Ann Thorac Surg 2007;83:120-125
© 2007 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Angiographic Fate of Collateral Vessels After Surgical Revascularization of the Totally Occluded Left Anterior Descending Artery
Yoshiyuki Takami, MD*,
Hiroshi Masumoto, MD
Division of Cardiovascular Surgery, Kasugai Municipal Hospital, Kasugai, Japan
Accepted for publication August 16, 2006.
* Address correspondence to Dr Takami, Department of Cardiovascular Surgery, Nagoya Daini Red Cross Hospital, 2-9 Myouken-cho, Showa-ku, Nagoya 466-8650 Japan (Email: takami{at}nagoya2.jrc.or.jp).
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Abstract
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BACKGROUND: Coronary artery bypass grafting (CABG) is best indicated for chronic total occlusion of the left anterior descending artery (LAD) with collaterals. We investigated angiographic changes in the collateral circulation after CABG.
METHODS: Preoperative and postoperative angiograms were reviewed in 42 patients who underwent grafting onto occluded LADs. We described the type, location, and size of collaterals, the Rentrop grading, and collateral frame count (CFC). Regional wall motion of the LAD area was also evaluated with the centerline method. Postoperatively, we measured the lengths of LAD proximal (Lp) and distal (Ld) to the graft anastomotic site.
RESULTS: Preoperative collaterals comprised 78 pathways (septal 42%, branch-branch 20%, atrial 19%, bridging 18%). After CABG, residual collaterals were identified, mainly through the septal pathways, in 6 patients (14%), most of whom were diabetic. The residual collaterals were a part of those which had been opacified in earlier phases of the preoperative angiograms (CFC: 17 ± 3 vs 25 ± 15, p = 0.01). Also, the Ld was shorter in these patients so that Lp/Ld was greater than in patients without residual collaterals (0.80 ± 0.24 vs 0.53 ± 0.28, p = 0.04). We found no association of residual collaterals with the improvement of LAD regional wall motion after CABG.
CONCLUSIONS: Even after successful CABG, some collaterals with earlier filling of the LAD remain, mainly through the septum. Although the clinical significance remains to be clarified, complex and diffuse atherosclerosis associated with more distal graft anastomoses may contribute to maintaining collaterals after CABG to the occluded LAD, especially in diabetic patients.
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Introduction
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Coronary collateral circulation may play an important role in maintaining viable myocardium after abrupt coronary occlusion [1]. The potential of individuals to develop coronary collateral circulation is of major importance in myocardial vulnerability [2]. Collaterals develop as a result of a pressure gradient across the occlusion that recruits preformed interarterial connections [3]. Percutaneous coronary intervention (PCI) serves as a useful model investigating development and regression of collateral circulation [4, 5]. Collateral vessels can regress with sufficient coronary perfusion during a relatively short period of time after successful PCI.
Even well-developed collaterals may not fully substitute normal coronary flow [6]. Chronic total occlusion (CTO) of the left anterior descending artery (LAD) with collaterals is a good indication for surgical revascularization with a left internal thoracic artery (LITA) [7]. In-situ LITA grafting to LAD has been a gold standard in coronary artery bypass grafting (CABG), with excellent long-term patency and clinical outcome [8]. In CABG, collaterals protect against perioperative myocardial infarction [9]. However, to our knowledge there have been few reports on the fate of collateral circulation after successful CABG, although collateral regression is theoretically expected. The purpose of our study was to evaluate whether collateral vessels regress completely after surgical revascularization of a CTO-LAD and to analyze the contributing factors to residual collaterals.
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Patients and Methods
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Study Patients
The study group comprised 42 consecutive patients (33 men and 9 women with a mean age ± SD of 65 ± 9 years) who underwent CABG, including grafts for CTO-LADs with collateral vessels, which were proved to be patent well in postoperative angiography. These patients received 2.5 ± 1.1 grafts and were approximately 21% of all patients who underwent CABG during the same period at our institute. Twelve patients (29%) underwent CABG without cardiopulmonary bypass. All patients underwent LITA grafting to the LAD, except for two patients using a radial artery graft and a right ITA. Written informed consent was obtained from each patient. This retrospective study was approved by the Institutional Review Board.
Angiographic Analysis of Collateral Vessels
Selective coronary angiography was performed by the Judkins technique using a 4 or 5 Fr catheter both preoperatively and postoperatively (14 ± 3 days after CABG). The angiograms were recorded at 30 frames per second in multiple projections and stored on digital media in Digital Imaging and Communications in Medicine format (512 x 512 matrix).
