Paraclinoid internal carotid artery aneurysm with delayed stent occlusion after deployment of a flow diverter stent involving the orifice of the anterior cerebral artery: illustrative case

Takayuki Imai Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and
Department of Neurosurgery, Fukaya Red Cross Hospital, Fukaya, Saitama, Japan

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Tatsuya Shimizu Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Yumeki Yamamoto Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Hiroya Shimauchi-Ohtaki Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Ryosuke Shintoku Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Kaoru Aishima Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Masanori Aihara Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Fumiaki Honda Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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Yuhei Yoshimoto Department of Neurosurgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

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BACKGROUND

In-stent thrombotic occlusion is a serious ischemic complication that can also result in ischemia in the distal perfusion territory and the territory of side branches for the artery in which the flow diverter (FD) stent is deployed.

OBSERVATIONS

A 49-year-old female with a large paraclinoid internal carotid artery (ICA) aneurysm was treated with an FD involving the orifice of the anterior cerebral artery (ACA). The antiplatelet dose was reduced because of an increased clopidogrel response postintervention. The patient developed aphasia 2 months later. Emergency magnetic resonance imaging and digital subtraction angiography of the brain indicated FD stent occlusion and a small infarct in the distal vascular territory of the ipsilateral ICA, but the anterior choroidal artery (AChoA) territory was preserved by collateral flow. Emergency superficial temporal artery to middle cerebral artery anastomosis was performed, and she was discharged without neurological deficit 2 weeks after the second operation.

LESSONS

In-stent occlusion after FD deployment involving the orifice of the ACA can cause severe cerebral ischemia that requires an adequate antiplatelet effect and careful follow-up. The AChoA territory can be preserved by collateral blood flow even in cases of in-stent occlusion.

ABBREVIATIONS

ACA = anterior cerebral artery; AChoA = anterior choroidal artery; AComA = anterior communicating artery; ASA = antiplatelet therapy with aspirin; CLP = clopidogrel; FD = flow diverter; ICA = internal carotid artery; MCA = middle cerebral artery; MRI = magnetic resonance imaging; PComA = posterior communicating artery; POD = postoperative day; PRAS = prasugrel; PRU = P2Y12 reaction unit

BACKGROUND

In-stent thrombotic occlusion is a serious ischemic complication that can also result in ischemia in the distal perfusion territory and the territory of side branches for the artery in which the flow diverter (FD) stent is deployed.

OBSERVATIONS

A 49-year-old female with a large paraclinoid internal carotid artery (ICA) aneurysm was treated with an FD involving the orifice of the anterior cerebral artery (ACA). The antiplatelet dose was reduced because of an increased clopidogrel response postintervention. The patient developed aphasia 2 months later. Emergency magnetic resonance imaging and digital subtraction angiography of the brain indicated FD stent occlusion and a small infarct in the distal vascular territory of the ipsilateral ICA, but the anterior choroidal artery (AChoA) territory was preserved by collateral flow. Emergency superficial temporal artery to middle cerebral artery anastomosis was performed, and she was discharged without neurological deficit 2 weeks after the second operation.

LESSONS

In-stent occlusion after FD deployment involving the orifice of the ACA can cause severe cerebral ischemia that requires an adequate antiplatelet effect and careful follow-up. The AChoA territory can be preserved by collateral blood flow even in cases of in-stent occlusion.

ABBREVIATIONS

ACA = anterior cerebral artery; AChoA = anterior choroidal artery; AComA = anterior communicating artery; ASA = antiplatelet therapy with aspirin; CLP = clopidogrel; FD = flow diverter; ICA = internal carotid artery; MCA = middle cerebral artery; MRI = magnetic resonance imaging; PComA = posterior communicating artery; POD = postoperative day; PRAS = prasugrel; PRU = P2Y12 reaction unit

The treatment of cerebral aneurysms with a flow diverter (FD) stent was initially indicated for aneurysms at the proximal anterior circulation with high clipping/coiling difficulty and high recurrence rates. Nowadays, the indication is expanding to smaller aneurysms and aneurysms in the posterior circulation.1–4 However, ischemic complications occur with a certain frequency, and risk management of these complications is essential for safe treatment.

