Spontaneous regression of a symptomatic developmental venous anomaly with capillary stain

Abstract

Background

Developmental venous anomalies are considered benign lesions; however, they can become symptomatic. A capillary stain, which is an atypical angiographical feature of developmental venous anomalies, is reported to be relevant to symptomatic developmental venous anomalies.

Case description

A 20-year-old man with no pertinent medical history had an epileptic seizure. Magnetic resonance imaging showed severe focal oedema and gadolinium contrast enhancement in the right precentral gyrus and inferior frontal gyrus adjacent to the Sylvian fissure, indicating venous congestion; these presentations had not been observed on magnetic resonance imaging 8 months before. Digital subtraction angiography revealed a developmental venous anomaly with capillary stain. After conservative treatment, the brain oedema resolved spontaneously and contrast enhancement of the lesion reduced significantly.

Conclusion

We report a rare case of a symptomatic developmental venous anomaly with unique radiological characteristics and its natural and clinical evolution. Despite the presence of a capillary stain, our patient exhibited temporary exacerbations and spontaneous regression, suggesting that the capillary stain was associated with a reversible condition. This is the first report to detail the spatiotemporal changes of a developmental venous anomaly with capillary stain through imaging, suggesting that regular follow-up imaging is warranted in the management of patients with developmental venous anomalies.

Introduction

Developmental venous anomalies (DVAs) are the most common subtype of cerebral vascular malformations and have been observed in up to 2.6% of autopsied brains. ¹ With the advent of head magnetic resonance imaging (MRI), the prevalence of DVAs is reported to be 0.48%–0.7%. ² DVAs are considered benign lesions and are asymptomatic in most cases. ³ However, they can sometimes present as abnormalities on images, and patients may experience neurologic deficits, seizures and haemorrhages. ⁴ A capillary stain is an atypical angiographical feature of DVAs and indicates neoangiogenesis secondary to venous hypertension and venous-induced ischemia. ⁵ Furthermore, the capillary stain has been reported to be relevant to symptomatic DVAs. ⁵ Herein, we report a case of a patient with a symptomatic DVA with a capillary stain that presented with spontaneous exacerbations and regression of brain oedema and a contrast-enhanced lesion. We present the detailed spatiotemporal changes in the imaging findings of the DVA.

Case report

A 20-year-old healthy man with no relevant medical history had an epileptic seizure, which was a simple partial seizure involving shaking movements of the neck. The seizure started after vigorous exercise, continued for few minutes, and stopped spontaneously. After the seizure, he had a fever that lasted for 3 days and a persistent headache. He was then admitted to the hospital. On admission, no neurological deficit was observed by the neurosurgeon. He did not have a history of gastrointestinal bleeding, and there were no cutaneous lesions. The focus of his fever was unclear on physical examination, and the fever subsided naturally. His blood tests showed no abnormalities, including a normal white blood cell count and C-reactive protein level. Chest radiography revealed no pneumonia. T2-weighted MRI revealed a high-intensity area in the right precentral gyrus and inferior frontal gyrus adjacent to the Sylvian fissure (Figure 1(a) to (c)), which had not been observed on MRI images taken at another hospital 8 months before (Figure 2). Diffusion-weighted imaging did not show restriction diffusion (Figure 1(d)). Gadolinium contrast-enhanced MRI revealed contrast enhancement in the lesion (Figure 1(e)). A dilated flow void was observed near the lesion on T2-weighted imaging (Figure 1(b)); therefore, vascular disease was suspected.

Figure 1.

MRI on admission. (a) MRI T1-weighted imaging shows a DVA in the right frontal lobe with a low-intensity area around the flow void of the cortical vein. (b), (c) T2-weighted imaging and fluid-attenuated inversion recovery imaging show a high-intensity area, indicating severe oedema. (d) Diffusion-weighted imaging indicates no restricted diffusion. (e) The gadolinium contrast-enhanced T1-weighted magnetic resonance image showing a strong enhancement in the right precentral gyrus and inferior frontal gyrus adjacent to the Sylvian fissure. (f) A high-density area consistent with the cortical vein is seen in the computed tomography image.

MRI: Magnetic resonance imaging; DVA: developmental venous anomaly.

Figure 2.

Spatiotemporal changes in imaging findings of the developmental venous anomaly head magnetic resonance imaging with gadolinium-enhanced T1-weighted (upper row) and T2-weighted (lower row) imaging sequences overtime during the follow-up period (8 months before, on admission, 13, 32 and 123 days after admission). Since there was no contrast-enhanced image 8 months before admission, non-contrast T1 is shown (asterisk). At the onset, the lesion showed a strong enhancement and severe brain oedema. About 1 month later, the contrast enhancement and brain oedema decreased and reduced significantly 4 months later.

