effect of carotid artery stenting on ophthalmic artery flow patterns

Seediscussions,stats,andauthorprofilesforthispublicationat:https://www.researchgate.net/publication/261034457

EffectofCarotidArteryStentingonOphthalmicArteryFlowPatterns

ARTICLEinJOURNALOFULTRASOUNDINMEDICINE:OFFICIALJOURNALOFTHEAMERICANINSTITUTEOFULTRASOUNDINMEDICINE·APRIL2014

ImpactFactor:1.54·DOI:10.7863/ultra.33.4.629·Source:PubMed

READS

21

6AUTHORS,INCLUDING:

NamıkKemalAltınbaşAnkaraUniversity

10PUBLICATIONS3CITATIONS

SEEPROFILE

EvrenUstuner

AnkaraUniversity


SEEPROFILE

SadikBilgic


SEEPROFILE

EbruDüşünceliAnkaraUniversity


SEEPROFILE

Availablefrom:NamıkKemalAltınbaşRetrievedon:09February2016

https://www.researchgate.net/publication/261034457_Effect_of_Carotid_Artery_Stenting_on_Ophthalmic_Artery_Flow_Patterns?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_2

https://www.researchgate.net/publication/261034457_Effect_of_Carotid_Artery_Stenting_on_Ophthalmic_Artery_Flow_Patterns?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_3

https://www.researchgate.net/?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_1

https://www.researchgate.net/profile/Namik_Altinbas?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_4


https://www.researchgate.net/institution/Ankara_University?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_6


https://www.researchgate.net/profile/Evren_Ustuner?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_4




https://www.researchgate.net/profile/Sadik_Bilgic?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_4



https://www.researchgate.net/profile/Ebru_Duesuenceli?enrichId=rgreq-ad458b15-1336-41e4-af76-d598954fbc65&enrichSource=Y292ZXJQYWdlOzI2MTAzNDQ1NztBUzoxOTE2NDczNzM0MjI1OTJAMTQyMjcwMzcwMjU1MA%3D%3D&el=1_x_4




Effect of Carotid Artery Stenting onOphthalmic Artery Flow Patterns

arotid artery stenosis is a major cause of cerebrovasculardisease and causes devastating impacts on health.1–4

Recently, in addition to medication and surgery, endovasculartechniques (angioplasty and stenting) have been introduced for treat-ment of carotid artery stenosis with success.2,3 Endovascular proce-dures are gaining wide popularity as alternatives and have similaroutcomes and periprocedural risks compared to endarterectomy.1–5

Carotid imaging using color Doppler sonography or angiographyis highly accurate in revealing carotid artery stenosis of 70% orgreater.6–9 Examination of the ophthalmic artery with Dopplersonography also provides valuable information about blood flow

Namik K. Altinbas, MD, Evren Ustuner, MD, Hasan Ozcan, MD, Sadik Bilgic, MD, Tanzer Sancak, MD,Ebru Dusunceli, MD

Received May 13, 2013, from the Department ofRadiology, Ankara University School of Medicine,Ankara, Turkey (N.K.A., E.U., H.O., S.B., E.D.);and Radiology Unit, Private Tobb-Etu Hospital,Ankara, Turkey (T.S.). Revision requested June 4,2013. Revised manuscript accepted for publicationAugust 5, 2013.

This study was presented as a oral presenta-tion at the Eighth Interventional RadiologyAnnual Meeting; March 28–31, 2013; Antalya,Turkey.

Address correspondence to Namik K.Altinbas, MD, Department of Radiology, AnkaraUniversity School of Medicine, Ibn-i Sina Hospital,06230 Ankara, Turkey.

E-mail: [email protected]

AbbreviationsEDV, end-diastolic velocity; PI, pulsatilityindex; PSV, peak systolic velocity; RI, resis-tive index

C

©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:629–638 | 0278-4297 | www.aium.org

ORIGINAL RESEARCH

Objectives—The purpose of this study was to assess the effect of carotid artery stentingon ophthalmic artery blood flow using transorbital color and spectral Doppler sonog-raphy and review the changes in relation to cerebral hemodynamics.

Methods—Twenty-eight consecutive patients with severe internal carotid artery steno-sis (≥70%) who were scheduled for carotid stenting were included. Ophthalmic arteryDoppler sonography was performed bilaterally before and after stenting. The flow direc-tion, peak systolic velocity (PSV), end-diastolic velocity (EDV), pulsatility index (PI),and resistive index in the ophthalmic artery were recorded.

