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Ann Thorac Surg 1997;63:395-401
© 1997 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Coagulase-Negative Staphylococcal Sternal Wound Infections After Open Heart Operations

Department of Infectious Diseases, Infection Control, and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio

Accepted for publication August 9, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. Coagulase-negative staphylococci are commonly isolated from wounds of patients after median sternotomy; however, the epidemiology of these infections is poorly described and the morbidity, mortality, and cost of care remain undefined.

Methods. Retrospectively, we studied all patients with sternal wound infections attributable to coagulase-negative staphylococci after 22,180 open heart procedures performed at the Cleveland Clinic between January 1, 1988, and December 31, 1994 (84 months). In an assessment of potential risk factors for sternal wound infections caused by coagulase-negative staphylococci, 17 patients with coagulase-negative staphylococcal sternal wound infections were compared with 29 patients who underwent open heart operations without subsequent sternal wound infections, as well as with another 22 patients in whom sternal wound infections attributable to other pathogens developed.

Results. A total of 436 sternal wound infections were identified (19 per 1,000 procedures), of which 100 (23%) were attributable to coagulase-negative staphylococci (4.5 per 1,000). Fifty-six percent of coagulase-negative staphylococcal sternal wound infections were superficial, 27% were deep, and 17% represented mediastinitis; 14% of patients had a concomitant secondary bloodstream infection. Ninety-two percent of coagulase-negative staphylococcal isolates were methicillin resistant. The mean interval from operation to onset of infection was 24 days (range, 4 to 388 days), and most patients had purulent discharge from the chest wound, fever, and leukocytosis. Adverse outcomes included reexploration (39%), flap operation (12%), and sternectomy (5%); 89% required parenteral antibiotics for a mean of 22 days. This resulted in 2,600 additional hospital days, with an average additional direct cost per case of $20,000. In both case-control studies, insulin-dependent diabetes mellitus was the only risk factor significantly associated with sternal wound infections attributable to coagulase-negative staphylococci (p value = 0.02 by two-tailed Fisher's exact test).

Conclusions. Sternal wound infections attributable to coagulase-negative staphylococci had a substantial impact on cardiothoracic surgery-related morbidity.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Infection of median sternotomy wounds remains a major problem complicating cardiac operations. The incidence of postoperative sternal wound infections (SWIs) ranges between 0.5% and 7% [1–5], and the mortality rate attributed to SWIs ranges between 7% and 20% [5]. The development of SWI is associated with the longest intensive care unit and hospital stay among all postoperative complications [6, 7]. At our institution, the direct cost of treatment of patients in whom mediastinitis developed after cardiac operations was three times that of patients without infection, and charges substantially exceeded reimbursement [1].

Risk factors for surgical site infections after open heart operation include diabetes mellitus [1, 4], obesity [1, 4], current cigarette smoking [4], large breast size [8], prolonged preoperative length of stay in the hospital [4], prolonged operative time [1, 3, 5], the use of both internal mammary arteries (IMAs) for coronary artery bypass grafting (CABG) [1, 2, 9, 10], excessive operative or postoperative bleeding [1, 2, 5], reexploration for the control of hemorrhage [2, 5], prolonged postoperative low cardiac output [2, 5, 11], and prolonged postoperative artificial ventilation [2, 3, 11].

Although antibiotic prophylaxis for cardiothoracic operations has resulted in a reduction in surgical site infection rates, it may result in the emergence of more resistant organisms [12, 13]. Cephalosporins are widely used for antibiotic prophylaxis in cardiac operations and may select for colonization of patients with antibiotic-resistant coagulase-negative staphylococci in the postoperative period [14, 15]. Coagulase-negative staphylococci are commonly isolated from median sternotomy wounds, but are often not considered to be pathogenic. We describe 100 patients with SWI attributable to coagulase-negative staphylococci after cardiac operation and assess the potential risk factors and the economic impact of these infectious complications.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background
Between 1988 and 1994, 22,180 median sternotomy procedures were performed at The Cleveland Clinic Foundation. Patients undergoing open heart operations routinely received perioperative prophylactic antibiotics with either cefamandole (from January 1988 to May 1991), cefuroxime (after May 1991), or vancomycin (for penicillin-allergic patients). Prophylactic antibiotics were routinely given in the operating room by the anesthesiologist immediately before the induction of general anesthesia, and their administration was continued for 48 hours postoperatively.

Cultures of purulent wound drainage are routinely sent to the clinical microbiology laboratory using either a culturette swab or in a capped syringe. Aerobic cultures were performed on all specimens, and the Vitek method (Biomerieux Vitek, Inc, Hazelwood, MO) was used to identify the organism and determine the antimicrobial susceptibility pattern of the isolates of coagulase-negative staphylococci.

