Carotid endarterectomy with bovine pericardium patch angioplasty: mid-term results.

Abstract

The objective of this study was to assess the efficacy of bovine pericardium (BP) as a patch material in carotid endarterectomy (CEA) in terms of peri- and postoperative complications and the incidence of recurrent stenosis. During a 4-year period, 148 CEAs were performed in 138 consecutive patients. The study group included elective, emergency, and combined with cardiac operation CEAs in both symptomatic and asymptomatic carotid artery disease patients. Patch angioplasty using the BP followed the standard CEA in all patients. Postoperative follow-up included clinical examination and periodical color duplex scans at 3, 6, and 12 months and yearly thereafter. Surgical outcome was evaluated by the operation-related parameters, early and late mortality and morbidity rates, and the incidence of recurrent stenosis. All CEAs were performed without any unfavorable event. In the early postoperative period, there were no deaths and the morbidity consisted of transient cranial nerve paresis (4.7%) in seven patients and two ipsilateral strokes (1.4%). During the follow-up period, three patients (2%) developed significant carotid restenosis, though they remain asymptomatic, while there were no deaths related to the CEA. Patch angioplasty of the carotid artery using BP showed unwittingly early and mid-term surgical outcome. Our results demonstrate the BP to be a suitable patch material for routine use in carotid surgery.

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Original Articles
Carotid Endarterectomy with Bovine
Pericardium Patch Angioplasty: Mid-Term
Results
Miltiadis I. Matsagas, MD, EBSQ-Vasc,1Christina Bali, MD,1Elena Arnaoutoglou, MD,2
John C. Papakostas, MD,1Christos Nassis, MD,3George Papadopoulos, MD,2and
Angelos M. Kappas, MD,1Ioannina, Greece
The objective of this study was to assess the efficacy of bovine pericardium (BP) as a patch
material in carotid endarterectomy (CEA) in terms of peri- and postoperative complications and
the incidence of recurrent stenosis. During a 4-year period, 148 CEAs were performed in 138
consecutive patients. The study group included elective, emergency, and combined with cardiac
operation CEAs in both symptomatic and asymptomatic carotid artery disease patients. Patch
angioplasty using the BP followed the standard CEA in all patients. Postoperative follow-up
included clinical examination and periodical color duplex scans at 3, 6, and 12 months and yearly
thereafter. Surgical outcome was evaluated by the operation-related parameters, early and late
mortality and morbidity rates, and the incidence of recurrent stenosis. All CEAs were performed
without any unfavorable event. In the early postoperative period, there were no deaths and the
morbidity consisted of transient cranial nerve paresis (4.7%) in seven patients and two ipsilateral
strokes (1.4%). During the follow-up period, three patients (2%) developed significant carotid
restenosis, though they remain asymptomatic, while there were no deaths related to the CEA.
Patch angioplasty of the carotid artery using BP showed invitingly early and mid-term surgical
outcome. Our results demonstrate the BP to be a suitable patch material for routine use in
carotid surgery.
INTRODUCTION
The role of carotid endarterectomy (CEA) in the
prevention of stroke has been well established in
both symptomatic and asymptomatic groups of
carotid artery disease patients by randomized con-
trolled trials.1-3The challenge to further improve
the perioperative and long-term outcomes of these
patients led to modification of the traditional CEA.
Patch angioplasty closure is a surgical technique
with increasing evidence of superiority over pri-
mary suture of the carotid arteriotomy.4-11It has
been reported to reduce the incidence of periop-
erative stroke and acute thrombosis or occlusion of
the carotid artery. It has been also characterized by
lower recurrent stenosis for the years following
CEA. The currently available materials include
autologous (vein) or heterologous, synthetic [Da-
cron?from DuPont, Wilmington, DE; polytetra-
fluoroethylene (PTFE)]
pericardium (BP)] patches. The ideal material re-
mains debatable because each one has its advan-
tages and limitations. A recent review of studies
comparing patch materials has shown that there is
little reliable evidence to guide surgeons upon
which material to use. Although more data are
needed to establish safe conclusions, the differences
between the compared materials were very small.12
orbiological[bovine
1Vascular Surgery Unit, Department of Surgery, School of Medicine,
University of Ioannina, Ioannina, Greece.
