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(Circulation. 2003;108:73.)
© 2003 American Heart Association, Inc.

Clinical Investigation and Reports

Staphylococcus aureus Bacteremia After Median Sternotomy

Clinical Utility of Blood Culture Results in the Identification of Postoperative Mediastinitis

Vance G. Fowler, Jr, MD, MHS; Keith S. Kaye, MD, MPH; David L. Simel, MD, MHS; Christopher H. Cabell, MD; Douglas McClachlan, MD, MPH; Peter K. Smith, MD; Scott Levin, MD; Daniel J. Sexton, MD; L. Barth Reller, MD; G. Ralph Corey, MD; Eugene Z. Oddone, MD, MHS

From the Department of Medicine (D.M.), Divisions of Infectious Diseases (V.G.F., K.S.K., D.J.S., L.B.R., G.R.C.), Cardiology (C.H.C.), and General Internal Medicine (D.L.S., E.Z.O.); Clinical Microbiology Laboratory (L.B.R.); Department of Surgery, Divisions of Cardiovascular (P.K.S.) and Plastic and Reconstructive Surgery (S.L.), Duke University Medical Center; and Center for Health Services Research in Primary Care (D.L.S., E.Z.O.), VA Medical Center, Durham, NC.

Correspondence to Vance Fowler, Box 3281, Duke University Medical Center, Durham, NC 27710. E-mail fowle003{at}mc.duke.edu

	Abstract

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Background— Mediastinitis is a complication of coronary artery bypass graft surgery (CABG) that can be difficult to diagnose. This study evaluated the utility of blood culture results in identifying patients with mediastinitis.

Methods and Results— All unique patients undergoing CABG at our institution over a 60-month study period (n=5500) and all blood cultures performed on these patients ≤90 days after CABG were identified. Mediastinitis was identified by prospective active infection control surveillance. Eight hundred fifty-five (15.5%) patients had ≥1 blood culture drawn within 90 days of CABG. Mediastinitis occurred in 46 of 60 (76.7%) patients with blood cultures positive for Staphylococcus aureus, 15 of 126 (11.9%) patients with blood cultures positive for other pathogens, 37 of 669 (5.5%) patients with blood cultures with no growth, and 44 of 4645 (0.9%) patients with no blood cultures obtained. The isolation of S aureus from even 1 blood culture drawn after ≤90 days of CABG was strongly associated with mediastinitis (likelihood ratio [LR], 25; 95% CI, 14.7 to 44.4). Bacteremia attributable to other organisms did not alter pretest suspicion for mediastinitis (LR, 1.0; 95% CI, 0.6 to 1.7). Patients with negative blood cultures were less likely to have mediastinitis (LR, 0.45; 95% CI, 0.35 to 0.58). The association between S aureus bacteremia and mediastinitis remained highly significant when all unique patients undergoing CABG were analyzed in a logistic regression model and when a case-control analysis was used to evaluate patients with ≥1 blood culture obtained after CABG.

Conclusions— Among patients with blood cultures drawn after CABG, S aureus bacteremia strongly suggests the presence of mediastinitis.

Key Words: infection • diagnosis • bypass • surgery

	Introduction

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Postoperative mediastinitis occurs in 1% to 3% of all patients undergoing median sternotomy. This devastating complication carries an associated mortality of up to 40%, perhaps in part because it is often difficult to make an early diagnosis.¹ Definitive diagnosis and treatment of mediastinitis requires reopening the mediastinum for direct inspection and debridement. These procedures subject patients to additional risks and significant health care costs.^2,3 Although several diagnostic strategies have been evaluated, none reliably identified patients with mediastinitis.

Previously, we reported an association between S aureus bacteremia and mediastinitis. Among 23 patients with S aureus bacteremia after a median sternotomy, the positive predictive value for mediastinitis was 91.3%.⁴ However, because the positive predictive value varies with disease prevalence⁵ and because these data were generated from a small number of patients, the results may not generalize to other clinical settings.

In the present investigation, we evaluated the clinical utility of blood cultures in identifying mediastinitis using a large sample size and methods that would result in greater generalizability. We hypothesized that the isolation of S aureus from blood cultures drawn as a part of routine care in a patient who had recently undergone median sternotomy would be highly associated with mediastinitis.

