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Ann Thorac Surg 2003;76:754-759
© 2003 The Society of Thoracic Surgeons


Original article: cardiovascular

Failure of internal thoracic artery grafts: conclusions from coronary angiography mid-term follow-up

Eric Bezon, MDa*, Jean N. Choplain, MDa, Yasser A. Maguid, MDa, Ahmed A. Aziz, MDa, Jean A. Barra, MDa

a Department of Cardiovascular and Thoracic Surgery, C.H.U. La Cavale Blanche, Brest, France

Accepted for publication March 13, 2003.

* Address reprint requests to Dr Bezon, Service de Chirurgie Cardiaque, Thoracique et Vasculaire, C.H.U. La Cavale Blanche, 29609, Brest Cedex, France
e-mail: eric.bezon{at}chu-brest.fr


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: The objective of this study was to identify causes of the failures of internal thoracic artery bypass grafts according to operative technique, the internal thoracic artery used, and the coronary artery grafted.

METHODS: This retrospective study concerns 302 follow-up angiographies performed in patients treated with 512 internal thoracic artery bypass grafts: 115 single grafts, 78 sequential grafts, and 109 grafts with two internal thoracic arteries (61 Y grafts). Postoperative angiography was performed after a mean period of 17.3 ± 4.1 months.

RESULTS: Failures consisted of 11 (2%) occluded grafts and 19 (4%) nonfunctioning grafts (threadlike internal thoracic artery). There was no difference in patency among the various types of left anterior descending artery bypass grafts anastomosed with the left internal thoracic artery. The failure rate was higher with the right internal thoracic artery (13%) than with the left internal thoracic artery (4%; p < 0.05). The failure rate of the left anterior descending artery bypass grafts (3%) was lower than that for the branches of circumflex artery bypass grafts (13%; p < 0.05). The 19 cases of nonfunctioning grafts did not include significant anastomotic stenosis: 14 were related to competitive blood flow, 4 to a poor recipient coronary arterial bed, and 1 to significant distal coronary stenosis.

CONCLUSIONS: At least two thirds of failures of bypass grafts could have been avoided by more objective analysis of the coronary stenosis on preoperative coronary angiography and better mastery of the surgical technique.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The superiority of the internal thoracic artery (ITA) over vein grafts for coronary artery bypass grafting has been demonstrated in terms of patency, reoperation rate, and patient survival [1, 2]. At 10 years, 50% of saphenous vein grafts are occluded [3]; 95% of ITA grafts are patent at 1 year and have a good patency rate at more than 10 years [1, 4].

Little data are available about failure of ITA grafts (occlusion, threadlike artery). The objective of this study was to identify the causes of these failures with regard to operative technique, whether the left or right ITA was used, and which coronary artery was grafted.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Material
The postoperative ITA graft patency of 302 patients who underwent coronary artery bypass graft operations between 1984 and 1992 was angiographically evaluated; 512 coronary artery bypass grafts were performed. This study is based on the data of previous prospective studies [58]: single left ITA grafting in 115 patients (1984 to 1986), sequential anastomosis with the left ITA in 78 patients (1985 to 1987), in situ bilateral ITA grafting in 48 patients (1987 to 1989), and reimplantation of the right ITA used as a free graft in the left in situ ITA (Y graft) in 61 patients (1989 to 1992).

Harvesting the ITA was performed using a nontraumatic dissection technique with preservation of the perivascular fat and the ITA pedicle. A diluted papaverine solution was manually injected through the free end of the ITA using an olive-tipped needle [9].

Table 1 shows the coronary artery grafted, the ITA used, and the type of surgical technique used. These techniques have been previously described [58].


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Table 1. Failures of Internal Thoracic Artery Coronary Artery Bypass Grafts

 
Angiographic measurements
In all these series the ITA graft angiographic follow-up was 17.3 ± 4.1 months. The subclavian origin of the ITA graft was selectively catheterized. One milligram of diluted nitroglycerine solution was injected directly in the catheter before injecting the dye. Coronary artery bypass grafts were evaluated by one cardiologist and two surgeons; Y anastomoses were not evaluated in our study. All grafts and coronary artery measurements were based on the angiographic diameter of the coronary catheter to avoid magnification bias.

