Head and neck arteriovenous malformations: University of Tennessee experience, 2012–2022

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  • 1 Department of Neurosurgery, University of Tennessee Health Sciences Center, Memphis, Tennessee;
  • | 2 Department of Neurosurgery, University of Kansas Medical Center, Kansas City, Kansas;
  • | 3 Department of Otolargyngology,
  • | 4 Department of Ophthalmology, and
  • | 5 Department of Neurology, University of Tennessee Health Sciences Center, Memphis, Tennessee
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OBJECTIVE

Head and neck arteriovenous malformations (AVMs) are complex lesions that represent a subset of vascular anomalies (VAs). The authors present an analysis of their institutional experience managing these lesions as a multidisciplinary team.

METHODS

A retrospective chart review was performed of head and neck AVM patients treated at the authors’ institution from 2012 to 2022. Recorded data included patient demographic characteristics, details of clinical presentation, Schöbinger clinical scale and Yakes AVM classification results, and details of all endovascular and surgical treatments. The primary outcome of the study was clinical response to treatment. Angiographic occlusion and complication rates were reported. Chi-square tests were used for comparative statistics.

RESULTS

Sixteen patients (9 female, 56%) with AVMs of the head and neck presented from age 3 to 77 years. The Schöbinger stage was stage II in 56% of patients (n = 9) and stage III in 44% of patients (n = 7). The Yakes AVM classification was nidus type (2a, 2b, or 4) in 7 patients (43%) and fistula type (1, 3a, or 3b) in 9 patients (57%). The majority of patients (n = 11, 69.0%) were managed with embolization as the only treatment modality, with an average of 1.5 embolizations/patient (range 1–3). Surgical resection was employed in 5 patients (4 in combination with embolization). Symptom resolution and symptom control were achieved in 69% and 31% of patients, respectively, in the entire cohort. A radiographic cure was demonstrated in 50% of patients. There were no statistical differences in clinical outcomes or radiographic cure rates between patients treated with different modalities.

CONCLUSIONS

Head and neck AVMs can be treated successfully with a primarily endovascular management strategy by a multidisciplinary team with the goal of symptomatic control.

ABBREVIATIONS

AVF = arteriovenous fistula; AVM = arteriovenous malformation; EVOH = ethylene-vinyl alcohol copolymer; HHT = hemorrhagic hereditary telangiectasia; ISSVA = International Society for the Study of Vascular Anomalies; n-BCA = n-butyl-2-cyanoacrylate; TA = transarterial; TRICKS = time-resolved imaging of contrast kinetics; TV = transvenous; VA = vascular anomaly.

OBJECTIVE

Head and neck arteriovenous malformations (AVMs) are complex lesions that represent a subset of vascular anomalies (VAs). The authors present an analysis of their institutional experience managing these lesions as a multidisciplinary team.

METHODS

A retrospective chart review was performed of head and neck AVM patients treated at the authors’ institution from 2012 to 2022. Recorded data included patient demographic characteristics, details of clinical presentation, Schöbinger clinical scale and Yakes AVM classification results, and details of all endovascular and surgical treatments. The primary outcome of the study was clinical response to treatment. Angiographic occlusion and complication rates were reported. Chi-square tests were used for comparative statistics.

RESULTS

Sixteen patients (9 female, 56%) with AVMs of the head and neck presented from age 3 to 77 years. The Schöbinger stage was stage II in 56% of patients (n = 9) and stage III in 44% of patients (n = 7). The Yakes AVM classification was nidus type (2a, 2b, or 4) in 7 patients (43%) and fistula type (1, 3a, or 3b) in 9 patients (57%). The majority of patients (n = 11, 69.0%) were managed with embolization as the only treatment modality, with an average of 1.5 embolizations/patient (range 1–3). Surgical resection was employed in 5 patients (4 in combination with embolization). Symptom resolution and symptom control were achieved in 69% and 31% of patients, respectively, in the entire cohort. A radiographic cure was demonstrated in 50% of patients. There were no statistical differences in clinical outcomes or radiographic cure rates between patients treated with different modalities.

CONCLUSIONS

Head and neck AVMs can be treated successfully with a primarily endovascular management strategy by a multidisciplinary team with the goal of symptomatic control.

Head and neck arteriovenous malformations (AVMs) are complex lesions that represent a subset of vascular anomalies (VAs). VAs have historically been managed by a variety of specialists, including dermatologists, plastic surgeons, head and neck surgeons, and more recently, neurointerventional surgeons and medical oncologists. The lack of a uniform classification or clear understanding of VA angioarchitecture, biology, and natural history has contributed to suboptimal outcomes for patients. The pioneering work of Mulliken and Glowacki in 1982 was the first attempt to classify VAs based on their biology.1 Building on the foundation of this seminal work, there has been tremendous growth in the understanding of VAs. Uniform adoption of the International Society for the Study of Vascular Anomalies (ISSVA) classification in 1992, which has most recently been updated in 2018, has aided in the organization and communication of management teams (Table 1).1,2 Despite the development of agreed-upon nomenclature and classification, the misuse and incorrect application of terms creates a persistent issue for patients and physicians alike.3 This issue is so pervasive that Hassanein and colleagues demonstrated that in 70% of the literature the vascular anomalies were mislabeled, which was associated with a significantly increased risk of inappropriate treatment.4

TABLE 1.

Overview of ISSVA classification for vascular anomalies

ISSVA TypeVascular Malformation
ICapillary malformation
IIaLymphatic malformation
IIIVenous malformation
IVAVM
IVAVF

Approved at the May 2018 ISSVA General Assembly in Amsterdam, the Netherlands

ISSVA Classification of Vascular Anomalies © 2018 International Society for the Study of Vascular Anomalies, available at “issva.org/classification.” Accessed May 11, 2022. CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/).

The ISSVA classification system dichotomizes VAs into two broad categories: vascular tumors and vascular malformations.2 Vascular tumors proliferate by endothelial hyperplasia and are associated with elevated levels of vascular endothelial growth factor (VEGF), cell nuclear antigen, and glucose transporter protein-1 (GLUT1). As neoplastic lesions, vascular tumors are not static entities. Rather, they grow independently of the patient’s somatic development throughout patients’ lives, with periods of rapid growth, quiescence, and involution depending on the exact pathology and malignant potential.5 The most common vascular tumors are benign infantile hemangiomas; however, rare malignant lesions can occur.

