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Grading Carotid Intrastent RestenosisA 6-Year Follow-Up Study

Carlo Setacci, MD; Emiliano Chisci, MD; Francesco Setacci, MD;Francesca Iacoponi, PhD; Gianmarco de Donato, MD

Background and Purpose—The accuracy of carotid ultrasound has not been well established in predicting intrastentrestenosis (ISR) after carotid artery stenting (CAS). The aim of this study is to determine different degrees of ISR usingultrasound velocity criteria compared to percentage of stenosis at angiography.

Methods—This is a 6-year prospective study. After CAS procedure, each patient underwent angiography for measuringISR (NASCET method) which was compared to peak systolic velocity (PSV), end diastolic velocity (EDV), and the ratiobetween PSV of internal carotid artery and common carotid artery (ICA/CCA). This was done within 48 hours, thuscreating a baseline value. Ultrasound (US) examination was performed at day 30, at 3, 6, 9, and 12 months, and thenyearly. Patients with an increase in PSV greater than 3 times the baseline value or in presence of PSV �200 cm/sunderwent angiography.

Results—814 CAS procedures, 6427 US examinations, and 1123 angiographies were performed. ISR �70% and ISR�50% was detected, respectively, in 22 patients and in 73 patients. We defined velocity criteria for grading carotid ISR:PSV �104 cm/s, if �30% stenosis; PSV:105 to 174 cm/s if 30% to 50% stenosis; PSV:175 to 299 cm/s if a 50% to70% stenosis; PSV �300 cm/s, EDV �140 cm/s, and ICA/CCA �3.8 if a �70% stenosis. Receiver operatorcharacteristic (ROC) curves for ISR �70% were, respectively, for PSV, EDV, and ICA/CCA: 0.99, 0.98, and 0.99.

Conclusions—US grading of carotid ISR can guarantee a correct follow-up after CAS if new customized velocity criteriaare validated by skilled operators using a specific protocol of follow-up in a certified laboratory. (Stroke. 2008;39:1189-1196.)

Key Words: follow-up study � stents � carotid stenosis � ultrasounds � angiography

Stroke is the third most common cause of death and theleading cause of disability1 in Western countries. Carotid

artery stenting (CAS) is a viable alternative2–7 to carotidendarterectomy (CEA) for the prevention of stroke for somepatients. Nowadays the number of patients undergoing CASis increasing rapidly, and these patients require intensivefollow-up to monitor the patency of the device and thepotential development of an intrastent restenosis (ISR). AnISR could reduce the benefit of the CAS in preventing stroke.

Duplex ultrasound (US) scanning is the standard techniqueto follow up patients who have undergone CEA or medicaltherapy alone. US velocity criteria such as peak systolicvelocity (PSV), end diastolic velocity (EDV), and the ratiobetween PSV of internal carotid artery and common carotidartery (ICA/CCA) correlate with angiographic percent steno-sis in nonstented carotid artery.8 Particularly, the appropriatethreshold velocities signifying different degrees of stenosishave been intensively analyzed and identified.9–12 However,US velocity criteria and threshold for different degrees ofrestenosis have not been well-established in patients whohave undergone CAS.13–21

The aim of this study is to show whether US examinationis accurate for the follow-up of patients with stented carotidarteries and to determine US velocity criteria and theirthresholds, compared to percentage of stenosis at angiogra-phy, highlighting a different degree of ISR.

Materials and MethodsStudy PopulationThis is a prospective study. Consecutive patients underwent CASduring a period of 6 years (December 2000 to Febraury 2006). Ourindications for treatment were the presence of a symptomatic carotidartery stenosis �70% or an asymptomatic stenosis of at least 80%according to the Doppler US criteria reported by Carpenter.12

Written informed consent for surgery was obtained from all patients.The endovascular procedure was routinely performed using a

guiding catheter technique via a femoral access. Demographicvariables and clinical, intraoperative, and follow-up data wereentered in a specific database by the operating team. Clinical dataand characteristics of carotid lesions, types of stents, and cerebralprotection devices used are shown in Table 1.

Follow-Up Protocol for CASOn completion of the CAS procedure, all patients underwentipsilateral cervical carotid angiography to exclude significant resid-

Received July 4, 2007; accepted September 7, 2007.From the Department of Surgery, Vascular and Endovascular Surgery Unit, University of Siena, Italy.Correspondence to Emiliano Chisci, MD, Department of Surgery, Vascular and Endovascular Surgery Unit, University of Siena, Italy. E-mail

[email protected]© 2008 American Heart Association, Inc.

Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.107.497487

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ual in-stent stenosis. Angiograms were obtained in anteroposterior,oblique, and lateral views. The view demonstrating the highestdegree of stenosis was used for the study. The degree of stenosis wasdetermined with North American Symptomatic Carotid Endarterec-tomy Trial (NASCET) criteria.22 The in-stent minimal luminaldiameter was compared with the distal nontapering portion of theICA serving as the reference segment. Diameters were measured byan independent blinded observer using a software program forquantitative digital angiographic analysis available at the imagingstation (MDQM; MEDCON Telemedicine Technology). Anyresidual stenosis 30% or greater was defined as a technical failureof CAS.

A US examination was performed within 48 hours of CAS andrepeated at day 30, at 3, 6, 9, and 12 months, and then yearly. TheUS examination measured the patency of the stented artery, thevalues of PSV, EDV, and ICA/CCA, and evidence of an internalthrombus or neointimal flap. All examinations were performed in thesame vascular laboratory, with the same US machines (UltramarkIU-22 and HDI 5000 ATL-Philips). The B-mode imaging frequencywas 7 MHz, and the pulsed-wave Doppler frequency was 4 MHz.

Velocity in the ICA was determined at distal, middle, andproximal portions of the stent. In addition, velocity was measured atany area of in-stent narrowing identified on B-mode images. Anangle of insonation of 60 degrees was used, with angle correctionwhere necessary (40 to 60°). We attempted to maintain the in-sonation of 60° all the time if possible, to standardize the study

methodology. The highest values for PSV, EDV, ICA/CCA wasconsidered in our study in all US examinations.

The angiography performed in all patients at the end of CAS wascompared to the US examination within 48 hours. Velocity data(PSV, EDV, ICA/CCA) were compared to the in-stent residualstenosis; this was the baseline value for each patient.

During the period of this study, patients with an increase in thevalue of PSV greater than 3 times the baseline value or in presenceof a PSV �200 cm/s underwent a diagnostic angiography. Moreover,on 89 patients who underwent contralateral CAS, an angiography ofthe first stented carotid artery was performed during the secondprocedure.

In all angiography procedures, patency and fracture of the deviceimplanted and the in-stent value of restenosis as described above(NASCET method) was evaluated. Patients with an ISR �70%(documented at angiography) underwent additional endovascularsurgery.

The results of all angiography were always compared to the USvelocity data by blinded operators.

Statistical AnalysisAll the parameters of this study are expressed as mean�SD. In alltests, probability value �0.05 is considered to indicate statisticalsignificance. The variables analyzed are PSV, EDV, and ICA/CCAversus the carotid in-stent percentage of stenosis at angiography (%of stenosis). These variables are compared with the Pearson coeffi-cient of correlation (R) and the relative probability value. Box plotsand scatter plots were constructed to visualize the correlations andthe distributions of percentage of stenosis classes. Thresholds fordifferent classes of percentage of stenosis were created (1��30%,2�30% to 50%, 3�50% to 70%; 4��70%), and receiver operatorcharacteristic (ROC) curves were generated for sensitivity andspecificity of various velocity criteria for the above-mentionedclasses. A function intended to determine the PSV trend in relationto the percentage of stenosis was created and is represented graph-ically (SAS System v.9.0, Inc).

Results814 CAS procedures were performed during the study period.Technical failure of CAS was 2.2% (18/814). The meanfollow-up period was 1364 days (4 to 2190 days). 21 patientsdied during the 6-year follow-up (4 to 1051 day postop). Theentire protocol of follow-up was completed by 29 patients at6 years, 103 patients at 5 years, 198 patients at 4 years, 374patients at 3 years, 552 patients at 2 years, and 783 patients at1 year. 6427 US examinations and 1123 angiographies wereperformed with a ratio of about 6:1 between US scans andangiographies. ISR �70% was detected in 22 patients,whereas ISR �50% was detected in 73 patients (all casesconfirmed by angiography). 3 intrastent thromboses, nointimal flap, dissections and asymptomatic intrastent occlu-sions were detected at US examinations and angiography. Nostent fracture was identified at angiography. Two of the ISR�70% patients were symptomatic (9%). Patients with ISR�70% underwent a new endovascular procedure and exitedfrom the study population.