2Anesthesiology, School of Medicine, University of Ioannina,
Ioannina, Greece.
3Intensive Care Medicine, School of Medicine, University of Ioann-
ina, Ioannina, Greece.
Correspondence to: Miltiadis I. Matsagas, MD, EBSQ-Vasc, Vascular
Surgery Unit, Department of Surgery, University Hospital of Ioannina,
S. Niarchos Avenue, 45500, Ioannina, Greece, E-mail: mimats@cc.
uoi.gr
Ann Vasc Surg 2006; 20: 614–619
DOI: 10.1007/s10016-006-9102-3
? Annals of Vascular Surgery Inc.
Published online: June 24, 2006
614

Page 2

Carotid patch angioplasty by stabilized BP was
reported first by Biasi et al.13During the last dec-
ade, only a few reports of BP patch angioplasty
(BPPA) in CEA have been published, showing
comparable results to the other materials.14-18The
most valuable characteristics of BP are reported to
be its availability, biological compatibility, and
resistance in suture bleeding.12,19
This study aims to evaluate the efficacy and to
widen the current experience of BPPA in CEA with
regard to the mid-term outcome. The evaluation
was focused on peri- and postoperative complica-
tions and the incidence of recurrent stenosis of the
carotid artery during the follow-up period.
MATERIAL AND METHODS
All consecutive patients undergoing CEA between
March 2001 and May 2005 at Ioannina University
Hospital were reviewed. Patients’ data during initial
hospitalization and follow-up were prospectively
collected and stored in an electronic database.
Patch angioplasty was adopted and performed in all
CEAs for closure of the arteriotomy. As patch
material, the stabilized BP (VascuGuard?; Synovis
Life Technologies, St. Paul, MN) was used in all
operations, which were performed by the same
vascular surgeon (M. I. M.).
The main indications for CEA were symptomatic
carotid artery stenosis >70% and asymptomatic
stenosis >80%. Age, gender, risk factors, and indi-
cation for operation were recorded in all patients.
Diagnostic investigation of the carotid arterial dis-
ease was based on clinical examination, brain
computed tomographic (CT) scan, and color duplex
in all patients. Additionally, we used CT or digital
subtraction angiography in those patients where
confirmation of the diagnosis was needed. All pa-
tients were carefully evaluated by an independent
experienced neurologist (C. N.) before and after the
operation.
All CEAs were performed under general anes-
thesia with standard hemodynamic monitoring
during the procedure. A single dose of antibiotics
(cefuroxime 750 mg) was intravenously adminis-
tered just before endotracheal intubation. The
internal carotid stump pressure was measured in all
patients before carotid clamping, and if pressure
was <45 mm Hg or less than one-third of the sys-
tolic blood pressure at the moment, a temporary
shunt was placed after the endarterectomy was
accomplished.20In that way we had better control
at the completion of the plaque removal, especially
at the distal end, and the ability to put sutures fast
and precisely. Intravenous heparin (2,500-5,000
IU) was given before carotid cross-clamping in all
cases. CEA was performed following the standard
principles, and the arteriotomy was closed by
BPPA. The patch was rinsed with normal saline
according to the manufacturer’s instructions, cut to
the appropriate dimensions, and sutured at the
arteriotomy site by continuous 6/0 prolene suture.
Operation-related parameters, such as back flow
(stump), internal carotid artery pressure, as well as
carotid occlusion time, were also recorded.
Postoperatively, all patients were administered
antiplatelet therapy (clopidogrel 75 mg) starting
within the first 12 hr. In general, patients with an
uneventful recovery were discharged from hospital
the third postoperative day. Follow-up and evalu-
ation of surgical outcome included periodical clin-
ical examination starting the first month after the
operation and color duplex scans at 3, 6, and 12
months postoperatively and yearly thereafter. Du-
plex scans assessed the presence and percentage of
restenosis. Recurrent disease was defined as reste-
nosis >50%. All but four patients (2.9%) who were
lost during the follow-up period due to moving out
of our hospital trust area, were followed and had
the same protocol. For the four patients who were
lost, we completed their follow-up until their last
visit to the outpatient clinic. They had all accom-
plished the first year of the follow-up period, while
two of them had also been examined 2 years after
the operation and one at the third-year appoint-
ment.