Definition and Ascertainment of Case Patients
A case patient was defined as any patient in whom an SWI attributable to coagulase-negative staphylococci developed after an open heart operation from January 1, 1988, through December 31, 1994. Only cultures from a sternal wound yielding coagulase-negative staphylococci as a sole isolate and fulfilling the Centers for Disease Control and Prevention definitions for surgical site infections were included in the study [16]. Superficial SWIs were defined as involving only skin or subcutaneous tissue; deep SWIs were defined as infections involving deep soft tissue (eg, fascial and muscle layers) of the incision; and mediastinitis was defined as infection involving any part of the anatomy (eg, organs or spaces), other than the incision, opened or manipulated during the operative procedure. A diagnosis of sternal osteomyelitis required histologic evidence of infection in excised bone. Fever was defined as an oral temperature of more than 37.5°C and leukocytosis was defined as a white blood cell count greater than 11,000/µL.

Active surveillance for surgical site infections in patients undergoing median sternotomy was performed by the same infection control practitioner (J.M.S.) during the entire study period. Retrospectively, we reviewed the cardiovascular wound registry at The Cleveland Clinic Foundation to obtain cases of SWI attributable to coagulase-negative staphylococci. Patient medical records were also reviewed for clinical and microbiologic information. Long-term follow-up was obtained by reviewing outpatient charts and by telephone calls to patients.

Case-Control Studies
Between October 1993 and March 1994, an increased incidence of SWI attributed to coagulase-negative staphylococci was noted. To assess potential risk factors for coagulase-negative staphylococci SWI, we conducted two case-control studies. A variety of host factors were evaluated, including modified APACHE (Acute Physiology, Age, Chronic Health Evaluation) score, sex, age, tobacco use, previous sternotomy, diabetes mellitus, obesity (defined as a body mass index more than 25), and operative factors (surgeon, procedure, antibiotic prophylaxis, duration of operation). In the first case-control study, 17 patients with coagulase-negative staphylococci SWI (case patients) were compared with 29 control patients without SWI who were operated on immediately before or after a case patient. In the second study, the 17 case patients were compared with 22 control patients in whom SWI developed during the same time period with organisms other than coagulase-negative staphylococci:Staphylococcus aureus (10 patients), culture-negative cases (5), Serratia marcescens, Pseudomonas aeruginosa, Proteus mirabilis, Branhamella catarrhalis, Diphtheroid bacilli, Bacillus species, and yeast (1 patient each).

Statistical Analysis
All data were entered into a computerized data base for analysis (Epi Info version 5.01; Center for Disease Control and Prevention, Atlanta, GA) [17]. Student's t test and Fisher's two-tailed exact test were used for univariate analyses of the significance of associations. The Mantel-Haenszel test was used for stratified analyses. Differences were considered statistically significant at a p value of less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Infection Rates
A total of 436 cases of SWI (19.6 of 1,000 procedures) were identified among 22,180 median sternotomy procedures during the 6-year study period, of which 100 (23%) were attributable to coagulase-negative staphylococci (4.5 per 1,000). Although the overall SWI rate did not vary significantly during the study period (Table 1), the rate of SWI attributable to coagulase-negative staphylococci was significantly higher during the last 36 months of the study period compared with the initial 48 months (27 of 12,194 procedures [2.2 per 1,000] versus 73 of 9,986 procedures [7.3 per 1,000]; p < 0.0001) (Fig 1).

View larger version (31K): [in this window] [in a new window]   Fig 1. . Emergence of coagulase negative staphylococcus (CNS) as a cause of sternal wound infection (SWI) after 22,180 median sternotomy procedures at The Cleveland Clinic Foundation; 1988–1994. (SWI = sternal wound infections.)

The mean interval from admission to the hospital to the index surgical procedure was 3.3 days (range, 0 to 37 days). The types of operative procedures included CABG using saphenous vein grafts and IMA (51%), CABG using saphenous vein grafts only (15%), valve replacement or repair (13%), CABG using saphenous vein grafts and valve replacement or repair (10%), thoracic aneurysm repair (4%), CABG using IMA only (3%), CABG using saphenous vein grafts and IMA and valve repair or replacement (2%), CABG using IMA and valve replacement or repair (1%), and cardiac transplantation (1%).

