A deceptive mass on neonatal ultrasound and a fetal brain MRI-confirmed complex dural arteriovenous fistula postnatally: illustrative case

Elliot T. Varney Departments of Radiology and

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Charlotte S. Taylor Departments of Radiology and

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Allen G. Crosthwait Departments of Radiology and

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Kristin Weaver Neurosurgery, University of Mississippi Medical Center, Jackson, Mississippi

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Todd Nichols Departments of Radiology and

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BACKGROUND

Dural arteriovenous fistulas (dAVFs) are direct, aberrant connections between dural arteries and cerebral veins. In neonates, delayed diagnosis results in grim outcomes. Treatment involves endovascular management because of its success and tolerability. Here, the authors present a case of a complex dAVF initially recognized with an in utero neurosonogram and fetal magnetic resonance imaging (MRI).

OBSERVATIONS

A 21-week fetal ultrasound of a nonspecific brain mass was confirmed with fetal MRI as a 2.7-cm T1-hyperintense posterior fossa mass. Although a large flow void in the left middle cranial fossa was present, postnatal computed tomography angiography ultimately revealed a high-flow dAVF communicating with the left transverse sinus. In the early postnatal period, the patient developed hydrocephalus. After successful partial embolization, 6-week postangiogram brain MRI indicated disease progression with the development of a venous varix causing brainstem compression. Repeat embolization resulted in complete cessation of early venous drainage.

LESSONS

Neonatal dAVFs are exceedingly rare and result in futile outcomes; however, detection in utero is possible. Although definitive therapy must be performed postnatally, constant monitoring and early delivery can prevent complications. Attention to fetal ultrasound is essential, and knowledge of fetal MRI in the detection of these complex lesions can significantly improve outcomes.

ABBREVIATIONS

AVM = arteriovenous malformation; CT = computed tomography; CTA = computed tomography angiography; dAVF = dural arteriovenous fistula; DSM = dural sinus malformation; MRI = magnetic resonance imaging

BACKGROUND

Dural arteriovenous fistulas (dAVFs) are direct, aberrant connections between dural arteries and cerebral veins. In neonates, delayed diagnosis results in grim outcomes. Treatment involves endovascular management because of its success and tolerability. Here, the authors present a case of a complex dAVF initially recognized with an in utero neurosonogram and fetal magnetic resonance imaging (MRI).

OBSERVATIONS

A 21-week fetal ultrasound of a nonspecific brain mass was confirmed with fetal MRI as a 2.7-cm T1-hyperintense posterior fossa mass. Although a large flow void in the left middle cranial fossa was present, postnatal computed tomography angiography ultimately revealed a high-flow dAVF communicating with the left transverse sinus. In the early postnatal period, the patient developed hydrocephalus. After successful partial embolization, 6-week postangiogram brain MRI indicated disease progression with the development of a venous varix causing brainstem compression. Repeat embolization resulted in complete cessation of early venous drainage.

LESSONS

Neonatal dAVFs are exceedingly rare and result in futile outcomes; however, detection in utero is possible. Although definitive therapy must be performed postnatally, constant monitoring and early delivery can prevent complications. Attention to fetal ultrasound is essential, and knowledge of fetal MRI in the detection of these complex lesions can significantly improve outcomes.

ABBREVIATIONS

AVM = arteriovenous malformation; CT = computed tomography; CTA = computed tomography angiography; dAVF = dural arteriovenous fistula; DSM = dural sinus malformation; MRI = magnetic resonance imaging

Dural arteriovenous fistulas (dAVFs) are defined as direct, aberrant connections between a dural artery and a cerebral vein and account for approximately 10% of all intracranial shunts in children.1,2 Although often confused with arteriovenous malformations (AVMs), dAVFs are distinct entities, given the characteristic lack of a plexiform nidus within AVMs. dAVFs are the most common cerebrovascular lesions at all ages, but they are rarely diagnosed in the neonatal period. Delayed diagnosis occurs due to symptoms and inciting events rarely manifesting before adulthood. However, when present in neonates, outcomes are usually grim due to the development of congestive heart failure, hypertension, and hydrocephalus.1,3–5 Treatment is multifaceted, and the exact treatment strategies for these entities are controversial. However, there is consensus on the utility of primary endovascular management due to its success and tolerability among patients.6–10

