J Neurosurg 72:698-702, 1990
Stereotactic resection of occult vascular malformations DUDLEY H . DAVIS, M . D . , AND PATRICK J. KELLY, M . D . Department o f Neurosurgery, Mayo Clinic and M a y o Medical School, Rochester, Minnesota
v" Angiographically occult vascular malformations can be identified on computerized tomography and magnetic resonance imaging. Surgical excision, when possible, is the treatment of choice in symptomatic lesions. Because these malformations are usually small and can be located in surgically treacherous areas of the brain, stereotactic resection should be considered. Stereotactic resection of a pathologically verified occult vascular malformation was performed in 26 patients in this series (13 females and 13 males, mean age 30 years). Seventeen patients presented with a seizure disorder, four with an intracerebral hemorrhage, and four with a progressive neurological deficit; one patient was asymptomatic. Sixteen patients had normal neurological examinations, nine had neurological signs referable to their lesion, and one had a visual field deficit related to a previous temporal lobectomy. In six patients evidence of acute hemorrhage was found on imaging studies or at surgery, and 11 patients had evidence of previous hemorrhage on imaging studies, determined at surgery or by histological examination. Three patients had evidence of both acute and previous hemorrhage and six patients had no evidence of hemorrhage. Lesions were located in cortical or subcortical areas in 21 patients, in the thalamus or basal ganglia in three, and in the posterior fossa in two. Following stereotactic resection, 24 patients were improved, one patient was unchanged, and one patient was worse. Without stereotaxis or intraoperative ultrasound studies, localization of these lesions at conventional craniotomy can be difficult. A stereotactic craniotomy is ideally suited to the treatment of these benign circumscribed, but potentially devastating lesions. KEY WORDS cryptic lesion 9 arteriovenous m a l f o r m a t i o n 9 seizure 9 occult arteriovenous malformation 9 stereotaxis 9 intracerebral h e m o r r h a g e ~
V
ASCULAR m a l f o r m a t i o n s o f the b r a i n m a y cause headache, a c u t e h e m o r r h a g e , seizures, or progressive n e u r o l o g i c a l deficits. 4"9'' ~"~8,2o.2, It is well established that s o m e m a l f o r m a t i o n s m a y be clinically silent or " c r y p t i c " p r i o r to h e m o r r h a g e . ~o.~2,~7T h e y m a y p r o d u c e no a n g i o g r a p h i c a b n o r m a l i t y with the exception o f m a s s effect a n d h a v e b e e n d e s c r i b e d as angiographically " O c c u l t . ''4"9"t5"2~ P r i o r to the d e v e l o p m e n t o f c o m p u t e r i z e d t o m o g r a p h y (CT) a n d m a g n e t i c resonance ( M R ) i m a g i n g such lesions c o u l d o n l y be suspected w i t h o u t surgical o r a u t o p s y verification. W i t h these i m a g i n g t e c h n i q u e s , d i a g n o s i s o f an occult vascular m a l f o r m a t i o n c a n be m a d e with a high degree o f accuracy. 2'9'13'15'16'21 O n CT, the lesions can a p p e a r as small, h y p e r d e n s e m a s s e s t h a t m a y show m o t t l e d calcification. T h e y s h o w m i l d to m o d e r a t e contrast enh a n c e m e n t a n d little m a s s effect in the absence o f h e m o r r h a g e . O n M R i m a g i n g , the lesions a p p e a r as heterogeneous, c i r c u m s c r i b e d masses that will have signal-void areas s e c o n d a r y to t h e p a r a m a g n e t i c effect o f h e m o s i d e r i n . L o w - g r a d e n e o p l a s m s are frequently in the differential diagnosis. 698
Surgical excision is the t r e a t m e n t o f choice to establish a histological diagnosis, a m e l i o r a t e s y m p t o m s a n d signs, a n d p r e v e n t f u r t h e r n e u r o l o g i c a l deterioration. 4"~'~'~s2~ Since t h e r e is n o a n g i o g r a p h i c a b n o r m a l i t y a n d the lesions are small, surgical localization m a y be difficult. F o r d e e p lesions or lesions l o c a t e d in essential areas, precise l o c a l i z a t i o n a n d resection are critical to a successful o u t c o m e . Stereotactic c r a n i o t o m y p e r m i t s a c c u r a t e l o c a l i z a t i o n a n d resection o f these lesions with m i n i m a l t r a u m a to t h e s u r r o u n d i n g tissues. Stereotactic resection o f a histologically verifiied occult vascular m a l f o r m a t i o n has b e e n a c c o m p l i s h e d in 26 patients a n d this g r o u p f o r m s t h e basis for this report. Operative Technique
T h e t e c h n i c a l details o f stereotactic c r a n i o t o m y have been r e p o r t e d p r e v i o u s l y ? -8 Briefly, all patients underw e n t a stereotactic C T scan a n d , in s o m e cases, a stereotactic M R i m a g e was o b t a i n e d as well. A stereotactic a n d stereoscopic c e r e b r a l a n g i o g r a m was o b t a i n e d unless an a n g i o g r a m h a d b e e n t a k e n p r i o r to referral, a n d o u r review c o n f i r m e d n o v a s c u l a r a b n o r m a l i t y . J. Neurosurg. / Volume 7 2 / M a y , 1990
Stereotactic resection of occult vascular malformations TABLE 1
Clinical summary of 26 patients with occult vascular malJormations Case No.
