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Ann Thorac Surg 2009;87:742-747. doi:10.1016/j.athoracsur.2008.12.050
© 2009 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Do You Need to Clamp a Patent Left Internal Thoracic Artery–Left Anterior Descending Graft in Reoperative Cardiac Surgery?

Robert L. Smith, MD*, Peter I. Ellman, MD, Peter W. Thompson, MD, Micah E. Girotti, MD, Bret A. Mettler, MD, Gorav Ailawadi, MD, Benjamin B. Peeler, MD, John A. Kern, MD, Irving L. Kron, MD

Department of Surgery, Division of Thoracic Cardiovascular Surgery, University of Virginia, Charlottesville, Virginia

Accepted for publication December 16, 2008.

* Address correspondence to Dr Smith, University of Virginia Health System, Box 800709, Charlottesville, VA 22908-0709 (Email: rls9t{at}virginia.edu).

Presented at the Poster Session of the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Comment
 References
 
Background: Dogma suggests optimal myocardial protection in cardiac surgery after prior coronary artery bypass graft surgery (CABG) with patent left internal thoracic artery (LITA) pedicle graft requires clamping the graft. However, we hypothesized that leaving a patent LITA–left anterior descending (LAD) graft unclamped would not affect mortality from reoperative cardiac surgery.

Methods: Data were collected on reoperative cardiac surgery patients with prior LITA-LAD grafts from July 1995 through June 2006 at our institution. With the LITA unclamped, myocardial protection was obtained initially with antegrade cardioplegia followed by regular, retrograde cardioplegia boluses and systemic hypothermia. The Society of Thoracic Surgeons National Database definitions were employed. The primary outcome was perioperative mortality. Variables were evaluated for association with mortality by bivariate and multivariate analyses.

Results: In all, 206 reoperations were identified involving patients with a patent LITA-LAD graft. Of these, 118 (57%) did not have their LITA pedicle clamped compared with 88 (43%) who did. There were 15 nonsurvivors (7%): 8 of 188 (6.8%) in the unclamped group and 7 of 88 (8.0%) in the clamped group (p = 0.750). Nonsurvivors had more renal failure (p = 0.007), congestive heart failure (p = 0.017), and longer perfusion times (p = 0.010). When controlling for independently associated variables for mortality, namely, perfusion time (odds ratio 1.014 per minute; 95% confidence interval: 1.004 to 1.023; p = 0.004) and renal failure (odds ratio 4.146; 95% confidence interval: 1.280 to 13.427; p = 0.018), an unclamped LITA did not result in any increased mortality (odds ratio 1.370; 95% confidence interval: 0.448 to 4.191). Importantly, the process of dissecting out the LITA resulted in 7 graft injuries, 2 of which significantly altered the operation.

Conclusions: In cardiac surgery after CABG, leaving the LITA graft unclamped did not change mortality but may reduce the risk of patent graft injury, which may alter an operation.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Comment
 References
 
Using the left internal mammary artery (LITA) as a pedicle graft to the left anterior descending artery (LAD) is near routine for primary coronary artery revascularization surgery. This grafting strategy is associated with improved surgical outcomes and a decreased need for reoperative cardiac surgery [1, 2]. In the setting of prior coronary artery bypass graft surgery (CABG) with LITA-LAD graft, preventing injury to the LITA is paramount. Injury to this graft is associated with increased morbidity and worsened survival [3, 4]. Injuries to the LITA tend to occur during redo sternotomy or with dissection of the LITA pedicle. The goal of clamping the LITA graft is to reduce cardioplegia washout and maximize myocardial protection while the heart is arrested. Although certain measures have been studied to reduce the risk of injuring the LITA during redo sternotomy, a few groups have looked at the possibility of avoiding dissection of the LITA graft and altering their myocardial protection strategies during mitral [5] and aortic valve surgery [6] after CABG to avoid injury to the LITA graft.

The purpose of this study is to evaluate whether the technique of avoiding a patent LITA to LAD pedicle graft during cardiopulmonary bypass (leaving it unclamped) may be applied to a broader population of redo cardiac surgery patients who had a prior CABG. We hypothesized that an unclamped LITA would not alter mortality outcomes and would potentially reduce injury to the graft.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Comment
 References
 
Patient Population
This study was conducted at the University of Virginia Health System and was approved by the Human Investigation Committee. The need for individual patient consent was waived. From July 1996 through June 2006, data were collected on all adult patients undergoing cardiac surgery and entered into the Society of Thoracic Surgeons National Database. Using our institution's data, those patients having reoperative surgery were selected for chart review to assure as complete capture as possible. By this process, patients who had undergone a prior CABG with a LITA pedicle graft and then had another cardiac operation were subsequently identified. Post-CABG patients undergoing heart transplant and pacemaker lead placements were excluded from the cohort because the influence of a patent LITA to LAD on myocardial preservation was not a factor in these cases.