Scatter plots of PSV, EDV, ICA/CCA are designed as afunction of percentage of stenosis at angiography. The Rcoefficient for any velocity criteria was always significant incases of percentage of stenosis with a probability value equalto 0.0001, as shown in Figure 1 (PSV versus % stenosis:R�0.55; EDV versus % stenosis: R�0.49; ICA/CCA versus% stenosis: R�0.71).

The percentage values of stenosis at angiography and thecorresponding values of PSV, EDV, and ICA/CCA observed

Table 1. Patients and Lesion Characteristics

PatientsCharacteristics Type Number %

Total procedures 814

Age, mean�SD* 73�8

Male gender 522 64.13

Symptomatic patients 385 47.3

Nicotine use 316 38.82

Hypertension 561 68.92

Diabetes 260 31.94

Polyvascular disease 323 39.68

Embolic protectiondevice Accunet filter 44 5.41

Filter wire 628 77.25

Angioguard 127 15.62

Spider 8 0.98

MO.MA. 6 0.74

Need of predilation 60 7.37

Stent Carotid wallstent 604 74.2

Nexstent 10 1.23

Precise 144 17.69

Acculink 49 6.02

Protégé 7 0.86

Ulceration† 225 27.64

Calcification‡ 316 38.82

Restenosis post-CEA 116 14.25

Plaque component‡(Gray-Wealeclassification44) 1 23 2.83

2 190 23.64

3 333 40.71

4 268 32.92

*Standard Deviation; †at angiography; ‡at ultrasound.

1190 Stroke April 2008



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Figure 1. Scatter plots of PSV (A), EDV(B), ICA/CCA (C) are plotted as a func-tion of percentage of stenosis at angiog-raphy. PSV indicates peak systolicvelocity; EDV, end diastolic velocity;ICA/CCA, ratio between PSV of internalcarotid artery and common carotidartery. The R coefficient is always signifi-cant with a probability value equal to0.0001 (PSV-stenosis: R�0.55; EDV-stenosis: R�0.49; ICA/CCA-stenosis:R�0.71).

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Figure 2. The distributions of classes of steno-sis (1��30%, 2�30% to 50%, 3�50% to70%; 4��70%) at angiography versus PSV(A), EDV (B), ICA/CCA (C) using box plots. PSVindicates peak systolic velocity; EDV, end dia-stolic velocity; ICA/CCA, ratio between PSV ofinternal carotid artery and common carotidartery.




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at US scans have been ordered into 4 classes: (1) % stenosis�30, (2) % stenosis 30 to 50, (3) % stenosis 50 to 70 and (4)% stenosis �70. The distributions of each class of stenosisare represented using box plots, as shown in Figure 2.

The values of percentage of stenosis and the correspondingvalues of PSV, EDV, and ICA/CCA grouped together inclasses are (mean value�SD): stenosis �30%�PSV:68.46�21.18 cm/s, EDV:27.20�10.46 cm/s, ICA/CCA:1.35�0.13;30% to 50% stenosis�PSV:142.32�35.51 cm/s, EDV:58.84�23.53 cm/s, ICA/CCA:1.97�0.39; 50% to 70% steno-sis�PSV:266.36�34.68 cm/s, EDV:123.5�18.42 cm/s,ICA/CCA:3.38�0.44; �70% stenosis�PSV:377.56�58.33cm/s, EDV:148.44�19 cm/s, ICA/CCA:4.08�0.71.

A few intervals for several velocity criteria (EDV, ICA/CCA) intersect each other and subsequently some observa-tions could point toward multiple classes, leading to amistaken classification for threshold velocity criteria. How-ever, the PSV values can be used to obtain potential thresh-olds in predicting different degrees of percentage of stenosis:a �30% stenosis�PSV �104 cm/s; a 30% to 50% steno-sis�PSV 105 to 174 cm/s; a 50% to 70% stenosis�PSV 175to 299 cm/s; whereas a �70% stenosis�PSV �300 cm/s.The EDV, ICA/CCA values failed to yield satisfactorythresholds for different degrees of stenosis, but 2 referencevalues for an ISR (�70% of stenosis) were identified: EDV�140 cm/s, ICA/CCA �3.8. See Table 2.

ROC curves were generated to evaluate the sensitivity andspecificity for identified threshold values of PSV for the 4different classes of percentage of stenosis and for EDV andICA/CCA in case of percentage of stenosis �70. All variablesdemonstrated significant discriminating capacity. The assumedPSV, EDV, and ICA/CCA values from the areas under the ROCcurve are respectively: for PSV and stenosis �30%�0.94; 30%to 50% stenosis�0.96; 50% to 70% stenosis�0.98; �70%stenosis�0.99 and for EDV and ICA/CCA �70% stenosis thevalues are respectively 0.98 and 0.99.

