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Ann Thorac Surg 2006;82:1747-1756
© 2006 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Red Cell Transfusion is Associated With an Increased Risk for Postoperative Atrial Fibrillation

Colleen Gorman Koch, MD, MSa,*, Liang Li, PhDb,c, David R. Van Wagoner, PhDc,d, Andra I. Duncan, MDa, A. Marc Gillinov, MDc,e, Eugene H. Blackstone, MDb,c,e

a Department of Cardiothoracic Anesthesia, The Cleveland Clinic Foundation, Cleveland, Ohio
b Department of Quantitative Health Sciences, The Cleveland Clinic Foundation, Cleveland, Ohio
d Department of Cardiovascular Medicine, The Cleveland Clinic Foundation, Cleveland, Ohio
e Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio
c Atrial Fibrillation Innovation Center (AFIC), The Cleveland Clinic Foundation, Cleveland, Ohio

Accepted for publication May 11, 2006.

* Address correspondence to Dr Koch, Department of Cardiothoracic Anesthesia (G-3), The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195. (Email: kochc{at}ccf.org).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Atrial fibrillation (AF) is a common complication after cardiac surgery and is associated with increased resource utilization. Recent evidence supports a role of inflammation in the development of AF. It is also known that red blood cell transfusion modulates inflammation by increasing plasma levels of inflammatory markers. Therefore, we tested the hypothesis that red blood cell transfusion increases the risk of postoperative AF for patients undergoing cardiac surgery.

METHODS: Between February 2002 and January 2005, 5,841 patients underwent isolated coronary artery bypass grafting with or without valve replacement. Patient and procedural variables associated with development of new-onset AF were identified by logistic regression. Propensity score matching was used to confirm results.

RESULTS: In addition to older age, prior history of AF, higher preoperative hematocrit, ß-blocker withdrawal, longer aortic clamp time, valve surgery, and intensive care unit inotropic usage, intensive care unit red blood cell transfusion increased risk for AF (odds ratio per unit transfused, 1.18; 95% confidence limits, 1.14, 1.23; p < 0.0001). For the 1,360 propensity-matched pairs, intensive care unit red blood cell transfusion was associated with a significant increase in new-onset AF (620 [46%] versus 522 [38%]; p < 0.001).

CONCLUSIONS: Intensive care unit red blood cell transfusion is associated with increased occurrence of postoperative AF after cardiac surgery. This factor should be considered in identifying patients who might benefit from prophylaxis to prevent this common postoperative complication.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
New-onset atrial fibrillation (AF) occurs in 10% to 43% of patients in-hospital after cardiac surgical procedures [1–10]. It has been reported to contribute to increased morbidity [1, 7], hospital length of stay [1, 3, 8], and resource utilization [1, 3, 8]. Although demographic [3, 5, 11, 12], clinical [2, 3, 7, 8], electrophysiologic substrates [2, 11, 13], and perioperative risk factors [1–3, 6–8, 14, 15] have been identified, the mechanism by which cardiac surgery predisposes patients to AF is unknown.

Recent evidence supports an inflammatory mechanism in the development of AF [16–19]. Red blood cell (RBC) transfusion modulates the inflammatory response to cardiac surgery by changing plasma concentrations of inflammatory mediators and augmenting the inflammatory response [20]. Therefore, we tested the hypothesis that RBC transfusion increases risk of postoperative AF for patients undergoing cardiac surgery with cardiopulmonary bypass. Our secondary objective was to examine whether the relationship was consistent for procedures performed without cardiopulmonary bypass (off-pump).


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patients and Data
Between February 2002 and January 2005, 5,841 patients underwent isolated coronary artery bypass grafting (CABG) with or without valve procedures on cardiopulmonary bypass. During the same time, 451 patients underwent off-pump CABG. Perioperative variables and blood component utilization forms were prospectively collected concurrently with patient care and entered into the Cardiothoracic Anesthesia Registry. The similarly concurrent Cardiovascular Information Registry was used for additional data. Both databases have been approved for research by our institutional review board, and individual patient consent was waived.

End Points
New-onset postoperative AF was defined as electrocardiographically demonstrated AF requiring treatment anytime during the hospital stay. All patients had continuous heart rhythm monitoring by means of telemetry throughout their hospital stay.

