Two case descriptions of urgent carotid endarterectomy: the characteristics of thrombosis and stroke at different time points

Introduction

Acute ischemic stroke (AIS) is associated with high disability and mortality rates, with thrombus being a major cause. Different types of thromboembolism lead to strokes with varying characteristics and prognoses (1). It is crucial to identify and implement appropriate methods to remove the thrombus promptly. Acute thrombosis is a common cause of carotid artery occlusion soon after carotid endarterectomy (CEA) (2). However, there is still ongoing debate in the guidelines regarding the diagnosis and treatment of acute stroke after CEA. Early case reports have suggested that urgent re-exploration could reverse the effects of cerebral hypoperfusion in acute stroke after CEA, and emphasized that cerebral angiography-related examinations are unnecessary (3,4). Subsequent literature and guidelines have emphasized the importance of cerebral angiography in identifying the cause of stroke and selecting appropriate treatment measures for patients after CEA (5). Carotid free floating thrombosis (FFT) is a rare phenomenon that often presents as a recurrent embolic ischemic event prior to revascularization (6,7). The natural course and pathological types of FFT are not yet fully understood, and there is no established classification for its pathological types. As a result, there is no consensus on the management of FFT, and neither surgical nor medical treatment has shown significant advantages. In this article, we discuss 2 cases of urgent CEA treatment of AIS caused by different types of thrombi, aiming to improve the identification of thrombus subtypes and evaluate the best indications for CEA based on clinical symptoms and imaging characteristics.

Case presentation

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was provided by the patients for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Case one

A 68-year-old woman presented to the hospital in November 2023 with numbness in her limbs. A thorough examination of the head and neck revealed bilateral carotid artery stenosis on a head and neck computed tomography angiography (CTA). Computed tomography perfusion (CTP) did not reveal specific abnormalities. Dynamic CTA demonstrated plentiful collateral circulation on the affected side, which was classified as level 4 according to the modified American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) based on dynamic CTA (Figure 1). She expressed reluctance to undergo the implantation of a foreign body. Due to the presence of good collateral circulation and the absence of high-risk factors such as congestive heart failure, myocardial infarction, or severe pulmonary and renal failure, the patient was deemed suitable and subsequently admitted to the hospital for CEA. The procedure was performed under general anesthesia, but within 8 hours after the operation, the patient experienced nausea, vomiting, and hemiplegia of the left limb. Emergency head and neck CTA showed occlusion of the surgical site in the patient’s right internal carotid artery (ICA) (Figure 2). Within 4 hours of symptom onset, urgent re-exploration of the right ICA was performed under general anesthesia with systemic heparinization. The re-exploration revealed a 1 cm occlusion from the bifurcation of the ICA to the distal end, along with intimal fragments and acute thrombosis (Figure 3). Additionally, a small intimal flap was observed in the external carotid artery (ECA). These tissues were successfully addressed using a Fogarty catheter to remove the thrombotic tissue and intimal fragments. Furthermore, the incision in the ECA was enlarged to remove any remaining intimal debris. Intraoperative angiography confirmed complete recanalization. The patient achieved a complete recovery and was discharged. Follow-up after 1 month revealed no recurrence of symptoms.

Figure 1 CTP (A-E) and dynamic CTA (F) images of a 68-year-old female patient with right ICA occlusion caused by acute thrombosis following CEA. CTP of the head demonstrating (A-E) no significant hypoperfusion. Dynamic CTA (F) image shows the right cerebral hemisphere with soft meningeal side compensatory vessels (blue arrow). CTP, computed tomography perfusion; CTA, computed tomography angiography; ICA, internal carotid artery; CEA, carotid endarterectomy.

Figure 2 VR reconstruction of the neck CTA demonstrates a blunt-shaped configuration of the right extracranial ICA (white arrow). VR, volume rendering; CTA, computed tomography angiography; ICA, internal carotid artery.

