Interactive Article Part 2


Embolization of Cerebral Arteriovenous Malformations: Part II­­Aspects of Complications and Late Outcome

Christer Lundqvist, M.D., Ph.D., Gunnar Wikholm, M.D., Ph.D., Paul Svendsen, M.D., Ph.D.

Departments of Neurology (CL) and Interventional Radiology (GW, PS), Sahlgrenska University Hospital, Göteborg, Sweden

OBJECTIVE: From 1987 through 1993, we performed embolizations on 150 patients with cerebral arteriovenous malformations (AVMs) at Sahlgrenska University Hospital. The patients ranged in age from 5 to 70 years (35.5 ± 14.8 yr, mean ± standard deviation) and were selected by neurosurgeons in Scandinavia. We analyzed the risk of complications and late outcome to have a better basis for the decision to perform embolization.
METHODS: The follow-up was a personal clinical examination of all surviving patients by a neurologist. Files for all patients were also studied.
RESULTS: In 34 patients, the AVMs were eliminated by embolization alone (20 patients) or by supplementary surgery (14 patients). In 66 patients, the AVMs were embolized to a size suitable for supplementary stereotactic radiation. The clinical course was stable for those 100 patients. Another group of 50 patients who had undergone embolization was only partially treated, and as a group, those patients had less favorable outcomes. The manifestations or symptoms leading to diagnosis were in concordance with other studies. Headache and epilepsy showed a positive response to treatment in patients whose AVMs had been eliminated as well as in those who received only partial treatment. A history of cerebral bleeding did not influence the prognosis of recurrent bleeding. Conversely, AVMs with feeder or nidus aneurysms were related to an increased risk of bleeding. If there was a history of bleeding in a patient with large, partially treated AVMs, the prognosis for survival was diminished.
CONCLUSION: The indication for treatment increases with the occurrence of AVMs with associated aneurysms. For patients with large AVMs, a history of bleeding justifies a more aggressive approach to treatment. The reduced risk of complications during the last years of the study also increases the indication for embolization.
(Neurosurgery 39:460­469, 1996)

Key words: Cerebral AVM, Complication, Efficacy studies, Embolization, Outcome

The prevalence of cerebral arteriovenous malformations (AVMs) is stated in various studies to be 0.06 to 0.14% (17, 19). The incidence has been estimated to be ~1 in 100,000 population. The natural course in patients with diagnosed AVMs is described by several authors (6, 7, 24). The annual risk of cerebral bleeding is considered to be on average 3 to 4% and the mortality ~1%. Traditionally, the treatment is surgical or radiotherapeutic intervention. During the 1980s, embolization of AVMs became an alternative therapy, alone or in combination with stereotactic radiation or surgery.

The goal in treatment of AVMs is primarily to eliminate the risk of cerebral bleeding; as far as is currently known, this can be achieved only by eliminating the AVMs. Irrespective of the method, there is a risk of complications, and it is important to determine this risk. With surgical intervention, the size and location of the AVMs are the most important prognostic factors (14). Stereotactic radiation therapy is thought to carry a low risk of complications but is an alternative only when the volume of the AVMs is <10 cc (27). Embolization of AVMs is associated with approximately the same incidence and level of complications as is surgical intervention (15). Lasjaunias et al. (22) reported that in a review of embolized AVMs with Spetzler-Martin Grades 1 through 3 (26), severe complications occurred in 5.2% and death in 2.0% of patients (1­3, 9, 10). In a study by Hurst et al. (16), endovascular treatment of deep central AVMs resulted in complications in 14.3% of patients.

The aims of this embolization study were as follows: 1) to describe the grade and frequency of complications; 2) to analyze the influence of embolization on bleeding incidents; 3) to examine the effect of treatment on headache, epilepsy, neurasthenic, and focal symptoms; and 4) to estimate late outcome for fully and partially treated patients (see Patients and Methods). With experience, this study will be supplemented by discussions of the indications for treatment of AVMs.


From 1987 through 1993, 150 patients underwent embolization for AVMs at Sahlgrenska University Hospital. Most patients were referred by neurosurgeons in Scandinavian hospitals and had AVMs that were regarded as unsuitable for surgical or stereotactic radiation treatment. During those years, an additional 34 patients with AVMs were rejected for the following reasons: 1) the AVM was considered impossible to embolize (10 patients), 2) the clinical gain was judged to be less than the risk of complications (6 patients), 3) the patient wanted to abandon furthe therapy after receiving information about the risk of complications (9 patients), or 4) the patient was recommended for other therapy (9 patients).

