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ORIGINAL RESEARCH

Speckle-Tracking Imaging to Monitor Myocardial Function After Coronary Artery Bypass Graft Surgery Zhe-Yu Yin, MD, Xiao-Feng Li, MD, PhD, Ying-Feng Tu, MD, Dan-Dan Dong, MD, Dong-Liang Zhao, MD, Baozhong Shen, MD, PhD Objectives—The purpose of this study was to investigate the changes in myocardial function in patients after coronary artery bypass graft (CABG) surgery using longitudinal and circumferential strain on speckle-tracking imaging. Methods—A total of 145 patients who successfully underwent CABG surgery with a left ventricular ejection fraction (LVEF) of 50% or greater were enrolled in this study. Patients were classified into 4 groups based on age: group 1 (33–59 years), group 2 (60–64 years), group 3 (65–69 years), and group 4 (70–79 years). Routine echocardiography and longitudinal and circumferential strain measurements on speckle-tracking imaging were performed 1 week before and 1, 3, and 6 months after the CABG. Received January 28, 2013, from the Department of Radiology, Fourth Hospital of Harbin Medical University, Harbin, China (Z.-Y.Y., Y.-F.T., D.-D.D., D.-L.Z., B.S.); Key Laboratory of Molecular Imaging, College of Heilongjiang Province, Harbin, China (Z.-Y.Y., Y.-F.T., D.-D.D., D.-L.Z., B.S.); and Department of Diagnostic Radiology, University of Louisville School of Medicine, Louisville, Kentucky USA (X.F.L.). Revision requested February 14, 2013. Revised manuscript accepted for publication April 2, 2013. We thank the cardiothoracic surgeons in our hospital for assistance and the reviewers’ invaluable comments and suggestions to improve this article. This study was supported in part by National Natural Science Foundation of China grant 81130028 and Science and Technique Foundation of Heilongjiang Province grant GA12C302. Address correspondence to Baozhong Shen, MD, PhD, Department of Radiology, Fourth Hospital of Harbin Medical University, 37 Yiyuan St, 150001 Harbin, Heilongjiang, China. E-mail: [email protected] Abbreviations

CABG, coronary artery bypass graft; CHD, coronary heart disease; LV, left ventricular; LVEDd, left ventricular end-diastolic dimension; LVEF, left ventricular ejection fraction; MRI, magnetic resonance imaging; 2D, 2-dimensional doi:10.7863/ultra.32.11.1951

Results—In all groups, longitudinal strain increased significantly at 3 and 6 months after CABG therapy compared to baseline (P < .05). A significant increase in circumferential strain was found 1 month after the CABG in groups 1, 2, and 3, and a continuous increase in the parameter was observed in all groups 3 months after therapy (P < .05). However, the LVEF, left ventricular end-diastolic dimension, and stroke volume measured by routine echocardiography were not significantly changed after successful CABG treatment in all groups during 6 months of follow-up. Conclusions—Based on the results of our study in all age groups, speckle-tracking imaging parameters are more effective than the LVEF, left ventricular end-diastolic dimension, and stroke volume for monitoring improvement in myocardial function after CABG surgery. Key Words—coronary artery bypass graft; coronary heart disease; echocardiography; speckle-tracking imaging

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oronary heart disease (CHD) is the leading cause of death worldwide; more than 1 million people die of CHD each year. It is predicted that CHD will cause about 14.2% of all deaths by 2030.1 The elderly population is at greater risk of CHD. In China, there were 185 million people 60 years or older at the end of 2011, and the number is expected to reach 200 million by the end of 2013. Coronary artery bypass graft (CABG) surgery has been accepted as an effective therapeutic strategy for CHD, which not only improves clinical symptoms but also reduces the risk of sudden cardiac death. A CABG can also increase myocardial function and enhance exercise tolerance.2,3 Elderly patients with CHD frequently receive CABGs; however, they are at a higher risk because of age-related impairment of organ function, poor surgical

©2013 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2013; 32:1951–1956 | 0278-4297 | www.aium.org


