Abstract
Current guidelines give priority to surgical treatment of carotid artery stenosis (CAS) before coronary artery bypass grafting (CABG), especially in symptomatic patients. Carotid artery stenting is an alternative treatment for narrowing of the carotid arteries. This study sought to demonstrate the role of severe CAS in predicting stroke after CABG and assess the efficacy of carotid artery stenting in preventing postoperative stroke in a Chinese cohort. From 2015 to 2021, 1799 consecutive patients undergoing isolated CABG surgery were retrospectively recruited in a Chinese cohort. The predictive value of severe CAS in postoperative stroke and carotid stenting in preventing postoperative stroke was statistically analyzed. The incidence of postoperative stroke was 1.67%. The incidence of CAS with stenosis ≥ 50% and ≥ 70% was 19.2% and 6.9%. After propensity matching, the incidence of stroke was 8.0% in the severe CAS group and 0% in the non-severe CAS group. We successfully established an optimal predictive nomogram for predicting severe CAS in patients undergoing CABG. Carotid artery stenting was found ineffective in preventing postoperative stroke. The present study provides the incidence of CAS and postoperative stroke in a Chinese cohort, identifies severe CAS as an independent risk factor for postoperative stroke after CABG, constructs a nomogram predicting the incidence of severe CAS, and evaluates the effectiveness of carotid artery stenting in preventing postoperative stroke after CABG.
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Introduction
Notwithstanding recent advances in coronary revascularization techniques and drug treatments, coronary artery disease (CAD) remains one of the most prevalent causes of death worldwide1. Coronary artery bypass grafting (CABG) has become the standard-of-care for patients with complex CAD due to its long-term reliability and effectiveness2,3,4. Data from previous large retrospective reports indicated that the overall incidence of perioperative stroke has decreased to 1.6%, and stroke remains one of the most common complications of CABG5,6. A previous study reported that approximately 40% of strokes occur intraoperatively and 58% postoperatively, with a peak at 40 h postoperatively6. Several studies reported that patients with stroke after CABG have more severe hospital complications, longer time in the ICU, longer postoperative stay, and higher in-hospital mortality5,6.
A few studies have shown that patients with carotid artery stenosis (CAS) have an increased risk of stroke after CABG6,7,8,9,10. However, controversy remains as to whether unilateral asymptomatic carotid stenosis is an independent risk factor for ipsilateral ischemic stroke after CABG11,12,13. In addition, carotid revascularization by concurrent carotid endarterectomy or carotid stenting appeared to be beneficial in patients with symptomatic carotid artery disease and bilateral carotid stenosis of 70–99%14,15,16. While other studies suggest that the benefit of such interventions was uncertain17,18. A previous study has shown that a stroke-history is correlated with CAS in a Chinese cohort undergoing CABG7. However, large-scale clinical studies and meta-analyses analyzing the incidence and risk of CAS in Chinese patients undergoing CABG are still scarce.
The aim of this study was to investigate the contemporary incidence of postoperative stroke and severe CAS in Chinese patients undergoing CABG, to perform a nomogram of severe CAS, and to assess the efficacy of carotid artery stenting in preventing postoperative stroke.
Methods
Study design and patients
From 2015 to 2021, 1799 consecutive patients undergoing isolated CABG surgery was recruited at Shandong Provincial Hospital in Jinan, Shandong Province, China. Patients having concomitant cardiovascular surgery (valve replacement, valve repair, and aneurysm removal) were excluded. Anonymous data were retrieved from the electronic medical record system. Ethical approval was obtained from the Biomedical Research Ethic Committee of Shandong Provincial Hospital (SWYX: NO. 2022–490). We confirmed that all research was performed in accordance with local regulations. Informed consent was waived because the study was retrospective according to Biomedical Research Ethic Committee of Shandong Provincial Hospital.
Postoperative stroke diagnosis
Postoperative stroke was diagnosed by a physician participating in the patient daily care and confirmed by a neurologist and imaging (computed tomography or magnetic resonance imaging). A postoperative stroke was characterized as any new focal or global neurological impairment that was not resolved within 24 h and could not be accounted for by other healthcare procedures.
