Eur J Cardiothorac Surg 2007;31:834-838. doi:10.1016/j.ejcts.2007.02.001
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved
Delayed re-exploration for bleeding after coronary artery bypass surgery results in adverse outcomes
Cliff K. Choonga,b,*,
Caroline Gerrarda,
Kimberley A. Goldsmitha,
Helen Dunninghama,c,
Alain Vuylstekea
a Papworth Hospital NHS Trust, Cambridge, United Kingdom
b University of Cambridge, Cambridge, United Kingdom
c Cambridge Perfusion Services, Papworth Hospital NHS Trust, Cambridge, United Kingdom
Received 19 October 2006;
received in revised form 1 February 2007;
accepted 2 February 2007.
* Corresponding author. Address: Papworth Hospital NHS Trust, Papworth Everard, Cambridge CB3 8RE, United Kingdom. Tel.: +44 1480 830541. (Email: cliffchoong{at}hotmail.com).
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Abstract
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Objective: We aimed to identify the impact of re-exploration for bleeding after coronary artery bypass grafting (CABG) and the effect of time delay, re-exploration within 12 h (<12 h) versus 12 h or later (
12 h). Methods: Analyses of prospective clinical data on 3220 consecutive patients who underwent CABG between 2003 and 2005 were performed. Pearson 
2 tests, Fisher's exact tests, Student's t-tests, Mann–Whitney U tests, or univariate logistic regression analysis were used to assess the effects of pre-operative and operative characteristics on re-exploration, and the effects of re-exploration and time delay on adverse outcomes. Predictors of re-exploration and its effect on adverse outcomes were further evaluated using multiple logistic regression analysis. Results: One hundred ninety-one patients (5.9%) underwent re-exploration for bleeding. Re-explored patients as a group in comparison to the non-re-explored group had increased postoperative blood loss, transfusion requirements, duration of mechanical ventilation, ICU stay, intra-aortic balloon pump (IABP) and haemofiltration support, and mortality (all p
< 0.001). One hundred fifty-seven (82%) of the 191 patients were re-explored <12 h. The group of patients who were re-explored <12 h in comparison to 12 h group had shorter ICU stay (median 3 vs 8.5 days; p
< 0.001), less IABP support (22.3 vs 44.1%; p
= 0.009) and a lower mortality (7 vs 29.4%; p
= 0.001). There was no significant difference in blood loss or transfusion requirements between the two groups. The predicted EuroSCORE risks of the <12 h group was 6.66% and the observed mortality was 7% (p
= 0.865). The observed mortality of 29.4% in the 12 h group was significantly higher than the predicted EuroSCORE risks of 7.59% (p
< 0.001). Conclusions: Patients requiring re-exploration for bleeding are at higher risk of adverse outcomes and this risk is increased if time to re-exploration is prolonged for 12 h or longer.
Key Words: Re-exploration • Coronary • Surgery • Bleeding
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1. Introduction
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Excessive bleeding after cardiac surgery remains a major source of morbidity and a risk of death for patients. Such patients are at greater risks from the hazards of transfusion reactions, infections and cardiac tamponade. There have been many studies examining the haemostatic derangements caused by cardiopulmonary bypass and others have evaluated the various strategies of blood conservation. In the past, there have been several studies evaluating re-exploration for haemorrhage after coronary artery bypass grafting surgery (CABG), however there has not been a recent appraisal on this topic. There have been several changes in the practices of cardiac surgery over the last decade and many of these are likely to have an impact on the rate of re-exploration after CABG. Among the changes are the preoperative use of aspirin, clopidogrel and other new antiplatelet agents, varying practice with regard to the use of antifibrinolytic agents, a greater number of older and sicker patients having surgery, an increased number of unstable patients undergoing surgery and many of whom are receiving heparin infusions prior to surgery. This study aimed to identify the impact of re-exploration for bleeding after CABG in a recent cohort of patients and the effect of time delay, re-exploration within 12 h (<12 h) versus 12 h or later (12 h).
