Download Effect of Internal Carotid Artery Stenting on Superior Thyroid Artery

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ORIGINAL RESEARCH
Effect of Internal Carotid Artery Stenting
on Superior Thyroid Artery Doppler Flow
Yasemin Gunduz, MD, Ramazan Akdemir, MD, Perihan Varim, MD, Lacin Tatli Ayhan, MD,
Mehmet Akif Cakar, MD, Mehmet Bulent Vatan, MD, Harun Kilic, MD
Objectives—Patients with carotid disease are frequently referred for carotid artery stenting based on the results of carotid duplex studies. During carotid artery stenting, the
stent is usually extended into the common carotid artery, thereby crossing the external
carotid artery. Previous studies have shown conflicting results regarding internal carotid
stenting and external carotid artery flow velocities, but the effect of stenting on ipsilateral superior thyroid artery velocities has not been defined. This study examined the
effect of internal carotid angioplasty and stenting on the ipsilateral superior thyroid
artery Doppler-derived flow parameters.
Methods—We prospectively studied preinterventional and postinterventional duplex
scans obtained from 41 patients (mean age ± SD, 64 ± 10 years) who underwent carotid
artery stenting. The Doppler-defined preprocedural peak systolic velocity (PSV) enddiastolic velocity (EDV), resistive index (RI), and pulsatility index (PI) in the ipsilateral
external carotid and superior thyroid arteries were compared with postprocedural
values.
Results—Among patients with stenting, the preprocedural PSV, EDV, RI, and PI in the
ipsilateral superior thyroid artery were 30 ± 11 cm/s, 13 ± 6 cm/s, 0.62 ± 0.11, and
1.04 ± 0.28, respectively; after stenting, they were 36 ± 8 cm/s, 14 ± 9 cm/s, 0.71 ± 0.07,
and 1.11 ± 0.19. The preprocedural PSV, EDV, RI, and PI in the ipsilateral external carotid
artery were 79 ± 24 cm/s, 17 ± 7 cm/s, 0.77 ± 0.26, and 1.27 ± 0.22; after stenting, they
were 94 ± 31 cm/s, 20 ± 6 cm/s, 0.80 ± 0.4, and 1.25 ± 0.31. Despite a slight increase in
superior thyroid and external carotid artery flow, there was no statistically significant
change from before to after stenting.
Conclusions—This study showed no differences in blood velocity profiles in the ipsilateral superior thyroid and external carotid arteries after stenting.
Received August 15, 2013, from the Departments
of Radiology (Y.G., L.T.A.) and Cardiology (R.A.,
P.V., M.A.C., M.B.V., H.K.), Sakarya University
Medical Faculty, Sakarya, Turkey. Revision
requested September 13, 2013. Revised manuscript accepted for publication January 23, 2014.
Address correspondence to Yasemin
Gunduz, MD, Department of Radiology, Sakarya
University Medical Faculty, 54100 Sakarya,
Turkey.
E-mail: [email protected]
Abbreviations
EDV, end-diastolic velocity; PI, pulsatility
index; PSV, peak systolic velocity; RI, resistive
index
doi:10.7863/ultra.33.10.1783
Key Words—carotid artery stenting; Doppler sonography; superior thyroid artery;
vascular ultrasound
C
arotid artery stenosis is a common diagnosis in general medical practice and is one of the main risk factors for ischemic
cerebrovascular events. Along with technological improvements in interventional neuroradiology, some cases of carotid stenosis have been treated by carotid angioplasty with stenting, especially
for patients with higher risk factors for carotid endarterectomy.1,2
Because lesions of the internal carotid artery often extend into the
common carotid artery, the stent is usually extended into the common carotid artery, thereby crossing the external carotid artery.3
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:1783–1789 | 0278-4297 | www.aium.org
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Gunduz et al—Effect of Internal Carotid Artery Stenting on Superior Thyroid Artery Doppler Flow
Furthermore, in vitro models have demonstrated abnormal
external carotid artery flow dynamics when the stent is
extended across the external carotid artery orifice.4
Doppler sonography can facilitate a quantitative evaluation of the blood flow in the arteries supplying the thyroid
gland and a qualitative evaluation of the parenchymal flow;
thus, it provides important diagnostic data to clinicians dealing with thyroid diseases.5–7 The thyroid gland is supplied
by a superior and an inferior thyroid artery, which are
branches of the external carotid artery and thyrocervical
trunk, respectively. Accurate positioning of the inferior thyroid artery is difficult because of its deep position. The superior thyroid artery originates as the first branch of the external
carotid artery. By contrast, the superior thyroid artery, which
is the chief artery supplying blood to the thyroid gland, is
superficial and can be easily positioned from its intersecting
point with the thyroid lobes. In addition, anatomic variation
of the superior thyroid artery rarely occurs.8,9
In contrast to the internal and external carotid arteries,
the superior thyroid artery was neglected in a previous
carotid model studied both experimentally and clinically
because of the geometric complexity caused by the presence
of this small vessel.4 In addition, to our knowledge, data
concerning the effect of carotid stent placement on the ipsilateral superior thyroid artery immediately after the procedure have not been published. This study examined the
effect of internal carotid angioplasty and stenting on the
ipsilateral superior thyroid artery Doppler-derived flow
parameters.
