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J Thorac Cardiovasc Surg 2006;132:481-490
© 2006 The American Association for Thoracic Surgery

Cardiopulmonary Support and Physiology

Microbiologically documented nosocomial infections after coronary artery bypass surgery without cardiopulmonary bypass

^a Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece
^b Department of Medicine, Henry Dunant Hospital, Athens, Greece
^f Department of Cardiac Surgery, Henry Dunant Hospital, Athens, Greece
^d Department of Intensive Care Unit, Henry Dunant Hospital, Athens, Greece
^c Department of Medicine, Tufts University School of Medicine, Boston, Mass
^e Department of Medicine, University of Crete, School of Medicine, Heraklion, Crete

Received for publication December 30, 2005; revisions received May 5, 2006; accepted for publication May 17, 2006.

^_* Address for reprints: Matthew E. Falagas, MD, MSc, Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos St, Marousi 151 23, Greece (Email: m.falagas{at}aibs.gr).

	Abstract

Top Abstract Introduction Patients and Methods Results Discussion References

 
OBJECTIVE: This study was undertaken to evaluate the frequency, characteristics, and risk factors of microbiologically documented nosocomial infections after off-pump coronary artery bypass grafting.

METHODS: A prospective cohort study was performed at Henry Dunant Hospital, Athens, Greece. It included all adult patients who underwent coronary artery bypass grafting with no valve surgery and without the use of cardiopulmonary bypass during a period of 3 years. Case patients were those with development of microbiologically documented nosocomial infections. Various variables were examined as possible risk factors for nosocomial infections.

RESULTS: Twenty-one of 782 studied patients (2.7%) acquired 26 microbiologically documented nosocomial infections after off-pump coronary artery bypass grafting. Eight of 782 studied patients had pneumonia (1.02%), 7 of 782 (0.90%) had bacteremia, 4 of 782 (0.51%) had superficial wound infection at the sternotomy site, 4 of 782 (0.51%) had urinary tract infection, 2 of 782 (0.26%) had mediastinitis, and 1 of 782 (0.13%) had pressure sore infection. Twenty-one infections were monomicrobial, whereas 5 were polymicrobial. All polymicrobial infections were wound infections. There was a statistically significant difference in mortality between patients with and without nosocomial infection (23.8% vs 1.2%, P < .001). Clinical response of the infection to the treatment administered was observed in 21 of 26 episodes (80.8%) in 21 patients. A backward stepwise multivariable logistic regression model showed that independent risk factors (P < .05) associated with development of microbiologically documented nosocomial infection were arterial hypertension, previous vascular surgery, urgent operation, postoperative atrial fibrillation, number of inotropes used during and after operation, transfusion of fresh-frozen plasma during the intensive care unit stay, and intensive care unit stay until development of infection.

CONCLUSION: Nosocomial infection after off-pump coronary artery bypass grafting is an uncommon but potentially life-threatening complication. The identification of independent risk factors, including arterial hypertension, associated with development of postoperative infection may help in the development of clinical strategies for the prevention, early diagnosis, and treatment of these infections.

	Introduction

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Coronary artery bypass grafting (CABG) on a beating heart (off-pump CABG, or OPCAB) has become common in the last 10 years in an attempt to decrease the complications associated with the use of extracorporeal circulation. OPCAB is associated with a significant reduction in inflammatory response, a fact supported by decreased production of interleukin 8, lower postoperative concentrations of elastase, and lower postoperative white blood cell, neutrophil, and monocyte counts.^1,2 A recent meta-analysis of 37 randomized trials that included 3369 patients showed OPCAB to be associated with improved outcome relative to conventional CABG with respect to hospital stay, intensive care unit (ICU) stay, and in-hospital and 1-year direct costs. Furthermore, OPCAB significantly decreased respiratory infections, postoperative atrial fibrillation, transfusions, and inotrope requirements. Another finding of the meta-analysis was that OPCAB did not have any impact on 30-day mortality or other postoperative complications, such as wound infections, myocardial infarction, stroke, renal dysfunction, use of intra-aortic balloon pump, rethoracotomy, and reintervention.³ Postoperative deep wound infection was reported in 0.3% of 7283 patients who underwent OPCAB in 4 study centers with significant beating-heart surgery experience, pneumonia was reported in 2%, and septicemia was reported in 0.3%.⁴ We designed this prospective study to examine the frequency, characteristics, and predisposing factors of all microbiologically documented nosocomial infections in a large cohort of patients undergoing OPCAB during a period of 3 years.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Discussion References

 
Study Design and Patient Population
This prospective cohort study was conducted at Henry Dunant Hospital, a tertiary care hospital in Athens, Greece. Approval was obtained from the institutional review board of the hospital. We studied all patients who underwent CABG without the use of cardiopulmonary bypass during a period of 39 months (January 2001-March 2004). All patients were admitted to the ICU immediately after cardiac surgery and subsequently transferred to the ward as appropriate to their medical condition (usually after 24 hours of ICU stay). Case patients were those who acquired microbiologically documented nosocomial infection. Patients who underwent valve surgery combined with CABG were excluded from the study.