Figure 3 A red clot was removed from the right ICA after urgent CEA. ICA, internal carotid artery; CEA, carotid endarterectomy.

Case two

A 71-year-old man presented at the hospital having experienced slurred speech, unresponsiveness, and slurred articulation for no apparent reason a week prior. He was admitted to the hospital for conservative anticoagulation treatment, but his condition worsened, and he developed right limb hemiplegia after 24 hours. Diffusion-weighted imaging (DWI) revealed acute cerebral infarction (Figure 4). CTA of the head and neck showed severe stenosis of the left ICA with a FFT (Figure 4). CTP revealed no evident abnormalities. Nevertheless, dynamic CTA indicated a decreased collateral circulation on the affected side in comparison to the contralateral side, graded as level 2 using the modified ASITN/SIR based on dynamic CTA (Figure 5). Urgent endarterectomy of the left ICA under general anesthesia with systemic heparin was performed to fully expose the artery. Atherosclerotic plaques and thrombi were found 1 cm from the origin of the ICA upon opening the carotid artery. Intraoperative angiography after plaque exfoliation showed complete recanalization. Postoperative head and neck CTA confirmed the patency of the left ICA lumen. Following the procedure, the patient exhibited transient confusion upon awakening from anesthesia due to low perfusion. Subsequent administration of symptomatic therapy resulted in the patient’s restoration of consciousness. The patient’s right limb muscle strength improved to grade 4, he regained consciousness, and he remained asymptomatic during a 1-month follow-up.

Figure 4 DWI (A) and MPR (B,C) images of a 71-year-old male patient with FFT in the left ICA. DWI (A) shows a hyperintense signal in the left MCA territory. Neck CTA with axial image (B) demonstrates a filling defect surrounded by contrast (red arrow). Neck CTA (C) with sagittal image demonstrates atherosclerotic plaque with free thrombus formation in the left ICA (red arrow). DWI, diffusion-weighted imaging; MPR, multi-planar reconstruction; FFT, free floating thrombosis; ICA, internal carotid artery; MCA, middle cerebral artery; CTA, computed tomography angiography.

Figure 5 CTP (A-E) and dynamic CTA (F) images of a 71-year-old male patient with FFT in the left ICA. CTP of head demonstrating (A-E) no significant hypoperfusion. Dynamic CTA (F) image shows the left cerebral hemisphere with soft meningeal side compensatory vessels (green arrow). CTP, computed tomography perfusion; CTA, computed tomography angiography; FFT, free floating thrombosis; ICA, internal carotid artery.

Discussion and conclusions

International guidelines recommend performing CEA within 2 weeks after a stroke. Over time, advancements in technology and increased experience have led to a shorter median time for CEA (8). Urgent CEA typically refers to performing CEA within 48 hours following the most recent symptomatic event (9). However, there is currently a significant debate regarding the appropriateness of early CEA within 48 hours. The risk of stroke recurrence within 48 hours after symptom onset is approximately 5.2% (10), suggesting the potential benefits of early CEA, When the perioperative stroke risk of early CEA is lower than the risk of stroke recurrence, it can provide certain clinical benefits to patients. Some studies have reported a postoperative risk of early CEA within 48 hours to be around 3.0–3.1% (11,12). The type of preoperative target event is one of the prognostic factors, highlighting the importance of accurately determining the best indications for early CEA, with neuroimaging methods serving as an essential reference standard.