Materials and Methods
Patient Demographics
At a single center, between May 2010 and March 2013,
41 patients were enrolled in this study. The study, which
complied with the Declaration of Helsinki, was approved
by the local Ethics Committee, and all patients enrolled in
the study gave written informed consent.
Exclusion criteria were pregnancy, thyroid hormone
use, thyroid disease, iodine-containing medications such as
contrast media and amiodarone, history of thyroid surgery,
history of heart failure and myocardial infarction 72 hours
before carotid artery stenting and major strokes after
stenting, contralateral internal carotid artery occlusion,
preprocedural and postprocedural external carotid artery
stenosis of 50% or greater, and intracranial stenosis of the
ipsilateral common carotid artery.
Seventy-six patients with carotid stenosis of 50% or
greater who were evaluated initially preprocedurally with
duplex sonography underwent carotid angiography, and
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we also analyzed carotid stenosis angiographically based on
the North American Symptomatic Carotid Endarterectomy
Trial criteria.10 Eight patients were excluded from the study
because their angiographic internal carotid artery stenosis
was less than 70%. Fifty symptomatic patients were treated
if the degree of internal carotid artery stenosis exceeded
70% according to the North American Symptomatic
Carotid Endarterectomy Trial angiographic criteria.10 For
18 asymptomatic patients, the cutoff point for treatment
was stenosis of 80% or greater. Sixty-eight patients underwent elective stenting of the internal carotid artery (37
right and 31 left), of whom 41 consecutive patients were
enrolled and 27 were excluded (5 with potential major
strokes within 48 hours after stenting, 11 with external
carotid artery stenosis of 50% or less [3 determined by preprocedural angiography and 8 by angiography after stenting], 3 with contralateral internal carotid artery occlusion,
2 with a lack of patient data, and 6 with a lack of control
sonographic data after stenting).
Doppler Examination Technique
Baseline carotid sonography was performed between 1 and
30 days before carotid angiography. All patients were examined after a 10-minute rest period to minimize changes in
blood pressure and heart rate to avoid influencing the
Doppler velocity parameters. A preliminary sonographic
examination of the thyroid of each patient was performed
to identify any gross abnormalities such as parenchymal
nodules and heterogeneity. Each lobe was scanned longitudinally and transversely in both the B-mode and color
flow mode. After the grayscale sonographic examination,
each patient underwent Doppler sonography. All Doppler
and grayscale measurements were performed by an
experienced radiologist using the same ultrasound device
(Aplio MX; Toshiba Medical Systems Co, Ltd, Tokyo,
Japan; frequency range, 2–12 MHz). All patients were evaluated preprocedurally and postprocedurally with duplex
sonography of the ipsilateral and contralateral common
carotid arteries, internal carotid arteries, external carotid
arteries, and superior thyroid arteries.
The sonographic study was performed with the patient
in a dorsal decubitus position with a cushion under the
shoulders and the neck hyperextended. To avoid underestimating the vascularization intensity, the probe was lightly
positioned on the skin without any compression. The transducer was manipulated to obtain a longitudinal image of
the common carotid artery by an anterolateral approach.
The superior thyroid artery, located just medial to the
common carotid artery at the upper pole of the thyroid
gland, was imaged with a slightly modified longitudinal
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Gunduz et al—Effect of Internal Carotid Artery Stenting on Superior Thyroid Artery Doppler Flow
scan. It is easily identified by its opposite flow direction relative to the adjacent common carotid artery.5,11,12 The superior thyroid artery was found by slowly moving the
transducer medially from the common carotid artery. The
images were obtained by color and pulsed Doppler sonography. The Doppler angle was corrected to 60° or less. The
sample volume was kept sufficiently large to contain the
whole lumen. The longitudinal view is used to avoid pitfalls in assessment of stenosis and should be moved or
changed as needed. Three consecutive blood velocity waveforms with a similar pattern were considered correct spectral samples.
