 22 patients, 9% did not have clear evidence of hemorrhage at the time of presentation. Of the remainder, 22% had two or more instances of hemorrhage documented by magnetic resonance imaging. After resection and during follow-up, 54% of patients had an improvement in their modified Rankin scale, whereas 14% were worse compared with their preoperative presentation; 32% were unchanged and 9% of patients were found to have residual cavernoma post-surgery. Ⅲ CONCLUSION: Our longitudinal experience has guided us to emphasize minimally invasive approaches during resection of the brainstem cavernous malformations, occasionally at the expense of achieving a complete resection, to improve patient outcomes.

INTRODUCTION Cavernous malformations (cavernomas) have an estimated prevalence of approximately 0.4% to 0.8% in the population (4, 25, 29, 37, 38, 40, 43), with approximately 40% discovered incidentally (28). Prospective observation has indicated an overall symptomatic rate of hemorrhage of 0.22% to 0.7% per year for these lesions (15, 26, 37). Nevertheless, data from cavernous malformations situated in the brainstem suggest a markedly greater propensity for bleeding. In retrospective analyses of patients with such lesions, a calculated annual average symptomatic hemorrhage rate of 2.7% to 5% and re-hemorrhage rate of 21% to 60% per year and per lesion was discovered (1, 14, 23, 25, 27, 33). In accordance with their location, hemorrhages of brainstem cavernous malformations carried with them a high level of morbidity and mortality (14, 23). Given the significant risk of death and disability presented by expectant manage-

ment of cavernous malformations of the brainstem (CMBs), surgical resection has been increasingly advocated for therapy (2, 13, 14, 16, 33, 39, 42). Over this timeframe, imaging technologies have significantly improved (5, 10-12, 43), and surgical techniques have been refined for approaching lesions of the brainstem (6, 13, 14, 24, 25, 32, 35, 39, 42). Here, we report our case series of 22 surgically treated brainstem cavernomas, their presentation, and outcomes, as well as describe the general principles guiding surgical resection.

cords were retrospectively reviewed, including outpatient, clinical, and surgical records and radiologic imaging. Diagnostic workup for all patients included magnetic resonance (MR) studies, usually with computed tomography scans at the time of initial presentation as well as Table 1. Deficits at Time of Presentation
Deficit CN deficit Ataxia % 77 59 55 41 27 27 23 14

PATIENTS AND METHODS From 2005 to 2010, 22 consecutive patients underwent 27 procedures for resections of brainstem cavernous malformations. Of these patients, 7 were men and 15 women, with a mean age of 43 years (SD 15 years; range, 8-69 years). Patients were drawn from Harborview Medical Center at the University of Washington in Seattle. Patient re-

Headache Diplopia Weakness Sensory changes Vertigo or dizziness Dysphagia
CN, cranial nerve.

WORLD NEUROSURGERY 79 [5/6]: 691-703, MAY/JUNE 2013



2 0. Postoperative nerve SSEP responses left arm weakness and hydrocephalus showed a marked decline.1016/j. BAEPs the pial unchanged surface 5 mm Anterolateral midbrain SEPs. Post-operative wound Partial right CN III and infection. BAEPs surface to superior colliculus unchanged F 60 Mesencephalic Transpetrosal 1.85 M 57 Mesencephalic Orbitozygomatic 0.3 Just Lateral midbrain beneath pial surface Left tibial and left median Somnolence.05 Entry Corridor Intraoperative Neurophysiology SEPs. SEPs. pneumonia. Mild right CN VI palsy. and right hemibody numbness.2012. nausea. CEREBROVASCULAR JEFFREY C. ataxia. MEPs. Headache. inferior SEPs. Follow. BAEPs unchanged Multiple hemorrhages in past with rebleed and worsening of diplopia. headaches. M 8 Mesencephalic Occipital transtentorial 0. Postoperative Symptoms Left hemiparesis.04.Pre Post up mRS mRS Recurrence? 20 32 4 2 2 1 No No 23 Mesencephalothalamic Orbitozygomatic 50 Mesencephalic Lateral supracerebellar At pial Lateral midbrain surface Just Dorsal lateral beneath midbrain pial surface At pial Lateral midbrain surface M 58 Mesencephalic Lateral supracerebellar 1. dizziness. managed conservatively. No impairment in work. BAEPs unchanged Right MEPs transiently decreased. Diplopia.3 At pial Anterolateral surface midbrain Severe headache. Mild left limb numbness. Diplopia resolved. MEPs. Diplopia resolved. requiring shunt No change in MEPs or placement. now stable. Persistent left hemiparesis. http://dx. diplopia. gait ataxia. M 37 Mesencephalic Orbitozygomatic 0.48 At pial Anterolateral surface midbrain F 38 Mesencephalic Orbitozygomatic 1. BAEPs unchanged Preoperative Symptoms Left hemiparesis. left hyperreflexia. emesis. Headaches persistent. MEPs. Post-operative jaw malocclusion. able to ambulate with assistance.Table 2. Headache. BAEPs unchanged SEPs. gait 25 2 1 No 12 1 0 No WORLD NEUROSURGERY. Right hemibody numbness slightly worse than pre-op.08 At pial Tectal plate. BAEPs unchanged F 60 Mesencephalic Orbitozygomatic 0. 692 www. left hemibody numbness. diplopia. MEPs. Right hemiparesis improved. with improvement. SEPs and BAEPs unchanged. Vertigo.2 Beneath Medial crus cerebri SEPs. and diplopia improved on follow-up. Surgical Approaches to Brain Stem Cavernous Malformations Sex Age F F Location Approach Volume. dysphagia. headache. MEPs.SCIENCEDIRECT. impaired tandem gait. MAI ET AL.wneu.1 SEPs. diplopia resolved. Diplopia on extreme lateral gaze without functional impairment. MEPs. Requiring nursing home care.doi.030 4 4 4 No RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM 11 1 1 No 21 2 2 No 22 2 1 No PEER-REVIEW REPORTS 24 1 1 No . Aspiration BAEPs. Tremor and dysphagia resolved. gait ataxia. MEPs. tremors. ’syncopal’ events. Right ptosis CN VI palsy. cm3 Depth 1. right hemiparesis. minor headaches.

