Journal of Clinical Neuroscience 17 (2010) 74–79



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A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79                                        75


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76                                                                            A.P.-H. Huang et al. / Journal of Clinical N...
A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79                                    77


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78                                                  A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–7...
A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79                                                 79...
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Brain stem cavernous malformations

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Brain stem cavernous malformations

  1. 1. Journal of Clinical Neuroscience 17 (2010) 74–79 Contents lists available at ScienceDirect Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn Clinical Study Brain stem cavernous malformations Abel Po-Hao Huang a,b, Jui-Sheng Chen a, Chi-Cheng Yang a,c, Kuo-Chuan Wang a, Shih-Hung Yang a, Dar-Ming Lai a, Yong-Kwang Tu a,* a Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital and National Taiwan University College of Medicine, 7 Chung Shan South Road, Taipei 100, Taiwan b Department of Surgery, National Taiwan University Hospital, Yun-Lin Branch, Yun-Lin, Taiwan c Department of Psychology, National Taiwan University, Taipei, Taiwan a r t i c l e i n f o a b s t r a c t Article history: We retrospectively reviewed the clinical experience of 30 patients with brain stem cavernous malforma- Received 30 April 2009 tions (BSCM) treated operatively and non-operatively at our hospital between 1983 and 2005 to elucidate Accepted 8 June 2009 the natural history of BSCM and the factors that affect surgical outcome. Inpatient charts, imaging stud- ies, operative records, and follow-up results were evaluated. The average follow up was 48.5 months. Twenty-two patients (73.3%) received surgical extirpation and of these 86.4% improved or stabilized Keywords: and 13.6% deteriorated with permanent or severe morbidity. There was no mortality. Size, preoperative Brain stem hemorrhage status, and surgical timing were factors related to surgical outcome. In the non-operative group, 50% of Cavernoma Cavernous malformation the patients were the same or better, 25% deteriorated, and 25% died. With appropriate patient selection, resection of BSCM can be achieved with acceptable morbidity compared with the ominous natural history of these lesions. Ó 2009 Elsevier Ltd. All rights reserved. 1. Introduction hemorrhage was also assessed and recorded. Hemorrhage in our series was defined radiologically as acute or subacute, extralesional Cavernous malformations account for 5% to 15% of all central or intralesional hemorrhage or more than a 30% increase in size nervous system (CNS) vascular malformations.1,2 Brain stem cav- with mass effect or perifocal edema. A neurological event was de- ernous malformation (BSCM) is rare, affecting only 0.4% to 0.9% fined as subjective worsening of neurological status with objective of the population,3,4 and representing 9% to 35% of all cavernous neurological signs, regardless of the radiological findings. malformations.5–7 With the advent of MRI, BSCM have been diag- The choice of surgical approach was determined by the ‘‘two- nosed more frequently. These lesions have a propensity to hemor- point method” and the ‘‘safe entry zones”, which have been de- rhage and rehemorrhage; they have a 20-fold increased incidence scribed.3,10 The goals of surgery included prevention of rehemor- of hemorrhage and rehemorrhage compared to their supratentorial rhage, minimization of damage to normal parenchyma, and counterparts.8,9 The rate of fatal hemorrhage may be as high as preservation of associated venous malformations. The surgical 21%.1 However, if total extirpation is achieved, these lesions are indications in our institution included at least one of the following one of the few curable brain stem lesions. criteria: exophytic lesions, progressive neurological deficits, or re- peated symptomatic hemorrhages. 