Neuroradiology https://doi.org/10.1007/s00234-017-1935-7
INTERVENTIONAL NEURORADIOLOGY
Recurrent stenosis following carotid artery stenting treated with a drug-eluting balloon: a single-center retrospective analysis C. Pohlmann 1 & J. Höltje 2 & M. Zeile 3 & F. Bonk 3 & P. P. Urban 1 & R. Brüning 3
Received: 21 June 2017 / Accepted: 5 October 2017 # Springer-Verlag GmbH Germany 2017
Abstract Purpose Early in-stent restenosis after stent-protected angioplasty of the carotid artery (SPAC) is an infrequent, but potentially harmful condition for patients with carotid artery disease. Methods In our retrospective single-center analysis of 176 patients with carotid artery stenting between 2009 and 2015, using duplex ultrasound, we detected 9 patients with highgrade carotid artery in-stent restenosis. All restenosis patients were treated with a drug-eluting balloon (DEB) to prevent recurrent neointimal hyperplasia. One patient had bilateral carotid artery disease with bilateral in-stent restenosis, and 1 patient needed repeated DEB treatment 19 months after the first DEB intervention, so 11 DEB procedures, in total, were performed. Results The median time-interval between primary carotid artery stenting and first DEB-treatment was 9 months. In 3 of the 11 interventions, the DEB treatment was assisted by an additional stent. One repeat DEB treatment was necessary, and three DEB treatments were followed by a secondary stent. No peri-interventional complications (TIA, stroke, or death) were observed during or after DEB intervention. Therefore, in the entire group, the 1y event-free survival (EFS) was 100%, and the 2y/3y/5y EFS was 83%.
* R. Brüning
[email protected] 1
Abteilung für Neurologie, Asklepios Klinik Barmbek, 22291 Hamburg, Germany
2
Radiologie und Neuroradiologie, Asklepios Klinik Wandsbek, 22043 Hamburg, Germany
3
Asklepios Klinik Barmbek, Radiology and Neuroradiology, Rübenkamp 220, D-22291 Hamburg, Germany
Conclusion DEB intervention seems to be an effective and safe treatment for patients with high-grade in-stent restenosis after SPAC. Keywords Drug eluting balloon (DEB) . Percutaneous transluminal angioplasty (PTA) . Stent-protected angioplasty of the carotid artery (SPAC) . Carotid stenosis . In-stent restenosis after carotid artery stenting
Introduction Stent-protected angioplasty of the carotid artery (SPAC) has become an established treatment in the management of patients with significant carotid artery disease as an alternative to carotid endarterectomy. The method had been investigated in a number of trials such as SAPPHIRE [1], CAVATAS [2], CREST [3], and SPACE [4], comparing it to carotid endarterectomy. The rate of restenosis after SPAC seems to be higher than after endarterectomy; however, in the long-term follow-up of the SPACE and CREST trials, there were no significant differences in terms of recurrent strokes or TIA [5]. We became interested in the time course of in-stent carotid artery restenosis after SPAC and potential treatment options for high-grade restenosis. Although in-stent restenosis is usually infrequent, it remains a challenging condition. A number of papers and case reports using varying methods to treat instent restenosis have been published with differing outcomes [6–8]. In terms of safety and efficacy, the most favorable data have been reported for drug-eluting balloons (DEB) after their initial introduction in femoral arteries [9] and consequently, the use of DEB has been recommended for other vessels [10]. However, limited data exist for the treatment of in-stent carotid artery restenosis with DEB [6].
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Therefore, our aim was to determine the outcomes based on treatment with DEB in our patients after carotid artery stenting (SPAC). Our hypothesis was that the use of DEB therapy would prevent recurrent in-stent restenosis and reintervention, compared with other published results.
