Abstract

Background: Meningioma and dural arteriovenous fistula (dAVF) located at the same site are rare. The present case demonstrated the transformation of tumor feeding vessels into the pial feeder of the dAVF over time, which may help to elucidate the pathogenesis of tumor-associated dAVF.

Case Description: A 71-year-old man presented with convulsion. Magnetic resonance (MR) imaging showed a right parasagittal sinus meningioma invading the superior sagittal sinus (SSS). Bilateral external carotid angiography showed dAVF at the SSS, near the site of tumor invasion. The right internal carotid angiography showed tumor staining from the anterior cerebral artery with intra-tumor arteriovenous shunting, with stagnation of tumor blood flow, suggesting impairment of perfusion to the SSS. Four years after the initial diagnosis, the patient was admitted to hospital with status epilepticus, and MR imaging showed an enlarged tumor. Carotid angiography revealed transformation of the tumor feeders to the pial feeder of the dAVF. The findings of shunting to the SSS had intensified, and stenosis had occurred in the posterior third of the SSS. The venous return showed retrograde flow anteriorly to the SSS. The patient underwent endovascular embolization and tumor resection. The shunt had disappeared.

Conclusion: This report supports the proposal that impaired venous return is an important factor in the shunt occurrence of dAVF. Neurosurgeons should consider that cases of meningioma invading the venous sinuses may be complicated by dAVF and changes may occur over time.

Keywords: Dural arteriovenous fistula, Meningioma, Venous pressure

INTRODUCTION

The etiology of dural arteriovenous fistula (dAVF) is still unclear, but may include congenital factors and acquired factors such as venous sinus hypertension caused by obstruction of the venous sinuses due to trauma, surgical invasion, infection, or tumor.[ 14 ] dAVF commonly coexists with meningioma, sometimes associated with occlusion of the venous sinuses by the meningioma.[ 1 - 3 , 5 - 9 , 13 - 17 ] dAVF may also occur at the same site or a distant site from the tumor. Most dAVFs occurring at the same site as the meningioma are located in the transverse-sigmoid sinus and rarely occur in the superior sagittal sinus (SSS).

We experienced a rare case, in which cerebral angiography showed that the tumor feeding vessels of a parasagittal meningioma with SSS invasion were transformed into the pial feeder for a dAVF that developed in the same region, with acute aggravation of the vessels. This observation may suggest a link to the pathogenesis of tumor-associated dAVF.

CASE DESCRIPTION

A 71-year-old man presented with convulsive symptoms. Computed tomography (CT) showed a 3-cm isodense mass in the right parasagittal region. T1-weighted magnetic resonance (MR) imaging showed prominent enhancement with dural tail sign after gadolinium-diethylenetriaminepenta-acid acid administration, suggestive of meningioma [ Figures 1a and b ]. Cerebral angiography showed tumor staining from the anterior cerebral artery (ACA) posterior internal frontal artery (PIFA), with an arteriovenous shunt. Simultaneous congestion findings suggested impaired drainage to the SSS [ Figures 1c and d ]. Bilateral external carotid angiography showed shunt blood flow from the bilateral MMAs, superficial temporal artery (STA), and occipital artery (OA) to the SSS colocated with the tumor invasion site [ Figures 1e and f ]. No occlusion of the SSS was detected at the site of tumor invasion, and the SSS was perfused progressively without cortical venous reflux, so the dAVF was Cognard type I.[ 4 ]

After the initial diagnosis, the seizures were controlled and the neurological findings detected no abnormalities. The patient did not wish to receive treatment and was discharged for follow-up. Four years after the first diagnosis, he was hospitalized with status epilepticus causing intractable convulsive aggravation, so deep sedation/ventilator control was established for 5 days with propofol and midazolam. On admission, CT showed small subcortical hemorrhage in the left frontal lobe [ Figure 2a ]. Subsequent to the period of sedation, the patient continued to have prolonged impaired consciousness, Glasgow Coma Scale E1V1M4, severe right paralysis, and aphasia. MR imaging showed that the tumor had increased to 4 cm in size compared to 4 years ago [ Figures 2b and c ]. Carotid angiography showed a pial shunt from the ACA PIFA to the SSS and slight tumor staining [ Figure 2d ]. The findings of stagnant perfusion from the ACA were improved compared to the initial carotid angiography taken 4 years before [ Figure 2e ]. The SSS at the site of tumor infiltration was mildly stenotic but not occluded. The stenosis of the posterior third of the SSS and the development of dAVF seemed to have caused retrograde blood flow anteriorly in the SSS, indicating left frontal cortical venous regurgitation [ Figures 2e and f ]. External carotid angiography showed an increased shunt from the bilateral STAs, OAs, and MMAs to the SSS similar to the tumor invasion [ Figures 2g and h ]. The presence of retrograde venous sinus reflux and cortical venous reflux changed classification of the dAVF to Cognard type II a + b.[ 4 ] Subcortical hemorrhage in the left frontal lobe was thought to be hemorrhage associated with increased left frontal cortical venous pressure.

