Intracranial arteriovenous malformations (AVMs) are rare congenital vascular lesions comprising arteriovenous shunts that appear as high-flow, dilated, tubular, tortuous vascular channels1, 2. Their prenatal diagnosis is complex, given their rarity and anatomical position, which means they may escape detection on routine ultrasound screening via axial planes of the fetal brain. Furthermore, due to the course of their development, they may not yet be present or visible at the time of the mid-trimester anatomical evaluation. Although most AVMs detected prenatally involve the vein of Galen, other rarer forms of congenital AVM involve the dura or pia mater1-7. Prenatal diagnosis of multiple intracranial AVMs was demonstrated recently by Krishnan et al.7. The prognosis of neonates with a congenital AVM is poor. Although there is a risk of complications such as intracranial bleeding, the high-output congestive heart failure that often develops in utero is the most common cause of death5, 6. Dedicated neurosonography using transvaginal high-resolution probes enables detailed evaluation of the fetal brain8, including its complex vascular system3. We report a case in which detailed neurosonography using three-dimensional (3D) color Doppler at 33 gestational weeks assisted in the diagnosis and characterization of a rare congenital pial AVM involving several fistulous ducts between the pial arteries and the superior sagittal sinus. A 35-year-old primigravida presented for a second opinion due to fetal findings of bilateral borderline ventriculomegaly of 10 mm and cardiomegaly noted on third-trimester ultrasound evaluation at approximately 33 weeks of gestation. Using a Voluson E10 system with a 5–9-MHz transvaginal probe (GE Healthcare, Zipf, Austria) and an approach through the fontanelle and sagittal suture, detailed multiplanar imaging of the fetal brain demonstrated a large, anechoic, tubular, interhemispheric structure extending to the left hemisphere. It was positioned supratentorially and occupied the space extending from the occiput to the mid portion of the corpus callosum and cranially to the subdural space (Figure 1). Strong, rapid vascular flow could be seen even on grayscale imaging (Videoclips S1 and S2). This was confirmed with color Doppler and appearance-enhancing radiantflowTM, on which high-velocity, turbulent, but mostly bidirectional, blood flow could be seen within the structure. Further assessment in sagittal and coronal planes using color Doppler imaging assisted in tracing the arterial feeders of the vascular shunts, including two distal branches of the pericallosal artery and a tortuous left middle cerebral artery (MCA), as they connected to the superior sagittal sinus (Figures 2 and 3 and Videoclips S3–S6). 3D ultrasound imaging using radiantflowTM and glass-body rendering® mode (GE Healthcare) were utilized to further enhance the image of the vascular anomaly and the spatial relationship of the AVM with the surrounding blood vessels, by overcoming the significant mass effect that it caused (Figure 4). The circle of Willis appeared dilated and distorted, and the dilated and tortuous MCA displayed high-velocity blood flow, with a peak systolic velocity of 100.9 cm/s (2.2 multiples of the median), confirming high-output shunting and the ‘steal’ phenomenon. Despite the mass effect of the dilated superior sagittal sinus, the brain anatomy was otherwise normal, with secondary, mild, bilateral ventriculomegaly of 11 mm and mild dilatation of the third ventricle. Additionally, both systemic and cardiac findings of congestive heart failure were noted, including globular cardiomegaly, significant right heart dominance (right ventricle and atrium larger than left), dilated and tortuous superior vena cava and jugular veins, tricuspid regurgitation and mild pericardial effusion (Figure 5). The fetal anatomical survey was otherwise normal. In summary, we diagnosed this fetus at 33 weeks of gestation with an extra-axial, supratentorial intracranial mass which was consistent with congenital AVM involving two branches of the pericallosal artery and the left MCA that connected directly to a markedly dilated superior sagittal sinus. In addition, systemic findings of high-output congestive heart failure were present. The woman, who had no relevant personal or family history, underwent extensive counseling and declined genetic evaluation with whole-exome sequencing. Delivery was scheduled in a center with pediatric neurosurgery and pediatric neuroradiology facilities and expertise in managing congenital AVM. Following delivery at approximately 37 weeks of gestation, postnatal imaging confirmed the prenatal diagnosis, and several multistage, palliative, transarterial embolizations were performed. The procedure was complicated by rupture of the MCA, leading to extensive intracranial hemorrhage and demise of the neonate. The parents declined further assessment. There is considerable uncertainty as to the mechanisms leading to the development of congenital AVM. Persistence of a primitive arteriovenous connection was suggested initially1, while a more recent