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Department of Biosurgery and Surgical Technology, and Surgical, Epidemiology Unit, Imperial College London, St. Mary's Hospital, London, United Kingdom
* Address correspondence to Mr Athanasiou, Department of Biosurgery and Surgical Technology, 10th Floor, QEQM Wing, St. Mary's Campus, London, W21 NY, United Kingdom (Email: t.athanasiou{at}imperial.ac.uk).
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Abstract |
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 Top Abstract IntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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Introduction |
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TopAbstractIntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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Sternal wound infection (SWI) is a recognized and important complication of coronary revascularization. A consensus definition of SWI does not exist in the literature, although it is evident that most definitions recognize a superficial and deep type of SWI based on anatomical aspects [2–5]. The most serious manifestation of an SWI is mediastinitis, which extends the previous anatomical classification to the risk of systemic sepsis. It is well known that an infection of the mediastinum can be severe and potentially debilitating. Our interest in this study was to investigate the complication of SWI involving the three previously described entities in the context of left internal thoracic artery use. It is also obvious that the selection to focus on these three entities has a practical role in terms of therapeutic management.
It is proposed that the method of conduit harvesting influences the incidence of postoperative SWI. There are two established "polarized" harvesting techniques that generate pedicled and skeletonized ITAs, and others "in the middle," such as semi-skeletonized ITA grafts. Whereas the pedicled technique dissects the artery away from the sternum with its accompanying veins, fascia, adipose tissue, and lymphatics generating a pedicled graft, skeletonization requires the ITA to be dissected free of all surrounding tissue, solely yielding the artery; this is partially achieved with semi-skeletonization.
Each technique is associated with its own respective advantages and disadvantages. Previous studies have compared skeletonization and pedicled techniques [6–9]. In a previous review we discussed the advantages and disadvantages of ITA skeletonization [6]. Behranwala and colleagues [7], Raja and Dreyfus [8] and Toumpoulis and colleagues [9] have subsequently reviewed the best evidence in the literature, attempting to elucidate this further. Even though it was concluded that skeletonized ITA grafts are preferable to pedicled grafts, the studies were qualitative, rather than quantitative, did not use statistical methodology, and did not focus specifically on SWI.
Another aspect is whether unilateral or bilateral ITAs should be used, which introduces further consequent advantages and disadvantages. Bilateral internal thoracic artery (BITA) use has been demonstrated to improve prognosis and reduce reinterventions in comparison with the use of single internal thoracic arteries [10]. However, the use of BITA grafts has been shown to have the potential for increased SWI, and this effect is believe to be amplified in diabetic patients [11, 12].
In planning surgical revascularization, the surgeon is presented with extensive choices. Successful outcome is dependent on achieving the best risk-to-benefit ratio. Every effort should be focused to decrease the SWI rate. Means for doing this include intraoperative avoidance tactics, which limit sternal devascularization. Beyond differing harvesting techniques, use of different equipment and specialized sternal closure devices may benefit. In addition, an aggressive prophylactic antibiotic protocol and optimized glycemic control are important. Halkos and colleagues [13] demonstrated that an elevated hemoglobin A1c level was strongly associated with the risk of developing a deep SWI after coronary artery bypass grafting in both diabetic and nondiabetic patients. Many of the influencing factors are surgeon and patient specific. Surgeon-specific aspects include the familiarity and expertise, with a particular harvesting technique or the personal preference on the use of one or two ITA conduits [14]. Patient-related factors include coronary and conduit anatomy, pre-existing comorbidities (such as diabetes, obesity, increased New York Heart Association score, and immunosuppression) or iatrogenic reasons, such as long-term corticosteroid use [14]. Other risk factors associated with the development of SWI, which must be considered may be classified into preoperative, intraoperative, and postoperative factors (presented in Table 1).
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Material and Methods |
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TopAbstractIntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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Data Extraction
Two reviewers (Srdjan Saso and David James) independently extracted the data from each study. Quantitative data was extracted as follows: logistics (first author, year of publication, study design); conduit factors (number of skeletonized versus pedicled, single ITAs vs BITA); and incidences of SWI (superficial SWI, deep SWI, mediastinitis, all SWI, SWI in diabetic patients only).