Unlike vascular tumors, vascular malformations are not neoplastic lesions but rather result from localized defects of vasculogenesis and possess quiescent endothelium. These lesions are classified by vessel of origin and flow characteristics. Slow-flow lesions include venous malformations, lymphatic malformations, and capillary malformations, whereas high-flow lesions are broadly classified as AVMs. Vascular malformations are also categorized as either simple or combined and distinguished by whether they involve a named vessel or are part of a syndrome of anomalies. Important advances have been made in elucidating the genetic basis of these conditions, and this information is included in the ISSVA classification. The germline mutations causing congenital syndromes such as capillary malformation–AVM (CM-AVM) syndrome and hemorrhagic hereditary telangiectasia (HHT) have been identified, and somatic mutations that may cause the majority of sporadic AVMs have been well described (Table 2).2

TABLE 2.

Associated genetic markers for AVM and AVF

AVM/AVF TypeCausal Gene
SporadicMAP2K1
IIaLymphatic malformation
HHT
 HHT1ENG
 HHT2ACVRL1
 HHT3SMAD4
JPHTSMAD4
CM-AVMRASA1/EPHB4

JPHT = juvenile polyposis/hereditary hemorrhagic telangiectasia syndrome

The Schöbinger classification scale for AVMs is the most commonly utilized clinical staging system (Table 3).6 This scale is based on the presenting symptoms and is helpful to guide treatment decisions. The four stages are quiescence (cutaneous blush and warmth), expansion (bruit, audible pulsations, and enlarging lesion), local tissue destruction (pain, ulceration, spontaneous bleeding, and infection), and decompensation with congestive heart failure.6 The advent of endovascular medicine has also led to a more complete understanding and angiographic classification of the architecture of AVMs. This approach defines the accessibility of the nidus. The Yakes classification scheme categorizes AVMs according to morphology into nidus and fistula types and is useful to articulate how amenable a given lesion might be to various endovascular treatment techniques (Table 3).7

TABLE 3.

Yakes classification scheme for head and neck AVMs

Yakes Classification TypeAngioarchitecture
Nidus
 1Single direct AVF
 2aMultiple artery inputs w/ typical nidus & multiple draining veins
 2bSame as 2a but w/ single aneurysmal outflow vein
Fistula
 3aMultihole fistula w/ single outflow vein
 3bMultihole fistula into aneurysmal venous outflow vein w/multiple smaller venous outflows
 4Innumerable microfistulas w/ normal intervening tissue w/ normal pathologic blood flow using shared venous outflow

Based on Yakes WF, Yakes AM. Arteriovenous malformations: the Yakes classification and its therapeutic implications. Egyptian J Vasc Endovasc Surg. 2014;10(1):9-23.

In this paper we describe our institutional experience managing head and neck AVMs during the period from 2012 to 2022. We provide this information to familiarize readers with the proper classification of head and neck AVMs, describe the common presentations through case presentations, and provide an overview of modern treatment techniques and the resultant outcomes that can be achieved when endovascular techniques are applied in the framework of a multidisciplinary team of specialists.

Methods

We retrospectively reviewed the charts of 16 patients with extracranial head and neck AVMs who were treated at our institution from 2012 to 2022. We defined AVMs based on the ISSVA classification for VAs.1 The diagnosis of an AVM was made preoperatively using a combination of patient history, clinical examination, and noninvasive radiographic imaging with ultrasonography, CT with contrast or CTA, and MRI/MRA. DSA was performed on all patients to confirm diagnosis at the time of embolization or in treatment planning for surgical resection. The details of the patient presentations, treatments, and outcomes were recorded. The primary outcome of this report was the clinical response to treatment, which was reported as resolution of presenting symptoms, improvement in presenting symptoms, no clinical improvement, or worsening of symptoms. The secondary outcome measure was the rate of radiographic cure. Surgical and endovascular complications rates were also reported. Chi-square tests were performed to compare clinical and radiographic outcomes.

Results

During the study period, 16 patients (median age 27.5 years, range 3–77 years; 9 female, 56%) presented with AVMs of the head and neck. The face (n = 5, 31%) and scalp (n = 4, 25%) were the two most common locations for AVMs. Four patients reported evidence of the vascular malformation at birth or in infancy. One patient developed symptoms following a fall and another had a history of trauma in childhood. One patient reported enlargement and progression of symptoms during and after pregnancy. The remainder of patients had progression of symptoms spontaneously without any clear precipitating factor. Details of individual patient symptoms at presentation, classification, treatments, and outcomes are reported in Table 4. The Schöbinger stage was II in 56% of patients (n = 9) and III in 44% of patients (n = 7). The Yakes AVM classification was nidus type 2a, 2b, or 4 in 7 patients (43%) and arteriovenous fistula (AVF) type 1, 3a, or 3b, in 9 patients (57%). Five patients underwent treatment at other institutions prior to referral to our center. These treatments included the following: attempted surgery (n = 3, patients 1, 9, 15) with proximal ligation of external carotid branches; embolization (n = 2) with gelfoam of a maxillofacial AVM (patient 9) feeding vessel; ethanol sclerotherapy embolization of the venous outflow of a scalp AVM complicated by scalp necrosis and permanent alopecia (patient 14); and intralesional steroid injection of a palpebral AVM that was misdiagnosed as an infantile hemangioma (patient 13).

TABLE 4.

