Diploic arteriovenous fistulas with marked cortical venous reflux

Abstract

Diploic arteriovenous fistulas are rare arteriovenous shunts involving the skull, which often drain antegradely into the internal or external jugular veins. Diploic arteriovenous fistulas with marked cortical venous reflux are extremely rare. Here, we present the case of a patient with diploic arteriovenous fistulas with marked cortical venous reflux and a literature review. A 73-year-old woman presented with headache. Magnetic resonance angiography revealed abnormal signal intensity in the diploic layer of the left frontal bone. Digital subtraction angiography demonstrated a diploic arteriovenous fistulas located in the left frontal bone. The arteriovenous fistulas were fed by multiple branches of the left external carotid artery, mainly from the middle meningeal artery, branches of the ophthalmic artery, and the inferolateral trunk. The fistulas drained into the cerebral cortical veins surrounding the frontal lobe via an emissary vein of the frontal bone. With the femoral arterial approach, transarterial catheterization into the shunted diploic vein was performed with a small tapered microcatheter, and the arteriovenous fistulas were completely embolized with N-butyl-2-cyanoacrylate. The patient was discharged without complications. No recurrent arteriovenous fistulas were observed during the 12-month follow-up period. Endovascular treatment is an effective technique for the curative treatment of diploic arteriovenous fistulas.

Introduction

Diploic veins (DVs) course within the diploë which is located between the inner and outer layers of the skull.¹ DVs communicate with the dural sinuses and pericranial veins, and they may become collateral routes when normal cerebral pathways are compromised. Arteriovenous fistulas (AVFs) involving the DVs are rare and are referred to as diploic AVFs or intraosseous dual AVFs.^2–10 Some authors have reported cases of diploic AVFs fed by branches of the external carotid artery (ECA) and draining into dural sinuses and pericranial veins.^2–10 Diploic AVFs with marked retrograde cortical venous reflux (CVR) are extremely rare. Here, we present a case of frontal diploic AVFs with marked cortical venous drainage with a literature review.

Case report

A 73-year-old woman presented with chronic headache and dizziness. She had no history of head trauma or cerebrovascular disease. Neurological examinations showed no abnormal findings, except for the bruit around the left frontal region. Magnetic resonance imaging (MRI) showed multiple flow voids surrounding the bilateral frontal lobes, and MR angiography showed a hyperintense signal in the diploic layer of the left frontal bone, and it connected with the frontal cortical veins via the emissary vein of the frontal bone. Left external carotid angiography showed diploic AVFs fed by multiple feeders from the left middle meningeal artery (MMA), the left superficial temporal arteries, and the maxillary artery (MA) and drained through the left frontal DV and the emissary of the frontal bone into the frontal cortical veins (Figure 1(a)). The anterior part of the superior sagittal sinus (SSS) was not delineated on internal carotid angiography (Figure 1(b)). The AVFs were also supplied by the anteromedial branch of the inferolateral trunk (ILT) of the left internal carotid artery (ICA) and the left ophthalmic artery (OPhA) (Figure 1(c) and (d)). Axial reconstructed images of rotational angiography of the left ECA and ICA clearly demonstrated the fistulous points and the draining veins of the cortical veins via the emissary vein (Figure 2(a) to (c)).

Figure 1.

(a) Frontal view of an angiogram of the left external carotid artery (ECA) showing the AVFs (white arrow) being fed by the middle meningeal artery, the superficial temporal artery, and the inferior maxillary artery, draining through the emissary vein into the cortical veins of the bilateral frontal lobe. (b) Lateral view of an angiogram of the left ECA showing an absence of the anterior part of superior sagittal sinus (black arrows). (c) Lateral view of an angiogram and (d) volume rendered image of the left internal carotid artery showing the AVFs fed by inferolateral trunk (white arrowheads) and the left ophthalmic artery.

Figure 2.

(a) Axial reconstructed images of rotational angiogram of the left external carotid artery showing diploic AVFs fed by multiple transosseous feeders from the left middle meningeal artery and the superficial temporal artery. (b) Axial reconstructed images of rotational angiogram of the left internal carotid artery showing the fistulous point (white arrowhead) fed by feeders from the left ophthalmic artery and the ILT. (c) Axial reconstructed images of rotational angiogram of the left internal carotid artery showing the diploic AVFs are draining through the emissary vein (EV) of the frontal bone into cortical vein.

MMA: middle meningeal artery.