Carotid artery stenosis diagnosis
In our institution, 1702 (94.6%) patients were analyzed for the presence and degree of stenosis using bilateral carotid duplex ultrasonography. The peak systolic velocity (PSV) of the internal carotid artery (ICA) and the velocity ratio of the internal and common carotid arteries (ICA: CCA) were recorded in the Duplex measurements. The definition of the degree of stenosis was consistent with radiological guidelines19,20, no to mild stenosis (< 50%) defined as PSV < 125 cm/s and ICA:CCA ratio < 2.0, moderate stenosis (50–69%) as PSV of 125 to 229 cm/s or ICA:CCA ratio in the range of 2. 0–3.9, severe stenosis (70–99%) as PSV ≥ 230 cm/s or ICA:CCA ratio ≥ 4.0, carotid artery occlusion was defined as a PSV and ICA:CCA ratio of 0 (Table 1).
Other diagnosis
Hypertension was defined as repeated measurements of systolic blood pressure (SBP) ≥ 140 mmHg and diastolic blood pressure (DBP) ≥ 90 mmHg or use of anti-hypertensive therapy. type II diabetes mellitus (T2DM) was defined as repeated measurements of episodic plasma glucose values ≥ 200 mg/dl (≥ 11.1 mmol/L), fasting plasma glucose ≥ 126 mg/dl (≥ 7.0 mmol/L) (fasting time 8- 12 h), or use of T2DM prescription drugs. Hyperlipidemia was determined as a serum low-density lipoprotein cholesterol (LDL-C) ≥ 140 mg/dL, high-density lipoprotein cholesterol (HDL-C) ≥ 40 mg/dL, total cholesterol (TCho) level ≥ 220 mg/dL, and serum triglycerides ≥ 150 mg/dL, or the use of lipid-lowering treatments. Chronic kidney disease (CKD) was defined as GFR 30 mg/g for ≥ 3 months.
CABG and support techniques
The CABG surgical approach (off-pump CABG: median sternotomy or anterior or lateral minimally invasive direct coronary artery bypass [MIDCAB] approach) is determined by the patient cardiac symptoms and the severity of the CAD or CAS. In most cases in this series, the median sternotomy approach is the standard strategy. The MIDCAB approach is preferred for grafting isolated proximal disease of the left anterior descending branch or the first diagonal artery. The operation of carotid artery stenting is determined by the neurologist's assessment and the severity of the CAS (≥ 70%). Percutaneous carotid artery stenting (transfemoral approaches) is performed in most cases one week before CABG. All patients were treated with dual antiplatelet (DAPT) therapy with aspirin and clopidogrel before receiving carotid artery stenting for two days and after the procedure. All carotid artery stent implantation procedures in this study were performed by the same neurosurgeon and their team, using conventional interventional techniques. The patient selection criteria for carotid artery stent implantation in this study were confirmed vascular stenosis of 70% or more by cerebral angiography or clinical symptoms with vascular stenosis of 50% or more.
End points
Stroke occurring after CABG was the primary study endpoint. Secondary endpoints included in-hospital mortality, postoperative myocardial infarction, length of hospital stay, intubation time, ICU stay, readmission to the ICU, and reoperation.
Data analysis
Presentation
Statistical analyses were performed using SPSS statistical software version 25.0 and Stata statistical software version 16.0. Continuous variables are expressed as mean ± SD or median and interquartile variance (IQR). Categorical data were expressed as frequencies or percentages. The t test or Mann–Whitney U test and χ2 test or Fisher's exact test were employed to test for the presence of significant differences between groups. Values less than 0.05 were considered statistically significant for all tests as two-sided tests.
Nomogram
Nomograms are increasingly used for prognostic analysis as a simpler, more intuitive, and more advanced method21. Univariate and multivariate logistic regression models were used to explore potential factors and estimate their weights by severe CAS. Variables with p < 0.05 and those possible predictor variables in the univariate model were entered into the multivariate logistic regression model and Forward: LR was performed with probabilities of entry and removal of 0.05 and 0.10, respectively. Based on these important risk factors, the screening was candidate nomogram models with appropriate predictive power. The predictive performance of the nomogram and other models to predict severe CAS rates was quantified using the area under the curve (AUC). The capability of the nomogram was also tested by fitting a well-calibrated curve. The clinical utility of nomograms was also carefully investigated using decision curve analysis (DCA) to compensate for the limitation that ROC curves do not achieve optimal sensitivity and specificity simultaneously.
