1; A. Hejčl
1,2; F. Cihlář
3; A. Sejkorová
1; M. Sameš
Neurochirurgická klinika Fakulty zdravotnických studií UJEP a Masarykovy nemocnice v Ústí nad Labem
1; Mezinárodní centrum klinického výzkumu, FN u sv. Anny v Brně
2; Radiologická klinika UJEP a Masarykovy nemocnice v Ústí nad Labem
Cesk Slov Neurol N 2019; 115(3): 350-351
Letter to editor
Aim: Anterior choroidal artery aneurysms (AChoAA) belong to less frequent cerebrovascular lesions and therefore there are still only a few reports describing their neurosurgical management. We decided to share our experience and present two unusual cases of AChoAA we have treated in our department. We also report one of the first published use of the Yasargil T-bar fenestrated clip for solving of a AChoAA.
Methods: We present two cases of unruptured AChoAA treated in 2016 with respect to patient's history, radiological and microsurgical anatomy of the aneurysm, surgical procedure and clinical follow-up. Results: Both aneurysms were successfully treated with surgical clipping. In case 1 we used a single T-bar fenestrated clip. To our best knowledge this might be the first reported use of such clip in treatment of AChoAA. In case 2 for a large AChoAA a standard straight Aesculap clip was used. Both procedures were performed with microvascular Doppler sonography and under electrophysiological monitoring with motor-evoked potentials (MEP). Temporary disturbance in MEP signal during surgery was observed in the T-bar clip case and led to reposition of the clip. Both patients had a good surgical outcome without any clinical or radiological signs of ischemia in the AChoA or any other territory.
Conclusion:As previous literature we confirm that surgical treatment of AChoAA is a good and safe alternative to endovascular treatment. We propose, using T-bar fenestrated clip might be appropriate solution for treatment of these lesions. We also suggest that combination of monitoring methods (MVDS, ICG and MEP monitoring) during AChoAA surgery is a very valuable way for prevention of ischemic infarction in the AChoA territory.
Anterior choroidal artery aneurysms represent 2–5% of intracranial aneurysms according to larger series. As other aneurysms of the supraclinoid segment of internal carotid artery (ICA) they are considered rather easily accessible surgical goals. Nevertheless, the tight anatomical relations between ICA, its main branches and perforating branches make it a surgical demanding area. The most problematic feature might be the number and position of the choroidal artery itself and its relationship with the aneurysm, as the vessel might be distorted or completely hidden by the sac. Therefore, a thorough knowledge of possible anatomical variations is vital for a surgeon. Safe position of anterior choroidal artery (AChoA) during clipping is also crucial because its occlusion might result in severe consequences such ascontralateral hemiplegia, hemianesthesia and hemianopia. Intraoperative accidental occlusion of AChoA or one of its main branches is considered the main cause of vascular insufficiency leading to permanent postoperative morbidity. To prevent this, firstly AChoA area should be precisely investigated. However, DSA is not often accurate enough to determine clear anatomy of the arterial branching. Therefore, perioperative electrophysiological motor evoked potentials (MEP) monitoring is considered necessary for avoiding territorial ischemia. AChoA generally supplies the posterior limb of internal capsule hence monitoring of pyramidal tract integrity during surgery might be reassuring while a clip is being placed.
The aim of this article is to emphasize the complexity of surgical clipping of aneurysms in anatomically complicated area of AChoA in case important perforators arise in close proximity or directly from the aneurysm. We also suggest the necessity of intraoperative monitoring for successful result.
A 44-year-old female patient was examined for several nonspecific symptoms such as remitent cefalea, left retrobulbar pressure, vertebrogenic pain syndrome of both cervical and lumbar spine, vertigo and upper limb acroparesthesia. CT and CTA scan was performed with incidental finding of left unruptured AChoAA with diameter of 6 mm. With DSA it was confirmed that the choroidal artery was arising from the neck of the sac (Fig. 1a–b). After discussion in our cerebrovascular team it was decided to proceed with surgical treatment of the aneurysm as the conventional coiling procedure would have a high risk of subsequent occlusion of AChoA with potential poor clinical result.
