Cortical malformation adjacent to a large pial arteriovenous fistula

Abstract

The coexistence of an arteriovenous fistula (AVF) and neuronal migration abnormalities is a rare phenomenon. The underlying pathophysiology responsible for these anomalies remains elusive. Neuronal architectural irregularities arise from complex neuronal formation, migration and organisation dysfunctions. Isolated cases of these associations are rarely described in the literature. Here, we present an unusual case involving the coexistence of a pial AVF and a pachygyria–polymicrogyria complex in an early childhood boy. We have provided a detailed description of the neuroimaging characteristics and the therapeutic embolisation in this case, along with follow-up. Additionally, we conduct a comprehensive review of potential hypotheses about the association, referencing prior case reports. The presence of an aberrant blood supply or deviant venous drainage from the developing cortex may contribute to a variety of neuronal migration anomalies.

Background

A pial arteriovenous fistula (AVF) is characterised as a high-flow vascular shunt that lacks an intervening capillary network.¹ This condition is very rare and accounts for only 1.6% of all intracranial vascular malformations.² The co-occurrence of a pial AVF alongside a cortical developmental malformation represents an even rarer association and has scarcely been documented in the literature. However, such an association has been described in patients with hereditary haemorrhagic telangiectasia (HHT), although the reported vascular anomalies included nidal type of arteriovenous malformation (AVM) and capillary telangiectasias distinct from pial AVFs.³ On the other hand, the incidence of cortical malformations in HHT is reported to be 5%–10%, polymicrogyria being the most common type.^3–5 In this article, we report a case of large pial AVF with adjacent pachygyria polymicrogyria complex and associated hemiatrophy.

Case presentation

An early childhood boy was referred to our institution with a 1-year history of generalised seizures which had partially been controlled by antiepileptics. The child was born at full term through normal vaginal delivery and had an uneventful perinatal period. He was achieving normal social, language and cognitive milestones for his age. On examination, mild motor weakness was observed in his left-hand grip and left foot as compared with the contralateral side. Subsequent MRI examination of his brain showed multiple prominent vascular flow voids on the surface of the right temporal-insular region. Additionally, the MRI revealed a pachygyria–polymicrogyria complex affecting the lateral surface of the right temporal lobe (figure 1A) and, insula and frontoparietal operculum (perisylvian cortices) (figure 1B,C). Dilated sulcal spaces and hemiatrophy were also apparent on the right side. (Figure 1D). Dilated vascular structures on the surface of the brain suggested the presence of AVF. Digital subtraction angiography was done under general anaesthesia to further characterise the lesions and treat them endovascularly, if feasible. A selective angiogram of the right internal carotid artery unveiled the presence of a conglomerate of multiple high-flow pial-AVF in the right perisylvian region. The arterial feeders were from the prominent right middle cerebral artery (MCA), and venous drainage was through multiple prominent cortical veins, including the Vein of Labbé, the Vein of Trolard and the superficial middle cerebral vein ultimately draining into the superior sagittal, right sigmoid and right cavernous sinuses, respectively (figure 2A,B). Marked arterial steal resulting in poor opacification of normal right MCA branches was noted. Compensatory collateralisation was evident from branches of the right anterior cerebral artery (ACA) and right posterior cerebral artery. Notably, the right ACA was receiving supply from the left side via the anterior communicating artery.

Figure 1.

MRI of the brain at initial presentation. (A,B) Axial T1-weighted image shows pachygyria with polymicrogyria in the lateral surface of the right temporal lobe (arrow in (A)) and the frontoparietal operculum (arrow in (B)) with blurring (arrow in (C)) of the grey-white matter junction in the right insula and opercular region on axial Fluid Attenuation Inversion Recovery (FLAIR) image(C). Coronal T1-weighted image (D) reveals widely spaced right temporal gyri (arrow in (D)) with right cerebral hemiatrophy.

Figure 2.

: First stage of arteriovenous fistula (AVF) embolisation. The anteroposterior (A) and lateral views (B) of the right internal carotid artery angiogram show a large arteriovenous fistula (arrow in (A)) with arterial feeders noted from the right middle cerebral artery M2 branches (MCA). The venous drainage is seen through prominent veins (*) into the superior sagittal sinus and sigmoid sinus (arrowhead in (B)). The right MCA cortical branches (arrow in (B)) are hypoplastic and become visible only in the delayed phase. The right anterior cerebral artery and the distal right MCA branches are not visualised in the right internal carotid artery run due to the steal phenomenon. (C,D) Microcatheter (arrow in (C)) run at AVF nidus followed by glue injection (arrow in (D)).