2. Materials and methods The diagnosis of BSCM were confirmed by histopathological examination. Intraoperative findings were recorded based on oper- We retrospectively reviewed the inpatient charts, imaging stud- ative reports. A lesion was defined as having an associated venous ies, pathological reports, and operative records of 30 patients with malformation if there were typical radiographic characteristics or BSCM who were treated at the National Taiwan University Hospital venous anomalies found adjacent to the bed of the cavernous mal- between January 1983 and March 2005. Imaging studies were as- formation upon intraoperative inspection. Lesions that reached the sessed for lesion location, number, size, distance to the pial surface, pial surface were defined as ‘‘exophytic”. Lesions that were not vis- and the presence of associated venous malformations. ible on initial exposure were termed ‘‘intrinsic”. Follow-up MRI The dates, episodes, presenting signs and symptoms of hemor- studies were obtained within 1 year postoperatively. Follow-up rhage were recorded. The degree of neurological recovery from the data were obtained by telephone conversation, outpatient clinic visits, or both. Patients were asked if they were ‘‘the same, * Corresponding author. Tel.: +886 2 2312 3456x5078; fax: +886 2 2341 7454. better, or worse” compared to their preoperative status or with E-mail address: yktu@ha.mc.ntu.edu.tw (Y.-K. Tu). their initial status. The Glasgow outcome scale (GOS) score and 0967-5868/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2009.06.009
  2. 2. A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79 75 the Karnofsky performance scale (KPS) score were used to provide 27.83% and repeated event rate was 42.27%. The average hemor- an objective measurement of the patients’ preoperative and post- rhage interval was about 44.2 months and ranged from seven days operative neurological status. We defined ‘‘poor outcome” as a to 17 years. GOS score lower than 3 or a KPS score lower than 60 on late fol- low-up (more than 1 month after surgery or the initial evaluation). 3.5. Surgical approaches We attempted to identify the risk factors indicative of a poor outcome using the following parameters: size, location, intrinsic/ Six patients had surgery via a transvermian approach; six via a extrinsic lesion, multiplicity, timing of operation, surgical ap- telovelar approach; three via a presigmoid approach; three via a sub- proach, hemorrhagic episodes, episodes of neurological events, temporal approach; two via a far-lateral approach; one via a trans- and neurological status on initial evaluation (GOS and KPS scores). sylvian approach; and one via a supracerebellar–infratentorial Since most of our patients were free of comorbidity, these factors approach. were not analyzed. The statistical methods we used for identifying the possible risk factors were Spearman correlation analysis and 3.6. Risk factors indicative of possible poor outcome linear regression. The risks factors indicative of a possible poor outcome in the 3. Results operative group included a lesion with a diameter >20 mm, poor initial neurological status, and more than two neurological events 3.1. Patient characteristics or hemorrhagic episodes. Additionally, a short interval (<3 weeks) between presentation and operation was a risk factor (p < 0.05). Thirty patients (15 male and 15 female) were included. The The risk factors in the non-operative group included old age (>60 median age was 40.4 years (range, 7–70 years). Three patients with years), large lesions (diameter > 20 mm), poor initial neurological pontine cavernoma had undergone prior surgery at another hospi- status, and more than two neurological events or hemorrhagic epi- tal. Two patients had undergone previous radiosurgery. Twenty- sodes (p < 0.05). two patients underwent surgical removal of the lesion and eight patients continued with conservative management. There were 3.7. Patient outcome no significant demographical differences between these two groups of patients. In the non-operative group, 50% of patients remained the same (three patients, [37.5%]) or improved (one patient, [12.5%]). How- 3.2. Clinical presentation and manifestation ever, two patients (25.0%) deteriorated and two patients (25.0%) died (Fig. 1). Both of these patients died at other institutions. Most patients (93.3%) presented with a hemorrhage. One pa- One had a cerebrovascular accident with aspiration pneumonia tient presented with seizures and was found to have multiple in- and sepsis 3 years after discharge. The other patient had a sudden tra-axial cavernous malformations. Another patient had a head onset cardiopulmonary arrest, which occurred 13 months after dis- injury from a motor vehicle accident and was found to harbor a charge. Both patients had exophytic lesions with moderate neuro- BSCM. In 20 (66.7%) patients, the onset of symptoms was sudden logical deficits in which surgery had been suggested. or acute. The clinical course was progressive in 22 patients In the operative group, 86.4% of patients improved (10 patients, (73.3%), relapsing-remitting in