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A
H. Hunt Batjer, M.D., lthough the first reported surgical expe- their ultimate diagnosis after further debilitat-
Department of Neurological Surgery, rience with brainstem cavernous mal- ing or even lethal hemorrhage (92). However,
Feinberg School of Medicine, formations (CMs) dates to 1928, when with widespread use of magnetic resonance
Northwestern University, Dandy evacuated a brainstem hematoma imaging (MRI) and the accumulation of numer-
676 North St. Clair Street,
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attributed to CM hemorrhage (18), studies of ous case reports and surgical series, awareness
Chicago, IL 60611. the natural history and management of these and a progressively more aggressive attitude
Email: h-batjer lesions have only begun to accumulate since toward these lesions has arisen in the literature.
the late 1980s. In the interim, many patients In this article, we comprehensively review nat-
Received, May 28, 2008. with angiographically occult vascular malfor- ural history, surgical, and radiosurgical studies
Accepted, November 5, 2008. mations (AOVMs) of the brainstem were diag- of these lesions, synthesizing clear recommen-
Copyright © 2009 by the
nosed with demyelinating disease (36, 63, 89), dations and highlighting the nuances of partic-
Congress of Neurological Surgeons neoplastic disease (65, 74, 75, 92), infection (36), ular surgical approaches to these malforma-
or brainstem infarction (36), only to receive tions.
Aiba et al., 110 Given for hemorrhagic Prospective New Sx ⫹ Given 0.39%/pt-y if seizures Prior hem, age Location
1995 (1) (110) lesions: 53% lobar Mean, 4.7 y intralesional or subdivided 22.9%/pt-y if prior hem ⬍40 y, F sex
24% BS perilesional bleed 0%/pt-y if 21.5%/pt-y if BS 40 y, F sex
11% BG/T incidental 34%/pt-y if ⬍40 y and F
8% cerebellar
3% callosal
Cantu et al., 133 (133) 55% lobar Retrospective “MRI 1.7%/pt-y 2.33%/pt-y if BS Nonlobar Age, sex
2005 (14) 19% BS Mean, 5 y documented” location
www.neurosurgery-online.com
BRAINSTEM CAVERNOUS MALFORMATIONS
NATURAL HISTORY
on bleed rate
Factors with
no effect
Four percent to 35% of CMs (mean, 15% [Table 1]) are located
BS, brainstem; BG, basal ganglia; T, thalamus; Sx, symptoms; pt-y, patient-year; hem, hemorrhage; supratent, supratentorial; MRI, magnetic resonance imaging; infratent, infratentorial; les-y, lesion-year; ASx,
in the brainstem. Despite the wide range of CM bleed rates
Sex
across our review of natural history studies (Table 1), the range
narrows to 0.7% to 3.1% per patient-year among nonfamilial,
prospective studies that defined hemorrhage as a symptomatic,
radiographically verified extralesional bleed (55, 70); these
deep location
increasing
bleed rate
Factors
Prior hem,c
0%/pt-y if superficial
Subdivided
bleed rates
Overall, 4.2%/pt-y
Patients with a presentation of radiographic hemorrhage and a focal neurological deficit had increased hemorrhage rates (P ⫽ 0.03).
6.5%/pt-y
series (12, 25, 26, 34, 57, 63, 73, 89). Most studies with more lax
definitions of CM hemorrhage (such as a change in symptoms
alone) reported increased hemorrhage rates among brainstem
Acute/subacute blood out-
New Sx ⫹ radiographic
outside ring or increase
Event ⫽ subjective ⫹
in lesion size by
Bleed
intralesional)
surgical series (12, 73). Hemorrhage clustering (6, 89) may con-
and follow-up
Study design
retrospective
Mean, 2.2 y
Mean: 2.2 y
Prospective
Prospective
143 les-y
282 les-y
Familial
46 pt-y
4% cerebellum
Lesion
6% cerebellar
72% lobar
83% lobar
5% BG/T
30% BS
11% BS
4% BS
31 (128)
Porter et al.,
1997 (64)
1991 (70)
1994 (93)
Continues
TABLE 2. Continued
No. of Resection
Series (ref. no.) Early morbidity and mortality Long-term outcome
patients rate
Porter et al., 1999, 117 97% 35% morbidity (12% perm) 87% improved/same,
2000 (62, 63) 10% trach/PEG (2% perm) 9% worse, 3.5% dead
3.5% dead (CP arrest/hem ven infarct) Mean GOS 4.53 (4.4 preop)
Sakai et al., 1991 (71) 5 100% 100% improved; 60% excellent
Samii et al., 2001 (72) 36 100% 67% morbidity (47% CN) Mean KPS 78.2 (70.3 preop), 44% KPS 90
Sandalcioglu et al., 12 100% 83% morbidity (8% perm, VI) –100 42% improved, 50% same, 8.3% worse
2002 (73) Mean mRS 1.6 (2.2 preop)
Scott et al., 1990, 1992 (74, 75) 4 0% 50% morbidity (25% perm) 75% improved (50% ASx), 25% worse
