|Year : 2018 | Volume
| Issue : 1 | Page : 27-34
Plasminogen activator inhibitor-1 as a predictor after cardiopulmonary bypass for postoperative atrial fibrillation
Suzy Fawzy1, Mohamed F Abdel Aleem1, Mohamed A El Badawy2, Islam H Mohamed3
1 Department of Critical Care Medicine, Cairo University, Cairo, Egypt
2 Department of Cardiothoracic Surgery, National Heart Institute, Cairo, Egypt
3 Department of Critical Care Medicine, National Heart Institute, Cairo, Egypt
|Date of Web Publication||24-Jan-2018|
PO Box 269, Orman, Giza 12612
Source of Support: None, Conflict of Interest: None
Background Following cardiac surgery, atrial fibrillation may be a common event. While postoperative atrial fibrillation (POAF) can be transient, it may lead to serious consequences, such as stroke, hemodynamic instability, and death. Plasminogen activator inhibitor-1 (PAI-1) serves as the primary inhibitor of tissue-type plasminogen activator, but also is mainly an acute-phase reactant. Increased PAI-1 promotes fibrosis and reduces extracellular matrix turnover, which modify the atrial substrate and potentially lead to POAF trigged by cardiac surgery.
Aim The aim the study was to assess the efficacy of PAI-1 as a predictor of POAF after cardiopulmonary bypass (CPB).
Patients and methods In this study, we enrolled 100 patients undergoing cardiac surgery requiring CPB and were in sinus rhythm at surgery time. Blood samples were obtained for the measurement of PAI-1 in the morning of the operation and immediately after separation from CPB and administration of protamine. Pearson’s χ2-test, Fisher’s exact test, area under the receiver operating characteristic curves, P-value less than 0.05, multivariable binary logistic regression were used.
Results This study has shown that the serum level of preoperative PAI-1 more than 15 ng/ml and post-CPB level of PAI-1 more than 23 ng/ml are associated with high incidence of POAF (P<0.01 and 0.01, respectively). Left atrial diameter more than 4 cm (P<0.01), advanced age (>60 years) (P=0.04), hypertension history (P=0.035), number of grafts (P=0.01), Right Coronary Artery (RCA) graft (P<0.01), prolonged time of CPB (P=0.03), postoperative administration of epinephrine and dobutamine (P=0.005), and postoperative reduced ejection fraction less than 35% (P=0.028) are other risk factors for POAF development.
Conclusion PAI-1 could be considered as a predictor of POAF whether measured preoperatively or postoperatively immediately after separation from CPB.
Keywords: cardiopulmonary bypass, plasminogen activator inhibitor-1, postoperative atrial fibrillation
|How to cite this article:|
Fawzy S, Abdel Aleem MF, El Badawy MA, Mohamed IH. Plasminogen activator inhibitor-1 as a predictor after cardiopulmonary bypass for postoperative atrial fibrillation. Res Opin Anesth Intensive Care 2018;5:27-34
|How to cite this URL:|
Fawzy S, Abdel Aleem MF, El Badawy MA, Mohamed IH. Plasminogen activator inhibitor-1 as a predictor after cardiopulmonary bypass for postoperative atrial fibrillation. Res Opin Anesth Intensive Care [serial online] 2018 [cited 2019 Mar 20];5:27-34. Available from: http://www.roaic.eg.net/text.asp?2018/5/1/27/223834
| Introduction|| |
Postoperative atrial fibrillation (POAF) leads to prolonged hospital stay and morbidity ,. It complicates 20–40% of surgeries requiring cardiopulmonary bypass (CPB) . Risk factors associated with POAF include atrial fibrillation (AF) history, advanced age, and postoperative withdrawal of β blocker . Growing evidence suggests that fibrosis and inflammation contribute to the pathogenesis of AF ,. The postoperative period is characterized by increased inflammatory markers including interleukin-6 ,, C-reactive protein (CRP) , and plasminogen activator inhibitor-1 (PAI-1) . PAI-1 that converts plasminogen to plasmin is the principal inhibitor of urokinase-type and tissue-type plasminogen activators (t-PAs) .