five patients (16.7%), and stable in [45.5%]) or stabilized (nine patients, [40.9%]) while three (13.6%) three patients (10.0%). Three of the five patients with a relapsing- patients deteriorated (Fig. 1). Of those three patients, one had hem- remitting course were erroneously diagnosed as having multiple orrhage from the residual cavernoma with locked-in syndrome and sclerosis at other institutions before admission. Most patients pre- the other two had residual hematoma with severe motor deficit sented with multiple neurological deficits. Common manifesta- and multiple cranial nerve deficits. Overall, the perioperative mor- tions were: facial dysesthsia (53.3%), diplopia (50.0%) and bidity rate in this study was 27.3%, with a long-term permanent hemiparesis (50.0%). Other manifestations included hemisensory morbidity rate of 13.6%. There was no mortality in this group. deficit (40%), facial nerve deficit (33.3%), vestibulocochlear nerve deficit (33.3%), lower cranial nerve deficit (33.3%), cerebellar deficit 3.8. Postoperative complications and deficits (16.7%), and headache (13.3%). Immediate postoperative complications reported in this study include hemiparesis (27.3%), ataxia (18.2%), diplopia (18.2%), 3.3. Lesion characteristics combined abducens and facial palsy (18.2%), lower cranial nerve The average lesion size was 13.5 mm and most were exophytic (70.0%). Multiple lesions were found in three patients (10.0%) and 100 adjacent venous malformations were seen on pre-operative MRI in four patients (13.3%). The most frequent lesion location was the 80 pons (56.7%), particularly the fourth ventricular floor. There were percentage of patients six (20.0%) midbrain lesions, three (10.0%) medullary lesions, two 60 (6.7%) pontomescencephalic lesions, and two (6.7%) pontomedul- lary lesions. Five patients (13.9%) had associated venous malforma- 40 tions at operation (Figs. 4 and 5A). 20 3.4. Hemorrhage from BSCM 0 The annual hemorrhage rate was 3.42% (30 patients experi- NOG OG enced 40 hemorrhages in 1170 patient-years of life) and the annual Fig. 1. A comparison of the non-operative (NOG) and operative groups (OG) neurological event rate was 4.19% (30 patients experienced 49 showing the percentage of improvement (solid bar), stabilization (grey bar), events in 1170 patient-years of life). The rebleeding rate was deterioration (open bar) and death (stippled bar).
  3. 3. 76 A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79 percentage of patients hemiparesis ataxia diplopia abducens low cranial rubral tremor one-and-a- and facial nerves half palsy deficiency syndrome Fig. 2. A comparison of immediate postoperative complications (black) and long-term complications (white) showing a reduction in motor deficit, lower cranial nerve deficits and diplopia over time. far-lateral approach developed a lower cranial nerve deficit. One 100 of the six patients (16.6%) who received the telovelar approach developed one-and-a-half syndrome. Of the six patients who re- ceived the transvermian approach, two (33.3%) developed truncal 80 ataxia, one (16.7%) developed rubral tremor, and one (16.7%) percentage of patients developed Parinaud’s syndrome. 60 3.9. Follow-up evaluation 40 All patients in both groups were available for follow-up except for two patients in the non-operative group. The average follow-up period was about 4 years. To date, there are no recurrences or de 20 novo lesions on follow-up imaging of patients in the operative group. In the operative group, serial follow-up MRI confirmed total excision in 20 (90.9%) cases and residual lesion in 2 (9.1%) cases. 0 Motor Sensory Cerebellar Cranial nerve 4. Discussion Fig. 3. A comparison of preoperative (grey bar), early (open bar) and late postoperative (solid bar) deficits showing recovery of most neurological and Brain stem cavernomas account for only 9% to 35% of intracra- functional nerve deficits. nial cavernomas and are most frequently found in the pons.4,8,11,12 Microscopically, a BSCM consists of caverns of sinusoidal spaces lined by a single layer of endothelium and a peripheral gliotic deficits (4.5%), and rubral tremor (4.5%). Long-term complications hemosiderin ring without intervening neural parenchyma. Macro- include hemiparesis (4.5%), ataxia (9.1%), diplopia (18.2%), com- scopically, it is a multilobulated mass resembling a mulberry. It is bined abducens and facial palsies (9.1%), one-and-a-half syndrome also known as a cavernoma, cavernous hemangioma, and cavern- (4.5%), and rubral tremor (4.5%). ous angioma. The average cavernoma size is 15 mm to 19 mm in The motor deficit, lower cranial nerve deficits, and diplopia diameter.11–13 Dynamic change in size depends on growth, hemor- tended