Figure 1:

Parasagittal meningioma. Axial (a) and coronal (b) T1-weighted magnetic resonance images showing an enhanced tumor in the right parasagittal region that extends toward the superior sagittal sinus (SSS) (white arrow). (c) Lateral right internal carotid angiogram, arterial phase, showing a tumor blush supplied by the anterior cerebral artery (ACA). (d) Lateral right internal carotid angiogram, capillary phase, showing stasis of tumor blood flow. (e) Lateral right external carotid angiogram showing that both the middle meningeal artery (MMA) and superficial temporal artery (STA) supply the dural arteriovenous fistula (dAVF). (f) Lateral left external carotid angiogram showing that both the MMA and STA supply the dAVF.

Figure 2:

(a) Computed tomography scan showing left frontal subcortical hemorrhage. Axial (b) and coronal (c) T1-weighted magnetic resonance images showing a homogeneous enhanced growing tumor in the right parasagittal region that extends toward the superior sagittal sinus (SSS) (white arrow). (d) Lateral right internal carotid angiogram, arterial phase, showing a pial AVF fed by the ACA (white dotted arrow). (e) Lateral right internal carotid angiogram, capillary phase, showing retrograde blood flow anteriorly in the SSS (white arrowhead). (f) Anteroposterior right internal carotid angiogram showing cortical venous reflux in the left frontal cortex (white asterisk). Lateral right (g) and left (h) external carotid angiograms showing that the MMA, STA, and occipital artery supply the dAVF and stenosis of the posterior third of the SSS (white arrowhead).

We hypothesized that the impaired cerebral venous drainage due to stenosis of the outflow tract of the SSS dAVF was the cause of the prolonged disturbance of consciousness. To reduce the shunt blood flow, ligation of bilateral STAs and embolization of the bilateral MMAs and OAs with platinum coils were performed. Post embolization angiography showed a significant decrease in shunt blood flow from the MMAs, OAs, and STAs. However, the tumor staining and pial shunt from the ACA, and the left frontal lobe cortical venous reflux persisted [ Video 1 ]. Ten days after the embolization, tumor removal and shunt dissection were performed [ Figure 3 ]. After coagulation and dissection of the feeding vessels from the ACA to the tumor, the shunting vein to the SSS was coagulated and dissected. The tumor was detached from the dural attachment, but the part that infiltrated into the SSS was not removed. The dural attachment was thoroughly coagulated but partially remained, resulting in Simpson Grade IV removal.

Video 1

Figure 3:

Tumor removal through right frontal craniotomy. The PIFA (white arrow) of the ACA was incised into the tumor (white asterisk) and a shunt vessel (white dotted arrow) was found on the anterior surface of the tumor.

Postoperative MR imaging showed partial removal of the tumor except for the part inside the SSS [ Figures 4a and b ]. Postoperative carotid angiography showed disappearance of tumor staining and shunt blood flow from the ACA, and disappearance of shunt blood flow from the bilateral OAs, STAs, and MMAs to the lesion [ Figures 4c-4f ]. The SSS showed anterograde blood flow and no cortical venous reflux in the left frontal lobe. The postoperative pathological findings were transitional meningioma. The patient’s condition slowly improved after the surgery, and right neglect disappeared. The right hemiparesis improved to manual muscle testing grade 2/5, and he was transferred to the rehabilitation center on postoperative day 12.

Figure 4:

Postoperative axial (a) and coronal (b) T1-weighted magnetic resonance images confirming gross total resection of the tumor except for the superior sagittal sinus (SSS) invasion (white arrow). (c) Postoperative lateral right internal carotid angiogram, arterial phase, demonstrating disappearance of a pial AVF fed by the ACA. (d) Lateral right internal carotid angiogram, venous phase, showing antegrade flow of the SSS. Lateral right (e) and left (f) external carotid angiograms demonstrating disappearance of the dAVF.

