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Clinical utility of carotid duplex ultrasound prior to cardiac surgery
From the Society for Vascular Surgery
Clinical utility of carotid duplex ultrasound prior to cardiac surgery Judith C. Lin, MD,a Loay S. Kabbani, MD,a Edward L. Peterson, PhD,c Khalil Masabni, MD,a Jeffrey A. Morgan, MD,b Sara Brooks, RVT,a Kathleen P. Wertella, RHIT,b and Gaetano Paone, MD, MHSA,b Detroit, Mich Objective: Clinical utility and cost-effectiveness of carotid duplex examination prior to cardiac surgery have been questioned by the multidisciplinary committee creating the 2012 Appropriate Use Criteria for Peripheral Vascular Laboratory Testing. We report the clinical outcomes and postoperative neurologic symptoms in patients who underwent carotid duplex ultrasound prior to open heart surgery at a tertiary institution. Methods: Using the combined databases from our clinical vascular laboratory and the Society of Thoracic Surgery, a retrospective analysis of all patients who underwent carotid duplex ultrasound within 13 months prior to open heart surgery from March 2005 to March 2013 was performed. The outcomes between those who underwent carotid duplex scanning (group A) and those who did not (group B) were compared. Results: Among 3233 patients in the cohort who underwent cardiac surgery, 515 (15.9%) patients underwent a carotid duplex ultrasound preoperatively, and 2718 patients did not (84.1%). Among the patients who underwent carotid screening vs no screening, there was no statistically significant difference in the risk factors of cerebrovascular disease (10.9% vs 12.7%; P [ .26), prior stroke (8.2% vs 7.2%; P [ .41), and prior transient ischemic attack (2.9% vs 3.3%; P [ .24). For those undergoing isolated coronary artery bypass grafting (CABG), 306 (17.8%) of 1723 patients underwent preoperative carotid duplex ultrasound. Among patients who had carotid screening prior to CABG, the incidence of carotid disease was low: 249 (81.4%) had minimal or mild stenosis (<50%); 25 (8.2%) had unilateral moderate stenosis (50%-69%); 10 (3.3%) had bilateral moderate stenosis; 9 (2.9%) had unilateral severe stenosis (70%-99%); 5 (1.6%) had contralateral moderate stenosis; 2 (0.7%) had bilateral severe stenosis; 4 (1.3%) had unilateral occluded with contralateral less than 50% stenosis, 1 (0.3%) had unilateral occluded with contralateral (70%-99%) stenosis; and 1 had bilateral occluded carotid arteries. Primary outcomes of patients who underwent isolated CABG showed no difference in the perioperative mortality (2.9% vs 4.3%; P [ .27) and stroke (2.9% vs 2.6%; P [ .70) between patients undergoing preoperative duplex scanning and those who did not. Primary outcomes of patients who underwent open heart surgery also showed no difference in the perioperative mortality (5.1% vs 6.9%; P [ .14) and stroke (2.6% vs 2.4%; P [ .85) between patients undergoing preoperative duplex scanning and those who did not. Operative intervention of severe carotid stenosis prior to isolated CABG occurred in 2 of the 17 patients (11.8%) identified who underwent carotid endarterectomy with CABG. Conclusions: In this study, the correlation between preoperative duplex-documented high-grade carotid stenosis and postoperative stroke was low. Prudent use of preoperative carotid duplex ultrasound should be based on the presence of cerebrovascular symptoms and the type of open heart surgery. (J Vasc Surg 2016;63:710-4.)
An association between carotid occlusive disease and coronary artery disease is well recognized.1 Perioperative stroke remains a major complication of coronary artery bypass graft (CABG) surgery leading to higher mortality, prolonged hospitalization, and increased health care From the Division of Vascular Surgerya and Division of Cardiothoracic Surgery,b Edith and Benson Ford Heart and Vascular Institute, and Department of Public Health,c Henry Ford Health System. Author conflict of interest: none. Presented at the Rapid-Paced Plenary Session of the 2015 Vascular Annual Meeting of the Society for Vascular Surgery, Chicago, Ill, June 1720, 2015. Correspondence: Judith C. Lin, MD, RVT, RPVI, FACS, Division of Vascular Surgery, Heart and Vascular Institute, Henry Ford Hospital, 2799 W Grand Blvd, Detroit, MI 48202 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2016 by the Society for Vascular Surgery. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jvs.2015.10.008
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costs.2,3 Routine, nonselective screening to identify patients with carotid artery disease in patients referred for CABG was deemed as a method to reduce the risk of postoperative stroke.4 However, selective screening for patients with either an age greater than 65 years, carotid bruit, or cerebrovascular disease would have reduced the screening load by nearly 40% with negligible impact on surgical management or neurologic outcomes.5 Thus, the 2011 American Heart Association guidelines recommended screening only in selected patients.6,7 Furthermore, the clinical utility and cost-effectiveness of carotid duplex examination prior to cardiac surgery have been questioned by the multidisciplinary committee creating the 2012 Appropriate Use Criteria for Peripheral Vascular Laboratory Testing.8 The objectives of this study were to determine whether preoperative carotid ultrasound would reduce postoperative neurologic symptoms of patients undergoing CABG and to analyze the clinical utility of carotid screening in patients who underwent carotid duplex ultrasound prior to CABG vs other cardiac surgery at a tertiary institution.
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Lin et al 711
All Cardiac PaƟents N=3233
CABG PaƟents
Other Cardiac PaƟents
N=1723
N=1510
CaroƟd Screening N= 306
No CaroƟd Screening N=1417
CaroƟd Screening N=209
No CaroƟd Screening N=1301
Fig. Summary of patient who underwent preoperative carotid screening.