Propensity matching
To assess the association between severe CAS and stroke, we used propensity matching to group patients with and without severe CAS. A parsimonious model was first developed using multivariate logistic regression, as described in the previous section. Clinically correlated variables that were not found to be substantially relevant to postoperative stroke were then appended to the fitted model to generate a propensity-matched model. The propensity matching model was quantified using Kdensity plots and propensity matching test plots.
Results
Incidence of CAS and postoperative stroke
Stroke occurred in 30 (1.67% [95% CI, 1.08%-2.26%]) of 1799 patients. 1702 (94.6%) patients with bilateral carotid duplex ultrasound data were divided into no to mild stenosis, moderate stenosis, severe stenosis, and carotid occlusion groups. Also, carotid stenosis was divided into left-only, right-only, unilateral (left + right-only), and bilateral groups (Table 2, Fig. 1). Patients with stroke had a longer hospital stay (P < 0.001) and ICU stay (P = 0.001). The optimal cut-off value for age (determined by the ROC curve and Youden index) was 65 years in patients with severe CAS and 60 years in patients with postoperative stroke as a concomitant disease. The clinical characteristics of patients who experienced a stroke were shown in Supplementary Table 1. Stroke occurred in 4 of 256 patients (1.56% [95% CI, 0.04%-3.08%]) in no to mild unilateral groups, 17 of 1347 (1.26% [95% CI, 0.67%- 1.86%]) in no to mild bilateral groups, 7 of 209 (3.35% [95% CI, 0.91%-5.79%]) in moderate unilateral groups, 0 of 30 (0%) in moderate bilateral groups, 6 of 97 (6.19% [95% CI, 1.39%-10.98%]) in severe unilateral groups, 3 of 20 (15.00% [95% CI, 0.65%- 30.65%]) in severe bilateral groups, 3 of 38 (7.89% [95% CI, 0.68%- 16.47%]) in occluded unilateral groups, and 0 of 3 (0%) in occluded bilateral groups (Fig. 2). There was a statistically significant difference in the incidence of postoperative stroke in the severe CAS group (P < 0.001), severe unilateral CAS group (P = 0.007), severe bilateral CAS group (P = 0.001), and occluded unilateral CAS group (P = 0.033) compared with all patients. It indicates that the greater the degree of stenosis, the higher the incidence of perioperative stroke, especially in the severe unilateral, severe unilateral, and occluded unilateral groups.
Risk factors for severe CAS
Severe carotid stenosis (70%-99%) was found in 117 of 1702 patients in our patient population (6.87%). Table 3 compared the clinical and demographic characteristics of patients after CABG classified by severe carotid stenosis. In univariate logistic regression analysis, a total of 11 factors (containing age ≥ 65 years, height, SBP, DBP, cerebrovascular accident, CKD, preoperative hemoglobin, C-reactive protein (CRP), B-type natriuretic peptide (BNP), eGFR, and left main disease) were detected statistically associated with the incidence of severe CAS. And multivariate logistic regression analysis found the following independent risk factors for severe CAS: age ≥ 65 years, SBP, DBP, CKD, and preoperative hemoglobin.
Nomogram model for severe CAS
To develop an optimal nomogram model, we evaluated the individual and combined performance of these five factors using ROC analysis (Fig. 3). The individual AUCs for age ≥ 65 years, SBP, DBP, CKD, preoperative hemoglobin, and prediction model were 0.598, 0.558, 0.554, 0.518, 0.606, and 0.681, respectively. In addition, as seen in Fig. 4, each of the chosen biomarkers was assigned a proportional score based on its value on the nomogram. To confirm the generality of the nomogram in predicting the incidence of severe CAS, we screened the nomogram for comprehensive validation. The well-fitted calibration curves showed high agreement in predicting the incidence of severe CAS, as shown in Fig. 5 (Hosmer–Lemeshow P value = 0.982). Also, DCA curves were created in Fig. 6. Regardless of the threshold, the nomogram model performed well across the various predictors, which ensured that maximum clinical benefit was achieved. Overall, the DCA curves indicate that the nomogram model is feasible to make a valuable and favorable assessment.
