Simultaneous Hybrid Revascularization by Carotid Stenting and Coronary Artery Bypass GraftingThe SHARP Study
Francesco Versaci, MD*,
Bernhard Reimers, MD ,
Costantino Del Giudice, MD ,
Joachim Schofer, MD||,
Alessandro Giacomin, MD,
Salvatore Saccà, MD,
Roberto Gandini, MD ,
Remo Albiero, MD¶,
Antonio Pellegrino, MD,
Fabio Bertoldo, MD,
Giovanni Simonetti, MD,
Luigi Chiariello, MD,*
* Divisione di Cardiologia, Università Tor Vergata, Rome, Italy
Divisione di Cardiochirurgia, Università Tor Vergata, Rome, Italy
Dipartimento di Diagnostica per Immagini e Radiologia Interventistica, Università Tor Vergata, Rome, Italy
Dipartimento Cardiovascolare, Ospedale Civile di Mirano, Venice, Italy
|| Heart Center, Hamburg, Germany
¶ Clinica San Rocco di Franciacorta, Ome (Brescia), Italy
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Abstract
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Objectives: In an attempt to reduce post-operative events we investigated a new therapeutic strategy consisting of a simultaneous hybrid revascularization by carotid artery stenting (CAS), immediately followed by an on-pump coronary artery bypass graft (CABG).
Background: Preventing stroke and cardiovascular events after coronary artery revascularization in patients with elevated surgical risk is a complex and multifaceted problem.
Methods: One hundred-one consecutive patients with severe carotid and coronary artery disease and a standard EuroSCORE  5 were included in this multicenter study. Immediately after CAS, patients underwent CABG. The primary end point was the incidence of stroke, acute myocardial infarction (AMI), or death at 30 days. Secondary outcomes were transient ischemic attacks; major local complications; bleeding and systemic complications within 30 days after treatment; and any stroke, AMI, or death occurring from the 31st day to the end of the 12-month follow-up. All clinical outcomes were assessed by an independent monitoring board.
Results: The rate of procedural success was 98%. The 30-day cumulative incidence of disabling stroke, AMI, or death was 4%: 2 patients died (2%) in the post-operative period, and 2 patients (2%) had a stroke immediately after CAS and before CABG. Three patients died from the 31st day to the 12th month after the procedure.
Conclusions: Our findings indicate that in high-risk patients with coronary artery disease suitable for CABG and carotid artery disease, the hybrid revascularization by CAS immediately followed by CABG is a promising and feasible therapeutic strategy.
Key Words: carotid arteries • coronary artery bypass grafts • new technology • stents • surgery complications
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Abbreviations and Acronyms
| | AMI = acute myocardial infarction | | CABG = coronary artery bypass graft | | CAD = coronary artery disease | | CAS = carotid artery stenting | | CEA = carotid endarterectomy | | CT = computed tomography | | EuroSCORE = European system for cardiac operative risk evaluation | | TIA = transient ischemic attack |
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The optimal management of patients with concomitant coronary and carotid artery disease is not known (1–4). The importance of this clinical problem is accentuated by the finding that patients frequently present atherosclerosis of both arterial systems: 8% to 14% of coronary artery bypass graft (CABG) patients have significant carotid artery stenosis (5), and 40% to 50% of carotid endarterectomy (CEA) patients have coronary artery disease (CAD) (6,7).
Among patients undergoing CEA in the Veterans Affair Cooperative Study (8) and the ACAS study (Asymptomatic Carotid Atherosclerosis Study) (4), 20% and 49% of deaths, respectively, were due to cardiac causes. Similarly, the incidence of perioperative stroke in patients undergoing CABG is elevated in those with concomitant severe carotid artery stenosis (4).