to improve between the early and the late postoperative rhage, reabsorption, and organization of the hematoma.14 Risk fac- period (Fig. 2). However, patients with cerebellar ataxia and com- tors of aggressive clinical behavior include previous hemorrhage, bined abducens and facial palsies generally did not recover fully. familial or multiple forms of the disease, previous whole-brain or One of our patients whose cavernoma was excised via a transver- stereotactic radiotherapy, incomplete removal, and associated ve- mian approach experienced a rubral tremor. One-and-a-half syn- nous malformation.15 drome occurs when the medial longitudinal fasciculus and the Hemorrhage from cavernoma may be asymptomatic or neuro- pontine gaze center are injured. One of our patients who under- logically devastating because of the precarious location of these le- went cavernoma excision via the telovelar approach developed this sions.3,8,16 Hemorrhage mechanisms include slow ooze that complication. contributes to the peripheral hemosiderin ring, intralesional hem- In this study, most patients experienced immediate, postopera- orrhage causing lesion expansion and mass effect, and extralesion- tive neurological and functional deterioration. Late postoperative al hemorrhage leading to significant neurological deficit depending follow-up, however, revealed that most of these deficits had im- on the location.9 proved (Fig. 3). Cerebellar complications were highly associated Cause is the most important predictor of clinical outcome in pa- with the transvermian approach and patients seldom recovered tients with brain stem hemorrhage,17 and the first episode of hem- fully from these deficits. orrhage in patients with BSCM is usually benign, while brain stem There were no complications for all the subtemporal, presigm- hemorrhage associated with hypertension is much more devastat- oid, transsylvian, supracerebellar–infratentorial approaches that ing. The estimated risk of hemorrhage from BSCM is about 0.7% to we performed. One of the two patients (50%) who underwent a 6.0% per year per lesion.4,9,13,14 The rehemorrhage rate is about 5%
  4. 4. A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79 77 to 30% per year per lesion.4,9,13,14 Differing definitions of hemor- demonstrating the inefficacy of stereotactic radiosurgery in treat- rhage account for the large variation of hemorrhage and rehemor- ing BSCM.6,7,23,24 Our institution does not at present offer radiosur- rhage rates in the literature. Risk of hemorrhage is higher with the gery to patients harboring these lesions. familial type, infratentorial lesions, deep lesions, and lesions with The criteria for patient selection for surgery remains controver- previous hemorrhage.7–9,18 sial. Our indications included progressive neurological deficits, le- Several authors have suggested a link between the incidence of sions that reached the pial surface, and repeated hemorrhages. cavernous hemorrhages and being female.9,13,15,16 They suggest that Intrinsic lesions can be approached if a safe entry zone is present. cavernous hemorrhages occur more frequently in females and some Some authors recommend surgery only for patients experiencing occur during pregnancy,9,12 implying a role of the endocrine system. more than two hemorrhages. Although we do not always have data There was no sex preponderance in our series and none of the hem- for the number of previous hemorrhages, most of our patients had orrhages occurred during pregnancy. We found no correlation be- at least one hemorrhage. In our experience, surgical management tween the location of the lesion and the frequency of hemorrhage, tended to improve outcome if the patient had a KPS score > 60 although some authors have reported a higher rate of hemorrhagic or a GOS score > 3 and a Glascow Coma Scale (GCS) score > 7. This events in patients with third ventricle and pontomesencephalic does not imply that surgery should be performed only in these pa- cavernomas.19 Additionally, we found no conclusive correlation be- tients, since different clinical situations dictate distinctly different tween surgical outcome and lesion location in our series. management approaches. Most of the patients (93.3%) presented with hemorrhage and Most important, the risk of bleeding and related neurological manifested multiple cranial nerve deficits. Consciousness impair- deterioration, and possible surgery-related complications, should ment, significant motor deficits, and hemiplegia are infrequent be explained to the patient to help them decide the optimal treat- and usually transient. This can be explained by the deep location ment. In general terms, surgery for BSCM is associated with an 8% of