Abstract
Most previous large studies of carotid artery stenting (CAS) in maintenance hemodialysis patients are old-era, do not describe the types of stents and method of protection, and their effectiveness is unknown. CAS has progressed remarkably, and tailor-made CAS is now possible in hemodialysis patients according to the lesion. We aimed to analyze the outcomes of CAS in maintenance hemodialysis patients treated in our institution.
We retrospectively investigated the data of patients who underwent elective CAS in our institution between January 2012 and April 2023. Firstly, we verified the outcomes of CAS in maintenance hemodialysis patients. Secondly, the outcomes of CAS in maintenance hemodialysis patients were compared with CAS in nondialysis patients during the same period.
During the study period, 212 patients with carotid stenosis underwent CAS. Among these, 18 patients undergoing maintenance hemodialysis were identified for analysis. All 18 patients underwent lesion-specific tailor-made CAS. All 18 patients were technically successfully stented with good vasodilation and improvement in stenosis. No symptomatic cerebral infarction occurred within 30 days after CAS. There was no difference between dialysis and nondialysis patients in the risk of symptomatic complications and death occurring within 30 days after surgery. There was a higher risk of hemorrhagic complications not associated with prognosis in the dialysis group (23.1% vs 1.0%, P = 0.0047). No in-stent restenosis (>50% stenosis) and ipsilateral cerebral infarction at 1 year occurred during follow-up.
CAS in hemodialysis patients may be safe and effective.
Keywords: carotid artery stenting, maintenance hemodialysis, FilterWire EZ
Introduction
Carotid artery stenosis is a major cause of cerebral infarction.1-4) The risk of cerebral infarction is 2-7 times higher in patients on maintenance hemodialysis than in patients with normal renal function.5,6) The prevalence of carotid artery stenosis in maintenance hemodialysis patients is 73.8%, which is higher than the rate in patients with normal renal function.7) The number of patients receiving maintenance hemodialysis is increasing worldwide, including in Japan.8,9) Therefore, clinicians should expect to treat more cases of carotid artery stenosis in maintenance hemodialysis patients in the future.
Previous studies have shown that carotid endarterectomy (CEA) may be effective in preventing stroke in maintenance hemodialysis patients.10-12) However, carotid artery stenting (CAS) may be more suitable than CEA in this subpopulation, considering that these patients commonly have risk factors for poor CEA outcome (cardiac disease, severe respiratory disease, contralateral carotid artery occlusion, contralateral recurrent laryngeal nerve palsy, history of irradiation or surgical approach for neck, restenosis after CEA)13) and are in worse general condition.14-16) CAS is generally considered equivalent to CEA for treating carotid artery stenosis, as studies have demonstrated that it is not inferior in terms of long-term functional outcomes.17)
However, maintenance hemodialysis patients are frequently excluded from clinical studies of CAS in carotid artery stenosis. Reasons include their high-risk status and the fact that CAS in these patients is somewhat controversial because of high rates of perioperative mortality and complications.18, 19) Most previous large studies of CAS in maintenance hemodialysis patients were conducted from 2000 to 2010 and did not describe the type of stent, method of protection, or specific embolic protection device.18-20) Technical advances in CAS have been remarkable, and even hemodialysis patients can now have CAS tailor-made according to their lesions. We review our CAS technique and perioperative management protocol in the maintenance of hemodialysis patients at our hospital between January 2012 and April 2023. An analysis of our patient outcomes is also presented.
Materials and Methods
Patients
A total of 344 patients received treatment for carotid artery stenosis at our institution between January 2012 and April 2023 (CEA = 116 [33.7%], CAS = 225 [65.4%], Percutaneous transluminal angioplasty (PTA) = 3 [0.9%]). Our strategy is basically to choose CAS if CAS is possible, and CEA in selected cases in the CAS high-risk group (e.g., many unstable plaques). Patients who underwent elective CAS at our institution during the study period were retrospectively reviewed (n = 212). Those who were also receiving maintenance hemodialysis were included for analysis (n = 18). The indication for CAS was basically ≥50% stenosis in symptomatic arteries and ≥80% stenosis in asymptomatic ones.