Seifert et al., 2003 (76) 4 100% 75% morbidity (0% perm) 25% ASx, 50% min def, 25% dependent
Shehab et al., 2001 (77) 4 75% 100% morbidity
75% hearing loss, 25% CSF leak
75% mild worse hearing, 25% rebled (residual)
Sindou et al., 2000 (78) 12 92% 83% morbidity (17% perm) Mean KPS 79.2 (60 preop)
58% resp difficulty (8% perm)
67% improved, 17% same, 17% worse
Smith et al., 2003 (79) 7 100% 43% morbidity (0% perm) 100% improved/same (28% ASx)
Mean GOS 4.6
Sola et al., 2007 (80) 17 88% 24% morbidity (12% CN, 12% sensory) 76% improved, 24% same; 82% RTW
Mean KPS 90.6 (70 preop)
Steiger et al., 2006 (82) 3 33% 33% morbidity (hearing) 67% improved, 33% worse (hearing)
Steinberg et al., 2000 (83)e 42 93%e 29% worsee 52% improved, 43% same, 5% worsee
Symon et al., 1991 (85) 7 100% 100% improved
Viñas et al., 2002 (87) 8 63% morbidity (50% CN, 0% perm) 100% improved/same
Wang et al., 2003 (89) 137 96% 72% improved/same,
28% worse, 1% dead; 89% working
Weil and Tew, 1990 (90)f 6 67%f 83% morbidityf 83% improved, RTW; 17% worsef
Yaşargil et al., 1988 (91) 5 100% 100% improved
Yoshimoto and Suzuki, 1986 (92) 3 100% 67% morbidity 33% improved, 67% same
Zausinger et al., 2006 (94) 13 100% 24% morbidity (15% HP, perm)
8% trach (all transient) 85 improved/same
14% slightly worse (mild HP)
Zhao et al., 2007 (95) 9 100% 11% neuro morbidity (0% perm) 100% improved/same
Ziyal et al., 1999 (97) 9 78% 56% morbidity (18% perm), 67% improved,
11% trach/PEG 22% same, 11% worse
Mean GOS 4.6 (4 preop)
a
Trach/PEG, tracheostomy and/or percutaneous gastrostomy; trans, transient; perm, permanent; def, deficit; RTW, return to work; III, third nerve palsy; KPS, Karnofsky Performance
Scale score; preop, preoperative; ASx, asymptomatic; resp, respiratory; GOS, Glasgow Outcome Scale score; VPS, ventriculoperitoneal shunt; postop, postoperative; VI, sixth nerve
palsy; sig, significant; HS, hemisensory; HP, hemiparesis; Sx, symptoms; CN, any cranial nerve palsy; neuro, neurological; min, minimal/minor; mod, moderate; mRS, modified Rankin
Scale score; CP, cardiopulmonary; hem ven, hemorrhagic venous; CSF, cerebrospinal fluid.
b
Eight percent of patients had KPS ⬍70; all of these patients had partially resected lesions that rebled (25).
c
Includes results from Bern only (26); results from Phoenix incorporated in the series of Porter et al. (62, 63).
d
Data for entire surgical series of 29 patients with cavernous malformations of brainstem, basal ganglia, and thalamus (52).
e
Results for entire surgical series of 57 cavernous malformations of the brainstem, basal ganglia, and thalamus (83).
f
Includes results from Kashiwagi et al. (36). A subsequent report by Lewis et al. (48) from the same group documented recurrence (by rebleeding) of 2 lesions. This report incorporated
the results of Weil and Tew (90) and mixed them with results for subsequent brainstem cavernous malformation and arteriovenous malformation extirpation, citing a 93% resection
rate, 56% early neurological morbidity rate, and 85% long-term symptomatic improvement rate.
rence rates as high as 3.5% (2 of 56 patients) and 3.4% (1 of 29 attributable to postoperative edema, intraoperative manipula-
patients) in the deep CM series of Steinberg et al. (83) and tion, and changes in microcirculation (8, 72, 83). In the series of
Mathiesen et al. (52), respectively. Porter et al. (63), 10% of patients required tracheostomy and/or
Early postoperative morbidity is high, ranging from 29% to placement of a feeding tube; similar rates were seen in the
67% in larger surgical series (8, 12, 25, 57, 62, 63, 72, 83). series of Ziyal et al. (97) and Lapras et al. (45), although these
Fortunately, many complications are transient and are likely measures, fortunately, were most often temporary. Long-term
condition was reported as improved in 71%, the same in 19%, Visualization of the quadrigeminal plate is improved, and the
worse in 10%, and dead in 1.9% across 35 series (316 patients). risk of damage to the colliculi is decreased (10). Occipital drain-
Across 45 series (683 patients), 85% of patients were the same ing veins are coagulated, the medial aspect of the occipital lobe
or improved, 14% were worse, and 1.9% were dead. Overall, 16 is then retracted superolaterally, and the tentorium is opened to
of 820 patients (2.0%) died from partially resected CM rebleed- afford clear visualization of the cerebellomesencephalic fissure.
