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Eur J Cardiothorac Surg 2008;33:673-678. doi:10.1016/j.ejcts.2008.01.002
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Deep sternal wound infection requiring revision surgery: impact on mid-term survival following cardiac surgery

Anand Sachithanandana, Prakash Nanjaiaha, Peter Nightingaleb, Ian C. Wilsona, Timothy R. Grahama, Stephen J. Rooneya, Bruce E. Keoghc, Domenico Paganoa,*

a Department of Cardiothoracic Surgery, University Hospital Birmingham NHS Foundation Trust, Birmingham B15 2TH, United Kingdom
b Wellcome Trust Clinical Research Facility, University Hospital Birmingham NHS Foundation Trust, United Kingdom
c National Institute for Clinical Outcomes Research, University College London, United Kingdom

Received 27 August 2007; received in revised form 1 January 2008; accepted 2 January 2008.

* Corresponding author. Tel.: +44 121 6272850; fax: +44 121 6272895. (Email: domenico.pagano{at}uhb.nhs.uk).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: To assess the impact of deep sternal wound infection on in-hospital mortality and mid-term survival following adult cardiac surgery. Methods: Prospectively collected data on 4586 consecutive patients who underwent a cardiac surgical procedure via a median sternotomy from 1st January 2001 to 31st December 2005 were analysed. Patients with a deep sternal wound infection (DSWI) were identified in accordance with the Centres for Disease Control and Prevention guidelines. Nineteen variables (patient-related, operative and postoperative) were analysed. Logistic regression analysis was used to calculate a propensity score for each patient. Late survival data were obtained from the UK Central Cardiac Audit Database. Mean follow-up of DSWI patients was 2.28 years. Results: DSWI requiring revision surgery developed in 1.65% (76/4586) patients. Stepwise multivariable logistic regression analysis identified age, diabetes, a smoking history and ventilation time as independent predictors of a DSWI. DSWI patients were more likely to develop renal failure, require reventilation and a tracheostomy postoperatively. Treatment included vacuum assisted closure therapy in 81.5% (62/76) patients and sternectomy with musculocutaneous flap reconstruction in 35.5% (27/76) patients. In-hospital mortality was 9.2% (7/76) in DSWI patients and 3.7% (167/4510) in non-DSWI patients (OR 1.300 (0.434–3.894) p = 0.639). Survival with Cox regression analysis with mean propensity score (co-variate) showed freedom from all-cause mortality in DSWI at 1, 2, 3 and 4 years was 91%, 89%, 84% and 79%, respectively compared with 95%, 93%, 90% and 86%, respectively for patients without DSWI ((p = 0.082) HR 1.59 95% CI (0.94–2.68)). Conclusion: DSWI is not an independent predictor of a higher in-hospital mortality or reduced mid-term survival following cardiac surgery in this population.

Key Words: Deep sternal infection • Survival


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Deep sternal wound infection (DSWI) is an uncommon but potentially devastating complication following cardiac surgery that results in significant morbidity and mortality. The reported incidence of DSWI ranges from 0.7% to 3% [1–9] with an in-hospital mortality of up to 25% [7]. Although different treatment strategies exist for the management of DSWI, the care of these patients remains challenging and often results in prolonged hospital stay and increased cost. Numerous risk factors have been identified as predictors of DSWI following cardiac surgery [1–11] which include obesity, advanced age, diabetes, smoking, use of bilateral mammary arteries (IMA), prolonged mechanical ventilation and re-exploration for bleeding but little is known regarding the impact of DSWI on mid-term survival following surgery.

The aim of this study was to evaluate the impact of DSWI on in-hospital mortality and mid-term survival following cardiac surgery.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Patient population
We reviewed data from the cardiac surgical database which holds prospectively collected clinical information on all patients undergoing cardiac surgery at our unit. The data is acquired prospectively as part of the patients’ pathway and is based upon the minimal dataset defined by the Society for Cardiothoracic Surgery in Great Britain and Ireland with some customised additions.1

Between January 2001 and December 2005, 4586 patients underwent a cardiac surgical procedure performed via median sternotomy. For the purpose of this study patients who underwent surgery on the thoracic aorta not performed via a median sternotomy, cardio-pulmonary transplantation or adult congenital procedures were excluded.