We also extracted qualitative data regarding previously recognized SWI risk factors; these factors are shown in Table 1. The factors are classified according to time onset: preoperative, intraoperative, and postoperative. We recorded the presence or absence of these risk factors in the studies analyzed. Additional factors recorded were: (1) preoperative factors (chronic renal failure, chronic obstructive pulmonary disease [COPD], corticosteroid use [long-term], obesity, previous radiation, macromastia [females] and previous smoking history); (2) intraoperative factors (excessive use of bone wax or diathermy, low cardiac output, prolonged cardiopulmonary bypass time, surgical experience, technique used to open and close sternum, and use of operative anti-sepsis prophylaxis); (3) postoperative factors (ventilation required > 24 hours postoperative multiple transfusions, need for cardiopulmonary resuscitation, prolonged stay in the intensive care unit, reopening of thorax due to hemorrhage, and unstable sternum).
Inclusion and Exclusion Criteria
All comparative studies of skeletonized versus pedicled ITAs in patient groups undergoing coronary artery bypass grafting reporting the incidence of SWI outcome were included. Those studies not reporting SWI outcome or reporting zero incidence in both the skeletonized and pedicled group were excluded. Other ITA harvesting techniques were excluded from our analysis.
Outcomes of Interest
The primary outcome of interest was the postoperative SWI incidence in all skeletonized versus pedicled ITAs. Secondary outcomes of interest were to identify subclassifications of SWI for specific patient populations (eg, BITA harvesting or diabetic patients).
Statistical Analysis
Meta-analysis was performed in line with recommendations from the Cochrane Collaboration and the Quality of Reporting of Meta-Analyses guidelines for reporting of meta-analyses [15]. For categorical variables, we used odds ratio (OR) as the summary statistic. This ratio represents the odds of an adverse event occurring in a skeletonized group compared with the pedicled group. An OR of less than 1 favors the skeletonized group, and the point estimate of the OR is considered statistically significant at the level of p < 0.05 if the 95% confidence interval (CI) does not include the value 1.
Aggregation of the overall rates of the outcomes of interest was performed with the Mantel-Haenszel method [16]. Yate's correction was used for those studies that contained a zero in one cell for the number of events of interest in one of the two groups. These "zero cells" create problems with the computation of ratio measure and its standard error of the treatment effect. This can be resolved by adding the value 0.5 in each cell of the 2 x 2 table for the study in question, and if there are no events for both skeletonized and pedicled groups, the study should be discarded from the meta-analysis [17].
In this study, we used both fixed-effect and random-effect models. In a fixed-effect model, it is assumed that the treatment effect in each study is the same. In a random-effect model, it is assumed that there is variation between studies and the calculated OR thus has a more conservative value [18, 19]. For surgical research, meta-analysis using the random-effect model is preferable particularly because patients that undergo operations in different centers have varying risk profiles and selection criteria for each surgical technique.
In the analysis of our results (Figs 1A–1D), squares indicate point estimates of treatment effect (OR), with the size of the square representing the weight attributed to each study and 95% CI indicated by horizontal bars. The diamond represents the summary OR from the pooled studies with 95% CI.
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To enable this, we devised a scoring system to quantify the study quality. We attributed a point to each study when compliant with 23 specified factors (see Appendix 2). This generated a median of 6.5. The range was then divided into quartiles, which were scored from 1 to 4. 3 studies qualified for the fourth quartile (9.75 to 12 matched factors) and these studies were separately analyzed.
Analysis was conducted by using Review Manager Version 4.2 (The Cochrane Collaboration, Software Update, Oxford) and the Sample Power 2.0 (SPSS Inc, Chicago, IL) for power analysis calculations. Results of the studies and overall analyses are demonstrated in Figures 1A to 1D and 2.
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Results |
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Sensitivity Analysis on Specific Subgroups (Random-Effect Model)
Sternal wound infection incidence in diabetic patients
On analysis of six studies that reported the SWI incidence separately for diabetic patients [24, 26–30], calculated OR for incidence of SWI was 0.20 (95% CI 0.12 to 0.34), with a nonsignificant chi-square heterogeneity of 2.16 (p = 0.83) (Fig 1B).
