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Ann Thorac Surg 2002;73:138-142
© 2002 The Society of Thoracic Surgeons

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Original article: cardiovascular

Association of bacterial infection and red blood cell transfusion after coronary artery bypass surgery

^a Departments of Medicine, Surgery, and Critical Care Medicine, Maine Medical Center, Portland, Maine, USA
^b Department of Medicine, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire, USA

Accepted for publication August 31, 2001.

* Address reprint requests to Dr Morton, Department of Surgery, Maine Medical Center, 22 Bramhall St, Portland, ME 04102, USA
e-mail: mortoj{at}mmc.org

	Abstract

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Background. Previous studies have shown an association between red blood cell transfusions (RBC) and bacterial infections following coronary artery bypass graft (CABG) surgery. We sought to assess whether there is an independent effect of RBC on the incidence of bacterial infections.

Methods. This was a prospective cohort study of 533 CABG patients over a 7-month period. Subjects were followed from time of CABG until 30 days postoperatively. Data were collected on patient and treatment characteristics, surgical management, and transfusion incidence.

Results. Seventy-five (14.1%) of 533 patients developed a bacterial infection. After controlling for patient and disease characteristics, invasive treatments, surgical time, and the transfusion of other substances, the adjusted rates of bacterial infection were 4.8% for no RBC transfusion, 15.2% with one to two units, 22.1% with three to five units, and 29.0% with greater than or equal to six units, (p_trend < 0.001). Diabetes was the only patient or disease factor significantly associated with bacterial infection (p < 0.001).

Conclusions. RBC transfusions were independently associated with a higher incidence of post-CABG bacterial infections. The risk of infection increased in proportion to the number of units of RBC transfused.

	Introduction

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Transfusion of red blood cells (RBC) is often done during or after cardiac surgery. Transfusion may be life saving and improve the cardiac function and quality of life of cardiac surgery patients but also carries some risks; these include transmission of infectious agents, allergic reactions to homologous blood, and possibly an increased risk of bacterial infection.

An association has been shown to exist between RBC transfusions and postoperative bacterial infections in the setting of orthopedic surgery [1], resection of colon cancer [2–6], and other intraabdominal operations [7, 8]. RBC transfusion has also been shown to be associated with higher infection rates after trauma [9–11] and burns [12].

The effect of RBC on bacterial infections following cardiac operations has been assessed previously. In retrospective studies, RBC transfusions were associated with a higher incidence of mediastinitis [13], sternal wound infection [14], and bacterial infections in general [15, 16]. A prospective study has shown that the risk of sternal wound complications is increased among patients receiving RBC [17]. Previous studies in coronary artery bypass graft (CABG) patients have been limited by their retrospective design, by limited scope (eg, considering only wound infections), and by non-uniform criteria for the determination of bacterial infection. We used uniform criteria to assess the association between RBC transfusion and the incidence of a variety of bacterial infections among consecutive patients undergoing isolated coronary artery bypass graft (CABG) surgery.

	Material and methods

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Patient selection
During a 7-month period, 605 adult patients underwent primary isolated CABG at Maine Medical Center, a tertiary care, university-affiliated teaching hospital. We excluded patients who received antimicrobial therapy during the 72 hours prior to surgery (n = 60), transfusion of any blood products during the week preceding surgery (n = 8), and those who expired within 48 hours of CABG (n = 4). The remaining 533 patients were enrolled in the study and followed postoperatively with daily reviews of the medical record. The Maine Medical Center Institutional Review Board approved the design of the study and, in accordance with the Office of Protection from Research Risk guidelines, exempted the requirement for patient informed consent.

Data collection
Patient characteristics included sex, age, body mass index, the presence of diabetes mellitus, dialysis-dependent renal failure, or renal insufficiency (preoperative creatinine > 1.8 mg/dL). Obesity was defined as weight greater than 120% of Ideal Body Weight as defined by Metropolitan Life Tables. Treatment characteristics included emergency surgery, preoperative use of a Foley catheter, insertion of a pulmonary artery catheter prior to surgery, or preoperative treatment with corticosteroids. Additional treatment characteristics included: the pre- or postoperative use of an intraaortic balloon pump; reexploration of the chest for any reason; the presence of chest tubes for greater than 48 hours; the use of a pulmonary artery catheter for greater than 72 hours; and the number of internal mammary arteries used during CABG surgery. Data were also collected on surgical times including the duration of surgery (incision to closure) and the duration of cardiopulmonary bypass.

Determination of bacterial infection
The primary outcome for each patient was development of a bacterial infection within 30 postoperative days or death. Infections were categorized and defined using standard Center for Disease Control (CDC) [18] criteria with one exception. The CDC definition for bronchitis/tracheitis/tracheobronchitis/bronchiolitis requires that sputum cultures be obtained from either deep tracheal aspirate or fiber optic bronchoscopy. We accepted an organism isolated from expectorated sputum as acceptable evidence for bronchitis, if the managing physician considered the sample to be reflective of a lower respiratory source, and treated the patient with antibiotics. Patients without infection at discharge were actively followed in the operating surgeon’s office until at least 30 days after CABG.

Determination of red blood cell transfusion
RBC transfusion data were collected from the Maine Medical Center Blood Bank Product Transfusion record and confirmed by concurrent medical record review. We recorded the number of units of packed red blood cells, platelets, fresh frozen plasma, and cryoprecipitate administered between 24 hours preoperative and 72 hours postoperation.