Propensity matching
To assess the association between severe CAS and postoperative stroke, we used a propensity-matched approach to group patients with and without severe CAS. A total of 8 factors (including age ≥ 65 years, male, hypertension, peripheral vascular disease, cerebrovascular accident, chronic kidney disease, left main artery disease, and carotid stenting) were included to form a propensity-matched model. The propensity matching model was quantified using Kdensity plots (Fig. 7 shows the Kdensity before matching and Fig. 8 shows the Kdensity after matching) and propensity matching test plots (Fig. 9). These tests showed that the two groups after propensity matching achieved a good match. The clinical and demographic characteristics of the patients after propensity-matched analysis by severe CAS were shown in Table 4. In univariate logistic regression analysis, a statistically significant difference in ICU length of stay (p = 0.041) was found. After matching, stroke occurred in 6 of 75 patients in the severe CAS group (8.0% [95% CI, 1.86%-14.14%]) and in 0 of 75 patients in the non-severe CAS group (0%) (p = 0.028).
Evaluating of carotid artery stenting
The symptomatic status of 13 patients with severe CAS was shown in Table 5 and 11 received carotid artery stenting. The severe CAS group was divided into a carotid stenting subgroup and a non-carotid stenting subgroup, with stroke occurring in 1 of 24 patients in the carotid stenting subgroup (4.17% [95% CI, -3.83%-12.16%]) and in 8 of 93 patients in the no-carotid stenting subgroup (8.60% [95% CI, 2.90%-14.30%]) (p = 0.766). Similarly, stroke occurred in 1 of 29 patients in the carotid stenting subgroup (3.45% [95% CI, 3.31%-10.21%]) and in 29 of 1673 patients in the no carotid stenting subgroup (1.73% [95% CI, 1.11%-2.36%]) among all patients (P = 1.000).
Discussion
Stroke has continued to be one of the potentially destructive complications of CABG, with significant clinical and economic implications for patients and healthcare systems6,22,23. In previous studies, incidence of stroke was 3.0%24, 1.7%25, 1.6%6 among patients undergoing CABG mainly in American and European area. Over the past 40 years, the incidence of stroke has declined despite increasing patient risk profiles, which benefited from improvements in preoperative assessment, surgical techniques, and postoperative care. The incidence and risk of CAS in Chinese patients undergoing CABG is still unclear. Thus, we compiled 1799 consecutive patients who underwent isolated CABG surgery at Shandong Provincial Hospital. We observed a similar incidence of postoperative stroke (1.67%) in our Chinese CABG cohort. Patients with stroke after CABG had a longer hospital stay and longer time in the ICU than patients without stroke. However, there was no statistical difference in the in-hospital survival between the two groups.
It is believed that carotid stenosis is one of the risk factors for stroke after CABG5,25,26. In addition, a previous meta-analysis of US and European CAS studies showed that the perioperative risk of stroke after cardiac surgery varied from 3.8% to 7.4% for patients with ≥ 50% CAS and increased to 2% to 9.1% for patients with ≥ 70% CAS27. In our study, the incidence of postoperative stroke after CABG was found to be similar, with 3.7% of patients with ≥ 50% CAS and 7.7% of patients with ≥ 70% CAS. A higher incidence of postoperative stroke was found in the severe unilateral group (P = 0.007), the severe bilateral group (P = 0.001), and the occluded unilateral group (P = 0.033) compared to the overall patients. It was shown that a more severe stenosis was associated with a higher incidence of postoperative stroke, particularly in the severe unilateral, severe unilateral, and occluded unilateral groups. After propensity matching, the incidence of stroke was 8.0% in the severe CAS group and 0% in the non-severe CAS group (p = 0.028). The present study is consistent with the prevailing view that severe CAS is an independent risk factor for postoperative stroke.