Cardiac surgical procedures were performed by a single surgical team with the use of bilateral skeletonized internal thoracic arteries when indicated, avoiding any procedure on the ascending aorta.⁵ The sternal closure technique was based on alternative placement of figure-of-eight (3 in total) and single sternal wires. Antibiotic prophylaxis with cefuroxime was given to all patients intravenously as a single dose (3 g) at the induction of anesthesia and afterward at 750 mg every 8 hours for 2 to 4 days. All patients had at least one central venous catheter. Thermodilution catheters were used only for high-risk cardiac surgical patients. Hematologic and biochemical tests and chest radiographs were performed preoperatively and every day during ICU stay and before discharge. In addition, laboratory tests and radiographs were performed as clinically indicated. All patients were evaluated daily to detect any nosocomial infection. Bacteriologic examinations of blood, tracheal secretions, urine, central venous catheter tips, and wound swabs were performed as clinically indicated.

Data Collection
All the microbiologically documented infectious complications that occurred in patients who underwent OPCAB during their hospital stay were identified by prospective active infection control surveillance. Subsequently, two different case report forms were designed. With the first case report form, data were collected for all patients undergoing OPCAB who did not acquire nosocomial infections. Variables that were considered of interest, including potential risk factors for development of nosocomial infection, were entered into a research database. Especially for patients who acquired microbiologically documented nosocomial infections, more elaborate data gathering was performed by using a second, more detailed case report form. The collected data included demographic and clinical features. Two blinded reviewers determined the development of noninfectious postoperative systemic inflammatory response syndrome in the first 24 hours after OPCAB, the type of the infection, the causative pathogens, and the clinical outcome.

Definitions of Infections and Outcomes
Pneumonia, bacteremia, surgical wound infection, urinary tract infection (UTI), and nosocomial infections of other body sites or fluids were defined according to the guidelines published by the Centers for Disease Control and Prevention.⁶ The primary end point of our analysis was the development of microbiologically documented nosocomial infection. The outcome of these infections was defined as follows: cure was defined as improvement and finally resolution of presenting symptoms and signs of the infection by the end of treatment and discharge from the hospital, and unresponsiveness was defined as persistence or worsening of presenting symptoms or signs of the infection despite treatment. Secondary outcome measured was in-hospital mortality. Patients were followed up for 180 days after OPCAB, as per study design.

Statistical Analysis
Data are expressed as mean ± SD for continuous variables and as percentages for categoric variables. For comparison of continuous variables, the Student t test or the Mann-Whitney test for normally and nonnormally distributed variables was used. Categoric variables were compared by ² or Fisher exact test. Variables associated with the development of microbiologically documented nosocomial infection after OPCAB in the bivariable analysis (P < .05) were included in a backward stepwise multivariable logistic regression model. All statistical analyses were performed with SPSS 11.0 (SPSS Inc, Chicago, Ill) and S-PLUS 6.1 Professional (Insightful Corporation; Seattle, Wash). A finding was considered statistically significant if there was a P value lower than 0.05 in the analysis of the variables.

	Results

Top Abstract Introduction Patients and Methods Results Discussion References

 
Twenty-one of 782 studied patients (2.7%) acquired microbiologically documented nosocomial infection after OPCAB. In Table 1, data from the bivariable analysis of predictors of development of microbiologically documented nosocomial infection after OPCAB are presented. Several variables were associated with the studied outcome. Table 2 demonstrates the demographic and clinical data, including comorbidities, of patients who acquired nosocomial infections. Furthermore, in Table 3 the characteristics of microbiologically documented nosocomial infections in the same group of patients are presented. Eight of 782 studied patients acquired pneumonia (1.02%), 7 of 782 (0.90%) bacteremia, 4 of 782 (0.51%) superficial wound infection at the sternotomy site, 4 of 782 (0.51%) UTI, 2 of 782 (0.26%) mediastinitis, and 1 of 782 (0.13%) pressure sore infection. Four patients had infections at two or more different sites. Specifically, 1 patient had UTI and mediastinitis, 1 had UTI and pressure sore infection, 1 had pneumonia and bacteremia, and 1 had pneumonia, UTI, and bacteremia. Thus there were 26 episodes of microbiologically documented infections in 21 patients. One patient had bacteremia related to the central venous catheter, whereas the remaining 4 cases of bacteremia were not associated with any other identifiable infected site. Seven of 21 patients with nosocomial infection (33.3%) underwent direct cardioversion for postoperative atrial fibrillation, ventricular tachycardia, or ventricular fibrillation. Of these 7 patients, 5 acquired pneumonia (5/8, or 62.5% of patients with pneumonia) and 2 acquired bacteremia (2/7, or 28.6% of patients with bacteremia).

