Ann Thorac Surg 2007;84:801-807
© 2007 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Epicardial Ultrasonography: A Potential Method for Intraoperative Quality Assessment of Coronary Bypass Anastomoses?
Per Kristian Hol, MDa,*,
Kai Andersen, MD, PhDb,
Helge Skulstad, MD, PhDc,
Per Steinar Halvorsen, MDa,
Per Snorre Lingaas, MDb,
Rune Andersen, MDd,
Jacob Bergsland, MDa,
Erik Fosse, MD, PhDa,e
a The Interventional Centre, Rikshospitalet-Radiumhospitalet University Hospital, Oslo, Norway
b Department of Thoracic and Cardiovascular Surgery, Rikshospitalet-Radiumhospitalet University Hospital, Oslo, Norway
c Department of Cardiology, Rikshospitalet-Radiumhospitalet University Hospital, Oslo, Norway
d Department of Radiology, Rikshospitalet-Radiumhospitalet University Hospital, Oslo, Norway
e Medical Faculty, University of Oslo, Oslo, Norway
Accepted for publication April 5, 2007.
* Address correspondence to Dr Hol, The Interventional Centre, Rikshospitalet University Hospital, Oslo, NO-0027, Norway (Email: per.kristian.hol{at}rikshospitalet.no).
| Dr Bergsland discloses that he has a financial relationship with MediStim, Inc.
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Abstract
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Background: Intraoperative quality assessment in coronary artery bypass surgery confirms graft patency and enables revision of failing grafts. The aim of this study was to evaluate graft quality intraoperatively by epicardial ultrasonography and to compare this technique with transit time flow measurements and intraoperative angiography, and to evaluate the ability of these methods to predict long-term patency as described by follow-up angiography.
Methods: Thirty-nine patients with mean age of 66 years (SD 9.5) who underwent off-pump coronary artery bypass surgery with internal mammary artery graft to the left anterior descending coronary artery were included. Epicardial ultrasonography and transit time flow measurement were performed after completion of the anastomoses, and coronary angiography after closure of the chest. Follow-up angiography was carried out after 156 days (SD 50).
Results: Diameter measurements obtained by epicardial ultrasonography correlated poorly with the same diameter measurements obtained by angiography. Epicardial ultrasonography revealed 5 abnormal grafts (13%), transit time flow measurements none, and intraoperative angiography 9 (23%). At follow-up angiography, 4 grafts (11%) were pathologic. Epicardial ultrasonography and transit time flow measurements indicated no need for graft revision; intraoperative angiography suggested need for revision in 3 cases.
Conclusions: Epicardial ultrasonography could be a useful method for intraoperative assessment of graft anastomosis quality, but needs to demonstrate its ability to predict grafts in need of revision. Angiography must be considered the gold standard in intraoperative imaging.
Anastomosis quality is crucial for the results of coronary artery bypass surgery. Evaluation of the grafts is particularly important during off-pump surgery, which can be technically more challenging. Intraoperative quality assessment is therefore necessary to ensure graft patency and to disclose technical errors, enabling on-table graft revision.
Transit time flow measurement is the current routine method for evaluating anastomosis quality, despite being difficult to interpret [1–3]. Epicardial echocardiography has been suggested as an alternative approach, as it provides both morphologic and functional information about the anastomosis quality [4–11]. However, coronary angiography is considered the gold standard for graft assessment, although normally not available in the operation theater.
The aim of this study was to evaluate intraoperative graft quality assessment by epicardial ultrasonography and to compare this technique with transit time flow measurements and intraoperative coronary angiography. Moreover, we studied the capability of all these methods to predict long-term patency as determined by follow-up angiography.
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Patients and Methods
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Thirty-nine patients who underwent off-pump coronary artery bypass surgery were included, with baseline characteristics as described in Table 1. The internal mammary artery (IMA) was grafted to the left anterior descending (LAD) artery, and saphenous vein grafts were used elsewhere. All patients were operated on through a median sternotomy, and our surgical technique for performing off-pump surgery has been previously described [12]. In this study, only the IMA-to-LAD anastomoses were assessed. All patients gave their informed consent, and the study was approved by the Regional Ethics Committee.