Hemorrhage* (acute/ previous)
Presentation
Location of Lesion
1
43, M
2 3
23, M 24, F
progressive neurological deficit seizures seizures
rt thalamus and rostral midbrain rt occipital rt temporal
-/+ -/+
4 5 6 7 8
45, 67, 16, 29, 50,
rt central-parietal rt frontal It temporal It temporal inferior vermis
-/+/-/-/-/+
9
23, M
seizures seizures seizures seizures progressive neurological deficit progressive neurological deficit seizures seizures seizures acute hemorrhage seizures seizures
increased deficit, died one postop seizure decreased seizure frequency no seizures no seizures no seizures no change in seizures deficit improved
caudal fourth ventricle
+/+
deficit improved
3
It frontal It central-frontal It temporal rt frontal rt temporal It temporal
+/-/-/+/+ -/+ -/+
no seizures no seizures no seizures no deficit no seizures decreased seizure frequency no seizures no deficit
16 40 13 36 23 8
no seizures one postop seizure no seizures no seizures deficit improved no deficit no deficit decreased seizure frequency deficit improved
25 15 3 4 9 13 4 6
M M M M M
10 11 12 13 14 15
35, 39, 35, 3, 20, 44,
F F F F F M
16 17
41, M 13, M
18 19 20 21 22 23 24 25
4, 30, 32, 3, 32, 43, 10, 12,
26
45, F
M F F M F F F F
-/+
seizures progressive neurological deficit seizures seizures seizures seizures acute hemorrhage acute hemorrhage incidental finding seizures
rt frontal It parietal
-/+ +/-
It frontal rt temporal rt frontal rt frontal It temporal rt basal ganglia rt frontal rt central-frontal
-/+ -/+ -/+ +/+/+/-/-/+
acute hemorrhage
rt basal ganglia
+/+
Result
Follow-Up Period (mos)
Age (yrs), Sex
55 2 2 54 1 22 3 29
15 24
3
* Evidence of acute hemorrhage was based on radiographic findings or operative findings; evidence of previous hemorrhage was based on magnetic resonance imaging signs of previous hemorrhage, operative findings of hemosiderin, or histological demonstration of hemosiderin. + = signs present; - = no signs.
Surgical planning was accomplished at a console* that displayed the imaging studies. A target volume was digitized from the stereotactic CT scan and/or stereot a c t i c M R i m a g e as d e t a i l e d i n p r e v i o u s r e p o r t s . 5'7"8 A central target point was then selected and viewed on the angiographic studies, and various trajectories could be simulated on the display screen. Sulci could be identified on the stereoscopic-stereotactic angiogram. In some cases a trajectory through a sulcus was selected to minimize the dissection to the lesion. Cross sections of the reconstructed lesional volume could be visualized along the trajectory with the outline of either a trephine opening or a stereotactic retractor superimposed on the i m a g e as r e p o r t e d p r e v i o u s l y ? "6 All p a t i e n t s u n d e r w e n t s t e r e o t a c t i c c r a n i o t o m y u n d e r * System, Model 3-260, m a n u f a c t u r e d by Sun Microsysterns, M o u n t a i n View, California; V M E image processor m a n ufactured by V i c o m Systems, San Jose, California; system, Model M V 7800, m a n u f a c t u r e d by D a t a General, Westboro, Massachusetts.
J. Neurosurg. / Volume 7 2 / M a y , 1990
general anesthesia. The target point was placed in the f o c a l p o i n t o f t h e s t e r e o t a c t i c f r a m e . A 1 89 d i a m e t e r trephine craniotomy was performed in line with the s e l e c t e d t r a j e c t o r y . F o r s u p e r f i c i a l l e s i o n s t h e c r o s s sect i o n s o f t h e r e c o n s t r u c t e d v o l u m e w e r e u s e d as a t e m p l a t e t o l o c a l i z e a n d e x c i s e t h e l e s i o n . F o r d e e p e r lesions, a stereotactic retractor was placed through a cortical incision and advanced to the lesion. Again using the volumetric reconstruction as a guide, the lesion was excised.
Summary of Cases Clinical D a t a The clinical profiles of the 26 patients are summar i z e d i n T a b l e 1. T h e r e w e r e 13 f e m a l e a n d 13 m a l e patients. Ages ranged from 3 to 67 years (mean 30 years). S e v e n t e e n p a t i e n t s p r e s e n t e d w i t h a s e i z u r e disorder, four patients with an acute hemorrhage, and four with a progressive neurological deficit; one patient was asymptomatic. Neurological examinations were normal 699
D. H. Davis and P. J. Kelly in 16 patients, while nine patients had neurological signs referable to their lesion. One patient had a superior quadrantanopsia related to a previous temporal lobectomy.