ing (4 cases) or surgically related causes: 5 from infectious com- Challenging dissection of the deep Galenic drainage system
plications, 2 from sudden cardiopulmonary arrest, 2 from ensues. As emphasized by Morcos et al. (54), this approach is
venous infarction, 1 from respiratory failure, and 2 from an limited to unilateral lesions, as the deep drainage system, the
unspecified cause. Importantly, these long-term outcome fig- falx, and the straight sinus obscure the view to lesions extend-
ures are heavily biased by larger surgical series and thus by the ing contralaterally. Despite lumbar drainage, postoperative
work of a few neurosurgeons who are uniquely experienced visual field deficits may be observed, owing to occipital lobe
with these generally rare lesions. Although the overall results retraction, and, more rarely, venous infarction may occur from
from Table 2 are therefore not applicable to the entire neurosur- sacrifice or stretching of bridging veins.
gical community at large, lessons learned from particular sur-
gical approaches (Table 3) to these lesions require emphasis. Anterior and Anterolateral Midbrain CMs
Complete resection of anterior and anterolateral mesencephalic
Posterior Midbrain CMs CMs appeared to meet with more difficulty when subgroups in
Long-term outcomes after resection of posterior midbrain surgical series were reviewed. As seen in all 7 patients (all same
CMs were generally quite good (Table 4): 26 of 30 patients were or improved) in the series of Porter et al. (63), good outcomes
the same or improved at follow-up. In the update of the series of may still be expected for the majority of these lesions, although
Zimmerman et al. (96) by Porter et al. (63), 6 additional patients the increased prevalence of incomplete resection among them (5
were reported as improved or the same. Postoperative oculomo- of 19 patients in Table 4) relatively hampered long-term out-
tor deficits may occur (10, 79, 88, 90), and, less frequently, come, compared with that of more posterior lesions. These CMs
obstructive hydrocephalus from scarring around the cerebral are typically approached via either a subtemporal (8, 24, 54) or
aqueduct has been reported (90). The most commonly used transsylvian approach (80, 97). The transsylvian approach pro-
approach was the supracerebellar infratentorial approach (Fig. 1) vides an ideal angle of attack for anterior or interpeduncular
(62, 83), which afforded excellent results in the majority of cases. CMs, whereas the subtemporal approach is well suited for
After unroofing of the transverse sinus and retraction of the anterolateral CMs. In addition, the subtemporal approach may
dural flap, bridging veins between the vermis and tentorium also be advantageous for more caudal pontomesencephalic CMs,
are divided close to the cerebellar surface. The dissection contin- as, unlike a retrosigmoid approach, it affords a direct viewing
ues with preservation of the precentral cerebellar veins until trajectory toward posterior aspects of the CM without requiring
exposure of the quadrigeminal plate. As illustrated by the 1 fatal- significant brainstem retraction. Lumbar drainage is used to min-
ity from rebleeding in the series of Cantore et al. (13), larger imize retraction injury to the temporal lobe, which, along with
lesions with a significant caudal extent into the pons and fourth potential injury to the third and/or fourth cranial nerves during
ventricle may not be amply exposed by this approach. Although tentorial manipulation (12), comprises the major disadvantage of
a paramedian supracerebellar infratentorial approach may be this approach. Fatal postoperative venous thrombosis was
useful for somewhat posterolateral lesions, more radical resec- reported in 1 case that we reviewed (13).
tion of bone superiorly (extending above the transverse sinus)
and laterally with skeletonization of the sigmoid and transverse Anterior and Anterolateral Pontine CMs
sinus may be used for more laterally situated lesions (88). The Modern, larger surgical series have noted improved long-term
extreme lateral supracerebellar infratentorial approach (modi- recovery after surgery among patients with anterolateral pontine
fied retrosigmoid), described by Vishteh et al. (88), averts the lesions (25, 63). All 15 patients with these lesions in the series of
problem of residual bone between the lateral aspect of the cran- Porter et al. (63) were the same or improved. Only 1 of 20 patients
iotomy and the sigmoid sinus impeding exposure of the lesion. with anterolateral pontine lesions in the series of Ferroli et al. (25)
The far posterior subtemporal approach is another option, had permanent postoperative deficits, compared with 29% of the
described by Smith et al. (79). The authors describe a remaining patients. The mean long-term Karnofsky Performance
horseshoe-shaped incision centered behind the ear. The cran- Scale score in the recent series of Sola et al. (80) was 90.6, and
iotomy is defined caudally by the temporal fossa floor, the ten- notably, the majority of lesions were in the anterolateral pons.
