long-term results of eversion carotid endarterectomy
TRANSCRIPT
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PresentedVascular SurgFebruary 1, 20
1Division oHospital, Balti
2DivisionRochester, Bal
3Division oBayview Medi
CorrespondHospital, HarvUSA, E-mail:
Ann Vasc SurDOI: 10.1016/� Annals of VPublished onli
92
Long-Term Results of Eversion CarotidEndarterectomy
James H. Black III,1 Joseph J. Ricotta,2 and Calvin E. Jones,3 Baltimore, Maryland
Background: Carotid endarterectomy (CEA) is supported by level 1 evidence as the standardof care for symptomatic and asymptomatic extracranial carotid stenosis. Eversion CEA (ECEA)has been proposed as an acceptable alternative to the standard bifurcation endarterectomy inmany patients; however, long-term follow-up of this technique has not been reported. This studywas designed to analyze the long-term durability of ECEA in symptomatic and asymptomaticpatients.Methods: From June 1989 to March 2002, 534 ECEAs were performed on 485 patients (60%male, 44% symptomatic, reoperative 1.0%). Preoperative characteristics, operative findings,and postoperative duplex data were entered prospectively into database. These data were retro-spectively reviewed to determine the incidence of major adverse cardiovascular events (MACEs)within 30 days of surgery, late survival, and the late incidence of ipsilateral carotid disease. Vari-ables associated with carotid restenosis were subjected to statistical analysis.Results: The mean follow-up period was 8.86 years (95% confidence interval [CI] 6.56-9.16,median 6.6). MACEs occurred in 19 patients (3.8%), including 13 strokes (2.6%) and six deaths(1.2%). MACEs when added to surgical siteerelated complications yielded a<30-day complicationrate of 5.3%. Survival by life-table analysis at 5 and 10 years was 75.2% and 50.1%, respectively.Recurrent stenosis of the ECEA site was noted in 20 patients (4.1%), with a mean time to recurrenceof 4.4 years (95% CI 2.92-6.07, median 4.0). Statistical analyses failed to implicate any specificpatient risk factor, symptomatic presentation, presence of hyperlipidemia or statin use, internalcarotid artery diameter, or presence of residual disease as predictive of recurrent stenosis.Conclusion: The current study represents the longest follow-up to date of patients undergoingECEA. The findings of this study support ECEA as a safe and durable long-term treatment forextracranial carotid disease presenting with or without acute symptomatology.
INTRODUCTION
The efficacy of carotid endarterectomy (CEA) to
prevent stroke has been demonstrated as superior
to medical therapy in several large randomized
at the 19th Annual Winter Meeting of the Peripheralery Society, Steamboat Springs, CO, January 30 -09.
f Vascular and Endovascular Surgery, Johns Hopkinsmore, MD.
of Vascular and Endovascular Surgery, Mayo Clinicetimore, MD.
f Vascular and Endovascular Surgery, Johns Hopkinscal Center, Baltimore, MD.
ence to: James H. Black III, MD, Johns Hopkinsey 611, 600 North Wolfe Street, Baltimore, MD 21287,[email protected]
g 2010; 24: 92-99j.avsg.2009.06.019ascular Surgery Inc.ne: September 7, 2009
trials.1-3 More recently, population-based studies
have demonstrated further improvements in stroke
and death rates after CEA, thus setting a high stan-
dard of care for comparison with evolving stent
therapies.4-6 Techniques for eversion CEA (ECEA)
have been evaluated in retrospective series,7,8
systematic reviews,9 and randomized trials10; and
ECEA has been proven a safe technique for extirpa-
tion of occlusive carotid lesions. While initial results
of carotid surgery have proven to be excellent, the
ability of CEA techniques to yield low rates of reste-
nosis in the long term has not been clearly defined.
As both surgical and endovascular therapies for
extracranial carotid disease evolve, initial results
will expectedly improve and long-term results of
competing therapies will assume greater therapeutic
relevance. As such, our study was designed to
analyze the long-term outcomes of ECEA in
symptomatic and asymptomatic patients.
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Vol. 24, No. 1, January 2010 Long-term results of eversion CEA 93
MATERIALS AND METHODS
A database of consecutive ECEAs performed at
Johns Hopkins Bayview Medical Center was main-
tained prospectively using data entry into Microsoft
Access and exported to Excel (Microsoft, Redmond,
WA). From June 1989 until March 2002, 534 ECEAs
were performed on 485 patients. Only ECEAs were
included in the study, and carotid surgeries per-
formed in conjunction with other vascular recon-
structive surgeries were excluded. During the same
period, 126 standard CEAs were performed using
patch angioplasty and intraluminal shunting; these
were performed in the setting of a period of random-
ization between standard and ECEA techniques.