Patient baseline characteristics, details of treatment, and outcomes

Pt No.Age, yrs/SexSchöbinger StageSiteClin FindingsPrior TxPreop ImagingYakes TypeEmbo Tx at Au CenterRouteEmbo AgentEmbo ComplicationOp Resection at Au CenterImagingOutcomeClin FU, mos
PostopFURadiographicClin
142/FIIIFace (maxilla)Facial pain, swelling, throbbing, excessive lacrimation, pulsatile tinnitus, & epistaxisSTR*CT w/ contrast2a1DP INn-BCANNNoneNoneResidual (on Tx DSA)Sx controlled 0.25
250/FIIFace (maxilla)Pulsating mass w/ bruit & tinnitus after fallNoneMRI3a2TA, DP TVCoils & n-BCANNDSA, MRI6 (DSA), 10 (MRI)No residualSx resolved36
317/MIIScalpPulsatile occipital mass w/ bruit, Hx childhood traumaNoneUS & MRI2a1TAOnyxNNMRI12No residualSx resolved12
410/FIIIAuricularEnlarging mass w/ intermittent bleeding present since birthNoneMRI42TA, DP TVn-BCA & OnyxNNNoneNoneResidual (on Tx DSA)Sx improved24
551/FIIScalpPulsatile tinnitus, bruit, & occipital neck painNoneCTA31TAn-BCANNNoneNoneNo residual (on Tx DSA)Sx resolved1
612/FIIIFace (intramandibular)Multiple episodes oral bleedingNoneCTA & MRI3a1TA, TF TVCoils & n-BCANNRadiographNoneNo residual (on Tx DSA)Sx resolved4
752/FIINeckEnlarging pulsatile posterior neck massNoneCTA & MRI3b3TA, DP TVCoils & n-BCANNMRI17ResidualSx improved17
830/FIIFace (maxilla)Painful & enlarging pulsatile mass w/ skin erythema, progression after pregnancyNoneCTA & MRI3a1TAn-BCANNDSA2No residualSx resolved2
922/MIIIFace (maxilla)Scar deformity, enlarging mass, difficulty eating & talking, occasional bleeding, skin discolorationSubtotal resection* & partial embo*CT max/ face w/ contrast, MRI, DSA2a2TA, DP TVn-BCANNNoneNoneResidual (on Tx DSA)Sx improved1
1025/MIIPeriauricularEnlarging, painful mass w/ pulsatile tinnitusNoneMRI3a1TAn-BCA & OnyxNNNoneNoneResidual (on Tx DSA)Sx resolved1
1177/MIIIOrbitalProptosis w/ multiple intraorbital hemorrhage & diplopia episodesNoneMRI11DP TVCoilsIntraorbital hemorrhage w/ DP requiring lat orbitotomy & cantholysisNDSA4No residualSx resolved4
129/MIIScalpPulsatile hairline mass w/ bruit, enlarging since birthNoneMRI3a1DP TVn-BCANYMRI4No residualCure7
133/MIIIPalpebralEnlarging mass since birth w/ episodic bleeding & eye-opening difficulty obstructing visionLocal steroid injections*MRI3b2TAn-BCANYMRI1ResidualSx improved1
1418/FIIIScalpEnlarging scabbing, painful, pulsatile mass w/ hair loss, present since birthEthanol embo*MRI2a3TAn-BCA & OnyxNYMRI36No residualCure36
1544/MIIPalpebralScar/deformity, enlarging eyelid obstructing visionSTR*CTA2a1DP INCoils & n-BCANYNoneNoneResidual (on Tx DSA but resected in same-day op)Sx resolved1
1658/FIIOrbitalEnlarging pulsatile mass w/ proptosis & chemosisNoneMRI2a0NANANAYMRI2ResidualSx resolved3

Au = author; DP = direct puncture; Clin = clinical; embo = embolization; FU = follow-up; Hx = history; IN = intranidal; NA = not applicable; STR = subtotal resection; Sx = symptoms; TF = transfemoral; Tx = treatment; US = ultrasound.

Patients who had incorrect ISSVA diagnosis and/or experienced morbidity related to treatment at prior institutions.

Planned follow-up imaging postsurgery pending.

Planned additional embolization.

Symptom resolution and symptom control were achieved in 69% and 31% of patients in the entire cohort. Radiographic cure was demonstrated in 50% of patients. The majority of patients (n = 11, 69.0%) in our series were managed with embolization as the sole modality of treatment, with an average of 1.5 embolizations per patient (range 1–3). The radiographic cure rate for embolization alone was 64.0%, with symptomatic resolution in 64.0% of patients and improvement in the remaining 36%. Average duration of follow-up was 9.3 months (range 0.25–36.0 months). At the time of this report 1 patient remained under active treatment with additional embolization planned.

Surgical resection was performed as the sole treatment in 1 patient (6.2%), with an orbital AVM that was debulked operatively with complete resolution of symptoms, despite some residual seen on postoperative MRI. The remaining 4 patients (25%) underwent a combination of embolization (average 1.75 embolizations/patient, range 1–3) and single-session surgical resection of lesions causing cosmetic scalp deformity (patients 12 and 14) and visual impairment due to palpebral deformity (patients 13 and 15). Radiographic cure was obtained in 40% of the patients who underwent surgical resection. Overall, 60% of patients experienced symptom resolution, and the remaining 40% had symptom improvement. Average duration of follow-up was 9.6 (range 1–36) months. At the time of this report 1 patient remained under active treatment with planned follow-up imaging pending after surgical resection (patient 15). There was no statistical difference in radiographic cure or symptomatic resolution rates among patients treated with endovascular treatment alone versus patients who underwent surgery (64.0% vs 40%, p = 0.59, and 64.0% vs 60%, p = 1.00).

There was no permanent morbidity or mortality related to surgical or endovascular treatment. The rate of endovascular complications was 4.3% due to an intraorbital hemorrhage after direct puncture transvenous embolization that required lateral canthotomy. There was no statistically significant difference in the rates of endovascular and surgical complications (4.3% vs 0.0%, p = 1.00).

The routes and embolic agents chosen for embolization are detailed in Table 2. The most common route of embolization was transarterial (TA), utilized in 11/15 patients (73%), which was the only route in 6 patients and was used in combination with direct puncture of the venous outflow in 4 patients, or via the transfemoral-transvenous (TF-TV) route in 1 patient. Direct puncture embolization was performed as the sole treatment in 4 patients (2 intranidal and 2 TV punctures). The most commonly employed technique was liquid embolic embolization, which was used in all but one procedure (n = 22, 96%), with coils utilized as the sole treatment in the l patient in whom liquid embolic agents were not employed. n-butyl-2-cyanoacrylate (n-BCA; Trufill n-BCA liquid embolic system, Cerenovus/Johnson & Johnson) was the most commonly used liquid embolic agent (n = 17, 78.0%) either as a stand-alone technique (n = 13, 57%) or in conjunction with coils (n = 4, 17%) or with the Onyx liquid embolic system (Onyx, Medtronic) in 1 patient. Onyx was used as the sole agent in four procedures.

