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Multimodality Treatment of Deep Periventricular Cerebral Arteriovenous Malformations Hoi Sang U, M.D., Charles W. Kerber, M.D., and Michael M . Todd, M .D. Division of Neurosurgery and Departments of Radiology and Anesthesia, University of California San Diego, San Diego, California

U HS, Kerber CW, Todd MM . Multimodality treatment of deep periventricular cerebral arteriovenous malformations . Surg Neurol 1992 ;38 :192-203 .

The surgical treatment of arteriovenous malformations (AVMs) located in deep periventricular regions such as the basal ganglia is associated with marked morbidity and mortality . Approaches through critical brain regions afford limited exposure of the lesions, while surgical dissection is sometimes complicated by acute severe brain swelling and/or hemorrhage in the surrounding tissues . In our approach to deep AVMs, our regimen has evolved from direct staged microsurgical excision under routine fentany-N 2 O-relaxant anesthesia (first four patients) to the use of elective high-dose barbiturate anesthesia (subsequent 12 patients) . In the first group of four patients, 11 operations were performed . Two patients improved, one of whom returned to normal neurologically. There were three episodes of acute brain swelling and/or hemorrhage . One patient died as a result, and another deteriorated. In the second group of 12 patients, all but two lesions were completely excised . Among the 10 patients in whom the AVM was completely excised, seven improved, six of whom achieved a good to excellent outcome, with two regaining full neurologic function . Three patients worsened (one as the result of acute brain swelling and/or hemorrhage) . There was no death in this group . Only one incidence of acute brain swelling and/or hemorrhage occurred in 26 operations . Even though the number of patients is too small in the first group for meaningful statistical comparison, our intraoperative observations and postoperative results suggest that our evolved multimodality regimen, such as staged excision and the use of elective high-dose barbiturates, was likely to have contributed to the improved treatment results of these formidable lesions . woRDs : Arteriovenous malformation ; Basal nuclei ; Embolization ; Staged excision ; Barbiturates KEY

The therapeutic options available to patients with arteriovenous malformations (AVMs) located in functionally critical regions of the cerebral cortex have increased significantly in recent years [5,8,9,26,29,34,36], and the morbidity and mortality associated with the surgical excision of these lesions has been reduced to acceptable levels in many centers . This improvement is partly due to the use of microsurgical techniques but has also been aided by innovations in interventional neuroradiology (e .g ., catheter embolization techniques) 16,12,14-17, and in the anesthetic management of patients 2 undergoing long and complex procedures [10,11, 30-32] . Despite these developments, the therapy of deeply seated periventricular AVMs continues to pose significant problems 118,24,25,33] . They must often be approached through functionally critical or eloquent areas of the brain . The surgical exposure is frequently limited, and it may be difficult to accurately localize the margins, particularly when the AVM is small and deep . Furthermore, surgical dissection is sometimes complicated by the occurrence of acute severe ("malignant") brain swelling and/or hemorrhage from the AVM or surrounding tissues [3,4,7,19-21,28,33] . In an effort to improve our results in the care of patients with such deep-seated AVMs, a therapeutic regimen has gradually evolved that now includes preoperative embolization and subsequent surgical excision performed in a series of separate staged operations, occasionally aided by intraoperative angiography . Each surgical procedure is carried out using a high-dose barbiturate anesthetic, with or without hypothermia [1,27] . This report details our experience in 16 patients treated between 1979 and 1989 and discusses the evolution of our current approach .

Materials and Methods Patient Population Address reprint requests to : Hoi Sang U, M .D ., Division of Neurosurgery, University of California San Diego, 225 Dickinson Street, San Diego, California 92103-8893 . Received November 18, 1991 ; accepted March 4, 1992 .

c)

1992 by Elsevier Science Publishing Co ., Inc .

