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Ann Thorac Surg 2005;79:580-584
© 2005 The Society of Thoracic Surgeons


Original article: Cardiovascular

Left Internal Thoracic Artery Graft Assessed by Means of Intraoperative Transesophageal Echocardiography

Kazumasa Orihashi, MD*, Taijiro Sueda, MD, Kenji Okada, MD, Katsuhiko Imai, MD

Division of Cardiovascular Surgery, Hiroshima University Hospital, Hiroshima, Japan

Accepted for publication July 12, 2004.

* Address reprint requests to Dr Orihashi, Division of Cardiovascular Surgery, Hiroshima University Hospital, Kasumi 1-2-3, Minami-ku, Hiroshima, 734-8551 Japan (E-mail: orichan{at}hiroshima-u.ac.jp).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: We report a method of intraoperative assessment of left internal thoracic artery (LITA) graft with transesophageal echocardiography regarding patency, stenosis, and presence of remnant branch artery.

METHODS: In 52 consecutive coronary artery bypass grafting surgery patients, blood flow velocity was measured at the origin of the LITA after coronary artery bypass grafting by means of transesophageal echocardiography. The flow pattern and velocity change at temporary clamping of the graft was examined and was compared with the postoperative angiographic findings.

RESULTS: The LITA was visualized in 47 of 52 cases (90.4%). The LITA flow was diastolic dominant, systolic dominant, or equivalent in 41, 3, and 3 cases, respectively. The anastomosis was stenotic in 2 of 6 cases of the latter two groups, but in none of the 41 cases with diastolic dominant flow (p = 0.0139). The branch artery was present in 4 of 6 cases of the latter two groups, but in only 2 of 41 cases with diastolic dominant flow (p = 0.0012). Remnant branch artery was found in all three cases with systolic dominant flow. The LITA flow was instantaneously reduced at clamping and recovered at declamping in every case with graft occlusion but one. The ratio of velocity change at clamping was less than 0.50 in all 41 cases without remnant branch, whereas it was more than 0.50 in 5 of 6 cases with a branch (p < 0.0001).

CONCLUSIONS: The transesophageal echocardiographic assessment with the clamp test is feasible intraoperatively in the majority of patients, enabling us to assess LITA graft patency, stenosis, or presence of a remnant branch.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
In coronary artery bypass grafting (CABG), occlusion or stenosis of grafts can occur despite the meticulous efforts of the surgeon. Although postoperative coronary angiography (CAG) can determine the success of CABG, this comes too late to save the situation. Therefore, a surgeon will often try to assess the graft, by palpation, while in the operating theater. However, this method is misleading because pulsation can be present within the graft even when the anastomosis is occluded. Thus, a number of diagnostic modalities have been introduced for assessing the graft, so as to allow the decision to redo the anastomosis to be made within the operating theater. These modalities include intraoperative CAG [1, 2], transit-time measurement [3, 4], color Doppler imaging [5, 6], continuous-wave Doppler [7], and thermal CAG [8]. However, additional dedicated equipment needs to be prepared for each modality, and the introduction of robotic surgery may further limit the use of these modalities.

Postoperative CAG occasionally reveals a remnant branch artery from the left internal thoracic artery (LITA), such as the intercostal artery or the thymic branch, to which the blood may be diverted when the anastomosis is stenotic. The branch artery can be divided if its presence is diagnosed in the operating theater; unfortunately, the diagnostic modalities listed above are not capable of detecting it.

We have recently developed a method for assessing the LITA graft as well as for detecting the presence of a remnant branch artery by means of intraoperative transesophageal echocardiography (TEE). This paper reports our technique for assessing the LITA flow using TEE, and presents the results of our experience.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
This study was approved by our institutional ethics committee on human research, and informed consent was obtained from every patient. The 52 consecutive patients who underwent CABG in our institute were enrolled. These included 37 men and 15 women, with ages ranging from 48 to 83 years (mean, 68.8 years). The LITA graft was anastomosed to the left anterior descending artery in every case. Off-pump CABG surgery was performed in four cases.

