Dural Arteriovenous Fistula in Children: Endovascular Treatment and Outcomes in Seven Cases

Dural AVF are uncommon vascular malformations that are rare in the pediatric population (1, 2). They may be a cause of life-threatening congestive heart failure in neonates. Expeditious diagnosis and treatment may be life saving in this setting. Older children with dural AVF tend to present with neurologic problems related to intracranial venous hypertension. For these children, prompt therapy is critical to prevent irreversible brain injury (1).

Endovascular embolization is currently the leading treatment option for dural AVF. Embolization of dural AVF achieves short-term palliation at least and may be curative at best. We report a series of seven children with dural AVF, describe their treatment using endovascular embolization techniques, and report their outcomes. In addition, we review the clinical and radiologic findings associated with this unusual and interesting disease.

Methods

Seven children had undergone endovascular treatment for simple or complex dural AVF at our institution since 1987. A retrospective analysis of these cases included review of the patients' charts and all available imaging studies, including transcranial sonography, MR imaging, CT, and angiography. Telephone interviews were conducted to obtain current follow-up information regarding patients who had not been recently seen.

Clinical information and imaging findings are summarized in Table 1. Treatment and outcomes are summarized in Table 2.

All patients were treated by embolization via transarterial, transvenous, or direct venous puncture approaches. Direct puncture techniques were used after neurosurgical exposure of the involved sinus and were usually used when the fistula nidus was inaccessible by conventional transarterial approaches or when such an approach would entail unacceptable risk for untoward embolization of the normal tissue. Embolization materials included fibered platinum microcoils, Guglielmi detachable coils, N-butylcyanoacrylate, polyvinyl alcohol particles, detachable balloons, and silk suture. Guglielmi detachable coils were used instead of fibered coils in specific circumstances. First, when the flow rate was high and there was a concern that the coil would migrate, the pre-detachment control led us to use Guglielmi detachable coils. Second, when using 0.010-in systems, the size options for fibered coils was limited and Guglielmi detachable coils were therefore used.

Our approach to the treatment of these lesions has evolved over the years as the materials have improved, and the long-term results of limited treatment have become evident. Because those patients with significant residual fistulae tended to do poorly (see Results), we have become more aggressive early in the course of the disease. Also, with modern materials, direct puncture access is usually no longer necessary because we are usually able to get sufficiently distal, via either the transarterial or transvenous route, to allow embolization. Our goal during the acute period is related to the presentation and status of the patient's condition. In those patients with congestive heart failure, a reduction of the flow sufficient for survival and growth is performed, with later attempts at cure (usually at 3–6 months of age) if this is not achieved at the time of the first embolization. However, if the brain continues to use the involved sinus as a major outlet, close follow-up is conducted and repeat embolization via a transarterial approach is attempted to prevent delayed brain injury. In those patients presenting later in the disease process, aggressive transarterial embolization is recommended because the onset of seizures and neurologic deficit indicates ongoing brain injury. It is possible, in some cases, to occlude the sinuses when rerouting of venous outflow has occurred. However, this is generally a late finding at which time brain injury has already occurred.

Our current materials of choice are fibered coils of sufficient size or with a detachment mechanism to prevent migration when embolizing from a transvenous approach. N-butyl cyanoacrylate is the agent of choice in transarterial approaches and in transvenous embolization after a sufficient nest of coils is placed to prevent untoward pulmonary embolization.

However, more important than any technique is that the family needs to know the severity of the disease process and why this leads to an aggressive treatment approach.

Results

Initial Imaging Findings

For the neonates, radiographs of the chest revealed cardiomegaly, pulmonary vascular congestion, and edema, consistent with their presentations with congestive heart failure. The initial CT scans obtained of these newborns showed enlargement of the involved venous sinuses but normal-appearing brain parenchyma. This contrasts with the initial imaging findings of some of the older children who, at the time of referral, had already developed hydrocephalus and evidence of brain ischemia. The evidence of parenchymal ischemic change included MR changes such as white matter thinning and T2 hyperintensity and CT findings of white matter hypodensity and dystrophic calcification (Fig 1). Patient 6, a 4-year-old child at the time of referral who had a very small dural AVF coupled with a large orbital vascular malformation, had no hydrocephalus or ischemic change revealed by the initial imaging. Also seen on the MR images was prolapse of the cerebellar tonsils through the foramen magnum in two patients (patients 4 and 7) (Fig 1) and large, increased flow voids in the involved venous sinuses.

