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The preliminary results of combined carotid endarterectomy and off-pump coronary
artery bypass grafting in patients with carotid and coronary artery disease
CHEN Xujun1, CHEN Xin1,XIE Donghua2, SHI Kaihu1, and XU Ming1
Department of Thoracic & Cardiovascular Surgery, Nanjing First Hospital affiliated to
Nanjing Medical University, Nanjing 210006, Jiangsu, China1

Division of Cardiovascular Medicine and Department of Medicine, Duke University
Medical Center, Durham, USA2
Correspondence to: Dr. CHEN Xujun, Department of Thoracic and Cardiovascular Surgery,
Nanjing First Hospital affiliated to Nanjing Medical University, Nanjing 210006, Jiangsu, China
Fax: 86-25-52247821
Telephone: 86-25-52247821
E-mail: [email protected]
1
Key words ：coronary artery bypass grafting ; endarterectomy, carotid； coronary artery disease；
carotid artery stenosis
ABSTRACT
Background Coronary and carotid artery diseases frequently coexist and patients with concomitant
significant disease of coronary and carotid arteries remain at high risk of perioperative stroke and myocardial
infarction after coronary bypass surgery. The aim of this study was to investigate the effect of combined
carotid endarterectomy (CEA) and off-pump coronary artery bypass grafting on patients with carotid and
coronary artery disease.
Methods
Consecutive patients with carotid and coronary artery disease underwent one-staged
unilateral CEA and off-pump coronary artery bypass grafting between January 2002 and December 2007 in
our heart institute. Perioperative complications including neurological events or major adverse cardiac
events were assessed and follow-up was carried out.
Results A total of 51 cases of isolated off-pump coronary artery bypass grafting and unilateral CEA
including 34 right and17 left was performed. Mean blocked time of carotid artery in CEA was 25.5 ± 7 mins.
Mean number of distal grafts per patient was 3.30 ± 0.45. Mean ventilation time，ICU stay and postoperative
hospital stay were 11.3±5.4 hours，2.1 ± 0.9 days and 12.5 ± 6.1days respectively. None of the patients had
stroke or myocardial infarct and there was one perioperative death due to acute cardiac failure, with
operative mortality of 1.96%. Follow-up was complete in 47 patients (92.16%). After mean follow-up of
39.5 ±12.5 months (6～73 months) , none of patient manifested with stroke , new angina or new-born
cardiac infarct and there was also no late death.
Conclusions Concomitant off-pump coronary artery bypass grafting and CEA is a safe and effective
procedure in selective patients with significant carotid and coronary artery disease.
2
As a result of systemic disease for atherosclerosis, coronary and carotid artery diseases frequently
coexist. The presence of more than 50% carotid artery stenosis in patients undergoing coronary artery
【1】
bypass grafting (CABG) has been reported in the literature to be as high as 22%
【2】
75% has to be 1.7% to 12％
and that of more than
【3】
. Among the patients undergoing carotid endarterectomy (CEA), 28%
of
them had severe coronary artery disease which was indicated for CABG. As a severe complication of
CABG, stroke was reported to be associated with high morbidity and mortality after surgery. Carotid artery
stenosis has been shown as the most powerful predictor of perioperative stroke in patients undergoing
CABG and the reported studies showed that CEA could result in a decreased incidence of stroke for
【3-4】
CABG
. Therefore, we performed combined CEA and off-pump CABG in 51 consecutive patients with
carotid and coronary artery disease between January 2002 and December 2007 and good results were
achieved.
METHODS
Patients
From January 2002
to December 2007, fifty-one consecutive patients were subjected to the combined
CABG and CEA in our heart institute, 35 male and 16 female, with a mean age of 67.2±7.7years old . Basic
demographic data of patients was shown in Table 1.
Definitions
Patients were categorized as symptomatic or asymptomatic in neurological status. Symptomatic
patients included those who had history of transient ischemic attack, amaurosis fugax or complete stroke.
