J Neurosurg 66:345-351, 1987 Interhemispheric approach for the surgical removal of thalamocaudate arteriovenous malformations ROBERT A. SOLOMON, M . D . , AND BENNETT M . STEIN, M . D . Department of Neurological Surgery, The Neurological Institute, Columbia-Presbyterian Medical Center, New York, New York u," A series of 250 surgically treated cerebral arteriovenous malformations (AVM's) is presented, in which 22 lesions were located primarily in the thalamus and caudate nucleus. A standardized interhemispheric approach through the posterior corpus callosum and into the atrium of the lateral ventricle was utilized for the surgical removal of these AVM's. Total removal was confirmed by angiography in 18 patients; removal was subtotal in four cases. There were no deaths in this group of patients. Disturbances of recent memory pre- and postoperatively were seen in half of the patients, but most of these deficits were temporary. Other complications included: postoperative homonymous hemianopsia (six cases), transient hemiparesis (three cases), hemisensory loss (two cases), Parinaud's syndrome (one case), and recurrent hemorrhage 2 years after surgery (one case). All 22 patients returned to their previous occupations and are leading independent lives. The results of this experience indicate that thalamocaudate AVM's can be effectively treated by resection. KEY WORDS 9 arteriovenous malformation 9 caudate nucleus 9 thalamus - surgical approach A RTERIOVENOUS malformations (AVM's) that involve the deep nuclei of the brain have always represented a dilemma for neurosurgeons. 5 Surgery for these lesions involves considerable risk to critical areas of the nervous system. However, rupture of an AVM in this location can lead to catastrophic parenchymal or intraventricular hemorrhage. Thus, an untreated diencephalic AVM must be considered a hazardous entity. In our series of 250 surgically treated intracerebral AVM's, 22 patients harbored malformations located primarily within the thalamus and basal ganglia. A standardized surgical approach was used in this group of patients. The presentation, surgical techniques, and outcome in these 22 patients are summarized and three illustrative cases are presented in fuller detail. The results of this experience indicate that these deep A V M ' s can be effectively treated by resection. Representative Cases Case 1 This 41-year-old man experienced a sudden intraventricular hemorrhage. Nine months after this episode, he came to the Neurological Institute for evaluation of J. Neurosurg. / Volume 66/March, 1987 short-term m e m o r y loss, a fight h o m o n y m o u s quadrantanopsia, and mild clumsiness of the right hand. Angiography demonstrated a small A V M medial to the trigone o f the left lateral ventricle and extending into the splenium o f the corpus callosum. The malformation was fed by branches of the posterior and anterior cerebral arteries. The venous drainage was into the straight sinus and vein o f Galen. Surgery was performed via a left parietal c r a n i o t o m y with the patient in the semisitting slouch position. An interhemispheric approach was used to expose the AVM. A cortical incision was made in the cingulate gyrus and the superior surface of the malformation was followed laterally. An area of old hemorrhage facilitated dissection a r o u n d the anterior margin o f the malformation into the thalamus. The lateral and posterior aspects o f the A V M were defined and the malformation was rolled medially on its venous pedicle, which was divided. Postoperatively, the patient had a h o m o n y m o u s hemianopsia. The remainder o f the neurological findings were unchanged. Angiography confirmed complete removal of the AVM. At his 6-month follow-up examination, he had returned to full e m p l o y m e n t and his recent m e m o r y was improving. 345 R. A. S o l o m o n and B. M. Stein FIG. 1. Case 2. Preoperative vertebral angiograms, anteroposterior (left) and lateral (right) views. Solid arrows point to the nidus of the malformation, and open arrows point to the medially draining vein. FIG. 2. Case 2. Postoperative vertebral angiograms, anteroposterior (left) and lateral (right) views, showing complete removal of the malformation (compare with Fig. 1). FIG. 3. Case 3. Preoperative contrast-enhanced coronal computerized tomography scan showing the location of the malformation (arrow). 