METHODS From March 2005 to March 2013, electronic medical records of all patients who underwent carotid duplex ultrasound within 13 months prior to open heart surgery were analyzed using the combined databases from our clinical vascular laboratory In Record Time, Inc (Fort Lauderdale, Fla) database and the Society of Thoracic Surgeons’ National Database. Included patients were those who underwent CABG without concomitant valve repair. A subgroup analysis of patients who underwent other cardiac operations was also performed (Fig). Individual consents were not obtained from each patient because this was a retrospective analysis. Approval for this study was obtained from the Henry Ford Hospital Institutional Review Board. Results of the carotid duplex ultrasound were classified as none or mild internal carotid stenosis (any type, 0%-49%), moderate internal carotid stenosis (50%-69%), severe internal carotid stenosis (70%-99%), and occluded (100%).9,10 Carotid consensus criteria were used for the interpretation of the carotid duplex study. All carotid ultrasound studies were performed using Philips iU22 transducers (Philips Healthcare, Bothell, Wash) in a clinical vascular laboratory, which is accredited by the Intersocietal Accreditation Committee. All noninvasive studies were performed by certified technologists with Registered Vascular Technologist (RVT) credential and the results interpreted by vascular surgeons with RVT and/or Registered Physician in Vascular Interpretation (RPVI) credentials. Preoperative, operative, and postoperative variables were retrieved from the Society of Thoracic Surgeons’ National Database, which included the following variables: age, gender, weight (in kilograms), height (in centimeters), and body mass index (in kg/m2). Comorbidities included dyslipidemia, smoking history, history of cerebrovascular accident, carotid stenosis, history of carotid surgery or stenting, family history of coronary artery disease, serum creatinine levels, diabetes, dialysis, hypertension, infective endocarditis, and chronic lung disease were analyzed. Procedure types included CABG, CABG with aortic valve repair, CABG with mitral valve repair, isolated aortic valve repair, isolated mitral valve repair, ascending or arch repair,
heart transplant, and left ventricular assist device placement. Carotid endarterectomy (CEA) was performed with bovine patch angioplasty in patients undergoing CABG in a staged or concomitant fashion by discretion of the board-certified vascular surgeons. Postoperative complications included mortality, cerebrovascular accident, and transient ischemic attack. Mortality included all deaths, regardless of cause, occurring during the hospitalization in which the operation was performed, even if after 30 days, and all deaths occurring after discharge from the hospital but before the end of the 30th postoperative day. Perioperative stroke or cerebrovascular accident was defined as any new focal or global neurologic deficit of abrupt onset caused by a disturbance in blood supply to the brain that did not resolve within 24 hours. Transient ischemic attack indicates the loss of neurological function that was abrupt in onset but with complete return of function within 24 hours. Patient outcomes between those who underwent carotid duplex scanning (group A) and those who did not (group B) were compared. Wilcoxon rank-sum testing was used to examine binary responses such as gender. Those variables with more than two classes were examined using Kruskal-Wallis techniques. If pairwise testing was required, it was done using the Wilcoxon rank-sum test. A P value less than .05 was considered as evidence of significance. All statistical computations were performed using SAS 9.4 (SAS Institute, Inc, Cary, NC). RESULTS Among 3233 patients in this cohort who underwent cardiac surgery, 515 (15.9%) of the patients underwent a carotid duplex ultrasound preoperatively, and 2718 (84.1%) patients did not (Table I). More male patients (72.0% vs 64.8%; P < .01) and more patients with dyslipidemia (68.7% vs 58.4%; P < .01) were in the carotid screening group prior to their open heart surgery. Other comorbidities were similar between those who were and were not screened were age, body mass index, current smoker, family history of coronary artery disease, serum creatinine level, dialysis, diabetes, hypertension, infectious
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Table I. Baseline characteristics for all cardiac surgical patients Variables
Group A (n ¼ 515)
Group B (n ¼ 2718)
Age, mean 6 SD, years 64.6 6 11.0 63.1 6 13.8 Sex (% male) 72.0 64.8 28.82 6 6.15 29.20 6 6.50 Body mass index, mean 6 SD, kg/m2 Current smoker 37.7 37.7 FHxCAD 6.8 8.7 Creatinine, 1.27 6 0.99 1.33 6 1.10 mean 6 SD, mg/dL Dialysis 5.7 5.6 Diabetes 36.7 36.7 Oral 37.0 40.8 Insulin 50.8 45.1 Diet 10.0 9.4 None 2.2 4.7 Dyslipidemia 68.7 58.4 Hypertension 80.2 83.3 Infectious endocarditis 3.7 3.9 Chronic lung disease 21.0 21.8 Cerebrovascular disease 10.9 12.7 Prior CVA 8.2 7.2 Prior TIA 2.9 3.3
P value .08 <.01 .20 .99 .15 .15
Table II. Severity of carotid stenosis among patients who underwent isolated coronary artery bypass grafting (CABG) (N ¼ 306) Ipsilateral severity of carotid stenosis
Contralateral severity of carotid stenosis
Ipsilateral mild <50% Ipsilateral moderate 50%-69%
Contralateral Contralateral Contralateral 50%-69% Contralateral Contralateral 50%-69% Contralateral 70%-99% Contralateral Contralateral 50%-69% Contralateral 70%-99% Contralateral
Ipsilateral severe 70%-99%
.94 .99 Ipsilateral occluded
<.01 .09 .82 .66 .26 .41 .24
CVA, Cerebrovascular accident; FHxCAD, family history of coronary artery disease; SD, standard deviation; TIA, transient ischemic attack. Data are presented as percentages unless otherwise indicated.