This analysis includes only those patients harboring cerebral AVMs that were primarily or substantially located in the basal ganglia, thalamus, hypothalamus, internal 0090-3019!92155 .00



Treatment of Deep Periventricular AVMs

capsule, or deep in the periventricular regions . In the latter locations (as in patients 11 and 15), parts of the AVM might have presented at the cortex, but this constituted only a small component of the lesion, whereas the bulk of the lesion was deep in the periventricular white matter . Patients with AVMs located solely inside the ventricular system or the brain stem and patients in whom a substantial portion of the AVM was present on the cortical surface are excluded . A total of 16 patients meeting these criteria were treated at the University of California at San Diego between 1979 and 1989 . Pretreatment Evaluations Each patient was initially evaluated with analog magnified cerebral angiography of the entire intracranial circulation . Angiography verified the diagnosis, indicated the degree of vascular shunting, located associated aneurysms, and delineated the draining veins . A computed tomographic (CT) scan in multiple planes was also performed . This allowed for the accurate appreciation of the relationship between the AVM and the ventricular and basal nuclei systems . In the last 3 years, most patients have also had magnetic resonance imaging (MRI) scans, which provided a clearer delineation of intracerebral structures . Intravascular Embolization In six patients, preoperative embolization of the arteriovenous shunts was undertaken in order to facilitate the surgical manipulation at each stage and to reduce the number of operative stages necessary for total AVM excision . Staged isolation and final excision of the AVM was undertaken only after all avenues of embolization were exhausted . Embolization was deemed not feasible in the remaining patients due to the tortuosity of the feeding vessels and their distal location . Superselective angiography and embolization was performed via the femoral percutaneous placement of 2F polyethylene or silicone microcatheters . Direct superselective amobarbital (Amytal) injection (25-45 mg) through the microcatheter allowed reversible functional testing. Then, various embolic agents, usually in combination, were introduced under direct live subtraction control . Agents used were primarily polyvinyl alcohol foam particles, 2-cm lengths of silk or Dacron suture, or various opaque tissue adhesives (cyanoacrylates) . No coils or detachable balloons were used, but occasionally the flow through the lesion was mechanically slowed by a proximal balloon in the middle cerebral artery to allow for more adequate penetration of the arteriovenous shunt by the emboli or glue . Most treatments were staged empirically .

Surg Neurol 19 3 1992 ;38 :192-203

Operative Approach Large periventricular lesions deep in the centrum semiovale frequently drained through cortical venous channels . The operative approach to these lesions, therefore, followed draining veins to the AVM nidus . The sulci involved were enlarged for adequate exposure . Lesions located in the basal nuclei, internal capsule, or thalamus presented through the ependymal lining of the floor of the lateral ventricle . The first three of these lesions were initially approached through the sylvian fissure (patients 1, 2, and 3) . Large feeding arteries of the lenticulostriate group or draining veins were identified and followed to the lesion . Excision was undertaken without deliberate exposure of the lateral ventricle . Due to the occurrence of unanticipated and fatal hemorrhage into the lateral ventricle in the third case early in our experience, this approach was abandoned in favor of a direct midfrontal gyrus approach to the ventricular system . In this latter exposure, an AVM presenting at the ependymal surface was dealt with in the same manner with which we excised cortical lesions . The part of the ventricular system associated with the AVM was isolated with packing to prevent any hemorrhage from entry into the rest of the ventricular chambers . The AVM was progressively isolated from the surrounding brain by section of any entering arteries or exiting veins located in the immediate perilesion gliotic plane. The entire lesion was excised only at the final operative stage . The two small periventricular lesions both presented with intracerebral and intraventricular hemorrhage (patients 7 and 14) . Surgery for complete AVM excision was undertaken at some intervals (weeks and months) after initial clot evacuation at other institutions . We entered through the previous operative approaches in the midfrontal gyrus and high parietal region, respectively .

Anesthetic Considerations The first four patients treated with staged excisions of large basal AVMs received routine fentanyl-N 2 0-relaxant anesthetics for a total of I 1 procedures . In view of the poor results as a result of the onset of sudden malignant swelling and hemorrhage-which occurred in three of these patients, who had to be treated with the emergent institution of barbiturate therapy-we elected to employ an elective, high-dose barbiturate anesthetic combined with induced hyporension . Our intent was to achieve the lowest possible global cerebral blood flows (and blood volumes) in these individuals at the time of resection, hoping to minimize vascular engorgement and the magnitude of any sudden changes in the hemodynamics of both the AVM and surrounding tissues during occlusion of feeding vessels .