There was a statistically significant difference in mortality between patients with microbiologically documented nosocomial infection (5/21, or 23.8%) and the rest of the patients (9/773, or 1.2%, P < .001). Clinical response of the infection to the administered treatment was observed in 21 of 26 episodes (80.8%) in 21 patients. Unresponsiveness was observed in 5 of 26 (19.2%) episodes. Three of 4 patients whose infections were unresponsive to the administered therapy had bacteremia. The causative pathogens were S aureus and P aeruginosa (cases 17-19 in Table 3); the fourth patient had a UTI and later mediastinitis from the same pathogen (K pneumoniae was isolated from the urine and then from pus at the sternotomy site in case 2 in Table 3).

The backward stepwise multivariable logistic regression model revealed the independent risk factors associated with development of microbiologically documented nosocomial infection to be arterial hypertension, previous vascular surgery, urgent operation, postoperative atrial fibrillation, number of inotropes used during and after operation, transfusions of fresh-frozen plasma during ICU stay, and ICU stay until development of infection. The odds ratios with 95% confidence intervals of the independent predictors of development of microbiologically documented nosocomial infection after OPCAB are presented in Table 4.

	Discussion

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The frequency of microbiologically documented nosocomial infection in our group of patients is similar to the frequency of major postoperative infection reported in some previous studies. For example, Fower and colleagues⁷ showed that major infection occurred in 11,636 of 331,429 (3.5%) patients who underwent CABG (CABG alone or in combination with valve surgery, on pump or off pump) from January 1, 2002, to December 31, 2003, according to the Society of Thoracic Surgeons National Cardiac Database of the United States. The frequencies of pneumonia, bacteremia, and superficial wound infection in this study are similar to the results of a previous retrospective analysis that included 7283 patients who underwent OPCAB.⁴ In keeping with results of other studies, our results do show that mortality among patients who acquired postoperative nosocomial infection was significantly greater than that among patients without a nosocomial infection.^7,8 In addition, certain nosocomial infections, such as bacteremia and mediastinitis from antibiotic-resistant pathogens, are associated with an increased risk of death. It is noteworthy that a high frequency of postoperative nosocomial infection after conventional CABG has been reported in some studies. For example, in a previous case-cohort study, 131 of 605 patients (21.7%) acquired at least one nosocomial infection after cardiac surgery with the use of extracorporeal circulation.⁸

The multivariable analysis revealed that among multiple risk factors, arterial hypertension was the most strongly associated with the development of microbiologically documented nosocomial infection after OPCAB. Bivariable analyses of risk factors of development of nosocomial infection after CABG in previous studies have also shown arterial hypertension to be a significant risk factor for acquiring nosocomial infection, but it was not found to be an independent risk factor in multivariable analyses.^7,9 A possible explanation for this association could be the effect of long-standing hypertension on arteriolar and arterial sclerosis, the subsequent reduction of the essential blood supply (and the subsequently intravenous antibiotics possibly given) to the tissues colonized with nosocomial pathogens. In addition, arterial hypertension is accompanied by significant increase in such vascular complications as hemorrhagic or atherothrombotic stroke, peripheral vascular disease, nephrosclerosis, and cardiac arrhythmias, complications that may prolong postoperative ICU stay and hospital stay, thus increasing the risk for development of nosocomial infection. Vascular surgery, a consequence of peripheral vascular disease caused by arteriosclerosis, was also found in our analysis to be an independent risk factor associated with development of nosocomial infection.

High preoperative resting systolic blood pressure is a significant predictor for postoperative atrial fibrillation.¹⁰ Furthermore, previous studies have shown that postoperative atrial fibrillation or a new onset of other type of supraventricular tachyarrhythmia in an otherwise stable patient should prompt a search for postoperative infection.^11,12 It is interesting that about 60% of patients with nosocomial pneumonia and 29% of patients with bacteremia in our study underwent direct cardioversion for termination of postoperative atrial fibrillation or ventricular arrhythmias before the diagnosis of nosocomial infection. There is no evidence supporting a role of direct cardioversion in the genesis of nosocomial infections such as pneumonia or bacteremia. On the other hand, several studies have shown that the activation of inflammatory processes, as evidenced by a significant increase of the C-reactive protein plasma concentration or white blood cell count, may lead to the development of postoperative atrial fibrillation. The variation of these inflammatory indices before and after cardioversion may have prognostic implications regarding sinus rhythm maintenance.^13-15