The combined surgical approach is associated with an increased risk of mortality and morbidity (5,9–11). In the staged surgical approach that addresses the carotid artery lesion with CEA first, followed within several days to several weeks by CABG, the incidence of perioperative stroke during CABG is reduced. However, the risk of acute myocardial infarction (AMI) during CEA and in the period preceding CABG is rather high (5,9,10). Carotid artery stenting (CAS) with cerebral protection devices is rapidly evolving as an alternative to CEA (12), mainly for patients with severe carotid artery stenosis at high surgical risk, such as patients with CAD (13). A staged CAS-CABG approach has been recently proposed, but the need for a dual antiplatelet aggregation therapy lasting 3 to 4 weeks after stenting might represent a limitation for CABG (14).
We recently proposed a new therapeutic strategy consisting of a simultaneous hybrid complete revascularization by CAS, immediately followed by on-pump CABG. Such an approach has the potential to minimize the incidence of cardiac events in patients at high surgical risk (15). In a subsequent larger study we demonstrated the feasibility of this therapeutic option (16). We carried out the prospective SHARP (Simultaneous Hybrid Revascularization by Carotid Artery Stenting and Coronary Artery Bypass Grafting) study to demonstrate the potential clinical applicability of this approach as an alternative to the combined or staged strategies currently adopted.
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Methods
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The study was conducted in 4 high-volume centers: Tor Vergata University Hospital, Rome, Italy (coordinating center); Ospedale Civile di Mirano, Venice, Italy; Heart Center, Hamburg, Germany; and Clinica San Rocco di Franciacorta, Ome, Italy. Only experienced cardiac surgeons (more than 300 CABG procedures performed/year) and interventional cardiologists or radiologist (more than 150 CAS procedures performed as primary operator and more than 50 CAS in the last 2 years) were involved in the study. The protocol was approved by the local institutional ethics committee, and all the patients provided written informed consent.
A team of physicians composed of neurologist, anesthesiologists, cardiac surgeons, and interventional physicians was assembled. The neurologist was responsible for the initial evaluation and neurological follow-up of the patients. An independent data and safety monitoring board of each center, not affiliated with the study investigators, reviewed clinical data to identify safety concerns. The monitoring board in each center was also responsible for selecting all patients with eligible criteria to be included in the registry.
Patients.
Patients were eligible if they were 18 years of age or older, had concomitant critical carotid and coronary disease with coronary arteries impossible to revascularize percutaneously, and were suitable for CABG. All patients had a surgical risk expressed as Standard European system for cardiac operative risk evaluation score (EuroSCORE) 5 (17,18), a carotid artery stenosis 50% in the symptomatic disease or 80% in asymptomatic disease, as determined by the NASCET (North American Symptomatic Carotid Endarterectomy Trial) criteria (19). The presence of carotid artery stenosis was evidenced by echocardiography duplex scanning, then confirmed by catheter angiography and either magnetic resonance angiography or computed tomography (CT) scan angiography. A CT scan with or without angiographic dye, depending on preprocedural serum levels of creatinine, was performed in all patients to provide the maximum information regarding the aortic arch, the extent of aortic disease, and the brain (Fig. 1). In case of bilateral carotid artery stenosis, the choice of the carotid artery to treat was made according to clinical criteria or to the severity and morphology of plaque in case of asymptomatic patients.
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Figure 1 Multidetector CT Scan of Epiaortich Vessels
An electrocardiographic, gated, 64-multidetector computed tomography (CT) scan is performed to provide the maximum anatomical information regarding the aortic arch, the amount of calcium, epiaortich vessels, and intracranial circulation. (A) A CT volume rendering shows a type III aortic arch. (B) Anatomical intracranial circulation. (C, D) Both carotid arteries are involved in critical ulcerated stenosis.
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Exclusion criteria were: coagulopathy; intolerance to heparin, aspirin, ticlopidine, or clopidogrel; ischemic stroke within the previous 6 weeks; presence of intraluminal carotid artery thrombus; peripheral vascular disease precluding use of catheter-based techniques; intracranial aneurism more than 9 mm in diameter; concomitant aortic and valve disease or hemodynamically significant valvular heart disease; life expectancy of <1 year; or pregnancy.