Operative Technique
At our institution, there is no standardized approach to myocardial protection in the setting of a patent LITA to LAD pedicle graft. Each surgeon operates independently, leaving discretion to clamping the LITA to each surgeon. The result is that there is a good mix of practice for comparison. All the operations reviewed were performed through a redo median sternotomy. The cannulation strategy was selected on a case-by-case basis. In general, aortic cannulation was accomplished in the vast majority of cases as was right atrial cannulation with a dual-stage venous cannula. However, before initiating the redo sternotomy, both femoral arterial and venous lines were placed to hasten access if emergent cardiopulmonary bypass was mandated. Access for both antegrade and retrograde (coronary sinus) cannulas were placed for cardioplegia delivery. If the LITA was to be clamped, it was dissected out and occluded with an atraumatic clamp. For difficult dissections, the entire lateral tissue mass encompassing the LITA graft was sometimes clamped with a large, noncrushing clamp. The patient was next cross-clamped and cooled, and cardioplegia was administered with an initial bolus antegrade followed by a retrograde boluses to achieve an isoelectric electrocardiogram. If the LITA was not going to be clamped, the patient was often cooled to 28° to 32°C, as opposed to our standard practice of 32° to 34°C for other noncirculatory arrest cases. Typical redosing of cardioplegia occurred at 20-minute intervals or at graft completion. Occasionally, if the LITA was unclamped, the redosing interval was shorter. The cases then proceeded as normal.

Statistical Analysis
After data collection, the crude rate of perioperative mortality was determined for the population and was the primary outcome of interest. Patients were divided into survivor and nonsurvivor groups for comparative analysis. All comparisons were unpaired. Bivariate comparative analysis of categorical variables was performed using {chi}2 testing with Yate's continuity correction. If the expected cell count was less than 5 for any cell, Fisher's exact test was used. Interval variables were evaluated for distribution. Normally distributed variables were compared using Student's t test; otherwise, the nonparametric Mann-Whitney U test was employed. All variables and outcomes were defined according to the Society of Thoracic Surgeons National Database [7].

A multivariable analysis, in which perioperative mortality was the dichotomous, dependent outcome variable, was performed by logistic regression employing the Wald statistic, forward stepwise selection method using 0.05 as the limit for acceptance and 0.10 as the limit for removal. Independent variables with a p value of 0.25 or less for an association with perioperative mortality were included in the multivariable analysis as was determined before the analysis. After the initial analysis, the variable "unclamped internal mammary artery" was forced into the model. A correlation matrix for the included variables was performed for each analysis. Testing for interaction between independent variables was included in the final analysis using product-terms. (No interactions were identified.) Model calibration and performance discrimination were assessed by the Hosmer-Lemeshow goodness-of-fit test and area under the receiver operator curve (AUC), respectively.

Values are expressed as means ± SE for interval variables or as a percentage of the group of origin for categorical variables. The results of the logistic regression are reported as odds ratios (OR) with 95% confidence intervals (CI). All p values are two-tailed, and p values of 0.05 or less indicate statistical significance. All statistical analysis in this study was performed using SPSS software, version 15.0 (SPSS, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Comment
 References
 
Over the 11-year period studied, there were 7,872 adult cardiac operations performed at the University of Virginia. Of these, 612 were redo sternotomies excluding those for transplantation, and 206 redo procedures were identified as having had a CABG with a patent LITA graft done earlier. The crude perioperative mortality of the population was 7.3% (15 of 206). The types of operations that were performed are listed in Table 1, with redo CABG being the most common. In this cohort, 43.2% (89 of 206) of patients had their LITA graft clamped during reoperation and 56.8% (117 of 206) did not. There was a significant difference (p = 0.02) in the distribution of cases between the clamped versus unclamped groups.