During the follow-up period, the early (within
30 days) and late postoperative morbidity and
mortality, the incidence of recurrent stenosis, and
the functional status and embedment of the BP
patch were recorded. Kaplan-Meier analysis was
used to assess survival, late neurological events,
and restenosis rates. Statistical calculations were
performed using the SPSS software program, ver-
sion 11.0 (SPSS, Chicago, IL). Statistical signifi-
cance was defined as p < 0.05.
RESULTS
During a 4-year period, 148 consecutive CEAs were
performed in 138 patients. Demographics and risk
factors of the patients are summarized in Table I. Of
carotid arteries that met the indications for CEA, 60
(40.5%) were asymptomatic and 88 (59.5%) were
symptomatic (Table II). In a subgroup of 18 (13%)
patients (19 carotids), the CEA procedure was
combined with coronary artery bypass grafting
(CABG) or aortic valve replacement (AVR). The
indication for CEA in this group was symptomatic
carotid disease in eight patients [three transient
Vol. 20, No. 5, 2006
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ischemic attacks (TIAs), five strokes] and asymp-
tomatic high-grade stenosis in 10 patients (one
asymptomatic patient underwent bilateral CEA
combined with AVR). Overall, in nine patients, the
contralateral carotid artery was completely oc-
cluded. Ten patients (7.2%) had bilateral carotid
artery stenosis, and bilateral CEA was performed in
two stages, except for the patient mentioned above
with bilateral CEA combined with AVR. Three
CEAs were performed on an emergency basis due
to crescendo TIAs in two patients and a stroke in
evolution in one patient. The diagnosis of carotid
artery disease was confirmed by digital subtraction
or CT angiography in 21 and 70 patients, respec-
tively. Low internal carotid stump pressure neces-
sitated the use of a shunt in 23 patients (15.5%).
The median occlusion time of the common carotid
artery was 35 min (interquartile range 28-40).
Even though the hemostasis time for the BP patch
was not calculated, it has to be mentioned that we
experienced no significant bleeding from the suture
line. In fact, in most cases, there was no bleeding at
all at the time of restoring the circulation.
During the early postoperative period, there
were no wound complications. Perioperative mor-
bidity consisted of minor complications in seven
patients (4.7%), who presented transient cranial
nerve paresis concerning the hypoglossal (n = 4)
and the inferior laryngeal (n = 3) nerves. All these
nerve injuries were reversed within the following
6-month period. Regarding major complications,
there were no deaths in this series, but two patients
(1.4%) developed a postoperative stroke. The first
stroke presented as a leg hemiparesis in a symp-
tomatic (TIA) diabetic patient with contralateral
occlusion and 90% ipsilateral stenosis. The neuro-
logical event occurred 4 hr after the end of the
procedure, while the patient had an uneventful
recovery. At reexploration, the internal carotid ar-
tery was patent and remained so for a 33-month
period thereafter. The CT scan was negative, so it
was considered a lacunar stroke. The patient
recovered well and is able to walk without help.
The second stroke related to a patient with history
of severe coronary artery disease and multiple re-
peated crescendo TIAs within the previous 8 days.
Both duplex examination and CT angio revealed
high-grade ipsilateral carotid stenosis (>90%).
Twelve hours after the CEA and while he had an
uneventful recovery, he had an episode of parox-
ysmal atrial fibrillation, resulting in an ischemic
stroke affecting the whole ipsilateral hemisphere.
The patient presented with hemiplegia and aphasia.
The internal carotid artery was thrombosed, but
reexploration was not attempted because of his
severe condition and the multiple lesions he had in
the intracranial internal carotid artery. Twelve
months later, the patient is alive and able to walk
but still suffering from aphasia.
