(Circulation. 2000;101:2916.)
© 2000 American Heart Association, Inc.
Clinical Investigation and Reports |
Prolonged Antibiotic Prophylaxis After Cardiovascular Surgery and Its Effect on Surgical Site Infections and Antimicrobial Resistance
Presented in part at the Ninth Annual Meeting of the Society of Healthcare Epidemiology of America, April 18–20, 1999, San Francisco, Calif.
From the Department of Epidemiology (S.H.), Harvard School of Public Health, and Division of Infectious Diseases (M.H.S., D.L., Y.C.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Mass. Dr Carmeli is now with the Division of Infectious Diseases, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel. Dr Samore is at the Division of Infectious Diseases, University Hospital of Utah, Salt Lake City.
Correspondence to Stephan Harbarth, MD, MS, Division of Infectious Diseases, Enders Bldg 609, The Children’s Hospital, 300 Longwood Ave, Boston, MA 02115. E-mail harbarth{at}a1.tch.harvard.edu
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Abstract |
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Background—Despite evidence supporting short antibiotic prophylaxis (ABP), it is still common practice to continue ABP for more than 48 hours after coronary artery bypass graft (CABG) surgery.
Methods and Results—To compare the effect of short (<48 hours) versus prolonged (>48 hours) ABP on surgical site infections (SSIs) and acquired antimicrobial resistance, we conducted an observational 4-year cohort study at a tertiary-care center. An experienced infection control nurse performed prospective surveillance of 2641 patients undergoing CABG surgery. The main exposure was the duration of ABP, and main outcomes were the adjusted rate of SSI and the isolation of cephalosporin-resistant enterobacteriaceae and vancomycin-resistant enterococci (acquired antibiotic resistance). Adjustment for confounding was performed by multivariable modeling. A total of 231 SSIs (8.7%) occurred after a median of 16 days, including 93 chest-wound infections (3.5%) and 13 deep-organ-space infections (0.5%). After 1502 procedures using short ABP, 131 SSIs were recorded, compared with 100 SSIs after 1139 operations with prolonged ABP (crude OR, 1.0; CI, 0.8 to 1.3). After adjustment for possible confounding, prolonged ABP was not associated with a decreased risk of SSI (adjusted OR, 1.2; CI, 0.8 to 1.6) and was correlated with an increased risk of acquired antibiotic resistance (adjusted OR, 1.6; CI, 1.1 to 2.6).
Conclusions—Our findings confirm that continuing ABP beyond 48 hours after CABG surgery is still widespread; however, this practice is ineffective in reducing SSI, increases antimicrobial resistance, and should therefore be avoided.
Key Words: bypass • infection • antibiotics
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Introduction |
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The unnecessary and improper use of antibacterial agents in treatment, and particularly for prophylaxis ... will have to be modified or stopped completely. Maxwell Finland, 19701
Surgical site infections (SSIs) in cardiovascular surgery are associated with adverse outcomes.2 3 4 Among the different approaches to prevent these infections, antimicrobial prophylaxis is of substantial importance. Despite evidence from randomized clinical trials and other data supporting antibiotic prophylaxis (ABP) for no longer than 48 hours,5 6 7 8 controversy persists about the optimal duration of prophylaxis.9 10 In particular, it is still common practice to continue ABP for >48 hours after cardiac surgery until all chest tubes are removed.11 12 13 14 15 This routine, although never substantiated by scientific evidence, is aimed at reducing SSI rates, but it has generated concerns about the emergence of antibiotic resistance and other adverse events.16
Therefore, this 4-year observational cohort study was designed to examine the effect of prolonged ABP on the risk of SSI and the selection of antibiotic-resistant microorganisms after coronary artery bypass graft (CABG) surgery.
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Methods |
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This observational cohort study was conducted at the West Campus of Beth Israel Deaconess Medical Center (Boston, Mass), a 320-bed teaching hospital with
600 cardiovascular operations
per year. Patients were included if they had been operated on for CABG
or CABG/valve procedure between September 1, 1993, and August 31, 1997.
Each patient was included only once. An experienced infection-control nurse (D.L.) monitored patients who underwent cardiac operations and reviewed microbiology logs and medical reports to detect SSI. These data were prospectively reviewed and validated by the hospital epidemiologist (M.H.S.). SSIs were defined on the basis of National Nosocomial Infection Surveillance (NNIS) System criteria.17 All patients were followed up for at least 3 months after hospital discharge to detect late-appearing infections.