Results—Twenty male and 8 female patients with 10 right-sided and 18 left-sidedstenoses were studied. The mean overall carotid stenosis ratio ± SD was 87.3% ± 9.9%.After stenting in the ophthalmic artery ipsilateral to the stenosis, significant increases inthe PSV (–3.87 ± 48.81 to 46.70 ± 25.33 cm/s; P < .001), and EDV (–3.02 ± 16.31 to11.24 ± 7.37 cm/s; P < .001) were detected, and the increase in the PI approached sig-nificance (1.40 ± 0.59 to 1.62 ± 0.52; P = .055). A change in the flow direction fromretrograde to antegrade was noted in 11 patients (39%) after stenting, and in 1 patientwith no detectable flow, reconstitution of flow was observed. Increases in the PSV andEDV (P = .03 for ΔEDV) were more pronounced in symptomatic patients than asymp-tomatic patients after stenting.

Conclusions—Substantially decreased ophthalmic artery velocity and retrograde floware suggestive of high-grade carotid artery stenosis (≳90%). Stenting improves oph-thalmic artery perfusion and positively changes cerebral hemodynamics in high-gradecarotid artery stenosis, especially in symptomatic patients, which can be monitored withophthalmic artery Doppler sonography.

Key Words—carotid artery stenosis; color and spectral Doppler sonography; endovas-cular treatment; ophthalmic artery; ophthalmologic ultrasound; stenting; stroke

Article includes CME test

doi:10.7863/ultra.33.4.629

3304jum557-712online_Layout 1 3/19/14 11:30 AM Page 629

patterns and hemodynamics of cerebral perfusion.10–17

The ophthalmic artery provides many advantages in thisregard, being a downstream intracerebral branch of theinternal carotid artery and also being easily accessible byDoppler sonography.

In this study, our aim was to investigate the immediateeffects of carotid artery stenting on ophthalmic artery flowpatterns in patients with internal carotid artery stenosis of70% or greater. In this way, we could indirectly observe intrac-erebral hemodynamic changes after stenting. In addition,using this information, we can obtain definite, quantitative,and measurable information about the effects of stentingon the ophthalmic artery, which may help us follow andplan endovascular treatments.

Materials and Methods

Patient Selection A total of 28 consecutive patients who had been referred tothe interventional radiology department for a carotid arterystenting procedure between June 2007 and August 2009were included in the study. All patients were confirmed tohave carotid artery stenosis of 70% or greater by selectivecontrast angiography at the time of stenting, and all werethoroughly examined and referred for a stenting procedure byneurologists before admission to the radiology department.Indications for stenting were made according to the guide-lines and evidence provided by the North American Symp-tomatic Carotid Endarterectomy Trial,18 the EuropeanCarotid Surgery Trial,19 and the Asymptomatic CarotidAtherosclerosis Study,20 which suggest that symptomaticpatients and asymptomatic patients benefit from theprocedure if they have severe stenosis (≥70%) and if theircomplication rates are less than 6% for symptomatic and3% for asymptomatic patients.18–21

As part of their treatment plan, all patients gaveinformed written consent before diagnostic angiographicand endovascular treatment (angioplasty and stenting)procedures. The patients also gave informed written con-sent for ophthalmic artery Doppler sonography before andafter the procedure. All of the procedures in this study weredone in accordance with the Declaration of Helsinki forhuman subjects, and the study was approved by our Insti-tutional Review Board.

Angiographic Evaluation and StentingDiagnostic cerebral angiography was performed in allpatients before the stenting procedure to assess theintracranial and extracranial cerebral circulation. Stenosisratios were calculated in accordance with the guidelines

provided by the North American Symptomatic CarotidEndarterectomy Trial.18 The stenting procedure wasperformed according to the guidelines and techniquesdescribed by Moran et al.22 After definite localization ofthe stenosis, self-expandable stents (Wallstent; BostonScientific, Galway, Ireland) were deployed using a pro-tective umbrella device (Emboshield; Abbott Ireland,Galway, Ireland). At the end of the procedure, the carotidartery and intracranial circulation was reevaluated for dis-section, vasospasm, and patency using anteroposteriorand lateral views.

Color and Spectral Doppler Sonographic ExaminationsDoppler sonography of the ophthalmic artery was per-formed in accordance with the standard technique describedby Belden et al.23 Doppler sonographic examinations ofthe ophthalmic artery were done on the same day beforestenting and 1 to 3 days after the procedure, when thepatients became ambulatory and hemodynamically stable,using Aplio SSA-770A/80 Doppler equipment (ToshibaMedical Systems Co, Ltd, Tokyo, Japan) with a 7.5-MHzmultifrequency linear transducer. The carotid artery andtransorbital ophthalmic artery were evaluated bilaterallyby Doppler sonography. To standardize Doppler sono-graphic measurements, all studies were performed bilaterallyby the same radiologist. First, carotid arteries were examinedon both sides for lumen and stent patency. Next, Dopplersonography of both ophthalmic arteries was done.The ophthalmic artery peak systolic velocity (PSV), end-diastolic velocity (EDV), pulsatility index (PI), and resistiveindex (RI) were all recorded. Care was taken not to applypressure on the globe during measurements by using thecorrect angles and sample width. During the spectral analy-sis mode, the spatial-peak temporal-average intensity wasalways kept below the threshold of 17 mW/cm2, as rec-ommended by the US Food and Drug Administration.16

The ages, sexes, medical histories (hypertension, diabetesmellitus, and atherosclerotic heart disease), and neurologicexamination findings of the patients were recorded as well(Table 1).