The median postoperative hospitalization was 3
days (interquartile range 3-6, range 2-23). The
median follow-up time was 20 months (inter-
quartile range 11-33, range 3-52). During the fol-
low-up period, three patients (2.2%) died. Two
deaths were due to cardiac disease, while the other
resulted from contralateral stroke due to atrial
fibrillation. Cumulative survival in this series was
estimated to be 86.7% at 48 months using Kaplan-
Meier analysis (standard error <10%, survival
curve not shown). The incidence of late neurolog-
ical events was 1.4% (two patients). As already
mentioned, in one patient that stroke proved to be
fatal. The other stroke was also attributed to the
contralateral carotid artery. The cumulative neu-
rological event-free rate was estimated to be 95.4%
at 48 months (standard error <10%, neurological
event-free rate curve not shown). Cumulative
Table I. Patients’ demographics and risk factors
Patients (n)
Gender
Male
Female
Mean age (± SD, years)
Range (years)
Smoking
Nonsmokers
Quit
Active
Hypertension
Diabetes
Dislipidemia
CAD
PAD
COPD
138
113 (81.9%)
25 (18.1%)
69.4 (±7.7)
43-83
34 (24.6%)
36 (26.1%)
68 (49.3%)
112 (81.2%)
40 (29%)
90 (65.2%)
90 (65.2%)
31 (22.5%)
22 (15.9%)
SD, standard deviation; CAD, carotid artery disease; PAD,
peripheral artery disease; COPD, chronic obstructive pulmonary
disease.
Table II. Presentation of carotid artery disease
according to neurological status
Frequency%
Asymptomatic
Symptomatic
Stroke
TIA
Amaurosis fugax
Global ischemia
60
88
39
37
9
3
40.5
59.5
26.4
25.0
6.1
2.0
616
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neurological event-free survival was estimated to
be 86.1% at 48 months (standard error <10%,
neurological event-free survival curve not shown).
Follow-up color duplex scans revealed restenosis
(>50%) of the carotid artery in three patients
(2.0%). The first patient was operated for asymp-
tomatic restenosis (>90%) of the carotid artery after
a previous eversion CEA in another hospital. The
12-month duplex scan showed a restenosis of about
50%, which remained unchanged for the following
20 months. The second patient, who underwent
combined CEA and CABG, presented with asymp-
tomatic total occlusion in the 3-month follow-up.
The third patient presented with restenosis, which
began at 18 months and rapidly progressed to total
occlusion. She was also asymptomatic. A thorough
review of this case revealed a second-degree rela-
tionship to the first patient with restenosis and a
history of familial hypercholesterolemia in both of
them. The cumulative restenosis-free rate in our
study group was estimated to be 97.2% at 48
months using Kaplan-Meier analysis (standard er-
ror <10%, Fig. 1). There was no aneurysm forma-
tion at the CEA site, and the BP patch seemed to be
well incorporated with the rest of the carotid artery
in all cases. In most of them, it appeared as a thin
echogenic line mainly seen in the carotid bulb but
rarely visualized in the internal carotid artery,
having the ultrasound characteristics of a vein
patch.
DISCUSSION
The best method for arterial closure after conven-
tional CEA with longitudinal arteriotomy remains
controversial. Patch angioplasty of the arteriotomy
has been suggested by prospective randomized tri-
als to be superior to primary suture for preventing
both perioperative neurological events and recur-
rent carotid stenosis.7,9,11AbuRahma et al.,11in a
well-designedprospective
compared primary closure to patch angioplasty in
bilateral CEAs in the same patient and showed the
superiority of patching angioplasty. Additionally, in
a recent review, the authors stated that, despite the
limitations of the data, the results appeared to favor
the routine use of patching.9Advocates of patch
angioplasty suggest that increasing the carotid lu-
men improves the blood flow characteristics and
decreases the amount of intimal hyperplasia, fac-
tors which are related with early and late resteno-
sis.5,7
Bond et al.,12in a systematic review, assessed
the safety and efficacy of different types of mate-
rials (vein and synthetic) used in carotid patch
angioplasty. The differences between the compared
patches were small and nonconclusive of the best
one. Quite recently, a small number of studies re-
ported that a biological material, derived from BP
and already known from cardiac surgery, could be
an alternative patch in CEA.13-17Biasi et al.,14
presenting their 9-year experience with BPPA,
summarize the advantages of BP. It is available at
any time, is easy to handle, and can be tailored to
the appropriate dimensions. It does not require
additional operation time to be harvested like the
vein patch. It has similar consistency to the artery,
low thrombogenic inner surface, and excellent host
tissue response and does not stimulate an inflam-
matory reaction due to its acellular conformation.14
Additionally, aneurysmal dilatation of the BP is
very rare: only two cases have been reported so
far.19,21In contrast, aneurysmal formation at the
site of the anastomosis has been reported as a
randomizedstudy,
Fig. 1. Cumulative restenosis-free
rate (standard error <10% for the
entire follow-up period). CAs,
carotid arteries.
