Menoufia Medical Journal

: 2020  |  Volume : 33  |  Issue : 4  |  Page : 1405--1409

Endovascular management of ruptured cerebral arteriovenous malformations in pediatric patients

Mohamed S.M. Elsanafiry1, Esam E. G. Saleh1, Magdy A. E. A. El-Mahalawy2, Hosam Eldin A. Habib1, Mohamed A Eltabl1,  
1 Department of Neurosurgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neurosurgery, Faculty of Medicine, Tanta University, Tanta, Egypt

Correspondence Address:
Mohamed S.M. Elsanafiry
21 Alnozha Street, Birket Elsaba, Menoufia


Objective To evaluate the efficacy, safety, and outcome of endovascular therapy (EVT) of ruptured cerebral arteriovenous malformation (c-AVM) in pediatric patients. Background Children with c-AVM have a higher annual risk of hemorrhage than adults (2–4 vs. 1–3% per year). Hemorrhage is fatal in ~25% of these children. Complete obliteration is most commonly achieved by multimodal therapy, which includes microsurgery, EVT, and stereotactic radiosurgery or a combination of two or more of these techniques. Patients and methods A prospective study included 18 patients (eight male and 10 female), with a mean age of 10.7 years (4–17 years). All had supratentorial c-AVMs, and none had a family history. According to the Spetzler–Martin grading system, two patients had grade I AVMs, six patients had grade II AVMs, eight patients had grade III AVMs, and two patients had grade IV AVMs. EVT was selected as the primary modality of treatment. Results A total of 10 patients had complete obliteration of the nidus, four patients had near-total obliteration, and four patients had incomplete obliteration requiring further treatment. After EVT, 10 patients had grade 0 in the Modified Rankin Scale, four patients had grade I, two patients had grade II, one patient had grade III, and one patient had grade IV. Conclusion In this article, EVT was an effective and safe technique for the treatment of c-AVMs showing a high cure rate as a single treatment modality or as a preprocedural technique facilitating other forms of treatment and improving the outcome of the cases.

How to cite this article:
Elsanafiry MS, Saleh EE, El-Mahalawy MA, Habib HA, Eltabl MA. Endovascular management of ruptured cerebral arteriovenous malformations in pediatric patients.Menoufia Med J 2020;33:1405-1409

How to cite this URL:
Elsanafiry MS, Saleh EE, El-Mahalawy MA, Habib HA, Eltabl MA. Endovascular management of ruptured cerebral arteriovenous malformations in pediatric patients. Menoufia Med J [serial online] 2020 [cited 2021 May 12 ];33:1405-1409
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Full Text


Cerebral arteriovenous malformations (c-AVMs) represent abnormalities of vascular development with tangles of tortuous abnormal arteries and veins that permit single or multiple direct connections and high-flow shunting of the blood from the arteries to the veins without intervening capillary beds. These AVMs look like a ball of worms that contains conspicuous gliotic nonfunctional neural tissue and vascular or interstitial calcification[1].

Pediatrics with c-AVM are different from adults with c-AVM in many ways. These differences, along with the long potential life span of pediatric patients, alter the considerations given to treatment[2]. The nidus in pediatric populations has been noted to have a higher occurrence of linear, vein-based malformations in contrast to compact type in adults[3]. They have a higher annual risk of hemorrhage than adults (2–4 vs. 1–3% per year)[4],[5],[6]. The next most common presenting feature is seizures 30%, followed by headache 5–14%[7].

Pediatric AVMs are more likely to be in eloquent locations than in adults, particularly in the basal ganglia and thalamus, although this has not been the case in all series: others found AVMs to be more prevalent in the posterior fossa in children than in adults[8]. Mortality rate is reported to be higher in children than adults, possibly because AVMs are more prevalent in the basal ganglia, thalamus, or posterior fossa in children than in adults, and possibly because children present more frequently with hemorrhage[9].

The Spetzler and Martin Grading was established to grade c-AVMs according to their degree of surgical difficulty and the risk of surgical morbidity and mortality, composed of six grades, based on nidus size, venous drainage, and eloquence of the adjacent brain region[10].

Successful treatment of c-AVMs depends on diagnostic information obtained from imaging techniques. The Digital Subtraction Angiography techniques remain the gold standard for defining the arterial and venous anatomy[11].

The ultimate goal of c-AVM therapy is the complete obliteration of the lesion because any residual c-AVM might result in hemorrhage, and partial treatment may increase the chances of bleeding. The treatment of c-AVMs is highly individualized. There is no universal algorithm or protocol to be followed when dealing with these unique and challenging lesions[12].

Complete obliteration is most commonly achieved by multimodal therapy that includes microsurgery, endovascular therapy (EVT), and stereotactic radiosurgery (SRS) or a combination of two or more of these techniques, and conservative treatment in some difficult cases[13].

The role of endovascular management can be summarized in five scenarios: one is preoperative, where embolization acts as a precursor to complete curative surgical resection; another is preradiosurgery; the third is targeted therapy where embolization is used to eradicate a specific bleeding source; the fourth is curative embolization where it is used alone for an attempted cure; and the fifth is palliative where it is used to palliate symptoms attributed to shunting[14].