Of the patients who underwent embolization, 67 were male and 83 were female patients. They ranged in age from 5 to 70 years (35.5 ± 14.8 yr, mean ± standard deviation [SD]) at the time of embolization. They underwent 1 to 9 embolization procedures (2.2 ± 1.5, mean ± SD), with varying intervals from days to months. The AVMs were diagnosed 2.7 ± 4.4 years after the first symptoms. In most patients, the presenting events or symptoms that led to diagnosis were cerebral bleeding, epilepsy, and headache (Table 1).

We used the Spetzler-Martin scale, which classifies the AVMs by size, location, and type of venous drainage, to facilitate comparison with surgically treated patients (26). For example, Spetzler-Martin Grade 5 indicates an AVM with a diameter >6 cm that is localized to an eloquent area and drains into the deep venous system of the brain.

TABLE 1. Events or Symptoms from Arteriovenous Malformations Leading to Diagnosis
Events/Symptoms No. of Patients % of Patients
Hemorraghia cerebri 60 40.0
Epilepsy 55 36.7
Headache 13 8.7
Focal symptomsa 18 12.0
Pulse synchronous sound 1 0.7
Hiccup 1 0.7
Accident 2 1.3

aNo sign of cerebral bleeding.

Definitions of full and partial treatment of patients

Patients who received full treatment had AVMs that were eliminated by embolization or by supplementary elective or emergency surgery. We also included patients with embolized AVMs who had been accepted for stereotactic radiation by independent institutions.

Patients who underwent partial treatment had AVMs that after embolization still had arteriovenous shunting. This group was not scheduled for further treatment aimed at total obliteration of the AVMs.

Embolization technique

In 95% of patients, the embolization was performed by injection of N-butylcyanoacrylate (Histacryl Bleu; Melsungen AG, Melsungen, Germany) into the nidus of the AVM. The catheter used from 1987 through 1989 had a balloon with a calibrated leak, as described by Kerber (21). After 1989, a gradual change took place from a guidewire-guided microcatheter to a flow-guided microcatheter. Currently, all embolizations are performed with a flow-guided microcatheter (Magic; Balt, Montmorency, France).

N-Butylcyanoacrylate was used as the only embolic agent in 66.0% of our patients. It was used in combination with polyvinyl alcohol (PVA) in an additional 24.6% of patients. PVA alone was used in 5.3% of patients. In the remaining 4.1% of patients, N-butylcyanoacrylate or PVA was used in combination with polylene threads or Viñuela cocktail (a mixture of contrast medium, ethanol, Avitene [bovine collagen; Medchem Products Inc., Woburn, MA], and PVA).

Complications of embolization

We studied the neurological or neuropsychological complications that occurred during the first 4 weeks after the embolization procedure. However, transitory symptoms that occurred ¾3 weeks were excluded. The complications were graded according to the National Institutes of Health stroke scale (Table 2) (4). According to this scale, a slight complication corresponds to 0 to 1 point, a moderate complication to 2 to 5 points, and a severe complication to >5 points. In practice, a slight complication indicates a negligible influence on functional status, a moderate complication indicates a deterioration of functional status but usually no influence on lifestyle, and a severe complication indicates an influence on quality and conduct of life.

TABLE 2. National Institutes of Health Stroke Scalea
Indicator Result Score
1a. Level of consciousness Alert 0
Drowsy 1
Stuporous 2
Coma 3
1b. Level of consciousness, questions Answers both correctly 0
Answers one correctly 1
Incorrect 2
1c. Level of consciousness, commands Obeys both correctly 0
Obeys one correctly 1
Incorrect 2
2. Pupillary response Both reactive 0
One reactive 1
Neither reactive 2
3. Best gaze Normal 0
Partial gaze palsy 1
Forced deviation 2
4. Best visual No visual loss 0
Partial hemianopsia 1
Complete hemianopsia 2
5. Facial palsy Normal 0
Minor 1
Partial 2
Complete 3
6. Best motor, arm No drift 0
Drift 1
Can't resist gravity 2
No effort against gravity 3
7. Best motor, leg No drift 0
Drift 1
Can't resist gravity 2
No effort against gravity 3
8. Plantar reflex Normal 0
Equivocal 1
Extensor 2
Bilateral extensor 3
9. Limb ataxia Absent 0
Present in upper or lower 1
Present in both 2
10. Sensory Normal 0
Partial loss 1
Dense loss 2
11. Neglect No neglect 0
Partial neglect 1
Complete neglect 2
12. Dysarthria Normal articulation 0
Mild to moderate dysarthria 1
Near unintelligible or worse 2
13. Best language No aphasia 0
Mild to moderate aphasia 1
Severe aphasia 2
Mute 3
14. Change from previous exam Same S
Better B
Worse W
15. Change from baseline Same S
Better B
Worse W

aS, same; B, better; W, worse.