Methods From our hospital database, we retrospectively selected patients in the time interval from 2009 to 2015, based on the German DRG BOPS^ (operations and procedures) code 883B (intervention with a drug-coated balloon) and matched them with the keywords carotid artery stent and drug-eluting balloon from the radiological database. Both symptomatic and asymptomatic patients with atherosclerotic occlusive disease and carotid artery stenting were included in the analysis. In this time interval, we performed 176 primary carotid artery stenting procedures, and a total of 11 DEB procedures on nine patients (median age at first intervention 66.0 years, standard deviation 11.7 years, six females and three men). One patient had bilateral carotid artery in-stent restenosis and received bilateral DEB PTA; another patient underwent repeated DEB intervention. Eight patients were treated with primary stenting in our center; a single patient was included who was treated with carotid artery stenting in an outside facility. Inclusion criteria in our retrospective evaluation were matching entries in the database and data available on follow-up. Duplex ultrasound was performed at least 12 months after the DEB procedure unless a patient was lost to follow-up. The longest follow-up period was 82 months in one patient. Duplex ultrasound was carried out by a high-end ultrasound system (Hitachi Preirus or Siemens Acuson S 2000) operated by an experienced and board-certified neurologist (German Ultrasound Society, DEGUM, LEVEL II). Each ultrasound examination was performed by the same neurologist. For high-grade restenosis, direct ultrasound criteria were administered according to published data [11, 12]. Additionally, we Table 1 Ultrasound criteria for high-grade carotid artery in-stent restenosis (> 70% NASCET)
PSV
applied different indirect ultrasound criteria to increase the diagnostic accuracy of high-grade stenosis (retrograde flow in the ophthalmic and/or supratrochlear artery, pre-stenotic decrease of diastolic flow velocity in the ipsilateral common carotid artery [13], or a post-stenotic decrease in the systolic flow velocity in the internal carotid artery of < 50 cm/s) (Tab. 1). Exclusion criteria for the retrospective analysis consisted of intracranial Bdistal^ stenosis of the internal carotid artery due to the use of different stent types there. Patients with unstable clinical conditions, such as an acute stroke and the necessity to perform emergency stenting and intracranial thrombectomy, were also excluded. Carotid artery stenting (SPAC) was carried out by experienced interventional neuroradiologists under anaesthesiological standby. All patients were not intubated and none of the patients received general anesthesia; only mild conscious sedation was carried out by the anesthesiologist. All interventions were performed via a transfemoral approach on a Philips Allura FD 20 (Philips Medical Systems, Best, The Netherlands). For the sessions, a 6-F, 90-cm guide sheath (CORDIS, Cardinal Health, Milpitas, CA, USA) was usually used and positioned with a 100-cm, 6-F catheter (Envoy, Codman Neuro, Raynham, MA, USA) either in the MPD or Simmons 2 configuration and was positioned proximal to the carotid bifurcation. For safety reasons, the catheter was continuously flushed with saline. A continuous infusion and an intravenous bolus of heparin (usually 2000 or 3000 international units, depending on pre-interventional aPTT) were administered to obtain an activated clotting time (ACT) of 200–250 s. We used a guidewire (PT Graphics; Boston Scientific, Marlborough, USA). Following the primary stent implantation angioplasty, a PTA balloon catheter was used in all cases (Ultrasoft SV; Boston Scientific, Marlborough, MA, USA). Stents used in the initial SPAC were Precise Pro Rx (CORDIS, Cardinal Health, Milpitas, CA, USA) in one examination, Protégé Carotid Stent (COVIDIEN/ Medtronic, Plymouth, USA) in one examination, and Carotid Wallstent (BOSTON SCIENTIFIC, Marlborough, MA, USA) in eight stent procedures, reflecting the predominant use of the latter stent model in our patient population. One SPAC was performed in another hospital.
> 300 cm/s*
EDV
> 125 cm/s*
ICA/CCA-index Indirect criteria for high-grade stenosis present
>4 •Retrograde flow in the ophthalmic and/or supratrochlear artery •Pre-stenotic decrease of diastolic flow velocity in the ipsilateral common carotid artery (increased pulsatility index) •Poststenotic decrease of systolic flow velocity in the internal carotid artery < 50 cm/s •Intracranial collaterals (contralateral anterior cerebral artery, ipsilateral posterior communicating artery)
PSV peak systolic velocity, EDV end diastolic velocity *In near occlusion ICA-stenosis (stenosis > 90%) variable PSV and EDV