	Methods

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Patient Selection
This investigation was approved by the Duke University Institutional Review Board and was performed in accordance with institutional guidelines. Patients were considered for inclusion if they underwent median sternotomy for coronary artery bypass graft surgery (CABG) at Duke University Medical Center from January 1, 1994, until December 31, 1998, and had ≥1 blood culture drawn within 90 days of the median sternotomy. Exclusion criteria included median sternotomy performed for procedures other than, or in addition to, CABG; CABG performed by surgical approaches other than median sternotomy; or no blood cultures obtained before the date of definitive/surgical diagnosis of mediastinitis. Only the first median sternotomy during the study period was included for each patient.

Potential study patients undergoing median sternotomy for CABG were identified using the Duke Database for Cardiovascular Diseases (DDCD), an ongoing prospective registry of all patients undergoing a cardiac procedure at our institution since 1971 (n=120 000).⁶ Missing data occurred in less than 0.5% of variables. Next, a database link was performed between the DDCD and the electronically archived records of all blood cultures performed in our clinical microbiology laboratory since 1992 (Cerner Pathnet, Kansas City, Mo). Thus, the final data set included all patients with ≥1 blood culture drawn within 90 days of CABG and the results of all blood cultures performed on these patients.

Mediastinitis Identification
Our primary outcome, mediastinitis within 90 days of CABG, was prospectively identified using active surveillance by infection control practitioners. Mediastinitis was defined according to Center for Disease Control (CDC) criteria as isolation of an organism from a culture of mediastinal tissue or fluid during surgery or needle aspiration; evidence of mediastinitis observed at surgery or by histopathologic examination; or fever (>38°C), chest pain, or sternal instability, plus purulent drainage from the mediastinal area, isolation of an organism from blood culture or drainage from the mediastinal area, or mediastinal widening on x-ray examination.⁷ The date of definitive diagnosis was defined as the date the patient met CDC criteria for mediastinitis.

Blood Culture Identification
Patients were defined as having S aureus bacteremia if any blood culture result yielded S aureus within the 90-day period. Patients were defined as having bacteremia attributable to other pathogens if blood cultures yielded any organism other than S aureus during the 90-day period. Patients whose blood cultures remained negative were defined as having blood cultures with no growth.

Patient Follow-Up
The outcomes of all study patients were established for a period of 90 days after CABG using the DDCD. Follow-up in this database is obtained for each patient at regular intervals for the first year after the procedure and annually thereafter. The self-reported follow-up is more than 97% complete and includes details regarding rehospitalization and adverse events (including death). The records of all study patients who were readmitted to a different hospital within 90 days of their median sternotomy were reviewed using a standard protocol followed by the DDCD.

Analysis
The association of S aureus bacteremia and mediastinitis was considered using multilevel test table, cohort, and case-control analyses. All statistics were obtained using SAS, version 8.1. Bivariate comparisons were performed using Fisher’s exact or ² tests; and to determine the association between blood culture results, a logistic regression model was created that included only different categories of blood culture results (eg, S aureus bacteremia and bacteremia other than S aureus). Continuous variables were analyzed with either the Student’s t test or Wilcoxon rank-sum test.

Multivariate analyses for data from Table 1 and Table 3 were performed using logistic regression. Each model included all variables from the respective table with P<0.2 in the bivariate analysis. Stepwise selection was used for retaining significant variables and was specified before any multivariate results were known. Risk factors were checked for confounding, and confounders were included in multivariate models if inclusion of the covariate changed the coefficient of any statistically significant variable in the regression model by 10% or greater. All tests were 2-tailed, and P≤0.05 was considered significant in the multivariate model.

View this table: [in this window] [in a new window]   TABLE 1. Characteristics Associated With Postoperative Mediastinitis Among 5500 Consecutive Patients Undergoing CABG

View this table: [in this window] [in a new window]   TABLE 3. Case-Control Analysis of 95 Patients With Mediastinitis and at Least 1 Blood Culture Performed (Cases) and 95 Randomly Selected Patients With at Least 1 Blood Culture Performed but Without Mediastinitis (Controls)

Multilevel Test Table Analysis
To consider the use of blood cultures as a diagnostic test for mediastinitis, 3 possible test results were identified: positive (S aureus bacteremia), nonpositive nonnegative (bacteremia other than S aureus), and negative (blood culture yields no growth). A 6-cell matrix approach was used as previously defined.⁸ The positive likelihood ratio (LR) and 95% CI was then calculated to provide the odds of disease (mediastinitis) given a positive test result (S aureus bacteremia).