Thus, the demographic and anatomic profiles of
these standard CEA patients are no different from
those of ECEA patients; they had similar immediate
major adverse cardiovascular events (MACEs) (but
longer operative times by approximately 30 min,
less plaque excised [grams], and higher cost due to
patch cost) but were not compiled for long-term
follow-up and, thus, are not considered further.
Patient demographics, surgical indications, oper-
ative details, and postoperative courses were
recorded from hospital records and prior clinic
assessments. Comorbid conditions and risk factor
categories for subsequent analysis were identified
and recorded in the database using reporting stan-
dards as described by the Society of Vascular Surgery
ad hoc committee.11 MACEs (myocardial event,
stroke, death) were identified within 30 days of
surgery. Surgical site complications (i.e., wound
infection, hematoma, nerve injury) were identified
from the medical record and included in the total
<30-day complication rate along with MACEs.
Long-term outcomes were identified from
hospital and office medical records. When hospital
or office records were incomplete, the patient or
a relative was contacted directly by telephone
(n¼ 60, 12.3%). For patients who could not be con-
tacted (n¼ 45, 9%), the date of death was identified
from the Social Security National Death Index.
Restenosis was defined as requirement to reoper-
ate on the index ECEA side or >60% diameter
reduction on duplex ultrasonography by a peak
systolic velocity (PSV)> 200. Duplex ultrasonog-
raphy was performed within 1-2 months of the
ECEA and yearly thereafter in the Intersocietal
Commission for the Accreditation of Vascular Labo-
ratories (ICAVL)ecertified vascular laboratory at
Johns Hopkins Medical Institutions. Routine axial
imaging techniques and angiography were not
used routinely for postoperative evaluation or
corroboration of duplex findings.
Postoperative survival and restenosis were
computed using life tables and Kaplan-Meier esti-
mate. Dichotomous variables and outcomes were
analyzed in contingency tables using a Fisher exact
test. Univariate models for variables associated with
restenosis were assessed using hazard ratios (HRs).
Data were presented as averages ± standard deviation
(SD), and p< 0.05 was considered statistically
significant.
All procedures were performed under general
anesthesia using systemic anticoagulation with
unfractionated intravenous heparin during the
eversion phase of the operation. During the clamp
interval, hypertension (systolic pressure 160-
180 mm Hg) was allowed or induced pharmacolog-
ically. All patients received antiplatelet medication
perioperatively to include 1,300 mg aspirin and
500 mL intravenous dextran during the first 10 post-
operative hours. The ECEA technique was per-
formed by transection of the common carotid
artery, as described by Etheridge12 and depicted in
Figure 1. To provide adequate exposure for the
ECEA, the occipital artery and vein are divided
routinely. The hypoglossal nerve can then be swept
medially, exposing the internal carotid artery (ICA)
beyond the posterior belly of the digastric muscle.
This exposure permits routine ICA clamping
4-5 cm beyond the carotid bifurcation. The superior
thyroid artery is usually divided to facilitate mobili-
zation of the carotid bulb. After common carotid
transection just proximal to the superior thyroid
artery, a deep endarterectomy plane is developed
to separate the plaque from the external elastic
lamina, appreciated as a pink, smooth interface in
the cleavage plane. The eversion is developed first
from the external carotid artery, then into the
ICA. Intimal tacking sutures were not used. Endar-
terectomy of the common carotid artery is accom-
plished for at least 2 cm, and the plaque is
transected flush to maintain an adherent proximal
intimal surface. End-to-end anastomosis of the
common carotid artery can then be accomplished.
A 6-0 coated polyester suture was preferred over
monofilament polypropylene suture for the
common carotid anastomosis due to the propensity
of monofilament to pursestring and leave an hour-
glass anastomotic deformity. The common carotid
artery anastomosis is accomplished in a fashion
that allows direct visualization of the lumen (see
Fig. 1). Sutures are placed exactly anterior and
posterior and tied. The sutures are rotated to facili-
tate a rapid suture line formation. After flushing,
blood flow is restored first to the external carotid
artery and then to the ICA. Redundancy of the
ICA can be removed by overlapping the proximal
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Fig. 1. Technique of ECEA. A The carotid mobilization
should include division of the vascular sling of the occip-
ital artery and vein branch of the external carotid artery,
which tethers the hypoglossal nerve in proximity to the
mid- and distal ICA. B The endarterectomy plane is
developed cephalad with retraction of the carotid
branches over the mandril of the plaque. C Sharp divi-
sion of the intimomedial plane flush against the common
carotid artery (CCA) eversion. DeF Anterioreposterior
suture placement facilitates rapid anastomotic
completion.