torium is divided, and the cerebellum may then be retracted if With the use of a retrosigmoid approach, 8 of 9 lesions in this
needed. Less cerebellar retraction and a potentially decreased series were completely resected, with all patients improving post-
risk of injury to cranial nerves are advantages of this approach; operatively (except 3 patients with preoperative Karnofsky
however, temporal lobe retraction-related edema and increased Performance Scale scores of 100) to a mean Karnofsky Perform-
risk of injury to the vein of Labbé are potential limitations (79). ance Scale score of 95.6. The retrosigmoid approach is a common
The occipital transtentorial approach (53, 54) is another alter- choice for lesions of the anterolateral pons (8, 46, 78, 80). Despite
native for patients with a steeply sloping tentorium, lateral limited ventral exposure, this approach was aptly chosen in 30
lesions, or lesions somewhat ventral to the tectal plate. cases reviewed, leading to complete resection in 93%. Only 3 of 30
a
OZ, orbitozygomatic; CSF, cerebrospinal fluid; CM, cavernous malformation; GSPN, greater superficial petrosal nerve; IV, fourth ventricle.
patients worsened postoperatively, whereas 14 of 30 patients were the ear, followed by craniotomy, limited posterior mastoidectomy,
neurologically intact at follow-up. The extended retrosigmoid skeletonization of the sigmoid sinus, and anterior mobilization of
approach is an alternative with added ventral exposure that was the sinus with a dural flap. The added exposure from this
recently described by Quiñones-Hinojosa et al. (66). The authors approach is balanced by the potential for venous sinus thrombo-
described a C-shaped skin incision from the mastoid tip around sis and increased risk of cerebrospinal fluid (CSF) fistula.
TABLE 4. Results for brainstem cavernous malformation resection, subdivided by location and approacha,b
No. of Resection Early
Series (ref. no.) Approach Long-term outcome
patients rate morbidity
Posterior midbrain
Bertalanffy et al., 1991 (9) 3 SI 3/3 100% intact (all obstructive HCP preop)
Bertalanffy et al., 2002 (8) 2 OT 2/2 1 same, 1 worse (cereb)
Bouillot et al., 1996 (10) 2 SI 0/2 1 IV 1 improved, 1 worse
Pendl et al., 1990, 1991 (59, 60) 2 SI Both improved (KPS 90, 100 from 20, 40 preop)
Sandalcioglu et al., 2002 (73) 2 SI 2/2 Both improved (mRS 0, 1 from 1, 2 preop)
Sindou et al., 2000 (78) 2 OT 2/2 1 improved, 1 worse (needing trach)
Smith et al., 2003 (79) 7 Far posterior ST 7/7 2 INO 100% same or improved (mean GOS
1 confusion, aphasia 4.6, 28% intact)
Vishteh et al., 1999 (88) 5 ELSI 4/5 1 IV All improved (all GOS 1)
Weil and Tew, 1990 (90) 3 Infratent 3/3 2 new CN, 1 HCP 2 improved, 1 worse
Vermis splitting 1 worse ataxia
Zimmerman et al., 1991 (96)c 2 SI 2/2 1 improved, 1 same
Anterior midbrain
Bertalanffy et al., 2002 (8) 3 ST 3/3 1 KPS 100, 2 KPS 90
Bouillot et al., 1996 (10) 4 ST 3/4 2 intact, 1 improved, 1 dead (VT)
Fahlbusch et al., 1991 (24) 2 ST Both improved
Houtteville, 1995 (33) 2 ST 1/2 Both improved, 1 intact
Kikuta et al., 2004 (39) 2 ST 1/2 mRS 3, 5 (mRS 2, 5 preop)
Morcos et al., 1999 (54) 2 ST 1/2 1 improved, 1 worse (rebled)
Sola et al., 2007 (80) 2 Pterional TS 1/2 1 transient diplopia Both KPS 100 (30 and 90 preop)
Viñas et al., 2002 (87) 2 ST 1 transient CN Both same/improved
Zimmerman et al., 1991 (96)c 2 ST 2/2 1 transient HP Both improved
Ziyal et al., 1999 (97) 2 OZ TS 2/2 No early neuro Both improved, mean
morbidity GOS 4.5 (4 preop)
Anterior/anterolateral pons
Bertalanffy et al., 2002 (8) 3 Retrosigmoid 3/3 1 CSF leak 2 improved, 1 same
Mean KPS 93.3 (70 preop)
Bertalanffy et al., 2002 (8) 2 ST ⫹ retrosigmoid 2/2 1 CSF leak Both improved to KPS 100
Lena et al., 2002 (46) 2 Retrosigmoid 1/2 Both intact
Sandalcioglu et al., 2002 (73) 4 Retromastoid 4/4 3 improved/same, 1 worse
Mean mRS 1.5 (2 preop)
