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Eur J Cardiothorac Surg 2008;33:232-238. doi:10.1016/j.ejcts.2007.11.016
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.

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Algorithm for primary closure in sternal wound infection: a single institution 10-year experience

Alain Jean Ponceleta,*, Benoit Lengelec, Bénédicte Delaereb, Francis Zechb, David Glineura, Jean-Christophe Funkena, Gebrine El Khourya, Philippe Noirhommea

a Department of Cardio-Vascular and Thoracic Surgery, Cliniques Universitaires Saint-Luc, Catholic University of Louvain, Belgium
b Department of Infectious Diseases, Cliniques Universitaires Saint-Luc, Catholic University of Louvain, Belgium
c Department of Plastic and Reconstructive Surgery, Cliniques Universitaires Saint-Luc, Catholic University of Louvain, Belgium

Received 4 June 2007; received in revised form 21 November 2007; accepted 22 November 2007.

* Corresponding author. Address: Cardio-Vascular and Thoracic Surgery Unit, Cliniques universitaires St-Luc, Université catholique de Louvain, Avenue Hippocrate 10, B-1200 Brussels, Belgium. Tel.: +32 2 7646107; fax: +32 2 7648960. (Email: poncelet{at}chir.ucl.ac.be).


    Abstract
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objectives: To evaluate a simple treatment algorithm in sternal wound infection (SWI) allowing for primary closure and to describe the different surgical techniques and their associated morbidity and mortality. Methods: A retrospective analysis of all patients operated on between 1996 and 2004 in a single tertiary care institution. All epidemiological and surgical data were prospectively collected in our database. Univariate and multivariate analysis were used to determine preoperative and perioperative risks factors for 90-day and long-term mortality. Results: Out of 5905 procedures, 146 sternal wound infections were documented (2.4%). The respective incidence of SWI for CABG, isolated valve, or combined procedures were 2.8%, 1.1%, and 3.2%. Pathogens involved were S. epidermidis (44.5%), S. aureus (31.5%), and gram-negative rods (19.2%). Re-operation was required in 131/146 patients. Mean time to the first re-operation was 17.3 ± 12 days. Modalities of treatment consisted of drainage alone (44 patients), rewiring (25 patients), debridement, rewiring and mediastinal lavage (52 patients), and partial/complete sternal resection (10 patients). Additional procedures were required in 49 patients (37.7%). The 90-day mortality for uninfected patients and patients with superficial SWI were 4.4% and 2.8% (p = 0.78) whereas for patients with deep SWI, 90-day mortality was 14.5% (DSWI vs others, p < 0.0001). Conclusions: Deep sternal wound infection (DSWI) remains a dreadful complication in contemporary cardiac surgery while risk factors are currently well defined. Using a simple approach of primary closure together with liberal use of vascularized flaps has allowed us to achieve satisfactory short-term outcome in this subset of patients.

Key Words: Surgery cardiothoracic • Bypass coronary surgery • Mediastinitis • Decision making


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Sternal wound infection (SWI) after cardiac surgery is an infrequent complication with a reported incidence varying from 1% to 4% [1–5]. The associated risk of hospital death has been reported to range from 7% to as much as 29% [1,4,6–8].

Short-term results have improved with the introduction of aggressive management [4] whereas patients’ long-term outcome was shown in several studies to be adversely affected [5–8].

Among risk factors identified as independent predictors of infection, some are patient-related (diabetes mellitus, obesity, chronic obstructive pulmonary disease (COPD), re-operation, peripheral vascular disease, renal failure), others are procedure-related (duration of surgery, use of both internal thoracic arteries, blood product requirements), and finally, others relate to the perioperative period (duration of ventilation, re-exploration for bleeding, pulmonary or G-I complications) [1–3,8].

Several surgical techniques were developed over the last decades: open wound dressing, closed irrigation, closed suction drainage and more recently, vacuum-assist drainage [9–15]. All along, autologous vascularized flap (pectoralis major, greater omentum, latissimus dorsi, or rectus abdominis) have been selectively used for definitive repair [16,17].

The aim of this study was to analyze our 10-year experience with a single algorithm of aggressive debridement and closed suction drainage, to identify risk factors for treatment failure, and to determine risk factors for in-hospital mortality in such patients.