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Prior to the induction of elective barbiturate coma anesthesia, both radial artery and pulmonary artery catheters were placed . A minimum of two electroencephalogram (EEG) channels were recorded using either a standard electroencephalograph or a Lifescan® computerized processor (lead placement was governed by the location of the planned surgical flap) . Other monitors were standard (electrocardiogram, pulse oximetry, expired gas analysis, etc .) . Anesthesia was then induced with thiopental (3-6 mg/kg), followed by fentanyl (8-15 ,ug/kg) and a nondepolarizing relaxant . Anesthesia was initially maintained with N 2O and isoflurane, while PaCO 2 was adjusted to values of 25-30 mm Hg. Cooling blankets placed above and below the patient were used to begin reducing body temperature (measured both in the nasopharynx and pulmonary artery) . An effort was made to achieve a target of 30°-32°C at a time shortly after dural opening . Sometime after skin incision, an infusion of pentobarbital was begun, with the dose titrated to achieve deep burst suppression on the EEG . The initial dose was approximately 10-15 mg/kg given over 30-60 minutes, and the dosage titrated thereafter to maintain the desired degree of EEG suppression . Isoflurane was discontinued . A temperature-uncorrected PaCO 2 of -30 mm Hg was maintained . While these patients were usually modestly hypotensive (systolic blood pressure --90-100 mm Hg), lower pressures were achieved, when required, using nitroprusside . Upon completion of the intracranial portion of the surgery, pentobarbital administration was discontinued and warming begun . Either a ventriculostomy or a fiberoptic intracranial pressure monitor (Camino) was placed, and PaCO 2 increased toward normal as long as intracranial pressure remained acceptable . Paralysis and sedation were maintained for 24 hours, during which time arterial pressures were rigorously controlled .

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in diameter), and 10 large (> 4 cm in diameter) lesions . One patient harbored an aneurysm, and another possessed two aneurysms . The most common presenting symptoms were intracranial hemorrhage (eight patients) and progressive neurologic deficits (four patients) (Table 2). Three patients presented with headaches initially but then developed progressive deficits . Similarly, one patient whose initial symptom was a seizure also developed a progressive deficit. The neurologic deficits in these patients at the time of presentation correlated well with the location of their lesions and were presumed to result from either local ischemia or hemorrhage . Occasionally, the clinical status (e .g., coma) reflected the presenting hemorrhagic event. Since most lesions were intimately associated with the internal capsule, hemiparesis or hemiplegia were the most common physical deficits (the hemiparesis being usually a severe deficit), occurring in 11 patients . In three of these, additional neurologic dysfunction was observed . One patient had diffuse, acute hemispheric swelling, presumably due to extensive ischemia as a result of the arteriovenous shunting and was markedly obtunded (patient 1) . She rapidly deteriorated, and surgery was performed emergently . Another patient with a large left caudate and frontal AVM had a right hemiparesis associated with decreased intellectual function and flat affect (patient 11) . A third patient who had bled from a left peritrigonal AVM presented with hemiparesis and memory loss (patient 14) . Of the remaining six patients, two manifested expressive dysphasia (lesions in the deep anterior and posterior speech areas), one had a mild hemianopsia (lesion in the deep temporal region), one had lost urinary control (lesion in the caudate and supplementary motor region), and two presented in coma as a result of acute intracerebral hemorrhage . Preoperative Intravascular Embolization

Intraoperative Angiography To assess the adequacy of operative excision, we examined all patients seen after November 1988 with digital intraoperative angiography using standard techniques .

