Vascular Surgery for Arteriovenous Malformations 

Updated: Feb 01, 2019
Author: Allison Leigh Speer, MD; Chief Editor: Vincent Lopez Rowe, MD 

Overview

Background

Vascular anomalies are among the most common congenital abnormalities in infants and children. Historically, their treatment has been impeded by confusing terminology and imprecise classification. Lesions were named with descriptive terms (eg, strawberry hemangioma or port-wine stain) or histopathologic terms (eg, capillary hemangioma, cavernous hemangioma, or lymphangioma). Although some vascular anomalies may appear similar, their biologic behavior differs markedly; therefore, treatment should be based on a proper classification system.[1, 2]

Classification

Classification of vascular anomalies is based on the landmark 1982 paper by Mulliken and Glowacki, which proposed a simplified categorization of these anomalies that was based on biologic activity.[3] As a result, the following two main types of vascular anomalies are generally recognized:

  • Vascular tumors
  • Vascular malformations

Differentiating between these two types of anomalies is essential because their treatment is quite different. The management of vascular anomalies is a dynamic and rapidly developing subspecialty, which requires interdisciplinary care and collaboration.

During its 1996 workshop, the International Society for the Study of Vascular Anomalies (ISSVA) adopted a classification system designed to provide a common language for guiding treatment. It was based on Mulliken and Glowacki’s biologic study but also further distinguished vascular malformations according to hemodynamics and predominant anomalous channels.[4, 5, 6, 7]  At its 20th workshop in 2014, the ISSVA approved a revised classification,[8]  which was further revised at the ISSVA General Assembly in May 2018 (see Table 1 below).[9]

Table 1. ISSVA Classification of Vascular Anomalies (May 2018 Revision) (Open Table in a new window)

Vascular Tumors Vascular Malformations

Benign vascular tumors

Infantile hemangioma/hemangioma of infancy

Congenital hemangioma

  • Rapidly involuting (RICH)
  • Noninvoluting (NICH)
  • Partially involuting (PICH)

Tufted angioma

Spindle-cell angioma

Epithelioid angioma

Pyogenic granuloma (lobular capillary hemangioma)

Others

Related lesions

Simple vascular malformations

Capillary malformation (CM)

  • Nevus simplex/salmon patch, "angel kiss," "stork bite"
  • Cutaneous/mucosal CM (port-wine stain)
  • Reticulate CM
  • CM of CM-AVM (arteriovenous malformation)
  • Cutis marmorata telangiectatica congenita (CMTC)
  • Others
  • Telangiectasia (hereditary hemorrhagic telangiectasia [HHT], others)

Lymphatic malformation (LM)

  • Common (cystic) LM (macrocystic, microcystic, mixed cystic)
  • Generalized lymphatic anomaly (GLA) (kaposiform lymphangiomatosis [KLA])
  • LM in Gorham-Stout disease
  • Channel-type LM
  • "Acquired" progressive lymphatic anomaly (acquired progressive "lymphangioma")
  • Primary lymphedema
  • Others

Venous malformation (VM)

  • Common VM
  • Familial VM cutaneomucosal (VMCM)
  • Blue rubber bleb nevus (Bean) syndrome VM
  • Glomuvenous malformation (GVM)
  • Cerebral cavernous malformation (CCM)
  • Familial intraosseous vascular malformation (VMOS)
  • Verrucous venous malformation (formerly verrucous hemangioma)
  • Others

Arteriovenous malformation (AVM)

  • Sporadic
  • In HHT
  • In CM-AVM
  • Others

Arteriovenous fistula (AVF) (congenital)