Radiographic Findings Twenty-one lesions were located in cortical or subcortical areas, three in the thalamus or basal ganglia and two in the posterior fossa (one in the vermis and one in the caudal fourth ventricle). All patients underwent CT and typical features o f an occult vascular malformation were found. All patients had angiography either at our institution or at their referring hospital. The angiograms were reviewed and showed no evidence of abnormal vascularity. Most lesions were 1 to 2 cm in diameter and only one lesion had a diameter greater than 3 cm. In this patient there had been a previous hemorrhage with h e m a t o m a adjacent to the lesion. Pathological Findings All patients had histological confirmation o f a vascular malformation. A diagnosis of arteriovenous malformation was m a d e in 18 cases, nonspecific "vascular malformation" in six cases, and cavernous hemangioma in two cases. Complications One patient (Case 1) who presented with diplopia was found to have a cystic contrast-enhancing lesion in the rostral midbrain and right thalamus. He had a protracted recovery with multiple problems including bilateral subdural hygromas, myocardial infarction, and pulmonary embolus. The follow-up neurological examination 33 months after surgery revealed excessive somnolence, cognitive impairment, and persistent ocular palsies. A C T scan revealed a small a m o u n t of residual calcification in the right thalamus. He died 55 months after surgery o f u n k n o w n causes. Minor complications occurred in nine patients including: transient increased left inferior quadrantanopsia (Case 2); transient increased leg paresis (Case 5); transient dysphasia (Cases 7 and 10); transient ataxia (Case 8); transient a r m weakness (Case 11); transient dysphasia and persistent fight superior quadrantanopsia (Cases 12 and 15); and transient facial paresis (Case 23). In all cases, the morbidity was related to the location of the lesion and the necessary surgical approach. In three of our patients (Cases 1, 3, and 22) complete removal o f the lesion m a y not have been accomplished, since postoperative C T scans in these patients showed persistent calcification or minimal contrast-enhancing tissue. N o n e o f these patients has had a documented hemorrhage and two have done well clinically. The other (Case 1) died o f u n k n o w n causes. Seizure Control Seventeen patients presented with a primary seizure disorder. Eight patients had partial seizures, six had partial-complex seizures, and three had generalized sei700
zures. Following resection of the occult vascular malformation, 11 patients were seizure-free, three patients had persistent seizures but their frequency was diminished, two patients suffered a single seizure following surgery, and one patient had no change in his seizure frequency. This patient also had substantial psychiatric difficulties and there was some question as to whether his seizures were psychogenic. Two patients who presented with a progressive neurological deficit and acute hemorrhage also had seizures. One patient is now seizure-free off medication and the other is seizure-free on medication. Detailed data on seizures are available on request.
Follow-Up Results The average follow-up period for this series was 16 months (range 1 to 55 months). No patient has had a documented hemorrhage in the follow-up period. One patient died of u n k n o w n causes. For the 17 patients presenting with a p r i m a r y seizure disorder, the followup period averaged 15 m o n t h s (range 1 to 40 months). Discussion Small vascular malformations have been recognized for decades as an etiological factor in intracerebral hemorrhage. 1~ With the development of CT and particularly M R imaging, angiographically occult vascular malformations have c o m e to be recognized as significant causes of seizures and progressive neurological deficits. 4"~'~'~'2~ Presumably, these neurological problems are related to repeated "silent" hemorrhages with hemosiderin deposition and local mass effect. On CT, occult vascular malformations may be confused with neoplasms but there is a characteristic M R appearance that, while not diagnostic, is highly suggestive of a vascular malformation. ~3"~5'~6Clearly, the distinction between a neoplasm and a vascular malformation is critical. There is general agreement that excision is the treatment of choice for both therapeutic and diagnostic p u r p o s e s . 4"9"15"j~'2~ Although stereotactic biopsy has been accomplished, 2 our own experience is that there is a significant risk of hemorrhage with stereotactic biopsy of an occult vascular malformation. 3 With the increasing utilization of CT and M R imaging, occult vascular malformations are being discovered more often as a cause of hemorrhage, seizures, and progressive neurological deficits. Occult vascular malformations are small intra-axial lesions that can be located anywhere within the brain. For lesions that are deep or located in critical areas, successful excision depends on precise localization. Intraoperative ultrasound studies ~~9 or stereotaxis can be employed. We believe that stereotactic craniotomy is ideally suited to the m a n a g e m e n t of occult vascular malformations. The surgical approach, or trajectory, can be planned to avoid functional cortex or m a j o r vascular structures. Stereoscopic angiography can identify sulci which may be utilized in the approach to minimize transcortical dis-
J. Neurosurg. / Volume 72/May, 1990
Stereotactic resection of occult vascular malformations
FIG. 2. Computerized tomography scans in Case 12.
FIG. 1. Computerized tomography scans in Case 26.
Left: Preoperative scan without contrast enhancement in this
patient who presented with left hemiplegia and obtundation secondary to hemorrhage. There is stippled calcification adjacent to the hematoma suggesting an occult vascular malformation. Right: Postoperative scan with contrast enhancement demonstrating complete resection of the occult vascular malformation and resolution of the hematoma. section. The lesion can be localized precisely, permitting a small craniotomy with a trephine. Volumetric reconstruction with cross sections along the viewline demonstrates the margins of these benign circumscribed lesions, contributing to a complete removal (Fig. 1). Four types o f vascular malformations are recognized: arteriovenous malformation, venous angioma, cavernous hemangioma, and capillary telangectasias. ~'22 Some believe that venous angiomas rarely produce symptoms and signs and should not be aggressively treated. ~4There were no venous angiomas in the present series, which suggests that they are a relatively rare cause of neurological symptoms. All pathological types of vascular malformations have been included in series of angiographically "occult" vascular malformations. 9,2~In addition, all of the recognized pathological types of vascular malformations have been described a s " c r y p t i c . ''1~ There is confusion in the terminological distinction between "cryptic" and "occult." In the strictest sense, cryptic vascular malformations are small and clinically silent prior to intracerebral hemorrhage. 1~ The term "cryptic" applies to clinical presentation whereas "occult" refers to angiographic findings. Neither term implies a histological diagnosis. The majority o f the patients in the present series were considered to have had thrombosed arteriovenous malformations, since their size would have permitted angiographic diagnosis in the absence of thrombosis. Thrombosis is likely due to previous subclinical hemorrhage or h e m o d y n a m i c factors. 2~ A specific pathological characterization was not possible in six of the specimens in this series, but a definitive diagnosis of vascular malformation was made in those cases. Difficulty in making a precise pathological diagnosis has been reported in other series. 9"~5
J. Neurosurg. / Volume 72/May, 1990
Left: Preoperative stereotactic scan with contrast enhance-
ment demonstrating mesial left temporal lesion in this patient with seizures. The lesion was resected with a posterior-inferior temporal approach. Right: Postoperative scan with contrast enhancement demonstrating complete resection of the lesion with preservation of the temporal lobe.
