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Ann Thorac Surg 1995;59:664-667
© 1995 The Society of Thoracic Surgeons

Resternotomy for Bleeding After Cardiac Operation: A Marker for Increased Morbidity and Mortality

M. Jonathan Unsworth-White, FRCS, Alexander Herriot, MBCh, Oswaldo Valencia, MD, Jan Poloniecki, DPhil, E. E. John Smith, FRCS, Andrew J. Murday, FRCS, D. John Parker, FRCS, Tom Treasure, FRCS

Cardiothoracic Unit, St. George's Hospital, London, United Kingdom

Accepted for publication November 15, 1994.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Over a 2-year period from January 1, 1992, to December 31, 1993, of 2,221 patients undergoing cardiac operations in our unit, 85 (3.8%) were reopened for the control of bleeding (9 patients more than once). The incidence of resternotomy in coronary cases was 2.3%, but resternotomy was more than three times as likely in valve cases (odds ratio, 3.4; 95% confidence interval, 2.1 to 5.4). Previous cardiac operation was more common among resternotomy patients than among the remainder (18% versus 9%, respectively; p = 0.018). An identifiable source of bleeding was found in 57 of the 85 patients (67%), but a concurrent coagulopathy was common (45 patients). Resternotomy patients, as a group, had higher preoperative risk scores (Parsonnet) than did the other patients (p < 0.0001), stayed longer in the intensive care unit (p < 0.0001), and had greater requirements for intraaortic balloon counterpulsation (14% versus 3%) and hemofiltration (9% versus 3%) (p < 0.0001 and p < 0.01, respectively). Nineteen resternotomy patients (22%) died in the hospital, a proportion significantly greater than the risk assigned to this group of patients preoperatively (12.8%) (p = 0.008). In contrast, the observed mortality for the other 2,136 patients (5.5%) was significantly less (8.3%) (p < 0.00006). Multiple forward stepwise logistic-regression analysis confirmed resternotomy for excessive bleeding after cardiac operation to be a significant independent predictor of a prolonged stay in the intensive care unit (p < 0.0001), the need for intraaortic balloon counterpulsation (p < 0.0001), and death (p < 0.0001).


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Excessive bleeding after cardiac operations remains a major source of morbidity and a risk of death for patients. Such patients may require urgent resternotomy and are at greater risk from the hazards of transfusion reactions and blood-borne infections. There have been many studies examining the hemostatic damage inflicted by the cardiopulmonary bypass circuit and others considering the various strategies for blood conservation. However, there has not been a recent appraisal of the incidence of emergency resternotomy for the management of excessive bleeding after cardiac operations nor an assessment of the morbidity and mortality incurred by this group of patients.

Saint George's Hospital is a regional referral center for cardiac surgery. Over a 2-year period (January 1, 1992, to December 31, 1993), we conducted 2,221 cardiac operations, including routine coronary and valve procedures, complex aortic procedures, and cardiac transplantation. This study was performed to examine the incidence, underlying cause, and outcome of resternotomy for excessive bleeding after a cardiac operation in our unit.


   Patients and Methods
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
All patients who underwent cardiac operations during the 2-year period January 1, 1992, to December 31, 1993, were entered prospectively onto our computer database. For each patient, the database included a preoperative risk profile and a record of the patient's course in the cardiac intensive care unit (ICU). Using this source, we identified 85 patients who underwent emergency resternotomy for excessive bleeding. Nine patients were reopened more than once, but the data used for these patients in this study pertain only to the first resternotomy. We have calculated the resternotomy incidence for each operation type and a Parsonnet score for each patient. The Parsonnet scoring system [1] stratifies cardiac operations into levels of operative risk on the basis of various preoperative characteristics, and has been validated in British cardiac practice [2].

We recorded the interval between the patient's arrival in the cardiac ICU and return to the operating room for resternotomy, the blood loss, the nature of hemostatic factor replacement therapy, the coagulation profiles during bleeding, and the findings at resternotomy. We also recorded the clinical outcome for each patient, including the time spent in the ICU as well as the morbidity and survival rates.

