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Ann Thorac Surg 2004;78:527-534
© 2004 The Society of Thoracic Surgeons
a Department of Cardiothoracic Surgery, the Cardiothoracic Centre–Liverpool, Liverpool, United Kingdom
b Department of Research and Development, the Cardiothoracic Centre–Liverpool, Liverpool, United Kingdom
c Department of Cardiothoracic Anesthesia, the Cardiothoracic Centre–Liverpool, Liverpool, United Kingdom
Accepted for publication February 20, 2004.
* Address reprint requests to Dr Karthik, Leeds General Infirmary, Great George St, Leeds LS17 8AP, UK
e-mail: suchkats{at}yahoo.com
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Abstract |
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METHODS: In all, 2,898 consecutive patients undergoing coronary artery bypass grafting between April 1999 and March 2002 were retrospectively analyzed from our cardiac surgery registry. Multivariate logistic regression analysis was used to identify risk factors for reexploration for bleeding. To assess the effect of preoperative aspirin and heparin, reexploration patients were propensity matched with unique patients not requiring reexploration. We carried out a casenote review to ascertain the timing and causes for bleeding in patients undergoing resternotomy.
RESULTS: Eighty-nine patients (3.1%) underwent reexploration for bleeding. Multivariate analysis revealed smaller body mass index (p = 0.003), nonelective surgery (p = 0.022), 5 or more distal anastomoses (p = 0.035), and increased age (p = 0.041) to have increased risks. Propensity-matched analysis showed that preoperative use of aspirin (p = 0.004) and heparin (p = 0.001) were associated with increased risk in the on-pump coronary surgery group only. Patients requiring resternotomy had a significantly greater need for inotropic agents (p < 0.001), and longer intensive care unit stay (p < 0.001) and postoperative stay (p < 0.001) than their propensity-matched controls. However, there was no significant difference in the mortality rate. Adverse outcomes were significantly higher when patients waited more than 12 hours after return to the intensive care unit for resternotomy.
CONCLUSIONS: Risk factors for reexploration for bleeding after coronary artery bypass grafting include older age, smaller body mass index, nonelective cases, and 5 or more distal anastomoses. Preoperative aspirin and heparin were risk factors for the on-pump coronary artery surgery group. Patients needing reexploration are at higher risk of complications if the time to reexploration is prolonged. Policies that promote early return to the operating theater for reexploration should be encouraged.
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Introduction |
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There have been several changes in the practices associated with cardiac surgery over the last decade, and many of these are quite likely to have some impact on the rates of reexploration after CABG. Among the many changes that are likely to affect the hematological profile of the patient after cardiac surgery are the preoperative use of aspirin and clopidogrel, an increased number of unstable patients undergoing surgery, many of whom are receiving heparin infusions, off-pump CABG, a greater number of older and sicker patients having surgery, and varying practices with regard to the use of antifibrinolytic drugs.
We performed a retrospective study at our center with a view to ascertain the risk factors that are associated with increased rates of reexploration after CABG. We also examined the effect of reexploration on adverse outcomes and the impact of delaying return to the operating theater.
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Material and methods |
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Outcomes collected, after reexploration, are listed in Table 3. In-hospital mortality was defined as death within the same hospital admission regardless of cause. All patients transferred from the base hospital to another hospital were followed up to confirm their status at discharge. Criteria for defining sternal wound infections were in accord with the published evidence-based guidelines by the Centers for Disease Control and Prevention [9]. Postoperative stroke was defined as a new focal neurologic deficit or comatose state occurring postoperatively that persisted for more than 24 hours after its onset. We excluded confused states, transient events, and intellectual impairment from our study to avoid any subjective bias. Renal failure was defined as patients with a postoperative creatinine level greater than 200 µmol/L or patients requiring dialysis.
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Statistical analysis
Due to nonnormal distributions (tested using the Shapiro-Wilk test), continuous variables are shown as median with 25th and 75th percentiles and comparisons were made with Wilcoxon rank-sum tests as appropriate. Categorical variables are shown as a percentage and comparisons were made with 
2 tests. Standard statistical methods were used to calculate odds ratios (OR) and 95% confidence intervals (CI). Multivariate logistic regression analysis was used, with forward stepwise techniques, to identify risk factors for reexploration for bleeding and to adjust for potentially confounding variables, including surgeon, anesthetist and time of operation (by year) [10]. If continuous variables were found to be significant, they were then assessed as dichotomous variables (eg, BMI < 25, 25 to 30, and so forth). Continuous variables were either included as dichotomous variables or in their original form in the final model depending on the strength of association. In all cases a p value less than 0.05 was considered significant. All statistical analysis was performed retrospectively with SAS for Windows Version 8.2 (SAS Institute, Cary, NC).