Seifert et al., 2003 (76) 4 Retrolabyrinthine 4/4 1 CSF leak, 1 1 intact, 2 minor deficits,
hearing, 1 TP 1 dependent
Shehab et al., 2001 (77) 4 Partial translab 3/4 1 CSF leak, 3 3 mildly worse hearing,
hearing, 1 CN 1 residual rebled
Sindou et al., 2000 (78) 2 Retrosigmoid 2/2 2 trans resp disturbances 2 improved (KPS 80, 90)
Sola et al., 2007 (80) 9 Retrosigmoid 8/9 6 improved, 3 same
Mean KPS 95.6 (84.4 preop)
Steiger et al., 2006 (82) 3 Transdural ant petrosal 1/3 1 worse hearing 2 improved, 1 worse
Viñas et al., 2002 (87) 4 Transpetrosal 1 CN All improved/same
Zausinger et al., 2006 (94) 10 Retromastoid 10/10 2 new HP 8 improved (4 intact), 2 new HP
Floor of fourth ventricle
Bertalanffy et al., 1991 (9) 7 Median suboccipital 7/7 4/7 morbidity 6 improved (3 intact), 1
worse (air embo, bedridden)
Bertalanffy et al., 2002 (8) 6 IT 6/6 5 improved (1 intact), 1 same
Mean KPS 78.3 (65 preop)
Continues
TABLE 4. Continued
No. of Resection Early
Series (ref. no.) Approach Long-term outcome
patients rate morbidity
Bertalanffy et al., 2002 (8) 2 Occip interhem 2/2 1 improved, 1 worse (worse ataxia, diplopia)
transtent transvelum Mean KPS 70 (70 preop)
Bouillot et al., 1996 (10) 9 Median suboccipital 7/9 1 rebled, 1 dead 7 improved (3 intact), 1 same, 1 dead
Bruneau et al., 2006 (12) 8 IT 8/8 2/8 neuro morbidity All improved/same
Di Rocco et al., 1997 (20) 3 Median suboccipital 3/3 1 transient VII All improved (1 intact)
Eisner et al., 1995 (22) 7 Inf vermis splitting 7/7 2 CN, 1 HP, 2 ocular All improved/same
Fahlbusch et al., 1991 (24) 6 Vermis splitting motility 5 improved, 1 worse
Isamat and Conesa, 1993 (34) 6 IT/inf vermis splitting 6/6 3/6 morbidity (3 CN) All improved, RTW; 3 intact
Kikuta et al., 2004 (39) 7 Median suboccipital 5/7 4 improved (2 intact); 2 same, 1 worse
Mean mRS 1.4 (2.7 preop)
Mizoi et al., 1992 (53) 4 Vermis splitting 4/4 All improved/same with “good” outcomes
Sakai et al., 1991 (71) 3 Vermis splitting 3/3 All improved, 1 “excellent”
Sandalcioglu et al., 2002 (73) 3 Subcerebellar 3/3 All same mRS score
Mean mRS 1.3
Sindou et al., 2000 (78) 6 IT 5/6 4/6 morbidity 3 improved, 2 same, 1 worse
2 resp disturbances, Mean KPS 80 (70 preop,
1 CSF fistula, 1 HCP 2 comatose)
Symon et al., 1991 (85) 6 Inf vermis splitting 6/6 1 trans loss of gag All improved
Weil and Tew, 1990 (90) 3 Inf vermis splitting 3/3 2/3 morbidity All improved, RTW
1 INO, ataxia; 1 VI, VII
Yoshimoto and Suzuki, 1986 (92) 2 Vermis splitting 2/2 1 trans oculomotor deficit Both improved
Zausinger et al., 2006 (94) 4 Median suboccipital 4/4 1 trach All improved
Ziyal et al., 1999 (97) 2 IT 1/2 Both worse (CN) Both improved, both GOS 5
1 trach, PEG; 1 VPS
a
SI, supracerebellar infratentorial; HCP, hydrocephalus; preop, preoperative; OT, occipital transtentorial; cereb, any cerebellar deficit; IV, fourth nerve palsy; KPS,
Karnofsky Performance Scale score; mRS, modified Rankin Scale score; trach, tracheostomy; ST, subtemporal; INO, internuclear ophthalmoplegia; GOS, Glasgow
Outcome Scale score; ELSI, extreme lateral supracerebellar infratentorial; infratent, infratentorial; CN, any cranial nerve deficit; VT, venous thrombosis; TS, transsylvian;
OZ, orbitozygomatic; neuro, neurological; CSF, cerebrospinal fluid; TP, tetraparesis; translab, translabyrinthine; trans, transient; resp, respiratory; ant, anterior; HP,
hemiparesis; embo, embolism; IT, intertonsillar/transcerebellomedullary fissure; occip interhem transtent transvelum, occipital interhemispheric transtentorial transvelum
medullare; VII, seventh nerve palsy; inf, inferior; RTW, return to work; VI, sixth nerve palsy; PEG, percutaneous gastrostomy; VPS, ventriculoperitoneal shunt.
b
From a review of series providing sufficient individual patient data for at least 2 patients undergoing the same approach.
c
Earlier detailed report of the first set of patients in the larger series of Porter et al. (62, 63).
