Eur J Cardiothorac Surg 2008;34:995-999. doi:10.1016/j.ejcts.2008.08.008
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
Effect of coronary artery bypass surgery on myocardial function as assessed by tissue Doppler echocardiography
Gerhard-Paul Dillera,*,
Balvinder S. Wasana,
Andreas Kyriacoua,
Niket Patela,
Roberto P. Casulab,
Thanos Athanasioub,
Darrel P. Francisa,
Jamil Mayeta
a International Centre for Circulatory Health, St Marys Hospital & National Heart and Lung Institute, Imperial College, London, UK
b Department of Cardiothoracic Surgery, St Marys Hospital, London, UK
Received 25 February 2008;
received in revised form 5 August 2008;
accepted 8 August 2008.
* Corresponding author. Address: International Centre for Circulatory Health, 59-61 North Wharf Road, London W2 1LA, UK. Tel.: +44 7973 105 394; fax: +44 707 505 5876. (Email: g.diller{at}imperial.ac.uk).
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Abstract
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Objective: Coronary artery bypass graft (CABG) surgery may induce myocardial stunning and thereby affect cardiac function. We aimed to assess whether myocardial function is affected by CABG in patients with preserved preoperative systolic function. Methods: Myocardial tissue peak velocities were recorded at the lateral and septal angle of the mitral annulus as well as at the lateral tricuspid annulus by pulsed wave tissue Doppler echocardiography before cardiac surgery, and then at 5 days, 6 weeks and 18 months after surgery. Results: Thirty-two consecutive patients with preserved systolic left ventricular function (31 male, 63 ± 10 years) undergoing CABG (9 with cardiopulmonary bypass on-pump, 23 beating heart off-pump) were included. Peak systolic velocity on tissue Doppler echocardiography was unchanged after surgery. In contrast, peak early diastolic velocities (E') improved significantly 5 days and 6 weeks after surgery in the septal area (6.2 ± 2.3 to 7.4 ± 2.6 and 7.6 ± 2.6 cm/s, respectively; p
< 0.05) and at the left ventricular lateral wall (9.1 ± 3.0 to 10.1 ± 3.0 and 11.3 ± 2.9 cm/s, respectively; p
< 0.05), and then declined slowly to preoperative values after 18 months. In contrast, right ventricular E' decreased significantly immediately after surgery (9.8 ± 2.7 preoperatively to 7.7 ± 1.7 cm/s at 5 days, p
= 0.005) with only incomplete recovery over time. This was similar in both the conventional and the off-pump CABG cohort. Conclusions: Left ventricular function did not deteriorate after CABG in patients with preserved preoperative systolic function. On the contrary, diastolic function improved immediately after CABG. Right ventricular function, in contrast, appeared to be damaged by surgery, to similar degrees regardless of whether patients underwent off-pump or on-pump surgery. Hypothermia and immune-inflammatory activation are, therefore, not plausible explanations for this decline in right ventricular function.
Key Words: Coronary artery bypass grafting (CABG) Tissue Doppler echocardiography Cardiopulmonary bypass Beating heart
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1. Introduction
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Coronary artery bypass graft (CABG) operation is the procedure of choice for patients with left main coronary artery disease and frequently a preferred method for patients with multi-vessel disease [1]. Yet, even in the current era of improved surgical technique and myocardial protection, instead of the hoped for improvement in cardiac function myocardial function may be depressed after surgery [2]. On the other hand, in the presence of significant coronary artery disease, successful revascularisation should augment myocardial blood supply and thereby improve myocardial function.
A family of three studies from one group have reported changes in ventricular function in the first year after conventional CABG for which a variety of explanations might be offered including the effect of cardiopulmonary bypass (CPB) [2–4]. In this study we set out to examine, over a longer 18-month period, the effect of CABG on both left ventricular and right ventricular function and determine whether any such effects differed between conventional on-pump CABG and beating heart (off-pump) surgery. To maximize the sensitivity of our study we used tissue Doppler imaging.
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2. Methods
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2.1 Patients
Thirty-two consecutive patients undergoing CABG were enrolled in this prospective study. The CABG operation was, at the surgeons discretion, on-pump (with CPB) or off-pump (beating heart). This study was approved by the local ethics committee and all patients provided informed consent.