endocarditis, and chronic lung disease. Specifically, there was no statistically significant difference in the risk factors of cerebrovascular disease (10.9% vs 12.7%; P ¼ .26), prior stroke (8.2% vs 7.2%; P ¼ .41), and prior transient ischemic attack (2.9% vs 3.3%; P ¼ .24). For those undergoing isolated CABG, 306 (17.8%) of 1723 patients underwent a preoperative carotid duplex ultrasound. Among patients who had carotid screening prior to CABG, the incidence of carotid disease was low: 249 (81.4%) had minimal or mild stenosis (<50%); 25 (8.2%) had unilateral moderate stenosis (50%-69%), 10 (3.3%) had bilateral moderate stenosis; 9 (2.9%) had unilateral severe stenosis (70%-99%), 5 (1.6%) had contralateral moderate stenosis, 2 (0.7%) had bilateral severe stenosis; 4 (1.3%) had unilateral occluded with contralateral less than 50% stenosis, 1 (0.3%) had unilateral occluded with contralateral (70%-99% stenosis), and 1 had bilateral occluded carotid arteries (Table II). None of the patients with moderate carotid stenosis underwent carotid revascularization. Among the 17 patients with severe or unilateral occluded carotid artery stenosis, two (11.8%) patients had CEA as a combined procedure with CABG: one patient with unilateral occluded and contralateral (70%-99%) stenosis, and one patient with bilateral (70%-99%) carotid stenosis. Of the screened patients, 33 (10.8%) had a prior history of stroke or transient ischemic attack. Among the patients with significant carotid artery stenosis, only one patient with unilateral (70%-99%) stenosis had a prior history of stroke. Primary outcomes of patients who underwent isolated CABG showed that there was no difference in the
No. (%)
mild <50% mild <50% moderate
249 (81.4) 25 (8.2) 10 (3.3)
mild <50% moderate
9 (2.9) 5 (1.6)
severe
2 (0.7)
mild <50% moderate
4 (1.3) 0
severe
1 (0.3)
occluded
1 (0.3)
Table III. Primary outcomes of coronary artery bypass grafting (CABG) Primary outcomes Death Stroke TIA
Group A carotid screening (n ¼ 306)
Group B no carotid screening (n ¼ 1417)
P value
2.9 2.9 0
4.3 2.6 0.2
.27 .70 .99
TIA, Transient ischemic attack.
perioperative mortality (2.9% vs 4.3%; P ¼ .27) and stroke (2.9% vs 2.6%; P ¼ .70) between the patients undergoing preoperative duplex scanning and those who did not (Table III). Among patients who were screened prior to isolated CABG, 9 (2.9%) of 306 patients developed stroke postoperatively between days 1 and 14. Stroke occurred in two patients who had unilateral (50%-69%) stenosis; however, location of the stroke was contralateral to the side of the carotid stenosis in both patients and occurred at postoperative day 1 in one patient and at postoperative day 2 in another. Among patients who were not screened, location of the stroke was right hemispheric in 25%, left hemispheric in 41.7%, and bilateral in 33.3%. Among patients who underwent carotid screening, patients undergoing CABG and left ventricular assist device placement had a higher incidence of carotid occlusive disease than other types of cardiac operations (P < .01). In this subset of patients, the incidence of carotid occlusive disease was also low: 458 (88.9%) had minimal or mild stenosis, 34 (6.6%) had moderate stenosis, 11 (2.1%) had unilateral severe stenosis, and 7 (1.4%) had unilateral occluded carotid disease. Primary outcomes of patients who underwent open heart surgery also showed that there was no difference in perioperative mortality (5.1% vs 6.9%; P ¼ .14) and stroke (2.6% vs 2.4%; P ¼ .85) between patients
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Table IV. Primary outcomes of patients with carotid screening versus no carotid screening prior to all cardiac surgery Primary outcomes Death, % CABG LVAD Aortic VR Mitral VR Ascending/arch repair Heart transplant Stroke, % TIA, %
Group A carotid screening (n ¼ 515)
Group B no carotid screening (n ¼ 2718)
P value
5.1 2.9 12.0 4.0 9.8 0
6.9 4.3 17.7 8.1 7.4 15.1
.14 .27 .20 .27 .54 .37
8.3 2.6 0
7.9 2.4 0.2
.99 .85 .99
CABG, Coronary artery bypass grafting; LVAD, left ventricular assist device; TIA, transient ischemic attack; VR, valve replacement.
undergoing preoperative duplex scanning and those who did not (Table IV). DISCUSSION We report our study as part of the quality initiative projects for the vascular laboratory to decrease health care costs without compromising patient outcomes. In our study, we investigated the value of selective preoperative carotid duplex prior to cardiac surgery at a tertiary institution. A previously published review of the literature concluded that preoperative carotid stenosis screening did not reduce perioperative stroke in patients undergoing CABG.11 Masabni et al state that carotid duplex ultrasound screening, whether selective or nonselective, identifies only the minority of patients who will develop perioperative stoke, and intervening on those with carotid disease might not decrease the risk of these neurologic events.11 Our study concurs that selective screening in asymptomatic patients also does not translate into better neurologic outcomes or improved mortality after cardiac surgery. In this cohort of patients, those who underwent a selective preoperative carotid duplex ultrasound had the same incidence of postoperative stroke as those who did not have carotid duplex prior to cardiac surgery. Thus, these results dispute the clinical utility and cost-effectiveness management strategy of carotid screening in patients with asymptomatic carotid disease undergoing cardiac surgery. This study also shows that preoperative carotid duplex evaluation did not alter the management in the majority of patients undergoing cardiac surgery. Although there was a higher incidence of carotid occlusive disease in patients undergoing CABG vs other types of cardiac surgery, carotid screening altered the management of a small number of patients and did not decrease perioperative stroke. Surgical management of severe carotid stenosis prior to isolated CABG occurred in 2 of the 17 patients (11.8%) identified who underwent CEA with CABG. Although these patients did well, CEA did not seem to reduce the overall outcome.