Cohort Study of CABG Patients
Bivariate analyses were performed on the entire cohort (n=5500) to identify clinical characteristics independently associated with mediastinitis. A multivariate logistic regression model was built to identify independent predictors of mediastinitis.

Case-Control Analysis
Only patients with ≥1 blood cultures obtained after CABG were included in the case-control analysis. Cases included patients with mediastinitis and ≥1 blood culture drawn within 90 days of CABG but before the diagnosis of mediastinitis. Controls included patients who had ≥1 blood culture drawn within 90 days of CABG and did not develop mediastinitis. Controls were randomly selected from the study data set. Characteristics for 95 of the 98 possible cases and 95 controls were collected on the calendar date that blood cultures were drawn and before surgical debridement. A logistic regression model was generated to determine independent predictors for mediastinitis.

	Results

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A total of 5500 unique patients underwent median sternotomy for CABG during the study period (Table 1). Eight hundred seventy-six patients (15.9%) had at least 1 blood culture performed during the 90-day follow-up period. Blood cultures drawn after definitive diagnosis of mediastinitis from 21 patients were excluded. Thus, 855 patients were included in the final analysis (Figure).

View larger version (25K): [in this window] [in a new window]   Identification of 855 patients with at least 1 blood culture drawn within 90 days of median sternotomy for CABG.

Mediastinitis
The overall rate of mediastinitis for the 5500 patients was 2.58%. Ninety-eight of the 855 study patients in whom blood cultures were obtained developed mediastinitis. All 98 patients fulfilled CDC criteria for mediastinitis independent of blood culture results. Mediastinitis occurred in 46 of 60 (76.7%) patients with blood cultures positive for S aureus, 15 of 126 (11.9%) patients with blood cultures positive for other pathogens, 37 of 669 (5.5%) patients with blood cultures with no growth, and 44 of 4645 (0.9%) patients with no blood cultures obtained. None of the 48 study patients readmitted to different hospitals during the 90-day follow-up were diagnosed with mediastinitis.

S aureus was identified in sternal cultures from 65 of the 98 study patients (66%) with mediastinitis. Methicillin-resistant S aureus was present in 32 of 65 sternal isolates (49%). Other pathogens isolated from the mediastinum included coagulase-negative staphylococci in 13 patients (13%), Gram-negative bacteria in 10 patients (10%), and other pathogens (Enterococcus species, viridans group streptococci, Candida species, Bacteroides species, and polymicrobial infection) in 6 patients (6%). Mediastinal cultures were negative in 4 patients (4%). Among the 46 patients with S aureus bacteremia and mediastinitis, another potential source of bacteremia was identified by culture of S aureus from other sites in 6 patients (endotracheal suction culture in 3 patients; saphenous vein harvest site, empyema, and central venous catheter in 1 patient each).

Blood Cultures
A total of 2884 blood cultures were obtained from 855 study patients. Eighty-four percent (2421 of 2884) of these blood cultures yielded no growth. S aureus was the most frequently identified pathogen, present in 177 blood cultures from 60 patients. Among the 126 patients with pathogens other than S aureus (including 19 patients with polymicrobial bacteremia), a total of 33 pathogens were isolated in 198 blood cultures. These pathogens included coagulase negative staphylococci (81 patients), Enterococcus species (19 patients), yeast (10 patients), enteric Gram-negative bacteria (35 patients), and 9 other pathogens from 18 patients.

Of the 61 patients with both positive blood cultures and mediastinitis, data on clinical signs and symptoms were available for 60 (98.4%). Of these 60 patients, 8 patients (13.3%) had no obvious signs of mediastinitis (sternal pain, drainage, or instability). Six of these 8 patients (75%) had S aureus bacteremia; 1 patient each had bacteremia attributable to Enterococcus species and coagulase negative staphylococci. Signs of mediastinitis (sternal pain, drainage, or instability) were present in the remaining 52 patients with mediastinitis and positive blood cultures. Of these, 39 patients (75%) had S aureus bacteremia, and 13 patients had other pathogens (coagulase negative staphylococci in 6 patients, enteric Gram-negative rods in 5 patients, viridans group streptococci and Candida species in 1 patient each).

