Keywords dissection - pseudoaneurysm - carotid-cavernous fistula - high-flow bypass - EC-IC bypass
Introduction
Traumatic intracranial pseudoaneurysms are uncommon, comprising less than 1% of intracranial aneurysms.[1 ] Even rarer are pseudoaneurysms originating from the supraclinoid segment of the internal carotid artery (ICA), especially when causing a direct carotid-cavernous fistula. The supraclinoid or intradural ICA pseudoaneurysms treatment includes surgical trapping,[1 ]
[2 ] reconstruction clip,[3 ] direct clipping,[4 ]
[5 ] and endovascular therapy.[6 ]
[7 ]
[8 ]
[9 ]
[10 ]
[11 ]
[12 ]
[13 ]
[14 ] Trapping the parent artery with revascularization could provide complete aneurysm occlusion and prevent rebleeding, aneurysm recurrence, and ischemic complications, regardless of the complexity of the procedure. This report describes the first case of traumatic supraclinoid ICA pseudoaneurysm causing a direct CCF treated with surgical trapping and revascularization to eradicate the aneurysms and fistula.
Case Description
Three days following a motorcycle accident, the patient, a 17-year-old male, was transferred to our department. Physical examination revealed a Glasgow coma score of 13 and grade IV right-sided motor function. No light perception was present in the left eye due to indirect traumatic optic neuropathy, along with moderate proptosis and conjunctival congestion. Initial brain computed tomography (CT) revealed an intracerebral hemorrhage in the right frontal lobe with diffuse subarachnoid hemorrhage ([Fig. 1A ]) and an extensive anterior skull base fracture ([Fig. 1B ]), suggesting a blunt cerebrovascular injury. CT-angiography revealed left cavernous sinus and superior ophthalmic vein enlargement ([Fig. 1C ]). Additionally, an aneurysm was detected in the right anterior cerebral artery (ACA) ([Fig. 1D ]). Injection of contrast material into the right ICA revealed a right proximal A2 aneurysm with faint crossflow to the left middle cerebral artery (MCA) ([Fig. 1E ]). Cerebral angiography of the left ICA injection revealed direct carotid-cavernous fistula (CCF) and cortical reflux to the Sylvian vein, where the left ACA could not be seen due to the steal effect ([Fig. 1F ]). The anterior choroidal artery (AChA) and the left posterior communicating artery (PcomA) were not visible. Along with the pseudoaneurysm and narrowing of the distal ICA, the fistula was rerouted from the supraclinoid ICA. An enlarged cavernous sinus venous pouch that empties into the superior ophthalmic vein and inferior petrosal sinus was seen ([Fig. 1G–I ]). Injection of the left vertebral artery (VA) demonstrated collateral to the right MCA territory and left cavernous sinus via the PcomA but not to the left MCA territory ([Fig. 1J,K ]). The patient was diagnosed with a ruptured right ACA traumatic pseudoaneurysm and a left ICA dissecting pseudoaneurysm with direct CCF. The goal of our treatment was to eradicate the aneurysm and fistula to prevent rebleeding. Concerning parent vessel sacrifice, we adhered to the universal bypass strategy because this patient had already developed right hemiparesis, indicating that the left cerebral hemisphere would not have been adequately supplied by collateral circulation. Moreover, the patient's hemiparesis could be attributed to the constriction of the left supraclinoid ICA and the steal phenomenon originating from the CCF. As a result, we decided to simultaneously occlude the left ICA with an extracranial-intracranial (EC-IC) bypass and the right A2 aneurysm with an A3-A3 side-to-side bypass.