MEPs. Improved to baseline. diplopia and weakness. diplopia. Persistent left CN VI palsy. hemiparesis. transpetrosal 2. Deep venous thrombosis. MEPs. dizziness. requiring right gold weight. Post-operative wound infection. 24 1 4 No F 24 Pontomesencephalic Subtemporal 0. now progressively worsening. gait ataxia. 12 1 1 No F 42 Pontine Suboccipital 0. dysphagia. Just Pontomesencephalic SEPs. neuropathic pain. MEPs. Diplopia resolved. Severe headaches. MEPs. Right hyperacusis and left limb coordination F 40 Pontomesencephalic Suboccipital 0. Left CN VI palsy. Right CN V1 decreased sensation and diminished right corneal reflex. Headaches. left dysmetria. MAY/JUNE 2013 www.56 Dysarthria. Left hearing loss. palsy. BAEPs beneath junction unchanged pial surface Just Mid-ventral pons beneath pial surface 6 mm 1) Lateral pons. 32 2 3 No PEER-REVIEW REPORTS F 43 Pontine Transpetrosal 0. Headaches resolved.JEFFREY C. BAEPs anterior to unchanged trigeminal root entry zone 21 4 0 No M 39 Pontomesencephalic Combined transtemporal. gait ataxia. left Left hemibody central hemipareis. MEPs. BAEPs unchanged 2) Transient changes in the left BAEP and right thenar MEP with recovery at closing. Persistent diplopia. BAEPs unchanged 7 3 1 No F 45 Pontine Combined transtemporal. Left CN V numbness. Two previous hemorrhages with left facial and hemibody numbness. headaches. severe headaches. transpetrosal Transmaxillarytransclival 0. MAI ET AL. diplopia. Gait ataxia. vertigo. Hydrocephalus diplopia. Numbness of the right face. MEPs and BAEPs unchanged. Left numbness unchanged. Left hemibody numbness.13 At pial Floor of the fourth SEPs. BAEPs surface ventricle.38 51 2 1 Yes M 35 Pontine 1) Retrosigmoid 2) Presigmoid.0 At pial Posterior to Poor to absent cortical surface trigeminal root entry SEPs on left consistent zone with pre-operative left hemibody numbness. left Resolution of prehemibody numbness and operative symptoms. ataxia. MEPs unchanged from baselines.44 At pial Posterolateral surface midbrain Right SEPs declined to 40% of baseline.84 Just beneath pial surface Superior and SEPs.WORLDNEUROSURGERY. WORLD NEUROSURGERY 79 [5/6]: 691-703. BAEPs beneath to trigeminal root unchanged pial entry zone surface 27 2 1 No 693 Continues CEREBROVASCULAR . No motor weakness and mild left dysmetria. headaches. requiring shunt. anterior to CN VII/ VIII root entry zone 2) More posterior and inferior approach to same region SEPs. Lightheadedness.07 1) SEPs. aspiration pneumonia. Feeding tube placement. superior to unchanged facial colliculus Left torsional nystagmus. Transsigmoid 0. Cerebrospinal fluid leak requiring lumbar drain. Nursing home for care. MEPs. dizziness.32 Just Posterior and inferior SEPs. 65 4 2 No RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM F 69 Pontine 0. Right CN VI and VII gait ataxia.

CMB volumes are calculated as a volume of a sphere.030 24 3 4 No 7 3 3 No 52 3 0 No 12 1 0 No RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM PEER-REVIEW REPORTS . BAEPs unchanged M 8 Medullary Suboccipital 0. MEPs. mRS. Persistent CN VI and III palsies. M 67 Medullary Suboccipital 0. male. female.04.7 1) SEPs. inferior to unchanged facial colliculus and medial to vagal trigone Details of the 22 patients included in this study are arranged by location of the cavernomas. F. floor of fourth ventricle lateral to striae medullaris Dizziness. as well as the neurophysiology monitoring details.14 Entry Corridor Intraoperative Neurophysiology Preoperative Symptoms Postoperative Symptoms 33 Pontine 15 mm Inferior and posterior SEPs.Pre Post up mRS mRS Recurrence? 68 3 1 No 24 4 4 Yes WORLD NEUROSURGERY. right. 694 Follow. somatosensory-evoked potentials. ataxia. MEPs. Headaches improved. MEPs. BAEP. Previous attempted resection.Mild left hemiparesis. left Persistent ataxia and hemiplegia. gait ataxia and coordination problems. dysarthria. MEP. with the results expressed as cubic centimeters. with the follow-up period listed in months. Diplopia resolved. BAEPs ventricle.16 Just Inferior cerebellar beneath peduncle pial surface At pial Floor of fourth surface ventricle. nausea. lateral to vagal trigone SEPs. Tracheostomy and gastrostomy postoperatively from previous dural arteriovenous fistula resection. modified Rankin scale. BAEPs to trigeminal root unchanged entry zone Just Lateral midbrain beneath pial surface Severe headaches. ’syncopal’ events. M. Where two operations have been performed. brainstem auditory-evoked potentials. Headaches. MEPs. BAEPs unchanged severe dysarthria.60 5 mm Anterolateral medulla. gait ataxia. http://dx. Impaired tandem gait. Left hemiparesis and left hemisensory loss. Left facial droop and vocal hoarseness. sided facial numbness. emesis.01 SEPs. F 57 Medullary 1) Subtemporal. dysphonia. bilateral CN VI and CN III palsies. tremors. they are indicated as 1) and 2) for both the approach. Numbness in bilateral upper extremities. headaches. Continued www. CEREBROVASCULAR JEFFREY C.06 Just beneath pial surface Floor of fourth SEPs. Preoperative mRS values (Pre-mRS) and results at follow-up are included (Post-mRS). left facial numbness. diplopia. Left upper extremity weakness. cm3 Depth 0. F 30 Pontine 1) Transpetrosal 2) Supracerebellar transtentorial 2. diplopia. facial paralysis.Table 2. infratentorial 2) Suboccipital 0. Wheelchair bound. motor-evoked potentials.2012. Wheelchair bound.wneu. Vertigo. Dysequilibrium. ataxia. MAI ET AL.doi.1016/j. minor headaches. titubation. Right greater than left dysmetria. BAEPs Three previous unchanged 2) SEPs. Pancerebellar ataxia. right-sided numbness of tongue. SEP. operations. emesis and right arm Sex Age F Location Approach Transpetrosal Volume. F 37 Medullary Suboccipital 0. Dysphagia. Residual or recurrent cavernomas discovered upon follow-up are listed in the Recurrence column. BAEPs unchanged Headaches. 1) Left upper extremity MEP decline to 20% of baseline value 2) Loss of left tibial SEP. MEPs.