Under general anesthesia, transarterial venous embolization was performed with the left femoral arterial approach. A 4F guiding sheath was advanced into the left ECA (Figure 3(a)), and a 1.3F microcatheter (DeFrictor, Medico's Hirata, Osaka, Japan) was advanced through the 4F guiding catheter into the anterior branch of the left MMA. The microcatheter was then introduced into the shunted DV via a transosseous feeder of the left MMA (Figure 3(b)). A balloon catheter (SHOURYU 7 mm/7 mm, Kaneka Medix, Osaka, Japan) was placed at the proximal portion of the left ECA to reduce the shunt flow. Then, 33% n-butyl-2-cyanoacrylate (NBCA) was injected into the DV through the microcatheter under flow control by balloon occlusion of the left ECA (Figure 3(c)). Immediately after embolization, angiography showed complete occlusion of the diploic AVFs (Figure 3(d)). The CT scans after the procedure showed the cast of NBCA in the DV of the left frontal bone and some feeders (Figure 3(e)). No complications were observed during or after the procedure. The symptoms resolved, and the patient was discharged uneventfully. Follow-up cerebral angiography 10 months after endovascular treatment showed no recurrent AVFs, and no symptoms recurred during the 12-month follow-up period.

Figure 3.

(a) Frontal view of selected angiograms of the left middle meningeal artery (MMA) showing the AVFs. (b) Frontal view of selective injection from a microcatheter advanced through the transosseous branch of the left MMA into the diploic vein. Black arrow indicates the tip of the microcatheter. (c) Frontal view of digital subtraction angiography during injection of 33% NBCA through the microcatheter in the left diploic vein showing NBCA-lipiodol filling in the diploic vein and feeders. (d) Frontal view of left external carotid angiography immediately after embolization showing complete obliteration of the diploic AVF. (e) CT scan after embolization showing NBCA cast in the diploic space and the emissary vein.

Discussion

DVs are lined by a single endothelial layer and are devoid of valves. These veins anastomose with each other and with a network of microscopic venous channels. The DVs are divided into four major channels: the frontal diploic vein (FDV), anterior temporal diploic vein (ATDV), posterior temporal diploic vein (PTDV), and occipital diploic vein (ODV). The FDV anastomoses with the supraorbital vein and the SSS. The ATDV anastomoses with the SSS, sphenoparietal sinus, and middle meningeal vein. The PTDV and ODV connect the posterior SSS with the transverse and sigmoid sinuses. From a clinical perspective, DVs may play an important role in collateral flow under pathological conditions such as sinus thrombosis or brain arteriovenous malformations and serve as the link between the CSF and circulatory system.¹

Diploic AVFs are rare entities, and their etiology remains unclear. We found 11 cases with 12 lesions, including our case, of AVFs involving DVs in the supratentorium by a literature review using Google Scholar and PubMed with a search index of “diploic arteriovenous fistula” and “intraosseous arteriovenous fistula” (Table 1). Several previously reported cases following trauma,⁴ spontaneous development,^2,5,8–10 and during the postpartum period suggest dural sinus thrombosis as an etiology.³ In the present case, there was no evidence of head trauma or sinus thrombosis. Regarding symptoms, 9 of 11 patients presented with benign symptoms including headache (n = 7), pulsatile tinnitus (n = 3), and the remaining two patients presented with aggressive neurological symptoms of disturbance of consciousness. Various drainage routes from the diploic AVFs have been reported. Rivera-Lara et al.⁵ proposed three potential venous outflow patterns: (1) dural sinus drainage only, (2) extracranial drainage only, (3) dural sinus and extracranial drainage. Yako et al.⁸ and White et al.¹⁰ reported a case of a diploic AVF draining into the cortical veins. In the present case, the diploic AVFs drained into the frontal cortical veins via the emissary vein of the frontal bone and showed marked CVR. We assume that the mechanism of marked CVR is hypoplasia of the anterior part of the SSS. Including our case, there were three lesions that had CVR, and two of the three cases showed conscious disturbance at presentation. CVR may be associated with aggressive symptoms as well as intracranial dural AVFs. Regarding feeding arteries, some authors have reported diploic AVFs fed by branches of the ECA.^2–10 Only one case of diploic AVFs fed by the pial artery was reported.² In this case, the diploic AVFs were fed by branches of the ECA, including the STA, MMA, MA, and branches of the ICA of OPhA and ILT. In the present case, the diploic AVFs were located near the supraorbital margin of the left frontal bone. The location of the AVFs is associated with the type of feeding arteries. For the cases fed by pial feeders and/or feeders from the ICA or OPhA, there is a potential risk or migration of embolic material into the ICA or OPhA and cortical branches via pial feeders during transarterial embolization with liquid embolic materials.