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  		Table 1 Types of Operations Performed With Existing Patent Left Internal Thoracic Artery (LITA) to Left Anterior Descending Artery (LAD) Graft
 
Patients were separated into survivor and nonsurvivor groups to discern variables with an unadjusted association for perioperative mortality. In Table 2, patient characteristics are evaluated. The results show that preexisting renal failure and congestive heart failure (CHF) were both significantly associated with perioperative mortality, being female and having diabetes mellitus trended toward a significant association. Table 3 summarizes the operative factors that were evaluated. Poorer outcomes were associated with emergent operative status and prolonged perfusion time. In this analysis, leaving the LITA unclamped was not associated with any worse outcome.


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  		Table 2 Patient Characteristics, Comparison of Survivors Versus Nonsurvivors
 

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  		Table 3 Operative Characteristics, Comparison Between Survivors and Nonsurvivors
 
Multivariate Analysis
To assess the patient and operative characteristics independently associated with perioperative mortality, a multivariate analysis was performed using logistic regression employing a forward stepwise selection method. As determined a priori, variables with a p value less than 0.25 for an association with mortality were selected for the analysis. Because there was considerable correlation between operative status (i.e., elective, urgent, or emergent status) and perfusion time, perfusion time was the variable selected for the analysis because, when included, there was a slight improvement in performance discrimination as determined by the AUC. The variable "unclamped LITA" was forced into the model regardless of its association with mortality by bivariate analysis. When adjusting for the presence and renal failure and increased perfusion time, an unclamped LITA was not associated with a worse outcome, nor did it predict any protection from mortality. Table 4 summarizes the findings. The model was analyzed separately to adjust for the case distribution difference between the clamped and unclamped groups noted in Table 1. There was no meaningful change to the analysis, and no significant associations with mortality for the different case types.


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  		Table 4 Multivariate Analysis
 
Injury to the LITA to LAD Graft
There were 9 cases of the 206 (1.5%) that had direct injuries to LITA to LAD graft. One injury occurred on redo sternotomy and was repaired primarily with a 6–0 polypropylene suture. Another injury occurred while dissecting the adhered graft free of the aorta to enable the aortotomy for aortic valve replacement; this injury was also repaired primarily with a 6–0 suture. The remaining 7 injuries came as a direct result of attempting to dissect the vessel for ultimately clamping it. Five of these injuries were repaired primarily. However, 1 injury, where the vessel was tortuous and densely adherent to the chest wall, required ligation and division with a saphenous vein graft to the LAD. The other injury came during a dissection of dense adhesions, and the LITA was transected. The graft was ultimately replaced with a free right IMA graft to the LAD. None of these patients died perioperatively.

Myocardial Protection
There are only limited data to describe the adequacy of myocardial protection in the unclamped LITA group. However, there is no notable difference suggested. There was no difference in perioperative myocardial infarction rates (p = 0.569). There were only 3 perioperative myocardial infarctions captured in the database. Two were from the 89 patients (2.2%) who had a clamped LITA, and 1 was from the 117 patients in the unclamped group (0.9%). Additionally, for the year 2006, among patients who had a cardiology read, intraoperative transesophageal echocardiogram (9 patients of 14 for the year), there were no differences noted in global or segmental wall function at the completion of the case when compared with the preoperative reading. Despite these findings, there was no significant difference in the intervals between delivery of cardioplegia (clamped 16.03 ± 1.49 minutes versus unclamped 17.86 ± 1.14 minutes, p = 0.354.)


   Comment
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Comment
References
 
The technique of leaving a patent LITA to LAD graft undissected and unclamped during a redo cardiac surgery is not novel. However, in this study, a broad population of redo surgeries has been evaluated to examine its effects on perioperative mortality. In this study, an 11-year history of redo cardiac surgery in the setting of a patent LITA to LAD was evaluated and failed to identify any association, unadjusted or adjusted, of avoiding the LITA to LAD graft during reoperation versus clamping it. We did note, though, there may be 7 fewer LITA injuries with an undissected, unclamped LITA.

The use of the LITA to LAD graft is near standard for the CABG procedure due to an association with prolonged survival and extended patency [1]. Therefore, the likelihood that reoperative patients will have a patent graft is increasing. The LITA to LAD provides extended benefits when patent in the reoperative patient, demonstrating improved outcomes from reoperative coronary artery surgery [2, 8, 9]. However, there are some serious concerns at the time of reoperation regarding the safety of the pedicle graft. Injury to the conduit at reoperation is reported to occur at a rate between 5% and 40% [3, 4, 10–12]. Injuries to the LITA at reoperation are associated with perioperative mortality rate ranging from 9% to 50% [3, 4, 10–12]. Therefore, operating under these conditions requires special considerations.

