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Ann Thorac Surg 2008;85:71-79. doi:10.1016/j.athoracsur.2007.08.026
© 2008 The Society of Thoracic Surgeons
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Original Articles: Cardiovascular

Coronary Collateral Circulation: Effect on Early and Midterm Outcomes After Off-Pump Coronary Artery Bypass Surgery

Massimo Caputo, MD*,*, Rafik R. Anis, MD*, Chris A. Rogers, PhD, Nazir Ahmad, MRCP, Syed I.A. Rizvi, MRCS, Andreas Baumbach, MD, FESC, Karl R. Karsch, MD, FRCP, Gianni D. Angelini, FRCS, Martin Oberhoff, MD, FESC

Bristol Heart Institute, Bristol Royal Infirmary, Bristol, United Kingdom

Accepted for publication August 13, 2007.

* Address correspondence to Dr Caputo, Bristol Heart Institute, Bristol Royal Infirmary, Bristol, BS2 8HW, United Kingdom (Email: m.caputo{at}bris.ac.uk).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Background: The purpose of this study was to assess the prognostic effect of coronary collaterals on early and midterm clinical outcomes in patients undergoing first time isolated off-pump coronary artery bypass (OPCAB) surgery.

Methods: Preoperative angiograms from 861 patients were evaluated to assess the presence and extent of coronary collaterals (Rentrop classification). Coronary collaterals (CC) were present in 485 (56.3%) patients (CC group). Patients with coronary collaterals had a higher incidence of preoperative myocardial infarction, lower ejection fraction, and higher Parsonnet scores compared with patients without coronary collaterals (no-CC group).

Results: Coronary collaterals were associated with myocardial protection during OPCAB surgery, as evidenced by a significantly lower incidence of intraoperative ST-segment changes (propensity matched cohort, p = 0.008). No other statistically significant differences in in-hospital outcomes were detected between the two groups. Five years after surgery patient survival was 84.8% (95% confidence interval [CI] 79.4 to 88.8) in the CC group compared with 89.2% (95% CI 84.4 to 92.6) in the no-CC group (p = 0.48). Cardiac-related event-free survival after 5 years was 50.6% (95% CI 43.5 to 57.3) in the CC group and 54.5% (95% CI 47.1 to 61.4) in the no-CC group (p = 0.96), with no significant differences between both groups, before or after risk adjustment, or when comparing propensity-matched cohort.

Conclusions: Although patients with coronary collaterals had more extensive coronary artery disease, poor left ventricular function, and more cardiac risk factors than patients without collaterals, the early and midterm clinical outcome after OPCAB surgery was comparable between the two groups.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Coronary collaterals play an important role in maintaining viable myocardium after abrupt coronary artery occlusion, and they are a primary determinant of left ventricular function recovery after myocardial infarction (MI) and reperfusion [1, 2]. Shimizu and colleagues [3] found a correlation between the presence of angiographic evidence of coronary collaterals and regional recovery of myocardial function in patients with good left ventricular function undergoing off-pump coronary artery bypass (OPCAB) surgery. Similarly, Kozman and colleagues [4] demonstrated that in patients with severe left ventricular dysfunction, the presence of well-developed coronary collaterals on the preoperative coronary angiogram is a sensitive predictor of left ventricular functional recovery after OPCAB surgery. Antoniucci and colleagues [5] have recently demonstrated a lower mortality rate in patients with coronary collateral circulation compared with patients without well-developed coronary collaterals, six months after primary angioplasty or stent implantation for acute MI. However, studies in which presence and degree of coronary collaterals are investigated as prognostic determinants of clinical outcomes after OPCAB surgery are hardly available.

As the popularity of OPCAB surgery has increased in recent years, it is very important to analyze the relationship between coronary collaterals and clinical outcomes. Nathoe and colleagues [6] have recently reported a lower incidence of perioperative MI and better one-year event-free survival in patients with coronary collaterals undergoing OPCAB surgery; however, this study included a small number of selected patients, which might be representative of the overall OPCAB population. The aim of our study is therefore to assess the significance of preoperative angiographic evidence of coronary collaterals in patients undergoing first time isolated OPCAB surgery, and its prognostic role in relation to early and midterm clinical outcomes.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Patient Selection and Data Collection
This retrospective study analyzed data for 861 patients who underwent first time isolated OPCAB surgery between April 1996 and December 2002 at the Bristol Royal Infirmary. Data came from four sources: (1) an institutional database of preoperative characteristics, surgical information, and in-hospital outcomes, including complications and adverse events, collected prospectively on all cardiac surgery patients treated in our unit (Patient Analysis & Tracking Systems: Dendrite Clinical Systems, London, UK); (2) death registration from the UK National Strategic Tracing Service (NSTS); (3) information about cardiac-related events from a postal questionnaire to patients and to their family physicians; and (4) review of the preoperative coronary angiograms. In-hospital death was defined as any death occurring during the same hospital admission for surgery [7, 8]. At the time this study was conceived, ethical approval for retrospective data-based studies such as this was not required in the UK. However, the study was approved by the departmental review committee. It was not possible to gain consent from all patients to use their data as part of this study (many were no longer living) but all those who returned a follow-up questionnaire gave explicit consent. Patients who state that they do not want their data included in any retrospective analysis are excluded (<0.3%).