Late outcome

The outcome of the treatment was assessed by complete and standardized examination by a neurologist (C.L.) of all surviving patients, with two exceptions. One patient refused to participate in the follow-up, but good information was provided by his wife. Another patient who had moved abroad was described by her parents.

The time lapse from last embolization to the clinical examination for late outcome is called observation or follow-up time. To describe the outcome, we used the following scale, slightly modified after Heros et al. (15): Excellent, patient returned to previous lifestyle; Good, patient returned to previous lifestyle but with a minor deficit; Fair, because of a new deficit, patient could not return to previous lifestyle but could lead an independent life; Poor, because of a new deficit, patient is dependent on others for daily living; Death from embolization, death ¾4 weeks after the treatment session; Death from AVM event, death directly related to AVM >4 weeks after the treatment session; Death from other cause, non-AVM-related death. This closely follows the definitions used by Heros.

In addition, assessment of headache, epilepsy, and neurasthenic symptoms was conducted. Patients were asked this question at follow-up: Are the symptoms eliminated, or very much improved (--), somewhat improved (-), unchanged (±), somewhat worse (­), or very much worse (­­)?


Most of the cerebral AVMs in this study corresponded to Spetzler-Martin Grade 3 (46.7%), Grade 4 (28.7%), and Grade 5 (8.7%) (Fig. 1). The AVM volume was >4 cc in most patients (Fig. 1).

FIGURE 1. Spetzler-Martin gradings (top) and volumes (bottom) of embolized AVMs. Descriptive statistics of Spetzler-Martin gradings (Grades 1­5; 3.3 ± 0.9 [mean ± SD]) and volumes (range, 0.5­280 cc; 25.8 ± 32.1 cc [mean ± SD]).

Through embolization, we eliminated the AVMs in 20 patients and reduced the AVMs to a size suitable for combined treatment in 80 patients; the AVMs were simply reduced in 50 patients. Supplementary treatment using a gamma knife was performed on 64 patients, mostly at Karolinska Hospital; the linear accelerator was used on 2 patients and surgical treatment was undertaken in 14 patients (2 patients were treated in an emergency situation).

Consequently, 100 patients were fully treated and 50 patients were partially treated (Table 3), ranging in age from 5 to 70 years (35.5 ± 15.7 yr, mean ± SD) and 7 to 65 years (35.2 ± 13.1 yr, mean ± SD), respectively. The observation time was 0.1 to 7.3 years (2.9 ± 1.7 yr, mean ± SD) in all patients, 0.1 to 7.3 years (2.8 ± 1.8 yr, mean ± SD) in the fully treated group, and 0.4 to 6.9 years (3.1 ±1.7 yr, mean ± SD) in the partially treated (embolized) group.

There were 38 patients with centrally located AVMs. Half of the AVMs were fully embolized, and one of those was totally obliterated by embolization. The mean Spetzler-Martin grade for this group was 3.9, compared to 3.3 for the whole study.

TABLE 3. Treatment in 150 Patients with Arteriovenous Malformations
No. of Patients Age Range (yr), Mean ± SDa Ratio, Female:Male
Full treatment
Embolization 20 12­70, 38.9 ±20.4 9:11
Embolization + surgery 14 8­56, 34.9 ±14.9 12:2
Embolization + radiosurgery 66 5­68, 34.8 ±14.3 39:27
Partial treatment
Partial embolization 50 7­65, 35.2 ±13.1 23:27

aSD, standard deviation.


Two patients (1.3%) died as a result of embolization. Severe complications occurred in 10 patients (6.7%), moderate complications in 23 patients (15.3%), and slight complications in 26 patients (17.3%). The relation to full or partial treatment is shown in Table 4. There was only one slight complication noted in the group with Spetzler-Martin Grade 1; in the remaining grades, the frequency of complications was not related to size and location of AVMs. However, more complications tended to result from centrally located AVMs; 2 patients (5.3%) experienced severe complications, 12 patients (31.6%) experienced moderate complications, and 3 patients (7.9%) experienced slight complications. In addition, one of the two patients who died as a result of complications had centrally located AVMs.