Clinical evaluation.
Exertional angina was classified according to the Canadian Cardiovascular Society classification (20). Patients were classified as having unstable angina according to Brauwald's criteria (21). Patients were classified as having had an AMI if they had definite electrocardiographic changes and documentation of abnormal cardiac enzyme levels (22). Patients were classified as having had a stroke according to the World Health Organization Task Force on Stroke and other Cerebrovascular Disorders (23).
CAS and CABG.
The CAS procedures were performed under local anesthesia through a percutaneous transfemoral access with the use of stents and protection devices approved by the Accreditation Committee. An introducer sheath was positioned in the femoral artery, and heparin (1 mg/kg) was administered intra-arterially as a bolus. Then a guiding catheter was placed in the common carotid artery, proximally to the bifurcation. A distal filter protection was used in all patients. If needed, the lesion was pre-dilated after the placement of the protection device. After deployment, stents were post-dilated to achieve a residual stenosis  30%. During and after CAS pressure monitoring was obtained to prevent hyperpefusion syndrome. At the end of the procedure, patients were transferred directly to the operating room for CABG. Surgeons performed CABG procedure according to standard practice. All CABG were performed on normothermic cardiopulmonary bypass with warm blood cardioplegia as myocardial cardioplegic protection.
Periprocedural pharmacological protocol.
Aspirin 100 mg once daily was started at least 3 days before CAS and daily after combined procedure was performed. As previously mentioned, heparin was administered 1 mg/kg as a bolus intra-arterially immediately before the stent implantation procedure and in the operating room before the cardiopulmonary bypass 2 mg/kg as a bolus. Activated clotting time (ACT) was checked every 30 min and was constantly maintained 250 s until the CABG procedure and 480 s until the end of the cardiopulmonary bypass. Tranexamic acid (TXA) 2 g in bolus was administered as an antifibrinolytic agent over 20 min before sternotomy and then as endovenous infusion (0.5 g/h) until the patient was admitted to the post-operative intensive care unit. Clopidogrel, 300 mg as a loading dose, followed by 75 mg/day for 1 month was started in the intensive care unit via a nasogastric tube 6 h after the end of CABG surgery, providing that surgical bleeding from the thoracic drains had either definitely stopped, or when it was <50 ml/h for 3 consecutive hours from the sixth post-operative hour on.
Follow-up and end points.
Neurological evaluation, including assessment according to the National Institutes of Health Stroke Scale, the Barthel Index of functional levels in activities of daily living, the Rankin scale of functional disability and monitoring for adverse clinical events, was performed within 24 h after the procedures, daily thereafter until hospital discharge, and at 6- and 12-month follow-up visits by a neurologist (24–26).
A computerized tomographic brain scan was performed before discharge from the hospital and compared with the pre-operative CT scan. Color duplex ultrasonography evaluation was repeated before hospital discharge and at the 6- and 12-month follow-up.
The primary end point was the combined incidence of stroke, AMI, or death within 30 days after the treatment. Secondary outcomes were the incidence AMI, TIA, major local complications, bleeding and systemic complications within 30 days after the treatment and the combined incidence of stroke, AMI, or death from the 31st day to 12 months of the follow-up. The occurrence of stroke, AMI, death, and other clinical events was assessed by an independent safety monitoring board that reviewed the data periodically.
Data collection and statistical analysis.
Clinical and procedural data were updated on a specific website to be analyzed by the data coordinating center (Division of Cardiac Surgery, Tor Vergata University of Rome). The investigators had full access to all data. Carotid and intracranial arteries angiography was performed before CAS, and the results were analyzed with the use of a computerized system. The study design, all analysis, and the decision to publish were determined solely by the principal investigator and the study investigators. The analysis of immediate, 30-day, and 12-month outcomes was possible for all the patients included in the registry. Continuous variables were tested for normal distribution with the Kolmogorov-Smirnov 1-sample test. Those variables with a normal distribution were expressed as mean ± SD. Variables with a skewed distribution were logarithmically transformed for statistical analysis and were expressed as medians and interquartile range. Categorical variables were expressed as proportion and percentages. Statistical analysis was performed according to "intention to treat" analysis. Kaplan-Meier survival analysis was used to analyze event-free survival.