The incidences of significant CAS stenosis (≥ 50%) were 12.8% to 22.1% and severe CAS stenosis (≥ 70%) were 4.6% to 5.0% in patients with CABG in the United States and European countries20,28. In our Chinese CABG cohort, the incidence of CAS with stenosis ≥ 50% and ≥ 70% was 19.2% and 6.9%, which were consistent with those of previous studies.
An optimal predictive nomogram incorporating age ≥ 65 years, SBP, DBP, CKD, and preoperative hemoglobin to predict severe CAS in patients with CABG was successfully established and carefully evaluated. The available evidence suggests that the nomogram could effectively predict patient prognosis, and its simplicity and intuitive nature facilitate the interpretation by clinical staff29,30. To our knowledge, the present study is the first report on the development of a nomogram for predicting severe CAS in patients with CABG using a number of baseline tests. In a multivariate logistic regression model, we observed that age ≥ 65 years, SBP, DBP, CKD, and preoperative hemoglobin were all independently associated with the incidence of severe CAS. Satisfactory accuracy was observed when the above five variables were included in the nomogram model (AUC = 0.681). In recent years, many studies have reported that the incidence of CAS increases with age31,32. In Durand DJ's study, age over 65 years was shown to be a significant predictor of CAS33. In previously conducted studies, SBP or DBP was considered as a predictor of carotid stenosis32,34,35. In addition, Puz P et al. found that CKD was an independent risk factor for symptomatic internal CAS36. It could be interpreted that CKD is independently associated with carotid atherosclerosis37. Furthermore, Dijk JM and other colleagues demonstrated that increased hemoglobin levels were associated with reduced severity of atherosclerosis, assessed as the presence of ≥ 50% CAS38. Fortunately, our findings showed that age ≥ 65 years, SBP, DBP, CKD, and hemoglobin were also significantly associated with the incidence of severe CAS in patients undergoing CABG, in agreement with these published findings. To avoid the limitations of a single predictor and to obtain higher prediction accuracy, this study combined five tested predictors to form a nomogram model. Our data confirmed that the nomogram was more effective at predicting severe CAS than any single predictor (AUC = 0.681). Moreover, DCA curves have been commonly used in many studies to assess the efficacy of specific clinical approaches39,40. In this study, we also used DCA curves to examine the underlying clinical effects of the nomogram, and our findings suggest that the nomogram was more valuable than other indicators in predicting the incidence of severe CAS.
Carotid endarterectomy is considered to be an effective treatment for both symptomatic patients and asymptomatic patients with CAS41,42. Carotid artery stenting is another treatment technique. However, evidence for the effect of carotid stenting in patients with severe CAS undergoing CABG is lacking, and its effectiveness preventing postoperative stroke remains controversial43. Although there were 117 patients with severe carotid artery stenosis confirmed by carotid ultrasound in the study, the number of patients who ultimately underwent carotid artery stenting did not exceed 30. It was because the degree of stenosis confirmed by cerebral angiography did not meet the above criteria in some of the remaining patients. And other patients could not tolerate carotid artery surgery or combined surgery due to severe conditions (such as frequent angina attacks or severe heart failure). Our study suggested that carotid stenting is not effective in preventing postoperative stroke. Possible explanations are as follows. First, carotid stenosis may be a marker of high atherosclerotic burden and stroke risk, rather than a direct stroke mechanism in most patients. Second, there was relatively few data on carotid artery stenting in our study. Third, combined CABG and carotid stenting are at higher risk than CABG alone.