the corticospinal tract in the pars ventralis. Focal disturbance to 12% morbidity rate and a 1% to3% mortality rate.3,8,9,13,15,25 Post- of the reticular formation or the ascending reticular activating sys- operative deterioration is frequent and mostly transient. On long- tems can lead to alteration in consciousness. Plum and Posner, term follow-up, 79% to 85% of patients will improve or at least stay however, in their analysis of human brain stem stroke, demon- the same, and 15% to 21% will deteriorate.8,9,13 strated that functional transection near the level of the vestibulo- Most authors agree that the appropriate timing of surgery after cochlear nucleus does not necessarily cause consciousness hemorrhage is during the subacute phase (2–6 weeks after ic- deterioration.20 It seems that only profuse involvement of the tus).5,8,13,21,26 During this time, most patients will stabilize neuro- reticular system, such as the raphe nuclei and the central nuclei, logically and hematoma liquification occurs, which facilitates causes consciousness alteration. Patients usually recovered from dissection and avoids excessive manipulation of the surrounding cavernous hemorrhage to some degree. Complete recovery, how- parenchyma. Reactive gliosis typically occurs months after extrale- ever, was rarely seen in this study. sional hemorrhage, which complicates dissection. Therefore, it MRI studies are the most sensitive imaging modalities for seems reasonable that the appropriate timing of surgery after hem- BSCM.11,15,21 Their radiographic appearance is divided into four orrhage is during the subacute phase. Statistical analysis has types: type I through to type IV.8 Cavernomas usually progress shown better outcomes in patients in whom resection was per- from type I to III, which is dependent on the age of blood they con- formed within 3 to 6 weeks post-hemorrhage. tain. Type IV lesions are small and are well visualized only on As stated previously, most patients experience immediate post- gradient-echo images. They appear as punctuate areas of hypoin- operative deterioration. Such neurological deterioration may be tensity that are similar in appearance to capillary telangiectasis.23 due to edema and swelling in the surrounding parenchyma precip- Whether this type of lesion is a capillary telangiectasia and a itated by surgical manipulation within such a critical region. These precursor lesion to the cavernoma is unclear. Type II is the most morbidities are often responsive to medical treatment and com- common form, and it appears as a nodular lesion with relatively monly transient. However, they may also be due to surgical com- short T1-weighted and long T2-weighted signals, circumscribed plications, either transient or permanent. by a hypointense ring giving the classic ‘‘popcorn” appearance of In our series, diplopia and motor deficit tended to improve over the cavernoma.5,11,14 time in most patients. However, patients with combined abducens Venous malformations are associated with 8% to 100% of and facial palsies seldom recovered spontaneously in contrast to BSCM.9,11 These venous anomalies may induce the formation of pure abducens palsy. This indicates possible damage near the facial cavernous malformations and have a role in their recurrence.9 colliculus where the genu of the facial nerve fibers wraps around The adjacent venous malformation must be carefully preserved the abducens nucleus. Permanent and severe motor deficit is rare, to maintain normal venous drainage and avoid devastating hemor- probably because the corticospinal tract is located deep in the pars rhagic infarction.9 In the present series, five patients (13.9%) with ventralis and cavernomas rarely reside in this area. Trucal ataxia, associated venous malformations were detected and preserved which is associated with the transvermian approach, showed a less intraoperatively, and in four patients these were noted on preoper- satisfactory recovery. This approach has been replaced by the telo- ative MRI (Figs. 4 and 5A). velar approach in recent years, and the incidence of cerebellar dys- Although their radiographic appearance is regarded as pathog- function has decreased.27 Other complications of the transvermian nomic, there are several pathologic entities that can mimic caver- approach such as mutism, neurobehavior change, and oropharyn- nomas clinically and radiologically. Hemorrhagic neoplasms, geal apraxia were not observed in our patients. especially metastatic cancer, is the most common. Others include Three of the operated patients had permanent and severe mor- meningiomas and gliomas. Vascular malformations other than bidity. One patient had a hemorrhage from residual cavernoma at