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Ann Thorac Surg 2007;84:1479-1484. doi:10.1016/j.athoracsur.2007.06.034
© 2007 The Society of Thoracic Surgeons
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Original Articles: Cardiovascular

Quality of Internal Thoracic Artery Grafts After Mediastinal Irradiation

Brigitte Gansera, MDa,*, Fabian Schmidtler, MDa, Ilias Angelis, MDa, Florian Botzenhardt, MDb, Tibor Schuster, MDc, Theodor Kiask, MDa, Ayman Haschemi, MDa, Bernhard M. Kemkes, MD, PhDa

a Department of Cardiovascular Surgery, Klinikum Munich-Bogenhausen, Munich, Germany
b Department of Cardiology, Klinikum Munich-Bogenhausen, Munich, Germany
c Institute for Medical Statistics and Epidemiology, Technische Universtität München, Munich, Germany

Accepted for publication June 8, 2007.

* Address correspondence to Dr Gansera, Department of Cardiovascular Surgery, Klinikum Bogenhausen, Englschalkinger Str 77, Munich, D-81925, Germany. (Email: brigitte_gansera{at}web.de).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: With the increase of patients of advanced age requiring coronary artery bypass grafting (CABG), the number of those with previous mastectomy and irradiation of the chest increases proportionally. The question of whether mediastinal irradiation leads to relevant internal thoracic artery (ITA) graft damage remains unclear. The aim of the present study was to proof the quality of ITAs and to evaluate the early clinical outcome after using one or both ITAs in this specific population.

Methods: One hundred twenty-five patients (group A) with previous mastectomy or Hodgkin/non-Hodgkin disease and mediastinal irradiation operated on between January 1993 and September 2006 underwent CABG (n = 88) or CABG plus valve replacement (n = 37). Sixty-two patients received bilateral, 43 received unilateral ITAs, and 20 patients received veins. Postoperative complications and mortality were analyzed and compared with a propensity score pair-matched control group of 125 patients receiving CABG or CABG plus valve replacement within the same period (group B). A histomorphologic investigation was performed in 133 irradiated distal ITA segments and compared with a control group of 133 nonirradiated ITAs.

Results: Thirty-day mortality revealed 3.2% in group A versus 5.6% in group B. Sternal instabilities were more frequent in group A (3.2%) than in group B (0%). Mediastinitis occurred in 1.6% (group A) versus 1.6% (group B). Histomorphologic investigations did not identify any severe irradiation induced fibrosis or damage of ITA grafts.

Conclusions: From the histologic point of view, there is no need for restrictions in use of ITA conduits after mediastinal irradiation. Compared with a control group, cardiac surgery was associated with a slightly enhanced incidence of sternal instabilities.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Mediastinal irradiation represents the common therapeutic treatment for patients with carcinoma of the breast or Hodgkin/non-Hodgkin lymphoma. The development of coronary artery disease [1, 2], valvular dysfunctions [3, 4], and various types of radiation-induced heart diseases [5–7] have been reported. Also, several authors have documented the experimental and clinical aspects of radiation-associated injuries to the heart and coronary arteries [8, 9].

As we experience in cardiac surgery an increasing number of patients of advanced age, the number of those with previous curative (relapse free) mastectomy or Hodgkin/non-Hodgkin lymphoma and irradiation of the chest increases proportionally. The optimal surgical strategy and treatment for this unique group of patients requiring coronary artery bypass grafting surgery (CABG) after mediastinal irradiation remains unclear. In particular, the question whether to use primarily venous grafts or internal thoracic artery (ITA) conduits for myocardial revascularization has not been conclusively answered by clinical studies.

A per se higher incidence of postoperative complications such as sternal instabilities and wound infections in these patients is considered to be potentially intensified after the use of one or both ITAs.

In this context, the well known long-term benefit of arterial revascularization, using one or both ITAs, is discussed controversially for this unique subgroup of patients after irradiation. A rare number of studies exist that provide conflicting results and include very small patient populations. Some of them recommended a restrictive use of ITA grafts owing to vessel friability in these patients [10, 11]; others consider ITA grafts in these patients as a viable conduit for myocardial revscularization when preoperative assessment shows patency [12–14]—albeit including very small patient cohorts.

The questions of whether mediastinal irradiation leads to a relevant ITA conduit damage [15] and whether CABG in these patients is associated with increased mortality and sternal wound complications, as described by Handa and colleagues [16], remain unclear. Recent data, published by Nasso and colleagues in 2005 [17] and including at least 49 patients after chest irradition, suggest that the use of one or both ITAs is not associated with enhanced graft failure or increased wound healing complications. This study supports our previous experiences with 70 such patients, published in 1999 [18].