as shown in Table 2. Three-month postoperative axial T2-weighted image demonstrating gross total resection (D). including brainstem auditory evoked responses. The mean volume of these lesions was 0. Intraoperative bilateral somatosensory and motor-evoked potentials were combined with cranial nerve monitoring. Case 1: CMB situated in the right midbrain peduncle. RESULTS Preoperative History All patients who were included in this study were symptomatic from their brainstem cavernomas. 24. and 19% in the medulla (Table 2). range. that is. with coregistration to the operating microscope used whenever possible. 35% in the pons. The volume of the lesions was calculated by estimating the volume of an ellipsoid (4/3 ϫ ␲ ϫ 1/2 sagittal diameter ϫ 1/2 axial diameter ϫ 1/2 coronal diameter) as determined by MR measurements. Follow-up information included outpatient neurologic examinations and calls to patients and their relatives. 64% of the patients had a single bleed at the time of presentation. with a standard deviation of 0. The approach is WORLD NEUROSURGERY 79 [5/6]: 691-703. 35). Red overlay depicts the operative corridor available for resection of the lesion via a right orbitozygomatic osteotomy approach. post-gadolinium (Gd) enhancement views demonstrate the location of the lesion. Patient outcomes pre. with one of these individuals undergoing separate surgical procedures for their CMBs.WORLDNEUROSURGERY. and 22% had sustained two or more hemorrhages by the time they were taken to the operating room. Episodes of hemorrhage related to the cavernomas were confirmed by an acute change in neurologic examination in correspondence with MR findings suggestive of acute bleeding (T2 hypointensity) (39). The three patients who did not have a clearly documented recent hemorrhage with acute neurologic deterioration were offered surgery because their lesions appeared to come to the surface of the brain stem on Surgical Approaches A broad range of approaches was used during surgical resection of brainstem cavernomas. sagittal (B).6 months (SD 18 months. MAI ET AL. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM MR imaging.PEER-REVIEW REPORTS JEFFREY C. Suspected episodes of bleeding in the past not confirmed by MR imaging were excluded from the calculations. 7. 4-68 months) was obtained. identified either on preoperative workup or intraoperatively. The remainder of lesions spanned multiple brainstem regions. 34). Minimal Access Technique The entry to the brainstem cavernoma is made through a pial opening if the lesion points to the surface through a defined “safe entry zone” ( 695 CEREBROVASCULAR . All lesions were resected under frameless stereotaxy. A total of 55% of patients presented with headache. many of which associated with diplopia (41%). as well as direct stimulation (44). cerebral angiography. the “minimal access” technique. The primary aim of surgery was to provide safe resection of the lesion through as small an access point through the brainstem as possible. A mean follow-up time of 26. and coronal (C) T1-weighted. Figure 1.65 cm3.69 cm3.and postsurgery and during long-term follow-up were assessed by use of the modified Rankin scale (mRS) (8. only three patients did not have an overt hemorrhage before coming to medical attention (Table 1). were left extant during surgery (2). 35). These numbers are generally in keeping with other previously published data (2. The vast majority presented with cranial nerve deficits (77%). Axial T2-weighted (A). Approaches were chosen to maximize exposure with as little brain retraction as possible as well as facilitate ready entry through brainstem ’safe’ entry zones (6. On the basis of MR findings in conjunction with patient reports of neurologic deterioration. MAY/JUNE 2013 www. 39. 21. 31% of cavernomas were located in the midbrain. Developmental venous anomalies associated with these cavernomas. In this series. Multiple cavernomas were found in six patients (27%). 42).

because the risk of seizures triggered by these residual tissues is nonexistent. in conjunction with neuroanatomical landmarks. Intraoperative neuronavigation is indispensable in delineating the entry approach. and gradually progressing to the margins. especially with large lesions. Solid portions of the cavernoma are removed piecemeal. coronal (B). including one mesencephalothalamic and three Figure 3.SCIENCEDIRECT.030 . 31% of the cavernomas were mesencephalic. Case 2: left tectal plate cavernous malformation. best determined with careful consideration of the anatomy and any available additional imaging information. Red overlay depicts the operative approach via a left occipital transtentorial approach. http://dx. and 19% were located in the medulla (Table 2). Care is taken to remove all of the cavernoma elements while preserving any major veins or en passage arteries.PEER-REVIEW REPORTS JEFFREY C. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM CEREBROVASCULAR Figure 2. any liquefied hematoma is drained. Operative Results A total of 27 operative procedures were performed for the 22 patients in the series for their brainstem cavernomas. Sagittal (A). Most cavernomas are removed in three to five pieces. Four lesions were large enough to span adjoining until the lesion is completely removed (Video 1). Case 3: left lateral supracerebellar infratentorial approach (red transparent overlay) to dorsal midbrain cavernoma. Vigorous removal of the gliotic. hemosiderin-stained margin of the cavernoma is not attempted. The incision into the brainstem and the tract are kept as narrow as possible until the cavernoma is reached.1016/j. MAI ET AL. 35% were pontine. Once inside the cavernoma.2012. and axial (C) T2-weighted images and axial T2weighted image 14 months postoperatively (D) demonstrating no obvious residual cavernoma. Sagittal T1weighted post-Gd (A) and axial T2-weighted preoperative (B) and postoperative scans at 2 months (C). 696 www. depending on their size and WORLD NEUROSURGERY. starting centrally. such as diffusion tensor imaging.