2.2 Tissue Doppler parameters
Transthoracic echocardiography was performed before CABG (within 24 h before surgery) as well as 5 days (±1.5 days), 6 weeks and 18 months after surgery.
All measurements were made by a single experienced investigator using an ATL HDI 5000 echo ultrasound imaging system with a 2.5 MHz transducer equipped with pulsed wave tissue Doppler. With the subject in the lateral supine position, Doppler recordings were obtained from the standard parasternal [5] and apical views. Myocardial tissue Doppler peak systolic (S'), early diastolic (E') and late diastolic (A') velocities were measured (in cm/s) with the sample volume positioned at the septal and lateral angles of the mitral annular ring as well as on the lateral angle of the tricuspid valve (Fig. 1
). In addition, pulsed wave Doppler mitral and tricuspid inflow velocities including E and A wave peak velocities (cm/s) were obtained from the apical 4-chamber view [6].

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Fig. 1. (A) Anatomic position of the pulsed wave tissue Doppler sample. (B) Example of a pulsed wave tissue Doppler tracing (cm/s) illustrating peak systolic myocardial velocity (S), peak early diastolic velocity (E) and peak late (atrial) diastolic velocity (A).
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3. Statistical analysis
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All values are presented as mean ± standard deviation. Comparisons between groups were made using Students t test, Mann–Whitney U test or Wilcoxon signed rank test as appropriate. Repeated measure analysis of variance (ANOVA) followed by post-hoc comparisons using paired t-tests with Bonferroni correction were used to compare tissue Doppler parameters before and at different time points after surgery. For all analyses a p value <0.05 was considered significant. StatView 5.0 package (Abacus Concepts, Berkeley, CA, USA) was used for statistical analysis.
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4. Results
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4.1 Patient characteristics
Thirty-two consecutive patients (31 male, 63 ± 10 years) undergoing elective CABG at our institution were included in this study. Of the 32 patients enrolled, 9 underwent conventional CABG (8 male, 68 ± 8 years), while 23 patients underwent off-pump surgery (23 male, 62 ± 10 years). Cold anterograde crystalloid cardioplegia was administered in all patients operated on cardiopulmonary bypass. In addition, surgery was performed in hypothermia (mean core body temperature was 32.8 ± 1.7 °C). Mean cardiopulmonary bypass time was 97 ± 29 min with a cross-clamp time of 63 ± 15 min. In the off-pump cohort a Medtronic Octopus 3 tissue stabilisation system along with intra-coronary shunts were used. Overall, 28 patients had 3-vessel coronary artery disease (including a significant stenosis of the left main stem in 6 patients), while 4 patients had 2-vessel disease (2 with a significant stenosis of the left main stem). The number of grafts was not significantly different between conventional and off-pump CABG (median = 3 in both, p
= 0.50). Furthermore, 3-vessel disease was not more common in patients undergoing conventional compared with those undergoing off-pump surgery (p
= 0.66). The majority of patients received three bypass grafts (median 3, range 2–4), and in all but one patient a left mammarian artery to the left-anterior descending coronary artery bypass graft was used. Preoperative medications included β-blockers in 25 (78%), ACE-inhibitors in 13 (40%), calcium channel blockers in 8 (25%), nitrates in 28 (88%) and diuretics in 7 (22%). Overall, 6 (19%) had diabetes mellitus and 18 patients (56%) had arterial hypertension.
4.2 Left ventricular myocardial function before and after CABG
Systolic left ventricular function was not affected by CABG (Table 1
). Diastolic peak left ventricular early diastolic function (E'), in contrast, improved significantly at 5 days after CABG in the septal area compared to preoperative values (Table 1). After 18 months E' values at the septal and lateral mitral annulus were not significantly different from the preoperative value (Figs. 2 and 3
).
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Table 1 Systolic (S'), early diastolic (E') and late diastolic (A') tissue Doppler velocities recorded at the lateral and septal angle of the mitral annulus as well as at the lateral tricuspid annulus by pulsed wave tissue Doppler echocardiography before CABG, as well as 5 days, 6 weeks and 18 months after CABG (mean ± SD)
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Fig. 2. Early diastolic (E') tissue Doppler velocities recorded at the lateral angle of the mitral annulus by pulsed wave tissue Doppler echocardiography before CABG, as well as 5 days, 6 weeks and 18 months after CABG (mean ± standard error). Comparisons were made by repeated measure ANOVA and paired t test with Bonferroni correction, respectively. The p value for interaction between time point and type of surgery was non-significant.