Fukuda and colleagues12 found that nonselective carotid ultrasound altered the management in only 4% of their patients. The strokes occurred in patients who underwent combined CABG and CEA and those with mild carotid stenosis. No strokes occurred in the patients with greater than 50% carotid stenosis who also did not undergo carotid revascularization. Stroke laterality also did not matter for patients with preoperative identification of carotid disease undergoing CABG. Li et al13 found that no direct causal relations exist between carotid stenosis and ipsilateral stroke. In our cohort, stroke location was contralateral to the side of the carotid stenosis in both patients with unilateral (50% to 69%) carotid stenosis and occurred after the CABG, not intraoperatively. Among patients who were not screened, location of the stroke was right hemispheric in 25%, left hemispheric in 41.7%, and bilateral in 33.3%. These findings refute the assumptions that carotid occlusive disease is causally related to perioperative stroke and that prophylactic carotid revascularization decreases its risk. Also, the stroke did not occur immediately after the cardiac procedure, but a few days later. We surmise from previous studies that most strokes occur postoperatively, not intraoperatively, because most postoperative strokes result from thromboembolic events.2,14,15 We did not analyze whether patients underwent on- or off-pump CABG. Proponents of off-pump CABG argue that patients are likely to have aortic arch atheroma as part of their diffuse atherosclerotic disease. Thus, intraoperative assessment of the aorta should be done before clamping, and strategies to decrease the shedding of emboli from the aorta intraoperatively include off-pump CABG.16 However, another study showed that the choice of performing CABG on- or off-pump did not seem to be influenced by the severity of carotid artery stenosis, and stroke occurrence was similar in patients undergoing on- or offpump surgery with mild, moderate, or severe carotid stenosis.17 Rather, stroke was due to decreased perfusion resulting from hypovolemic shock and occurred in patients without carotid artery stenosis. A significant limitation of this study is that this is a retrospective analysis of carotid screening in patients undergoing cardiac surgery. The decision to obtain carotid duplex ultrasound is based on the discretion of the cardiothoracic surgeon, and the decision to perform carotid revascularization is based on the discretion of the vascular surgeon. Due to the low incidence of events and few carotid interventions among the total screened vs no screening, we conducted a power analysis to support the findings. The sample size was fixed by the number of patients we could identify. We ended with a fairly large sample size of 515 patients with carotid screening and 2718 with no screening. In this study, we assume that the no-screening group is fixed, and we look at what a test with 80% power and a two-sided 0.05 alpha value we can detect. We also assume that carotid screening makes the rate decrease. Thus, using these assumptions, the rate we can detect is: death, 3.9; CABG, 2.0; left ventricular assist device, 12.9; aortic valve replacement, 4.8; mitral valve
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replacement, 4.3; ascending/arch repair, 10.6; and heart transplant, 4.7. The rates for stroke, transient ischemic attack and coma were too small, so no lower rate could be defined. For Table III, a similar computation calculated these detectable rates of death at 1.5 and stroke at 0.6. Thus, this power analysis indicates that the sample size is sufficient, and the lack of difference observed is not secondary to a type 2 error. The overall findings of this study recommend against carotid screening in asymptomatic patients with carotid occlusive disease undergoing cardiac surgery. The Society of Thoracic Surgeons and the American College of Cardiology/American Heart Association recommend ultrasound screening for carotid artery stenosis only in selected patients (class IIA recommendation, level of evidence C).6,7 This study supports the Choose Wisely Campaign from the Society of Thoracic Surgeons: “Don’t initiate routine evaluation of carotid artery disease prior to cardiac surgery in the absence of symptoms or other high-risk criteria.”18
7.
8.
CONCLUSIONS In this cohort, the correlation between preoperative, high-grade carotid stenosis and postoperative stroke was low. We believe that prudent use of carotid screening prior to cardiac surgery should be based on the presence of cerebrovascular symptoms.
9.
10.
AUTHOR CONTRIBUTIONS Conception and design: JL Analysis and interpretation: JL, LK, EP, KM, JM, GP Data collection: JL, SB, KW Writing the article: JL, EP, KM Critical revision of the article: JL, LK, KM Final approval of the article: JL, LK, EP, JM, GP Statistical analysis: EP Obtained funding: JL, GP Overall responsibility: JL
11.
12.
13.
14.
REFERENCES 1. Naylor AR, Mehta Z, Rothwell PM, Bell PR. Carotid artery disease and stroke during coronary artery bypass: a critical review of the literature. Eur J Vasc Endovasc Surg 2002;23:283-94. 2. Tarakji KG, Sabik JF 3rd, Bhudia SK, Batizy LH, Blackstone EH. Temporal onset, risk factors, and outcomes associated with stroke after coronary artery bypass grafting. JAMA 2011;305:381-90. 3. John R, Choudhri AF, Weinberg AD, Ting W, Rose EA, Smith CR, et al. Multicenter review of preoperative risk factors for stroke after coronary artery bypass grafting. Ann Thorac Surg 2000;69:30-5. 4. Wanamaker KM, Moraca RJ, Nitzberg D, Magovern GJ Jr. Contemporary incidence and risk factors for carotid artery disease in patients referred for coronary artery bypass surgery. J Cardiothorac Surg 2012;7:78. 5. Durand DJ, Perler BA, Roseborough GS, Grega MA, Borowicz LM Jr, Baumgartner WA, et al. Mandatory versus selective preoperative carotid screening: a retrospective analysis. Ann Thorac Surg 2004;78:159-66. 6. Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, et al. 2011 ACCF/AHA guideline for coronary artery bypass graft