  • Sporadic
  • In HHT
  • In CM-AVM
  • Others

Locally aggressive or borderline vascular tumors

Kaposiform hemangioendothelioma

Retiform hemangioendothelioma

Papillary intralymphatic angioendothelioma (PILA), Dabska tumor

Composite hemangioendothelioma

Pseudomyogenic hemangioendothelioma

Polymorphous hemangioendothelioma

Hemangioendothelioma not otherwise specified

Kaposi sarcoma

Others

Combined vascular malformations

CM + VM = CVM

CM + LM = CLM

CM + AVM = CAVM

LM + VM = LVM

CM + LM + VM = CLVM

CM + LM + AVM = CLAVM

CM + VM + AVM = CVAVM

CM + LM + VM + AVM = CLVAVM

Malignant vascular tumors

Angiosarcoma

Epithelioid hemangioendothelioma

Others

Anomalies of major named vessels (channel-type or truncal vascular malformations)

Affecting

  • Lymphatics
  • Veins
  • Arteries

Anomalies of

  • Origin
  • Course
  • Number
  • Length
  • Diameter
  • Valves
  • Communication (AVF)
  • Persistence (of embryonal vessel)
 

Vascular malformations associated with other anomalies

Klippel-Trenaunay syndrome

Parkes Weber syndrome

Servelle-Martorell syndrome

Sturge-Weber syndrome

Limb CM + congenital nonprogressive limb overgrowth

Maffucci syndrome

Macrocephaly-CM

Microcephaly-CM

CLOVES syndrome

Proteus syndrome

Bannayan-Riley-Ruvalcaba syndrome

CLAPO syndrome

C=capillary, V=venous, L=lymphatic, A=arterial, M=malformation, F=fistula.  

A few vascular anomalies remain provisionally unclassified.[9]  Additional information is available on the ISSVA Web site.

Pathophysiology

The pathogenesis of AVMs is not well understood[10, 11] but is thought to involve abnormal vasculogenesis. Multiple biologic studies since 1982 have demonstrated clear differences between vascular tumors (hemangiomas) and vascular malformations. Some have hypothesized that infantile hemangiomas result from excess angiogenesis, whereas vascular malformations are due to errors in vessel remodeling.[12] Although some vascular malformations thicken, expand, or multiply with time, whether true angiogenesis occurs is unclear.

Marler et al suggested that vascular malformations may be angiogenesis-dependent disorders. They found that urinary high-molecular-weight matrix metalloproteinases (hMW MMPs) and basic fibroblast growth factor (bFGF) levels are elevated in vascular tumors and some vascular malformations (eg, lymphatic malformations [LMs], lymphaticovenous malformations [LVMs], and AVMs) and that the urinary increase in these proteins parallels the tissue remodeling seen in diffuse and expanding vascular malformations.[13] They suggested that drugs targeting bFGF or MMPs may be an adequate therapeutic strategy for patients suffering from these vascular anomalies.

Inherited forms of vascular malformations are rare[5] but may offer insight into the molecular mechanisms and signaling pathways involved in the pathogenesis of these lesions. This may in turn identify potential novel therapeutic targets, though at present, it is unclear whether the more common sporadic vascular malformations share similar biologic mechanisms with the infrequent inherited vascular malformations.

An AVM is a hemodynamically active fast-flow vascular malformation. Arterial feeders and enlarged draining veins directly connect through micro- and macroarteriovenous fistulas that create the nidus or epicenter of the AVM. AVMs may occur both superficially and viscerally. They are usually present at birth and rarely regress.[5] They have a normal endothelial cell cycle and grow commensurately with the child.[3, 1]

The natural history of AVMs is organized into a clinical staging system proposed by Schobinger at the 1990 ISSVA meeting in Amsterdam (see Table 2 below).[14]

Table 2. Schobinger Staging for AVMs (Open Table in a new window)

Stage

Description

I - Quiescence

Pink-bluish stain, warmth, and arteriovenous shunting are revealed by Doppler scanning. The arteriovenous malformation mimics a capillary malformation or involuting hemangioma.

II - Expansion

The description is the same as stage I, plus enlargement, pulsations, thrill, and bruit and tortuous/tense veins.

III - Destruction

The description is the same as stage II, plus dystrophic skin changes, ulceration, bleeding, persistent pain, or tissue necrosis. Bony lytic lesions may occur.

IV - Decompensation

The description is the same as stage III, plus congestive cardiac failure with increased cardiac output and left ventricle hypertrophy.