We therefore created a function intended to determine thePSV trend in relation to the percentage of stenosis atangiography. Because the population study is unbalanced,with 88.3% of the observations for patients with intrastentstenosis �50%, we separated the observations into 2 groups.The first group contains the observations with a percentage ofstenosis less than 50%. The second group contains theobservations with a percentage of stenosis greater than orequal to 50%. The correlation between percentage of stenosisand PSV in the first group corresponds to a value of R of 0.37

(P�0.0001) and in the second group to a value of R of 0.87(P�0.0001).

The sample statistics for the first and the second grouphave, respectively, a mean percentage of stenosis of 7.29�7.7with a mean PSV of 69.41�22.9 and 67.76�9.96 with amean PSV of 286.90�78.71. There are 2 equations, one foreach group, representing the model that compares PSV to thepercentage of stenosis at angiography. The R values for themodels are 0.37 and 0.91, respectively. Both models displaythe quadratic form of the percentage of stenosis (S): log(PSV)��S��S2, and the regression is represented in Figure3. In the first model both � and � have the same probabilityvalue (�0.0001), whereas in the second model � has aprobability value �0.0001 and � has a probabilityvalue�0.02.

DiscussionCAS induces permanent alterations of the physiological flowbehavior. In particular, the compliance mismatch between thenative carotid artery and the stented segment,23 the positivearterial remodelling (stent expansion),24,25 and the enhancedstiffness of the stent-arterial wall complex16 can inducealterations in compliance and in carotid hemodynamics andmodifications of Peterson’s elastic modulus of the stentedvessel.16 Moreover, changes in wall shear stress can bringendothelial dysfunction ultimately leading to intimal hyper-plasia and restenosis26–28 (negative arterial remodelling).25

These alterations lead to an increase in velocity and empha-size the need to develop customized velocity criteria for usein the follow-up of patients who have undergone CAS.16–21

Many authors reported Doppler-US criteria developed fornonstented arteries could not be utilized for stented arter-ies,14,15 many studies have reported altered blood flow veloc-ity after CAS, and some investigators disagree about thereliability of US examination after CAS.14,15

The literature is not conclusive about CAS follow-up.13,16–21 Different velocity thresholds for a particular degreeof ISR can be found, as shown in Table 3.

To our knowledge, this is the largest study—in terms ofpopulation study and time of follow-up—of the correlation ofUS velocity criteria to percentage of stenosis at angiographyin patients who have undergone CAS.

Creating a baseline value is important to reduce the numberof false restenoses, because the values of velocity tend to bemuch higher in stented artery than in native carotid. Imme-diate poststenting US examination provides a valuable base-line value for future follow-up comparisons.16 ISR continuesto be the “Achilles heel” of catheter surgery, and theincidence of ISR of CAS is variable in different reports from1% to 50%.17,29–33 In our study the incidence of ISR (�70%)was 2.7%. Recurrent stenosis in the course of artery healingafter endovascular treatment is considered the biologicalover-response to vascular injury secondary to endovascularsurgery.25

Our data indicate that PSV, EDV, and ICA/CCA increasewith stenosis to a greater extent in stented carotid arteries thanin native arteries and confirmed the strong correlationsbetween angiographic measurement and PSV, EDV, andICA/CCA. Measuring PSV is the most important component

Table 2. Potential Thresholds in Predicting Different Degree ofPercentage Stenosis at Angiography for Diverse VelocityCriteria

% Stenosis PSV(cm/s) EDV(cm/s) ICA/CCA

�30 �104 � � � � � �

30 to 50 105–174 � � � � � �

50 to 70 175�299 � � � � � �

�70 �300 �140 �3.8

PSV indicates peak systolic velocity; EDV, end diastolic velocity; ICA/CCA,ratio between PSV of internal carotid artery and common carotid artery.




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BFigure 3. Correlation of PSV and NASCET angiographic measurements in stented carotid arteries. Percentage of stenosis at angiogra-phy: % of stenosis (S): log (PSV)��S��S2. A, Observations with a percentage of stenosis less than 50%. R�0.37 (P�0.0001). B,Observations with a percentage of stenosis greater than or equal to 50%. R�0.87 (P�0.0001). PSV indicates peak systolic velocity;SD, standard deviation.