Single-session embolisation of the fistula was not feasible due to contrast dose limitations, high radiation exposure and perfusion pressure breakthrough. The first stage of AVF embolisation was done using 95% glue at the time of diagnosis (figure 2C,D), which resulted in a minimal reduction in the size of AVF. Subsequent second (figure 3A) and third (figure 3B) stages of embolisation were performed. Improvement in clinical symptoms was noted after second stage. The final (third) stage of embolisation resulted in a partial reduction in the size of the AVF, accompanied by an improvement in MCA collaterals (figure 3C). Postembolisation Non-contrast computed tomography (NCCT (figure 3D) showing no infarct. No periprocedural complications were seen. After each embolisation procedure, the child was followed up every 3 months in outpatient department (OPD).

Figure 3.

Second stage and third stage embolisation. Lateral view of the right internal carotid artery angiogram after the completion of the second stage (A) and third stage (B) of embolisation, respectively, revealed a partial reduction in the size of AVF nidus. (C) Left internal carotid artery angiogram in anteroposterior view revealing pial collaterals (arrow). These collateral vessels play a significant role in maintaining blood flow in the affected region. (D) Postembolisation NCCT axial image reveals no parenchymal hypodensity or infarct. The arrow shows the glue cast.

Outcome and follow-up

To date, the child is on continuous follow-up in the OPD. His left upper hand weakness has completely improved after second embolisation sitting. He has been seizure free for the last 2 years, and his antiseizure medication is gradually being reduced. His scholastic performance is normal according to age.

Discussion

Large pial AVFs exert a substantial impact on blood flow within normal brain tissue, often resulting in the occurrence of seizures. The pathology underlying congenital pial AVF formation has been suggested to be due to increased angiogenesis, as many cases are linked to underlying vascular syndromes such as Rendu-Osler-Weber disease, Klippel-Trenaunay-Weber syndrome^6–9 and RAS-1 mutation.¹⁰ It is well established that ischaemic insult during brain development can lead to malformations of cortical development.¹¹ Ngam et al ¹² put forward the hypothesis that the aetiology of malformation of cortical development and agenesis of the corpus callosum in cases of pial AVF is related to ischemia resulting from the ‘steal phenomenon’.¹² In our case, the observed pachygyria–polymicrogyria was confined to the MCA territory adjacent to the AVF, further supporting the notion of ischaemic insult as a contributing factor. Our case did not undergo genetic analysis and was negative for curacao criteria for diagnosis of HHT.

Klostrance et al ³ presented findings from a cohort of 142 patients with HHT and demonstrated that seven cases exhibited polymicrogyria in imaging studies. Among these, six were associated with brain AVMs nearby, and only two cases presented with symptomatic seizures. This association raises suspicion of a common insult triggering the development of both lesions. Notably, the impact during fetal development appears to be one sided and localised, often resulting in clinically unnoticed polymicrogyria.^{3 4} While abnormal or prominent venous drainage has been reported in connection with cortical dysplasia, these vascular anomalies do not appear to involve arteriovenous shunts or fistulas.^{13 14} In the case report by Abe et al,¹⁴ cortical dysplasia was associated with opercular arterial dysplasia, featuring a large superficial vein draining into the superior sagittal sinus and normal distal MCA branches. Additionally, two cases of ectatic cerebral arteries without Arterio-venous (AV) shunts associated with congenital disorders of cellular migration have been described,^{15 16} suggesting that leptomeningeal damage during neuronal cell migration could lead to the development of a dysplastic arterial anomaly alongside cortical dysplasia.

While the literature has described cortical malformations, mainly polymicrogyria, in association with arteriovenous malformations in Osler-Weber-Rendu syndrome or HHT, instances involving large pial AVFs and arterial steal phenomena have been notably absent. In our case, the presence of a significant vascular steal due to the AVF has emerged as a significant contributor. In conclusion, a comprehensive review of the literature underscores the role of arterial steal due to AV fistulas and leptomeningeal damage in abnormal neuronal architecture as the underlying aetiology for the coexistence of AV malformations and neuronal migration abnormalities.

Patient’s perspective.

Our child was suffering from seizure disorder and weakness in the left hand. The doctors expertly diagnosed and managed the problems gave him medications and treated arteriovenous fistula. Sincere gratitude and appreciation to the doctors. Now our child is symptom-free and doing well in his daily life activities.

Learning points.

• Pial arteriovenous fistulas (AVFs) are a type of angiogenesis and have a congenital aetiology. Hence, other congenital anomalies, such as malformations of cortical development, can be coassociated.

• Physicians should be vigilant during the examination of cortical malformations on MRI to identify adjacent arteriovascular malformations.

• Treatment of the associated high-flow pial AVF can improve neurological symptoms, such as weakness, as observed in our case, which is caused by arterial steal phenomena.

Ethics statements

Patient consent for publication

Consent obtained from parent(s)/guardian(s).