Patients with seizures due to an occult vascular malformation benefit from excision of the lesion and hemosiderin-laden tissue. 2~ Identification of an occult vascular malformation and its removal may preclude the necessity for a more extensive cortical or lobar resection (Fig. 2). In fact, two patients in this series (Cases 4 and 16) had a previous temporal lobectomy with unsuccessful seizure control, and responded to resection of an occult vascular malformation. Stereotactic craniotomy offers significant advantages in the surgical m a n a g e m e n t o f angiographically occult vascular malformations. The a m o u n t of brain tissue that must be exposed in the removal of these lesions is limited, the surgical approach is direct and simulated preoperatively, and the c o m p u t e r reconstructions aid the surgeon in developing a plane around the lesion. Acknowledgment
The authors thank Mrs. Ruth Vrieze for her preparation of the manuscript. References
1. Chandler WF, Knake JE, McGillicuddy JE, et al: Intraoperative use of real-time ultrasonography in neurosurgery. J Neurosurg 57:157-163, 1982 2. Daumas-Duport C, Mann M, Munari C, et al: Cryptic vascular malformations diagnosed by stereotactic biopsies - - a preliminary study. Appl Neurophysiol 48:440-443, 1985 3. Davis DH, Kelly PJ, Marsh WR, et al: Computer-assisted stereotactic biopsy of intracranial lesions. Appl Neurophysiol 50:172-177, 1987 4. Giombini S, Morello G: Cavernous angiomas of the brain. Account of fourteen personal cases and review of the literature. Acta N e u r o c h i r 40:61-82, 1978 5. Kelly PJ: Volumetric stereotactic surgical resection of intra-axial brain mass lesions. Mayo Clin Proc 63: 1 1 8 6 - 1 1 9 8 , 1988 6. Kelly PJ, Goerss SJ, Kall BA: The stereotaxic retractor in computer-assisted stereotaxic microsurgery. Technical
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D. H. Davis and P. J. Kelly note. J Neurosurg 69:301-306, 1988 7. Kelly PJ, Kall BA, Goerss S, et al: Computer-assisted stereotaxic laser resection of intra-axial brain neoplasms. J Neurosurg 64:427-439, 1986 8. Kelly PJ, Kall BA, Goerss S, et al: Results of computerassisted stereotactic laser resection of deep-seated intracranial lesions. Mayo Ciin Proc 61:20-27, 1986 9. Lobato RD, Perez C, Rivas J J, et al: Clinical, radiological, and pathological spectrum of angiographically occult intracranial vascular malformations. Analysis of 21 cases and review of the literature. J Neurosurg 68:518-531, 1988 10, Margolis G, Odom GL, Woodbalt B, et al: The role of small angiomatous malformations in the production of intracerebral hematomas. J Neurosurg 8:564-575, 1951 11. McCormick WF: Pathology of vascular malformations of the brain, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 44-63 12. McCormick WF, Nofzinger JD: "Cryptic" vascular malformations of the central nervous system. J Neurosurg 24:865-875, 1966 13. New PF, Ojemann RG, Davis KR, et al: M R and CT of occult vascular malformations of the brain. AJNR 5: 985-993, 1986 14. Ogilvy CS, Heros RC: Angiographically occult intracranial vascular malformations. J Neurosurg 69:960-961, 1988 (Letter) 15. Ogilvy CS, Heros RC, Ojemann RG, et al: Angiographically occult arteriovenous malformations. J Neurosurg 69:350-355, 1988
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16. Rigamonti D, Drayer BP, Johnson PC, et al: The MRI appearance of cavernous malformations (angiomas). J Neurosurg 67:518-524, 1987 17. Russell DS: Discussion: the pathology of spontaneous intracranial haemorrhage. Proe R Soc Med 47:689-693, 1954 18. Simard JM, Garcia-Bengochea F, Ballinger WE, et al: Cavernous angioma: a review of 126 collected and 12 new clinical cases. Neurosurgery 18:162-172, 1986 19. Voorhies RM, Engel I, Gamache FW Jr, et al: Intraoperative localization of subcortical brain tumors: further experience with B-mode real-time sector scanning. Neurosurgery 12:189-194, 1983 20. Wakai S, Ueda Y, Inoh S, et al: Angiographically occult angiomas: a report of thirteen cases with analysis of the cases documented in the literature. Neurosurgery 17: 549-556, 1985 21. Wharen RE Jr, Scheithauer BW, Laws ER Jr: Thrombosed arteriovenous malformations of the brain. An important entity in the differential diagnosis of intractable focal seizure disorders. J Neurosurg 57:520-526, 1982 22. Wilkins RH: Natural history of intracranial vascular malformations: a review. Neurosurgery 16:421-430, 1985
Manuscript received August 9, 1989. Accepted in final form November 20, 1989, Address reprint requests to: Dudley H. Davis, M.D., Department of Neurosurgery, Mayo Clinic, Rochester, Minnesota 55905.