Epidemiology

Although vascular anomalies are among the most common pediatric abnormalities, occurring in approximately 1% of children,[15] AVMs are rare.[5]

Most AVMs are evident at birth (40% in a study of 200 AVMs by Enjolras et al),[16] though they may not be clinically relevant. Mulliken and Glowacki noted that 90% of vascular malformations were present at birth in a series of 23 patients; however, these lesions were predominantly venous in type and may not be representative of AVMs per se.[3]

The female-to-male ratio for vascular malformations is 1:1.[3, 16]

Prognosis

AVMs never regress and usually follow the stages outlined by Schobinger (see Pathophysiology). Morbidity and mortality are dependent on several factors, as follows:

  • Location and size of the AVM
  • Whether the AVM is surgically accessible or amenable to palliative embolization/sclerotherapy
  • Presence or absence of congestive heart failure

The prognosis is excellent when AVMs are managed by an interdisciplinary team, and the best success is achieved in surgically accessible lesions treated with combined embolization and complete surgical resection. (See the image below.)

Panel A: 12-year-old female with right facial arte Panel A: 12-year-old female with right facial arteriovenous malformation (AVM) s/p sclerotherapy. Panel B: 12.5-year-old female 4 months after resection of right facial AVM with preoperative embolization, complex closure, and lip reconstruction with rotational advancement flaps. Panel C: 13-year-old female with good recovery and no residual palpable or pulsatile AVM. Panel D: 14-year-old female with regrowth of AVM after the onset of puberty.
 

Presentation

History

Arteriovenous malformations (AVMs) are commonly misdiagnosed in infancy and childhood as an involuting hemangioma or capillary malformation because the lesion is not yet fast-flow, warm, or pulsatile.[10] They may become more clinically evident during the second or third decade of life.[17, 14] Enjolras et al observed a progression during childhood to grade II in 84% of patients.[16] Puberty (32%), pregnancy (25% adult women), or trauma (20%) can trigger expansion.[5, 16, 1, 10] These lesions grow proportionately with the child and never regress.

Physical Examination

The head and neck area is the most common location (70%) for AVMs, with a higher incidence of intracranial lesions than of extracranial lesions. Next in frequency are AVMs of the extremity, trunk, and viscera.[5, 1, 10]

When fully developed, AVMs deepen in color with increased erythema, and local warmth, a palpable thrill, and a bruit. Patients with facial AVMs of the skin or facial bones may present with facial asymmetry, gingival hypertrophy, unstable teeth, periodontal bleeding, or skin or mucosal ulcers with secondary infection. Nasal AVMs may cause epistaxis. Bony AVMs create osteolysis (3/200 in the series by Enjolras et al).[16]

Lower-limb skin changes resembling curious dry, brown-violaceous plaques may appear and are known histologically as pseudo-Kaposi sarcomas.[1, 10] Distal-extremity AVMs may lead to ischemia of the tips of fingers or toes associated with arterial steal and venous hypertension. (See the image below.)

Ischemic contractures secondary to a right hand ar Ischemic contractures secondary to a right hand arteriovenous malformation (AVM). Panel A: ventral. Panel B: dorsal. Panel C: excellent outcome after surgical resection/amputation.

Later consequences of expanding AVMs with arteriovenous shunting include ischemic changes, indolent ulceration, intractable pain, and sudden life-threatening hemorrhage or recurrent intermittent bleeding.[10] Increased cardiac output with subsequent congestive heart failure occurs in fewer than 2% of cases (5/200 in the series by Enjolras et al)[5] and usually in newborns with a massive AVM or in young adults with a large rapidly worsening AVMs in the limb or trunk.[1, 10]

Complications

Complications that may be apparent before embolization/sclerotherapy or surgical excision include the following:

  • Dystrophic skin changes
  • Ulceration
  • Tissue necrosis
  • Hemorrhage
  • Intractable pain
  • Congestive heart failure
 

DDx

 