Data recorded included patient characteristics (age, gender, degree of stenosis, plaque characteristics, medical history, smoking, modified Rankin score [mRS] at admission), symptomatic status (amaurosis fugax, transient ischemic attack, or stroke), surgical technique (protection device, stent type), intraoperative hypotension or/and bradycardia, perioperative complications, and clinical outcomes including peak systolic velocity (PSV) in carotid artery echocardiography (post-CAS: PSV/pre-CAS PSV, PSV at 1 year/pre-CAS PSV, PSV at 1 year/post-CAS PSV, ≥50% in-stent stenosis at 1 year and ipsilateral cerebral infarction at 1 year, mRS at 1 year). The degree of stenosis was measured using the North American Symptomatic Carotid Endarterectomy Trial method at the time of angiography. Preoperative plaque evaluation was performed using ultrasonography and magnetic resonance imaging (MRI). Unstable plaque was defined as low-intensity plaque or mobile plaque on ultrasonography and/or high-density plaque on T1-weighted or time-of-flight imaging. Calcified lesions were defined as those exhibiting calcification on computed tomography. Intraoperative hypotension and/or bradycardia was defined as the need for drug administration. Perioperative complications were defined as symptomatic cerebral infarction, hyperperfusion, hemorrhagic complications, myocardial infarction, and death occurring within 30 days after surgery. Hemorrhagic complications were defined as extracranial hemorrhage requiring blood transfusion and cerebral hemorrhage. Previous studies have shown that PSV correlates with stenosis rate.21,22) In our institute, carotid echocardiography was performed with a Canon Apkio i700 (Canon, Tochigi, Japan) in the supine position in all patients. 7.5 MHz linear array deep palpation was used to measure PSV. If there were multiple stenoses in the stent, the PSV value at the site of the most severe stenosis was used as the PSV value. Postoperative stenosis improvement was assessed by post-CAS PSV/pre-CAS PSV. For restenosis at one year, ≥50% in-stent stenosis and PSV at 1 year/post-CAS PSV were assessed.
Procedural technique
Multiple antiplatelet drugs (clopidogrel 75 mg + aspirin 100 mg or prasugrel 3.75 mg + aspirin 100 mg) were administered daily for ≥14 days before the procedure. Platelet function testing was performed before treatment to evaluate the effect of the medications using VerifyNow (Accumetrics, San Diego, CA, USA). In hyperresponders, we reduced the dose of clopidogrel or prasugrel. In cases of ineffectiveness of prasugrel, clopidogrel or aspirin, we have responded by increasing the dose or adding cilostazol. CAS was performed under local anesthesia via transfemoral catheterization using a 9-Fr Radifocus Introducer II H (Terumo, Tokyo, Japan). Intraarterial heparin (3,000-5,000 U) was administered to maintain an activated clotting time of ≥275 secs. An 8-Fr Fubuki (Asahi Intecc Co., Ltd., Tokyo, Japan) or 9-Fr Optimo (Tokai Medical Products, Ehime, Japan) guiding catheter was placed in the common carotid artery. A Carotid GuardWire PS embolic protection device (Medtronic, Minneapolis, MN, USA) was used in the internal carotid artery (ICA) if the risk of an iatrogenic embolic complication was thought to be high. A FilterWire EZ (Boston Scientific, Natick, MA, USA) distal embolic protection device was placed into the petrous portion of the ICA after the lesion was carefully crossed where it was kept stable until filter deployment. If there is a high risk of embolic complications during lesion cross or a large amount of vulnerable plaque, proximal protection with flow reversal of external carotid artery (ECA) + common carotid artery or proximal protection + distal protection is used to tailor the procedure. Predilation was performed using a 2.0 to 3.5 mm balloon catheter. Stenting was preferentially performed using a Carotid Wallstent (Boston Scientific) of an appropriate length to span the lesion. Alternatively, a Precise stent (Cordis, Santa Clara, CA, USA) and Casper (Terumo Co., Tokyo, Japan) were used. Dilation was performed after stent placement using a 4.5-6.0 mm balloon catheter. After the procedure, the patient's systolic blood pressure was maintained between 90 and 140 mmHg; argatroban was administered for 48 hrs in addition to dual antiplatelet therapy (DAPT). DAPT was continued for a minimum of 3 months; thereafter, the doses were reduced as needed. Dialysis was basically performed the day after CAS. MRI and carotid echocardiography were performed 1 to 2 days after CAS and basically, postoperative follow-up with echo and MRI is performed every 3 months for 1 year after surgery, and every 6 months thereafter for cases with no problems. For the hyperperfusion high-risk group (such as near occlusion and stage II), Arterial spin labeling (ASL) and Single photon emission computed tomography (SPECT) were performed.