Statistical Methods
Unadjusted comparisons by AF and transfusion status for both on-pump and off-pump patients were examined with two-sample Student's t test, Wilcoxon rank-sum test, Fisher's exact test, or {chi}2 test as appropriate. Because missing values for variables were rare, mean imputation was used for preoperative hematocrit in 106 patients, aortic clamp time in 91, and length of intensive care unit (ICU) stay for 4 in the on-pump population. Preoperative hematocrit valves were imputed for 11 patients in the off-pump population. Total RBC transfused was truncated at 10 or more units.

On-pump population
A logistic regression model was developed to identify patient and procedural variables associated with development of new-onset postoperative AF. Baseline variables in Table 1 as well as a number of interaction terms were examined. The number of units of RBC transfused in the operating room and in the ICU were analyzed separately, which permitted us to examine whether there was a risk-adjusted dose-dependent relationship between each unit of RBC transfused and new-onset AF in each setting. Backward elimination and stepwise model selection resulted in the same models.


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  		Table 1. Baseline Variables and Operative Factors by Postoperative New-Onset Atrial Fibrillation for the On-Pump Population a
 
To confirm the influence of transfusion on AF, we calculated propensity scores, in logit units, from a logistic model that included all variables contained in Table 1 for on-pump population [21, 22]. The propensity scores represent a summary of all baseline characteristics for each observation. Patients who received and did not receive ICU RBC transfusions were matched [23]. Before propensity matching of the on-pump population, 1,671 patients received RBC transfusions in the ICU and 4,170 did not. Greedy matching selected 1,360 propensity-matched pairs. Comparisons were made between the propensity-matched pairs using Student's t test or Wilcoxon rank-sum test for continuous variables and {chi}2 test or Fisher's exact test for categorical variables.

Off-pump population
Because our results demonstrated a different relationship between operating room transfusion and ICU transfusion, we performed a separate analysis of the off- pump population to examine whether results of transfusion were consistent. Using similar logistic and propensity-based methods; we examined the influence of RBC transfusion on postoperative AF. For the off-pump patients before matching, 136 patients received an ICU RBC transfusion and 315 did not. Greedy matching selected 120 propensity-matched pairs.

Isolated coronary artery bypass grafting population
Similar statistical methodology was applied separately to the isolated CABG data set for comparison with the off-pump CABG population.

The authors had full access to the data and take responsibility for its integrity. All authors have read and agree to the manuscript as written. All results were obtained using SAS 8.2 software (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
On-Pump Population
Thirty-seven percent (2,174) of patients had postoperative new-onset AF. The profile for patients who had AF was substantially different with regard to demographics, laboratory values, comorbid conditions, and perioperative factors compared with those who did not have AF (Table 1). Among the patients who had AF, the most common time of occurrence was postoperative day 2. A majority of patients had an ICU length of stay of 1 day (Fig 1).


Figure 1
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  		Fig 1. (A) Postoperative intensive care unit (ICU) length of stay in days. (B) Time to first atrial fibrillation (AF) event in days for patients who had new-onset postoperative atrial fibrillation. The histogram bar at 15 days includes all patients who had atrial fibrillation more than 2 weeks after surgery.

 
Transfusion and postoperative atrial fibrillation
Among more than 9,000 units transfused, about half were transfused in the operating room and half in the ICU. Red blood cell transfusion in the ICU was identified as a risk factor associated with development on new-onset AF (p < 0.0001; Table 2). Other risk factors for new-onset AF included older age, prior history of AF, higher preoperative hematocrit, ß-blocker withdrawal, longer aortic clamp time, valve surgery, and ICU inotropic usage. Preoperative statin therapy and female sex were associated with a decreased occurrence of postoperative AF. Operating room RBC transfusion was associated with a reduced risk of AF. The interaction between female sex and valve surgery was added after model selection and was associated with new-onset AF (p = 0.004). The variable reoperation for bleeding was not identified as a variable chosen to be significantly associated with new-onset AF in the multivariable models selection procedure for the overall population. A number of interaction terms between RBC transfusion, statin usage, and valve surgery were examined, but none were found to be significant.


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  		Table 2. Risk Factors for Developing New-Onset Postoperative Atrial Fibrillation for the On-Pump Population From the Multivariable Logistic Regression Model
 
Figure 2 displays the probability of new-onset AF for a low-risk 65-year-old man undergoing valve surgery with the following profile: no history of preoperative AF, preoperative hematocrit 39%, no preoperative ß-blocker therapy, aortic clamp time 71 minutes, and no operating room RBC transfusion or ICU inotropic therapy. The probability of developing AF increases as units of transfused RBC increased. Patients receiving preoperative statin therapy had lower probability of experiencing AF with increasing units of RBC administered.