hypothesis proposes that later development of AVMs is due to abnormal angiogenesis and cell signaling altering the normal embryogenetic process2, 4, 7. It has been suggested that prenatal arteriovenous shunting involving a pial AVM develops initially in the subarachnoid space, and gradually dilates in synchronization with the development of the fetal brain. The increase in abnormal blood inflow secondarily creates new, small AVM shunts, mainly in the brain parenchyma. This secondary shunt formation may also be a component in the development of pial AVMs in adults1. When detected prenatally, intracranial AVMs are largely intra-axial and are believed to be derived from persistent embryonic sinuses, venous varices, aneurysmal malformations and emissary veins, resulting in development of venous brain anomalies2. Some congenital intracranial shunts may present as capillary malformation–AVMs, which have been described recently in association with several genetic mutations4. The symptomatology and prognosis of these lesions vary tremendously based on their time of presentation (prenatal, neonatal, infancy, childhood or adulthood), with earlier, more severe manifestation being associated with a much grimmer prognosis. Strategies of endovascular treatment for these vascular lesions are discussed by Lv et al.4, who believe that a better understanding of these AVMs will lead to improvement in their diagnosis and postnatal treatment4. Our case illustrates the value of dedicated multiplanar neurosonography via a transvaginal approach to provide detailed understanding of the fetal brain vascular system. In this rare case of congenital pial AVM, this methodology enhanced our ability to diagnose and characterize the complex vascular connections, and to visualize the arterial feeders of the pial AVM draining into the dilated superior sagittal sinus. Detailed assessment is key in order to provide accurate counseling to the parents regarding the severity of the fetal condition and regarding the potential need for additional assessments of family members or fetal genetic analyses to determine the risk of a similar condition in other family members or recurrence in future pregnancies. Furthermore, it is essential in order to prepare properly for delivery in a center with appropriate expertise and to provide the necessary postnatal treatment. The data that support the findings of this study are available on request from the corresponding author. Videoclip S1 Transvaginal scan of the fetal brain via the sagittal suture to obtain the midsagittal plane at 32 + 6 weeks. A large sonolucent lesion is visible supratentorially, occupying the space from the occiput to the mid portion of the corpus callosum and cranially to the subdural space, and appearing as a dilated superior sagittal sinus (arrow). The high-velocity blood flow within the sinus is evident even on grayscale imaging. Videoclip S2 Transvaginal scan of the fetal brain via the anterior fontanelle and the sagittal suture to obtain a coronal sweep at 32 + 6 weeks. This evaluation of successive coronal views of the brain demonstrates a large, tubular, space-occupying, tortuous, sonolucent, interhemispheric structure in the posterior portion of the brain. It extends to the left hemisphere, and is positioned supratentorially, occupying the space from the occiput to the mid portion of the corpus callosum and cranially to the subdural space. The views of the anterior and mid portion of the brain demonstrate normal anatomy. Videoclip S3 Transvaginal scan of the fetal brain via the sagittal suture to obtain the midsagittal and parasagittal planes at 32 + 6 weeks. RadiantflowTM mode demonstrates the high-velocity blood flow within the dilated superior sagittal sinus (arrow). Doppler evaluation assisted in tracing the arterial feeders of the vascular shunts, which included two distal branches of the pericallosal artery and a tortuous left middle cerebral artery, which were dilated and connected directly to the superior sagittal sinus. Videoclip S4 Transvaginal scan of the fetal brain via the sagittal suture to obtain the coronal and midsagittal planes using radiantflowTM at 32 + 6 weeks. The color filling demonstrates the high-velocity blood flow within the dilated superior sagittal sinus with a typical ‘yin and yang’ distribution of blue and red colors. The arterial feeders from two distal branches of the pericallosal artery are traced as they enter the superior sagittal sinus. Videoclips S5 and S6 Transvaginal scan of the fetal brain via the sagittal suture, enabling sagittal and coronal evaluation through the brain lesion, using radiantflowTM at 32 + 6 weeks. The high-velocity blood flow within the dilated superior sagittal sinus (arrows) is evident and the arterial feeders of the vascular shunts can be traced. These include two distal branches of the pericallosal artery and a tortuous left middle cerebral artery, which are dilated and connected directly to the superior sagittal sinus. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
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Apr 16, 2024
L. Dade Lunsford + 24
Open Access