Case Studies

Case 1: Curative TA Embolization of a Buccal AVM—Schöbinger Grade II/Yakes Type 3a

This case involved a 30-year-old female patient with painful enlargement of a soft tissue pulsatile buccal mass with overlying skin erythema (Fig. 1 and Table 4, patient 8). Given the high-flow characteristics and location of the lesion proximate to the facial nerve, surgical resection was not recommended. The patient underwent single-session curative treatment with balloon-assisted flow control TA embolization via the left facial artery with BCA. Follow-up angiography 2 months after embolization demonstrated complete occlusion of the lesion without recurrence. This case demonstrates the relative simplicity with which endovascular techniques can be used to cure selected high-flow lesions. In this patient, surgery following embolization was not needed, because the cosmetic deformity (erythema and swelling) was due to high flow in the perilesional tissues and regressed once the lesion was selectively occluded.

FIG. 1.
FIG. 1.

Case 1. Left facial (buccal) AVM cured with balloon-assisted n-BCA embolization. A: Axial T2 MR image demonstrates prominent flow voids in the left buccal region with associated edema with T2 hyperintensity in the surrounding soft tissue. B and C: Anteroposterior (AP) and lateral left common carotid DSA demonstrates a massively dilated left facial artery leading to a multihole fistula-type AVM (Yakes classification). D and E: Unsubtracted images demonstrate distal catheterization of the facial artery with a dual-lumen microballoon inflated in the facial artery to produce flow arrest and facilitate embolization with a liquid embolic agent. F and G: AP and lateral left facial artery DSA with the balloon inflated demonstrates the lesion and pinpoints the exact sites of fistulization from artery to vein (red arrows). H and I: AP and lateral fluoroscopic images demonstrate the n-BCA glue cast that encompasses the entire lesion. J: Lateral left common carotid artery DSA immediately postembolization demonstrates no residual lesion. K: Lateral left common carotid artery DSA 3 months postembolization demonstrates stable complete occlusion of the lesion and downregulation of the facial artery to normal size.

Case 2: Curative TA and TV Embolization of a Mandibular AVF—Schöbinger Grade III/Yakes Type 3a

This patient was a 12-year-old girl who presented with several episodes of spontaneous oral bleeding that occurred while sleeping and would soak her bedsheets. MRI evaluation was consistent with a high-flow vascular malformation. T1 MRI with gadolinium time-resolved imaging of kinetics (TRICKS) sequences is an imaging modality that is a valuable adjunct to standard MRI and can provide a noninvasive cross-sectional imaging tool to distinguish high- and low-flow VAs. Given the clinical history of this patient, we proceeded to angiography with intention to treat.

TA embolization with n-BCA and coils was performed from multiple pedicles. Because of the innumerable arterial connections, cure from a TA route was not possible. TV embolization with coils and n-BCA permitted complete occlusion of the lesion (Fig. 2 and Table 4, patient 6).

FIG. 2.
FIG. 2.

Case 2. TA and TV curative coil and liquid embolic embolization of a mandibular AVF. A: T1 MR image with gadolinium TRICKS demonstrates a high-flow lesion in the mandible fed by external carotid artery branches. B and C: AP and lateral left external carotid artery angiograms demonstrate a high-flow AVF of the mandible. D–F: Lateral DSA from the left greater descending palatine, inferior alveolar, and facial arteries demonstrating the extensive arterial supply of the lesion and venous outflow through the mandibular vein. G: Microcatheter digital subtraction venogram from the left mandibular vein after retrograde transfemoral venous catheterization. H: Lateral DSA from the left external carotid artery after TA embolization of multiple arterial pedicles with n-BCA and coils and TV coiling. The image demonstrates residual shunting due to the innumerable transosseous external carotid artery feeding vessels despite embolization. I: Lateral DSA from the left external carotid artery post TV embolization with n-BCA demonstrates complete occlusion of the lesion. J: Axial CT image preembolization demonstrates expansion of the left mandibular ramus with associated bone erosion and thinning at the site of the AVF. K: Axial CT image postembolization demonstrates a metallic artifact from the intermandibular coil mass with positive remodeling of the surrounding bone, which has significantly thickened. L: Panorex jaw radiograph demonstrates the coil mass in the venous pouch and the linear coil mass in the inferior alveolar artery as well as a glue cast in the alveolar vein adjacent to the coil mass.

Case 3: Direct Puncture TV Embolization of a Maxillofacial AVM—Schöbinger Grade III/Yakes Type 2a

This patient was a 22-year-old man with a maxillofacial AVM who had undergone two previous attempts at surgical resection and one attempt at embolization prior to presentation at our center. Despite these multiple treatments, the patient had a significant residual lesion and growth of the lesion with ongoing pain, deformity, and bleeding. We performed two embolization sessions with a combination of TA and direct puncture embolization into the venous drainage of the lesion (Fig. 3 and Table 4, patient 9). Direct puncture was necessary because previous attempts at surgery and embolization resulted in proximal ligations of the feeding arteries with surgical clips or with gelfoam that did not address the nidus. These proximal ligations impeded direct access to the nidus via TA routes and caused recruitment of an adjacent collateral external carotid artery supply that was not suitable for TA access. After two embolization sessions, the lesion was near angiographic cure with minimal arteriovenous shunting. This case illustrates the futility of endovascular or surgical treatments that do not address the nidus or exact point of fistulous connections.

FIG. 3.
FIG. 3.

Case 3. Direct puncture TV immobilization of a maxillofacial AVM. A: Unsubtracted lateral fluoroscopic image with proximal ligation of external carotid artery branches. Multiple surgical clips from previous surgery at an outside institution are visible throughout the midface. B: External carotid angiogram demonstrates extensive AVM in the premaxillary region. The red dashed circle demonstrates recruitment of arterial-to-arterial anastomosis to the nidus below this region due to previous proximal surgical ligations. These proliferative angiogenic changes complicate direct TA treatment of the AVM. C and D: Direct percutaneous puncture of the AVM draining vein with a 20-gauge spinal needle. E and H: AP and lateral angiograms of the transverse facial artery demonstrate the AVM nidus and principal draining vein that was punctured (red arrow). F and I: AP and lateral angiograms from the spinal needle demonstrating puncture of the draining vein of the AVM. G and J: n-BCA glue cast after embolization with retrograde occlusion of the nidus of the AVM. K and L: AP and lateral fluoroscopic images demonstrate the final n-BCA glue cast after additional embolization of the AVM from the microcatheter in the transverse facial artery. M and N: Final postembolization AP and lateral external carotid angiograms demonstrate no significant arteriovenous shunting.

