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Eur J Cardiothorac Surg 2001;19:848-852
© 2001 Elsevier Science NL

An evaluation of the intraoperative transit time measurements of coronary bypass flow

Takashi Hirotani, Tadashi Kameda, Shogo Shirota, Yoshihisa Nakao

Department of Cardiovascular Surgery, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-ku, Tokyo 108-0073, Japan

Received 26 September 2000; received in revised form 16 February 2001; accepted 21 March 2001.

Corresponding author. Tel.: +81-3-3451-8211; fax: +81-3-3457-7949
e-mail: hero.takashi{at}nifty.ne.jp


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Objective: The intraoperative measurement of the coronary bypass flow enables the identification of technical errors while the sternum is still open. The transit-time flow method is able to effectively measure the internal thoracic artery graft flow. The aim of the present study was to analyze the factors which affected the bypass flow rate. Methods: We measured the blood flow of 291 in situ internal thoracic artery (ITA) and 190 saphenous vein (SV) grafts constructed in 171 patients undergoing coronary artery bypass grafting from December 1996 to March 2000 using this method during the surgery. All patients underwent postoperative coronary angiography before the patients were discharged. The blood flow rate of all bypass grafts constructed was assessed after the patients were weaned from cardiopulmonary bypass. Results: The mean flow rate of all ITA grafts was 65.1±36.7 ml/min and that of all SV grafts was 56.4±29.9 ml/min. According to analyses using correlation tests, the graft flow was found to significantly correlate with the grafted perfusion areas and the diameter of the bypassed coronary arteries. However, no significant difference was observed between the flow rates of the ITA grafts with and without stenosis or string phenomenon, but significant (P<0.0001) correlation was observed between the occurrence of a string sign and the degree of proximal stenosis of the recipient coronary artery. Regarding SV grafts, the mean flow rate of occluded grafts (29.2±20.5 ml/min) was significantly (P<0.0001) less than non-occluded grafts (56.4±29.9 ml/min). Conclusions: The bypass flow was affected by such a large number of factors that only measuring the bypass flow rate could not sufficiently predict either stenosed or narrowed grafts. However, ITA grafts bypassed to the coronary arteries with less stenosis were shown to more easily become narrowed.

Key Words: Flow • Coronary artery • Bypass grafting • Transit-time • String • Internal thoracic artery


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
The intraoperative measurement of coronary bypass flow enables the identification of technical errors while the sternum is still open. However, non-invasive flow measurements during surgery have been associated with a low sensitivity and a high variability. Flow measurements using electromagnetic waves have been shown to be useful in detecting occluded or severely stenosed saphenous vein grafts intraoperatively [1], but these measurements are affected by a large number of variables such as serum hemoglobin concentration or the angle between the probe and vessel. Especially, it appears unsteadier for them to measure the blood flow through small-caliber vessels like internal thoracic artery (ITA) grafts. On the other hand, ITA grafts are commonly used for the revascularization of the key vessels. Therefore, in the recent coronary artery surgery, it is quite important to measure ITA graft flow correctly. The transit-time method using the CardioMed Trace System (CM 2008; Medi-Stim AS, Oslo, Norway) is based on the Doppler principle and several studies have demonstrated this system to effectively measure the blood flow through arterial grafts [2].

We therefore measured the blood flow of 291 ITA grafts and 190 saphenous vein grafts constructed in 171 patients using this transit-time method during surgery. All of these patients underwent postoperative coronary angiography (CAG) before being discharged and all bypass grafts were checked to see whether or not technical errors were present. The aim of the present study was to analyze, especially regarding ITA grafts, the factors which affect the bypass graft flow rate and also evaluate the ability of this method to identify grafts with any technical problems or string signs before closing the sternum.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 5. Conclusion
 References
 
From December 1996 to March 2000, 213 consecutive patients undergoing coronary artery bypass grafting (CABG) at our institute all routinely underwent flow measurements of all bypass grafts using the transit-time method except for right gastroepiploic artery grafts because of their vasospastic characteristic. Among these 213 patients, 171 patients underwent postoperative CAG just before being discharged, and the status of all grafts was checked. The other 42 patients were excluded from this study since they did not undergo CAG postoperatively due to either patient refusal (n=24), renal dysfunction (n=17) or death (n=1). In this study, the data from these 171 patients who underwent postoperative CAG were retrospectively analyzed. Nineteen free ITA grafts which were made in these patients were also excluded from the subjects because most of our free ITA grafts were bypassed between the two segments of the same coronary artery beyond the stenotic lesion (coronary–coronary bypass) and therefore another variable, i.e. the amount of inflow to the grafts, might affect the bypass flow. As a result, the number of left and right in situ ITA grafts evaluated in this study was 159 and 132, respectively, while the number of saphenous vein grafts totaled 190.