Anesthetic, Surgical Technique, and Postoperative Management
Anesthetic technique, method of exposure, and stabilization for performing anastomoses during OPCAB surgery have been described previously [9]. Preconditioning was not used. The left anterior descending coronary artery (LAD) was grafted first in the majority of patients and the proximal anastomosis was constructed at the end. In order to detect signs of ischemia intraoperatively, continuous 12-lead electrocardiogram changes were monitored during the construction of the anastomosis and ST-segment changes were recorded. After surgery, patients were transferred to the intensive therapy unit and managed according to the Unit protocol [7, 8]. Clinical diagnostic criteria for perioperative MI were Q-waves greater than 0.04 ms and(or) a reduction in R waves greater than 25% in 2 or greater leads; MB isoenzyme creatinine kinase (CK-MB) and troponin values were not available. Low cardiac output syndrome and need for inotropic support were defined according to the Unit protocol [7, 8].

Patient Follow-Up After Hospital Discharge
Deaths after hospital discharge were obtained from National Health Service Strategic Tracing Service (NSTS) in January 2005 and 99.4% of the study cohort was successfully matched to the NSTS database. Because most deaths are reported to NSTS within two months of the event, the survival time was calculated from the date of surgery to October 31, 2004 for surviving patients. For the five patients who could not be traced through NSTS, the survival time was censored at hospital discharge.

Annual follow-up was by postal questionnaire, sent to patients and their family physician [10]. Reminders were sent to nonresponders. Nonfatal cardiac-related events included the following: (1) the need for a further coronary revascularization procedure (whether reoperation or percutaneous coronary intervention [PCI]); (2) patient-reported hospital attendance for MI, coronary angiography, congestive heart failure, or recurrent angina; (3) Canadian Cardiovascular Society class 3 or 4; (4) report of cardiac-related hospital admission by the family physician. These criteria for cardiac-related events are similar to those used previously to validate the accuracy of reporting of events by patients and their family physicians [10]. Patients free from cardiac-related events were censored at last follow-up.

Coronary Angiography, Coronary Artery Lesion, and Coronary Collateral Assessments
Preoperative coronary angiograms were evaluated at the same time by two experienced cardiologists blinded to the results of the OPCAB surgery. The degree of coronary narrowing was determined by visual assessment from a review of at least two orthogonal views of each coronary artery. Coronary artery stenosis was graded as significant if the lumen is narrowed greater than 50% in the left main coronary artery and greater than 70% in the other coronary arteries. Each of the three epicardial arteries (LAD, circumflex [CX], right coronary artery [RCA]) was divided into proximal, middle, and distal segments and each segment was analyzed using the following criteria: 0, normal; 1, lesion occludes less than 50% of the coronary artery lumen; 2, lesion occludes 50 to 70% of the coronary artery lumen; 3, lesion occludes greater than70% of the coronary artery lumen; and 4, total occlusion of the artery. Lesions in diagonal-1 (D1) and diagonal-2 (D2) were considered with LAD group lesions. Similarly, lesions in the obtuse marginal branch-1 (OM1) and obtuse marginal branch-2 (OM2) were considered with CX group lesions. Lesions in the posterior descending artery (PDA) and ventricular artery were considered with the RCA group lesions.

Coronary collaterals were graded according to Rentrop classification [11]: 0 = no visible collaterals, 1 = collateral filling of the vessel branches without reaching the epicardial artery, 2 = partial filling of the epicardial artery, and 3 = complete filling of the epicardial artery. The presence of coronary collaterals was evaluated for each of the three major epicardial arteries (LAD, CX, and RCA) [11]. Collateral circulation was assessed for each segment (proximal, middle, and distal) of each epicardial artery. Patients were divided into a group with angiographic evidence of coronary collateral flow; "CC group," where Rentrop score was 1 or greater and a group in which coronary angiography did not show any coronary collateral flow, and "no-CC group" (Rentrop score = 0).