Statistical AnalysisNormal distribution of the variables was assessed by theShapiro-Wilk test. Comparisons of pre- and post-stentophthalmic artery velocity variables were evaluated by theWilcoxon signed ranks test. The Mann-Whitney U test wasused to test the difference between two groups. Nominalvariables were tested by the Fisher exact test. The degree ofassociation between the stenosis ratio and differencesbetween pre- and post-stent ophthalmic artery velocity

Altinbas et al—Effect of Carotid Artery Stenting on Ophthalmic Artery Flow Patterns

J Ultrasound Med 2014; 33:629–638630


variables were assessed by the Spearman ρ coefficient.P < .05 was considered significant. SPSS version 15.0 soft-ware for Windows (IBM Corporation, Armonk, NY) wasused for statistical evaluations.

Results

The carotid stenting procedure was performed in 20 maleand 8 female patients. Stents were placed on the right sidein 10 patients and on the left side in 18. None of the patientsreceived bilateral stents during the same procedure orunderwent a later contralateral stent placement procedure.The mean age of the study group ± SD was 71 ± 7.9 years(range, 53–87 years). The total mean stenosis ratio was87.3% ± 9.9% (range, 70%–98%). Stenosis was signifi-cantly higher on the left side (P < .05).

Results of the spectral Doppler sonographic examina-tions of the ophthalmic artery before and after stenting arepresented in Table 2. The PSV in the ophthalmic arteryipsilateral to the stenosis before stenting was –3.87 ± 48.81cm/s and increased significantly to 46.70 ± 25.33 cm/safter stenting (P < .001). To sum up, statistically significantincreases in ophthalmic artery flow values on the stentedside (PSV, EDV, and PI) were noted after the stenting pro-cedure (Table 2). A mild to moderate relationship wasnoted between the changes from the pre- to post-stent PSVand EDV compared to the stenosis ratio (ΔPSV, r = 0.4731;P = .018; ΔEDV, r = 0.0473; P = .001). Scattergrams showthe pre- and post-stent changes in ophthalmic artery veloc-ities in relation to the stenosis ratio (Figures 1–3).

In 11 patients (39%), retrograde flow was noted in theophthalmic artery before the procedure. After stenting,spectral analysis showed that the flow direction changed

J Ultrasound Med 2014; 33:629–638 631


Table 1. Patient Demographics

ICA Stenosis, %

Patient Age, y Sex Right Left Stented Side Symptom Status Comorbidities

1 75 Male 80 30 Right Mild right MCA infarct HL, dementia

2 87 Male 85 86 Right Asymptomatic None

3 85 Female 71 0 Right Asymptomatic None

4 63 Female 92 100 Right Right upper extremity paresis HL, HT

5 62 Male 70 100 Right Left amaurosis fugax None

6 67 Female 98 70 Right Right amaurosis fugax, TIA DM, HL, HT

7 74 Male 74 100 Right TIA None



10 75 Male 96 0 Right Left hemiparesis None

11 66 Female 100 70 Left Asymptomatic None

12 58 Male 40 92 Left TIA, syncope, confusion TX

13 64 Male 60 92 Left TIA HL, COPD, CVD

14 71 Male 60 80 Left TIA HL, HT, CVD

15 69 Male 63 96 Left Right lower extremity paresis,

left lacunar infarcts TX, HL, HT, CAD

16 65 Male 40 95 Left Asymptomatic None

17 63 Male 78 87 Left TIA None

18 76 Male 50 98 Left Right arm hemiparesis None

19 80 Female 30 95 Left TIA, right hemiparesis DM, HT

20 53 Male 70 95 Left Right upper extremity paresis,

left amaurosis fugax None

21 73 Male 33 70 Left Small left MCA infarct HT

22 77 Male 50 90 Left Right hemiparesis None



25 65 Female 30 92 Left TIA None


27 75 Female 50 98 Left Motor aphasia, small left MCA infarct HL

28 76 Female 100 92 Left Left hemianopsia,

right upper extremity paresis None

CAD indicates coronary artery disease; COPD, chronic obstructive pulmonary disease; CVD, cardiovascular disease; DM, diabetes mellitus; HL,

hyperlipidemia; HT, hypertension; ICA, internal carotid artery; MCA, middle cerebral artery; TIA, transient ischemic attack; and TX, thyrotoxicosis.