Asymptomatic patients had no evidence of neurological findings. Transient ischemic attack was defined as
【5】
focal cerebral dysfunction of presumed vascular origin that resolved completely within 24 hours
【5】
，stroke
was as focal or global cerebral dysfunction of presumed vascular origin lasting more than 24 hours,
【5】
perioperative neurologic events
were as transient ischemic attack, reversible ischemic neurologic deficit,
or complete stroke within 30 days of the operation, perioperative myocardial infarction was as either new
Q waves, more than 10% elevation of myocardial band, fraction of creatinine phosphokinase, or new wall
【5】
motion abnormality on echocardiogram, major adverse cardiac events
( MACEs) were as death from any
【6】
cause, nonfatal repeat acute myocardial infarction, and needed revascularization, and operative mortality
was as any death occurring within 30 days of the operation or death during the same hospital admission as
the operation.
Patient selection and surgical indication
【7】
According to guideline for CEA as described by Biller J and colleagues
, the patients with
coronary and carotid artery diseases with following surgical indication were enrolled in the present study
when: (1) unilateral carotid stenosis ≥50% with symptoms of TIA and ischemic stroke and /or history of
3
cerebral accident or unilateral carotid stenosis ≥75% occurred; (2) It was showed by selective coronary
angiographies that two-vessel or three vessel disease with stenosis ≥75%, with diameter ≥1.5 mm in
targeted coronary artery, and with left ventricular ejection fraction ≥0.40 happened.
Patients requiring emergency surgery , patients with left ventricular ejection fraction (LVEF)<40% ,
patients with small size（＜1.5 mm）in targeted artery , patients with severe left main disease， patients
with heart valve disease or aneurysm needed to be surgically treated , and patients with severe bilateral
carotid stenosis ≥75%, and patients with the European System for Cardiac Operative Risk Score
（Euroscore） >10 were excluded in the present study.
Preoperative Screening of carotid artery stenosis
All patients scheduled for CABG were screened for carotid disease. Carotid screening was performed
firstly by duplex ultrasonography,
then followed by computer tomography angiography（CTA） in case
the initial screen indicated significant disease，according to a predefined paradigm as depicted in Figure 1.
CTA was used to evaluate the accurate degree and location of carotid stenosis. Lastly，transcranial
doppler sonography （TCD）was necessarily performed to show the stenosis of intracranial segment of
inner carotid artery and collateral circulation between intracranial artery and carotid artery for patients
with positive CTA examination. It was defined positive when carotid stenosis showed by duplex
ultrasonography was more than 50%，when unilateral carotid stenosis was more than 50% showed by CTA
with symptoms of TIA or ischemic stroke and /or history of cerebral accident or when unilateral carotid
stenosis was more than 75%，and when TCD-showed more severe stenosis in intracranial segment of
internal carotid artery than extracranial or poor collateral circulation between intracranial artery and
carotid artery occurred in the study.
Surgical approach
Informed consent was obtained from each patient with respect to the surgical method.
Technique of CEA
All patients received general anesthesia with tracheal intubations. Combined CABG/CEA operation
was conducted by one team. CEA was performed before CABG, but after harvesting the conduits of radial
artery and saphenous vein as previously described
【8-9】
. The patient was prepped, with his head turned to
the contralateral. An incision of 8-10 cm was made parallel to the anterior border of the
sternocleidomastoid muscle. The carotid sheath was opened and the common carotid artery, internal
carotid artery, and the external carotid artery were exposed，mobilized, taped and clamped while the
patient was heparinized by 1.5 mg per kg of heparin. Athermanous debris from the media was
meticulously removed. After thoroughly irrigation of the lumen and homeostasis，the arteriotomy was
closed either by direct suture or by a SV patch or polytetrafluoroethylene patch. The neck wound was left
open until the heparin was reversed with protamine after CABG and then was closed with drainage of
4
rubber-tissue.