Fig. 1 (A ) Preoperative CT brain showed right frontal intracerebral hemorrhage with diffuse subarachnoid hemorrhage. (B ) Fracture of the ethmoid (arrowheads ) and sphenoid sinus (arrow ). (C ) Preoperative CT-angiography revealed enlargement of the left cavernous sinus (arrow ) and superior ophthalmic vein (arrowheads ). (D ) Sagittal view showing an out-pouching lesion at an ACA (arrow ). (E ) Right ICA injection showing right proximal A2 pseudoaneurysm (arrow ) with the faint collateral to left MCA territory (arrowheads ). (F ) Anteroposterior (AP) view of left ICA injection showing a direct CCF drained to intercavernous sinus (arrowheads ) and reflux to the Sylvian vein (arrow ). (G ) An early phase of left ICA injection in lateral view showing pseudoaneurysm and fistula arising from supraclinoid ICA (arrow ) with tapering of the distal ICA (arrowheads ). (H , I ) (continued) Pseudoaneurysm sac (asterisk ) and daughter bleb (black
arrow ) shunted to the cavernous sinus which drained into the inferior petrosal sinus (arrowheads ) and the superior ophthalmic vein (white
arrow ). (J, K ) AP and lateral view of left VA injection showing collateral to right MCA territory and to the left cavernous sinus via PcomA without supplying the left MCA territory (arrowheads ).
Operation
The patient was brought to the hybrid operating room on the fifth post-rupture day. We decided to perform an ICA trapping with EC-IC bypass to:
Restore the flow to the left cerebral hemisphere for the prevention of ischemia due to hemodynamic change during anesthesia,
Eliminate the rupture risk during surgery in which the bleeding could be massive since it was an ICA aneurysm, and
Facilitate the subsequent A3-A3 bypass by reducing the brain edema caused by cortical reflux.
Due to the cortical reflux, the arterialized Sylvian vein and moderate brain edema were observed following durotomy ([Fig. 2A ]). The superficial temporal artery (STA)-middle cerebral artery (MCA) bypass was performed to supply distal flow during the EC-IC bypass ([Fig. 2B ]). Then, an EC-IC bypass was undertaken using saphenous vein graft ([Fig. 2C,D ]). During microsurgical dissection, active bleeding occurred; consequently, the cervical ICA was ligated, and a clip was placed on the intracranial ICA proximal to the origin of an anterior choroidal artery. As a result, the pseudoaneurysm and cavernous sinus pouch enlargement were identified ([Fig. 2E ]). However, the bleeding persisted despite ICA occlusion, which could be explained by retrograde flow from an ophthalmic artery (OA) and external carotid artery (ECA)-ICA anastomosis ([Fig. 2F,G ]). The cavernous sinus was then packed with Gelfoams, and a second clip was placed adjacent to the cavernous sinus roof to obliterate retrograde flow from an ophthalmic artery ([Fig. 2H,I ]).
Fig. 2 Intraoperative findings following durotomy. (A ) Arterialized Sylvian vein with brain congestion due to cortical reflux (arrowheads ). (B ) Patent STA-MCA anastomosis (asterisk ) confirmed with indocyanine green videography. (C ) EC-IC bypass using saphenous vein graft (black asterisk ) was anastomosed to the superior division of the left M2 segment while the STA graft (white asterisk ) supplied the distal flow during temporary occlusion. (D ) Saphenous vein graft was then anastomosed to the prepared ECA (asterisk ). (E ) The left subfrontal approach showing outlined of the pseudoaneurysm (black dotted line ) of left ICA (asterisk ) protruded through the cavernous sinus roof (arrow ) with clip application distal to the pseudoaneurysm. Anteroposterior (AP) and lateral view of left ECA injection (F , G ) Filling of contrast to the left cavernous sinus from ECA-ICA anastomoses (arrowheads ). (H ) Gelfoams (asterisk ) were packed to obliterate the CCF. (I ) Another clip application at proximal supraclinoid ICA. (J ) The previous arterialized vein was returned to normal (arrowheads ) after fistula obliteration with patent EC-IC anastomosis (asterisk ). AP and lateral view of left ECA injection showing (K ) Patency of the saphenous vein graft (black arrowheads ) filling to left cerebral hemisphere and (L ) Middle meningeal artery (white arrowheads ) supplying the ophthalmic collaterals. (M ) Sequential slice showing the retinal blush (arrow ) supplied by the ECA collaterals. (N ) Left VA contrast injection showing the ACA aneurysm (arrow ) by the flow through right PcomA (arrowheads ) without filling the fistula.