346 Case 2 This 29-year-old w o m a n was 3 m o n t h s pregnant when she experienced a sudden severe headache associated with vomiting. A computerized tomography (CT) scan showed a small hemorrhage into the right trigone of the ventricle. Except for meningismus she had no neurological signs. An angiogram demonstrated a small AVM in the right pulvinar region with feeding vessels from the anterior and posterior choroidal arteries (Fig. 1). The pregnancy was terminated and the patient was transferred to the Neurological Institute for surgery 2 months later. The operation was performed through a right parietal craniotomy with the patient in the semisitting slouch position. Via the interhemispheric route, a 1-cm opening was made in the posterior aspect of the corpus callosum and the right lateral ventricle was entered. The AVM was encountered on the floor of the lateral venJ. Neurosurg. / Volume 6 6 / M a r c h , 1987 Interhemispheric approach for thalamocaudate AVM's FIG. 4. Case 3. Preoperative angiograms showing the malformation (arrows) after lateral internal carotid artery injection (left), after lateral vertebral artery injection (center), and after anteroposterior vertebral injection (right). tricle just lateral to the choroid plexus. A circumscribing incision was m a d e around the malformation. The dorsal aspect o f the pulvinar was resected, and the dissection was carried deep into the dorsal medial region of the thalamus and anteriorly to about 3 to 4 m m posterior to the foramen of Monro. In this fashion the malformation was removed. Postoperatively, the patient complained of numbness of the left side o f the face and body. Testing revealed decreased pain sensation on the left side but preservation of two-point and stereognostic sensation. These minor deficits cleared within days of the operation and the patient was discharged h o m e in normal condition. Angiography revealed no residual malformation (Fig. 2). At her 3-month follow-up examination, she had returned to work and her usual activities. Case 3 This 28-year-old w o m a n was in good health except for a 1-year history of generalized headaches and episodic numbness in the left arm. The neurological examination was completely normal. Radiological studies showed an A V M with no evidence of hemorrhage. The malformation was 2 cm in diameter, was located in the posterior cingulate gyrus and corpus callosum, and extended to the floor o f the lateral ventricle on the right (Fig. 3). The A V M was supplied by a large anterior cerebral artery, the posterior cerebral artery via a posterior callosal artery, and the fight lateral posterior choroidal artery (Fig. 4). An operation was performed via a fight parietal craniotomy with the patient in the semisitting slouch position. Via an interhemispheric approach the corpus callosum was exposed and feeding vessels to the malJ. Neurosurg. / Volume 66/March, 1987 formation were divided. The m a l f o r m a t i o n was then followed laterally to the forceps major o f the corpus callosum and inferiorly into the floor of the lateral ventricle at the location o f the pulvinar and right fornix. The vascular supply from the choroidal vessels was secured and the entire m a l f o r m a t i o n was rolled out on the medial venous pedicle and removed. Postoperatively, the patient had no neurological deficits. Angiography and C T scanning (Fig. 5) showed no evidence of residual AVM. Detailed psychometric testing done both pre- and postoperatively failed to d e m onstrate any change in language or m e m o r y function. FIG. 5. Case 3. Postoperative contrast-enhanced coronal computerized tomography scan showing a hypodense area corresponding to the site of arteriovenous malformation resection. 347 R. A. S o l o m o n and B. M. Stein S u m m a r y of Cases This series of 22 patients includes 13 males and nine females. Their ages ranged from 14 to 42 years (mean 28 years). A s u m m a r y of these cases is presented in Table 1. Clinical Presentation Twenty-one patients presented with sudden intraventricular or intracerebral hemorrhage as the first manifestation of their AVM. One patient (Case 3) presented with sensory aberrations and headaches, and was the only patient in this series to c o m e to medical attention for reasons other than a hemorrhagic event. Initially, m a n y of the patients had profound neurological deficits, such as c o m a and hemiplegia. All patients showed dramatic i m p r o v e m e n t in their neurological status so that within 1 m o n t h after hemorrhage all patients were alert, oriented, ambulatory, and capable of