The peak systolic velocity (PSV), end-diastolic velocity
(EDV), resistive index (RI), and pulsatility index (PI) were
obtained automatically from both the superior thyroid and
external carotid arteries, and the mean values were measured for all patients before and 24 to 48 hours after the
carotid intervention. An example is shown in Figure 1.
Normal value ranges for the external carotid artery in adults
include a PSV of 57 to 87 cm/s, an EDV of 11 to 21 cm/s,
and an RI of 0.72 to 0.84; the superior thyroid artery
normally has a PSV of 25 cm/s. In addition, the RI can be
calculated from spectral measurements by using the equation RI = (PSV – EDV)/PSV. The PI can be calculated by
using the equation PI = (PSV – EDV)/MV, where MV is
the mean flow velocity during the cardiac cycle. These divisions eliminate the need for angular corrections.12,13
Carotid Artery Stenting Protocol
Symptomatic patients were treated if the degree of internal
carotid artery stenosis exceeded 70%, according to the
North American Symptomatic Carotid Endarterectomy
Trial angiographic criteria.10 For asymptomatic patients,
the cutoff point for treatment was stenosis of 80% or greater.
All procedures were performed under local anesthesia
from a groin approach by an experienced interventional cardiologist using a 0.014-in platform with a distal embolus protection device (Emboshield NAV6; Abbott Laboratories,
Figure 1. Automatic Doppler measurement of the flow velocity in the superior thyroid artery. The probe was positioned in the oblique sagittal plane,
close to the superior thyroid pole. HR indicates heart rate; S/D, systolic-to-diastolic ratio; Ved , end-diastolic velocity; Vm, mean velocity; Vmax, maximum
velocity; and Vmin, minimum velocity.
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Gunduz et al—Effect of Internal Carotid Artery Stenting on Superior Thyroid Artery Doppler Flow
North Chicago, IL). Overstenting of the carotid bifurcation
was defined as covering the external carotid artery origin by
stent placement from the internal carotid artery extending
into the common carotid artery (Figure 2, A and B).
Several different appropriately sized self-expandable
carotid stents (Abbott XACT) were used throughout the
study. Patients were monitored in the recovery room and,
barring any complications, were discharged in 3 days.
Concomitant Medical Therapy
The purpose of such treatment was to control risk factors
such as hypertension, hyperlipidemia, the metabolic state
in diabetes mellitus, and cigarette smoking and to provide
standardized antiplatelet therapy. All patients were treated
with aspirin at 100 mg/d plus clopidogrel at 75 mg/d for at
least 7 days before carotid artery stenting and 1 month
afterward. During stenting, patients received intravenous
heparin (5000–10,000 U) to maintain an activated clotting
time of greater than 250 seconds. Atropine (0.5–1 mg) was
injected intravenously immediately before stent dilation.
Statistical Analysis
Statistical evaluation was performed with the SPSS version
15.0 software package for Windows (IBM Corporation,
Armonk, NY). Quantitative variables are given as mean ±
standard deviation, and qualitative variables are expressed
as percent and frequency. Groups (before and after stenting) were compared by the Student t test for continuous
variables and the χ2 test for categorical variables. Using a
linear regression model, multivariate analysis was fitted for
Doppler velocity parameters with the ipsilateral superior
thyroid artery as the dependent variable, with adjustments
for age, sex, smoking status, hypertension, diabetes mellitus,
and hyperlipidemia. For all analyses, 2-tailed P < .05 was
considered statistically significant.
angiography core laboratory, decreased from 84% ± 21%
before the procedure to 12% ± 7% after the procedure, and
the lesion length was 1.0 ± 0.7 mm.
Among patients with carotid stenting, the preprocedural PSV, EDV, RI, and PI in the ipsilateral external
carotid artery were 79 ± 24 cm/s, 17 ± 7 cm/s, 0.77 ± 0.26,
and 1.27 ± 0.22, respectively; after stenting, they were
94 ± 31 cm/s, 20 ± 6 cm/s, 0.80 ± 0.4, and 1.25 ± 0.31.
The preprocedural PSV, EDV, RI, and PI in the ipsilateral
superior thyroid artery were 30 ± 11 cm/s, 13 ± 6 cm/s,
0.62 ± 0.11, and 1.04 ± 0.28; after stenting, they were
36 ± 8 cm/s, 14 ± 9 cm/s, 0.71 ± 0.07, and 1.11 ± 0.19.
Despite a 20% increase in superior thyroid and external
carotid artery flow parameters, there was no statistically
significant change from before to after ipsilateral stenting
(Table 1).
