Spontaneous middle meningeal arteriovenous fistula without cortical venous reflux presenting with acute subdural hematoma: illustrative case

Masahiro Yabuki Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba, Iwate, Japan; and

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Yosuke Akamatsu Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba, Iwate, Japan; and
Department of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan

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Hiroshi Kashimura Department of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan

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Yoshitaka Kubo Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba, Iwate, Japan; and

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Kuniaki Ogasawara Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba, Iwate, Japan; and

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BACKGROUND

Dural arteriovenous fistula (AVF) without cortical venous reflux (CVR) has a relatively benign course. Here, the authors describe a patient presenting with subdural hematoma due to a middle meningeal AVF without CVR.

OBSERVATIONS

A 17-year-old male was admitted to the emergency department with acute headache without an episode of head trauma. Computed tomography demonstrated a left acute subdural hematoma (SDH). Because the nontraumatic SDH raised the suspicion of vascular pathology, emergent angiography was performed, which demonstrated an AVF fed by the middle meningeal artery and draining to the diploic vein via the serpentine meningeal vein without CVR. T2-weighted magnetic resonance imaging (MRI) revealed no signs of venous congestion. Given the proximity of the AVF to the SDH and the MRI findings, we suspected that the serpentine meningeal vein was responsible for the SDH. The patient was successfully treated with transarterial Onyx embolization. During the injection, Onyx migrated to the extravascular space following its penetration into the serpentine meningeal vein, suggesting the meningeal vein was a bleeding source of the subdural hematoma.

LESSONS

Despite the absence of cortical venous reflux, serpentine meningeal venous drainage of middle meningeal AVF can be a source of subdural hemorrhage.

ABBREVIATIONS

AVF = arteriovenous fistula; CT = computed tomograpy; CVR = cortical venous reflux; MMAVF = middle meningeal arteriovenous fistula; MMA = meningeal artery; MRA = magnetic resonace angiography; MRI = magnetic resonance imaging; SDH = subdural hematoma.

BACKGROUND

Dural arteriovenous fistula (AVF) without cortical venous reflux (CVR) has a relatively benign course. Here, the authors describe a patient presenting with subdural hematoma due to a middle meningeal AVF without CVR.

OBSERVATIONS

A 17-year-old male was admitted to the emergency department with acute headache without an episode of head trauma. Computed tomography demonstrated a left acute subdural hematoma (SDH). Because the nontraumatic SDH raised the suspicion of vascular pathology, emergent angiography was performed, which demonstrated an AVF fed by the middle meningeal artery and draining to the diploic vein via the serpentine meningeal vein without CVR. T2-weighted magnetic resonance imaging (MRI) revealed no signs of venous congestion. Given the proximity of the AVF to the SDH and the MRI findings, we suspected that the serpentine meningeal vein was responsible for the SDH. The patient was successfully treated with transarterial Onyx embolization. During the injection, Onyx migrated to the extravascular space following its penetration into the serpentine meningeal vein, suggesting the meningeal vein was a bleeding source of the subdural hematoma.

LESSONS

Despite the absence of cortical venous reflux, serpentine meningeal venous drainage of middle meningeal AVF can be a source of subdural hemorrhage.

ABBREVIATIONS

AVF = arteriovenous fistula; CT = computed tomograpy; CVR = cortical venous reflux; MMAVF = middle meningeal arteriovenous fistula; MMA = meningeal artery; MRA = magnetic resonace angiography; MRI = magnetic resonance imaging; SDH = subdural hematoma.

Although aggressive presentation of a dural arteriovenous fistula (AVF) is usually related to cortical venous reflux (CVR), dural AVFs without CVR commonly have a benign course.1–4 Middle meningeal arteriovenous fistula (MMAVF) is a direct connection between the middle meningeal artery and the middle meningeal vein.5–14 The natural course of most MMAVFs is likely benign given the lack of a direct connection with cortical veins. However, a limited number of patients have presented with aggressive symptoms such as intracranial hemorrhage.7,9,12–14 We demonstrate a rare case of spontaneous acute subdural hematoma (SDH) caused by an MMAVF without CVR and discuss the mechanism of hemorrhagic presentation based on the findings during transarterial Onyx embolization.