Yin et al—Speckle-Tracking Imaging After Coronary Artery Bypass Graft Surgery

tolerance, and related increases in complications.4 Thus, it is important to accurately evaluate the temporal pattern of postoperative changes in myocardial function with various parameters. Noninvasive detection of myocardial function recovery is critically important in patients who undergo CHD treatments such as a CABG, coronary artery stenting, and drug therapy. Magnetic resonance imaging (MRI) is considered a standard strategy for this purpose. It can analyze myocardial deformation mechanical characteristics accurately; however, MRI has its limitations for use in multiple-point follow-ups because of its high cost and timing-consuming nature.5 Echocardiography is a widely used noninvasive imaging modality for evaluating regional wall motion and the left ventricular ejection fraction (LVEF) in patients with CHD. However, some patients with heart failure may have a normal LVEF measured by 2-dimensional (2D) echocardiography.6 Therefore, the echocardiographically measured LVEF may not accurately reflect the myocardial function status. Speckle-tracking imaging is a novel sonographic technique developed in recent years. It is designed to track the motion of myocardial tissues frame by frame in the form of 2D speckles in the region of interest, actually reflecting the motion and deformation and acquiring the speed, displacement, strain, and strain rate of myocardial tissues to analyze myocardial motion.7,8 This technique is able to evaluate myocardial deformation and quantitatively track ventricular wall motion abnormalities. Speckle-tracking echocardiography is able to distinguish between normal and abnormal myocardial deformation and detect subclinical left ventricular (LV) dysfunction.9 In this study, we observed temporal myocardial functional improvement in patients after CABG surgery using speckle-tracking imaging parameters and compared those to parameters measured by routine 2D echocardiography. We found that the speckle-tracking imaging parameters were more effective than the LVEF, left ventricular end-diastolic dimension (LVEDd), and stroke volume measured by conventional echocardiography for monitoring improvement in myocardial function after CABG surgery.

the Fourth Hospital of Harbin Medical University. All patients had chest tightness, shortness of breath, unstable angina pectoris, and ST-segment depression of 0.05 mV (ie, 0.5 mm) or greater on electrocardiography (Table 1). Coronary artery stenosis was confirmed by coronary arteriography in all patients, and patients with either multivessel coronary artery stenosis of 75% or greater or left main coronary artery stenosis of 50% or greater were included. A total of 145 patients met these criteria and were enrolled in the study. According to the American College of Cardiology/American Heart Association guidelines,10,11 only those patients with no evidence of myocardial infarction, without other organic diseases, such as chronic obstructive pulmonary disease, renal insufficiency, arrhythmia, and severe valvular disease, and patients who underwent CABG surgery without other concurrent surgical procedures (eg, ventricular aneurysmectomy and valve replacement) with an LVEF of 50% or greater were included in the study. Patients were divided into 4 groups according to age: group 1 (33–59 years, 64 patients), group 2 (60–64 years, 24 patients), group 3 (65–69 years, 29 patients), and group 4 (70–79 years, 28 patients). Detailed patient information is summarized in Table 2. Image Acquisition Echocardiography was performed 1 week before (at baseline), and 1, 3, and 6 months after CABG surgery. At each follow-up, echocardiography was performed by an experienced sonographer who was blinded to the clinical findings. Echocardiography was performed with an iU22 ultrasound scanner (Philips Healthcare, Andover, MA) equipped with an S5-1 probe (1.0–5.0 MHz) with the patient in the left lateral recumbent position. Electrocardiography was recorded simultaneously. All patients were instructed to breathe evenly during image acquisition. Parameters including the LVEF, acquired by the biplane Simpson method, left LVEDd, and stroke volume were measured by conventional echocardiography. After the Table 1. Electrocardiographic Data Parameter

Materials and Methods Patients This study was approved by the Institutional Review Board of the Fourth Hospital of Harbin Medical University according to the Declaration of Helsinki. From January 2009 to March 2012, a total of 265 patients underwent CABG surgery at the Department of Cardiac Surgery of

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n

ST-segment depression, mm 0.5–1 1–2 >2 Leads with ST-segment depression V1–V3 V1–V6 II, III, aVF V1–V6, I, aVL

114 25 6 81 49 246 85

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procedure, 2D dynamic images with 3 consecutive cardiac cycles in 3 standard apical views (4-chamber, 2-chamber, and long axis) and 3 LV short-axis views (level of the mitral valve, papillary muscle, and apex) were collected and saved. The frame rates were 55 to 70 frames per second. Speckletracking imaging was analyzed in a QLAB 7.0 workstation (Philips Healthcare). Data Analysis Advanced Tissue Motion Quantification software on the QLAB 7.0 workstation was used for offline speckletracking imaging analysis. The software creates regions of interest automatically by marking the outline of the endocardium in the Tissue Motion Quantification mode, which can be manually adjusted. The software calculated predetermined functional parameters automatically. The LV long-axis view included the basal, midventricular, and apical sections or slices. The LV short-axis view included the anterior septum, anterior wall, lateral wall, posterior wall, inferior wall, and posterior septum. After all trackings were performed, the software computed the longitudinal and circumferential strain, recorded the systolic strain peak of all curves with the start of the electrocardiographic R wave as the starting point of LV systole and the R-R interval as one cardiac cycle, and then separately calculated the global mean strain. Statistical Analyses All statistical analyses were performed with SPSS version 18.0 software (SPSS Inc, Chicago, IL). The F test was used for statistical analysis of data among groups and within the same group before and each point after CABG surgery. The Q test was used for multiple comparisons. Data were

expressed as mean ± standard deviation, and P < .05 was considered statistically significant.