Additional demographic and microbiological data were collected from administrative, pharmacy, and laboratory computerized databases by use of a relational database management system (Access, Microsoft Corp). The databases and related methods of data collection were described before.18
Before surgery, patients took a chlorhexidine shower, and
chest hair was clipped without shaving either the night before or on
the morning of the operation. Immediately before surgical incision,
povidone-iodine was applied for cutaneous disinfection of the operative
site. In the operating room, beginning shortly before the first
incision, prophylactic intravenous antibiotics
(principally cefazolin 1 g; in some cases vancomycin 1 g,
ceftriaxone 1 g, or a combination of these agents) were
administered to each patient. In case of a prolonged intervention (
5
hours), the second dose of cefazolin was administered after completion
of cardiopulmonary bypass before closure of the sternal wound
to ensure an adequate serum level of the antibiotic agent. After
surgery, ABP was encouraged to be given for no more than 48 hours, but
it could be continued at the surgeon’s discretion.
The main exposure was duration of ABP (<48 hours versus >48 hours). The outcomes of interest were the occurrence of SSIs and isolation of a pathogen with acquired antibiotic resistance from a clinical specimen. For the purpose of the logistic regression analysis, patients with both chest and leg infections were classified as chest infections. In addition, first- and third-generation cephalosporin resistance in enterobacteriaceae (eg, Escherichia coli, Klebsiella spp, Proteus mirabilis) and vancomycin resistance in enterococci were considered to be acquired resistance and were the pathogens further examined.
Statistical Analysis
We used 
2 or t tests to
screen the following potential risk factors for SSI: Time from
admission to operation, previous intensive care unit (ICU) stay,
calendar time of the intervention (in 3-month intervals), sex, age,
number of comorbidities (defined as pulmonary, renal,
gastrointestinal, or hepatic conditions or malignant disease process
causing serious disability), American Society of Anesthesiologists
(ASA) classification (5-point assessment of the patient’s physical
condition conducted by the anesthesiologist immediately before
surgery), severe obesity (body mass index >37
kg/m2), diabetes mellitus (requiring either oral
therapy or insulin treatment), chronic kidney disease (chronic
underlying renal disorder), chronic lung disease (resulting in
functional disability), emergency operation (surgery performed shortly
after admission to avoid unnecessary morbidity or death), direct
hospital admission (patients admitted from home), anemia (prebypass
hematocrit: men 
35%, women 30%), renal insufficiency (prebypass
level of serum urea nitrogen >40 mg/dL), internal mammary artery
graft, antimicrobial prophylactic agent, surgeon, history
of previous cardiac surgery, additional valve replacement, and duration
of surgery (time from first incision to wound closure). Variables
with a value of P0.1 in the univariate
analysis were candidates for multivariable
analysis, as well as the main variable of interest
(duration of ABP). Multivariable modeling was performed by use of
conventional logistic regression analysis. Variables were
tested for significance by a Wald 2
statistic.
In a separate analysis, we analyzed the effect of
extended ABP on the isolation of microorganisms with acquired
antibiotic resistance irrespective of the calendar time and the
antibiotic agent used. To avoid confounding by indication and temporal
trends, we performed conditional logistic regression matched on the
type of prophylactic agent and calendar time. Variables
with a value of P0.1 in the crude analysis were
considered candidates for multivariable analysis and were
added to the model. Duration of prophylaxis was again forced into the
model. In addition, we tested variables for confounding by adding
them one at a time to the model and examining their effects on the ß
coefficients of the main exposure variable. Variables that
caused substantial confounding (change in ß coefficient of >10%)
were included in the final model. Effect modification was examined by
use of clinically important interaction terms.
All statistical tests were 2-tailed. Values of P<0.05 were considered significant. Statistics were run on SPSS 8.0 (SPSS) and STATA 5.0 (STATA Corp).
