Introduction: Arteriovenous malformations (AVMs) are the commonest cause of hemorrhagic stroke in children. Endovascular embolization is a feasible treatment modality, but cure rates are heterogenous from one series to another. We aimed to describe the immediate obliteration rates and periprocedural complications of embolization of pediatric AVMs. Methods: Between 2011 and 2019, participants below 18 years of age with AVMs treated by the same neurosurgeon at a single center were included. The clinical features, immediate angiographic results, and periprocedural complications were retrospectively collected from the clinical records. Results: Thirty-four embolization sessions were performed on 20 children (12 females with a mean age of 13). Intracranial hemorrhage was the most common presentation (75%), and the majority were frontal (30%) and basal ganglia (30%) lesions. An immediate complete angiographic obliteration was achieved in 9 patients (45%) with low-grade lesions (Spetzler-Martin grade I and II). NBCA was the most common embolic agent used (52.9%). Complications were reported in 3 (8.8%) out of 34 sessions. Two of them were intraoperative perforations with clinical consequences. A slight cortical hemorrhage during the procedure was observed in 1 patient without clinical repercussions. Discussion: This single-surgeon single-center experience suggests that endovascular treatment is a safe and efficient treatment for pediatric AVMs. Pediatric prognostic scores for a suitable selection of candidates are needed. Further studies are required to validate these results.

Arteriovenous malformations (AVMs) are structural vascular alterations, which consist of dysplastic vessels that comprise a nidus fed by the arteries with venous drainage, without capillary interaction in between [1, 2]. It is thought that its origin occurs in the embryonic stage, especially in the pediatric age, although cases of de novo AVMs have been described [3, 4].

Although there is no pharmacological treatment for AVMs, there are other therapeutic options, such as endovascular treatment, microsurgery, or radiosurgery, which can be performed alone or in combination [2, 5]. It has been stipulated that endovascular embolization prior to radiosurgery has shown lower obliteration rate [6]. Moreover, in certain cases, embolization can be performed as a modality with intent to cure [7, 8]. In pediatric AVMs, endovascular embolization shows the capability of complete obliteration in small lesions or as an effective adjunctive therapy in larger AVMs [9]. However, rates of complete occlusion are heterogeneous from one series to another [10-12].

Embolization with intent to cure has been considered an option with higher complication rates compared with adjunctive embolization [13]; however, this has not been firmly established in the pediatric population. Then, we aimed to report a single-center experience regarding the immediate obliteration rates and periprocedural complications of embolizing treatment of AVMs in pediatric patients.

Patients Selection

We retrospectively reviewed the clinical records and imaging studies of 20 pediatric patients with a diagnosis of AVM who underwent an embolization procedure with intent to cure (immediate complete occlusion) between January 2011 and December 2019. All the patients included were below 18 years old and were only treated by a single endovascular neurosurgeon (R.V.T.) in all of the sessions. The study was performed at a single institution that only performs endovascular treatment; therefore, all the patients presenting an AVM were evaluated for endovascular embolization.

The data for this study were obtained after approval from the institutional review board. The demographics, clinical and radiological features, immediate obliterations rates, and the complications were evaluated. For all the patients, the obliteration outcome was obtained from the immediate post procedure angiogram of the final embolization session.

Embolization Technique

The procedure was performed under general anesthesia and without systemic heparin. Continuous pressurized irrigation through saline solutions with 1,500 UI of heparin were maintained during the procedure. Between January 2011 and January 2016, the procedures were performed in a C-arm Philips BV Pulsera (Philips, the Netherlands). From January 2016 to the present, the embolization sessions were performed in a biplane angiogram Philips Allura Xper FD20/10 (Philips). The femoral approach was used in all the cases, and a 5F or 6F guide catheter was used depending on the patients’ age and size. Transvenous approach was not used in this subgroup of patients due to the lack of experience of the operator using this technique. The navigation into the artery of interest was done without complications. Once in the selected feeder of the AVM and under road mapping, the microcatheter (nondetachable tip and detachable tip) was navigated over a 0.007-inch microguidewire as close as possible to the AVM nidus in order to inject the embolic material. The type of microcatheters employed depended on the embolic agent used: Magic (Balt, Montmorency, France), Marathon (ev3, Neurovascular, CA, USA), Headway Duo (Microvention, CA, USA), and Sonic (Balt). The embolic agents used were NBCA, Onyx (ev3, Neurovascular, CA, USA), Squid 18 (Balt), and a precipitating hydrophobic injectable liquid (PHIL; Microvention). Once in the AVM nidus, the injection was performed manually in a continuous fashion with control of the reflux into the selected feeder. The procedure finished when the reflux was maximal, the penetration into the nidus was optimal, the foot of the vein was obliterated, and when an adequate cast of the embolic agent was made. An immediate control angiogram was conducted to determine the total or partial obliteration of the AVM. Finally, the microcatheter was withdrawn and manual compression of the femoral artery was done.

