Implications of the Collar Sign in Incompletely Occluded Aneurysms after Pipeline Embolization Device Implantation: A Follow-Up Study

Endothelialization of the Pipeline Flow Diverter

As described in preclinical studies, endothelialization along the stent strut of the PED has been identified as the key underlying mechanism of aneurysmal exclusion from the intracranial circulation and subsequent aneurysm occlusion.^2⇓⇓⇓-6 Likewise, this mechanism of endothelialization along the PED strut has been confirmed in humans.^1,7 Initially, the collar sign was thought to be indicative of future aneurysmal occlusion following PED implantation. Nonetheless, our results demonstrate that this sign is likely a sign of persistent aneurysmal flow even at long-term follow-up, regardless of any additional PED implantation.

Although the underlying mechanism is still unknown, we found branch arteries originating from the aneurysm dome in 14 of 19 cases (73.7%). On the basis of this finding, we hypothesized that an aspiration effect led by a pressure gradient between the parent arteries and branches is the likely cause of inhibition of complete endothelialization along the PED strut and subsequent persistence of flow into the branches through the aneurysm. Two of 3 aneurysms with complete occlusion did not have a branch arising from the aneurysm at the initial follow-up angiogram, which further supports this hypothesis. Furthermore, patient 1 had an ophthalmic artery that arose from the aneurysm dome, which had been opacified at the first follow-up angiogram. Subsequently, both the aneurysm and the ophthalmic artery were found to be occluded on the final follow-up angiogram without any visual sequelae, suggesting collateral compensation to the distal segment of the ophthalmic artery and depletion of aspiration effect. Therefore, the collar sign is likely an indication of partial endothelialization, seen more commonly in aneurysms with a branch arising from the dome, which demands persistent blood supply and subsequently inhibits complete endothelialization required to cover the aneurysm neck. A negative correlation between aneurysm occlusion and branch vessels arising from the aneurysm neck or dome following PED implantation in patients with paraophthalmic artery aneurysms has been reported.⁸

On the other hand, the collar sign was observed in a thrombosed aneurysm without an associated branch vessel (aneurysm 15). In the case of thrombosed aneurysms, reports have described a heterogeneous thrombosis status, in which both thrombotic and thrombolytic processes take place inside the aneurysm. These result from a cycle of repeat adventitial inflammation, capillary proliferation, and bleeding within the aneurysmal wall in such thrombosed aneurysms.^9,10 Therefore, endothelialization along the aneurysm neck is less likely to occur following PED implantation.

Management Strategies for Incompletely Occluded Aneurysms with the Collar Sign

In the present study, complete occlusion was achieved in only 3 aneurysms (15.8%) with the collar sign. Aneurysm enlargement was observed in only 1 patient with a thrombosed aneurysm as mentioned previously. In contrast, most of the aneurysms with a collar sign were stable or even decreased in size (10.5% and 68.4%, respectively), suggesting a stabilizing effect of the PEDs on the aneurysm. Furthermore, because the rates of complete occlusion of the aneurysm were very low regardless of the number of PED treatments, retreatment with adjunctive PED implantation is unlikely to be effective in aneurysms with a collar sign. Under these circumstances, radiologic follow-up may be more appropriate than retreatment. Thus, patients are not committed to the risk of an additional procedure in the absence of the expected benefit of aneurysm occlusion.