The purpose of the present study was to evaluate the quality of ITAs, their adequacy as a conduit determined by observed flow patterns or histomorphologic investigations, to analyze operative data, early clinical outcome, and postoperative complication rate after revascularization using one or both ITAs in a large cohort of such patients with prior irradiation of the chest.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
From January 1993 to September 2006, 138 patients in our department underwent cardiac surgery after previous mediastinal irradiation. The Ethics Committee approved the study and waived the need for patient consent as individual patients were not identified. Nevertheless, written individual consent for the collection of surgical tissue was obtained previously from each patient.

One hundred twenty-five of these patients (group A: mean age, 68.1 ± 9.0 years; range, 39 to 82; 74% females) with previous (6 months to 37 years; mean, 14 years) mastectomy or Hodgkin/non-Hodgkin disease and mediastinal irradiation (1.0% of a total of 13,111 patients) underwent isolated CABG (n = 88) or concomitant CABG plus aortic valve replacement (AVR [n = 31]) or mitral valve replacement (MVR [n = 6]).

Mediastinal radiation reference dose was 50 Gy at 2 Gy daily over 5 weeks with parasternal, supraclavicular, and axillary fields applied in patients after mastectomy (n = 98), and the mantlefield technique used in patients with Hodgkin or non-Hodgkin disease (n = 27). All these patients were curatively treated and classified as relapse free at the moment of cardiac surgery. Inclusion criteria were one- to three-vessel disease and severe aortic/mitral valve stenosis or insufficiency. Thirteen patients with previous irradiation operated on within this period underwent isolated valve replacement or aortic surgery and were not included in the study.

Sixty-two patients received bilateral ITAs, 43 patients unilateral ITAs, and 20 patients only veins. Operative data, postoperative complications, mortality, and incidence of sternal infection or refixation were analyzed and compared with a propensity score matched patient group receiving CABG or CABG plus valve replacement in the same period (group B: n = 125; mean age, 68.3 ± 9.7 years). For every group A patient, a matching patient with the closest pair score was selected from a pool of 13,111 patients operated on within the same period.

Concerning the analysis of sternal instabilities and sternal wound infections, the groups were divided into patients receiving both, one, or no ITA, as follows: group A1, bilateral ITA, n = 62; group A2, unilateral ITA, n = 43; group A3, no ITA, n = 20; and group B1, bilateral ITA, n = 58; group B2, unilateral ITA, n = 48; group B3, no ITA, n = 19.

A histomorphologic investigation (van Gieson stain with emphasis on media and intima fibrosis) of distal ITA segments was performed in 98 patients and 133 irradiated ITAs and compared with a control group of 133 nonirradiated ITAs. This control group consists of a age-matched population (mean, 68.7 years) with isolated hypertension, hyperlipidemia, or peripheral vascular disease (n = 133). The classification was performed semiquantitatively by two independent pathologists using four categories: none, slight, medium, and severe fibrosis.

Statistical Analysis
Continous variables are expressed as mean ± SD. Chi-square tests and Fisher’s exact tests, if appropriate, were used for group comparison of categorical variables. Distribution of quantitative variables between both groups was compared using the Mann-Whitney U test. All patient data were subjected to logistic regression analysis, and the propensity score was calculated for each patient. For every group A patient, a matching patient with the closest score was selected from a large pool of patients receiving CABG or CABG plus valve replacement within the same period (group B). Statistical analysis was performed with the software SPSS (version 14; SPSS, Chicago, Illinois). A p value less than 0.05 (two-tailed) was considered to indicate significance. Maximum propensity score deviation revealed 0.035. Propensity score match pair analysis was performed using the SAS software (release 8.2; SAS Institute, Cary, North Carolina).

Surgical Technique
All patients were operated on using conventional techniques with median sternotomy. Dissection of ITAs was performed from the origin of the subclavian artery to the bifurcation of the vessel, using a small pedicle of surrounding tissue. The use of electrocoagulation was avoided to protect the graft from thermal damage. The CABG was done using extracorporeal circulation under moderate hypothermia (34°C), with crystalloid cardioplegia (Bretschneiders Solution; HTK Köhler Chemistry, Alsbach, Germany).