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DEB dilation was performed in an identical setting using second-generation drug-eluting balloons: in 6 procedures, we used a SeQuent Please® (Braun Melsungen AG, Vascular Systems, 12,359 Berlin, Germany) and in 5 procedures, the IN.PACT Amphirion ® balloon (Medtronic, Minneapolis, MN, USA). Angiographic stenosis was determined in the diagnostic runs using the NASCET [14] scale both before and after treatment. In both DEB, balloons used the nominal pressure and dilatation time was performed according on the suggestions of the manufacturers: the SeQuent Please® balloon was recommended to be used with an inflation time of Ba minimum of 30 s^ and with a dilatation pressure of B8–12 atm^. In contrast, the use of the IN.PACT Amphirion balloon was at a nominal pressure of 7 atm with no minimal inflation time. Each of the maneuvers was a single inflation and was not repeated, followed by a diagnostic DSA run. The use of protection filters was at the discretion of the neurointerventionalist and were not used in these procedures. Care was taken to have the anticoagulation checked at this time. In all cases, patients were informed in detail about the specific use and the off-label indications of DEBs in carotid artery restenosis and written informed consents were obtained from all patients. Following all interventions, the patients were transferred to our stroke unit for close monitoring, especially of blood pressure (Target systolic blood pressure < 150 mmHg) and clinical neurological conditions for at least 24 h. All patients received orally administered acetylsalicylic acid (100 mg/day) and clopidogrel (75 mg/day) at least 3 days before the procedure. If clopidogrel treatment or acetylsalicylic acid could not be started 3 days before the procedure, a loading dose (300 mg clopidogrel or 500 mg acetylsalicylic acid) was administered the day before intervention. In all patients, we evaluated the efficacy of acetylsalicylic acid and Clopidogrel treatments by performing a Multiplate Analysis (Roche Diagnostics International Ltd., CH-6343 Rotkreuz, Switzerland). In the case of insufficient platelet inhibition, a reloading dose of acetylsalicylic acid (500 mg) or clopidogrel (300 mg) was delivered, and the respective daily dose was increased (Clopidogrel 150 mg/day or acetylsalicylic acid 250 mg/ day). Sufficient platelet inhibition was tested by repeated Multiplate Analysis. Peri-procedurally, all patients were treated with i.v. heparin the day before stenting or DEB-PTA to achieve stable anticoagulation (target aPTT 50–60 s). Treatment with heparin was continued for 24 h after intervention and aPTT was closely monitored before and after endovascular therapy. All patients were discharged with a 3-month prescription for acetylsalicylic acid and clopidogrel; single antiplatelet therapy (acetylsalicylic acid or clopidogrel) was continued thereafter, providing that no relevant restenosis was detected. Duplex ultrasound was performed on each patient during the first 24 h after endovascular therapy. Further ultrasound
examinations were carried out 3 and 9 months after intervention. In case of an early detected restenosis (increased systolic blood flow velocity inside the stent), a closer monitoring every 3 months was scheduled (Table 1).
Results The patients’ treatment outcome and follow-up data are shown in Table 2 for the time between primary carotid artery stenting and restenosis; these restenoses usually occurred within the first year, the median interval between both interventions being 9 months. Accordingly, in our group, at 9 months, the eventfree survival (EFS) was 50%, the 1y EFS was 20%, and the 2y EFS 10%. Table 3 shows the existence of typical cardiovascular risk factors (arterial hypertension, diabetes mellitus, smoking, and hypercholesteremia) and other known vascular diseases or risk factors in our patient group. In all patients, hypercholesteremia was present, nevertheless, all restenosis arose despite treatment with statins. All but one patient had arterial hypertension, five of nine patients were active smokers, two more patients stopped smoking years before primary treatment of the carotid artery stenosis. In four of nine patients, diabetes mellitus was present. Only one patient had another vascular disease (fibromuscular dysplasia of renal and subclavian arteries) and suffered from hyperlipoproteinemia(a). After treatment of restenosis with a DEB, one single restenosis event was observed in our group, 18.9 months after the first DEB procedure. Therefore, in the entire group, the 1y EFS was 100%, and the 2y/3y/5y EFS was 83%. A typical case of restenosis detected by duplex ultrasound, its treatment with DEB PTA, and the normalized ultrasound examination is shown in Fig. 1a–d. During DEB-interventions, there were no interventional complications leading to new or aggravated neurological deficits in the patients. Technical success of the restenosisintervention was achieved in 100% of cases; however, in three cases, the DEB-intervention in our series was followed by a secondary stent implantation; an angiographically safe situation could only be achieved followed by a second (carotid wall) stent due to persistent edge-stenosis (RS, GG); in the third patient (JH), an asymptomatic dissection occurred. In the first of these cases (RS) in a 74 year old patient, there was elastic recoiling in a distal edge-stenosis in the initial control after DEB angioplasty, which was in the same session treated with an overlapping 5 × 30 mm Boston Wall stent with good angiographic result. The second intervention was on an at the time of intervention 63-year-old male (GG), who had a proximal edge-stenosis at a Boston Scientific Wall stent and was combinedly treated by an DEB 5 × 40-mm balloon and a 7 × 30-mm Wall stent. The third intervention was on a 48year-old female with severe peripheral arteriosclerosis (JH), who had a proximal edge-stenosis and where initial
Neuroradiology Table 2 Drug-eluting balloon (DEB) interventional treatment: patient data; all patients had high-grade restenosis (> 70%) according to duplex ultrasound Pt.