Case 4. Case 5. Case 1. and weakness with two symptomatic hemorrhages from a right middle cerebellar peduncle cavernous malformation (Figure 4).WORLDNEUROSURGERY. We approached the lesion by a lateral supracerebellar infratentorial approach. and gait ataxia. MAY/JUNE 2013 www. ataxia. A 43-year-old woman presented with right V1-V3 facial numbness. we found these fibers to be medially displaced. she has progressed from an mRS 4 to an mRS 2 with persistence of her mild left-sided weakness. She developed transient left facial weakness and worsening of her left hemiparesis postoperatively. mRS 1.PEER-REVIEW REPORTS JEFFREY C. WORLD NEUROSURGERY 79 [5/6]: 691-703. dysphagia. The tectal plate cavernoma was in the right peduncle. and at 1 year. Red overlay illustrates a right transpetrosal approach. ataxia. In this aches. Because the lesion was located in the midline and did not clearly reach the surface. patient has resolution of diplopia but slight worsening of right body numbness. residual cavernoma was identified on post-operative imaging. transtentorial approach using frameless stereotaxy (Figure 2). No postoperative mortality was observed in this series. Case 2. Case 3. (D) Axial T2-weighted image at 10-month postoperative follow-up. Nevertheless. and vomiting year-old woman developed and was found to have at least left hemiparesis with distal weakness seven supra. At 27 months postoperatively. In 9% of patients.and infratentorial cavernous greater than proximal in the arms in legs malformations. and no further surgeries were required in these patients. she is able to drive a vehicle. As her cavernoma was situated orrhage on MR imaging. affords an excellent work- Figure 4. Pons. confirming that entry from a lateral approach would be safest. left dysmetria. In this case. Three-dimensional diffusion tensor imaging demonstrates medial displacement of rostralcaudal fibers with cavernoma coming to surface of the lateral pons (C). we opted for a right transpetrosal approach for the lesion. diffusion tensor imaging was used during preoperative planning to map the direction of displaced tracts in a rostral-caudal axis. MAI ET AL. nausea. A 58-year-old man with known history of CMB and multiple hemorrhages presented with rebleed accompanied by diplopia. a transfacial LeFort I maxillotomy was used. as illustrated in Figure 5. At 20 months after the procedure. ral orbitozygomatic approach was undertaken (Figure 1). mRS 2. although technically demanding. mRS 0. This approach. right hemibody numbness. including the largest in the (graded 4/5) and hyperreflexia on the ipsitectum. This 23WORLDNEUROSURGERY. T2-weighted sagittal (A) and axial (B) images. her diplopia had 697 CEREBROVASCULAR . RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM approached via a left occipital. which had evidence of recent hemlateral side. An 8-year-old boy presented with vertigo. but she has developed a right diminished corneal reflex and slightly worsened V1-V3 numbness. Case 4: CMB located in the right cerebellar peduncle. The cavernoma was located on the left dorsal mesencephalon (Figure 3). we opted for a transmaxillaryϪtransclival approach. left hemibody numbness and weakness (4/5). A 91% gross total resection rate was achieved. and vertigo with a central pontine hemorrhage secondary to a cavernoma (Figure 5). and her mRS improved from a 2 to a 1. with a clivectomy performed with neuronavigation used to guide the trajectory directly to the lesion. As the lesion came to the surface. and another in the medulla. A 69-year-old woman presented with acute onset of headache. In comparing the side of the brainstem with the cavernoma to the contralateral unaffected side. gross total resection was possible. headVideo available at Midbrain. with new postoperative diplopia noted at 2 months follow-up. diplopia. At 25 months follow-up. as assessed by serial MR imaging. Given the location. a right frontotempopontomesencephalic cavernomas. he was asymptomatic.

followed by application of DuraSeal (Confluent Surgical Inc.030 . Of the 9% of patients with residual brainstem cavernomas. A 37-year-old woman presented with baseline disequilibrium and previous subtotal resection of dorsal medullary brainstem cavernoma by another neurosurgeon. left hemibody numbness. http://dx. including the basilar artery and its associated paramedian perforators. ing view of the ventral pontine surface.1016/ During this WORLD NEUROSURGERY. An additional two layers of fascia were applied to the outside. and gait disturbance was found to have a left lateral pontine hemorrhage as the result of underlying cavernoma (Figure 6). 39. At present. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM Case 7. and truncal ataxia. After resection. both of these patients have declined reoperation. CEREBROVASCULAR Figure 5. a right transpetrosal and presigmoid approach was used for extirpation of the lesion. Her mRS improved from 2 to 1 at 44 months’ follow-up.. Massachusetts. As shown in Figure 7. ventral pontine cavernoma approached via a transmaxillary-transclival approach (red transparent overlay). no instances of rehemorrhage were recorded. it represents the most direct pathway to the lesion. dizziness. including numbness in her right arm. For deeper seated lesions. 54% of patients were noted to improve compared with their preoperative status. New York. 14% of patients had declined compared with their preoperative status. A far lateral retrosigmoid approach was used. At 7 months postoperatively. the patient had improved from an mRS of 3 to an mRS of 1 and reported improving numbness on the left side and mild left dysmetria. The distribution of preoperative mRS and long-term mRS is shown in Figure 9.04.PEER-REVIEW REPORTS JEFFREY C. and the sphenoid rostrum was covered with a mucosal flap. where the cavernous malformation was observed to come to the surface. the basilar artery was moved gently aside.wneu. MAI ET AL. In general. USA). A 57-year-old man who developed sudden onset of headache. At 42 months’ follow-up. A left subtemporal approach with zygomatic osteotomy was used to gain access to the lateral pons. exposing a small area of discoloration in the midline representing the cavernoma’s emergence at the surface of the pons. Here. thereby facilitating their preservation. Case 5: Midline. Case 8.doi. the patient had improved from an mRS score of 2 to an mRS of 1. the defect in the clival dura was repaired with placement of two pieces of abdominal fascia beneath the inner surface of dura. she has now made a complete recovery (mRS 0). A 39-year-old man with two previous hemorrhages of a right dorsal lateral pontine cavernoma re-presented with progressive left facial droop. and axial (C) images. T1-weighted post-Gd sagittal (A). and difficulty breathing. without the need to traverse normal brainstem tissue to reach the lesion. A right frontal external ventriculostomy drain was placed at the time of surgery to minimize risk of CSF leak and was weaned by postoperative day 9. a second bleed or progressive neurologic deficit necessitates surgical extirpation of the brainstem cavernoma because it suggests the propensity of the 698 www. intermittent dysphagia. Case 6. Medulla. whereas 32% remained generally unchanged from a neurologic standpoint. In addition. She represented with sudden deterioration.2012. New York. secured again with a layer of DuraSeal and Gelfoam (Pfizer. Waltham.SCIENCEDIRECT. (D) T2-weighted axial scan at 3-year follow-up. and gross total resection was achieved (Figure 8). we are willing to delay surgical management of these lesions after a single bleeding ictus unless the patient’s cardiac or neurologic instability necessitates emergent evacuation or the lesion clearly abuts the pial or ependymal surface on T1-weighted MR imaging (18. USA). DISCUSSION Indications for Removal The vast majority of brainstem cavernous malformations come to attention after a hemorrhage. Long-Term Outcomes During the course of follow-up. coronal (B). At 22 months’ follow up. 42).

