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Surgical Resection of Cavernous Malformations of the Brainstem: Evolution of a Minimally Invasive Technique
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 䡲 Brainstem 䡲 Cavernoma 䡲 Cavernous malformation 䡲 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: [email protected]] Citation: World Neurosurg. (2013) 79, 5/6:691-703. http://dx.doi.org/10.1016/j.wneu.2012.04.030 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2013 Published by Elsevier Inc.
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-
䡲 OBJECTIVE: The purpose of this study is to provide an institutional retrospective review of surgically treated brainstem cavernous malformations. 䡲 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. 䡲 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. 䡲 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.
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
77
Ataxia
59
PATIENTS AND METHODS
Headache
55
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-
Diplopia
41
Weakness
27
Sensory changes
27
Vertigo or dizziness
23
Dysphagia
14
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CN, cranial nerve.
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Sex Age
Location
Approach
Volume, cm3 Depth
Entry Corridor
Intraoperative Neurophysiology
Preoperative Symptoms
Postoperative Symptoms
Follow- Pre Post up mRS mRS Recurrence?
1.2
At pial Lateral midbrain surface
SEPs, MEPs, BAEPs unchanged
Left hemiparesis, left hyperreflexia.
Left hemiparesis, with improvement.
20
4
2
No
F
50 Mesencephalic
Lateral supracerebellar
0.05
Just Dorsal lateral beneath midbrain pial surface
SEPs, MEPs, BAEPs unchanged
Headache, ataxia, diplopia.
Headaches persistent. Diplopia on extreme lateral gaze without functional impairment.
32
2
1
No
M
58 Mesencephalic
Lateral supracerebellar
1.1
At pial Lateral midbrain surface
SEPs, MEPs, BAEPs unchanged
Multiple hemorrhages in past with rebleed and worsening of diplopia, gait ataxia, and right hemibody numbness.
Diplopia resolved. Right hemibody numbness slightly worse than pre-op, now stable. No impairment in work.
25
2
1
No
M
8 Mesencephalic
Occipital transtentorial
0.08
At pial Tectal plate; inferior SEPs, MEPs, BAEPs surface to superior colliculus unchanged
Vertigo, diplopia, headaches, nausea, emesis, ’syncopal’ events.
Diplopia resolved, minor headaches.
12
1
0
No
F
60 Mesencephalic
Transpetrosal
1.3
Just Lateral midbrain beneath pial surface
4
4
4
No
M
37 Mesencephalic
Orbitozygomatic
0.2
Beneath Medial crus cerebri SEPs, MEPs, BAEPs the pial unchanged surface
Mild left limb numbness. Post-operative wound Partial right CN III and infection. Right ptosis CN VI palsy. and diplopia improved on follow-up.
11
1
1
No
F
60 Mesencephalic
Orbitozygomatic
0.85
5 mm
SEPs, MEPs, BAEPs unchanged
Diplopia, gait ataxia, headache, right hemiparesis.
Right hemiparesis improved, diplopia resolved.
21
2
2
No
M
57 Mesencephalic
Orbitozygomatic
0.48
At pial Anterolateral surface midbrain
Right MEPs transiently decreased. SEPs and BAEPs unchanged.
Headache, dizziness, impaired tandem gait.
Post-operative jaw malocclusion, managed conservatively.
22
2
1
No
F
38 Mesencephalic
Orbitozygomatic
1.3
At pial Anterolateral surface midbrain
SEPs, MEPs, BAEPs unchanged
Severe headache, tremors, dysphagia.
Mild right CN VI palsy. Tremor and dysphagia resolved.
24
1
1
No
Anterolateral midbrain
Left tibial and left median Somnolence, gait ataxia, Postoperative nerve SSEP responses left arm weakness and hydrocephalus showed a marked decline. left hemibody numbness. requiring shunt No change in MEPs or placement. Aspiration BAEPs. pneumonia. Persistent left hemiparesis; able to ambulate with assistance. Requiring nursing home care.
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Table 2. Surgical Approaches to Brain Stem Cavernous Malformations
Suboccipital
0.44
At pial Posterolateral surface midbrain
F
24 Pontomesencephalic
Subtemporal
0.84
Just beneath pial surface
M
39 Pontomesencephalic
Combined transtemporal, transpetrosal
2.0
F
45 Pontine
Combined transtemporal, transpetrosal
F
69 Pontine
M
Right SEPs declined to 40% of baseline. MEPs and BAEPs unchanged.
24
1
4
No
Severe headaches, left dysmetria, gait ataxia. Left CN V numbness.
Post-operative wound infection. Improved to baseline.
21
4
0
No
At pial Posterior to Poor to absent cortical surface trigeminal root entry SEPs on left consistent zone with pre-operative left hemibody numbness. MEPs unchanged from baselines.
Two previous hemorrhages with left facial and hemibody numbness, now progressively worsening.
Left numbness unchanged. No motor weakness and mild left dysmetria.
7
3
1
No
0.56
Just Pontomesencephalic SEPs, MEPs, BAEPs beneath junction unchanged pial surface
Dysarthria, diplopia, left Left hemibody central hemipareis, gait ataxia, neuropathic pain. severe headaches. Headaches resolved.
65
4
2
No
Transmaxillarytransclival
0.38
Just Mid-ventral pons beneath pial surface
SEPs, MEPs, BAEPs unchanged
Headaches, left Resolution of prehemibody numbness and operative symptoms. hemiparesis. Gait ataxia, dysphagia, vertigo.
51
2
1
Yes
35 Pontine
1) Retrosigmoid 2) Presigmoid, Transsigmoid
0.07
6 mm
1) SEPs, MEPs, BAEPs unchanged 2) Transient changes in the left BAEP and right thenar MEP with recovery at closing.
Lightheadedness, dizziness, diplopia, headaches. Left CN VI palsy.
Cerebrospinal fluid leak requiring lumbar drain. Left hearing loss. Persistent left CN VI palsy.
12
1
1
No
F
42 Pontine
Suboccipital
0.13
At pial Floor of the fourth SEPs, MEPs, BAEPs surface ventricle, superior to unchanged facial colliculus
Left torsional nystagmus, Right CN VI and VII gait ataxia. palsy, requiring right gold weight. Right hyperacusis and left limb coordination problems.
32
2
3
No
F
43 Pontine
Transpetrosal
0.32
Just Posterior and inferior SEPs, MEPs, BAEPs beneath to trigeminal root unchanged pial entry zone surface
Numbness of the right face, dizziness, ataxia, diplopia and weakness.
27
2
1
No
Superior and SEPs, MEPs, BAEPs anterior to unchanged trigeminal root entry zone
1) Lateral pons, anterior to CN VII/ VIII root entry zone 2) More posterior and inferior approach to same region
Right CN V1 decreased sensation and diminished right corneal reflex. Diplopia resolved.
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Left hemibody numbness, Hydrocephalus diplopia, headaches. requiring shunt. Deep venous thrombosis, aspiration pneumonia. Feeding tube placement. Persistent diplopia. Nursing home for care.
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Sex Age
Location
Approach
Volume, cm3 Depth
Entry Corridor
Intraoperative Neurophysiology
Preoperative Symptoms
33 Pontine
Transpetrosal
0.14
15 mm Inferior and posterior SEPs, MEPs, BAEPs to trigeminal root unchanged entry zone
F
30 Pontine
1) Transpetrosal 2) Supracerebellar transtentorial
2.7
Just Lateral midbrain beneath pial surface
1) SEPs, MEPs, BAEPs Three previous unchanged 2) SEPs, MEPs, operations. Headaches, BAEPs unchanged severe dysarthria, dysphonia, facial paralysis, bilateral CN VI and CN III palsies. Wheelchair bound. Right greater than left dysmetria.
F
57 Medullary
1) Subtemporal, infratentorial 2) Suboccipital
0.60
5 mm
1) Left upper extremity MEP decline to 20% of baseline value 2) Loss of left tibial SEP.
Dysphagia, gait ataxia. Left upper extremity weakness. Tracheostomy and gastrostomy postoperatively from previous dural arteriovenous fistula resection.
M
67 Medullary
Suboccipital
0.16
Just Inferior cerebellar beneath peduncle pial surface
F
37 Medullary
Suboccipital
0.01
At pial Floor of fourth surface ventricle; lateral to vagal trigone
M
8 Medullary
Suboccipital
0.06
Just beneath pial surface
Anterolateral medulla; floor of fourth ventricle lateral to striae medullaris
68
3
1
No
Pancerebellar ataxia, tremors, titubation. Persistent CN VI and III palsies. Wheelchair bound.
24
4
4
Yes
Dizziness, ataxia, dysarthria. Left hemiparesis and left hemisensory loss.
24
3
4
No
SEPs, MEPs, BAEPs unchanged
Headaches, left Persistent ataxia and hemiplegia, ataxia, left facial numbness. diplopia. Left facial droop and vocal hoarseness.
7
3
3
No
SEPs, MEPs, BAEPs unchanged
Dysequilibrium, emesis and right arm numbness. Impaired tandem gait. Previous attempted resection.
Numbness in bilateral upper extremities, right-sided numbness of tongue.