TABLE 4. Complications after Full and Partial Treatmenta
No. of Patients (%) with
Total No. of Patients Slight Comp. Moderate Comp. Severe Comp. Deaths n (%)
Full treatment 100 16 (16) 16 (16) 6 (6) 0 (0)
Partial treatment 50 10 (20) 7 (14) 4 (8) 2 (4)

aSee Patients and Methods. Comp., complications. Slight complication, deficit with 0­1 point in National Institutes of Health scale (4); moderate complication, 2­5 points; severe complication, >5 points (4).

At assessment of outcome, 6 patients with severe complications had improved to the level of moderate complications and 12 patients had improved from the moderate to the slight level. No patient with complications deteriorated during the follow-up time. The consequences of severe and moderate complications are presented in terms of points on a status scale (Table 5).

TABLE 5. Neurological Deficit Measured as Scores from National Institutes of Health Scalea before Embolization, 3 Weeks after Complication, and at Follow-up (Late Outcome)
Complications Before Embolization After 3 Weeks Follow-up
Severe 1.6 ± 1.5b 11.9 ± 4.1 10.3 ± 4.8
Moderate 1.6± 1.7 4.7 ± 2.0 3.1 ± 1.6

aSee Table 2.
bValues are mean ± standard deviation.

Cerebral bleeding occurred within minutes after embolization in one patient and after 8 hours in another and resulted in death in both patients. The cause of the severe complications was hemorrhage in four patients and ischemia in six patients. The cause of the moderate complications was hemorrhage in 4 patients, suspected hemorrhage in 1 patient, and ischemia in 18 patients.

The neurological deficit and functional status of severe and moderate complications are presented in Table 6. At assessment of outcome, improvement was seen in all patients (one patient regained use of a hand, and four patients with severe complications had restored gait) (Table 5).

TABLE 6. Symptoms Caused by Moderate or Severe Complications of Embolization (Number of Patients)
Deficit of Complication Severe Moderate
Aphasia/dysphasia 2 + 2a 6 + 2a
Hemianopsia 0 + 1a 2
Memory impairment 4 + 1a 1 + 2a
Hemiparesis 6 + 4a 6 + 6a
Hemisensory 5 + 1a 4 + 3a
Coordination 1 0
Fine motor skills 4 7 + 6a
Useless hand 5 0 + 2a
Deteriorated gait 2 4 + 2a
Wheelchair bound 4 + 3a 0

aDeterioration of previous symptoms.

Risk of cerebral bleeding

A history of bleeding before embolization was given by 74 patients; 76 patients had no history of bleeding. The same distribution, 19 patients, respectively, was found in patients with centrally located AVMs. Twelve patients experienced cerebral bleeding during the observation time, 0.7 to 6.9 years (4.0 ± 2.0 yr, mean ± SD) from the last embolization to assessment of outcome (Table 7).

TABLE 7. History of Bleeding Incidents Related to Bleeding after Last Embolizationa
Bleeding before Embolization No Bleeding before Embolization
Fully treated (No. of patients) 52 48
Observation time (yr) 2.9 ± 1.6 2.7 ± 1.8
No. of patients with bleeding incident(s) 2 1
Time to incident (yr) 0.5 ± 0.4 1.0 ± 0.0
Partially treated (No. of patients) 22 28
Observation time (yr) 4.3 ± 1.8 2.9 ± 1.6
No. of patients with bleeding incident(s) 3 6
Time to incident (yr) 2.6 ± 2.9 3.0 ± 1.8

aObservation time (mean ± standard deviation [SD]), time lapse from last embolization to follow-up; time to the incident (mean ± SD), time lapse from last embolization to the incident of cerebral bleeding.

The three bleeding incidents in the fully treated patients occurred in one patient 5 months after embolization before planned radiotherapy, in a second patient 6 months after embolization from an aneurysm on a feeding artery before planned surgical clipping, and in a third patient before supplementary elective surgery.

The bleeding incidents in nine patients who received partial treatment (two with centrally located AVMs) occurred after a mean observation time of 4.2 years and were unrelated to the history of bleeding. The incidence exceeds that expected from the natural course (Fig. 2). Among the patients with centrally located AVMs, only one bleeding incident occurred during the follow-up period.

FIGURE 2. Survival free of hemorrhage after embolization for patients who received full (top) and partial (bottom) treatment.

Feeder or nidus aneurysms were seen in 43 patients before therapy. One of 19 patients with occluded aneurysms had one episode of cerebral bleeding during the observation time. In contrast, 7 of 22 patients with persistent aneurysms had bleeding incidents. Compared with patients without aneurysms after therapy, the risk of bleeding was significantly higher (P < 0.05).

