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Ann Thorac Surg 2000;69:1104-1109
© 2000 The Society of Thoracic Surgeons

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ORIGINAL ARTICLES: CARDIOVASCULAR

Coagulase-negative staphylococci and sternal infections after cardiac operation

^a Division of Infectious Diseases, Department of Health and Environment, and Division of Cardiothoracic Surgery, Department of Medicine and Care, Faculty of Health Sciences, Linköping University, Linköping, Sweden

Address reprint requests to Dr Tegnell, Division of Infectious Diseases, Department of Health and Environment, Faculty of Health Sciences, Linköping University, S-581 85 Linköping, Sweden
e-mail: anders.tegnell{at}inf.liu.se

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Coagulase negative staphylococci (CoNS) have been recognized as important pathogens in nosocomial infections, especially in connection with implanted foreign materials. In cardiac operation they are among the most common pathogens isolated from infected sternal wounds. The definition of the infection is very important. In this study we focus on deep postoperative chest infections.

Methods. By studying 33 infected patients retrospectively and comparing them to 33 matched uninfected controls, we studied the characteristics and costs of the infections.

Results. Typical for these infections is the late and insidious onset, and that the infections initially give only minor symptoms such as pain, redness, and serous secretion. We found the following risk factors for infection: number of preoperative days in a hospital, the total length of the operation, and if the patient had undergone an early reoperation due to causes other than infection. This kind of infection more than doubled the hospital costs for the patients affected.

Conclusions. Coagulase negative staphylococci are the most important pathogens in deep postoperative infections in this material. They cause infections that are difficult to recognize since they give only discrete symptoms and start well after the patients leave the hospital. The risk factors for patients with CoNS infections are mostly associated with a long exposure to the hospital environment. The treatment is often difficult and costly because of multiresistant bacteria and frequent need for repeated surgical revisions.

	Introduction

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Sternal infection after cardiac operation is a rare but important complication, with an incidence ranging between 0.9% and 20% in different studies [1]. The reason for the wide range is partly due to the fact that different diagnostic criteria have been used in different studies. Criteria for defining deep and superficial infections have been published [2], and the Center for Disease Control in the United States has also established criteria for reporting surgical site infections [3]. Deep infections, such as sternitis and mediastinitis, cause high morbidity and mortality, increased costs for the healthcare system, and added suffering for the patients. Prevention, registration, and the early recognition of these infections have become important means for reducing these complications of cardiac operation.

In the past coagulase negative staphylococci (CoNS) were often dismissed as a contaminant when found in a bacterial culture from a surgical wound. In recent studies CoNS have proved to be one of the most important pathogens in postoperative infections after cardiac operation [4, 5]. Reports about pathogens causing postoperative infections indicate a shift from gram negative to gram positive bacteria, especially CoNS, in recent years [6]. Coagulase negative staphylococci is known to be an important pathogen when foreign material is implanted. This is always the case in cardiac operations where stainless steel wires are used for closure of the sternotomy.

The diagnosis of postoperative infections caused by CoNS is difficult. The infections often have a slow and late onset, with few of the classical symptoms of wound infection [7]. Levels of markers for inflammation such as C-reactive protein (CRP) and fever may be normal [8].

The use of risk factors as predictors for postoperative complications has been tried in many studies. The outcomes of these studies have been conflicting. The onset of deep infections related to cardiac operation is sometimes late, well after the patients have been discharged from the hospital where operation was performed. Since the trend is toward shorter hospital stays, the proportion of postoperative infections presenting at other health facilities will probably increase. In the present study we retrospectively studied the characteristics and costs of deep postoperative sternal infections.

	Material and methods

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During the period 1990 to 1994, 3,075 cardiac operations, mainly coronary artery bypass grafting (CABG) and heart valve operations, were performed at the University Hospital in Linköping, Sweden. Patients were referred for operation from the surrounding region comprising approximately 950,000 inhabitants and 9 referring hospitals. The University Hospital is the only hospital in this region performing cardiac operation, and all major complications, including reoperations, were managed there.

Patients were normally admitted to the ward either from their home or directly from another ward or hospital, 2 days before operation. Preoperative preparation of the patients included two showers with hexachlorophene soap and the clipping of excessive hair where necessary. During the study period (1990 to 1994), cloxacillin 2 g, 3 times daily starting 30 minutes before the incision, was used as standard perioperative antibiotic prophylaxis, and patients with a history of allergy to penicillin received clindamycin (600 mg, 3 times daily). During the first 2 years the antibiotic prophylaxis period was 3 days, and in the last year it was shortened to 1 day. Surgery was performed through a median sternotomy. Cardiopulmonary bypass and systemic hypothermia to 28 to 32°C was used. Most patients were sent to their referring hospitals 5 to 6 days after the operation.