52
3
0
No
Vertigo, diplopia, headaches, nausea, emesis, ’syncopal’ events.
Diplopia resolved, minor headaches.
12
1
0
No
Details of the 22 patients included in this study are arranged by location of the cavernomas. Where two operations have been performed, they are indicated as 1) and 2) for both the approach, as well as the neurophysiology monitoring details. CMB volumes are calculated as a volume of a sphere, with the results expressed as cubic centimeters. Preoperative mRS values (Pre-mRS) and results at follow-up are included (Post-mRS), with the follow-up period listed in months. Residual or recurrent cavernomas discovered upon follow-up are listed in the Recurrence column. mRS, modified Rankin scale; F, female; SEP, somatosensory-evoked potentials; MEP, motor-evoked potentials; BAEP, brainstem auditory-evoked potentials; M, male.
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Floor of fourth SEPs, MEPs, BAEPs ventricle; inferior to unchanged facial colliculus and medial to vagal trigone
Severe headaches, right- Mild left hemiparesis. sided facial numbness, Headaches improved. gait ataxia and coordination problems.
Follow- Pre Post up mRS mRS Recurrence?
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Postoperative Symptoms
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MR imaging. The vast majority presented with cranial nerve deficits (77%), many of which associated with diplopia (41%). A total of 55% of patients presented with headache. These numbers are generally in keeping with other previously published data (2, 39, 42). On the basis of MR findings in conjunction with patient reports of neurologic deterioration, 64% of the patients had a single bleed at the time of presentation, and 22% had sustained two or more hemorrhages by the time they were taken to the operating room. In this series, 31% of cavernomas were located in the midbrain, 35% in the pons, and 19% in the medulla (Table 2). The remainder of lesions spanned multiple brainstem regions. The mean volume of these lesions was 0.65 cm3, with a standard deviation of 0.69 cm3. Multiple cavernomas were found in six patients (27%), with one of these individuals undergoing separate surgical procedures for their CMBs.
Figure 1. Case 1: CMB situated in the right midbrain peduncle. Axial T2-weighted (A), sagittal (B), and coronal (C) T1-weighted, post-gadolinium (Gd) enhancement views demonstrate the location of the lesion. Red overlay depicts the operative corridor available for resection of the lesion via a right orbitozygomatic osteotomy approach. Three-month postoperative axial T2-weighted image demonstrating gross total resection (D).
cerebral angiography. 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). Suspected episodes of bleeding in the past not confirmed by MR imaging were excluded from the calculations. The volume of the lesions was calculated by estimating the volume of an ellipsoid (4/3 ⫻ ⫻ 1/2 sagittal diameter ⫻ 1/2 axial diameter ⫻ 1/2 coronal diameter) as determined by MR measurements. Follow-up information included outpatient neurologic examinations and calls to patients and their relatives. A mean follow-up time of 26.6 months (SD 18 months; range, 4-68 months) was obtained. Patient
outcomes pre- and postsurgery and during long-term follow-up were assessed by use of the modified Rankin scale (mRS) (8, 34).
RESULTS Preoperative History All patients who were included in this study were symptomatic from their brainstem cavernomas; only three patients did not have an overt hemorrhage before coming to medical attention (Table 1). 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
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Surgical Approaches A broad range of approaches was used during surgical resection of brainstem cavernomas, as shown in Table 2. The primary aim of surgery was to provide safe resection of the lesion through as small an access point through the brainstem as possible, that is, the “minimal access” technique. 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, 7, 21, 24, 35). Developmental venous anomalies associated with these cavernomas, identified either on preoperative workup or intraoperatively, were left extant during surgery (2). All lesions were resected under frameless stereotaxy, with coregistration to the operating microscope used whenever possible. Intraoperative bilateral somatosensory and motor-evoked potentials were combined with cranial nerve monitoring, including brainstem auditory evoked responses, as well as direct stimulation (44).
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” (24, 35). The approach is
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CEREBROVASCULAR Figure 2. Case 2: left tectal plate cavernous malformation. Sagittal T1weighted post-Gd (A) and axial T2-weighted preoperative (B) and
postoperative scans at 2 months (C). Red overlay depicts the operative approach via a left occipital transtentorial approach.
best determined with careful consideration of the anatomy and any available additional imaging information, such as diffusion tensor imaging. Intraoperative neuronavigation is indispensable in delineating the entry approach, in conjunction with neuroanatomical landmarks. The incision into the brainstem and the tract are kept as narrow as possible until the cavernoma is reached. Once inside the cavernoma, any liquefied hematoma is drained. Solid portions of the cavernoma are removed piecemeal, starting centrally, and gradually progressing to the margins, until the lesion is completely removed (Video 1). Most cavernomas are removed in three to five pieces, depending on their size and consistency. Care is taken to remove all of the cavernoma elements while preserving any major veins or en passage arteries. Vigorous removal of the gliotic, hemosiderin-stained margin of the cavernoma is not attempted, especially with large lesions, because the risk of seizures triggered by these residual tissues is nonexistent.
Figure 3. Case 3: left lateral supracerebellar infratentorial approach (red transparent overlay) to dorsal midbrain cavernoma. Sagittal (A), coronal (B), and axial (C) T2-weighted images and axial T2weighted image 14 months postoperatively (D) demonstrating no obvious residual cavernoma.
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Operative Results A total of 27 operative procedures were performed for the 22 patients in the series for their brainstem cavernomas; 31% of the cavernomas were mesencephalic, 35% were pontine, and 19% were located in the medulla (Table 2). Four lesions were large enough to span adjoining domains, including one mesencephalothalamic and three
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approached via a left occipital, transtentorial approach using frameless stereotaxy (Figure 2). As the lesion came to the surface, gross total resection was possible, with new postoperative diplopia noted at 2 months follow-up, and at 1 year, he was asymptomatic, mRS 0. Case 3. A 58-year-old man with known history of CMB and multiple hemorrhages presented with rebleed accompanied by diplopia, right hemibody numbness, and gait ataxia, mRS 2. The cavernoma was located on the left dorsal mesencephalon (Figure 3). We approached the lesion by a lateral supracerebellar infratentorial approach. At 25 months follow-up, patient has resolution of diplopia but slight worsening of right body numbness, mRS 1.
Figure 4. Case 4: CMB located in the right cerebellar peduncle. T2-weighted sagittal (A) and axial (B) images. Three-dimensional diffusion tensor imaging demonstrates medial displacement of rostralcaudal fibers with cavernoma coming to surface of the lateral pons (C). Red overlay illustrates a right transpetrosal approach. (D) Axial T2-weighted image at 10-month postoperative follow-up.
ral orbitozygomatic approach was undertaken (Figure 1). She developed transient left facial weakness and worsening of her left hemiparesis postoperatively. At 20 months after the procedure, she has progressed from an mRS 4 to an mRS 2 with persistence of her mild left-sided weakness. Case 2. An 8-year-old boy presented with vertigo, headVideo available at Midbrain. Case 1. This 23WORLDNEUROSURGERY.org aches, nausea, and vomiting year-old woman developed and was found to have at least left hemiparesis with distal weakness seven supra- and infratentorial cavernous greater than proximal in the arms in legs malformations, including the largest in the (graded 4/5) and hyperreflexia on the ipsitectum, which had evidence of recent hemlateral side. As her cavernoma was situated orrhage on MR imaging, and another in the medulla. The tectal plate cavernoma was in the right peduncle, a right frontotempopontomesencephalic cavernomas. A 91% gross total resection rate was achieved, as assessed by serial MR imaging. In 9% of patients, residual cavernoma was identified on post-operative imaging. No postoperative mortality was observed in this series, and no further surgeries were required in these patients.
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Pons. Case 4. A 43-year-old woman presented with right V1-V3 facial numbness, diplopia, ataxia, and weakness with two symptomatic hemorrhages from a right middle cerebellar peduncle cavernous malformation (Figure 4). Given the location, we opted for a right transpetrosal approach for the lesion. In this instance, diffusion tensor imaging was used during preoperative planning to map the direction of displaced tracts in a rostral-caudal axis. In comparing the side of the brainstem with the cavernoma to the contralateral unaffected side, we found these fibers to be medially displaced, confirming that entry from a lateral approach would be safest. At 27 months postoperatively, her diplopia had resolved, but she has developed a right diminished corneal reflex and slightly worsened V1-V3 numbness. Nevertheless, she is able to drive a vehicle, and her mRS improved from a 2 to a 1. Case 5. A 69-year-old woman presented with acute onset of headache, left hemibody numbness and weakness (4/5), left dysmetria, ataxia, dysphagia, and vertigo with a central pontine hemorrhage secondary to a cavernoma (Figure 5). Because the lesion was located in the midline and did not clearly reach the surface, we opted for a transmaxillary⫺transclival approach, as illustrated in Figure 5. In this case, a transfacial LeFort I maxillotomy was used, with a clivectomy performed with neuronavigation used to guide the trajectory directly to the lesion. This approach, although technically demanding, affords an excellent work-
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Case 7. A 39-year-old man with two previous hemorrhages of a right dorsal lateral pontine cavernoma re-presented with progressive left facial droop, left hemibody numbness, and truncal ataxia. As shown in Figure 7, a right transpetrosal and presigmoid approach was used for extirpation of the lesion. 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. Medulla. Case 8. A 37-year-old woman presented with baseline disequilibrium and previous subtotal resection of dorsal medullary brainstem cavernoma by another neurosurgeon. She represented with sudden deterioration, including numbness in her right arm, intermittent dysphagia, and difficulty breathing. A far lateral retrosigmoid approach was used, and gross total resection was achieved (Figure 8). At 42 months’ follow-up, she has now made a complete recovery (mRS 0).