Results Patient Population A total of 16 patients harboring deep periventricular AVMs were treated (Table 1) . This group of patients consisted of 11 women and five men, their average age being 32 years (range 12-60 years) . Six lesions were located in the dominant left hemisphere ; the remaining 11 AVMs resided in the right hemisphere . There were two small (< 2 cm in diameter), four moderate (2-4 cm

Preoperative embolization was performed in six patients, with partial but significant obliteration of the AVMs . Two developed transient focal deficits during or after embolization (patients 12 and 13), but all had recovered to baseline within days . The remaining patients harbored AVMs with feeding arteries that were too small or tortuous to catheterize . Operative Treatment The first three patients were treated with operations that approached the lesions by tracing the feeding arteries or draining veins from the sylvian subarachnoid space into the brain substance . This afforded excellent exposure of the superficial aspects of the malformations . Patient 2 harbored a giant AVM that presented with headache and



Treatment of Deep Periventricular AVMs

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Table 1 . Summary of Arteriovenous Malformation

Case

Age, yr/sex

Lesion

Chief complaint

OP

dates

1

30/F

R basal ganglia

Seizures, hemiparesis

12/79, 12/79

2

l4/M

R temporo-occipital

Headaches

3

60/F

R

10/80, 10/80, 12/80 . 12/80, 1/81 9/81, 10/81

4

40/F

L basal ganglia

5

28/M

R

6

basal ganglia

Hemiparesis

Preop condition

Embol . ization

Hemiparesis, marked & progressive obrundation Hemianopsia

x 2

Hemiparesis

x 2

Headache, dysphasia

9/81, 12/81, 8/82

Dysphasia, hemiparesis

thalamus

Hemorrhage

1/82, 7/82

Apraxia, hemiparesis

12/F

R Thalamus

Hemorrhage

Hemiparesis

7

26/M

R

basal ganglia

Hemorrhage

3/82, 4/82, 6/82, 7/82 3/84, 3/84

8

28/F

R

basal ganglia

Hemorrhage

7/83, 2/84, 7/84, 11/84

Hemiparesis

9 10

27/F 31/F

Lbasal ganglia R basal ganglia

Hemorrhage Hemorrhage

Hemiplegia/aphasia Hemiparesis

ll

40/F

x I

24/M

Numbness, clumsiness, memory deficit Headache, dysphasia

Numbness, dysphasia

12

Rostra/ corpus callosum, mesial frontal L deep angular

3/85 1/87, 2/87, 3/87 8/87, 9/87, 1/88 2/87

Dysphasia, hemiparesis

x 11

13 14

38/F 21/F

Hemiparesis Hemorrhage

5/88, 7/88 9/88

Normal Hemiparesis

x2`

15

42/M

Deep R parietal Deep L angular gyros Deep L frontal paramedian R basal ganglia

Voiding problem

6189,7/89

Normal

X

Hemiparesis

52/ F Hemorrhage 12/89 Coma Abbreviations : Op, operation; Preop, preoperative; 10, intraoperative ; Postop, postoperative ; F, female ; R, right. N/ N/R, nitrous oxide/narcotic/relaxant, male ; Rx, treatment with ; L, left ; B, elective barbiturate anesthesia; Pt, patient. " Rapid awakening from methohexital anesthesia, hypertensive hemorrhage . Preoperative embohzation complicated by dysarthria and right-sided hemiparesis. ` First preoperative embolization aborted due to vasospasm; second preoperative embolization complicated by left-sided hemiparesis . 16

hemianopsia. The AVM was excised in five stages, and the patient has done very well, aside from a residual field defect . In the first and third patients, the basal ganglia lesions were extensive and presented at the lateral ventricles . The AVM was excised from patient 1 in two operations . She recovered completely from deep obtundation and hemiplegia and returned to full employment . During the second-stage operation in patient 3, unrecognized hemorrhage into the lateral ventricle contributed to the concurrent acute brain swelling . The outcome was fatal, Since this occurrence, we have adopted a transfrontal approach to basal lesions that adjoined the ventricular system, so that the ventricular space associated with the lesion can be isolated. The transfrontal, transventricular approach to basal

1

M,

AVMs afforded improved exposure to the ventricular system from the frontal horn to the trigone . Lesions in the lateral aspect of the internal capsule could be approached with ease . After division of the feeding arteries and draining veins from one aspect of the AVM, the surface of the lesion was shrunk by coagulation . This further developed the dissection plane and minimized the need for brain retraction, which enabled us to achieve a total excision of all but three lesions . We incompletely removed three lesions (patients 7, 8, and 10) . In patient 7, the caudate head AVM was small and had been separated into discrete components by the initial hemorrhage . The majority of the components were removed during our approach . The postoperative angiogram, however, still demonstrated a small