we advocate surgical resection as the primary means for treatment for high-risk cavernomas of the brainstem. as the resultant postoperative complications of nystagmus and internuclear ophthalmoplegia. It is incumbent upon the surgeon to recognize the normal anatomy of the region WORLD NEUROSURGERY 79 [5/6]: 691-703. From a posterior 699 CEREBROVASCULAR . Broadly. 21. we advocate carefully tailoring the surgical approach to each individual’s lesion. a suboccipital or occipital transtentorial approach can be used to reach lesions centered near the posterior midbrain. Complicating this situation is the paucity of widely used and reliable intraoperative methods to identify these displaced and distorted structures. when the blood products will undergo liquefaction (13. 17). Fluid-attenuated inversion recovery sagittal (A). MAY/JUNE 2013 www. Slightly more laterally. as well as take into careful consideration the distortion in surrounding anatomy that can arise as a result of the lesion as well as associated hemorrhage. pons. carefully weighing the risk of morbidity from surgery compared with that of future re-hemorrhage. The use of radiosurgery for cavernous malformations has been reported. With regard to timing of surgery after a hemorrhage. Case 6: Left. an extended transsylvian corridor is used. Approaches to the Brainstem Unlike with supratentorial cavernous malformations. Through experience. MAI ET AL. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM surrounding the cavernomas.WORLDNEUROSURGERY. remains controversial. The pons is the largest region of the brainstem and the most common location for Figure 6. with the assistance of an orbitozygomatic craniotomy (18). lateral pontine cavernoma with a left subtemporal approach with zygomatic osteotomy depicted with the red overlay. 18. Pons. although some surgeons advocate delaying surgery until the subacute phase. midline approaches through the tectal plate should be avoided whenever possible given their postoperative morbidity. entry at the lateral mesencephalic sulcus may be used to avoid injuring oculomotor and trochlear nuclei and the medial longitudinal fasciculus situated more medially (17. T1weighted post-Gd coronal (B). those associated with CMBs present a special challenge to the surgeon due to the presence of surrounding brainstem nuclei and tracts (7. Given the eloquence of the brainstem. waiting much beyond the first several weeks risks development of gliosis. respectively. tips the balance in favor of surgical intervention (18). Unless the cavernoma comes clearly to the pial surface. depending on the location of the cavernomas. including those of the brainstem. 39). Midbrain. In the anteromedial approach for interpeduncular lesions. a subtemporal approach can be used. and posterior. we and others have learned that avoidance of injury to the central tegmentum and adjacent medial longitudinal fasciculus is vital. lesion to rebleed in the future. This is especially true if deep-seated lesions can be approached through “safe entry” corridors. and medulla. 24. are particularly debilitating during recovery (17). In these instances. As with others. The midbrain is subdivided into three general approaches: anteromedial. 35). 35). The supracollicular and infracollicular lines that delineate the rostral and caudal extent of the lamina quadrigemina represent other potential corridors of entry along the midline (9. As such. the direction of approach may not always be optimally defined as the shortest path from the surface to the lesion. with mixed results (27. and T2-weighted axial preoperative (C) and 22 months postoperative (D) images. the use of radiosurgery as a primary treatment modality for cavernous malformations. or in combination with a transsylvian route (31). even a thin parenchymal layer overlying the cavernoma can harbor critical tracts. lateral. 30). which may hinder complete resection. Otherwise. we have subcategorized approaches to the brainstem with respect to the midbrain. a supracerebellar-infratentorial or petrosal approach can be used to reach mesencephalic cavernomas. At present. including the tectal plate. on the basis of the natural history of these lesions. 17.PEER-REVIEW REPORTS JEFFREY C. Laterally. Posteriorly.

