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Ann Thorac Surg 2005;80:1765-1772
© 2005 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Incidence of Sternal Infection in Diabetic Patients Undergoing Bilateral Internal Thoracic Artery Grafting

Cardiothoracic Department, King's College Hospital, London, United Kingdom

Accepted for publication April 26, 2005.

^_* Address correspondence to Dr Momin, Cardiothoracic Department, King's College Hospital, Denmark Hill, London, SE5 9RS United Kingdom (Email: aziz.momin{at}kcl.ac.uk).

Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.

	Abstract

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
BACKGROUND: Bilateral internal thoracic artery (BITA) bypass grafts have advantages over single internal thoracic artery (SITA) bypass grafts in the medium term, particularly in diabetics. However, the perceived higher sternal complication rates seen in diabetics have led many surgeons to avoid the use of BITA surgery. The aim of our study was to assess the validity of this approach by assessing the incidence of sternal infections over a 10-year period in one institution.

METHODS: A retrospective analysis was made of our coronary artery bypass graft (CABG) patients over a 10-year period (7,581 patients). Nine hundred and twenty-two of the patients were diabetics (261 insulin-dependent diabetes mellitus [IDDM]). Of the insulin-dependent diabetics, 166 had SITA, and 95 had BITA grafts.

RESULTS: There was no significant difference in this subgroup in terms of gender, preoperative angina, dyspnea class, left ventricular function, and number of distal anastomoses. Comparing the rates of sternal wound complications of SITA and BITA in IDDM are the following: (1) superficial sternal infection, 6.6% in SITA, 1.1% in BITA (p = 0.04); (2) deep sternal infection, 1.2% in SITA, 3.2% in BITA (p = 0.27); (3) sternal dehiscence, 1.2% in SITA, 3.2% in BITA (p = 0.27).

CONCLUSIONS: Our data do not support the perception that BITA grafting increases the risk of sternal complications in insulin-dependent diabetic patients.

	Introduction

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Diabetes mellitus is a major independent risk factor for the development of coronary artery disease [1]. The prevalence of type 2 diabetes is set to reach epidemic proportions in the Western world in the next 20 years. The severity and diffuse nature of diabetic coronary atherosclerosis make this an increasingly significant health problem in the long term. Outcomes of the Bypass Angioplasty Revascularisation Investigation (BARI) trial and others support the notion that diabetics stand to gain the most benefit from coronary artery bypass grafting not just in terms of survival, but also in relief of symptoms and freedom from repeat revascularization [2, 3]. Arterial revascularization is believed to be the key to this benefit and the improved survival of diabetics is thought to be related to the use of at least one internal thoracic artery. There is evidence in the literature [4, 5] demonstrating the excellent short and long term benefits of single internal thoracic artery (SITA) grafting in terms of survival, patency of graft, and recurrence of symptoms. The left internal thoracic artery grafted to the left anterior descending artery is the "gold standard" for coronary artery revascularization with patency rates of 90% to 95% at ten years compared with up to 70% saphenous vein graft failure at ten years [5].

It has been reported that bilateral internal thoracic artery (BITA) grafts result in better event free survival [4, 6–8] than a SITA in the long term (10 years). This appears to be particularly important in the diabetic population [6]. An elegant study by Lev-Ran and colleagues [9] has demonstrated that left-sided BITA grafting confers improved long-term survival and event free survival in oral-treated diabetics. However, it has been suggested that the use of BITA grafts in type 2 diabetic patients requiring insulin (insulin-dependent diabetes mellitus [IDDM]) results in greater sternal wound complications. This has contributed to the widespread practice among surgeons of avoiding the routine use of BITA grafts, especially in diabetics, due to the fear of deep sternal wound infections, sternal dehiscence, and the associated risk of mediastinitis [10–13]. The adoption of this strategy may deny survival benefit to diabetic patients who may stand to gain the most long-term benefits from BITA grafts.