Although combined far lateral-subtemporal and retrosigmoid- observed in 3 of 4 patients, although it was mild. Translabyrin-
subtemporal approaches are always options, the wider, more thine and transcochlear exposures, considerations for patients
ventral exposure afforded by the transpetrosal approaches with preoperative complete hearing loss, are exceedingly rarely
makes them an attractive choice for surgeons who are well indicated. The anterior transpetrosal (Kawase) approach has
versed in petrous bone drilling for added ventral exposure (Table been described for 4 CMs in our reviewed series (8, 82). Its added
3). The posterior transpetrosal approaches fall along a spectrum caudal exposure, as compared with the standard subtemporal
of increasing petrous bone resection, affording progressively approach, makes it an option for ventral lesions of the middle
wider, more anterior exposure. As more bone is resected, the third of the pons (54). In the series of Steiger et al. (82), which
risk of complications such as CSF leaks and seventh and eighth emphasized the ability to tailor petrous apex resection via trans-
nerve palsies progressively increases as well. We feel that the dural drilling, 1 of 3 lesions was completely resected. Although
retrolabyrinthine approach, combined with a far lateral or sub- the medial aspect of the petrous bone can theoretically be
temporal exposure if needed, is sufficient for the vast majority of resected “with impunity,” 1 of 3 patients with CMs (1 of 9 over-
anterior/anterolaterally situated brainstem CMs. Among larger all) had postoperative hearing loss.
series, Porter et al. (63) used a retrolabyrinthine approach in 5 of
86 cases; Ferroli et al. (25) used it for 3 of 52 cases. The partial CMs Abutting the Floor of the Fourth Ventricle
labyrinthine approach is a hearing-preserving alternative with Lesions abutting or protruding into the floor of the fourth
added exposure via drilling of the petrous apex (32, 77). When ventricle were traditionally resected after a median suboccipi-
applied to CM resection by Shehab et al. (77), hearing loss was tal, vermis-splitting approach (24, 53, 71, 90, 92). The potential
term permanent morbidity rates from radiation injury and shown to be significantly greater than radiosurgery of arteri-
rebleeding ranging from 7% to 27% and mortality rates ranging ovenous malformations (35, 61). As hemorrhage clustering
from 0% to 13% (3, 21, 28, 40, 49). The general radiosurgical among aggressive lesions may abate after a “natural” 2-year
series of Hasegawa et al. (30) and Pollock et al. (61) have latency period (6), the efficacy of radiosurgery remains
reported permanent radiation-induced morbidity rates of 12% unproven, making it an alternative to observation, not to sur-
(6 of 52 patients) and 33% (4 of 12 patients), respectively, for gery, of aggressive lesions.
patients with brainstem AOVMs. Several general radiosurgical
series have demonstrated dramatic decreases of annual CM
Surgical Approach and Excision
rebleed rates after a 2-year “latency period” to as low as 0.8% The vast majority of authors advocate subacute CM removal
(15, 30, 50, 61). This phenomenon was not seen in all radiosur- (12, 24, 34, 48, 57, 80, 83, 89), allowing for posthemorrhage
gical series, however (35, 38), and may merely reflect the natu- edema to diminish and hematoma liquification. At times, the
ral history of the lesions (6). hematoma can facilitate excision by creating a clean dissection
plane (12, 24, 48, 83, 89). In the chronic stage after hematoma
DISCUSSION organization, gliosis, and malformation adherence to the gliotic
capsule, dissection planes are often obscured (12, 48, 83, 89).
Patient Selection and Timing Several series have shown late surgery to be significantly asso-
ciated with worse outcomes (12, 24, 73); however, early relief of
While increasing familiarity with the surgical treatment of mass effect, at least in part, contributes to improved results of
brainstem CMs may broaden the neurosurgeon’s criteria for early surgery. Frameless stereotaxy, brainstem auditory evoked
surgical management, lessons learned from natural history potentials, somatosensory evoked potentials, and intraopera-
studies and surgical results have led us to the following inclu- tive mapping of cranial nerve nuclei (22, 84) are important intra-
sion criteria: 1) at least 2 prior clinically significant hemorrhagic operative adjuncts (8, 48, 62, 73, 80, 83, 97). Ultrasound may be
events, and 2) pial or ependymal representation on T1-weighted useful as well, assisting with intraoperative brainshift affecting
MRI scans (Fig. 1). With the exception of life-threatening emer- neuronavigation (95) and ensuring complete excision (48).
gent cases and patients with significant, progressive neurologi- Several recent series advocate a respect for the floor of the
cal deterioration, we generally await a second clinical event to fourth ventricle (12, 25, 63). We concur; if a CM is not visible on
essentially define the CM as aggressive. It is clear from natural the floor, we will conclude the operation. This conservative
history studies that some lesions have the potential for a benign approach is based on recent results showing worse outcomes
course (23, 47, 49). Asymptomatic patients who may very well for lesions of the floor of the fourth ventricle (23, 25, 63) and the
never experience hemorrhage from their lesion should not face fact that a small rim of functional parenchymal tissue may be
the 29% to 67% risk of early morbidity and 15% risk of long- compressed between the lesion and ependymal surface.