All patients undergoing cardiac operation were screened before operation for coagulation abnormalities. This included history-taking and a clinical examination combined with coagulation studies (prothrombin time, activated partial thromboplastin time, and thrombin clotting time). Further hematologic tests were performed when indicated. Patients who were bleeding excessively postoperatively were screened again to search for correctable causes of their bleeding diathesis.

Most patients undergoing elective procedures were asked to discontinue aspirin therapy at least 5 days before admission for their operation. However, many of our patients were urgent referrals who were still receiving aspirin or intravenous heparin up until the time of operation. Hemostatic factors (antifibrinolytic agents and platelets or fresh frozen plasma) were not routinely given. Exceptions included anticoagulated heart transplant recipients, patients with infective endocarditis, and anticoagulated patients undergoing redo valve operations. Patients were anticoagulated before cardiopulmonary bypass with 3 mg/kg of sodium heparin (approximately, 3 U/mL), and the pump prime contained an additional 10,000 units. During bypass, anticoagulation was adjusted to maintain the activated clotting time at greater than 400 seconds. Heparin was reversed after decannulation with protamine sulfate on a 1:1 basis or until the activated clotting time had returned to within 20 seconds of its prebypass value. During bypass, all of the blood from the pericardial and pleural cavities was returned to the bypass circuit by means of cardiotomy suction. At the end of bypass, all remaining blood in the cardiotomy reservoir was returned to the patient. Postoperative autotransfusion of shed mediastinal blood was used in approximately 30% of our patients during the study period.

Statistical analysis was performed using Fisher's exact and Mann-Whitney tests and analysis of proportions, as described by Altman [3]. Multiple forward stepwise logistic-regression analysis was used to assess the influence of resternotomy on morbidity and mortality when Parsonnet scores were taken into account.

The decision to perform resternotomy was made by the surgeon responsible, in line with our published policy [4], which is essentially that as promulgated by Kirklin and Barratt-Boyes [5], as follows:

  1. Drainage of:
  2. Excessive bleeding that restarts (indicating a possible surgical cause).
  3. Sudden massive bleeding.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Patient Characteristics
Eighty-five patients underwent resternotomy for excessive bleeding (3.8% of the total undergoing cardiac operations). Their sex, age, and preoperative risk stratification (Parsonnet score) are summarized in Tables 1 and 2GoGo. The sex ratio and age distribution were not significantly different from those of the remaining patients. Taken as a group, the Parsonnet scores in the resternotomy patients were significantly higher than those in the remaining patients (Mann-Whitney, p < 0.0001).


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  		Table 1. . General Characteristics of Resternotomy Patients and Total Patient Population
 

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  		Table 2. . Parsonnet Score Distribution Among Resternotomy and Remaining Patients
 
The types of operations performed in these 85 patients are listed in Table 3Go. In comparing the findings for coronary and valve operations (with or without concurrent coronary artery grafting), valve patients were noted to be more likely to undergo resternotomy for the management of bleeding (p < 0.00006), with an odds ratio of 3.4 (95% confidence interval, 2.1 to 5.4).


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  		Table 3. . Distribution of Operation Types Among the Resternotomy Group and the Total Patient Population
 
Fifteen patients (18%) had undergone previous cardiac procedures. This contrasts with a figure of 9% for the remaining patients (p = 0.018). Of the 85 resternotomy patients, 8 were anticoagulated with warfarin and another 9 with unstable angina were receiving heparin infusions up until the time of operation. Five of these latter patients had also taken aspirin the day before operation, as had another 9 who were not otherwise anticoagulated.

Cause of Bleeding
Postoperative coagulation studies were performed in 78 patients before resternotomy, and results were abnormal in 71 (91%). Forty-five of these 71 patients had a surgically correctable cause for their bleeding, in addition to their coagulopathy.

Overall, a surgical cause of the bleeding was found in 57 of the 85 patients (67%). A surgical cause was defined as a clearly identifiable source, and these are listed in Table 4Go. Twenty-three patients were described as having a ``general ooze'' from the raw surfaces of the mediastinum without a surgical cause being found to explain their excessive blood loss.