Use of bilateral internal thoracic artery conduits
In the 6 studies where only BITA grafts were used [24, 26–30], calculated OR was 0.31 (95% CI 0.17 to 0.56), with a nonsignificant chi-square of heterogeneity of 8.81 (p = 0.12) (Fig 1C). With the exception of one study [26] all of these studies compared BITA use in diabetic patients. Excluding this study demonstrated an OR of 0.19 (95% CI 0.10 to 0.36), with a nonsignificant chi-square of heterogeneity of 2.05 (p = 0.73) (Fig 1D).
Sternal wound infection subgroups
Superficial Sternal Wound Infection
In the four studies that reported the postoperative incidence of superficial SWI [25–27, 31], calculated OR was 0.51 (95% CI 0.29 to 0.87), with a nonsignificant chi-square of heterogeneity of 1.93 (p = 0.59).
Deep Sternal Wound Infection
In the seven studies that reported the postoperative incidence of deep SWI [14, 23, 26, 28, 30, 31], calculated OR was 0.42 (95% CI 0.18 to 0.97), with a nonsignificant chi-square of heterogeneity of 8.74 (p = 0.19).
Mediastinitis
In the three studies that reported the postoperative incidence of mediastinitis [27, 29, 32], calculated OR was 0.19 (95% CI 0.04 to 0.94), with a nonsignificant chi-square heterogeneity of 0.20 (p = 0.90).
Study quality score—4 (assessment of study quality)
The distribution of the risk factors for SWI between skeletonized and pedicled groups is shown in Appendix 2, which also demonstrates the matching of factors between studies and their "quality score." Three studies matched > 9.75 factors scoring 4 points for quality [23, 27, 30]. Calculated OR for incidence of wound infection was 0.26 (95% 0.13 to 0.52) with a nonsignificant heterogeneity of 0.69 (p = 0.88).
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Comment |
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We recognize that the definition of SWI differs between studies and this nonuniformity has the potential to introduce computational error. The model classification of SWIs was first published by El Oakley and Wright [2] in 1996. Subsequent infection definitions have been used to audit SWI rates, such as those by Garner and colleagues [3] and Mangram and colleagues [4]. Different studies use different criteria, which may be anatomical or microbiologic criteria, such as positive blood and swab cultures or are related to operative time or onset time [35]. It was not the aim of this study to validate SWI definitions, and we recognize variations exist between established and classification systems that are used. From a practical point of view, the SWI definitions have been used to clearly reflect the variation in therapeutic management.
We conclude from this study that the method of ITA harvesting enables significant advantages in reducing postoperative SWI rates. The results demonstrate that skeletonized conduits are superior to pedicled conduits when considering the SWI outcome in the populations studied.
We present the following four conclusions: (1) our first finding is that the risk of all SWI decreases by 60% when skeletonizing the ITA; (2) this advantage is amplified in diabetic patients in which an even greater benefit was demonstrated (eg, in diabetics, when skeletonizing the ITA, the incidence of SWI was reduced from 21.3% to 3.57%); (3) when harvesting BITA, the advantage of skeletonization is maintained with a reduction of postoperative SWI rates from 11.7% to 2.96% for all studies and from 14.2% to 2.4% in diabetic patients; and (4) the subgroup analyses demonstrate that the reduction in SWI rates is maintained for the whole spectrum of postoperative SWI including mediastinitis. These findings are extremely important because they scientifically strengthen the justification for using this excellent conduit.
In considering harvesting methods, pedicled grafts are less technically demanding and time consuming and pose a smaller risk of damage to the vessel [24, 25]. Skeletonization may protect collateral vessels supplying the sternum and experimental evidence demonstrates increased sternal vascularity with SKT and ITA compared pedicled grafts and ITA [25]. This difference in the degree of sternal devascularization between methods may account for the difference in SWI rates. In addition, skeletonized grafts confer further benefit in terms of increased conduit internal diameter and longer than pedicled grafts [24, 32]. Furthermore, BITA recruitment enables total arterial revascularization, which may improve survival and reduce the incidence of stroke, possibly as a result of limited ascending aorta manipulation [36].