Figure 5. Case 5: Midline, ventral pontine cavernoma approached via a transmaxillary-transclival approach (red transparent overlay). T1-weighted post-Gd sagittal (A), coronal (B), and axial (C) images. (D) T2-weighted axial scan at 3-year follow-up.
ing view of the ventral pontine surface, including the basilar artery and its associated paramedian perforators, thereby facilitating their preservation. In addition, it represents the most direct pathway to the lesion, without the need to traverse normal brainstem tissue to reach the lesion. Here, the basilar artery was moved gently aside, exposing a small area of discoloration in the midline representing the cavernoma’s emergence at the surface of the pons. After resection, the defect in the clival dura was repaired with placement of two pieces of abdominal fascia beneath the inner surface of dura, followed by application of DuraSeal (Confluent Surgical Inc., Waltham, Massachusetts, USA). An additional two layers of fascia were applied to the outside, secured again with a layer of DuraSeal and Gelfoam
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(Pfizer, New York, New York, USA), and the sphenoid rostrum was covered with a mucosal flap. 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. Her mRS improved from 2 to 1 at 44 months’ follow-up. Case 6. A 57-year-old man who developed sudden onset of headache, dizziness, and gait disturbance was found to have a left lateral pontine hemorrhage as the result of underlying cavernoma (Figure 6). A left subtemporal approach with zygomatic osteotomy was used to gain access to the lateral pons, where the cavernous malformation was observed to come to the surface. At 22 months’ follow up, the patient had improved from an mRS score of 2 to an mRS of 1.
Long-Term Outcomes During the course of follow-up, 54% of patients were noted to improve compared with their preoperative status, whereas 32% remained generally unchanged from a neurologic standpoint. During this time, 14% of patients had declined compared with their preoperative status. The distribution of preoperative mRS and long-term mRS is shown in Figure 9. Of the 9% of patients with residual brainstem cavernomas, no instances of rehemorrhage were recorded. At present, both of these patients have declined reoperation.
DISCUSSION Indications for Removal The vast majority of brainstem cavernous malformations come to attention after a hemorrhage. In general, 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, 39, 42). For deeper seated lesions, a second bleed or progressive neurologic deficit necessitates surgical extirpation of the brainstem cavernoma because it suggests the propensity of the
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surrounding the cavernomas, 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. Unless the cavernoma comes clearly to the pial surface, the direction of approach may not always be optimally defined as the shortest path from the surface to the lesion. Given the eloquence of the brainstem, even a thin parenchymal layer overlying the cavernoma can harbor critical tracts. Complicating this situation is the paucity of widely used and reliable intraoperative methods to identify these displaced and distorted structures. Broadly, we have subcategorized approaches to the brainstem with respect to the midbrain, pons, and medulla.
Figure 6. Case 6: Left, lateral pontine cavernoma with a left subtemporal approach with zygomatic osteotomy depicted with the red overlay. Fluid-attenuated inversion recovery sagittal (A), T1weighted post-Gd coronal (B), and T2-weighted axial preoperative (C) and 22 months postoperative (D) images.
lesion to rebleed in the future. In these instances, carefully weighing the risk of morbidity from surgery compared with that of future re-hemorrhage, on the basis of the natural history of these lesions, tips the balance in favor of surgical intervention (18). This is especially true if deep-seated lesions can be approached through “safe entry” corridors. The use of radiosurgery for cavernous malformations has been reported, with mixed results (27, 30). As such, the use of radiosurgery as a primary treatment modality for cavernous malformations, including those of the brainstem, remains controversial. At present, we advocate surgical resection as the primary means for treatment for high-risk cavernomas of the brainstem. With regard to timing of surgery after a
hemorrhage, although some surgeons advocate delaying surgery until the subacute phase, when the blood products will undergo liquefaction (13, 18, 39); waiting much beyond the first several weeks risks development of gliosis, which may hinder complete resection.
Approaches to the Brainstem Unlike with supratentorial cavernous malformations, those associated with CMBs present a special challenge to the surgeon due to the presence of surrounding brainstem nuclei and tracts (7, 17, 24, 35). As with others, we advocate carefully tailoring the surgical approach to each individual’s lesion. It is incumbent upon the surgeon to recognize the normal anatomy of the region
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Midbrain. The midbrain is subdivided into three general approaches: anteromedial, lateral, and posterior. In the anteromedial approach for interpeduncular lesions, an extended transsylvian corridor is used, with the assistance of an orbitozygomatic craniotomy (18). Slightly more laterally, a subtemporal approach can be used, or in combination with a transsylvian route (31). Laterally, a supracerebellar-infratentorial or petrosal approach can be used to reach mesencephalic cavernomas. Posteriorly, a suboccipital or occipital transtentorial approach can be used to reach lesions centered near the posterior midbrain, including the tectal plate. From a posterior approach, depending on the location of the cavernomas, 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, 21, 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, 17). Otherwise, midline approaches through the tectal plate should be avoided whenever possible given their postoperative morbidity. Through experience, we and others have learned that avoidance of injury to the central tegmentum and adjacent medial longitudinal fasciculus is vital, as the resultant postoperative complications of nystagmus and internuclear ophthalmoplegia, respectively, are particularly debilitating during recovery (17). Pons. The pons is the largest region of the brainstem and the most common location for
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CEREBROVASCULAR Figure 7. Case 7: Right transpetrosal and presigmoid approach (red overlay) to a right dorsal lateral pontine cavernoma. T1-weighted post-Gd axial (A), T2-weighted axial (B), T1-weighted post-Gd sagittal (C), and postoperative 3-month T2-weighted axial image (D). Intraoperative image demonstrating bimanual removal of cavernoma through a small portal in the brainstem (E) and image after gross total resection (F).
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brainstem cavernomas (13, 18, 33, 42). Given its size, a variety of surgical approaches are available to the surgeon, depending on the precise location of the cavernous malformation (Table 2). We have defined approaches to the pons into four categories: dorsal, central, anterolateral, and lateral. From a dorsal approach, a midline suboccipital approach can be used. In such cases, it is paramount to minimize dividing the vermis given associated complications, including truncal ataxia (44). Alternately, a subtonsillar-transcerebellomedullary (telovelar) approach can be used (13, 44), which involves dividing the cerebellomedullary fissure. This approach is useful in accessing pontomedullary and medullary lesions. Unfortunately, unless the cavernoma clearly emerges at the surface of the floor of the fourth ventricle, injury to the medial longitudinal fasciculus, facial, and abducens nerve are common when operating along this region (3, 44). As with others (13, 17, 18, 33), we view the floor of the fourth ventricle with great caution when approaching CMBs, despite the published morphometric descriptions of safe entry zones in the infra- and supra-abducental or facial regions (6, 7, 24). These lesions can be approached if the locations of the facial, vagal, and hypoglossal nuclei are carefully established intraoperatively by direct stimulation. Nevertheless, it may be difficult to avoid the intrinsic portion of the facial nerve tract or the abducens nucleus when resecting cavernomas in immediate vicinity. Postsurgical brainstem tract and nucleus-related complications have been reduced as we have shifted away from posterior approaches to the pons over time. We prefer more lateral or anterolateral approaches to the brainstem, particularly when dealing with deep-seated lesions of the pons. The anterior and anterolateral brainstem tracts are generally more resilient to surgical manipulation than the dorsal pontine and medullary surfaces. A transpetrosal (19, 22, 31, 45) or retrosigmoid approach will enable access to the more anterior surface of the pons (16, 31). A presigmoid approach will yield a more lateral, albeit more direct, view of the pons (20). From any of these approaches, the peritrigeminal area, a “safe entry zone,” can be accessed and safely traversed horizontally, following along the plane of the fibers. This triangular region is bound medially by the
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the posterior intermediate and posterior lateral sulci (9, 17). Generally, a far lateral retrosigmoid approach will suffice for reaching pontomedullary lesions (13). 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, 31). From either approach, safe medullary access is realized by way of entry through the retro-olivary sulcus, which does not result in clinically evidence deficits (35). Finally, strictly anterior cavernomas of the ventral medulla can be reached via a transoral route (36, 44). This was not used in our series due to the absence of any cases requiring it. Because of the concern for CSF leak and associated infection, an alternative is the subtemporal infratemporal approach for these lesions (41). In each case, the guiding principle is to avoid breaching major brainstem tracts or nuclei. If there is no option, then traversing the most accessible route to the brainstem cavernoma must then be chosen on a caseby-case basis. Figure 8. Case 8: Suboccipital approach (red transparent overlay) to cavernous malformation of the dorsal medulla previously with subtotal resection. T2-weighted sagittal (A), coronal (B), and axial preoperative (C), and 3 year postoperative (D) images shown.