Statistical analysis
Clinical and angiographic data were analyzed. Continuous variables are expressed as means with standard deviation and were compared using t test. Categorical variables are expressed as frequencies with percentage and were compared using Fisher's exact test. P < 0.05 was considered significant. Statistical analyses were performed using EZR software (Saitama Medical Center, Jichi Medical University, Saitama, Japan).
Results
In 212 patients with carotid stenosis underwent CAS, 18 patients undergoing maintenance hemodialysis were analyzed (Table 1). Mean age was 75.9 ± 7.0 years and 88.9% were men in the dialysis group. Calcified plaque was present in 14 arteries and vulnerable plaque in 4. These patients were also more likely to be with coronary artery disease (88.9% vs 46.9%, P < 0.001), peripheral artery disease (77.8% vs 23.7%, P < 0.001), and with calcified lesions (77.8% vs 51.0%, P = 0.0458). Other patient characteristics did not significantly differ between the dialysis patients and nondialysis patients.
Table 1.
Baseline characteristics
| Patients characteristics | Overall (N = 212) | Dialysis patients (n = 18) | Nondialysis patients (n = 194) | P value |
|---|---|---|---|---|
| Age, y, average (SD) | 75.1 (7.8) | 75.9 (7.0) | 75.0 (7.9) | 0.6500 |
| Sex, Male, no. (%) | 186 (87.7) | 16 (88.9) | 170 (87.6) | 1.0000 |
| Stenosis*, average (SD) | 74.3 (13.3) | 79.7 (10.4) | 73.8 (13.4) | 0.0719 |
| Symptomatic, no. (%) | 91 (42.9) | 4 (22.2) | 87 (44.8) | 0.0818 |
| Plaque, no. (%) | ||||
| calcification | 113 (53.3) | 14 (77.8) | 99 (51.0) | 0.0458 |
| vulnerable plaque | 82 (38.7) | 4 (22.2) | 78 (40.2) | 0.2050 |
| Comorbid conditions, no. (%) | ||||
| Diabetes mellitus | 97 (45.8) | 12 (66.7) | 85 (43.8) | 0.0831 |
| Coronary artery disease | 107 (50.5) | 16 (88.9) | 91 (46.9) | <0.001 |
| Peripheral artery disease | 60 (28.3) | 14 (77.8) | 46 (23.7) | <0.001 |
| Hypertension | 170 (80.2) | 17 (94.4) | 153 (78.9) | 0.1340 |
| Dyslipidemia | 127 (59.9) | 8 (44.4) | 119 (61.3) | 0.2090 |
| Congestive heart failure | 36 (17.0) | 5 (27.8) | 31 (16.0) | 0.1990 |
| Smoking, no. (%) | 154 (72.6) | 10 (55.6) | 144 (74.2) | 0.0855 |
| Preoperative mRS, average (SD) | 0.95 (1.7) | 1.1 (1.6) | 0.7 (1.2) | 0.1680 |
SD: standard deviation; mRS: modified Rankin Scale *NASCET criteria.