2.2 Definitions and inclusion criteria
In accordance with the Centres for Disease Control and Prevention (CDCP) Guidelines [12], a sternal infection was defined as an infection of the anterior mediastinal space with one of the following criteria: (1) isolated micro-organism from cultures of mediastinal tissue or fluid; (2) evidence of mediastinitis during operation; or (3) presence of either sternal pain or instability or pyrexia >38 °C, and either purulent discharge from the mediastinum or isolation of an organism from blood cultures or culture of drainage of the mediastinal area. We additionally defined a DSWI as a sternal infection that required surgical revision. Any patient with a mild sternal discharge confined to only the skin or subcutaneous tissues and not associated with underlying sternal instability that settled with simple dressings and antibiotic therapy was deemed to have a superficial sternal wound infection and excluded from the study. For the purpose of the analysis patients without DSWI were considered a control group. Any patient requiring insulin or oral hypoglycaemic therapy was defined as diabetic whilst any patient still smoking within 6 months of surgery was classed a smoker.

2.3 Patient follow-up
In-hospital mortality was tracked from our database and post-discharge survival data was obtained from the National Central Cardiac Audit Database, which is linked to the Office of National Statistics (census date 1 December 2006). In-hospital mortality was defined as death within 30 days of the operation or at any time within the same hospital admission.

2.4 Statistical analysis
Patients were classified into two groups based on the presence or absence of a DSWI. Numerical variables were presented as the mean ± standard deviation (SD) or median with interquartile range, and categorical variables summarised by percentages. Comparisons between the groups were made using t tests, Mann–Whitney tests, Fisher's exact tests or Kendall's tau-b statistics as appropriate. Stepwise logistic regression analysis was used for multivariable analysis, all variables with a p value of <0.05 in univariable analysis being available for inclusion. Kaplan–Meier analysis was used to compare survival in the two groups. The outcome measure in these survival analyses was all-cause mortality.

For each patient a propensity score was calculated representing the estimated probability that a given individual patient would develop a DSWI following cardiac surgery based on the variables considered. The propensity score was determined by logistic regression analysis with all preoperative, intraoperative and postoperative variables being entered into the model (Goodness of fit, Hosmer and Lemeshow test, Chi-square statistic = 6.42 with eight degrees of freedom, p = 0.60). The propensity score was then entered as a covariate into a Cox proportional hazards regression model to compare survival in the two groups whilst adjusting for baseline differences in patient and disease characteristics.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Incidence, patient and disease characteristics
DSWI requiring further surgery developed in 76 of 4586 patients (1.65%). Fifty-two patients developed a DSWI during the index hospitalisation and 24 patients developed a DSWI after discharge from the hospital and required readmission. The patients’ baseline characteristics are shown in Table 1 and surgical procedures are illustrated in Table 2 .


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  		Table 1 Patient demographics
 

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  		Table 2 Operative procedures
 
Organisms were isolated in 65 patients and included methicillin resistant Staphylococcus aureus (n = 21), other staphylococcus species (n = 27), pseudomonas (n = 8), serratia (n = 5), mixed growth (n = 4), klebsiella (n = 2), coliform (n = 2), Escheria coli (n = 1), enterobacter (n = 1), vancomycin resistant enterococcus (n = 1), and Stenotrophomonas maltophilia (n = 1).

There was no growth identified in 11 patients (n = 11). All patients were commenced on ‘best guess’ intravenous antibiotics at initial diagnosis and treatment was subsequently tailored according to culture and sensitivities.

The various surgical procedures undertaken for treatment of DSWI are listed in Table 3 . In the subgroup of patients who had sternal reconstruction with a musculocutaneous flap (n = 27), (35.5%) the following procedures were performed: isolated bilateral pectoralis major flaps (n = 14), isolated unilateral pectoralis major flap (n = 6), rectus abdominus flap (n = 3), omental flap (n = 1), unilateral pectoralis major + rectus abdominus flap (n = 2), and bilateral pectoralis major + omental flap (n = 1). All but one of these patients had previous vacuum assisted closure (VAC) therapy dressings (n = 26) prior to definitive sternal closure. Six patients had a concomitant split skin graft at sternal flap reconstruction.


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  		Table 3 Revision surgery for DSWI
 
3.2 Risk factors for developing DSWI
Univariate analysis identified increased age, prolonged preoperative hospital stay, increased duration of ventilation, diabetes, renal disease (serum creatinine >200 µmol/l or functioning renal transplant), and smoking as predictors for developing DSWI (Table 1). In patients undergoing CABG the use of an IMA was not a significant risk factor. Multivariable analysis identified diabetes, smoking, advanced age and prolonged ventilation as independent predictors for developing DSWI (Table 4 ).