Statistical Analysis
Data are reported as number and percentage (categoric data), mean and standard deviation (normally distributed continuous variables), or median and interquartile range (continuous variables with a skewed distribution). Baseline characteristics were compared using the {chi}2 or Fisher exact tests (categoric variables) or the Wilcoxon rank sum test (continuous or discretely measured variables). The effect of coronary collaterals on in-hospital outcomes and 5-year survival was assessed using standard regression methods: logistic regression for binary variables and Cox proportional hazards regression for time to event variables. The proportional hazards assumption was checked by testing for a nonzero slope in a generalized regression of the scaled Schoenfeld residuals of time. Survival curves were constructed using the Kaplan-Meier method.

The effect of coronary collaterals is reported with and without adjustment for differences in preoperative risk factors (demographic and cardiac factors, and comorbidity). These potential confounding variables included those that showed imbalance between the CC and no-CC groups plus risk factors for early postoperative mortality and morbidity, which were specified in advance of the analysis. Missing preoperative data were imputed using the median (continuous measures) or mode (category measures). Except for aspirin (13% missing) and body mass index (2% missing), data were missing for less than 0.5% of cases.

Analyses comparing outcomes for the CC group and a propensity score-matched group of no-CC patients, were also carried out. Patient and operative variables included in the adjusted analyses were used to calculate the propensity score. Clinically plausible interactions were not prespecified and so were not included. Fractional polynomials were used to assess the functional form for continuous measures. There was no evidence to suggest higher order terms were needed. A greedy algorithm with hierarchical nearest available pair matching was used to select the propensity-score matched pairs of CC and no-CC patients. Best matches, those with five matching digits on propensity score, were selected first. Those that remained were then matched on 4 digits of the propensity score. This continued down to a 1-digit match on propensity score. If more than one unmatched CC patient matched to a no-CC patient, the CC patient was selected at random. Robust standard errors, clustered by matched pair, were used to account for the propensity matching in the analyses.

Our interpretation of the findings is based on the consistency of the findings and their magnitude as well as their statistical significance. Results are reported as effects sizes (odds ratios or hazard ratios) with 95% confidence intervals and associated p values. Analyses were carried out using Stata version 8.2 (Stata Corporation, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 
Coronary angiography, carried out for all 861 patients studied at the Bristol Royal Infirmary, were retrieved and evaluated for the presence and extent of coronary collateral circulation. Collaterals were present in 485 patients (56.3%). The preoperative and operative characteristics are described in Table 1. Patients with coronary collaterals had a significantly higher incidence of previous MI, insulin-dependent diabetes, lower ejection fraction, and overall higher Parsonnet scores compared with patients without collaterals. They also had more extensive coronary artery disease, with a greater proportion of patients with double and triple vessel disease; over 80% of patients in the CC group had complete occlusion in at least one vessel compared with less than 15% in the no-CC group. Lesions in the LAD territory were predominant in both groups (88% and 93% in the no-CC and CC groups, respectively; p = 0.02), while patients with coronary collaterals presented with a higher incidence of CX/RCA stenosis 50% or greater (CX/RCA: 69%/79% in the CC group vs 55%/58% in the no-CC group; p < 0.001). Overall, 88% of patients in the CC group had filling of an epicardial artery with Rentrop score greater than 1; 39% had LAD collaterals, 56% had RCA collaterals, and 13% had CX collaterals. In the group with LAD collaterals, 68% were partially filled, whereas in the group with RCA collaterals almost 60% had complete filling of one or more segments of the RCA. Similar numbers of patients with collaterals to the CX had partial and complete filling of one or more segments. Half of the patients in the CC group had coronary collaterals from the RCA to LAD/CX.


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  		Table 1 Baseline Characteristics and Operative Details
 
The frequencies of several short-term/in-hospital outcomes for the CC and no-CC groups are described in Table 2. The effect of the presence of coronary collaterals on these outcomes, both unadjusted and adjusted for prognostic factors and after matching on propensity scores, are shown in Table 3. A total of 313 propensity score matched pairs were identified. For the remaining 63 no-CC patients no suitably matched CC patient could be found. The propensity model fitted the data well (test for lack of fit by decile, p = 0.52) and showed moderate discrimination (c-statistic = 0.68). Patient and operative characteristics were similar across the two propensity-matched groups (see Table 1). The number of diseased vessels in the two propensity-matched groups was similar, although due to the significant imbalance in the complete cohort the number of occluded vessels remained imbalanced between the groups. The adjusted analysis indicates that the presence of coronary collaterals was associated with a significantly lower incidence of intraoperative ST-segment changes. No other significant differences in in-hospital outcome were detected between the two groups. The propensity-matched analysis also suggested that the incidence of intraoperative ST-segment changes was significantly lower among the CC patients (Tables 2; 3).