To prevent injury to the LITA graft, several reports document techniques to protect the graft at reoperation. Maneuvers taken at the first operation include creating a slit in the pericardium to permit the LITA to be tucked down away from the posterior table of the sternum and keep it off of the aorta [2, 13]. Additionally, the left lung should be allowed to inflate over the graft and provide an added anterior level of protection [14]. We routinely practice these techniques. Other suggestions include using polytetrafluoroethylene membrane to cover the LITA [15] or creating a pericardial flap and routing the LITA through a posterior hole in the pericardium [16]. Before the reoperation, it is important to carefully evaluate the lateral and posteroanterior chest roentgenograms for establishing the course of the IMA graft and its proximity to the chest wall. Computed tomography scan has also been used for this assessment and been proven beneficial [17]. Lastly, it has been suggested that early initiation of cardiopulmonary bypass allows for decompression of the heart and easier dissection as well as having the potential for improved tolerance to cardiac injury [18]. During the course of our study, the majority of reoperative patients had femoral arterial and venous access to assist in going on cardiopulmonary bypass should the sternotomy or dissection lead to injury, or if there was perceived significant risk of that.

Another option for avoiding a patent LITA graft is to not use a redo median sternotomy, and choose an alternative surgical approach that provides access to the pathology of interest and can be performed off pump. These approaches include minimally invasive directed coronary artery bypass for lesions of the LAD [19], left lateral thoracotomy for addressing lateral wall lesions [19, 20], and the subxiphoid approach for access to the inferior wall [21]. Performing redo revascularization off pump negates the concern for clamping a patent LITA graft [19]. For isolated mitral valvular disease, an approach through a right thoracotomy is an excellent technique [22]. While these alternative approaches have all been used successfully at specialized centers, the most common approach remains through a redo median sternotomy, which provides the best exposure to multiple sites requiring revascularization and allows access to treat valvular disease.

The strategies listed above are generally employed to reduce injury at the time of redo sternotomy or during dissection of the sternum off the adherent undersurface. However, according to a recent study, prebypass, postresternotomy injuries accounted for 39% of redo cardiac surgery injuries [23]. Based on our experience, this is a very susceptible time for the graft to be injured. The most common reason for injury of the LITA to LAD graft is so it can be clamped in an effort to maximize myocardial protection. In this setting, the patent graft is thought to compromise myocardial protection owing to enhanced cardioplegia washout in the internal mammary artery territory due to the unencumbered flow through the graft. The border zones of perfused versus arrested myocardium are therefore at potentially higher risk to ischemic injury.

The idea of avoiding dissection of the LITA graft was first introduced into the literature by Lytle and colleagues [2]. This technique has been further explored in the setting of mitral valve [5] and aortic valve surgery [6] after CABG and has demonstrated excellent results. Often times, this technique is accompanied by deep hypothermia (approximately 20°C) [5, 6]. However, Ueda and colleagues [24] described performing aortic valve replacement after CABG with a patent LITA to LAD on a beating heart under normothermic conditions with continuous retrograde coronary sinus perfusion of oxygenated blood. Our experience under this condition has been to deepen the hypothermia only modestly from a standard of 32° to 34°C to 28° to 32°C for most cases. Additionally, we occasionally increase the frequency of the cardioplegia redosing, but this is not usual. During a case where the LITA is unclamped, the duration of an isoelectric electrocardiogram is variable. Ventricular fibrillation occurs at a moderate rate. When fibrillation occurs, the patient's hypothermia is deepened, and often time topical cooling solution is added. Additionally, particular attention is placed on assuring thorough decompression of the heart. Currently, we have no significant indications that this impairs function (comparable perioperative myocardial infarction rates and no noticeable changes on postoperative transesophageal echocardiography). Although not specifically evaluated, experience indicates that patients with greater territory supplied by the LITA graft are more likely to have fibrillation between cardioplegia doses. These are typically the patients who are more aggressively cooled systemically and with topical hypothermia. It is clear that the optimal technique for this needs further assessment but may be relatively pliable, possibly based on the territory supplied by the LITA graft.