We present an unusual case of a complex dAVF initially recognized with an in utero neurosonogram and fetal magnetic resonance imaging (MRI). Here, we hope to show the utility of ultrasound, fetal and postnatal MRI, computed tomography (CT), and fluoroscopic imaging in the diagnosis and successful treatment of this rare manifestation of a relatively common pathology. This case highlights our experience with a prenatal infant with a complex dAVF turned dural venous malformation through a complicated postnatal course.

Illustrative Case

A 44-year-old G3P1011 female presented for a routine prenatal 21-week fetal ultrasound. She had a history of prior expectant abortion at 13 weeks for anencephaly and a prior child with translocation. An outside ultrasound finding of a nonspecific brain mass led to referral to our institution for specialty evaluation (Fig. 1). Fetal brain MRI was conducted and demonstrated a 2.7-cm T1 hyperintense extra-axial mass centered in the left posterior fossa, just inferior to the left occipital lobe (Fig. 2A). The mass was causing moderate mass effect with anterior displacement of the occipital lobe and inferior displacement of the tentorium without brainstem compression or significant hydrocephalus. In addition, a large flow void in the right middle cranial fossa directed to the T1-hyperintense mass was a clue to the possibility of a vascular malformation (Fig. 2B).

FIG. 1.
FIG. 1.

Prenatal neurosonogram performed at 21 weeks’ gestation. Transcerebellar view of the fetal brain shows a 1.9-cm hyperechoic mass (measured) in the posterior cranial fossa on the superior border of the cerebellum, posterior to the temporal lobes (arrows) and thalami (Th).

FIG. 2.
FIG. 2.

Follow-up fetal MRI upon transfer to a higher level of care. A: Sagittal T1-weighted MRI showed a heterogeneously T1-hyperintense mass (yellow arrowhead) in the posterior cranial fossa. B: Axial T2-weighted MRI showed a prominent flow void (red arrow) in the middle cranial fossa with direct connection to an enlarged left sigmoid and transverse sinuses (green arrowhead) posterior to the cerebellum (yellow) suggesting a dAVF. Temporal lobe is circled in orange. C: Sagittal T2-weighted MRI showed a heterogeneously hypointense mass (red arrowhead) centered in the posterior cranial fossa.

Follow-up targeted ultrasonography demonstrated good fetal movement, adequate amniotic fluid volume, and normal cardiac activity. Initially, the child was diagnosed with an extra-axial hematoma of unknown ethology, and plans were made for close monitoring and a scheduled birth at term.

The early-term infant was born via cesarean section at 37 weeks 6 days with Apgar scores of 8 and 9. The infant was transferred to the neonatal intensive care unit for further evaluation of the known “brain mass.” MRI from day of life 1 demonstrated previous findings but also indicated the possibility of a vascular malformation.

Computed tomography angiography (CTA) revealed a large, high-flow dAVF. Arterial supply primarily stemmed from the left middle meningeal artery, which communicated with the left transverse sinus. There were signs of arterialization of tortuous and dilated left sigmoid and transverse sinuses. In addition, there was concern for fistulous contribution from the right middle meningeal artery to the posterior third of the right superior sagittal sinus (Fig. 3). A subsequent CT venogram showed additional components of significant dilatation of the right transverse sinus, the straight sinus, the vein of Galen, and the left basal vein of Rosenthal. Importantly, there were also signs of thrombus within the left transverse/sigmoid sinus.

FIG. 3.
FIG. 3.

CTA of the head confirmed a prominent left middle meningeal artery (A and C; red arrows) with direct connection to the sigmoid and transverse sinuses. In addition, there was central nonopacification of the enlarged left transverse sinus (B; green arrow), suggesting a dural venous thrombus.

