Journal of Radiosurgery, Vol. I, No. 3, 1998

Radiosurgery for Cerebral Arteriovenous Malformations

Lucia Zamorano, M.D., Dr. med,1,3 Amgad Matter, M.D.,1 Laurie Caspar, M.D.,2 ArturoSaenz, M.D.,1 Razvan Buciuc, M.D.,1 James Fontanesi, M.D.,2 Azucena Garzon, M.S.,3 andFernando Diaz, M.D., Ph.D.1

From September 1991 to May 1997, a total of 59 patients diagnosed with cerebral arteriovenousmalformations were treated using radiosurgery. There were 29 men and 30 women, with an agerange of 5 to 75 years (mean 36). Of these patients, 39 patients were treated using a LINAC-basedsystem (group 1) and 20 using the Leksell y-knife unit (group 2). Tumor volume ranged from0.38 to 35 cc, and the number of isocenters varied from 1 to 3 in group 1 and from 2 to 15 ingroup 2. Lesion location was as follows: 14 temporal, 8 basal ganglionic, 8 frontal, 6 parietal, 6thalamic, 5 intraventricular, 5 cerebellar, 3 brain stem, 3 occipital, and 1 corpus callosal. Sevenpatients underwent prior embolization and three patients had prior surgery with incomplete resec-tion of their lesions. The marginal radiation dose ranged between 1500 and 2000 cGy with a meanof 1800 cGy. Twelve patients had concomitant embolization done on the morning of radiosurgery.Follow-up ranged from 1 month to 4 years. Thirty-six patients have been followed for more than1 year. Thirty had an angiography during the follow-up period that showed complete obliterationof the lesion in 28 patients. The rate of obliteration was estimated to be 47.1% at 1 year, 82.3%at 2 years and 88.2% at 3 years.

INTRODUCTION

The ideal treatment for cerebral arteriovenous mal-formations (AVMs) has been a point of controversy fordecades. In the past two decades, considerable advanceshave been made in the three primary treatment modali-ties currently used for AVMs, namely, microsurgery,embolization, and radiosurgery. Although surgery is thegold standard for the treatment of brain AVMs, surgicaltechniques may not be suitable for some patients becauseof anatomical factors or poor medical condition, and al-

1 Neurological Surgery Department, Wayne State University, Detroit,Michigan.

2Radiation Oncology Department, Wayne State University, Detroit,Michigan.

3To whom correspondence should be addressed at Neurological Sur-gery Department, Harper Professional Building, Suite 930, 3990 JohnRoad, Wayne State University, Detroit, Michigan 48201; e-mail:zamorano@neurosurg.wayne.edu

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ternative methods of treatment may be indicated (1, 2).The risk for the development of a new neurological def-icit after microsurgical resection can be high, especiallyif the AVM is located in areas of critical brain function.

Radiosurgery was first used to treat patients withAVMs in Sweden in the 1970s (3, 4). Radiosurgery isbelieved to result in AVM obliteration via endothelialcell proliferation, progressive vessel wall thickening, andeventual luminal closure (5, 6). Arteriovenous malfor-mations can be safely and effectively treated withLINAC radiosurgery (7, 8), and with -y-knife radiosur-gery (9, 10). In the present study we discuss our expe-rience in the radiosurgical treatment of AVMs.

MATERIAL AND METHODS

From September 1991 to May 1997, 59 patientswith angiographically visible AVMs underwent radio-

1096-4053/98/0900-0225$15.00/0 O 1998 Plenum Publishing Corporation

KEY WORDS: Arteriovenous malformation; y knife; LINAC; radiosurgery.

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Table II.

Location

TemporalBasal ganglionicFrontalParietalThalamicCerebellarIntraventricularBrain stemOccipitalCorpus callosal

Locations of the Lesions

Cases

Number

14886655331

%

23.713.613.610.210.28.58.55.15.11.7

surgical procedures to treat their lesions. Of the 59 pa-tients, 39 were treated using a LINAC-based system(group 1) and 20 using the Leksell r-knife unit "201-

Fig. 1. Contrast-enhanced axial CT scan of a patient with thalamic AVM treated with LINAC-based radiosurgery showingplan of the treatment.