In order to assess the effect of preoperative aspirin and heparin use, plus the impact of reexploration for bleeding on outcomes, we performed a case note review on propensity-matched patients. Patients requiring reexploration for bleeding were propensity-matched with unique patients not reexplored. To do this, logistic regression [10] was used to develop a propensity score for reexploration for bleeding for all patients who underwent CABG [11]. The propensity score was constructed using all the variables listed in Table 4. The C statistic, which is equivalent to the receiver-operating characteristic curve, for this model was 0.76 [12]. Patients reexplored were matched with patients not reexplored who had an identical 5-digit propensity score. If this could not be done, we then proceeded to a 4-, 3-, 2-, or 1-digit match [13]. 5-digit matches were achieved in 31 of the patients reexplored, while 46 were matched with a 4-digit propensity score and 7 were matched with a 3-digit match. 5 patients who were reexplored for bleeding could not be matched and hence, they were not included in the propensity-matched study.
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Results |
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Of the 89 patients reexplored, the primary indication for reexploration was bleeding (n = 75). Other indications included 10 cases of tamponade, 2 cardiac arrests with bleeding, and 2 others. The major sites of bleeding were as follows: 42 graft/anastomoses, 23 sternal/left internal mammary artery bed, 6 extra-pericardial, 2 cannulation sites, and 16 unspecified.
The median time to reexploration after initial departure from theater was 8.5 hours (25th and 75th percentiles: 5 to 12 hours), with the longest time being 168 hours. Median blood loss before reexploration was 1,680 mL (25th and 75th percentiles: 1,050 mL to 2,340 mL), with the greatest blood loss being 6,480 mL. Eight patients required more than one reexploration.
Patient characteristics
Patient preoperative and operative characteristics are shown in Tables 1 and 2, respectively. In the univariate analyses, only BMI (p = 0.045) and priority of surgery (p = 0.021) were significantly associated with the need for reexploration for bleeding. Off-pump CABG had no association with the need for reexploration (p = 0.346).
Risk factors
The results of the multivariate logistic regression analysis (Table 5) showed that the independent predictors of reexploration for bleeding were BMI less than 25 kg/m2 (p = 0.003), nonelective surgery (p = 0.022), five or more grafts (p = 0.035), and increased age (p = 0.041). The discriminatory ability of the logistic model, as measured by the C statistic, was 0.65, indicating a reasonable, although weak, ability to discriminate between patients who required reexploration for bleeding and those who did not. The predicted risks of individual patients were rank ordered and divided into deciles. Within each decile of estimated risk, the number of reexplorations predicted was accumulated against the number of observed reexplorations. The Hosmer-Lemeshow goodness-of-fit statistic across deciles of risk was not statistically significant (p = 0.893), indicating minimal departure from a perfect fit.
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Analysis of all 89 patients who required reexploration for bleeding and the association between time to reexplore and postoperative outcomes is shown in Table 6. The incidence of major adverse outcomes after CABG was greater when there was a greater delay in taking the patients back for resternotomy, especially if this was greater than 12 hours after the initial return to ICU. All the patients who died after retsernotomy also belonged to this group.
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Comment |
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An obvious site for bleeding was found in 73 of these 89 cases (82%). This number is substantially higher than that of Unsworth-White and coworkers [2], who found an obvious cause in 67% of their patients. The most common site was from the conduit or the anastomosis in 42 (57.5%), from the sternum or internal mammary artery bed in 23 (31.5%), from extrapericardial bleeders in 6 cases (8.2%), and from cannulation and cardiotomy sites in 2 cases (2.8%). In their study, Unsworth-White and coworkers found the conduit and anastomosis to be the site for bleeding in 26%, but found a significantly higher incidence of bleeding from cannulation and cardiotomy sites (21%) than we did. We believe that most cases of bleeding after CABG have a surgical cause, and hence, there is a stronger case for early reexploration of patients who continue to bleed after their return to the ICU.