Twenty patients were treated with 34 embolization sessions (1.7 embolizations per patient). There were 12 (60%) females and 8 (40%) males with a mean age of 13, a median of 14, and a range of 6–17. Detailed data of the 20 patients are shown in Table 1.

Table 1.

Summary of patients with AVM treated with embolization

Summary of patients with AVM treated with embolization
Summary of patients with AVM treated with embolization

Clinical Presentation

The most common clinical presentation was intracranial hemorrhage in 15 (75%) patients. In the hemorrhagic presentation group, the associated symptoms were headache in 9 patients, focal neurological deficit in 6 patients (motor: 3 and sensitive: 3), and seizures in 4 patients. In the nonhemorrhagic presentation group, headache was present in 3 patients, and seizures were present in 2.

Imaging Findings

Prior to the embolization, all the 20 AVMs were confirmed by an angiography. The locations were the frontal lobe in 6 (30%) patients, the basal ganglia and thalamus in other 6 (30%) patients, and the parietal lobe in 4 (20%) of them. The remaining 4 patient’s AVMs were located in the insular region, the cerebellar hemisphere, the occipital lobe, and in the temporal lobe. The size ranged from 1.2 to 5.5 cm (mean 3.2 cm SD 1.2). Fourteen (70%) AVMs were located in eloquent size. According to the Spetzler-Martin (SM) classification, there were 2 (10%) grade I AVMs, 9 (45%) grade II AVMs, 5 (25%) grade III AVMs, and 4 (20%) grade IV AVMs. Intranidal aneurysms were identified in 5 cases (cases 2, 4, 8, 13, and 17). One of these (case 2), also presented a single dilated and tortuous vein draining to the vein of Galen. In case 19, a stenosis was localized proximal to a prenidal aneurysm, and a fistula associated to its AVM was described.

Immediate Results of Embolization

Complete obliteration was achieved in 9 (45%) patients in a total of 13 sessions. In 7 (35%) patients, the AVM total obliteration was achieved in a single session (shown in Fig. 1). Among these 7 AVMs, the majority were localized on eloquent areas (4/7), and almost all (6/7) were low-grade lesions (SM grade I and II). In the 11 (55%) patients with an incomplete obliteration, a total of 21 sessions were performed, and the majority (7/11) were high-grade AVMs (SM grade III and IV). The relationship between the SM grade and the obliteration result is shown in Table 2.

Table 2.

SM grade according to the obliteration outcome

SM grade according to the obliteration outcome
SM grade according to the obliteration outcome
Fig. 1.

a Unruptured parietal AVM supplied by the middle cerebral artery. b Superselective angiogram in lateral view showing AVM nidus and draining vein. c Embolic agent injection and penetration into the AVM nidus in lateral view. d Immediate control angiogram showing total obliteration of the AVM. e Embolic agent cast in lateral view. AVM, arteriovenous malformation.

Fig. 1.

a Unruptured parietal AVM supplied by the middle cerebral artery. b Superselective angiogram in lateral view showing AVM nidus and draining vein. c Embolic agent injection and penetration into the AVM nidus in lateral view. d Immediate control angiogram showing total obliteration of the AVM. e Embolic agent cast in lateral view. AVM, arteriovenous malformation.