Causes of death

Eleven of 150 patients died because of the following complications: 1) complications of embolization (2 patients); 2) cerebral bleeding as a consequence of supplementary planned surgery (1 patient); 3) cerebral bleeding ranging from 0.5 to 5.0 years (3.5 ± 1.9, mean ± SD) after embolization (6 patients, 2 of whom underwent surgical treatment 2 weeks after the bleeding incidents but died without regaining consciousness 1­2 mo later); 4) other causes (2 patients, 1 of whom died because of cancer, and 1 of whom had a long history of psychiatric illness and committed suicide). Four of the six patients who died as a result of spontaneous hemorrhage from the AVMs during the follow-up period had a history of cerebral bleeding, and one patient had centrally located AVMs.


Occurrence of headache, epilepsy, and neurasthenic symptoms, including disturbance of memory and concentration ability, and the influence of the treatment were analyzed (Table 8). We found a significant improvement with respect to headache and epilepsy in patients who received both full and partial embolizations. Focal symptoms of causes other than hemorrhage were present in 18 patients. Most had stationary symptoms or episodes of deterioration. Two patients had progressive symptoms. During the observation time, two patients died, six patients had regression of symptoms, seven patients were stationary, and three patients experienced progression of symptoms resulting from complications.

TABLE 8. Effect of Treatment on Symptoms and Comparison between Time before Embolization and at Follow-up (Late Outcome)a
No. of Patients ­­ (%) ­ (%) ± (%) + (%) ++ (%)
Fully treated
Headace 40 0 10 35 30 25
Epilepsy 46 0 13 52 28 7
Neurasthenic symptoms 26 4 34 54 8 0
Partially treated
Headache 25 0 12 20 40 28
Epilepsy 24 4 4 50 29 13
Neurasthenic symptoms 17 0 41 47 12 0

a++, very much improved; +, somewhat improved; ± , unchanged; ­, somewhat worse; ­­, very much worse.

Late outcome

The result of the treatment in terms of influence on lifestyle, dependence, and death is shown in Table 9. An excellent or good outcome was seen in 78% of patients who underwent full treatment and 70% of patients who underwent partial treatment. Death in relation to AVMs occurred in two patients (2%) who underwent full treatment and seven patients (14%) who were partially treated. The result of full and partial treatment related to Spetzler-Martin grades is shown in Tables 10 and 11.

TABLE 9. Late Outcome with Full (n = 100) and Partial (n = 50) Treatment
Late Outcomea Full Treatment, n (%) Partial Treatment, n (%)
Excellent 65 (65) 22 (44)
Good 13 (13) 13 (26)
Fair 15 (15) 6 (12)
Poor 3 (3)b 2 (4)
Death related to AVMsc 2 (2) 7 (14)
Complication of embolization 0 (0) 2 (4)
Complication of surgery 1 (1) 0 (0)
Spontaneous bleeding 1 (1) 5 (10)
Death from other causes 2 (2) 0 (0)

aModified Heros scale.
bComplication of surgery.
cAVM, arteriovenous malformation.

TABLE 10. Late Outcome in 100 Patients with Arteriovenous Malformations That Were Fully Treated Related to the Spetzler-Martin Scale: Distribution by Number of Patientsa
Outcome S-M 1 (n = 5) S-M 2 (n = 19) S-M 3 (n = 53) S-M 4 (n = 21) S-M 5 (n = 2)
Excellent 4 14 33 12 2
Good 1 2 7 3 0
Fair 0 0 9 6 0
Poor 0 1 2 0 0
Death related to AVMs 0 1 1b 0 0
Death from other causes 0 1 1 0 0

aS-M, Spetzler-Martin grades (26); AVMs, arteriovenous malformations.
bDeath from complication of treatment.

TABLE 11. Late Outcome in 50 Patients with Arteriovenous Malformations That Were Partially Treated Related to the Spetzler-Martin Scale: Distribution by Number of Patientsa
Outcome S-M 1 (n = 5) S-M 2 (n = 19) S-M 3 (n = 53) S-M 4 (n = 21) S-M 5 (n = 2)
Excellent 0 0 6 11 5
Good 0 0 6 5 2
Fair 0 0 1 4 1
Poor 0 0 1 1 0
Death related to AVMs 0 0 3b 1 3
Death from other causes 0 0 0 0 0

aS-M, Spetzler-Martin grades (26); AVMs, arteriovenous malformations.
bDeath from complication of embolization in two cases.

Of the patients with central AVMs, 28 patients (73.7%) had an excellent or good outcome, whereas 1 patient died of cerebral bleeding as a consequence of embolization and surgery, respectively, and 1 patient died of spontaneous bleeding 4 years after partial treatment.