Table I. Clinical Characteristics of the Patients

Factor

SexFemaleMale

Presenting symptomsSeizuresHemorrhageHeadacheNeurological deficits

Spetzler-Martin gradeGrade IGrade IIGrade IIIGrade IVGrade VI

Prior treatmentSubtotal resectionEmbolization

Cases

Number

3029

2120144

1291883

37

%

50.849.2

35.633.923.7

6.8

1.749.230.513.65.1

5.111.9

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source Cobalt-60" (group 2). Twenty-nine patients weremen and 30 were women. Ages ranged from 5 to 75years (mean 36). Most patients were considered unsuit-able for microsurgical excision because of perceived un-acceptable risks for the development of new neurologicaldeficits.

The clinical characteristics of the patients areshown in Table I. The presenting symptoms were as fol-lows: 21 patients had seizures, 20 had intracranial hem-orrhages, 14 had headaches, and 4 had neurologicaldeficits. The Spetzler and Martin grading system wasused to classify all AVMs according to size, critical lo-cation, and venous drainage pattern. In our study, onlyone patient had an AVM that was grade I. The mostcommon grade was grade II, with 29 patients. Eighteenpatients had AVMs that were grade III, and 8 patientshad AVMs that were grade IV. Three patients hadAVMs classified as inoperable (grade VI), all of themwere brain stem AVMs. No patient with a grade V AVMwas treated with radiosurgery in this series.

The locations of the lesions are listed in Table II.There were 14 temporal, 8 basal ganglionic, 8 frontal, 6

parietal, 6 thalamic, 5 intraventricular, 5 cerebellar, 3brain stem, 3 occipital, and 1 corpus callosal. Seven pa-tients underwent prior embolization and three patientshad prior surgery with incomplete resection of their le-sions.

Radiosurgical Techniques

Group 1 consisted of patients treated with theLINAC-based system. All patients in this group under-went contrast-enhanced computed tomographic (CT)imaging scans and cerebral angiography under stereo-tactic conditions using the Zamorano-Dujovny (FischerLeibinger, Freiburg, Germany) stereotactic frame as thelocalizing unit. Images derived from CT were then trans-ferred via network and registered for radiosurgical plan-ning. The patient was then transferred with the headframe in place to the LJNAC holding zone waiting forthe treatment after the planning. The radiosurgical plan-ning was performed using the STP 3.0 software devel-oped by Fischer Leibinger. A variety of techniques,

Fig. 2. MRI of left thalamic AVM treated with -y-knife unit showing treatment plan.

Zamorano et al.

Fig. 3. Angiogram of a patient with deep frontoparietal AVM treated with r-knife unit. (A) pretreatment anteroposte-rior; (B) pretreatment lateral; (C) anteroposterior 1 year after treatment; (D) lateral 1 year after treatment.

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Radiosurgery for AVMS

Fig. 3. Continued.

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230 Zamorano et al.

including arc weighting, different collimator sizes fordifferent arcs, and multiple isocenters, were used to gen-erate a treatment isodose line that conformed to the nidusof the AVM (Fig. 1). After the optimum dose plan hadbeen developed the patient was then transferred to theLINAC unit and attached to the gantry and treated.

Group 2 consisted of patients treated with the Lek-sell -y-knife unit. All patients in this group had applicationof the Leksell Model G stereotactic coordinate frame andunderwent magnetic resonance imaging (MRI) scans andcerebral angiography. After transferring the images viathe network, the treatment isodose, central dose, and doseto the margin were determined using LGP 4.0 softwareaccompanying the Leksel r-knife unit (Fig. 2). The pa-tient was attached to the r-knife device after the coordi-nates of the stereotactic frame had been set.

The mean radiation dose to the periphery of thelesions of both groups was 1800 cGy (range 1500-2000cGy). This treatment dose was almost always deliveredto the 80% isodose line (range 70-90%) in group 1 andto the 50% isodose line in group 2. In both groups thevolume of the nidus ranged from 0.38 to 35 cc (mean4.7), the volume was defined by correlating the differentimaging modalities. The number of the isocenters variedfrom 1 to 3 in group 1 and from 2 to 15 in group 2.Twelve patients had concomitant embolization done onthe morning of the radiosurgery. Patients were usuallydischarged from the hospital on the day after treatment.

Follow-up

Duration of follow-up of the entire AVM groupranged between 1 month and 4 years. Follow-up studyconsisted of clinical examination and gadolinium-en-hanced MR imaging every 3 months after treatment.Once there were no flow-void signals on the MRI, ahigh-resolution angiogram was requested.