The collateral pathway anatomy was categorized as proposed by Rockstroh and Brown [10]: septal (SE), atrial (AT), branch-branch in ventricular free walls (BR), and bridging across lesions (BL). The arterial sources were classified anatomically as follows: left circumflex (CX); diagonal (DX); acute margina (AM)l; atrioventricular nodal branch (AV); and posterior descending branch (PD) of the right coronary artery (RCA). The size of collaterals was graded as discontinuous (size 0), continuous connection just visible (size 1, 0.1 to 0.3 mm), continuous of small side-branch size (size 2, 0.4 to 0.5 mm), and large (size 3, >0.5 mm). The grading of the collateral size was confirmed by a caliper measurement of the minimum diameter of the collateral when it appeared maximally filled using computer-assisted analyzing software (CCIP-310/W, CATHEX Co, Tokyo, Japan). Collateral circulation was also graded according to the classical criteria of Rentrop and colleagues [11] as follows: grade 0 = no filling; grade 1 = filling of side branches only, without visualization of the epicardial segment; grade 2 = partial epicardial vessel filling by collaterals; and grade 3 = complete epicardial vessel filling by collaterals. To quantify the collateral fillings, the collateral frame count (CFC) was used, which is the number of cine-frames required for contrast media to reach the recipient vessel [12]. The first frame was defined as that frame in which dye extends across greater than 70% of either donor artery. The last frame counted was defined as the frame in which dye first enters the recipient epicardial artery; complete opacification of the recipient artery was not required, only initial entry of dye into the recipient artery. Thus, the last frame was the very next frame in which the recipient vessel reappeared. Because the last frame is more easily determined, the initial opacification of the recipient artery was identified first and then we moved frame by frame in reverse order until the donor artery appeared.
Postoperative Quantitative Graft Angiography
A dose of 2 mg isosorbide dinitrate was injected before the contrast agent selectively in each bypass graft. All grafts were examined from at least three different views. Especially, the graft to the CTO-LAD was observed in detail in a 60 degree left anterior-oblique view. Using the computer-assisted analyzing software (CCIP-310/W), the length of the LAD opacified with the graft injection was measured to determine the segment proximal to the anastomosis site (Lp) and that distal to the anastomosis (Ld) by calibrating with the diameter of the catheter used, as illustrated in Figure 1.
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Fig 1. Measurement of the length of the left anterior descending artery (LAD) in the postoperative angiogram of the graft injection with contrast medium. In a 60 degree left anterior-oblique view, the segmental lengths proximal to the anastomosis site (Lp) and distal to the anastomosis (Ld) are measured by calibrating with the diameter of the catheter used.
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Quantitative Left Ventriculography
The left ventriculogram in a 30 degree right anterior-oblique view was obtained in all patients at the time of the angiography. The left ventricular (LV) chamber volume was determined with the area-length method, from which the ejection fraction (EF) was calculated. The regional LV function was analyzed using the centerline method [13]. A computer generated the centerline between the systolic and diastolic contours, and 100 equally spaced chords were drawn perpendicular to the centerline. The measured motion of each chord was normalized for heart size by dividing it by the length of the end-diastolic perimeter and then expressed in terms of SD units above or below the normal mean motion of chords. To evaluate the regional function of the LAD area, we calculated the mean chord shortening within the LAD region between chord number 10 and 58, which were expressed as standard deviations per chord (SD/CD).
Statistical Analysis
All data were expressed as means ± SD. The patients were classified into two groups depending on the presence of residual collateral vessels in the postoperative coronary angiography; group A with collaterals disappeared and group B with residual collaterals. To compare the two groups, we used the Fisher exact test for analysis of discrete variables and the Mann-Whitney U test for analysis of continuous variables. A p value of less than 0.05 was considered to be statistically significant.
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Results
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Preoperative Collaterals
A total of 78 collateral pathways to the CTO-LAD were observed in the preoperative angiography. An average of 1.9 ± 0.6 pathways were identified in each patient. The principal pathways were SE in 42%, BR in 20%, AT in 19%, and BL in 18%, as shown in Table 1. The most frequent distribution was SE/PD. The mean size of Rockstroh was 1.5 ± 0.9 and the mean grade of Rentrop was 1.9 ± 0.8. The CFC of Gibson was 25.4 ± 15.5.
Surgical Outcomes
There were no perioperative deaths, therefore all patients underwent postoperative angiography. Although 34 patients (86%) complained of angina pectoris preoperatively, no patients had symptomatic angina or showed any ischemic changes on the stress electrocardiograms. Therefore, no patients underwent additional PCI procedures immediately after CABG. Postoperative angiography revealed that the graft patency rates were 100% in the grafts onto the CTO-LADs and 97% in the grafts onto the other coronary arteries; 100% (2 of 2) in ITA, 100% (28 of 28) in radial, 86% (6 of 7) in gastroepiploic, and 96% (26 of 27) in saphenous vein, respectively.