J. Neurosurg. / Volume 7 2 / M a y , 1990
Stereotactic resection of occult vascular malformations DUDLEY H . DAVIS, M . D . , AND PATRICK J. KELLY, M . D . Department o f Neurosurgery, Mayo Clinic and M a y o Medical School, Rochester, Minnesota
v" Angiographically occult vascular malformations can be identified on computerized tomography and magnetic resonance imaging. Surgical excision, when possible, is the treatment of choice in symptomatic lesions. Because these malformations are usually small and can be located in surgically treacherous areas of the brain, stereotactic resection should be considered. Stereotactic resection of a pathologically verified occult vascular malformation was performed in 26 patients in this series (13 females and 13 males, mean age 30 years). Seventeen patients presented with a seizure disorder, four with an intracerebral hemorrhage, and four with a progressive neurological deficit; one patient was asymptomatic. Sixteen patients had normal neurological examinations, nine had neurological signs referable to their lesion, and one had a visual field deficit related to a previous temporal lobectomy. In six patients evidence of acute hemorrhage was found on imaging studies or at surgery, and 11 patients had evidence of previous hemorrhage on imaging studies, determined at surgery or by histological examination. Three patients had evidence of both acute and previous hemorrhage and six patients had no evidence of hemorrhage. Lesions were located in cortical or subcortical areas in 21 patients, in the thalamus or basal ganglia in three, and in the posterior fossa in two. Following stereotactic resection, 24 patients were improved, one patient was unchanged, and one patient was worse. Without stereotaxis or intraoperative ultrasound studies, localization of these lesions at conventional craniotomy can be difficult. A stereotactic craniotomy is ideally suited to the treatment of these benign circumscribed, but potentially devastating lesions. KEY WORDS cryptic lesion 9 arteriovenous m a l f o r m a t i o n 9 seizure 9 occult arteriovenous malformation 9 stereotaxis 9 intracerebral h e m o r r h a g e ~
V
ASCULAR m a l f o r m a t i o n s o f the b r a i n m a y cause headache, a c u t e h e m o r r h a g e , seizures, or progressive n e u r o l o g i c a l deficits. 4"9'' ~"~8,2o.2, It is well established that s o m e m a l f o r m a t i o n s m a y be clinically silent or " c r y p t i c " p r i o r to h e m o r r h a g e . ~o.~2,~7T h e y m a y p r o d u c e no a n g i o g r a p h i c a b n o r m a l i t y with the exception o f m a s s effect a n d h a v e b e e n d e s c r i b e d as angiographically " O c c u l t . ''4"9"t5"2~ P r i o r to the d e v e l o p m e n t o f c o m p u t e r i z e d t o m o g r a p h y (CT) a n d m a g n e t i c resonance ( M R ) i m a g i n g such lesions c o u l d o n l y be suspected w i t h o u t surgical o r a u t o p s y verification. W i t h these i m a g i n g t e c h n i q u e s , d i a g n o s i s o f an occult vascular m a l f o r m a t i o n c a n be m a d e with a high degree o f accuracy. 2'9'13'15'16'21 O n CT, the lesions can a p p e a r as small, h y p e r d e n s e m a s s e s t h a t m a y show m o t t l e d calcification. T h e y s h o w m i l d to m o d e r a t e contrast enh a n c e m e n t a n d little m a s s effect in the absence o f h e m o r r h a g e . O n M R i m a g i n g , the lesions a p p e a r as heterogeneous, c i r c u m s c r i b e d masses that will have signal-void areas s e c o n d a r y to t h e p a r a m a g n e t i c effect o f h e m o s i d e r i n . L o w - g r a d e n e o p l a s m s are frequently in the differential diagnosis. 698
Surgical excision is the t r e a t m e n t o f choice to establish a histological diagnosis, a m e l i o r a t e s y m p t o m s a n d signs, a n d p r e v e n t f u r t h e r n e u r o l o g i c a l deterioration. 4"~'~'~s2~ Since t h e r e is n o a n g i o g r a p h i c a b n o r m a l i t y a n d the lesions are small, surgical localization m a y be difficult. F o r d e e p lesions or lesions l o c a t e d in essential areas, precise l o c a l i z a t i o n a n d resection are critical to a successful o u t c o m e . Stereotactic c r a n i o t o m y p e r m i t s a c c u r a t e l o c a l i z a t i o n a n d resection o f these lesions with m i n i m a l t r a u m a to t h e s u r r o u n d i n g tissues. Stereotactic resection o f a histologically verifiied occult vascular m a l f o r m a t i o n has b e e n a c c o m p l i s h e d in 26 patients a n d this g r o u p f o r m s t h e basis for this report. Operative Technique
T h e t e c h n i c a l details o f stereotactic c r a n i o t o m y have been r e p o r t e d p r e v i o u s l y ? -8 Briefly, all patients underw e n t a stereotactic C T scan a n d , in s o m e cases, a stereotactic M R i m a g e was o b t a i n e d as well. A stereotactic a n d stereoscopic c e r e b r a l a n g i o g r a m was o b t a i n e d unless an a n g i o g r a m h a d b e e n t a k e n p r i o r to referral, a n d o u r review c o n f i r m e d n o v a s c u l a r a b n o r m a l i t y . J. Neurosurg. / Volume 7 2 / M a y , 1990
Stereotactic resection of occult vascular malformations TABLE 1
Clinical summary of 26 patients with occult vascular malJormations Case No.