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Results |
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Study Population
From September 1993 through August 1997, 2641 adult patients underwent CABG, including 186 patients who received combined CABG and valve replacement procedures. The median age of the patients was 68 years (range, 29 to 91 years), with 75% of the population >59 years old. Of these patients, 831 (31.5%) were female. A total of 1467 patients (55%) were transferred from another healthcare institution; 116 patients underwent emergency operations shortly after admission. The median preoperative stay for all patients was 2 days (range, 0 to 28 days); 631 patients (23.9%) stayed in the ICU before the operation. Operation time averaged 5 hours (±1.1 hour). The median overall length of hospital stay was 9 days (range, 2 to 118 days), with a decreasing trend from 10 days in 1994 to 8 days in 1997 (Spearman’s r=-0.26, P<0.001).
With regard to ABP, 2180 patients received cefazolin, 385 patients vancomycin, and 222 patients ceftriaxone; 1502 patients (57%) received ABP for <48 hours (mean, 35.5±7.9 hours) and 1139 (43%) received ABP for >48 hours (mean, 76.0±30.2 hours).
Infections
Overall, 231 SSIs occurred after a median time interval of 16
days, corresponding to a rate of 8.7 SSIs per 100 operations. Chest
wound infections occurred after 93 operations (3.5%), and leg wound
infections without chest involvement after 138 interventions (5.2%).
The proportion of patients with deep-organ-space involvement
(mediastinitis) and sepsis requiring reexploration and drainage was 0.5
per 100 operations.
Among 231 SSIs, 176 (76%) were cultured (chest infections, n=82; leg infections, n=94). Positive cultures were recovered in 70% (123 of 176) of the cultured SSIs and most commonly yielded coagulase-negative staphylococci (n=52), enterococci (n=21), and Gram-negative organisms (n=51), whereas Staphylococcus aureus was encountered only infrequently (n=15). It is noteworthy that Enterobacter spp (n=8), Serratia spp (n=11), and Pseudomonas aeruginosa (n=11) were the 3 most prominent Gram-negative organisms obtained in wound cultures.
ABP and Risk of SSI
The effect of the duration of ABP on the risk of SSI was first
examined by univariate analysis and showed that the
rates were almost identical in both groups: 131 SSIs (8.7%) were
recorded after 1502 procedures with short prophylaxis compared with
100 SSIs (8.8%) after 1139 operations with prolonged prophylaxis
(crude OR, 1.0; CI, 0.8 to 1.3). In contrast, 11 other variables
were found to be associated with an increased risk of SSI by
univariate analysis (P0.1): female
sex, obesity, direct hospital admission, diabetes mellitus, chronic
kidney disease, chronic lung disease, number of comorbidities, ASA
classification, anemia, renal insufficiency, and duration of surgery
(Table 1
). After inclusion of
these variables in a multivariate logistic
regression model and after control for seasonal variation, the risk of
SSI was significantly correlated with female sex (OR, 1.6; CI, 1.1 to
2.2), obesity (OR, 2.5; CI, 1.2 to 5.4), number of comorbidities (OR
increase per increment, 2.2; CI, 1.1 to 4.4), ASA score IV (OR, 1.6;
CI, 1.1 to 2.4), duration of surgery (OR increase in 1-hour increments,
1.1; CI, 1.0 to 1.3), and direct hospital admission (OR, 1.6; CI, 1.1
to 2.2). After adjustment for the above-mentioned independent risk
factors for SSI, prolonged ABP was not associated with a decreased risk
of SSI (adjusted OR, 1.2; CI, 0.8 to 1.6). In a separate
analysis, we confirmed these results for the association
between extended prophylaxis and sternal wound infections only
(adjusted OR, 0.9; CI, 0.6 to 1.4).
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ABP and Isolation of Resistant Organisms
Of 2641 patients, 1094 (41%) had had cultures taken at any body
site. In 426 patients (16%), 1 microorganism resistant to
the administered prophylactic agent was isolated; leading
pathogens were coagulase-negative staphylococci (20%),
Candida spp (19%), and Enterococcus spp (16%).
In 166 patients (6%), cephalosporin-resistant
enterobacteriaceae (excluding other Gram-negative rods such as
Pseudomonas aeruginosa) or vancomycin-resistant
enterococci were recovered. Enterobacteriaceae resistant to
first-generation cephalosporins were retrieved in 97%,
enterobacteriaceae resistant to third-generation cephalosporins
in 23%, and enterococci resistant to vancomycin in 4% of
these 166 patients.