There were no haemorrhagic changes. Magnetic resonance spectroscopy showed no elevation of lactate levels. An 18F-fluorodeoxyglucose positron emission tomography scan showed no uptake. Five days after admission, digital subtraction angiography (DSA) revealed a DVA that was consistent with the lesion observed on MRI. There was a venous anomaly from the middle cerebral artery to the superficial Sylvian vein–vein of Labbe-sigmoid sinus and cortical vein-superior sagittal sinus. A fine network of vessels forming a ‘blush’ in the arterial phase, which is called a ‘capillary stain’, was detected (Figure 3). Early filling of the draining vein was not observed, suggesting that there was no arteriovenous shunt (i.e. arteriovenous malformations (AVMs) or arteriovenous fistula) in the lesion.

Figure 3.

Digital subtraction angiography images of the developmental venous anomaly with a capillary stain DSA of the right internal carotid artery at the lateral view revealed a DVA in the right frontal lobe. (a) The arterial phase; (b) capillary phase; and (c) venous phase. A venous anomaly was observed from the middle cerebral artery to the superficial Sylvian vein–vein of Labbe-sigmoid sinus (grey arrowheads) and cortical vein-superior sagittal sinus (black arrowheads). A fine network of vessels forming a ‘blush’ around the middle cerebral artery was detected, which is a capillary stain (white arrowheads) (a).

DSA: digital subtraction angiography; DVA: developmental venous anomaly.

Based on the imaging findings, the T2 hyper-intense lesion in the right frontal lobe was diagnosed as venous congestion due to the DVA. Gadolinium enhancement of the lesion was suggested to be caused by capillary staining. This lesion was considered to be the cause of the seizure. The imaging and laboratory findings were not suggestive of venous thrombosis. Thus, treatment with antiepileptic drugs was started, but no anticoagulation or anti-oedematous drugs, surgery or radiation therapy was initiated. MRI was performed 13, 32 and 123 days after admission for regular follow-up. Although the DVA itself did not disappear, contrast enhancement of the lesion decreased 1 month after treatment and significantly reduced 4 months later (Figure 2). The brain oedema also resolved. During the follow-up period, the seizure was controlled, and there was no re-exacerbation of the brain oedema.

Discussion

DVAs are the most common subtype of cerebral vascular malformations.^1,2 Cerebral vascular malformations are classified into capillary telangiectasia, AVMs, cavernous malformations (CMs) and DVAs. The term ‘developmental venous anomaly’ was proposed by Lasjaunias et al. ⁶ and is widely used as a synonym for cerebral venous medullary malformation, venous malformation or venous angioma. DVAs are regarded as normal anatomical variants and are assumed to be congenital. ⁷ In a previous study, DVAs were detected in neonatal brains. ⁸ Thus, DVAs are considered benign and asymptomatic in most cases, ³ although they can uncommonly present with headache, progressive neurologic deficits, seizures, haemorrhage and abnormal images. ⁴ The haemorrhage risk associated with DVAs was reported to be 0.22% per year. ⁹ However, DVAs coexist with CMs in some cases, and CMs seem to be responsible for most haemorrhagic cases of DVAs. ¹⁰ In some rare cases, the coexistence of DVAs with AVMs and DVAs demonstrating shunting themselves without AVMs were reported, and these arterio-venous (AV) shunts were considered to be the cause of haemorrhage.^11,12 DVAs are also known to be associated with systemic diseases such as blue rubber bleb nevus syndrome. In such cases, consideration of a history of gastrointestinal bleeding is important. ¹³

Herein, we report a case of a patient with symptomatic DVA with capillary stain, who presented with spontaneous exacerbations and regression. In this patient, the asymptomatic DVA became symptomatic, presenting with a partial seizure accompanied by capillary stain and focal oedema, which resolved spontaneously. This is the first report to present details of the spatiotemporal changes found on imaging of DVA with capillary stain.

The pathophysiology of symptomatic DVAs can be categorised as mechanical compression, decreased outflow or thrombosis or increased inflow. ¹⁴ The underlying cause of most symptomatic DVAs is venous hypertension, typically secondary to either decreased outflow, stenosis or outright thrombosis.