it is paramount to minimize dividing the vermis given associated complications. We prefer more lateral or anterolateral approaches to the WORLD NEUROSURGERY.SCIENCEDIRECT. The anterior and anterolateral brainstem tracts are generally more resilient to surgical manipulation than the dorsal pontine and medullary surfaces. which involves dividing the cerebellomedullary fissure. facial. T1-weighted post-Gd sagittal (C). including truncal ataxia (44). and hypoglossal nuclei are carefully established intraoperatively by direct stimulation. and abducens nerve are common when operating along this region (3. 45) or retrosigmoid approach will enable access to the more anterior surface of the pons (16. a midline suboccipital approach can be used. 7. a subtonsillar-transcerebellomedullary (telovelar) approach can be used (13.doi. In such cases. Case 7: Right transpetrosal and presigmoid approach (red overlay) to a right dorsal lateral pontine cavernoma. despite the published morphometric descriptions of safe entry zones in the infra. 22. 33. We have defined approaches to the pons into four categories: dorsal. MAI ET AL. From any of these approaches. http://dx.and supra-abducental or facial regions (6.PEER-REVIEW REPORTS JEFFREY C. 42). 18. injury to the medial longitudinal fasciculus. and postoperative 3-month T2-weighted axial image (D). central. From a dorsal approach. and lateral. it may be difficult to avoid the intrinsic portion of the facial nerve tract or the abducens nucleus when resecting cavernomas in immediate vicinity. A transpetrosal (19. a “safe entry zone. following along the plane of the fibers. anterolateral. 18. T2-weighted axial (B).04. 33). As with others (13. depending on the precise location of the cavernous malformation (Table 2).org/10. the peritrigeminal area. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM Figure 7. view of the pons (20). This triangular region is bound medially by the CEREBROVASCULAR 700 www.wneu.2012. we view the floor of the fourth ventricle with great caution when approaching CMBs.1016/j. 24). Alternately.” can be accessed and safely traversed horizontally. 17. 44). albeit more direct. T1-weighted post-Gd axial (A). These lesions can be approached if the locations of the facial. Unfortunately. vagal. Intraoperative image demonstrating bimanual removal of cavernoma through a small portal in the brainstem (E) and image after gross total resection (F). This approach is useful in accessing pontomedullary and medullary lesions. 44). unless the cavernoma clearly emerges at the surface of the floor of the fourth ventricle. Given its size. Nevertheless. Postsurgical brainstem tract and nucleus-related complications have been reduced as we have shifted away from posterior approaches to the pons over time. 31. 31). particularly when dealing with deep-seated lesions of the pons. a variety of surgical approaches are available to the surgeon. A presigmoid approach will yield a more lateral. brainstem cavernomas (13.030 .

PEER-REVIEW REPORTS JEFFREY C. If there is no option. along the inferior floor of the fourth ventricle. and axial preoperative (C). Intraoperative cranial nerve monitoring is generally more important for dorsal approaches. and 3 year postoperative (D) images shown. Furthermore. 31). respectively. This was not used in our series due to the absence of any cases requiring it. pyramidal tract. so that the corridor for entry through the brainstem may not be as apparent. motor-evoked potentials are obligatory.6 months with a range of 2-68 months. 31). anterior. SD of 17. 18. MAI ET AL. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM the posterior intermediate and posterior lateral sulci (9. which prevents adequate tractography. 44). Medulla. which does not result in clinically evidence deficits (35). 17. Evolution of a Minimally Invasive Resection Technique Once the decision has been made to proceed with resection. It is performed when lesions do not appear to come to the pial surface on MR imaging. and laterally just medial to the root entry zone of cranial nerve V (35). risk of injury to the nucleus of XII medially and the nucleus X laterally with resultant ipsilateral tongue weakness and cardiac/respiratory instability. comparing the contralateral side tracts as a point of reference and compensating for anticipated displacement of the tracts on the ipsilateral side can be helpful. makes entry from this direction generally contraindicated (13. Intraoperatively. Finally. Generally. strictly anterior cavernomas of the ventral medulla can be reached via a transoral route (36. we have used diffusion tensor imaging to study the distortion of the underlying white matter tracts surrounding the lesion (11). When possible. Case 8: Suboccipital approach (red transparent overlay) to cavernous malformation of the dorsal medulla previously with subtotal resection. 33). a far lateral retrosigmoid approach will suffice for reaching pontomedullary lesions (13). Figure 8. For the lower dorsal medulla. Cavernomas situated directly on the ventral midline surface of the pons require a central approach. a midline suboccipital craniotomy with a telovelar approach can be used to reach the dorsal medullary surface (17. T2-weighted sagittal (A). careful preoperative planning is essential. the medial longitudinal fasciculus underlies these structures medially. From either approach. For these difficult. safe medullary access is realized by way of entry through the retro-olivary sulcus. As with the pons. safe entry zones are defined by Bricolo as the posterior median fissure and Figure 9. real-time guidance with frameless stereotaxy registered to the operating microscope WORLD NEUROSURGERY 79 [5/6]: 691-703. The utility of such imaging can be limited by susceptibility artifact when one is resecting a relatively fresh hemorrhage. in such cases. Mean follow-up time was 26. but fortunately rare. lesions. we advocate a transmaxillary-transclival approach. In the upper dorsal 701 CEREBROVASCULAR . In each case. Bar graph showing the distribution of the preoperative mRS scores for the 22 patients compared with the distribution at last follow-up. an alternative is the subtemporal infratemporal approach for these lesions (41). coronal (B). inferiorly by the pontomedullary sulcus out to the flocculus. 17). MAY/JUNE 2013 www. For anterior and lateral approaches to the brainstem. the guiding principle is to avoid breaching major brainstem tracts or nuclei.7 months. The medulla can be approached from the following routes: dorsal. then traversing the most accessible route to the brainstem cavernoma must then be chosen on a caseby-case basis. An extreme far lateral approach with the resection of the jugular tubercle (the transtubercular approach) will enable access to the anterolateral lesions originating in the medulla down to the upper cervical spinal cord (18. which we used during the resection of one of our pontine cavernomas in our series (Table 2). and anterolateral corridors.WORLDNEUROSURGERY. Nevertheless. Because of the concern for CSF leak and associated infection.