After induction of anesthesia, a 5-MHz biplane TEE (EUB-555; Hitachi Medical Co Inc, Tokyo, Japan) was instituted for intraoperative monitoring and diagnostic imaging. The TEE examination for LITA assessment was conducted by a single TEE operator (KO) in every case. The origin of the LITA was visualized with TEE as previously reported [9]. The long-axis view of the aortic arch was visualized in the transverse scan (0 degrees for multiplane TEE) with a horizontal scanning plane. By withdrawing the probe, the image of the aortic arch was replaced with the short-axis view of the left subclavian artery (LSCA), often adjacent to the left common carotid artery. As the probe was further withdrawn, keeping the LSCA in the screen by rotating the probe counterclockwise, the LSCA coursed horizontally and was depicted in the long axis, extending to the bottom of the screen. The LITA was found to arise from the LSCA toward the left of the screen (or anteriorly, within the body; Fig 1). The color Doppler mode was often helpful for finding the LITA flow. When it was difficult to visualize the LSCA in the transverse scan, the longitudinal scan (90 degrees for multiplane TEE) was used instead, in which case the LITA arose from the LSCA toward the left of the screen (or caudally, in the body).



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Fig 1. (A) Computed tomogram showing the orientation of scanning plane of transesophageal echocardiography for visualizing the left internal thoracic artery (LITA) arising from the left subclavian artery (LSCA: arrow). The sector indicates the scanning area. (B) The transesophageal echocardiographic view of the LSCA and the LITA, which is directed toward the small arrow. The large arrow indicates the direction of flow in the LSCA. (E = esophagus; T = trachea.)

 
After the LITA was anastomosed to the left anterior descending coronary artery and the clamp was released, the blood flow velocity was measured using pulsed-wave Doppler mode with the sampling volume placed on the LITA a few millimeters distal to the origin to avoid collecting the signal from the LSCA. While the blood flow was clearly and stably recorded, the LITA graft was clamped for a few seconds (by the surgeon), and then declamped (this is called the clamp test). Images of the LITA and changes in blood flow between clamping and declamping were recorded on S-VHS tape for later analysis.

From the recorded data, the following variables were measured with an off-line personal computer: (1) the distance from the transducer (at the esophagus) to the origin of the LITA (the sampling position); (2) the character of the flow pattern in the LITA graft, which was either systolic dominant or diastolic dominant, or systolic/diastolic equivalent (S/D equivalent); and (3) the velocity change by clamping, calculated as the ratio of diastolic peak velocity at clamping to that at declamping (Vc/Vd). In determining the flow pattern, the time-velocity integral of both the diastolic and systolic components of the LITA flow was measured, and the ratio of diastolic time-velocity integral to systolic time-velocity integral was calculated. When this ratio was higher than 1.10, the flow was defined as diastolic dominant. When it was lower than 0.90, the flow was defined as systolic dominant. The flow was defined as S/D equivalent when the ratio was between 0.90 and 1.10.

In the postoperative CAG, which was routinely performed at approximately 2 weeks postoperatively, the LITA graft was assessed with regard to (1) patency of the graft; (2) stenosis or occlusion at the anastomosis; and (3) presence of remnant branch arteries from the LITA graft. The branch artery was determined to be significant when its diameter was larger than 50% of that of the LITA graft.

The data were expressed as mean ± standard deviation. The difference in incidence between the two groups was examined according to the {chi}2 method using Fisher's exact probability test. The difference was considered to be statistically significant when the p value was less than 0.05.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
The intraoperative and postoperative courses were uneventful in all but 1 patient, in which the LITA graft was occluded during surgery (described in detail below). There were no complications related to the TEE manipulations for visualizing the LITA. No evidence of graft injury by the clamp test was found in the postoperative CAG.

The LITA was successfully visualized, and the blood flow was successfully recorded during the clamp test in 47 of 52 patients (90.4%). The remaining analysis is restricted to these 47 patients. The origin of the LITA was located close to the esophagus: the distance varied from 16.6 to 74.6 mm (29.7 ± 9.9 mm), and was within 40 mm in 42 of the 47 patients. The postoperative CAG revealed that the LITA graft was patent in every case, but with significant stenosis (>75%) at the anastomosis in 2 patients (4.3%). A remnant branch artery on the LITA graft was found in 6 patients (12.8%).