The primary objective is to identify PAI-1 as a predictor for the development of POAF after CPB.
| Patients and methods|| |
This is a self-controlled, cohort study conducted from April 2014 to October 2014 at the National Heart Institute. The study included 100 patients scheduled to undergo on-pump cardiac surgery. Inclusion criteria were: adults undergoing coronary artery bypass graft (CABG) surgery, valve surgery, or combined CABG and valve surgery who were in sinus rhythm at the time of surgery. As per the exclusion criteria patients with any of the following were excluded from the study: patients who were in AF at the time of surgery or at the time of their preoperative evaluation within a week before surgery, patients with old rheumatic heart disease with enlarged left atrium more than 5 cm in diameter, patients who underwent off-pump procedures, patients who did not have a post-CPB blood sample available, or patients who developed any other types of arrhythmias apart from AF.
All patients were subjected to detailed medical history and physical examination. Continuous ECG monitoring was done by a three-channel screen. A 12-lead ECG recording was performed the day before operation, then daily, or when needed to confirm the rhythm. Daily routine labs and follow-up were done when needed: complete blood count, electrolytes (Na+, K+), urea, creatinine, coagulation profile (prothrombin time, partial thromboplastin time, and international normalized ratio), cardiac enzymes [Creatine Kinase (CK), Creatine Kinase-MB (CK-MB), and troponin], liver function tests, and arterial blood gases. Chest radiography was done daily till removal of chest tubes and then on demand. Full echocardiographic examination including: ejection fraction% (EF%), regional wall motion abnormalities, left atrial dimension, and left ventricular diastolic and systolic dimensions. Two arterial blood samples were collected from patients undergoing on-pump cardiac surgery for measurement of PAI-1 level, the first sample in the morning of the operation and the second sample immediately after separation from CPB and administration of protamine. Samples were separated immediately after collection by centrifuge and then plasma were collected in plastic tubes and frozen till all samples were collected and then used.
The Invitrogen Hu PAI-1 kit (Invitrogen, Waltham, Massachusetts, USA) is a solid-phase sandwich enzyme-linked immunosorbent assay. A monoclonal antibody specific for Hu PAI-1 has been coated onto the wells of the microtiter strips provided. Samples were subjected to washing and after washing, streptavidin–peroxidase (enzyme) is added. This binds to the biotinylated antibody to complete the four-member sandwich. After incubation and washing to remove all the unbound enzyme, a substrate solution is added, which is acted upon by the bound enzyme to produce color. The intensity of this colored product is directly proportional to the concentration of Hu PAI-1 present in the original specimen. Normal plasma concentration of PAI-1 is 5–40 ng/ml .
Each patient signed an informed consent form for blood sampling, data analysis, and his acceptance to be included in the study. Approval for our study was obtained from the Ethics Committee of Cairo University Hospital.
| Results|| |
In this study, 100 patients were enrolled in which 59 patients had CABG, 38 patients had valve surgery, and three patients had combined surgery. Among the 59 CABG patients, 50 patients did not need DC shock after cross-clamp removal, four patients received one DC shock, three patients received two DC shocks, and two patients received three DC shocks. Regarding valve surgery patients (38 patients), 30 patients required three DC shocks, four patients required two DC shocks, two patients required one DC shock, and two patients did not require DC shock. All combined surgery patients (three patients) required three DC shocks.
From the 59 CABG patients, 39 patients had no POAF and 20 patients had POAF. Among the 38 patients with valve surgery, 31 patients had no POAF, and seven patients had POAF. In patients with combined surgery, two patients had no POAF and one patient had POAF. The development of POAF regarding the type of surgical procedure whether CABG, valve surgery, or combined showed no statistical significance (P=0.168, 0.125, and 0.94, respectively).
Patients were classified into two groups according to POAF occurrence. The first group (72 patients) had no POAF, while the second group (28 patients) experienced POAF. In [Table 1], incidence of POAF is more observed in patients with age 60 years or more and hypertensive patients (P=0.01 and 0.035, respectively).
