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Ann Thorac Surg 2006;81:139-143
© 2006 The Society of Thoracic Surgeons


Original article: Cardiovascular

Benefit of Partial Right-Bilateral Internal Thoracic Artery Harvesting in Patients at Risk of Sternal Wound Complications

Jacob Zeitani, MD a , * , Alfonso Penta de Peppo, MD b , Ruggero De Paulis, MD a , Paolo Nardi, MD a , Antonio Scafuri, MD a , Saverio Nardella, MD a , Luigi Chiariello, MD a

a Division of Cardiac Surgery, Tor Vergata University, Rome, Italy
b Second University of Naples, Naples, Italy

Accepted for publication June 8, 2005.

* Address correspondence to Dr Zeitani, Division of Cardiac Surgery, Tor Vergata University, Via Oxford 85, Rome 00133, Italy (Email: zeitani{at}hotmail.com).


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Excellent long-term patency of the internal thoracic artery (ITA) graft promotes use of bilateral ITA bypass grafting; sternal devascularization, however, increases the risk of wound complications. We hypothesized that restricting right ITA (RITA) harvesting to a short proximal skeletonized segment (3 to 5 cm) would result in adequate residual blood supply to reduce that risk.

METHODS: Seventy-eight patients with numerous risk factors for wound complications underwent composite double ITA grafting, utilizing the RITA segment anastomosed to the left skeletonized ITA and to the obtuse marginal branch in Y fashion. Blood flow in the distal RITA was assessed by parasternal transthoracic Doppler ultrasonography. Comparisons were made with prospectively collected data of patients undergoing pedicled single (n = 160) or skeletonized bilateral ITA grafting (n = 143) during the same period.

RESULTS: Incidence of obesity, chronic obstructive pulmonary disease, diabetes, and peripheral vascular disease was higher in study patients. Postoperative Doppler ultrasonography detected reversed systolic dominant flow pattern. Wound complications occurred in 2 of 78 (2.6%) patients, compared with 14 of 143 (9.8%) after bilateral ITA (p = 0.04) and 8 of 160 (5%) after single ITA grafting (p = ns). Technique of bilateral ITA harvesting (partial right versus full length; odds ratio, 0.2; confidence interval: 0.04 to 0.9) and diabetes mellitus (odds ratio, 2.7; 95% confidence interval: 1.1 to 6.3) were independent predictors of wound complications in the entire series.

CONCLUSIONS: Substantial residual blood supply is detectable after partial RITA harvesting and may prevent wound complications in high-risk patients.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Evidence of better long-term patency of internal thoracic artery (ITA) grafts, compared with vein grafts [1], promotes the use of arterial grafts for myocardial revascularization. Despite availability of various arterial conduits, the ITA remains the ideal arterial graft [2], and several investigations appear to confirm the benefit of bilateral ITA (BITA) over single ITA (SITA) grafting for myocardial revascularization [3–5]. Bilateral harvesting implies, however, extensive devascularization of the sternum and increases the risk of postoperative tissue ischemia, leading to wound infection and dehiscence [6], in particular in patients with additional risk factors of wound complications as diabetes mellitus, obesity, chronic obstructive pulmonary disease, or peripheral arteriopathy [7–10]. As a consequence, although the technique of skeletonization of the ITA may limit the extent of devascularization of the sternum and reduce the risk of complications [11–17], BITA harvesting is frequently avoided in patients with multiple risk factors. To maintain the benefit of receiving two ITAs in those high-risk patients, we proposed a method of partial right BITA harvesting and composite arterial graft fashioning [18], which seems to offer substantial residual blood flow to the middle and distal portions of the right hemisternum. The aim of this study was to assess the extent and pattern of that residual blood flow and the occurrence of wound complications in selected patients.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
One thousand three hundred patients underwent isolated myocardial revascularization at our institution from January 2002 to December 2004; of those, 78 patients requiring revascularization of the left anterior descending artery and of at least one large proximal obtuse marginal branch, presenting two or more risk factors of sternal wound complications (obesity, diabetes mellitus, chronic obstructive pulmonary disease, peripheral vascular disease, depressed left ventricular function), underwent BITA bypass grafting by using the method of partial right ITA (RITA) harvesting and assembling the composite graft in Y fashion. Ethical Review Board approval (December 10, 2001) and individual patient informed consent for surgical and additional radiologic procedures were obtained.