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10 Angio

Bleeding/ swelling

U et al

Postop condition

Comments

N/N/R

Total resection

outcome

Total recovery . over 1 year

Yes

Excellent

N/N/R

Yes

Rx barbiturates

Unchanged

Yes

Excellent

N/N/R

Yes

Rx barbiturates

Comatose

No

Died

N/N/R twice, then B B

Yes

Rx barbiturates

Hemiparesis unchanged

Yes

Fair

Acute postop hemorrhage'

Yes

Poor

B

Hemiparesis, altered mentation Unchanged

Yes

Good

B

Improved

No

Dysphasia, hemiparesis unchanged, mentarion improved

No

Good (Pt refused further treatment) Fair

Dysphasia Unchanged

Yes No

Normal

Yes

Good Fair (Pt refused further treatment) Excellent

Improved dysphasia

Yes

Excellent

Normal Improved

Yes Yes

Excellent Good

Mild hemiparesis

Yes

Good

Emergence from coma

Yes

Poor

B

Yes

B B B

Early pulsation, postop hemorrhage, temporal lobectomy, clot removal High K + cardiac arrest

Yes

-

B B B

Yes

B

Yes

Yes

B

Yes

No

Failed 10 embolization, posrop pulmonary embolization Embolization, transient hemiplegia

Swelling at angiography well controlled

portion with an early draining vein (Figure 1) . The patient is much improved from the presenting hemiplegia but declined further surgery . He moved from California for employment reasons and, despite subsequent repeated follow-up by telephone, has insisted against sur-

Table 2 . Presentations of Deep-Seated Arteriovenous Malformations Presentation

No .

Intracranial hemorrhage Progressive neurologic deficits Headaches -+ progressive neural deficits Seizures -> progressive neural deficits

S 4 3 1

gery to completely remove his AVM . Patient 10 harbored a moderate-sized right basal ganglia AVM that presented with hemorrhage, resulting in a severe hemiparesis . The lesion was approached in stages . She adamantly refused the intended final-stage excision and still has a small residual component of her AVM . The severe hemiparesis she presented with is only mildly improved . Patient 8 harbored a large right basal ganglia AVM that demonstrated significant arteriovenous shunting on angiography . The lesion was approached in stages, using elective barbiturate coma anesthesia. During dural closure after an otherwise uneventful fourth-stage operation, sudden uncontrollable brain swelling and hemorrhage occurred . This led to central herniation, as well as massive intraventricular and infratemporal hemorrhage,



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Figure 1 . Patient 7 . a 41-year-old man, presented with intracerebral hemorrhage.(A) Preoperative frontal .wbtracted right internal carotid artery injection demonstrated a single feeder to this deep-seated AVM nidus . Arrows outline the nidus . Early veins drained deep into the internal cerebral vein . (B) Postoperative right anterior oblique view, early arterial phase . The single feeding vessel and the AVM nidus was again rioted (arrows) . One-half second later, prominent deep venous drainage appeared . (C) Postoperative unsubtracted Town view . right internal carotid injection, 2 .0 seconds after contrast injection . Arrows demonstrate the persistent early draining vein passing into the infernal cerebral rein,

necessitating temporal lobectomy and intraventricular clot evacuation . Nevertheless, she recovered from coma and eventually received proton beam obliteration of a small residual AVM . Five and one-half years after the intraoperative catastrophe, she continues to improve in her ability to ambulate and is leading a meaningful life as an active member of her family . Her intellectual function, however, has remained compromised .

Anesthetic Considerations Prior to 1982, 11 operations were performed on four patients using the standard nitrous oxide-narcotics-

relaxant technique (Table 3) . Three incidents of acute malignant cerebral swelling and/or hemorrhage were encountered in separate patients . There was no warning of any of these events, which usually reached their full extent within 2 minutes . Execution of standard methods of brain relaxation (i.e ., hyperventilation, mannitol, head elevation) was never successful . Finally, large doses of thiopental (2-5 g) were administered to achieve adequate cerebral relaxation [19,33] . Despite this, one patient (patient 3) died as a result of cerebral herniation, and two others suffered mild but permanent impairment [33] .