Multivariable analysis including postoperative
antibiotic therapy and length of ICU stay, as well as relevant
preoperative and perioperative variables,
demonstrated that 4 variables were associated with an increased
risk of isolation of enterobacteriaceae or enterococci with acquired
resistance (Table 2): antibiotic therapy
after CABG, age >65 years, combined CABG/valve surgery, and prolonged
ABP. Thus, even after control for confounding, prolonged ABP was
associated with an increased risk of acquired antibiotic resistance
(OR, 1.6; CI, 1.1 to 2.6).
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Discussion |
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Antimicrobial prophylaxis complements meticulous technique in reducing the incidence of SSI after cardiovascular surgery. Although the principles of surgical prophylaxis have been outlined on numerous occasions, there is still misuse of antimicrobials for this purpose.16 19 Our results demonstrate that prolonging ABP beyond 48 hours after CABG surgery is still frequently practiced but does not decrease the risk of SSI. Moreover, it results in an increased risk of acquired antibiotic resistance and should therefore be avoided.
Some researchers have suggested that extended prophylactic use of antibiotics is appropriate when drains or catheters remain in situ for several days after cardiac surgery.20 The antibiotics would presumably protect the wound from a secondary infection that originated in the foreign body and reached the wound by a hematogenous route. Therefore, surgeons tend to continue antibiotics as long as perioperatively placed transthoracic devices are left in place. For instance, in a survey among 43 pediatric cardiovascular surgery centers in the United States, up to 76% continued antibiotics while chest tubes were in place.13 A questionnaire sent to 120 UK cardiac surgeons showed that 28% continued antibiotic use until the removal of all chest drains.12 In a French survey among 1473 anesthetists, 23% prescribed >48 hours of antibiotics after cardiovascular surgery.
However, results from our study and other reports appear to invalidate this practice. Already 20 years ago, in a double-blind, randomized clinical trial comparing a 6-day with a 2-day regimen of cephalothin prophylaxis, Goldmann et al5 showed that a 6-day course of prophylactic antibiotics after cardiac surgery is not justified. The only published study comparing single-dose prophylaxis versus extended prophylaxis after thoracostomy in chest trauma patients showed no need for use of prophylaxis for as long as the chest tube was in place.21 These findings are also in line with a recent meta-analysis of single- versus multiple-dose prophylaxis for major surgery that indicated no benefit for multiple-dose regimens in preventing SSI in various surgical interventions requiring postoperative drainage.22 In contrast, prolonged antibiotic use after surgery induces antimicrobial resistance and may facilitate the colonization of foreign devices with antimicrobial-resistant organisms.23 24 25 Therefore, in place of extended ABP, meticulous handling of catheters, strict compliance with hand disinfection, maintenance of closed drainage systems, and early catheter removal are the preferred means to avoid infections related to foreign devices.26
Observational cohort studies should complement controlled clinical trials dealing with ABP, because the latter have a limited ability to detect adverse effects such as acquisition of resistant microorganisms, provide information only about patients who satisfy the criteria for study entry, and often concentrate on the efficacy of specific agents rather than evaluate variations in the duration of prophylaxis.27 In addition, randomized trials do not provide data on the effect of therapeutic interventions in actual clinical practice. In contrast to many previously reported clinical trials, the present study focused on the duration of prophylaxis rather than on antibiotic choice. All patients undergoing coronary bypass surgery were included in the analysis, thereby increasing the generalizability of the study results. However, as in all observational studies, there may have been unknown or unmeasured confounding factors for which adjustment was not possible. For instance, despite adjustment for important covariates such as age, number of comorbidities, length of ICU stay, and postoperative antibiotic therapy, it is difficult to completely exclude the possibility of residual confounding among subjects with acquired resistance.
The inappropriate prophylactic antibiotic administration in our cardiovascular surgery unit may have arisen primarily from misconceptions regarding the optimal use of prophylaxis. In some cases, ceftriaxone was chosen as prophylactic agent because of its pharmacokinetic profile, including high serum levels, high tissue penetration, and long elimination half-life, which makes it potentially suitable for prophylaxis in prolonged surgery.28 However, shortly before the end of the study period, we introduced strict antibiotic guidelines and stopped this practice because of antibiotic resistance concerns and cost implications.