The aim of this study was to evaluate the rates of sternal wound complications in diabetic patients who received single and bilateral ITAs. Our study is the largest reported for diabetic patients and type 2 diabetics requiring insulin undergoing pedicled SITA or BITA grafts in relation to sternal wound complications. A retrospective analysis was performed of prospectively collected data from a single institution over a 10-year period in patients undergoing coronary artery bypass grafting (CABG).

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
We analyzed prospectively collected data on consecutive patients who underwent first-time CABG from April 1, 1992 to March 31, 2002. The data were collected and entered into the Patient Analysis and Tracking System database at our unit. The study was approved by the Institutional Review Board and patient consent was waived.

Patient Characteristics
A total of 7,581 first-time CABGs were performed in this period, of which 922 were diabetic patients. Among these 922 diabetics, 261 were insulin dependent, 473 were treated with oral hypoglycemic agents, and 188 were diet-controlled.

The diabetic population of patients was subdivided into those that underwent either single ITA grafting (n = 524; 56.8%) [group A] and those that had BITA grafting (n = 396; 43%) [group B]. Only 2 diabetic patients did not receive an ITA graft during the 10-year period.

Propensity scoring was used to match the two groups in this retrospective analysis. Univariate and multivariate logistic regression were applied to identify risk factors for the outcome deep sternal wound infection and sternal dehiscence among diabetics. Although the patients were matched using propensity scores, the two diabetic groups, A and B, prior to propensity matching were similar with respect to gender, emergent nature of surgery, preoperative angina status, preoperative myocardial infarction (MI), dyspnea class, left ventricular (LV) function, peripheral vascular disease, and smoking status (Table 1). Group B patients were younger, had more men, and less hypertension, renal impairment, chronic obstructive pulmonary disease (COPD), and preoperative MI prior to matching. Body mass index (BMI) and Parsonnet score were also significantly less in group B (Table 1).

Both ITAs were immersed in a solution of blood and sodium nitroprusside. Operations were performed with and without the use of cardiopulmonary bypass. Prior to closure of the sternum, hemostasis was secured with minimal use of low setting electrocautery on presternal tissues and the chest wall. The sternum was reapproximated using a minimum of 6 stainless steel wires. Absorbable suture was used to close the presternal space in two layers. The skin was closed using an absorbable subcuticular suture.

Sternal Wound Classification
The classification used for sternal wound infection was as follows.

1 Superficial sternal wound infection defined as wound erythema and purulent discharge without evidence of sternal or mediastinal involvement [15].

2 Deep sternal wound infection was defined according to the guidelines of the Centers for Disease Control and Prevention, with patients meeting at least one of the following criteria [16]:

(a) isolation of an organism from culture of mediastinal tissue or fluid;

(b) evidence of mediastinitis during sternal reexploration; or

(c) chest pain, sternal instability, or fever present in combination with purulent discharge from the mediastinum or an isolated organism from blood or tissue cultures.

Statistical Analysis
Univariate and multivariate logistic regression were used to identify risk factors for deep sternal infection and sternal dehiscence among diabetics. The risk factors examined were type of operation (SITA vs BITA grafting), diabetes status, gender, age, dyspnea grading, pulmonary disease, smoking, hypertension, vascular disease, LV function, severity of coronary artery disease (CAD), distal anastomoses, and bypass time.

To ascertain whether types of patients were more or less likely to receive the BITA based on their symptoms, propensity scores were calculated and these were used in the multivariate model to control for symptom selection. The risk factors used in generating the propensity score were type of operation (SITA vs BITA grafting), diabetes status, gender, age, pulmonary disease, smoking, hypertension, vascular disease, and LV function.

The same techniques were used to examine the different rates of infection for the different diabetic groups and also the rate of mortality at 30 days. The statistical software, Stata version 7.0 (SAS, Cary, NC), was used to analyze the data.