Postoperative Collaterals
By coronary angiography, the collateral circulation to the LAD disappeared after CABG in 36 patients (group A, 86%). Figure 2
shows the preoperative and postoperative angiograms in a 68-year-old male patient whose collateral vessels to the LAD disappeared after CABG with LITA-LAD grafting. The preoperative coronary angiograms showed two pathways of collaterals to the CTO-LAD: branch-branch one from the CX (BR/CX, size 3, grade 3, CFC 13) and atrial one from the AM of RCA (AT/AM, size 2, grade 2, CFC 19). These collateral pathways disappeared completely in the postoperative angiograms. In contrast, residual collateral vessels were identified after CABG in six patients (group B, 14%), SE/PD in five patients, and BR/PD in one patient. [Figure 3
shows angiograms in a 74-year-old male patient whose collaterals to the LAD did not disappear after CABG. The preoperative angiograms showed three pathways of collaterals: septal one from the PD of RCA (SE/PD, size 2, grade 2, CFC 17), branch-branch one from the PD (BR/PD, size 3, grade 3, CFC 15), and atrial one from the AM (AT/AM, size 1, grade 2, CFC 25). In the postoperative angiograms, a part of the SE/PD pathway remained, while other pathways disappeared.
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Fig 2. Angiograms in a 68-year-old male patient whose collaterals to LAD disappeared after coronary artery bypass grafting. The preoperative coronary angiograms show two pathways of collaterals (arrows): branch-branch one from CX (size 3, grade 3, CFC 13) and atrial one from AM of RCA (size 2, grade 2, CFC 19). These collateral pathways disappeared completely in the postoperative angiograms. (AM = acute marginal branch; CFC = collateral frame count; CX = left circumflex artery; LAD = left anterior descending artery; LCA = left coronary artery; LITA = left internal thoracic artery; OM = obtuse marginal branch; RA = radial artery; RAO = right anterior-oblique view; RCA = right coronary artery.)
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Fig 3. Angiograms in a 74-year-old male patient whose collaterals to LAD did not disappear after coronary artery bypass grafting. The preoperative angiograms show three pathways of collaterals (arrows): septal one from the PD of RCA (size 2, grade 2, CFC 17), branch-branch one from the PD (size 3, grade 3, CFC 15), and atrial one from the AM (size 1, grade 2, CFC 25). In the postoperative angiograms, a part of the septal pathway from PD remained (arrow), while other pathways disappeared. (AM = the acute marginal branch; CFC = collateral frame count; LAD = left anterior descending artery; LAO = left anterior-oblique view; LCA = left coronary artery; LITA = left internal thoracic artery; PD = posterior descending branch; RAO = right anterior-oblique view; RCA = right coronary artery.)
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Contributing Factors to Residual Collaterals After CABG
To obtain the contributing factors to the residual collaterals after CABG, we compared groups A and B in terms of patient characteristics, preoperative collateral vessels, operative variables, postoperative LAD length, and SD/CD in the LAD region, as shown in Table 2. There was no difference in age, gender, left ventricle ejection fraction, history of anterior myocardial infarction, Q waves in the preoperative electrocardiography, and frequency distribution of five coronary risk factors, except for diabetes mellitus. Diabetes was significantly more frequent in group B than group A (p = 0.009). In the preoperative angiograms, there was no difference in number of pathways, Rockstroh’s size, and Rentrop’s grade of the collaterals to the LAD. However, the values of Gibson’s CFC were significantly smaller in group B than in group A (p = 0.01). Regarding the operative variables, the two groups showed no differences in frequency of off-pump CABG, graft number, mean graft flow, and postoperative myocardial enzyme release. In the postoperative graft angiography, the Lp and therefore Lp/Ld were significantly greater in group B than in group A (p = 0.04, p = 0.04). With regard to the regional wall motion of the LAD area, expressed as SD/CD, no significant differences were observed between the two groups both preoperatively and postoperatively. In each group, the SD/CD was decreased after CABG, even though the difference was not statistically significant.
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Table 2. Comparisons Between Group A With Disappeared Collaterals and Group B With Residual Collaterals After Surgical Revascularization
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Comment
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There have been few studies on the fate of collateral circulation after successful CABG, probably due to the theoretical expectation of complete regression. The main findings of this study were threefold: (1) Residual collaterals were found, mainly through the septal pathways, in 14% of patients, most of whom were diabetic, undergoing successful CABG to the CTO-LAD; (2) the residuals were a part of collaterals opacified in earlier phases of the preoperative angiogram, irrespective of their size; (3) in the patients with residual collaterals, the graft anastomosis site on the CTO-LAD was more distal than in patients with disappeared collaterals.