After the fistula was repaired, a red Sylvian vein was turned into normal ([Fig. 2J ]). Intraoperative digital subtraction angiography (DSA) demonstrated complete aneurysm and fistula obliteration, as well as EC-IC bypass patency ([Fig. 2K ]). Because the ICA was trapped, an ophthalmic artery could not be visualized, but the ECA injection showed that the retinal blush supplied by the ECA collaterals via the middle meningeal artery ([Fig. 2L,M ])
Left VA injection revealed an ACA aneurysm through the PcomA without filling to the fistula ([Fig. 2N ]).
The planned ACA trapping with bypass was not performed due to brain edema caused by prior venous congestion, which made the interhemispheric approach difficult. Instead, craniectomy was performed based on brain edema, with consideration for the patency of the anastomosis due to elevated intracranial pressure. The second surgery was performed a week after the brain edema had subsided. First, the bicoronal incision was extended from the previous cut. Then, an additional right pterional in conjunction with a bifrontal craniotomy was performed. Finally, after conducting a side-to-side A3-A3 bypass via an interhemispheric approach ([Fig. 3A,B ]), the aneurysm was trapped through the lateral subfrontal corridor ([Fig. 3C ]). Intraoperative DSA demonstrated the complete disappearance of an aneurysm and A3-A3 bypass patency ([Fig. 3D,E ]).
Fig. 3 Intraoperative findings of the second operation. (A, B ) Patency of A3-A3 side-to-side anastomosis via an interhemispheric approach confirmed with indocyanine green videography. (C ) Surgical view of right lateral subfrontal approach showing clips application at proximal (arrow ) and distal (asterisk ) to a pseudoaneurysm (black dotted line ) without violating recurrent artery of Heubner (arrowheads ). AP and lateral view of right ICA injection. (D, E ) Complete disappearance of an aneurysm (arrow ) with patent A3-A3 anastomosis (arrowheads ). (F ) CT brain at 3 months follow-up showing no infarction with evidence of left craniectomy.
Postoperative Course
The postoperative course was uneventful. At discharge, the patient was graded on a scale of 1 on the modified Rankin scale (mRS). The motor on the right side has returned to grade V. His left visual acuity improved in response to hand motion. Three months later, CT showed no evidence of infarction ([Fig. 3F ]). CT-angiography revealed complete obliteration of the aneurysms with no remaining fistula, and all anastomoses were patent ([Fig. 4A ], [4B ]). The cranioplasty had been planned.
Fig. 4 (A ) Schematic drawing of the procedures (B ) 3D reconstruction via CT angiography, showing patency of EC-IC bypass (arrowheads ) and A3-A3 anastomosis (arrow ) without evidence of the pseudoaneurysms. AChA, anterior choroidal artery; ECA, external carotid artery; ICA, internal carotid artery; OA, ophthalmic artery; RAH, recurrent artery of Heubner.
Discussion
To our knowledge, our case is the first to perform successful surgical trapping with EC-IC bypass in traumatic supraclinoid ICA pseudoaneurysm associated with direct CCF. Furthermore, this case was complicated by an ACA pseudoaneurysm where another in situ A3-A3 bypass was required. The reported cases of traumatic supraclinoid ICA dissecting aneurysm associated with carotid-cavernous fistula are summarized in [Table 1 ].