Close modal

NBCA (Braun) was used as the embolic material in 18 (52.9%) procedures, Onyx (ev3) in 8 (23.5%), Squid (Balt) in 6 (17.6%), and PHIL (Microvention) in 3 (8.8%). The relationship between the embolic materials used and the obliteration rates are shown in Table 3.

Table 3.

Embolic material used according to the obliteration outcome

Embolic material used according to the obliteration outcome
Embolic material used according to the obliteration outcome

Five cases were treated with different embolic materials. Case 2 was treated with Squid in the first session and NBCA in the second and third sessions. Case 10 was treated with PHIL and NBCA in the same procedure. Three cases (Case 4, 5 and 6) were treated with Onyx and NBCA in different sessions.

Complications

At the end of all the embolization procedures, complications were reported in 3 (8.8%) out of 34 sessions. In case 17, the surgeon noticed the extravasation of NBCA through a microperforation localized in the proximal tang of the AVM. This patient presented an IV-grade AVM and developed right hemiparesis immediately after the end of the procedure. Similarly, extravasation of the embolic agent was evidenced on the superselective angiogram during the AVM embolization of case 10 (shown in Fig. 2). The surgeon withdrew the microcatheter, and a new one was navigated toward the nidus in order to inject NBCA, and a subtotal obliteration of the malformation was performed. The immediate CT scan revealed an intracerebral and subarachnoid hemorrhage. This patient developed a left-eye anisocoria when the procedure concluded.

Fig. 2.

Case 10: intraoperative rupture of a previously ruptured frontal AVM. a Brain CT scan shows reabsorption of hematoma and malacia. b Angiography revealed a left frontal ruptured AVM (circle). c, d Superselective angiography in frontal and lateral views, respectively, showed the AVM nidus (circle). e, f Intraoperative rupture (arrow) with contrast extravasation to parenchyma and subarachnoid space. g Immediate CT scan showing the embolic agent, intracerebral hematoma and subarachnoid hemorrhage. h CT scan 4 days after the complication, with reabsorption of subarachnoid hemorrhage, brain edema and intracerebral hemorrhage present. AVM, arteriovenous malformation.

Fig. 2.

Case 10: intraoperative rupture of a previously ruptured frontal AVM. a Brain CT scan shows reabsorption of hematoma and malacia. b Angiography revealed a left frontal ruptured AVM (circle). c, d Superselective angiography in frontal and lateral views, respectively, showed the AVM nidus (circle). e, f Intraoperative rupture (arrow) with contrast extravasation to parenchyma and subarachnoid space. g Immediate CT scan showing the embolic agent, intracerebral hematoma and subarachnoid hemorrhage. h CT scan 4 days after the complication, with reabsorption of subarachnoid hemorrhage, brain edema and intracerebral hemorrhage present. AVM, arteriovenous malformation.

Close modal

In the second session of case 3, during the superselective angiogram, a cortical arteriolar branch presented slight bleeding, which was corrected with an NBCA injection without leaving any clinical manifestation. The patient was treated conservatively with good evolution. Deaths were not reported in the population studied.

The aim of AVM’s treatment is to achieve complete angiographic obliteration without leaving any neurological sequelae; however, choosing a treatment is an extremely complex issue. Endovascular embolization is a modality of treatment with 5 main uses: preoperative flow reduction, preradiosurgical volume reduction, the targeting of specific angioarchitectural features, palliative flow reduction, and complete curative occlusion [14, 15]. To date, diverse series have reported complete occlusion achieved with embolization, and in this scenario, some of AVM’s characteristics (size, feeding arteries, location, SM classification, and morphology) are predictive factors of an endovascular cure. In children, only few studies exist, and these have shown heterogeneous results regarding the safety and efficacy of the endovascular treatment [16-18]. A review of these series is presented in Table 4. Thus, we reported a single-surgeon single-institutional experience from treating AVMs with embolization in 20 pediatric patients. We observed that this modality is effective (complete obliteration rate of 45%) and safe (complications rate of 8.8%).

Table 4.