[Table 2] shows significant association of POAF among the redo surgery RCA grafting, and prolonged bypass time group (P=0.03, <0.001, and 0.032, respectively). Moreover POAF is significantly associated with a higher number of grafts.
Patients with POAF had been given both epinephrine+dobutamine, experienced postoperative myocardial ischemia, and had EF% less than 35% (P=0.005, 0.01, and 0.028, respectively). Patients with longer stay in ICU and need of postoperative Mechanical Ventilation (MV) are significantly associated with POAF. This is illustrated in [Table 3].
Levels of PAI-1 pre-CPB and post-CPB are significantly higher in the group that developed POAF (P<0.01 and <0.01, respectively). This is shown in [Table 4] and [Figure 1].
|Table 4 Comparison of precardiopulmonary bypass and postcardiopulmonary bypass levels of plasminogen activator inhibitor-1|
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|Figure 1 Box plot showing preoperative and postcardiopulmonary bypass (CPB) levels of plasminogen activator inhibitor-1 (PAI-1) in patients developing or not developing postoperative atrial fibrillation.|
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The data obtained from [Figure 2] show that the preoperative PAI-1 level had a fair predictive value as evidenced by an area under the receiver operating characteristic curve of 0.724 [95% confidence interval (CI): 0.626–0.809, P<0.0001]. The best cut-off value was a preoperative PAI-1 level of more than 15 ng/ml. This had a sensitivity of 71.43% (95% CI: 51.3–86.8), a specificity of 70.83% (95% CI: 58.9–81.0), a positive predictive value of 48.8% (95% CI: 32.7–65.1), and a negative predictive value of 86.4% (95% CI: 75.0–94.0) ([Table 5]).
|Figure 2 Receiver operating characteristic curve analysis for the prediction of postoperative atrial fibrillation using preoperative plasminogen activator inhibitor-1 (PAI-1) level: P less than 0.0001 for preoperative PAI-1 as a predictor of postoperative atrial fibrillation.|
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|Table 5 Multivariable binary logistic regression model for the prediction of postoperative atrial fibrillation|
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Post-CPB PAI-1 level had a good predictive value as evidenced by an area under the receiver operating characteristic curve of 0.79 (95% CI: 0.697–0.865, P<0.0001). The best cut-off value was a post-CPB PAI-1 level of more than 23 ng/ml. This had a sensitivity of 85.71% (95% CI: 67.3–96.0), a specificity of 76.39% (95% CI: 64.9–85.6), a positive predictive value of 58.5% (95% CI: 42.1–73.7), and a negative predictive value of 93.2% (95% CI: 83.4–98.1). This is indicated in [Figure 3].
|Figure 3 Receiver operating characteristic (ROC) curve for the prediction of postoperative atrial fibrillation using postcardiopulmonary bypass (CPB) plasminogen activator inhibitor-1 (PAI-1) level. P value less than 0.0001 for post-CPB PAI-1 as a predictor of postoperative atrial fibrillation. Post-CPB PAI-1 level had a good predictive value as evidenced by an area under the ROC curve (AUC) of 0.79. The best cut-off value was a post-CPB PAI-1 level of more than 23 ng/ml with a sensitivity of 85.71% and a specificity of 76.39%.|
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[Table 6] shows that POAF developed in patients with left atrial diameter more than 4 cm and the level of pre-PAI-1 and post-PAI-1 are higher among the group with left atrial diameter more than 4 cm.
|Table 6 Effect of left atrial dilatation on the development of postoperative atrial fibrillation and on preoperative and postoperative levels of plasminogen activator inhibitor-1|
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[Table 7] shows that POAF developed in patients who experienced postoperative myocardial ischemia more than those who did not experience ischemic events.
|Table 7 Postoperative myocardial ischemia in patients with and without postoperative atrial fibrillation|
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| Discussion|| |
AF may complicate 20–40% of cardiac surgical procedures requiring CPB . Although off-pump CABG surgery has been associated with a reduction in AF, the incidence of POAF is still 22%. This suggests that not only CPB, but also surgery itself contributes to POAF development . In this study, we examined PAI-1 measured preoperatively and immediately after cardiac surgery for predicting the development of POAF. We also examined other factors that may predict the development of POAF.