Figure 2
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  		Fig 2. Predicted probability for developing new-onset postoperative atrial fibrillation (Post-op AF) by red blood cell (RBC) units transfused and preoperative statin therapy (solid line, with statin; dashed line, without statin) for a low-risk patient undergoing valve surgery. As the number of red cell units transfused increases, the probability of developing atrial fibrillation also increases. Preoperative statin therapy ameliorates the impact of red blood cell transfusion on new-onset postoperative atrial fibrillation. (ICU = intensive care unit.)

 
Confirmation of effect of transfusion on postoperative atrial fibrillation
Propensity matching on ICU RBC transfusion for the on-pump population resulted in 1,360 patient pairs with a similar distribution of preoperative and operative characteristics (Table 3). Among matched pairs, ICU RBC transfusion was associated with an increased occurrence of new-onset AF (620 [46%] versus 522 [38%]; p < 0.001.


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  		Table 3. Propensity-Matched On-Pump Population: Intensive Care Unit Transfusion Versus No Intensive Care Unit Transfusion a
 
Off-Pump Coronary Artery Bypass Grafting Population
In the off-pump population 131 patients (29%) had new-onset AF. Baseline variables and operative factors for the off-pump population are listed in Table 4. Intensive care unit RBC transfusion was associated with an increased risk for new-onset postoperative AF (odds ratio, 1.2; 95% confidence limits, 1.05,1.41; p = 0.0075). In addition, patients who experienced AF were older, more commonly had a history of AF, and were more likely to be men (Table 4). Preoperative statin therapy was not associated with a reduction in AF for off-pump CABG (Table 5). Among the 120 propensity-matched pairs, transfusion of RBC was associated with an increased risk for having new-onset AF (46 [38%] versus 29 [24%]; p = 0.018; Table 5).


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  		Table 4. Baseline Variables and Operative Factors by Postoperative New-Onset Atrial Fibrillation for the Off-Pump Population a
 

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  		Table 5. Propensity-Matched Off-Pump Population: Intensive Care Unit Transfusion Versus No Transfusion in Intensive Care Unit a
 
Comparison of Off-Pump Coronary Artery Bypass Grafting With Isolated On-Pump Coronary Artery Bypass Grafting
Of 2,395 patients undergoing isolated on-pump CABG, 29% (693) had postoperative AF. Intensive care unit RBC transfusion was associated with an increased occurrence of new-onset AF (odds ratio, 1.2; 95% confidence limits, 1.1, 1.3; p < 0.0001). The odds for having AF per unit RBC transfusion were similar for both off-pump and on-pump CABG. History of AF, increasing age, and male sex were associated with increased AF (Table 6). In contrast, statin usage was not associated with a reduced risk for AF in the isolated on-pump CABG population in the multivariable logistic regression model.


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  		Table 6. Risk Factors for Developing New-Onset Postoperative Atrial Fibrillation for the Off-Pump and Isolated On-Pump Coronary Artery Bypass Grafting Populations From the Multivariable Logistic Regression Models
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
We report that ICU RBC transfusion is associated with an increased risk for new-onset AF after cardiac surgery, even after controlling for traditional risk factors. Although increasing age, male sex, history of AF, preoperative medication usage, and perioperative variables were also associated with experiencing AF after surgery, ICU RBC transfusion remained consistently associated with its development. Multivariable logistic regression and propensity matching of both on-pump and off-pump surgical procedures confirmed this association.

Recent reports have supported a role of inflammation as a risk factor for developing AF. With increasing evidence linking AF and inflammation [16, 18, 19], we hypothesized that RBC transfusion would be related to an increased occurrence of AF through its influence on inflammatory mediators. Red blood cell transfusion elicits an inflammatory response by direct infusion of inflammatory mediators and through an augmentation of the inflammatory process [20] that further amplifies the intense inflammatory response that occurs as a consequence of cardiopulmonary bypass and cardiac surgery [24, 25].

Although we do not know the precise mechanism by which transfusion contributes to AF, we speculate that the inflammatory response associated with RBC transfusion in the ICU may be exaggerated, thereby contributing to the increased occurrence of AF in our patients receiving transfusion. It is possible that the temporal confluence of early inflammatory stimuli associated with RBC transfusion in the ICU may result in enhanced leukocyte activation and atrial tissue injury. We have shown that increased leukocyte count is associated with the occurrence of postoperative AF [26]. Infiltration of neutrophils is associated with tissue injury, increased fibrosis, and increased duration of AF in canine surgical models [27, 28]. Furthermore, a rise in body temperature and leukocytosis in postcardiopulmonary bypass patients begins 24 hours after surgery, signifying an ensuing acute phase reaction [29]. Bruins and colleagues [29] described a biphasic activation of the complement system and release of proinflammatory cytokines after cardiac surgery. They described the first phase of complement activation occurring in the operating room in response to the blood–bypass circuit exposure. The second phase occurred within several days after surgery, involved C-reactive protein (CRP), and was associated with postoperative arrhythmias [29].