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Table 3. Brain Swelling and Hemorrhage with and without Barbiturate Coma Anesthesia

Without barbiturate coma With barbiturate coma

Operations (stages), no .

Malignant brain swelling/hemorrhage, no .

11

3

26

1

was discovered (Figure 2) . The dissection resumed, and a second angiogram confirmed complete removal . In the other five cases, angiography confirmed the surgical impression of total AVM excision . However, acute cerebral hyperemia and moderate local swelling developed at the time of angiography in one patient (patient 15) ; this led to the development of mild but permanent hemiparesis .

Summary of Treatment Results Following these events, we induced barbiturate coma in a controlled fashion as the elective anesthesia, with the patient under full cardiopulmonary and electrophysiologic monitoring for the next 26 operations . The practical implementation of this anesthetic approach has undergone a long evolution . A large series of patients (most not included here) were anesthetized with thiopental, pentobarbital, or methohexital concurrently with an extensive evaluation of the hemodynamic impact of drug doses in excess of those needed to render the EEG isoelectric [10,11,30-32] . Early patients given thiopental for the duration of their procedures (81-14 hours) required several days to awaken . Methohexital, a much shorter acting barbiturate, was then used . Its hemodynamic effects were identical to thiopental, and emergence was indeed much faster . However, three patients developed withdrawal seizures, and one patient (patient 5) awoke very suddenly, became severely hypertensive, and suffered an intraventricular hemorrhage . The drug was then abandoned . Finally, after evaluating a high-dose pentobarbital anesthetic, the current anesthetic regimen was chosen . In all cases, the brain was subjectively more relaxed, thus facilitating the operative approach . Acute cerebral swelling and hemorrhage did occur in one patient (patient 8), resulting in permanently impaired intellect and motor function . This adverse event occurred without warning at the end of an uneventful operation . This same patient had marked cerebral pulsation in a prior operation after we eliminated many of the arteriovenous shunts . That operation was terminated without any untoward sequelae . In those patients treated with elective barbiturate coma as currently used, the immediate postoperative course (most specifically, blood pressure control) was smooth throughout . The patients awoke in 36-48 hours .

Intraoperative Angiography Since November 1988, intraoperative angiography was performed after visual inspection of the surgical field led the surgeon to believe that the AVM was completely excised . In one case, a 1 x 1 x 1-cm residual portion

Four patients were treated with staged obliteration of their AVMs using standard anesthetic techniques (Table 4) . One patient recovered fully from hemiplegia and rapid progression to semicoma . Incapacitating headache (the presenting complaint) resolved in patient 2, but his homonymous hemianopsia remained (although he is otherwise normal) . Patient 4 developed a hemiparesis and dysphasia, and patient 3 died . Both these latter events developed as a result of acute brain swelling and/or hemorrhage . Twelve patients received staged treatment of their AVM under elective barbiturate anesthesia (Table 4) . The AVM was completely removed or obliterated in 10 patients . Two of these patients regained full neurological function . Four patients had marked improvement of neurological dysfunction, while one patient who presented in coma from a hemorrhage improved only to a state in which she could utter a few words . Three patients worsened-one from acute intraoperative brain swelling and hemorrhage, one from hypertensive hemorrhage due to unexpected awakening, and one from cerebral swelling during intraoperative angiography . Of the two patients who did not achieve complete AVM obliteration, hemiparesis was significantly improved in one but remained unchanged in the other . There were no deaths in this latter group .