Workup

Laboratory Studies

No laboratory tests reliably diagnose arteriovenous malformations (AVMs). Serum levels of vascular endothelial growth factor (VEGF) are significantly higher in proliferating hemangiomas than in involuting hemangiomas and vascular malformations.[18] In addition, urinary high-molecular-weight (hMW) matrix metalloproteinases (MMPs) are elevated in vascular tumors and some vascular malformations; however, they can not distinguish between the two types of vascular lesions.[13]

If a patient has spontaneous bleeding, perform a complete blood count (CBC), coagulation studies such as prothrombin time (PT) and partial thromboplastin time (PTT), a disseminated intravascular coagulation (DIC) panel, and a type and screen. This will allow a rapid diagnosis of anemia, coagulopathy, or DIC, if present, and will allow resuscitation with the appropriate intravenous fluids or blood products.

Imaging Studies

Clinical diagnosis is confirmed by means of ultrasonography (US) with color Doppler examination. Magnetic resonance imaging (MRI) is best for evaluating the extent of the AVM.

Plain radiography

Bony AVMs may demonstrate osteolysis.[5, 16]

Ultrasonography

US with color Doppler of an AVM usually demonstrates low-resistance high-velocity arterial flow above the baseline, with high diastolic flux, and pulsatile venous flow below the baseline. Vessels are tortuous. Arteriovenous shunting is seen. Pulsed Doppler measures the arterial output on the affected side compared with the normal side (eg, carotid, humeral, femoral arteries). This noninvasive technique is an excellent and reliable way to follow the course of an AVM or to monitor response to treatment.[5]

Computed tomography

Computed tomography (CT) does not easily distinguish between hemangiomas and vascular malformations. CT with iodinated contrast identifies AVMs as a highly enhancing lesion and can demonstrate soft-tissue involvement, as well as dilated feeding and draining vessels[5] .

CT angiography (CTA; see the image below) provides three-dimensional (3D) reconstruction of the AVM. Cone-beam CTA (also referred to as rotational angiography) appears to be promising in the treatment of AVMs, both for facilitating preoperative surgical planning and for providing an intraoperative reference.[19, 20]

CT Angiogram of a pulmonary arteriovenous malforma CT Angiogram of a pulmonary arteriovenous malformation (AVM).

Magnetic resonance imaging

MRI of an AVM (see the image below) demonstrates a collection of vascular flow voids (black tubular structures) corresponding to fast-flow vessels, in all sequences (spin-echo T1- and T2-weighted sequences). No contrast parenchymal enhancement (no tumor aspect) exists. If signal abnormalities are present, they may exist in relation to a fibrofatty matrix.[21, 22] Magnetic resonance angiography (MRA) also provides a 3D reconstruction of the AVM and its anomalous vascular network.[5]

MRI of a rectal arteriovenous malformation (AVM). MRI of a rectal arteriovenous malformation (AVM). Panel A: Axial, intraperitoneal rectum. Panel B: Axial, extraperitoneal rectum. Panel C: Coronal, posterior to lumbosacral prominence.

Angiography

Angiography (see the image below) is not solely diagnostic but can be therapeutic with embolization. Angiography demonstrates variably dilated or tortuous feeding arteries, arterial venous shunting (occasionally with visualization of discrete fistulae), and dilated draining veins. Feeding arteries may be aneurysmal in older patients.[10]

Angiogram of a rectal arteriovenous malformation ( Angiogram of a rectal arteriovenous malformation (AVM). Panel A: arterial phase. Panel B: venous phase.

