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Ann Thorac Surg 2008;86:1167-1173. doi:10.1016/j.athoracsur.2008.06.029
© 2008 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Effects of Shed Mediastinal Blood on Cardiovascular and Pulmonary Function: A Randomized, Double-Blind Study

Munir Boodhwani, MD, MMSc, Howard J. Nathan, MD, Thierry G. Mesana, MD, PhD, Fraser D. Rubens, MD, MS*, Cardiotomy Investigators

Divisions of Cardiac Surgery and Cardiac Anesthesia, University of Ottawa Heart Institute, Ottawa, Ontario, Canada

Accepted for publication June 9, 2008.

* Address correspondence to Dr Rubens, Division of Cardiac Surgery, H3401, 40 Ruskin St, Ottawa, Ontario, K1Y 4W7, Canada (Email: frubens{at}ottawaheart.ca).


Cardiothoracic anesthesiology: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Shed mediastinal blood during cardiopulmonary bypass (cardiotomy blood) contains fat, particulate matter, and vasoactive mediators that can adversely affect the pulmonary and systemic vasculature, as well as impair gas exchange. Our aim was to evaluate the effects of processing cardiotomy blood on cardiovascular and pulmonary function after cardiac surgery.

Methods: Patients undergoing coronary artery bypass or aortic valve surgery, or both, using cardiopulmonary bypass were randomly allocated to receiving processed (treated, n = 132) or unprocessed shed blood (control, n = 134) In the treated group, shed blood was processed by centrifugation, washing, and additional filtration. Pulmonary function, arterial and venous blood gases, and hemodynamics were measured before, immediately after, and 2 hours after cardiopulmonary bypass in a consecutive subset of patients (n = 154). Patients and treating physicians were blinded to treatment assignment.

Results: Preoperative characteristics were similar between groups. There were no significant differences between groups in indexes of pulmonary mechanical function at any of the measured time points. Patients in the treated group demonstrated reduced pulmonary and systemic vascular resistance (both p < 0.01) as well as increased cardiac index in the perioperative period (2.6 ± 0.07 versus 2.3 ± 0.06 L · min–1 · m–2 at 2 hours after CPB, p = 0.004). Larger volumes of cardiotomy blood were associated with greater changes in systemic and pulmonary vascular resistance. Indicators of pulmonary gas exchange were similar between groups at all measured time points. Treated patients demonstrated a trend toward reduced length of ventilation (11.0 ± 1.9 versus 13.9 ± 2.4 hours, p = 0.12).

Conclusions: Processing of shed mediastinal blood improves cardiopulmonary hemodynamics and may reduce ventilatory requirements after cardiac surgery.

Cardiopulmonary bypass (CPB) is a key technology for most cardiac surgical procedures. However, its use is associated with a number of adverse sequelae [1, 2]. It is now recognized that one of the major contributors to CPB-induced morbidity is the recirculation of shed pericardial and mediastinal blood, which is typically suctioned from the operative field back to the CPB circuit (cardiotomy blood). This blood has been shown to be a major contributor to thrombin generation during CPB [3], and it has been demonstrated to be a major source of fat [4], particulate matter [5, 6], and vasoactive mediators [7, 8].

Reinfusion of unprocessed cardiotomy blood can theoretically lead to increased bleeding [3, 9, 10], and it may adversely affect the pulmonary and systemic vasculature [11]. Processing of cardiotomy blood, through centrifugation and additional filtration, can potentially improve the quality of the transfused blood and reduce associated adverse effects [11–14]. Despite the theoretical advantages of this approach, no adequately powered, randomized controlled trials assessing clinically relevant endpoints have been reported to date. As a result, there continues to be considerable practice variation in the management of cardiotomy blood in cardiac surgical centers [15].

The Cardiotomy Trial [16] was a randomized, double-blind study undertaken to evaluate whether processing of cardiotomy blood with centrifugation and filtration affected postoperative neurocognitive outcomes as well as bleeding and transfusion rates after cardiac surgery. We found that processing of cardiotomy blood had no effect on postoperative neurocognitive deficits, but did result in increased postoperative bleeding and blood product use.