We chose the lateral supraorbital approach to reach the aneurysm. After release of cerebrospinal fluid from chiasmatic cistern to relax the surrounding brain we dissected the arachnoid from the medial side of ICA to expose a thin posterior communicating artery (PCom) and AChoA with its two branches encircling tightly the fundus of the aneurysm. AChoA arose from proximal part of the neck. The anatomical relations did not allow us to approach the neck of aneurysm from either the medial or the lateral side, neither was possible to separate the artery from the fundus. After quick reconsideration we decided to occlude the aneurysm using the Yasargil titanium T-bar clip from above during occlusion of ICA with a temporary clip. After doing so, we used microvascular Doppler ultrasonography to check for flow in surrounding vessels including AChoA. Confident that the blood supply was safe, we decided to add another fenestrated clip for a tiny remnant distally on the neck of the aneurysm. However, at the time of application we witnessed a MEP modification signalling a lower signal to contralateral hand. Now we see a conflict between the second clip and perforating branches coming from ICA bifurcation, which were previously out of view. After removal of the clip the MEP normalize. Knowing that, rather than adding another clip to the area of many crucial perforating branches we decided to only slightly adjust position of the T-bar clip to both exclude the remnant and to not compromise flow in other vessels. Microvascular Doppler confirmed that the sac has been excluded from the circulation.
The patient had an uneventful postoperative course. The CTA after surgery did not show any evidence of complication or remnant of the aneurysm. (Fig. 2–3)
The second patient a 56-year-old male presented with a sudden temporary episode of memory loss and elevated blood pressure. An incidental left large AChoAA (20 mm) was found on CTA. (Fig. 4a–c) The finding was then confirmed with DSA followed by balloon occlusion test (BOT) to evaluate an effect of potential parent artery occlusion in case this strategy of treatment was necessary. The BOT was well tolerated by the patient.
After thorough consideration with regard to feasible therapeutic approaches we preferred surgical clipping over flow-diverting.
In this case a pterional craniotomy approach was chosen. After durotomy we reached the chiasmatic cistern to release cerebrospinal fluid in order to relax the surrounding brain. Then we dissected the proximal Sylvian fissure to fully expose the large laterally and inferiorly aiming aneurysmal sac with PCom and AChoA closely adhering to it. We proceeded with careful dissection of these two vessels from medial side of ICA, as they were deviated by the pressure of the large sac. A tiny gap between the aneurysmal neck and origin of AChoA allowed us to gradually separate the adhering aneurysm wall from AChoA to prevent any constriction or kink of the artery when placing a clip. Afterwards, we can trap the sac using clip on ICA proximal from PCom origin, PCom itself and ICA proximal to the AChoA origin. In this situation the aneurysm was fully trapped and AChoA was supplied via contralateral ACom. We confirmed our assumption with unaffected MEP and TCD signal. Afterwards we decided to follow the direct suction decompression method to improve aneurysmal neck visualisation. This made possible for us to safely use a straight clip on the neck with visual control of PCom and AChoA. After removal of other clips trapping the aneurysm the flow in ICA is restored with fully excluded sac. At the end of the clipping procedure preserved patency of ICA, PCom, AChoA and surrounding perforating branches is confirmed using both MDS and ICG angiography.
The second patient had an uneventful postoperative course as well. The postoperative CTA did not show any sign of complication or sac residue. (Fig. 5a–b)
Aneurysms of anterior choroidal artery belong to less common cerebrovascular lesions constituting only 2–5% of intracranial aneurysms [1–8]. Nevertheless, their close relation to parent artery and complex anatomy of their surroundings make them a challenging topic for successful treatment.
Anterior choroidal artery is a small but important branch of the supraclinoid communicating segment of ICA. The anatomy of the origin of AChoA is fairly inconsistent but in most of the cases (68–88%) it is the first branch distal to the PCom coming from posterolateral aspect of ICA. It arises closer to the PCom origin than the ICA bifurcation. It is a rather small vessel with average diameter of 0.5 to 2.0 mm. The artery may constitute one main trunk or arise as multiple vessels. [1,2,5,6,9,10] (Fig. 6a–c) We witnessed this variety in our first presented case. The AChoA is normally divided into two main segments: cisternal, which extends to choroidal fissure and gives most of the perforating branches and plexal (choroid) supplying the choroid plexus [1,5,9].
The aneurysms of AChoA are mostly classified according to relation between the neck and the origin of AChoA. First group contains aneurysms arising from ICA right next to the AChoA possibly obscuring its origin (our second case). Second is represented with AChoA arising from the neck of the aneurysm (our first case). Finally, the least common option are aneurysms arising directly from the main trunk of AChoA [1,5,11] (Fig. 7a–c). The area supplied by AChoA and its branches is quite large and contains inferior aspect of optic chiasm, posterior majority of optic radiation, anterior hippocampus with dentate gyrus and half of amygdala, tail of caudate nucleus, medial part of globus pallidus, genu and posterior limb of internal capsule, middle third of cerebral peduncle, substantia nigra, red nucleus, portion of subthalamic region, part of thalamic nuclei, lateral geniculate body and lastly the choroid plexus of the lateral ventricle. The precise region supplied with AChoA varies with existence of collaterals from other arteries mainly ICA, PCom and MCA. [1,5,6]
Ongoing studies dealing with both surgical and endovascular procedures are also important because ischemic complications in above described AChoA territory may lead to severe consequences known as the AChoA syndrome. Originally, it was first presented by Foix in 1925, who observed trias of contralateral hemiplegia, hemianesthesia and homonymous hemianopsia . However, the typical full combination of these is unusual. The most common deficit in case of AChoA ischemia is contralateral hemiparesis or hemiplegia affecting mainly upper extremity, supporting results of anatomical studies observing that posterior limb of internal capsule is the most poorly collateralized area in AChoA territory. Other clinical sequelae connected with occlusion of AChoA include dysarthria, lethargy and cognitive dysfunction [1–6,13].