The blood flow in the LITA graft was diastolic dominant (Fig 2A) in 41 patients, as reported by several investigators [7, 10, 11], and was systolic dominant (Fig 2B) or S/D equivalent (Fig 2C) in 3 patients each. The anastomosis was stenotic in 2 of 6 patients with nondiastolic dominant flow (S/D equivalent or systolic dominant); none of the 41 patients with diastolic dominant flow had a stenotic anastomosis (p = 0.0139). The flow pattern was S/D equivalent in both patients with stenotic anastomosis. The branch artery was present in 4 of 6 patients with nondiastolic dominant flow, but in only 2 of 41 patients with the diastolic dominant pattern (p = 0.0012). In particular, all 3 patients with systolic dominant flow had a significant remnant branch artery.



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Fig 2. Three patterns of left internal thoracic artery blood flow measured with transesophageal echocardiography. (A) Diastolic (D) dominant pattern. (B) Systolic (S) dominant pattern. (C) Systolic/diastolic equivalent pattern.

 
As soon as the LITA graft was clamped, the diastolic component of LITA flow was noticeably reduced (Fig 3A), but it returned to the previous level immediately after declamping (Fig 3B). The Vc/Vd ratio varied among individual patients from 0.19 to 0.80 (0.39 ± 0.12); it was greater than 0.50 in 5 of 6 patients with remnant branch artery, whereas it was less than 0.50 in all of the remaining 41 patients (p < 0.0001).



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Fig 3. The left internal thoracic artery (LITA) flow change at clamping (A) and declamping (B) the LITA graft measured by transesophageal echocardiography. As soon as the graft is clamped, the velocity is apparently reduced and it recovers to the previous level on declamping. (D = diastolic flow; S = systolic flow.)

 
One patient (a 72-year-old woman) had an unusual intraoperative course. Left ventricular contraction was good immediately after she was weaned from cardiopulmonary bypass. The LITA flow velocity was apparently reduced by clamping the graft (Vc/Vd was 0.40), but the flow pattern was systolic dominant. After chest closure, ST elevation appeared, and TEE demonstrated dyskinesis at the left ventricular apex. The chest was immediately reopened, and the LITA graft was explored for the cause of this event. Although the surgeon could feel pulsation of the LITA graft, its flow pattern was to-and-fro as if the graft had been clamped. There was no change of velocity during the clamp test. The surgeon decided to reanastomose the LITA graft. The graft was found to be occluded as a result of localized dissection near the anastomosis. After the graft was reanastomosed, the LITA flow became diastolic dominant. The left ventricular contraction improved. The clamp test showed an appropriate velocity change. Although she had repeated events of nonsustained ventricular tachycardia postoperatively, these were able to be medically controlled and she recovered without sequelae. Postoperative CAG showed that the LITA graft was patent without stenosis. Thus, absence of velocity change at clamping occurred only in this 1 patient, whereas apparent velocity change was present in the remaining 46 patients (p = 0.0213). There were no false-positive or false-negative results.


    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
This study has clarified that (1) the origin of the LITA can be successfully visualized by TEE in more than 90% of CABG cases; (2) the flow pattern in the LITA is normally diastolic dominant, as reported by other investigators [7, 10, 11]; (3) a nondiastolic dominant flow pattern may predict undesirable results of grafting or anastomosis, whereas an S/D equivalent flow pattern is closely related to stenotic anastomosis, and a systolic dominant flow pattern is associated with the presence of a remnant branch artery; (4) an inadequate decrease of flow during the clamp test indicates the presence of a remnant branch artery; and (5) a to-and-fro pattern of LITA flow with or without velocity change during the clamp test indicates an occluded graft. The possible mechanism is illustrated in Figure 4.