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Fig. 3. Early diastolic (E') tissue Doppler velocities recorded at the septal angle of the mitral annulus by pulsed wave tissue Doppler echocardiography before CABG, as well as 5 days, 6 weeks and 18 months after CABG (mean ± standard error). Comparisons were made by repeated measure ANOVA and paired t test with Bonferroni correction, respectively. The p value for interaction between time point and type of surgery was non-significant.
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4.3 Right ventricular myocardial function before and after CABG
In the right ventricle tissue Doppler measures of systolic (S') and early diastolic function (E') decreased significantly at 5 days and 6 weeks after CABG compared to preoperative values (p
< 0.05 for each, Fig. 4A and B). Even after 18 months E' and S' values at the lateral tricuspid annulus were significantly lower compared to preoperative value (p
= 0.007) (Fig. 4).

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Fig. 4. (A) Early diastolic (E') tissue Doppler velocities and (B) systolic tissue Doppler velocities (S') recorded at the lateral tricuspid annulus by pulsed wave tissue Doppler echocardiography before CABG, as well as 5 days, 6 weeks and 18 months after CABG (mean ± standard error). Comparisons were made by repeated measure ANOVA and paired t test with Bonferroni correction, respectively. The p value for interaction between time point and type of surgery was non-significant for both systolic and early diastolic function.
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4.4 Off-pump versus on-pump CABG
There was no significant difference between the changes in left and right ventricular systolic or diastolic function between patients undergoing on- or off-pump surgery. There was, however, a non-significant trend towards a smaller decrease in right ventricular diastolic function in patients who underwent off-pump surgery (p
= 0.08 at 18 months postoperatively).
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5. Discussion
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Our study shows that left ventricular diastolic function improves within days after coronary artery bypass surgery, even in patients with preserved preoperative myocardial function. In contrast, right ventricular systolic and diastolic function decreases after coronary artery bypass surgery with only incomplete recovery over time. Right ventricular function deteriorated to a similar degree in patients undergoing off- or on-pump surgery, although the results of the current study show a non-significant trend that off-pump surgery may be associated with less right ventricular damage.
5.1 The value of tissue Doppler echocardiography in assessing myocardial function
Tissue Doppler echocardiography represents a robust, quick and relatively simple method for sensitively detecting systolic and diastolic dysfunction [7,8]. Unlike conventional visual assessment of regional wall motion abnormalities it does not rely on subjective interpretation and can be quantified objectively. Its potential in identifying myocardial dysfunction associated with ischaemia has been established in different experimental and clinical settings [9,10]. Impaired long-axis function has been described in patients with coronary artery disease and during experimental coronary artery occlusion [11,12]. Interestingly, it has been demonstrated that longitudinal left ventricular dysfunction precedes circumferential dysfunction (assessed by conventional echocardiography) in patients with coronary artery disease [8]. Therefore, tissue Doppler echocardiography has the potential to reveal myocardial hibernation before left ventricular systolic dysfunction becomes evident on conventional echocardiography.
5.2 Impact of CABG on left ventricular function
In the current study we could not demonstrate any reduction in systolic left ventricular function as an early or long-term effect of cardiac surgery. On the contrary, left ventricular diastolic function improved early after surgery. This finding is consistent with data published by Hedman et al. [4]. Our results, however, expand on this previous report showing that diastolic function returns to preoperative values during long-term (1
-year follow-up). The reasons for this decline in diastolic function over time remain unclear but may be related to the natural course of coronary artery disease. Our data suggest that any perioperative myocardial damage is more than offset by successful revascularisation in the early- and mid-term follow-up. Furthermore, the results of the current study indicate that myocardial hibernation must have been present before CABG (even in the absence of evident left ventricular systolic dysfunction on conventional 2D echocardiography) allowing for improved longitudinal function as an effect of cardiac surgery. This is consistent with a previous report showing improved subendocardial function after coronary angioplasty [8] or coronary artery bypass surgery [4]. Myocardial relaxation during diastole is an energy dependent process relying on adequate oxygen supply [13]. Furthermore, coronary perfusion occurs predominantly during diastole [14]. We speculate that this may provide the pathophysiologic rationale for improved diastolic myocardial function after CABG observed in the current study.