Records on patients with deep sternal infections were retrieved through the diagnosis register at the Department of Cardiothoracic Surgery. Cases of deep sternal infections included in this study were defined as any patient undergoing CABG or valvular operation through a median sternotomy starting in January 1990 until and including June 1994, and who were registered at the department as having mediastinitis or sternitis, by the surgeon performing the revision, before the end of 1995. Surgeons’ notes on revisions were retrospectively reviewed to classify the infections according to the following criteria:

1. Superficial infection:
   
2. Infection that involves only skin or subcutaneous tissue
   
3. Deep infection:
   
4. Infection that goes below the fascia without involvement of the bone or the retrosternal tissue;
   
5. Infection involving the retrosternal tissue;
   
6. Infection involving the bone and the retrosternal tissue;
   
7. Infection with osteitis.
   

Infection type 2 B, C, and D would all be called mediastinitis according to the classification of El Oakley and colleagues. They have made subtypes according time of presentation, risk factors, and treatment failures while we have followed Horan and colleagues and made a classification according to anatomical structures involved. The remaining classes 1 and 2 A (not represented in this study) could have different names in the literature such as deep incisional infection and superficial infection, respectively [2, 3].

The study was retrospective. Records of infected patients were compared with the records of the same number of control patients. The controls were selected from the surgical register with a match for time of procedure, age ± 5 years, and type of operation. The next patient registered in the surgical register, with a comparable age who had undergone the same procedure was selected. Variables before, during, and after operation that were retrieved from patient records including variables characterizing the infection, are depicted in Table 1.

According to an agreement between the Swedish National Board of Health and Welfare and the hospitals providing care, the latter are reimbursed with a fixed sum per day of care per patient. The amount is dependent on the level of the health facility where the care is given. Procedures such as CABG and heart valve operation are reimbursed with a fixed sum irrespective of the number of days spent in the hospital (up to a certain maximum postoperative days). The reimbursements in this agreement were used to calculate the cost of each of the infected and control patients. All costs were based on the 1998 agreement.

All data are given as median and range. Statistical analysis was performed using Staview (Abacus Concepts, Inc, Berkeley, CA) and STATA (Stata Corporation) computer programs. To evaluate potential risk factors the Mann Whitney U test was used for continuous variables. For discontinuous variables, odds ratios were calculated, and the McNemar test was used to establish the level of significance. The difference was considered significant if the calculated p value was less than 0.05.

	Results

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The incidence of deep sternal infections in this series was 0.9% (33 patients), calculated as a ratio of all procedures performed. There was no difference between CABG (1.1%), valve replacement (1.0%) or combined procedures (0.8%). Infected patients had a longer hospital stay before operation and a longer duration of the cardiac operation than did control patients. There was no difference between the groups in median height, weight, time on CPB, blood transfusion, days in the intensive care unit, or time with chest tubes (Table 2). Reoperation in the early postoperative course for complications such as postoperative bleeding was a significant risk factor for development of sternal wound infection, while gender, smoking, earlier cardiac operation, type of antibiotic prophylaxis, other antibiotic treatment, and emergency operations, were not (Table 3).

The symptoms recorded at the time of the surgical debridement for sternal infection were compared between the different groups of infection. Patients with type B infection had more symptoms, more frequently had pus and fever, but had less pain than those with type D infection. The C-reactive protein (CRP) level and white blood cell count (WBC) were higher in type B infections than in type D infections, median 182 (range 36 to 333) mg/mL versus 25 (10 to 135) mg/mL and median 12 (range 7 to 28) x 10⁹/L versus 7 (3 to 20) x 10⁹/L, respectively (p < 0.005).

Table 4 shows the type of bacteria found in the cultures taken during the first revision of the infected wounds. In the 11 patients with a recurrent infection, CoNS were cultured from 10, although other bacteria had been found in initial cultures from 3 patients. Three out of 7 patients (42%) with type B infections had CoNS in their cultures and in an additional 2 (29%) patients CoNS were found together with other bacteria. CoNS were cultured from 20 (86%) of the 26 patients with type D wound infections and in 18 patients (69%) it was the only isolated pathogen; in 2 patients coagulase negative staphylococci and another bacterial species was isolated. The antibiotic resistance pattern of isolated CoNS strains are shown in Table 5. Seventy-three percent of the CoNS found were resistant to methicillin.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
To define and classify postoperative infections in a standardized way is of great importance to be able to compare results from different studies and in the development of treatment protocols. We have based our definitions on the United States Center for Disease Control criteria, and have developed them further for sternal infections in order to make them useful in the decision about what treatment to use.