    2. Material and methods
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Study population
From January 1996 to October 2004, 5905 patients underwent open-heart surgery through a complete sternotomy at our university hospital. All epidemiological and surgical data were prospectively recorded in our cardiac surgery database. The protocol for infection prophylaxis remained identical over the entire period. Patients were hair-clipped the day prior to surgery, and showered with povidone–iodine soap the day prior and on the morning of surgery. The operative field was painted with povidone–iodine solution and the skin was covered with an adhesive plastic sheet (Vi-drape®, MCD Inc., H & W, Glabbeek, Belgium). Sternum closure was performed using interrupted stainless steel wires followed by two layers of running absorbable sutures. Skin was closed by an absorbable subcuticular suture in all cases (Vicryl, Ethicon Inc., Somerville, NJ, USA). A closed suction system to drain the subcutaneous space was not used systematically and left to the discretion of the surgeon.

Prophylaxis against infection included 1.5 g of a second-generation cephalosporin (Zinacef®, GlaxoSmithKline AG, Rixensart, Belgium) administered intravenously 1 h prior to surgery, with a similar dose given during the cardio-pulmonary bypass. Two additional doses were administered postoperatively at 8 h intervals in all patients. For all patients, we measured arterial plasma glucose concentration every 30 min, starting just before anesthetic induction by an automated blood gases and blood pH test system (ABL 700, Radiometer Copenhagen, Denmark). Patients did not receive insulin during surgery unless their glucose levels exceeded 11.1 mmol/l (200 mg/dl). If glucose concentration was above 11.1 mmol/l (200 mg/dl), patients received an intravenous bolus of 4 units insulin followed by an intravenous pump infusion of insulin that was continued until the glucose level was less than 8.3 mmol/l (<150 mg/dl).

2.2 Management of infection
Diagnosis of sternal infection was based on at least one of the following findings: wound tenderness, purulent drainage, cellulitis, fever and/or leukocytosis and/or sternal instability.

Sternal wound infections were classified according to the guidelines of the Center for Disease Control and Prevention (CDC) [18]. Briefly, superficial infections (SSWI) were defined as being limited to the subcutaneous and soft tissue without periosteal involvement. Diagnosis of deep sternal wound infection (DSWI) required at least one of the following criteria: (1) an organism was isolated from culture of mediastinal tissue or fluid; evidence of mediastinitis was seen during operation; or (2) one of the following: chest pain, sternal instability, or fever 38 °C, was present and there was either purulent discharge from the mediastinum or an organism isolated from blood culture or culture of drainage of mediastinal area.

Simultaneously, all deep sternal wound infections (DSWI) were classified according to the criteria proposed by El Oakley and Wright [19].

In case of limited superficial wound infection, our strategy consisted of systemic oral antibiotic therapy together with daily povidone–iodine dressing. Surgical debridement was to be performed only if conservative management failed (group I, n = 15). In all other cases of SWI, patients were brought back to the operating room and wounds were re-explored. For infection localized to the subcutaneous tissues (group II, n = 44), the wound was debrided, subsequently irrigated with povidone–iodine solution and primary closed with a 14-Fr closed suction drainage. For wound infection contiguous to the sternal bone (group III, n = 25), all sternal wires, fascia, and subcuticular sutures were removed, staged specimen (skin to periosteum) were taken for culture, the sternum was closed over a mediastinal 18-Fr closed suction drain and the subcutaneous space was primarily closed as for group II. For wound infection involving the sternum (group IV, n = 52), in addition to the steps described for group III, the sternum edges were debrided, and after appropriate culture sampling, both the pleural space and the pericardial sac were vigorously irrigated, firstly with 4–5 l of normothermic saline solution, followed by povidone–iodine solution. All cavities were drained and the wound was primarily closed as for groups II and III. For patients in whom the infection had extensively altered the bony structures (group V, n = 10), in addition to the steps described for group IV, extensive sternal debridement led to such defects that autologous muscular or greater omentum flaps were required at the first re-operation.

In groups III, IV, and V, intravenous antibiotic therapy was given according to the results of the in vitro sensitivity assays and continued for 3–6 weeks. Cultures were taken from drains twice weekly. When the infection recurred despite the primary procedure, the patient was brought back to the operating room and the same algorithm based on tissue involvement (as described above) was used. Additional debridement, lavage, and rewiring were performed in 27 patients, whereas additional omental and/or pectoralis major transfers were required in 30 patients.

2.3 Data collection and follow-up
A computerized registry database (Summit Vista, Summit Medical Systems Inc., Knoxville, TN, USA) of all cardiac procedures performed from 1996 through 2004 was analyzed. Hospital and outpatient records of patients with sternal wound complication were extracted for the study and reviewed.

Multiple variables related both to the patient and the procedure were recorded prospectively and analyzed retrospectively as predictors of 90-day and long-term mortality. Variables and their definitions are listed in Appendix A. 90-day mortality was defined as any death occurring within 90 days following the initial procedure. Long-term mortality was defined as any death occurring after the initial procedure (including 90-day deaths).