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fig 1.

Patient 7 was a 10-year-old girl with a complex, multifocal dural AVF (infantile type dural arteriovenous shunt), who presented late with advanced neurologic symptoms.

A, Axial view contrast-enhanced CT scan obtained at the time of referral shows dystrophic calcification in the brain parenchyma, hydrocephalus, thinning of white matter that is abnormally hypodense, and enlarged right sphenoparietal and superior sagittal sinuses. This patient had already developed irreversible brain injury related to her dural AVF.

B, Sagittal view T1-weighted MR image shows a significantly enlarged flow void in the superior sagittal sinus and torcular herophili, some of the sites of arteriovenous shunting in this patient. Also note the prolapse of the cerebellar tonsils at the craniocervical junction, the so-called acquired Chiari I malformation that can also be seen with the vein of Galen malformation.

The original angiograms documented the dural AVF in each patient. The arteries that were involved in most patients were the middle meningeal and occipital arteries (Fig 2). The first angiogram obtained of patient 5 (Fig 3) showed bilateral sigmoid sinus occlusions. No other patient had sinus occlusions revealed by initial angiography, although two patients acquired sinus stenoses later (patients 4 and 7).

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fig 2.

Patient 1 was a newborn with severe congestive heart failure.

A, Anteroposterior view angiogram of the right external carotid artery shows a large left transverse and sigmoid sinus dural AVF (dural sinus malformation) supplied by enlarged right occipital artery branches, subsequently embolized using coils and N-butylcyanoacrylate. Note the coil mass already present in the left transverse sinus that was placed via direct puncture at an outside institution at 1 day of age.

B, Anteroposterior view shows left common carotid artery injection, venous phase, with prominent venous collateral channels draining to the right transverse sinus.

C, Lateral view shows left external carotid artery injection before embolization. The large left transverse and sigmoid sinus dural AVF is supplied by a markedly enlarged left middle meningeal artery that arises from the left ophthalmic artery. There is abnormal enlargement of the artery of the foramen rotundum (arrowhead) that supplies an enlarged middle meningeal artery (large arrows). The middle meningeal artery has a variant origin from the ophthalmic artery (small arrows).

D, Lateral view shows left common carotid artery injection after embolization. After complete embolization using microcoils and N-butylcyanoacrylate, there is stagnation of flow in the stump of the middle meningeal artery (open arrow), no evidence of arteriovenous shunting, and good filling of the normal intracranial circulation.

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fig 3.

Patient 5, with a dural sinus malformation, was an 18-month-old who presented with seizures and prominent facial veins.

A, Anteroposterior view angiogram of the right external carotid artery, venous phase, shows bilateral sigmoid sinus occlusions and an enlarged occipital vein. The arterial phase (not shown) showed enlarged right occipital artery feeders to a large right transverse sinus dural fistula.

B, Lateral view angiogram of the right common carotid artery, obtained after complete embolization of the dural AVF, shows development of collateral venous drainage, ultimately draining through the superior ophthalmic veins (arrow), which is seen to be markedly dilated.

Discussion

There are few case reports of intracranial dural AVF occurring in the pediatric population. The two largest reported series to date were 11 cases reported by Garcia-Monaco et al (3), only four of which were described in detail because of their unusual complexity, and 29 cases described by Lasjaunias et al (1), which probably included some cases from the other series. In addition to those 29 cases, there are only 20 others reported in the literature (4–17). Dural AVF account for approximately 10% of all intracranial arteriovenous shunts in children, lower than the 10% to 20% estimated for adults (3, 18, 19). When occurring in children, dural AVF have a greater incidence of multifocality and tend to have a more aggressive clinical course (eg, congestive heart failure, hypertensive venopathy, hydrocephalus) (1, 20). In this series of children with dural AVF, we also observed greater complexity and multiplicity than is usually seen in cases of adult dural AVF.

Dural AVF are direct arteriovenous connections with the dura itself, with drainage into dural sinuses or cortical veins. Meningeal and pial vessels can contribute to the fistula. Pathologically, the malformation consists of a network of arteriovenous microfistulae in the wall of a dural sinus (19–21). The most common locations of dural AVF are the sigmoid-transverse, cavernous, and superior sagittal sinuses (22). Those affecting the occipital-suboccipital region are reported to account for 50% of all dural AVF (2).