For the superior thyroid artery Doppler study, the PSV,
RI, and PI were not significantly different between men and
women, patients with and without hypertension, and
patients with and without diabetes. Univariate analysis
revealed that there was no significant correlation between
superior thyroid artery flow and age, presence of coronary
artery disease, hypertension, diabetes mellitus, smoking, or
hyperlipidemia (age, r = 0.521; coronary artery disease, r =
0.365; hypertension, r = 0.187; diabetes mellitus, r = 0.079;
smoking, r = 0.173; low-density lipoprotein, r = 0.481;
and triglycerides, r = 0.642).
Technical success (<30% poststenting angiographic
stenosis) was achieved in all patients, and postprocedural
angiography showed a patent external carotid artery in all
patients. Two patients had transient ischemic attacks, and
1 had a minor stroke; there were no deaths or major strokes
during the procedures. The Doppler velocity parameters
for the internal and common carotid arteries before and
after stenting are presented in Table 2.
Results
Sixty-eight patients underwent elective stenting of the
internal carotid artery (37 right and 31 left), of whom 41
were enrolled and 27 were excluded from the study.
The mean age of the patients was 64 ± 10 years (range, 43–
78 years). Coronary artery disease was present in 53% of
the patients (n = 22); 64% (n = 26) had a history of hypertension; 39% (n = 16) had a family history of cardiovascular disease; 35% (n = 14) had diabetes mellitus; and
46% (n = 19) were smokers. In addition, the low-density
lipoprotein level was 141 ± 38 mg/dL; triglycerides, 154
± 48 mg/dL; and thyrotropin, 2.2 ± 0.7 mIU/L. The percentage of internal carotid artery stenosis, as assessed by the
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Table 1. Doppler Flow Parameters for the Superior Thyroid and External
Carotid Arteries
Parameter
STA PSV, cm/s
STA EDV, cm/s
STA RI
STA PI
ECA PSV, cm/s
ECA EDV, cm/s
ECA RI
ECA PI
Before Stenting
30 ± 11
13 ± 6
0.62 ± 0.11
1.04 ± 0.28
79 ± 24
17 ± 7
0.77 ± 0.6
1.27 ± 0.22
After Stenting
36 ± 8
14 ± 9
0.71 ± 0.07
1.11 ± 0.19
94 ± 31
20 ± 6
0.80 ± 0.4
1.25 ± 0.31
P
.156
.332
.370
.072
.076
.154
.798
.892
ECA indicates external carotid artery; and STA, superior thyroid artery.
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Figure 2. Angiographic sequence of carotid stenting. A, Baseline angiogram. CCA indicates common carotid artery; ECA, external carotid artery; ICA,
internal carotid artery; and STA, superior thyroid artery. B, The stent was extended from the internal carotid artery into the common carotid artery,
crossing the external carotid artery (arrows). C, Angiogram after the procedure. Note that the superior thyroid artery is still patent.
Discussion
Large-scale randomized trials have demonstrated that
carotid artery stenting is an effective treatment for prevention of cerebrovascular events in patients with symptomatic
and asymptomatic carotid artery stenosis. More recently,
percutaneous carotid artery stenting has been tested as an
alternative treatment and has been shown to be beneficial
among high-risk patients. These results have led to a large
increase in the number of carotid artery stenting procedures
over the past decade.2,14–16 Furthermore, noninvasive
duplex sonography has been a standard method for clinical
evaluation of the carotid arteries, and patients with carotid
disease are frequently referred for carotid revascularization
based solely on the results of carotid duplex studies.17–20
Most high-grade arteriosclerotic lesions are located at
the carotid bifurcation, usually at the proximal internal
carotid artery and the distal common carotid artery. During
carotid artery stenting, it is preferable to extend the bare
stent from the internal carotid artery into the common
carotid artery. That the stent covers the orifice of the external
carotid artery might be a further argument against carotid
stenting.21,22 The superior thyroid artery is the first external
carotid artery branch, and measurement of the superior
thyroid artery is more complicated because of its smaller
transverse diameter compared to external carotid artery
lesions.23–25 Furthermore, ipsilateral external carotid artery
lesions affect the flow parameters of the superior thyroid
artery.26 In all of these studies, duplex scan–based flow criteria were used.27 Ascer et al28 used the PSV of the external
carotid artery to grade external carotid artery stenosis.
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In addition, the PSV is also quantitative and reflects the
blood supply status of the thyroid, and the mean superior
thyroid artery PSV is proven to be practical, accurate, and reliable in the differential diagnosis of thyrotoxicosis.29–31 However, the presence of the small artery has a considerable
effect on both the flow field and wall shear stress in the
common-external side branch, but it has very little effect
on the flow field and wall shear stress distribution in the
common-internal side branch.32
As far as we know, a few studies have been published
so far with data concerning the effect of carotid stent placement on the ipsilateral external carotid artery immediately
after the procedure.21,33 Some reports demonstrated abnormal external carotid artery flow dynamics when the stent
was extended across the external carotid artery orifice.