After the first few days of life, a clinical plan was made to closely monitor the child and delay definitive treatment until further growth or until clinical symptoms arose. At 3 months of age, the patient began to show clinical manifestations of the dAVF in the form of hydrocephalus and venous engorgement of the scalp veins. Other than limited extraocular movements, the patient had been doing well previously. Cerebral angiography with intent to treat was performed, given the development of clinical symptoms.

A bilateral common carotid angiogram confirmed the complexity of the dAVF with extensive arterial involvement, more extensive than previously believed. Arterial supply was seen arising from the left middle meningeal, left occipital, left tentorial, left posterior auricular, left superior cerebellar, left anterior inferior cerebellar, left posterior meningeal, right middle meningeal, and right occipital arteries (Fig. 4A). The primary venous drainage was via the left transverse sigmoid junction. After successful embolization of the left middle meningeal, left occipital, left posterior auricular, and right middle meningeal arteries, there was a significant decrease in blood flow through the fistulous connection.

FIG. 4.
FIG. 4.

A: Preembolization arteriograms, anteroposterior and lateral views, of the left external carotid artery (ECA), left vertebral artery, and right ECA show the complexity of the fistula/malformation with extensive arterial supply from the left middle meningeal, occipital, tentorial, posterior auricular, superior cerebellar, anterior inferior cerebellar, and posterior meningeal arteries with early venous filling in the left sigmoid sinus, transverse sinus, and torcula. Right middle meningeal and right occipital artery feeders were also confirmed with right ECA arteriogram, demonstrating early venous filling in the region of the torcula. B: Postembolization follow-up neonatal brain MRI. Axial T2-weighted (left) and sagittal T1-weighted (middle) MRI scans and coronal MRI venogram (MRV; right) show the development of moderate obstructing supratentorial hydrocephalus from a new heterogeneously T2-hypointense, T1-isointense mass (red arrows) confirmed by MRV to be a large obstructing varix from the residual fistula.

Six-week postangiography follow-up including brain MRI indicated persistent high flow in the fistula despite previous embolization. Although head circumference stabilized and scalp veins improved, there was interval development of a large venous varix in the region of the straight sinus and vein of Galen causing brainstem compression (Fig. 4B), and plans for repeat embolization via transvenous approach were made.

Successful embolization of the venous side of the fistula resulted in significant reduction in flow through the fistula with slight persistence of early venous drainage (Fig. 5A). Additional coil embolization within the venous varix just distal to the fistula resulted in cessation of flow within the fistula (Fig. 5B).

FIG. 5.
FIG. 5.

A: Pre–final embolization left vertebral artery arteriogram demonstrating the persistence of early venous filing within the left sigmoid sinus and early opacification of the large posterior midline-obstructing varix previously seen on MRI and MRI venogram. B: Post–final embolization arteriogram of the left vertebral artery after embolization on the venous side of the fistula and within the venous varix just distal to the fistula. There is complete cessation of flow within the fistula with no evidence of early venous filling.

At post-treatment follow-up, the patient had persistent hypertension, which was well controlled with low-dose oral medication. The patient was tolerating a regular oral diet, pain was controlled, and follow-up MRI showed stable ventriculomegaly. The patient was discharged home with plans for close short-term follow-up with MRI.

Discussion

Observations

dAVFs in the neonatal period are rare, and they present a unique challenge due to their propensity to form extensive collateralization. Lasjaunias et al.9 described three distinct types of dural arteriovenous shunts in children: (1) dural sinus malformations (DSMs), which are congenital malformed sinuses with malformations of the jugular bulb where sinus thrombosis or occlusion is the central clinical concern; (2) infantile-type dural arteriovenous shunts, which are high-flow, multifocal lesions with patent sinuses and induced pial arteriovenous shunts; and (3) adult-type dural arteriovenous shunts, which are high-flow lesions almost always secondary to a prior insult.