The aim of this substudy was to determine the effects of cardiotomy blood processing on prospectively identified endpoints evaluating cardiovascular function, pulmonary mechanics, and gas exchange in a subset of the total cohort. We hypothesized that processing of cardiotomy blood would result in improved cardiovascular hemodynamics as well as improved pulmonary gas exchange, without change in mechanical pulmonary function.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Population
The study protocol was approved by the Human Research Ethics Board of the University of Ottawa Heart Institute, and written informed consent was obtained from all patients. A total of 266 patients undergoing isolated, nonemergent coronary artery bypass surgery or aortic valve replacement, or both, using CPB at the Heart Institute were recruited. Patients with known neurologic deficits, preoperative coagulopathy, bleeding diathesis, or thrombocytopenia (<140,000/µL) as well as those with renal insufficiency (creatinine > twice normal) or hepatic insufficiency (elevated liver function tests, elevated baseline international normalized ratio) were excluded. A subset of 154 consecutive patients (n = 77 per group) underwent additional cardiovascular and pulmonary evaluation and serve as the cohort for this analysis.

Randomization and Blinding
Randomization, supervised by the data manager, was computer-generated in blocks of 8 (SAS version 8.2; SAS Institute, Cary, North Carolina) stratified for age (<75 years), and the assignment was concealed until the interventions were assigned. A sealed opaque envelope containing the treatment allocation was opened by the research coordinator just before the patient received heparin prior to the initiation of CPB. The perfusionist was informed of the treatment assignment. The patients and all clinical and research staff were blinded to treatment assignment. Intraoperative blinding of all members of the surgical team (except for the perfusionist) was accomplished by the positioning of an opaque drape over the CPB circuit and the cell-saving device. All intraoperative decisions to transfuse during CPB were made by the anesthetist, who was unaware of treatment assignment.

Intraoperative Protocol
A narcotic-based anesthetic was used. After sternotomy and conduit preparation, patients were administered heparin to achieve an activated clotting time greater than 400 s. Cardiopulmonary bypass was conducted using a roller pump, a membrane oxygenator (COBE CML Duo; COBE Cardiovascular, Arvada, Colorado), a 43-µm arterial filter (COBE Sentry with PrimeGard), a closed venous reservoir bag, an ascending aortic cannula, and a two-stage venous cannula. The circuit was primed with 1,300 mL Ringer's Lactate. Bypass flows were maintained at 2.4 to 3.2 L · m–2 · min–1.

The heart was arrested using antegrade cardioplegia, and topical cooling was used at the discretion of the surgeon. During cardiac ischemia, the body temperature was reduced to a systemic temperature of 34°C, and at the completion of the procedure, patients were rewarmed taking care to never exceed 37°C (nasopharyngeal).

Study Interventions
During CPB in the control group, suctioned blood was collected in the cardiotomy reservoir and transferred directly to the oxygenator after passage through the integrated cardiotomy filter (40 µm). In the treatment group, cardiotomy blood was diverted into the cell-saving device for centrifugal washing (BRAT; COBE Cardiovascular) and then readministered into the pump after passage through a leukoreduction filter, used to augment fat globule and leukocyte removal (Pall LeukoGuard RS Filter; Pall Biomedical Products, East Hills, New York).

Assessment of Cardiopulmonary Function
Indicators of cardiovascular and pulmonary function were measured at the time of anesthetic induction, immediately after CPB, and 2 hours after CPB. Indexes of pulmonary mechanics recorded included tidal volume, peak inspiratory pressure, and positive end-expiratory pressure. Arterial and mixed venous blood gases were measured. In addition to heart rate and blood pressure, cardiac index was measured, and systemic and pulmonary vascular resistances were calculated using a Swan-Ganz pulmonary artery catheter. Dynamic pulmonary compliance, pulmonary shunt (QS/QT) oxygen extraction ratio, alveolar-arterial oxygen gradient, and oxygen delivery index were calculated as previously reported [17].

Postoperative Management
All clinical staff were blinded to treatment assignment. Various aspects of postoperative care including surgical reexploration, blood product use, extubation, and intensive care unit discharge were conducted according to predefined and previously published protocols used at the Ottawa Heart Institute [18]. Serum creatine kinase was measured 8 hours after surgery, and troponin T was measured for creatine kinase greater than 800 IU/L or if clinically indicated. Perioperative myocardial infarction was diagnosed by the treating physician in the presence of new Q waves longer than 0.04 s in two or more contiguous leads, and elevations in cardiac enzymes.

