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Asian Cardiovasc Thorac Ann 2007;15:86-90
© 2007 Asia Publishing EXchange Ltd


ORIGINAL CONTRIBUTIONS

Effect of the Cardiac Cycle on the Coronary Anastomosis Assessed by Ultrasound

Khalid S Ibrahim, MD1, Lasse Løvstakken, MSc1, Idar Kirkeby-Garstad, PhD2, Hans Torp, PhD1, Harald Vik-Mo, PhD1, Rune Haaverstad, PhD1,2

1 Institute of Circulation and Imaging Techniques, Norwegian University of Science and Technology
2 Department. of Cardiothoracic Surgery, Trondheim University Hospital, Trondheim, Norway

For reprint information contact: Rune Haaverstad, PhD Tel: 47 73 867 000 Fax: 47 73 867 029 Email: rune.haaverstad{at}ntnu.no, Department of Cardiothoracic Surgery, University Hospital of Trondheim, N-7018 Norway.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Anastomosis of the left internal mammary artery to the left anterior descending artery was performed in 9 pigs to evaluate the effect of changes in the cardiac cycle and the choice of ultrasound mode on assessment of graft morphology. The length of the anastomosis and the diameters of the left anterior descending artery at the toe and heel of the anastomosis, as well as downstream, were measured in end-systole and end-diastole with both B-mode and color Doppler imaging. None of the diameters were influenced by the cardiac cycle using either ultrasound mode. B-mode yielded larger diameters at all points except the toe of the anastomosis. It was concluded that provided the scanning is perpendicular to the vessel, the morphology of an anastomosis can be assessed without paying much attention to the phase of the cycle or the mode of ultrasound applied.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The success of coronary artery bypass grafting (CABG) is determined by the long-term patency of the graft. This depends mainly on the quality of distal anastomoses, particularly that between the left internal mammary artery (LIMA) and the left anterior descending artery (LAD).1 Although off-pump CABG may reduce some of the risks and complications related to on-pump CABG, it is technically more demanding and carries a higher risk of technical failure.2 Thus, quality control of distal anastomoses before completion of the operation is of the utmost importance, particularly during off-pump CABG. Detecting an anastomotic error enables the surgeon to revise the anastomosis, and so reduce postoperative morbidity and mortality.3

Distal anastomoses can be evaluated intraoperatively by graft flow measurements or by direct visualization using ultrasound scanning or angiography. Transit-time flowmetry is the most common intraoperative method used to assess coronary bypass grafts, but it is not very sensitive as blood flow is influenced by resistance in the peripheral coronary circulation. This technique detects a technical failure only if there is severe stenosis in the graft or at the site of anastomosis.46 Epicardial imaging of coronary arteries and anastomoses with high frequency ultrasound is simple and safe.7 It has several advantages over angiography; it is noninvasive, requiring no injection of contrast medium.8 Moreover, comparing epicardial ultrasound with angiography at the 8-month follow-up has shown that the former has excellent prognostic value.8 B-mode (Figure 1Go) and color-flow (Figure 2Go) imaging allow visualization of the anastomosis and its components (coronary artery and graft conduit) as well as the bloodstream.7 However, the best modality for determining the morphology of the anastomosis has not been investigated. Moreover, the effects of the cardiac cycle on the coronary arteries are largely unknown. Hence, we assessed the morphology of LIMA-LAD anastomoses in the pig together with the changes induced by the cardiac cycle, using B-mode and color Doppler ultrasound scanning.


Figure 1
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Figure 1. Ultrasound scan of the left internal mammary artery-left anterior descending artery anastomosis in longitudinal view by B-mode. The anterior and posterior intimal echo patterns are shown by arrows. The intimal echo pattern indicates that the ultrasound beam is perpendicular to the left anterior descending artery intima. The left internal mammary artery is seen top right and the flow direction is to the left of the picture.

 

Figure 2
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Figure 2. Color-flow image of the left internal mammary artery-left anterior descending artery anastomosis in longitudinal view. The left internal mammary artery is top right and the direction of blood flow is to the left of the picture.