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surgery: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines developed in collaboration with the American Association for Thoracic Surgery, Society of Cardiovascular Anesthesiologists, and Society of Thoracic Surgeons. J Am Coll Cardiol 2011;58: 2584-614. Brott TG, Halperin JL, Abbara S, Bacharach JM, Barr JD, Bush RL, et al. 2011 ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/ SAIP/SCAI/SIR/SNIS/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease: executive summary: a report of the American College of Cardiology Foundation/ American Heart Association Task Force on Practice Guidelines, and the American Stroke Association, American Association of Neuroscience Nurses, American Association of Neurological Surgeons, American College of Radiology, American Society of Neuroradiology, Congress of Neurological Surgeons, Society of Atherosclerosis Imaging and Prevention, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of NeuroInterventional Surgery, Society for Vascular Medicine, and Society for Vascular Surgery. J Am Coll Cardiol 2011;57:1002-44. Mohler ER, Gornik HL, Gerhard-Herman M, Misra S, Olin JW, Zierler RE. ACCF/ACR/AIUM/ASE/ASN/ICAVL/SCAI/SCCT/ SIR/SVM/SVS 2012 appropriate use criteria for peripheral vascular ultrasound and physiological testing part I: arterial ultrasound and physiological testing. J Am Coll Cardiol 2012;60:242-76. Grant EG, Benson CB, Moneta GL, Alexandrov AV, Baker JD, Bluth EI, et al; Society of Radiologists in Ultrasound. Carotid artery stenosis: grayscale and Doppler ultrasound diagnosiseSociety of Radiologists in Ultrasound consensus conference. Ultrasound Q 2003;19: 190-8. Masabni K, Sabik JF 3rd, Raza S, Carnes T, Koduri H, Idrees JJ, et al. Nonselective carotid artery ultrasound screening in patients undergoing coronary artery bypass grafting: is it necessary? J Thorac Cardiovasc Surg 2016;151:402-9. Masabni K, Raza S, Blackstone EH, Gornik HL, Sabik JF 3rd. Does preoperative carotid stenosis screening reduce perioperative stroke in patients undergoing coronary artery bypass grafting? J Thorac Cardiovasc Surg 2015;149:1253-60. Fukuda I, Gomi S, Watanabe K, Seita J. Carotid and aortic screening for coronary artery bypass grafting. Ann Thorac Surg 2000;70: 2034-9. Li Y, Walicki D, Mathiesen C, Jenny D, Li Q, Isayev Y, et al. Strokes after cardiac surgery and relationship to carotid stenosis. Arch Neurol 2009;66:1091-6. Hogue CW Jr, Murphy SF, Schechtman KB, Davila-Roman VG. Risk factors for early or delayed stroke after cardiac surgery. Circulation 1999;100:642-7. Filsoufi F, Rahmanian PB, Castillo JG, Bronster D, Adams DH. Incidence, topography, predictors and long-term survival after stroke in patients undergoing coronary artery bypass grafting. Ann Thorac Surg 2008;85:862-70. Blauth CI, Cosgrove DM, Webb BW, Ratliff NB, Boylan M, Piedmonte MR, et al. Atheroembolism from the ascending aorta. An emerging problem in cardiac surgery. J Thorac Cardiovasc Surg 1992;103:1104-11. Manabe S, Shimokawa T, Fukui T, Fumimoto KU, Ozawa N, Seki H, et al. Influence of carotid artery stenosis on stroke in patients undergoing off-pump coronary artery bypass grafting. Eur J Cardiothorac Surg 2008;34:1005-8. Society of Thoracic Surgeons. Five things physicians and patients should question; 2013 [cited 2013 September 4]. Available at: http://www. choosingwisely.org/wp-content/uploads/2015/02/STS-Choosing-WiselyList.pdf. Accessed May 30, 2015.
Submitted Jul 20, 2015; accepted Oct 7, 2015.
Clinical utility of carotid duplex ultrasound prior to cardiac surgery Judith C. Lin, MD,a Loay S. Kabbani, MD,a Edward L. Peterson, PhD,c Khalil Masabni, MD,a Jeffrey A. Morgan, MD,b Sara Brooks, RVT,a Kathleen P. Wertella, RHIT,b and Gaetano Paone, MD, MHSA,b Detroit, Mich Objective: Clinical utility and cost-effectiveness of carotid duplex examination prior to cardiac surgery have been questioned by the multidisciplinary committee creating the 2012 Appropriate Use Criteria for Peripheral Vascular Laboratory Testing. We report the clinical outcomes and postoperative neurologic symptoms in patients who underwent carotid duplex ultrasound prior to open heart surgery at a tertiary institution. Methods: Using the combined databases from our clinical vascular laboratory and the Society of Thoracic Surgery, a retrospective analysis of all patients who underwent carotid duplex ultrasound within 13 months prior to open heart surgery from March 2005 to March 2013 was performed. The outcomes between those who underwent carotid duplex scanning (group A) and those who did not (group B) were compared. Results: Among 3233 patients in the cohort who underwent cardiac surgery, 515 (15.9%) patients underwent a carotid duplex ultrasound preoperatively, and 2718 patients did not (84.1%). Among the patients who underwent carotid screening vs no screening, there was no statistically significant difference in the risk factors of cerebrovascular disease (10.9% vs 12.7%; P [ .26), prior stroke (8.2% vs 7.2%; P [ .41), and prior transient ischemic attack (2.9% vs 3.3%; P [ .24). For those undergoing isolated coronary artery bypass grafting (CABG), 306 (17.8%) of 1723 patients underwent preoperative carotid duplex ultrasound. Among patients who had carotid screening prior to CABG, the incidence of carotid disease was low: 249 (81.4%) had minimal or mild stenosis (<50%); 25 (8.2%) had unilateral moderate stenosis (50%-69%); 10 (3.3%) had bilateral moderate stenosis; 9 (2.9%) had unilateral severe stenosis (70%-99%); 5 (1.6%) had contralateral moderate stenosis; 2 (0.7%) had bilateral severe stenosis; 4 (1.3%) had unilateral occluded with contralateral less than 50% stenosis, 1 (0.3%) had unilateral occluded with contralateral (70%-99%) stenosis; and 1 had bilateral occluded carotid arteries. Primary outcomes of patients who underwent isolated CABG showed no difference in the perioperative mortality (2.9% vs 4.3%; P [ .27) and stroke (2.9% vs 2.6%; P [ .70) between patients undergoing preoperative duplex scanning and those who did not. Primary outcomes of patients who underwent open heart surgery also showed no difference in the perioperative mortality (5.1% vs 6.9%; P [ .14) and stroke (2.6% vs 2.4%; P [ .85) between patients undergoing preoperative duplex scanning and those who did not. Operative intervention of severe carotid stenosis prior to isolated CABG occurred in 2 of the 17 patients (11.8%) identified who underwent carotid endarterectomy with CABG. Conclusions: In this study, the correlation between preoperative duplex-documented high-grade carotid stenosis and postoperative stroke was low. Prudent use of preoperative carotid duplex ultrasound should be based on the presence of cerebrovascular symptoms and the type of open heart surgery. (J Vasc Surg 2016;63:710-4.)