The ratio of ITA diameter to the grafted coronary artery diameter indicated the rate of graft patency in our study (Fig 1). A ratio equal to or greater than 1 indicates perfect ITA graft patency. A ratio less than 1 with the ITA graft diameter less than 1 mm (threadlike artery) indicates nonfunctioning ITA graft. The ratio of occluded ITA graft was 0. Internal thoracic artery graft occlusion and threadlike ITA are considered as graft failure.



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Fig 1. Analysis of the postoperative coronary angiography. Angiographic measurements were made of the diameter of the internal thoracic artery 1 cm proximal to the anastomosis (A), the diameter of the grafted coronary artery 1 cm distal to the anastomosis (B), the length of the anastomosis (C), the angle between the internal thoracic artery and the coronary artery grafted (D), the diameter of the grafted coronary artery 2 cm distal to the anastomosis (E), the diameter of the grafted coronary artery 4 cm distal to the anastomosis (F), and the diameter of the grafted coronary artery 6 cm distal to the anastomosis (G).

 
The shape and the quality of the anastomosis were evaluated by the ratio of the length of the anastomosis to the ITA diameter (Fig 1). A ratio more than 1 indicated good anastomosis. A ratio between 0.5 and 1 indicated nonsignificant anastomotic stenosis. Significant anastomotic stenosis had a ratio less than 0.5.

The proximal angle between the ITA and the grafted coronary artery (Fig 1) was measured in angiographic front view and perpendicular view. Any kinking of the ITA along its course was recorded.

The distribution of flow from the ITA to the grafted coronary artery was analyzed while injecting dye through the ITA and classified into three categories. Absence of competitive blood flow is indicated by opacification of the grafted coronary up to the proximal coronary stenosis. Presence of mild competitive flow is indicated by opacification of the grafted coronary artery without retrograde flow of the dye up to the proximal coronary stenosis. Presence of true competitive flow is indicated by the following conditions: absence of opacification of the grafted coronary artery and retrograde opacification of the distal segment of the ITA near the anastomosis during selective injection of dye into the native grafted coronary artery. In case of the presence of true competitive flow, proximal stenosis of the involved coronary artery was reevaluated on follow-up coronary angiography and then compared with preoperative coronary angiography.

The recipient coronary arterial bed was assessed by measuring its diameter 2, 4, and 6 cm distal to the anastomosis (Fig 1). This recipient coronary arterial bed was considered poor when the mean value of the three measurements was less than 1 mm.

Statistics
Data are presented as simple percentages. Comparison of these percentages was conducted by a {chi}2 test or Fisher’s exact test for small number of cases. Statistical significance was defined as a p value less than 0.05. The power of the test (1-ß) was calculated according to Casagrande and Pike’s formula [10].


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
There were 30 failures of the ITA graft (Table 1): 11 occluded ITA grafts (2%) and 19 threadlike ITAs (4%).

Failure rate of internal thoracic artery grafts
Failure rates according to the surgical technique are displayed in Table 1. There was not significant difference of failure rate between single (3%) and sequential grafts performed by the in situ left ITA (5%; p > 0.05; 1-ß < 50%). There was not a significant difference of the failure rate between the bilateral in situ ITA graft technique (6%) and bilateral ITA grafting using Y technique (9%; p > 0.05; 1-ß < 50%). The failure rate of single graft performed by the in situ left ITA (3%) is less than the failure rate of the bilateral ITA grafting using Y technique 9% (p < 0.05). The failure rate of the left anterior descending artery (LAD) graft by the left ITA was 2% in cases with a single graft, 3% in cases with a sequential graft, 3% in cases with a bilateral in situ ITA graft technique, and 7% in cases with a bilateral ITA grafting using Y technique (p > 0.05; 1-ß < 50%).

Failure rates according to the right or the left ITA used and according to the coronary artery bypassed are displayed in Table 2.


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Table 2. Graft Patency According to Internal Thoracic Artery Used and Coronary Artery Grafted

 
Causes of threadlike internal thoracic artery
The causes of the threadlike ITAs are displayed in Table 3.


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Table 3. Causes of Threadlike Internal Thoracic Artery

 
Competitive flow was the cause of threadlike ITA in 14 cases. In eight cases, proximal stenosis of the native coronary artery had been overestimated on the preoperative coronary angiography. The first estimation of the stenosis was more than 70%, but when it was reevaluated, the stenosis proved to be less than 60%. In four cases, the degree of stenosis decreased after surgery; significant preoperative angiographic stenosis became nonsignificant in the follow-up coronary angiography. Steal phenomenon is the cause of threadlike ITA in two cases because of a patent nonligated proximal branch of the ITA.