J Ultrasound Med 2014; 33:629–638632

Table 2. Pre- and Post-Stent Ophthalmic Artery PSV, EDV, RI, and PI Values

Parameter Pre-Stent Post-Stent P

PSV, cm/s –3.87 ± 48.81 46.70 ± 25.33 <.001

10.75 (–112.8 to 62.7) 44.95 (–16.6 to 95.5)

EDV, cm/s –3.02 ± 16.31 11.24 ± 7.37 <.001

1.95 (–49.3 to 20.3) 9.8 (–3.4 to 28.5)

RI 0.71 ± 0.18 0.77 ± 0.09 .093

0.74 (0 to 0.98) 0.78 (0.59 to 0.9)

PI 1.40 ± 0.59 1.62 ± 0.52 .055

1.45 (0 to 2.62) 1.63 (0 to 2.35)

Data are presented as mean ± SD and median (range).

Figure 1. Scattergrams of pre- and post-stent ophthalmic artery PSV (A) and EDV (B). Open blue circles indicate asymptomatic patients with con-

tralateral internal carotid artery stenosis of less than 70%; open red diamonds, symptomatic patients with contralateral internal carotid artery stenosis

of less than 70%; solid blue circles, asymptomatic patients with occlusion of the contralateral internal carotid artery; solid red diamonds, symptomatic

patients with occlusion of the contralateral internal carotid artery; solid blue squares, asymptomatic patients with contralateral stenosis of 70% or

greater; and solid red squares, symptomatic patients with contralateral stenosis of 70% or greater.

A B

Figure 2. Scattergram of ophthalmic artery ΔPSV (post-stent PSV –

pre-stent PSV) versus stenosis ratio. Symbols are as in Figure 1.

Figure 3. Scattergram of ophthalmic artery ΔEDV (post-stent EDV –

pre-stent EDV) versus stenosis ratio. Symbols are as in Figure 1.


to the positive side of the spectrum and was antegrade in allcases (Figure 4). In 1 patient, no detectable ophthalmicartery flow was noted on the stenotic side, but after the pro-cedure, vivid antegrade ophthalmic artery flow with a highPSV was detected in the spectral analysis (Figure 5).

The circle of Willis was complete in all patients, but 6patients had total occlusion, and 4 had stenosis of 70% orgreater in the contralateral internal carotid artery beforestenting. A decrease or absence of flow in the contralateralinternal carotid artery did not correlate with the presenceof negative ophthalmic artery PSV flow before stenting orchanges in ophthalmic artery velocities after stenting.

Before the procedure, 9 patients were asymptomaticand 19 were symptomatic. Being symptomatic did notcorrelate with negative pre-stent ophthalmic artery PSV flow,but symptomatic patients showed much greater increasesin the ophthalmic artery PSV and EDV compared to asymp-tomatic patients after stenting. This change was statisticallysignificant for the EDV (ΔPSV, 30.40 ± 45.92 cm/s inasymptomatic patients and 60.12 ± 57.32 cm/s in symp-tomatic patients; P = .06; ΔEDV, 7.82 ± 14.12 cm/s inasymptomatic patients and 17.31 ± 18.82 cm/s in sympto-matic patients; P = .03). A scattergram shows the changesin ophthalmic artery velocities in relation to the symptomstatus (Figure 6).

J Ultrasound Med 2014; 33:629–638 633


Figure 4. A, Angiogram from a patient with right 79% internal carotid

artery stenosis. A patent stent with alleviation of the stenosis was

observed after the stenting procedure. B, Before stenting, retrograde

flow was present in the ipsilateral ophthalmic artery (PSV, –29.5 cm/s at

end systole; EDV, –0.7 cm/s; the spectral display was reversed by the

operator). C, After stenting, the flow reversed to antegrade (PSV, 39.3

cm/s at end systole; EDV, 8 cm/s).

A

B C

3304jum557-712online_Layout 1 3/19/14 11:30 AM 33


J Ultrasound Med 2014; 33:629–638634

A relationship was also noted regarding stenosis andsymptoms. In symptomatic patients, when stenosis ratioswere greater than 85%, significant increases in the PSV(>25 cm/s) and EDV (>15 cm/s) were noted compared toasymptomatic patients (P = .0108 and .006, respectively).Comorbidities such as hypertension, diabetes, hyperlipi-demia, and thyrotoxicosis were detected in 10 patients.Having comorbidities did not correlate with the changesin ophthalmic artery velocities or having negative pre-stentophthalmic artery flow.

