Cerebral hemodynamic monitoring in the early stage after simultaneous bilateral carotid artery stenting
Introduction
Atherosclerotic carotid stenosis is a significant contributor to ischemic stroke, accounting for approximately 15% to 20% of all stroke cases (1). For patients at high risk due to atherosclerotic carotid disease, carotid artery stenting (CAS) has emerged as a viable alternative to carotid endarterectomy (CEA) (2). The occurrence of bilateral carotid disease is not uncommon, with prevalence rates ranging from 8.1% to 39% among patients undergoing CAS due to carotid stenosis (3). Since the late 1990s, there have been numerous reports documenting the successful outcomes of simultaneous bilateral carotid artery stenting (SBCAS) (4-6). SBCAS is associated with several advantages, including lower medical costs, reduced vascular trauma from vessel access, immediate treatment of bilateral lesions, and greater convenience for patients compared to staged bilateral CAS (7). Despite these benefits, there are concerns regarding the theoretical risks associated with SBCAS, particularly the potential for complications such as cerebral hyperperfusion syndrome (CHS), hemodynamic depression (HD), myocardial infarction, and stroke. A recent meta-analysis has indicated an elevated risk of CHS in patients who undergo SBCAS when compared to those receiving unilateral CAS (UCAS) (8). This heightened risk is believed to stem from a greater increase in cerebral blood flow during bilateral artery treatment.
To monitor these risks, transcranial color-coded Doppler (TCCD) can serve as an effective clinical tool for assessing changes in cerebral hemodynamics and for detecting cerebral hyperperfusion (CHP) post-CAS (9). However, the routine application of these methods for the monitoring of acute hemodynamic alterations and the detection of CHS in patients undergoing SBCAS remains underexplored. Therefore, this study aimed to investigate the very early changes in cerebral hemodynamics after CAS in patients undergoing SBCAS and to compare these findings with those observed in patients receiving UCAS. By highlighting the importance of hemodynamic monitoring, we aim to enhance the early diagnosis and preventative strategies for CHS in this patient population. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1222/rc).
Methods
Participants
From June 2013 to June 2023, patients who underwent CAS were enrolled in this retrospective observational noninterventional study after providing written informed consent. Patients with staged bilateral CAS, total carotid occlusion, absence of a suitable bone window for ultrasound imaging, and nonatherosclerotic carotid lesions (e.g., fibromuscular dysplasia, blunt trauma dissection, and Takayasu arteritis) were excluded from the study. Meanwhile, patients with CAS accompanied by near-occlusion lesions were included (10,11). Ultimately, 25 patients with SBCAS and 165 patients with UCAS were included (Figure S1). For both groups, demographic data and data related to vascular risk factors, lesion characteristics, perioperative systolic blood pressure (SBP), CHP, CHS, HD, and periprocedural complications were collected and analyzed.
CAS protocol
Asymptomatic or symptomatic patients with ≥70% carotid artery stenosis were evaluated for CAS in accordance with the criteria set forth by the North American Symptomatic Carotid Endarterectomy Trial (12,13). All patients provided written informed consent prior to the procedure. Preoperative antithrombotic therapy comprising 100 mg of aspirin and 75 mg of clopidogrel was administered at least 72 hours before CAS. A transfemoral catheterization was performed, with 2% lidocaine being used for local anesthesia. Following selective catheterization of the target artery, an intravenous bolus of 3,000 units of heparin was given, followed by a continuous transarterial heparin and saline infusion through the guiding catheter. In the presence of bilateral stenosis, the side with severe stenosis was prioritized for treatment and designated as the ipsilateral side. All lesions received distal embolic protection during the procedure. A near-occlusion lesion was considered present if at least two of the following four criteria are satisfied: delayed time of contrast arrival, evidence of collateral circulation, internal carotid artery (ICA)-to-ICA comparison of diameter reduction, and ICA-to-external carotid artery (ECA) comparison of diameter reduction (10,11).