	Results

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Sternal Complications in Diabetics (n = 920) Who Underwent Pedicled Single or Bilateral ITA Grafting
Intraoperative and postoperative outcome in all diabetic patients (n = 920) receiving either the SITA or BITA are summarized in Tables 3 and 4. The direct comparisons of the incidence of sternal wound complications in all diabetic patients who underwent ITA grafting are shown in Table 4. The incidence of superficial sternal wound infection was 3.4% in the SITA group compared with 2.0% in the BITA group (p = 0.2, confidence interval [CI] –1 to 3.5). The incidence of deep sternal infection was 1.3% in the SITA group compared with 2% in the BITA group (p = 0.42, CI –2.4 to 1.0). The rate of sternal dehiscence was no different in the two groups at 1.5% (p = 0.98, CI –1.6 to 1.6). This is prior to the implementation of the propensity score models that take into account preoperative patient characteristics.

Sternal Complications in Nondiabetics (n = 6,659) Who Underwent Pedicled Single or Bilateral ITAs
There were only 15 cases of deep sternal wound infection in 3,676 nondiabetics receiving the SITA over 10 years, in comparison with the BITA incidence of 21 cases of deep sternal wound infection from a population of 2,983 nondiabetics. This translated to low rates of deep sternal wound infection in nondiabetics of 0.41% receiving the SITA compared with 0.7% with BITA usage. The dehiscence rates were similar in both groups of nondiabetics undergoing SITA or BITA grafting (0.7% vs 0.9%) (Table 7).

Using Propensity Scores
Univariate and multivariate logistic regression were used to identify risk factors for deep sternal infection and sternal dehiscence among all diabetics (n = 920). The risk factors examined were type of operation (SITA vs BITA), diabetes status, gender, age, dyspnea grading, pulmonary disease, smoking, hypertension, vascular disease, LV function, severity of CAD, distal anastomoses, and bypass time.

The only statistically significant univariate risk factor for deep wound infection was chronic obstructive airway disease (COAD) (odds ratio [OR] 6.05, 95% CI 1.84 to 19.98, p = 0.003). The COAD was still a risk factor when controlling for all other recorded confounders as listed above (OR 6.04, 95% CI 1.44 to 25.28, p = 0.01). The COAD was also a univariate risk factor for sternal dehiscence (OR 4.45, 95% CI 1.19 to 16.68) but was not significant when adjusting for other confounders (OR 4.30, 95% CI 0.87 to 21.34). Diabetes status was not a significant risk factor for deep wound infection or sternal dehiscence.

To ascertain whether types of patients were more or less likely to receive the BITA based on their symptoms, propensity scores were calculated and these were used in the multivariate model to control for symptom selection. Table 8 shows the results of the multivariate analysis of the predictors of choosing BITA over SITA revascularization. The chance of BITA grafting being performed instead of SITA increased when the patient was younger, male, had no dyspnea, and was type II diabetic-controlled on tablet or insulin compared with diet-controlled. The factors that decreased the chances of BITA were older age, female, dyspnea, and hypertension. Interestingly, pulmonary vascular disease, emphysema, and smoking did not influence the chance of having BITA harvest.

	Comment

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
The predicted explosion in the prevalence of diabetes in the Western world over the next 20 years is likely to increase the proportion of these patients requiring revascularization. There will therefore be an increasing cohort of patients requiring coronary revascularization at an earlier age with diabetic coronary atherosclerosis, which will be difficult to revascularize by percutaneous interventions. The current evidence suggests [2, 17, 18] that diabetics have better outcomes with CABG than percutaneous intervention and this benefit is due to the use of ITA grafts. The use of multiple arterial grafts appears to be advantageous in diabetics [19]. There is also recent evidence from two meta-analyses that BITA grafting has long-term survival benefits over SITA grafting, although no randomized trials have been published to confirm these findings [20]. The Arterial Revascularization Trial (ART) study, a randomized trial, will answer this question in the long term. The benefit of ITA grafts in diabetics may lie in the diffuse nature of diabetic coronary lesions and a small caliber of their coronary arteries. One of the additional advantages in this latter group is the avoidance or reduction in the length of the long saphenous vein harvest wound with its potential for infection.