 

    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Nine pigs weighing 60–85 kg underwent LIMA-LAD grafting under general anesthesia at the animal experimental laboratory at Trondheim University Hospital. Seven pigs had off-pump CABG, and 2 had LIMA grafting under cardiopulmonary bypass. All operations were carried out by the same surgeon (RH). Animals received humane care in accordance with the European Convention on Animal Care and the Norwegian national regulations; the Norwegian Ethics Committee on Animal Research approved the protocol. All pigs were premedicated with intramuscular azaperone 6 mg · kg–1 and diazepam 0.15 mg · kg–1. Anesthesia was induced with intravenous atropine 0.15 mg · kg–1, ketamine 7 mg · kg–1, and thiopentone 3 mg · kg–1. Maintenance infusions were of fentanyl 63 µg · kg–1 · min–1 and midazolam 0.6 mg · kg–1 · min–1 combined with isoflurane 1% in a 1:2 mixture of oxygen and air. The pigs were artificially ventilated through a tracheotomy tube.

After a median sternotomy and full heparinization (3 mg · kg–1), the LIMA was harvested with its pedicle, and prepared. The LAD was identified and snared with 4/0 pledgeted polypropylene suture proximal to the coronary arteriotomy. After 3–5 min of ischemic preconditioning, the snare was released and an Axius Xpose access device (Guidant, Santa Clara, CA, USA) and an Axius vacuum stabilizer were applied to pull the heart and immobilize the LAD site chosen for grafting. After arteriotomy, an Axius coronary shunt was placed into the vessel lumen. The coronary anastomosis was performed with a continuous 7/0 polypropylene suture, aiming to create a patent anastomosis without technical failure. The snare was applied again to the LAD proximal to the anastomosis. Following epicardial ultrasound assessment of the anastomoses, the apical stabilizer was removed and the heart placed back into the pericardium.

For on-pump LIMA-LAD anastomosis, the approach to the heart, LIMA harvesting, and heparinization were the same as in the off-pump group. Cardiopulmonary bypass was instituted by cannulation of the left axillary artery and the right atrium. After aortic cross clamping, crystalloid cardioplegia solution was infused into the aortic root. The coronary anastomosis was performed with a continuous 7/0 polypropylene suture. The snare was applied again to the LAD proximal to the anastomosis. The 2 pigs were easily weaned off cardiopulmonary bypass without inotropic support so that LIMA-LAD scanning could be carried out.

After completion of the LIMA-LAD anastomosis and with the stabilizer still in place, epicardial ultrasound imaging was performed with a GE Vingmed Vivid 7 (GE Vingmed Ultrasound, Horten, Norway) ultrasound scanner and a GE i13L probe. This probe is a linear-array mini-transducer designed for intraoperative imaging, operating at frequencies of 10–14 MHz. The ultrasound system was optimized for high-resolution color-flow imaging applications and achieved a frame rate of 16 frames per second. Using gel as the conduction medium, the transducer was gently applied directly on the anastomosis, between the paddles of the stabilizer. Real-time ultrasound images of the complete anastomosis as well as the distal run-off were stored as digital data for later analysis. The morphology of the anastomosis was assessed by measuring its dimensions (Figure 3Go): the length of the anastomosis proper (DA), the LAD diameter at the toe (D1) and heel (D3) of the anastomosis, and 5–10 mm distal to the toe (D2). The electrocardiogram was recorded continuously together with the images and was used to define diastole. Intraoperatively and before the epicardial ultrasound, graft flow was monitored by transit-time flowmetry (Medi-Stim Butterfly Flowmeter, Medi-Stim AS, Oslo, Norway).


Figure 3
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Figure 3. Diagram of the left internal mammary artery-left anterior descending artery anastomosis: diameters of the left anterior descending artery at the toe of the anastomosis (D1), 5–10 mm distal to the toe (D2), and at the heel (D3), DA = diameter of the anastomosis proper.

 
The results are presented as mean ± 1 standard deviation. Analysis of variance (ANOVA) for repeated measurements was used to assess the impact of the ultrasound modality (B-mode or color-flow), the cardiac cycle (end-systole or end-diastole), and the sites of measurement (D1, D2, D3, or DA) on the morphology of the anastomosis and the LAD. For variables significantly influencing the measured dimensions, we applied the paired t test with the Bonferroni correction, according to the number of comparisons carried out, as post hoc analyses for identification of the difference between values. A p value less than 0.05 was considered significant. The statistical analysis was carried out using SPSS version 12 software (SPSS Inc, Chicago, IL, USA).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
All animals remained hemodynamically stable throughout the operation, as confirmed by a satisfactory mean arterial pressure of 76 ± 6.3 mm Hg. The mean systolic blood pressure was 111 ± 8.1 mm Hg and the mean diastolic blood pressure was 57 ± 6.6 mm Hg. All 9 LIMA-LAD anastomoses were satisfactory and found to be fully patent by both ultrasound modalities.