Results Of the 145 patients, 117 had asymptomatic angina, and 28 had alleviative symptoms of angina 1 month after CABG surgery. All patients had no symptoms 3 months after surgery. Myocardial infarction was not evident during the perioperative period. Among the 145 patients, there were 461 coronary artery lesions with stenosis of 75% or greater or left main coronary artery lesions with stenosis of 50% or greater (Table 2). The left thoracic artery was chosen for single vascular lesions, and 3 bridge grafts were placed for multiple coronary artery lesions. For major vessel lesions, the anterior descending branch used the left thoracic artery bridge, and all others used vein bridges. Coronary angiography was repeated in 104 patients 6 months after CABG surgery; all grafted blood vessels were completely patent without anastomotic strictures. As shown in Table 3, the LVEDd, LVEF, and stroke volume measured by conventional echocardiography did not change significantly even after successful CABG treatment, with apparent improvement in cardiac function in all groups during the 6-month follow-up period (P > .05 for all). In all groups, longitudinal strain on speckle-tracking imaging increased significantly 3 and 6 months after CABG therapy (P < .05), although longitudinal strain declined mildly, but there was no statistical difference 1 month after CABG therapy (P > .05). Interestingly, longitudinal strain increased continuously during the 3- to 6month period after CABG surgery only in group 4: the

Table 2. Patient Characteristics and Coronary Arteriographic Results Parameter Patients, n (%) Male Female Age, y Male Female Coronary arteries involved, n LAD LCX RCA LM Total

Group 1 (n = 64)

Group 2 (n = 24)

Group 3 (n = 29)

Group 4 (n = 28)

Total (n = 145)

47 (73.44) 17 (26.56)

17 (70.83) 7 (29.17)

16 (55.17) 13 (44.83)

21 (75.00) 7 (25.00)

101 (69.66) 44 (30.34)

52.09 ± 5.99 53.29 ± 4.24

62.11 ± 1.93 62.14 ± 1.86

67.56 ± 1.26 67.46 ± 1.39

73.07 ± 2.85 72.71 ± 3.55

60.45 ± 9.62 61.98 ± 8.19

58 53 52 37 200

23 21 24 15 83

25 23 28 19 95

24 22 23 14 83

130 119 127 85 461

Data are expressed as mean ± SD where applicable. LAD indicates left anterior descending coronary artery; LCX, left circumflex coronary artery; LM, left main coronary artery; and RCA, right coronary artery.


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Table 3. Echocardiographic Parameters Before and After CABG Surgery Parameter LVEDd, mm Group 1 Group 2 Group 3 Group 4 LVEF, % Group 1 Group 2 Group 3 Group 4 Stroke volume, mL Group 1 Group 2 Group 3 Group 4

Patients, n

Before CABG

1 mo

After CABG 3 mo

6 mo

64 24 29 28

49.77 ± 6.36 52.67 ± 5.51 48.41 ± 5.19 49.46 ± 5.00

49.27 ± 5.66 50.67 ± 6.03 47.41 ± 6.14 49.07 ± 4.24

48.05 ± 5.52 49.75 ± 5.91 46.93 ± 5.13 47.93 ± 3.51

47.83 ± 4.38 50.54 ± 5.52 46.59 ± 4.56 47.71 ± 3.49

64 24 29 28

59.81 ± 8.56 58.25 ± 8.31 60.07 ± 6.88 58.71 ± 6.68

56.45 ± 7.67 56.04 ± 6.89 57.14 ± 6.01 56.21 ± 6.09

61.77 ± 7.14 59.96 ± 6.14 60.66 ± 8.18 57.54 ± 5.23

61.58 ± 5.66 60.79 ± 5.75 61.83 ± 5.98 60.43 ± 5.05

64 24 29 28

70.05 ± 8.33 77.09 ± 8.76 66.86 ± 6.95 72.53 ± 7.92

64.12 ± 5.86 68.35 ± 7.79 59.24 ± 6.44 64.03 ± 7.85

67.57 ± 6.23 70.67 ± 8.24 62.07 ± 6.59 66.77 ± 8.23

66.87 ± 6.47 71.49 ± 8.05 63.61 ± 6.16 68.71 ± 8.40

Data are expressed as mean ± SD. No significant differences in LVEF, LVEDd, and stroke volume before and after the CABG were noted in any group (P > .05).

oldest patients (P < .05; Figure 1A). A significant increase in circumferential strain on speckle-tracking imaging was found 1 month after CABG surgery in groups 1, 2, and 3. A continuous increase in circumferential strain was observed in all groups 3 months after therapy (P < .05; Figure 1B).