Discussion Treatment of large, deep periventricular AVMs still poses a considerable challenge [18,24,25,33] . All 16 patients reported here were treated because of intracranial hemorrhage or progressive neurologic deficits . With the exception of patients 13 and 15, all had disabling neurologic deficits . The goal of therapy was complete excision of the AVM . With the employment of transvascular embolization and particularly the use of elective barbiturate coma anesthesia [10,11,19,30-32], the microsurgical excision of these formidable lesions has become feasible. This report details the evolution of our experience, which shows that in the latter group of 12 patients whose AVM was treated with staged excision



Surg Neurol 199 1992 ;38 :192-203

Figure 2 . Magnified subtraction views of cerebral angiogram, patient 11 . (A) Computed tomography of the AVM . The bulk of the AVM occupied the gene of the corpus callosum and the left caudate head. (B) Lateral view, right internal carotid artery injection . A series of images showed almost immediate filling of a 5 X 5 x 6-cm AVM nidus. Frontal views demonstrated filling of the nidus via a large anterior communicating artery . The lesion was actually within the patient's left cerebral hemisphere ; the left internal carotid artery was completely occluded, None of the normal distal branches of either anterior cerebral arteries was visualized . (C) Lateral left vertebral artery injection . Contrast agent passed anteriorly through a patient's large posterior communicating artery to fill the distal left internal carotid artery . The internal carotid artery was occluded from the bifurcation in the neck to this point . The etiology of that occlusion is not determinable . Arrows point to large posterior pericallosal collaterah . (D) Early frontal view, right internal carotid artery injection . A 2F balloon-tipped microcatheter was then guided across the large anterior communicating artery and into the main feeding vessel. Using real-time fluoroscopy, about 0 .5 mL of tantalum-opacefied isobutyl-2-ryanoacrylate was delivered into the depths of the nidus. (E) Frontal view, right internal carotid artery injection . Final surgical result. Note absence of both anterior cerebral arteries and the good filling of the middle cerebral artery complex now that the shunt has been removed. Even on delayed films, no AVM nidus remained .



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under elective barbiturate coma (in 26 operations), the morbidity was improved, and there was no mortality . Most of the patients treated had suffered severe neurologic deficits as a result of their AVMs . The majority of these lesions were of a size most likely inappropriate for radiation therapy, and thus, surgical excision was the only available therapeutic modality . Our indications for surgical treatment were stringent and were limited to

U et al

only intracranial hemorrhage and progressive neurologic deficits . The evolution of our approach to these deep lesions occured at a time when no "standard" approach to these abnormalities was available . Even though the first two patients achieved an excellent outcome, the occurrence of malignant hemorrhage and/or swelling, frequently at sites distant from the AVM nidus, rendered an overall unsatisfactory result in the first four patients



Treatment of Deep Periventricular AVMs

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Table 4 . Outcome of Treatment of Deep-Seated Arteriovenous Malformations

Neurologically intact Improved Unchanged Deteriorated Death

Without barbiturate anesthesia

With barbiturate anesthesia

1 1

2 5 2 3" -

- One patient had a postoperative hemorrhage due to hypertension (methohexital used as anesthetic) ; one patient deteriorated from malignant brain swelling and hemorrhage ; and one patient developed a mild hemiparesis during intraoperane angiography .

treated with standard microsurgical and anesthetic techniques . These therapeutic techniques were therefore modified with the adaptation of the transventricular approach to basal lesions and the use of elective barbiturate coma as the anesthetic . One of the most pressing issues in approaching large, deep AVMs with significant arteriovenous shunting is acute cerebral swelling and/or hemorrhage [2-4, 7,19-21,28,37,38] . Some of these events may have occurred as a result of intraoperative hemorrhage from residual AVM clusters deep in the brain substance, which are hard to approach . These latter hemorrhages are usually localized in nature and are unlikely to lead to diffuse panhemispheric swelling or multiple hemorrhages at sites distant from the AVM bed . Nevertheless, these localized hemorrhages were, and can be, addressed by improved microsurgical techniques . On the other hand, acute massive swelling with or without hemorrhage, especially at sites distant from the AVM bed, cannot be so easily explained . Such swelling may have resulted either from the overly rapid redistribution of blood to the surrounding vasculature, which has been rendered incapable of autoregulation as the result of prolonged hypoperfusion, or from the dysfunction of vasomotor centers located in the periventricular regions [13,22] . This acute swelling and hemorrhage may occur without warning and, in our experience, has in each instance led to significant morbidity and mortality . One means of assisting the surrounding vasculature to accommodate this acutely changing hemodynamic state is to eliminate these shunts in stages [1,27,33] . This graded approach has permitted the excision of large lesions with what we believe to be a reduced incidence of acute brain swelling or hemorrhage . Nevertheless, this potentially catastrophic event still occurs without warning, as in the first four patients in this series (three times in 11 operations) . Whenever the brain extruded through the craniotomy, the administration of large doses of barbiturate was invariably needed for brain relaxation ; even then, impairment of the protruded cortex would ensue .