Position of AChoA a small vessel with significant but variable hemodynamics in close proximity of aneurysm makes surgical clipping a demanding procedure. Additionally, the goal of complete occlusion of the sac has to be achieved with preserving other close structures namely PCom, ICA perforators, AChoA branches and oculomotor nerve. Pterional, lateral supraorbital or supraorbital keyhole approaches have been preferred in previous literature [2,4,5,14]. Normally we use the lateral supraorbital (LSO) approach earlier presented by Hernesniemi et al  or its modification according to our department , however in case of larger lesions the pterional approach might be advantageous as ICA to achieve safe proximal clipping area. Opening chiasmatic cistern for relaxing the surrounding brain tissue is strongly advisable. Afterwards gentle dissection is continued along the medial side of ICA towards ICA bifurcation preventing any retraction of the artery medially that may cause premature rupture of the aneurysm, especially when attached to temporal lobe. Then we expose both M1 and A1 segments. As soon as the proximal and distal sites for temporary clips are prepared our attention focuses on the lateral and posterior side of ICA. To avoid accidental premature rupture and to reduce pressure in the dome while dissecting with intention to expose AChoa and PCom we temporary clip ICA or M1 and A1. With temporary clips in place the dissection might safely proceed with visualizing of the entire proximal segment of AChoA and all local perforators. It is crucial to gently free the AChoA from the sac to ascertain the precise anatomical relation between the aneurysm and the vessel. Only with exact anatomical perception the optimal clip might be chosen and kinking, or occlusion of the adjacent branches prevented. The blade in proximity of the origin of AChoA should be placed a small distance away from the origin to avoid any constriction of it.  After inserting the smallest possible final clip, it is necessary to in detail inspect the tips of the clip to rule out any conflicts with surrounding vessels [4–6]. This should be done after removal of any retraction forces to avoid any unwanted rotation of the clip [5,17].
Complex anatomy of AChoA and potential severe outcome in case of ischemic infarction after clipping have taught us to use several monitoring intraoperative techniques to assess patency of AChoA and other vessels during surgery. Firstly, we routinely use microvascular Doppler sonography (MVDS) with a 1 mm probe, which has been proved effective by Shibata and Neuloh [18,19]. MVDS is able to assess obliteration of aneurysm after clipping, direction and velocity of local blood flow of adjacent vessels and collateral flow after possible trapping of a sac at a specific point in time. Another monitoring method during clipping of AChoAA, which we regularly use is MEP monitoring. It is considered a highly sensitive method in reflecting potential functional motor deficit . In comparison to MVDS MEP allows us to get a continuous view of functional integrity, whereas MVDS shows immediate local flow conditions, therefore we ponder that combination of these methods during AChoAA clipping is strongly preferable and helps physician to avoid possible irreversible ischemia [19,20]. As no intraoperative method is totally reliable, we also add Indocyanine Green (ICG) Angiography to exclude a neck remnant or residual sac filling and also to assess blood flow in neighbouring arteries. It is believed that the main advantage of ICG is the possibility to evaluate flow in the small perforating branches visible within the microscope’s view. [21–23] Many of these important vessels are particularly common in ICA – AChoA area .
In our second case of the large aneurysm we performed a balloon occlusion test (BOT) prior to the surgery to assess patient’s tolerance of ICA occlusion in case the parent artery needs to be sacrificed during the surgery. After administration of 5000 U of heparin the carotid artery was occluded by inflating the balloon at the level of C1 vertebra for 20 min. During this time the patient was repeatedly neurologically monitored and functional assessment of collaterals was performed. Patient did not show any neurological symptoms; therefore the occlusion was well tolerated and the test was considered negative.