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  		Table 2 Clinical Outcomes
 

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  		Table 3 Unadjusted and Adjusted Risk of In-Hospital and Midterm Outcomes in Relation to the Presence of Collaterals
 
Follow-up data was available for 730 patients, which, excluding those who died before follow-up commenced, represent 90.1% of the eligible study cohort. Of the 80 eligible patients who failed to respond, 7 have since died, 2 refused to participate, 1 cannot be traced, and 70 patients (8.1% of the total cohort) remain alive and not contacted. The median duration of follow-up of survivors was 3.7 years in the CC and 3.8 years in the no-CC group. Patient survival to 5 years is illustrated in Figure 1; over 90% of patients in both groups remained alive 3 years after surgery and more than 80% were alive at 5 years (Table 2). Survival to 5 years did not differ significantly between the two groups when compared with or without adjustment for potentially confounding factors or when comparing propensity-matched groups (Table 3). For the subgroup of patients with a previous MI or low ejection fraction (386 patients, 64% with CC), the unadjusted risk of death was greater for those with CC (hazard ratio [HR] = 2.19, 95% CI 0.98 to 4.89, p = 0.055); after risk adjustment and when comparing propensity-matched patients the survival difference was reduced and nonsignificant (adjusted HR = 1.63, 95% CI 0.56 to 4.71, p = 0.37; propensity-matched HR = 1.30, 95% CI 0.547 to 2.93, p = 0.53).


Figure 1
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  		Fig 1. Kaplan-Meier curves showing the observed cumulative percentage of patients with or without coronary collaterals who died with increasing duration from the time of operation.

 
Overall, 193 patients reported one or more nonfatal cardiac-related event during the follow-up. For a further 68 discharged patients death was the first event. Details of the cardiovascular events reported during the follow-up, both in total and as the first event, are shown in Table 4. The most common event, reported by more than 15% of patients in both groups, was recurrent angina not requiring hospital reattendance; less than 7% of patients visited hospital after surgery for recurrent angina. Cardiac-related event-free survival to 5 years is illustrated in Figure 2; after 3 years, fewer than 30% of patients in both groups had died or experienced an event and at 5 years this had increased to almost 50%. No statistically significant differences in cardiac event-free survival were found between the two groups, with or without adjustment for potentially confounding factors or when comparing propensity-matched groups (Table 3).


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  		Table 4 Cardiac-Related Events up to 5 Years After Surgery
 

Figure 2
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  		Fig 2. Cardiac event-free survival. Kaplan-Meier curves showing the observed cumulative percentage of patients with or without coronary collaterals who died or experienced one or more cardiac-related event(s) with increasing duration from the time of operation. (— = no collaterals visible; --- = collaterals visible.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 
Coronary collaterals are recruited mainly by prolonged periods of ischemia [1–5]. They play a crucial role in protecting the myocardium in patients with coronary artery disease by providing an alternative blood supply when the original blood vessel fails to provide a sufficient blood flow [1–5]. Indeed, several studies in patients with acute MI have shown the importance of coronary collaterals in minimizing the infarct area and extending the period of time available until coronary reperfusion is carried out [1, 2, 5, 12]. However, studies investigating the effect of coronary collaterals as prognostic determinants of early and long-term clinical outcomes are few, especially after OPCAB surgery.

This study involves a large number of patients to evaluate the effect of coronary collaterals on early and long-term clinical outcomes after OPCAB surgery. Our study suggests that, in an unselected group of patients undergoing OPCAB surgery, coronary collaterals are an indicator for a patient population with lower ejection fraction, more extensive coronary artery disease, and an overall worse risk profile than patients without coronary collaterals. Nathoe and colleagues [6] have recently shown a protective effect of coronary collaterals against perioperative MI (defined by a MB to creatinine kinase ratio [CK-MB] >10%) and better 1-year event-free survival in patients undergoing OPCAB surgery. The small selected group of patients (142 in total) and the short follow-up (1 year) might explain why their results appear to differ from our findings. One of the benefits of coronary collaterals identified in our study was the decreased incidence of intraoperative ST-segment changes while constructing the distal anastomosis, which supports the hypothesis that coronary collaterals protect the myocardium against ischemic stress. However, this intraoperative protection was not associated with a decreased incidence of perioperative events. The incidence of perioperative events in our study is much lower than that by Nathoe and colleagues [6], probably due to the different definitions used in the two studies. Antonucci and colleagues [5] have recently demonstrated an early and long-term protective role of coronary collaterals after coronary revascularization in patients undergoing primary angioplasty or stent implantation for acute MI. The differences observed between these reports and our study are probably due to the fact that, by using intracoronary shunts during the anastomosis, the intraoperative ischemic and hemodynamic problems are avoided [13–17]. Also, the need for repeated interventions is lower after OPCAB surgery than after PCI, due to the completeness of revascularization.