Illustrative Case

A 17-year-old previously healthy male presented to our emergency department with the acute onset of headache. The patient had no history of head trauma. Computed tomography (CT) revealed a left acute SDH without significant mass effect (Fig. 1A). T2-weighted magnetic resonance imaging (MRI) performed on admission showed no signal, suggesting venous congestion (Fig. 1B). Serial source images of 1.5-T time-of-flight magnetic resonance angiography (MRA) demonstrated the connection of abnormal flow-related enhancement from the dura mater to the diploic space (Fig. 1C). Because the nontraumatic SDH raised the suspicion of vascular pathology, the patient underwent six-vessel angiography 2 days after admission, which showed a dural AVF fed by the middle meningeal artery (MMA) and draining into the diploic vein without CVR on the left external carotid injection (Fig. 1D and E). Given the consistency of the site of the fistula and SDH, we suspected that the serpentine meningeal vein was responsible for the SDH and decided to perform transarterial Onyx embolization.

FIG. 1.
FIG. 1.

A: Admission brain CT showing a left acute SDH. B: Axial T2-weighted MRI revealing a SDH without a hyperintensity sign in the left cerebral hemisphere. C: Serial time-of-flight MRA scans demonstrating abnormal flow-related enhancement arising from dura mater (arrow) in the diploic space (arrowheads). D and E: Left external carotid injection, anteroposterior and lateral views, demonstrating a dural AVF fed by the MMA and draining into the diploic vein. Black arrowheads indicate the fistulous connection.

A 6-Fr FUBUKI dilator kit (Asahi Intec Co. Ltd.) was introduced into the left external carotid artery via a right femoral access. After systemic heparinization, a DeFrictor Bull catheter (Medico’s Hirata) was navigated into the left MMA over a CHIKAI ×10 200-cm microguidewire (Asahi Intech Co. Ltd.). Superselective injection from the left MMA, just proximal to the AVF, clearly showed a serpentine middle meningeal vein draining into the diploic vein (Fig. 2A and B). Based on these findings, we diagnosed the AVF as an MMAVF. Thereafter, continuous injection of Onyx 18 (EV3) was performed through the microcatheter. During the Onyx injection, the liquid embolic migrated to the extravascular space after its penetration into the serpentine meningeal vein, suggesting that the serpentine meningeal vein was the bleeding source of the SDH (Fig. 2C). A postoperative T2-weighted MRI demonstrated the deposition of Onyx in the superficial area of the SDH (Fig. 2D). Postoperative left external carotid injection 6 months after the intervention showed durable obliteration of the fistula (Fig. 2E and D). Because the patient presented no neurological symptoms, hematoma removal was not performed. The patient was free from symptoms of recurrence up to the 2-year follow-up examination.

FIG. 2.
FIG. 2.

A and B: Magnified images of the left MMA injection, anteroposterior and lateral views, showing MMAVF draining into the diploic vein (white arrows) through the serpentine middle meningeal vein (black arrows). Black arrowheads indicate a microcatheter placed just proximal to the fistulous point. C: Magnified on-subtracted image, lateral view, showing the Onyx cast in the serpentine middle meningeal vein (black arrows) and the extravasated Onyx (white dotted line). D: Sagittal T2-weighted magnetic resonance image obtained 2 days after embolization, showing the artifact of Onyx at the surface of the SDH (white arrowheads). E and F: Left external carotid injection, anteroposterior and lateral views, 6 months after the treatment showing durable obliteration of the fistula.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

We report a patient with an idiopathic MMAVF who presented with acute subdural hemorrhage. This case report highlights the important issue that an MMAVF without CVR can cause intracranial hemorrhage if the serpiginous meningeal draining system exists.