In-stent thrombotic occlusion is a serious ischemic complication that can cause infarction not only in the distal perfusion territory, but also in the territory of the side branches of the artery in which the FD is deployed. Herein, we present the case of a large paraclinoid internal carotid artery (ICA) aneurysm treated with a deployed FD involving the orifice of the anterior cerebral artery (ACA). Stent occlusion occurred 2 months later, resulting in infarction within the distal perfusion territory, but no ischemia occurred in the territory of the side branches including the anterior choroidal artery (AChoA). This case is reported because of its importance as an example of ischemic complications of FD treatment.

Illustrative Case

A 49-year-old female underwent magnetic resonance imaging (MRI) of the head for investigation of blunt trauma to the left eye, revealing an 8-mm aneurysm in the C2 segment of the left ICA. The aneurysm had been under observation but had increased to 10 mm in diameter within 2 years, and treatment was planned. On admission, astigmatism was observed due to ophthalmological postoperative effects on the left eye after lens reconstruction for blunt trauma, but there was no significant visual field impairment or other neurological deficits. Digital subtraction angiography showed an aneurysm with a maximum diameter of 11.1 mm in the C2 segment of the left ICA, a neck diameter of 5.8 mm, and an origin of the ophthalmic artery that was separated from the aneurysm (Fig. 1A–C). Collateral circulation was good via the anterior communicating artery (AComA) but was poor via the posterior communicating artery (PComA) in the balloon occlusion test. After approximately 40 minutes of occlusion at the cervical portion of the ICA, no neurological symptoms appeared. We planned treatment with an FD, and dual antiplatelet therapy with aspirin (ASA; 100 mg/d) and clopidogrel (CLP; 75 mg/d) was started 2 weeks before the procedure. P2Y12 reaction units (PRUs) as measured using a VerifyNow system (Accumetrics) 2 days before treatment was 64, identifying the patient as a CLP hyperresponder. CLP was skipped the day before treatment and reduced to 50 mg on the day of treatment.

FIG. 1
FIG. 1

Digital subtraction angiograms (A and B) showing an aneurysm in the C2 segment of the internal carotid artery. Three-dimensional rotational angiogram (C) showing an aneurysm. Digital subtraction angiogram (D) showing a working view of FD stent placement. E: Placing the FD stent using a Pipeline Flex device (3.5 × 16 mm). Maximum intensity projection angiography (F) showing insufficient expansion of the proximal end of the stent. Arrowheads indicate the proximal end; arrows, the distal end.

Endovascular treatment was performed with the patient under general anesthesia. An 8-Fr Fubuki guiding catheter (Asahi Intecc) was inserted into the left ICA. The diameter of the parent artery was measured as 2.9 mm distal to the aneurysm and 3.5 mm proximal to the aneurysm. A Pipeline Flex device (3.5 × 16 mm, Medtronic) was deployed from a position approximately 5 mm distal in the M1 segment of the left middle cerebral artery (MCA) to the C3 segment of the ICA (Fig. 1D and E). Slight malposition was observed proximal to the FD after it was straightened, but other areas showed good adherence to the vessel wall (Fig. 1F). Postdeployment imaging showed contrast stagnation inside the aneurysm (eclipse sign) and preservation of the ACA, PComA, and AChoA.

No postoperative deterioration of neurological findings was identified. MRI on postoperative days (PODs) 1 and 7 showed no infarctions. PRU was 0 on POD 6, so CLP was withdrawn and switched to prasugrel (PRAS) on POD 11. On POD 13, MRI revealed microinfarction in the left parietal lobe. On POD 15, PRU was 181, which was within the optimal range. The patient was discharged with ASA 100 mg/d and PRAS 3.75 mg/d. PRU was 37 on POD 25, so the dose of PRAS was reduced to 2.5 mg/d. On POD 47, PRU was 58, so the dose of PRAS 2.5 mg was further reduced to administration every other day. On POD 55, the patient developed aphasia and presented to the emergency department. MRI showed a new infarction in the left parietal cortex and occlusion of the ICA and MCA, suggesting FD stent occlusion (Fig. 2A and B). Angiography showed complete occlusion of the FD and poor collateral circulation via the AComA (Fig. 2C and D). Rotational angiography showed salvage of the AChoA by collateral flow from the posterior choroidal artery (Fig. 2E and F). The next day (POD 56), MRI showed that the infarction had expanded into the deep white matter of the left hemisphere. Because aphasia remained unimproved, emergency superficial temporal artery to MCA anastomosis was performed (Fig. 3). Her aphasia gradually improved, and the patient was discharged with a modified Rankin Scale score of 1 at 13 days after the second operation. Figure 4 illustrates the clinical course, drug adjustments, and course of PRU.