Hemorrhage* (acute/ previous)
Presentation
Location of Lesion
1
43, M
2 3
23, M 24, F
progressive neurological deficit seizures seizures
rt thalamus and rostral midbrain rt occipital rt temporal
-/+ -/+
4 5 6 7 8
45, 67, 16, 29, 50,
rt central-parietal rt frontal It temporal It temporal inferior vermis
-/+/-/-/-/+
9
23, M
seizures seizures seizures seizures progressive neurological deficit progressive neurological deficit seizures seizures seizures acute hemorrhage seizures seizures
increased deficit, died one postop seizure decreased seizure frequency no seizures no seizures no seizures no change in seizures deficit improved
caudal fourth ventricle
+/+
deficit improved
3
It frontal It central-frontal It temporal rt frontal rt temporal It temporal
+/-/-/+/+ -/+ -/+
no seizures no seizures no seizures no deficit no seizures decreased seizure frequency no seizures no deficit
16 40 13 36 23 8
no seizures one postop seizure no seizures no seizures deficit improved no deficit no deficit decreased seizure frequency deficit improved
25 15 3 4 9 13 4 6
M M M M M
10 11 12 13 14 15
35, 39, 35, 3, 20, 44,
F F F F F M
16 17
41, M 13, M
18 19 20 21 22 23 24 25
4, 30, 32, 3, 32, 43, 10, 12,
26
45, F
M F F M F F F F
-/+
seizures progressive neurological deficit seizures seizures seizures seizures acute hemorrhage acute hemorrhage incidental finding seizures
rt frontal It parietal
-/+ +/-
It frontal rt temporal rt frontal rt frontal It temporal rt basal ganglia rt frontal rt central-frontal
-/+ -/+ -/+ +/+/+/-/-/+
acute hemorrhage
rt basal ganglia
+/+
Result
Follow-Up Period (mos)
Age (yrs), Sex
55 2 2 54 1 22 3 29
15 24
3
* Evidence of acute hemorrhage was based on radiographic findings or operative findings; evidence of previous hemorrhage was based on magnetic resonance imaging signs of previous hemorrhage, operative findings of hemosiderin, or histological demonstration of hemosiderin. + = signs present; - = no signs.
Surgical planning was accomplished at a console* that displayed the imaging studies. A target volume was digitized from the stereotactic CT scan and/or stereot a c t i c M R i m a g e as d e t a i l e d i n p r e v i o u s r e p o r t s . 5'7"8 A central target point was then selected and viewed on the angiographic studies, and various trajectories could be simulated on the display screen. Sulci could be identified on the stereoscopic-stereotactic angiogram. In some cases a trajectory through a sulcus was selected to minimize the dissection to the lesion. Cross sections of the reconstructed lesional volume could be visualized along the trajectory with the outline of either a trephine opening or a stereotactic retractor superimposed on the i m a g e as r e p o r t e d p r e v i o u s l y ? "6 All p a t i e n t s u n d e r w e n t s t e r e o t a c t i c c r a n i o t o m y u n d e r * System, Model 3-260, m a n u f a c t u r e d by Sun Microsysterns, M o u n t a i n View, California; V M E image processor m a n ufactured by V i c o m Systems, San Jose, California; system, Model M V 7800, m a n u f a c t u r e d by D a t a General, Westboro, Massachusetts.
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general anesthesia. The target point was placed in the f o c a l p o i n t o f t h e s t e r e o t a c t i c f r a m e . A 1 89 d i a m e t e r trephine craniotomy was performed in line with the s e l e c t e d t r a j e c t o r y . F o r s u p e r f i c i a l l e s i o n s t h e c r o s s sect i o n s o f t h e r e c o n s t r u c t e d v o l u m e w e r e u s e d as a t e m p l a t e t o l o c a l i z e a n d e x c i s e t h e l e s i o n . F o r d e e p e r lesions, a stereotactic retractor was placed through a cortical incision and advanced to the lesion. Again using the volumetric reconstruction as a guide, the lesion was excised.
Summary of Cases Clinical D a t a The clinical profiles of the 26 patients are summar i z e d i n T a b l e 1. T h e r e w e r e 13 f e m a l e a n d 13 m a l e patients. Ages ranged from 3 to 67 years (mean 30 years). S e v e n t e e n p a t i e n t s p r e s e n t e d w i t h a s e i z u r e disorder, four patients with an acute hemorrhage, and four with a progressive neurological deficit; one patient was asymptomatic. Neurological examinations were normal 699
D. H. Davis and P. J. Kelly in 16 patients, while nine patients had neurological signs referable to their lesion. One patient had a superior quadrantanopsia related to a previous temporal lobectomy.