Epicardial Ultrasonography Assessments
Anastomosis assessment was performed by epicardial ultrasonography with a 10-MHz linear array GE Vingmed sterilized transducer connected to a GE Vingmed System FiVe, Vivid 5 or Vivid 7, echocardiography system (GE Vingmed, Horten, Norway). The recordings were made while the device stabilizing the anastomotic site (Octopus; Medtronic, Minneapolis, Minnesota) was still applied. Grayscale and color Doppler images were recorded and stored, with subsequent analysis performed by EchoPAC software (GE Vingmed). Measurements were made of the length of the anastomosis proper (DA), the diameters of the distal IMA (DM), LAD at the heel of the anastomosis (D0), LAD at the toe of the anastomosis (D1), and LAD 5 mm distal to the toe (D2; Fig 1), by two independent readers and repeated by one reader on a later occasion. Masked to the results of transit time flow measurement and angiography, the quality of all anastomoses was graded visually by the most experienced observer, based on information obtained from B-mode and color Doppler recordings. Lesions were graded as described by FitzGibbon and associates [13]: A, normal or less than 50% reduction in diameter; B, a significant stenosis of more than 50% diameter reduction; and O, occluded. As the need for revision not only would be decided by the degree of stenosis, the following assessments were additionally performed: N, no need for graft revision; I, indeterminate with regard to need for on-table revision; and R, revision required. With reference to previous angiographic studies [12, 14, 15], significant stenoses were not necessarily considered to need revision, while occluded grafts and grafts with potential for occlusion, like dissection, were used as criteria for operative revision.
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Fig 1. Intraoperative epicardial ultrasonography demonstrating a patent internal mammary artery to left anterior descending artery anastomosis, with diameter measurements performed at five different sites. (DA = length of the anastomosis proper; DM = diameter of the distal mammary artery; D0 = diameter of the heel of the anastomosis; D1 = diameter of the toe of the anastomosis; D2 = diameter of left anterior descending coronary artery.)
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Flow Measurements
Transit time flow measurement [1–3] (Butterfly Flowmeter 2000 and VeriQ; Medi-Stim, Oslo, Norway) was performed with the probe around the distal part of the graft. Based on simultaneous evaluation of the flow value, the pulsatility index and visual inspection of the flow curve, the necessity for on-table graft revision was graded by the surgeon during operation and reassessed by an independent reader postoperatively. The pulsatility index was defined as the difference between maximum forward flow and maximum negative flow divided by mean flow, and a normal flow curve was defined as demonstrating mainly diastolic flow pattern with minimal systolic peaks [2]. A lowest acceptable mean flow value was not adopted; the mean flow value was always interpreted together with the flow curve and the pulsatility index [2]. Pulsatility index above 5, low flow value, and a flow curve with systolic flow pattern indicated obstructed flow [2].
Angiographic Assessment
Operations were performed in a combined catheterization and operating room containing fixed angiographic equipment (Angiostar OR; Siemens, Erlangen, Germany) [16]. By percutaneous femoral approach, angiography with at least two orthogonal projections of each anastomosis was performed after closure of the chest with the patients still under general anesthesia, enabling immediate on-table graft revision if necessary. Follow-up angiography was carried out after 156 days (SD 50), using radial access. Measurement of the diameters of the anastomosis as described for epicardial ultrasonography was made by two independent radiologists using quantitative analyzing program (Sectra Angiography and Cardiology Package 1.0.1; Linköping, Sweden). Moreover, the measurements were repeated by one reader on a later occasion. As for epicardial ultrasonography, patency grading (A, B, or O) and grading the necessity for on-table graft revision (N, I, or R) were made for intraoperative angiography, and patency grading (A, B, or O) was also performed during follow-up angiography.
Statistical Analyses
Data were analyzed using SPSS, version 13.0 (SPSS, Chicago, Illinois), and expressed as mean and standard deviation for normally distributed data and as median with range for data not normally distributed. Agreement between the methods was assessed by linear regression analyses and the method of Bland-Altman [17]. Not normally distributed data were correlated using Spearman’s rank coefficient. Differences were considered statistically significant when p was less than 0.05.
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Results
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Whereas epicardial ultrasonography was performed once in all 39 patients, transit time flow measurements and intraoperative angiography were repeated in 2 patients, leaving 41 measurements for analyses. Thirty-six patients had follow-up angiography.
On-Table Findings
The result of the diameter measurements are shown in Table 2, describing the mean diameters measured at five different sites around the distal anastomosis. The intraobserver variation of the diameter measurement by epicardial ultrasonography was better than the interobserver variation with mean correlation coefficient of 0.66 (p < 0.01) and 0.50 (p < 0.01), respectively. For the diameters measured by intraoperative angiography, the intraobserver and interobserver mean correlation coefficients were 0.81 (p < 0.01) and 0.71 (p < 0.01), respectively. A poor correlation was found between the diameters measured by epicardial ultrasonography versus intraoperative angiography (r = 0.27; Fig 2), between epicardial ultrasonography and follow-up angiography (r = 0.26), and between intraoperative and follow-up angiography (r = 0.32).