Procedural characteristics and outcomes are shown in Table 2. All 18 patients underwent lesion-specific tailor-made CAS. The Carotid Wallstent (Boston Scientific) was used in 14 cases (77.8%), the Precise (Cordis) in 3 cases (16.7%) and Casper (Terumo) in one case (5.6%) for dialysis patients. The FilterWire EZ (Boston Scientific) was used in 17 cases (94.4%). Proximal protection was used in 4 (22.2%). There was no difference between dialysis and nondialysis patients in the used stents and protection devices. Post-CAS PSV/pre-CAS PSV showed a 0.44-fold improvement in flow velocity in both the hemodialysis and non-hemodialysis groups. PSV at 1 year/post-CAS PSV also not significantly different. There was no difference between dialysis and nondialysis patients in the risk of ipsilateral cerebral infarction, hyperperfusion syndrome, hypotension, myocardial infarction, and death occurring within 30 days after surgery. There was a higher risk of hemorrhagic complications in the dialysis group (23.1% vs. 1.0%, P = 0.0047). All bleeding complications in hemodialysis patients were gastrointestinal bleeding and the complications in nondialysis patients were cerebral hemorrhage and gastrointestinal hemorrhage. No in-stent restenosis (>50% stenosis) and ipsilateral cerebral infarction at 1 year occurred during follow-up. The mRS at 1 year was not significantly different between the dialysis and nondialysis groups.
Table 2.
Result
| Result | Overall (N = 212) | Dialysis patients (n = 18) | Nondialysis patients (n = 194) | p value |
|---|---|---|---|---|
| Stent, no. (%) | 0.4650 | |||
| Wallstent | 177 (83.5) | 14 (77.8) | 163 (84.0) | |
| Precise | 20 (9.4) | 3 (16.7) | 17 (8.8) | |
| Casper | 15 (7.1) | 1 (5.6) | 14 (7.2) | |
| Protection, no. (%) | 0.4630 | |||
| FilterWire EZ | 127 (60.0) | 13 (72.2) | 114 (58.8) | |
| FilterWire EZ + CCA and ECA balloon protection | 40 (18.9) | 2 (11.1) | 38 (19.6) | |
| FilterWire EZ + CCA balloon protection | 33 (15.6) | 2 (11.1) | 31 (16.0) | |
| CCA + ECA balloon protection only | 9 (4.2) | 0 (0.0) | 9 (4.6) | |
| Others | 3 (1.4) | 1 (5.6) | 2 (1.0) | |
| Intraoperative hypotension or/and bradycardia 30-day outcomes, no. (%) |
35 (16.5) | 2 (11.1) | 33 (17.0) | 0.7440 |
| Ipsilateral cerebral infarction | 8 (3.8) | 0 (0.0) | 8 (4.1) | 1.0000 |
| Hyperperfusion syndrome | 6 (2.8) | 0 (0.0) | 6 (3.1) | 1.0000 |
| Hypotension | 28 (13.2) | 3 (16.7) | 25 (12.9) | 0.7130 |
| Hemorrhagic complications | 5 (2.4) | 3 (23.1) | 2 (1.0) | 0.0047 |
| Myocardial infarction | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1.0000 |
| Death, no. (%) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1.0000 |
| Post-CAS PSV/pre-CAS PSV (SD) | 0.44 (0.34) | 0.44 (0.24) | 0.44 (0.35) | 0.9750 |
| PSV at 1 year/pre-CAS PSV (SD) | 0.48 (0.34) | 0.37 (0.23) | 0.49 (0.34) | 0.2710 |
| PSV at 1 year/post-CAS PSV (SD) | 1.18 (0.49) | 0.95 (0.38) | 1.20 (0.49) | 0.0971 |
| Stent, no. (%) | 0.95 (1.65) | 1.22 (1.92) | 0.92 (1.63) | 0.4640 |
| Ipsilateral cerebral infarction at 1 year, no. (%) | 1 (0.5) | 0 (0.0) | 1 (0.5) | 0.6230 |
| In-stent stenosis at 1 year, no. (%) | 14 (6.6) | 0 (0.0) | 14 (6.6) | 0.6140 |
CAS: carotid artery stenting; CCA: common carotid artery; ECA: external carotid artery; PSV: peak systolic velocity; SD: standard deviation
Representative case