The patient profiles of the subjects are summarized in Table 1.


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  		Table 1. Preoperative patient characteristicsa

 
2.1. Operative technique
After performing a median sternotomy, single or bilateral ITAs were mobilized from their origin to the distal end close to the bifurcation. The ITA pedicle was then wrapped with a gauze swab immersed in a papaverine solution. After systemic heparinization, the ascending aorta was cannulated. Next, the ITAs were dissected distally and a 0.05% papaverine solution was injected through a small Silastic cannula into the ITA. Thereafter, its free flow was assessed while the systolic blood pressure was kept above 100 mmHg. When it was lower than 100 mmHg, sufficient volume was loaded through the cannula inserted into the ascending aorta. Cardiopulmonary bypass (CPB) was performed under moderate hypothermia. Myocardial protection was carried out with antegrade crystalloid cardioplegia and topical cooling. Both proximal and distal anastomoses were performed during a single period of aortic occlusion. Grafting was attempted on all vessels measuring 1.5 mm or greater in diameter with 75% or greater obstruction regardless of the degree of distal runoff.

Left ITAs were used for the revascularization of left anterior descending arteries (LAD) and left circumflex arteries (LCX) as usual. Right ITAs were used for the revascularization of LAD anterior to the heart, LCX through the transverse sinus and right coronary arteries (RCA). The region to which each left or right ITA graft was bypassed is shown in Table 2. The saphenous vein grafts (n=190) were anastomosed to the LAD regions in 17 patients, the LCX regions in 90 patients and the RCA regions in 83 patients.


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  		Table 2. Regions to which each left or right ITA grafts were bypassed and the flow rate of the ITA graftsa

 
In principle, ITAs were used to revascularize the coronary artery with stenosis greater than 90% for fear that a competitive flow of the native coronary artery might cause the ITAs to become narrowed, although both the LAD and other coronary arteries with poor distal runoff were revascularized exclusively using ITA grafts regardless of the degree of the proximal stenosis.

After completing all distal and proximal anastomoses, blood flow was measured in all arterial and venous grafts, while grafts showing no wave forms on this examination were carefully checked and any distal anastomoses strongly suspected to have any problems were reconstructed. Finally, the blood flow rate of every bypass constructed was assessed after the patients were weaned from CPB, and the mean flow rate displayed on the monitor was noted as the bypass flow rate.

The bypass flow was measured by the transit-time method using the CardioMed Trace System with probes measuring 2 or 3 mm in size in order for them to fit the actual size of the vessels.

2.2. Statistical analysis
Quantitative variables that approximated a normal distribution were used as the means±standard deviation and were analyzed using Student's unpaired t-test. The correlation between the variables and the bypass flow rate was analyzed by the Spearman's correlation test, the Mann–Whitney test and the Kruskal–Wallis test as appropriate. Statistical significance was considered to exist with a P-value of less than 0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 5. Conclusion
 References
 
An average of 3.1±1.2 distal anastomoses was performed at operation. All patients received at least one arterial graft. Left ITAs were used in 167 patients as either pedicled (n=159) or free grafts (n=8), and right ITAs were used in 143 patients as either pedicled (n=132) or free grafts (n=11). Bilateral in situ ITAs were used in 125 patients (73%). Right gastroepiploic arteries were used in 26 patients. One patient died of pulmonary infarction (mortality 0.6%).