The arterial supply and venous drainage observed in this series of pediatric dural AVF are similar to those reported in the literature. The transverse-sigmoid, superior sagittal sinus, and torcular herophili were the most commonly involved fistula sites. In addition, either the middle meningeal or occipital arteries or both initially supplied all the malformations. After transarterial embolization of these main arterial feeders, follow-up angiography frequently revealed interval recruitment of smaller arterial feeders by the dural AVF. This secondary development of new shunts in the region of a partially treated dural AVF has been well described in the literature (3, 4, 21). The new shunts can be dural, pial, or both. Explanations that have been proposed for the development of these secondary shunts include abnormal angiogenetic activity and/or a venous “sump” effect related to the dural AVF (1, 3, 21).

In the adult patient, dural AVF is generally accepted as being an acquired disorder. Because of the increased incidence of concomitant venous sinus thrombosis with dural AVF, many authors have ascribed sinus thrombosis a pathogenetic role in the formation of these vascular malformations (22–26). Adults with dural AVF frequently have etiologic risk factors for venous sinus thrombosis, including head trauma, neurologic surgery, and ear or sinus infection (24, 25). That some patients with dural AVF have no evidence of previous sinus thrombosis and that a venous thrombosis can be acquired from a dural AVF add further confusion regarding the pathogenesis of these malformations (26). Lasjaunias et al (1) proposed that a primary structural weakness of the dura coincided with a trigger factor, resulting in the formation of a dural AVF. Congenital causes have also been theorized, but several observations have been made regarding dural AVF in infants and children that oppose a true congenital (embryologic) cause (27). First, dural AVF have not been shown to be familial or associated with other vascular malformations. Second, in several pediatric cases of dural AVF, Garcia-Monaco et al (3) observed the presence of mature arterial and venous configurations and the absence of persistent embryonic vascular patterns. They therefore theorized that dural AVF in children develop after the third month of intrauterine life and may be considered acquired, although the acquisition may occur prenatally. Still, the exact intrauterine events leading to the development of these lesions remain unknown, and a multifactorial process is likely.

Clinical manifestations vary by age, location of fistula, and severity of arteriovenous shunting. Lasjaunias et al (1) describe three types. First is the dural sinus malformation, which typically occurs in neonates. Second is the infantile type dural arteriovenous shunt, which occurs in children. Third is the adult type dural arteriovenous shunt, which is less frequent but also occurs in children. The neonates with dural AVF, in whom direct arteriovenous shunting is severe at birth, tend to present immediately with congestive heart failure as a result of the increased venous return and volume overload. The babies also usually have an objective cranial bruit. We observed this presentation in patients 1, 2, and 3. These three patients and patient 5 correspond to the dural sinus malformation classification presented by Lasjaunias et al. The leading clinical differential consideration in cases such as these is a vein of Galen malformation. This diagnosis can be excluded by imaging findings of a normal sized vein of Galen and straight sinus. The lesion often affects the torcular herophili or lateral sinus. If the lesion involves the lateral sinus, a direct transvenous approach can be curative with preservation on normal brain venous outflow through the torcular herophili and contralateral sinus. If the torcular herophili is involved, the sinus can be taken only when venous rerouting has occurred (as in patient 5).

In general, we found that the degree of arteriovenous shunting was less severe in the older children. If their dural AVF were present at the time of birth, either their hearts compensated for the lesser arteriovenous shunting or venous outflow restriction allowed the fistula to remain clinically silent until cerebral venous hypertension became symptomatic. Cerebral venous hypertension, due to direct arteriovenous shunting, may cause venous ischemia or infarction, hemorrhage, and/or problems with CSF dynamics. When the pressure within the superior sagittal sinus approximates or exceeds the pressure in the subarachnoid space, there is resultant failure of resorption CSF, thus producing an imbalance in brain water or volume and ventricular size (3). We also found that a later presentation was more variable by location of the dural AVF. As in adults, the children with dural AVF involving the cavernous sinus region presented with proptosis and chemosis (patients 6 and 7). Of interest is that older children with dural AVF often have objective but non-subjective cranial bruits, which suggests that the noise was always present in the natural acoustic environment of the child and was thus probably present at birth (3, 4).

The radiologic findings of these children also tended to vary by patient age. The brains of the newborns were essentially normal, except for the enlarged venous structures related to the dural AVF. With such an early presentation, no radiographic or clinical brain injury had yet occurred. We found that the longer the dural AVF remained undiagnosed and cerebral venous hypertension went unchecked, the more irreversible was the brain injury. Ischemic brain injury was evidenced by dystrophic calcification in the brain parenchyma (Fig 1) and white matter abnormalities, such as thinning and abnormal density or intensity.