cavernomas can sometimes look similar, as can parasitic diseases postoperative day 7 that resulted in locked-in syndrome. After dis- such as cysticercosis, rarely. cussion with the family, a second operation was performed. The The benefit of surgery in the treatment of BSCM is well estab- other two patients had residual hematoma with significant motor lished. It is also the only way to avoid further devastating hemor- deficit and multiple cranial nerve deficits. Inadvertent cranial nu- rhage in patients with recurrent symptomatic hemorrhages.9,22 clei and long-tract injury is the most likely explanation. The use of stereotactic radiosurgery is still controversial due to Incomplete resection of BSCM may occur when the operative its unpredictable outcome, the high incidence of radionecrosis, view is restricted by bleeding or because the lesion is located in and its neurological sequelae.6,23 There are abundant publications a deep cavity. Adjuncts such as neuronavigation, ultrasonography,
  5. 5. 78 A.P.-H. Huang et al. / Journal of Clinical Neuroscience 17 (2010) 74–79 Fig. 4. (Left) T1-weighted axial MRI showing a pontine cavernoma with adjacent venous malformation. The cavernoma was approached using the retrosigmoid approach for total excision. (Right) T1-weighted axial MRI 2 months after resection, showing no residual lesion. Note the preserved venous malformation. Fig. 5. A pontine cavernoma in which the floor of the 4th ventricle is exposed via the telovelar approach showing (A) the associated venous malformation (white arrows) and (B) using a bipolar stimulator for mapping the facial (asterisk) and trigeminal nuclei (dotted line) to determine the safe entry zone. (This figure is available in colour at www.sciencedirect.com.) and neuroendoscopy aid in confirmation of total extirpation of is usually sufficient. However, when the lesion is heterogenous, the these lesions. We have found neuronavigation useful in planning organized septum or cavern wall might be mistaken for the gliotic the entry zone for patients with intrinsic BSCM. The greatest limi- rim, which makes the operation is more difficult.28 In our experi- tation of surgical navigation is intraoperative brain shift. However, ence, neuronavigation is extremely helpful when the trajectory this problem can usually be compensated with surgical foresight. view guides surgical entrance into different compartments of the We have found the navigation system extremely useful in reoper- cavernoma (Supplementary Fig. 1). ation or in patients who received previous radiosurgery, when the normal anatomical landmarks may be distorted and the adhesions 5. Conclusion severe (Supplementary Fig. 1). In our experience, brain shift in these patients seems to be minimal and navigation is mostly extre- Size, preoperative functional status, and timing of operation mely accurate. Some advocate the use of neuroendoscopy to avoid were the major factors that correlated to surgical outcome in our incomplete resection of the cavernous malformation; the 3-mm, ri- series. Factors that affect outcome during surgery are complete- gid, wide-angle scope is used to obtain a complete resection of the ness of resection and avoidance of injury to the adjacent normal lesion and meticulous hemostasis.25 Others have reported that parenchyma and venous malformation. Failure to meet these goals continuous electromyographic monitoring helps in localizing cra- contributes to significant morbidity and even mortality. nial nerve motor nuclei and may reduce postoperative morbidity.23 Intraoperative electrophysiological monitoring of the floor of the fourth ventricle has been used in our institution in recent years Appendix A. Supplementary material to determine safe entry zones to approach BSCM located in the fourth ventricle floor. This technique is most useful where the nor- Supplementary data associated with this article can be found, in mal facial colliculus could not be identified, and direct stimulation the online version, at doi:10.1016/j.jocn.2009.06.009. localizes the facial nuclei and its tract therefore helps to determine the safe entry zone. The incidence of combined abducens and facial References nerve palsy decreased in our later series. In our experience, homogenous lesions usually have a well- 1. Di Rocco C, Iannelli A, Tamburrini G. Cavernous angiomas of the brain stem in children. Pediatr Neurosurg 1997;27:92–9. demarcated peripheral gliotic rim and total extirpation is immi- 2. Moriarity JL, Clatterbuck RE, Rigamonti D. The natural history of cavernous nent after dissection reaches this plane, thus operative affirmation malformations. Neurosurg Clin N Am 1999;10:411–7.
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