pyramidal tract, inferiorly by the pontomedullary sulcus out to the flocculus, and laterally just medial to the root entry zone of cranial nerve V (35). Cavernomas situated directly on the ventral midline surface of the pons require a
Figure 9. Bar graph showing the distribution of the preoperative mRS scores for the 22 patients compared with the distribution at last follow-up. Mean follow-up time was 26.6 months with a range of 2-68 months, SD of 17.7 months.
central approach. For these difficult, but fortunately rare, lesions, we advocate a transmaxillary-transclival approach, which we used during the resection of one of our pontine cavernomas in our series (Table 2). Medulla. The medulla can be approached from the following routes: dorsal, anterior, and anterolateral corridors. As with the pons, a midline suboccipital craniotomy with a telovelar approach can be used to reach the dorsal medullary surface (17, 31). In the upper dorsal medulla, along the inferior floor of the fourth ventricle, risk of injury to the nucleus of XII medially and the nucleus X laterally with resultant ipsilateral tongue weakness and cardiac/respiratory instability, respectively, makes entry from this direction generally contraindicated (13, 17, 18, 33). Furthermore, the medial longitudinal fasciculus underlies these structures medially. For the lower dorsal medulla, safe entry zones are defined by Bricolo as the posterior median fissure and
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Evolution of a Minimally Invasive Resection Technique Once the decision has been made to proceed with resection, careful preoperative planning is essential. When possible, we have used diffusion tensor imaging to study the distortion of the underlying white matter tracts surrounding the lesion (11). It is performed when lesions do not appear to come to the pial surface on MR imaging, so that the corridor for entry through the brainstem may not be as apparent. The utility of such imaging can be limited by susceptibility artifact when one is resecting a relatively fresh hemorrhage, which prevents adequate tractography. Nevertheless, in such cases, 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. Intraoperative cranial nerve monitoring is generally more important for dorsal approaches. For anterior and lateral approaches to the brainstem, motor-evoked potentials are obligatory. Intraoperatively, real-time guidance with frameless stereotaxy registered to the operating microscope
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conservatively with monitoring by serial imaging. These recurrences are tempered against the reduction of expected post-operative complications. We have generally opted for repeated resections, if indicated, for residual brainstem cavernomas, as they do present a risk of rehemorrhage.
Future Developments As technology advances, we anticipate the development of specialized microsurgical instrumentation, including flexible endoscopes and other articulated devices that will facilitate working through highly constrained operative corridors, thereby minimizing damage to the surrounding brainstem tracts and nuclei. The use of the carbon dioxide laser has already been employed for selected cavernomas in the brainstem (G. Steinberg, personal communication, 2010), and we are presently exploring the utility of the flexible CO2 laser (OmniGuide, Cambridge, Massachusetts, USA) at our institution.
CONCLUSION
Figure 10. General technique for resection of brain stem cavernomas. A small window to the cavernous malformation is created, with the direction of access defined by the safest anatomical corridor possible. In this example, for a deep seated lesion in the pons, a lateral ventral approach is chosen (A, inset). From this minimally invasive portal, the cavernoma is initially centrally debulked, and gradually, the wall is gently liberated from the surrounding brainstem parenchyma and removed piecemeal to minimize injury to the surrounding tracts and nuclei (A-E).
field of view is of particular importance during resection of small cavernomas. In the senior author’s experience (L.N.S.), a general approach to brainstem cavernous malformations is to create as small a portal for access to the lesion as feasible, a “minimal access” technique. Through this window, the cavernoma is resected as much as possible, given the constraints of the surrounding anatomic structures. In these cases, the cavernoma generally is internally debulked to decompress the lesion, and the wall is then gently taken down from the surrounding brains-
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tem and disconnected with the use of a bimanual technique (Figure 10). Any associated developmental venous anomalies, which are commonly associated with these lesions (1, 3, 32), or hemosiderin-stained tissue is preserved. This method has been able to yield generally favorable results in the majority of brainstem cavernomas, with the drawback that given the small surgical window, a gross total resection may be impossible to achieve. Reviewing the retrospective data shown above, there have been two recurrences after surgery: both were managed
Our approach to cavernous malformations of the brainstem represents a progressive and iterative refinement of surgical techniques during the past two decades. We have sought to incorporate new technologies, such as image guidance and diffusion tensor imaging, wherever practical. From experience, we have opted to eschew midline approaches to the dorsal midbrain and to the floor of the fourth ventricle, instead selecting operative corridors that are directed more laterally and anteriorly to the brainstem. Finally, we recommend a minimal access technique, wherever possible, which reduces the likelihood of postoperative morbidity due to brainstem nuclear and tract injury at the expense of achieving gross total resection.
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3. Asaad WF, Walcott BP, Nahed BV, Ogilvy CS: Operative management of brainstem cavernous malformations. Neurosurg Focus 29:E102010. 4. Batra S, Lin D, Recinos PF, Zhang J, Rigamonti D: Cavernous malformations: natural history, diagnosis and treatment. Nat Rev Neurol 5:659-670, 2009. 5. Beltramello A, Lombardo MC, Masotto B, Bricolog A: Imaging of brain stem tumors. Op Tech Neurosurg 3:87-105, 2000. 6. Bogucki J, Czernicki Z: Surgical treatment of brainstem tumours with special emphasis on the operative approach through the fourth ventricle floor. Folia Neuropathol 41:227-230, 2003. 7. Bogucki J, Czernicki Z, Gielecki J: Cytoarchitectonic basis for safe entry into the brainstem. Acta Neurochir (Wien) 142:383-387, 2000. 8. Bonita R, Beaglehole R: Recovery of motor function after stroke. Stroke 19:1497-1500, 1988. 9. Bricolo A: Surgical management of intrinsic brain stem gliomas. Op Tech Neurosurg 3:137-154, 2000. 10. Campbell PG, Jabbour P, Yadla S, Awad IA: Emerging clinical imaging techniques for cerebral cavernous malformations: a systematic review. Neurosurg Focus 29:E62010. 11. Chen X, Weigel D, Ganslandt O, Buchfelder M, Nimsky C. Diffusion tensor imaging and white matter tractography in patients with brainstem lesions. Acta Neurochir (Wien) 1492007;1117-1131discussion 1131. 12. Dammann P, Barth M, Zhu Y, Maderwald S, Schlamann M, Ladd ME, Sure U: Susceptibility weighted magnetic resonance imaging of cerebral cavernous malformations: prospects, drawbacks, and first experience at ultra-high field strength (7-Tesla) magnetic resonance imaging. Neurosurg Focus 29: E52010. 13. Ferroli P, Sinisi M, Franzini A, Giombini S, Solero CL, Broggi G. Brainstem cavernomas: long-term results of microsurgical resection in 52 patients. Neurosurgery 562005;1203-1212discussion 1212-1204. 14. Fritschi JA, Reulen HJ, Spetzler RF, Zabramski JM: Cavernous malformations of the brain stem. A review of 139 cases. Acta Neurochir (Wien) 130:35-46, 1994. 15. Garner TB, Del Curling O, Jr., Kelly DL, Jr., Laster DW: The natural history of intracranial venous angiomas. J Neurosurg 75:715-722, 1991. 16. Garrett M, Spetzler RF. Surgical treatment of brainstem cavernous malformations. Surg Neurol 72suppl 22009;S3-S9discussion S9-10. 17. Giliberto G, Lanzino DJ, Diehn FE, Factor D, Flemming KD, Lanzino G: Brainstem cavernous malformations: anatomical, clinical, and surgical considerations. Neurosurg Focus 29:E92010. 18. Gross BA, Batjer HH, Awad IA, Bendok BR. Brainstem cavernous malformations. Neurosurgery 642009;E805-E818discussion E818.
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19. Harsh GR, Sekhar LN: The subtemporal, transcavernous, anterior transpetrosal approach to the upper brain stem and clivus. J Neurosurg 77:709-717, 1992. 20. Hauck EF, Barnett SL, White JA, Samson D: The presigmoid approach to anterolateral pontine cavernomas. J Neurosurg 2010. 21. Ishihara H, Bjeljac M, Straumann D, Kaku Y, Roth P, Yonekawa Y: The role of intraoperative monitoring of oculomotor and trochlear nuclei-safe entry zone to tegmental lesions. Minim Invasive Neurosurg 49: 168-172, 2006. 22. Kawase T: Technique of anterior transpetrosal approach. Op Tech Neurosurg 2:10-17, 1999. 23. Kim DS, Park YG, Choi JU, Chung SS, Lee KC. An analysis of the natural history of cavernous malformations. Surg Neurol 481997;9-17discussion 17-18. 24. Kyoshima K, Kobayashi S, Gibo H, Kuroyanagi T: A study of safe entry zones via the floor of the fourth ventricle for brain-stem lesions. Report of three cases. J Neurosurg 78:987-993, 1993. 25. Mathiesen T, Edner G, Kihlstrom L: Deep and brainstem cavernomas: a consecutive 8-year series. J Neurosurg 99:31-37, 2003. 26. McLaughlin MR, Kondziolka D, Flickinger JC, Lunsford S, Lunsford LD. The prospective natural history of cerebral venous malformations. Neurosurgery 431998;195-200discussion 200-191. 27. Monaco EA, Khan AA, Niranjan A, Kano H, Grandhi R, Kondziolka D, Flickinger JC, Lunsford LD: Stereotactic radiosurgery for the treatment of symptomatic brainstem cavernous malformations. Neurosurg Focus 29:E112010. 28. Moriarity JL, Wetzel M, Clatterbuck RE, Javedan S, Sheppard JM, Hoenig-Rigamonti K, Crone NE, Breiter SN, Lee RR, Rigamonti D. The natural history of cavernous malformations: a prospective study of 68 patients. Neurosurgery 441999;1166-1171discussion 1172-1163. 29. Otten P, Pizzolato GP, Rilliet B, Berney J: [131 cases of cavernous angioma (cavernomas) of the CNS, discovered by retrospective analysis of 24,535 autopsies]. Neurochirurgie 35(82-83):128-131, 1989.