Urgent operation, the use of inotropes after operation, and ICU stay were also associated with the development of postoperative infection in previous studies.^7,16 Infusion of inotropes and prolonged ICU stay may indicate the presence of severe postoperative complications. In one study, 46% of cardiac surgical patients with severe sepsis in the ICU had serious operative complications, and 98% had severe complications.¹⁷ Transfusion of fresh-frozen plasma during ICU stay was also found in our study to be an independent risk factor associated with nosocomial infection after OPCAB. The results of previous studies on that subject, however, are contradictory. A recent retrospective study that examined the effect of perioperative transfusion of platelets and fresh-frozen plasma on infection rates after cardiac surgery showed that fresh-frozen plasma was not associated with postoperative infection.¹⁸ To the contrary, another retrospective study of 276 patients who underwent CABG and acquired postoperative infection revealed transfusion of fresh-frozen plasma to be a possible risk factor for the development of bloodstream, respiratory, or deep surgical wound infections after cardiac surgery.⁹

With data from the Society of Thoracic Surgeons National Cardiac Database of the United States, Fower and colleagues⁷ showed that risk factors independently associated with major infection after CABG were as follows: body mass index greater than 40 kg/m², hemodialysis, cardiogenic shock, age older than 85 years, immunosuppressive treatment, diabetes mellitus, perfusion time longer than 200 minutes, placement of an intra-aortic balloon pump, and the presence of three or more anastomoses.⁷ In a previous study of our group on postoperative infections after cardiac surgery with the use of extracorporeal circulation, we found that history of immunosuppression, transfusion of more than 5 units of red blood cells during the first postoperative day in both the operating room and ICU, and development of acute renal failure during the first 2 postoperative days were independent risk factors for acquisition of postoperative infection in a group of 2122 patients.¹⁹ Another multivariate risk factor analysis in 4474 patients who underwent CABG demonstrated age, obesity, and diabetes mellitus as independent predictors for surgical site infection. It is interesting that age, obesity, and diabetes mellitus were not found to be independently associated with development of microbiologically documented nosocomial infection after OPCAB in our group of patients. This constitutes a noteworthy difference between this study and previous publications, especially if we take into account the relatively high percentage of patients with diabetes in our study and the fact that most of them underwent OPCAB with the use of bilateral internal thoracic arteries.

This study has several limitations. First, because of the design of the study, only microbiologically documented nosocomial infections after OPCAB were evaluated. Thus other possible postoperative infections that were not microbiologically documented were excluded from the analysis. The reason for this exclusion is the fact that the diagnosis of nosocomial infection that is not microbiologically documented in this patient population is sometimes difficult, because clinical and laboratory signs of inflammation and the systemic inflammatory response syndrome may be caused not only by infection but also by tissue injury. Additionally, the prolonged antibiotic prophylaxis that was given for 2 to 4 days after operation may, in addition to promoting the development of antimicrobial resistance, have had a considerable effect on the isolation of microorganisms from blood specimens, increasing the probability of false-negative blood culture results. Second, although we studied a relatively large group of patients, the small number of patients with the end point of interest increases the probability of type II error, not finding a true association between a variable and the outcome of interest. Third, we did not include a group of patients with postoperative microbiologically documented nosocomial infection with the use of extracorporeal circulation (on-pump CABG) for comparison. Although it would be valuable to compare infections after OPCAB with infections after on-pump CABG to contrast the advantages and disadvantages of the two types of CABG, we did not have a sufficient number of patients who underwent on-pump CABG in our institution to perform a meaningful statistical comparison. Fourth, the antibiotic prophylaxis regimen of cefuroxime that was administered during the study period is not the currently recommended regimen according to recent guidelines issued by Medicare as part of the Surgical Care Infection Project. The fact that most of the causative pathogens in our study were resistant to cefuroxime forced us to change the antibiotic prophylaxis regimen for high-risk patients undergoing OPCAB in our hospital. The prolonged antibiotic prophylaxis that was given for 2 to 4 days after operation is a major limitation of our study. We believe that our results cannot be generalized to other hospitals, including most US hospitals. It should be mentioned that antibiotic prophylaxis for as long as 72 hours is recommended for cardiothoracic surgical patients by the American Society of Health-System Pharmacists and has been adopted in the advisory statement from the National Surgical Infection Prevention Project. The authors of the relevant guidelines, however, suggest that prophylaxis for 24 hours or less may be appropriate.^20,21

In conclusion, nosocomial infection after OPCAB is an uncommon but potentially life-threatening complication. It is of interest that arterial hypertension was found to be an independent risk factor for the development of microbiologically documented nosocomial infection after OPCAB. The identification of independent risk factors associated with development of postoperative infection would help clinicians to develop clinical strategies for the prevention, early diagnosis, and treatment of these infections, improving patient outcomes after OPCAB.

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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): Sotirios N. Prapas Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Falagas, M. E. Articles by Prapas, S. N. Search for Related Content PubMed PubMed Citation Articles by Falagas, M. E. Articles by Prapas, S. N. Related Collections Coronary disease