wneu.403-414discussion 414-405. instead selecting operative corridors that are directed more laterally and anteriorly to the brainstem. Massachusetts. Steinberg. there have been two recurrences after surgery: both were managed REFERENCES 1. Through this window. Cambridge. The use of the carbon dioxide laser has already been employed for selected cavernomas in the brainstem (G. Neurosurgery 682011. Turner JD. with the drawback that given the small surgical window. wherever practical. a lateral ventral approach is chosen (A. Reviewing the retrospective data shown above. We have sought to incorporate new technologies. Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients. given the constraints of the surrounding anatomic structures. and we are presently exploring the utility of the flexible CO2 laser (OmniGuide.04. Porter R. or hemosiderin-stained tissue is preserved.SCIENCEDIRECT. Abla AA. Turner JD. if indicated. which are commonly associated with these lesions (1. personal communication. In the senior author’s experience (L. Future Developments As technology advances. http://dx. a general approach to brainstem cavernous malformations is to create as small a portal for access to the lesion as feasible. the cavernoma is initially centrally debulked. de Oliveira JG. thereby minimizing damage to the surrounding brainstem tracts and nuclei. CONCLUSION Our approach to cavernous malformations of the brainstem represents a progressive and iterative refinement of surgical techniques during the past two decades.S. we anticipate the development of specialized microsurgical instrumentation. Abla AA. the cavernoma generally is internally debulked to decompress the lesion. USA) at our institution. and gradually. Any associated developmental venous anomalies. We have generally opted for repeated resections. field of view is of particular importance during resection of small cavernomas.030 . a “minimal access” technique. A small window to the cavernous malformation is created. MAI ET AL. 2.). Spetzler RF: Surgical approaches to brainstem cavernous malformations. From this minimally invasive portal. This method has been able to yield generally favorable results in the majority of brainstem cavernomas. including flexible endoscopes and other articulated devices that will facilitate working through highly constrained operative corridors. In these cases. the wall is gently liberated from the surrounding brainstem parenchyma and removed piecemeal to minimize injury to the surrounding tracts and nuclei (A-E).N. Finally. wherever possible. for residual brainstem cavernomas.doi.2012. These recurrences are tempered against the reduction of expected post-operative complications. for a deep seated lesion in the pons. inset). 3. CEREBROVASCULAR Figure 10. 702 www. a gross total resection may be impossible to achieve. we recommend a minimal access technique. the cavernoma is resected as much as possible. From experience. with the direction of access defined by the safest anatomical corridor possible. Neurosurg Focus 29:E82010. such as image guidance and diffusion tensor imaging. Mitha AP.PEER-REVIEW REPORTS JEFFREY C.1016/ WORLD NEUROSURGERY. Lekovic GP. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM conservatively with monitoring by serial imaging. and the wall is then gently taken down from the surrounding brains- tem and disconnected with the use of a bimanual technique (Figure 10). as they do present a risk of rehemorrhage. 2010). In this 32). which reduces the likelihood of postoperative morbidity due to brainstem nuclear and tract injury at the expense of achieving gross total resection. General technique for resection of brain stem cavernomas. we have opted to eschew midline approaches to the dorsal midbrain and to the floor of the fourth ventricle. Spetzler RF.