Statistical Analysis
Descriptive data are depicted as mean ± SD for normally distributed variables and median (interquartile range) for variables not following a Gaussian distribution. Categorical variables are shown as the number (%). Mixed models were used to analyze repeated measures data utilizing an unstructured covariance matrix. The model included terms for the effect of time, treatment, and time by treatment interaction, which evaluated differential change over time in treated versus control subjects. Multivariable linear regression models were used to determine predictors of improved postoperative cardiac index. Covariates were included the model if there was a presence of a univariate association, using a liberal threshold of p less than 0.2, or if there was sufficient biologic rationale. No automated selection algorithms were used, but models were construced to be parsimonious and to minimize confounding and collinearity. Nonsignificant covariates (p > 0.05) were excluded from the final model. The relationship between the amount of cardiotomy blood and postoperative vascular resistance was explored using Spearman correlation. Statistical analyses were performed using SAS v.9.1 (SAS Institute, Cary, North Carolina).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Patient Population
Patient screening, recruitment, and evaluation are depicted in Figure 1. Baseline characteristics were similar between groups (Table 1). There were no significant differences in intraoperative variables including CPB time, cardiac ischemia time, number of distal anastomoses, and types of conduits used (Table 2). The volume of cardiotomy blood collected was 704 ± 548 mL in the control group and 830 ± 690 mL in the treatment group (p = 0.21).


Figure 1
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  		Fig 1. Patient screening and enrollment for the Cardiotomy Trial. (CNS = central nervous system; Opcab = off-pump coronary artery bypass graft surgery.)

 

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  		Table 1 Preoperative Data a
 

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  		Table 2 Intraoperative and Postoperative Data a
 
Pulmonary Function
Indicators of mechanical pulmonary function and gas exchange were evaluated before CPB, immediately after CPB, and 2 hours after CPB (Table 3). There were no differences in indexes of mechanical pulmonary function including tidal volume, peak inspiratory pressure, and positive end-expiratory pressure at any of the three time points. Compared with baseline, impaired oxygen exchange was evident in both groups immediately after CPB. These impairments manifested as significant reductions in arterial PO2 and oxygen delivery index, and an increase in alveolar-arterial oxygen gradient, pulmonary shunt, and oxygen extraction ratio (all p < 0.01). These indexes of pulmonary gas exchange improved 2 hours after CPB. However, there were no significant differences between the control and treated patients.


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  		Table 3 Pulmonary Function Variables a
 
Cardiovascular Effects
Patients receiving processed cardiotomy blood demonstrated a reduction in pulmonary and systemic vascular resistance both immediately and 2 hours after CPB termination (Fig 2). This was accompanied by improved cardiac index in treated patients after surgery (2.6 ± 0.6 versus 2.3 ± 0.5 L · min–1 · m–2, p = 0.004; Fig 3). Seventeen preoperative and intraoperative variables were used to construct a parsimonious multivariable linear regression model predicting postoperative cardiac index (2 hours after CPB). This multivariable analysis revealed that shorter duration of cardiac ischemia (β = –0.004 per minute of cardiac ischemia, p = 0.02), higher hemoglobin level (β = 0.009 per 1 g/L increase in hemoglobin, p = 0.003), and being in the treatment group (β = 0.25, p = 0.007) were the only significant independent predictors of improved postoperative cardiac index.


Figure 2
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  		Fig 2. (A) Pulmonary vascular resistance (PVR) and (B) systemic vascular resistance (SVR) in control patients (diamonds) and treated patients (squares [mean ± SEM; *p < 0.01]). Patients receiving processed cardiotomy blood (treated) demonstrated lower systemic and pulmonary vascular resistance in the postoperative period. (CPB = cardiopulmonary bypass.)

 

Figure 3
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  		Fig 3. Cardiac index measured before cardiopulmonary bypass (Pre-CPB), immediately after (post-CPB), and 2 hours after CPB in control patients (solid bars) and treated patients (shaded bars [mean ± SEM]). Treated patients had improved cardiac index in the perioperative period (*p = 0.07; **p = 0.004).

 
Exploratory analyses revealed a dose-dependent relationship between cardiotomy blood volume and postoperative hemodynamics. The magnitude of reduction in systemic vascular resistance (spearman r = –0.16, p = 0.04) as well as amount of pheynlephrine used (r = 0.29, p < 0.001) was greater with higher volumes of cardiotomy blood collected. The relationship between systemic vascular resistance and volume of cardiotomy blood was stronger in the treatment group (r = –0.26, p = 0.02), and a similar trend was also observed in association with pulmonary vascular resistance in the treatment group (r = –0.21, p = 0.08).