Proximal embolization of feeding vessels is contraindicated and should never be performed. After a period of improvement, a vascular recruitment phenomenon occurs with rapid recruitment of flow from nearby arteries, which allows new collaterals to supply the nidus. This allows the lesions to recur and progress. In addition, proximal arterial embolization denies access for subsequent embolization.[5, 1, 10]

Angiography typically precedes interventional therapy or surgical resection. Patients with AVMs that are unresectable may undergo palliative superselective arterial or retrograde venous embolization for control of pain, hemorrhage, or congestive heart failure. Typically, palliative embolization provides only transient improvement. Resectable AVMs may be surgically removed 24-72 hours after arterial embolization for temporary nidus occlusion. Embolization can be with coils or glue.[10]

Sclerotherapy is another radiologic option that uses angiography and involves the injection of ethanol into the nidus. The risk of soft-tissue and neurologic damage is high; therefore, this technique should be performed only by an experienced endovascular specialist in carefully selected patients.[1] Although preoperative embolization or sclerotherapy may minimize intraoperative bleeding, these techniques do not reduce the limits of resection.

Histologic Findings

Vascular malformations are composed of vascular channels lined by flat “mature” epithelium and are not hypercellular, in contrast to hemangiomas. The endothelium is not proliferative. AVMs have predominately arterial and venous anomalous channels.[3]

 

Treatment

Nonoperative Therapy

The mainstays of management of vascular malfomations are not medical; rather, they involve interventional radiology procedures and surgery (eg, embolization, sclerotherapy, surgical resection, and reconstruction).[5, 1, 10, 23, 24]

Embolization/sclerosing agents

Absolute to 80% ethanol, N-butyl cyanoacrylate (NBCA) glue, various types of coils, and/or contour particles such as Ivalon (First Aid bandage Company, New London, CT) can be used in various combinations, simultaneously or in stages, as primary or adjunctive embolization/sclerosing agents, depending upon the location, severity, and extent of an arteriovenous malformation (AVM).

Ethanol is usually contraindicated and NBCA relatively contraindicated for high-flow fistulous lesions because of the high risk of early wash into the systemic circulation. These fistulous AVMs can generally be treated through a staged approach. Coil embolization is used as a preliminary procedure to slow down the flow, resulting in decreased risk of subsequent distal thromboembolism. Then, agents such as ethanol or NBCA glue can be used to definitively treat the lesion.

Absolute to 80% ethanol can be given via transarterial, transvenous, or direct puncture injection. Ethanol injection has a high complication rate but results in the fewest recurrences when used as a primary treatment for surgically inaccessible lesions. Major complications include deep vein thrombosis, transient nerve palsy, and ear cartilage necrosis. Minor complications are mainly skin changes.[25]

NBCA glue is predominantly used for surgically excisable lesions as preoperative embolization therapy to reduce blood loss intraoperatively. It is not typically used as a permanent sclerosing agent, because convincing evidence that it induces permanent damage to endothelial cells is lacking. Pulmonary embolism is rare but can occur.[25]

Surgical Therapy

Treatment is rare during infancy and early childhood for stage I AVM. Stage I AVMs can be followed with yearly examinations. Infrequently and after careful consideration, resection may be performed for a well-localized quiescent stage I AVM (ie, when complete resection is possible without poor cosmesis; however, this remains controversial).

Usually, invasive treatment is delayed until local endangering signs (stage III) are present or cardiac complications (stage IV) develop. In the uncommon occurrence of congestive heart failure caused by an AVM, prompt embolization may be necessary.

As mentioned previously, proximal embolization of feeding arterial vessels should never be performed, because this leads to rapid recruitment of new vessels from adjacent arteries to supply the nidus, with growth and progression of the lesion. Similarly, partial surgical excision leads to only temporary improvement, followed by reexpansion of the AVM over time.

Management of AVMs is challenging because selecting the optimal therapy to minimize recurrence is often difficult. Sometimes, complete resection is not possible or would result in severe disfigurement, as in the case of diffuse or infiltrating AVMs that invade pelvic tissues, permeate deep craniofacial structures, or penetrate all tissue planes of an extremity. In these cases, embolization or sclerotherapy is indicated and may be successful.

Generally, the treatment of AVMs is either palliative to control a complication (intractable pain, skin ulceration, tissue necrosis, bleeding, or lytic bone lesion with risk of fracture) or aims to be curative (embolization followed by wide surgical resection and reconstruction).[5, 1]  Indications for surgery are listed in Table 3 below.