. Surg Neurol 481997. Pizzolato GP. Microsurgical anatomy of the safe entry zones on the anterolateral brainstem related to surgical approaches to cavernous malformations. Bricolog A: Imaging of brain stem tumors. Batra S. 30. RESECTION OF CAVERNOUS MALFORMATIONS OF THE BRAINSTEM 4. Porter RW. 20. Acta Neurochir (Wien) 142:383-387. Mathiesen T. Bendok BR. Bogucki J. Maderwald S. Ferroli P. Buchfelder M. 21. Schlamann M. Awad IA. anterior transpetrosal approach to the upper brain stem and clivus. 2000. Garrett M.1016/j. Magdinec M. Neurosurg Focus 29: E52010. Zhu Y. Kondziolka D. Spetzler RF: Surgical approaches to the brain stem. Factor D. 6. Ishihara H. Porter RW. Bricolo A: Surgical management of intrinsic brain stem gliomas. Zabramski JM: Cavernous malformations of the brain stem. 2006. An analysis of the natural history of cavernous malformations. Monaco EA. McCoy KE. 25. Yadla S. 23. Foote RL. Reisch Available online: www. Baskin JJ. Bjeljac M. Chen X. 34. Grandhi R. Arch Neurol 35:323325. 18. 1990. 37. Recinos PF. Little JR: Natural history of the cavernous angioma. Flickinger JC. Roth P. Neurochirurgie 35(82-83):128-131. 38.PEER-REVIEW REPORTS JEFFREY C. Fritschi JA. Robinson JR. diagnosis and treatment. Diffusion tensor imaging and white matter tractography in patients with brainstem lesions. 22. Surg Neurol 592003. Crone NE. 13. Spetzler RF. Nat Rev Neurol 5:659-670. Received 12 September 2011. 17. Minim Invasive Neurosurg 49: 168-172. Neurosurg Focus 29:E72010. Report of three cases. Zhang J. Barnett SL. J Neurosurg 77:709-717. Flemming KD. (2013) 79. McCormick WF: Intracerebral venous angioma. Scott Med J 2:200215. 12. Sen CN.444454discussion 454. 1978. Sarwar M. Case report and review. Matthies C: Surgical management of brainstem cavernomas. Carvalho GA. Chung SS. Sure U: Susceptibility weighted magnetic resonance imaging of cerebral cavernous malformations: prospects.04. Rigamonti D. 7. Folia Neuropathol 41:227-230. Zabramski JM: Cavernous malformations of the brainstem: experience with 100 patients. Lunsford S. Nimsky C. MAY/JUNE 2013 www. J Neurosurg 75:715-722. Sinisi M. Campbell PG.195-200discussion 200-191. 9. J Neurosurg 75:709-714. Kyoshima K. 32. Kelly DL. Asaad WF.S3-S9discussion S9-10. and surgical considerations. 27. Javedan S. Acta Neurochir (Wien) 130:35-46. http://dx. Otten P. Gibo H. Gross BA. 2003. 106-115discussion 115-106.see front matter © 2013 Published by Elsevier Inc.sciencedirect. 2000. Robinson JR. Awad IA. Kaku Y. Czernicki Z: Surgical treatment of brainstem tumours with special emphasis on the operative approach through the fourth ventricle floor. Br J Neurosurg 13:366-375. Breiter SN. clinical. 10. Neurosurg Focus 29:E92010. Bonita R. Garner TB. 1957. J Neurosurg 2010. Eghbal R. Detwiler PW. Surgical management of brain-stem cavernous malformations: report of 137 cases. 1991. Sekhar LN. Prognosis. II. Lombardo MC. 19. Czernicki Z. Washington CW. Choi JU. 28. Clatterbuck RE. 31. Awad IA. Jabbour P. 2003. J Neurosurg 93:987991. Bogucki J. Ladd ME. Pollock BE. 2001. 2001. Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Op Tech Neurosurg 4:24-29. Sun B. 1999. 2000.9-17discussion 17-18. discovered by retrospective analysis of 24. Op Tech Neurosurg 3:87-105. Figueiredo EG. Ogilvy CS: Operative management of brainstem cavernous malformations. Surg Neurol 72suppl 22009. 2000. Kobayashi S. Neurosurg Focus 29:E112010. Lunsford LD: Stereotactic radiosurgery for the treatment of symptomatic brainstem cavernous malformations. Reulen HJ. 40.535 autopsies].1203-1212discussion 1212-1204. 8. 2009. Park YG. Niranjan A.915discussion 15-17. Acta Neurochir (Wien) 1492007.030 Journal homepage: www. Del Curling O. Porter RW. Factors predisposing to clinical disability in patients with cavernous malformations of the brain. Op Tech Neurosurg 3:137-154. Surg Neurol 562001. Ziyal IM. 5/6:691-703. 1991. J Neurosurg 99:31-37.1117-1131discussion 1131. Sen C: Surgical management of cavernous malformations of the brain stem. Solero CL. Neurosurgery 321993. Straumann D. J Neurosurg 73:345-354. Lanzino DJ. Sekhar LN: The subtemporal. 35. Kihlstrom L: Deep and brainstem cavernomas: a consecutive 8-year series. Neurosurgery 562005. Paranandi L. A review of 139 cases. Giliberto G. Weigel D. Jr.WORLDNEUROSURGERY. Diehn FE.wneu. 45. 24. Ganslandt O. Spetzler RF: Surgical technique for resection of cavernous malformations of the brain stem.WORLDNEUROSURGERY. J Neurosurg 78:987-993. Zhao YL. Walcott BP. Spetzler RF. Rigamonti D: Cavernous malformations: natural history. .E805-E818discussion E818. Zubay G. Spetzler RF. 41. Hoenig-Rigamonti K. Nahed BV. Lee KC. Samii M. Schomberg PJ. Perneczky A.. Awad IA: Emerging clinical imaging techniques for cerebral cavernous malformations: a systematic review. Flickinger JC. Rankin J: Cerebral vascular accidents in patients over the age of 60. 26. 16. Kano H. Broggi G. Beltramello A. Samson D: The presigmoid approach to anterolateral pontine cavernomas. Bettag M. Neurosurg Focus 29:E102010. 43. Berney J: [131 cases of cavernous angioma (cavernomas) of the CNS. McLaughlin MR. 1999. accepted 14 April 2012 Citation: World Neurosurg. Zipfel GJ: Update on the natural history of cavernous malformations and factors predicting aggressive clinical presentation. and first experience at ultra-high field strength (7-Tesla) magnetic resonance imaging. 1993. Edner G. 42. The prospective natural history of cerebral venous malformations.doi. 1988. Kawase T: Technique of anterior transpetrosal 703 CEREBROVASCULAR 3. J Neurosurg 95:825-832. 2000. Lawton MT. Neurosurgery 622008. Recalde RJ. White JA. Sekhar LN: The subtemporal and preauricular infratemporalapproachtointraduralstructuresventralto the brain stem. The natural history of cavernous malformations: a prospective study of 68 patients. Laster DW: The natural history of intracranial venous angiomas. Porter RW. Batjer HH.1166-1171discussion 1172-1163. 15. Dammann P. Derksen PT. Liu A.2012. Giombini S. 1989. Gielecki J: Cytoarchitectonic basis for safe entry into the brainstem. Jr. 44. Neurosurgery 431998. Brainstem cavernous malformations. Neurosurgery 642009. transcavernous. Op Tech Neurosurg 3:124-130. Rilliet B. Yonekawa Y: The role of intraoperative monitoring of oculomotor and trochlear nuclei-safe entry zone to tegmental lesions. 36. Masotto B. Stafford SL. Neurosurgery 441999. Franzini A. drawbacks. Moriarity JL.730-735discussion 735-736. Wang CC. Link MJ: Stereotactic radiosurgery for cavernous malformations. Salas E. Op Tech Neurosurg 2:10-17. Beaglehole R: Recovery of motor function after 1878-8750/$ . Surgical treatment of brainstem cavernous malformations. Lee RR. Barth M. Neurosurg Focus 29:E62010. Brainstem cavernomas: long-term results of microsurgical resection in 52 patients. de Oliveira E. Kondziolka D. Kim DS. 1992. Sheppard JM. MAI ET AL. 33. 39. Lunsford LD. Wetzel M. J Neurosurg 90:50-58. Kuroyanagi T: A study of safe entry zones via the floor of the fourth ventricle for brain-stem lesions. Jr.. Garces YI. Hauck EF. Harsh GR. Lin D. 5. 14. Stroke 19:1497-1500. Khan AA. WORLD NEUROSURGERY 79 [5/6]: 691-703. 11. 1994. Lanzino G: Brainstem cavernous malformations: anatomical. 2000. Zhang JT. Op Tech Neurosurg 3:114-123. Detwiler PW. Spetzler RF: Transpetrosal approaches. 1999. Detwiler PW. Transoral transclival removal of anteriorly placed cavernous malformations of the brainstem.

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