Clinical Outcomes
Postoperative outcomes are depicted in Table 2. There was no difference in mortality between groups. Four patients (5.2%) in the control group had clinically diagnosed perioperative myocardial infarction compared with none in the treated group (p = 0.12). Postoperative creatine kinase levels were also significantly higher in control patients (p = 0.003), but troponin levels, when measured, were similar between groups. Furthermore, use of inotropes and the intra-aortic balloon pump was similar between groups. There was a trend toward reduced length of ventilation in patients receiving processed cardiotomy blood (11.0 ± 1.9 versus 13.9 ± 2.4 hours, p = 0.12).


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Management of shed cardiotomy blood during CPB remains a controversial issue, with significant practice variation among perfusionists, surgeons, and centers [15]. In this randomized, double-blind study, we sought to evaluate the effects of cardiotomy blood processing (centrifugal washing and lipid/leukocyte filtration) on cardiovascular and pulmonary function. We found that processing of cardiotomy blood had no effect on mechanical pulmonary function or on indexes of pulmonary gas exchange. However, significant hemodynamic changes were observed as a result of cardiotomy blood processing and included lower systemic and pulmonary vascular resistances and improved cardiac index in the postoperative period. While clinical outcomes were largely similar between groups, we observed a trend toward reduced ventilation time in patients receiving processed cardiotomy blood. In summary, processing of cardiotomy blood improves cardiovascular and hemodynamic performance without significant improvements in mechanical pulmonary function or gas exchange.

The use of CPB induces an inflammatory response that has been associated with postoperative complications that can involve the heart, lungs, kidneys, the vasculature, and the brain [2, 19]. Among other factors, cardiotomy blood has been identified to be an important pool of proinflammatory mediators, and its unprocessed retransfusion has been shown to cause elevations in serum levels of multiple cytokines including tumor necrosis factor-{alpha}, interleukin-6, and C3a [7, 8]. These cytokines can have variable vascular effects and can also have depressive effects on the myocardium. Westerberg and colleagues [11] have further demonstrated that reinfusion of unprocessed cardiotomy blood, while on CPB, is associated with an acute reduction in systemic vascular resistance and hypotension, an effect that is correlated with levels of tumor necrosis factor-{alpha}. These studies have clearly demonstrated the proinflammatory and vasoactive nature of cardiotomy blood, and the findings from our study further support this idea.

We found that the retransfusion of unprocessed cardiotomy blood led to a 30% elevation in systemic vascular resistance, which was evident immediately after CPB and persisted in the postoperative period. A similar increase was observed in pulmonary vascular resistance. Importantly, these changes were also associated with reduced cardiac performance in the control group. Processing of cardiotomy blood, on the other hand, was associated with a 13% increase in cardiac index in the postoperative period. These differences were present despite similar use of vasopressors (phenylephrine) while on CPB and similar incidence of inotrope and vasopressor use in the postoperative period between groups. These observations are further strengthened by the presence of a dose-dependent effect, namely, larger volumes of cardiotomy blood transfused were associated with greater changes in systemic and pulmonary vascular resistances. Our findings of increased systemic and pulmonary vascular resistances in the control group are in contrast with Westerberg and colleagues [11], who demonstrated a reduction in systemic vascular resistance. Whereas their study evaluated focused on the effects of retransfusion during CPB, we report the effects during the hours after CPB. The difference in the time of evaluation may account for the discrepant findings and may be explained by the elaboration of cytokines with different vasoactive profiles in the post-CPB period.

In this study, the control group also demonstrated higher levels of creatine kinase in the postoperative period, but the levels of the cardiac-specific marker, troponin T, were similar between groups. The incidence of clinically diagnosed myocardial infarction was also nonsignificantly higher in the control group; however, this study was not powered to detect significant differences in this endpoint. The role of cardiotomy blood processing in reducing myocardial injury is thus plausible and cannot be ruled out. A sensitivity analysis reconfirmed that the hemodynamic findings remained significant even after exclusion of the 4 patients with perioperative myocardial infarctions. Lastly, a multivariable analysis identified shorter duration of cardiac ischemia, higher hemoglobin levels, and cardiotomy blood processing as independent predictors of improved postoperative cardiac performance.