An 81-year-old man on maintenance dialysis for chronic renal failure with a history of ischemic heart disease and pacemaker placement for complete atrioventricular block was admitted with paralysis of the right upper and lower extremities caused by a left cerebral infarction. Initial treatment was aspirin 100 mg and clopidogrel 75 mg daily. A 95% right ICA stenosis with severe calcification was found during a diagnostic workup (Fig. 1). General anesthesia was deemed too risky, and he was considered a suitable candidate for CAS, which was performed 16 days after admission. A 9-Fr long sheath was placed in the right femoral artery. Then, a 90 cm 9-Fr Optimo (Tokai Medical Products) was placed in the common carotid artery and a Carotid GuardWire PS (Medtronic) in the ECA (Fig. 2A). Once the balloons were inflated, a FilterWire EZ (Boston Scientific) was placed into the petrous portion of the ICA after crossing the lesion. The balloons were then deflated and the FilterWire EZ (Boston Scientific) deployed. Because of the calcification (Fig. 1), predilation was performed using a 2 × 9 mm Gateway Balloon Dilatation Catheter (Boston Scientific) at 6 atm for 30 secs, followed by staged angioplasty with 3 × 30 mm and 3.5 × 20 mm Coyote Balloon Dilatation Catheters (Boston Scientific) in stages (Fig. 2B). A 8 × 29 mm Carotid Wallstent (Boston Scientific) was implanted and angioplasty performed with a 5 × 20 mm Sterling Balloon Dilatation Catheter (Boston Scientific) for 30 secs at 6, 10, and 12 atm, respectively. Angiography showed a patent stent and adequate blood flow (Fig. 2C, D). After the procedure, the patient's blood pressure was maintained between 90 and 140 mmHg and argatroban was administered for 48 hrs; DAPT was continued. Carotid artery echocardiography the next day showed no in-stent occlusion or protrusion. The patient was transferred to a rehabilitation hospital with mRS score 3 on postoperative day 20. At the time of discharge from the rehabilitation hospital, his right upper and lower extremity strength had improved and his mRS score was 1.
Fig. 1.
Maximum intensity projection CTA images revealed severe calcification at the right carotid bifurcation extending into the internal carotid artery.
CTA: Computed Tomography Angiography
Fig. 2.
Right common carotid artery angiogram. A) Right common carotid angiography before treatment showed severe internal carotid artery stenosis. B) The stenosis partially improved after predilation. The stenosis improved even more after (C) stent placement and (D) subsequent dilation.
Discussion
In this study of maintenance hemodialysis patients who underwent CAS, no symptomatic cerebral infarction, myocardial infarction, or death occurred in the first 30 days after the procedure. There was no difference between dialysis and nondialysis patients in the risk of ipsilateral cerebral infarction, hyperperfusion syndrome, hypotension, myocardial infarction, and death occurring within 30 days after surgery. No in-stent restenosis and ipsilateral cerebral infarction at 1 year occurred during follow-up. The results of CAS in maintenance hemodialysis patients at our hospital were better than other reports to date.18-20) Possible reasons for this include our use of an embolic protection device in all patients and the use of proximal protection when the possibility of an embolic complication was considered high. We also performed platelet aggregation testing in all patients, which can assist in preventing both hemorrhagic and ischemic complications.