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2. Patients and methods
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Over a 3-year-period, between January 2003 and December 2005, 3220 consecutive patients underwent CABG at this hospital. There were 76 (2.4%) reoperations for recurrent angina. Concomitant valve surgery was performed in 544 (16.9%) patients. The mean age of the 3220 patients was 68.5 (median 70, range 34–96) years and 22.6% were females. The internal mammary graft was utilised in 2868 patients (89%), radial artery in 362 patients (11%), and arterial grafts supplied 3461 (38%) of the total 9097 distal anastomoses. Chest tubes were generally placed in the pericardium and in any pleura that was opened. For elective CABG, antiplatelet medications were discontinued 7 days before surgery and anticoagulation treatment was withdrawn at least 3 days prior to the operation.
2.1 Reoperations for bleeding
The amount of bleeding was calculated from the time of arrival at the intensive care unit (ICU). Re-exploration for bleeding was generally performed in the case of: bleeding that exceeded 3 ml/kg/h in the first 3 h, continued bleeding of more than 200 ml/h that did not cease, excessive bleeding that restarted indicating a possible surgical cause or sudden massive bleeding. Re-exploration was also performed if there were clinical signs of tamponade such as decreasing urine output, tachycardia, hypotension and increasing central venous pressure, often associated with sudden decrease of chest tube drainage.
2.2 Statistical methods
In-hospital data were prospectively collected, entered into an electronic database and subsequently extracted for this study. Continuous variables are presented as median with range or interquartile range (IQR), or mean with standard deviation. Relationships between pre-operative/operative characteristics and re-exploration for bleeding, and the effect of re-exploration and time of re-exploration for bleeding on outcomes were examined. Categorical predictor variables were evaluated using Pearson
2 tests or Fisher's/Fisher–Freeman–Halton exact tests. Continuous variables were evaluated using the Student's t-test, or the Mann–Whitney U test if not normally distributed. EuroSCORE predicted mortality and hospital death were compared using a
2 goodness of fit test. Pre-operative and operative characteristics as predictors of re-exploration for bleeding, and re-exploration for bleeding as a predictor of adverse outcomes were further explored using multiple logistic regression analysis. Forward stepwise logistic regression based upon the likelihood ratio test with p
= 0.2 for inclusion and p
= 0.05 for removal of variables were used. All data analysis was performed using Statistical Package for the Social Sciences (SPSS 14.0 for Windows; SPSS Inc., Chicago, IL).
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3. Results
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Of the 3220 patients, 191 patients (5.9%) underwent re-exploration for bleeding. The preoperative and intraoperative characteristics of the group of patients who had re-exploration in comparison to those without are shown in Table 1
. Various preoperative and intraoperative characteristics were identified as risk factors for re-exploration for bleeding on univariate analysis (Table 1). Logistic regression analysis however revealed that only older age, smaller body mass index (BMI), cessation of aspirin within 4 days of surgery, the usage of clopidogrel type of operation, a longer cardiopulmonary bypass (CPB) duration and a lack of usage of an antifibrinolytic agent during surgery to be independent risk factors (all p
0.035) of re-exploration for bleeding. Re-explored patients as a group in comparison to the non-re-explored group had increased postoperative blood loss, transfusion requirements, duration of mechanical ventilation, ICU stay, intra-aortic balloon pump (IABP) support and haemofiltration (all p
< 0.001) (Table 2
). Multiple forward stepwise logistic-regression analysis confirmed re-exploration for bleeding to be a significant independent predictor of a prolonged stay in the intensive care unit, the need for IABP support, duration of mechanical ventilation, haemofiltration, and death (all p
0.02). Risk factors for hospital death are shown on (Table 3
).