In addition to inflammatory mediators, cardiotomy blood has been demonstrated to contain fat, activated leukocytes, and particulate matter from the surgical field [5, 6, 12]. When transfused into the venous circulation, it can result in pulmonary microemboli that have the potential to impair pulmonary gas exchange. The presence of activated leukocytes in cardiotomy blood has also been suggested to contribute to lung injury [20]. Processing of cardiotomy blood, which involves washing and the use of a lipid- and leukocyte-removing filter, can ameliorate these effects by reducing the levels of circulating cytokines (eg, tumor necrosis factor-{alpha} [11] and thromboxane-B2 [21]) and free radicals [22] as well as the number of activated leukocytes and fat microemboli [4, 14, 21, 22]. Thus, processing may be expected to have a beneficial effect on postoperative pulmonary function. A number of measures of pulmonary mechanics and gas exchange have been used in the postoperative setting and were utilized in this study [17]. We found, as has been previously demonstrated, that indicators of pulmonary gas exchange worsened after CPB, but we did not observe any significant differences between the control and treatment groups, suggesting that this is likely not a clinically significant phenomenon. We did, however, observe a trend toward shorter ventilation times among the treated patients, which may be the result of improved hemodynamics in this population.

The Cardiotomy Trial [16] was a randomized, double-blind study of 266 patients with the primary outcome of evaluating the effects of cardiotomy blood processing on neurologic outcome, coagulation variables, and bleeding. We have recently reported that processing of cardiotomy blood does not reduce the incidence of neurocognitive deficits, but does result in increased postoperative bleeding and transfusion requirements. The increased bleeding is associated with impairments in various coagulation factors and is likely due to the loss of coagulation factors that occurs with processing. This substudy evaluated the effects of cardiotomy blood processing on cardiovascular and pulmonary function and demonstrates the beneficial effects of processing on postoperative hemodynamic performance. The results of the Cardiotomy Trial thus reemphasize the complex and multifaceted effects of cardiotomy blood transfusion and its processing on multiple organ systems. The clinician, therefore, needs to incorporate this information into a tailored approach to the use of this intervention in selected populations. While the hemodynamic benefits may seem small and clinically insignificant for low-risk populations, processing may have important implications for patients with significant left ventricular dysfunction. On the other hand, patients with normal left ventricular function who are at high risk of bleeding complications may benefit from unprocessed retransfusion. Lastly, another alternative is to discard the cardiotomy blood altogether. However, this is only feasible when it is a small volume.

In conclusion, processing of cardiotomy blood through centrifugation, washing, and filtration results in reduced systemic and pulmonary vascular resistance and improved cardiac performance in the perioperative period. A tailored approach to the management of cardiotomy blood should be utilized, keeping in mind the different effects on different organ systems, to provide the maximum benefit to patients.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
Cardiotomy Investigators: Cardiac surgery: Pierre Bedard, William Goldstein, Paul Hendry, Buu-Khanh Lam, Roy Masters, Thierry Mesana, Fraser Rubens, and Marc Ruel. Cardiac anesthesia: Michael Bourke, Charles Cattran, Gilles de la Salle, Jean-Yves Dupuis, Mark Hynes, Stephan Lambert, Bernie MacDonald, Marise Mathieu, Howard Nathan, Donna Nicholson, James Robblee, Peter Wilkes, and Homer Yang. Perfusion: Andrew Babaev, Dean Belway, Geoffrey Dix, Gurinder Gill, Brian Henley, Debbie Hubble, Jason Kennedy, Nusrat Saleem, and Moira Watson. Epidemiology: George Wells and Kathryn Williams. Data Safety Monitoring Board: Stephen Fremes (University of Toronto), William Ghali (University of Calgary), and David Mazer (University of Toronto). Research staff: Sharon Finlay, Suzanne Picard, Marlie Poirier, Denyse Winch, Denise Wozny, and Rosendo Rodriguez.

This trial was funded by Clinical Trials Grants MCT-44149 and MCT-70887 from the Canadian Institute of Health Research. The LeukoGuard RS filters were provided by Pall Biomedical (East Hills, New York).


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Rubens FD, Mesana T. The inflammatory response to cardiopulmonary bypass: a therapeutic overview Perfusion 2004;19(Suppl 1):5-12.
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  16. Rubens FD, Boodhwani M, Mesana T, Wozny D, Wells G, Nathan HJ. The Cardiotomy Trial: a randomized, double-blind study to assess the effect of processing of shed blood during cardiopulmonary bypass on transfusion and neurocognitive function Circulation 2007;116:I89-I97.[Medline]
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