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Fig 4. Schematic illustration showing the mechanism of flow changes. (A) The left internal thoracic artery (LITA) flow indicates the inflow to the left anterior descending coronary artery (LAD). (B) When the anastomosis is stenotic, the diastolic (D) component is reduced, showing systolic/diastolic equivalent pattern. (C) When the graft is occluded, the flow is markedly reduced. The systolic (S) component becomes a to-and-fro pattern. (D) As the graft is temporarily clamped, the flow pattern becomes to-and-fro. (E) When the remnant branch artery is present, the systolic component is increased. (F) The blood flow remains after the graft is clamped and reduction in the LITA flow is inadequate. (LSCA = left subclavian artery.)

 
Previous investigators have studied the patterns of LITA flow without clamping and reported that (1) the blood flow pattern in the LITA graft is diastolic dominant after anastomosis and (2) when the graft is occluded, the blood flow in diastole is reduced or absent and the flow pattern becomes systolic dominant [7, 10–12]. Clamping of the graft temporarily produces an occlusion, and the LITA flow pattern becomes to-and-fro (Figs 4A–4D). A similar pattern was seen in the patient with accidental graft occlusion. When the anastomosis is stenotic, the diastolic component is reduced and the flow pattern becomes S/D equivalent, as was seen in 2 patients in this series (Fig 4B).

The systolic dominant pattern detected in 3 patients indicated the presence of a remnant branch artery (Fig 4E). When the branch artery is present, the LITA conveys the flow to the coronary artery as well as to the branch artery; when the graft is clamped, the former component is lost and the latter remains (Fig 4F). Thus, inadequate reduction of flow by clamping indicates the presence of a remnant branch. The cutoff value of Vc/Vd ratio for detecting the remnant branch was 0.5 in this study, but this figure can vary in accordance with the criteria for a significant branch artery. After this series, we experienced 1 patient with a Vc/Vd ratio larger than 0.50. On the basis of this information, the surgeon searched for the remnant branch artery, which was found. As it was divided, the Vc/Vd ratio became greater than 0.5. These results indicate that the branch artery is perfused not only during systole but also during diastole and that more than half of the diastolic blood flow is directed to the branch artery.

Our method is unique in its tactic of examining the change in blood flow velocity during temporary occlusion of the LITA graft. The change occurs instantaneously and is readily apparent. Although the incidence angle of the ultrasound transducer to the LITA is often large and is not suitable for measuring the absolute value of velocity, this presents no problem because only the flow patterns and velocity change ratio at clamping are important.

The current method is advantageous because no additional equipment needs to be prepared and the surgical procedures are minimally interrupted. It should be equally feasible and convenient during minimally invasive CABG or even in robotic surgery. In addition, the LITA flow pattern can be assessed after chest closure, at which time there is the potential for the LITA graft to become kinked at the pericardium.

There are, however, several limitations to this method. It is not always easy to identify the origin of the LITA using TEE; the technique requires practice to master it. We failed to visualize the origin of the LITA in 3 patients despite elaborate manipulations of the TEE. Also, it occasionally took longer than several minutes to visualize the LITA, and it was considered futile to spend more than 10 minutes trying to find it. Therefore, we abandoned the attempt to visualize the LITA when the surgeon was ready to close the pericardium.

The time lag between TEE assessment and postoperative CAG is another limitation because there can be changes at both the LITA graft and the anastomosis during this period, including tissue edema, local spasm, and thrombosis.

Color Doppler imaging was often helpful to locate the LITA. A useful clue was the tendency for diastolic dominant flow in the LITA in contrast to the systolic dominant flow in other arteries. The LITA was ultimately identified by confirming the presence of velocity change during the clamp test. Unfortunately, this method is only applicable to the LITA (and possibly the right internal thoracic artery) at present, and not to other grafts with proximal anastomoses to the ascending aorta. Further study is needed to be able to visualize and assess every graft using TEE.

Although not feasible for every patient, this method gives confidence to the surgeon once the LITA is successfully visualized and seen to have a diastolic dominant flow pattern and velocity change during the clamp test (with Vc/Vd > 0.50). In all 38 patients with these TEE findings, the postoperative assessment was excellent, whereas 8 of 9 patients who did not meet one or more criteria proved to have either stenotic anastomosis or a remnant branch artery (p < 0.0001). Lisboa and coworkers [13], by using transthoracic echocardiography in 72 consecutive patients, reported an LITA image and flow signal acquisition rate of 90.3%, a specificity of 96.8%, and a sensitivity of 50% when compared with the postoperative angiographic assessment. The diagnostic accuracy of our method seems to be comparable to transthoracic echocardiographic assessment, although further investigation with more patients is needed to confirm this.