Electromagnetic flow measurements were not performed regularly, but a Parsonnet probe was carefully passed through the graft to make sure that no stenosis was present. If the flow appeared to be unacceptable, ITAs were not used for grafting. If bilateral ITAs were used, the right ITA was directed to the left anterior descending artery, and the left ITA to the circumflex artery or obtuse marginal branch. In cases where only the left ITA was used, the graft was regularly directed to the left anterior descending artery.

The position of ITAs was fixed by three sutures of the pediculus, and the right ITA was covered by a polytetrafluoroethylene (PTFE) sleeve (Gore-Tex; WC Gore, Putzbrunn, Germany) for protection in case of reoperations (Fig 1). Additional bypasses were done with saphenous vein grafts.


Figure 1
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  		Fig 1. Operative view before sternal closure. Right internal thoracic artery is covered with a polytetrafluoroethylene sleeve.

 

   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Both groups were comparable with high homogeneity concerning demographic data (age, p = 0.80; BMI, p = 0.71; sex, p = 0.66), risk factors (diabetes mellitus, p = 0.35; ejection fraction, p = 0.98;.emergent operations, p > 0.99), and procedural variables (use of both or one ITAs, p = 0.61 or 0.36; concomitant procedures, p = 0.88; number of anastomosis, p = 0.74). Maximum propensity score deviation revealed 0.035.

No severe surgical technique problems, apart from some adhesions between pericardium and epicardium, were present in any irradiated patient. Internal thoracic artery dissection was slightly prolonged compared with the control group (mean, 17 minutes versus 13 minutes). We observed no significant difference in aortic cross-clamp time and bypass time (Table 1). The number of anastomoses did not differ significantly between group A and B (mean, 2.78 versus 2.82). Duration of surgery (skin to skin) revealed 174.6 ± 43.3 minutes versus 182.5 ± 65.4 minutes (p = 0.87).


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  		Table 1 Operative Data Group A Versus B
 
All ITAs used showed a widely patent lumen, excellent flow without macroscopic visible fibrosis, and in particular, without difference between irradiated and contralateral side. Fifty percent of the patients received bilateral ITAs. Owing to peripheral localization of native coronary vessel stenosis or inadequate target vessel (no left anterior descending artery stenosis), only one ITA could be used in 34%. Sixteen percent of patients received isolated saphenous veins after destruction of the ITA graft surgically; only 5 ITAs were rejected because of insufficient quality or flow pattern of the conduit. Internal thoracic arteries of these 5 patients showed no stenosis, with histomorphologically normal elastic pattern of the media without intimal thickening, but intima dissections presumably caused iatrogenic by surgical injury.

Thirty-day mortality revealed 3.2% in group A, versus 5.6% in group B (p = 0.36). Sternal instabilities as well as wound infections were more frequent in group A (3.2% and 4.8%) versus group B (0% and 4.0%; Table 2). Mediastinitis occurred in 1.6% in both groups (Table 2) and was associated with bilateral ITA grafting (Table 3).


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  		Table 2 Complications and Mortality Group A Versus B
 

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  		Table 3 Sternal/Wound Healing Complications After Both, One, or No Internal Thoracic Artery (ITA)
 
Histomorphologic investigations, performed by two independent pathologists, did not identify any severe fibrosis or irradiation-induced damage of ITA grafts. Examples of histomorphologic examinations (van Gieson stain) are depicted in Figures 3 and 4. Go


Figure 3
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  		Fig 3. Left internal thoracic artery of irradiated side shows slight fibrosis of intima and media.

 

Figure 4
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  		Fig 4. Right internal thoracic artery from the same patient depicted in Figure 3 shows discreet fibrosis of intima and media.

 
Histomorphologic Investigations
The ITA slide preparations from 98 patients and 133 ITA segments showed no severe irradiation-induced fibrosis (Table 4). There was no statistical significance concerning the graduation of medium or severe intima fibrosis between both groups (p = 0.11). In about 50% of all ITAs (irradiated as well as of the control group), a slight intima and media fibrosis was observed (Fig 3). Histomorphologic differences between ITA segments of the ipsilateral, irradiated side of mastectomy and the contralateral side were at most discreet (Figs 3 and 4) and did not differ between patients with Hodgkin/non-Hodgkin lymphoma or cancer of the breast. Irradiation dose-dependent differences were not present.


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  		Table 4 Histomorphologic Stainings of 133 Irradiated and 133 Nonirradiated Internal Thoracic Artery (ITA) Segments
 
In 1 patient who had undergone mastectomy and irradiation of both sides, an infiltration of carcinoma cells (positive for estrogen receptors) in the perivascular tissue and adventitia of right ITA was observed. The arterial wall, media, and intima showed no infiltration, and the left ITA and its pedicle were free of carcinoma cell infiltration.