independent lives. Three patients had a mild residual hemiparesis, two had hemianopsia, and six had some disturbance of recent m e m o r y function. Five of the six patients with a preoperative m e m o r y disorder bled from lesions involving the left pulvinar, caudate, and fornix. Location o f the A V M Two patients had bilateral involvement of diencephalic structures; one o f these malformations extended TABLE 1 Clinical summary of 22 patients with thalamocaudate A VM's* Feature clinical presentation hemorrhage intraventricular subarachnoid seizures location right side left side bilateral surgical approacht interhemispheric parietal (semisitting) frontal (supine) inferior temporal (lateral) posterior fossa (sitting) subfrontal (supine) reoperation (residual AVM) operative results total removal mortality return to premorbid occupation memory disturbance homonymous hemianopsia transient hemiparesis sustained hemisensory loss Parinaud's syndrome recurrent hemorrhage * AVM = arteriovenous malformation. t Five patients had two operations. 348 No. of Cases 12 9 1 14 6 2 21 2 1 1 1 1 18 0 22 11 6 3 2 1 1 infratentorially. The remaining patients had supratentorial AVM's that were lateralized: 14 were on the right side and six were on the left side. Twenty of the 22 malformations in this series were located adjacent to the atrium o f the lateral ventricle. One patient had a malformation situated anteriorly in the septal region extending into the anterior aspect of the right thalamus, and one had an extensive AVM that followed the entire corpus callosum, the septal region, fornices, and roof of the third ventricle. Vascular A n a t o m y Although most malformations in this series were supplied by two or more m a j o r arteries, the choroidal arteries form the primary vascular supply to AVM's situated near the atrium of the lateral ventricle. Thirteen maltbrmations were fed by the posterior choroidal arteries, and four received input from the anterior choroidal artery. The posterior pericallosal artery as well as other penetrating branches from the posterior cerebral artery in the region of the fusiform gyrus supplied 13 of the AVM's. The distal segment of the anterior pericallosal artery was involved in nine cases. Although thalamoperforating arteries were angiographically demonstrated to supply only three malformations, small penetrating vessels supplying the deep aspect of the malformations were encountered during surgery in almost all cases. The venous drainage from these malformations was always toward the midline. In one case, the primary draining vein ascended in the interhemispheric fissure to reach the superior sagittal sinus. In the remaining 21 cases, the venous drainage was into the deep venous system of the brain: internal cerebral veins, the basal vein of Rosenthal, the vein o f Galen, and the straight sinus. Surgical Technique Surgery was performed on all patients in this series via an interhemispheric route ipsilateral to the malformation (Fig. 6). A spinal drainage catheter is inserted and the patient is placed in a semisitting slouch position. The head is straight and maximally flexed to bring the curved portion of the parietal bone parallel to the floor. A 4 x 4-cm bone flap is formed to the fight or left including the midline. The medial burr holes are placed slightly to the opposite side o f the superior sagittal sinus with the posterior hole adjacent to the lambda. A dural flap is created along the sinus, and medially draining veins are preserved whenever possible. Retractors are placed on the falx and on the parietal lobe to expose the posterior aspect of the corpus callosum. At this point in the operation some aspect of the malformation m a y be visualized. When the malformation lies entirely in the floor or wall of the lateral ventricle, the corpus callosum must be divided before the AVM can be appreciated. Resection of the malformation is begun, based on the C T scan, magnetic resonance imaging J. Neurosurg. / Volume 66/March, 1987 Interhemispheric approach for thalamocaudate AVM's (MRI), and angiographic information as well as defined principles of A V M surgery that have been outlined elsewhere. 