The rate of threadlike ITA related to competitive flow graft was greater when the graft was anastomosed to the circumflex artery branches (CX) (6%) than when the graft was anastomosed to the LAD (2%; p < 0.05). The rate of threadlike ITA relative to poor recipient coronary arterial bed (Fig 2) was greater when the graft was anastomosed to the CX (3%) than when the graft was anastomosed to the LAD (0%; p < 0.05).



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Fig 2. Failure of an internal thoracic artery graft. (CX = circumflex artery branch with poor recipient coronary arterial bed; ITA = threadlike right internal thoracic artery.)

 
There was not significant anastomotic stenosis in our study. There were seven anastomoses with a stenosis less than 50%. There were four cases of kinking: one in the ITA graft proximal to each anastomosis in a triple sequential graft and one along the course of the left ITA graft of the LAD. All these anastomoses were classified as having perfect patency.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Limits of the study
This study is based on a pool of follow-up coronary angiographies extracted from several previous prospective studies [58] performed to evaluate new techniques: single left ITA grafting, sequential anastomosis with the left ITA, and bilateral in situ ITA grafting and Y technique. These techniques represent the milestones of our practice. The method of evaluation in all these series was the 1-year follow-up angiography of the ITA grafts. Patients in each series were consecutively operated on; 80% of the patients were angiographically assessed (in a few cases angiography was refused by the patient or medically contraindicated). Clinical results are not involved in this study, which is focused on the causes of angiographic graft failure.

In our study, each group consists of small number of cases. The power of the statistical tests is not sufficient to give indisputable conclusions when we find a p greater than 0.05. However, the failure rate of the ITA graft is small. Thus, a large series of follow-up coronary angiography, which is not available in the literature, is needed to form solid conclusions about comparisons of patency rates of different ITA grafts. Our conclusions can be considered valuable because there are not enough data on this topic in the literature.

Threadlike ITA and occluded ITA are considered ITA graft failures. A threadlike ITA is a patent graft but is not functioning; on the follow-up coronary angiography, the dye opacifies the ITA but does not opacify the grafted coronary artery. The percentage of ITA occlusion (2%) and that of threadlike ITA (4%) are similar to the published data [1, 2, 4]. The causes of graft failure can be related to anatomic and technical factors.

Anatomic factors of internal thoracic artery failure
The ITA is rarely affected by arteriosclerosis [11]. It is a reactive conduit that adapts its flow to the recipient blood flow demand [12]. This flow relies on the blood pressure, the recipient coronary arterial bed, and the remaining native artery blood flow. However, ITA failure related to significant stenosis of the supplying subclavian artery has been described [4]; this cause did not occur in our series. Subclavian arteries were routinely injected during the preoperative coronary angiography.

Despite the fact that right and left ITAs have the same histologic structure, in our study overall left ITA patency is greater than that of the right ITA (p < 0,05). Some authors published the same results [13, 14]; others did not find any differences [15]. In our series, the right ITA was anastomosed more often to the CX than to the LAD (p < 0.05). Regardless of whether the left or right ITA was used, the failure rate is higher when the graft is anastomosed to the CX than to the LAD (Table 2). We can postulate that the difference of failure rate between the left and right ITAs was mainly owing to the nature of the coronary artery grafted.

The LAD grafting with ITA (left or right) gives better results than the CX grafting (p < 0.05). This has been also reported for venous grafts [16]. This could be related to the following factors: greater risk of technical defect with the CX than with the LAD (difficulties of exposure, need of longer ITA graft, and smaller diameter of the ITA at this level, greater risk of axial twist), and smaller diameter of the CX.

Surgical technique factors of internal thoracic artery failure
In our series the rate of competitive flow is 2% (2 of 115) in cases of single in situ left ITA anastomosis, 2.5% (4 of 159) in cases of sequential graft, and 3% (4 of 137) in cases of bilateral ITA grafting using Y technique (p > 0.05; 1-ß < 50%). Hence, increasing the number of anastomoses per ITA does not seem to increase the risk of graft failure relative to competitive flow.

When using the Y technique, the failure rate of the ITA graft is higher than the failure rate of the single in situ left ITA graft (p < 0.05). This can be related to the fact that the CX had been bypassed in each case in the series of Y technique (100%). The rate of CX grafting with the single left in situ ITA was only 12% (p < 0.05).