Although most of the previous cases have been the subject of case reports, the majority of MMAVFs have been associated with traumatic or iatrogenic insults,8,10,11 although some idiopathic cases have also been reported.5,11 The natural history of MMAVF remains unknown given the rarity of the lesion. Based on a nonfixed cadaveric study, there are no direct connections between cortical veins and the middle meningeal veins or the parietal dioploic veins; middle meningeal veins communicate with the diploic veins and the dural sinus via the emissary veins.15,16 Therefore, MMAVFs are unlikely to be associated with CVR or intracranial hemorrhage, except in some conditions, including extensive thrombosis, variations of dural drainage, or high-flow fistulas. There have been six cases of MMAVF presenting with spontaneous intracranial hemorrhage, including four cases of acute subdural hemorrhage and two cases of intraparenchymal hemorrhage (Table 1).7,9,12–14 Among these six cases, fistulous flow drained into the diploic vein via the serpentine middle meningeal vein without CVR in five cases. Although only one case had cortical venous drainage, the meningeal draining veins were indirectly connected with cortical vein through the diploic vein and falcine vein due to the high flow of the fistula.12 Therefore, direct connections between the feeding artery and cortical veins were not observed in all cases. Yamauchi et al.13 reported a case of MMAVF without CVR presenting with SDH and verified that the thin-walled and serpentine meningeal vein located at the dura propria (inner layer of the dura mater) was a bleeding source. Sato et al.14 reported a case of spontaneous intraparenchymal hematoma from an idiopathic MMAVF without CVR and proposed that varix development in the middle meningeal vein was a significant factor in hemorrhagic presentation. In the present case, during transarterial Onyx injection, the cast firstly penetrated into the serpentine middle meningeal vein and was subsequently extravasated into the subdural space. Furthermore, postoperative MRI demonstrated Onyx cast on the surface of the SDH and no apparent edematous change in the cerebral cortices. Therefore, we concluded that the serpentine middle meningeal vein was the source of the SDH.

TABLE 1.

Literature review of middle meningeal arteriovenous fistula presenting with intracranial hemorrhage

Outcome
Authors & YearAge (yrs)/SexHemorrhage TypeFeeding ArteryDraining VeinTreatmentAngiographicmRS Score
Kohyama et al., 2009760/MSubduralMMAMeningeal vein & diploic veinTAECO0
Ogawa et al., 2010927/MSubduralMMA, OAMeningeal vein & diploic veinOpCO0
Yako et al., 20151262/FSubcorticalMMADiploic vein & indirect connection w/ cortical veinTAECO3
Yamauchi et al., 20191329/MSubduralMMAMeningeal vein & diploic veinTAE & opCO0
Sato et al., 20211445/FSubcorticalMMAMeningeal veinTAECO0
Present case15/MSubduralMMAMeningeal vein & diploic veinTAECO0

CO = complete obliteration; MMA = middle meningeal artery; mRS = modified Rankin Scale; OA = occipital artery; TAE = transarterial embolization.

In terms of the treatment of MMAVFs, most MMAVFs are fed by the convexity branch of the MMA and amenable to the endovascular approach. In the present case, transarterial Onyx embolization was performed without hematoma removal because of the slight mass effect of the SDH. However, surgical disconnection of the fistula and removal of the hematoma should also be considered if mass effect of the intracranial hematoma is significant.

Lessons

MMAVFs draining into serpentine middle meningeal veins can lead to intracranial hemorrhage. Regardless of the presence of CVR, early complete obliteration of the fistula should be considered in those cases presenting with intracranial hemorrhage because rebleeding can occur and lead to adverse outcomes.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Akamatsu, Ogasawara. Acquisition of data: Akamatsu, Kashimura, Kubo. Analysis and interpretation of data: Akamatsu, Kashimura, Kubo. Drafting the article: Akamatsu, Yabuki. Critically revising the article: all authors. Reviewed submitted version of manuscript: Akamatsu, Yabuki. Approved the final version of the manuscript on behalf of all authors: Akamatsu. Administrative/technical/material support: Kubo. Study supervision: Kashimura.