The mean free flow rate of the left and right ITAs was 89.5±31.5 ml/min and 97.6 ±36.8 ml/min, respectively. The difference was not statistically significant. Among 159 in situ left ITA grafts, four grafts were observed to have more than 75% stenosis at their anastomotic site and five grafts showed a string sign on the pre-discharge CAG. No left ITA grafts were occluded. Among 132 in situ right ITA grafts, one graft was observed to be occluded and three grafts were observed to have more than 75% stenosis at their anastomotic site. In addition, six grafts showed a string sign. The patency rate of all in situ ITA grafts was 99.7%, while the rate of in situ ITA grafts without occlusion, stenosis or a string sign was 93.5%. Regarding saphenous vein grafts, among the 190 grafts evaluated, 11 grafts were observed to be occluded and two grafts had more than 75% stenosis. The patency rate of all saphenous vein grafts was 94.2%. No grafts with any problems were found in both 19 free ITA grafts and 26 right gastroepiploic artery grafts. All patients in whom any problem in the bypass grafts was identified underwent stressed radioisotope (201Tl) scintigraphy before being discharged, and no residual ischemia was found anywhere.

The mean flow rate of all in situ ITA grafts without occlusion, stenosis or a string sign was 65.1±36.7 ml/min (left ITAs: 64.6±35.5 ml/min, right ITAs: 65.6±37.3 ml/min). The same rate of stenosed ITA grafts (n=7) was 53.6±26.2 ml/min and no statistically significant difference was found between that of ITA grafts with and without stenosis. The mean flow rate of ITA grafts which showed a string sign at the pre-discharge CAG (n=11) was 52.8±33.8 ml/min. No significant difference was found between the flow rate of ITA grafts with and without a string sign. The flow rate of one occluded ITA graft was 10 ml/min. This bypass was not reconstructed since a fine wave form was observed in the flow measurement.

One ITA graft showing no wave forms on the flow measurement was found to be kinked at its anastomotic site, and therefore it was reconstructed. Then, its mean flow rate increased from 0 to 30 ml/min.

The difference in the bypass flow rate according to the grafted perfusion areas is shown in Table 2. All left or right ITA grafts had a greater blood flow when it was bypassed to the LAD region than when it was bypassed to the diagonal artery (D) or the LCX region, and the difference was statistically significant (P=0.0002). In addition, regarding right ITA grafts, a significantly higher blood flow was observed when it was bypassed to the RCA region than when it was bypassed to either the D or the LCX region (P<0.0001).

The correlation tests were performed to determine the variables which had a significant correlation with the bypass flow rate among the following variables: the patients’ mean arterial blood pressure during the bypass flow measurements, the usage of a left or right ITA, the existence of stenosis at an anastomotic site, the existence of a string sign, grafted perfusion areas (LAD, D, LCX or RCA), the free flow rate of ITAs, the degree of the proximal stenosis of the bypassed coronary arteries, and the diameter of the bypassed coronary arteries determined by intraoperative probing of the vessel. Among these variables, the ITA graft flow correlated significantly with grafted perfusion areas and the diameter of the bypassed coronary arteries (Table 3).


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  		Table 3. Correlation between the bypass flow rate and variables

 
In four of 11 patients in whom the ITA graft showed a string sign at the pre-discharge CAG, the degree of proximal stenosis of the recipient coronary artery had regressed in comparison to that observed at the preoperative CAG. The Kruskal–Wallis test indicated a significant (P<0.0001) correlation between the occurrence of a string sign and the degree of stenosis observed on the native coronary artery bypassed, thus suggesting that ITAs bypassed to the coronary arteries that showed less stenosis tended to more easily become narrowed.

The mean flow rate of saphenous vein grafts was 54.9±30.0 ml/min which was significantly (P<0.0001) less than that of ITA grafts. The mean flow rate of occluded saphenous vein grafts was 29.2±20.5 ml/min which was significantly (P=0.0007) less than that of non-occluded saphenous vein grafts (56.4±29.9). As a result, in saphenous vein grafts, it appeared that intraoperative bypass flow measurements were able to identify grafts with early occlusion.