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Table 2 Mean Diameters (mm) of the IMA-LAD Anastomosis, Assessed by Epicardial Ultrasonography and Intraoperative and Follow-Up Angiography
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Fig 2. The diameters measured by epicardial ultrasonography were poorly correlated with the measurements by intraoperative angiography, exemplified by the diameter of the distal mammary artery. The differences of the diameter measurements plotted against the mean diameters (circles), with mean difference and 95% limits of agreement are indicated (Bland-Altman analyses). The mean difference is 0.06 mm, but the limits of agreements are –0.95 and +1.06 mm.
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The results of the visual grading of the quality of the anastomoses are summarized in Table 3, describing scores indicating abnormalities. When abnormal grafts were defined as pathologic either by the FitzGibbon classification (ABO) [13] or by the need-of-revision classification (NIR), epicardial ultrasonography revealed 5 abnormal findings (13%), all significantly stenosed, but not thought to be in need of revision. All 39 grafts were stated to be normal by transit time flow measurements with no need for graft revision. There were no differences in flow values and pulsatility indexes between grafts graded A and B by intraoperative angiography. Angiographic grade A grafts had median mean flow and pulsatility index of 27.5 mL/min (14 to 92) and 2.6 (1.1 to 5.0), respectively. Corresponding values for angiographic grade B grafts were 27.5 mL/min (22 to 28) and 2.6 (1.7 to 3.1), respectively. At intraoperative angiography, 9 grafts (23%) were found abnormal. One of the anastomoses was occluded, 6 were significantly stenosed, and 3 were thought to be in need of revision. One of the grafts scored to be in need of revision was also scored occluded. The significant lesions described by epicardial ultrasonography and intraoperative angiography were all found in different cases. The sensitivity, specificity, and positive and negative predictive values of epicardial ultrasonography versus pathologic findings as defined by intraoperative angiography were 0.22 (2 of 9), 0.90 (27 of 30), 0.40 (2 of 5), and 0.79 (27 of 34), respectively. The negative predictive value of transit time flow measurement was 0.77 (30 of 39).
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Table 3 Abnormal Scores (FitzGibbon Grading ABO and Need-of-Revision Grading NIR) at Epicardial Ultrasonography Transit Time Flow Measurement, and Intraoperative and Follow-Up Angiography
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The 3 grafts (8%) thought to need revision after evaluation by intraoperative angiography were all revised. Two of these were revised owing to dissection, not detected by epicardial ultrasonography or transit time flow measurement (Table 3, cases 8 and 14). At surgery, dissection was found in the LAD around the distal anastomotis in case 8 (Fig 3) and in the distal IMA in case 14. The third graft was revised owing to angiographic finding of LAD occlusion proximally and distally to the anastomotic site. That was detected neither by epicardial ultrasonography nor by transit time flow measurement (Table 3, case 34). Surgical inspection confirmed technical error at the sites described by angiography.
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Fig 3. Dissection in left anterior descending artery around the distal anastomosis, demonstrated by (A) intraoperative angiography, but not detected by (B) epicardial ultrasonography.
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Long-Term Patency
After FitzGibbon classification, 4 grafts (11%) were pathologic at follow-up angiography, 3 were significantly stenosed, and 1 was occluded, giving a patency rate of 97%. The sensitivity, specificity, and positive and negative predictive values of epicardial ultrasonography were 0.25 (1 of 4), 0.86 (28 of 32), 0.2 (1 of 5), and 0.9 (28 of 31), respectively; and of intraoperative angiography 0.75 (3 of 4), 0.81 (26 of 32), 0.33 (3 of 9), and 0.96 (26 of 27), respectively (Table 4). The negative predictive value of transit time flow measurements was 0.89 (32 of 36).
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Table 4 Pathologic (Significant Lesions, Occlusions, and Grafts Graded in Need of Revision) and Normal Findings by Epicardial Ultrasonography, Transit Time Flow Measurement, and Intraoperative Angiography Versus Pathologic and Normal Findings at Follow-Up Angiography
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Clinical Data at Follow-Up
The 1 graft found occluded at follow-up angiography (case 16) was successfully reoperated on with a radial artery graft to LAD. Of the 3 patients with significant graft stenosis, 1 (case 14) had percutaneous coronary intervention on the native LAD; the 2 others (cases 21 and 39) had stenoses at the heel of the distal anastomoses, had freedom from angina, and were left untreated. No major cardiac events were reported in the remaining patients at follow-up.
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Comment
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Epicardial ultrasonography is reported to be successfully used on all sides of the heart [18], but we limited the design to minimal manipulation and only the IMA-to-LAD anastomoses were assessed. The current study is the first to compare epicardial ultrasonography with intraoperative angiography. Normal findings by epicardial ultrasonography, transit time flow measurement and intraoperative angiography, largely predicted normal findings at follow-up examination.