Pediatric series of AVMs treated with endovascular embolization

Pediatric series of AVMs treated with endovascular embolization
Pediatric series of AVMs treated with endovascular embolization

AVMs are the commonest cause of hemorrhagic stroke in children [19]. In more than half of the cases, the clinical picture is characterized by an intracranial hemorrhage, a headache, seizures, and focal neurological deficits, and it can also be asymptomatic [2]. In fact, in the pediatric population, intracranial hemorrhages represent 75–85% of the initial presentation [20]. This is in accordance with our pediatric series where 75% had a hemorrhagic presentation.

Immediate complete angiographic obliteration was achieved in 9 (45%) children and the majority from this group presented low-grade AVMs. In the pediatric population, angiographic cure rates range from 4 to 91% [10, 11, 16, 17, 21]. However, making a comparison is difficult between these studies without knowing the primary intention of the endovascular procedure. Furthermore, in certain studies, a presurgical embolization could achieve the complete occlusion of the AVM, or in other scenarios, only when the endovascular treatment fails, the patient is referred for complementary treatment [14].

Our study included patients from a center where all the embolization procedures were performed with intent to cure, and no other complementary treatment is done. Darsaut et al. [10] reported an initial cure rate of 4% in the patients who received endovascular embolization as a single-modality therapy. Moreover, these were low-grade AVMs, which is in accordance with our results. Conversely, De Castro-Afonso et al. [11] reported an immediate cure rate of 91.3% in 23 pediatric AVMs also treated with embolization using Onyx. Also, this study was performed in an institution where complementary treatment is indicated only when the embolization with intent to cure has not achieved complete occlusion. In addition, Ashour et al. [12] reported a cure rate of 11.8% using Onyx for attempting a curative embolization in 34 children. The variable cure rates from these studies could be a consequence of the different experiences and abilities from the participating neurosurgeons who performed the procedure. Conversely, in our study, all the procedures were performed by a single neurosurgeon employing a unique technique.

Several variables have been associated to a successful curative embolization of AVMs. It has been reported that a small size, a low number of feeding pedicles, superficial feeding arteries, and a superficial and non-eloquent AVM location are positive factors for an effective embolization [14]. Also, the SM grading scale has been associated with complete embolization due to its components: the size and the non-eloquent location [22]. In our pediatric series, we observed higher complete obliteration rates among low-grade AVMs (SM grade I and II) compared with high-grade AVMs (SM III and IV). In the study realized by Darsaut et al. [10], the 2 lesions cured by embolization were low-grade AVMs: a frontal grade I and a cerebellar grade II lesion. Furthermore, the majority of the pediatric AVMs cured with embolization reported by Zheng et al. [16] were low-grade AVMs (SM grade I and II). Our immediate results are in accordance with a similar pediatric series. However, the SM grade classification has not been validated to address endovascular interventions with the intention to cure nor has it been validated in the adult and pediatric population [7].

NBCA was used in 52.9% procedures, and its complete obliteration rate was 35.29%. This is a highly adhesive agent that allows a reliable and immediate vessel occlusion, and the reported obliteration rate varies between 13.7 and 40% [23, 24]. In our case series, we found an occlusion rate according to what has been reported. In this study, we assessed the obliteration rate immediately after the embolization; however, NBCA has shown a higher cure rate over time, which we were unable to assess [25].

Onyx was employed in 8 procedures with a cure rate of 25%. In a pediatric population, the cure rate was of 12% when the embolization with Onyx was performed as preoperative therapy [17]. Despite embolization with this embolic agent is usually performed as part of a preoperative plan, the cure rates when it is used as a curative therapy range between 11.8 and 91.3% [11, 12]. Thus, some authors prefer to use Onyx when attempting curative AVM embolization [12, 17]. Onyx precipitates slowly and precisely in a radial fashion as DMSO diffuses out of the solution; thus, an increased injection time and the ability to perform a controlled angiography are the advantages of this agent [26].

Squid was used in 6 procedures with a total occlusion rate of 33.33%. This is an EVOH copolymer that, compared to Onyx, is less viscous so that improves vascular penetration. In one study where 16 AVMs where treated with Squid, they found a complete obliteration of 37.5%, which agrees with our study [27]. Also, PHIL was used in only 2 sessions and achieved a complete obliteration in only one of them.