An association between carotid occlusive disease and coronary artery disease is well recognized.1 Perioperative stroke remains a major complication of coronary artery bypass graft (CABG) surgery leading to higher mortality, prolonged hospitalization, and increased health care From the Division of Vascular Surgerya and Division of Cardiothoracic Surgery,b Edith and Benson Ford Heart and Vascular Institute, and Department of Public Health,c Henry Ford Health System. Author conflict of interest: none. Presented at the Rapid-Paced Plenary Session of the 2015 Vascular Annual Meeting of the Society for Vascular Surgery, Chicago, Ill, June 1720, 2015. Correspondence: Judith C. Lin, MD, RVT, RPVI, FACS, Division of Vascular Surgery, Heart and Vascular Institute, Henry Ford Hospital, 2799 W Grand Blvd, Detroit, MI 48202 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2016 by the Society for Vascular Surgery. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jvs.2015.10.008
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costs.2,3 Routine, nonselective screening to identify patients with carotid artery disease in patients referred for CABG was deemed as a method to reduce the risk of postoperative stroke.4 However, selective screening for patients with either an age greater than 65 years, carotid bruit, or cerebrovascular disease would have reduced the screening load by nearly 40% with negligible impact on surgical management or neurologic outcomes.5 Thus, the 2011 American Heart Association guidelines recommended screening only in selected patients.6,7 Furthermore, the clinical utility and cost-effectiveness of carotid duplex examination prior to cardiac surgery have been questioned by the multidisciplinary committee creating the 2012 Appropriate Use Criteria for Peripheral Vascular Laboratory Testing.8 The objectives of this study were to determine whether preoperative carotid ultrasound would reduce postoperative neurologic symptoms of patients undergoing CABG and to analyze the clinical utility of carotid screening in patients who underwent carotid duplex ultrasound prior to CABG vs other cardiac surgery at a tertiary institution.
JOURNAL OF VASCULAR SURGERY Volume 63, Number 3
Lin et al 711
All Cardiac PaƟents N=3233
CABG PaƟents
Other Cardiac PaƟents
N=1723
N=1510
CaroƟd Screening N= 306
No CaroƟd Screening N=1417
CaroƟd Screening N=209
No CaroƟd Screening N=1301
Fig. Summary of patient who underwent preoperative carotid screening.
METHODS From March 2005 to March 2013, electronic medical records of all patients who underwent carotid duplex ultrasound within 13 months prior to open heart surgery were analyzed using the combined databases from our clinical vascular laboratory In Record Time, Inc (Fort Lauderdale, Fla) database and the Society of Thoracic Surgeons’ National Database. Included patients were those who underwent CABG without concomitant valve repair. A subgroup analysis of patients who underwent other cardiac operations was also performed (Fig). Individual consents were not obtained from each patient because this was a retrospective analysis. Approval for this study was obtained from the Henry Ford Hospital Institutional Review Board. Results of the carotid duplex ultrasound were classified as none or mild internal carotid stenosis (any type, 0%-49%), moderate internal carotid stenosis (50%-69%), severe internal carotid stenosis (70%-99%), and occluded (100%).9,10 Carotid consensus criteria were used for the interpretation of the carotid duplex study. All carotid ultrasound studies were performed using Philips iU22 transducers (Philips Healthcare, Bothell, Wash) in a clinical vascular laboratory, which is accredited by the Intersocietal Accreditation Committee. All noninvasive studies were performed by certified technologists with Registered Vascular Technologist (RVT) credential and the results interpreted by vascular surgeons with RVT and/or Registered Physician in Vascular Interpretation (RPVI) credentials. Preoperative, operative, and postoperative variables were retrieved from the Society of Thoracic Surgeons’ National Database, which included the following variables: age, gender, weight (in kilograms), height (in centimeters), and body mass index (in kg/m2). Comorbidities included dyslipidemia, smoking history, history of cerebrovascular accident, carotid stenosis, history of carotid surgery or stenting, family history of coronary artery disease, serum creatinine levels, diabetes, dialysis, hypertension, infective endocarditis, and chronic lung disease were analyzed. Procedure types included CABG, CABG with aortic valve repair, CABG with mitral valve repair, isolated aortic valve repair, isolated mitral valve repair, ascending or arch repair,
heart transplant, and left ventricular assist device placement. Carotid endarterectomy (CEA) was performed with bovine patch angioplasty in patients undergoing CABG in a staged or concomitant fashion by discretion of the board-certified vascular surgeons. Postoperative complications included mortality, cerebrovascular accident, and transient ischemic attack. Mortality included all deaths, regardless of cause, occurring during the hospitalization in which the operation was performed, even if after 30 days, and all deaths occurring after discharge from the hospital but before the end of the 30th postoperative day. Perioperative stroke or cerebrovascular accident was defined as any new focal or global neurologic deficit of abrupt onset caused by a disturbance in blood supply to the brain that did not resolve within 24 hours. Transient ischemic attack indicates the loss of neurological function that was abrupt in onset but with complete return of function within 24 hours. Patient outcomes between those who underwent carotid duplex scanning (group A) and those who did not (group B) were compared. Wilcoxon rank-sum testing was used to examine binary responses such as gender. Those variables with more than two classes were examined using Kruskal-Wallis techniques. If pairwise testing was required, it was done using the Wilcoxon rank-sum test. A P value less than .05 was considered as evidence of significance. All statistical computations were performed using SAS 9.4 (SAS Institute, Inc, Cary, NC). RESULTS Among 3233 patients in this cohort who underwent cardiac surgery, 515 (15.9%) of the patients underwent a carotid duplex ultrasound preoperatively, and 2718 (84.1%) patients did not (Table I). More male patients (72.0% vs 64.8%; P < .01) and more patients with dyslipidemia (68.7% vs 58.4%; P < .01) were in the carotid screening group prior to their open heart surgery. Other comorbidities were similar between those who were and were not screened were age, body mass index, current smoker, family history of coronary artery disease, serum creatinine level, dialysis, diabetes, hypertension, infectious
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Table I. Baseline characteristics for all cardiac surgical patients Variables
Group A (n ¼ 515)
Group B (n ¼ 2718)
Age, mean 6 SD, years 64.6 6 11.0 63.1 6 13.8 Sex (% male) 72.0 64.8 28.82 6 6.15 29.20 6 6.50 Body mass index, mean 6 SD, kg/m2 Current smoker 37.7 37.7 FHxCAD 6.8 8.7 Creatinine, 1.27 6 0.99 1.33 6 1.10 mean 6 SD, mg/dL Dialysis 5.7 5.6 Diabetes 36.7 36.7 Oral 37.0 40.8 Insulin 50.8 45.1 Diet 10.0 9.4 None 2.2 4.7 Dyslipidemia 68.7 58.4 Hypertension 80.2 83.3 Infectious endocarditis 3.7 3.9 Chronic lung disease 21.0 21.8 Cerebrovascular disease 10.9 12.7 Prior CVA 8.2 7.2 Prior TIA 2.9 3.3
P value .08 <.01 .20 .99 .15 .15
Table II. Severity of carotid stenosis among patients who underwent isolated coronary artery bypass grafting (CABG) (N ¼ 306) Ipsilateral severity of carotid stenosis
Contralateral severity of carotid stenosis
Ipsilateral mild <50% Ipsilateral moderate 50%-69%
Contralateral Contralateral Contralateral 50%-69% Contralateral Contralateral 50%-69% Contralateral 70%-99% Contralateral Contralateral 50%-69% Contralateral 70%-99% Contralateral
Ipsilateral severe 70%-99%
.94 .99 Ipsilateral occluded
<.01 .09 .82 .66 .26 .41 .24
CVA, Cerebrovascular accident; FHxCAD, family history of coronary artery disease; SD, standard deviation; TIA, transient ischemic attack. Data are presented as percentages unless otherwise indicated.