Figures 3 and 4, longitudinal sections of left ITA (Fig 3) and right ITA (Fig 4), with van Gieson staining, show slight fibrosis of intima and media at the left ITA and discreet fibrosis at the right ITA, without distinct difference, after left-sided irradiation and both-sided mastectomy in a 77-year-old woman with carcinoma of the breast.


   Comment
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Chest irradiation might induce a wide spectrum of heart diseases such as pericarditis [19], pancarditis, cardiomyopathy [20], valvular dysfunction [3, 4, 21], aortic calcifications, and coronary artery disease [7–9, 12, 21]. Although modern techniques in radiotherapy reduce cardiac exposure (using computed tomography and magnetic resonance imaging for accurate calculation of tumor dose, cardiac shielding, altering the depth of fields), a large cohort of patients have been exposed to orthovoltage irradiation or inadequate shielding.

Irradiation-induced coronary artery disease must be considered in any patient treated with a dose of 30 Gy or more [13]. Patients requiring CABG after mediastinal irradiation show some characteristic findings that might influence standard surgical techniques. Radiation fields for breast carcinoma or Hodgkin disease commonly include the course of the ITA. With the internationally accepted consensus that ITA bypasses, in particular bilateral ITA bypasses, improve long-term survival rates [23], the use of the left ITA as a conduit in myocardial revascularization has become surgical standard.

As advocates of bilateral ITA grafting, we have performed in our department in more than 5,500 patients bilateral ITA bypasses with encouraging clinical results [22], angiographically proven superior graft patency [25], and without significant enhancement of sternal complications [22]. On the other hand, the routine use of both ITAs was restricted by early studies that reported an increased perioperative mortality, enhanced postoperative complication rates such as bleeding, and subsequent rethoracotomy or sternal wound healing complications [24].

Only a rare number of studies with very few patients reported their experiences in patients requiring CABG after mediastinal radiation therapy. In particular, five available series [10, 12–14, 17] emphasize the use of unilateral or bilateral ITAs after previous mediastinal irradiation as a suitable method. The most recent study concerning this subject was carried out by Nasso and colleagues in 2005 [17]. This group included 49 patients after chest irradiation receiving at least one ITA and compared them, using a highly sophisticated statistical analysis using a propensity score matched model, with 49 patients who had a history of cancer (mostly of the breast) but who were treated without radiation. Flow measurements, as well as histomorphologic investigations in terms of intimal and media thickening, showed no difference of irradiated compared with nonirradiated ITA segments. These results underline favorably our own results, although their surgical strategy of ITA dissection was skeletonized whereas we preferred the pedicled technique. Perioperative mortality was revealed as 2.0%, superior to our results, but that might have been influenced by the younger age (mean, 57 ± 6.4 years versus 68.1 ± 9.0 in our cohort) and in particular by the phenomenon that combined procedures were excluded. Two of 4 deaths in our population were related to patients’ receiving CABG plus valve replacements.

Deep mediastinitis in the mentioned study occurred exclusively in the nonirradiated group, in 4.1% (2 patients), and was associated in both cases with bilateral ITA grafting. Hicks and colleagues [10] rejected the routine use of ITAs in these patients after the experience of 14 such patients in whom ITAs were dissected in 92% but could be used owing to conduit friability and mediastinal fibrosis in only 3 of these cases. In 2 of 7 irradiated patients, severe stenosis of ITA grafts was detected angiographically by Reber and colleagues [12]; therefore, preoperative angiographic assessment of the vessel was recommended. Van Son and colleagues [13] consider ITA as a viable conduit in 7 of 10 such patients, provided that preoperative assessment (Doppler analysis or angiogram of ITA) shows patency. They detected histologically dense fibrosis of the ITA wall with complete obliteration; in another 2 patients, they found normal elastic pattern of the media without intimal thickening. In our study, histomorphologic examinations of 133 distal ITA-segment-preparations with prior irradiation showed no severe intima or media fibrosis.

The risk of cardiac infiltration remains unclear. Histomorphologic investigation detected in the adventitia of one ITA segment an infiltration of carcionoma cells. For secure prevention of cardiac infiltration by carcinoma cells, intraoperative immediate section before the use of ITAs should be recommended.

Eighty-four percent of our patients received at least one ITA; the frequency of bilateral ITA grafting amounted to almost 50% (62 patients). Owing to adhesions, dissection of ITA continues to be more demanding, but the risk of surgical injury to the graft seems not to be higher compared with the control group. In 7 patients, the left ITA was injured primarily surgically.