The study has several limitations. First, the study design was retrospective and non-randomized. In addition, data from a single medical center were analyzed and only selective patients were included. Due to less than thirty patients who underwent carotid artery stent implantation in this study, sample size was indeed limited. Therefore, the results of the study may not be generalizable to other Asian populations and studies with larger sample sizes and higher-quality are needed to confirm our findings. Second, we were unable to determine whether the etiology of each stroke was embolic, thrombotic, or hypoperfused. In this study, all stroke patients were diagnosed with ischemic stroke. However, due to the clinical situations in China and the difficulty in differential diagnosis of stroke etiology, it is challenging to accurately determine whether the stroke is caused by thrombosis, embolism, plaque rupture, or perioperative hypoperfusion and etc. In theory, we could differentiate the etiology of stroke to some extent based on the course of the disease and cranial magnetic resonance imaging (MRI). However, in practice, it is difficult to perform these assessments. Especially since most patients have steel wires fixating the sternum in the thoracic cavity postoperatively, and many patients have unstable conditions in the early stage after surgery, which makes it challenging to perform comprehensive cranial MRI examinations. Third, some patients who underwent emergency surgery were not included in the study because of the lack of ultrasound. Finally, current guidelines give priority to surgical treatment of CAS before CABG, especially in symptomatic patients44. Carotid stenting is an alternative treatment and in this study patients with CAS requiring carotid artery treatment were treated only endovascularly. We hope to continue further research comparing carotid endarterectomy and stenting in patients undergoing CABG in the future.
Conclusions
The incidence of postoperative stroke was 1.67% and severe CAS was in 6.87% patients who underwent CABG in the last 7 years in a single center in China, similar to recent studies in the United States and Europe. More severe carotid stenosis was found to be associated with a higher incidence of postoperative stroke, especially in the severe unilateral group, severe unilateral group, and occluded unilateral group, and severe CAS was an independent risk factor for postoperative stroke. A nomogram constructed from age ≥ 65 years, SBP, DBP, CKD, and hemoglobin could provide an accurate and favorable prediction of the incidence of severe CAS. Carotid artery stenting is ineffective in preventing postoperative stroke.
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Kandaswamy, E. & Zuo, L. Recent advances in treatment of coronary artery disease: role of science and technology. Int. J. Mol. Sci. 19(2), 424 (2018).
Chen, X., Zhang, X., Yan, Y. & Wang, G. The better option of revascularization in complex coronary artery disease patients complicate with chronic kidney disease: A review and meta-analysis. Curr. Probl. Cardiol. 46(9), 100886 (2021).
Head, S. J. et al. Mortality after coronary artery bypass grafting versus percutaneous coronary intervention with stenting for coronary artery disease: a pooled analysis of individual patient data. Lancet. 391(10124), 939–948 (2018).
Thuijs, D. et al. Percutaneous coronary intervention versus coronary artery bypass grafting in patients with three-vessel or left main coronary artery disease: 10-year follow-up of the multicentre randomised controlled SYNTAX trial. Lancet. 394(10206), 1325–1334 (2019).
Filsoufi, F., Rahmanian, P. B., Castillo, J. G., Bronster, D. & Adams, D. H. Incidence, topography, predictors and long-term survival after stroke in patients undergoing coronary artery bypass grafting. Ann. Thorac. Surg. 85(3), 862–870 (2008).
Tarakji, K. G., Sabik, J. F. 3rd., Bhudia, S. K., Batizy, L. H. & Blackstone, E. H. Temporal onset, risk factors, and outcomes associated with stroke after coronary artery bypass grafting. JAMA. 305(4), 381–390 (2011).
Cheng, Y., Gao, J., Wang, J., Wang, S. & Peng, J. Risk factors for carotid artery stenosis in Chinese patients undergoing coronary artery bypass graft interventions. Med. Baltimore. 94(28), e1119 (2015).
De Feo, M. et al. The risk of stroke following CABG: One possible strategy to reduce it?. Int. J. Cardiol. 98(2), 261–266 (2005).
John, R. et al. Multicenter review of preoperative risk factors for stroke after coronary artery bypass grafting. Ann. Thorac. Surg. 69(1), 30–35 (2000).
Ruka, E. et al. Relationship between the degree of carotid stenosis and the risk of stroke in patients undergoing cardiac surgery. Can. J. Cardiol. 38(3), 347–354 (2022).
Baiou, D., Karageorge, A., Spyt, T. & Naylor, A. R. Patients undergoing cardiac surgery with asymptomatic unilateral carotid stenoses have a low risk of peri-operative stroke. Eur. J. Vasc Endovasc. Surg. 38(5), 556–559 (2009).