endocarditis, and chronic lung disease. Specifically, there was no statistically significant difference in the risk factors of cerebrovascular disease (10.9% vs 12.7%; P ¼ .26), prior stroke (8.2% vs 7.2%; P ¼ .41), and prior transient ischemic attack (2.9% vs 3.3%; P ¼ .24). For those undergoing isolated CABG, 306 (17.8%) of 1723 patients underwent a preoperative carotid duplex ultrasound. Among patients who had carotid screening prior to CABG, the incidence of carotid disease was low: 249 (81.4%) had minimal or mild stenosis (<50%); 25 (8.2%) had unilateral moderate stenosis (50%-69%), 10 (3.3%) had bilateral moderate stenosis; 9 (2.9%) had unilateral severe stenosis (70%-99%), 5 (1.6%) had contralateral moderate stenosis, 2 (0.7%) had bilateral severe stenosis; 4 (1.3%) had unilateral occluded with contralateral less than 50% stenosis, 1 (0.3%) had unilateral occluded with contralateral (70%-99% stenosis), and 1 had bilateral occluded carotid arteries (Table II). None of the patients with moderate carotid stenosis underwent carotid revascularization. Among the 17 patients with severe or unilateral occluded carotid artery stenosis, two (11.8%) patients had CEA as a combined procedure with CABG: one patient with unilateral occluded and contralateral (70%-99%) stenosis, and one patient with bilateral (70%-99%) carotid stenosis. Of the screened patients, 33 (10.8%) had a prior history of stroke or transient ischemic attack. Among the patients with significant carotid artery stenosis, only one patient with unilateral (70%-99%) stenosis had a prior history of stroke. Primary outcomes of patients who underwent isolated CABG showed that there was no difference in the
No. (%)
mild <50% mild <50% moderate
249 (81.4) 25 (8.2) 10 (3.3)
mild <50% moderate
9 (2.9) 5 (1.6)
severe
2 (0.7)
mild <50% moderate
4 (1.3) 0
severe
1 (0.3)
occluded
1 (0.3)
Table III. Primary outcomes of coronary artery bypass grafting (CABG) Primary outcomes Death Stroke TIA
Group A carotid screening (n ¼ 306)
Group B no carotid screening (n ¼ 1417)
P value
2.9 2.9 0
4.3 2.6 0.2
.27 .70 .99
TIA, Transient ischemic attack.
perioperative mortality (2.9% vs 4.3%; P ¼ .27) and stroke (2.9% vs 2.6%; P ¼ .70) between the patients undergoing preoperative duplex scanning and those who did not (Table III). Among patients who were screened prior to isolated CABG, 9 (2.9%) of 306 patients developed stroke postoperatively between days 1 and 14. Stroke occurred in two patients who had unilateral (50%-69%) stenosis; however, location of the stroke was contralateral to the side of the carotid stenosis in both patients and occurred at postoperative day 1 in one patient and at postoperative day 2 in another. Among patients who were not screened, location of the stroke was right hemispheric in 25%, left hemispheric in 41.7%, and bilateral in 33.3%. Among patients who underwent carotid screening, patients undergoing CABG and left ventricular assist device placement had a higher incidence of carotid occlusive disease than other types of cardiac operations (P < .01). In this subset of patients, the incidence of carotid occlusive disease was also low: 458 (88.9%) had minimal or mild stenosis, 34 (6.6%) had moderate stenosis, 11 (2.1%) had unilateral severe stenosis, and 7 (1.4%) had unilateral occluded carotid disease. Primary outcomes of patients who underwent open heart surgery also showed that there was no difference in perioperative mortality (5.1% vs 6.9%; P ¼ .14) and stroke (2.6% vs 2.4%; P ¼ .85) between patients
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Table IV. Primary outcomes of patients with carotid screening versus no carotid screening prior to all cardiac surgery Primary outcomes Death, % CABG LVAD Aortic VR Mitral VR Ascending/arch repair Heart transplant Stroke, % TIA, %
Group A carotid screening (n ¼ 515)
Group B no carotid screening (n ¼ 2718)
P value
5.1 2.9 12.0 4.0 9.8 0
6.9 4.3 17.7 8.1 7.4 15.1
.14 .27 .20 .27 .54 .37
8.3 2.6 0
7.9 2.4 0.2
.99 .85 .99
CABG, Coronary artery bypass grafting; LVAD, left ventricular assist device; TIA, transient ischemic attack; VR, valve replacement.