It is the associated risks of ITA harvest that counter-balance the prognostic excellence. This is especially apparent in those considered "at high risk" of developing sternal infections and when harvesting both ITAs. It has been suggested that when skeletonizing, the vessel loses its "milieu," which may be a negative influence on conduit longevity, and this remains an area of debate [37].
However, the findings of this meta-analysis are reassuring because they indicate that the ITA can be safely harvested (by skeletonization), even in high-risk infection susceptible groups, and bilaterally without worsening the sternal infection rate. This means that the prognostic benefit of this conduit can be offered to these patient groups in some cases without compromising the risk-to-benefit balance. This must be interpreted with caution because the high-risk groups are not necessarily homogenous. For example, a diabetic patient may have super-added risk factors such as obesity and chronic obstructive pulmonary disease. Therefore, not all diabetic patients will be suitable for ITA harvesting. This data may be extrapolated to other groups at high risk of infection (eg, immunocompromised patients on corticosteroids or obese patients). However, as explained by De Paulis and colleagues [26], a more conservative approach (ie, use of a single ITA) can still be justified, because the chance of a sternal infection increases exponentially in the presence of two or more risk factors (eg, diabetic patients with chronic obstructive pulmonary disease, peripheral arteriopathy, or obesity).
In considering BITA alone, we identified 6 studies analyzing the use of these skeletonized conduits. The prognostic benefit of BITA usage is established [10]. The counter argument is supported by concern of inappropriate patient anatomy, increased technical difficulty and risk of SWI. Skeletonization may facilitate overcoming these technical difficulties in that the technique provides longer, wider conduits [24]. This study weakens the concerns of ITA harvest because we demonstrate that this is not the case.
The reason for this overall reduction in infection rates is likely because of the fact that the collateral blood supply to the sternum is better preserved after skeletonization of the ITA [38]. By having a better blood supply, sternal skin tissue is less likely to become ischemic and would therefore be better equipped to combat infection. This is of particular benefit in diabetic patients who may have a micro-angiopathy devascularizing their sternum.
Study Strengths and Limitations
We performed this meta-analysis to further investigate the effect of skeletonization on SWI rates. We recognize there are previous reviews partially investigating this effect, but these studies were nonquantitative and did not focus on the diabetic subgroup or those who had BITA conduits. We have performed a quantitative meta-analysis addressing these points, thus justifying the relevance of this study.
One of the aims of a meta-analysis is to identify and explain causes of heterogeneity. Overall, our study does not demonstrate statistically significant heterogeneity. This is the case despite the potential source of heterogeneity due to study design mixture introduced by the merging of retrospective and prospective data.
The fact that only 4 of 13 studies demonstrated a significant result [24, 26, 27, 29] is not surprising. This maybe explained by the "power" of the individual studies to identify a statistically significant result. The benefit of performing a meta-analysis in this scenario is that it allows one to combine the results from all 13 relevant studies, and therefore increase the overall sample size of the analysis.
Although no statistical heterogeneity was identified, it is possible that clinical heterogeneity can be present. Heterogeneity can be introduced by the variability of surgical ability by different surgeons, use of varied equipment, conduits, anesthetic protocols, monitoring techniques influenced by the expertise and designation of whoever assesses the wound-related outcome, and the range of prophylactic antibiotic protocols.
It is important to note that the incidence of deep SWI in The Society of Thoracic Surgeons' database can be different compared with that reported in our meta-analysis; this can be due to the fact that quality of data entry compliance may vary as there are no standardized reporting criteria in terms of the diagnosis and severity of the SWI. In addition we need to keep in mind that some of these infections can present after the patient's discharge, which can underestimate the true figures.
Postoperative variables predisposing susceptibility to SWI were not directly assessed for in this study. These would include sepsis secondary to a urinary tract, pulmonary or gastrointestinal infection, and alternative states of immunosuppression (other than diabetes). These combined factors potentially add a degree of subjectivity to the final results. To overcome this possibility of subjectivity, it would be necessary to devise a blocked, randomized, controlled trial design that would be incredibly expensive and time-consuming, and therefore would be impractical.