term worsening (in the best of hands) after surgery (rates based Neuroanatomic landmarks and intraoperative mapping may
on series with primarily symptomatic patients). CMs in patients become unreliable (63). The literature describing “safe entry
who have experienced 2 hemorrhages are far more likely to fol- zones” through the floor of the fourth ventricle is conflicted,
low the aggressive paths described by Pozzati et al. (65) and with some authors advocating a paramedian incision to avoid
Tung et al. (86). The neurological risk of surgery at this point is damage to the medial longitudinal fasciculus (13, 24) and oth-
less than the expected morbidity of a third hemorrhage, which, ers advocating a median incision to avoid the risk of disrupting
as these 2 aforementioned studies have shown, is likely to be the dorsolateral pontomedullary vascular supply (8, 10, 11).
more severe and persistent. On the other hand, with intraoperative neuronavigation, we
The eloquence of the brainstem necessitates being afforded advocate the use of small (⬍1 cm) longitudinal incisions on
with a direct surgical view of the lesion, namely via pial or the anterolateral aspect of the pons in the peritrigeminal area if
ependymal representation. Preoperatively, this is best assessed needed (68). These incisions are generally well tolerated, as the
by T1-weighted MRI scans to avoid being misled by the poten- area contains the transverse fibers of the middle cerebellar
tial “blooming effect” from the ferromagnetic properties of peduncle (25, 63, 78). Recalde et al. (68) recently presented
hemosiderin (83) on T2-weighted imaging. Nonetheless, even detailed anatomic descriptions of the “relatively safe” entry
T1-weighted images may inaccurately depict the lesion’s rela- zones to the mesencephalon (lateral mesencephalic sulcus) and
tion to the brainstem surface (58, 94). Although some series medulla (olivary body) as well. We never allow a simple
have demonstrated impressive results after the extirpation of “bulge” of the brainstem to dictate an incision point for CM
deep-seated CMs (8, 11, 12), our experience is more consistent removal; it may contain vital functional tissue (84), and the CM
with that of Ferroli et al. (25) in their large series (9% worse itself may be unexpectedly deep.
long-term condition if superficial versus 29% worse if deep), Once the lesion and hematoma are reached, the hematoma is
fashioning our surgical inclusion criteria. drained and a peripheral cleavage plane is defined. Small feed-
Patients with deep- seated, surgically inaccessible, and ers to the CM are coagulated at low power at the surface of the
aggressive CMs may be considered for radiosurgery at modest CM with ongoing irrigation. Larger lesions are removed piece-
doses (12–14 Gy marginal dose, to decrease complications [50]). meal to minimize retraction. After removal, the cavity is thor-
Nonetheless, the morbidity of AOVM radiosurgery has been oughly inspected for hemostasis and residual lesion. Complete
extirpation is the rule, leaving the surrounding hemosiderin- 6. Barker FG 2nd, Amin-Hanjani S, Butler WE, Lyons S, Ojemann RG, Chapman
stained parenchyma and developmental venous anomaly intact PH, Ogilvy CS: Temporal clustering of hemorrhages from untreated cavernous
malformations of the central nervous system. Neurosurgery 49:15–24, 2001.
(25, 63, 73, 83, 89). 7. Batay F, Bademci G, Deda H: Critically located cavernous malformations.
Minim Invas Neurosurg 50:71–76, 2007.
Recent Advances 8. Bertalanffy H, Benes L, Miyazawa T, Alberti O, Siegel AM, Sure U: Cerebral
cavernomas in the adult. Review of the literature and analysis of 72 surgically
The burden of inaccurate preoperative MRI may soon abate
treated patients. Neurosurg Rev 25:1–55, 2002.
with preoperative 3-dimensional constructive interference in 9. Bertalanffy H, Gilsbach JM, Eggert HR, Seeger W: Microsurgery of deep-
steady state MRI, as described by Zausinger et al. (94). These seated cavernous angiomas: Report of 26 cases. Acta Neurochir (Wien)
authors reported improved judgment of the thickness of the 108:91–99, 1991.
10. Bouillot P, Dufour H, Roche PH, Lena G, Graziani N, Grisoli F: Angio-
parenchymal layer over the lesion, a sharper peripheral rim of
graphically occult vascular malformations of the brain stem: Apropos of 25
the lesion, and clearer visualization of the spatial relations of cases [in French]. Neurochirurgie 42:189–201, 1996.
the lesion to fairly safe entry zones. In addition to neuronavi- 11. Bricolo A, Turazzi S: Surgery for gliomas and other mass lesions of the brain-
gation, intraoperative endoscopy to ensure complete lesion stem. Adv Tech Stand Neurosurg 22:261–341, 1995.