Discussion

The ophthalmic artery is an intracranial artery with uniqueproperties. It can reflect hemodynamic changes related tocerebrovascular disease at the intracranial level. The acousticbarrier formed by bone imposes a great problem duringexaminations of intracranial vessels by Doppler sonography.However, such a barrier does not exist for the ophthalmicartery when a transorbital approach is used. The study canbe performed in an easy and reliable manner with linear

Figure 5. Images from a patient with 96% stenosis in the left internal carotid artery. A, No notable flow was in the left ophthalmic artery before stent-

ing. B, After stenting, an antegrade normal flow pattern with a high PSV (71.9 cm/s at end systole) was detected in the left ophthalmic artery. C and

D, Left internal carotid artery stent patency was confirmed on grayscale (C) and on color Doppler (D) sonography after the stenting procedure.

A B

C D


7.5-MHz probes that are also used in standard Dopplersonographic examinations of the carotid artery. The imagercan have a direct view of the ophthalmic artery and thus canexamine a major vessel of the intracranial circulation. A decrease in the velocity and pulsatility of the incomingflow is indirect proof of severe upstream stenosis. The oph-thalmic artery is located downstream of the internal carotidartery. The inflow artery for the ophthalmic artery is theinternal carotid artery, and the ophthalmic artery can reflectchanges in the petrous and cavernous portions of the inter-nal carotid artery.16,17

The responses to cerebral ischemia and compensationmechanisms show differences among individuals. Studieshave shown that in high-grade stenosis, collateral pathwaysand circle of Willis collaterals come into play. If circle ofWillis collaterals decompensate, alternative mechanisms willbecome manifest.10–12,24 Absence of collaterals or reversal ofnormal antegrade flow in the ophthalmic artery is a gravefinding suggestive of decompensation from the contralat-eral internal carotid artery (mainly via the anterior com-municating artery).1,3,10,12,14,17 In such a situation, theophthalmic artery is often filled by collaterals from the ipsi-lateral external carotid artery but not from the Circle ofWillis.10,12,24 The direction of blood flow in the ophthalmicartery is maintained by blood pressure differences betweenthe ipsilateral internal carotid artery and external carotidartery.10 Patients with inadequate collaterals have beenreported to benefit most from carotid endarterectomyprocedures.1

In a study by Fujioka et al,10 6 different ophthalmicartery flow patterns in carotid artery stenosis were described,depending on the collateral flow, grade of stenosis, andblood pressure. Retrograde flow in the ophthalmic arterywas correlated with high-grade stenosis and ipsilateralexternal carotid artery collateralization of the ophthalmicartery with absence of a Circle of Willis contribution.The same abnormal flow patterns were also observed in ourstudy. We detected retrograde flow, absence of flow, andchanges in the shapes of systolic and diastolic peaks in cor-relation with a decrease in the flow velocity and resistance.

In a study by Schneider et al,17 transorbital and tran-scranial color Doppler sonographic findings for 25 internalcarotid artery occlusions and 10 normal internal carotidarteries were examined. In cases with retrograde ophthalmicartery flow, a decrease in the middle cerebral artery flowvelocity was noted, which was presumed to be related toinadequate intracranial collateral flow. The ophthalmicartery PSV (38 ± 10.2 cm/s) and PI in internal carotidartery occlusions decreased on the occluded side com-pared to the nonoccluded side and the control group.17

Another study by Fujioka13 suggested that a decrease inthe PSV of less than 10 cm/s and the presence of retro-grade flow (<0 cm/s) in the ophthalmic artery were find-ings suggestive of high-grade or occlusive carotid arterystenosis, and they referred such patients for carotid exam-inations with a prediagnosis of severe stenosis. Such anobservation was also made in a study by Hu et al,16 whoobserved that in severe high-grade carotid artery stenosis(≥75%) and occlusion, the ophthalmic artery PSV was29 cm/s or lower in addition to flow reversal (89.6% sensi-tivity and 81.7% specificity).16 In a randomized study byPaivansalo et al,15 in 94 patients with carotid artery stenosis,the ophthalmic artery velocity was correlated with internalcarotid artery stenosis; a significant decrease in the oph-thalmic artery flow velocity occurred only in the presenceof high-grade stenosis (≥80%). Retrograde ophthalmicartery flow was detected in 92% of patients with internalcarotid artery occlusion and in 47% of patients with stenosisof greater than 90%.15 In a study by Kawaguchi et al,25

carotid artery stenting was reported to be effective inimproving the ocular circulation and chronic ocular ischemicsyndrome caused by severe carotid artery stenosis. All ofthe above studies were in accordance with our study.