Angioplasty balloon catheters of 4.0–5.0 mm (Boston Scientific, Natick, MA, USA) were used in routine fashion to perform predilation and the appropriate stent device (Precise RX, Cordis, Miami Lakes, FL, USA; Carotid WALLSTENT, Boston Scientific; Acculink, Abbott Laboratories, Chicago, IL, USA) was chosen based on the anatomical location and artery diameter. Postdilation was performed only when ≥30% residual stenosis remained. After stent deployment, carotid angiography, along with angiography of the distal cerebral vasculature, was conducted to assess the outcomes of the procedure.
TCCD
A TCCD machine (LOGIQ e, GE HealthCare, Chicago, IL, USA) fitted with 2.0-MHz sector array transducers was used for the examination. The middle cerebral artery (MCA) was insonated bilaterally through the temporal window at a depth of 50–60 mm. The peak systolic velocity (PSV) and the pulsatility index (PI) were recorded on the day before CAS as well as 1 hour after the CAS procedure. All TCCD examinations were performed by a single trained physician to ensure consistent insonation depths, angles, and skin-probe contact points.
Management
Standard blood pressure (BP) measurements were obtained from the same arm both before and after the procedure. If there was a difference in BP between the two arms, the measurements from the higher BP arm were recorded and monitored. Urapidil and/or nicardipine were administered before balloon predilation to keep the SBP below 160 mmHg. After predilation and stent deployment, the SBP for all patients was maintained in the range of 90–140 mmHg. CHP was defined as an increase of more than 100% in the MCA-PSV on either side compared to the preoperative value (14). CHS was diagnosed based on the following criteria: (I) the presence of an ipsilateral throbbing headache, with or without accompanying nausea, vomiting, or ipsilateral focal seizures, or the manifestation of a focal neurologic deficit in the absence of radiographic evidence of infarction (15); and (II) with or without CHP diagnosed by TCCD. Once CHP was diagnosed in patients, a more stringent BP management protocol was initiated, the aim of which was to achieve target BP levels of 120/80 mmHg (16). Subsequently, measurements of MCA-PSV and SBP were obtained at 3-hour intervals after surgery until the cessation of CHP. Patients who experienced periprocedural hypotension (BP <90/60 mmHg) or bradycardia (heart rate<50 beats per minute) were diagnosed with HD and treated with intravenous dopamine and/or atropine as necessary (17). Persistent HD was defined as HD lasting at least 1 hour (18). Minor stroke was defined as a National Institutes of Health Stroke Scale score of 3 or lower (19).
Ethical statement
The protocol for this study was approved by the Institutional Review Board of Peking University First Hospital and conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Anonymized data were obtained from the Department of Interventional Radiology and Vascular Surgery at Peking University First Hospital. Informed consent was obtained from all participating patients.
Statistical analysis
Statistical analyses were performed with SPSS version 26.0 (IBM Corp., Armonk, NY, USA). The data are presented as the median, mean, standard deviation (SD), and proportions. Paired t-tests were used to compare PSV and PI values measured the day before and 1 hour after CAS. Differences between groups were analyzed via independent t-tests and chi-squared tests.
To adjust for 11 factors—including gender, age (≥70 years), hypertension, diabetes mellitus, dyslipidemia, smoking status, symptomatology, degree of ipsilateral stenosis (≥90%), presence of near occlusion lesions, stent types, and simultaneous stenting of the vertebral—propensity scores were applied. A well-balanced cohort was created by matching each patient in the SBCAS group with no more than two patients in the UCAS group for data comparison. A P value <0.05 was considered statistically significant.
Results
Table 1 shows baseline data of patients with SBCAS and UCAS in this study. There were no statistically significant differences between the two groups in terms of the rate of gender, age, hypertension, diabetes mellitus, dyslipidemia, smoking history, types of stents used, baseline SBP, or baseline MCA-PSV. However, patients in the SBCAS group exhibited more severe ipsilateral stenosis (P=0.006).