Table 1
Summary of reported cases of traumatic supraclinoid ICA pseudoaneurysm associated with carotid-cavernous fistulas
Author, Year
Age (years)/sex
Dissection/pseudoaneurysm location
Presentations
Treatment
Complete occlusion
Complications/
second treatment
Benoit et al, 1973[1 ]
45/M
Right supraclinoid ICA pseudoaneurysm-CS fistula
Right direct CCF
Surgical trapping with cavernous sinus packing
Yes
Oculomotor paresis
Reddy et al, 1981[2 ]
14/M
Left supraclinoid ICA giant pseudoaneurysms-CS fistula
Left direct CCF
Surgical trapping with cavernous sinus packing
Yes
Transient abducens nerve palsy
Komiyama et al, 1991[6 ]
42/M
Right supraclinoid ICA dissection with pseudoaneurysms-CS fistula
Right direct CCF
Transarterial balloon embolization
Yes
Ruptured of the pseudoaneurysm /ICA proximal occlusion by balloon
Masana et al, 1992[3 ]
28/M
Left supraclinoid ICA pseudoaneurysms-CS fistula
Left direct CCF
Surgical reconstruct clipping
Yes
None
Tytle et al, 1995[4 ]
46/F
Right PcomA-CS fistula
Right direct CCF
Surgical clipping of PcomA origin
Residual
None
Kinugasa et al, 1995[7 ]
24/M
Left PcomA-CS fistula
Left direct CCF
Transvenous coil embolization
Yes
None
Fu et al, 2002[5 ]
16/M
Right PcomA-CS fistula
Right direct CCF
Direct surgical clipping of aneurysm neck and PcomA origin
Yes
None
Weaver et al, 2003[8 ]
42/M
Left PcomA-CS fistula
Left direct CCF
Transarterial coil embolization
Yes
None
Lee et al., 2004[9 ]
19/M
Right supraclinoid ICA dissection with pseudoaneurysms-CS fistula
SAH and ICH
Right direct CCF
Transarterial and transvenous coil embolization with stenting
Yes
None
Oran et al, 2004[10 ]
30/M
Right supraclinoid ICA-CS fistula
Right direct CCF
Transarterial coil embolization
Yes
None
Cho et al, 2006[11 ]
31/M
Right supraclinoid ICA-CS fistula
Right direct CCF
Transarterial coil embolization
Yes
Second coil embolization at 2 wks due to recurrence
Zhao et al, 2012[12 ]
40/M
Left supraclinoid ICA giant pseudoaneurysms-CS fistula
Left direct CCF
Balloon-assisted transarterial coil and onyx embolization
Yes
None
Karanam et al, 2014[13 ]
40/M
Left supraclinoid ICA pseudoaneurysms-CS fistula
Left direct CCF
Transarterial coil embolization
Yes
None
Narayan et al, 2018[14 ]
29/M
Left supraclinoid ICA giant pseudoaneurysms-CS fistula
Left direct CCF
Transarterial coil embolization
Yes
None
Present case, 2022
17/M
Left supraclinoid ICA dissection and pseudoaneurysm-CS fistula and right A2 segment of ACA
SAH and ICH,
left direct CCF
Left ICA trapping with EC-IC bypass and cavernous sinus packing, right A2 trapping with A3-A3 bypass
Yes
None
Abbreviations: ACA, anterior cerebral artery; CCF, carotid-cavernous fistula; CS, cavernous sinus; EC-IC, extracranial-intracranial; F, female; ICA, internal carotid artery; ICH, intracerebral hemorrhage; M, male; PcomA, posterior communicating artery; SAH, subarachnoid hemorrhage.
Intracranial Pseudoaneurysm with Direct CCF
Intracranial pseudoaneurysm resulting from blunt cerebrovascular injury can be explained by the following mechanisms: (1) direct injury from skull base fractures, (2) rotational injury or shearing of the carotid siphon, and (3) avulsion by an adjacent bony structure.[3 ]
[5 ] Consequently, traumatic direct CCFs of the cavernous segment ICA are frequently encountered due to the overstretching of the mobile portion of an ICA and its location near the cranial base. In contrast, injuries originating from the supraclinoid or intradural portion of an ICA are uncommon. When a carotid-cavernous fistula is formed directly between the supraclinoid ICA and cavernous sinus, the rupture of the ICA pseudoaneurysm into the lacerated superior wall of the cavernous sinus could be the cause.