undergoing preoperative duplex scanning and those who did not (Table IV). DISCUSSION We report our study as part of the quality initiative projects for the vascular laboratory to decrease health care costs without compromising patient outcomes. In our study, we investigated the value of selective preoperative carotid duplex prior to cardiac surgery at a tertiary institution. A previously published review of the literature concluded that preoperative carotid stenosis screening did not reduce perioperative stroke in patients undergoing CABG.11 Masabni et al state that carotid duplex ultrasound screening, whether selective or nonselective, identifies only the minority of patients who will develop perioperative stoke, and intervening on those with carotid disease might not decrease the risk of these neurologic events.11 Our study concurs that selective screening in asymptomatic patients also does not translate into better neurologic outcomes or improved mortality after cardiac surgery. In this cohort of patients, those who underwent a selective preoperative carotid duplex ultrasound had the same incidence of postoperative stroke as those who did not have carotid duplex prior to cardiac surgery. Thus, these results dispute the clinical utility and cost-effectiveness management strategy of carotid screening in patients with asymptomatic carotid disease undergoing cardiac surgery. This study also shows that preoperative carotid duplex evaluation did not alter the management in the majority of patients undergoing cardiac surgery. Although there was a higher incidence of carotid occlusive disease in patients undergoing CABG vs other types of cardiac surgery, carotid screening altered the management of a small number of patients and did not decrease perioperative stroke. Surgical management of severe carotid stenosis prior to isolated CABG occurred in 2 of the 17 patients (11.8%) identified who underwent CEA with CABG. Although these patients did well, CEA did not seem to reduce the overall outcome.
Fukuda and colleagues12 found that nonselective carotid ultrasound altered the management in only 4% of their patients. The strokes occurred in patients who underwent combined CABG and CEA and those with mild carotid stenosis. No strokes occurred in the patients with greater than 50% carotid stenosis who also did not undergo carotid revascularization. Stroke laterality also did not matter for patients with preoperative identification of carotid disease undergoing CABG. Li et al13 found that no direct causal relations exist between carotid stenosis and ipsilateral stroke. In our cohort, stroke location was contralateral to the side of the carotid stenosis in both patients with unilateral (50% to 69%) carotid stenosis and occurred after the CABG, not intraoperatively. Among patients who were not screened, location of the stroke was right hemispheric in 25%, left hemispheric in 41.7%, and bilateral in 33.3%. These findings refute the assumptions that carotid occlusive disease is causally related to perioperative stroke and that prophylactic carotid revascularization decreases its risk. Also, the stroke did not occur immediately after the cardiac procedure, but a few days later. We surmise from previous studies that most strokes occur postoperatively, not intraoperatively, because most postoperative strokes result from thromboembolic events.2,14,15 We did not analyze whether patients underwent on- or off-pump CABG. Proponents of off-pump CABG argue that patients are likely to have aortic arch atheroma as part of their diffuse atherosclerotic disease. Thus, intraoperative assessment of the aorta should be done before clamping, and strategies to decrease the shedding of emboli from the aorta intraoperatively include off-pump CABG.16 However, another study showed that the choice of performing CABG on- or off-pump did not seem to be influenced by the severity of carotid artery stenosis, and stroke occurrence was similar in patients undergoing on- or offpump surgery with mild, moderate, or severe carotid stenosis.17 Rather, stroke was due to decreased perfusion resulting from hypovolemic shock and occurred in patients without carotid artery stenosis. A significant limitation of this study is that this is a retrospective analysis of carotid screening in patients undergoing cardiac surgery. The decision to obtain carotid duplex ultrasound is based on the discretion of the cardiothoracic surgeon, and the decision to perform carotid revascularization is based on the discretion of the vascular surgeon. Due to the low incidence of events and few carotid interventions among the total screened vs no screening, we conducted a power analysis to support the findings. The sample size was fixed by the number of patients we could identify. We ended with a fairly large sample size of 515 patients with carotid screening and 2718 with no screening. In this study, we assume that the no-screening group is fixed, and we look at what a test with 80% power and a two-sided 0.05 alpha value we can detect. We also assume that carotid screening makes the rate decrease. Thus, using these assumptions, the rate we can detect is: death, 3.9; CABG, 2.0; left ventricular assist device, 12.9; aortic valve replacement, 4.8; mitral valve
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replacement, 4.3; ascending/arch repair, 10.6; and heart transplant, 4.7. The rates for stroke, transient ischemic attack and coma were too small, so no lower rate could be defined. For Table III, a similar computation calculated these detectable rates of death at 1.5 and stroke at 0.6. Thus, this power analysis indicates that the sample size is sufficient, and the lack of difference observed is not secondary to a type 2 error. The overall findings of this study recommend against carotid screening in asymptomatic patients with carotid occlusive disease undergoing cardiac surgery. The Society of Thoracic Surgeons and the American College of Cardiology/American Heart Association recommend ultrasound screening for carotid artery stenosis only in selected patients (class IIA recommendation, level of evidence C).6,7 This study supports the Choose Wisely Campaign from the Society of Thoracic Surgeons: “Don’t initiate routine evaluation of carotid artery disease prior to cardiac surgery in the absence of symptoms or other high-risk criteria.”18
7.
8.
CONCLUSIONS In this cohort, the correlation between preoperative, high-grade carotid stenosis and postoperative stroke was low. We believe that prudent use of carotid screening prior to cardiac surgery should be based on the presence of cerebrovascular symptoms.
9.
10.
AUTHOR CONTRIBUTIONS Conception and design: JL Analysis and interpretation: JL, LK, EP, KM, JM, GP Data collection: JL, SB, KW Writing the article: JL, EP, KM Critical revision of the article: JL, LK, KM Final approval of the article: JL, LK, EP, JM, GP Statistical analysis: EP Obtained funding: JL, GP Overall responsibility: JL
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14.
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Submitted Jul 20, 2015; accepted Oct 7, 2015.