Local factors accompanying overstenting of the external
carotid artery orifice might be considered, although the
nature of these factors remains unclear.4,33 Flow turbulence
caused by passage through the mesh of the stent wall to the
external carotid artery might be a plausible explanation
Table 2. Doppler Flow Parameters for the Internal and Common
Carotid Arteries
Parameter
ICA PSV, cm/s
ICA EDV, cm/s
ICA-CCA ratio
CCA PSV, cm/s
CCA EDV, cm/s
CCA RI
Before Stenting
297 ± 68
117 ± 37
4.1 ± 1.8
117 ± 34
34 ± 7
0.77 ± 0.47
After Stenting
72 ± 18
35 ± 7
1.3 ± 0.7
111 ± 18
30 ± 12
0.76 ± 0.33
P
<.001
<.001
<.001
.543
.621
.896
CCA indicates common carotid artery; and ICA, internal carotid artery.
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Gunduz et al—Effect of Internal Carotid Artery Stenting on Superior Thyroid Artery Doppler Flow
for the enhanced external carotid artery flow parameters.
Furthermore, during stent placement, atheromatous
material might be pushed from the common and internal
carotid arteries into the origin of the external carotid artery.
It is assumed that flow turbulence caused by passage through
the mesh of the stent wall to the external carotid artery
might be a plausible explanation for the increased narrowing of the external carotid artery.21,22,33
Some studies, however, obtained different results.
Ascer et al,28 being the first to compare preoperative and
postoperative duplex evaluation of the external carotid
artery, found no significant early or late influence of
carotid artery stenting on disease progression in the ipsilateral external carotid artery. In another study, the ipsilateral external carotid artery flow ratio decreased on day 1 after
stenting, but its tendency was not statistically significant.33
To our knowledge, data concerning the effect of
carotid stent placement on the ipsilateral superior thyroid
artery immediately after the procedure and during followup have not been published previously. Interestingly, in
our study, the superior thyroid artery velocities were actually increased at 1 to 2 days, which may have been an artifactual increase related to the change in flow through the
internal and external carotid arteries. It could also have
been due to architectural changes in the external carotid
artery after stent placement (eg, metallic stent struts,
plaque compression, and shifting). Regardless, the increased
velocities would certainly suggest no immediate detrimental effects of stent coverage. Thus, the metallic struts of
the stent did not occlude flow to the external carotid artery.
Furthermore, the external carotid artery and superior thyroid artery remained widely patent in all patients despite
stent coverage (Figure 2).
This study reports the short-term fate of the superior
thyroid artery after carotid stenting. Our results show that
no significant difference in flow velocity occurred in the
superior thyroid artery between the preprocedural and
postprocedural duplex evaluations on days 1 and 2 (P > .05).
Thus, we sought to determine whether patients undergoing
carotid artery stenting had any change in external carotid
artery patency and superior thyroid artery flow.
Limitations of this study were as follows: Our results
were based on experience at a single center, and our study
was limited by the small number of patients. Although it
was a prospective study with meticulous clinical procedures,
and it included 68 carotid artery stenting procedures, the
duration of study was limited to 1 to 2 days after stenting.
Additionally, most studies of the external carotid artery
were performed in the first month after stenting, but some
were performed several months later. Any progression of
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disease in the carotid arteries could increase or decrease
flow velocities in the ipsilateral external carotid and superior
thyroid arteries and thereby increase or decrease the
effect on flow velocities observed after ipsilateral stenting.
In addition, the small sample size yielded wide standard
deviations, limiting the power of the study to detect a 20%
velocity difference.
In conclusion, carotid artery stenosis has been treated
by carotid angioplasty with stenting, especially for patients
with higher risk factors for carotid endarterectomy. The
stent is usually extended into the common carotid artery,
thereby crossing the external carotid artery. The superior
thyroid artery originates as the first branch of the external
carotid artery1–3,8 and is the main source of arterial flow to
the thyroid gland, upper part of the larynx, and neck
region.19 Furthermore, this study showed no difference in
blood velocity profiles in the ipsilateral superior thyroid
artery after carotid artery stenting. Thus, in our opinion,
this study may be a guide for assessing the impact of carotid
artery stenting on the differential diagnosis of hyperthyroidism and to solving confusion that may occur in the
future.
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