Univariate analysis of patient characteristics revealed patients with smaller BMI to have a significantly higher risk of reoperation for bleeding (p = 0.045). The other group of patients at a significant risk of needing reoperation for bleeding were the nonelective surgery patients. Off-pump CABG was not associated with any significant risk for reoperation. On multivariate analysis, BMI less than 25 kg/m2 (p = 0.003), nonelective surgery (p = 0.022), patients requiring 5 or more grafts (p = 0.035), and elderly patients were at a greater risk of needing reexploration for bleeding. Most studies looking at risk factors for bleeding after cardiac surgery have found increased risk in older patients, smaller body surface area, longer CPB times, greater number of distal anastomosis, dialysis dependant renal failure, and the use of the internal mammary artery [1, 3, 5, 6].
Our finding of an association between BMI less than 25 kg/m2 and increased reexploration for bleeding is similar to the findings from Dacey and colleagues [1] from the Northern New England Cardiovascular Disease Study Group. Those investigators demonstrated that reexplorations increased as body surface area decreased. The reasons behind this relationship are unclear but may be due to dilution of coagulation factors [1].
It is likely that both the mediastinal and pericardial fat have a tamponading effect on the small bleeders in the mediastinum. We also think that, as a group, patients with smaller BMI are less likely to tolerate major blood losses. Hence, the threshold for resternotomy is usually lower in these patients.
We were unable to find a significant relationship between CPB time and reexplorations for bleeding, although increasing number of grafts was a significant predictor irrespective of the use and duration of CPB. This association between number of grafts and reexploration can partly be explained by longer times on CPB, but may more realistically be due to an increased number of potential bleeding sites and to the overall complexity of the procedure.
Dacey and coworkers [1] found that both CPB duration and number of grafts were associated with reexploration for bleeding. This difference between both studies may be due to sample size, with the Dacey study having more than 8,000 patients.
Aspirin (in a dose of 75 mg to 300 mg daily) is a strong inhibitor of the platelet cycloxygenase, thus inhibiting the production of thromboxane A2. Thromboxane A2 is essential for the initiation of clot formation by platelets. This loss of function due to aspirin is permanent for the lifetime of the platelet. Because the average lifespan of platelets is about 7 days, the usual practice of stopping aspirin a week before surgery was considered appropriate. The association between bleeding and clotting abnormalities and various components of CPB and heparinization are very well known and documented. Cardiopulmonary bypass also tends to affect platelet function quite severely. These could be the reasons for the increased risk of bleeding seen in many studies of patients undergoing on-pump CABG [15, 16].
We undertook a propensity score match study to evaluate the effect of preoperative aspirin and heparin on the need for reexploration for bleeding. This analysis revealed that the preoperative use of aspirin and heparin were more common in patients reexplored for bleeding compared with a propensity-matched group who were not reexplored. After taking into account the use of CPB, this relationship still existed in on-pump CABG but disappeared for CABG patients who avoided CPB.
This finding concurs with previous work from our institution, by Srinivasan and coworkers [17], which showed that continued aspirin does not increase postoperative blood loss, resternotomy rates, and blood or blood product requirements in patients who undergo off-pump CABG. This would suggest that the interaction of preoperative aspirin or heparin with CPB is a significant cause for increased risk of resternotomy for bleeding.
The debate around aspirin use in conventional on-pump CABG is still undecided. Dacey and colleagues [18], in a study by the Northern New England Cardiovascular Disease Study Group, showed that preoperative aspirin significantly reduced mortality without increasing bleeding-related morbidity. However, the Veterans Administration Cooperative Study found higher rates of reoperation and bleeding when using preoperative aspirin [15].
The propensity score matching gave us the ability to look at outcomes of patients needing resternotomy. Although there was a trend toward a greater incidence of mortality and major morbidity in the resternotomy group compared with the propensity-matched control group, we did not find any significant difference in the mortality rates and major morbidity, including sternal wound infection, stroke, renal failure, and need for intraaortic balloon support, in these two groups. These patients were more likely to need inotopes postoperatively and had longer average ICU and postoperative stays.