Case 4: TA Embolization and Surgical Excision of a Palpebral AVM—Schöbinger Grade III/Yakes Type 3b

This patient was a 3-year-old boy who presented with progressive enlargement of a palpebral vascular mass that was obstructing his vision and causing amblyopia. He underwent two sessions of TA embolization with n-BCA followed by planned surgical excision and palpebral reconstruction by the oculoplastic surgery service to remove excess tissue and relieve mechanical obstruction (Fig. 4 and Table 4, patient 13). The patient did well postoperatively with improvement in his vision. This case illustrates the importance of surgical resection for accessible lesions that result in functional and/or cosmetic impairment despite endovascular obliteration of the lesion.

FIG. 4.
FIG. 4.

Case 4. TA embolization and surgical excision of a palpebral AVM. A and B: Preoperative clinical and T2 MR images demonstrate a vascular mass that encompasses the mid- to lateral aspect of the superior eyelid but results in regional hyperemia and skin discoloration beyond the borders of the lesion and expands the soft tissue, with resultant obstruction of vision. C and D: Right external and internal carotid diagnostic cerebral angiograms demonstrate an AVM with a blood supply from palpebral branches of the superficial temporal artery and ophthalmic artery (Inset), which is massively dilated due to the high-flow nature of the lesion. E and F: Inset images of the n-BCA glue cast in the palpebral branches of the superficial temporal artery and ophthalmic arteries. Dashed red lines indicate the segment of the corresponding arteries that were embolized on the high-magnification views of the external and internal carotid arteries. G and H: Postembolization DSAs of the external and internal carotid arteries demonstrate complete occlusion of the lesion. I: Immediate postoperative clinical images demonstrate significant resolution of hyperemia and tissue discoloration, but redundant skin remains that would obstruct vision. J: Operative image with incision in the crease along the superior eyelid exposing the embolized lesion. K: En bloc excision of the lesion and redundant tissue. L: Immediate postoperative reconstruction with relief of overhanging lid tissue. M: Clinical image 3 weeks postoperatively demonstrates improvement in postoperative swelling and relief of pupillary obstruction, which allowed for improvement in vision.

Discussion

In this series we demonstrate excellent clinical outcomes with a treatment philosophy guided by a focus on symptom control and employing endovascular treatment as the primary therapeutic modality. AVMs of the head and neck are dynamic lesions that may present in childhood or adulthood. Our series reflects this natural history within a wide age range of patients. Although the exact triggers are unknown, progression or enlargement of AVMs is common and unpredictable and may occur at any point in a patient’s lifetime. It has been noted that puberty, pregnancy, and trauma can precipitate more rapid phase of disease progression. The increased blood flow and engorgement of the high-pressure draining veins that occur with disease progression cause perilesional ischemia with subsequent pain, ulceration, and skin changes.8–10 There were no patients in our series with Schöbinger stage I lesions, which is not surprising due to the minimal symptoms associated with lesions at this stage and thus lower likelihood of patients in this stage of illness to come to medical attention. AVMs in stage I have been reported to be well tolerated and therefore are often treated with observation. We are not able to comment on this treatment strategy due to the lack of stage 1 patients in our cohort. The published literature remains unclear regarding whether early treatment of patients in stage I should be considered to prevent progression. Our approach has been to offer endovascular treatment to mildly symptomatic patients with stage II or stage III lesions because at these stages the lesions have a very low likelihood of spontaneous regression or stabilization without treatment.9,10 Our philosophy for treatment of these lesions is not to pursue radiographic cure at the expense of morbidity. The goal of treatment is to reduce or eliminate symptoms, prevent progression, decrease the risk of potentially life-threatening bleeding, and correct cosmetic deformity when possible.

We found that endovascular treatment was equally as effective as surgical resection to achieve both symptom resolution and radiographic cure. Our results are consistent with the published modern experience on the treatment of AVMs of the head and neck demonstrating modest cure rates of 27%–67% with high rates of symptomatic control when using a primary endovascular treatment paradigm.11–15 Higher cure rates have been reported in older series using ethanol embolization strategies at the expense of much higher complications rates compared to those in our series of up to 45%.16 Reports of long-term follow-up and recurrence rates of head and neck AVMs is very limited in the available literature. Dmytriw et al. reports that for those lesions treated by embolization alone, recurrence rates were 7.1%.14 For this reason, delayed follow-up imaging or angiography is typically recommended to ensure long-term cure, usually in the 6- to 12-month window. Our short follow-up period and inconsistent postoperative imaging would suggest that there is a possibility that if patients were followed longer, our cure rate might in fact be lower, which is a shortcoming of this series. One must also understand that the goal of treatment in these lesions is not always to cure but often rather to palliate symptoms, especially in extensive and complicated AVMs.

Understanding that the crux of AVM pathophysiology lies in the nidus and/or fistulous connections is the guiding principle of any surgical or endovascular treatment. Unfortunately, this essential concept remains poorly understood, as reflected by the patients who sought a second opinion at our center. Prior to referral, a quarter of our patients underwent procedures that caused morbidity and were not clinically helpful because they did not treat the nidus directly or were the result of a misdiagnosis. Disrupting the normal arterial supply by proximal embolization or surgical ligation of feeding vessels and/or sacrifice of venous drainage of the AVM without treating the nidus/fistulous point has been demonstrated to cause morbidity, including necrosis of the overlying skin.8,17 The location of head and neck AVMs makes primary surgical resection fraught with risks, including cranial nerve damage, excessive bleeding, and poor cosmetic outcomes in the majority of cases.18

The route of embolization and materials used are operator dependent, and successful treatment may be obtained with multiple strategies. There are technical nuances and endovascular strategies that we believe contribute to our favorable outcomes. In terms of route of embolization, a direct TA route when available is preferred and is often curative for nidus morphology lesions (Yakes type 2a and 2b). Achieving flow control with a dual-lumen balloon microcatheter is helpful in the management of high-flow lesions. This tool facilitates understanding of the angioarchitecture and allows accurate deployment of liquid embolic agents (Fig. 1). Retrograde TV access is often best for fistula morphology lesions (Yakes type 1, 3a, and 3b) because occlusion of the recipient vein is often curative. This strategy is the most efficient means to produce cure, particularly with Yakes type 3a and 3b lesions, which have a multitude of arterial inputs (Fig. 2). We reserve direct puncture of the nidus or draining veins for cases in which TA or TV access is limited due to inaccessible tortuous arterial anatomy or because of previous proximal ligation surgeries (Fig. 3).

