Abstract

Background: Arteriovenous malformation (AVM) and developmental venous anomaly (DVA) rarely coexist. Developing a surgical strategy to treat this co-occurrence is difficult due to the unclear pathogenesis. We report the use of super-selective digital subtraction angiography (DSA) and Three-dimensional (3D) rotational digital subtraction venography (DSV) to develop a surgical strategy for complex AVM draining into a DVA.

Case Description: A 58-year-old woman presented with left hemiparesis and unconsciousness. Plain and contrast computed tomography showed a right frontal subcortical hematoma and a heterogeneous contrast lesion anterior to the hematoma, leading to a dilated vessel. The hematoma was removed due to worsening unconsciousness. DSA revealed a right frontal AVM of Spetzler-Martin grade 2 with superficial drainage into a DVA, and 3D-DSV revealed that the intermediate part of the DVA involved normal parenchyma. Interventional transarterial embolization and surgical nidus removal were planned. Preoperative super-selective DSA showed two medullary veins draining from the AVM into the DVA. Thus, we decided to separate the two medullary veins from the nidus. Postoperative angiography revealed complete removal of the AVM and preservation of the DVA.

Conclusion: Treating a complex AVM draining into a DVA is challenging; surgeons have to remove only the AVM portion and preserve the DVA. Super-selective DSA and 3D rotational DSV were performed to develop the surgical strategy.

Keywords: Three-dimensional-rotational digital subtraction venography, Arteriovenous malformation, Developmental venous anomaly, Digital subtraction angiography, Super-selective digital subtraction angiography

INTRODUCTION

Developmental venous anomaly (DVA) is a variation of normal medullary veins and the most common brain vascular malformation, with an incidence of approximately 2.6%.[ 6 ] DVA consists of radially arranged dilated medullary veins and an enlarged transcortical or subependymal collector vein. The characteristic appearance of angiography is called “caput medusae.” DVAs are considered benign lesions with an annual bleeding rate of 0.2%. However, DVAs may hemorrhage when associated with other vascular malformations.[ 1 , 12 ] Arteriovenous malformation (AVM) is a congenital vascular anomaly with an annual symptomatic hemorrhage rate of 2–3% caused by high shunting flow without an intervening capillary bed.[ 18 ]

A DVA coexisting with an AVM is rare, with only about 30 reported cases, and the pathogenesis of this co-occurrence is unclear, making the development of a treatment strategy difficult. Several treatments were developed in previous reports, including surgical resection, transarterial embolization, stereotactic radiosurgery, and a combination of these techniques.[ 12 ] Surgical treatment of this mixed vascular malformation to prevent severe complications is challenging.[ 1 , 9 , 12 , 13 ] Herein, we report the use of super-selective digital subtraction angiography (DSA) and three-dimensional (3D) rotational digital subtraction venography (DSV) of the AVM draining into the DVA to obtain detailed angioarchitectures for developing a surgery strategy.

CASE PRESENTATION

A 58-year-old woman with no notable past medical or family history visited our hospital due to left hemiparesis and unconsciousness. Plain and contrast computed tomography (CT) revealed a right frontal subcortical hematoma and a heterogeneous contrast lesion anterior to the hematoma, leading to a dilated vessel [ Figures 1a and b ]. The unconsciousness worsened at the hospital. Thus, the hematoma was removed. DSA 8 days after the hemorrhage showed a Spetzler-Martin grade 2 AVM with a 20 mm nidus fed by the callosomarginal and pericallosal arteries [ Figures 2a and b ] and a DVA draining AVM blood flow and medullary veins from the right anterior frontal lobe [ Figures 2c and d ]. 3D DSV showed that the intermediate part of the DVA involved normal parenchyma [ Figure 2e ] and should be preserved during treatment.

Figure 1:

(a) Axial plain computed tomography revealed a right frontal subcortical hematoma. (b) Axial computed tomographic angiography showed a heterogeneous contrast lesion (arrowhead) and a dilated vessel (arrow) in the right frontal lobe.

Figure 2:

Digital subtraction angiography from the right internal carotid artery. (a and b) Arterial phase, (c and d) venous phase, and (e) 3D rotational digital subtraction venography; the arrowhead exhibits the intermediate segment of developmental venous anomaly.

The patient was diagnosed with subcortical hemorrhage due to a ruptured AVM, and surgical treatment for the AVM was planned. Transarterial embolization of the two arteries was performed to reduce the flow of the AVM 36 days after the hemorrhage. Super-selective DSA revealed the AVM draining into an intermediate part of the DVA through two medullary veins [ Figures 3a and b]. The two medullary veins were separated from the nidus. Then, surgical resection was performed 37 days after hemorrhage. The AVM was removed by entering the brain parenchyma through the hematoma cavity, and the nidus was identified and resected [ Figures 3c and d ]. No additional neurological disorders were detected during the postoperative period. DSA after surgical treatment revealed that the AVM was resected, and the intermediate DVA was preserved [ Figure 4 ]. The patient had left hemiparesis but no evident brain hemorrhage up to 14 months after surgery.