The main question regarding what influence elimination or partial treatment of the AVMs has on the incidence of cerebral bleeding cannot be answered simply. However, no evidence was found in our study to contradict the finding of others that eliminated AVMs do not bleed. In patients who have undergone full treatment, many of the essential requirements for elimination with time were reached, in addition to those AVMs eliminated by embolization or supplementary surgery, but a risk of bleeding remained until late effects of stereotactic radiotherapy had eliminated the AVM.

The patients in our study seemed to have an unsatisfactory number of complications of embolization in comparison with similar studies (1). One reason could be the higher Spetzler-Martin profile in our study. In a similar study with surgical elimination of AVMs, the outcome was comparable to that in corresponding fully treated patients with AVMs in our study. Most of those patients were considered by neurosurgeons to be unsuitable for surgical treatment (15, 23).

In 14 patients with AVMs <4 cc in volume, we saw one complication with persistent symptoms, which turned out to be moderate at follow-up (see Part I of this study [29]), indicating a low risk comparable with the very low morbidity of stereotactic radiation of small AVMs of the brain (27). However, our study includes too few patients with small AVMs to express the risk factor as a percentage.

A comparison of complications between the patients who were embolized from 1987 through 1988 and 1992 through 1993 showed an apparent improvement (28). Of the latter group, comprising 27 patients, 11% had moderate complications and there were no severe complications or deaths. Improved technique and embolization material could explain this development, but a more likely explanation is uniform management of the whole embolization procedure, including intensive care, with measures to achieve continuous low blood pressure. In our experience, avoidance of blood pressure peaks during the embolization procedure and for days after probably reduces the risk of complications from bleeding. As expected, embolization of centrally located AVMs results in most complications (16), whereas AVMs of small size carry a low risk irrespective of the choice of therapy (15, 27).

Of our patients who underwent partial embolization and experienced bleeding during the follow-up time, most had no history of prior bleeding incidents (Table 7). In contrast, four of six patients who died as a consequence of spontaneous bleeding had a history of bleeding. For more reliable information, the follow-up time must be longer than in our study.

Small AVMs are considered to carry a higher risk of cerebral bleeding than larger ones, but we could not find such a relation in our study (18). This can probably be explained by the selection of patients. Small AVMs that present with hemorrhage are assumed to be overrepresented for surgical treatment (7).

Large AVMs, partially treated, account for the deviation from an expected natural risk of bleeding (Fig. 2). This implies a greatly increased risk in this subgroup, which is supported by Brown et al. (6) regarding risk of hemorrhage in nonruptured AVMs. Other studies do not confirm the association of large AVMs and risk of bleeding (13, 18). The implication is that partial embolization of AVMs with large volumes could increase the risk of bleeding. However, data from Karolinska Hospital show a decreased risk of bleeding before stereotactic radiation has eliminated the AVM, which supports the view that partial embolization is valuable (20). That the embolization was minimal in patients with spontaneous hemorrhage and a fatal outcome also supports this conclusion. In patients with centrally located AVMs, the late outcome did not deviate from that in the whole study, despite the increased frequency of moderate complications (Table 11). Others have also achieved good results by endovascular treatment of deep centrally located AVMs (16). Feeder and nidus aneurysms were shown to be predictors for cerebral bleeding, making it important to perform selective angiography before making a decision on treatment in patients with AVMs (5, 11).

The estimation of epilepsy and headache during the follow-up time is based on recollection by patients of their experience of intensity and frequency. Epilepsy occurred in nearly half of the patients studied. The influence of treatment is discussed in only a few studies and with diverging results (8, 25). This study indicates positive effects in both groups of patients (those who underwent full and partial embolizations). A more detailed analysis of the epilepsy related to embolization will be published later. Regarding headaches, an even clearer improvement was seen. Neuropsychological disturbances have been noted in only a few patients but can be an underrated consequence of treatment (12).

In summary, patients with AVMs in eloquent areas or whose lesions are too extensive to be cured by stereotactic radiosurgery now have the possibility of obtaining elimination of their AVMs by embolization alone or in combination with other therapies. The indications for therapy must be weighed against not only the estimated risk of cerebral bleeding but also the risk of complications of treatment. Selective angiography is a decisive factor because of the information it yields about the prognosis of the natural course. Aneurysms, which are not detectable by ordinary angiography, as well as venous stenoses, carry a documented increased risk (1). The decreased number of complications during the last years of the study also increases the indication for treatment (28). Another reason to completely embolize AVMs, even if only partial embolization is expected, is the level of clinical symptoms (30). In addition, improved embolization techniques and our experience provide reasons for a more aggressive approach to embolization; fewer patients would need to undergo partial embolizations, and more patients would have full embolizations.