On DSA, DVAs are typically seen only during the venous phase. Previous studies have reviewed rare cases of DVAs with early venous filling, and various terms have been used, such as venous angiomas with AV shunts, ¹⁵ DVA with an arterial component, ¹⁶ DVA with an AV shunt, ¹⁷ or arterialized venous angioma. ¹⁸ One type of DVA with the early venous filling was reported to be characterised by capillary brush-like shunts. ¹⁴ Roccatagliata et al. ⁵ defined the capillary stain as a fine network of vessels forming a ‘blush’ in the arterial phase. The aetiology of DVAs with early venous filling is unknown; however, the hypothesis is that venous hypertension and venous-induced ischemia may trigger secondary neoangiogenesis and blood-brain barrier dysfunction.^17,19–21 This biological process is typically observed as a capillary stain. Although the role of the capillary stain remains unclear, one previous study reported that the prognosis of DVAs with AV shunts is essentially benign like that of DVAs without AV shunts. ¹⁵ On the other hand, some reports indicated that the DVAs with a capillary stain had a higher risk of cerebral haemorrhage than DVAs without a capillary stain.^5,16–18 This unique imaging finding was reported to be associated with symptomatic DVAs involving neurological deficits and seizures. ⁵

Our patient was originally asymptomatic with no imaging abnormalities. The DVA became symptomatic, and subsequently, the capillary stain and brain focal oedema appeared, indicating underlying venous hypertension and venous-induced ischemia. The cause of the symptoms of the DVA in our patient seemed to be categorised into increased inflow or decreased outflow without any venous thrombosis. It has been reported that the capillary stain is one of the subtypes of DVA with AV shunts, indicating increased inflow. ²² However, because follow-up DSA was not performed, the possibility of venous stenosis cannot be excluded. The exact trigger for the onset of symptoms of the DVA in our patient is unclear. A prominent flow void was found on T2-weighted imaging 13 days after admission, and it became less remarkable more than 32 days after admission. This indicated temporary dilation of the draining vein. It is possible that the draining flow was congested or that the flow increased; however, the exact mechanism of dilation is unknown. Although the DVA itself did not disappear, MRI showed a temporary increase, attenuation and disappearance of the gadolinium contrast enhancement. A previous study has shown that the capillary stain is present in a subgroup of symptomatic DVAs and is associated with severe symptoms. ⁵ In our patient, despite the presence of the capillary stain, the DVA showed a temporary exacerbation and spontaneous regression. This clinical course was considered to reflect reversible pathological conditions such as increased vascular permeability due to venous hypertension. In a previous study, the capillary stain was reported to be triggered by secondary neoangiogenesis, which is an irreversible biological process.^17,19–21 Since follow-up DSA was not performed, it is unclear whether the capillary stain disappeared. However, our case suggested that the capillary stain could be associated with a reversible condition. Future studies are required to clarify the pathological entity of DVA with capillary stain, for it can affect the management of patients with DVAs.

The morbidity of DVAs is generally attributed to co-existing CMs or other vascular malformations. ¹⁹ Thus, conservative therapy of isolated DVAs is warranted, and neither surgical intervention nor stereotactic radiosurgery is indicated. However, in rare cases involving haemorrhage or thrombosis, surgical treatment or anticoagulation may be an option for therapy. ²³ The possibilities of treatment for symptomatic DVAs with capillary stain are limited. Surgical treatments are indicated in few patients with haemorrhage and CMs. ⁵ Radiosurgery also has limited benefits for patients with arterialized DVAs. ¹⁷ Embolisation may be an option in patients with micro-arteriovenous shunts, which can be a target for endovascular therapy. ⁵ Like in our patient, DVAs with capillary stain can present spontaneous exacerbations and regression. Therefore, regular follow-up imaging is warranted for the management of patients with DVAs.

One limitation of this study is that follow-up DSA was not performed. In the natural clinical course, focal oedema and gadolinium enhancement on MRI regressed spontaneously; however, it is not clear whether the capillary stain accompanied by the DVA disappeared. To clarify whether the capillary stain associated with DVA is a reversible pathological condition, it is necessary to continue to accumulate similar cases and to closely examine the DSA images over time.

Conclusion

We report a case of symptomatic DVA with capillary stain. The patient presented with spontaneous exacerbations and regression of brain oedema and a contrast-enhanced lesion. In this patient, the asymptomatic DVA became symptomatic presenting with a partial seizure accompanied by a capillary stain and focal oedema. Despite the presence of the capillary stain, our patient exhibited spontaneous regression, suggesting that the capillary stain was associated with a reversible condition. This is the first report with imaging details on the spatiotemporal changes of a DVA with capillary stain, suggesting that regular follow-up imaging is warranted in the management of patients with DVAs.