Combined antegrade and retrograde transarterial approaches for embolization of a traumatic carotid‑cavernous fistula with concomitant middle meningeal arteriovenous fistula

Abstract

Endovascular treatment (EVT) is a useful modality for traumatic carotid‑cavernous fistulas (CCFs); in rare cases, combined antegrade and retrograde transarterial approaches may be applied for embolization of the fistula with concomitant internal carotid artery (ICA) sacrifice and preservation of the ophthalmic artery (OphA). A 62‑year‑old female patient sustained a motor vehicle accident and developed proptosis, chemosis, and congestion in her right eye, while no abnormalities in ocular motility or visual acuity were noted. Computed tomography angiography confirmed the CCF. Under general anesthesia, digital subtraction angiography revealed a right CCF supplied antegradely by the ICA and retrogradely by the posterior communicating artery (PcomA). A left middle meningeal arteriovenous fistula was identified. Access to the basilar artery was established. A microcatheter was retrogradely navigated via the PcomA to reach the proximal ICA across the fistula. Then, another microcatheter was advanced into the cavernous sinus via an antegrade ICA approach. Subsequently, combined antegrade and retrograde transarterial coiling with ICA sacrifice for the CCF was successfully performed. During coiling, the patency of the OphA was monitored through the PcomA microcatheter. Afterwards, the middle meningeal arteriovenous fistula was embolized. At the 1‑month follow‑up, her right eye redness and swelling resolved, and at the 3‑month follow‑up, she had recovered well and returned to her normal status. Therefore, when embolizing the CCF with ICA sacrifice, if the PcomA is well‑developed, the combined antegrade and retrograde transarterial approaches can be used, which may facilitate the obliteration of the CCF and preservation of the OphA.

Introduction

Traumatic carotid‑cavernous fistula (CCF) is an abnormal direct shunt between the internal carotid artery (ICA) and cavernous sinus (CS) [1]. After trauma, a skull fracture or deformation can injure the cavernous ICA, resulting in immediate or delayed communication with the CS. The classic triad of acute proptosis, pulsatile tinnitus (or bruit), and chemosis signals the need for urgent intervention [2]. Endovascular treatment (EVT) is the current first‑line choice for CCF. Various EVT strategies exist, including reconstructive approaches that preserve the ICA and deconstructive approaches that occlude it [3].

When the ICA rupture is severe and large, and the CCF is high-flow with adequate collaterals, a deconstructive approach is indicated. During this approach, if the posterior communicating artery (PcomA) is well developed, coiling only the proximal ICA at the CCF site may still allow the PcomA to supply the fistula [4]. In addition, coiling the ICA beyond the CCF can occlude the CCF; however, excessive coiling can occlude the ophthalmic artery (OphA) origin and cause blindness. To avoid this, combined antegrade and retrograde transarterial coiling of the CS with ICA sacrifice, along with monitoring and protection of the OphA origin, is crucial. Nevertheless, this technique has been rarely reported.

In the present case, this method was employed. Additionally, the CCF was accompanied by a rare middle meningeal artery (MMA)‑to‑middle meningeal vein (MMV) fistula, which was also embolized.

Case presentation

Patient’s onset of symptoms and diagnosis

A 62-year-old female patient presented with redness and swelling of the right eye that had lasted for two weeks. One month prior, she was involved in a motor vehicle accident and fell to the ground. She experienced mild epistaxis and did not lose consciousness. She was taken to a local hospital, where head computed tomography (CT) showed no intracranial hemorrhage or skull fracture. On the same day, the epistaxis resolved. Over the following two weeks, she progressively developed redness and swelling of the right eye and began to hear a bruit. She was subsequently admitted to our hospital.

On physical examination, she was alert and followed commands appropriately. Muscle strength was 5/5 in all extremities. The right eye showed proptosis, chemosis, and congestion, with normal visual acuity and intact ocular motility. Auscultation over the right orbit and temporal region clearly revealed a bruit synchronous with the pulse. She denied any history of hypertension, diabetes mellitus, or cerebrovascular illnesses. Head CT and CT angiography were performed, revealing a right parasellar vascular abnormality with drainage via the right ophthalmic vein (OphV) and facial vein (Figs. 1A–C).