94 Black et al. Annals of Vascular Surgery
and distal transected ends of the common carotid
artery and shortening the length of the proximal
common carotid artery.
Electroencephalographic monitoring was not
performed to determine cerebral ischemia.
Intraluminal shunts were not employed in the
study, and carotid stump pressure was not assessed
routinely to evaluate collateral hemispheric circula-
tion. ECEA does allow passage of an intraluminal
shunt after the bulk of the internal carotid plaque
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Table I. Medical comorbidities of patients
undergoing ECEA
% n
Aspirin use 94% 507
Heart disease 57% 278
Hypertension (>1 drug) 29% 119
Diabetes 13% 66
Vol. 24, No. 1, January 2010 Long-term results of eversion CEA 95
is completed, but the ECEAs in this series were per-
formed without an intraluminal shunt. Completion
intraoperative angiography using plate radiographs
was performed in the first 24 months of the series
but was found to have no clinical value. Thereafter,
only if continuous wave Doppler insonation sug-
gested residual stenosis was completion angiography
performed.
Renal insufficiency 11% 55Tobacco use (current + recent) 62% 291
Hypercholesterolemia 73% 356
Drug-controlled 42% 204
Table II. Surgical indications and variables for
ECEA
n %
Asymptomatic 299 56%
Symptomatic 235 44%
TIA/TMB 142 26%
Stroke 93 17%
Reoperative 5 1%
Mean stenosis 79% ± 10.8% range 55-99%
Mean ICA diameter 4.16 ± 1.7 mm range 2.5-8
Operative time 126 ± 28 min range 67-270
Mean carotid
clamp time
18 ± 10 min range 12-35
RESULTS
There were 534 ECEAs performed on 485 patients
during the study interval. Sixty percent of the
patients were male (n¼ 291) and 40% female
(n¼ 194). The average age of the patients was 71
years (range 42-93). Medical comorbidities are
typical of patients with arteriosclerosis and are
summarized in Table I.
The indications for surgery (see Table II) were
asymptomatic, severe stenosis in 56% (n¼ 299)
and symptomatic lesions in 44% (n¼ 235). For
symptomatic disease, 26% (n¼ 142) were for tran-
sient ischemic attack (TIA) or episodic amaurosis
fugax and 17% were for stroke (n¼ 93). Average
operative time was 126 min, and average carotid
clamp time to perform the ECEA was 18 min (range
12-35). ICA diameter averaged 4.16 ± 1.7 mm, with
187 ECEAs (35%) having an outer diameter of
3.5 mm or less.
A total complication rate of 5.3% was noted
within 30 days of ECEA. Site complications were
noted in eight ECEAs (1.8%), with five cranial
nerve palsies (three CN XII, two CN X). None of
these cranial nerve events led to permanent deficit.
Wound hematoma was noted in three ECEAs,
requiring exploration; in all cases the bleeding site
was not the common carotid anastomosis. Death
occurred in six patients (1.2%), with half involving
major stroke and the remaining cardiovascular
events. There were 13 strokes , with recovery of
six ECEA patients, yielding a major permanent
stroke risk of 1.2%. Strokes were identified by the
operating surgeon and resident teams and
confirmed by formal neurological exam by a neurol-
ogist. A major cardiovascular event rate (MACE) in
the ECEA patients was 3.8% at 30 days.
The mean follow-up period was 8.86 years (95%
CI 6.56-9.16, median 8.6). Duplex evaluation of the
operated carotid was performed in 98.2% of patients
at year 1, 95% at year 2, and 90% at year 5. By
10 years, duplex evaluation was available in 75%
of surviving patients. Follow-up data for survival
were available for all 485 patients. Kaplan-Meier
curve estimates for survival were 75.2% at 5 years
and 50.1% at 10 years post-ECEA (see Fig. 2).
Fisher’s exact test failed to demonstrate any associa-
tion of gender ( p¼ 0.42), tobacco use ( p¼ 0.21),
hyperlipidemia ( p¼ 0.35), or statin use ( p¼ 0.65)
with survival.
Restenosis was identified in 20 patients (4.1%).