The most commonly used embolic agent in our series was n-BCA. We feel it has several advantages compared with Onyx or ethylene-vinyl alcohol copolymer (EVOH) due to its intrinsic properties and mechanism of action. EVOH is cohesive and causes a secondary thrombosis by its obstructive presence in the vessel, whereas n-BCA causes an exothermic reaction as it polymerizes and is adhesive, which leads to direct thrombosis of the vasculature. This has the advantage that smaller volumes of n-BCA with shorter injection times can lead to similar results without the mass effect (which itself may be disfiguring) produced by large-volume injections of EVOH. In addition, n-BCA can be visualized with ethiodol, whereas tantalum is presuspended in EVOH for fluoroscopic visualization, which limits the use of EVOH in facial lesions because of the potential for cosmetic disfigurement and skin tattooing with tantalum.19 We also routinely inject n-BCA through dual-lumen balloons, and although there is a risk of balloon deflation or rupture due to the ethiodol, this practice is rendered safe by the location of the microcatheter proximate or within the AVM nidus in the external carotid artery circulation in conjunction with the high-flow nature of the lesions. We did not experience any balloon ruptures or any nontarget embolizations in this series, results that attest to the safety of this technique. The other major advantage of n-BCA is the operator’s ability to customize the amount of n-BCA in each injection. This allows control of the polymerization time tailored to the unique flow conditions of the lesion.

Our team employed surgical resection primarily for debulking to enhance both cosmetic (e.g., scalp debulking) and functional outcomes (e.g., eyelid reconstruction). Sufficient devascularization of the lesion to minimize intraoperative blood loss is a requisite for successful surgery.8 It is essential that perilesional tissue distant to the nidus that is used for surgical reconstruction not be devascularized, as wound healing will be impeded by inadequate blood flow postsurgery. The interventionalists and surgeons should coordinate a plan to define the goals and limits of each other’s treatments.

There are important limitations in our case series, including the retrospective design, small number of patients, incomplete imaging follow-up, and variable follow-up duration. Recurrence rates of up to 80% have been reported for head and neck AVMs, so our success rates may not be completely representative of longer-term outcomes.13 As such, in our practice we will continue to follow all of our patients, even those with radiographic cure and/or symptom resolution, for extended periods of time.

Although multidisciplinary treatment of AVMs as described in our series offers the possibility of favorable outcomes, patients often have ongoing and/or recurrent symptoms despite expert management. Modern understanding of the biology of AVMs offers hope for medical treatments that will address the genetic origins of this condition. Recent studies have demonstrated that a large portion of these lesions are the result of somatic mutations in the MAP2K1 and KRAS genes. These cell-signaling pathways are involved in cellular proliferation and cell migration and have been identified in both CNS and peripheral AVMs in humans. This understanding has opened the door for genotype-based treatment with parenteral inhibitors of the enzymes mitogen-activated protein kinase (MEK) 1 and 2. These medications are commercially available and approved for a variety of malignancies affecting this pathway and more recently their use has been reported in selected cases to cause regression of non-CNS AVMs.20,21

Conclusions

Head and neck AVMs require a multidisciplinary approach for safe and effective treatment. Embolization has a primary role in the management of patients with AVMs. Multiinstitutional prospective studies with larger patient cohorts, standardized long-term follow-up, and integration of novel biological therapies are needed to improve outcomes in this challenging group of patients.

Disclosures

Adam S. Arthur reports ownership in Azimuth, Bendit, Cerebrotech, EndoStream, Magneto, Mentice, Neurogami, Neuros, Scientia, Serenity, Synchron, Tulavi, Vastrax, and VizAI and being a consultant for Arsenal, Balt, Johnson & Johnson, Medtronic, MicroVention, Penumbra, Scientia, Siemens, and Stryker. Lucas Elijovich reports being a consultant for MicroVention, VizAI, Cerenovus, MIVI, and Corindus.

Author Contributions

Conception and design: Elijovich, Peterson, Gleysteen, Fowler, Arthur. Acquisition of data: Elijovich, Dawkins, Motiwala, Peterson, Gleysteen, Fowler. Analysis and interpretation of data: Elijovich, Dawkins, Peterson, Gleysteen, Fowler. Drafting the article: Elijovich, Dawkins, Motiwala. Critically revising the article: Elijovich, Dawkins, Gleysteen, Fowler, Arthur. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Elijovich. Statistical analysis: Elijovich. Administrative/technical/material support: Elijovich, Arthur. Study supervision: Elijovich.

References

  • 1

    Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg. 1982;69(3):412422.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    ISSVA classification for vascular anomalies. International Society for the Study of Vascular Anomalies.Accessed May 16, 2022.http://www.issva.org/classification

    • Search Google Scholar
    • Export Citation
  • 3

    Shatzkes DR. Vascular anomalies: description, classification and nomenclature. Appl Radiol. 2018;47(9):813.

  • 4

    Hassanein AH, Mulliken JB, Fishman SJ, Greene AK. Evaluation of terminology for vascular anomalies in current literature. Plast Reconstr Surg. 2011;127(1):347351.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Finn MC, Glowacki J, Mulliken JB. Congenital vascular lesions: clinical application of a new classification. J Pediatr Surg. 1983;18(6):894900.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Schöbinger R. Schöbinger classification of arteriovenous malformations. In: Proceedings of International Society for the Study of Vascular Anomalies Congress;Rome, Italy,June 23–26, 1996.