Surgical Technique
Surgery was performed after skin preparation with povidone-iodine solution and antibiotic administration (1 g intravenous ceftizoxime) before incision; antibiotic prophylaxis was continued for 48 hours postoperatively. The partial right BITA harvesting technique and the method of composite arterial graft fashioning have been described previously [18]. Briefly, the left parasternal endothoracic fascia is incised longitudinally, and the left ITA (LITA) with the adjoining veins are visualized. The artery is then harvested in a scheletonized fashion for the full sternal length, by using titanium clips and scissors to dissect collateral branches. Similarly, a proximal RITA segment is dissected in a skeletonized fashion, from its origin to the second or third intercostal space (3 to 5 cm) Then, the free ends of the residual artery are clipped with titanium clips, the segment is removed and anastomosed as a "free graft" end-to-side to the "in-situ" LITA, in a Y-graft configuration, approximately at the level where it crosses the left pericardial border when distended toward the left anterior descending artery. The RITA segment is anastomosed to the first obtuse marginal branch and the in-situ LITA to the left anterior descending artery. In 45 patients the LITA was also sequentially anastomosed to a diagonal branch, and in 7 patients the RITA segment was sequentially anastomosed the first and second obtuse marginal branches. The sternum was reapproximated at the end of the procedure by using a single stainless steal wire (A&E Medical Corporation, Farmingdale, New Jersey) for each 10 kg of body weight. The fascia, subcutaneous layers and skin were closed with running absorbable sutures.

Ultrasonography and Radiography
To assess the preoperative blood flow in the distal RITA and the postoperative residual flow in the residual distal RITA, a transthoracic color Doppler ultrasound scan (Sonos 5500 and 7.5 MHz transducer; Hewlett Packard, Andover, Massachusetts) was performed with intercostal approach at the fourth to fifth right parasternal space, obtaining two-dimensional images and pulsed Doppler signals preoperatively and from the fourth to sixth postoperative day.

In 10 patients, an anteroposterior chest radiograph was obtained in the operating room with portable equipment, protected by sterile drapes, after injection of 30 mL of iodine solution through an 18G cannula inserted into the still unclipped end of the undissected distal RITA, to visualize the residual vascular supply to the right hemisternum (the distal RITA and corresponding intercostal branches). On the fourth postoperative day, a multislice computed tomography (CT) scan was performed in the same patients after injection of iodine solution in a peripheral vein, visualizing the distal RITA, veins, and the corresponding intercostal branches.

Wound complications were observed during hospitalization or detected by physical examination at the outpatient clinic during the first 2 postoperative months of follow-up; they included instability of the sternum, without evidence of tissue infection, or sternal wound infection, according to the guidelines for prevention of surgical site infection of the Hospital Infection Control Practices Committee [19]. In particular, superficial infection was defined as wound erythema and purulent discharge involving the skin and the subcutaneous layers without involvement of sternal or mediastinal tissues; deep infection was diagnosed in case of one of the following: visual evidence of mediastinitis, isolation of an organism from culture of mediastinal tissue or fluid, or fever or instability of the sternum associated with purulent drainage from the mediastinum. Patients' characteristics and occurrence of sternal wound complications were compared with the prospectively collected data of 143 consecutive patients undergoing isolated bypass grafting with skeletonized BITAs during the same period, and of 160 patients submitted to pedicled SITA grafting on the same dates (2 days before or after). The decision for the number of ITAs and the method of harvesting was taken by one of the four attending surgeons involved in the series. Patients undergoing off-pump bypass or concomitant procedures were excluded.

Statistical Analysis
Comparisons of variables were performed by the unpaired Student's t test, {chi}2 or Fisher's exact test, as appropriate. Influence of variables on wound complications was assessed by univariate analysis; factors potentially affecting sternal wound complications included age, sex, III to IV New York Heart Association functional class, echocardiographic left ventricular ejection fraction lower than 50%, diabetes mellitus, obesity (body mass index ≥ 30 kg/m2), chronic obstructive pulmonary disease, peripheral vascular disease, type of ITA harvesting (single in pedicled fashion, skeletonized full-length bilateral, skeletonized partial right bilateral), and time of cardiopulmonary bypass. Factors with a probability (p) value less than 0.1 were then included in a stepwise logistic regression prediction model. Variables are presented as mean ± 1 SD. A p value less than 0.05 was considered statistically significant. Statistical analysis was done by SPSS statistical software package (SPSS, Chicago, Illinois).