Of 66 patients who were treated with a combination of embolization and stereotactic radiation, 44 received angiographic study at 2 years' follow-up. Angiograms showed elimination or near elimination (>90% reduction) of AVMs in 34 (78%) patients. Recanalization was not seen. To present the best treatment strategy, we must wait for more studies, including our current one, which is the second follow-up including angiographic results.

Received, October 25, 1995.
Accepted, March 20, 1996.
Reprint requests: Gunnar Wikholm, M.D., Department of Radiology, Section of Interventional Neuroradiology, Sahlgrenska University Hospital, S-413 14 Göteborg, Sweden.


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Lundqvist et al. present a critical review of their experience with 150 patients with cerebral arteriovenous malformations (AVMs). This two-part article is an ambitious retrospective analysis of the radiological and clinical data in embolization of relatively high-grade (Grades 3­5) AVMs with liquid adhesive and polyvinyl alcohol. The study reflects the world standard regarding the technique of embolization and includes both surgical and radiosurgical treatment as well as AVMs treated with embolization alone. This careful analysis of the cases presented to a single center provides important information regarding the efficacy of embolization in preventing hemorrhage from AVMs and further defines complication rates for embolization of high-grade AVMs.

One hundred and fifty patients met the inclusion criteria for the study, of which 84% were greater than Grade 3. Forty-four percent were referred for subsequent radiosurgery. The total procedural morbidity rate was ~40%, although most of the morbidity was minor with a 1.3% overall procedural mortality rate. However, over the course of the study period, six patients died as a result of AVM hemorrhages. Five might be expected for a cohort of 150 patients followed for 6 years, but if more than 5 patients died during the study period, it would imply that the natural history of this cohort was worsened by treatment or by the selection bias of inclusion criteria (i.e., high-grade or lesion angioarchitecture).

The division of the analysis into "completely treated" and "partially treated" lesions provides important data regarding the effect of embolization on the hemorrhage rate of AVMs. Patients considered to be "fully treated" (100 patients) included those with complete obliteration of the nidus by embolization alone (10%), as well as those with lesions reduced to a size suitable for radiosurgery. Three postprocedural hemorrhages occurred in this group while the patients were awaiting further therapy, which implies that there was no protective effect of embolization on hemorrhage rate. Of greater concern is the group of patients with "partially treated" lesions; there were nine hemorrhages after treatment in the follow-up period of 4.2 years, which exceeds the expected natural history. This observation raises the serious question of whether these patients should be treated by embolization alone. Smaller AVMs are not more benign.

Scott C. Standard
L. Nelson Hopkins

Buffalo, New York

Lundqvist et al. report anatomic and long-term clinical outcome in 150 patients with brain AVMs treated either with embolization alone, embolization and stereotactic radiosurgery, or embolization and then surgical removal of the residual AVM nidus.

They used standard techniques of intracranial navigation with either flow-guided or over-the-guidewire microcatheters, and acrylics were used as embolic material in >90% of patients. The authors report a consistent decrease in technical complications when comparing their early versus later clinical results, which was probably related to important improvements in the quality of microcatheters, better technical control of embolic materials and delivery systems, and better clinical judgment. The reasons for the technical/clinical complications are similar to those reported in the literature.

Most of the AVMs were in Grades 3, 4, and 5 of the Spetzler-Martin classification, and 66 of 150 patients (44%) underwent postembolization stereotactic radiosurgery. This embolization/stereotactic therapeutic strategy has been pragmatically incorporated in numerous neurointerventional institutions around the world. The interventional neuroradiologist attempts to reduce the size of the AVM nidus and/or occlude high-flow arteriovenous fistulas and intranidal aneurysms. These preliminary long-term anatomic and clinical results reported by Lundqvist et al. in 60 patients is reassuring; this strategic modality might play a positive role in a special population of nonsurgical AVMs.

The authors also report that, based on the long-term clinical outcome, partial embolization and then by full treatment of AVMs has a positive affect on the natural history of the residual AVM nidus (fewer hemorrhagic complications and improvement in the medical therapy of headaches and epilepsy).

The authors show a unique and genuine effort to compare the clinical presentation, anatomic results, and long-term clinical outcomes of patients, objectively collected by a neurologist. One may or may not agree with their conclusions, but the data will be valuable to engender further critical discussions.