Another imaging finding of these children, previously described in conjunction with vein of Galen malformation, is cerebellar tonsillar prolapse (Fig 1). This tonsillar prolapse has been shown to be reversible after endovascular treatment and is thought to be a result of hydrovenous dysfunction of the posterior fossa (28).

A frequent angiographic finding that has been reported in association with dural AVF is venous sinus occlusion and/or stenosis (22, 23, 26, 28). It is often not possible to determine whether the venous sinus occlusion/stenosis preceded the development of the dural AVF, possibly playing an etiopathogenic role, or was caused by the dural AVF. In addition, the combination of intracranial hypertensive venopathy and arterialized, turbulent blood flow can also lead to progressive veno-occlusive disease in the cortical veins and dural sinuses by an as yet undefined mechanism (29, 30). In this series, bilateral sigmoid sinus occlusion was observed on the initial angiogram in one patient and two other patients acquired sinus stenoses during staged embolization treatment.

Endovascular treatment of dural AVF is now widely considered the first primary method of therapy. Appropriate medical management with inotropic agents and diuretics is also vital at the onset of cardiac manifestations (31). Surgical resection after partial embolization may be successful in small dural AVF, as in patient 6 (classified as adult type dural arteriovenous shunt). Surgical treatment without previous embolization carries a risk of significant operative blood loss, which is a particular concern in infants (4). Radiation therapy has been used in adults with localized slow flow dural lesions but is not an appropriate treatment in infants or children with extensive dural AVF (32).

Endovascular therapy should be targeted to the specific area of shunting that is thought to be most responsible for the individual patient's symptoms. In infants with cardiac decompensation, the area of highest arteriovenous shunting should be embolized first (Fig 2). As with all such procedures, embolization at the nidus of the lesion is critical if cure is to be achieved. Proximal embolization, although possibly resulting in transient symptomatic improvement, is associated with a high rate of recurrence and may serve to isolate the involved sinus so as to make further transvascular treatment attempts difficult or impossible. Because of the recruitment of secondary shunts at the fistula nidus, it has been our experience that cure can be achieved only after complete occlusion of the involved venous sinus. This is most easily done in cases of dural AVF that are relatively simple and involve single sinuses or short segments of larger sinuses; in such cases in this series, embolization was most successful. Our typical treatment approach began with transarterial embolization of the main arterial feeders with a permanent agent such as N-butylcyanoacrylate. If necessary, transvenous packing of the involved sinus was then performed to accomplish complete sinus occlusion.

Multifocal dural shunts (infantile type dural arteriovenous shunts) that involve nearly all the major dural venous sinuses, as in patients 4 and 7, cannot be immediately cured by current embolization techniques because complete occlusion of all the involved venous sinuses would result in severe venous outflow problems. When a major dural sinus becomes occluded, the cerebral venous drainage must reroute, which is usually accomplished without difficulty in the setting of a single area of dural sinus occlusion. If multiple major venous sinuses are occluded, the venous outflow typically becomes redirected through cortical veins or deep venous sinuses. It is in this setting that collateral venous drainage may prove inadequate, resulting in dangerous cerebral venous hypertension. Therefore, in patients with complex, multifocal dural AVF, endovascular treatment is generally aimed at symptomatic relief. However, patient 4 developed sinus thrombosis after repeated arterial embolizations resulted in cure.

If the cerebral venous drainage successfully reroutes through adequate venous collaterals, cure may be achieved after complete occlusion of the involved venous sinuses. We observed this phenomenon in patient 5 (Fig 3). When this patient was referred to us at 18 months of age, his initial angiogram showed bilateral sigmoid sinus occlusions and the presence of collateral venous drainage pathways eventually draining through the superior ophthalmic veins. It was the presence of these important venous collaterals that proved crucial to his favorable outcome after complete embolization of most of the posterior venous sinuses.

Conclusion

Pediatric dural AVF are more often multiple and are usually more complex than adult dural AVF. Early, aggressive treatment is critical to prevent long-standing cerebral venous hypertension and resultant irreversible brain injury. Endovascular embolization is currently the best treatment option for dural AVF and may be life saving in the setting of neonatal congestive heart failure. Embolization strategies must be individualized to the patient's presenting symptoms. Depending on the complexity of the fistula, treatment may be either palliative or curative, but in our experience, cure can be achieved only after total occlusion of the involved sinus.