Vascular malformations have many etiologies; however, AVFs specifically can be idiopathic or secondary to prior insult, such as trauma, surgery, or infection.8,9 When occurring in children, dAVFs have a greater incidence of multifocality and tend to have a more aggressive clinical course.5 Mechanisms of formation have been proposed for congenital dAVFs, and many authors describe a pathogenetic role secondary to sinus thrombosis, suggesting that many are acquired.1,3,4,11–13

This case is unique in that it does not fit into one clear category defined by Lasjaunias et al.9 To our knowledge, there has not been a dural arteriovenous shunt of this kind reported in the literature. Although initial imaging work-up describes a dAVF, after an initial treatment angiogram, the shunt morphed/progressed into an acquired DSM with the development of a dural varix near the vein of Galen. This phenomenon of the recruitment of arterial feeders with secondary development of new shunts in a partially treated dAVF has been well described; however, the mechanism is poorly understood.2,5,14–16 In addition, infants usually experience the sequelae of shunt vasculature, including heart failure, heart murmur, and hydrocephalus, none of which were initially seen in this case.9,17–19

Most often, dAVFs present in early childhood or adulthood, and neonatal dAVFs are often overlooked. One theory behind the optimal outcome here is the detection in utero with prompt management in the postnatal period. Prenatal detection with ultrasound and fetal MRI served a vital role in the diagnosis and eventual management of this patient. Sonography with spectral Doppler serves as the optimal opportunistic screening modality because it can detect arteriovenous shunting and provides needed information to suggest the presence of a vascular malformation despite not having precise diagnostic ability.19–21 With the advancement of fetal MRI, detailed evaluation can be made to understand the complexity of the lesion, the integrity of the brain and surrounding structures, and the potential complications to expect before a postnatal angiogram. Precise diagnosis may also be achievable with fetal MRI, as seen in this case. CTA/venography is best used to evaluate precise vascular anatomy. This case demonstrates the benefits of the multimodality approach seen in this case as well as the utility of both fetal neurosonogram and fetal MRI for prenatal monitoring and obstetric management to optimize early postnatal management of suspected neonatal AVMs/AVFs.

Yet another consideration in neonatal cases of vascular malformations must be the potential complications associated with diagnostic and treatment fluoroscopic angiograms. Although advancements in angiographic techniques and radiation safety have made significant progress in reducing the risk of complications associated with fluoroscopic angiography, knowledge of these risks (i.e., stroke, arterial injury, and complications from anesthesia) is important before treatment. Most known risk factors influencing neurological complications during cerebral angiography include long procedures (>60 minutes), use of large-volume contrast agents, increased serum creatinine levels, symptomatic atheromatous disease, and the use of three or more catheters, most if not all of which are not usually encountered in the pediatric population.22 It is well documented that cerebral angiography is indeed a safe procedure for neonates and infants in the setting of vascular malformations with neurological complication rates from iatrogenic embolization reaching up to only 0.4% and nonneurological or radiographic complications ranging from 0.0% to 4.5%.23,24

Lessons

Neonatal dAVFs are exceedingly rare entities that often result in futile outcomes; however, detection in utero is possible with the use of advanced imaging techniques such as fetal MRI. Although definitive therapy cannot be performed until the postnatal stages, constant monitoring and potentially early delivery may be needed to prevent these fatal complications. This case demonstrates the necessity of attention to fetal ultrasound and knowledge of fetal MRI in the detection of these complex lesions, because they can continue to morph into complex malformations and can result in devastating systemic effects early in life. Prompt detection and diagnosis leads to proper obstetric and early postnatal management to optimize the outcome of future cases with similar characteristics.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Varney, Taylor, Crosthwait, Nichols. Acquisition of data: Varney, Taylor, Crosthwait. Analysis and interpretation of data: Varney, Taylor, Crosthwait. Drafting the article: Varney, Taylor, Crosthwait. Critically revising the article: Varney, Taylor, Crosthwait, Weaver, Nichols. Reviewed submitted version of manuscript: Varney, Taylor, Crosthwait, Weaver. Approved the final version of the manuscript on behalf of all authors: Varney.