Fig. 1.

Diagnostic images of the case. (A) Left panel: CT of the sellar region demonstrates abnormally high density (asterisk) of the right CS. Right panel: CT of the lateral ventricle shows no abnormalities. (B) Bone window CT images reveal abnormal vascular dilatation within the CS (frame). No obvious skull fracture is identified. (C) Panel 1: Anteroposterior (left) and lateral (right) CTA views show abnormal drainage from the orbital cavity into the FV, which communicates with the OphV. Abnormal venous drainage is also seen in the suboccipital region (arrowhead). Panel 2: CTA demonstrates the dilated right CS (asterisk). Panel 3: CTA demonstrates that the dilated right CS (asterisk) drains into the superior OphV and subsequently into the FV. (D) Left panel: Arterial phase DSA of the right ICA shows that the ICA terminates at the CS, confirming a CCF; the asterisk marks the ruptured point of the ICA. Right panel: Venous phase DSA shows drainage into the CS, then into the bilateral IPSs and the right SPS, with multiple cortical venous drainages (arrowheads). No arteries are seen. (E) DSA images of the right VA illustrate that the posterior circulation supplies the CCF via the right posterior cerebral artery, then flows retrogradely into the PcomA (arrows) and right supraclinoid ICA, and finally reaches the ruptured point of the ICA (asterisks). (F) DSA images of the right ECA show no blood supply to the CCF. (G) DSA images of the left carotid artery identify a left MMA-MMV fistula (asterisks). In the right panel, compensation from the anterior circulation to the right MCA (frame) via the AcomA is seen.

Abbreviations: AcomA, anterior communicating artery; CCF, carotid-cavernous fistula; CS, cavernous sinus; CT, computed tomography; CTA, CT angiography; DSA, digital subtraction angiography; ECA, external carotid artery; FV, facial vein; ICA, internal carotid artery; IPS, inferior petrous sinus; L, left; MCA, middle cerebral artery; MMA, middle meningeal artery; MMV, middle meningeal vein; OphV, ophthalmic vein; PcomA, posterior communicating artery; R, right; SPS, superior petrous sinus; VA, vertebral artery.

A CCF was confirmed. All preoperative laboratory and imaging findings confirmed her eligibility for EVT.

Therapeutic process

Under general anesthesia, digital subtraction angiography (DSA) was performed, revealing a right traumatic CCF supplied antegradely by the right extracranial ICA and retrogradely by the posterior circulation via the right posterior cerebral artery (PCA), PcomA, and supraclinoid ICA. The CCF drained into the CS, then into the right OphV, the superior and inferior petrosal sinuses, and multiple cortical veins (Figs. 1D and E). The right external carotid artery was not involved as a feeder to the CCF (Fig. 1F). Additionally, a left MMA-MMV fistula was identified, with compensatory flow from the left anterior circulation to the right side clearly observed via the anterior communicating artery (AcomA) (Fig. 1G).

A 6F guiding support catheter was used to establish access to the right extracranial ICA. Access to the basilar artery (BA) was then established using a 6F long sheath and a 4.6F distal access catheter (AccuMedical, Beijing, China). An Echelon-10 microcatheter (Medtronic, Minneapolis, MN, USA) was retrogradely navigated, guided by a Synchro-14 microguidewire (Stryker Neurovascular, Fremont, CA, USA), to reach the right proximal ICA across the CCF via the right PCA, PcomA, and intracranial ICA (Fig. 2A). Another Echelon-10 microcatheter was then antegradely advanced into the CS (Fig. 2B).

Fig. 2.