Radiographic Findings Twenty-one lesions were located in cortical or subcortical areas, three in the thalamus or basal ganglia and two in the posterior fossa (one in the vermis and one in the caudal fourth ventricle). All patients underwent CT and typical features o f an occult vascular malformation were found. All patients had angiography either at our institution or at their referring hospital. The angiograms were reviewed and showed no evidence of abnormal vascularity. Most lesions were 1 to 2 cm in diameter and only one lesion had a diameter greater than 3 cm. In this patient there had been a previous hemorrhage with h e m a t o m a adjacent to the lesion. Pathological Findings All patients had histological confirmation o f a vascular malformation. A diagnosis of arteriovenous malformation was m a d e in 18 cases, nonspecific "vascular malformation" in six cases, and cavernous hemangioma in two cases. Complications One patient (Case 1) who presented with diplopia was found to have a cystic contrast-enhancing lesion in the rostral midbrain and right thalamus. He had a protracted recovery with multiple problems including bilateral subdural hygromas, myocardial infarction, and pulmonary embolus. The follow-up neurological examination 33 months after surgery revealed excessive somnolence, cognitive impairment, and persistent ocular palsies. A C T scan revealed a small a m o u n t of residual calcification in the right thalamus. He died 55 months after surgery o f u n k n o w n causes. Minor complications occurred in nine patients including: transient increased left inferior quadrantanopsia (Case 2); transient increased leg paresis (Case 5); transient dysphasia (Cases 7 and 10); transient ataxia (Case 8); transient a r m weakness (Case 11); transient dysphasia and persistent fight superior quadrantanopsia (Cases 12 and 15); and transient facial paresis (Case 23). In all cases, the morbidity was related to the location of the lesion and the necessary surgical approach. In three of our patients (Cases 1, 3, and 22) complete removal o f the lesion m a y not have been accomplished, since postoperative C T scans in these patients showed persistent calcification or minimal contrast-enhancing tissue. N o n e o f these patients has had a documented hemorrhage and two have done well clinically. The other (Case 1) died o f u n k n o w n causes. Seizure Control Seventeen patients presented with a primary seizure disorder. Eight patients had partial seizures, six had partial-complex seizures, and three had generalized sei700
zures. Following resection of the occult vascular malformation, 11 patients were seizure-free, three patients had persistent seizures but their frequency was diminished, two patients suffered a single seizure following surgery, and one patient had no change in his seizure frequency. This patient also had substantial psychiatric difficulties and there was some question as to whether his seizures were psychogenic. Two patients who presented with a progressive neurological deficit and acute hemorrhage also had seizures. One patient is now seizure-free off medication and the other is seizure-free on medication. Detailed data on seizures are available on request.
Follow-Up Results The average follow-up period for this series was 16 months (range 1 to 55 months). No patient has had a documented hemorrhage in the follow-up period. One patient died of u n k n o w n causes. For the 17 patients presenting with a p r i m a r y seizure disorder, the followup period averaged 15 m o n t h s (range 1 to 40 months). Discussion Small vascular malformations have been recognized for decades as an etiological factor in intracerebral hemorrhage. 1~ With the development of CT and particularly M R imaging, angiographically occult vascular malformations have c o m e to be recognized as significant causes of seizures and progressive neurological deficits. 4"~'~'~'2~ Presumably, these neurological problems are related to repeated "silent" hemorrhages with hemosiderin deposition and local mass effect. On CT, occult vascular malformations may be confused with neoplasms but there is a characteristic M R appearance that, while not diagnostic, is highly suggestive of a vascular malformation. ~3"~5'~6Clearly, the distinction between a neoplasm and a vascular malformation is critical. There is general agreement that excision is the treatment of choice for both therapeutic and diagnostic p u r p o s e s . 4"9"15"j~'2~ Although stereotactic biopsy has been accomplished, 2 our own experience is that there is a significant risk of hemorrhage with stereotactic biopsy of an occult vascular malformation. 3 With the increasing utilization of CT and M R imaging, occult vascular malformations are being discovered more often as a cause of hemorrhage, seizures, and progressive neurological deficits. Occult vascular malformations are small intra-axial lesions that can be located anywhere within the brain. For lesions that are deep or located in critical areas, successful excision depends on precise localization. Intraoperative ultrasound studies ~~9 or stereotaxis can be employed. We believe that stereotactic craniotomy is ideally suited to the m a n a g e m e n t of occult vascular malformations. The surgical approach, or trajectory, can be planned to avoid functional cortex or m a j o r vascular structures. Stereoscopic angiography can identify sulci which may be utilized in the approach to minimize transcortical dis-
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Stereotactic resection of occult vascular malformations
FIG. 2. Computerized tomography scans in Case 12.
FIG. 1. Computerized tomography scans in Case 26.
Left: Preoperative scan without contrast enhancement in this
patient who presented with left hemiplegia and obtundation secondary to hemorrhage. There is stippled calcification adjacent to the hematoma suggesting an occult vascular malformation. Right: Postoperative scan with contrast enhancement demonstrating complete resection of the occult vascular malformation and resolution of the hematoma. section. The lesion can be localized precisely, permitting a small craniotomy with a trephine. Volumetric reconstruction with cross sections along the viewline demonstrates the margins of these benign circumscribed lesions, contributing to a complete removal (Fig. 1). Four types o f vascular malformations are recognized: arteriovenous malformation, venous angioma, cavernous hemangioma, and capillary telangectasias. ~'22 Some believe that venous angiomas rarely produce symptoms and signs and should not be aggressively treated. ~4There were no venous angiomas in the present series, which suggests that they are a relatively rare cause of neurological symptoms. All pathological types of vascular malformations have been included in series of angiographically "occult" vascular malformations. 9,2~In addition, all of the recognized pathological types of vascular malformations have been described a s " c r y p t i c . ''1~ There is confusion in the terminological distinction between "cryptic" and "occult." In the strictest sense, cryptic vascular malformations are small and clinically silent prior to intracerebral hemorrhage. 1~ The term "cryptic" applies to clinical presentation whereas "occult" refers to angiographic findings. Neither term implies a histological diagnosis. The majority o f the patients in the present series were considered to have had thrombosed arteriovenous malformations, since their size would have permitted angiographic diagnosis in the absence of thrombosis. Thrombosis is likely due to previous subclinical hemorrhage or h e m o d y n a m i c factors. 2~ A specific pathological characterization was not possible in six of the specimens in this series, but a definitive diagnosis of vascular malformation was made in those cases. Difficulty in making a precise pathological diagnosis has been reported in other series. 9"~5
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Left: Preoperative stereotactic scan with contrast enhance-
ment demonstrating mesial left temporal lesion in this patient with seizures. The lesion was resected with a posterior-inferior temporal approach. Right: Postoperative scan with contrast enhancement demonstrating complete resection of the lesion with preservation of the temporal lobe.