9-~2 In all cases in this series, the corpus callosum was divided over a distance o f about 1 to 2 cm, and the fornix, which lies just deep to the corpus callosum, was sectioned ipsilaterally. These maneuvers were necessary to gain access to the atrium of the ventricle. In some patients, the m a l f o r m a t i o n actually involved the corpus callosum and the ipsilateral fornix. Five patients in this group required two operations. One patient had incomplete removal and required reoperation. One patient underwent a suboccipital infratentorial approach to remove residual malformation in the region o f the quadrigeminal plate. One patient had a subtemporal operation to resect residual malformation extending into the fusiform gyrus. One patient required two interhemispheric operations for a large AVM extending from the anterior third ventricle to the splenium of the corpus callosum. The fifth patient was first operated on by a subfrontal approach to eliminate feeding vessels entering the malformation through the anterior perforated substance. His second operation was an interhemispheric exposure of the anterior right lateral ventricle where the malformation was removed from the head of the caudate and the septal region. Surgical Outcome There were no operative deaths in this series, and all 22 patients were able to resume their previous occupations after surgery. The most c o m m o n postoperative complication was a disturbance of recent m e m o r y . Eleven patients were noted to have at least transient problems in acquiring new knowledge. However, six o f these patients had suffered a preoperative m e m o r y disturbance as a result o f hemorrhage, and only three o f these were believed to be worse after surgery. All patients showed considerable i m p r o v e m e n t with time. Six patients were found to have a contralateral h o m o n y m o u s field defect after the operation. Two of these patients had field cuts preoperatively. Only two of these six patients had visual loss in the d o m i n a n t hemisphere; neither displayed a disabling disconnection syndrome and both were capable of reading and naming colors postoperatively. There were three cases o f postoperative hemisensory loss: one cleared completely within 1 week and two are persistent. Three patients had transient hemiparesis, and all of these regained essentially normal strength in 2 to 12 months. One patient with an A V M extending into the quadrigeminal region developed a profound e y e - m o v e m e n t disorder after surgery. Another patient who was neurologically normal developed a sterile ventriculitis and required prolonged steroid therapy. All 22 patients were studied with postoperative angiography. Total removal o f the A V M was confirmed in 18 cases, and residual malformation was noted in four. Reoperation in one o f these four patients again failed to obliterate the malformation. This patient rebled from the A V M 2 years after the second surgery, and a third operation at that time removed the residual lesion. FIG. 6. Drawings of the surgical approach. CC = corpus callosum; C = caudate nucleus; T = thalamus; LV = lateral ventricle; F = fornix; IC = internal capsule. Left: Coronal section of the brain in the region of the atrium of the lateral ventricle demonstrating the operative exposure of the thalamocaudate arteriovenous malformations (AVM's) in this series. Right: Operative exposure of the thalamocaudate AVM's as seen during surgery. Retractors are shown on the medial surface of the right parietal lobe. J. Neurosurg. / Volume 66/March, 1987 349 R. A. S o l o m o n and B. M. Stein Discussion Operative resection of AVM's in the thalamus and caudate region constitutes a formidable challenge for the neurosurgeon. These vascular malformations are located deep within the brain substance adjacent to several vital structures o f the central nervous system. It can therefore be anticipated that surgery for these lesions might produce profound and disabling neurological sequelae. However, the retrospective analysis presented in this report indicates that these lesions can be safely removed with current neurosurgical techniques. The preoperative preparation of these patients requires sophisticated neuroradiological studies. Highresolution CT scanning and, more recently, MRI have proved invaluable for the precise localization of the AVM's, and for defining their relationships to the tentorium, brain stem, and ventricular system. Stereoangiography has been useful in appreciating the threedimensional vascular anatomy, which is often critical for planning the surgical approach. Embolization has been a useful adjunct to the surgical treatment o f large supratentorial AVM's; ~3 however, malformations deep in the thalamus and the caudate region are generally not suitable for this