As expected, the intraobserver variation of the diameter measurements in epicardial ultrasonography and intraoperative angiography was less than the interobserver variation. The diameter measurements obtained by epicardial ultrasonography correlated poorly with the same measurements obtained by both intraoperative and follow-up angiography. The good correlation between diameters measurements found by Tjomesland and colleagues [11], Suematsu and colleagues [10], and McPearson and associates [19] could thus not be confirmed in this series. The main explanatory factor for the lacking correlations is probably the analyses variability as reported by both methods. Accurate measurements of these diameters are difficult, particularly when using digital calipers. A quantitative analyzing system with arterial contour detection provides better reproducibility [20], but is difficult to implement automatically in the anastomosis area. A new method as epicardial ultrasonography should therefore probably not be evaluated by such diameter measurement alone, but compared with other techniques such as intraoperative angiography, allowing validation of the method’s capability to predict revision, like the NIR grading system.
For the visual grading of abnormal lesions and necessity for graft revision, few positive scores were present in this study, and therefore caution should be used in making conclusions. The correlation of angiography and epicardial ultrasonography was poor, as significant lesions after the FitzGibbon-classification in epicardial ultrasonography could not be found in intraoperative angiography and vice versa. The three grafts graded as thought to need revision by angiography were revised, and all had technical errors at surgical inspection. None of these findings was detected by epicardial ultrasonography or transit time flow measurements. Intraoperative angiography could thus be superior in detecting grafts in need of revision. One of these grafts, the only graft with obstructed flow (case 34), could have thrombosed in the time after the performance of epicardial ultrasonography and transit time flow measurement. The two other grafts revised because of dissection had nonobstructed flow, and were consequently difficult to detect by the ultrasound techniques.
Spasm is reported to be a problem in coronary artery surgery [21, 22], and spasm has already been shown to generate problems in the interpretation of intraoperative angiography [12, 14, 15, 23–25]. Considering the time delay between the performance of epicardial ultrasonography, transit time flow measurement, and intraoperative angiography, spasm may be another explanatory factor for the conflicting findings by the various methods. Spasm present at epicardial ultrasonography could have resolved at the time angiography was performed, and vessel wall edema or hemorrhage and intraluminal thrombus formation could have had time to develop in the time delay before angiography. The main cause of intraoperative spasm is probably the surgical manipulation of the arteries. Manipulation of the arteries by quality assessment instruments like the transit time flow probe, epicardial ultrasound probe, or angiographic catheters and injection of contrast media could also cause spasm, but are probably of less importance. In intraoperative evaluation of graft quality, the possible presence of spasm must therefore always be taken into account [12, 15, 23, 25]. Revision is reported to be performed after findings of significant lesions detected by one single measurement [3, 6, 23]. At our institution, we have become cautious in revising grafts based on one measurement only [14, 26]. By repeated measurement, after a time delay, the initial abnormalities often normalize and unnecessary revisions are avoided. Spasm and other intraoperative lesions are known to resolve at later follow-up examination [12]; therefore, special caution should be used in making conclusions when epicardial ultrasonography is compared with angiography performed postoperatively [4, 10, 11].
Verification of graft patency intraoperatively is problematic owing to the presence of intraoperative spasm [12, 25], the later normalizing of intraoperative lesions [12, 24], and the discrepancies between the different intraoperative graft assessment tools. The relationship between flow and morphology is complex, and the flow value per se is not a good indicator of the quality of the anastomosis [2]. Visual assessment of the flow curves of transit time flow measurements are probably not able to detect significant lesion with lesser degree than nearly occlusions [3], and discrepancies in graft assessment between transit time flow measurement and coronary angiography as found in this study are also earlier reported [26–28]. Desai and colleagues [29] showed that indocyanine green angiography, another promising method for intraoperative graft quality assessment, correlated well with coronary angiography, but provided better diagnostic accuracy for detecting lesions than transit time flow measurement. Many publications on epicardial ultrasonography are only feasibility studies [5, 8, 9], and are thus not able to evaluate the discrepancies found in our study.
In conclusion, these series indicated that intraoperative angiography is superior to epicardial ultrasonography and transit time flow measurements in detecting grafts in need of revision. Angiography must be considered the gold standard in intraoperative imaging. Epicardial ultrasonography could be a useful method in graft quality assessment, but needs to be further evaluated, preferably in comparative studies with intraoperative angiography.
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Acknowledgments
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We thank Milada Smaastuen, MS, Department of Medical Biostatistics, Rikshospitalet-Radiumhospitalet University Hospital, for help with the statistical analyses. The study was partly financed by a research grant from the Norwegian Association of Heart and Lung Patients.
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References
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Abstract
Introduction