The findings should be interpreted in the context of the study design. First, because routine surveillance cultures were not obtained from study patients, one may raise questions about the possible underestimation of the frequency of acquired antibiotic resistance. However, by matching for antibiotic agent, adjusting for calendar time, and including only patients with positive cultures, we minimized the possibility of significant detection bias. Second, an explanation for the association of combined CABG/valve surgery with increased antibiotic resistance is not directly apparent from our study results. We hypothesize that these patients are more likely to have received previous courses of antibiotics for prophylaxis or treatment of endocarditis due to underlying valve abnormalities, thus increasing the risk of acquiring antibiotic resistance. Third, the patient population reported in this study is notable for a high frequency of diabetes and referral from other institutions. These characteristics may have increased the SSI rate (but not the rate of mediastinitis, which was similar to that reported elsewhere), although the observed overall infection rate also probably reflected the intensive nature of the surveillance program. However, we do not believe that these surveillance methods and patient characteristics distorted the generalizability of our study findings.
In conclusion, our study confirms that ABP for CABG surgery is frequently extended beyond 48 hours. It shows that prolonged prophylaxis does not reduce the rate of SSI and is associated with an increased risk of acquired antibiotic resistance. We urge surgeons and all concerned physicians not to ignore the potentially harmful and costly effect of prolonged ABP after CABG surgery.
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Acknowledgments |
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Dr Harbarth was the Harvard University Holtzer Scholar when this work was performed and is currently recipient of Max-Kade Fellowship.
Received October 26, 1999; revision received January 7, 2000; accepted February 1, 2000.
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M. A. Olsen, T. M. Sundt, J. S. Lawton, R. J. Damiano Jr, D. Hopkins-Broyles, P. Lock-Buckley, and V. J. Fraser Risk factors for leg harvest surgical site infections after coronary artery bypass graft surgery J. Thorac. Cardiovasc. Surg., October 1, 2003; 126(4): 992 - 999. [Abstract] [Full Text] [PDF]
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H. L. Keyserling, R. L. Sinkowitz-Cochran, J. M. Harris II, G. L. Levine, J. D. Siegel, B. H. Stover, S. A. Lau, and W. R. Jarvis Vancomycin Use in Hospitalized Pediatric Patients Pediatrics, August 1, 2003; 112(2): e104 - 111. [Abstract] [Full Text] [PDF]
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S. Harbarth, K. Ferriere, S. Hugonnet, B. Ricou, P. Suter, and D. Pittet Epidemiology and Prognostic Determinants of Bloodstream Infections in Surgical Intensive Care Arch Surg, December 1, 2002; 137(12): 1353 - 1359. [Abstract] [Full Text] [PDF]
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M. A. Olsen, P. Lock-Buckley, D. Hopkins, L. B. Polish, T. M. Sundt, and V. J. Fraser The risk factors for deep and superficial chest surgical-site infections after coronary artery bypass graft surgery are different J. Thorac. Cardiovasc. Surg., July 1, 2002; 124(1): 136 - 145. [Abstract] [Full Text] [PDF]
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S. Harbarth, S. Cosgrove, and Y. Carmeli Effects of Antibiotics on Nosocomial Epidemiology of Vancomycin-Resistant Enterococci Antimicrob. Agents Chemother., June 1, 2002; 46(6): 1619 - 1628. [Full Text] [PDF]
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M. Carrier, R. Marchand, P. Auger, Y. Hebert, M. Pellerin, L. P. Perrault, R. Cartier, D. Bouchard, N. Poirier, and P. Page Methicillin-resistant Staphylococcus aureus infection in a cardiac surgical unit J. Thorac. Cardiovasc. Surg., January 1, 2002; 123(1): 40 - 44. [Abstract] [Full Text] [PDF]
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 P. Eggimann and D. Pittet Infection Control in the ICU Chest, December 1, 2001; 120(6): 2059 - 2093. [Abstract] [Full Text] [PDF]
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M. Carrier, L. P. Perrault, M. Pellerin, R. Marchand, P. Auger, G. B. Pelletier, M. White, N. Racine, and D. Bouchard Sternal wound infection after heart transplantation: incidence and results with aggressive surgical treatment Ann. Thorac. Surg., September 1, 2001; 72(3): 719 - 723. [Abstract] [Full Text] [PDF]
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 General Medicine: Prolonged Postoperative Antibiotics May Be Harmful Journal Watch Dermatology, August 28, 2000; 2000(828): 12 - 12. [Full Text]
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 Prolonged Postoperative Antibiotics May Be Harmful Journal Watch (General), July 7, 2000; 2000(707): 5 - 5. [Full Text]
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