Postoperative complications other than SWI included respiratory failure requiring prolonged mechanical ventilation (12%), low cardiac output states requiring insertion of an intraaortic balloon pump (10%), cerebrovascular strokes (8%), acute renal failure requiring hemodialysis (6%), gastrointestinal bleeding requiring transfusion (5%), cardiac arrest (4%), peripheral arterial emboli (2%), and other complications (17%) (chest wound left open postoperatively [5%], emergent reoperation to control bleeding [5%], to relieve cardiac tamponade [2%], or to coapt dehiscence of a sternal wound [1%], coagulopathy [3%], and ventricular tachycardia [1%]).

Incisional Site Characteristics
The mean duration from the operative date to the onset of SWI was 23.8 days (range, 4 to 388 days). In 56 patients (56%) the SWIs were superficial, 27 (27%) were deep, and 17 (17%) were mediastinitis. Purulent discharge was present in 77% of patients, fever in 44%, and leukocytosis in 60%. A concomitant bloodstream infection with coagulase-negative staphylococci occurred in 14% of patients, 2 of whom had subsequent development of prosthetic valve infective endocarditis (Table 2).

View larger version (37K): [in this window] [in a new window]   Fig 2. . Organisms causing 436 sternal wound infections after 22,180 median sternotomy procedures at the Cleveland Clinic Foundation; 1988–1994. (CNS = coagulase-negative staphylococci.)

View larger version (23K): [in this window] [in a new window]   Fig 3. . Susceptibility pattern of coagulase-negative staphylococci to tested antibiotics. All coagulase-negative staphylococci isolates were tested; refer to Table 1 for the exact number of isolates identified each year.

A total of 89% of patients were seen in consultation by an infectious disease staff physician, and 89% of the patients received intravenous antibiotic therapy. The mean duration of antibiotic therapy (intravenous and oral) was 27 days (range, 0 to 84 days), and the mean duration of intravenous antibiotic therapy was 22 days (range, 0 to 42 days). Forty-eight percent received intravenous antibiotic therapy after discharge from the hospital using peripherally inserted central venous catheters (33%), tunneled central venous catheters (14%), or peripheral intravenous catheters (1%). The intravenous antibiotics used for treatment included vancomycin (85%), clindamycin (11%), gentamicin (3%), and oxacillin (1%). Oral antibiotics used for treatment included dicloxacillin, amoxicillin-clavulanate, cephalexin, trimethoprim-sulfamethoxazole, rifampin, doxycycline, and ciprofloxacin.

Outcome
A total of 94% of patients with SWI attributable to coagulase-negative staphylococci were successfully treated, 6% died of other causes before completion of therapy, and 90% were alive at follow-up. The median interval of follow-up was 146.5 days (range, 0 to 2,156 days), and the median interval to complete wound healing was 2 months (range, 1 to 48 months). In the 10 patients who died, the mean duration between the operation date and death was 67 days (range, 36 to 113 days); no deaths were directly attributed to coagulase-negative staphylococcal SWI. Causes of death included multisystem organ failure (4 patients), cerebrovascular accident (2), congestive heart failure (2), pneumonia (1), and fungemia (1 patient).

Results of Case-Control Studies
In the first case-control study, case patients were significantly more likely to have insulin-dependent diabetes mellitus than control patients (p = 0.002). No other risk factors were found to be significantly associated with the development of coagulase-negative staphylococcal SWI (Table 3).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

The overall prognosis of our patients was favorable: 94% were successfully treated and no deaths were directly attributed to coagulase-negative staphylococcal SWI. However, SWI attributable to coagulase-negative staphylococci had a substantial impact on cardiothoracic operation-related morbidity. Forty-two percent of our patients were readmitted to the hospital for management of their SWI, resulting in an additional 2,600 hospital days. The majority of patients required both a surgical intervention and treatment with intravenous antibiotics. The duration of antibiotic therapy was often prolonged, and 48% of patients received intravenous antibiotics after discharge from the hospital. The excess economic cost attributed to surgical site infections after open heart operations is substantial [1, 6, 7]. A previous study at our institution estimated the cost of mediastinitis after an open heart operation to be three times that of uninfected cases [1]. We estimated the average additional direct cost per case of coagulase-negative staphylococcal SWI to be $20,000 (1994 dollars).

Resistance of coagulase-negative staphylococci to multiple antibiotics further complicates therapy. Because of the high prevalence of methicillin resistance among coagulase-negative staphylococcal isolates causing SWI, vancomycin was the most commonly chosen antibiotic for therapy. Our rates of methicillin resistance among coagulase-negative staphylococci are similar to the rates reported by others [20–22].