It is currently believed that acute isolated extracranial carotid artery occlusion is an indication for urgent CEA. ICA occlusion caused by acute thrombosis is known to be one of the causes of early stroke after CEA (2). Urgent re-exploration after CEA has a long history (3,4,13,14). Najafi suggested that urgent CEA is suitable for patients who are in good condition during CEA but experience postoperative stroke due to arterial thrombosis (3). Kwaan et al. reported 3 cases wherein patients experienced stroke due to carotid artery occlusion within 24 hours after CEA and were successfully reopened within 1 hour of symptom onset (4). Radak et al. also stated that immediate reoperation is beneficial for early postoperative stroke (14). However, most literature focuses on the importance of time in reversing neurological deficits and does not emphasize the necessity of preoperative cerebral angiography. Therefore, the early school demonstrated the benefits of urgent CEA but overlooked other possible causes of stroke after CEA, such as intracranial embolism, hemorrhage, and distal carotid artery dissection, which could limit the benefits of re-exploration of CEA. During the intraoperative plaque stripping process of patient 1, due to the incomplete intraoperative visual field exposure resulting from the wedge-shaped incision of the ECA and the soft texture of the ECA plaques, some of the plaques were incompletely peeled off intraoperatively. This resulted in a less smooth ECA lining. Throughout the procedure, the patient maintained a stable systolic blood pressure range of 100–110 mmHg, with postoperative nursing records indicating normal body fluid intake and output, ruling out ICA occlusion due to dehydration. In case 1, only occlusion of the C1 segment of the ICA was observed in the surgical area, without clear signs of dissection (long-segment gradual stenosis, intimal tears, double cavities) (15). Additionally, imaging of the patient revealed no filling defects in the intracranial internal artery. Pseudo-occlusion resulting from distal occlusion and dissection may present as a characteristic “flame-shape” in the extracranial ICA, whereas true occlusion of the ICA often appears as a “blunt shape” (16). Consequently, the occurrence of cerebral ischemic events subsequent to CEA in patients is predominantly attributed to acute thrombosis, which results in the true occlusion of the ICA. During the urgent re-exploration of CEA, a small amount of intima was discovered in the ECA. Consequently, the ECA was incised separately during the operation to remove the residual intima. Although there are limited documented cases of complications arising from incomplete dissection of the ECA, Takolander et al. previously reported a patient who developed thrombotic occlusion post-CEA due to dissection of the ECA, suggesting that it could also serve as a potential source of thrombosis (17).

Carotid FFT is an elongated thrombus attached to the artery wall. The natural history of FFT is unknown, and atherosclerosis is a common cause (7,18). Acute thrombosis on CTA can present as a typical “donut sign” (19), However, in case 2, the shape of the filling defect in the head and neck CTA was atypical. We believe that FFT, secondary to unstable plaque formation, may exhibit irregular filling due to blood flow erosion. We consider that the patient in case 2 experienced worsening ischemic stroke due to unstable plaque and small emboli detaching from an FFT, resulting in obstruction of the distal lumen. Generally, the risk of CEA is higher as symptoms progress (20). However, urgent CEA is appropriate for progressively worsening stroke due to FFT, which is consistent with the findings of Cancer-Perez et al. (21). The likelihood of small embolus escape and early infarction due to soft and loose fresh thrombus and thrombus caused by unstable plaque is lower during intraoperative thrombus removal in CEA compared to carotid artery stenting (CAS) (22). Tsumoto et al. stated that all 3 patients with carotid plaque and thrombosis developed embolic lesions after CAS with distal balloon protection (23). In addition, Tolaymat et al. pointed out that the thrombus is highly migratory and there is a risk of incomplete thrombus coverage or involvement of the stent in the vessel wall at the time of stenting, as well as the possibility of thrombus rupture and distal embolization (24). Although DWI showed that the patient had multiple acute cerebral infarctions and the lesions were larger than 1.0 cm, we used CTP to comprehensively evaluate the patient’s cerebral blood perfusion. We found that the patient’s cerebral blood perfusion had not been significantly affected, and the patient could tolerate surgery. Therefore, CTP plays an important role in guiding whether patients with acute cerebral infarction caused by FFT should undergo urgent CEA.