There was no significant effect of the cardiac cycle on LAD diameters D1, D2, D3, and DA by either B-mode or color Doppler imaging ( p = 0.989 by ANOVA; Table 1Go). B-mode imaging yielded larger diameters than color-flow Doppler, regardless of the phase of the cardiac cycle ( p ≤ 0.0001 by ANOVA). B-mode showed larger LAD diameters at the heel (D3) and downstream LAD (D2), as well as a longer anastomosis (DA) than that observed in color Doppler imaging. The diameter of the LAD at the toe was found to be similar with both ultrasound modes (Table 2Go).


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Table 1. Diameters of LIMA-LAD Anastomoses in End-Systole and End-Diastole in B-mode and Color Doppler
 

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Table 2. Mean (Systolic and Diastolic) Diameters of LIMA-LAD Anastomoses in B-mode and Color Doppler
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although porcine coronary arteries have been measured by epicardial ultrasound, this study used the best available technology, emphasizing key technical aspects to obtain good quality images and reliable measurements.9 Small changes in coronary diameters during the cardiac cycle have been found using intravascular ultrasound (IVUS); a 10% increase was detected in healthy vessels and a 2%–12% increase in atherosclerotic vessels.1013 Although most of the coronary blood flow occurs in diastole, the systolic expansion of coronary vessels can be explained by the increase in coronary intraluminal pressure during systole.10 Instantaneous recording of coronary flow and pressure along with IVUS measurements of coronary internal diameters have demonstrated that systolic expansion is preceded by an increase in intraluminal pressure and a maximal increase in diameter occurring in mid to late systole. In our study, no significant changes in the diameter of the LAD at the heel, toe, anastomosis proper, or distally were detected during the cardiac cycle. We believe that the different outcome was most likely due to the following reasons. Firstly, epicardial imaging is not as sensitive as IVUS to discriminate very minor changes; a systolic increase of coronary diameter of 10% is equivalent to a 0.1–0.15-mm increase in diameter. Secondly, grafting of the LAD caused stiffness of the vessel wall, and this may well have reduced systolic expansion of the coronary artery, whereas IVUS measurements were taken on coronary vessels that had not undergone any surgical manipulation.

The color-flow image mode showed a slightly longer DA measurement in systole than in diastole. This morphological difference between the two phases of the cardiac cycle might be attributable to distension of the LIMA wall secondary to the increase in intraluminal pressure that occurs in the distal part of the mammary artery in systole. This hypothesis is supported by the results of an IVUS study demonstrating elongation and thinning of the vessel wall during systole.9 Nonetheless, the length of the anastomosis proper is usually adequate throughout the cardiac cycle and is not likely to impair blood flow through the LIMA-LAD anastomosis. Changes in the dimensions of the coronary vessel wall during the cardiac cycle may be more accurately detected by IVUS, as this technique is better for visualizing the complete internal circumference of the vessel by transverse view plane and synchronous measurement of intracoronary blood pressure. On the other hand, intraoperative epicardial scanning is much easier to perform than IVUS, because the latter entails sophisticated equipment and invasive manipulations that greatly limit its routine application.

On clinical grounds, provided the scanning is directed perpendicular to the vessel, this study showed that the surgeon can assess the morphology of an anastomosis without paying much attention to the phase of the cardiac cycle or the mode of ultrasound applied. B-mode imaging complies fully with the peristaltic movement of the artery, whereas color filling more easily enters the vessel boundaries. Therefore, we believe that B-mode yields more precise measurements because it gives a more detailed view of the anastomosis, enabling the surgeon to assess the intimal echo pattern very clearly. Color Doppler, however, enables the surgeon to evaluate graft patency because it provides very useful information on the pattern and direction of blood flow within the anastomosis. For a thorough evaluation of a coronary distal anastomosis, both B-mode and color-flow imaging should be applied in addition to flowmetry; color-flow with the aim of assessing anastomotic patency, and B-mode to provide precise measurements of the anastomosis dimensions.