34. Rankin J: Cerebral vascular accidents in patients over the age of 60. II. Prognosis. Scott Med J 2:200215, 1957. 35. Recalde RJ, Figueiredo EG, de Oliveira E. Microsurgical anatomy of the safe entry zones on the anterolateral brainstem related to surgical approaches to cavernous malformations. Neurosurgery 622008;915discussion 15-17. 36. Reisch R, Bettag M, Perneczky A. Transoral transclival removal of anteriorly placed cavernous malformations of the brainstem. Surg Neurol 562001; 106-115discussion 115-106. 37. Robinson JR, Awad IA, Little JR: Natural history of the cavernous angioma. J Neurosurg 75:709-714, 1991. 38. Robinson JR, Jr., Awad IA, Magdinec M, Paranandi L. Factors predisposing to clinical disability in patients with cavernous malformations of the brain. Neurosurgery 321993;730-735discussion 735-736. 39. Samii M, Eghbal R, Carvalho GA, Matthies C: Surgical management of brainstem cavernomas. J Neurosurg 95:825-832, 2001. 40. Sarwar M, McCormick WF: Intracerebral venous angioma. Case report and review. Arch Neurol 35:323325, 1978. 41. Sen CN, Sekhar LN: The subtemporal and preauricular infratemporalapproachtointraduralstructuresventralto the brain stem. J Neurosurg 73:345-354, 1990. 42. Wang CC, Liu A, Zhang JT, Sun B, Zhao YL. Surgical management of brain-stem cavernous malformations: report of 137 cases. Surg Neurol 592003;444454discussion 454. 43. Washington CW, McCoy KE, Zipfel GJ: Update on the natural history of cavernous malformations and factors predicting aggressive clinical presentation. Neurosurg Focus 29:E72010. 44. Ziyal IM, Sekhar LN, Salas E, Sen C: Surgical management of cavernous malformations of the brain stem. Br J Neurosurg 13:366-375, 1999.
30. Pollock BE, Garces YI, Stafford SL, Foote RL, Schomberg PJ, Link MJ: Stereotactic radiosurgery for cavernous malformations. J Neurosurg 93:987991, 2000.
45. Zubay G, Porter RW, Spetzler RF: Transpetrosal approaches. Op Tech Neurosurg 4:24-29, 2001.
31. Porter RW, Detwiler PW, Spetzler RF: Surgical approaches to the brain stem. Op Tech Neurosurg 3:114-123, 2000.
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.
32. Porter RW, Detwiler PW, Spetzler RF: Surgical technique for resection of cavernous malformations of the brain stem. Op Tech Neurosurg 3:124-130, 2000.
Received 12 September 2011; accepted 14 April 2012 Citation: World Neurosurg. (2013) 79, 5/6:691-703. http://dx.doi.org/10.1016/j.wneu.2012.04.030 Journal homepage: www.WORLDNEUROSURGERY.org
33. Porter RW, Detwiler PW, Spetzler RF, Lawton MT, Baskin JJ, Derksen PT, Zabramski JM: Cavernous malformations of the brainstem: experience with 100 patients. J Neurosurg 90:50-58, 1999.
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Key words 䡲 Brainstem 䡲 Cavernoma 䡲 Cavernous malformation 䡲 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: [email protected]] Citation: World Neurosurg. (2013) 79, 5/6:691-703. http://dx.doi.org/10.1016/j.wneu.2012.04.030 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2013 Published by Elsevier Inc.
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-
䡲 OBJECTIVE: The purpose of this study is to provide an institutional retrospective review of surgically treated brainstem cavernous malformations. 䡲 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. 䡲 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. 䡲 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.
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
77
Ataxia
59
PATIENTS AND METHODS
Headache
55
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-
Diplopia
41
Weakness
27
Sensory changes
27
Vertigo or dizziness
23
Dysphagia
14
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CN, cranial nerve.
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Sex Age
Location
Approach
Volume, cm3 Depth
Entry Corridor
Intraoperative Neurophysiology
Preoperative Symptoms
Postoperative Symptoms
Follow- Pre Post up mRS mRS Recurrence?
1.2
At pial Lateral midbrain surface
SEPs, MEPs, BAEPs unchanged
Left hemiparesis, left hyperreflexia.
Left hemiparesis, with improvement.
20
4
2
No
F
50 Mesencephalic
Lateral supracerebellar
0.05
Just Dorsal lateral beneath midbrain pial surface
SEPs, MEPs, BAEPs unchanged
Headache, ataxia, diplopia.
Headaches persistent. Diplopia on extreme lateral gaze without functional impairment.
32
2
1
No
M
58 Mesencephalic
Lateral supracerebellar
1.1
At pial Lateral midbrain surface
SEPs, MEPs, BAEPs unchanged
Multiple hemorrhages in past with rebleed and worsening of diplopia, gait ataxia, and right hemibody numbness.
Diplopia resolved. Right hemibody numbness slightly worse than pre-op, now stable. No impairment in work.
25
2
1
No
M
8 Mesencephalic
Occipital transtentorial
0.08
At pial Tectal plate; inferior SEPs, MEPs, BAEPs surface to superior colliculus unchanged
Vertigo, diplopia, headaches, nausea, emesis, ’syncopal’ events.
Diplopia resolved, minor headaches.
12
1
0
No
F
60 Mesencephalic
Transpetrosal
1.3
Just Lateral midbrain beneath pial surface
4
4
4
No
M
37 Mesencephalic
Orbitozygomatic
0.2
Beneath Medial crus cerebri SEPs, MEPs, BAEPs the pial unchanged surface
Mild left limb numbness. Post-operative wound Partial right CN III and infection. Right ptosis CN VI palsy. and diplopia improved on follow-up.
11
1
1
No
F
60 Mesencephalic
Orbitozygomatic
0.85
5 mm
SEPs, MEPs, BAEPs unchanged
Diplopia, gait ataxia, headache, right hemiparesis.
Right hemiparesis improved, diplopia resolved.
21
2
2
No
M
57 Mesencephalic
Orbitozygomatic
0.48
At pial Anterolateral surface midbrain
Right MEPs transiently decreased. SEPs and BAEPs unchanged.
Headache, dizziness, impaired tandem gait.
Post-operative jaw malocclusion, managed conservatively.
22
2
1
No
F
38 Mesencephalic
Orbitozygomatic
1.3
At pial Anterolateral surface midbrain
SEPs, MEPs, BAEPs unchanged
Severe headache, tremors, dysphagia.
Mild right CN VI palsy. Tremor and dysphagia resolved.
24
1
1
No
Anterolateral midbrain
Left tibial and left median Somnolence, gait ataxia, Postoperative nerve SSEP responses left arm weakness and hydrocephalus showed a marked decline. left hemibody numbness. requiring shunt No change in MEPs or placement. Aspiration BAEPs. pneumonia. Persistent left hemiparesis; able to ambulate with assistance. Requiring nursing home care.
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23 Mesencephalothalamic Orbitozygomatic
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Table 2. Surgical Approaches to Brain Stem Cavernous Malformations
Suboccipital
0.44
At pial Posterolateral surface midbrain
F
24 Pontomesencephalic
Subtemporal
0.84
Just beneath pial surface
M
39 Pontomesencephalic
Combined transtemporal, transpetrosal
2.0
F
45 Pontine
Combined transtemporal, transpetrosal
F
69 Pontine
M
Right SEPs declined to 40% of baseline. MEPs and BAEPs unchanged.
24
1
4
No
Severe headaches, left dysmetria, gait ataxia. Left CN V numbness.
Post-operative wound infection. Improved to baseline.
21
4
0
No
At pial Posterior to Poor to absent cortical surface trigeminal root entry SEPs on left consistent zone with pre-operative left hemibody numbness. MEPs unchanged from baselines.
Two previous hemorrhages with left facial and hemibody numbness, now progressively worsening.
Left numbness unchanged. No motor weakness and mild left dysmetria.
7
3
1
No
0.56
Just Pontomesencephalic SEPs, MEPs, BAEPs beneath junction unchanged pial surface
Dysarthria, diplopia, left Left hemibody central hemipareis, gait ataxia, neuropathic pain. severe headaches. Headaches resolved.