Rupture of the cavernous segment ICA pseudoaneurysm would result in CCFs or massive epistaxis if the pseudoaneurysm protruded into the sphenoid sinus, which could be controlled by packing. In the meantime, bleeding from a supraclinoid ICA pseudoaneurysm can result in a catastrophic SAH with devastating consequences. Hence, in an aneurysm originating from the intradural segment of an ICA, the prevention of re-rupture is therefore crucial.
Reconstructive Techniques
Because the preferred treatment of direct CCF is to close the fistula while preserving the parent artery, endovascular therapy using balloon/coil embolization or stentings may be considered first-line treatment.[15 ]
[16 ] Concerning lesions in the supraclinoid segment of an ICA, the endovascular approach has a lower likelihood of distal navigation. However, it carries the risk of pseudoaneurysm rupture due to catheter or coil perforation of the fragile fibrous wall.[6 ] Endovascular coil embolization of an intracranial pseudoaneurysm may have the advantage of preserving the ICA with an ophthalmic artery; however, it is risky to rupture the pseudoaneurysm because the embolic material must be densely packed in the fibrous aneurysm wall and attached to the ICA orifice. Despite this, recurrence is a significant concern with coil embolization.[17 ] However, some authors reported successful endovascular embolization with favorable outcomes for intracranial pseudoaneurysms.[7 ]
[8 ]
[9 ]
[10 ]
[12 ]
[13 ]
[14 ]
Regarding the reconstructive strategy, the flow-diverting stent is a potential endovascular treatment option for parent artery reconstruction and promoting epithelialization, which is advantageous for pseudoaneurysm obliteration.[18 ] The disadvantages are the absence of immediate thrombosis and the need for dural antiplatelets, during which patients are at risk of rebleeding. The reported cases are also limited to lesions originating from the cavernous segment of an ICA. Moreover, the deployment of flow-diverting stents in supraclinoid ICA may be complicated by distal navigation, vascular tortuosity, and perforator preservation. Additional research is required concerning the safety and effectiveness of flow-diverting stents in these conditions.
Deconstructive Techniques
In cases of failed endovascular therapy or recurrent CCFs, however, surgical trapping with or without bypass may be necessary using the deconstructive strategy.[5 ]
[19 ]
[20 ] Because neck clipping may not be feasible for pseudoaneurysms, surgical trapping may provide definitive, complete obliteration of the aneurysms and fistulas. As for bypass, there have been reported cases of surgical trapping without revascularization,[1 ]
[2 ] in which collateral circulation was sufficient. Nevertheless, up to 20% of patients who pass the balloon test occlusion still develop ischemic complications. As a result, a universal high-flow bypass should be conducted to prevent ischemic complications resulting from the sacrifice of an ICA, particularly in cases where collateral flow is insufficient, as in our case.
Regarding the ophthalmic artery, trapping would be performed by placing a clip proximal to the origin of the ophthalmic artery in conjunction with cervical ICA ligation in the case of a cavernous segment ICA lesion that permits retrograde flow from the distal ICA to the ophthalmic artery.[19 ]
[20 ] In cases of supraclinoid ICA lesions, however, the clip would have been placed distal to the ophthalmic artery origin to achieve complete aneurysm and fistula obliteration. The latter could impair the patient's vision unless the ECA supplied the ophthalmic collaterals, as in our cases where vision was preserved.
Conclusion
The surgical trapping and revascularization of intracranial traumatic pseudoaneurysms are effective for aneurysm obliteration to prevent rebleeding and ischemic complications. However, the management strategy should be individualized depending on the location of the aneurysm, its association with carotid-cavernous fistulas, and the patient's collateral circulation.