References

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    • Crossref
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    Kincaid PK, Duckwiler GR, Gobin YP, Viñuela F. Dural arteriovenous fistula in children: endovascular treatment and outcomes in seven cases. AJNR Am J Neuroradiol. 2001;22(6):12171225.

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    Andreou A, Ioannidis I, Nasis N. Transarterial balloon-assisted glue embolization of high-flow arteriovenous fistulas. Neuroradiology. 2008;50(3):267272.

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    Lasjaunias P, ter Brugge KG, Berenstein A. Dural arteriovenous shunts. In: Surgical Neuroangiography: Clinical and Interventional Aspects in Children. 2nd ed. Springer; 2006:389437.

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    Bun YY, Ming CK, Ming CH, Ling CY, Ming CC. Endovascular treatment of a neonate with dural arteriovenous fistula and other features suggestive of cerebrofacial arteriovenous metameric syndromes. Childs Nerv Syst. 2009;25(3):383387.

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    Houser OW, Campbell JK, Campbell RJ, Sundt TM Jr. Arteriovenous malformation affecting the transverse dural venous sinus—an acquired lesion. Mayo Clin Proc. 1979;54(10):651661.

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    Chaudhary MY, Sachdev VP, Cho SH, Weitzner I Jr, Puljic S, Huang YP. Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR Am J Neuroradiol. 1982;3(1):1319.

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    Lasjaunias P, Magufis G, Goulao A, et al. Anatomoclinical aspects of dural arteriovenous shunts in children. Review of 29 cases. Interv Neuroradiol. 1996;2(3):179191.

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    • PubMed
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    Caponigro M, Filly RA, Dowd CF. Diagnosis of a posterior fossa dural arteriovenous fistula in a neonate by cranial ultrasonography. J Ultrasound Med. 1997;16(6):429432.

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  • Collapse
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  • FIG. 1.

    Prenatal neurosonogram performed at 21 weeks’ gestation. Transcerebellar view of the fetal brain shows a 1.9-cm hyperechoic mass (measured) in the posterior cranial fossa on the superior border of the cerebellum, posterior to the temporal lobes (arrows) and thalami (Th).

  • FIG. 2.

    Follow-up fetal MRI upon transfer to a higher level of care. A: Sagittal T1-weighted MRI showed a heterogeneously T1-hyperintense mass (yellow arrowhead) in the posterior cranial fossa. B: Axial T2-weighted MRI showed a prominent flow void (red arrow) in the middle cranial fossa with direct connection to an enlarged left sigmoid and transverse sinuses (green arrowhead) posterior to the cerebellum (yellow) suggesting a dAVF. Temporal lobe is circled in orange. C: Sagittal T2-weighted MRI showed a heterogeneously hypointense mass (red arrowhead) centered in the posterior cranial fossa.

  • FIG. 3.

    CTA of the head confirmed a prominent left middle meningeal artery (A and C; red arrows) with direct connection to the sigmoid and transverse sinuses. In addition, there was central nonopacification of the enlarged left transverse sinus (B; green arrow), suggesting a dural venous thrombus.

  • FIG. 4.

    A: Preembolization arteriograms, anteroposterior and lateral views, of the left external carotid artery (ECA), left vertebral artery, and right ECA show the complexity of the fistula/malformation with extensive arterial supply from the left middle meningeal, occipital, tentorial, posterior auricular, superior cerebellar, anterior inferior cerebellar, and posterior meningeal arteries with early venous filling in the left sigmoid sinus, transverse sinus, and torcula. Right middle meningeal and right occipital artery feeders were also confirmed with right ECA arteriogram, demonstrating early venous filling in the region of the torcula. B: Postembolization follow-up neonatal brain MRI. Axial T2-weighted (left) and sagittal T1-weighted (middle) MRI scans and coronal MRI venogram (MRV; right) show the development of moderate obstructing supratentorial hydrocephalus from a new heterogeneously T2-hypointense, T1-isointense mass (red arrows) confirmed by MRV to be a large obstructing varix from the residual fistula.

  • FIG. 5.

