In the treatment of peri-ophthalmic aneurysms with PEDs, physicians are most concerned about factors related to aneurysm occlusion and changes in vision. However, the effect of the anatomical relationship between the ophthalmic artery and aneurysm on treatment is poorly studied. We reviewed peri-ophthalmic aneurysms treated in the PLUS study and explored factors that promote aneurysm occlusion and reduce visual symptoms.
Preoperative visual symptoms, preoperative mRS score, maximum aneurysm diameter, and aneurysm neck width in the PED + coils group in this study were more frequent/higher compared with the PED-only group, probably due to significant clinical symptoms produced by the large aneurysm diameter by compression of peripheral vessels, optic nerves, ophthalmic nerves, and trochlear nerves[22]. Previous studies suggest that PED + coils should be used for large wide-necked aneurysms, either to reduce jet flow, increase aneurysm wall protection and reduce the risk of aneurysm re-rupture, or act as a scaffold to fix the PED and prevent long-term PED migration and shortening[14]. Differences in morphology between the two groups may lead to greater selection bias in treatment. In this study, PED + coils treatment was used in 37.1% of patients. To avoid this effect, we analyzed the two treatment methods separately. Lin et al.[14] compared PED-only treatment with PED + coils treatment for intracranial aneurysms with a mean follow up of 7.8 months. They reported 74.7% occlusion in the PED-only group and 93.1% in the PED + coils group. Although only peri-ophthalmic aneurysms were included in our study, with a median follow-up time of 6.8 months, the occlusion rate was 78.7% in the PED-only group and 93.1% in the PED + coils group. A meta-analysis by Touzé et al.[25] examined 913 cases of ophthalmic segment aneurysm. In this meta-analysis, most studies used a PED only with an average follow-up duration of 16.4 months, and the aneurysm occlusion rate reached 85%. In our study, the median follow-up time was 6.8 months, and the total occlusion rate of peri-ophthalmic aneurysms reached 84%. This shows that PED + coils treatment significantly increases aneurysm occlusion rate.
In the present study, the relationship between ophthalmic artery origin and aneurysm was categorized according to the classification of Griessenauer et al.[10]. Since Type 3 only occurred in two cases, we classified Type 1 as Type A and Type 2 and Type 3 as Type B. In a retrospective study by Griessenauer et al.[9] 66 cases of para-ophthalmic aneurysm were followed up for 6 months and 18 months, and the aneurysm occlusion rates were 70.9% and 85.5%, respectively. Among 11 cases of incomplete aneurysm occlusion, ophthalmic arteries originated from the aneurysm body in two cases. It is believed that the ophthalmic artery originating from the aneurysm is an influencing factor for incomplete occlusion. In the PED-only group, the occlusion rate of Type A aneurysms was 87.8%, while the occlusion rate of Type B aneurysms was only 60%. Univariate and multivariate analyses in the PED-only group showed that Type B aneurysm with the ophthalmic artery originating from the neck of the aneurysm was an independent risk factor for incomplete aneurysm occlusion. This result is consistent with the conclusion of Griessenauer et al.[10] on the importance of the anatomical relationship between the ophthalmic artery and the aneurysm. For aneurysms where the ophthalmic artery originates from the aneurysm body or aneurysm neck, after PED implantation, if the ophthalmic artery still has a sufficient pressure gradient to maintain forward blood flow, sufficient blood flow will be retained in the aneurysm to prevent thrombosis, resulting in an aneurysm that is difficult to occlude[12, 15]. This is similar to why aneurysms are difficult to occlude when a PED is used to treat fetal posterior communicating aneurysm[11, 26]. In our study, the occlusion rate of Type A aneurysm in the PED + coils group was 96.1%, and the occlusion rate of Type B aneurysm was 85.7%, compared with the 60% occlusion rate of Type B aneurysm in the PED-only group, indicating that application of coils increases the occlusion rate of Type B aneurysms. Univariate and multivariate analyses in the PED + coils group did not identify other factors that promote aneurysm occlusion. The long-term effects of coils on the ophthalmic artery and visual symptoms are worth exploring.