Based on early reports, it has been commonly perceived that BITA grafts should not be performed in diabetics (particularly insulin-dependent diabetes mellitus [IDDM]) [11]. The reasons for avoidance of BITA include a belief that BITA grafting is accompanied by increasing rates of deep sternal wound infection and sternal dehiscence leading to mediastinitis, septicemia, and death [21]. Diabetics are more prone to infection and poorer healing, thus most surgeons believe it is an unnecessary risk to harvest BITAS in this group. Insulin-dependent diabetes makes most surgeons even more reluctant to harvest BITAs, despite the evidence that it is this group who will benefit most from BITA grafting in the long term.

It has been recently suggested [15, 22] that harvesting skeletonized ITA reduces the risk of sternal wound complications. As described, a pedicled technique was used in our study and we believe that with this technique the risk of devascularization of the sternum is small. This is accomplished by the utilization of low electrocautery (20–30W) settings and the ligation of arterial branches rather than their cauterization. This, we believe, preserves sternal vascularity in diabetics compared with higher electrocautery settings used to rapidly harvest ITAs without any hemostatic clips to arterial branches. The benefits of this technique are seen mostly in the higher risk patients of sternal complications (eg, diabetics and IDDM) who are prone due to their poor tissue healing powers. We recommend that the more limited use of electrocautery is important in this diabetic population for sternal complications. It is still uncommon practice to offer patients with IDDM, BITA, and revascularization procedures. The mortality rate and complication rates for BITA harvest, while appearing high compared with current standards of practice, were related to the early stage of the review (pre-1995) when our institution adopted widespread complete arterial revascularization. The complication rates post-1995 are comparable with currently acceptable standards of practice. This study demonstrates that the BITA does not lead to an increase in deep sternal wound infection or dehiscence after BITA grafting both in diabetics in general, and moreover, in the high-risk group of IDDM, compared with the use of the SITA. Although the numerical incidence of deep sternal wound infection is higher with the BITA than the SITA in all diabetics, but not reaching statistical significance, the complication rates of sternal dehiscence are identical in both groups. The failure to demonstrate statistical significance in the large numbers examined over 10 years suggests that any such difference is minimal. However, it is noted that the SITA group and the BITA were not "identical" and there is a tendency in the bilateral group for a lower incidence in other factors that may predispose to sternal dehiscence prior to propensity matching. This may represent a certain degree of surgeon selection and means that the results from our study may be indicative rather than definitive. Using propensity matching to remove selection bias and confounding, we found that none of the risk factors were statistically significant with regard to 30-day mortality, deep sternal wound infection, and sternal dehiscence. Avoidance of the use of the BITA in diabetics may deny these patients the potential long-term benefits of BITA revascularization. Thus, the results of our study suggest that with appropriate patient selection and surgical technique, the use of the BITA in diabetics is safe and does not lead to an increase of sternal complications.

This was a retrospective study on prospectively collected data and was not a designed randomized study, but until the ART trial results are published, we have found no studies to date in this field to answer these important questions. The data were checked for accuracy and validated. We have presented the data in two forms, with and without propensity matching. It should be noted that the number of infections and dehiscences were very small.

	Discussion

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DR A. NORMAN LEWIN (Buffalo, NY): I enjoyed your presentation very much and you are to be commended on some excellent results. Others have reported excellent results also; Dr. Calafiore and the group from Israel, and in Buffalo, New York we have done this for many years, but with one caveat, we skeletonize the IMAs (internal mammary arteries), and that seems to have reduced the incidence of infection to that of nondiabetic patients.