References

  • 1

    Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194(3):671680.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg. 1995;82(2):166179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace MC. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg. 1996;85(5):830837.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Kuwayama N, Kubo M, Tsumura K, Yamamoto H, Endo S. Hemodynamic status and treatment of aggressive dural arteriovenous fistulas. Acta Neurochir Suppl (Wien). 2005;94(5):123126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chandrashekar HS, Nagarajan K, Srikanth SG, Jayakumar PN, Vasudev MK, Pandey P. Middle meningeal arteriovenous fistula and its spontaneous closure. A case report and review of the literature. Interv Neuroradiol. 2007;13(2):173178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Pritz MB, Pribram HF. Intracerebral hemorrhage from a middle meningeal arteriovenous fistula with a giant venous varix. Surg Neurol. 1992;37(6):460463.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Kohyama S, Ishihara S, Yamane F, Kanazawa R, Ishihara H. Dural arteriovenous fistula presenting as an acute subdural hemorrhage that subsequently progressed to a chronic subdural hemorrhage: case report. Minim Invasive Neurosurg. 2009;52(1):3638.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Sakata H, Nishimura S, Mino M, et al. Serial angiography of dynamic changes of traumatic middle meningeal arteriovenous fistula: case report. Neurol Med Chir (Tokyo). 2009;49(10):462464.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Ogawa K, Oishi M, Mizutani T, Maejima S, Mori T. Dural arteriovenous fistula on the convexity presenting with pure acute subdural hematoma. Acta Neurol Belg. 2010;110(2):190192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Abla AA, Albuquerque FC, Theodore N, Spetzler RF. Delayed presentation of traumatic cerebral and dural arteriovenous fistulae after a BB gun accident in a pediatric patient: case report. Neurosurgery. 2011;68(6):E1750E1754, discussion E1754–E1755.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Almefty RO, Kalani MY, Ducruet AF, Crowley RW, McDougall CG, Albuquerque FC. Middle meningeal arteriovenous fistulas: A rare and potentially high-risk dural arteriovenous fistula. Surg Neurol Int. 2016;7(9)(suppl 9):S219S222.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Yako R, Masuo O, Kubo K, Nishimura Y, Nakao N. A case of dural arteriovenous fistula draining to the diploic vein presenting with intracerebral hemorrhage. J Neurosurg. 2016;124(3):726729.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Yamauchi K, Takenaka S, Iida T, Sakai H. A case of spontaneous acute subdural hemorrhage caused by a dural arteriovenous fistula on the convexity without cortical venous reflux. Case Rep Neurol. 2019;11(3):312318.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sato D, Saito H, Suzuki T, Ota T. Idiopathic middle meningeal artery and middle meningeal vein fistula presenting as temporal intraparenchymal hemorrhage. Interv Neuroradiol. 2021;27(2):281284.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    San Millán Ruíz D, Fasel JH, Rüfenacht DA, Gailloud P. The sphenoparietal sinus of breschet: does it exist? An anatomic study. AJNR Am J Neuroradiol. 2004;25(1):112120.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Coppini L, Sciascia R. Recent contribution to the knowledge of the venous circulation of the head: breschet’s spheno-parietal sinus. Article in Italian. Boll Soc Ital Biol Sper. 1963;39:13051309.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • FIG. 1.

    A: Admission brain CT showing a left acute SDH. B: Axial T2-weighted MRI revealing a SDH without a hyperintensity sign in the left cerebral hemisphere. C: Serial time-of-flight MRA scans demonstrating abnormal flow-related enhancement arising from dura mater (arrow) in the diploic space (arrowheads). D and E: Left external carotid injection, anteroposterior and lateral views, demonstrating a dural AVF fed by the MMA and draining into the diploic vein. Black arrowheads indicate the fistulous connection.

  • FIG. 2.