Ghosh, J., Murray, D., Khwaja, N., Murphy, M. O. & Walker, M. G. The influence of asymptomatic significant carotid disease on mortality and morbidity in patients undergoing coronary artery bypass surgery. Eur. J. Vasc. Endovasc. Surg. 29(1), 88–90 (2005).
Manabe, S. et al. Influence of carotid artery stenosis on stroke in patients undergoing off-pump coronary artery bypass grafting. Eur. J. Cardiothorac. Surg. 34(5), 1005–1008 (2008).
Augoustides, J. G. Advances in the management of carotid artery disease: Focus on recent evidence and guidelines. J. Cardiothorac. Vasc. Anesth. 26(1), 166–171 (2012).
Venkatachalam, S., Gray, B. H., Mukherjee, D. & Shishehbor, M. H. Contemporary management of concomitant carotid and coronary artery disease. Heart. 97(3), 175–180 (2011).
Venkatachalam, S. & Shishehbor, M. H. Management of carotid disease in patients undergoing coronary artery bypass surgery: Is it time to change our approach?. Curr. Opin. Cardiol. 26(6), 480–487 (2011).
Feldman, D. N. et al. Comparison of trends and in-hospital outcomes of concurrent carotid artery revascularization and coronary artery bypass graft surgery: The United States experience 2004 to 2012. JACC Cardiovasc. Interv. 10(3), 286–298 (2017).
Klarin, D. et al. Concomitant carotid endarterectomy and cardiac surgery does not decrease postoperative stroke rates. J. Vasc. Surg. 72(2), 589–596 (2020).
Grant, E. G. et al. Carotid artery stenosis: Gray-scale and Doppler US diagnosis–society of radiologists in ultrasound consensus conference. Radiology. 229(2), 340–346 (2003).
Wanamaker, K. M., Moraca, R. J., Nitzberg, D. & Magovern, G. J. Jr. Contemporary incidence and risk factors for carotid artery disease in patients referred for coronary artery bypass surgery. J. Cardiothorac. Surg. 7, 78 (2012).
Huang, L. et al. Development and validation of a prognostic model to predict the prognosis of patients who underwent chemotherapy and resection of pancreatic adenocarcinoma: A large international population-based cohort study. BMC Med. 17(1), 66 (2019).
Dacey, L. J. et al. Perioperative stroke and long-term survival after coronary bypass graft surgery. Ann. Thorac. Surg. 79(2), 532–536 (2005).
Mohamed, M. O. et al. Incidence and predictors of postoperative ischemic stroke after coronary artery bypass grafting. Int. J. Clin. Pract. 75(5), e14067 (2021).
Roach, G. W. et al. Adverse cerebral outcomes after coronary bypass surgery. Multicenter study of perioperative ischemia research group and the ischemia research and education foundation investigators. N. Eng. J. Med. 335(25), 1857–1863 (1996).
Naylor, A. R., Mehta, Z., Rothwell, P. M. & Bell, P. R. Carotid artery disease and stroke during coronary artery bypass: A critical review of the literature. Eur. J. Vasc. Endovasc. Surg. 23(4), 283–294 (2002).
Nishiyama, K. et al. Temporal pattern of strokes after on-pump and off-pump coronary artery bypass graft surgery. Ann. Thorac. Surg. 87(6), 1839–1844 (2009).
Naylor, A. R. & Bown, M. J. Stroke after cardiac surgery and its association with asymptomatic carotid disease: An updated systematic review and meta-analysis. Eur. J. Vasc. Endovasc. Surg. 41(5), 607–624 (2011).
Santarpino, G. et al. Prognostic impact of asymptomatic carotid artery stenosis in patients undergoing coronary artery bypass grafting. Eur. J. Vasc. Endovasc. Surg. 56(5), 741–748 (2018).
Chen, L. et al. A sample model established by S-index predicting overall survival after curative resection of primary hepatocellular carcinoma. Cancer Manag. Res. 11, 693–703 (2019).
Lei, Z. et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the milan criteria. JAMA Surg. 151(4), 356–363 (2016).
de Weerd, M. et al. Prevalence of asymptomatic carotid artery stenosis in the general population: an individual participant data meta-analysis. Stroke. 41(6), 1294–1297 (2010).