Timing of Blood Cultures and Mediastinitis
The median time from CABG to diagnosis of mediastinitis was 21 days (interquartile range [IQR], 13 to 36 days). The median interval from obtaining blood cultures to definitive diagnosis of mediastinitis was 3 days for both the overall cohort (IQR, 1 to 9 days) and patients with S aureus bacteremia (IQR, 1 to 8 days). Blood cultures from patients with mediastinitis were drawn significantly later after CABG than blood cultures from patients without mediastinitis (16 days [IQR, 9 to 26 days] versus 5 days [IQR, 3 to 13 days], P<0.001). Similarly, positive blood cultures among patients with mediastinitis occurred significantly later after CABG than positive blood cultures from patients without mediastinitis (15 days [IQR, 10 to 26 days] versus 11 days [IQR, 6 to 19 days], P=0.008).

Multilevel Test Table Analysis
The isolation of S aureus from even 1 blood culture drawn within 90 days of CABG was strongly associated with the subsequent diagnosis of mediastinitis. Patients with S aureus bacteremia were significantly more likely to have mediastinitis than patients without S aureus bacteremia (LR, 25; 95% CI, 14.7 to 44.4) (Table 2). Bacteremia attributable to other pathogens did not alter the pretest suspicion for mediastinitis, (LR, 1.0; 95% CI, 0.6 to 1.7). Patients with negative blood cultures were less likely to have mediastinitis (LR, 0.45; 95% CI, 0.35 to 0.58).

View this table: [in this window] [in a new window]   TABLE 2. Clinical Utility of Blood Culture Results in the Identification of Mediastinitis in 855 Patients Undergoing Median Sternotomy for CABG

Cohort Study of CABG Patients
In bivariate analysis of the entire cohort of 5500 patients, S aureus bacteremia was strongly associated with mediastinitis (Table 1). When multivariate modeling was performed on the entire cohort, S aureus bacteremia remained strongly associated with mediastinitis (OR, 52.98; 95% CI, 26.46 to 106.08) (model c-index, 0.844) (Table 1). When the model was repeated to include both 90-day all-cause mortality and mediastinitis as end points, the association between S aureus bacteremia and mediastinitis persisted (OR, 49.61; 95% CI, 20.50 to 120.08). Multivariate modeling of S aureus-specific demographic parameters demonstrated no characteristics significantly associated with mediastinitis among patients with S aureus bacteremia because of the small sample size of this subpopulation and because most patients with S aureus bacteremia had mediastinitis.

Case-Control Analysis of Patients With ≥1 Blood Cultures After CABG
Clinical signs and symptoms of infection among the 95 cases with mediastinitis and ≥1 blood culture were compared with 95 randomly selected control patients with ≥1 blood culture and no mediastinitis (Table 3). Among these 190 patients, S aureus bacteremia was strongly associated with mediastinitis by both bivariate (OR, 35.13; 95% CI, 10.23 to 120.62) and multivariate (OR, 152.12; 95% CI, 21.40 to >999.99) analyses. Sternal instability was also strongly associated with mediastinitis by bivariate analysis. Because no control patients had sternal instability, we could not evaluate this variable in the multivariate model. However, when the final multivariate model was performed among patients without sternal instability, S aureus bacteremia remained strongly associated with mediastinitis.

	Discussion

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Although mediastinitis is frequently fatal, rapid diagnosis is often difficult.⁹ The ability to more easily identify this complication would help clinicians to rapidly provide effective treatment. To our knowledge, this investigation is the first to evaluate the clinical utility of blood culture results in the identification of mediastinitis.