The SAS software (version 8.2, SAS Institute, Inc., Cary, North Carolina) was used for all the analyses. The authors vouch for the completeness and veracity of data and data analyses.
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Results
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Patients and treatment.
Between February 2006 and March 2007, 101 high-risk consecutive patients with severe carotid artery disease and CAD were enrolled in the study. At the time the procedures were performed, 26 patients (26%) had unstable angina, 41 (41%) had exertional angina class III/IV, and 16 (16%) had had a previous cerebrovascular accident. Fifty-six patients (55%) had significant bilateral carotid artery stenosis, 79 (78%) had 3-vessel CAD, and 41 (41%) had left main stem involvement. The mean Standard EuroSCORE was 8.6 ± 2.5. Other baseline clinical characteristics of the patients are reported in Table 1.
In 77 of the 101 patients (76%), the loading dose of clopidogrel was administered 6 h after the end of CABG and, in the remaining 24 patients (24%), 10 h after CABG. Procedural data are reported in Table 2.
End points.
The rate of procedural success was 98%, and the 30-day cumulative incidence of disabling stroke, AMI, or death was 4%. Two patients (2%) with severe bilateral carotid artery disease had a stroke immediately after carotid artery stent implantation, with a transient aphasia associated with mild hemiparesis in 1 patient and with paralysis of the left arm in the other patient. In these cases the cardiac surgical procedure was delayed for 2 months, after a partial functional neurological recovery was achieved. One other patient had a brief and transient post-stenting cerebral ischemia that was completely resolved by the end of the stenting procedure. This patient underwent neurological evaluation and CT scan to rule out hemorrhage before inducing general anesthesia for the planned surgical procedure.
Two patients (2%) with a standard EuroSCORE >8 died of multiple-organ failure approximately 30 days after CABG (Table 3).
The 12-month cumulative incidence of stroke, AMI, or death was 7% (95% confidence interval: 0.91 to 0.99) (Fig. 2). Secondary outcomes are reported in Table 3. In particular, 3 patients had post-operative bleeding requiring reintervention, and 1 patient had pericardial tamponade requiring pericardial drainage 4 days after CABG. Three patients died from the 31th day to 12 months after the procedures.
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Figure 2 Actuarial Event-Free Survival at 12 Months
Kaplan-Meier event-free survival in patients that underwent simultaneous hybrid revascularization by carotid artery stenting and coronary artery bypass graft surgery. The 12-month cumulative incidence of disabling stroke, acute myocardial infarction, or death was 7%. Three patients died between the 31st day and 12 months after intervention.
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The median duration of post-operative hospital stay was 9 days (interquartile range, 7 to 14 days). The median duration of intensive care unit stay was 2 days (interquartile range, 2 to 3 days), and the median ventilation time was 12 h (interquartile range, 7.3 to 13.8 h). The incidence of primary outcome events at 12 months is summarized in Table 4.