3.1 Amount of bleeding, time to re-exploration and source of bleeding
The median total blood loss from the chest tubes until reoperation was 1050 ml IQR: 750–1575 (mean 1236, range 100–10661) (Fig. 1
). The most common indication for re-exploration was persisting bleeding from chest tubes accounting for 82% of the cases while the remaining patients underwent re-explorations for cardiac tamponade. The median duration from arrival at the ICU to re-exploration was 4.7 h IQR: 2.9 to 9.7 (mean 18.3, range 0.17–35) (Fig. 2
). 157 (82%) of the 191 patients were re-explored <12 h. Of the 34 patients who were re-explored 12 h, 15 (44%) were re-explored because of clinical evidence of cardiac tamponade. The decision and the timing of the remaining 19 patients who were re-explored 12 h were dependent on the clinical circumstances of the patients with decisions being made by the individual surgeons who were in charge of their respective patients. The source of bleeding identified during re-exploration is shown in Table 4
.
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Fig. 1. Amount of bleeding in ml until re-exploration for bleeding after coronary artery bypass surgery.
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3.2 Effect of time delay
The group of patients who were re-explored <12 h in comparison to 12 h group had shorter ICU stay (median 3 vs 8.5 days; p
< 0.001), less IABP support (22.3 vs 44.1%; p
= 0.01) and a lower mortality (7 vs 29.4%; p
< 0.001) (Table 5
). There was no significant difference between blood loss or transfusion requirements between the two groups. The predicted EuroSCORE risks of the <12 h group was 6.7% and the observed mortality was 7.0% (p
= 0.87). The observed mortality of 29.4% in the 12 h group is significantly higher than the predicted EuroSCORE risk of 7.6% (p
< 0.001). The cardiac tamponade subgroup was analysed separately and those re-explored <12 h had lower mortality in comparison to those re-explored 12 h (0 vs 46.7%; p
= 0.01).
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4. Discussion
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In the early days of extracorporeal bypass for cardiac procedures, resternotomy rate for the control of bleeding was in excess of 15% [1]. Improvements in perioperative care, surgical techniques, cardiopulmonary bypass support and blood conservation strategies have markedly decreased the re-exploration rate to range between 2 and 6% [2-4]. A rate of 5.9% from the recent cohort of patients in this study falls within the range of previous published data. Continuing blood loss from bypass graft side branches and anastomotic sites have been found to be the major sources of bleeding in patients who require re-exploration following CABG [3,5]. In this series, bleeding from bypass graft side branches and anastomotic sites accounted for nearly half (49.2%) of the sources of bleeding and continue to be significant causes for excessive postoperative haemorrhage.
Older age, lower BMI, nonelective surgery, longer CPB duration, the use of internal mammary artery, and greater number of distal anastomoses, have been associated with increased risk of resternotomy for bleeding [2,4–7]. Multivariate analysis in this study identified older age, lower BMI, cessation of aspirin within 4 days of surgery, preoperative use of clopidogrel a lack of usage of an antifibrinolytic agent during surgery, type of operation and a longer cardiopulmonary bypass duration to be independent risk factors for re-exploration for bleeding. Several studies have now shown that the intraoperative usage of antifibrinolytic agents is associated with decreased postoperative blood loss and transfusion requirements [8–10]. This beneficial effect is however most likely offset by an increased number of older patients, nonelective cases with patients who did not have adequate time to discontinue antiplatelet medications, or complex cases which would require a longer duration of CPB. The interaction of preoperative aspirin (defined as continuing the use of aspirin within 7 days of surgery) or clopidogrel with CPB further compounds the risk of re-exploration for bleeding as both of these cause platelet dysfunction.
In this study, we found a significantly higher mortality rate, increased need for IABP support, haemofiltration, prolonged ventilation and ICU stay in the group requiring re-exploration. Re-exploration was a significant multivariate indicator of increased morbidity and mortality. These findings are consistent with other studies which had found that re-exploration for haemorrhage was an independent risk factor of adverse outcomes [3,6]. Very few studies however have examined the impact of the effect of time delay to the operating theatre. In this study, 157 of the 191 patients (82%) needing re-exploration were taken back within 12 h of returning to the ICU. This group of patients had shorter ICU stay, less IABP support and a lower mortality. There was however no significant difference in blood loss or transfusion requirements between the two groups. The observed mortality of the <12 h group was 7% (predicted EuroSCORE risks was 6.7%) while those of the 12 h group had an observed mortality of 29.4%, which was significantly higher than the predicted EuroSCORE risk of 7.6%. Similar findings were found in a study by Karthik et al. where 58 of the 89 patients (65.2%) needing resternotomy for haemorrhage were taken back within 12 h of returning to the ICU [5]. In that study, there was a significantly higher rate of mortality and major complications including stroke, renal failure, and longer ICU stay among patients who had a greater delay (longer than 12 h) in return to the operating theatre. These findings most likely reflect the continued haemodynamic instability of these patients for a longer time, greater blood loss, and greater need for blood products.