PAI-1 is mainly an acute-phase reactant but also serves as the primary inhibitor of t-PA. As a consequence of reduced t-PA activity, less plasmin, a proteolytic enzyme that plays an important role in extracellular matrix turnover is formed from plasminogen .
Thus, increased PAI-1 promotes fibrosis and reduces extracellular matrix turnover, which can modify the atrial substrate and potentially lead to POAF, given a trigger event such as cardiac surgery ,.
In our study population, both preoperative and postoperative PAI-1 antigen concentrations were significantly higher in patients who developed POAF. Pretorius et al.  have shown nearly similar results as our study. They enrolled 253 adult patients undergoing elective cardiac surgery requiring CPB and who were in sinus rhythm at the time of surgery. In their study, patients who developed POAF, levels of postoperative PAI-1 (P=0.014), N-terminal prohormone brain natriuretic peptide (P=0.028), and interleukin-6 (P=0.019) concentrations were significantly higher in their blood. Logistic regression identified postoperative PAI-1 (P=0.036) as an independent predictor of POAF. Moreover, when preoperative PAI-1 antigen concentrations were included in the model preoperative PAI-1 (P=0.015) was identified as an independent predictor of POAF. The χ2 automatic interaction detection model indicated that postoperative PAI-1 antigen concentration determined the risk of AF (13% if PAI-1≤28.5 ng/ml vs. 46% if PAI-1>28.5 ng/ml).
Similarly, Drabik et al.  have found that PAI-1 antigen was higher in patients with AF compared with controls. Moreover, Wu et al.  have conducted a meta-analysis of observational studies to evaluate the association between hemostatic markers and AF. They found that PAI-1 and t-PA were significantly increased in AF cases compared with controls [0.87 (95% CI: 0.28–1.47) and 0.86 (95% CI: 0.04–1.67), respectively].
In regard to the effect of left atrial dilatation on POAF in this study, we excluded patients with left atrial diameter more than 5 cm as it was suspected that they may develop POAF, thus we cannot be sure about the sensitivity and specificity of PAI-1 as an early predictor of POAF. Therefore, we divided our studied patients into two groups: the first group with left atrial diameter 4 cm or less and the second with left atrial diameter more than 4 cm. In our study, patients with left atrial diameter more than 4 cm developed POAF more than those with left atrial diameter 4 cm or less with statistically significant difference (P=0.0001). Moreover, there was statistically significant difference in the level of PAI-1 before and after surgery (P=0.009 and 0.0005, respectively) between these two groups. This shows that the dilated left atrium more than 4 cm could be a significant predictor of POAF and also could be used as a significant predictor of higher levels of preoperative and postoperative PAI-1. Correspondingly, other studies have shown that the dilated left atrium is a predictor of POAF: a clinical research was carried by Leung et al.  on three 100 patients undergoing elective CABG surgery and were monitored with intraoperative transesophageal echocardiography to determine LA dimensions and function. Moreover, POAF was monitored continuously until hospital discharge. By univariate analysis, patients who subsequently developed POAF had a larger LA area and LA appendage area. Besides, our study was comparable with the data of other several studies regarding the left atrial diameter being associated with POAF and being an independent predictor of POAF after CABG ,.
In the current study, there is a statistically significant difference in developing POAF among patients older than 60 years (P=0.04) similar to the other studies in which advanced age was identified and was strongly associated with POAF with mean age of 65.9 years ,. Fibrosis and dilatation of atria have been shown to increase with age with a loss of side to side electrical coupling between groups of atrial muscle fibers . Thus, the incidence of AF after CPB could also increase with age. Also, in the study carried by Mathew et al.  and Koletsis et al.  age was found to be an independent risk factor for AF after cardiac surgery. Another study carried by Onk and Erkute  showed that age, low left ventricular EF, and left atrial diameter were predictors for POAF.