The follow-up coronary angiography revealed that the rate of anastomotic defect is low: only seven nonsignificant stenosis and four cases of kinking. These surgical defects did not affect the graft function; in these cases, the ratio of ITA diameter to the grafted coronary artery diameter is more than 1, which indicates perfect ITA graft patency. The careful technique we used to perform anastomosis could explain this good result. To avoid surgical trauma, arterial walls were never grasped with the surgical forceps (no-touch technique). The angle of landing of the ITA onto the coronary vessel was always less than 30 degrees; an angle greater than 90 degrees is a cause of anastomotic stenosis [17]. The length of the anastomosis was 8 to 10 mm, and the time required to perform each anastomosis was, on average, 15 minutes. Finally, human fibrin glue was used to fix the graft in a suitable position to avoid subsequent graft folding or kinking.

Follow-up coronary angiography can reveal anastomotic defects but cannot analyze the causes of ITA graft occlusion. It is well acknowledged that technical mistakes during ITA harvesting are important factors of ITA graft occlusion. These mistakes include excessive use of electrocoagulation, which damages the ITA wall; thermal conduction through the metallic clips that burns the artery wall; and excessive traction on the ITA collateral branch, which can provoke intimal tear and subsequent intimal dissection [18]. Direct intravascular injection of papaverine solution to avoid ITA spasm [9] can also damage the ITA intimal layer [19].

Causes of threadlike internal thoracic artery
A high level of residual blood flow supplied by the native coronary artery causes competitive flow. The flow in the ITA decreases according to the degree of native artery competitive flow. In response, the ITA decreases its diameter and becomes threadlike. The main cause of competitive flow is a low degree of proximal coronary artery stenosis less than 60% [20, 21]. In our study, overestimation of proximal coronary stenosis is the most frequent cause (60%) of threadlike ITA related to competitive flow. The rate of competitive flow is greater in grafting involving the CX than the LAD (p < 0.05). It appears to be more difficult to estimate stenosis of the CX. Measurement of the fractional flow reserve [22] could theoretically reduce the number of these cases of threadlike ITA and would prevent overestimation of coronary stenosis. At the time when follow-up coronary angiographies were performed, that test was not practiced in our center. However, some studies proved that some of these noncritical lesions with time became significant with subsequent reenlargement of the diameter of ITAs resulting in reversal of the threadlike ITA phenomenon [23, 24].

Four cases of threadlike ITA with competitive flow had occurred owing to the spontaneous decrease of the degree of stenosis in the postoperative period. Atheromatous plaque regression and lysis of thrombotic materials proved to be the cause of this spontaneous regression of the degree of stenosis [25].

We had two case of combined threadlike ITA and patent nonligated proximal branches of the ITA. Patent nonligated proximal branches of the ITA as a cause of threadlike ITA remains an issue of controversy [26]. Stolen flow owing to the nonligated collateral branch of the ITA could cause threadlike distal ITA, or threadlike ITA could provoke dilatation of nonligated collateral branch of the ITA. In 1 patient in our study, proximal native coronary artery stenosis was critical and the nonligated ITA proximal branch was believed to be the only obvious cause of threadlike ITA. In another patient, the native coronary stenosis was only 60% and a native competitive coronary blood flow could be involved.

In four cases of threadlike ITA, the diameter of the recipient coronary arterial bed was less than 1 mm (Fig 2). Although in these cases the ratio of ITA to coronary artery diameter was 1, the low flow in the ITA graft was not sufficient to allow its enlargement. When the recipient coronary arterial bed is thin with a small dependent myocardial mass, the ITA blood flow is low and the ITA graft adapts its diameter to this low flow demand and decreases its diameter, resulting in threadlike ITA [12].

Conclusions
The rate of ITA graft failure is low in our study depending on the analysis of the 17-month follow-up angiographic findings. Although this rate of ITA graft failure is too small to make an accurate statistical analysis, we can state that sequential anastomosis and Y reimplantation of the right ITA into the left ITA do not seem to decrease the patency rate of LAD grafting with the left ITA.

The failure rate of the ITA graft anastomosed to the LAD is less than that of the CX. This fact is because of the higher incidence of competitive blood flow and the higher incidence of bad recipient coronary arterial bed in cases of CX grafting.

Finally, among 30 cases of ITA graft failure, only four cases of threadlike ITAs owing to competitive flow because of regressed coronary stenosis were unavoidable. All other cases of ITA graft failure are the result of preventable human factors.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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