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Discussion
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Neurological complications of varying severity unfortunately are relatively common after CABG, in particular in a certain high-risk group of patients. Extracranial carotid artery disease is significantly associated with a type I adverse neurological outcome (i.e., death due to stroke or hypoxic encephalopathy, nonfatal stroke, TIA, stupor, or coma at the time of discharge) (27). Hemodynamically significant carotid artery stenoses are associated with as many as 30% of early post-operative CABG strokes (28). These complications can have important clinical and psychological effects on the affected patients. Roach et al. (27) showed that adverse neurological events occurred in 6.1% of patients, nearly one-half of whom (3.1%) had severe complications including stroke and coma. In those who had complication after CABG, the mortality rate was very high (21%). Preventing stroke and cardiovascular events after CABG is an important and complex problem. The trend to perform coronary surgery in an increasingly elderly population underscores the importance of the issue (29,30). Concomitant carotid artery disease might be a major factor contributing to the occurrence of post-operative stroke (31,32). Other factors, however, might be equally important. Carotid artery disease might be a marker of diffuse atherosclerosis, affecting also aortic arch, arch vessels, and intracranial vessels. The presence of generalized atherosclerosis might increase the occurrence of hemorrhage, watershed ischemia, or emboli, all of which might result in a stroke. Otherwise, concomitant significant CAD increases the mortality among patients undergoing CEA (2,3). In patients with such a disease, a simplified operative management like hybrid revascularization by CAS and CABG can minimize the negative impact of diffuse atherosclerotic disease. In fact, our findings indicate that, in symptomatic patients with combined carotid artery disease and CAD at high surgical risk, the approach that we proposed is a feasible therapeutic option with good immediate and mid-term clinical results.
Recently, a series published by a single institution in the last 7 years has shown that in 1,769 patients undergoing combined procedures the incidence of stroke and TIA averages 3.8%, AMI averages 3.1%, and mortality averages 4.5% (11). Recently, Hertze and Mascha (33) confirmed these results, reporting a post-operative stroke and operative mortality rate of 10.3% for simultaneous CEA and CABG surgical interventions. According to these results, in a previous series of 180 consecutive patients undergoing combined surgical revascularization at the Tor Vergata University of Rome between 1991 and 2002, the 30-day mortality and stroke rate was 10% and 1.1%, respectively (34), with a mortality rate of 14.5% when the standard EuroSCORE was 6 or more and 3.4% when it was lower than 5. These high-risk patients could be treated by an alternative strategy such as the hybrid approach proposed in this study.
In fact, in a recent study, we demonstrated a reduction of the mortality rate to 5.4% when the hybrid approach was used in high-risk patients (16). Remarkably, 14% of these patients treated with CAS and CABG also underwent valve surgery repair.
As compared with combined surgical revascularization, the hybrid strategy requires a shorter surgical time and less extensive surgical trauma, thus reducing cofactors known to increase morbidity and mortality. A recent meta-analysis demonstrated a superiority of CEA as compared with CAS regarding the evaluation of death and stroke at 30 days (35). However, this superiority is not evident if combined hard end point analysis such as death, stroke, and myocardial infarction are considered (34). As compared with CEA, CAS has uncertain efficacy and safety in patients at risk for stroke for atherosclerotic stenosis of the internal carotid artery (36). In particular in high-risk patients for CEA, mainly due to severe CAD, the SAPPHIRE (Stenting and Angioplasty with Protection in Patients at High Risk for Endarterectomy) trial showed that CAS was safer than CEA, because it had a lower postprocedure risk of AMI at 30 days as compared with surgery (13). This is likely to be the case mainly in patients with elevated surgical risk, such as the patients involved in the SHARP (Study of Heart and Renal Protection) study. In fact, according to our inclusion criteria, we enrolled only patients with a standard EuroSCORE equal to or above 5, with an elevated surgical mortality. In particular, when the standard EuroSCORE is 8, as it is in our study, the surgical mortality rate might be as high as 14.5% (18,37,38). In this high-risk subset of patients, specific surgical complications are also elevated: Fukuda et al. (37) reported a morbidity rate of 56.5%. In particular, when both internal carotid arteries have significant stenosis, the risk of stroke after cardiac surgery is particularly high: 25%, as reported by Tunio et al. (38). On the contrary, with the percutaneous hybrid approach as in our study, the stroke rate was only 2% (2 patients), considering that 55% of our patients had bilateral internal carotid artery disease. Such results might also be due to the fact that our study involved only high-volume centers and all the procedures were performed by experienced operators.