Similarly, Yin et al.  have conducted meta-analysis published studies to examine the risk factors for the occurrence of AF after CABG. Although their studies provided conflicting results, the overall outcomes suggested that advanced age may increase the occurrence of AF after CABG. Likewise, in the stepwise regression analysis by Mendes et al. , age was the most powerful prediction for AF, followed by right coronary stenosis. Similarly, Fleming et al.  have found that advanced age is associated with higher incidence of POAF (P<0.001).
In our study, a history of hypertension and the number of vessels bypassed have a significant effect in developing POAF with P value of 0.035 and 0.014, respectively. Similarly, Yin et al.  in a meta-analysis suggest that previous hypertension and greater number of bridging vessels may increase the occurrence of AF after CABG.
In the current study, the revascularization to the RCA vessel showed statistically significant difference in developing POAF in comparison to revascularization of other vessels (P<0.001). As the blood supply of sinoatrial node and atrioventricular node are from the RCA proximal and median segments, lesions in those segments may influence their function and lead to the occurrence of AF post-CABG. Similar observations were made by Mendes et al.  and Koletsis et al.  supporting the role of diseased right coronary artery in the development of post-CABG AF. Conversely, Zaman et al.  did not find a significant relationship between AF and right coronary artery stenosis.
In our study, the CPB time longer than 2 h is statistically related to POAF than those with CPB timeless than 2 h (P=0.032). Similar studies supported this finding, in which the longer the duration of CPB time, the higher the risk of development of POAF ,,,,,.
Also, in this study, patients with reduced EF less than 35% showed a statistical relation in developing POAF than patients with EF 35% or more (P=0.028). Similarly, Amar et al.  have found that postoperative low cardiac output was independently associated with AF risk after CABG (odds ratio: 3.0, 95% CI: 1.7–5.2, P<0.01). Also, this observation was validated in other studies where an EF lower than 40% was statistically related to the incidence of POAF ,,,.
Regarding the postoperative data in this study, POAF occurred in patients with postoperative myocardial ischemia than in patients without postoperative myocardial ischemia (P<0.001). Similarly, Narducci et al.  have concluded that patients undergoing CABG, neither peripheral nor tissue preoperative CRP levels, but only postoperative high-sensitivity CRP and troponin T levels, are correlated with POAF, suggesting the primary role of an ischemic trigger of AF (P=0.016).
In our study, there is a statistically significant difference in developing POAF in patients with postoperative use of both epinephrine and dobutamine than patients with postoperative use of dobutamine only, epinephrine only, or without inotropic support (P=0.005). Fleming et al.  have found that milrinone use is an independent risk factor for POAF after elective cardiac surgery and is associated with an increased risk of POAF (58.2 vs. 26.1% in nonusers, P<0.001). Others, in their studies, found that high inotropic support was statistically related to the incidence of POAF ,,,,,.
Our study shows that patients who developed POAF have statistically significant longer ICU stay (P=0.016). Equally, Fleming et al.  have found that patients who developed AF stayed in the hospital longer (P<0.001) and were more likely to die (P=0.02). As well, Koletsis et al.  have validated that patients with POAF stayed longer in the ICU. Other studies have found that the median length of ICU stay was significantly higher in patients with POAF compared with those remaining in sinus rhythm .
| Conclusion|| |
PAI-1 could be considered as a predictor of POAF after CPB whether measured preoperatively or postoperatively immediately after separation from CPB.
Preoperative serum level of PAI-1 more than 15 ng/ml and post-CPB serum level of PAI-1 more than 23 ng/ml may be associated with high incidence of POAF.
This study supports the hypothesis that POAF may occur secondary to fibrosis and inflammation, as PAI-1 may be an inflammatory and fibrinolytic biomarker.
Dilated left atrial diameter more than 4 cm could be considered as a predictor of POAF after CPB.
Advanced age (>60 years old), history of hypertension, graft to right coronary artery, number of grafts, and prolonged time of CPB could be included as risk factors (significant predictors) for the development of POAF.
Future clinical trials are suggested to evaluate if drugs that attenuate PAI-1 can reduce the incidence of POAF.
In this regard, the measurement of biomarkers at a single time point represents a potential limitation of this study.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]