The benefit of statin therapy in patients undergoing valve surgery may reflect its pleiotropic antiinflammatory effects. Ability of statin therapy to reduce levels of inflammatory markers such as CRP [30] may be related to the observed reduction in AF in the valve cohort. Others have reported a beneficial impact of statin therapy on AF [31, 32]. Reduction in occurrence of postoperative AF, possibly mediated by inhibition of inflammatory mediators, was also demonstrated by Prasongsukarn and colleagues [33] in their investigation of short-term steroid administration in patients undergoing CABG.

Others have suggested a role of inflammation in the development of AF through findings of a strong association between CRP and AF [16, 18, 34, 35]. Anderson and colleagues recently reported increasing CRP levels as an increasing independent risk factor for development of AF [16]. C-reactive protein levels have been shown to be elevated in patients with postoperative and nonpostoperative AF. For example, Lo and colleagues [17] reported an association between elevated baseline plasma CRP levels and development of postoperative AF after cardiac surgery. Chung and colleagues [19] reported an association between elevated CRP in nonpostoperative patients with AF when compared with a control group without a history of atrial arrhythmias.

Clinical Implications
Our findings offer important prognostic information for development of postoperative AF beyond traditionally described risk factors. We are unaware of any investigations that have examined risk for postcardiac surgery AF related to perioperative RBC transfusion. Whether the increased occurrence of AF in patients receiving a transfusion is related to inflammatory changes or whether it is through another mechanism is unknown; nevertheless, transfusion is strongly and consistently associated with increased risk for AF.

Perioperative identification of factors related to development of AF is valuable because AF is a frequent complication associated with postoperative morbidity and cost. To successfully risk-stratify patients for interventional pharmacologic trials aimed at reducing AF, there needs to be a clearer understanding of the factors that predispose patients to development of AF in the postoperative period. Transfusion of RBC is a modifiable process of care variable that increases the risk for this common postoperative complication. Strategies to reduce the complication after cardiac surgery will impact morbid outcomes and hospital resource utilization.

Limitations
Although this was a prospective investigation, it was not a randomized trial with respect to transfusion, and therefore, there may be biases with respect to unmeasured or uncontrolled variables. To reduce bias, we provided a matched comparison on the basis of propensity methodology [21, 22]. Our focus was solely on the perioperative period without follow-up information on AF after discharge from the hospital. Prevalence of AF has been reported to be greater than in the general population in the weeks after CABG [36]. Furthermore, timing for transfusion was not a measured variable; however, in our clinical practice, a majority of RBC transfusions in the ICU are administered within the perioperative period, and the postoperative ICU length of stay was approximately 1 day for a majority of patients. Occurrence of postoperative AF occurred in a majority of patients on postoperative days 2 and 3, after discharge from the ICU (Fig 1).

The mechanism whereby RBC transfusion contributes to the development of AF by modulating systemic or atrial inflammation, or by other processes, needs further investigation. We did not have baseline assessment of inflammatory markers such as CRP or tumor necrosis factor, which have been associated with developing postoperative AF [17]. Regardless of whether RBC transfusion enhanced baseline levels of inflammation, it remained consistently associated with an increased risk for AF for on-pump and off-pump procedures. We speculate, owing to our current practice patterns, that ß-blocker withdrawal is the explanation for increased occurrence of AF for patients on preoperative ß-blocker therapy. In general, we have patients continue their medications, including ß-blocker therapy, until the morning of surgery and resume when able to take oral medications in the ICU after surgery. Inconsistencies such as patients stopping oral intake including medications the evening before surgery could theoretically have the patients off ß-blocker therapy for approximately 48 hours.