RESULTS

Thirty-six patients have been followed for morethan 1 year after treatment; 30 of them have been fol-lowed for more than 2 years after treatment. Four pa-tients suffered intracranial bleeding within the first 6months after the procedure and before the completeobliteration of the AVM. Of these patients, one died,one was treated surgically and the malformation was ex-cised, and the last two were treated medically. Fifteenpatients of the 21 patients with seizures before radiosur-gery were evaluated from 1 to 3 years after treatment.Of these, 11 had improvement of their seizure condition,

denned by the decreased frequency of fits and decreasedanitepileptic drug dose, and 4 had no change in theirseizures. Chronic headaches were evaluated during thefollow-up period in 10 patients of the 14 who had head-aches before radiosurgery. Seven had improvement and3 had no change. Five patients of the 36 patients whohave been followed for more than 1 year developed tran-sient clinical symptomatology consistent with radione-crosis, demonstrated by MRI. All of them improved aftershort courses of steroids.

Assessment of AVM Obliteration

Complete obliteration was defined as the absenceof any angiographically visible AVM. Among the 36patients who have been followed for more than 1 year,30 had an angiography in their follow-up, which showedcomplete obliteration of the lesion in 28. The rate ofobliteration of the overall group of AVM was estimatedto be 47.05% at 1 year, 82.35% at 2 years, and 88.23%at 3 years (Fig. 3). From the -y-knife-treated group, onepatient had complete obliteration of the lesion in 11months of follow-up; his MRI showed no flow-void sig-nal and the angiogram confirmed the obliteration. Therewere flow-void signals in the MRI of one of the patients3 years after treatment in even though her angiogramshowed obliteration of her AVM at that time.

DISCUSSION

Complete obliteration of an AVM was defined byLindquist and Steiner (11) as an angiographic appear-ance with "normal circulation time, complete absenceof pathological vessels in the former nidus of the mal-formation, and the disappearance or normalization ofdraining veins from the area." Steinberg (12) definedobliteration as "the absence of any angiographically vis-ible arteriovenous shunt." The total obliteration rate var-ied from one series to another. For patients treated withLINAC radiosurgery, Colombo reported a 52% 1-yearthrombosis, and 75% 2-year thrombosis using dosesranging from 18.7 to 40 Gy (13). Loeffler and colleagues(14) reported the treatment of AVMs with a LINAC sys-tem using doses ranging from 15 to 25 Gy, and theirtotal obliteration rate was 45% 1 year and 73% 2 yearsafter treatment. Friedman reported an overall angio-graphic cure rate of 80% 3 years after treatment withdoses ranging from 1000 to 2500 cGy (8). In their re-ports on r-knife radiosurgery for AVMs, Steiner andcolleagues (3, 15) reported 1-year occlusion rates rang-ing from 33.7 to 39.5% and 2-year occlusion rates rang-

Radiosurgery for AVMS 231

ing from 79 to 86.5%. The majority of their patientsreceived at least 20 to 25 cGy. Yamamoto reported thatthe 2-year complete thrombosis rate was 64% and the3-year thrombosis rate was 73% (16). In our study thetotal obliteration rate was 47.05% at 1 year, 82.35% at2 years, and 88.23% at 3 years after treatment.

Multiple series reported that the hemorrhage ratefor AVMs treated but not yet obliterated with radiosur-gery is the same as if they had not been treated (3, 4,17). In this study, 4 patients suffered intracranial bleed-ing within the first 6 months after the procedure andbefore the complete obliteration of the AVM. Delayedradiation-induced complications have been reported byall groups performing radiosurgery. The percentage ofsymptomatic radiation necrosis in different reports var-ied from 2 to 9% and increased with larger doses (3, 10,14, 15). In our study, 5 patients developed transient clin-ical symptoms consistent with radionecrosis, demon-strated by MRI, all of which improved after shortcourses of steroids. There were no permanent neurolog-ical deficits due to radiation.

CONCLUSIONS

Stereotactic radiosurgery is an important method toobliterate AVMs, especially those previously consideredinoperable. The results we obtained in our study supportthe usefulness of the radiosurgical approach in the man-agement of selected patients with AVMs. The AVM vol-ume, as such, was not an exclusionary factor fromradiosurgical management. The practice of AVM radio-surgery has evolved as experience with the technique hasgrown. Radiosurgery should be considered an acceptabletreatment for selected patients with AVMs of the brain,including some of those who were thought to have beenunsuitable for treatment a few years ago.

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