The current investigation’s findings depended on several factors: (1) a database containing clinical and follow-up information on a large cohort of consecutive, prospectively identified patients undergoing the same surgical procedure for the same therapeutic indication; (2) a second database incorporating the timing and results of all blood cultures taken from the study group; and (3) a third database containing prospectively identified patients with mediastinitis using well-accepted diagnostic criteria. Combining information from these databases led to the conclusion that S aureus bacteremia identified during routine clinical care was strongly associated with mediastinitis. This finding persisted when multilevel test table analysis, logistic regression, or case-control analysis was performed and is consistent with prior investigations.^1,10–13 However, unlike these prior studies, our investigation provides a clinically relevant means of quantifying the clinical significance of blood culture results to identify the presence of a devastating complication that is often difficult to diagnose.

Clinicians managing patients who have recently undergone median sternotomy need to know if a febrile patient with positive blood cultures is likely or unlikely to have mediastinitis. The findings of our study help such clinicians answer this question with three key observations: (1) if S aureus is present in blood cultures, the likelihood of mediastinitis greatly increases; (2) if another organism is present in blood cultures, the finding does not alter the pretest suspicion and additional evaluation will be needed when the suspicion is high; and (3) if blood cultures are negative, the patient is less likely to have mediastinitis.

Before the results of the current investigation, there were no diagnostic tests to reliably identify mediastinitis. Because of this limitation, a variety of diagnostic approaches to the diagnosis of mediastinitis have been evaluated, including aspiration of the mediastinal space,^14,15 ₁ acid glycoprotein and C-reactive protein measurements,¹⁶ procalcitonin level,¹⁷ and culture of perioperative instruments.¹⁸ Even advanced, expensive methods of radiographic imaging such as computed tomography,^19,20 fluorine-18 fluorodeoxyglucose positron emission tomography,^21,22 gallium-67 scintigraphy,²³ 99Tcm-labeled leukocyte scintigraphy, ^24,25 or single photon emission computed tomography with 99mTc-hexamethylpropylene amine oxime-labeled leukocytes²⁶ are either of limited benefit in identifying patients with postoperative mediastinitis or are widely unavailable. For example, the sensitivity and positive predictive value of computed tomography in the diagnosis of mediastinitis were as low as 25% and 71%, respectively.¹⁹ By contrast, the presence of S aureus bacteremia has high clinical utility (LR 25). Thus, a simple, inexpensive, and widely available diagnostic test such as blood culture is of great potential benefit to clinicians in identifying the presence of mediastinitis.

Likelihood ratios help clinicians to interpret the diagnostic value of a test before the disease status is known. In the present investigation, the LR for mediastinitis among patients with S aureus bacteremia is 25. A LR of this magnitude is clinically meaningful.²⁷ This association between S aureus bacteremia and mediastinitis remained strong when the entire cohort was evaluated with logistic regression modeling and when a case-control analysis was conducted among patients with blood cultures performed after CABG. Finally, because LR estimates are independent of disease prevalence, the significance of these findings should extend to other patient populations.

The investigation has several limitations. First, blood cultures were drawn based on clinical practice rather than as part of a study protocol. However, we believe that this fact enhances the utility of these results when applied to blood cultures drawn as a part of routine clinical care and expands the generalizability of the findings. Second, patients with mediastinitis dying before accurate diagnosis may also be a source of bias. However, when the analysis was adjusted for study patients who died during the 90-day follow-up period, the association of S aureus bacteremia and mediastinitis persisted. Similarly, when the analyses were repeated to include blood cultures obtained after the definitive diagnosis of mediastinitis, the association between mediastinitis and S aureus bacteremia also persisted. Finally, the findings in this study require validation within a separate cohort.

In summary, these results should help clinicians interpret blood culture results from patients who have recently undergone median sternotomy. The finding of S aureus bacteremia should make such clinicians highly suspicious for mediastinitis even if the clinical findings of a surgical site infection are minimal or indeterminate. The prompt identification of mediastinitis in such patients may in turn lead to early surgical drainage and a better outcome of this serious and sometimes fatal complication.

	Acknowledgments

 
Supported by K23 Awards AI-01647 (to Dr Fowler) and HL70861 to (to Dr Cabell) from the National Institutes of Health. The authors gratefully acknowledge the assistance of Lawrence H. Muhlbaier, PhD (Department of Biostatistics, Duke University Medical Center, Durham, NC).

Received February 4, 2003; revision received April 7, 2003; accepted April 9, 2003.

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