Conclusions
Red blood cell transfusion is associated with a risk-adjusted increase in occurrence of postoperative AF after cardiac surgery. Our investigation supports the literature regarding the enhanced scrutiny needed for perioperative RBC transfusion, particularly in light of this previously unreported association with postoperative AF. Trials are necessary to determine the mechanism whereby RBC transfusion modulates the inflammatory state. Strategies to identify patients at increased risk for experiencing AF and for modifying these factors could favorably impact surgical outcomes, improve hospital resource utilization, and decrease costs.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported in part by a grant from the State of Ohio's Third Frontier Project; State of Ohio TECH 05–066, Atrial Fibrillation Innovation Center.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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A. Vivacqua, C. G. Koch, A. M. Yousuf, E. R. Nowicki, P. L. Houghtaling, E. H. Blackstone, and J. F. Sabik III
Morbidity of Bleeding After Cardiac Surgery: Is It Blood Transfusion, Reoperation for Bleeding, or Both?
Ann. Thorac. Surg., June 1, 2011; 91(6): 1780 - 1790.
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M. McKenny, T. Ryan, H. Tate, B. Graham, V. K. Young, and N. Dowd
Age of transfused blood is not associated with increased postoperative adverse outcome after cardiac surgery
Br. J. Anaesth., May 1, 2011; 106(5): 643 - 649.
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 J. Thorac. Cardiovasc. Surg.Home page
L. Weltert, S. D'Alessandro, S. Nardella, F. Girola, A. Bellisario, D. Maselli, and R. De Paulis
Preoperative very short-term, high-dose erythropoietin administration diminishes blood transfusion rate in off-pump coronary artery bypass: A randomized blind controlled study
J. Thorac. Cardiovasc. Surg., March 1, 2010; 139(3): 621 - 627.
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 CirculationHome page
R. Gill, M. Herbertson, A. Vuylsteke, P. S. Olsen, C. von Heymann, M. Mythen, F. Sellke, F. Booth, and T. A. Schmidt
Safety and Efficacy of Recombinant Activated Factor VII: A Randomized Placebo-Controlled Trial in the Setting of Bleeding After Cardiac Surgery
Circulation, July 7, 2009; 120(1): 21 - 27.
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A. Anselmi, G. Possati, and M. Gaudino
Postoperative Inflammatory Reaction and Atrial Fibrillation: Simple Correlation or Causation?
Ann. Thorac. Surg., July 1, 2009; 88(1): 326 - 333.
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D. Kaireviciute, A. Aidietis, and G. Y.H. Lip
Atrial fibrillation following cardiac surgery: clinical features and preventative strategies
Eur. Heart J., February 2, 2009; 30(4): 410 - 425.
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 J. Thorac. Cardiovasc. Surg.Home page
M. P. Sakwa, R. W. Emery, F. L. Shannon, J. M. Altshuler, D. Mitchell, D. Zwada, and A. R. Holter
Coronary artery bypass grafting with a minimized cardiopulmonary bypass circuit: a prospective, randomized trial.
J. Thorac. Cardiovasc. Surg., February 1, 2009; 137(2): 481 - 485.
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R. C. Becker
Emerging constructs to maintain safety among patients with acute coronary syndromes requiring surgical coronary revascularization
Eur. Heart J. Suppl., May 1, 2008; 10(suppl_D): D12 - D22.
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 CirculationHome page
J. D. Rawn
Blood Transfusion in Cardiac Surgery: A Silent Epidemic Revisited
Circulation, November 27, 2007; 116(22): 2523 - 2524.
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P. C. Austin
Propensity-score matching in the cardiovascular surgery literature from 2004 to 2006: A systematic review and suggestions for improvement
J. Thorac. Cardiovasc. Surg., November 1, 2007; 134(5): 1128 - 1135.
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G. Mariscalco, R. Lorusso, C. Klersy, S. Ferrarese, M. Tozzi, D. Vanoli, B. V. Domenico, and A. Sala
Observational Study on the Beneficial Effect of Preoperative Statins in Reducing Atrial Fibrillation After Coronary Surgery
Ann. Thorac. Surg., October 1, 2007; 84(4): 1158 - 1164.
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 Anesth. Analg.Home page
M. D. McEvoy, S. T. Reeves, J. G. Reves, and F. G. Spinale
Aprotinin in Cardiac Surgery: A Review of Conventional and Novel Mechanisms of Action
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 PerfusionHome page
S. Gunaydin, K. Ayrancioglu, E. Dikmen, K. Mccusker, V. Vijay, T. Sari, T. Tezcaner, and Y. Zorlutuna
Clinical effects of leukofiltration and surface modification on post-cardiopulmonary bypass atrial fibrillation in different risk cohorts
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 Ann. Thorac. Surg.Home page
T. B. Ferguson Jr
Invited commentary
Ann. Thorac. Surg., November 1, 2006; 82(5): 1756 - 1757.
[Full Text] [PDF]

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