In particular, the invasive cardiologist or radiologist involved in the study performed more than 150 CAS as primary operator, according to the consensus document on carotid stenting procedures (39).
Another potential advantage of the simultaneous hybrid approach as compared with a combined surgical approach is that during the CAS procedure the patient is awake and the neurological outcome will be known instantly rather than after the patient emerges from general anesthesia. However, our strategy might have some additional advantages as compared with staged CEA- or CAS-CABG, because it seems to reduce the risk of AMI during CEA (13) or in the time elapsing between the 2 procedures, because this interval is virtually eliminated (40). In fact, the AMI rate in the time the patient is waiting for CABG after carotid artery procedure was 4.4% and 5.8%, respectively, when CEA- and CAS-CABG was performed (11,38). Finally, we reported the same intensive care and hospital stay, compared with our low-risk patients, despite the elevated risk of morbidity of patients enrolled. This fact is very important also for economic reasons, because costs are reduced in the high-risk subset of patients, as in those with high EuroSCORE (41).
Normothermic cardiopulmonary bypass has been used in our patients. Although hypothermia might be safer from a neurological point of view (42), it carries a higher risk of bleeding, due to platelet dysfunction, in patients that should undergo aggressive antiplatelet aggregation treatment after CAS (43).
It is likely that off-pump techniques might further reduce the overall stroke risk, especially in patients with aortic wall disease.
Nonetheless, our study also demonstrated safety of the periprocedural pharmacological protocol and the timing of antiplatelet administration proposed: in fact, the bleeding rate after surgical intervention was low. Only 1 patient had pericardial tamponade requiring pericardiocentesis, and 3 patients had bleeding after surgery requiring reintervention. In all patients the need for post-operative blood transfusions was not different from those who underwent conventional treatment where antiplatelet aggregation therapy was stopped before CABG (44).
Moreover, no cardiovascular event, stroke, or TIA occurred from hospital discharge to the first 30-days of the follow-up.
Therefore, in patients with combined carotid artery disease and CAD at high surgical risk, the proposed hybrid approach seems to be a possible alternative therapeutic strategy.
Study limitations.
This study has a certain number of limitations. It was not a randomized trial comparing hybrid approach (CAS and CABG) versus an all surgical approach (CEA and CABG). The patient population is not very large, although composed of carefully selected individuals coming from 4 high-volume centers. Indeed, at the present time a larger number of patients with multivessel CAD are treated percutaneously, with drug-eluting stents in particular, when at high surgical risk.
The use of angiographic dye during the CAS procedure might be the major drawback of this approach, in particular in high-risk patients with chronic renal failure. In our study only 1 patient with chronic renal failure had transient renal impairment after the procedure. Particular attention was made to reduce the amount of angiographic dye (i.e., a "road-mapping" X-ray acquisition was used during the stent implantation, and in patients with chronic renal failure, a pre-treatment with fluid administration and acetilcysteine was made) (45).
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Conclusions
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Even if a randomized clinical study is needed to verify our clinical approach, our findings indicate that, in high-risk patients with CAD suitable for CABG and carotid artery disease, hybrid revascularization by CAS immediately followed by CABG is a feasible and promising therapeutic strategy.
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Acknowledgments
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The authors are most grateful to Achille Gaspardone, MPhil, MD, for his critical review of the manuscript.
* Reprint requests and correspondence: Dr. Luigi Chiariello, Cattedra di Cardiochirurgia, Università di Roma Tor Vergata, Policlinico Tor Vergata, Viale Oxford, 81-00133 Rome, Italy (Email: lchiariello{at}tiscali.it).
Manuscript received December 1, 2008;
revised manuscript received January 21, 2009,
accepted February 7, 2009.
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J. G. Byrne, M. A. Robbins, and M. Leacche
A New Approach for Combined Carotid and Coronary Disease: The SHARP Study
J. Am. Coll. Cardiol. Intv.,
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