Follow-up of discharged patients was 100% complete (127/127 patients) until closure of the study as of 01/04/2005. All follow-ups were done through the referring cardiologist, the primary physician or patient's family when appropriate.

2.4 Statistical analyses
Length of hospital stay (LOS) was calculated from the day of the initial surgery to the day of initial discharge whether the patient returned home or to a rehabilitation facility. Additional in-hospital days related to the sternal wound infection were cumulated to the initial LOS.

Survival was calculated from the date of the first surgery to the end-point (90-day mortality), or to the date of latest follow-up (long-term mortality), or death. For analysis of descriptive statistics and categorical variables, Chi-square or Fisher's exact test were used for comparisons of dichotomic variables, Student's t-test was used for comparisons of continuous variables, and a log rank test was used for comparisons of intervals of time as length of stay, length of time to re-operation, or length of survival. Survival percentages were computed by the Kaplan–Meier method. Univariate and multivariate regressions of survival data were done by the maximum likelihood method with the Cox proportional-hazards model. All preoperative and perioperative predictors were included in the univariate analysis whereas variables with a p value equal or <0.10 by univariate analysis were selected for multivariate analysis. A backward conditional method was used for variable selection by the Cox multivariate regression analysis. All statistical analyses were performed with SPSS version 11.5 software (SPSS, Inc., Chicago, IL).


    3. Results
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Patient's characteristics are summarized in Table 1 . As expected, when we compared the two groups (SWI vs no SWI), SWI patients were more frequently obese, had more risk factors such as smoking, COPD, diabetes, peripheral vascular disease, and congestive heart failure. SWI patients had a lower mean ejection fraction. In SWI group, patients were younger, more patients were operated on for CABG, had BITA harvesting, required perioperative intra-aortic balloon pump (IABP) or were re-operated for ischemia and/or bleeding. In this study, there was no difference in the duration of aortic cross-clamp and/or bypass time between infected and non-infected patients. More patients in the SWI group were operated on a non-elective basis. The respective incidence of SWI for isolated CABG, isolated valve, and combined procedures was 2.8% (106/3737 patients), 1.1% (14/1334 patients), and 3.2% (26/811 patients). Among 146 patients, 36 patients fulfilled CDC criteria as described in material and methods for superficial SWI and 110 fulfilled criteria for deep SWI [4,18]. Table 2 summarizes the El Oakley and Wright's classification of patients with deep SWI. A total of 197 procedures were performed among the 131 patients from group II to V (mean: 1.5 re-operation/patient).


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Table 1 Pre- and perioperative characteristics of study cohort (n = 146 vs 5759 patients)
 

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Table 2 Classification of deep sternal wound infections (DSWI) (n = 110)
 
3.1 Intent to treat (ITT) procedures and primary success rates
The median time to re-operation for SWI was 13 days [range 3–102 days]. Sixteen patients (12.3%) were re-operated for SWI within 1 week from primary surgery, 59 patients (45.4%) were re-operated between the first and the second week, 23 patients (16.7%) were re-operated between the second and the third week, and 33 patients (24.6%) were re-operated beyond the third week after their initial surgery.

As described in Fig. 1 , we divided the study cohort in five groups according to the initial treatment applied once the diagnosis of sternal wound infection was confirmed. There was no statistical difference in delay from primary surgery between groups II, III, IV, and V; however there was a trend for a longer time for group V (median delay 15, 10, 13, and 17 days, respectively; p = 0.06 (log rank test)).


Figure 1
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Fig. 1. Primary success rate of treatment according to ‘intention to treat’. Group I: conservative treatment + oral antibiotics; group II: lavage + drainage; group III: lavage + drainage + rewiring; group IV: high volume lavage + drainage + sternal debridement + rewiring; group V: primary sternal resection + autologous vascularized flaps.

 
In group I (n = 15), no attempt for wound revision was made and those patients were treated with local antiseptic and systemic antimicrobial therapy. There was no treatment failure and all patients were discharged with a median duration of hospitalization of 13 days. In group II (n = 44), 25 patients (57%) were successfully treated with lavage and drainage alone, including our last two patients in whom a vacuum-assist device (VAC) was used to fasten the healing process. However, 19 patients (43%) required additional procedures, of which 10 required autologous vascularized flaps (Fig. 2 ). In group III (n = 25), 16 patients (64%) were successfully treated with lavage, drainage, and rewiring. Out of nine treatment failures, six patients required autologous vascularized flaps for successful infection control (Fig. 2).