My question to you is this. What is your technique of harvesting the IMAs? Do you skeletonize the vessels, or how thick is your pedicle, how wide is your pedicle?

DR MOMIN: Thank you very much for your kind comments. First of all, during the 10 years between 1992 and 2002, we used the pedicled technique. This technique comprised of using low setting electrocautery and very thin pedicles. Using this method we avoided removing excessive tissue away from the sternum and thus devascularization of the sternum. Recently we have started using the skeletonization method, and we will present those results at a later date.

DR J. FEHRENBACHER (Indianapolis, IN): Were these subgroups matched for age? More specifically was the bilateral mammary group younger? Did you look at obesity or BMI (body mass index) scores?

DR MOMIN: Those are very good questions. Yes, the bilateral group was younger. It was a retrospective analysis. In analysis of the five patients whom had sternal dehiscence in the insulin-dependent group, whether it is single or bilateral ITAs, all five patients were age 74 and older, two of the patients had vascular disease, and two of the patients had renal disease. In reviewing obesity, the BMIs were 22.11, 26.12, 28.36, 29.93, and 42.93. This shows a trend that BMI scores close to 30 and above in three out of the five patients. But due to the small numbers these factors did not reach statistical significance.

DR WILLIAM COLTHARP (Nashville, TN): By my calculations, you had an overall incidence of 11% of diabetic patients in your population and the incidence of insulin-dependent diabetics was 3%. In Nashville, the incidence of diabetics in coronary artery patients is 28%. I am not sure I can draw the same conclusions from your data and apply it to my patients as you do.

The second point is, in our patients, we have found an extraordinarily high incidence of previously undiagnosed diabetes based on the American Diabetic Association definition of greater than 6.2% hemoglobin A1c as a diagnosis of diabetes. And interestingly, we found 20 to 24% of our patients, previously undiagnosed diabetics, fall into that range, which gives us almost 50% of patients with either previously diagnosed diabetes or no previously diagnosed diabetes. So it is hard for me to correlate your data with an 11% incidence of diabetics and only a 3% incidence of insulin-dependent diabetics with our population in Nashville, and I would just like to hear your comments on that.

DR MOMIN: Thank you for your comments. During the 10 years our incidence of diabetes in coronary artery patients has increased from 11% in 1992 to 25% in 2002. We do not measure, routinely, hemoglobin A1c and thus we believe if we employed the strict criteria like you we also would have an even higher incidence of diabetes.

Also, we are much stricter with our control of diabetes postoperative, with strict 48-hour glycemic control by insulin infusions in all types of diabetes.

DR ROBERT ROBBINS (Stanford, CA): That was one thing I was going to ask. Was the use of bilateral mammaries versus single mammaries equally distributed over your time of study? And were you more aggressive? For instance, did you use more bilateral mammaries recently and more aggressive with glucose control recently?

DR MOMIN: The data I present is up to 2002. In the last few years we have been much more aggressive with bilateral ITA usage in all, but this is still also surgeon-dependent. This data is for five surgeons, and some were more aggressive than others in the sense they would give bilateral ITA usage to all patients and all-comers.

DR OSMAN AL-RADI (Toronto, Ontario): I suspect that your analysis is significantly under-powered (all diabetic patients: power = 14%, IDDM [insulin-dependent diabetes mellitus] patients: power = 23%). Your conclusions state the two groups have no significant difference in the incidence of wound infection. To prove equivalence between two groups the power of the analysis has to be even higher than the classical point of 80%, somewhere close to 95%.

DR MOMIN: That is why we actually did a Fisher's exact test to validate the data.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
The authors thank Andrew Forsyth and Lindsay John.

	References

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Aziz U. Momin Ranjit Deshpande Ahmed El-Gamel Michael T. Marrinan Jatin B. Desai Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Momin, A. U. Articles by Desai, J. B. Search for Related Content PubMed PubMed Citation Articles by Momin, A. U. Articles by Desai, J. B. Related Collections Coronary disease