The aim of the work was to evaluate the efficacy, safety, and outcome of endovascular management of ruptured c-AVM in pediatric patients.

 Patients and Methods

From March 3/2016 to 2/2018, a prospective study included 18 patients who presented with ruptured c-AVM under the age of 18 years old, admitted to Neurosurgery Department, Faculty of Medicine, Menoufia and Tanta University Hospitals. An approval from the Ethics Committee of the Faculty of Medicine, Menoufia and Tanta Universities, was taken. Written consent was taken from every patient.

Patients received EVT as the primary modality of treatment. All had supratentorial c-AVMs. None of them had a family history of c-AVMs and were not associated with medical problems. All patient presentations were intracranial hemorrhage. The initial clinical grading was performed according to the Glasgow Coma Scale. Patients were also examined for the presence of any neurological deficit [Table 1]. The motor power was assessed, and every muscle group was given a grade from 1 to 5.{Table 1}

Multislice computed tomography (CT) scan (Philips Medical Systems Technologies Ltd, Eindhoven, the Netherlands) with thin cuts, CT angiography, MRI (Toshiba Medical Systems Corporation, Tochigi, Japan), magnetic resonance angiography (MRA), and magnetic resonance venography (MRV) were very useful in the diagnosis of the type of c-AVM.

All patients in this study were investigated by kidney function tests (urea and creatinine), as well as prothrombin time and activity.

For all patients presented with hemorrhage, conservative management was the role till stabilization of the case, improvement of the conscious level, and resolution of the hematoma, which was followed up by serial CT scans. Immediate postinterventional CT brain was obtained in all patients. CT was done on the axial plane with coronal and sagittal reconstruction images of both the bone and soft windows to evaluate the embolization material cast.

Follow-up MRI/MRA and MRV brain were obtained after 3 months in all patients. Confirmatory Digital Subtraction Angiography was obtained in selected cases when there was any doubt in MRI/MRA and MRV findings. Clinical follow-up of patients was decided according to their condition. Patients with total obliteration and good recovery were instructed to attend the outpatient clinic every 3 months. For patients with incomplete obliteration, earlier visits were arranged for the arrangement of further intervention procedures after 3 months.

Data management

Data were collected, tabulated, and statistically analyzed using an IBM personal computer with statistical package for the social sciences (SPSS), version 23 (2015; released by SPSS Inc., Chicago, Illinois, USA. IBM SPSS statistics for Windows, version 23.0; IBM Corp., Armonk, New York, USA), where the following statistics were applied. Descriptive statistics with quantitative data were presented in the form of mean, SD, and range. Qualitative data were presented in the form of numbers and percentages.


There were eight (44.4%) males and 10 (55.6%) females, aged 4–17 years (mean, 10.7 years). Pre-embolization angiographic assessment and grading according to Spetzler and Martin Grading were done [Table 2]. Of the 18 patients who underwent EVT for the c-AVM, angiographic outcome at the final control angiogram was evaluated. In the cured group, this was achieved in one session; most of them were small (<3 cm), most had the fistulous type of nidus, and most did not require additional forms of treatment. In the incompletely cured group, most c-AVMs were medium-sized or large lesions (3–6 cm or >6 cm), and most had plexiform nidus. In this group, three (16.7%) patients underwent SRS. Two of them had two sessions of embolization and one patient had one session, and one (5.6%) patient did surgery after one session of embolization [Table 2].{Table 2}

Modified Rankin Scale was used to follow-up on the patients treated by EVT [Table 3].{Table 3}

In our series, two (11.1%) patients had complications related to EVT in the form of arterial device-induced vasospasm, which was temporary and resolved without any sequelae after stopping the manipulation, catheter withdrawal, and infusion of the calcium-channel blocker nimodipine [Table 4]. Two (11.1%) patients had temporary neurological deficits. One (5.6%) patient experienced paresthesia in one side of the body, which resolved after 1 day spontaneously. The other (5.6%) patient had hemiparesis and dysphasia as a result of hyperemia after embolization of a parietal c-AVM supplied by the Rolandic artery. These manifestations subsided after ~3 days, and motor power was regained. One (5.6%) patient had a neurological deficit in the form of hemiplegia as a result of postembolization hemorrhage. This deficit was explained by venous thrombosis, which caused breakthrough bleeding. The patient was managed conservatively and the motor power improved to grade IV. Distal perforation by the microwire occurred in one (5.6%) patient and was immediately managed by Onyx deposition (Onyx Aneurysm System, Toledo Way, CA, USA, ONYX HD-500 Model 105-8101-500) at the perforation site. No complication resulted from the perforation [Figure 1].{Table 4}{Figure 1}

Of 18 patients, two (11.1%) patients had hemiparesis as a complication of Intracerebral hemorrhage (ICH). No ICH-related mortality was recorded. Of 18 patients, one (5.6%) had hemiparesis as a complication of EVT. No technique-related mortality was recorded.

Four (22.2%) patients in the study required two sessions, and this was arranged after 3 months. Two (11.1%) patients were in near-total obliteration group and arranged for follow-up after the second session. The other two (11.1%) patients were in the incomplete obliteration group and received SRS after the second session.