65
4
2
No
Transmaxillarytransclival
0.38
Just Mid-ventral pons beneath pial surface
SEPs, MEPs, BAEPs unchanged
Headaches, left Resolution of prehemibody numbness and operative symptoms. hemiparesis. Gait ataxia, dysphagia, vertigo.
51
2
1
Yes
35 Pontine
1) Retrosigmoid 2) Presigmoid, Transsigmoid
0.07
6 mm
1) SEPs, MEPs, BAEPs unchanged 2) Transient changes in the left BAEP and right thenar MEP with recovery at closing.
Lightheadedness, dizziness, diplopia, headaches. Left CN VI palsy.
Cerebrospinal fluid leak requiring lumbar drain. Left hearing loss. Persistent left CN VI palsy.
12
1
1
No
F
42 Pontine
Suboccipital
0.13
At pial Floor of the fourth SEPs, MEPs, BAEPs surface ventricle, superior to unchanged facial colliculus
Left torsional nystagmus, Right CN VI and VII gait ataxia. palsy, requiring right gold weight. Right hyperacusis and left limb coordination problems.
32
2
3
No
F
43 Pontine
Transpetrosal
0.32
Just Posterior and inferior SEPs, MEPs, BAEPs beneath to trigeminal root unchanged pial entry zone surface
Numbness of the right face, dizziness, ataxia, diplopia and weakness.
27
2
1
No
Superior and SEPs, MEPs, BAEPs anterior to unchanged trigeminal root entry zone
1) Lateral pons, anterior to CN VII/ VIII root entry zone 2) More posterior and inferior approach to same region
Right CN V1 decreased sensation and diminished right corneal reflex. Diplopia resolved.
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Left hemibody numbness, Hydrocephalus diplopia, headaches. requiring shunt. Deep venous thrombosis, aspiration pneumonia. Feeding tube placement. Persistent diplopia. Nursing home for care.
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Sex Age
Location
Approach
Volume, cm3 Depth
Entry Corridor
Intraoperative Neurophysiology
Preoperative Symptoms
33 Pontine
Transpetrosal
0.14
15 mm Inferior and posterior SEPs, MEPs, BAEPs to trigeminal root unchanged entry zone
F
30 Pontine
1) Transpetrosal 2) Supracerebellar transtentorial
2.7
Just Lateral midbrain beneath pial surface
1) SEPs, MEPs, BAEPs Three previous unchanged 2) SEPs, MEPs, operations. Headaches, BAEPs unchanged severe dysarthria, dysphonia, facial paralysis, bilateral CN VI and CN III palsies. Wheelchair bound. Right greater than left dysmetria.
F
57 Medullary
1) Subtemporal, infratentorial 2) Suboccipital
0.60
5 mm
1) Left upper extremity MEP decline to 20% of baseline value 2) Loss of left tibial SEP.
Dysphagia, gait ataxia. Left upper extremity weakness. Tracheostomy and gastrostomy postoperatively from previous dural arteriovenous fistula resection.
M
67 Medullary
Suboccipital
0.16
Just Inferior cerebellar beneath peduncle pial surface
F
37 Medullary
Suboccipital
0.01
At pial Floor of fourth surface ventricle; lateral to vagal trigone
M
8 Medullary
Suboccipital
0.06
Just beneath pial surface
Anterolateral medulla; floor of fourth ventricle lateral to striae medullaris
68
3
1
No
Pancerebellar ataxia, tremors, titubation. Persistent CN VI and III palsies. Wheelchair bound.
24
4
4
Yes
Dizziness, ataxia, dysarthria. Left hemiparesis and left hemisensory loss.
24
3
4
No
SEPs, MEPs, BAEPs unchanged
Headaches, left Persistent ataxia and hemiplegia, ataxia, left facial numbness. diplopia. Left facial droop and vocal hoarseness.
7
3
3
No
SEPs, MEPs, BAEPs unchanged
Dysequilibrium, emesis and right arm numbness. Impaired tandem gait. Previous attempted resection.
Numbness in bilateral upper extremities, right-sided numbness of tongue.
52
3
0
No
Vertigo, diplopia, headaches, nausea, emesis, ’syncopal’ events.
Diplopia resolved, minor headaches.
12
1
0
No
Details of the 22 patients included in this study are arranged by location of the cavernomas. Where two operations have been performed, they are indicated as 1) and 2) for both the approach, as well as the neurophysiology monitoring details. CMB volumes are calculated as a volume of a sphere, with the results expressed as cubic centimeters. Preoperative mRS values (Pre-mRS) and results at follow-up are included (Post-mRS), with the follow-up period listed in months. Residual or recurrent cavernomas discovered upon follow-up are listed in the Recurrence column. mRS, modified Rankin scale; F, female; SEP, somatosensory-evoked potentials; MEP, motor-evoked potentials; BAEP, brainstem auditory-evoked potentials; M, male.
PEER-REVIEW REPORTS
Floor of fourth SEPs, MEPs, BAEPs ventricle; inferior to unchanged facial colliculus and medial to vagal trigone
Severe headaches, right- Mild left hemiparesis. sided facial numbness, Headaches improved. gait ataxia and coordination problems.
Follow- Pre Post up mRS mRS Recurrence?
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Postoperative Symptoms
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MR imaging. The vast majority presented with cranial nerve deficits (77%), many of which associated with diplopia (41%). A total of 55% of patients presented with headache. These numbers are generally in keeping with other previously published data (2, 39, 42). On the basis of MR findings in conjunction with patient reports of neurologic deterioration, 64% of the patients had a single bleed at the time of presentation, and 22% had sustained two or more hemorrhages by the time they were taken to the operating room. In this series, 31% of cavernomas were located in the midbrain, 35% in the pons, and 19% in the medulla (Table 2). The remainder of lesions spanned multiple brainstem regions. The mean volume of these lesions was 0.65 cm3, with a standard deviation of 0.69 cm3. Multiple cavernomas were found in six patients (27%), with one of these individuals undergoing separate surgical procedures for their CMBs.
Figure 1. Case 1: CMB situated in the right midbrain peduncle. Axial T2-weighted (A), sagittal (B), and coronal (C) T1-weighted, post-gadolinium (Gd) enhancement views demonstrate the location of the lesion. Red overlay depicts the operative corridor available for resection of the lesion via a right orbitozygomatic osteotomy approach. Three-month postoperative axial T2-weighted image demonstrating gross total resection (D).
cerebral angiography. 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). Suspected episodes of bleeding in the past not confirmed by MR imaging were excluded from the calculations. The volume of the lesions was calculated by estimating the volume of an ellipsoid (4/3 ⫻ ⫻ 1/2 sagittal diameter ⫻ 1/2 axial diameter ⫻ 1/2 coronal diameter) as determined by MR measurements. Follow-up information included outpatient neurologic examinations and calls to patients and their relatives. A mean follow-up time of 26.6 months (SD 18 months; range, 4-68 months) was obtained. Patient
outcomes pre- and postsurgery and during long-term follow-up were assessed by use of the modified Rankin scale (mRS) (8, 34).
RESULTS Preoperative History All patients who were included in this study were symptomatic from their brainstem cavernomas; only three patients did not have an overt hemorrhage before coming to medical attention (Table 1). 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
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Surgical Approaches A broad range of approaches was used during surgical resection of brainstem cavernomas, as shown in Table 2. The primary aim of surgery was to provide safe resection of the lesion through as small an access point through the brainstem as possible, that is, the “minimal access” technique. 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, 7, 21, 24, 35). Developmental venous anomalies associated with these cavernomas, identified either on preoperative workup or intraoperatively, were left extant during surgery (2). All lesions were resected under frameless stereotaxy, with coregistration to the operating microscope used whenever possible. Intraoperative bilateral somatosensory and motor-evoked potentials were combined with cranial nerve monitoring, including brainstem auditory evoked responses, as well as direct stimulation (44).
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” (24, 35). The approach is
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CEREBROVASCULAR Figure 2. Case 2: left tectal plate cavernous malformation. Sagittal T1weighted post-Gd (A) and axial T2-weighted preoperative (B) and
postoperative scans at 2 months (C). Red overlay depicts the operative approach via a left occipital transtentorial approach.
best determined with careful consideration of the anatomy and any available additional imaging information, such as diffusion tensor imaging. Intraoperative neuronavigation is indispensable in delineating the entry approach, in conjunction with neuroanatomical landmarks. The incision into the brainstem and the tract are kept as narrow as possible until the cavernoma is reached. Once inside the cavernoma, any liquefied hematoma is drained. Solid portions of the cavernoma are removed piecemeal, starting centrally, and gradually progressing to the margins, until the lesion is completely removed (Video 1). Most cavernomas are removed in three to five pieces, depending on their size and consistency. Care is taken to remove all of the cavernoma elements while preserving any major veins or en passage arteries. Vigorous removal of the gliotic, hemosiderin-stained margin of the cavernoma is not attempted, especially with large lesions, because the risk of seizures triggered by these residual tissues is nonexistent.
Figure 3. Case 3: left lateral supracerebellar infratentorial approach (red transparent overlay) to dorsal midbrain cavernoma. Sagittal (A), coronal (B), and axial (C) T2-weighted images and axial T2weighted image 14 months postoperatively (D) demonstrating no obvious residual cavernoma.