Two saphenous vein grafts showing no wave forms on the flow measurement were found to be twisted along their course, and they were reconstructed and their mean flow rate increased from 0 to 40 and 54 ml/min, respectively.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
5. Conclusion
 References
 
Graft failure remains one of the most important problems in patients undergoing CABG since it is associated with a high risk of perioperative myocardial infarction and postoperative hemodynamic instability [3]. If every graft failure could be detected during surgery, it would greatly improve not only the overall operative results but also improve the cost-effectiveness of CABG. To recognize graft failure during surgery, flow measurements of bypass grafts using electromagnetic wave have been reported in past decades [1,4,5]. This method measures the deflection of the magnetic force created by the movement of the iron atoms in the hemoglobin complex, and therefore such measurements depend on the concentration of serum hemoglobin. In addition, minor changes in the angle between the probe and vessel affects the accuracy of the measurements. On the other hand, the recordings obtained using the transit-time method are stable and not affected by the concentration of serum hemoglobin. In addition, since this method directly measures the mean volume blood flow, it does not need a homogenous distribution of the blood flow within the cross-sectional area of the vessel while the ultrasound Doppler technique [6,7] requires it. Several reports have demonstrated that the measurement of bypass grafts including arterial grafts using this transit-time method was reliable and easy to perform [2,8–10]. However, no studies have yet reported the results of both the intraoperative flow measurements and the angiographic evaluations of ITA grafts with as large a number of subjects as the 291 grafts evaluated in our study.

According to correlation analyses, the ITA graft flow correlated significantly with the grafted perfusion areas (LAD, D, LCX or RCA) and the diameter of the bypassed coronary arteries, although the correlation was very poor. However, neither anastomotic stenosis nor a string sign of an ITA graft significantly affected the ITA graft flow, thus indicating that only measuring bypass flow rate during surgery was not able to sufficiently predict stenosed or narrowed grafts. This inability was considered to be due to the possibility of the bypass flow being affected by so many factors such as technical problems, a dissection of ITA grafts occurring during harvesting, the diameter and length of ITA grafts, the degree of stenosis and runoff of the recipient coronary arteries, the hemodynamic state of the patient during the flow measurements, and the route of the ITA grafts. In addition, the bypass flow was measured at rest and a stenosis of 75% under such condition was not critical to show diminished flows. However, analyzing the wave forms of the bypass flow displayed on the monitor or analyzing the flow response of ITA grafts to such vasodilating drugs as adenosine is considered to potentially improve the ability to detect bypass failure [9], although such drugs were not used in our study.

The flow rates of ITA grafts assessed in our series were higher than those of most other published series [11,12] and they were even higher than those of saphenous vein grafts. It appeared that one of the reasons for these results was due to the fact that the mean height of Japanese is quite lower than Euro-American and therefore, ITA grafts of Japanese are also shorter and have lower vascular resistance. Another reason may be attributed to the procedure of papaverine solution injection through a small Silastic cannula into the ITA grafts. In addition, ITA grafts were bypassed mainly to the larger perfusion areas such as LAD or the proximal RCA regions than saphenous vein grafts which were bypassed mainly to the distal RCA or posterolateral branches of LCX arteries.

The ITA string sign has been described as a narrowing of the whole length of ITA grafts. It has been assumed that this phenomenon was attributed to a competitive flow from the native coronary artery with insufficient stenosis. In our institute, we try to complete revascularization using ITA grafts as much as possible, but have avoided anastomosing ITA grafts to coronary arteries with insufficient stenosis, while the LAD was revascularized exclusively using ITA grafts regardless of the degree of the proximal stenosis. In this study, ITA grafts of 11 patients showed a string sign at the pre-discharge CAG. In four of these 11 patients, the degree of proximal stenosis of the recipient coronary artery had regressed spontaneously in comparison to that observed at the preoperative CAG. As a result, in six patients the recipient coronary arteries had less than 90% stenosis and in three patients the recipient coronary arteries had only 50% stenosis at the pre-discharge CAG. Consequently, our findings demonstrated a significant correlation between the occurrence of a string sign and the degree of stenosis of the recipient coronary arteries, which thus supports the findings of some previous reports demonstrating the competitive flow to be responsible for the occurrence of string sign [13,14].

The damaged endothelium of the ITA is usually known as one of the reasons which cause a string phenomenon. However, a string sign which was observed in 11 patients of our study was not considered to be attributed to an endothelial damage such as an intimal fracture or dissection, since the mean free flow rate of ITAs in these 11 patients was 77.2±37.1 ml/min (range 32–147) and was not significantly less than that of ITA grafts without a string sign.

Our study could not show that ITA grafts which showed a string sign at the pre-discharge CAG had a lower flow rate than ITA grafts without a string sign. It was assumed that one of the reasons for this was due to the possibility that ITA grafts did not change their diameter according to the flow demand of the recipient coronary arteries immediately after surgery.