    • Search Google Scholar
    • Export Citation
  • 7

    Yakes WF, Vogelzang RL, Ivancev K, Yakes AM. New arteriographic classification of AVM based on the Yakes classification system. In: Kim YW, Lee BB, Yakes W, Do YS, eds.Congenital Vascular Malformations. Springer;2017.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Wu JK, Bisdorff A, Gelbert F, Enjolras O, Burrows PE, Mulliken JB. Auricular arteriovenous malformation: evaluation, management, and outcome. Plast Reconstr Surg. 2005;115(4):985995.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Fowell C, Jones R, Nishikawa H, Monaghan A. Arteriovenous malformations of the head and neck: current concepts in management. Br J Oral Maxillofac Surg. 2016;54(5):482487.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Liu AS, Mulliken JB, Zurakowski D, Fishman SJ, Greene AK. Extracranial arteriovenous malformations: natural progression and recurrence after treatment. Plast Reconstr Surg. 2010;125(4):11851194.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Thiex R, Wu I, Mulliken JB, Greene AK, Rahbar R, Orbach DB. Safety and clinical efficacy of Onyx for embolization of extracranial head and neck vascular anomalies. AJNR Am J Neuroradiol. 2011;32(6):10821086.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Dabus G, Linfante I, Benenati J, Perlyn CA, Martínez-Galdámez M. Interventional management of high-flow craniofacial vascular malformations: a database analysis and review of the literature. J Neurointerv Surg. 2017;9(1):9296.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Meila D, Grieb D, Greling B, et al. Endovascular treatment of head and neck arteriovenous malformations: long-term angiographic and quality of life results. J Neurointerv Surg. 2017;9(9):860866.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Dmytriw AA, Ter Brugge KG, Krings T, Agid R. Endovascular treatment of head and neck arteriovenous malformations. Neuroradiology. 2014;56(3):227236.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Griauzde J, Wilseck ZM, Chaudhary N, et al. Endovascular treatment of arteriovenous malformations of the head and neck: focus on the Yakes classification and outcomes. J Vasc Interv Radiol. 2020;31(11):18101816.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Park KB, Do YS, Kim DI, et al. Predictive factors for response of peripheral arteriovenous malformations to embolization therapy: analysis of clinical data and imaging findings. J Vasc Interv Radiol. 2012;23(11):14781486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Dingman RO, Grabb WC. Congenital arteriovenous fistulae of the external ear. Plast Reconstr Surg. 1965;35(6):620628.

  • 18

    Kohout MP, Hansen M, Pribaz JJ, Mulliken JB. Arteriovenous malformations of the head and neck: natural history and management. Plast Reconstr Surg. 1998;102(3):643654.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Arat A, Cil BE, Vargel I, et al. Embolization of high-flow craniofacial vascular malformations with onyx. AJNR Am J Neuroradiol. 2007;28(7):14091414.

  • 20

    Nikolaev SI, Vetiska S, Bonilla X, et al. Somatic activating KRAS mutations in arteriovenous malformations of the brain. N Engl J Med. 2018;378(3):250261.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Edwards EA, Phelps AS, Cooke D, et al. Monitoring arteriovenous malformation response to genotype-targeted therapy. Pediatrics. 2020;146(3):e20193206.

Illustration from Agosti et al. (E5). Used with permission of Mayo Foundation for Medical Education and Research. All rights reserved.

  • View in gallery

    Case 1. Left facial (buccal) AVM cured with balloon-assisted n-BCA embolization. A: Axial T2 MR image demonstrates prominent flow voids in the left buccal region with associated edema with T2 hyperintensity in the surrounding soft tissue. B and C: Anteroposterior (AP) and lateral left common carotid DSA demonstrates a massively dilated left facial artery leading to a multihole fistula-type AVM (Yakes classification). D and E: Unsubtracted images demonstrate distal catheterization of the facial artery with a dual-lumen microballoon inflated in the facial artery to produce flow arrest and facilitate embolization with a liquid embolic agent. F and G: AP and lateral left facial artery DSA with the balloon inflated demonstrates the lesion and pinpoints the exact sites of fistulization from artery to vein (red arrows). H and I: AP and lateral fluoroscopic images demonstrate the n-BCA glue cast that encompasses the entire lesion. J: Lateral left common carotid artery DSA immediately postembolization demonstrates no residual lesion. K: Lateral left common carotid artery DSA 3 months postembolization demonstrates stable complete occlusion of the lesion and downregulation of the facial artery to normal size.

  • View in gallery

    Case 2. TA and TV curative coil and liquid embolic embolization of a mandibular AVF. A: T1 MR image with gadolinium TRICKS demonstrates a high-flow lesion in the mandible fed by external carotid artery branches. B and C: AP and lateral left external carotid artery angiograms demonstrate a high-flow AVF of the mandible. D–F: Lateral DSA from the left greater descending palatine, inferior alveolar, and facial arteries demonstrating the extensive arterial supply of the lesion and venous outflow through the mandibular vein. G: Microcatheter digital subtraction venogram from the left mandibular vein after retrograde transfemoral venous catheterization. H: Lateral DSA from the left external carotid artery after TA embolization of multiple arterial pedicles with n-BCA and coils and TV coiling. The image demonstrates residual shunting due to the innumerable transosseous external carotid artery feeding vessels despite embolization. I: Lateral DSA from the left external carotid artery post TV embolization with n-BCA demonstrates complete occlusion of the lesion. J: Axial CT image preembolization demonstrates expansion of the left mandibular ramus with associated bone erosion and thinning at the site of the AVF. K: Axial CT image postembolization demonstrates a metallic artifact from the intermandibular coil mass with positive remodeling of the surrounding bone, which has significantly thickened. L: Panorex jaw radiograph demonstrates the coil mass in the venous pouch and the linear coil mass in the inferior alveolar artery as well as a glue cast in the alveolar vein adjacent to the coil mass.