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Operative Results A total of 27 operative procedures were performed for the 22 patients in the series for their brainstem cavernomas; 31% of the cavernomas were mesencephalic, 35% were pontine, and 19% were located in the medulla (Table 2). Four lesions were large enough to span adjoining domains, including one mesencephalothalamic and three
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approached via a left occipital, transtentorial approach using frameless stereotaxy (Figure 2). As the lesion came to the surface, gross total resection was possible, with new postoperative diplopia noted at 2 months follow-up, and at 1 year, he was asymptomatic, mRS 0. Case 3. A 58-year-old man with known history of CMB and multiple hemorrhages presented with rebleed accompanied by diplopia, right hemibody numbness, and gait ataxia, mRS 2. The cavernoma was located on the left dorsal mesencephalon (Figure 3). We approached the lesion by a lateral supracerebellar infratentorial approach. At 25 months follow-up, patient has resolution of diplopia but slight worsening of right body numbness, mRS 1.
Figure 4. Case 4: CMB located in the right cerebellar peduncle. T2-weighted sagittal (A) and axial (B) images. Three-dimensional diffusion tensor imaging demonstrates medial displacement of rostralcaudal fibers with cavernoma coming to surface of the lateral pons (C). Red overlay illustrates a right transpetrosal approach. (D) Axial T2-weighted image at 10-month postoperative follow-up.
ral orbitozygomatic approach was undertaken (Figure 1). She developed transient left facial weakness and worsening of her left hemiparesis postoperatively. At 20 months after the procedure, she has progressed from an mRS 4 to an mRS 2 with persistence of her mild left-sided weakness. Case 2. An 8-year-old boy presented with vertigo, headVideo available at Midbrain. Case 1. This 23WORLDNEUROSURGERY.org aches, nausea, and vomiting year-old woman developed and was found to have at least left hemiparesis with distal weakness seven supra- and infratentorial cavernous greater than proximal in the arms in legs malformations, including the largest in the (graded 4/5) and hyperreflexia on the ipsitectum, which had evidence of recent hemlateral side. As her cavernoma was situated orrhage on MR imaging, and another in the medulla. The tectal plate cavernoma was in the right peduncle, a right frontotempopontomesencephalic cavernomas. A 91% gross total resection rate was achieved, as assessed by serial MR imaging. In 9% of patients, residual cavernoma was identified on post-operative imaging. No postoperative mortality was observed in this series, and no further surgeries were required in these patients.
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Pons. Case 4. A 43-year-old woman presented with right V1-V3 facial numbness, diplopia, ataxia, and weakness with two symptomatic hemorrhages from a right middle cerebellar peduncle cavernous malformation (Figure 4). Given the location, we opted for a right transpetrosal approach for the lesion. In this instance, diffusion tensor imaging was used during preoperative planning to map the direction of displaced tracts in a rostral-caudal axis. In comparing the side of the brainstem with the cavernoma to the contralateral unaffected side, we found these fibers to be medially displaced, confirming that entry from a lateral approach would be safest. At 27 months postoperatively, her diplopia had resolved, but she has developed a right diminished corneal reflex and slightly worsened V1-V3 numbness. Nevertheless, she is able to drive a vehicle, and her mRS improved from a 2 to a 1. Case 5. A 69-year-old woman presented with acute onset of headache, left hemibody numbness and weakness (4/5), left dysmetria, ataxia, dysphagia, and vertigo with a central pontine hemorrhage secondary to a cavernoma (Figure 5). Because the lesion was located in the midline and did not clearly reach the surface, we opted for a transmaxillary⫺transclival approach, as illustrated in Figure 5. In this case, a transfacial LeFort I maxillotomy was used, with a clivectomy performed with neuronavigation used to guide the trajectory directly to the lesion. This approach, although technically demanding, affords an excellent work-
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Case 7. A 39-year-old man with two previous hemorrhages of a right dorsal lateral pontine cavernoma re-presented with progressive left facial droop, left hemibody numbness, and truncal ataxia. As shown in Figure 7, a right transpetrosal and presigmoid approach was used for extirpation of the lesion. 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. Medulla. Case 8. A 37-year-old woman presented with baseline disequilibrium and previous subtotal resection of dorsal medullary brainstem cavernoma by another neurosurgeon. She represented with sudden deterioration, including numbness in her right arm, intermittent dysphagia, and difficulty breathing. A far lateral retrosigmoid approach was used, and gross total resection was achieved (Figure 8). At 42 months’ follow-up, she has now made a complete recovery (mRS 0).
Figure 5. Case 5: Midline, ventral pontine cavernoma approached via a transmaxillary-transclival approach (red transparent overlay). T1-weighted post-Gd sagittal (A), coronal (B), and axial (C) images. (D) T2-weighted axial scan at 3-year follow-up.
ing view of the ventral pontine surface, including the basilar artery and its associated paramedian perforators, thereby facilitating their preservation. In addition, it represents the most direct pathway to the lesion, without the need to traverse normal brainstem tissue to reach the lesion. Here, the basilar artery was moved gently aside, exposing a small area of discoloration in the midline representing the cavernoma’s emergence at the surface of the pons. After resection, the defect in the clival dura was repaired with placement of two pieces of abdominal fascia beneath the inner surface of dura, followed by application of DuraSeal (Confluent Surgical Inc., Waltham, Massachusetts, USA). An additional two layers of fascia were applied to the outside, secured again with a layer of DuraSeal and Gelfoam
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(Pfizer, New York, New York, USA), and the sphenoid rostrum was covered with a mucosal flap. 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. Her mRS improved from 2 to 1 at 44 months’ follow-up. Case 6. A 57-year-old man who developed sudden onset of headache, dizziness, and gait disturbance was found to have a left lateral pontine hemorrhage as the result of underlying cavernoma (Figure 6). A left subtemporal approach with zygomatic osteotomy was used to gain access to the lateral pons, where the cavernous malformation was observed to come to the surface. At 22 months’ follow up, the patient had improved from an mRS score of 2 to an mRS of 1.
Long-Term Outcomes During the course of follow-up, 54% of patients were noted to improve compared with their preoperative status, whereas 32% remained generally unchanged from a neurologic standpoint. During this time, 14% of patients had declined compared with their preoperative status. The distribution of preoperative mRS and long-term mRS is shown in Figure 9. Of the 9% of patients with residual brainstem cavernomas, no instances of rehemorrhage were recorded. At present, both of these patients have declined reoperation.
DISCUSSION Indications for Removal The vast majority of brainstem cavernous malformations come to attention after a hemorrhage. In general, 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, 39, 42). For deeper seated lesions, a second bleed or progressive neurologic deficit necessitates surgical extirpation of the brainstem cavernoma because it suggests the propensity of the
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surrounding the cavernomas, 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. Unless the cavernoma comes clearly to the pial surface, the direction of approach may not always be optimally defined as the shortest path from the surface to the lesion. Given the eloquence of the brainstem, even a thin parenchymal layer overlying the cavernoma can harbor critical tracts. Complicating this situation is the paucity of widely used and reliable intraoperative methods to identify these displaced and distorted structures. Broadly, we have subcategorized approaches to the brainstem with respect to the midbrain, pons, and medulla.
Figure 6. Case 6: Left, lateral pontine cavernoma with a left subtemporal approach with zygomatic osteotomy depicted with the red overlay. Fluid-attenuated inversion recovery sagittal (A), T1weighted post-Gd coronal (B), and T2-weighted axial preoperative (C) and 22 months postoperative (D) images.
lesion to rebleed in the future. In these instances, carefully weighing the risk of morbidity from surgery compared with that of future re-hemorrhage, on the basis of the natural history of these lesions, tips the balance in favor of surgical intervention (18). This is especially true if deep-seated lesions can be approached through “safe entry” corridors. The use of radiosurgery for cavernous malformations has been reported, with mixed results (27, 30). As such, the use of radiosurgery as a primary treatment modality for cavernous malformations, including those of the brainstem, remains controversial. At present, we advocate surgical resection as the primary means for treatment for high-risk cavernomas of the brainstem. With regard to timing of surgery after a
hemorrhage, although some surgeons advocate delaying surgery until the subacute phase, when the blood products will undergo liquefaction (13, 18, 39); waiting much beyond the first several weeks risks development of gliosis, which may hinder complete resection.
Approaches to the Brainstem Unlike with supratentorial cavernous malformations, those associated with CMBs present a special challenge to the surgeon due to the presence of surrounding brainstem nuclei and tracts (7, 17, 24, 35). As with others, we advocate carefully tailoring the surgical approach to each individual’s lesion. It is incumbent upon the surgeon to recognize the normal anatomy of the region
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Midbrain. The midbrain is subdivided into three general approaches: anteromedial, lateral, and posterior. In the anteromedial approach for interpeduncular lesions, an extended transsylvian corridor is used, with the assistance of an orbitozygomatic craniotomy (18). Slightly more laterally, a subtemporal approach can be used, or in combination with a transsylvian route (31). Laterally, a supracerebellar-infratentorial or petrosal approach can be used to reach mesencephalic cavernomas. Posteriorly, a suboccipital or occipital transtentorial approach can be used to reach lesions centered near the posterior midbrain, including the tectal plate. From a posterior approach, depending on the location of the cavernomas, 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, 21, 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, 17). Otherwise, midline approaches through the tectal plate should be avoided whenever possible given their postoperative morbidity. Through experience, we and others have learned that avoidance of injury to the central tegmentum and adjacent medial longitudinal fasciculus is vital, as the resultant postoperative complications of nystagmus and internuclear ophthalmoplegia, respectively, are particularly debilitating during recovery (17). Pons. The pons is the largest region of the brainstem and the most common location for
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CEREBROVASCULAR Figure 7. Case 7: Right transpetrosal and presigmoid approach (red overlay) to a right dorsal lateral pontine cavernoma. T1-weighted post-Gd axial (A), T2-weighted axial (B), T1-weighted post-Gd sagittal (C), and postoperative 3-month T2-weighted axial image (D). Intraoperative image demonstrating bimanual removal of cavernoma through a small portal in the brainstem (E) and image after gross total resection (F).