Coagulase-negative staphylococci are present on the skin overlying the sternum in 80% to 90% of the population and are the most common cause of perioperative contamination in "clean" operations [20]. Previous studies have shown that patients undergoing open heart operations are often colonized preoperatively with methicillin-susceptible strains of coagulase-negative staphylococci, but methicillin-resistant coagulase-negative staphylococci postoperatively [13]. In one study, 87% of physicians and nurses were found to be colonized with coagulase-negative staphylococci in their nares, and almost 50% of the coagulase-negative staphylococci were methicillin-resistant [23]. Outbreaks of coagulase-negative staphylococci infections among patients undergoing cardiac operations have been linked to carriage of the organism on either the hands or in the nares of the surgeons [24, 25]. We found no epidemiologic evidence, by either surgeon-specific rates or in the case-control studies, to link any cases of coagulase-negative staphylococcal SWI to a particular surgeon or surgical team.

Because of the significant morbidity and costs associated with surgical site infections after open heart operations, there are compelling reasons to look at risk factors that may be modified to affect outcome. Our study identified two potential strategies for intervention for reducing the risk of SWI attributable to coagulase-negative staphylococci among our patients: antibiotic prophylaxis and glycemic control in diabetic patients. The timing of administration of antibiotics for surgical prophylaxis is very important in determining their efficacy, and prophylaxis should be administered within 2 hours of the skin incision [26]. The second-generation cephalosporins cefuroxime and cefamandole have emerged as the prophylactic antibiotics of choice for patients undergoing cardiac operation [27–29]. Cefuroxime has a longer half-life, thus requiring less frequent administration, offering substantial cost savings [28, 29]. Given the high prevalence of methicillin resistance among staphylococci, the use of vancomycin as prophylaxis for cardiac operation in certain groups of patients is being considered at our institution. Animal data suggest greater efficacy of prophylactic vancomycin versus cefazolin in a guinea pig model of Staphylococcus aureus wound infection [30]. There is considerable reluctance, however, to use vancomycin as the prophylactic agent for all median sternotomy procedures because of its restricted spectrum of activity (Gram-positive organisms) and the need for a slower infusion rate to avoid hypotension and "red-man syndrome" associated with rapid administration. More important, routine use of vancomycin has the potential for increasing resistance among nosocomial pathogens, particularly enterococci [31].

There is a growing body of clinical evidence that hyperglycemia increases the risk of nosocomial infections in the postoperative period. Diabetes mellitus also increases the risk for coronary artery disease, and approximately 15% of patients undergoing CABG at our institution are diabetic. Diabetes mellitus has been previously shown in our experience to be an independent risk factor for sternal wound complications, especially among diabetic patients who received bilateral IMA grafts [1]. We found patients with insulin-dependent diabetes mellitus to be at highest risk for SWI with coagulase-negative staphylococci after median sternotomy.

The integrated measures of glycemic control, such as hemoglobin A1c, reflect periods of glycemic control that are a function of the half-life of the glycosylated protein in the body. In the case of hemoglobin A1c, this is a period of about 2 months with a normal red blood cell life span. If one can demonstrate that poor chronic glycemic control (as measured by hemoglobin A1c values) is a risk factor for surgical site infections in diabetic patients undergoing open heart operations, then one could justify intervention in the preoperative period to normalize or improve glycemic control before operation.

There are several limitations to our study that should be recognized. Patients undergoing open heart operations at The Cleveland Clinic Foundation are often a referred population and therefore our findings may not be generalizable to other hospitals performing open heart operations. In addition, the majority of data were abstracted retrospectively by chart review, and the management and treatment of patients were not randomized or controlled by protocol. Because we only included patients in whom coagulase-negative staphylococci were the sole pathogen isolated from an infected wound, we excluded cases of SWI in which coagulase-negative staphylococci were isolated concomitantly with other organisms, and this may have resulted in exclusion of some patients in whom coagulase-negative staphylococci were the major pathogen in the development of infection. Case ascertainment also may not have been complete as most SWIs occur after discharge from the hospital [32].

In summary, we conclude that SWI attributable to coagulase-negative staphylococci had a substantial impact on cardiothoracic operation-related morbidity. Diabetes mellitus, which has been reported to be a risk factor for postoperative infections, was shown here to be specifically associated with coagulase-negative staphylococcal SWI after open heart operation. Interventions to decrease the risk of such infections may include aggressive glycemic control in diabetic patients undergoing open heart operations and the use of prophylactic antibiotics active against methicillin-resistant coagulase-negative staphylococci. Prospective studies will be required, however, to validate both of these approaches.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Gordon, Department of Infectious Diseases, The Cleveland Clinic Foundation, Mailstop S-32, 9500 Euclid Ave, Cleveland, OH 44195-5066 (e-mail: GordonS{at}CESMTP.CCF.ORG).

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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