The mean time to recurrence was 4.4 years, with
a median of 4 years. Three of these restenosis
patients underwent redo ECEA without event; two
patients were treated with redo CEA by longitudinal
arteriotomy and Dacron patch angioplasty. Of these
five redo carotid surgeries, the indication was symp-
tomatic lesion in four. The remaining patients man-
ifested duplex criteria suggesting >60% stenosis,
but intervention was deferred due to stable veloci-
ties and asymptomatic state, patient preference, or
other mitigating medical comorbid event. Statistical
analysis (Fisher’s exact test) failed to implicate any
specific patient risk factordsymptomatic presenta-
tion ( p¼ 0.15), statin use ( p¼ 0.52), ICA diameter
<3.5 mm ( p¼ 0.28), or presence of residual disease
on intraoperative angiographydas predictive of
recurrent stenosis ( p¼ 0.76). Hyperlipidemia did
not reach significance in predicting restenosis, but
statistical analysis suggested an effect may be
present ( p¼ 0.08) (Fig. 3).
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Fig. 2. Kaplan-Meier survival curves for 485 patients
after ECEA. Standard error of the mean <10% for all
points on graph.
Fig. 3. Freedom from restenosis >60% after ECEA. Stan-
dard error of the mean <10% for all points on graph.
96 Black et al. Annals of Vascular Surgery
DISCUSSION
Debakey et al.13 originally mentioned carotid tran-
section and eversion endartectomy for extended
common carotid artery lesions, as well as for ICA
straightening. Etheridge12 then realized a similar
technique could be used to safely evert the carotid
bifurcation and achieve a simple endarterectomy.
The advantage of this ECEA technique is the restora-
tion of a vessel that appears more anatomically and
physiologically normal, theoretically reducing
turbulence that would incite intimal hyperplasia.
The suture line is created across the bulb, where
intimal hyperplasia would be least expected to
produce significant luminal narrowing, as opposed
to longitudinal arteriotomy, which places a suture
line on the critical ICA outflow. Patch materials
are avoided, thus reducing infectious risk.
Patients in this series underwent ECEA without
intraluminal shunting. Our perioperative stroke
risk approximated most of the contemporary series
regarding CEA, which have reported major stroke
risks of 1-2% and included shunting to reduce cere-
bral ischemia.10,14-16 Our ECEA technique allows
for passage of an intraluminal shunt after the ICA
plaque has been removed. However, plaque
removal from the ICA is the most time-consuming
portion of the operation, the remaining common
carotid eversion (as shown in Fig. 1) is rapid, and
final closure is usually extremely simplified, taking
usually less than 2-3 min; thus, shunt placement is
not likely to produce meaningful time savings. On
average, the total cross-clamp time was 18 min,
during which systemic hypertension was main-
tained to encourage collateral flow. Our contention
is stroke after ECEA is embolic in nature. Intraoper-
ative cerebral ischemia is considered to be a rela-
tively uncommon cause of embolic stroke.17-19
Indeed, in analysis of 66 strokes in a series of over
3,000 carotid surgeries performed with selective
shunting, 65% of strokes were thought to be attrib-
utable to technical errors in the CEA and contralat-
eral occlusion (wherein cerebral ischemia would be
theoretically highest) was not an independent
predictor of stroke.20 While it cannot be denied
that ICA clamping may produce cerebral ischemia
in some patients, it is likely such ischemia is reversed
with either shunting or opening flow after clamp
removal on the carotid territory. Magnetic reso-
nance imaging with diffusion-weighted imaging
was not available during the entire study interval
to interrogate the distinction of embolic or water-
shed infarct, but our clinical position is supported
by our experience in three of our ECEA patients
with major strokes, who awoke immediately with
major deficit and immediate exploration revealed
plateletefibrin aggregates lining the endarterec-
tomy plane.