After careful preparation, we experienced only 5 cases of ITA grafts with an unacceptable flow. These patients received, as did 15 others without left anterior descending artery stenosis as an adequate target vessel for the LITA, only saphenous veins. Internal thoracic arteries in these 5 patients showed no stenosis, histologically normal elastic pattern of the media, without intimal thickening or fibrosis, but surgically induced intima dissections. We regularly passed through all ITA grafts carefully with a Parsonnet probe (1.5 mm), to make sure that no severe stenosis was present. In our opinion, this procedure reliably replaces the need for preoperative angiography. If easy passage throughout the graft is not possible, it should be rejected.

The routine use of both ITAs was restricted by studies that reported an enhanced perioperative mortality and an increased number of postoperative sternal wound complications, in particular among diabetic or extremely obese patients [24]. A higher rate of sternal complications might be expected in patients after chest irradiation, especially when both ITAs were used. Until now, very few clinical reports were related to this problem [16, 17]. Our own study [18] carried out in 1999 consisting of 70 patients, but including lower bilateral ITA frequency, showed no increased wound infections (3.7% versus 4.2%) or sternal instabilities (0% versus 2.8%) in patients after irradiation compared with a control group of corresponding age. These results compared favorably with those of Nasso and colleagues [17].

Now, 7 years later, after expanding the use of bilateral ITAs in a large cohort of irradiated patients, sternal wound healing complications seem to be more frequent compared with the control group—nevertheless, in our opinion, to a justifiable extent. In contrast to our results, Van Son and associates [13] as well as Hicks and coworkers [10] reported no sternal complications after CABG in these patients, albeit in very small cohorts (10 and 14 patients) and after using at best one ITA. Handa and colleagues [16] reported a high (6.8%) operative mortality and alarming (6.8%) sternal infection rate in 44 isolated CABG patients with previous mediastinal radiation therapy, but satisfying midterm survival rates in a total follow-up of 6.2 ± 5.1 years. A differentiation concerning ITA frequency was not performed in this study. In our cohort, perioperative mortality after isolated CABG was revealed as 2.3% (2 of 88 irradiated patients).

One patient with single ITA, 2 patients with bilateral ITAs, and 1 patient without an ITA suffered from postoperative sternal instability. Two patients with severe mediastinitis received either one or both ITAs; therefore, bilateral ITA grafting per se seems not to be responsible for mediastinitis but was associated with an enhanced incidence of sternal instabilities. Superficial sternal wound healing complications, without need of surgical treatment, occurred exclusively in 3 patients with one ITA and 3 other patients with isolated saphenous vein graft. Nevertheless, incidence of sternal wound complications was not increased in patients with bilateral ITAs of the propensity score matched control group.

The emphasis of the present study was primarily to verify the suitability of irradiated ITAs from the functional and histomorphologic point of view. We have evaluated the largest available series in this context; therefore, the results might represent an important contribution concerning this issue.

In conclusion, the restricted use of ITA conduits after mediastinal irradiation is not justified, as histomorphologic investigations did not identify any severe irradiation-induced graft damage. In comparison with a match paired control group, cardiac surgery in these patients was associated with a slightly enhanced incidence of sternal complications.Fig 2 [26]


Figure 2
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  		Fig 2. An angiographic example of a 68-old-man with mediastinal irradiation due to Hodgkin disease. Control angiography was performed 4 years postoperatively. Angiographic findings: right internal thoracic artery (RITA) to left anterior descending artery (LAD) and left internal thoracic artery (LITA) to circumflex artery (to CX).

 


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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  13. Van Son JAM, Noyez L, van Asten WN. Use of internal mammary artery in myocardial revscularization after mediastinal irradiation J Thorac Cardiovasc Surg 1992;104:1539-1544.
  14. Gharagozloo F, Clements IP, Mullany CJ. Use of the internal mammary artery for myocardial revscularization in a patient with radiation-induced coronary artery disease Mayo Clin Proc 1992;67:1081-1084.
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  17. Nasso G, Canosa C, De Filippo CM, et al. Thoracic radiation therapy and suitability of internal thoracic arteries for myocardial revascularization Chest 2005;128:1587-1592.
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M. L. Brown, H. V. Schaff, and T. M. Sundt
Conduit choice for coronary artery bypass grafting after mediastinal radiation.
J. Thorac. Cardiovasc. Surg., November 1, 2008; 136(5): 1167 - 1171.
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