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brainstem cavernomas (13, 18, 33, 42). Given its size, a variety of surgical approaches are available to the surgeon, depending on the precise location of the cavernous malformation (Table 2). We have defined approaches to the pons into four categories: dorsal, central, anterolateral, and lateral. From a dorsal approach, a midline suboccipital approach can be used. In such cases, it is paramount to minimize dividing the vermis given associated complications, including truncal ataxia (44). Alternately, a subtonsillar-transcerebellomedullary (telovelar) approach can be used (13, 44), which involves dividing the cerebellomedullary fissure. This approach is useful in accessing pontomedullary and medullary lesions. Unfortunately, unless the cavernoma clearly emerges at the surface of the floor of the fourth ventricle, injury to the medial longitudinal fasciculus, facial, and abducens nerve are common when operating along this region (3, 44). As with others (13, 17, 18, 33), we view the floor of the fourth ventricle with great caution when approaching CMBs, despite the published morphometric descriptions of safe entry zones in the infra- and supra-abducental or facial regions (6, 7, 24). These lesions can be approached if the locations of the facial, vagal, and hypoglossal nuclei are carefully established intraoperatively by direct stimulation. Nevertheless, it may be difficult to avoid the intrinsic portion of the facial nerve tract or the abducens nucleus when resecting cavernomas in immediate vicinity. Postsurgical brainstem tract and nucleus-related complications have been reduced as we have shifted away from posterior approaches to the pons over time. We prefer more lateral or anterolateral approaches to the brainstem, particularly when dealing with deep-seated lesions of the pons. The anterior and anterolateral brainstem tracts are generally more resilient to surgical manipulation than the dorsal pontine and medullary surfaces. A transpetrosal (19, 22, 31, 45) or retrosigmoid approach will enable access to the more anterior surface of the pons (16, 31). A presigmoid approach will yield a more lateral, albeit more direct, view of the pons (20). From any of these approaches, the peritrigeminal area, a “safe entry zone,” can be accessed and safely traversed horizontally, following along the plane of the fibers. This triangular region is bound medially by the
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the posterior intermediate and posterior lateral sulci (9, 17). Generally, a far lateral retrosigmoid approach will suffice for reaching pontomedullary lesions (13). 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, 31). From either approach, safe medullary access is realized by way of entry through the retro-olivary sulcus, which does not result in clinically evidence deficits (35). Finally, strictly anterior cavernomas of the ventral medulla can be reached via a transoral route (36, 44). This was not used in our series due to the absence of any cases requiring it. Because of the concern for CSF leak and associated infection, an alternative is the subtemporal infratemporal approach for these lesions (41). In each case, the guiding principle is to avoid breaching major brainstem tracts or nuclei. If there is no option, then traversing the most accessible route to the brainstem cavernoma must then be chosen on a caseby-case basis. Figure 8. Case 8: Suboccipital approach (red transparent overlay) to cavernous malformation of the dorsal medulla previously with subtotal resection. T2-weighted sagittal (A), coronal (B), and axial preoperative (C), and 3 year postoperative (D) images shown.
pyramidal tract, inferiorly by the pontomedullary sulcus out to the flocculus, and laterally just medial to the root entry zone of cranial nerve V (35). Cavernomas situated directly on the ventral midline surface of the pons require a
Figure 9. Bar graph showing the distribution of the preoperative mRS scores for the 22 patients compared with the distribution at last follow-up. Mean follow-up time was 26.6 months with a range of 2-68 months, SD of 17.7 months.
central approach. For these difficult, but fortunately rare, lesions, we advocate a transmaxillary-transclival approach, which we used during the resection of one of our pontine cavernomas in our series (Table 2). Medulla. The medulla can be approached from the following routes: dorsal, anterior, and anterolateral corridors. As with the pons, a midline suboccipital craniotomy with a telovelar approach can be used to reach the dorsal medullary surface (17, 31). In the upper dorsal medulla, along the inferior floor of the fourth ventricle, risk of injury to the nucleus of XII medially and the nucleus X laterally with resultant ipsilateral tongue weakness and cardiac/respiratory instability, respectively, makes entry from this direction generally contraindicated (13, 17, 18, 33). Furthermore, the medial longitudinal fasciculus underlies these structures medially. For the lower dorsal medulla, safe entry zones are defined by Bricolo as the posterior median fissure and
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Evolution of a Minimally Invasive Resection Technique Once the decision has been made to proceed with resection, careful preoperative planning is essential. When possible, we have used diffusion tensor imaging to study the distortion of the underlying white matter tracts surrounding the lesion (11). It is performed when lesions do not appear to come to the pial surface on MR imaging, so that the corridor for entry through the brainstem may not be as apparent. The utility of such imaging can be limited by susceptibility artifact when one is resecting a relatively fresh hemorrhage, which prevents adequate tractography. Nevertheless, in such cases, 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. Intraoperative cranial nerve monitoring is generally more important for dorsal approaches. For anterior and lateral approaches to the brainstem, motor-evoked potentials are obligatory. Intraoperatively, real-time guidance with frameless stereotaxy registered to the operating microscope
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conservatively with monitoring by serial imaging. These recurrences are tempered against the reduction of expected post-operative complications. We have generally opted for repeated resections, if indicated, for residual brainstem cavernomas, as they do present a risk of rehemorrhage.
Future Developments As technology advances, we anticipate the development of specialized microsurgical instrumentation, including flexible endoscopes and other articulated devices that will facilitate working through highly constrained operative corridors, thereby minimizing damage to the surrounding brainstem tracts and nuclei. The use of the carbon dioxide laser has already been employed for selected cavernomas in the brainstem (G. Steinberg, personal communication, 2010), and we are presently exploring the utility of the flexible CO2 laser (OmniGuide, Cambridge, Massachusetts, USA) at our institution.
CONCLUSION
Figure 10. General technique for resection of brain stem cavernomas. A small window to the cavernous malformation is created, with the direction of access defined by the safest anatomical corridor possible. In this example, for a deep seated lesion in the pons, a lateral ventral approach is chosen (A, inset). From this minimally invasive portal, the cavernoma is initially centrally debulked, and gradually, the wall is gently liberated from the surrounding brainstem parenchyma and removed piecemeal to minimize injury to the surrounding tracts and nuclei (A-E).
field of view is of particular importance during resection of small cavernomas. In the senior author’s experience (L.N.S.), a general approach to brainstem cavernous malformations is to create as small a portal for access to the lesion as feasible, a “minimal access” technique. Through this window, the cavernoma is resected as much as possible, given the constraints of the surrounding anatomic structures. In these cases, the cavernoma generally is internally debulked to decompress the lesion, and the wall is then gently taken down from the surrounding brains-
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tem and disconnected with the use of a bimanual technique (Figure 10). Any associated developmental venous anomalies, which are commonly associated with these lesions (1, 3, 32), or hemosiderin-stained tissue is preserved. This method has been able to yield generally favorable results in the majority of brainstem cavernomas, with the drawback that given the small surgical window, a gross total resection may be impossible to achieve. Reviewing the retrospective data shown above, there have been two recurrences after surgery: both were managed
Our approach to cavernous malformations of the brainstem represents a progressive and iterative refinement of surgical techniques during the past two decades. We have sought to incorporate new technologies, such as image guidance and diffusion tensor imaging, wherever practical. From experience, we have opted to eschew midline approaches to the dorsal midbrain and to the floor of the fourth ventricle, instead selecting operative corridors that are directed more laterally and anteriorly to the brainstem. Finally, we recommend a minimal access technique, wherever possible, which reduces the likelihood of postoperative morbidity due to brainstem nuclear and tract injury at the expense of achieving gross total resection.
REFERENCES 1. Abla AA, Lekovic GP, Turner JD, de Oliveira JG, Porter R, Spetzler RF. Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients. Neurosurgery 682011;403-414discussion 414-405. 2. Abla AA, Turner JD, Mitha AP, Spetzler RF: Surgical approaches to brainstem cavernous malformations. Neurosurg Focus 29:E82010.
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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.
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Received 12 September 2011; accepted 14 April 2012 Citation: World Neurosurg. (2013) 79, 5/6:691-703. http://dx.doi.org/10.1016/j.wneu.2012.04.030 Journal homepage: www.WORLDNEUROSURGERY.org
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