Myocardial protection and less ischemic stress during the OPCAB surgery is an advantage provided by CC in the CC-group; this advantage is confirmed by the study. However, as the study population is highly selected, because all patients had clinical and anatomic conditions that required coronary artery bypass surgery, this means that coronary collateral development by definition was not sufficient to prevent myocardial ischemia. Thus, the characteristics of this population, more than coronary collateral, per se, may explain the absence of differences in early and midterm clinical outcome between patients with coronary collateral and patients without coronary collateral. Although this is one of the largest series to compare outcomes after OPCAB surgery for patients with and without coronary collaterals, the power to detect statistically significant differences was low as the events were few, especially for in-hospital outcomes.

Limitations
The distribution of prognostic factors in the CC and no-CC groups indicates that the no-CC patients had fewer preoperative risk factors. Patients with coronary collaterals had more extensive coronary artery disease, evidenced by the more severe stenosis of the coronary arteries (LAD, CX, or RCA), higher incidence of previous MI, and a lower ejection fraction than the no-CC group patients. The similar long-term clinical outcome for the CC and no-CC group patients could be explained by the protective effect of coronary collaterals despite of the presence of negative prognostic risk factors. Multivariable regression analysis and comparisons of propensity-matched groups can never entirely account for imbalances between the groups, and the estimates of the effect of coronary collaterals may still be subject to some residual confounding.

Other limitations are (1) that diagnosis of perioperative myocardial infarction was based only on electrocardiogram criteria with no corroboration with biochemical tests (CK-MB, troponin), and (2) that we were unable to include patients for whom the preoperative angiogram was unavailable. These were mostly patients referred from other hospitals who had their angiogram locally.

Finally, coronary angiography is not considered as a gold standard for the assessment of the effectiveness of coronary collateral. Angiographic collateral circulation is weakly related to the function of the microvessel network. Coronary angiography visualizes collateral vessels of greater than100 µm diameter [18] and, as many coronary collaterals are smaller than this, they are not visualized by coronary angiography. This fact may explain, at least in part, the absence of differences in clinical outcome between patients with angiographic evidence of coronary collateral and patients without angiographic evidence of coronary collateral.

Conclusion
Although patients with coronary collaterals had more extensive coronary artery disease, poor left ventricular function, and more cardiovascular risk factors, the short and midterm clinical outcomes after first time isolated OPCAB surgery were similar to patients without coronary collaterals who had a better cardiovascular profile.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 
This work was supported by the British Heart Foundation, Garfield Weston Trust.


   Footnotes
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 
* The first and the second authors contributed equally to the study. Back


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 

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  6. Nathoe HM, Buskens E, Jansen EWL, et al. Role of coronary collaterals in off-pump and on-pump coronary bypass surgery Circulation 2004;110:1738-1742.[Abstract/Free Full Text]
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  8. Angelini GD, Taylor FC, Reeves BC, Ascione R. Early and midterm outcome after off-pump and on-pump surgery in Beating Heart Against Cardioplegic Arrest Studies (BHACAS 1 and 2): a pooled analysis of two randomised controlled trials Lancet 2002;359:1194-1199.[Medline]
  9. Watters MP, Ascione R, Ryder IG, Ciulli F, Pitsis AA, Angelini GD. Haemodynamic changes during beating heart coronary surgery with the ‘Bristol Technique’ Eur J Cardiothorac Surg 2001;19:34-40.[Abstract/Free Full Text]
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  11. Rentrop KP, Cohen M, Blanke H, Phillips RA. Changes in collateral filling immediately after controlled coronary artery occlusion by an angioplasty balloon in human subjects J Am Coll Cardiol 1985;5:587-592.[Abstract]
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  14. Yeatman M, Caputo M, Narayan P, et al. Intracoronary shunts reduce transient intraoperative myocardial dysfunction during off-pump coronary operations Ann Thorac Surg 2002;73:1411-1417.[Abstract/Free Full Text]
  15. Grundeman PF, Borst C, Verlaan CWJ, Meijburg H, Moues CM, Jansen EWL. Exposure of circumflex branches in the tilted, beating porcine heart: echocardiographic evidence of right ventricular deformation and the effect of right or left bypass J Thorac Cardiovasc Surg 1999;118:316-323.[Abstract/Free Full Text]
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