Patients with seizures due to an occult vascular malformation benefit from excision of the lesion and hemosiderin-laden tissue. 2~ Identification of an occult vascular malformation and its removal may preclude the necessity for a more extensive cortical or lobar resection (Fig. 2). In fact, two patients in this series (Cases 4 and 16) had a previous temporal lobectomy with unsuccessful seizure control, and responded to resection of an occult vascular malformation. Stereotactic craniotomy offers significant advantages in the surgical m a n a g e m e n t o f angiographically occult vascular malformations. The a m o u n t of brain tissue that must be exposed in the removal of these lesions is limited, the surgical approach is direct and simulated preoperatively, and the c o m p u t e r reconstructions aid the surgeon in developing a plane around the lesion. Acknowledgment
The authors thank Mrs. Ruth Vrieze for her preparation of the manuscript. References
1. Chandler WF, Knake JE, McGillicuddy JE, et al: Intraoperative use of real-time ultrasonography in neurosurgery. J Neurosurg 57:157-163, 1982 2. Daumas-Duport C, Mann M, Munari C, et al: Cryptic vascular malformations diagnosed by stereotactic biopsies - - a preliminary study. Appl Neurophysiol 48:440-443, 1985 3. Davis DH, Kelly PJ, Marsh WR, et al: Computer-assisted stereotactic biopsy of intracranial lesions. Appl Neurophysiol 50:172-177, 1987 4. Giombini S, Morello G: Cavernous angiomas of the brain. Account of fourteen personal cases and review of the literature. Acta N e u r o c h i r 40:61-82, 1978 5. Kelly PJ: Volumetric stereotactic surgical resection of intra-axial brain mass lesions. Mayo Clin Proc 63: 1 1 8 6 - 1 1 9 8 , 1988 6. Kelly PJ, Goerss SJ, Kall BA: The stereotaxic retractor in computer-assisted stereotaxic microsurgery. Technical
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D. H. Davis and P. J. Kelly note. J Neurosurg 69:301-306, 1988 7. Kelly PJ, Kall BA, Goerss S, et al: Computer-assisted stereotaxic laser resection of intra-axial brain neoplasms. J Neurosurg 64:427-439, 1986 8. Kelly PJ, Kall BA, Goerss S, et al: Results of computerassisted stereotactic laser resection of deep-seated intracranial lesions. Mayo Ciin Proc 61:20-27, 1986 9. Lobato RD, Perez C, Rivas J J, et al: Clinical, radiological, and pathological spectrum of angiographically occult intracranial vascular malformations. Analysis of 21 cases and review of the literature. J Neurosurg 68:518-531, 1988 10, Margolis G, Odom GL, Woodbalt B, et al: The role of small angiomatous malformations in the production of intracerebral hematomas. J Neurosurg 8:564-575, 1951 11. McCormick WF: Pathology of vascular malformations of the brain, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 44-63 12. McCormick WF, Nofzinger JD: "Cryptic" vascular malformations of the central nervous system. J Neurosurg 24:865-875, 1966 13. New PF, Ojemann RG, Davis KR, et al: M R and CT of occult vascular malformations of the brain. AJNR 5: 985-993, 1986 14. Ogilvy CS, Heros RC: Angiographically occult intracranial vascular malformations. J Neurosurg 69:960-961, 1988 (Letter) 15. Ogilvy CS, Heros RC, Ojemann RG, et al: Angiographically occult arteriovenous malformations. J Neurosurg 69:350-355, 1988
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16. Rigamonti D, Drayer BP, Johnson PC, et al: The MRI appearance of cavernous malformations (angiomas). J Neurosurg 67:518-524, 1987 17. Russell DS: Discussion: the pathology of spontaneous intracranial haemorrhage. Proe R Soc Med 47:689-693, 1954 18. Simard JM, Garcia-Bengochea F, Ballinger WE, et al: Cavernous angioma: a review of 126 collected and 12 new clinical cases. Neurosurgery 18:162-172, 1986 19. Voorhies RM, Engel I, Gamache FW Jr, et al: Intraoperative localization of subcortical brain tumors: further experience with B-mode real-time sector scanning. Neurosurgery 12:189-194, 1983 20. Wakai S, Ueda Y, Inoh S, et al: Angiographically occult angiomas: a report of thirteen cases with analysis of the cases documented in the literature. Neurosurgery 17: 549-556, 1985 21. Wharen RE Jr, Scheithauer BW, Laws ER Jr: Thrombosed arteriovenous malformations of the brain. An important entity in the differential diagnosis of intractable focal seizure disorders. J Neurosurg 57:520-526, 1982 22. Wilkins RH: Natural history of intracranial vascular malformations: a review. Neurosurgery 16:421-430, 1985
Manuscript received August 9, 1989. Accepted in final form November 20, 1989, Address reprint requests to: Dudley H. Davis, M.D., Department of Neurosurgery, Mayo Clinic, Rochester, Minnesota 55905.
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