In a similar study by Cohn et al,26 conducted on 25patients who underwent carotid endarterectomy, reducedophthalmic artery flow was found to be significantlyincreased after the surgery on ophthalmic artery Dopplersonography and to be correlated with severe stenosis, and8 patients who had retrograde flow before the procedure

J Ultrasound Med 2014; 33:629–638 635


Figure 6. Scattergram of ophthalmic artery ΔEDV and ΔPSV. Symbols

are as in Figure 1.


had a return to normal antegrade flow after treatment. Asin our study, low preoperative ophthalmic artery flow didnot correlate with the ocular symptomatic status. The meanpreoperative ophthalmic artery PSV in their study was21.6 cm/s, compared to –3.81 cm/s in our study, whichwas much lower; however, the post-stent ophthalmicartery PSV was 38.6 cm/s, which was similar to 46.7 cm/s inour study. As in their 8 patients, in 11 of our patients, retro-grade flow was detected before stenting and returned toantegrade after stenting.26 In our study, stenosis of greaterthan 90% was present in 16 patients, 9 (56%) of whom hadretrograde flow in the ophthalmic artery. Also, in 1 patient,complete stent occlusion was detected 1 month later, andretrograde ophthalmic artery flow again reappeared on thesame side of stent occlusion. In another patient with nodetectable ophthalmic artery flow, the return of a normalophthalmic artery flow pattern with a high PSV wasobserved after stenting. Thus, retrograde flow, no detectableflow, or a substantial decrease in ophthalmic artery flow toless than 10 cm/s can be interpreted as an indicator of high-grade (≥87% to ≈90%) carotid artery stenosis.

In a study by Zbornikova and Skoglung,14 hemody-namic changes in the ophthalmic artery, carotid siphon,and intracranial arteries were studied with transcranialDoppler sonography after carotid endarterectomy. In accor-dance with our findings, they detected reversal of all retro-grade systolic flow to antegrade after carotid endarterectomyand a significant increase in the ophthalmic artery PSV onthe operated sides. They concluded that transcranial Dopplerstudies provide important and early information aboutinternal carotid artery patency and hemodynamic changesafter carotid endarterectomy.14 We found that the samechanges observed after carotid endarterectomy applied tocarotid angioplasty and stenting procedures.

Identification of patients who have a higher risk ofstroke and consequently would benefit more from revas-cularization procedures is an important topic. Therefore,attention is focused on detecting patients with cranialhypoperfusion. Evidence suggests that carotid bruit (end-systolic turbulence in the carotid spectral waveform),27

ophthalmic artery hypotension on ocular pneumoplethys-mography,28,29 an ophthalmic pulse delay on ocular pneu-moplethysmography,30 and decreased middle cerebral arterysystolic velocities14 are such indicators. Ophthalmicartery flow, which appears to be influenced by the ipsilat-eral grade of internal carotid artery stenosis and symptomstatus, may prove to be such an indicator as well.

As far as symptoms are concerned, the risk of stroke isreported to increase in some subgroups of patients withcritical stenosis (≥70%), such as those who have monocular

blindness, are older than 75 years, are male, are sympto-matic with a transient ischemic attack or stroke history, andhave stenosis of greater than 90% to 94% and no collaterals.31

Our ophthalmic artery flow findings related to symptomaticpatients and patients who had higher-grade stenosis (>90%)seem to support this evidence. An interesting relationshipthat emerged from our study was that symptomatic patientswith high-grade stenosis (≥85%) had a marked ophthalmicartery flow increase after stenting compared to asympto-matic patients.

In all of our patients, Circle of Willis arteries were com-plete, but in 6 patients, complete occlusion of the contralat-eral internal carotid artery was present, and in 4 patients,severe stenosis of 70% or greater in the contralateral internalcarotid artery was present. Statistical analysis showed thatthe ophthalmic artery flow changes after stenting were notstatistically different in this group of patients compared topatients with a patent contralateral internal carotid artery.In the study by Gee et al,28 which studied pre- and post-ocular blood flow in 701 carotid endarterectomy casesusing ocular pneumoplethysmography, 27% and 47%improvements on the side of the repaired carotid artery weredetected when there was severe stenosis (>70%) and totalocclusion of the contralateral carotid artery, respectively. Thisincrease was only 16% when the contralateral side wasfunctionally patent.28 Although a similar increase waspresent in our study, it was not statistically significant,perhaps because our study group was small or somehowwell compensated due to having patent Circle of Willisarteries, or because ophthalmic artery flow is subject toautoregulation, whereas ocular blood flow is not. In ourstudy, ophthalmic artery flow appeared to be driven moreby the ipsilateral internal carotid artery stenosis rather thanthe contralateral internal carotid artery. Having comor-bidities did not influence ophthalmic artery flow changes.

Both angiography and color Doppler sonographyhave high accuracy for detection of stenosis of greater than70% and follow-up after intervention. Color Dopplersonography is widely used to assess stent patency after theprocedure.6–9 Ophthalmic artery Doppler sonography canbe effectively incorporated into the routine carotid arterysonographic protocol and may prove useful in decisionmaking when unequivocal carotid artery stenosis cases areencountered.