5.3 Impact of CABG on right ventricular function
As expected, right ventricular function deteriorated as a consequence of cardiac surgery with only incomplete recovery during long-term follow-up. This finding is consistent with previous reports [2,3]. Our study expands on these previous reports by providing information on longitudinal ventricular function up to 1
years after surgery. Off-pump CAB represents an acceptable alternative to conventional on-pump surgery [15] and has been reported to be associated with reduced oxidative stress [16] and less pro-inflammatory cytokine expression compared to conventional CABG [17]. The results of the current study support the notion that off-pump surgery may be associated with less right ventricular damage. However postoperative right ventricular dysfunction was found in both, the on- and off-pump cohort.
Pericardiotomy has been reported to result in perturbation of myocardial blood flow in the right ventricle [18] and pericardiotomy negatively affects right ventricular end-diastolic pressure [19]. On cellular level, systemic inflammatory response due to the release of pro-inflammatory cytokines is a recognised feature of cardiopulmonary bypass [20]. The available literature, however, does not permit definitive conclusions on the advantages of off-pump surgery with regard to the systemic inflammatory response [21]. It has been argued that the relatively thin wall of the right ventricle would precipitate right ventricular dysfunction as a consequence of even minor inflammation, effusion or haematoma associated with surgery, potentially primarily affecting diastolic function and right ventricular filling. Velissaris et al. [22] reported that off-pump CABG triggers a considerable systemic stress hormone response that may be comparable to on-pump surgery, potentially explaining the findings of the current study.
The result of the current and previous studies suggests that the negative effect of surgery on right ventricular function may be independent of the use of cardiopulmonary bypass. Whether improved surgical technique could avoid right ventricular damage remains to be elucidated. Intra-coronary shunts have been demonstrated to reduce postoperative troponin I release in patients undergoing off-pump CABG [23] and may therefore be associated with less postoperative myocardial damage. However, as the right ventricle is supplied to a greater extent by coronary collaterals and less dependent on diastolic perfusion compared to the left ventricle, continued coronary perfusion should theoretically confer less benefit for the right ventricle. Despite the use of coronary shunts in all off-pump CABG patients included, right ventricular dysfunction was evident postoperatively in the current study. Ischaemic injury during distal anastomosis in off-pump surgery has been linked to transient haemodynamic deterioration due to cardiac manipulation suggesting that cardiac manipulation should be reduced to a minimum [24,25]. However, these haemodynamic effects have been found to be transient only and are unlikely to explain deterioration in right ventricular function over 18 months of follow-up. Ultimately, effects of surgical technique on symptoms and mortality are the drivers to change clinical practice. Different studies have shown reduced morbidity, lower incidence of atrial fibrillation, pulmonary complications and duration of hospitalisation after off-pump CABG [20]. It remains to be elucidated whether right ventricular dysfunction correlates with clinical outcome in patients undergoing CABG.
5.4 Limitations of the study
The current study used only tissue Doppler velocity imaging at the atrio-ventricular valve annulus to assess longitudinal ventricular function. Other measurement technologies might have yielded other results, but tissue Doppler is a universally accepted method of quantifying longitudinal myocardial behaviour and is widely used in clinical practice. Larger studies may also be able to compare changes in myocardial velocities in areas targeted by the operation to those in areas outside the revascularised myocardium. Furthermore, larger studies may be required to investigate whether off-pump CABG is associated with less right ventricular damage compared to on-pump surgery. The results of the current study, however, indicate that this difference is small and may allow for power calculations for subsequent multi-centre studies.
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6. Conclusions
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In this study we have found that left ventricular diastolic function improves early after coronary artery bypass surgery, returning to preoperative values during long-term. In contrast, right ventricular function decreases after coronary artery bypass surgery with only incomplete recovery over time. Right ventricular function deteriorated to a similar degree in patients undergoing off- or on-pump surgery, although the current study was not adequately powered to detect a small difference between them.
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Acknowledgments
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We acknowledge the support of the NIHR Biomedical Research Centre Scheme.
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