Table 1
| Variable | SBCAS group (n=25) | UCAS group (n=165) | P |
|---|---|---|---|
| Male | 24 (96.0) | 147 (89.1) | 0.474 |
| Age ≥70 years | 12 (48.0) | 61 (37.0) | 0.291 |
| Hypertension | 23 (92.0) | 128 (77.6) | 0.096 |
| Diabetes mellitus | 10 (40.0) | 61 (37.0) | 0.770 |
| Dyslipidemia | 6 (24.0) | 48 (29.1) | 0.599 |
| Smoking | 12 (48.0) | 94 (57.0) | 0.400 |
| Asymptomatic | 6 (24.0) | 68 (41.2) | 0.100 |
| Ipsilateral stenosis degree ≥90% | 20 (80.0) | 84 (50.9) | 0.006* |
| Ipsilateral NO lesions | 6 (24.0) | 24 (14.5) | 0.361 |
| Contralateral stenosis degree | 81.6±8.9 | ||
| Stent type | |||
| Precise RX | 24 (48.0) | 81 (49.1) | 0.892 |
| WALLSTENT | 13 (26.0) | 47 (28.5) | 0.731 |
| Acculink | 13 (26.0) | 37 (22.4) | 0.600 |
| Simultaneous vertebral artery stenting | 1 (4.0) | 10 (6.1) | >0.999 |
| Baseline SBP (mmHg) | 147±14 | 144±16 | 0.499 |
| Baseline iMCA-PSV (cm/s) | 77.9±25.0 | 79.3±23.0 | 0.420 |
| Outcomes | |||
| Transient or permanent HD | 6 (24.0) | 31 (18.8) | 0.732 |
| Transient HD | 4 (16.0) | 25 (15.2) | 0.912 |
| Permanent HD | 2 (8.0) | 6 (3.6) | 0.633 |
| CHP | 3 (12.0) | 4 (2.4) | 0.072 |
| CHS | 0 | 1 (0.6) | |
| Minor stroke | 1 (4.0) | 2 (1.2) | 0.876 |
| Intracranial hemorrhage | 0 | 0 | |
| Myocardial infarction | 0 | 0 | |
| Renal failure | 0 | 0 | |
| Disabling strokes | 0 | 0 | |
| Deaths | 0 | 0 |
Data are presented as n (%) or mean ± standard deviation. *, P<0.05 was considered statistically significant. CHP, cerebral hyperperfusion; CHS, cerebral hyperperfusion syndrome; HD, hemodynamic depression; iMCA-PSV, ipsilateral middle cerebral artery-peak systolic velocity; NO, near occlusion; SBCAS, simultaneous bilateral carotid artery stenting; SBP, systolic blood pressure; UCAS, unilateral carotid artery stenting.
In the SBCAS group, 1 hour after CAS, the TCCD showed a significant increase in PSV in the ipsilateral MCA (35% increase; from 78±25 to 105±22 cm/s; P<0.001) and in the contralateral MCA (24% increase; 89±24 to 108±27 cm/s; P<0.001). The average PI also increased in the ipsilateral MCA (from 0.75±0.17 to 0.91±0.19; P<0.001) and in the contralateral MCA (from 0.83±0.16 to 0.94±0.19; P=0.002) (Table S1). In the UCAS group, 1 hour after CAS, significant increases in PSV were observed in the ipsilateral MCA (27% increase; 79±23 to 100±28 cm/s; P<0.001) and in the contralateral MCA (3% increase; 91±27 to 94±28 cm/s; P=0.010). The average PI in the ipsilateral MCA also increased (from 0.82±0.18 to 0.93±0.21; P<0.001). However, there was no significant increase in PI in the contralateral MCA 1 hour after CAS (P=0.529) (Table S2).
The increase in ipsilateral MCA-PSV in the SBCAS group was significantly greater than that in the UCAS group (35% vs. 27%; P=0.043) (Table 2). There were no significant differences between the two groups regarding the rate of BP decrease or the rate of increase in ipsilateral MCA-PI (P=0.475).