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of the carotid Doppler examination.34 As a function of thearea of the residual lumen, PSV increases with the narrowingof a stented artery, implying its usefulness for grading carotidintrastent stenosis,34 although factors such as ICA/CCA andEDV provide additional valuable information for quantifyingthe stenosis34–39 but with less accuracy of PSV. However,both ultrasound (screening test) and angiography (gold stan-dard) are operator and machine dependent, with considerablevariability in the equipment used and the criteria for inter-pretation.38,40–42 It is also erroneous to apply the same rigidvelocity cut-off to different ultrasound machines, because thefrequencies and geometry of the beams vary widely.38 As aresult, velocity recorded in one laboratory may differ signif-icantly from that recorded in another laboratory.43

Therefore, it is now widely accepted that individual labo-ratories validate the customized velocity criteria instead ofadopting reported criteria from other laboratories.38

Because grading carotid intrastent stenosis is an essentialpart of determining the risk of stroke, its accuracy should beassessed regularly with a prospective registry of ultrasoundand other correlative methods, usually angiography. Rigoroustraining at an established laboratory followed by an on-siteprospective comparison of ultrasound findings with angiog-raphy is always necessary.

In our laboratory we have found values of PSV �300 cm/s,EDV �140 cm/s, and ICA/CCA �3.8 as criteria for stenosis�70%. The specificity and sensitivity obtained by combiningthese parameters together are high (99% and 98%, respec-tively). When defining an ISR the velocity cut-off has to beset higher in the screening test: this increases specificity at thecost of sensitivity.

The mathematical function that we constructed (log(PSV)��S��S2, where (S) is the % of stenosis) is only

intended to highlight the upward tendency of the curvebetween the percentage of stenosis at angiography and log(PSV) values. For each increment in the percentage ofstenosis there is a corresponding exponential increase in PSV,and this is described well by a curve with a quadraticfunction, where there are significant coefficients (� and �).

A weakness of our study is the small number of patientswith ISR �50%: 95 (11.7%) patients out of the total numberof 814 patients.

SummaryThe compliance and the flow characteristics of a stentedcarotid artery are extremely different when compared to anative artery. Ultrasound grading of carotid intrastent stenosisneeds customized validated criteria because the standardvelocity criteria used for nonstented carotid arteries areinappropriate. The new thresholds of velocity criteria fordifferent degrees of ISR have to be increased. In our experi-ence we found the discriminator value of PSV �300 cm/s,EDV �140 cm/s, and ICA/CCA �3.8 as able to individuatea ISR �70%. A greater sensitivity and specificity of ultra-sound screening can be achieved by applying diagnosticcriteria specific to each validated laboratory. Our studyconfirms the high accuracy of PSV as an index of ISR andemphasizes the need for regular US examinations and clinicalfollow-up of patients after CAS to monitor long-termcomplications.

DisclosuresNone.

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Table 3. Literature Review of Velocity Criteria at Ultrasoundfor Intrastent Restenosis After CAS

Authors Pts ISR % PSV EDV ICA/CCA

Robbin 199714 170 �60 � � � � � � � � �

Ringer 200215 112 � � � � � � � � � � � �

The only reliable indication of restenosis found byUS examination was the net change in PSV and

ICA/CCA.

Lal 200416 90 �20 �150 cm/s � � � �2, 16

Levy 200517 142 �60 �200 cm/s � � � �2, 2

�70 �250 cm/s � � � �2, 8

Peterson 200518 158 �70 �170 cm/s �120 cm/s � � �

�50% increase in PSV-EDV over immediatepostoperative values.

Stanziale 200519 118 �50 �225 cm/s � � � �2, 5

�70 �350 cm/s � � � �4, 75

Chi 200720 260 �50 �240 cm/s � � � �2, 45

�70 �450 cm/s � � � �4, 3

Chahwan 200721 71 �50 �125 cm/s � � � � � �

�70 �300 cm/s 100–139 cm/s � � �

PSV indicates peak systolic velocity; EDV, end diastolic velocity; ICA/CCA,ratio between PSV of internal carotid artery and common carotid artery; US,ultrasounds.




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DonatoCarlo Setacci, Emiliano Chisci, Francesco Setacci, Francesca Iacoponi and Gianmarco de

Grading Carotid Intrastent Restenosis: A 6-Year Follow-Up Study

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