Fernando Viñuela
Interventional Neuroradiologist
Los Angeles, California

Wikholm, Lundqvist, and Svendsen are well-known individuals in the field of interventional neuroradiology and endovascular neurosurgery. I have followed their work for over 20 years. The senior author, Svendsen, has always been a highly reliable and honest individual who follows his patients carefully. Therefore, this information is of great assistance in understanding the role of embolization in the overall management of cerebral arteriovenous malformations. For the most part, the results, degree of occlusion, type of complications, and outcome are similar to others as reported. The authors' excellent ability to follow patients gives us some insight as to the efficacy of this treatment. The authors' persistence and honesty, as well as their ability to have the material reviewed by independent neurologists helps us all in the treatment of AVMs. Important concepts are mentioned in this article that are compatible with those reported in our series (1). We also concur with the authors' analysis of the angioarchitecture and correlation with hemorrhage. Patients in whom they were able to close the intranidal, or pedicle, aneurysm were protected against hemorrhage. However, seven patients in whom they did not achieve this goal developed hemorrhages; two of the patients died. This again is compatible with our experience. Also compatible with our experience are those patients in whom hemorrhage occurred after embolization. The outcome in this group, which may be caused by a very select group of patients with very difficult malformations, seems to be worse than the outcome after spontaneous hemorrhage. We also concur with the authors that the location of the malformation is less critical from an endovascular point of view than it is from a surgical point of view. Endovascular treatment aims to close the abnormality and preserve all normal arteries in the vicinity, regardless of location in an "eloquent" or "noneloquent" area. Therefore, location as a risk factor seems to be less critical for endovascular embolization. We also concur with the authors that the preliminary angiogram, showing the size of the malformation and presence of perforators as part of the supply to the malformation, will predict success for endovascular treatment.

The authors seem to have a higher complication rate than the rates reported in other series, but it is probably related to their more honest and more thorough analysis and neurological examination. The complications of all interventional neuroradiological procedures in large series such as this one may get lost in view of the fact that these series are comprehensive and are conducted over a long period of time (7 yr). In the last several years, the use of nonballoon-tipped catheters and flow-guided catheters has markedly decreased the complication rate because vessel perforation and rupture are related to trauma from balloons or guidewires. On the other hand, microcatheter gluing has also decreased because of the decreased concentration of NBCA in the mixture. Therefore, longer injections are now possible and bonding of the glue to the microcatheter and vessel wall has also been markedly decreased. This group of investigators also follows several of our concepts; anatomic guidelines are the most important predictors of potential hazards and neurological complications, reaching the nidus and preserving all normal vessels decreases the risk, and sodium amytal was not used as a "provocative" test and the outcome was very good. Therefore, the use of sodium amytal as an excuse for poor technique, lack of superselectivity, or lack of knowledge of anatomy is clearly established in this group of patients. We also concur that the Spetzler-Martin classification is a surgical description of surgical skills and does not correlate with endovascular treatment. We do concur with the authors that we use this classification for the sake of comparison, because it is frequently requested by interventional neuroradiologists. Again, we do concur that this does not correlate with the difficulty of managing patients from an endovascular point of view. Furthermore, no matter how effective the embolization, we can only try to affect the "size" of the remaining malformations. However, no interventional procedure can change the location of the malformations, venous drainage, or, in reality, size. Therefore, the Spetzler-Martin classification is difficult to change with endovascular procedures. We also concur with the statement that in those patients in whom cure is not possible by either embolization or a combination of techniques, the aim of the embolization is a targeted approach in an attempt to close the "weakness" of the angioarchitecture of the malformation, such as intranidal aneurysms or aneurysms in the pedicle, or to reduce the pressure in the veins that have an outflow restriction (1). We agree with the technique of embolization and, for the most part, use the same approach. Based on the experience of the authors as well as ours, embolization may play a role even in small malformations that are suitable for radiosurgery to reduce the weakness of the angioarchitecture and hopefully afford protection during the latency period of the radiosurgery and to further reduce the volume (the smaller the volume, the more effective the radiosurgery).

Overall, this article is very important for the understanding of the long-term efficacy of this intervention. For the authors' benefit, the techniques available currently for intranidal embolization (Moret J, personal communication) are far superior to those available at the beginning of the study; the future outcome should be further improved because of these technical advancements. The authors also clarify the long-standing controversy concerning the use of liquid adhesive versus particles, confirming our own experience that particles are less effective and carry similar risks.

Alex Berenstein
Interventional Neuroradiologist
New York, New York

  1. Berenstein A, Lasjaunias P: Classification of brain arteriovenous malformations: Angioarchitecture, in Surgical Neuroangiography. Heidelberg, Springer-Verlag, 1993, vol 4.

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