Table 1.

Literature review of AVF involving the DVs.

References	Symptoms	Predisposing factor	Feeders	Locations	Venous drainage	Treatment	Complications	Result	Follow-up
									Period (months)	Results
Benndorf and Lehmann2	Headache	–	MMA, Rt.MCA	Parietal	SS, SSS	TVE (coils), TAE (NBCA)	NA	Reduction	11	CO
			MMA	Parietal	SS, SSS	TAE (NBCA)	NA	CO	6	CO
Burger et al.3	Headache, pulsatile tinnitus	Pregnancy	MMA, STA	Parietal	Retro-auricular vein	Surgery, TVE (coils)	NA	CO	NA	NA
Shim et al.7	Headache, pulsatile tinnitus	Yelling	MMA	Frontal	MMV, TS	TAE (Onyx)	–	CO	NA	NA
Yako et al.8	Disturbance of consciousness	–	MMA	Frontal	CV	TAE (NBCA)	NA	CO	12	CO
Yoshioka et al.9	Headache, nausea	–	MMA	Frontal	EV	TAE (NBCA)	–	CO	NA	NA
Sakuma et al.6	Pulsatile tinnits	–	MMA, OA	Occipital	Rt.IJV	TAE (PVA, coils), TVE (coils)	NA	Reduction	3	CO
Rivera-Lara et al.5	Headache	–	MMA	Parietal	EV	TAE (NBCA)	–	CO	NA	NA
	Headache	–	MMA, OA, STA	Parietal	EV	TAE (NBCA, coils)	–	Reduction	4	Residual
Ishii et al.4	Speech impairment	Trauma	MMA	Parietal	NA	Not operated	Not operated	–	–	–
White et al.10	Confusion, word finding difficulty, short memory loss	–	ECA	Frontal	CV	TVE (coils, Onyx)	–	CO	3	CO
Present study	Headache	–	MMA, STA, MA, OPhA, ILT	Frontal	CV	TAE (NBCA)	–	CO	10	CO

ICH: intracranial hemorrhage; AEH: acute epidural hematoma; ECA: external carotid artery; MMA: middle meningeal artery; MCA: middle cerebral artery; OA: occipital artery; STA: superficial temporal artery; MA: maxially artery; OPhA: ophthalmic artery; ILT: inferiolateral trunk; CV: cortical vein; EV: extracranial veins; IJV: internal jugular vein; SSS: superior sagittal sinus; SS: sigmoid sinus; TS: transverse sinus; TVE: transvenous embolization; TAE: transarterial embolization; PVA: polyvinyl alcohol; NBCA: N-butyl cyanoacrylate; CO: complete occlusion; NA: not assessable.

Regarding the treatment, 11 lesions were treated by endovascular treatment, including transarterial embolization mainly, with NBCA or Onyx (n = 8), transvenous embolization with coils (n = 4), and transvenous embolization combined with surgery. The remaining one lesion was conservatively treated. Among the 11 lesions treated by endovascular techniques, 8 lesions were completely occluded immediately after embolization and 3 lesions showed reduction in the AVFs. Neither recurrence of AVFs nor procedure-related complications were reported.

In our review, transvenous and transarterial approaches have been applied more often. The transvenous approach is an effective approach when the AVF drains via an accessible venous channel to the jugular vein. In this case, we chose the transarterial approach using a small size microcatheter (1.3F) because the diploic AVFs drained into cortical veins alone. We could navigate the microcatheter into the shunted DV, and NBCA injection was performed from venous side. It is an important point for successful result for this case. Because the AVFs were fed by numerous feeders including some dangerous feeders from OPhA and ILT, NBCA injections from each branch would be needed if we could not catheterize into the shunted DV. It is essential for successful endovascular treatment of diploic AVFs to analyze the accessible feeders and the use of an appropriate technique and devices.

Diploic AVFs are rare arteriovenous shunts that usually drain into extracranial veins surrounding the skull, jugular veins, or dural sinuses but rarely into the cortical veins. Selective transarterial intravenous catheterization and embolization is a feasible and effective technique by using a small sized microcatheter for the curative treatment of diploic AVFs.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Kohei Tokuyama https://orcid.org/0000-0002-5807-4067