procedure. These AVM's tend to be supplied by distal branches of the major arteries such as the choroidal, posterior cerebral, anterior cerebral, and thalamoperforating arteries. These vessels generally have small intraluminal diameters and arise from parent vessels at fight angles. These factors make embolization hazardous and therefore are not usually indicated for malformations in this location. The interhemispheric transcallosal approach to the deep paramedian lesions has been described previously in relation to medial hemisphere AVM's ~1 and AVM's that follow the tentorial ring? ~ This approach was first used by Dandy ~for removing posterior third ventricular tumors, and we have found it ideal for treating vascular malformations in the region of the atrium of the lateral ventricle. These AVM's invariably drain into the deep medial venous structures of the brain, and the arterial supply derives almost exclusively from the pericallosal and choroidal arteries. With hemispheric retraction, one may reach the posterior cerebral artery as it courses around the lateral side o f the brain stem and still have good visualization out to the atrium of the lateral ventricle. Therefore, a medial interhemispheric approach affords unequaled access to the arterial and venous components of these malformations. Other surgeons have operated on AVM's in the thalamus and caudate region via a transverse incision in the parietal lobe, 4 the superior temporal gyrus, 2 the middle temporal gyrus, ~5'~7 or the inferior temporal gyrus. 3 These approaches have the disadvantage of transgressing normal functioning brain before the malformation is reached. In addition, the AVM is first visualized on its lateral surface whereas the blood supply and the venous drainage are on the medial surface. The 350 surgeon must then work around the margins of a tense malformation to secure the arterial feeders. The postoperative complications and the neurological sequelae of hemorrhage observed in these patients with AVM's near the atrium of the lateral ventricle provide some insight into the functional neuroanatomy of this region of the nervous system (Fig. 6 left). The roof and posterior face of the atrium is formed by the posterior body and splenium of the corpus callosum. The body of the caudate nucleus lies inferolaterally, while the floor is formed by the posterior thalamus. The fornix lies on the medial side in the region of the choroidal fissure. Six patients in this series bled from malformations involving these structures on the left (dominant) side. Five o f these six patients developed memory problems consequent to AVM rupture. The other 16 patients had right-sided or bilateral lesions, and only one of these patients had a preoperative memory disturbance. Postoperatively, five additional patients displayed m e m o r y dysfunction, and one of these patients had a bilateral AVM that required sacrifice of both fornices and the corpus callosum. These data imply that dominance extends to the limbic system, and that the left fornix, thalamus, and/ or caudate nucleus are critical for recent memory function. Although considerable improvement in memory occurred in every impaired patient, in no instance did memory function return to normal once it had been damaged. The experience of Drake, 2 Kunc, 5 and Ya~argil, et al.,18 in dividing the posterior corpus callosum indicates that no serious functional impairment results. Several of our patients underwent psychometric testing following partial surgical division o f the splenium of the corpus callosum. In all instances a visual disconnection syndrome was demonstrable, but no patient was functionally impaired by this disconnection. Preservation of reading and naming functions, even when there was a dominant-hemisphere hemianopsia, was due to the limited section of the corpus callosum that we utilized. The splenium was never completely divided. G a m m a irradiation for the treatment of small AVM's has been advocated by Steiner, ~4who reported successful treatment of a large group of patients with complete obliteration of the malformations. The major drawback to this method is the long latency between treatment and obliteration o f the malformation. In many instances, this period exceeds 2 years, during which time the patient is at risk for hemorrhage. Additionally, the long-term deleterious effect of this high-energy radiation is unknown. Therefore, patients should be chosen carefully for radiosurgery. Four patients