Table 2
| Parameter | SBCAS group | UCAS group | P |
|---|---|---|---|
| SBP increase rate (%) | −20±10 | −18±12 | 0.475 |
| iMCA-PSV increase rate (%) | 44±41 | 26±26 | 0.043* |
| iMCA PI increase rate (%) | 24±21 | 16±22 | 0.098 |
| cMCA-PSV increase rate (%) | 24±22 | 3±18 | <0.001* |
| cMCA PI increase rate (%) | 14±18 | 1±15 | <0.001* |
Data are presented as mean ± standard deviation. *, P<0.05 was considered statistically significant. CAS, carotid artery stenting; cMCA, contralateral middle cerebral artery; iMCA, ipsilateral middle cerebral artery; PI, pulsatility index; PSV, peak systolic velocity; SBCAS, simultaneous bilateral carotid artery stenting; SBP, systolic blood pressure; UCAS, unilateral carotid artery stenting.
The rate of complications following CAS was similar in both the SBCAS and UCAS groups. In the month following the procedure, none of the 190 participants experienced intracranial hemorrhage, myocardial infarction, renal failure, disabling strokes, or death. CHP was noted in three patients from the SBCAS group and in four patients from the UCAS group after CAS, with all cases presenting ipsilateral CHP (Table S3). The SBCAS group had a higher incidence of CHP, although this difference was not statistically significant (P=0.696). Only one patient in the UCAS group was diagnosed with CHS, manifesting as a mild headache, and this symptom and CHP resolved after 5 hours. There were 37 cases of transient or persistent HD reported in both groups. Among the eight patients with persistent HD, intravenous dopamine treatment alleviated symptoms within 48 hours.
After propensity score matching (PSM), two groups were analyzed: the PSM SBCAS group, which included 22 patients, and the PSM-UCAS group, which included 34 patients (Table 3). No differences in baseline characteristics were observed between the two patient groups. Previous studies have indicated that increases in ipsilateral MCA-PSV are significantly greater in patients with severe stenosis (20). Even after this risk factor was controlled for, the increase in ipsilateral MCA-PSV in the PSM-SBCAS group remained significantly higher than that in the PSM-UCAS group (48% vs. 31%; P=0.031). Additionally, no significant differences in the incidence of CHP or CHS were found between the two groups.
Table 3
| Variable | PSM SBCAS group (n=22) | PSM UCAS group (n=34) | P |
|---|---|---|---|
| Male | 21 (95.5) | 32 (94.1) | >0.999 |
| Age ≥70 years | 9 (40.9) | 15 (44.1) | 0.813 |
| Hypertension | 19 (86.4) | 31 (91.2) | 0.899 |
| Diabetes mellitus | 10 (45.5) | 17 (50.0) | 0.740 |
| Dyslipidemia | 4 (18.2) | 7 (20.6) | >0.999 |
| Smoking | 11 (50.0) | 18 (52.9) | 0.830 |
| Asymptomatic | 5 (22.7) | 9 (26.5) | 0.752 |
| Ipsilateral stenosis degree ≥90% | 17 (77.3) | 24 (70.6) | 0.581 |
| Ipsilateral NO lesions | 4 (18.2) | 9 (26.5) | 0.473 |
| Stent type | |||
| Precise RX | 21 (47.7) | 17 (50.0) | 0.842 |
| WALLSTENT | 12 (27.3) | 10 (29.4) | 0.835 |
| Acculink | 11 (25.0) | 7 (20.6) | 0.647 |
| Simultaneous vertebral artery stenting | 1 (4.5) | 3 (8.8) | 0.940 |
| Baseline SBP (mmHg) | 143±15 | 145±17 | 0.472 |
| Baseline iMCA-PSV (cm/s) | 77.1±24.3 | 78.3±23.4 | 0.424 |
| Outcomes | |||
| Transient or permanent HD | 6 (27.3) | 8 (23.5) | 0.752 |
| Transient HD | 4 (18.2) | 7 (20.6) | >0.999 |
| Permanent HD | 2 (9.1) | 1 (2.9) | 0.696 |
| CHP | 2 (9.1) | 1 (2.9) | 0.696 |
| CHS | 0 | 0 | |
| Minor stroke | 1 (4.5) | 1 (2.9) | >0.999 |
| Intracranial hemorrhage | 0 | 0 | |
| Myocardial infarction | 0 | 0 | |
| Renal failure | 0 | 0 | |
| Disabling strokes | 0 | 0 | |
| Deaths | 0 | 0 | |
| SBP increase rate (%) | −19±10 | −16±14 | 0.291 |
| iMCA-PSV increase rate (%) | 48±35 | 31±21 | 0.031* |