Statistical methods
Univariate analyses were performed with differences assessed using ² tests for nominal and categorical data and the t test for normally distributed data. Logistic regression was used to determine the association between the number of packed RBC transfused and post-CABG bacterial infections, and to calculate adjusted rates of bacterial infections. In this regression model, we included patient, disease, and treatment variables. The relative operating characteristic area, a measure of discrimination of the logistic regression model, was calculated. The Hosmer-Lemeshow goodness-of-fit test assessed the correspondence between the logistic regression model and the data. Results are presented as adjusted odds ratios, 95% confidence intervals (CI_95%), and p-values and as adjusted rates. Adjusted rates are those rates that would be expected if the patients in each RBC transfusion group were identical with respect to each of the variables considered. p-Values at a level less than 0.05 were considered to be statistically significant. Statistical analyses were performed using Stata Statistical Software: Release 6.0. (StataCorp, 1999, College Station, TX).

	Results

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Seventy-five of 533 patients developed a bacterial infection during the study (14.1%). Of these, 46 (61.3%) developed bacterial infection prior to hospital discharge and 29 (38.7%) developed infection after discharge. Nine patients died; 5 of 75 (6.7%) with bacterial infection died, while 4 of 458 (0.9%) of non-infected patients died (p < 0.001). The endpoint of the study for the remaining 485 patients was their 1-month post-discharge office visit. The questionnaire response rate for these patients was 100%; no patient was lost to follow-up. Using CDC definitions, the sites of bacterial infections were 32.4% respiratory, 41.9% superficial surgical site infection (SSI), 8.1% deep SSI (all sternal wounds), and 17.6% at other sites. Table 1 lists the organisms isolated from 49 of these sites where cultures were obtained.

View larger version (23K): [in this window] [in a new window]   Fig 1. Rates of bacterial infection by site and number of units of red blood cells (RBC) transfused. (SSI = surgical site infection.)

	Comment

Top Abstract Introduction Material and methods Results Comment References

There are two limitations of this study that deserve mention. Among these 533 patients there were only 75 bacterial infections, thus the rates in some transfusion groups, eg, patients receiving greater than or equal to six units, is rather small resulting in some statistical instability in the site specific rates. However, the overall positive monotonic association between units of RBC transfused and the rate of bacterial infections was statistically robust. Secondly, there were differences in the patients receiving RBC transfusions and those that did not. This raises concerns about the adequacy of our risk adjustment method. In Table 2, we describe the association between patient and treatment characteristics, including surgical times and the incidence of bacterial infection. The variables were selected from a review of the current literature and are clinically reasonable. Adjustment for these variables does lower the rate of bacterial infections especially in the group receiving large numbers of units of transfused RBC. However, we cannot exclude the existence of other variables unknown to us, and to the published literature, and uncorrelated to the variables that we used. We think that this is an unlikely explanation for our findings.

Our findings confirmed and expanded upon results found in previous studies of open-heart surgery. Blood transfusions have been shown to have a relative risk of causing sternal wound complications of 1.05 per unit in a study that considered all blood transfusions up to the time of infection [14]. In another retrospective study, suppurative mediastinitis following open-heart surgery was related to RBC transfusions in a volume-dependent manner [13]. Miholic and colleagues [15] found that the risk of post-cardiac surgery infection was higher in patients receiving greater than 2,500 cc of RBC, while Murphy and coworkers [16] showed in a retrospective study that blood transfusion as a continuous variable was significantly predictive of post-CABG bacterial infections.

Although the overall incidence of bacterial infections in our study (14.1%) was higher than reported in some studies (6.7% [1]) and lower than in others (16% [19]), the differences may be due in part to different definitions of infections, different surveying techniques, and different patient populations. Also, since the proposed mechanism of immunologic suppression should increase the incidence of all infection, we looked at all bacterial infections, not just wound infections. This approach also reduced the impact of operative technique [1]. In our study, the incidences of wound infections (6.8%) and sternal wound infections (3.2%) were comparable to those in other studies [20, 21].

Not all studies assessing infections following cardiac surgery have demonstrated a relationship to RBC transfusions. He and coworkers [22] demonstrated no association between blood transfusion and sternal wound infections, but the study was designed to investigate the effect of bilateral internal mammary arteries grafting on infection and mortality and thus had a small sample size with only 5 of 199 patients developing infection. Utley and coworkers [23] noted that intraoperative transfusion is associated with mortality, bleeding, renal failure, and respiratory failure, but not with bacterial infections. However, Utley and coworkers were primarily comparing male and female differences in operative outcome, rather than overall incidence of bacterial infections, and did not include postoperative transfusions.

Is it biologically plausible that the transfusion of RBC is causal or it is an epi-phenomenon? The most likely mechanism to explain this association has been hypothesized to be a suppressive effect of RBC on the immune system [24, 25], and has been supported by studies in numerous settings. Renal allograft survival is longer among patients receiving homologous RBC [26], and RBC transfusion is associated with an increased likelihood of colon cancer recurrence [5]. The specific immunologic defect is not well-defined [27], but may relate to altered circulating lymphocytes [28, 29]. Recent animal and human studies suggest that a simultaneous suppression of cell mediated immunity and stimulation of humoral immunity through alterations in cytokine regulation might be the working mechanism [30]. The presence of donor leukocytes in transfused blood appears to play a role in this effect. This hypothesis is further supported by the observation that infection rates are lower with autologous blood transfusions than in homologous transfusions [4, 31]. We believe that this supposition is reasonable but unproven and that further study of immune system components and their association with RBC transfusion and with bacterial infection is required. Whatever the pathophysiologic mechanisms, these data clearly show a significant increase in bacterial infections among cardiac surgery patients receiving RBC transfusion.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Jeremy R. Morton Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Chelemer, S. B. Articles by Morton, J. R. Search for Related Content PubMed PubMed Citation Articles by Chelemer, S. B. Articles by Morton, J. R. Related Collections Coronary disease