The long-term survival of our patients was similar
to that in many series describing outcomes in the 5-
and 10-year time frame.14,21 Other studies have
demonstrated that hyperlipidemia or statin use influ-
ences mortality unfavorably14 or favorably,22,23 but
our statistical analysis could not identify any predic-
tion of long-term outcome based on control of hyper-
lipidemia. We suspect that failure to conclude an
effect of hyperlipidemia, or its treatment, on our
patients’ long-term survival likely represents a type
II statistical error. Our current practice is to initiate
statin medications based upon the evidence
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Vol. 24, No. 1, January 2010 Long-term results of eversion CEA 97
supporting a risk reduction in cardiovascular events
in the perioperative22,23 and long-term24-26 time
frames. Intensified statin regimens are encouraged
as benefit has been shown in patients with peripheral
arterial disease, but dose escalation is left to the
discretion of the primary-care physician.27,28
Restenosis is the Achilles’ heel of any vascular
intervention. Our restenosis rate was very low at
4.1% with an average follow-up of 8.86 years. In
addition, as several of the identified restenosis
events were in the time frame of 5-10 years, it is
possible that recurrence of native atherosclerotic
disease may account for some of these cases rather
than the typical biology of restenosis and myointi-
mal hyperplasia. We did not identify any patient
or anatomic factor associated with risk of restenosis
and conclude that absence of such findings suggests
a confluence of suitability of the ECEA for our
patients, diligent technique to avoid residual
disease, and the possibility that the event rate was
too low to have statistical power. The eversion tech-
nique has been shown by others to yield similarly
low long-term restenosis. Cao et al.29 reported
4-year follow-up of 1,353 patients randomized to
ECEA or standard CEA, and the ECEA cumulative
restenosis rate was 3.6% vs. 9.2% for standard
CEA. In analysis, ECEA was a negative predictor of
restenosis (HR¼ 0.3, p¼ 0.004). Their trial was crit-
icized for including both primary closure and patch
closure under the same treatment arm, but the low
rate of restenosis with ECEA was affirmed by others
who included >4 years of follow-up.9,30
Restenosis of ECEA is likely to have different
implications from standard CEA restenosis; without
the ICA suture line, ECEA restenosis may be even
more benign and less likely to produce symptoms.
Overall, recurrent stenosis is an uncommon source
of recurrent carotid symptomatology, often quoted
to be 3% or less of symptomatic carotid lesions.31,32
In examination of restenosis after ECEA, Green
et al.33 reported that recurrent stenosis at the distal
end of an ECEA was only 0.9% vs. 5% with standard
CEA. For Green et al.,33 most ECEA recurrences
developed at the proximal edge of the common
carotid eversion. We would echo their recommenda-
tion to fully expose the common carotid artery to
ensure all proximal disease is detected. Our experi-
ence with restenosis was similar to that of Green
et al.,33 with most early restenosis events occurring
in the common carotid artery (8/10 patients identi-
fied in the first 5 years of follow-up) versus the ICA
end point. Our later recurrences seem to be more
diffuse and have no predilection for location,
perhaps suggesting recurrence of atherosclerotic
disease and not typical myointimal hyperplasia.
Although Green et al.’s33 follow-up was only
1 year, the chronobiology of recurrent stenosis
suggests most of the restenosis events were captured
by their study. In an analysis of the Medline data-
base, the rate of restenosis for all CEAs was estimated
at 10% within the first year, 3% in the second year,
and 2% in the third year, suggesting that the rate of
restenosis is clearly not a linear biological process.32
As such, we believe the completeness of our duplex
follow-up is sufficient to identify patients who devel-
oped restenosis in our long-term time frame.
Carotid angioplasty and stenting (CAS) is rapidly
assuming a position in the armamentarium of
vascular specialists, inviting comparison with
ECEA or standard CEA with patch placement. Early
and mid-term CAS results have been strongly
debated, with supporters and detractors occasionally
degenerating into calls of misrepresentation.34 Prior
reports have not clarified the in-stent restenosis
rate, with a range of <5% to >20% reported.35,36
Long-term results are now emerging to demonstrate
the durability of CAS. de Donato and colleagues37
reported a 5-year restenosis rate of 6%, which
would seem to compare favorably with ECEA. We
believe that earlier reports demonstrating poor
restenosis rates may have included CAS technology
that was immature and incited exuberant intimal
damage, but in the absence of good data concerning
lowe and moderateecardiovascular risk patients
and CAS, we continue to advocate ECEA or standard
CEA technique with patch angioplasty closure for
our patients. Our experience suggests ECEA can
achieve excellent long-term results and may have
advantages over standard CEA techniques; thus, it
may be considered the ‘‘gold standard’’ to which
CAS results should be compared.
CONCLUSIONS
ECEA is a safe procedure with acceptable periopera-
tive results to address extracranial carotid disease,
produces admirable long-term results that compare
favorably with patch closure, and outperforms
primary longitudinal closure. Given our findings,
ECEA should be included among ‘‘best surgical
treatments’’ when comparison is made to CAS
results. Regardless of the technique of CEA, the
long-term results of carotid surgery will assume
greater importance as the long-term benefit of cath-
eter-based techniques to address carotid occlusive
disease has not been well defined. It is incumbent
on vascular surgeons and interventionalists to
recommend the safest proceduredone with strong
initial results and that delivers the most favorable
long-term outcomes.
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98 Black et al. Annals of Vascular Surgery
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