12. Bruneau M, Bijlenga P, Reverdin A, Rilliet B, Regli L, Villemure JG, Porchet F,
excision was reported by Sandalcioglu et al. (73). Quiñones-
de Tribolet N: Early surgery for brainstem cavernomas. Acta Neurochir
Hinojosa et al. (67) used a modified Kartush stimulator to intra- (Wien) 148:405–414, 2006.
operatively map descending corticospinal tracts in the cerebral 13. Cantore G, Missori P, Santoro A: Cavernous angiomas of the brain stem. Intra-
peduncle before excision of a peduncular CM with hemo- axial anatomical pitfalls and surgical strategies. Surg Neurol 52:84–94, 1999.
14. Cantu C, Murillo-Bonilla L, Arauz A, Higuera J, Padilla J, Barinagarrementeria
siderin staining at the brainstem surface. Chen et al. (17) used F: Predictive factors for intracerebral hemorrhage in patients with cavernous
diffusion tensor imaging with white matter tractography trans- angiomas. Neurol Res 27:314–318, 2005.
ferred to their intraoperative neuronavigation system to clearly 15. Chang SD, Levy RP, Adler JR Jr, Martin DP, Krakovitz PR, Steinberg GK:
visualize the relation of the lesion to the lemnisci and descend- Stereotactic radiosurgery of angiographically occult vascular malformations:
14-year experience. Neurosurgery 43:213–221, 1998.
ing corticospinal tracts. Results from this series were impres- 16. Chaskis C, Brotchi J: The surgical management of cerebral cavernous
sive (Table 2); all pyramidal and sensory deficits were the same angiomas. Neurol Res 20:597–606, 1998.
or improved postoperatively. 17. 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) 149:1117–1131, 2007.
CONCLUSIONS 18. Dandy WE: Venous abnormalities and angiomas of the brain. Arch Surg
17:715–793, 1928.
Brainstem location, prior hemorrhage, and female sex all 19. Del Curling O Jr, Kelly DL Jr, Elster AD, Craven TE: An analysis of the natu-
increase the risk for subsequent clinically significant bleeding ral history of cavernous angiomas. J Neurosurg 75:702–708, 1991.
20. Di Rocco C, Iannelli A, Tamburrini G: Cavernous angiomas of the brain stem
from CMs, whereas lesion size does not. Patients with at least in children. Pediatr Neurosurg 27:92–99, 1997.
2 prior symptomatic bleeds or progressive neurological deficits 21. Duma CM, Lunsford D, Kondziolka D, Bissonette DJ, Somaza S, Flickinger
with pial or ependymal representation of their CM are good JC: Radiosurgery for vascular malformations of the brain stem. Acta
candidates for microsurgical extirpation. Patients with asymp- Neurochir Suppl (Wien) 58:92–97, 1993.
22. Eisner W, Schmid UD, Reulen HJ, Oeckler R, Olteanu-Nerbe V, Gall C,
tomatic lesions should be observed. Complete microsurgical Kothbauer K: The mapping and continuous monitoring of the intrinsic motor
excision is the rule. Retrosigmoidal or other approaches to the nuclei during brain stem surgery. Neurosurgery 37:255–265, 1995.
anterolateral pons are generally less morbid than excision via 23. Esposito P, Coulbois S, Kehrli P, Boyer P, Dietemann JL, Rousseaux P, Auque
the floor of the fourth ventricle; extirpation of intrinsic lesions J, Maitrot D: Place of surgery in the management of brainstem cavernomas:
Results of a multicentric study [in French]. Neurochirurgie 49:5–12, 2003.
through the floor of the fourth ventricle should be avoided. 24. Fahlbusch R, Strauss C, Huk W: Pontine- mesencephalic cavernomas:
Indications for surgery and operative results. Acta Neurochir Suppl (Wien)
Disclosure 53:37–41, 1991.
The authors have no personal financial or institutional interest in any of the 25. Ferroli P, Sinisi M, Franzini A, Giombini S, Solero CL, Broggi G: Brainstem
drugs, materials, or devices described in this article. cavernomas: Long-term results of microsurgical resection in 52 patients.
Neurosurgery 56:1203–1214, 2005.
26. Fritschi JA, Reulen HJ, Spetzler RF, Zabramski JM: Cavernous malformations of
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Marco Lee
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97. Ziyal IM, Sekhar LN, Salas E, Sen C: Surgical management of cavernous mal-
T he authors present an extremely thorough review of brainstem CMs
based on the relevant literature and their own expertise in cere-
brovascular neurosurgery. Cogent points in the natural history section
formations of the brain stem. Br J Neurosurg 13:366–375, 1999. include a discussion on how the estimated annual bleeding rate of CMs
varies widely in previous reports on the basis of the definition of hem-
COMMENTS orrhage, and the observation that many patients have complete neuro-
logical recovery after a single bleeding episode. The recommendation