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
References
 
The bypass flow was affected by so many factors that only measuring the bypass flow rate during surgery could not accurately predict stenosed or narrowed grafts. However, the ITA graft flow significantly correlated with grafted perfusion areas (LAD, D, LCX or RCA) and the diameter of the bypassed coronary arteries.

In addition, the occurrence of a string sign could not be predicted during surgery. However, ITA grafts bypassed to the coronary arteries with less stenosis were shown to more easily become narrowed.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 

  1. Marco J.D., Barner H.B., Kaiser G.C., Codd J.E., Mudd J.G., Willman V. Operative flow measurements and coronary bypass graft patency. J Thorac Cardiovasc Surg 1976;71:545-547.[Abstract]
  2. Lausten J., Pedersen E.M., Terp K., Steinbrüchel D., Kure H.H., Paulsen P.K., Jørgensen H., Paaske W.P. Validation of a new transit time ultrasound flowmeter in man. Eur J Vasc Endovasc Surg 1996;12:91-96.[Medline]
  3. Barner H.B. Coronary flow reserve physiologically important, operatively altered, and clinically emerging. Ann Thorac Surg 1988;45:469-470.[Medline]
  4. Foxworthy J.V., Monro J.L., Lewis B. The response to papaverine in coronary artery bypass graft flows. J Cardiovasc Surg 1985;26:439-442.[Medline]
  5. Laugie Y.A., Haxhe J.P., Buche M., Schoevaerdts J.C. Intraoperative electromagnetic flowmeter measurements in coronary artery bypass grafts. Ann Thorac Surg 1994;57:357-364.[Abstract]
  6. DeBono D.P., Samani N.J., Spyt T.J., Hartshorne T., Thrush A., Evans D.H. Transcutaneous ultrasound measurement of blood-flow in internal mammary artery grafts. Lancet 1992;339:379-381.[Medline]
  7. Crowley J.J., Shapiro L.M. Noninvasive assessment of left internal mammary artery graft patency using transthoracic echocardiography. Circulation 1995;92((II)):25-30.[Abstract/Free Full Text]
  8. Walpoth B.H., Müller M.F., Genyk I., Aeschbacher B., Kipfer B., Althaus U. Evaluation of coronary bypass flow with color-Doppler and magnetic resonance imaging techniques: comparison with intraoperative flow measurements. Eur J Cardio-thorac Surg 1999;15:795-802.[Abstract/Free Full Text]
  9. Walpoth B.H., Bosshard A., Genyk I., Kipfer B., Berdat P.A., Hess O.M., Althaus U., Carrel T. Transit-time flow measurement for detection of early graft failure during myocardial revascularization. Ann Thorac Surg 1998;66:1097-1100.[Abstract/Free Full Text]
  10. D'Ancona G., Karamanoukian H.L., Salerno T.A., Schmid S., Bergsland J. Flow measurement in coronary surgery. Heart Surg Forum 1999;2:121-124.[Medline]
  11. Voigtlander T., Dahm M., Kreitner K.F., Frick C., Wittlinger T., Nowak B., Kaiden P., Hake U., Mayer E., Bickel C., Meyer J. Intraoperative flow measurement of coronary bypass grafts using the ultrasound transit time flowmeter. Z Kardiol 1999;88:773-779.[Medline]
  12. Canver C.C., Cooler S.D., Murray E.L., Nichols R.D., Heisey D.M. Clinical importance of measuring coronary graft flows in the revascularized heart. Ultrasonic or electromagnetic?. J Cardiovasc Surg (Torino) 1997;38:211-215.[Medline]
  13. Seki T., Kitamura S., Kawachi K., Morita R., Kawata T., Mizuguchi K., Hasegawa J., Kameda Y., Yoshida Y. A quantitative study of postoperative luminal narrowing of the internal thoracic artery graft in coronary artery bypass surgery. J Thorac Cardiovasc Surg 1992;104:1532-1538.[Abstract]
  14. Siebenmann R., Egloff L., Hirzel H., Rothlin M., Stider M., Tartini R. The internal mammary artery ‘string phenomenon’. Analysis of 10 cases. Eur J Cardio-thorac Surg 1993;7:235-238.[Abstract]



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