    A and B: Magnified images of the left MMA injection, anteroposterior and lateral views, showing MMAVF draining into the diploic vein (white arrows) through the serpentine middle meningeal vein (black arrows). Black arrowheads indicate a microcatheter placed just proximal to the fistulous point. C: Magnified on-subtracted image, lateral view, showing the Onyx cast in the serpentine middle meningeal vein (black arrows) and the extravasated Onyx (white dotted line). D: Sagittal T2-weighted magnetic resonance image obtained 2 days after embolization, showing the artifact of Onyx at the surface of the SDH (white arrowheads). E and F: Left external carotid injection, anteroposterior and lateral views, 6 months after the treatment showing durable obliteration of the fistula.

  • 1

    Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194(3):671680.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg. 1995;82(2):166179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace MC. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg. 1996;85(5):830837.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Kuwayama N, Kubo M, Tsumura K, Yamamoto H, Endo S. Hemodynamic status and treatment of aggressive dural arteriovenous fistulas. Acta Neurochir Suppl (Wien). 2005;94(5):123126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chandrashekar HS, Nagarajan K, Srikanth SG, Jayakumar PN, Vasudev MK, Pandey P. Middle meningeal arteriovenous fistula and its spontaneous closure. A case report and review of the literature. Interv Neuroradiol. 2007;13(2):173178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Pritz MB, Pribram HF. Intracerebral hemorrhage from a middle meningeal arteriovenous fistula with a giant venous varix. Surg Neurol. 1992;37(6):460463.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Kohyama S, Ishihara S, Yamane F, Kanazawa R, Ishihara H. Dural arteriovenous fistula presenting as an acute subdural hemorrhage that subsequently progressed to a chronic subdural hemorrhage: case report. Minim Invasive Neurosurg. 2009;52(1):3638.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Sakata H, Nishimura S, Mino M, et al. Serial angiography of dynamic changes of traumatic middle meningeal arteriovenous fistula: case report. Neurol Med Chir (Tokyo). 2009;49(10):462464.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Ogawa K, Oishi M, Mizutani T, Maejima S, Mori T. Dural arteriovenous fistula on the convexity presenting with pure acute subdural hematoma. Acta Neurol Belg. 2010;110(2):190192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Abla AA, Albuquerque FC, Theodore N, Spetzler RF. Delayed presentation of traumatic cerebral and dural arteriovenous fistulae after a BB gun accident in a pediatric patient: case report. Neurosurgery. 2011;68(6):E1750E1754, discussion E1754–E1755.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Almefty RO, Kalani MY, Ducruet AF, Crowley RW, McDougall CG, Albuquerque FC. Middle meningeal arteriovenous fistulas: A rare and potentially high-risk dural arteriovenous fistula. Surg Neurol Int. 2016;7(9)(suppl 9):S219S222.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Yako R, Masuo O, Kubo K, Nishimura Y, Nakao N. A case of dural arteriovenous fistula draining to the diploic vein presenting with intracerebral hemorrhage. J Neurosurg. 2016;124(3):726729.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Yamauchi K, Takenaka S, Iida T, Sakai H. A case of spontaneous acute subdural hemorrhage caused by a dural arteriovenous fistula on the convexity without cortical venous reflux. Case Rep Neurol. 2019;11(3):312318.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sato D, Saito H, Suzuki T, Ota T. Idiopathic middle meningeal artery and middle meningeal vein fistula presenting as temporal intraparenchymal hemorrhage. Interv Neuroradiol. 2021;27(2):281284.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    San Millán Ruíz D, Fasel JH, Rüfenacht DA, Gailloud P. The sphenoparietal sinus of breschet: does it exist? An anatomic study. AJNR Am J Neuroradiol. 2004;25(1):112120.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Coppini L, Sciascia R. Recent contribution to the knowledge of the venous circulation of the head: breschet’s spheno-parietal sinus. Article in Italian. Boll Soc Ital Biol Sper. 1963;39:13051309.

    • PubMed
    • Search Google Scholar
    • Export Citation

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