FIG. 2
FIG. 2

Postoperative day 55. Diffusion-weighted image (A) showing multiple small infarctions in the left cerebral hemisphere. Magnetic resonance angiography (B) showing occlusion of the ICA. Digital subtraction angiography (C) showing occlusion of the ICA. Collateral circulation via the anterior communicating artery is poor (D). Digital subtraction angiography (E and F) showing salvage of the anterior choroidal artery by collateral flow from the posterior choroidal artery.

FIG. 3
FIG. 3

A: Intraoperative photograph. B: Indocyanine green videoangiography. C: Magnetic resonance angiography showing anastomosis of the superficial temporal artery to the MCA.

FIG. 4
FIG. 4

Time course of PRU and antiplatelet dosages. Dual antiplatelet therapy with ASA at 100 mg/d and CLP at 75 mg/d is started 14 days before the intervention. The dosage of CLP or PRAS is adjusted depending on PRU, as measured by VerifyNow.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

Ischemic complications with FD treatment reportedly occur in 2% to 6% of cases.3,5–7 As in our case, ICA occlusion due to in-stent thrombosis also occurs in 2% to 4% of cases,1,8–10 but occlusion in the paraclinoid or cavernous portion of the ICA is often asymptomatic due to collateral blood flow through the circle of Willis, such as the AComA and PComA. In addition, occlusion of side branches covered by an FD deployed into the supraclinoid portion of the ICA is often not a problem because endothelialization of the FD is slow and collateral flow develops.11–13 The occlusion rate for antegrade flow in the PComA is approximately 20% to 50%, relatively frequent but rarely symptomatic.12–14 The occlusion rate of the ophthalmic arteries is reported at approximately 6%, with symptomatic complications occurring in less than 1%.14–16 The AChoA is occluded in only approximately 0% to 4% of cases, and symptomatic occlusion is extremely rare.13,14,17,18 In our case, despite in-stent occlusion, the AChoA territory was preserved by collateral flow from the posterior choroidal artery and did not become symptomatic. However, symptomatic occlusion can occur in situations in which the AChoA is branching from the dome of the aneurysm.13 When the orifice of the ACA is included in the FD, a high rate of occlusion of antegrade flow has been reported in the ACA (14%–64%), but this occlusion is not symptomatic because of sufficient contralateral blood flow through the AComA. However, when in-stent occlusion occurs, as in the present case, the perfusion territory of the MCA is extensively ischemic, resulting in an extremely dangerous situation. The deployed FD should not cover the ACA, but occasionally does so because of limitations in the diameter of the parent artery and size variations in the FD. In this case, the diameter of the parent artery was 2.9 to 3.5 mm. The FD was estimated to be longer even using a Pipeline Flex device 3.5 × 16 mm, the shortest size available in Japan. A bend was present in the proximal C4 segment, and there were concerns regarding failure of deployment due to twisting of the FD, so we chose to deploy the FD from the M1 segment of the MCA. The proximal FD position after deployment was more distal than expected, which may have been caused by errors in preoperative measurement. This is a problem with FDs that can vary in length due to elasticity, and the development of shorter FDs is desirable in the future.