Figure 2
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Fig. 2. Additional procedures after primary failure. Group II: lavage + drainage; group III: lavage + drainage + rewiring; group IV: lavage + high volume lavage + drainage + sternal debridement + rewiring; group V: primary sternal resection + vascularized flaps. (*) Out of five primary sternal resection with pectoralis major flaps, three will subsequently require additional greater omentum interposition.

 
In group IV (n = 52), the success rate of primary treatment by high volume lavage, sternal debridement, rewiring, and drainage was 79% (41/52 patients) and among 11 patients with initial treatment failure, only 6 patients required autologous vascularized flaps (Fig. 2). For groups II, III, and IV, the median duration of hospitalization was 30, 31, and 44 days, respectively (p = 0.05, log rank test). In the 10 patients in whom the sternal destruction was so advanced at the first re-operation that first-line autologous vascularized flap was required (group V), only 4 patients (40%) were successfully treated at the first attempt. Three out the six treatment failures required additional autologous vascularized flaps. Group V had by far the longest in-hospital stay with a median duration of 69 days (p < 0.002, log rank test).

Overall, among 131 re-operated patients, 83 patients (63.8%) underwent a single-stage procedure, 33 patients (25.4%) underwent a two-stage procedure, and 15 patients (11.5%) underwent three or more procedures. For the entire group, the median hospital stay was 39 days (mean 40.8 ± 23.7 days).

Analysis of the primary success rate for the subgroups II–V revealed an inter-group difference that was significant (p = 0.04), with the highest primary success rate (79%) in the group of patients in whom the most aggressive, though conservative, treatment was applied at the time of first re-exploration (high volume lavage, sternal debridement, rewiring, and drainage).

3.2 Pathogens
Microorganisms obtained from tissue culture are summarized in Table 3 . One patient received prolonged oral antibiotic therapy prior to admission and cultured specimen remained negative. The commonest pathogens were Staphylococcus epidermidis (n = 65) and Staphylococcus aureus (n = 46), together representing 111 patients (75.5%) whereas in 28 patients (19.2%), a gram-negative microorganism was the confounding pathogen. Of note, two or more pathogens were found in 21 patients (14.4%).


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Table 3 Pathogens isolated from wound secretions and/or mediastinal fluids in SWI patients (n = 146)
 
Positive blood culture was present in 50 patients (34.5%) and was similarly found in gram-positive (32.4%) and gram-negative infections (37.9%) (Fisher's exact, p = 0.45). The mean duration of antimicrobial treatment after re-operation was 31 ± 17 days.

3.3 Univariate analysis of risk factors for 90-day mortality
Among the 146 patients, 17 died within 90 days from initial surgery (11.6%). The mortality among SWI patients differed significantly according to the initial procedure: 9.6% for CABG (10/104 patients), 7.7% in combined procedures, and 35.7% among the isolated valve(s) procedures (Chi-square p = 0.03). Excluding two patients with endocarditis from the ‘valve’ group, the difference in mortality (33% vs 9.2% for CABG ± valve) remained of borderline significance (Chi-square p = 0.08). Interestingly, in the CABG group, 8 (out of 43) and 2 (out of 61) patients died in the single and bilateral ITA groups, respectively (p = 0.01). As expected, the 90-day mortality was higher in the DSWI group (14.5% vs 2.8% in SSWI) (p = 0.04).

As shown in Table 4 , several other risk factors for early mortality were identified. Among the patient-related factors, pre-existing chronic renal failure (HR 4.1), prior cardiac surgery (HR 3.6) were the strongest predictors of early death. Among the procedure-related factors, prolonged ICU stay (HR 3.3), postoperative renal failure (HR 9.6), and perioperative transfusion requirements (HR 3.9) were all significant predictors of mortality. Finally, among the infection-related variables, the need for flap interposition at the first repair procedure (HR 4.5), the presence of concomitant bacteremia, and S. aureus infections were significantly correlated to 90-day mortality (HR 7.2 and HR 5.5, respectively).


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Table 4 Predictors of 90-day mortality by univariate analysis
 
3.4 Multivariate analysis of risk factors for 90-day mortality
In multivariate analysis, as shown in Table 5 , among the patient-related factors, pre-existing chronic renal failure (HR 4.8) remained strong predictors of early death. Among the procedure-related factors, only postoperative renal failure (HR 4.8) was found to be significant. Finally, among the infection-related variables, the presence of concomitant bacteremia was significantly correlated to 90-day mortality (HR 6.2).