| iMCA PI increase rate (%) | 25±19 | 18±23 | 0.108 |
| cMCA-PSV increase rate (%) | 25±21 | 4±16 | <0.001* |
| cMCA PI increase rate (%) | 15±17 | 1±14 | <0.001* |
Data are presented as n (%) or mean ± standard deviation. *, P<0.05 was considered statistically significant. CHP, cerebral hyperperfusion; CHS, cerebral hyperperfusion syndrome; cMCA, contralateral middle cerebral artery; HD, hemodynamic depression; iMCA, ipsilateral middle cerebral artery; NO, near occlusion; PI, pulsatility index; PSM, propensity score matching; PSV, peak systolic velocity; SBCAS, simultaneous bilateral carotid artery stenting; SBP, systolic blood pressure; UCAS, unilateral carotid artery stenting.
Discussion
This retrospective observational noninterventional study investigated the early changes in cerebral hemodynamics following CAS in patients treated with SBCAS and in those treated with UCAS. Among studies on this subject, ours employed the largest sample size to date in evaluating early cerebral hemodynamic changes following SBCAS. Our results indicate that the SBCAS group showed significantly higher postoperative cerebral blood perfusion compared to the UCAS group, without an increased risk of CHP or CHS. These findings underscore the low risk of CHP and CHS among patients treated with SBCAS at our center and highlight the crucial role of TCCD monitoring. Effective management of cerebral perfusion and postoperative BP through these monitoring techniques is vital for preventing CHS.
For bilateral carotid artery stenosis, there remains no consensus regarding the most appropriate treatment strategy. Although SBCAS may be considered a viable option, alternatives such as CEA or a combination of CEA and CAS—both as staged or simultaneous approaches—have demonstrated positive outcomes in several studies (21-24). However, SBCAS offers distinct advantages, including minimized invasiveness, reduced contralateral stroke risk, lower medical costs, and greater convenience for patients (3). Given these compelling advantages, SBCAS presents a promising therapeutic option and may be regarded as a primary treatment modality for bilateral artery stenosis.
It is important to note that a meta-analysis conducted by Lai et al. found there to be a higher incidence of CHS in patients treated with SBCAS compared to those with UCAS (3.33% vs. 2.27%) (8,25). However, it should be emphasized that the indirect comparison of the two meta-analytic findings, the substantial heterogeneity among the included studies, and the inadequate adjustment for potential confounding variables may compromise the generalizability and robustness of the conclusions. In addition, the cerebral hemodynamic monitoring applied in this study might have potentially contributed to the prevention of CHS occurrence (26). In our study, none of the patients with SBCAS developed CHS (0/25) at our center. In the study by Hayakawa et al., staged angioplasty was found to be an effective and safe approach to carotid revascularization aimed at avoiding CHS (27). However, several concerns persist regarding this method, including the lack of a standardized protocol for anesthesia, the selection of protective measures, the timing of submaximal angioplasty in relation to stenting, the protocol to follow if recoil occurs during the second session, the criteria for evaluating CHS, and the relatively high incidence of CHS within certain subgroups (16,27). Consequently, the choice between SBCAS and staged bilateral CAS remains a topic of controversy. At our facility, the high prevalence of comorbidities among patients, coupled with extended hospitalization waiting periods, has led healthcare providers to favor the implementation of SBCAS.