In conclusion, TEE assessment of the LITA flow pattern along with the clamp test is a clinically feasible technique in the majority of CABG patients and provides postoperative assessment of the LITA within the operating theater.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Hol PK, Fosse E, Lundblad R, et al. The importance of intraoperative angiographic findings for predicting long-term patency in coronary artery bypass operations Ann Thorac Surg 2002;73:813-818.[Abstract/Free Full Text]
  2. Lazzara RR, McLellan BA, Kidwell FE, et al. Intraoperative angiography during minimally invasive direct coronary artery bypass operations Ann Thorac Surg 1997;64:1725-1727.[Abstract/Free Full Text]
  3. Walpoth BH, Bosshard A, Genyk I, et al. Transit-time flow measurement for detection of early graft failure during myocardial revascularization Ann Thorac Surg 1998;66:1097-1100.[Abstract/Free Full Text]
  4. Hirotani T, Kameda T, Shirota S, et al. An evaluation of the intraoperative transit time measurements of coronary bypass flow Eur J Cardiothorac Surg 2001;19:848-852.[Abstract/Free Full Text]
  5. Arruda AM, Dearani JA, Click RL, et al. Intraoperative application of power Doppler imaging: visualization of myocardial perfusion after anastomosis of left internal thoracic artery to left anterior descending coronary artery J Am Soc Echocardiogr 1999;12:650-654.[Medline]
  6. Oda K, Hirose K, Nishimori H, et al. Assessment of internal thoracic artery graft with intraoperative color Doppler ultrasonography Ann Thorac Surg 1998;66:79-81.[Abstract/Free Full Text]
  7. Cartier R, Dias OS, Pellerin M, et al. Changing flow pattern of the internal thoracic artery undergoing coronary bypass grafting: continuous-wave Doppler assessment J Thorac Cardiovasc Surg 1996;112:52-58.[Abstract/Free Full Text]
  8. Falk V, Walther T, Philippi A, et al. Thermal coronary angiography for intraoperative patency control of arterial and saphenous vein coronary artery bypass grafts: results in 370 patients J Card Surg 1995;10:147-160.[Medline]
  9. Orihashi K, Matsuura Y, Sueda T, et al. Aortic arch branches are no more blind zone for transesophageal echocardiography: a new eye for aortic surgeons J Thorac Cardiovasc Surg 2000;120:466-472.[Abstract/Free Full Text]
  10. Arruda AM, Pellikka PA, Mahoney DW, et al. Transthoracic Doppler echocardiographic comparison of left internal mammary grafts to left anterior descending coronary artery with ungrafted right internal mammary arteries in patients with and without myocardial ischemia by dobutamine stress echocardiography Am J Cardiol 2000;86:919-922.[Medline]
  11. Katz WE, Zenati M, Mandarino WA, et al. Assessment of left internal mammary artery graft patency and flow reserve after minimally invasive direct coronary artery bypass Am J Cardiol 1999;84:795-801.[Medline]
  12. Hata M, Shiono M, Orime Y, et al. Doppler features of occlusion of the internal thoracic artery due to preoperative branch embolization Jpn Circ J 1999;63:819-821.[Medline]
  13. Lisboa LA, Dallan LA, De Figueiredo LF, et al. A prospective comparison of Doppler echocardiography and postoperative angiography in the assessment of left internal thoracic artery graft in 72 patients submitted to minimally invasive direct coronary artery bypass Heart Surg Forum 2002;5(Suppl 4):S362-77.



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K. Orihashi, K. Okada, K. Imai, T. Kurosaki, T. Takasaki, S. Takahashi, K. Morifuji, and T. Sueda
Intraoperative assessment of coronary bypass graft to posterior descending artery by means of transesophageal echocardiography
Interactive CardioVascular and Thoracic Surgery, May 1, 2009; 8(5): 507 - 511.
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