Some studies have found re-exploration for bleeding to be an independent risk factor of sternal wound infection [6,11]. Talamonti et al undertook a study to determine the role of mediastinal re-exploration in relation to the effect of time delay in the development of sternal wound complications [12]. From a series of 2271 patients undergoing median sternotomy for open-heart surgery, 71 (3.1%) were re-explored for excessive bleeding. Nine of these patients died in the early postoperative period of noninfectious complications. The remaining patients were divided into two groups. Group 1 (54 patients) were re-explored without subsequent problems. Group 2 (eight patients) developed sternal and costochondral wound complications. Comparison of age, intercurrent and pre-existing disease, total bypass time, crossclamp time, and postoperative haemodynamic status showed no statistical difference. All patients bled an average rate of 247 ml/h. The authors however found that the average time before re-exploration was 7.6 h in group 1 compared to 13.8 h in group 2 and that a delay in the return to theatre was a significant risk factor (p
< 0.001) of wound complications. As a result of their study, they have advocated an earlier return to theatre for re-exploration to minimise the risks of sternal wound complications [12].
There are several limitations of this study. The primary limitation was that this was a retrospective study although the data were collected prospectively. It is not, however, feasible to carry out a randomised controlled trial with regard to re-exploration for bleeding. Another limitation is the small number of patients who required re-exploration and in particular the impact of the effect of time delay with the potential risk of type II errors. We also did not evaluate the effect of time delay of shorter duration however will plan to do so in the future.
In summary, re-exploration for bleeding continues to be a significant source and independent marker of morbidity and mortality. Patients requiring re-exploration for bleeding are at higher risk of adverse outcomes and this risk is increased if time to re-exploration is prolonged for 12 h or longer. On this basis, we would strongly recommend a policy of early re-exploration for bleeding, as it does not seem to increase the risk of mortality and an identifiable cause is usually found.
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Appendix A
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Conference discussion
Dr U. Lockowandt (Stockholm, Sweden): Thank you very much for the presentation with the important message that one should be aggressive in re-exploring.
Sometimes the surgeons, after an operation, have a mental state of satisfaction and sometimes of denial. But when you compare these groups, do you really compare the same kind of patients? Are not the patients who are reoperated after 12 h different from the patients who are reoperated earlier? I mean, they are not delayed on purpose, but they are perhaps quite fine and then after 12 h something else comes up, a big bleed or a tamponade or something like that. So there is not really the same kind of reasons for exploring.
Dr Choong: Yes, I think there will be some patients who have delayed re-exploration, as you pointed out, due to clinical features of cardiac tamponade. However, there are also patients who may have some ongoing bleeding and it is the individual surgeon's decision whether these patients are re-explored early or late. Each of the consultant surgeon make their own decision as to when they would re-explore the patient.
Dr R. Dion (Leiden, The Netherlands): Did you change something in your practice? Do you go back faster?
Dr Choong: I think the purpose of this study is to evaluate the effect of time delay and, therefore, with these findings, we would encourage earlier re-exploration rather than late re-exploration providing the patients are not coagulopathic.
Dr Dion: Would you reduce the accepted amount of bleeding? 200 cc/h, 2 h in succession, would you go back and not wait for a third and a fourth hour?
Dr Choong: I think it depends on the clinical condition of the individual patients. If the patient has got clear coagulopathy, then that needs to be corrected first. And if the patient still bleeds, then yes, the patient should then undergo re-exploration.
On the other hand, if the patients have no evidence of coagulopathy, then I think the idea is to re-explore them as early as possible rather than later.
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Footnotes
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\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.
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Abstract
1. Introduction