Embolization of c-AVMs has taken a large step forward in the past decade. The introduction of the new nonadhesive polymer ethylene vinyl alcohol has largely replaced the use of acrylic glue for the obliteration of the nidus in many centers. Moreover, the use of the detachable tip microcatheter has made the procedure easier and safer.

With growing experience, advanced biplane imaging with rapid subtraction fluoroscopy, and refinements of technique in the use of ethylene vinyl alcohol, small and intermediate-size c-AVMs can be completely obliterated at a low complication rate.

In this study of 18 patients with c-AVMs, EVT resulted in a satisfactory degree of obliteration in most c-AVMs. A total of 10 (55.6%) patients showed complete obliteration, four (22.2%) patients showed near-total obliteration with only remaining perinidal angiogenesis, and four (22.2%) patients showed incomplete obliteration. Regarding the number of embolization sessions, complete obliteration was achieved in one session in all patients (55.6%).

This goes with Valavanis et al.[15] who reported 40% cure rate in a series of 644 patients by EVT alone as defined by complete embolization of the c-AVM nidus and 71% cure rate by a combination of embolization and other treatment modalities including radical microneurosurgical removal and radiosurgical obliteration of the remaining c-AVM.

The lower cure rate was achieved by Weber et al.[16] who reported 20% complete obliteration rate in a series of 93 patients and 53% cure rate by embolization and surgery. Maimon et al.[17] reported 37% complete occlusion rate in a series of 43 patients.

Amytal and temporary occlusion tests for prediction of neurologic dysfunction were not performed in our series. Instead, the benefit of this test was achieved by using MRI, superselective angiography, and thorough knowledge of the neurovascular anatomy. Such tests cannot replace the major importance of such knowledge in dealing with neurovascular anomalies.

In our series, the smaller c-AVM size was associated with better angiographic outcome. Overall, 10 (55.6%) patients with a small c-AVMs (<3 cm) were cured by embolization alone. Of eight (44.4%) patients with medium-sized or large c-AVMs, four (22.2%) patients only were cured by embolization alone.

This goes with Weber et al.[16] who reported high occlusion rates with micro c-AVMs (eight out 13 patients). Moreover, Wikholm et al.[18] reported success as heavily dependent on the size of the c-AVM nidus, with complete obliteration rates of 71% with c-AVMs smaller than 4 ml and only 15% with c-AVMs ranging from 4 to 8 ml.

In contrast to these results, Weber and colleagues reported high occlusion rates when the c-AVM is cortical in location, the nidus is compact and plexiform, and when the c-AVM has a small number of supplying feeders and one superficial draining vein.

Valavanis et al.[15] did not find that c-AVM volume significantly predicted the potential for endovascular cure. Rather, they had a 74% rate of curative embolization in a subgroup of patients with favorable angiographic features such as one or few dominant feeding arteries, no perinidal angiogenesis, and a fistulous nidus.

In our series, of six (33.3%) patients requiring further postembolization treatment, three (16.7%) patients did SRS, one (5.6%) patients did surgery, and two (11.1%) patient was scheduled for further embolization sessions.

This goes with Weber et al.[16] who reported SRS as a complementary form of treatment in eight (34.7%) patients and surgery in two (0.8%) patients. In contrast, Valavanis et al.[15] reported cure in 23% of patients by embolization followed by surgery and 8% by embolization followed by radiosurgical obliteration of the remaining nidus.

In our series, we encountered six (33.3%) complications related to the EVT, all of which resulted in no permanent disability except in one (5.6%).

Valavanis et al.[15] reported 1.5% permanent neurological morbidity rate with embolization alone and 2.8% morbidity in the total cure group.

Weber et al.[16] reported 6% device-related complication rate, including stuck catheters and distal perforation and 12% embolization-related complication rate including acute intracranial hemorrhage.

Maimon et al.[17] reported six technical complications (7–8% per procedure) including distal perforation, unintended microcatheter disconnection, and guidewire breakage in distal tortuous vessels. All events resulted in no permanent disability except in one (0.2%) patient who experienced a mild sensory deficit.

In our series, no ICH-related and no technique-related mortality was recorded. Weber et al.[16] reported the death of one (0.8%) patient from the uncontrollable rise in intracranial pressure after surgical evacuation of frontal hematoma after complete embolization of micro-AVM. The zero mortality rates in our series may be attributed to a small sample of the series in contrast to other series.

In our series, no new episodes of hemorrhage were reported during the follow-up period. Maimon and colleagues reported bleeding in one (0.2%) female patient during the follow-up period. She had a large c-AVM (Spetzler–Martin grade IV) with intraventricular bleeding and underwent embolization followed by radiosurgery. She was scheduled for surgery to remove the remnant, which was the source of rebleeding[15].


In this article, EVT was an effective and safe technique for the treatment of c-AVMs showing a high cure rate either as a single treatment modality or as a preprocedural technique facilitating other forms of treatment and improving the outcome of the cases.

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Conflicts of interest

There are no conflicts of interest.


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