The literature reports a mortality incidence from 0 to 4.3% and morbidity from 0 to 22% when embolization with intent to cure is performed [14]. Some studies selected patients with specific AVM characteristics (a small size and a few pedicles) to receive this mode of treatment, and they observed no mortality and low complication rates [28, 29]. Moreover, a prognostic score has been developed to predict new deficits immediately after AVM embolization and is composed of the following: size <3 cm (1 point), size >6 cm (2 points), eloquent location (1 point), deep venous drainage (1 point), and need for >1 embolization session (1 point) [30]. In our 3 pediatric patients in whom complications were reported, 2 of them presented a lesion with superficial venous drainage, all of them had the malformation on an eloquent area, 2 developed the complication on their first embolization session, and 2 had a <3 cm AVM. Our results suggest that this prognostic score might not be accurate in the pediatric population because it was developed on a nonspecific population (age range of 4–75 years old). Thus, the risks factors for complications should be considered when a child is selected for embolization, especially when the intention is to cure the AVM.

We observed periprocedural complications in 3 (8.8%) out of 34 embolization sessions, and 2 of them presented a clinical repercussion. In the pediatric cohort of De Castro-Afonso et al. [11], only 3 complications were reported from which 2 of them presented an acute rupture of the AVM with ataxia and complete hemiparesis as clinical consequences. The complication rate per session reported by Darsaut et al. [10] was 7.7%; however, they considered all the sessions, even the ones where the treatment was not curative. Interestingly, the embolization-associated complications rates range between 6.7 and 26% in pediatric AVMs treated without intent to cure [17, 18]. Thus, despite endovascular therapy with intent to cure has been considered more aggressive and the complication rates in adults being slightly higher when compared with embolization as an adjunctive therapy [31], in pediatric AVMs, this mode of treatment could be as safe as the embolization performed without a curative purpose.

Five patients in the series presented unruptured AVMs, which developed headaches and seizures. One of these patients presented an intraoperative rupture. Since ARUBA recommended conservative treatment in this group of patients, multiple studies reported lower morbidity and mortality rates after treatment of unruptured AVMs (surgery, embolization, and radiosurgery) following the publication of ARUBA [32]. Based on this, the rational for the treatment of our patients with unruptured AVMs was the good outcomes obtained after treatment and the potential risk of future hemorrhage since this is a pediatric population.

This study presented certain limitations. First, the main consideration is the small sample size and the single-center design. Second, the absence of follow-up data does not allow the assessment of long-term outcomes related to the safety and efficacy of the endovascular treatment. Also, the fact that all the AVMs were treated in a center where only endovascular treatment is performed could lead to bias. Therefore, these issues impede the drawing of definitive conclusions, and our results should be analyzed carefully.

In conclusion, this single-surgeon single-center experience showed that embolization of AVMs in pediatric patients is a safe and efficient procedure. The embolic materials used (NBCA, Onyx, PHIL, and Squid) were useful in the included cohort. However, to confirm these results, larger prospective series with continued clinical and angiographic follow-up are needed. Prognostic scores that differentiate the lesions suitable for curative endovascular treatment are necessary in this population and should include the angioarchitectural characteristics of the lesion.

The authors hereby state that this research was conducted ethically in accordance with the World Medical Association Declaration of Helsinki. The Institutional Review Board of “Hospital Nacional Guillermo Almenara Irigoyen” with reference number RCEI-9 approved the study, and there was no need for informed consent.

The authors have no conflicts of interest to declare.

The authors did not receive any funding.

Aaron Rodriguez: conceptualization, methodology, investigation, writing – original draft, writing – review & editing, supervision, and project administration. Diego Bustamante: methodology, investigation, writing – original draft, and writing – review & editing. Kiara Camacho: methodology, investigation, writing – original draft, and writing – review & editing. Angie Mayoria: methodology, investigation, writing – original draft, and writing – review & editing. Giancarlo Saal: conceptualization, methodology, investigation, resources, writing – original draft, writing – review & editing, and supervision. Rodolfo Rodriguez: resources, writing – review & editing, and supervision.

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