Insufficient inhibition of platelet aggregation, particularly with thienopyridines, is associated with thromboembolic complications.19 Monitoring with VerifyNow PRU values is widely used, showing a low complication rate for PRU values of 60 to 240 in some reports.20,21 However, no recommendations for an appropriate perioperative PRU value of FD treatment have been established, and this monitoring is not covered by insurance in Japan. In our case, the patient showed a strong response to CLP and was switched to a regular dose of PRAS (3.75 mg). The asymptomatic microinfarction was observed during this transitional period. One week later, the PRAS dose was reduced because the PRU dropped at a relatively rapid pace to 37. A further reduction of PRAS to intermittent dosing because of a PRU of 58 at 6 weeks postoperatively may have triggered stent occlusion 2 weeks later. For proper management, it may be necessary to take into account not only the current PRU values but also the previous changes that occurred. In cases of microinfarction events or A1 jailing, which can lead to major ischemic complications, adjusting the antiplatelet dose so that the PRU remains low for a certain period of time (at least 6 months) may be necessary. However, the PRU value at 2 hours after stroke onset was 155, within the optimal range. PRU monitoring has been reported to be more effective as a predictor of hemorrhagic complications than of ischemic complications,21,22 which may represent a limitation of monitoring.

Insufficient adherence of the FD to the vessel is considered a risk factor for thromboembolism, as endothelialization of the stent surface is prevented.23,24 In this case, mild malpositioning was observed at the proximal end of the FD, which may have triggered thrombus formation. Balloon angioplasty after FD deployment may have been necessary.

Lessons

Stent occlusion after FD deployment involving the orifice of the ACA can cause severe cerebral ischemia, requiring an adequate antiplatelet effect and careful follow-up. The AChoA can be preserved by collateral blood flow even in cases with in-stent occlusion.

Author Disclosures

Conception and design: Imai, Shimizu, Aishima. Acquisition of data: Imai, Shimizu, Shimauchi-Ohtaki, Shintoku, Aihara. Analysis and interpretation of data: Imai. Drafting the article: Imai, Shimizu. Critically revising the article: Imai. Reviewed submitted version of manuscript: Imai, Shimauchi-Ohtaki, Aishima, Aihara. Approved the final version of the manuscript on behalf of all authors: Imai. Statistical analysis: Imai. Administrative/technical/material support: Imai, Yamamoto, Honda. Study supervision: Imai, Shimizu, Yoshimoto.

References

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  • 2

    Becske T, Brinjikji W, Potts MB, et al. Long-term clinical and angiographic outcomes following pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the pipeline for uncoilable or failed aneurysms trial. Neurosurgery. 2017;80(1):4048.

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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
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  • FIG. 1

    Digital subtraction angiograms (A and B) showing an aneurysm in the C2 segment of the internal carotid artery. Three-dimensional rotational angiogram (C) showing an aneurysm. Digital subtraction angiogram (D) showing a working view of FD stent placement. E: Placing the FD stent using a Pipeline Flex device (3.5 × 16 mm). Maximum intensity projection angiography (F) showing insufficient expansion of the proximal end of the stent. Arrowheads indicate the proximal end; arrows, the distal end.

  • FIG. 2

    Postoperative day 55. Diffusion-weighted image (A) showing multiple small infarctions in the left cerebral hemisphere. Magnetic resonance angiography (B) showing occlusion of the ICA. Digital subtraction angiography (C) showing occlusion of the ICA. Collateral circulation via the anterior communicating artery is poor (D). Digital subtraction angiography (E and F) showing salvage of the anterior choroidal artery by collateral flow from the posterior choroidal artery.

  • FIG. 3

    A: Intraoperative photograph. B: Indocyanine green videoangiography. C: Magnetic resonance angiography showing anastomosis of the superficial temporal artery to the MCA.

  • FIG. 4

    Time course of PRU and antiplatelet dosages. Dual antiplatelet therapy with ASA at 100 mg/d and CLP at 75 mg/d is started 14 days before the intervention. The dosage of CLP or PRAS is adjusted depending on PRU, as measured by VerifyNow.

  • 1

    Becske T, Kallmes DF, Saatci I, et al. Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology. 2013;267(3):858868.