Table 3. Indications for Surgical Treatment of AVMs (Open Table in a new window)

Absolute Indications

Relative Indications

Hemorrhage

Ischemia (arterial insufficiency or ulceration, gangrene)

Chronic venous insufficiency with venous hypertension

Lesions that compromise breathing, vision, hearing, or eating

High-output cardiac failure

Poor quality of life (disabling or intractable pain, functional impairment, severe cosmetic deformity)

Lesions with potentially high risk of complications (eg, hemarthrosis, fracture, or limb-threatening location)

Vascular-bone syndrome with limb length discrepancy

Table modified from Lee et al.[25]

Preoperative surgical planning should involve a thorough review of results from magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), or angiography. Surgical resection is usually preceded by arterial embolization for temporary nidus occlusion. This minimizes intraoperative bleeding but does not reduce the limits of the planned resection. Both the AVM nidus and the involved skin must be excised widely, though if the overlying skin appears normal, it can be saved. (See the image below.)

Left thigh arteriovenous malformation (AVM). Panel Left thigh arteriovenous malformation (AVM). Panel A: intraoperative. Panel B: bisected.

To minimize recurrence, the goal of surgery for an AVM is complete resection, in contrast to the staged resection applicable to slow-flow vascular malformations. The best wound coverage is primary closure with local or distant tissue flaps. Amputation is a viable option for the ischemic or nonfunctional extremity. Combined embolization and surgical resection is most successful for well-localized stage I/II AVMs. However, these patients must still be followed for years.

In one series, all 16 patients with surgically accessible, localized, noninfiltrating AVMs who underwent preoperative angioembolization with subsequent surgical excision demonstrated no evidence of recurrence on angiography during a follow-up averaging 24.3 months.[25]

A computed tomography (CT)-guided frameless robotic radiosurgical approach to intracranial AVMs has been described. Early results reported by Oermann et al in a retrospective study of 26 patients (median age, 41 years) at a median of 25 months' follow-up suggest that this approach can yield results comparable to those of frame-based methods.[26]

Surgical risk has commonly been determined by using the AVM grading system proposed by Spetzler and Martin.[27]  In this system, AVMs were graded from I through V by adding up the numerical values for the following three variables:

  • Size of nidus - Small (< 3 cm), 1; medium (3-6 cm), 2; large (>6 cm), 3
  • Eloquence of adjacent brain - Noneloquent, 0; eloquent, 1
  • Venous drainage - Superficial only, 0; deep, 1

Grade VI lesions are essentially unresectable. Lawton et al described a supplement to the Spetzler-Martin system that added up to five additional points for three more variables: age, unruptured presentation, and diffuseness.[28]

In 2011, Spetzler and Ponce simplified the original Spetzler-Martin grading into a three-tier system, by which grades I and II were combined into class A, grade III became class B, and grades IV and V were combined into class C.[29]

Complications

Complications that may occur after embolization/sclerotherapy or surgical excision include the following:

  • Expansion
  • Recurrence
  • Poor cosmesis, disfigurement

Diet

No special diet is required or recommended.

Activity

Activity is not limited unless the patient is undergoing an interventional or surgical procedure.

Prevention

 

 

Long-Term Monitoring

As mentioned previously, the management of vascular anomalies requires interdisciplinary care and collaboration between many specialities. Specific consultations depend on the type of vascular anomaly and its location. With regard to AVMs in particular, possible consultations include the following:

  • Pediatric or general surgery
  • Plastic surgery
  • Vascular surgery
  • Neurosurgery
  • Otolaryngology
  • Orthopedic surgery
  • Radiology
  • Interventional radiology
  • Hematology
  • Gastroenterology
  • Physical therapy
  • Occupational therapy
  • Speech therapy

Medical Care

The chance of recurrence after surgical resection of an AVM is high, and experienced surgeons recognize that long-term follow-up is critical to ensure a cure.[5, 1]  Accordingly, patients must be followed for years with regular physical examination, ultrasonography (US), MRI, or some combination thereof.

Surgical Care