The risk of CHS after CAS is estimated to be between 3.1% and 6.8%, with the majority of cases occurring in the early postoperative period (25). In this study, after adjustments were made for the risk factor of ipsilateral severe stenosis, the increase in cerebral perfusion in the PSM SBCAS group was significantly greater than that in the PSM UCAS group. Importantly, there was no corresponding increase in the risk of CHP or CHS. Among the 190 patients with SBCAS or UCAS in our study, only one developed mild CHS, with symptoms resolving after 5 hours. Our findings indicate that although the SBCAS group exhibited a more pronounced increase in cerebral perfusion, there is no associated elevated risk of CHP or CHS within this cohort. These results are in alignment with the observations reported by Jiang et al. (3).
Prior studies have demonstrated that TCCD measurements have high sensitivity for detecting and predicting CHS (28-30). As a bedside, ionizing radiation-free, and cost-effective assessment tool, TCCD presents a promising strategy for preventing CHS in at-risk patients. The use of TCCD monitoring facilitates the prompt detection of CHP and enables more stringent management of BP. This approach has been shown to effectively reduce the risk of CHS in patients undergoing CAS (31). It is important to note that the diagnosis of CHS has shown considerable heterogeneity across various studies (14). We define CHS as the presence of pulsating headache occurring either alone or in combination with nausea, vomiting, or other associated symptoms in the absence of any evidence of cerebral infarction (8). Given that this diagnostic approach relies on clinical symptomatology, it holds significant clinical relevance and can effectively guide subsequent therapeutic decisions. CHP represents a valuable hemodynamic finding that may indicate the likelihood of CHS. In a prospective study, the sensitivity and specificity of CHP for predicting CHS were 47.6% and 93.6%, respectively (32). Furthermore, performing TCCD at 1 hour post-CAS, rather than immediately after the procedure, may help mitigate artifacts caused by transient reactive hyperemia (33). Notably, a BP control strategy guided by ipsilateral MCA-PSV changes—rather than a sole reliance on empirical approaches—may play a vital role in preventing CHS at our center. Future studies should confirm these findings.
Previous studies have reported increases in ipsilateral MCA-PSV shortly after CAS, as evaluated by TCCD (20,34). Our earlier studies also indicated that elevations in MCA-PSV were more pronounced in patients with higher initial stenosis and near-occlusion lesions (10,20). Future investigations will include multivariate statistical analyses of cerebral hemodynamic changes following CAS to better understand the impact of varying lesion types and surgical modalities on MCA-PSV elevation.
This study involved several limitations. First, we employed a retrospective observational design with inherent selection bias. Second, measurement uncertainty may exist in TCCD examinations, but attempts were made to minimize this (16). Third, our cohort exhibited a higher proportion of male patients, primarily attributable to the high incidence of carotid artery stenosis in males and the greater likelihood of an absent temporal window in females. Finally, although certain studies have assessed the safety of SBCAS in comparison to staged bilateral CAS (7,35), we excluded patients with staged bilateral CAS due to the limited sample size of this subgroup. In future research, we will conduct a more in-depth investigation into the hemodynamic alterations associated with SBCAS in comparison to staged bilateral CAS.
Conclusions
This retrospective cohort study revealed that ipsilateral MCA-PSV and PI significantly increased 1 hour post-CAS in patients with both SBCAS or UCAS. Importantly, the elevation in ipsilateral MCA-PSV was significantly more pronounced in the SBCAS group than in the UCAS group. Our study supports the potential benefit of immediate postoperative TCCD evaluation in patients post-CAS, allowing for timely adjustment of therapeutic strategies based on the findings. This approach demonstrates the potential value in reducing the risk of CHS. To further substantiate our findings and enhance clinical management strategies, additional well-designed studies, including prospective and randomized controlled trials, are imperative.
Acknowledgments
None.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1222/rc
Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1222/dss
Funding: This work was funded by
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1222/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. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Peking University First Hospital’s institutional review board and informed consent was obtained from the patients.
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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