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  		Table 4. . Findings at Resternotomy
 
The median blood loss before resternotomy, including drainage from the time of chest closure to arrival in the ICU, was 2,156 mL (interquartile range, 1,440 to 2,435 mL) and ranged between 400 and 7,910 mL. The median time to resternotomy was 6.4 hours (interquartile range, 3 to 9 hours), although there were 2 patients well outside this interquartile range: one patient collapsed after removal of his epicardial pacing wires on postoperative day 6 and the other had delayed cardiac tamponade 8 days after aortic valve replacement. The median hourly blood loss for patients with a surgical cause was 305 mL (interquartile range, 203 to 432 mL), and was 431 mL (interquartile range, 240 to 620 mL) for the nonsurgical bleeders (Mann-Whitney, p = 0.12).

Before being returned to the operating room, resternotomy patients received a median of 4 units of blood (interquartile range, 2 to 6 units). In addition, many patients received other hemostatic factors, as shown in Table 5Go.


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  		Table 5. . Hemostatic Factors Received by Resternotomy Patients
 
Morbidity and Mortality
The postoperative morbidity was considerable in this group of patients, and the types are summarized in Table 6Go. Thirty-three patients required inotropic support (balloon counterpulsation in 12 of these-14% of the resternotomy patients), and 8 patients (9%) required hemofiltration after resternotomy. In comparison, among the 2,136 nonresternotomy patients, only 66 received intraaortic balloon counterpulsation (3%) and only 71 patients (3%) required hemofiltration (Fisher's exact test, p < 0.0001 and p < 0.01, respectively). Consistent with the increased morbidity associated with resternotomy, the ICU stay was also significantly greater in patients reopened for bleeding (Mann-Whitney, p < 0.0001) (Table 7Go).


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  		Table 6. . Morbidity After Resternotomy for Bleeding
 

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  		Table 7. . Length of Stay in Intensive Care Unit
 
The mortality was also high in the resternotomy group. Nineteen patients (22%) died in the hospital, a proportion significantly greater than the death rate observed for the remaining patients (p < 0.00006). Not all of this excess mortality is accounted for by the higher preoperative Parsonnet risk scores in the patients who ultimately required resternotomy. The observed mortality for these patients was significantly greater than the preoperative risk of 12.8% that was allocated to this group (p = 0.008). In contrast, the observed mortality for the 2,136 patients who did not undergo resternotomy was significantly less than the preoperative risk (5.5% versus 8.3%; p < 0.00006).

Multiple forward stepwise logistic-regression analysis (taking the Parsonnet scores into account) confirmed resternotomy for excessive bleeding after cardiac operations to be a significant independent predictor of prolonged ICU stay (p < 0.0001), the need for intraaortic balloon counterpulsation (p < 0.0001), and death (p < 0.0001). The independent prediction of hemofiltration was of borderline significance (p = 0.05).


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Continuing blood loss from bypass graft side branches, anastomotic sites, and other identifiable sources is compounded by a multifactorial hemostatic defect [6]. In this series of resternotomy patients, more than half were found to have both a surgical cause for their bleeding and an abnormality in their clotting screen. Twenty-seven of these patients were either fully anticoagulated before operation or had continued receiving aspirin up to the day of operation, which has been shown to be related to an increased postoperative blood loss and increased resternotomy risk [7].

Our overall resternotomy rate of 3.8% is in keeping with that cited for other published series [8, 9], and the rate for coronary operations is relatively low. These rates demonstrate a dramatic improvement since the early days of extracorporeal bypass for cardiac procedures, when resternotomy rates in excess of 15% were reported [10].

The age and sex profiles between the resternotomy and nonresternotomy patients were comparable, but the preoperative Parsonnet scores were significantly higher in the resternotomy group. The Parsonnet risk stratification includes operation type and redo operations in its additive model, and therefore part of this difference is accounted for by the distribution of these variables in our resternotomy set. Patients undergoing valve procedures were more than three times as likely to undergo resternotomy for bleeding than were patients undergoing coronary grafting, and 18% of the resternotomy patients had undergone redo cardiac procedures, compared with only 9% in the remainder. This emphasizes the importance of considering the case mix when comparing resternotomy rates among cardiac units.

The burden of morbidity and mortality for patients reopened for hemorrhage is considerable. More than 1 in 5 resternotomy patients in our series subsequently died and many more suffered considerable morbidity. The cost to the unit in terms of added operating room time, extra blood products, invasive interventions, and prolonged ICU stay has been large. Indeed, we have shown in this study that intraaortic balloon counterpulsation and hemofiltration were employed more commonly and that the ICU stay was significantly longer in patients reopened for bleeding.