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  		Table 4 Risk factors for DSWI (multivariable analysis)
 
3.3 In-hospital outcomes
There were seven in-hospital deaths (7/76) (9.2%) in patients with a DSWI and 167 in-hospital deaths (167/4510) (3.7%) in the control group (p = 0.024). However, risk adjusted analysis incorporating the propensity score in-hospital mortality showed no difference between the groups (OR 1.300; 95% CI 0.434–3.894; p = 0.639).

Patients with a DSWI were more likely to develop renal failure requiring haemofiltration, require reventilation, require a tracheostomy, and were at increased risk of a postoperative stroke (Table 5 ).


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  		Table 5 Major postoperative morbidity
 
The median postoperative stay of patients who developed a DSWI during their index hospitalisation (N-52) was 52 days (IQR 33–75.5) compared to 8 days (IQR 6–13) for patients without a DSWI (N-4534) (p < 0.001).

3.4 Post-discharge survival
Patients with a DSWI had a mean follow-up of (2.28 years) 832 days (range 15–1652) (173 patient-years) and the mean follow-up for the control group was (1.71 years 626 days (range 0–1652) (7973 patient-years).

Unadjusted freedom from all-cause mortality in patients with DSWI at 1 year, 2 years, and 3 years after surgery was 78.6 ± 4.8% (95% CI 69–88.2%), 75.6 ± 5.0% (95% CI 65.6–85.6%) and 69.4 ± 5.8% (95% CI 57.8–81%) respectively compared with 92.8 ± –0.4% (95% CI 92.4–93.2%), 90.7 ± 0.5% (95% CI 90.2–91.2%) and 87.7 ± 0.6% (95% CI 87.1–88.3%) for patients without DSWI (p < 0.001 Log rank (Mantel–Cox)) (Fig. 1 ).


Figure 1
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  		Fig. 1. Kaplan–Meier survival curve for unadjusted freedom from all cause mortality.

 
Risk adjusted predicted survival (Fig. 2 ) showed freedom from all-cause mortality in patients with DSWI at 1 year, 2 years, 3 years and 4 years following surgery was 91%, 89%, 84% and 79%, respectively compared with 95%, 93%, 90% and 86%, respectively for patients without DSWI ((p = 0.082) HR 1.59 95% CI (0.94–2.68)).


Figure 2
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  		Fig. 2. Risk adjusted Cox proportional hazard curve (incorporating propensity score as covariate). DSWI: deep sternal infection group; control: Non-infected group.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
Appendix A
 References
 
The aim of our study was to assess the impact of DSWI on survival in patients undergoing cardiac surgery. Our series indicate that DSWI is more likely to occur in patients with risk factors known to adversely influence the risk of surgery and the post-discharge outcome [13]. When adjusting for these risk factors, the development of DSWI was not a significant independent predictor of in-hospital mortality or reduced post-discharge survival. The findings on in-hospital outcomes are similar to those reported previously [2,9,14]. However, other studies had reported a negative impact of DSWI on long-term survival following coronary surgery [6–10,14] in contrast with our findings. Our study was not designed to compare different treatment strategies for DSWI, however a more favourable outcome of patients with this complication has been linked to different treatment strategies adopted. In previous series reporting adverse long-term survival for these patients [6–10,14] the treatment of DSWI consisted mostly of conventional methods, which included simple dressings, debridement and rewiring with or without irrigation. In our series, treatment of DSWI included VAC therapy in the majority (62 of 76) of patients (81.5%) with some requiring further definitive sternal reconstruction. Patients with VAC-treated mediastinitis have been shown to have a similar long-term survival (up to 5 years) as patients without mediastinitis following coronary surgery [15]. Vacuum-assisted closure provides an isolated wound with effective drainage in addition to sternal stabilisation. The negative pressure system stimulates granulation tissue formation, increases blood flow in adjacent tissues and assists with approximation of the wound edges [16,17].

Although sternal preservation should be a priority in the treatment of DSWI, debridement and eradication of infected material is the first priority. In some patients in our series, debridement resulted in a large defect and VAC therapy was utilised to sterilise and contract the wound to facilitate definitive closure. Sternectomy and musculocutaneous flap reconstruction was deemed necessary and performed by plastic surgeons. In this subgroup of patients (n = 27) (35.5%), pectoral major flaps were used either unilaterally or bilaterally, either in isolation or in combination with other flaps in 23 patients altogether. Previous studies have shown that use of a pectoralis major muscle flap reduces the mortality in patients with a DSWI [18,19].