Poorthuis, M. H. F. et al. Development and internal validation of a risk score to detect asymptomatic carotid stenosis. Eur. J. Vasc. Endovasc. Surg. 61(3), 365–373 (2021).
Durand, D. J. et al. Mandatory versus selective preoperative carotid screening: a retrospective analysis. Ann. Thorac. Surg. 78(1), 159–166 (2004).
de Weerd, M. et al. Prediction of asymptomatic carotid artery stenosis in the general population: identification of high-risk groups. Stroke. 45(8), 2366–2371 (2014).
Zhang, K., Lin, Q., Zhang, T., Guo, D. & Cao, L. Contemporary Prevalence and risk factors of carotid artery stenosis in asymptomatic low-income Chinese individuals: a population-based study. Postgrad. Med. 132(7), 650–656 (2020).
Puz, P. et al. Factors associated with the symptomatic status of carotid artery stenosis: identification in a cross-sectional study and development of a scoring system. Pol. Arch. Int. Med. 131(1), 17–25 (2021).
Ohara, T. et al. Impact of chronic kidney disease on carotid atherosclerosis according to blood pressure category: The Suita study. Stroke. 44(12), 3537–3539 (2013).
Dijk, J. M. et al. Hemoglobin and atherosclerosis in patients with manifest arterial disease. SMART-Study. Atheroscler. 188(2), 444–449 (2006).
Kerr, K. F., Brown, M. D., Zhu, K. & Janes, H. Assessing the clinical impact of risk prediction models with decision curves: Guidance for correct interpretation and appropriate use. J. Clin. Oncol. 34(21), 2534–2540 (2016).
Lamain-de Ruiter, M. et al. External validation of prognostic models to predict risk of gestational diabetes mellitus in one Dutch cohort: prospective multicentre cohort study. BMJ. 354, i4338 (2016).
Adams, R. J. et al. Update to the AHA/ASA recommendations for the prevention of stroke in patients with stroke and transient ischemic attack. Stroke. 39(5), 1647–1652 (2008).
Goldstein, L. B. et al. Primary prevention of ischemic stroke: a guideline from the American heart association/American stroke association stroke council: cosponsored by the atherosclerotic peripheral vascular disease interdisciplinary working group; cardiovascular nursing council; clinical cardiology council; Nutrition, physical activity, and metabolism council; and the quality of care and outcomes research interdisciplinary working group. Circulation. 113(24), e873-923 (2006).
Lamanna, A. et al. Carotid artery stenting: Current state of evidence and future directions. Acta Neurol. Scand. 139(4), 318–333 (2019).
Naylor, R. et al. Editor’s choice—European society for vascular surgery (ESVS) 2023 Clinical practice guidelines on the management of atherosclerotic carotid and vertebral artery disease. Eur. J. Vasc. Endovasc. Surg. 65(1), 7–111 (2023).
Acknowledgements
This study was supported by the grants from the National Natural Science Foundation of China (81800255), the Nature Science Foundation of Shandong Province (ZR2020MH044; ZR2021MH112; ZR2021QH016) and Jinan Science and Technology Plan Project (202019165; 202225050).
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C.Z. review and editing (equal). X.M. Conceptualization (lead); writing—original draft (lead); formal analysis (lead); writing—review and editing (equal). T.G. review and editing (equal). S.C. Software (lead); writing—review and editing (equal). S.Z. Methodology (lead); writing—review and editing (equal). H.Z. Conceptualization (supporting); Writing—original draft (supporting). C.M. Writing—review and editing (equal). Y.L. Writing—review and editing (equal). Y.Y. review and editing (equal). X.Z. review and editing (equal). J.C. review and editing (equal). Y.L. review and editing (equal).
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Chen, S., Mi, C., Zhang, S. et al. The role of carotid artery stenosis in predicting stroke after coronary artery bypass grafting in a Chinese cohort study. Sci Rep 13, 21536 (2023). https://doi.org/10.1038/s41598-023-47640-5
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DOI: https://doi.org/10.1038/s41598-023-47640-5
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