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Table 5 Predictors of 90-day mortality by multivariate analysis
 
3.5 Univariate and multivariate analysis of risk factors for long-term mortality
In univariate analysis, all variables that influenced 90-day mortality (by univariate analysis) remained significant for long-term mortality. In addition to those, other variables that had significant impact on long-term mortality were peripheral vascular disease (HR 4.8), congestive heart failure at surgery (HR 2.7), need for re-exploration other than infection (HR 2.4), and perioperative TIA/CVA (HR 2.9). In multivariate analysis, all variables that influenced 90-day mortality (by multivariate analysis) with the exception of bacteremia remained significant for long-term mortality. In addition to those, other variables that significantly impacted on long-term mortality were peripheral vascular disease (HR 3.3), need for re-exploration other than infection (HR 2.2), use of flap for coverage at first re-intervention for infection (HR 2.8) and S. aureus infection (HR 2.3).


    4. Discussion
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
In this study, the overall incidence of SWI according to the CDC definition was found to be 2.4% in our cardiac surgical population. The respective incidence of SWI for isolated CABG, isolated valve, and combined procedures of 2.8%, 1.1%, and 3.2% are in agreement with several other published studies for which only the DSWI rates have often been reported [1–5].

For the last decade, our algorithm for SWI has been an aggressive approach of re-exploration together with primary closure as often as possible.

Pursuing this approach enabled us to obtain an overall primary repair success rate of 64% (for those patients re-operated on). This figure includes the few patients (10/130) with extensive bony destruction at the time of SWI diagnosis. Analysis of subgroups according to the type of re-operation highlighted the significant improvement in the primary success rate when extensive lavage and tissue debridement were performed when compared to the three other groups; with 79% of patients in whom this re-operation led to successful eradication of infection.

Another finding of this study is the high primary failure rate of primary closure in patients with extensive bony destruction at the time of SWI diagnosis. Those patients, in our series, were diagnosed late in the course of infection (28 days after initial surgery) and only 4/10 patients where successfully treated upfront with vascularized flaps. Noteworthy, three out of five patients with pectoralis major transpositions had to be converted later on to greater omentum transfers, whereas patients with greater omentum interposition either healed successfully or required only minor revisions at subsequent re-operations. This should prompt us to raise a word of caution in using muscular flaps for primary closure in the setting of massive bony destruction where either a delayed closure or the use of greater omentum should be advocated. Despite recent studies reporting on the use of vacuum-assisted drainage in SWI patients that showed high success healing rates [12–15], none of those studies have so far provided a detailed analysis of their results in such cohort of patients that combines 50% of bilateral ITA harvesting and 40% of diabetic patients as we presented in this series.

Our 90-day mortality (12.2% for the patients who where re-operated on, 11.6% overall) compares favorably to contemporary large studies. Indeed, Kirsch et al. [11] and Douville et al. [4] reported an in-hospital mortality rate of 23.6% and 14%, in series of 72 and 57 patients, respectively. Similarly, Tempoulis et al. [8] reported an in-hospital mortality of 15%.

In univariate analysis, we found several risk factors for death after SWI: patients-related factors such as preoperative renal failure, peripheral vascular disease, re-operation, CHF are all well-recognized risk factors for mortality in cardiac surgery [3,20]. The negative correlation (protective effect) of BITA use in this study must be seen in the light of the very high mortality in the group of SWI patients who had received valve surgery (33%). Interestingly, we found a strong association between death in SWI patients and re-exploration for bleeding, or with transfusion requirements, variables that have been shown to be important in large-scale studies [2,21]. To note, the incidence of re-exploration for bleeding before the onset of SWI was three-fold higher in our study group when compared to the 5759 patients who did not develop SWI during the same study period. Thus, re-exploration for bleeding predisposes to SWI that, in turn, leads to further transfusion requirements and increases the likelihood of death.

Finally, as it has been shown by others [11], infection-related factors such as S. aureus and positive blood culture are strongly related to the severity of SWI and to survival outcome. In their study, Gardlund et al. [22] were able to show a correlation between the pathogenic microorganism and patients factors such as COPD, obesity, and re-exploration for bleeding. In our study, we could not corroborate their findings. Moreover, contrary to their conclusion, we did find a correlation between bacteremia and in-hospital mortality.

In conclusion, SWI remains a potentially devastating event in contemporary cardiac surgery. With several periprocedural risk factors being elucidated, every effort should be made to minimize the incidence of sternal infections. We believe that an early, aggressive approach to SWI that includes mediastinal lavage, sternal edge debridement, and rewiring has led to a significant improvement in the primary closure success rate, with obvious downstream benefits to the patients such has a decreased need for repeat interventions, a decreased rate of autologous tissue transfers, better cosmetics, and finally but not least, improved outcome.


    Appendix A
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Variables assessed in predictive models

Related to patient


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Related to the procedure


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Related to the infection


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    References
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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