Grafting strategy and off-pump CABG
Left internal mammary artery (LIMA), the SV and radial artery (RA) were routinely harvested as
【9】
previously described
. Off-pump CABG was performed through the procedure of full median sternotomy
or inferior mini-sternotomy. Target artery immobilization and regional myocardial control were achieved
through a commercially available Stabilizer (Octopus，Medtronic or CTS，Cardiothoracic Systems ) in
which intraluminal shunt and a CO2 blower was routinely used for anastomosis. The distal anastomosis
was constructed with continuous 7-0 polypropylene and the proximal was with 6-0 polypropylene. A 4.5
mm opening was created with puncher in the ascending aorta. Aortic connector (Enclose, St Jude Medical)
was applied when a patient's aorta was severely calcified. After side clamp was released, diltiazem was
-1
-1
-1
intravenously delivered with a dose of 0.3 to 0.5 µg ·min ·kg and daily use of 90 mg was taken for 3-6
months postoperatively and continuously for patients with RA conduits.
Postoperative treatment and Postoperative complication
Neck wound was compressed with sand bag. Dehydration with mannitol or glycerol and fructose was
routinely used and reactive hypertension was controlled in intensive care unit. Electrocardiography was
used to detect angina and myocardial infarct postoperatively on day 1, day 2 and day 5 respectively.
Postoperative complication including neurological or cardiac events was assessed and morbidity as well as
mortality was calculated. At discharge，carotid CTA was again performed to examine
the surgically
treated carotid artery for possible residual stenosis.
Follow-up
After hospital discharge, follow-up was performed by way of clinic visit at the outpatient once a month
for 1 year and thereafter once per 3 months. All patients underwent electrocardiography and
ultrasonography at the outpatient and dynamic and loaded electrocardiography was employed to check for
suspected patients to identify myocardial ischemia. Survival and any cardiac events (recurrent angina,
myocardial infarction and congestive heart failure) or neurological status were assessed.
Statistical analysis
All data were expressed as mean and standard deviation. The left ventricular ejective fraction and
New York Heart Association classifications were statistically compared by means of the paired Student's
t-test. Computations were performed with software SPSS 11.0.
RESULTS
A total of 51 cases of isolated off-pump CABG and unilateral CEA including 34 right and17 left
was performed. Fifty one distal anastomoses were done with the LIMA，47 with the RA and 91 with the
SV. Mean number of distal grafts per patient was 3.30 ± 0.45. Mean time of blocked time of carotid
5
artery in CEA was 25.5±7 mins. A total of direct closure of arteriotomy was in 10 patients. Carotid
patching was used with SV in 34 patients and with polytetrafluoroethylene patches in 7. All thickened
intima and atherosclerotic plaque in carotid stenosis was thoroughly released.
IABP was delivered to 7
patients, pre-operatively in 4 and intra-operatively in 3. There was no evidence of neck hematoma that
would have needed re-exploration or neck wound infection. Mean intubation time，ICU Stay and
postoperative hospital stay were 11.3±5.4 hours,2.1 ± 0.9 days and 12.5 ±6.1days respectively.It was
showed by CTA that there was obvious improvement of carotid stenosis after operation at discharge than
that of pre-operation as shown in Figure 2 and Figure 3.
None of the patients had stroke and myocardial infarction. Only 1 patient in the present group died
due to acute cardiac failure, with operative mortality of 1.96%. Two patients manifested with atrial
fibrillation and recovered in 2 days. One patient experienced acute renal function failure, with full
recovery after an early dialysis.
Complete follow-up information was obtained in 47 patients , with mean time of 39.5±12.5 months
(6～73 months) and there was no late death, stroke，new angina and new-born cardiac infarct .
Postoperatively at 6 month, mean LVEF had increased to 0.51 ±0.12, compared to that of 0.43 ± 0.11
preoperatively (P = 0.027). Forty-one patients were in New York Heart Association class II and 6 in III.
Mean New York Heart Association class was 1.52 ± 0.50 postoperatively at 6 month, compared with that
of 3.0 ± 0.4 preoperatively (P = 0.003).