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Patients undergoing partial right BITA harvesting were older and presented more risk factors of wound complications than patients undergoing SITA or full-length BITA harvesting (Table 1). The preoperative transthoracic color Doppler ultrasonography detected antegrade flow in the distal RITA with the normal pattern of a peripheral artery. A shorter operative time was required for dissection of the proximal segment than for dissection of the full sternal length of the RITA (5.7 ± 0.7 versus 19.8 ± 2.6 minutes, p < 0.001). Intraoperative chest radiographs after direct injection of iodine solution in the residual distal RITA showed the artery and the corresponding intercostal branches from the fourth to fifth intercostal spaces; that residual vascular supply was also well identified at postoperative CT scanning (Fig 1). Aortic cross-clamp time was about 5 minutes longer during BITA than SITA bypass grafting; among BITA patients, an average of 2.7 distal ITA anastomoses were performed with the composite Y grafting procedure, a number significantly higher than with in situ BITAs (Table 1). The postoperative Doppler analysis detected systolic dominant inverted flow in the distal RITA.


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Table 1. Data of Patients Who Received Skeletonized Bilateral Internal Thoracic Arteries (BITAs) or Pedicled Single Internal Thoracic Artery (SITA)
 


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Fig 1. Postoperative multislice computed tomography scan of a patient after harvesting of the proximal segment of the right internal thoracic artery, showing the residual artery (arrow), vein, and corresponding intercostal branches (roman numerals indicate intercostal spaces).

 
Mediastinitis did not occur. Analysis of the entire series of 381 patients showed that the rate of wound complications was higher among patients with diabetes mellitus (12 of 107, 10%, versus 12 of 250, 4.6%; p = 0.04); incidence of deep infection or dehiscence was also higher in diabetic patients (5 of 114, 4.2%, versus 2 of 260, 0.8%; p = 0.02). Wound complications were less frequently observed after partial right than after full-length BITA harvesting (2.6% versus 9.8%, p = 0.03). Instability of the sternum without evidence of tissue infection occurred in 2 patients (1.4%) in the full-length BITA group; deep wound infection was diagnosed in 4 more patients (2.8%) in that group, in 1 patient (0.6%) in the SITA group, and in no patient in the partial right BITA group. Incidence of deep wound complications was higher in the full-length than in the partial right BITA group, although at low statistical power (4.2% versus 0%, p = 0.06); nevertheless, comparisons with patients receiving a SITA demonstrated a significantly higher rate of deep wound problems after full-length but not after partial right BITA harvesting (4.2% versus 0.6%, p = 0.03, and 0% versus 0.6%, p = not significant; Table 1). A multivariate analysis in the entire series was then performed, showing that both diabetes and technique of BITA (partial versus full-length RITA) harvesting were independent predictors of wound complications (Table 2).


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Table 2. Predictors of Sternal Wound Complications
 
All patients with deep wound complications underwent reoperation for debridement of necrotic and devascularized tissue and direct closure of the sternum, fascia, and superficial layers, associated with intravenous antibiogram-guided antibiotic therapy in patients with positive cultures or wide-spectrum antibiotic prophylaxis in aseptic sternal dehiscence. They experienced complete wound healing. Patients with superficial wound complications were also treated by surgical debridement, primary closure of wound dehiscence and antibiotic treatment, as described previously [20]; one procedure failed and was crossed over to conventional topical treatment until secondary wound healing.


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Different surgical strategies have been developed during the last decade to achieve the optimal myocardial revascularization for each patient. It is now well documented that the ITA graft compares favorably with other conduits, owing to the relatively large vessel diameter and the physiologic properties of the arterial wall, which provide for high flow and long-term patency [1, 2]. Use of BITAs has been recently reported to improve survival and freedom from recurrent angina [3–5] but, at the same time, to cause extensive devascularization of the sternum, increasing the risk of wound infection and dehiscence [6]. That risk appears to increase seriously in patients with additional known risk factors as diabetes mellitus or chronic obstructive pulmonary disease [7–10]. Recently, for example, Molina and colleagues [10] reported an high incidence of wound infection in obese patients, with a high mortality rate, and questioned whether BITA harvesting should be performed in these patients. Unlike pedicled ITA harvesting, the technique of skeletonization reduces the extent of devascularization of the chest wall, leaving veins, muscle and surrounding endothoracic tissue in place and is, therefore, potentially associated with fewer postoperative wound complications: indeed, occurrence of sternal wound infection appears consistently low after routine use of bilateral skeletonized ITAs [15–17]. For example, the 2.8% rate of deeper wound infection in the present series is similar to the recently reported rates of 1.7% by Matsa and associates (13), 2.2% by Pevni and colleagues [21], or 2.4% by Sauvage and coworkers [22]. Other recently published investigations in patients with diabetes also report a very moderate prevalence of wound problems after BITA skeletonization, with deep sternal infection rates from 1.3% to 4% [11, 13, 23].