There was a higher risk of hemorrhagic complications in the dialysis group. Dialysis patients have been known to have an increased bleeding risk.23) Bleeding event rates for dialysis range between 42 and 89/1,000 person-years24-28) compared with 0.5-0.9/1,000 person-years in nondialysis patients. The increased bleeding risk could be explained by anemia, platelet dysfunction and impaired interaction between platelets and the vessel wall.29-31) Although there were no complications worsening of mRS score at discharge, hemorrhagic complications should be noted in dialysis patients.
Many previous studies examining CAS in maintenance hemodialysis patients have questioned the indications for CAS in maintenance hemodialysis patients due to the high perioperative mortality rate, perioperative complications, and short survival of maintenance hemodialysis patients.18-20) In a cohort study of 1,109 maintenance hemodialysis patients who underwent CAS, Arhuidese et al. reported perioperative stroke, death, and myocardial infarction rates of 9.6%, 3.2%, and 5.2%, respectively, in symptomatic patients; in asymptomatic patients, the corresponding rates were 4.7%, 2.9%, and 5.7%, respectively. These rates are significantly higher than those reported in patients not on dialysis.18) Adil, et al. reported perioperative neurological complication, death, and myocardial infarction rates of 1.6%, 2.1%, and 2.2%, respectively, which are superior to those reported by Arhuidese et al.18, 19) However, because their study had ahigh rates of perioperative mortality and morbidity, they suggested that CAS is a high-risk surgical procedure in dialysis patients and a careful analysis of the risk: benefit ratio needs to be made in such patients.
The studies mentioned above did not describe the type of stent, method of protection, or specific embolic protection device, so they may not reflect a contemporary level of medical care because of the age of the studies. In fact, the 30-day CAS stroke incidence and mortality rates in previous large studies have improved over time since the procedure was introduced.32) This may be due to device evolution, advances in technology, and increased practitioner experience. Most previous large studies of CAS in maintenance hemodialysis patients were conducted from 2000 to 2010. Our series only includes patients treated in 2012 and thereafter.
Patients with chronic kidney disease are more likely to have an unstable plaque than those without.33) Although various embolic protection devices have been developed to prevent embolic complications,33) randomized clinical trials have not shown that they clearly provide a benefit.34,35) However, we suggest that distal embolic protection devices are effective in preventing symptomatic embolization.36) In a recent large Japanese study, distal protection filters were the most commonly used device for preventing embolism (41.4%).37) Ishida et al.38) reported that 60 patients with carotid artery stenosis with unstable plaque (plaque/muscle ratio ≥1.5) were treated with a single set of devices: the FilterWire EZ (Boston Scientific) and Carotid Wallstent (Boston Scientific). Their report demonstrated that the frequency of symptomatic cerebral infarction was reported to be 0% (8.3% asymptomatic) and the rate of new lesions after CAS with vulnerable plaque was much lower than that in previous studies.38) In our series, a similar study was performed using the FilterWire EZ (Boston Scientific) and Carotid Wallstent (Boston Scientific).
The study has several limitations including its retrospective single-center design, small sample size, and short follow-up. Selection bias was likely present. Outcomes in maintenance hemodialysis patients are frequently poor18-20) and the indications should be carefully considered. Therefore, future large-scale clinical trials are warranted to confirm our finding that CAS is useful in the maintenance of hemodialysis patients.
Conclusion
The results of CAS in maintenance hemodialysis patients were better than previously reported. CAS in dialysis patients may be safe and effective.
Disclaimer
Author Haruhiko Kishima is one of the Editorial Board members of the Journal. This author was not involved in the peer-review or decision-making process for this paper.
Conflicts of Interest Disclosure
All authors have no conflict of interest.
All authors pledge that this manuscript does not contain previously published material and is not under consideration for publication elsewhere.
Acknowledgments
We thank Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.
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