Therapeutic course for the CCF of the case. (A) Left panel: DSA of the BA shows retrograde filling of the right CCF. Right panel: Roadmap image shows the microcatheter (arrow) passing retrogradely beyond the rupture point of the ICA into the proximal ICA via the BA, right PCA, PcomA, and right ICA. The asterisks indicate the rupture point of the ICA. (B) Roadmap images of the right ICA in anteroposterior (left panel) and lateral (right panel) views show the microcatheter (arrows) passing antegradely into the CS. The asterisk in the right panel indicates the rupture point of the ICA. (C) Left panel: Roadmap image shows antegrade coiling of the CS via the right ICA. Right panel: X‑ray image shows retrograde coiling of the rupture point of the ICA (asterisk) via the microcatheter advanced from the PcomA. (D) DSA via the PcomA microcatheter demonstrates the relationships among the ICA rupture point (asterisk), the origin of the OphA (arrow), the origin of the PcomA (arrow), and the coil masses. (E) Microcatheter angiography confirms patency of the right OphA. (F) X‑ray image shows the occlusion of the right proximal ICA below the CCF by coiling (asterisk). (G) DSA images via the PcomA microcatheter in lateral (left panel) and anteroposterior (right panel) views show patent OphA and intracranial ICA vessels. (H) DSA images of the right VA in anteroposterior (left panel) and lateral (right panel) views show the compensation from the posterior circulation via the PcomA to the right intracranial vessels.

Abbreviations: BA, basilar artery; CCF, carotid‑cavernous fistula; CS, cavernous sinus; DSA, digital subtraction angiography; ICA, internal carotid artery; MCA, middle cerebral artery; OphA, ophthalmic artery; PCA, posterior cerebral artery; PcomA, posterior communicating artery; R, right; VA, vertebral artery.

Antegrade coiling of the CS was first performed via the Echelon-10 microcatheter in the right extracranial ICA, with the following coils deployed: a MicroFrame 24mm–70cm coil (MicroPort NeuroTech Shanghai Co., Ltd.), a Target 14mm–30cm coil (Stryker Neurovascular, Fremont, CA, USA), a Target 11mm–30cm coil, and a Target 10mm–30cm coil. Then, the ruptured ICA was coiled retrogradely via the right PcomA using a Target 8mm–30cm coil (Figs. 2C and D). The microcatheter in the PcomA was subsequently withdrawn to monitor the OphA, thereby preventing its occlusion during further coiling (Fig. 2E). Next, the proximal ICA was coiled antegradely with Target 8mm–30cm and 7mm–30cm coils. Finally, the CS, the distal ICA, and the proximal ICA across the CCF were occluded, resulting in complete closure of the CCF (Fig. 2F).The OphA remained patent, and collateral flow to the right middle cerebral artery territory was adequate via the PcomA and AcomA (Figs. 2G and H).

After EVT for the CCF, the 6F long sheath and a 4.6F distal access catheter were repositioned into the left external carotid artery, clearly revealing the left MMA-MMV fistula. An Echelon-10 microcatheter was then advanced into the MMA near the fistula, and Onyx liquid embolic agent (Medtronic, Irvine, CA, USA) was injected (Figs. 3A and B). A residual fistula from the deep temporal artery remained and was embolized with Onyx. The MMA-MMV fistula was thereby obliterated (Figs. 3C–F).

Fig. 3.

Therapeutic course for the MMA-MMV fistula of the case. (A) DSA images of the left ECA demonstrate an MMA-MMV fistula (asterisks). (B) Left panel: Roadmap image shows the microcatheter (arrow) accessing the fistula point via the MMA. Right panel: X-ray image reveals the Onyx cast. (C) Left panel: DSA of the left ECA indicates that the DTA (arrow) still supplied the fistula (asterisk). Right panel: Roadmap image illustrates the microcatheter (arrow) accessing the fistula via the DTA. (D) Left panel: Roadmap image displays the Onyx cast penetrating the fistula point (asterisk). Right panel: X-ray image shows the Onyx cast. (E) Left panel: DSA of the left ECA confirms that the MMA-MMV fistula was obliterated. Right panel: DSA of the left carotid artery presents the compensation (frame) from the left anterior cerebral artery to the right middle cerebral artery. (F) Left panel: Reconstructed Xper CT bone window demonstrates the Onyx in the fistula. Right panel: Xper CT shows no abnormality in the cranium.