Historically, before endovascular treatment of cerebral aneurysm became an established procedure AChoAA were treated only surgically, however first published results carried a morbidity up to 33% and mortality up to 29% [24–26]. Reasons for that were obviously the tangled anatomy of AChoAA and the critical region supplied by AChoA often resulting in direct AChoA damage or conflict between the artery and clip with successive ischemia. A few studies also suggested that AChoAA anatomy might play an important role in the final outcome. Aneurysms with AChoA arising from the neck or aneurysms coming directly from the main trunk seem to have higher incidence of postoperative ischemia. [1,6,27] A number of patients surprisingly suffered from AChoA syndrome, although postoperative angiography showed well patent AChoA. Friedman et al hypothesized that causal role might be played by temporary AChoA stenosis in the time of initial attempts of clipping or by vasospasms . With the invention and use of intraoperative monitoring methods such as MVDS, MEP and ICG surgeons have been allowed to receive a better picture of actual situation. Even though neurosurgeon’s confidence about patency of regional vessels might be high, it is believed that this impression is not reliable enough and often brings poor postoperative results . Our two successful cases and other reports suggest that combination of aforementioned monitoring might successfully lower the risk of postoperative infarction, making it a safe method in treatment of AChoAA [18,20,28].
In recent years reports on endovascular treatment (EVT) of AChoAA have been presented. One of the first articles describing coling of AChoAA aneurysms were reported by Piotin et al in 2004. They concluded, that with both mortality and morbidity of 5.5% in their series of 18 aneurysms, the EVT compares favourably with those of the surgical series of that time . Also, Kim et al (37 patients) and Kang et al (88 patients) concluded that EVT is a safe and effective method in case of treatment of AChoAA [29,30]. Kim also hypothesized that an advantage of EVT is the option of continuous periprocedural control of parent artery patency and possibility of an immediate remedy in case of its occlusion . Kang presented a large series of patients with favourable outcome in 90% of them. He observed higher number of complications in choroidal artery arising from the neck of aneurysm. All the symptomatic procedure-related complications were associated with this type of AChoAA . It is advisable to follow the policy of safely preserving the important parent artery, rather than complete occlusion with coils at any price. This is particularly critical in AChoA-incorporated aneurysms. However, this inevitably brings the necessity of long-term follow-up and higher incidence of recurrence in such aneurysms [28–30].
Another endovascular option of aneurysmal occlusion with flow-diverter has been shown effective. Recent studies demonstrated good results using Pipeline Embolization Device in the treatment of ICA aneurysms with AChoA ostium covering [31–33]. All three studies concluded that unavoidable placement of flow-diverter across the artery is a safe and effective method. In cohort by Raz et al 4 AChoA originated from the aneurysm fundus. In two of these variants the AChoA flow was impaired and only one aneurysm was fully occluded. Placing of numerous diverters over AChoA origin in order to properly reconstruct the arterial flow has not been associated with higher risk of ischemia .
Kim et al also retrospectively evaluated clinical outcome and complications after endovascular coiling and surgical clipping in 4 institutions between 1999 and 2006. Both methods were comparable in clinical outcome with significantly higher incidence of AChoA infarction in surgical group . In more recent report by Aoki et al they compared 22 patients between 2008 and 2014, 10 in endovascular group and 12 in surgical group. They did not find any significant difference in clinical outcome. They claim that surgery performed under combined monitoring has become safer. In their opinion careful selection of treatment method is crucial, suggesting that the best indication for coiling are non-AChoA-incorporated aneurysms, low dome-to-neck ratio and high-grade SAH. They do not set any limit for surgical clipping .
In our first case we present use of the Yasargil T-bar clip for clipping an AChoAA. To our best knowledge it is the first report on this type of clip for saccular choroidal aneurysm in neurosurgical literature. This clip was first introduced in 2006 with two different angles of blades: 45° and 90°. Baskaya et al reported successful application of such clip for treatment of fusiform intracranial aneurysm. They suggest that these clips are particularly useful for helping the surgeon to reach in tight spots. In addition, this clip seems to be a good option when the vessel is not easily accessible and does not lie perpendicular to the surgeon. Also, the closing pressure is equally distributed along the two tines of the clip in compare to unequal distribution in right-angled fenestrated clip . Zada in 2009 with report on using fenestrated clips in anterior communicating artery aneurysms surgery came to the conclusion that using these tools might minimize the requirement of dissection and retraction of neighbouring vessels. In our opinion, this might count for AChoAA as well, especially when anatomical conditions do not allow using standard straight clips and the artery is inseparable from the sac .
Aneurysms of anterior choroidal artery belongs to less common cerebrovascular lesions. Nevertheless, they deserve our attention as their treatment may be associated with significant complications for the patient. We propose, using T-bar fenestrated clip might be appropriate solution for treatment of these lesions, mainly when the aneurysm neck cannot be safely attained with standard straight clip and AChoA is inseparable from the sac. With our two cases we follow other recent findings that surgical clipping, supported with combination of monitoring methods, is a safe method even with anatomical obstacles and a good alternative to endovascular treatment.
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