Thrombus is a common cause of stroke, and understanding the characteristics of stroke events before and after CEA and neuroimaging methods is crucial for clinical diagnosis and treatment. CTA, magnetic resonance imaging (MRI), and cerebral perfusion imaging can provide information about the extent of cerebral infarction and brain tissue function, aiding clinicians in analyzing the type of thrombus and determining the most suitable surgical indications. Prognostic factors such as collateral circulation and cerebral blood perfusion are of great importance (1). Collateral circulation plays a crucial role in determining the final volume of cerebral infarction and the prognosis following an AIS. Patients with more robust collateral circulation typically experience better clinical outcomes. The modified ASITN/SIR collateral scores offer a quick and accurate assessment of the degree of collateral circulation openness (25). In case 2, despite the absence of preoperative perfusion abnormalities, the patient experienced short postoperative hypoperfusion due to a collateral circulation score of 2 (indicating poor collateral circulation) on the affected side. Although digital subtraction angiography may be invasive and time-consuming, its accuracy as the gold standard for evaluating collateral circulation is unquestionable. When combined with interventional treatment, the time required becomes acceptable. Therefore, several studies have reported the feasibility of neurointerventional therapy for FFT and acute thrombosis after CEA (6,26-28). In cases of patients with both extracranial and intracranial occlusions, the effectiveness of CEA is not satisfactory. In such cases, combining CAS with mechanical thrombectomy at the site of intracranial embolization can rapidly restore cerebral blood perfusion and reduce cerebral ischemic damage (26,27). However, urgent CEA offers several advantages in the management of ultra-early cerebral ischemic events. First, in cases of extracranial ICA occlusion due to acute thrombosis and progressive stroke resulting from free thrombus, urgent CEA can be performed to rapidly open and restore blood flow, thereby restoring cerebral perfusion, and has a lower risk of distal embolism due to thrombus escape. Second, CEA has a lower probability of cerebral hemorrhage and intracranial hematoma formation due to intracranial hemorrhage (ICH) compared to CAS. Hussain and Singh present that CAS is more likely to cause ICH than CEA and most of these hemorrhages may be due to ICH (29,30), and Singh reported that CAS is also more likely to cause intracranial hematoma formation (30). The main causes of ICH include balloon dilatation and stent placement, which may interfere with carotid pressure receptor reflexes (31), and mandatory postoperative dual antiplatelet therapy with aspirin and clopidogrel. Finally, timely preoperative imaging to assess the cerebral perfusion and the degree of opening of the collateral circulation, as well as intraoperative real-time transcranial Doppler monitoring of middle cerebral artery flow, can accurately and effectively reflect the patient’s cerebral perfusion situation and tolerance. Once it is found that a hypoperfusion situation is present, diversion tubes can provide a part of the brain tissue to enable partial blood flow, reduce the ischemic time of the brain tissue around the infarction, and allow the brain tissue to adapt to the part of blood flow to reduce the incidence of ICH following the opening of ICA. CEA, which has a significant effect in preventing stroke, is considered the preferred method according to international guidelines. This has convinced us of the great potential of urgent CEA. Indications for urgent CEA include unstable plaques with a risk of intracranial embolism, new cerebral infarcts <1.0–1.5 cm, the absence of significant neurological impairment (coma), and hemorrhagic stroke (21). This case also suggests that FFT and isolated thrombosis after CEA can be indications for CEA. We firmly believe that urgent CEA re-exploration can effectively address fresh thrombi formed after surgery and can also be effective in progressively enhanced strokes caused by FFT. Lastly, we emphasize the utilization of multimodal imaging techniques, including CTA and MRI, which play a crucial role in identifying the most suitable indication for urgent CEA. Furthermore, the assessment of brain tissue viability and the degree of collateral opening through CTP and dynamic CTA serves as essential benchmarks to aid in determining the procedure’s benefits and whether it outweighs the associated risks.

Acknowledgments

Funding: This work was founded by the Natural Science Foundation of the Tibet Autonomous Region in 2024 (No. XZ2024ZR-ZY109[Z]).

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-422/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was provided by the patients for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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