We therefore altered the anesthetic technique to one involving elective barbiturate coma, as a result of these incidents of acute swelling and hemorrhage . The brain was much more relaxed, and exposure of deep structures was greatly facilitated . Localized hemorrhages were easily dealt with . In addition, the incidence of acute swelling and hemorrhage was reduced (one occurrence in 26 operations) . We attribute this to the reduction of blood flow and blood volume as a result of reduced cerebral metabolism . Since total cerebral blood flow and blood volume are reduced by these large doses of barbiturates (and by the accompanying hypotension), the amount of blood "available" for redistribution to the surrounding vasculature or present to fill a paralyzed vascular system is likewise reduced . When cerebral swelling did occur, it was much easier to treat with standard brain relaxation techniques. The result of treatment also improved . Thus, the addition of barbiturate anesthesia to staged elimination of the AVMs by way of the transventricular approach has substantially aided us in achieving total excision, with progressively better results . The remaining dilemma resides in the extent of each staged excision one could perform before progression to acute swelling . Vasomotor instability was suggested by the increased pulsation of the surrounding brain as elimination of the arteriovenous shunt progressed . Whenever this occurrence was observed, we have aborted the operation, without progression to acute brain swelling or hemorrhage . It is not clear whether brain swelling would ensue should the operation be continued . In addition to the use of elective barbiturate anesthesia, other operative adjuncts have been employed . The availability of intraoperative angiography has permitted us to verify the completeness of AVM excision. This is of particular importance in surgery for small lesions or lesions composed of multiple compartments . Had intraoperative angiography been available during the excision of the AVM in patient 7, we most likely would have discovered the small residuum and removed it . From a practical standpoint, angiography in the operating room would eliminate the need for wound closure and patient transport to a separate angiographic suite for investigation of the operative progress . The risks of wound infection and prolonged anesthesia would likewise be reduced . We encountered one episode of cerebral hyperemia and moderate cerebral swelling while performing an intraoperative angiogram . The relationship between these two events could not be clearly determined, although a similar event has been reported during attempted embolization . AVMs not completely excised can be as hazardous as ones left untreated . We therefore strived for total excision and/or elimination of all lesions whenever feasible .



2 02

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In this experience, three AVMs were not totally surgically excised . In patient 8, the small residual AVM was finally eliminated by proton beam irradiation . This patient has continued a remarkable recovery in mentation and gait, 7 years following her last surgery . Patients 7 and 10 initially declined irradiation and have adamantly refused any further treatment whatsoever, despite multiple attempts to convince them of the risks of harboring a residual AVM . In summary, the use of hyperselect embolization and elective barbiturate coma in the staged treatment of extensive deep AVMs has enabled us to successfully treat these lesions with decreased morbidity and mortality. In the initial four patients, a 50% excellent outcome was attended by a 25% morbidity and 25% mortality . After the adoption of our evolved techniques, there was no mortality in the second group of 12 patients . In the 10 patients in whom total AVM elimination was achieved, seven (70%) improved, of whom six had a good to excellent outcome . Three patients (30%) deteriorated following our therapeutic attempts, though they both maintain functional life styles . Therefore, although the treatment of large, deep AVMs remains a formidable problem, these lesions should no longer be considered inoperable . The authors would like to thank Drs . J . Alksne, L. Marshall, H. Shapiro, J. Drummond, M . Zornow, M . Scheller, J . Fleischer, the neurosurgical house staff, the operating room nursing staff, and particularly the neurosurgical intensive care unit staff at UCSD Medical Center for their support and dedication in the care of critically ill patients . We would also like to thank Dr . C . Wilson at UCSF for his helpful input during the preparation of this manuscript, and R . Morgan for his unfailing and excellent editorial assistance .

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