DISCUSSION
There continues to be a dilemma regarding the best means of surgical management of significant
carotid artery disease in patients requiring coronary artery bypass surgery. Staged, synchronous, and “reverse
staged” procedures
[2]
are among the approaches used in this type of patients. In a staged procedure, the
carotid lesion is corrected first and the coronary bypass performed subsequently following a variable time
interval. A “reverse” staged procedure corrects the coronary ischemia by CABG followed by subsequent
CEA under a separate anesthetic. One-staged procedure or combined surgery，initiated by Bernhard and
colleagues
【10】
in the year of 1972， is performing CEA, immediately followed by CABG under the same
anesthesia. The main advantage of the one-staged procedure was that a decreased incidence of stroke and
【5-6】
mortality could be achieved for patients with coronary and carotid artery diseases in some recent studies
【11】
although an earlier study by Hertzer and colleagues
，
reported an elevated stroke and mortality rates after
the combined approach. It was also showed in the present study that none of the patients had stroke or
myocardial infarct and operative mortality was 1.96%, obviously lower than others
【5-6】
，suggesting that
combined surgery should be preferred for patients with coronary artery and carotid disease. The other
advantage of one-staged procedure involved shorter hospital stay and decreased costs
【12-13】
as a result of a
combined procedure performed under the same anesthetic.
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The possible reasons why good results could be achieved in the present study are as following:
(1) Isolated off-pump CABG. It has been widely accepted
【14】
that off-pump CABG could give rise to
lower incidence of stroke than on-pump CABG as a result of less embolism from aortic manipulation and
freedom of embolism from extracorporeal circulation, could avert cerebral hypoperfusion due to hypotension,
and could also give additional benefits of decreased morbidity in terms of blood loss, use of blood and blood
products, of shorter intensive care unit stay and hospital stay. Moreover, it was demonstrated in the
【6】
controlled study
that stroke in combined off- pump CABG/CEA was obvious lower than on-pump
CABG/CEA . Only unilateral CEA performed in our study could be responsible for shorter time of CEA
operation, which could result in low incidence of stroke and mortality. We perform CEA before CABG. This
has the advantage of avoiding the negative effects of hemodynamic disturbances during OPCAB on carotid
circulation. Maintenance of perioperative hemodynamic stability and effective operative management is
important during the procedure. We maintain the systolic pressure above 100 mm Hg during CABG, using
inotropes whenever necessary. The conduits are harvested before CEA. This avoids the total heparinization
time and avoids excessive operative bleeding.
(2) Appropriate treatment of arteriosclerosis of the ascending aorta. Arteriosclerosis of the ascending
aorta is an important risk factor
【15】
for cerebral embolism and stroke in coronary bypass surgery. Carotid
stenosis and ascending aortic atherosclerosis sometimes coexisted in CABG candidates and carotid stenosis
【15】
was also one of the risk factors of ascending aortic atherosclerosis
. In the present study, 31.37% (16/51)
patients were found to have concomitant arteriosclerosis of the ascending aorta. Use of aortic connector in
【16-17】
CABG was reported to contribute to a decreased incidence of strokes after surgery in some studies
.
Enclose aortic connectors were applied in 13.73% patients with severely calcified aorta, which might likely
lead to fewer strokes in our study. Sequential and Y-graft grafting techniques among RA, SV and LIMA
were employed in a effort to decrease number of proximal ends in the ascending aorta in the present study
【8-9】
and this maneuver has been proved to be effective in our earlier study
.
(3) Unilateral CEA. Obviously, unilateral CEA can result in shorter blocked time of carotid artery in
CEA and so, less disturbance to blood perfusion to brain. Therefore, only unilateral CEA was performed in
our study. If bilateral carotid stenosis more than 75% existed, the stricter side was preferred to perform CEA.
(4) Strict preoperative screening and patient selection. In our experience it is mandatory to perform
preoperative screening with duplex ultrasonography, CTA and TCD for CABG/CEA candidates among
patients with coronary and carotid artery diseases. Patients with more severe stenosis in intracranial segment
of internal carotid artery than extracranial or poor collateral circulation between intracranial artery and
internal carotid artery displayed by TCD were at high risk and therefore should be excluded in order to lower
incidence of preoperative death or stoke according to our experience. It is also important and necessary for
patient selection as described in our study for off-pump CABG, in order to obtain short surgical time, stable
7
circulation status, decreased operative death and increased long-term patency of conduit. Those preoperative
screening strategy and method for patient selection might also attribute to good results in this study.