Sex
Age at DEB-PTA (years)
Time interval between SPAC and DEB-PTA (months)
Angiographic restenosis grade (% NASCET)
Symptomatic (S) or asymptomatic (A) restenosis
Residual stenosis after DEB (% NASCET)
Recurrent stenosis after DEB
Peri-procedural stroke/TIA/ death
EH
F
83
9.0
A
90
0
−
−
IF
M
62
6.4
A
75
20
−
−
RS JH
M F
74 48
n.d. 3.8
A A
75 80
20 20
− −
− −
GG EB*
M F
63 74
13.8 11.5
A A
90 75
20 25
− −
− −
EB* IH# IH# ML
F F F F
74 65 66 52
9.7 4.3 23.2+ 24.9
A A S A
95 85 85 80
15 20 25 20
− + − −
− − − −
HT
F
76
6.7
A
95
10
−
−
66.0
9.0
85
20
Median
SPAC stent-protected angioplasty of the carotid artery, n.d. not determined (specific date of primary SPAC in another hospital not known) *Pt. EB received bilateral carotid artery stenting and bilateral DEB treatment #
Pt. IH developed restenosis after DEB-treatment and needed repeat DEB intervention
+
Interval between primary stenting and second DEB intervention (these interval data were not included in the analysis)
During the surveillance/follow-up after the DEB procedure, there was one single event of a symptomatic recurrent stenosis 19 months after the DEB-PTA (IH). The patient with repeated DEB-PTA had experienced an ipsilateral transient ischemic attack before the second DEB-PTA. All other patients that we could follow remained free from stroke or TIA. Three patients were lost to follow-up: one deceased due to a bronchial carcinoma 11 months after DEB, one deceased due to urosepsis 20 months after the first DEB intervention, and one is continuously hospitalized due to dementia and was not available for repeated ultrasound. Both deaths were not related to DEB treatment.
redilatation with a 4.5-mm Ultrasoft balloon, then a 5-mm Seqent Please DEB resulted in a small dissection, which was treated by a 7 × 30-mm Boston Wall stent. We correlated our pre-interventional ultrasound findings with gradings of angiographic stenosis. During duplex ultrasound examination, all patients had a restenosis grade of > 70%. All angiographic stenosis grades were also > 70%, so there were no false ultrasound diagnoses. High-grade instent restenosis could therefore be safely detected by duplex ultrasound performed by an experienced board-certified neurologist using direct and indirect criteria for duplex ultrasound. Table 3 Cardiovascular risk factors or other known vascular diseases of the patients with highgrade restenosis after SPAC
Pt.
Sex
ArtHTN
DM
Smoking
HypChol
Other vascular diseases/risk factors
EH IF
F M
+ −
+ −
+ − (ex-smoker)
+ +
− −
RS JH
M F
+ +
+ −
+ +
+ +
GG
M
+
+
− (ex-smoker)
+
− FMD renal and subclavian arteries, HLP(a) −
EB IH
F F
+ +
− −
− +
+ +
− −
ML
F
+
+
+
+
−
HT
F
+
−
−
+
−
ArtHTN arterial hypertension, DM diabetes mellitus, HypChol hypercholesteremia, FMD fibromuscular Dysplasia, HLP(a) hyperlipoproteinemia(a)
Neuroradiology Fig. 1 a–d 75-year-old female (HT) underwent primary stenting of a symptomatic left carotid artery stenosis. A 7 × 30-mm Carotid WALLSTENT was implanted. Six months later, a highest-grade (near occlusion) recurrent carotid artery stenosis due to severe neointimal hyperplasia was detected by duplex ultrasound (a); b shows DSA before and c after DEB intervention. Duplex ultrasound 14 months after DEB procedure (d) confirms the good long term result
Discussion In-stent restenosis is an infrequent but well-known risk after carotid artery stenting usually resulting from early neo-intimal hyperplasia. The problem appears to be very real as the number of physicians performing carotid artery stenting worldwide is increasing [15], partly because of the encouraging results of trials such as SAPHHIRE [15] or CREST [5]. Recent work such as from Gandini et al. described a restenosis rate of about 5% in a larger population [6]. However, other reports have shown large variations in rates of restenosis in most series with a small number of high-grade stenosis [16] up to asymptomatic restenosis rates as high as 10% after 49 months [17] . Even higher rates were published [18]. In part, these vast differences may be explained by different standards to define an in-stent restenosis or on the restenosis criteria used for the duplex ultrasound follow-up. Welldefined international guidelines that indicate the best treatments for management of these recurrences are lacking [6], but most centers choose to treat these restenoses after a high grade of stenosis is observed. Certain anatomical risk factors for in-stent restenosis have been identified, including high-grade stenosis or a lack of coverage of the common carotid artery [19]. Additionally, in patients with persisting stenosis, or with contralateral disease, Wasser et al. described increased risks on immediate postinterventional ultrasound [20]. In a secondary analysis of the