Abbreviations: CT, computed tomography; DSA, digital subtraction angiography; ECA, external carotid artery; DTA, deep temporal artery; L, left; MMA, middle meningeal artery; MMV, middle meningeal vein.

Postoperative and follow-up outcomes

Postoperatively, no complications were observed. Her right eye redness and swelling progressively resolved (Fig. 4A). On postoperative day 3, magnetic resonance (MR) images revealed no acute infarction (Fig. 4B). MR angiography demonstrated sufficient compensatory flow to the right middle cerebral artery via the AcomA and PcomA (Fig. 4C), and MR venography showed no evidence of any residual fistula (Fig. 4D). At the 1-month follow-up, her right eye appeared completely normal (Fig. 4E). By the 3-month follow-up, she had recovered well and resumed her normal daily activities.

Fig. 4.

Postoperative images of the case. (A) Photograph shows mild redness and swelling of the right eye. (B) Axial diffusion‑weighted MR images show no acute infarction. (C) MR angiography shows that after right ICA occlusion; no fistula is evident. Instead, the right intracranial vessels receive compensation from the left anterior circulation via the anterior communicating artery and right ACA (arrow), and from the posterior circulation via the right PcomA (arrow). (D) MR venography shows no evidence of the CCF or MMA‑MMV fistula. (E) One‑month postoperative follow‑up photograph shows that the right eye is normal.

Abbreviations: ACA, anterior cerebral artery; ICA, internal carotid artery; MMA, middle meningeal artery; MMV, middle meningeal vein. MR, magnetic resonance; PcomA, posterior communicating artery.

Discussion

For high‑flow traumatic direct CCFs, EVT is the preferred initial treatment (Fig. 5A). The goal is to obliterate the communication between the ICA and the CS while preserving ICA flow [5]. Available techniques include transarterial detachable balloon packing of the CS, placement of a covered stent in the ICA across the CCF to seal the ruptured ICA, and transarterial or transvenous packing of the CS using coils or other embolic materials (Figs. 5B–D). The flow diverter (FD) has also been used as an option [6]. After FD placement, the high‑flow CCF can be converted into a low‑flow, low‑pressure fistula, which may lead to spontaneous resolution due to thrombosis [7]. However, this technique should be applied with caution. For patients with severe ocular venous hypertension who cannot tolerate a slow resolution of the CCF, this technique may not be considered (Fig. 6).

Fig. 5.

Angiography and treatment of CCF with detachable balloons and coils. (A) CCF angiography. Panel 1: A case of traumatic direct CCF. DSA of the left ICA in anteroposterior (left) and lateral (middle) views demonstrates a CCF. The arrows indicate the intracranial ICA branches. The intracranial venous system is involved in the drainage pathway. Three‑dimensional DSA (right) reveals the ICA rupture (asterisk) leading to the CCF. Panel 2: Another case. DSA of the right ICA in anteroposterior (left) and lateral (middle) views depicts a CCF. The arrows indicate the intracranial ICA. The main drainage is through the OphV. Three‑dimensional DSA (right) identifies the ICA rupture (asterisk) leading to the CCF. (B) Detachable balloon occlusion. Left panel: DSA of the ICA reveals a CCF draining into the OphV, MCV, and IPS. Middle panel: X‑ray image shows a detachable balloon (arrow) positioned in the CS to seal the ICA rupture site. Right panel: Postoperative DSA confirms complete CCF closure. (C) Coil embolization. Left panel: DSA of the ICA demonstrates a CCF draining into the OphV, IPS, and PP. Middle panel: Unsubtracted DSA depicts coils (arrows) packing the CS. Right panel: Six-month follow‑up DSA confirms complete CCF closure. (D) Balloon‑assisted coil embolization. Left panel: DSA of the ICA illustrates a CCF draining into the OphV, MCV, IPS, and SPS. Middle panel: Roadmap image shows coils packing the CS with balloon protection (arrow). Right panel: Postoperative DSA confirms complete CCF closure.