There is always a possibility of stenosis beyond theextracranial segment of the carotid artery, which may affectthe success of the stenting procedure. Such stenosis mayinterfere with ophthalmic artery flow patterns after stentingas well. The ophthalmic artery PSV was noted to decreasein response to siphon stenosis and a tortuous common


J Ultrasound Med 2014; 33:629–638636


carotid artery.24 Intracranial atherosclerotic disease maybe present in 20% to 50% of patients with extracranialcarotid artery stenosis.9,32 Fortunately, endarterectomystudies have shown that the presence of such substantialintracranial stenosis greater than 50% is quite low and doesnot affect surgical success, the prognosis, or stroke ratiosafter endarterectomy.32 The prognosis is much better inintracranial vascular stenosis than internal carotid arterystenosis and does not change the mortality and morbidityratios. Also, the degree of calcification in the carotid siphonis not used as a prognostic factor in cerebral stroke.32

Patients with mild to moderate intracranial atheroscleroticdisease and severe carotid artery stenosis are consideredideal candidates who can benefit the most from carotidendarterectomy.1 Such severe intracranial stenosis was notdetected in any of our patients, but in patients with noapparent extracranial carotid artery stenosis presentingwith findings suggestive of intracranial arterial occlusivedisease, substantially decreased ophthalmic artery flow orretrograde flow may prompt further investigation forintracranial atherosclerotic disease.

In conclusion, transorbital Doppler sonography canprovide information about early cerebral hemodynamicchanges after angioplasty and stent placement in carotidartery stenosis. Even indirect information about internalcarotid artery stent patency can be inferred. Simultaneoususe of ophthalmic artery Doppler sonography with carotidDoppler sonography during the same scan session can yieldmore diagnostic information. Retrograde flow or substan-tially decreased flow (<10 cm/s) in the ophthalmic artery issuggestive of high-grade (≈90%) ipsilateral carotid arterystenosis. In cases of high-grade stenosis (≳90%) and retro-grade ophthalmic artery flow and in symptomatic patients,the positive contribution of the carotid artery stenting pro-cedure to cerebral hemodynamics becomes more obvious.Therefore, intervention is justified. Critical deterioration ofcerebral perfusion and lateralization of disease can bededuced from the ophthalmic artery, which may help intimely institution of treatment and preventive measures.

References

1. Barnett HJ, Meldrum HE, Eliasziw M; North American SymptomaticCarotid Endarterectomy Trial (NASCET) collaborators. The appropri-ate use of carotid endarterectomy. CMAJ 2002; 166:1169–1179.

2. Gomez CR. Carotid angioplasty and stenting: new horizons. Curr AtherosclerRep 2000; 2:151–159.

3. Jordan WD Jr, Schroeder PT, Fisher WS, McDowell HA. A comparisonof angioplasty with stenting versus endarterectomy for the treatment ofcarotid artery stenosis. Ann Vasc Surg 1997; 11:2–8.

4. Chaturvedi S, Aggarwal R, Murugappan A. Result of carotid endarterec-tomy with prospective neurologist follow-up. Neurology 2000; 55:769–772.

5. Timaran C, Mantese VA, Malas M, et al; CREST Investigators.Differential outcomes of carotid stenting and endarterectomy performedexclusively by vascular surgeons in the Carotid RevascularizationEndarterectomy Versus Stenting Trial (CREST). J Vasc Surg 2013; 57:303–308.

6. Alexandrov AV, Brodie DS, McLean A, Hamilton P, Murphy J, Burns PN.Correlation of peak systolic velocity and angiographic measurement ofcarotid stenosis revisited. Stroke 1997; 28:339–342.

7. Erickson SJ, Mewissen MW, Foley WD, et al. Stenosis of the internalcarotid artery: assessment using color Doppler imaging compared withangiography. AJR Am J Roentgenol 1989; 152:1299–1305.

8. Koga M, Kimura K, Minematsu K, Yamaguchi T. Diagnosis of internalcarotid artery stenosis greater than 70% with power Doppler duplexsonography. AJNR Am J Neuroradiol 2001; 22:413–417.

9. Khaw KT. Does carotid duplex imaging render angiography redundantbefore carotid endarterectomy? Br J Radiol 1997; 70:235–238.

10. Fujioka S, Karashima K, Nakagawa H, Saito Y, Nishikawa N. Classifica-tion of ophthalmic artery flow in patients with occlusive carotid artery dis-ease. Jpn J Ophthalmol 2006; 50:224–228.

11. Kerty E, Nyberg-Hansen R, Dahl A, Bakke SJ, Russell D, Rootwelt K.Assessment of the ophthalmic artery as a collateral to the cerebral circu-lation: a comparison of transorbital Doppler ultrasonography and regionalcerebral blood flow measurements. Acta Neurol Scand 1996; 93:374–379.