Figure 3:

(a and b) Super-selective digital subtraction angiography from the right pericallosal artery and the right callosomarginal artery showed two medullary veins (white arrowheads). (c and d) The two draining veins were visualized and resected during surgery (black arrowheads) (c and d).

Figure 4:

Digital subtraction angiography from the right common carotid artery after nidus resection. (a and b) Arterial phase and (c and d) venous phase.

DISCUSSION

DVAs are considered benign cerebrovascular variants. However, when coexisting with other cerebrovascular malformations, DVAs may cause symptomatic hemorrhaging.[ 12 , 15 ] DVA with early venous filling, referred to as arterial DVA, DVA with arterial component, or atypical AVM with venous predominance, is one of the coexisting cerebrovascular malformations that may cause hemorrhaging.[ 1 , 10 ] DVA with early venous filling can be classified into two types: micro-shunts draining into the DVA and a true AVM draining into the DVA.[ 2 , 12 ] The risk of bleeding is high for DVAs with early venous filling; in particular, an AVM draining into a DVA tends to cause hemorrhaging more frequently than micro-shunts into a DVA.[ 1 , 2 , 10 ]

To address the higher bleeding risk, Pereira et al. suggested preventive treatment even for asymptomatic patients with a true AVM draining into a DVA.[ 11 ] However, treatments for these lesions are challenging. Obliteration of DVAs is not recommended because DVAs have normal parenchymal venous drainage, and obliteration may cause venous infarction, hemorrhage, and edema.[ 7 - 9 , 12 , 13 ] Meyer et al. reported a case of hemorrhagic infarction after complete DVA obliteration.[ 9 ] Other reports recommended targeting the AVM component while preserving the DVA.[ 5 , 7 , 8 , 12 , 13 , 18 ] However, no reports established clinical methods to evaluate safe surgical approaches.

DSA and 3D rotational DSA are standard imaging tools for evaluating complex vascular lesions. These tools are useful for neurosurgery, endovascular treatment, and radiosurgery.[ 3 , 14 ] Raz et al. performed venous 3D-DSA following arterial 3D-DSA to improve the visualization of a DVA. Arterial and venous 3D-DSA may allow better visualization of the relationship between the arteries and the veins to understand cerebrovascular architectures.[ 14 ] Holmes et al. performed super-selective cone-beam angiography for radio-surgical planning. Super-selective angiographies allow better visualization than computed tomographic or magnetic resonance angiography.[ 3 ]

In our case, 3D-DSV and super-selective DSA showed the angioarchitectures of the coexisting AVM and DVA; 3D-DSV revealed that the intermediate DVA collected the medullary veins and should be preserved. In addition, super-selective DSA revealed that the AVM drained into the intermediate part of DVA through two medullary veins. Thus, we preoperatively decided to detach the two medullary veins and preserve the intermediate part of the DVA.

We performed a literature search using PubMed to identify other surgical cases of AVMs draining into DVAs and identified 9 surgical cases [ Table 1 ]. DSA was performed in eight of the nine cases[ 2 , 4 , 7 , 9 , 10 , 16 , 18 ], and other diagnostic methods were identified in four cases.[ 7 , 10 , 16 , 17 ] Truwit performed time-of-flight magnetic resonance imaging (MRI) because the AVM could not be confirmed with DSA.[ 16 ] Wurm et al.[ 17 ] mentioned only MRI in their report. Oran et al.[ 10 ] reported a case of embolization and resection of an AVM; super-selective DSA was used for the embolization procedure. In that case, the AVM and, subsequently, the DVA were removed because a large hematoma compressed the motor cortex after embolization. Li et al.[ 7 ] reported a hybrid surgery to resect an AVM; the AVM was diffuse, so the DVA was also removed, and the patient did not experience neurological deficits, but CT after surgery revealed cerebral edema. To the best of our knowledge, ours is the first case of an AVM draining into a DVA in which super-selective DSA and 3D-DSV were performed to preserve the DVA during surgery.

Table 1:

Summary of nine cases of surgical treatment for AVM draining into developmental venous anomaly.

CONCLUSION

A hemorrhagic case of a true AVM directly draining into a DVA is described. Preventive treatment for this complex lesion was recommended due to the hemorrhagic presentation; however, surgeries for these deformities are challenging with high complication rates. Therefore, 3D-DSV and super-selective DSA were employed to obtain detailed angioarchitectures, which were useful for developing a safe surgical approach.

Ethical approval

The research/study was approved by the Institutional Review Board at Japanese Redcross Shizuoka Hospital, number 2024-15, dated September 19, 2024.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript, and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

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