A recent study [7] including as many as 8,000 patients revealed that CTO was found in 52% of patients with significant coronary disease in an unselected and community-based population. Although the immediate success has improved over time, PCI of CTO remains a major challenge for cardiologists, mainly due to inability to cross the occlusion with a guidewire and higher rates of restenosis [14]. Therefore, patients with CTO are recommended for CABG or medical therapy more frequently than PCI [7]. Especially, the CTO-LAD is a good indication for CABG using LITA [8]. However, there are some obstacles to obtain more favorable revascularization of the CTO-LAD. The anastomosis site cannot be planned adequately based upon the preoperative angiograms, in which it is difficult to determine precisely the coronary pathology of the LAD opacified poorly through the collaterals, mainly in the proximal and septal parts. Therefore, the anastomosis is sometimes performed at the distal LAD, as observed in our study. More distal anastomosis, resulting in longer graft length and narrower anastomosis area, may be one of the contributing factors to residual collaterals. In addition, the CTO-LAD are usually presented with more complex and diffuse pathologic conditions, not only in the main artery but also in septal and diagonal branches. Greater CTO lesion length and diffuse coronary atherosclerosis result in the anastomosis being placed more distally into a healthier LAD. Only a simple distal graft anastomosis can not warrant complete perfusion of the LAD area. Severe atheromatous plaques can leave the septal perforators isolated from the graft perfusion to the LAD. The graft can also be placed distal to another stenosis. Such complex and diffuse disease, especially in diabetic patients, may contribute to residual collaterals through the septal pathways, as observed in this study. Although the clinical significance of the residual collaterals remains to be clarified, the results of our study may provoke the technical improvements in surgical revascularization of the CTO-LAD. As Takanashi and colleagues [15] and Fukui and colleagues [16] reported, long segmental coronary reconstruction with LITA in combination of plaque exclusion or endarterectomy may be necessary for more favorable revascularization of the CTO-LAD.
A previous study [17] demonstrated that, although angiographically not visible, collateral circulation may persist even 24 hours after successful PCI of a CTO, using myocardial contrast echocardiography that is suitable for assessment of myocardial perfusion through collateral flow. They speculated that PCI may induce direct mechanical damage to collaterals and subsequent release of vasoactive substances, resulting in microvascular dysfunction of collaterals. However, no previous studies have evaluated factors affecting the residual collaterals after PCI and CABG. Our study addresses this issue and therefore provides useful information.
One of the limitations of the present study is that it does not reveal the clinical significance of the residual collaterals after CABG. The presence of well-developed collateral circulation on preoperative coronary angiography has been found to be a sensitive predictor of LV functional recovery after CABG [18]. However, in our study, the improvement in the regional LV function was not significant in either patients with, or patients without, residual collaterals. One reason for our results may be associated with the time of postoperative evaluation. Left ventricular recovery starts within one to four weeks after CABG and is usually complete within three months [19]. We should have evaluated regional LV function four weeks or more after CABG, although it was not practical. Another reason may be related to the finding of Werner and colleagues [3] that recovery of LV function after recanalization by PCI of CTO is independent of collateral function and that regional LV recovery requires a preserved microcirculation of interarterial connections. Lower microvascular resistance in the myocardium distal to the CTO, which was not investigated in our study, is mandatory to LV functional recovery. To more precisely define the physiologic consequence of persistent collaterals, we should perform stress studies with nuclear myocardial imaging.
Another limitation of this study is that we used the semiquantitative angiographic grading of collaterals. The invasive assessment using Doppler and pressure microsensors seems superior to the angiographic assessment in order to describe collateral function as indexes of collateral and peripheral vascular resistance [20]. However, it can be performed only during PCI, and therefore we did not use it. We applied the grading based upon the recent report [21] revealing that the angiographic grading of collaterals in CTOs shows a close association with invasively determined parameters of collateral function. In addition, we incorporated CFC, proposed by Gibson and colleagues [12], into the methods for more quantitative assessment of collaterals in the angiography.
In conclusion, a part of collaterals with earlier filling of the LAD remain mainly through the septal pathways, even after successful CABG. Although the clinical significance remains to be clarified, complex and diffuse coronary atherosclerosis, associated with more distal graft anastomosis, may contribute to residual collaterals after CABG to the occluded LAD, especially in diabetic patients.
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Abstract
Introduction