Abbreviations: CCF, carotid‑cavernous fistula; CS, cavernous sinus; DSA, digital subtraction angiography; FV, facial vein; ICA, internal carotid artery; IPS, inferior petrosal sinus; L, left; MCV, middle cerebral vein; OphV, ophthalmic vein; PP, pterygoid plexus; R, right; SPS, superior petrosal sinus.

Fig. 6.

FD‑assisted embolization for CCF. (A) A case. Panel 1: CT reveals a left temporal lobe hematoma. Panel 2: CTA demonstrates dilated left OphV and FVs. Panel 3: DSA of the left ICA depicts a left CCF mainly draining into the OphV. Panel 4: Roadmap image shows the microcatheter (arrow) in the CS. Panel 5: X‑ray image (left) and unsubtracted DSA (right) illustrate the FD covering the ruptured ICA and coils in the CS. Panel 6: A postoperative 1‑week photograph documents regression of congestion in the left eye. Panel 7: Six-month follow-up DSA confirmed complete CCF closure. (B) Another case. Panel 1: CTA reveals dilated periorbital veins (circle) and FVs. Panel 2: DSA images of the left ICA in anteroposterior (left) and lateral (right) views show a left CCF with an extensive venous drainage involving the left OphV. Panel 3: DSA of the left external carotid artery demonstrates an MMA‑MMV fistula (arrow). Panel 4: X‑ray image shows coils in the CS and a microcatheter (arrow) in the distal middle cerebral artery. Panel 5: X‑ray image reveals the FD deployed in the ICA with good wall apposition. Panel 6: After coiling and FD deployment, DSA shows reduced CCF flow; the arrow indicates coiling to occlude the OphV origin. Panel 7: A postoperative 1‑week photograph shows regression of edema and congestion in the left eye.

Abbreviations: CCF, carotid‑cavernous fistula; CS, cavernous sinus; CT, computed tomography; CTA, CT angiography; DSA, digital subtraction angiography; FD, flow diverter; FV, facial vein; ICA, internal carotid artery; L: left; MMA, middle meningeal artery; MMV, middle meningeal vein; OphV, ophthalmic vein.

Traumatic direct CCFs have complex angiographic features. Chi et al. (2014) classified traumatic direct CCFs into small, medium, and large fistulas based on opacification of the anterior cerebral artery and/or middle cerebral artery. Specifically, opacification of both arteries defines a small fistula; either artery indicates a medium fistula; and neither defines a large fistula [8]. Based on this classification, coils are the preferred embolic material for small fistulas, whereas detachable balloons are recommended for medium and large ones. In cases where extensive ICA injury makes a large fistula ineligible for ICA preservation, ICA sacrifice may be necessary and serves as the last resort (Fig. 7).

Fig. 7.

ICA occlusion for CCF. (A) A case. Panel 1: DSA images of the left ICA in lateral (left) and anteroposterior (right) views reveal a CCF with extensive venous drainage involving the MCV and OphV. Panel 2: Three‑dimensional DSA confirms the ruptured point of the ICA (asterisk) that forms the CCF. The red frame indicates the left ICA; other visible vessels belong to the venous drainage. Panel 3: After coiling the ICA, DSA shows the OphA course; the arrow indicates the OphA origin. Panel 4: X‑ray image shows coils in the CS and ICA. The arrow indicates that the coils within the ICA cover the OphA origin. Panel 5: DSA of the right ICA demonstrates cross‑compensation to the left middle cerebral artery. (B) Another case. Panel 1: DSA images of the right ICA in anteroposterior (left) and lateral (right) views depict a CCF with extensive venous drainage involving the MCV, IPS, and OphV. Panel 2: Roadmap image shows two microcatheters in the CS ready for coiling the CCF. Panel 3: During coiling, DSA shows a coil loop entering the supraclinoid ICA (arrow). Panel 4: X‑ray image shows coils in the CS and ICA. The arrow indicates that the coils in the ICA occlude the OphA origin. Panel 5: DSA of the left ICA shows cross‑compensation to the right middle cerebral artery.