  • 2

    Becske T, Brinjikji W, Potts MB, et al. Long-term clinical and angiographic outcomes following pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the pipeline for uncoilable or failed aneurysms trial. Neurosurgery. 2017;80(1):4048.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Hanel RA, Kallmes DF, Lopes DK, et al. Prospective study on embolization of intracranial aneurysms with the pipeline device: the PREMIER study 1 year results. J Neurointerv Surg. 2020;12(1):6266.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Hanel RA, Cortez GM, Lopes DK, et al. Prospective study on embolization of intracranial aneurysms with the pipeline device (PREMIER study): 3-year results with the application of a flow diverter specific occlusion classification. J Neurointerv Surg. 2023;15(3):248254.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chancellor B, Raz E, Shapiro M, et al. Flow diversion for intracranial aneurysm treatment: trials involving flow diverters and long-term outcomes. Neurosurgery. 2020;86(1)(suppl 1):S36S45.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol. 2011;32(1):3440.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Kallmes DF, Hanel R, Lopes D, et al. International retrospective study of the pipeline embolization device: a multicenter aneurysm treatment study. [published correction appears in AJNR Am J Neuroradiol. 2015 May;36(5):E39-40]. AJNR Am J Neuroradiol. 2015;36(1):108115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Fujii T, Teranishi K, Yatomi K, et al. Long-term follow-up results after flow diverter therapy using the pipeline embolization device for large or giant unruptured internal carotid artery aneurysms: single-center retrospective analysis in the Japanese population. Neurol Med Chir (Tokyo). 2022;62(1):1927.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Oishi H, Teranishi K, Nonaka S, Yamamoto M, Arai H. Symptomatic very delayed parent artery occlusion after flow diversion stent embolization. Neurol Med Chir (Tokyo). 2016;56(6):350353.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Chiu AH, Cheung AK, Wenderoth JD, et al. Long-term follow-up results following elective treatment of unruptured intracranial aneurysms with the pipeline embolization device. AJNR Am J Neuroradiol. 2015;36(9):17281734.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Cagnazzo F, Lefevre PH, Mantilla D, et al. Patency of the supraclinoid internal carotid artery branches after flow diversion treatment. A meta-analysis. J Neuroradiol. 2019;46(1):914.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Wu X, Tian Z, Li W, et al. Patency of branch vessels after pipeline embolization: comparison of various branches. Front Neurol. 2019;10:838.

  • 13

    Hosoo H, Tsuruta W, Dofuku S, Hara T, Ishikawa E, Matsumaru Y. Delayed occlusion of the anterior choroidal artery following flow diverter stent deployment for unruptured aneurysm: a case report and literature review. NMC Case Rep J. 2021;8(1):167175.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Bhogal P, Ganslandt O, Bäzner H, Henkes H, Pérez MA. The fate of side branches covered by flow diverters-results from 140 patients. World Neurosurg. 2017;103:789798.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Rangel-Castilla L, Munich SA, Jaleel N, et al. Patency of anterior circulation branch vessels after Pipeline embolization: longer-term results from 82 aneurysm cases. J Neurosurg. 2017;126(4):10641069.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Griessenauer CJ, Ogilvy CS, Foreman PM, et al. Pipeline Embolization Device for small paraophthalmic artery aneurysms with an emphasis on the anatomical relationship of ophthalmic artery origin and aneurysm. J Neurosurg. 2016;125(6):13521359.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Neki H, Caroff J, Jittapiromsak P, et al. Patency of the anterior choroidal artery covered with a flow-diverter stent. J Neurosurg. 2015;123(6):15401545.

  • 18

    Raz E, Shapiro M, Becske T, et al. Anterior choroidal artery patency and clinical follow-up after coverage with the pipeline embolization device. AJNR Am J Neuroradiol. 2015;36(5):937942.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Saatci I, Yavuz K, Ozer C, Geyik S, Cekirge HS. Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol. 2012;33(8):14361446.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

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    Delgado Almandoz JE, Crandall BM, Scholz JM, et al. Last-recorded P2Y12 reaction units value is strongly associated with thromboembolic and hemorrhagic complications occurring up to 6 months after treatment in patients with cerebral aneurysms treated with the pipeline embolization device. AJNR Am J Neuroradiol. 2014;35(1):128135.

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