This study has some important limitations that deserve discussion. First, this is a retrospective study. While the data collected for the STS database is done so prospectively, it is not done so to suit the designs of this study and limited the queries that could be performed. Additionally, reviewing the operative reports for data collection is limited. Second, using perioperative mortality as a primary outcome is limiting in that it is a relatively rare event. The expectation in most logistic regression modeling is that there will be at least 10 outcomes per model variable. Because of this, the model could be questioned regarding its fitness [25]. However, the Hosmer-Lemeshow goodness-of-fit test demonstrated that the model was well calibrated, the AUC was adequate for showing model performance, and the results were biologically plausible. Therefore, we believe the analysis is correct in not associating unclamped LITA with mortality. Third, the potential assumption is that because leaving the LITA to LAD graft unclamped was not associated with perioperative mortality, it is safe. While we believe this, we do not have good intermediate-term or long-term outcomes to evaluate at this time. Specifically, functional data (e.g., postoperative and 1-month echocardiography or functional magnetic resonance imaging) would be a better outcome measure for this intervention. Lastly, a good question is whether the differences in the groups between clamped and unclamped were sufficiently accounted for in our methods. It is possible that variables contained in the database are not specific enough to make this determination. Perfusion times between the groups were similar (unclamped group 134.1 ± 5.4 minutes versus clamped group 141.2 ± 5.3 minutes, p = 0.356). Also, although the distribution of cases was different between the groups, it fell out in the stepwise logistic regression analysis. The ideal strategy for accounting for differences between groups is clearly patient randomization. That would help alleviate selection bias inherent in the process of determining who is a good candidate for not clamping the LITA graft. A graft that is deeply embedded in scar will less likely be clamped. Randomization and a priori subset analysis of case types and ease of LITA graft accessibility could help determine if the LITA graft should ever be clamped or remain unclamped.

The first step in evaluating a strategy of this nature, which defies traditional but sound physiologic dogma, is to document that it does not result in any immediate poor short- term outcomes such as perioperative mortality. The next step is a more elaborate prospective evaluation that should be more rigorously performed with randomization to improve the robust quality of the results and to provide more in-depth analysis about functional quality that could impact quality of life and hospital and rehabilitation time as well as intermediate and long-term mortality. This is the subsequent direction of this work.

In conclusion, reoperative cardiac surgery after CABG with a LITA to LAD occurs for a variety of reasons. Although dogma has encouraged clamping of the LITA to LAD graft to optimize myocardial protection, the necessity of this maneuver has become increasingly questioned because it exposes the graft to increased injury risk. In this study, we failed to demonstrate any increased risk in perioperative mortality from leaving the LITA graft unclamped. This study is not unique in this finding and supports the work of others who have investigated the technique in isolated valvular disease. Further work is needed to investigate the effect of this "hands-off" technique on functional outcomes and intermediate and long-term mortality.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Comment
 References
 

  1. Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events N Engl J Med 1986;314:1-6.[Medline]
  2. Lytle BW, McElroy D, McCarthy P, et al. Influence of arterial coronary bypass grafts on the mortality in coronary reoperations J Thorac Cardiovasc Surg 1994;107:675-683.[Abstract/Free Full Text]
  3. Gillinov AM, Casselman FP, Lytle BW, et al. Injury to a patent left internal thoracic artery graft at coronary reoperation Ann Thorac Surg 1999;67:382-386.[Abstract/Free Full Text]
  4. Ivert TS, Ekestrom S, Peterffy A, Welti R. Coronary artery reoperations. Early and late results in 101 patients. Scand J Thorac Cardiovasc Surg 1988;22:111-118.[Medline]
  5. Byrne JG, Aranki SF, Adams DH, Rizzo RJ, Couper GS, Cohn LH. Mitral valve surgery after previous CABG with functioning IMA grafts Ann Thorac Surg 1999;68:2243-2247.[Abstract/Free Full Text]
  6. Byrne JG, Karavas AN, Filsoufi F, et al. Aortic valve surgery after previous coronary artery bypass grafting with functioning internal mammary artery grafts Ann Thorac Surg 2002;73:779-784.[Abstract/Free Full Text]
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  10. Coltharp WH, Decker, MD, Lea JWt, et al. Internal mammary artery graft at reoperation: risks, benefits, and methods of preservation Ann Thorac Surg 1991;52:225-229.[Abstract/Free Full Text]
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  16. Pacifico AD, Sears NJ, Burgos C. Harvesting, routing, and anastomosing the left internal mammary artery graft Ann Thorac Surg 1986;42:708-710.[Abstract/Free Full Text]
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ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
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