The overall incidence of DSWI in our study was 1.65%, which is in accordance with the published literature [1–9]. However, varying definitions for DSWI can make comparison between studies somewhat cumbersome. We defined DSWI according to the standardised CDCP guidelines [12] with the additional criteria that surgical revision was required as this was a robust and objective clinical outcome measure thus selecting patients with objectively more advanced disease.

Advanced age, duration of ventilation, diabetes and smoking were independent predictors of DSWI following cardiac surgery. Most of these factors cannot be modified to reduce the incidence of this complication. However, tight perioperative glycaemic control with intravenous insulin in these patients can successfully reduce infective complications [20]. Although obesity and the use of BIMAs especially in diabetics are well-established risk factors for DSWI, neither were significant predictors for the development of DSWI in our study.

This finding could be explained by the low and comparable use of BIMA in both groups in our study (1.5%) and a similar incidence of obesity (defined as BMI > 30) in both groups. Although the long-term survival of patients developing DSWI was not significantly reduced in our series, a doubling of risk cannot be excluded. The development of this complication was associated with significant morbidity and prolonged length of stay in accordance with other studies [6,10].

4.1 Study limitation
The first limitation of our study is inherent in its observational nature. Although we analysed prospectively collected data, the database was not constructed to specifically address this issue. We do not have data to address the impact of different treatment modalities for patients with DSWI. We could not reliably exclude patients with superficial wound infection from the control group. In summary, this study confirms that higher risk patients are more likely to develop DSWI and when accounting for these, there is no evidence that DSWI affects survival following cardiac surgery.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
References
 
Conference discussion

Dr F. Robicsek (Charlotte, NC): This study in the United States will have a special significance because we are not only sued if our patients develop a sternal infection and die, but we are also if the patient survives because it's alleged that those patients have a shorter life expectancy. So I can tell you, you will be the darling of all defense attorneys in America.

I have only a few questions: one, obesity and bilateral mammary harvesting combined with diabetes have been listed as significant risk factors in practically all papers on the subject but not in yours. I would like to ask you why?

I myself tried to find the reason for this interesting conclusion that you made, and I think the only explanation could be that those patients who developed deep sternal infection and survived were the ‘durable’ ones. They have already withstood the test mediastinitis and probably had fewer other risk factors versus those patients who didn’t develop one. I’d like to ask what is your opinion on this?

Dr Sachithanandan: In relation to your first question, as you have rightly said, diabetes and the harvesting and use of bilateral internal mammary arteries is a well-established risk factor for the development of a deep sternal infection, and this did not emerge as a significant risk factor in our study.

If we look in terms of the incidence of diabetes, we had a significantly higher proportion of diabetics – sorry, I beg your pardon. I think you mentioned obesity and the use of bilateral IMAs, would that be right?

Dr Robicsek: Exactly.

Dr Sachithanandan: We looked at obesity in terms of the body mass index as a categorical variable, BMI above and below 30, and you will see that in our sternal wound group, the incidence of obese patients, which we defined with a BMI above 30, approximated to 25% which is a very little variation from the incidence in the control group. And that's probably why we were not able to demonstrate a difference in terms of this being a risk factor.

In relation to the other point –

Dr V. Gulielmos (Thessaloniki, Greece): Yes, excuse me, but the question was shouldn’t it be higher in the group with the sternal wound infection? That was Dr Robicsek's question, why wasn’t it higher?

Dr Sachithanandan: Well, this in essence is an observational study and is therefore retrospective in its nature.

Dr Gulielmos: He was asking do you have a feeling for this? Do you have an explanation?

Dr Pagano: In essence, the incidence of obesity was similar in the two groups and the use on bilateral IMA was also similar and less then 2% in both groups. For this reason, these well known factors contributing to risk of wound infection were not statistically relevant in our study.

Dr Robicsek: I have only one more question. What kind of rewiring method did you use?

Dr Sachithanandan: In the majority of cases, it was a modification of the technique that you originally described, so it was a modified Robicsek.

Dr Robicsek: Now, I understand your good results.


   Acknowledgments
 
We would like to thank Viv Barnett who ensures completeness of data collection in our cardiac surgery database. Professor R.S. Bonser was part of the study group; his exclusion from the co-author list is due to compliance with editorial requirements. This study was conducted as part of the Clinical Outcome and Performance Monitoring Unit initiative of the University Hospital Birmingham.


   Footnotes
 
{star} Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.

1 Society of Cardiothoracic Surgeons of Great Britain and Ireland. National Cardiac Surgical database. Minimum surgical dataset definitions. http://www.scts.org/mindata97.html. Back


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

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