Is resternotomy for the management of bleeding an independent risk factor for morbidity and mortality after cardiac operations? Parsonnet scores allow us to compare the preoperative risk and observed mortality rates. The observed mortality rate for our resternotomy patients was significantly greater than the risk allocated by the Parsonnet model; that for the remainder was significantly less. Logistic regression modeling, taking Parsonnet scores into account, has confirmed that, not only is resternotomy for excessive bleeding an independent risk factor for death, but also for a prolonged ICU stay and the need for intraaortic balloon counterpulsation, and possibly also for the need for postoperative hemofiltration.

In summary, we have shown that the more complicated cases are at greater risk for requiring resternotomy for bleeding, and that resternotomy is a significant independent marker for morbidity and mortality after cardiac operations. This is in keeping with the concept of a general inflammatory response to cardiopulmonary bypass, which might reasonably be expected to link extensive disruption of the hemostatic mechanisms with other end-organ damage.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
Mr M. Jonathan Unsworth-White was supported by the British Heart Foundation during the conduct of this study.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Treasure, Department of Cardiothoracic Surgery, St. George's Hospital, London SW17 ORE, UK.


   References
Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Parsonnet V, Dean D, Bernstein AD. A method of uniform stratification of risk for evaluating the results of surgery in acquired adult heart disease. Circulation 1989;79:1-3–12.[Abstract/Free Full Text]
  2. Nashef SAM, Carey F, Silcock MM, Oommen PK, Levy RD, Jones MT. Risk stratification for open heart surgery: trial of the Parsonnet system in a British hospital. BMJ 1992;305:1066–7.
  3. Altman DG. Practical statistics for medical research. London: Chapman and Hall, 1991:232–5.
  4. Kallis P, Tooze JA, Talbot S, Cowans D, Bevan DH, Treasure T. Aprotinin inhibits fibrinolysis, improves platelet adhesion and reduces blood loss. Eur J Cardiothorac Surg 1994;8: 315–23.[Abstract]
  5. Kirklin JW, Barratt-Boyes BG. Cardiac surgery. New York: Wiley, 1986:158–9.
  6. Woodman RC, Harker LA. Bleeding complications associated with cardiopulmonary bypass. Blood 1990;76:1680–97.[Abstract/Free Full Text]
  7. Kallis P, Tooze JA, Talbot S, Cowans D, Bevan DH, Treasure T. Pre-operative aspirin decreases platelet aggregation and increases post-operative blood loss: a prospective, randomised, placebo controlled, double blind clinical trial in 100 patients with chronic stable angina. Eur J Cardiothorac Surg 1994;8:404–9.[Abstract]
  8. Kaiser GC, Naunheim KS, Fiore AC, et al. Reoperation in the intensive care unit. Ann Thorac Surg 1990;49:903–7.[Abstract]
  9. Talamonti MS, LoCicero J, Hoyne WP, Sanders JH, Michaelis LL. Early reexploration for excessive postoperative bleeding lowers wound complication rates in open heart surgery. Am Surg 1987;53:102–4.[Medline]
  10. Craddock DR, Logan A, Fadali A. Reoperation for haemorrhage following cardiopulmonary by-pass. Br J Surg 1968;55:17–20.[Medline]



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L. J. Dacey, J. J. Munoz, Y. R. Baribeau, E. R. Johnson, S. J. Lahey, B. J. Leavitt, R. D. Quinn, W. C. Nugent, J. D. Birkmeyer, G. T. O'Connor, et al.
Reexploration for Hemorrhage Following Coronary Artery Bypass Grafting: Incidence and Risk Factors
Arch Surg, April 1, 1998; 133(4): 442 - 447.
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M. J. Moulton, L. L. Creswell, M. E. Mackey, J. L. Cox, and M. Rosenbloom
REEXPLORATION FOR BLEEDING IS A RISK FACTOR FOR ADVERSE OUTCOMES AFTER CARDIAC OPERATIONS
J. Thorac. Cardiovasc. Surg., May 1, 1996; 111(5): 1037 - 1046.
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