The other important highlights to obtain good results in the present study in our experience were: (1)
maintenance of higher blood pressure in the process of CEA. Generally, we maintain the systolic pressure
above 100 mm Hg and averaged arteral pressure ≥ 20%~30% of that of pre-operation in CEA operation,
【5-6】
using inotropes whenever necessary. This maneuver has been considered as a routine by most surgeon
to
avert the occurrence of brain ischemia in CEA. (2) Control of hypertension and routine brain dehydration
after surgery. One of the most important risk factors after carotid endarterectomy is hypertension. Poorly
controlled hypertension increases the risk of postoperative complications, including neck hematoma and
【18】
hyperperfusion syndrome. Bove and colleagues
reported a 19% incidence of postoperative hypertension
after carotid endarterectomy and noted a 10% incidence of fixed neurological deficits in these patients.
【19】
Caplan and colleagues
reported an increased risk of intracerebral hemorrhage after carotid endarterectomy
when uncontrolled postoperative hypertension persisted. Thus, it is an important aspect to control blood
pressure after surgery in orders to minimize neurological complications and mortality. Brain dehydration
therapy with mannitol or glycerol and fructose and low-dose dexamethasone of daily 5mg for 3 days was
also imperative and helpful for patients with long history, severe stenosis in carotid artery, advanced age or
severe hypertension in our experience. (3) Freedom from shunt in CEA operation. Although some surgeons
【20-21】
recommended that intravascular shunt should be used to protect brain ischemia in high risk patients,
we do not use it in order to prevent any possible embolus during insertion of the shunt. Similarly, it was also
demonstrated by Eern and colleagues
【 22 】
that good results could be achieved in CEA without any
intravascular shunt. Moreover，short blocked time of 25.5±7 mins of carotid artery in CEA in the present
study could avoid the need of any intravascular shunt according to our experience.
The main limitation of the present study is associated with relatively small sample size of patients
subjected to combined surgery and the inclusion of patient is strictly selected in our study. This is a result of
the single-center design of the study itself, which is another limitation.
In summary, concomitant off-pump CABG and CEA is a safe and effective procedure in selected
patients.
REFERENCES
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Huh J, Wall MJ Jr, Soltero ER. Treatment of combined coronary and carotid artery disease. Curr
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Brown KR. Treatment of concomitant carotid and coronary artery disease. Decision-making
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10
Table 1
Demographic clinical characteristics of 51 patients
Variable
Patients (%)
Males
35 (68.6)
Females
16 (31.4)
Age (years)
67.2±7.7
Unstable angina
100 (51)
Previous myocardial infarction
41.2 (21)
Heart function（New York Heart Association）
Class Ⅰ
3 (5.9)
ClassⅡ
14 (27.5)
class III
10 (19.5)
class IV
24 (47.1)
Diabetes mellitus
Hypertension
19 (37.3)
Hypercholesterolemia
23 (45.1)
Chronic obstructive pulmonary disease
49 (96.1)
5 (9.8)
Chronic renal insufficiency
10 (19.5)
Neurological history
Asymptomatic
7 (13.7)
Transient ischemic attacks
9 (17.6)
Reversible neurological deficit
8 (15.7)
Permanent stroke
27 (52.9)
Peripheral vascular disease,
10 (19.6)
coronary angiography
Left main disease
One-vessel disease
Two-vessel disease
Three-vessel disease
Mean left ventricular ejective fraction
carotid stenosis (>75%)
Left
Right
4 (7.8)
2 (3.92)
12 (23.5)
37 (72.6)
0.43 ± 0.11
21 (41.2)
30 (58.8)
11
coronary heart disease for off-pump CABG
(＋)
carotid duplex ultrasonography
ultrasonography
ultrasonography
(－)
carotid CTA
(－)
(＋)
TCD
(＋)
(－)
off-pump CABG/CEA
off-pump CABG
Figure 1 Screening strategy for combined off-pump CABG and CEA. TCD:
transcranial doppler sonography; CTA: computer tomography angiography.
12
Figure 2.
Figure 3
narrowed carotid artery demonstrated by CTA before CEA (black arrow)
widened carotid artery demonstrated by CTA after CEA (black arrow)
13