It would have been of interest to specifically analyze the impact of glycemic control in diabetics relative to SWI rates. We have not been able to do this because the data was not available. We also acknowledge that the diabetic group itself can be extremely heterogeneous, including a wide spectrum of diabetic severity and multiple comorbidities. These factors may influence the accuracy of data in such a study.
We also acknowledge that this meta-analysis did not include any randomized controlled trials from which further conclusions could be drawn.
Finally, in the study by Bonacchi and colleagues [23], two different skeletonized groups were compared with a single pedicled group that may have affected the statistical analysis in terms of accuracy because of duplication of the control group.
Implications of Our Study and Conclusions
This study has implications for both the patient and the healthcare provider. As far as the patient is concerned, the study demonstrates that skeletonized grafts, with BITA grafts already shown to improve survival, can be used without necessarily increasing the risk of postoperative SWIs. This effect also applies to the high-risk subgroup of diabetic patients, implying that this procedure is not always contraindicated in those at increased risk of infection. The implications for the healthcare provider are smaller costs for the surgical procedure because of the decreased risk of sternal infection and the fact that the patient has undergone a procedure associated with reduced mortality, reoperation, and angioplasty rates [33]. This would reduce the cost of treating the patient in the future.
We propose that it is essential to accurately define and classify SWIs within the field of cardiothoracic surgery to enable future comparisons and communication between clinicians. A standard definition should be applied uniformly across all future studies for each of the following: SWI, superficial SWI, deep SWI, and mediastinitis. In addition, because the findings support this harvesting method, we recommend that skeletonization should qualify as a "required skill" and feature within the cardiovascular surgical curriculum.
We also acknowledge that these findings are redundant if the primary goal of revascularization, that is, conduit longevity, is compromised by skeletonization. Del Campo [37] highlights this concern and describes that ITA skeletonization might have a deleterious effect on the long-term resistance of the artery to atherosclerosis. Long-term patency data are not available, and for this reason, we would encourage authors of previously published reports to collect and publish such data. Before this technique can be universally recommended, it is important to establish these facts.
The results of this study ideally suggest the need for a large-scale, multi-center, prospective, randomized trial of skeletonized versus pedicled grafts in high-risk patients for postoperative SWI (as a primary end-point). We recognize that although indicated in terms of pure science, such a trial would be logistically and economically unfeasible.
An alternative would be to ensure that existing or planned trials should include factors in their demographic data enabling future extrication of relevant data to test this hypothesis further (ie, by performing individual patient data meta-analyses). We believe this would be necessary before drawing definitive conclusions on exactly what type of graft should be used in a specific population to reduce the incidence of postoperative SWI in patients undergoing surgical revascularization, and prior to implementing a change in the surgical practice.
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Appendix 1 |
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TopAbstractIntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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Appendix 2 |
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TopAbstractIntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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NB = A star in the appendix designates that a particular factor has been reported in both the skeletonized and pedicle groups of the study.
Matched factors: A = age; B = chronic renal failure; C = chronic obstructive pulmonary disease; D = corticosteroid use (long-term); E = diabetes mellitus; F = obesity; G = previous radiation; H = macromastia (females); I = smoker/ex-smoker; J = decision to use single internal thoracic artery or bilateral internal thoracic artery grafts; K = excessive use of bone wax; L = excessive use of diathermy; M = low cardiac output; N = prolonged extracorporeal circulation time; O = surgical experience; P = surgical technique used to open and close sternum; Q = use of operative anti-sepsis prophylaxis; R = ventilation required > 24 hours postoperatively; S = multiple transfusions; T = need for cardiopulmonary resuscitation; U = prolonged stay in intensive care unit; V = re-opening of thorax due to hemorrhage; W = unstable sternum.
Study Score: 1 = matched for 0 to 3.25 factors; 2 = matched for 3.25 to 6.5 factors; 3 = matched for 6.5 to 9.75 factors; and 4 = matched for 9.75 to 12 factors.
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TopAbstractIntroductionMaterial and MethodsResultsCommentAppendix 1Appendix 2References |
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