Previous reports have shown that with PED treatment of ophthalmic artery segment aneurysms, the preservation rate of the ophthalmic artery is between 68% and 97%[1, 3, 4, 7-9, 15, 17-19, 27]. Moreover, a recent meta-analysis by Touzé et al. suggested an ophthalmic artery preservation rate of 90%[25]. The overall ophthalmic artery preservation rate in this group was 93.3%, 94.3% in the PED-only group, and 91.7% in the PED + coils group. Although ophthalmic arteries with diminished flow and occlusion occurred more frequently in the PED + coils group compared with the PED-only group, there were no significant differences between the two groups.
Previous studies have shown that 16%–40% of patients with para-ophthalmic aneurysms have visual symptoms[5, 13, 20-22]. Among the 194 aneurysms in this group, 26 (13.4%) were associated with visual symptoms as the chief complaint, and 20 (76.9%) were associated with improved visual symptoms postoperatively. In a meta-analysis of ophthalmic segment aneurysms that presented with visual symptoms preoperatively, Sliva et al.[21] reported improvements of 58% and 49% after clipping and embolization, respectively, compared with an improvement of 71% after flow diverter device (FDD) placement. In Sliva’s recent study, 15 patients with preoperative visual symptoms had an improvement of 93% after PED implantation[22]. The postoperative visual symptom improvement rate in this group was 76.9%, which is between the range presented Sliva et al.[21, 22] indicating that for patients with preoperative visual symptoms, FDD treatment has obvious advantages compared with other treatment methods. Because visual symptoms are most often caused by the aneurysmal mass effect, clipping may aggravate these symptoms due to optic nerve separation. Traditional embolization with dense coils cannot reduce the compression effect of aneurysms. After FDD implantation, as a thrombus forms within the aneurysm sac, the aneurysm gradually shrinks and compression on surrounding structures is relieved[21, 22, 28].
In our study, three cases of new visual symptoms after surgery accounted for 1.7% of the non-visual symptoms group. In the study of FDD treatment for para-ophthalmic aneurysms that focused on visual symptoms, the proportion of patients with new visual symptoms was less than 5%, but this proportion was higher in studies using specialized ophthalmic examinations[6, 7, 10, 17, 23, 24]. At present, no study has illustrated that changes in the ophthalmic artery are associated with new visual symptoms in patients. Touzé et al.[24] believed that the ophthalmic artery has abundant external carotid anastomotic branch compensation, and when the origin of the ophthalmic artery is covered by FDD, the ophthalmic artery and the external carotid anastomotic branch need to achieve a new pressure balance. During establishment of this process, if retinal perfusion pressure is reduced, symptoms of amaurosis fugax may be apparent. For Type B aneurysms, dislodged microthrombi also cause emboli in retinal branch arteries after intra-aneurysmal thrombosis, resulting in visual field defects[19, 24].
In this study, although the visual symptom rate at final follow up was 5.6% in the PED + coils group and 4.1% in the PED-only group, there was no significant difference between the two groups. The multivariate analysis showed that the visual symptoms at final follow up had no correlation with changes in the ophthalmic artery, aneurysm type, or treatment method. This is consistent with the conclusion that visual symptoms at final follow up were not related to changes in the ophthalmic artery in a previous study[25]. In our study, 66.7% of patients with visual symptoms at final follow up had preoperative visual symptoms. First, it takes time to recover from the visual symptoms caused by the aneurysmal mass effect. Second, previous studies have suggested that 1 month of onset may be the optimal time for recovery of visual symptoms, since long-term compression may cause difficulty in recovery[2, 28], but the patients in our study all had visual symptoms for more than 2 months. In addition, we did not conduct objective and systematic eye examinations during follow up, thus, there may be certain deviations that affect the final multi-factor analysis results.
Limitations
There are some limitations to this study that should be noted. First, the study was a retrospective, multi-center study, and heterogeneity in operators’ surgical preferences cannot be well quantified. Second, patients did not undergo an objective and systematic eye examination during follow up, which may have influenced the final results. We believe a prospective study with a systematic design is required to evaluate the current treatment of para-ophthalmic artery aneurysms with FDDs.