12. Hu HH, Wang S, Chern CM, Yeh HH, Sheng WY, Lo YK. Clinical sig-nificance of the ophthalmic artery in carotid artery disease. Acta NeurolScand 1995; 92:242–246.

13. Fujioka S. Use of orbital color Doppler imaging for detecting internalcarotid artery stenosis in patients with amaurosis fugax. Jpn J Ophthalmol2003; 47:276–280.

14. Zbornikova V, Skoglund L. Early haemodynamic changes in the oph-thalmic artery, siphon and intracranial arteries after carotid endarterec-tomy estimated by transcranial Doppler and duplex scanning. Eur J VascEndovasc Surg 1998; 15:67–77.

15. Päivänsalo M, Riiheläinen K, Rissanen T, Suramo I, Laatikainen L. Effectof an internal carotid stenosis on orbital blood velocity. Acta Radiol 1999;40:270–275.

16. Hu HH, Sheng WY, Yen MY, Lai ST, Teng MM. Color Doppler imag-ing of orbital arteries for detection of carotid occlusive disease. Stroke 1993;24:1196–1203.

17. Schneider PA, Rossman ME, Bernstein EF, Ringelstein EB, Otis SM.Noninvasive assessment of cerebral collateral blood supply through theophthalmic artery. Stroke 1991; 22:31–36.

18. North American Symptomatic Carotid Endarterectomy Trial Collabo-rators. Beneficial effect of carotid endarterectomy in symptomatic patientswith high-grade carotid stenosis. N Engl J Med 1991; 325:445–453.

19. European Carotid Surgery Trialists’ Collaborative Group. MRC EuropeanCarotid Surgery Trial: interim results for symptomatic patients with severe(70–99%) or with mild (0–29%) carotid stenosis. Lancet 1991; 337:1235–1243.

J Ultrasound Med 2014; 33:629–638 637



20. Executive Committee for the Asymptomatic Carotid AtherosclerosisStudy. Endarterectomy for asymptomatic carotid stenosis. JAMA 1995;273:1421–1428.

21. Barnett HJ, Eliasziw M, Meldrum HE, Taylor DW. Do the facts and figureswarrant a 10-fold increase in the performance of carotid endarterectomyon asymptomatic patients? Neurology 1996; 46:603–608.

22. Moran CJ, Cross DT III, Derdeyn CP. Techniques of carotid angioplastyand stenting. Neuroimaging Clin N Am 2007; 17:337–353.

23. Belden CJ, Abbitt PL, Beadles KA. Color Doppler US of the orbit.Radiographics 1995; 15:589–608.

24. Drakou AA, Koutsiaris AG, Tachmitzi SV, Roussas N, Tsironi E,Giannoukas AD. The importance of ophthalmic artery hemodynamicsin patients with atheromatous carotid artery disease. Int Angiol 2011;30:547–554.

25. Kawaguchi S, Sakaki T, Iwahashi H, et al. Effect of carotid artery stentingon ocular circulation and chronic ocular ischemic syndrome. CerebrovascDis 2006; 22:402–408.

26. Cohn EJ, Sandager GP, Benjamin ME, Lilly MP, Hanna DJ, Flinn WR.Assessment of ocular perfusion after carotid endarterectomy with colorflow duplex scanning. J Vasc Surg 1999; 29:665–671.

27. Gutierrez IZ, Makula PA, Gage AA. The asymptomatic carotid bruit. AmSurg 1985; 51:388–391.

28. Gee W, Perline RK, Madden AE. Physiology of carotid endarterectomywith ocular pneumoplethysmography. J Vasc Surg 1986; 4:129–135.

29. Gee W, Lucke JF, Madden AE. Reappraisal of ocular pneumoplethys-mography after carotid endarterectomy. J Vasc Surg 1986; 4:517–521.

30. Kartchner MM, McRae LP. Carotid occlusive disease as a risk factor inmajor cardiovascular surgery. Arch Surg 1982; 117:1086–1088.

31. Benavente O, Eliasziw M, Streifler JY, Fox AJ, Barnett HJ, Meldrum H;North American Symptomatic Carotid Endarterectomy Trial Collabo-rators. Prognosis after transient monocular blindness associated withcarotid artery stenosis. N Engl J Med 2001; 345:1084–1090.

32. Taoka T, Iwasaki S, Nakagawa H, et al. Evaluation of arterioscleroticchanges in the intracranial carotid artery using the calcium score obtainedon plain cranial computed tomography scan: correlation with angio-graphic changes and clinical outcome. J Comput Assist Tomogr 2006;30:624–628.


J Ultrasound Med 2014; 33:629–638638


639


640


effect of carotid artery stenting on ophthalmic artery flow patterns

Documents