Abbreviations: CCF, carotid‑cavernous fistula; CS, cavernous sinus; DSA, digital subtraction angiography; FV, facial vein; ICA, internal carotid artery; IPS, inferior petrous sinus; L: left; MCV, middle cerebral vein; OphA, ophthalmic artery; OphV, ophthalmic vein; R: right.

In the presented case, the CCF was classified as a large fistula. Because the ICA on the side of the CCF terminated at the fistula with no visible intracranial arteries, the ICA failed to provide intracranial perfusion. The distal intracranial vasculature was compensated via the AcomA and ipsilateral PcomA, and preoperatively, the patient exhibited no ischemic symptoms. Thus, the ipsilateral ICA was functionally equivalent to occlusion. Occlusion of the ruptured ICA segment along with the involved CS was considered safe. Because the distal ICA was not visible by antegrade angiography, antegrade passage of a microcatheter into the distal ICA was prevented. In selective cases with adequate collateral circulation and a well-developed PcomA, if the PcomA caliber is sufficient for safe microcatheter navigation, a retrograde approach via the PCA, PcomA, and intracranial ICA can be used.

In the presented case, the retrograde approach successfully allowed access through the fistula into the proximal ICA; however, the tortuous and lengthy route made retrograde delivery of such stiff equipment as a covered stent, balloon catheter, or FD challenging. Despite this, the retrograde approach was still significant; it could be used to perform coiling and facilitate the safety of OphA preservation. In the absence of a well-developed PcomA, occluding the CCF along with its proximal ICA segment alone is sufficient [4]. Conversely, when the well-developed PcomA contributes to CCF filling, the occlusion should be performed distal to the ICA tear to block retrograde flow from the supraclinoid ICA. Therefore, the combined antegrade and retrograde approach was used in this case to occlude the ICA.

Retrograde access for EVT of a traumatic CCF has been reported. In Pagiola et al.'s report (2021), an arterial retrograde approach via the vertebral artery was used for CCF occlusion with coils because the ipsilateral ICA was dissected due to trauma [9]. In Crowe et al.'s report (2024), deconstructive coiling of the CCF via a retrograde approach was performed because of traumatic ICA occlusion. Coils achieved complete cure of the CCF and restoration of cerebral perfusion distal to the treated CCF [4].

During ICA trapping, sparing the OphA is strongly advised, since its obliteration may threaten vision. Nevertheless, if robust external carotid artery collaterals exist, the OphA can often be occluded without visual compromise [[10], [11], [12], [13]]. Hence, safeguarding the OphA is important. To avoid OphA occlusion in this case, combined antegrade and retrograde transarterial approaches were used. This technique not only occludes the segment distal to the presumed ICA tear to block retrograde flow from the ICA, but also allows identification of the OphA location for protection. This technique was therefore significant.

Due to cranial trauma, a rare MMA–MMV fistula coexists with CCF. This fistula, formed by simultaneous injury to the MMA and MMV, is a direct shunt from the MMA to the MMV. The drainage of the MMV can communicate with the diploic vein, superior sagittal sinus, and pterygoid plexus [14]. For such a fistula, liquid embolic agent embolization is a good choice. However, this fistula has a potential supply from the deep temporal artery, which results in residual fistula after embolization via the MMA. Subsequent embolization via the deep temporal artery had to be performed to obliterate it.

Conclusion

For traumatic direct CCFs supplied by a well‑developed PcomA, the combined antegrade and retrograde transarterial approaches can be employed—antegradely via the ipsilateral ICA and retrogradely via the PcomA—which may facilitate the obliteration of the CCF and preservation of the OphA.

Limitation

As this is a case report, the results should be interpreted cautiously. The combined antegrade and retrograde approaches are not necessary in all CCFs with a well‑developed PcomA; preserving the OphA and avoiding retrograde filling of the CCF from the PcomA may also be achievable with a conventional antegrade approach. In addition, the safety of microcatheter navigation via the PcomA should be considered, especially when the PcomA is not sufficiently thick. However, the case is significant because the combined approaches could facilitate the obliteration of the CCF and preservation of the OphA.

Patient consent

Written and informed consent was obtained from the patients for publication of this case report.