Moulton and coworkers [5] found a significantly higher mortality rate and increased risk of renal failure, sepsis, and need for prolonged ventilation in the group needing reexploration. They concluded that reexploration is a significant multivariate indicator of increased morbidity and mortality in all patients, but more so in a selected low-risk subgroup of patients. They also felt that the amount of bleeding is a significant risk factor rather than the act of reexploration. Unsworth-White and coworkers [2] also found an association between reexploration and increased mortality and morbidity. A possible reason for the difference in outcomes of patients needing resternotomy for bleeding in our study compared with those of Moulton and Unsworth-White could be the "time-delay" factor. In our study, 58 of the 89 patients (65.2%) needing resternotomy were taken back within 12 hours of returning to the ICU. While no details regarding this time delay are available from the Moulton and Unsworth-White study, that is, as our study shows, one of the main causes for adverse outcomes after resternotomy for bleeding (Table 6).
There was a significantly greater incidence of mortality and major complications including stroke, renal failure, and longer ICU stay among patients who faced a greater delay (longer than 12 hours) in return to the operating theater for reexploration. That indicates the continued instability of these patients for a longer time, greater blood loss, and greater need for blood products. Although not statistically significant, the incidence of sternal wound infection is slightly greater in the group reexplored early (ie, within 3 hours). Many of the patients from this group were hemodynamically unstable and required emergency reopening in the ICU, rather than in the operating theater in a better environment, and that could explain the higher sternal wound infection rate in this group of patients.
Since conducting this study, we have strictly followed the protocol promulgated by Kirklin and Barratt-Boyes at our institution to promote early return to the operating theater for resternotomy for bleeding. Although this was the guiding protocol even before this study, since performing this study, we have adhered to its principles even more strictly to minimize the time delay and the risk that this delay poses.
There are some limitations, which may affect the conclusions drawn from our study. The primary limitation of the study is its retrospective nature. Propensity score adjustment is no substitute for a properly designed, randomized, controlled trial. The retrospective nature of the study cannot account for the unknown variables affecting the outcome that are not correlated strongly with measured variables. However, retrospective comparisons with propensity score adjustment are more versatile and offer a useful way of interpreting large amounts of audit data and seeking answers to questions that may present insuperable difficulties in the design of randomized, controlled trials.
Another limitation of the study is the small number of patients who required reexploration, especially while analyzing the impact of preoperative aspirin or heparin and the effect of time delay. We run the potential risk of type II errors. That is highlighted when looking at sternal wound infections in the resternotomy and control groups, where we have a p value more than 0.05, but the infection rate is almost double in the patients who required resternotomy. Previous work from our institution would suggest that reexploration for bleeding is associated with sternal wound infection [4].
A further limitation is that we only assessed the use of preoperative aspirin and heparin. The continued use of clopidogrel until the day of surgery has been a relatively recent phenomenon at our center, and during the study time period there were just 3 patients in the resternotomy group receiving clopidogrel. Hence, we were unable to evaluate its impact on resternotomy. However, this will be of interest in the future. A final limitation is that we do not have complete data on the use of antifibrinolytic agents. None of our patients undergoing CABG received aprotinin; however, a small proportion (about 5%) have been given tranexamic acid, 2 g, after being weaned from CPB, which was a reflection of the individual practice of two anesthetists.
In conclusion, our study reemphasizes the known risk factors of reexploration after CABG, including age, smaller BMI, greater number of grafts, and nonelective cases. It also highlights the role of preoperative aspirin and its association with a greater risk of bleeding after on-pump but not off-pump CABG. This finding is of importance as a greater number of patients are on aspirin until the day of surgery, and hence, there may be an associated increase in the incidence of resternotomy for bleeding. That may also represent one of the potential advantages of avoiding CPB in patients undergoing CABG, especially if they are at a higher risk for bleeding and continue to take aspirin until the day of surgery.
Our study shows that in most cases a surgical explanation for bleeding is apparent on reexploration. Also, on comparing similar groups of patients, resternotomy itself does not seem to add to the mortality and morbidity after CABG. One must remember that often these patients have several characteristics that put them at a greater risk of adverse outcomes after surgery. Our major finding is the direct link between the incidence of major complications and mortality after reexploration and the time delay to reexploration. We found that the outcomes are significantly worse and the mortality rate is greater if there is a delay of more than 12 hours to resternotomy after CABG.
On this basis, we would strongly recommend a policy of early reexploration for bleeding, as it does not seem to add to the risk and a cause is usually found. The major cause for poor outcome after resternotomy for bleeding is the associated time delay and not the resternotomy itself.
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Acknowledgments |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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