in this series had incomplete removal. One of these patients had two operations, both of which failed to obliterate the malformation. We have noted that many of these deep malformations have indistinct margins, and this factor indicates the increased technical difficulties that may accompany surgical removal of thalamocaudate AVM's. Only one patient rebled from J. Neurosurg. / Volume 66/March, 1987 Interhemispheric approach for thalamocaudate AVM's an incompletely r e m o v e d A V M , but the possibility of incomplete removal m u s t be factored into the equation when considering operating on malformations in this location. Twenty-one o f 22 patients in this series presented with intracerebral h e m o r r h a g e as the first s y m p t o m of a thalamocaudate A V M . This m o d e o f presentation would be expected since these malformations were essentially all deep-seated lesions less than 2.5 c m in diameter. Larger m a l f o r m a t i o n s bleed less frequently, 8 and A V M ' s involving cortical structures can often induce seizures as an initial manifestation. 7 Reliable criteria to relate the surgical m o r b i d i t y for thalamocaudate A V M ' s to their natural history will probably never be available. Nonetheless, the incidence o f death or serious morbidity from h e m o r r h a g e o f deep-seated A V M ' s is substantial, 16 and this factor warrants surgical intervention. C o m p a r e d to the risk o f morbidity due to an untreated A V M , which approaches 50%, 6,t3 no patient in this series o f 22 patients with thalamocaudate A V M ' s was significantly impaired by surgery. References 1. Dandy WE: Diagnosis, localization and removal of tumors of the third ventricle. Bull Johns Hopkins Hosp 33: 188-189, 1922 2. Drake CG: Cerebral arteriovenous malformations: considerations for and experience with surgical treatment in 166 cases. Clin Neurosurg 26:145-208, 1979 3. Heros RC: Arteriovenous malformations of the medial temporal lobe. Surgical approach and neuroradiological characterization. J Neurosurg 56:44-52, 1982 4. Juhfisz J: Surgical treatment of arteriovenous angiomas localised in the corpus callosum, basal ganglia and near the brain stem. Acta Neurochir 40:83-101, 1978 5. Kunc Z: Deep seated arteriovenous malformations: a critical review, in Carrea R (ed): Neurological Surgery, with Special Emphasis on Non-Invasive Methods of Diagnosis and Treatment. Amsterdam: Excerpta Medica, 1978, pp 188-193 6. Luessenhop A J: Natural history of cerebral arteriovenous malformations, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp I2-23 J. Neurosurg. / Volume 66/March, 1987 7. Mohr JP: Neurological manifestations and factors related to therapeutic decisions, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp l-11 8. Morello G, Borghi GP: Cerebral angiomas. A report of 154 personal cases and a comparison between the results of surgical excision and conservative management. Aeta Neurochir 28:135-155, 1973 9. Solomon RA, Stein BM: Management of arteriovenous malformations of the brain stem. J Neurosurg 64: 857-864, 1986 10. Solomon RA, Stein BM: Surgical management of arteriovenous malformations that follow the tentorial ring. Neurosnrgery 18:708-715, 1986 11. Stein BM: Arteriovenous malformations of the medial cerebral hemisphere and the limbic system. J Neurosurg 60:23-3 l, 1984 12. Stein BM: General techniques for the surgical removal of arteriovenous malformations, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 143-155 13. Stein BM, Wolpert SM: Arteriovenous malformations of the brain. II. Current concepts and treatment. Arch Nenrol 37:69-75, 1980 14. Steiner L: Treatment of arteriovenous malformations by radiosurgery, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 295-313 15. U HS: Microsurgical excision of paraventricular arteriovenous malformations. Neurosurgery 16:293-303, 1985 16. Viale GL, Turtas S, Pau A: Surgical removal of striate arteriovenous malformations. Surg Neurol 14:321-324, 1980 17. Wilson CB, Martin NA: Deep supratentorial arteriovenous malformations, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 184-208 18. Ya~argil MG, Jain KK, Antic J, et al: Arteriovenous malformations of the splenium of the corpus callosum: microsurgical treatment. Surg Neurol 5:5-14, 1976 Manuscript received May 29, 1986. Accepted in final form September 23, 1986. Address reprint requests to: Robert A. Solomon, M.D., Room 204, The Neurological Institute, 710 West 168th Street, New York, New York 10032. 351