CREST trial, female sex, dyslipidemia, and diabetes were independent risk factors for in-stent restenosis and restenosis after carotid endarterectomy, whereas smoking only increased the risk of restenosis after endarterectomy but not after SPAC [21]. All common vascular risk factors (arterial hypertension, diabetes mellitus, hypercholesteremia, and smoking) could be observed in our small patient group with high-grade restenosis (Table 3). Every patient had hypercholesteremia and developed restenosis despite statin treatment. This suggests that statin treatment does not prevent intimal hyperplasia. Due to the small sample size, we did not perform any further statistical analysis concerning the vascular risk factors in our patient group. Except one patient with hyperlipoproteinemia (a) and previously diagnosed fibromuscular dysplasia of renal and subclavian arteries no additional vascular diseases or risk factors could be detected. Previous experience using DEB in this situation included seven patients with carotid in-stent restenosis treated with DEB and a mean follow-up of 14 months [22]. In that report, one patient developed an ipsilateral minor stroke 2 months after DEB treatment, despite normal ultrasound and angiographic findings. DEB was performed without the use of filter-based neuroprotection devices, as this use was at the discretion of the interventionalists, as previously described by Wasser et al. [20], compared to the obligatory filter use in series such as the work from Gandini et al. [6].
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Vajda et al. recently reported DEB treatment of intracranial stent restenoses in 51 patients, seven of those with a stenosis located in the carotid artery, and described a low recurrence rate (9%) at 8-month follow-up compared to conventional balloon PTA (50%) [23]. We were able to reproduce the low recurrence rate, however, we only included proximal extracranial carotid artery stenoses. Regarding the time point of restenosis, interestingly, in our group restenosis occurred significantly earlier (50% of events within the first 9 months), as described by Gandini [6], who detected restenosis at 18, 25, and 32 months following carotid stenting. As the technique used was almost similar, we did not observe a significant reason for this difference. Further data is necessary to clarify this incongruity. One patient experienced a transient ischemic attack before the second DEB-PTA, all other cases of restenosis in our study group were diagnosed as asymptomatic during the clinical and duplex ultrasound-based surveillance. Symptomatic restenoses have also been reported, for example in 1/7 patients by Zou [24]. Willforth-Ehringer et al. [25] reported two major cerebral events within 3 months of restenosis treatment. Nearterm duplex ultrasound is therefore crucial to detect early instent restenosis due to neointimal hyperplasia. Monetary considerations can be a potential drawback on the use of DEB. In our institution, the cost of DEB were high compared to PTA balloons; however, cost range about 2/3 compared to a carotid stent and about ½ of a filter protection system. In three of the 11 procedures, the angiographic control run following DEB-PTA showed a suboptimal result and was followed by a second stent procedure. We believe this to be a strong argument that these procedures have to be supervised by an experienced interventional neuroradiologist and have to be performed under the same precautions as the original stenting. However, under these precautions, the additional stent implantations were carried out without any complication. Limitations of the presented data include the small sampling size of a single center and the retrospective character of our study. Furthermore, we could not follow all patients on a long-term basis so we might have missed some restenotic events. As in three of 11 procedures, DEB-PTA treatment had to be combined with repeated stent-protected angioplasty our series does not exclusively represent DEB-PTA treatment results. In conclusion, endovascular treatment of in-stent carotid restenosis with DEB is safe and feasible; however, it may be necessary to perform repeated stenting in some cases. DEB therapy was able to extend the time-free interval from in-stent restenosis to re-intervention. DEB therapy still remains an individual treatment option. As it is an infrequent complication after carotid artery stenting, a prospective randomized trial probably might not be feasible.
Compliance with ethical standards Funding No funding was received for this study. Conflict of interest The authors declare that they have no conflict of interest. Ethical approval All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent Informed consent was obtained from all individual participants included in the study.
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