    A: Pre–final embolization left vertebral artery arteriogram demonstrating the persistence of early venous filing within the left sigmoid sinus and early opacification of the large posterior midline-obstructing varix previously seen on MRI and MRI venogram. B: Post–final embolization arteriogram of the left vertebral artery after embolization on the venous side of the fistula and within the venous varix just distal to the fistula. There is complete cessation of flow within the fistula with no evidence of early venous filling.

  • 1

    Hetts SW, Moftakhar P, Maluste N, et al. Pediatric intracranial dural arteriovenous fistulas: age-related differences in clinical features, angioarchitecture, and treatment outcomes. J Neurosurg Pediatr. 2016;18(5):602610.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Garcia-Monaco R, Rodesch G, Terbrugge K, Burrows P, Lasjaunias P. Multifocal dural arteriovenous shunts in children. Childs Nerv Syst. 1991;7(8):425431.

  • 3

    Djindjian R. Super-selective arteriography of branches of the external carotid artery. Surg Neurol. 1976;5(3):133142.

  • 4

    Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194(3):671680.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Kincaid PK, Duckwiler GR, Gobin YP, Viñuela F. Dural arteriovenous fistula in children: endovascular treatment and outcomes in seven cases. AJNR Am J Neuroradiol. 2001;22(6):12171225.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Iizuka Y, Koda E, Tsutsumi Y, et al. Neonatal dural arteriovenous fistula at the confluence presenting with paralysis of the orbicularis oris muscle. Neuroradiol J. 2013;26(1):4751.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Andreou A, Ioannidis I, Nasis N. Transarterial balloon-assisted glue embolization of high-flow arteriovenous fistulas. Neuroradiology. 2008;50(3):267272.

  • 8

    Cognard C, Januel AC, Silva NA Jr, Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol. 2008;29(2):235241.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Lasjaunias P, ter Brugge KG, Berenstein A. Dural arteriovenous shunts. In: Surgical Neuroangiography: Clinical and Interventional Aspects in Children. 2nd ed. Springer; 2006:389437.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Bun YY, Ming CK, Ming CH, Ling CY, Ming CC. Endovascular treatment of a neonate with dural arteriovenous fistula and other features suggestive of cerebrofacial arteriovenous metameric syndromes. Childs Nerv Syst. 2009;25(3):383387.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Houser OW, Campbell JK, Campbell RJ, Sundt TM Jr. Arteriovenous malformation affecting the transverse dural venous sinus—an acquired lesion. Mayo Clin Proc. 1979;54(10):651661.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Chaudhary MY, Sachdev VP, Cho SH, Weitzner I Jr, Puljic S, Huang YP. Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR Am J Neuroradiol. 1982;3(1):1319.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Mironov A. Pathogenetical consideration of spontaneous dural arteriovenous fistulas (DAVFs). Acta Neurochir (Wien). 1994; 131(1–2):4558.

  • 14

    Albright AL, Latchaw RE, Price RA. Posterior dural arteriovenous malformations in infancy. Neurosurgery. 1983;13(2):129135.

  • 15

    Iizuka Y, Rodesch G, Garcia-Monaco R, et al. Multiple cerebral arteriovenous shunts in children: report of 13 cases. Childs Nerv Syst. 1992;8(8):437444.

  • 16

    Liu CA, Chen HC, Luo CB, et al. Dural sinus malformation with arteriovenous fistulae in a newborn: positive outcome following endovascular management. J Chin Med Assoc. 2012;75(1):4346.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lasjaunias P, Magufis G, Goulao A, et al. Anatomoclinical aspects of dural arteriovenous shunts in children. Review of 29 cases. Interv Neuroradiol. 1996;2(3):179191.

  • 18

    Barbosa M, Mahadevan J, Weon YC, et al. Dural sinus malformations (DSM) with giant lakes, in neonates and infants. Review of 30 consecutive cases. Interv Neuroradiol. 2003;9(4):407424.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Caponigro M, Filly RA, Dowd CF. Diagnosis of a posterior fossa dural arteriovenous fistula in a neonate by cranial ultrasonography. J Ultrasound Med. 1997;16(6):429432.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

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