Discussion The morbidity and mortality associated with CHD are increasing, and more and more elderly patients are being treated with CABG surgery in recent years. A coronary artery revascularization therapy, CABG surgery can improve the myocardial blood supply and increase the con-

tractility of the surviving myocardium.12–14 The results of coronary arteriography did not reflect the myocardial function, although it clearly depicted the patency of the bypass grafts. In addition, it is generally not acceptable to perform this invasive technique multiple times. Noninvasive detection of myocardial function recovery is critically important in patients who undergo CHD treatments. Echocardiography is the primary method for evaluating the heart function of patients with CHD; however, routine 2D echocardiography greatly depends on subjective judgment. The clinical value of routine echocardiography is limited because it cannot accurately evaluate the motion of the ventricular wall. We found that the

Figure 1. Longitudinal strain (LS; A) and circumferential strain (CS; B) before and after CABG surgery. *P < .05 versus Pre; **P < .01 versus Pre; ÇP < .05 versus 1 month after CABG; #P < .05 versus 3 months after CABG. A

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B




LVEDd, LVEF, and stroke volume measured by conventional echocardiography did not change significantly even after successful CABG treatment, with apparent improvements in cardiac function in all groups (Table 3). This finding may be due to the fact that these parameters are not direct measurements of the improvement in the myocardial function and depend on many other biological factors, such as preload, afterload, valve functions, heart rate, and others. Our findings indicate that the speckle-tracking imaging parameters, longitudinal strain and circumferential strain, were more effective and better reflected post-CABG cardiac function recovery (Figure 1), whereas the LVEF, LVEDd, and stroke volume failed to show the improvement (Table 3). As a novel technique, speckle-tracking imaging has been used recently to evaluate global and regional myocardial function, and it can provide reproducible data on myocardial deformation, not only in radial and circumferential directions but also in the longitudinal direction.15–20 The LV myocardium consists of 3 different anatomic layers: subendocardial, midmyocardial, and subepicardial.21 Longitudinal strain on speckle-tracking imaging can quantitatively measure the elongation force of the subendocardial myocardium in the longitudinal direction, and circumferential strain can measure the midmyocardial shortening deformation in the peripheral direction.19,20 Longitudinal strain can assess global and regional LV systolic function with good accuracy and reproducibility.17 Helle-Valle et al18 demonstrated that regional myocardial strain measurement by speckletracking echocardiography highly agreed with measurement by cardiac MRI. The strain rate has been reported to be a better parameter for evaluating intrinsic myocardial contraction,22 but its use is limited because of poor reproducibility and instability. Our findings indicate that the recovery of myocardial function 3 months after reperfusion in most patients may be due to the fact that myocardial improvement in the ischemic regions requires considerable time after revascularization. In addition, cardiac arrest, extracorporeal circulation, and other surgical procedures when CABG surgery is performed may also worsen ischemic reperfusion injury, especially to subendocardial muscle fibers. In this study, the contractibility of the subendocardial myocardium measured by longitudinal strain was delayed (Figure 1); subendocardial myocardial ischemia is the leading cause of decreased longitudinal strain.23 Finally, surgical trauma causing severe edema and contracture of the ventricular wall and hemorrhagic cell infiltration24,25 may also delay the recovery of myocardial function.


We found that the longitudinal and circumferential strain parameters in the oldest group (group 4) were lower and recovered more slowly after CABG surgery than in the other groups, indicating that myocardial strain may be associated with aging; this finding agrees with the results of 3-dimensional MRI tissue-tagging studies.26,27 A decrease in the amount of viable myocardial cells, an increase in cell size, an elevated amount of interstitial collagens and elastins, progressive cardiac amyloidosis and collagenous degeneration, and diffuse fibrosis of the endocardium and myocardium may develop in older patients and may prolong the recuperation time for myocardial function. The impact of age on pre- and post-CABG recovery of myocardial function should be considered before CABG surgery in elderly patients. This study had some limitations. We did not address individual myocardial segment revascularization after CABG surgery in this study. In addition, although we followed patients for 6 months, longer-term outcomes of CABG surgery need to be observed to better understand the pattern of myocardial function in post-CABG patients. In conclusion, the speckle-tracking imaging parameters, longitudinal strain and circumferential strain, are more effective and better than echocardiographic parameters such as the LVEDd, LVEF, and stroke volume for monitoring improvements in myocardial function after CABG surgery. Because of the structure of the LV and the locations of the myocardial regions damaged by coronary artery stenosis, longitudinal strain takes more time to improve than does circumferential strain. The latter would therefore be more sensitive for detecting early recovery of cardiac function.

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