DISCUSSION

The rapid worsening of this case was apparently caused by stenosis of the posterior third of the SSS, which is the outflow route of the dAVF with increased shunt blood flow. In addition, cerebral angiography confirmed transformation of the tumor feeding vessels into the pial feeder of the dAVF.

dAVF is a rare disease, accounting for 10–15% of all intracranial arteriovenous malformations. However, the causes of dAVF are still unknown, but are thought to be associated with a history of head trauma or craniotomy, tumor, infection, or cerebral venous sinus embolism.[ 11 ] Meningeal tumor is often reported as associated with dAVF.[ 1 - 3 , 5 - 9 , 13 - 17 ] Most previous reports describe single cases, but a series of ten cases was reported in 2014.[ 2 ] However, the tumor and dAVF were located far apart in all cases, with no cases that occurred at the same site. Only ten cases of dAVF in the vicinity of meningeal tumor invading the venous sinuses are shown [ Table 1 ].[ 2 , 3 , 5 - 9 , 13 , 15 , 16 ] Five of these ten cases occurred in the transverse-sigmoid sinus,[ 2 , 3 , 5 , 6 , 16 ] four cases were tumor invasion of the SSS with concomitant dAVF,[ 8 , 9 , 13 , 15 ] one of which was not resected and was treated only as dAVF,[ 15 ] and two were hemangiopericytomas.[ 8 , 9 ] Only one case was meningioma.[ 13 ] Acute exacerbation of dAVF at the same region as an enlarging parasagittal meningioma has only been reported in our case.

Table 1:

Summary of patients with dAVF associated with meningeal tumor.

The mechanism of secondary dAVF in intracranial tumors has not been clarified. The proposed mechanisms by which meningiomas may be associated with dAVFs include direct increase in venous pressure due to invasion or compression of the venous sinuses by the tumor, indirect increase in venous pressure due to brain edema around the tumor, increase in venous pressure due to meningioma with abundant blood flow, hypercoagulability of the tumor itself, or induction of angiogenic substances such as hypoxia-inducible factor-1 and vascular endothelial growth factor by the meningioma.[ 2 , 5 - 7 , 14 ] The previous animal studies have shown that elevated venous pressure contributes to the formation of dAVF.[ 12 ] In this case, we speculate that the SSS stenosis caused by infiltration of the parasagittal meningioma into the SSS may have led to an increase in venous pressure and triggered the secondary development of dAVF.

Changes in the angiographic findings were also noteworthy. At the time of the first seizure, carotid angiography showed that the blood flow of the ACA, which is the feeding vessel of the tumor, stagnated due to the increased venous pressure of the SSS. However, 4 years later, the findings of flow stagnation in the tumor feeders were improved and predominantly appeared as a pial feeder of the dAVF in the SSS. At the time of the first seizure, flow stagnation in the tumor feeder may reflect relatively early changes in intracranial blood flow due to the venous hypertension associated with dAVF. Then, we speculate that the persistent stagnation of the tumor blood flow from the ACA may have triggered the formation of a pial shunt from the ACA to the SSS dAVF. We also speculate that the persistent increase in venous pressure caused stenosis of the SSS, leading to acute exacerbation of the dAVF symptoms. Therefore, this case may provide valuable data for elucidating the mechanism of secondary dAVF associated with tumors, based on our imaging of the changes in the shunting of the dAVF.

No definitive treatment policy has been established for cases of dAVF associated with meningioma. Some cases of dAVF spontaneously disappeared after only meningioma removal,[ 1 , 3 , 10 ] suggesting that elevated venous pressure due to tumor may be a cause of secondary dAVF. In our case, the SSS was not completely occluded, so the tumor inside the SSS was allowed to remain. Postoperative carotid angiography showed that the compression of the SSS by the tumor improved and the perfusion of the venous sinus progressively improved, but the tumor persisted in the SSS, so elevated venous pressure may have continued. Therefore, we believe that careful imaging follow-up is necessary not only to detect tumor recurrence, but also to monitor for dAVF recurrence in the future.

CONCLUSION

This case report may support the proposal that impaired venous return is an important factor in the shunting of dAVF. Neurosurgeons should consider that cases of meningioma invading the venous sinuses may be complicated by dAVF and changes may occur over time.

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Conflicts of interest

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