Our study shows that CoNS are an important cause of deep sternal infections after cardiac operation. We found the proportion of CoNS to be 64%, which is considerably higher than has been reported in other studies, where the reported incidence was 0% to 46% [9]. It could be argued that CoNS in some cases might represent a contamination, but in all of these cases CoNS was the only bacteria isolated, and in most cases a successful cure was not achieved until they received antibiotic therapy effective against the CoNS found.

In 73% of our patients with sternal infections there was a long interval (more than 3 weeks) between cardiac operation and reintervention. All these patients had type D infection. It could be argued that this chronic osteomyelitis of the sternum might be due to not having surgically revised the sternum at an early stage of the infection [10]. When we retrospectively scrutinized the patient records for symptoms of infection at the time of diagnosis and subsequent reintervention, it was found that discrete symptoms had been present for some time, ie, a median of 20 days (0 to 240). The evaluation of symptoms of infection in a retrospective study has an inherent weakness. However, at the time of diagnosis we consistently found chest pain, redness, and serous secretion as major symptoms. We also found that patients presenting with a sternal infection after an interval of more than 3 weeks also had fewer and less obvious symptoms and less pronounced infective markers like CRP and WBC than those presenting earlier, which also makes the diagnosis of late infections more difficult. The lack of prominent, classical symptoms of infection is thus one possible explanation for the long time interval between heart surgery and readmission for surgical treatment of the sternal infection. The predominance of CoNS as the major pathogen in this study is probably one of the reasons for the scarcity of symptoms and for the long interval between cardiac operation and treatment of the infection. This is in agreement with what Mossad and colleagues found in their study on CoNS infections [5]. He reported a mean interval of 26 days (range 4 to 403) between discharge and readmission as compared to a median of 48 days (range 4 to 270) between operation and reintervention in our study. In both series this time interval is much longer than the follow-up period generally used in studies of postoperative sternal infections. Thus, it is likely that the incidence of postoperative sternal infections is often underestimated, since all infections caused by CoNS may not be reported.

Interestingly, however, the time until diagnosis of CoNS infections was not significantly longer in our study, as would be expected with a type of bacteria that is known to cause indolent infections [11]. The number of non CoNS infections were too small to allow for further statistical analysis of differences between infections caused by CoNS and infections caused by other bacteria.

We have found some reports on the incidence of a recurrence of deep sternal infection in the literature. In one report, 1 out of 19 patients with deep infection had a recurrence [12]. In our study, 11 of 33 cases had a recurrence of the infection. Seven of these were caused by CoNS, and an additional 4 by mixed infection where one of the bacteria was CoNS. When looking at cultures from the second revision, 10 out of 11 had growth of only CoNS. It is difficult to establish whether or not recurrence is a finding related to CoNS infections. The well-known ability of CoNS to adhere to foreign materials [13] such as the stainless steel wires in the sternum may be one reason to assume that recurrence is more common in infections caused by CoNS.

Which of the risk factors that are most important for the development of postoperative sternal infection is still under debate [1]. In our study, we found only three risk factors out of the 27 variables recorded that were related to this infection. These risk factors have also been found in several other studies [14]. Whether infections caused by different bacteria have different risk factors has been studied by Rodriguez-Hernandez [15], who compared gram positive and gram negative infections. He found few differences, but the risk factors consistently had higher impact in patients with infections caused by gram negative bacteria.

A possible reason for the scarcity of risk factors in our study could be that the study deals mainly with infections caused by CoNS. The risk factors we found in our study may be related to an increased exposure to the hospital environment with multiresistant CoNS strains [16], and probably not to factors related to the individual. This is another reason for believing that pathogens that are the major cause of infection might inherently determine which risk factors are found in the patient population under study. In other words, different bacteria may have different pathogenic mechanisms for infecting surgical wounds. Since different patients may vary in their susceptibility to these pathogenic mechanisms, and conditions in the hospital might favor certain mechanisms, this may explain the variation in risk factors found in different studies of postoperative sternal infections.

A number of studies have been published in which estimates of the costs of cardiac operation and its complications have been made. Most are from the United States. In our study we found that a postoperative sternal infection doubles the hospital cost. Additional costs for the patient, such as loss of income, travel expenses, etc, may add substantially to this. Different health care systems calculate the cost of care differently, which makes direct comparisons difficult. Mauldin and associates calculated that in the United States the cost of a CABG procedure was estimated to be $25,000 [17]. The extra cost for the sternal infection in their study was only minor compared to the total cost. In other studies the increase in costs due to postoperative infection is in the same range as in our study [17, 18].

	References

Top Abstract Introduction Material and methods Results Comment References

 

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