Previous observations at our institution [14] also suggest a lower rate of wound infections after skeletonization of BITAs than after harvesting both arteries in a pedicled fashion; indeed, skeletonization may preserve a number of sternal and intercostal branches arising as a common trunk from the ITA [24], maintaining some collateral flow to the sternum. Also, implantation of bilateral in-situ ITAs has the advantage of maintaining two separate blood supplies to the myocardium, avoiding additional anastomoses to fashion a composite graft. Nonetheless, we also found that the risk of wound complications seemed to increase greatly in patients with several risk factors for wound infection; the present study suggests that the proposed method of partial right BITA harvesting and skeletonization may further improve residual blood supply, and therefore wound healing, in those high-risk patients.

We hypothesized that a proximally limited dissection of the RITA would leave a residual vascular supply to the right hemisternum through the distal RITA, promoting more efficient wound healing, in particular in patients presenting with numerous risk factors for complications. Although use of the distal arterial segment would result in residual antegrade perfusion to the chest wall, the proximal ITA segment was preferred as it presents a larger diameter, which facilitates fashioning of the composite graft. Interestingly, postoperative Doppler analysis of blood flow in the distal RITA, which could now be considered as the terminal branch of the right superior epigastric artery, showed inverted systolic dominant flow pattern, as previously reported [18]. Connections to the lower intercostal branches and to the inferior epigastric artery appear to provide, therefore, for a persistent blood supply to the middle and distal portions of the right hemisternum that should be advantageous to promote wound healing. Indeed, owing to the inclusion criteria, patients selected for the described technique presented several potential risk factors of wound complications; yet, sternal wound problems rarely occurred in these patients, showing a significantly lower rate of wound complications all together when compared with control BITA graft patients. Also, fewer deep wound complications were observed in the former group, but at a low statistical power, possibly as result of the several inclusion criteria selecting a homogeneous but relatively small group of coronary patients for the partial right BITA harvesting procedure; nevertheless, occurrence of deep complications after full-length, but not partial right, BITA harvesting compared unfavorably with single ITA harvesting, thus enhancing the clinical significance of these observations in that subset of complications and underlining the overall benefit of the proposed technique in preventing wound problems. Findings were confirmed by a multivariate analysis of the potential risk factors in the entire series of 381 patients, still showing that type of BITA harvesting (partial versus full-length RITA) and diabetes mellitus were independent predictors of wound complications.

It has to be noted that the observed rate of 4.2% of deep wound complications after full-length BITA skeletonization appears relatively high when compared with prevalence of deep sternal infection, the more frequently reported wound problem, in the literature; that may account for the statistical significance of that figure in the present study. It should be considered, however, that postoperative sternal instability without evidence of infection is potentially related, as sternal infection, to the extent of sternal devascularization and therefore to the technique of harvesting, thus validating our definition of deep wound complication that was anyhow adopted for all observations in the series.

Feasibility of the described composite Y grafting procedure requires a favorable coronary anatomy, with a large and proximally located obtuse marginal branch; in that case, a rather short proximal segment of the RITA appears adequate, as part of the composite Y graft, to reach the first and sometimes the second marginal branches. Otherwise, should further sternal devascularization be required to harvest a longer segment, other arterial grafts, as the radial artery, may replace the RITA as second conduits to reach the circumflex territory, accomplishing complete arterial revascularization of the left ventricle with, one hopes, a good patency rate. In our technique, the proposed length of the RITA segment may vary from 3 to 5 cm, depending on the number and location of the marginal branches needing revascularization; that aspect can usually be assessed preoperatively, after evaluation of coronary angiograms. Intraoperative inspection of the obtuse marginal branches is also recommended before RITA harvesting. Furthermore, the proposed composite Y-graft technique provides the possibility of sequential grafting of the LITA to the left anterior descending artery and diagonal branches; consequently, more arterial distal anastomoses per patient were performed with that technique than with bilateral in-situ ITA grafting.

In conclusion, the proposed method of BITA grafting, preserving substantial vascular supply to middle and distal sternal tissues, appears to prevent wound complications in selected patients at high risk of this complication, who may therefore benefit from receiving two or more grafts by means of the two ITAs at acceptable risk.

Limitations of the Study
Patients selected for partial right BITA harvesting presented more numerous risk factors for wound complications than control patients. That observation could be expected to strengthen the positive influence of that method on occurrence of wound complications; nevertheless, comparisons among groups carry a potential selection bias. To better define this aspect, however, type of harvesting was also assessed in a multivariable model including data from the entire series, demonstrating that type of harvesting (partial versus full-length RITA) as well as diabetes mellitus were independent predictors of wound complications. It should also be mentioned that the present investigation implies the limitations of nonrandomized studies; more observations are therefore required to confirm the reported findings.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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