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possible complication in both vein and synthetic
patches.14,22,23Thus, the BP patch has all the
advantages of the autologous vein, giving also the
benefit of sparing the vein for future use in CABG
or peripheral vascular bypass grafting, the likeli-
hood of which is high in this group of patients. On
the other hand, compared to synthetic patches, the
BP patch is more compliant to needle expansion,
which could result in less suture line bleeding, less
thrombogenic surface, and better endothelializa-
tion pattern.14,17Finally, it is available at a rea-
sonable cost comparable with that of synthetic
material.
During the last 4 years, we have adopted BPPA
as the standard procedure in all our cases of CEA.
Our series represents the second largest experience,
after that of Biasi et al.,14including 148 CEAs
performed in 138 patients. The handling charac-
teristics of the BP provided the advantage of easy
application and suturing. Consequently, the med-
ian carotid occlusion time in our series was mini-
mized to 35 min, which is less than in any previous
report.14,15,22This study includes mostly elective
cases but also emergency cases, cases with com-
bined treatment of cardiac disease, and between
them cases with contralateral carotid occlusion.
Thus, it is possible that in some patients hemody-
namic status during or after the operation might
have been affected to some level. In spite of this
fact, the surgical outcome and complication rate
were kept at low levels and comparable to the re-
lated studies.14-18In the early postoperative period,
we had no wound complications (hematoma,
infection), which was in part due to meticulous
hemostasis, low suture line bleeding, and probably
resistance of the BP patch to infection. The inci-
dence of cranial nerve injuries (4.7%) was within
the acceptable published range.1-3There was no
death and only one of the two postoperative strokes
could be attributed to the CEA, though there was
coexistent cardiac arrhythmia. These data show
that the BPPA site remains patent, protecting the
carotid bifurcation from an early acute thrombosis.
The good surgical outcome was maintained in
the majority of patients during the follow-up peri-
od. The BP patch incorporated well with the carotid
artery, having the characteristics of a vein patch in
ultrasound examination, while there were no cases
of BP patch aneurysmal dilatation or rupture,
which is in agreement with the other published
studies.13-18During the follow-up period, three
patients died, but the cause of death was irrelevant
to the CEA. Similar late death rates have been re-
ported by all BP-favoring authors.13-18Reevalua-
tion of the carotid artery patency with color duplex
in fixed time periods showed that only three CEAs
(2%) had significant restenosis. The degree of
restenosis was 50% in one patient, and total
occlusion in the other two patients. The time of
diagnosis was 12, 3, and 18 months, respectively.
The 50% restenosis appeared in a patient who was
reoperated due to recurrent stenosis after eversion
CEA elsewhere. The second-degree relationship
with the second patient who developed total
occlusion at 18 months postoperatively and the
background of familial lipid disorder might have
been predisposing factors in restenosis occurrence.
The restenosis rate is reported to be relevant to the
patch material, ranging 0–13%.24
showed a favorable restenosis rate when compared
with recent publications regarding BPPA (1.2-
5.4%).14-16,18
Our results
CONCLUSION
Our experience with the routine use of BP as a
patch material in CEA is promising. We especially
appraised the accessibility, handling characteristics,
durability, and excellent incorporation of this
material. Overall, BP shares the advantages of both
vein and synthetic material, without having most
of their limitations. Additionally, by performing the
BPPA, we valued the low morbidity and mortality
rates regarding either the perioperative or the mid-
term outcome. Since no study has reported signif-
icant differences between the patch materials used
in CEA, our results indicate that BP may be a
suitable material for routine use in carotid surgery.
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