We believe that future intraoperative evaluation of coronary grafts and anastomoses will consist of the combined approach of flowmetry and epicardial ultrasound. Patency of grafts is assessed by flow analysis, whereas ultrasound is applied to detect anastomotic failures. In this animal study, the cardiac cycle did not play any significant role in the assessment by epicardial ultrasound. Thus, if this is confirmed clinically, combined flowmetry and epicardial ultrasound has the potential for complete graft assessment in CABG surgery.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Grover FL, Johnson RR, Marshall G, Hammermeister KE. Impact of mammary grafts on coronary bypass operative mortality and morbidity. Department of Veterans Affairs Cardiac Surgeons. Ann Thorac Surg 1994;57:559–69.[Abstract]

  2. D’Ancona G, Karamanoukian HL, Salerno TA, Schmid S, Bergsland J. Flow measurement in coronary surgery. Heart Surg Forum 1999;2:121–4.[Medline]

  3. Haaverstad R, Vitale N, Tjomsland O, Tromsdal A, Torp H, Samstad SO. Intraoperative color Doppler ultrasound assessment of LIMA-to-LAD anastomoses in off-pump coronary artery bypass grafting. Ann Thorac Surg 2002;74:S1390–4.[Abstract/Free Full Text]

  4. Barnea O, Santamore WP. Intraoperative monitoring of IMA flow: what does it mean? Ann Thorac Surg 1997;63:S12–7.[Medline]

  5. Jaber SF, Koenig SC, BhaskerRao B, VanHimbergen DJ, Cerrito PB, Ewert DJ, et al. Role of graft flow measurement technique in anastomotic quality assessment in minimally invasive CABG. Ann Thorac Surg 1998;66:1087–92.[Abstract/Free Full Text]

  6. Hol PK, Fosse E, Mork BE, Lundblad R, Rein KA, Lingaas PS, et al. Graft control by transit time flow measurement and intraoperative angiography in coronary artery bypass surgery. Heart Surg Forum 2001;4:254–8.[Medline]

  7. Haaverstad R, Vitale N, Williams RI, Fraser AG. Epicardial colour-Doppler scanning of coronary artery stenoses and graft anastomoses. Scand Cardiovasc J 2002;36:95–9.[Medline]

  8. Tjomsland O, Wiseth R, Wahba A, Tromsdal A, Samstad SO, Haaverstad R. Intraoperative color Doppler ultrasound assessment of anastomoses of the left internal mammary artery to the left anterior descending coronary artery during off-pump coronary artery bypass surgery correlates with angiographic evaluation at the 8-month follow-up. Heart Surg Forum 2003;6:375–9.[Medline]

  9. Klein P, Meijer R, Eikelaar J, Gründeman PF, Borst C. Epicardial ultrasound in off-pump coronary artery bypass grafting: potential aid in intraoperative coronary diagnostics. Ann Thorac Surg 2002;73:809–12.[Abstract/Free Full Text]

  10. Weissman NJ, Palacios IF, Weyman AE. Dynamic expansion of the coronary arteries: implications for intravascular ultrasound measurements. Am Heart J 1995;130:46–51.[Medline]

  11. Ge J, Erbel R, Gerber T, Gorge G, Koch L, Haude M, et al. Intravascular ultrasound imaging of angiographically normal coronary arteries: a prospective study in vivo. Br Heart J 1994;71: 572–8.[Abstract/Free Full Text]

  12. Peters RJ, Kok WE, Rijsterborgh H, van Dijk M, Koch KT, Piek JJ, et al. Reproducibility of quantitative measurements from intracoronary ultrasound images. Beat-to-beat variability and influence of the cardiac cycle. Eur Heart J 1996;17:1593–9.[Abstract/Free Full Text]

  13. Alfonso F, Macaya C, Goicolea J, Hernandez R, Segovia J, Zamorano J, et al. Determinants of coronary compliance in patients with coronary artery disease: an intravascular ultrasound study. J Am Coll Cardiol 1994;23:879–84.[Abstract]





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