  • View in gallery

    Case 3. Direct puncture TV immobilization of a maxillofacial AVM. A: Unsubtracted lateral fluoroscopic image with proximal ligation of external carotid artery branches. Multiple surgical clips from previous surgery at an outside institution are visible throughout the midface. B: External carotid angiogram demonstrates extensive AVM in the premaxillary region. The red dashed circle demonstrates recruitment of arterial-to-arterial anastomosis to the nidus below this region due to previous proximal surgical ligations. These proliferative angiogenic changes complicate direct TA treatment of the AVM. C and D: Direct percutaneous puncture of the AVM draining vein with a 20-gauge spinal needle. E and H: AP and lateral angiograms of the transverse facial artery demonstrate the AVM nidus and principal draining vein that was punctured (red arrow). F and I: AP and lateral angiograms from the spinal needle demonstrating puncture of the draining vein of the AVM. G and J: n-BCA glue cast after embolization with retrograde occlusion of the nidus of the AVM. K and L: AP and lateral fluoroscopic images demonstrate the final n-BCA glue cast after additional embolization of the AVM from the microcatheter in the transverse facial artery. M and N: Final postembolization AP and lateral external carotid angiograms demonstrate no significant arteriovenous shunting.

  • View in gallery

    Case 4. TA embolization and surgical excision of a palpebral AVM. A and B: Preoperative clinical and T2 MR images demonstrate a vascular mass that encompasses the mid- to lateral aspect of the superior eyelid but results in regional hyperemia and skin discoloration beyond the borders of the lesion and expands the soft tissue, with resultant obstruction of vision. C and D: Right external and internal carotid diagnostic cerebral angiograms demonstrate an AVM with a blood supply from palpebral branches of the superficial temporal artery and ophthalmic artery (Inset), which is massively dilated due to the high-flow nature of the lesion. E and F: Inset images of the n-BCA glue cast in the palpebral branches of the superficial temporal artery and ophthalmic arteries. Dashed red lines indicate the segment of the corresponding arteries that were embolized on the high-magnification views of the external and internal carotid arteries. G and H: Postembolization DSAs of the external and internal carotid arteries demonstrate complete occlusion of the lesion. I: Immediate postoperative clinical images demonstrate significant resolution of hyperemia and tissue discoloration, but redundant skin remains that would obstruct vision. J: Operative image with incision in the crease along the superior eyelid exposing the embolized lesion. K: En bloc excision of the lesion and redundant tissue. L: Immediate postoperative reconstruction with relief of overhanging lid tissue. M: Clinical image 3 weeks postoperatively demonstrates improvement in postoperative swelling and relief of pupillary obstruction, which allowed for improvement in vision.

  • 1

    Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg. 1982;69(3):412422.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    ISSVA classification for vascular anomalies. International Society for the Study of Vascular Anomalies.Accessed May 16, 2022.http://www.issva.org/classification

    • Search Google Scholar
    • Export Citation
  • 3

    Shatzkes DR. Vascular anomalies: description, classification and nomenclature. Appl Radiol. 2018;47(9):813.

  • 4

    Hassanein AH, Mulliken JB, Fishman SJ, Greene AK. Evaluation of terminology for vascular anomalies in current literature. Plast Reconstr Surg. 2011;127(1):347351.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Finn MC, Glowacki J, Mulliken JB. Congenital vascular lesions: clinical application of a new classification. J Pediatr Surg. 1983;18(6):894900.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Schöbinger R. Schöbinger classification of arteriovenous malformations. In: Proceedings of International Society for the Study of Vascular Anomalies Congress;Rome, Italy,June 23–26, 1996.

    • Search Google Scholar
    • Export Citation
  • 7

    Yakes WF, Vogelzang RL, Ivancev K, Yakes AM. New arteriographic classification of AVM based on the Yakes classification system. In: Kim YW, Lee BB, Yakes W, Do YS, eds.Congenital Vascular Malformations. Springer;2017.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Wu JK, Bisdorff A, Gelbert F, Enjolras O, Burrows PE, Mulliken JB. Auricular arteriovenous malformation: evaluation, management, and outcome. Plast Reconstr Surg. 2005;115(4):985995.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Fowell C, Jones R, Nishikawa H, Monaghan A. Arteriovenous malformations of the head and neck: current concepts in management. Br J Oral Maxillofac Surg. 2016;54(5):482487.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Liu AS, Mulliken JB, Zurakowski D, Fishman SJ, Greene AK. Extracranial arteriovenous malformations: natural progression and recurrence after treatment. Plast Reconstr Surg. 2010;125(4):11851194.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Thiex R, Wu I, Mulliken JB, Greene AK, Rahbar R, Orbach DB. Safety and clinical efficacy of Onyx for embolization of extracranial head and neck vascular anomalies. AJNR Am J Neuroradiol. 2011;32(6):10821086.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Dabus G, Linfante I, Benenati J, Perlyn CA, Martínez-Galdámez M. Interventional management of high-flow craniofacial vascular malformations: a database analysis and review of the literature. J Neurointerv Surg. 2017;9(1):9296.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Meila D, Grieb D, Greling B, et al. Endovascular treatment of head and neck arteriovenous malformations: long-term angiographic and quality of life results. J Neurointerv Surg. 2017;9(9):860866.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Dmytriw AA, Ter Brugge KG, Krings T, Agid R. Endovascular treatment of head and neck arteriovenous malformations. Neuroradiology. 2014;56(3):227236.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Griauzde J, Wilseck ZM, Chaudhary N, et al. Endovascular treatment of arteriovenous malformations of the head and neck: focus on the Yakes classification and outcomes. J Vasc Interv Radiol. 2020;31(11):18101816.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Park KB, Do YS, Kim DI, et al. Predictive factors for response of peripheral arteriovenous malformations to embolization therapy: analysis of clinical data and imaging findings. J Vasc Interv Radiol. 2012;23(11):14781486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Dingman RO, Grabb WC. Congenital arteriovenous fistulae of the external ear. Plast Reconstr Surg. 1965;35(6):620628.

  • 18

    Kohout MP, Hansen M, Pribaz JJ, Mulliken JB. Arteriovenous malformations of the head and neck: natural history and management. Plast Reconstr Surg. 1998;102(3):643654.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Arat A, Cil BE, Vargel I, et al. Embolization of high-flow craniofacial vascular malformations with onyx. AJNR Am J Neuroradiol. 2007;28(7):14091414.

  • 20

    Nikolaev SI, Vetiska S, Bonilla X, et al. Somatic activating KRAS mutations in arteriovenous malformations of the brain. N Engl J Med. 2018;378(3):250261.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Edwards EA, Phelps AS, Cooke D, et al. Monitoring arteriovenous malformation response to genotype-targeted therapy. Pediatrics. 2020;146(3):e20193206.

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