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Ann Thorac Surg 2002;73:1446-1450
© 2002 The Society of Thoracic Surgeons

Original article: cardiovascular

Intraoperative evaluation of coronary anastomosis by transit-time ultrasonic flow measurement

Tetsuro Morota, MD, PhD*a, Francis G. Duhaylongsod, MDa, William R. Burfeind, MDa, Ching-Tsorng Huang, MDa

a Department of Surgery, Duke University Medical Center, Durham, North Carolina, USA

Accepted for publication February 5, 2002.

* Address reprint requests to Dr Morota, Department of Cardiothoracic Surgery, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
e-mail: morotat-sur{at}h.u-tokyo.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Intraoperative assessment of the anastomosis is important during coronary bypass on a beating heart. The purpose of this study is to predict the quality of anastomosis using transit-time flow measurement and to find out the most accurate indicator.

Methods. Eight swine underwent internal thoracic-anterior descending coronary artery bypass grafting on a beating heart. Flow measurement and angiography were performed at various degrees of stenosis created on the graft. As flow parameters, total flow, systolic flow, diastolic flow, diastolic/total flow ratio, systolic peak flow, diastolic peak flow, systolic/diastolic peak flow index, and pulsatility index were used. Mixed procedure and probability test (negative means successful anastomosis) were used to analyze the diagnostic ability.

Results. Diastolic flow, diastolic/total flow ratio, diastolic peak flow, systolic/diastolic peak flow index, and pulsatility index showed significant variance with increased stenosis. Among these measures, diastolic/total flow ratio showed the highest value of area under the curve (0.91) and the highest specificity (82%) at 90% sensitivity with actual value of 42%.

Conclusions. Diastolic/total flow ratio was the most reliable indicator to predict critical stenosis in coronary artery bypass grafting.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Intraoperative assessment of an anastomosis is recommended after off-pump coronary artery bypass grafting (CABG) because of its technical difficulties and high incidence of early occlusion [1–3]. Although angiography is the gold standard in detecting anastomotic failure, it demands time and expense. On the other hand, transit-time ultrasonic flow (TTF) measurement, which has become recently available, gives flow volume tracings using a simple procedure [4]. It remains unknown how much flow or which kind of flow pattern corresponds to each degree of anastomotic stenosis.

The purposes of this study are to analyze the relationship between TTF measurements and angiographic findings, to find out which indicator is the most accurate predictor for the quality of anastomosis, and finally, to identify a critical stenosis after off-pump CABG with only TTF measurement, eliminating angiography.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Male crossbred swine weighing 25 to 30 kg were used in this study. All animals received humane care in compliance with the Institutional Animal Care and Use Committee at Duke University and the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985).

Surgical procedure
Eight swine underwent CABG on a beating heart without cardiopulmonary bypass. Each animal was anesthetized initially with ketamine hydrochloride (20 mg/kg) and sodium pentobarbital (10 mg/kg), and then maintained with isoflurane (2% to 3%) inhaled on mechanical ventilation. The sternum was fully divided and the left internal thoracic artery (LITA) was dissected. After systemic heparinization (100 U/kg), the LITA was clamped and divided. The pericardium was opened and cradled. Intravenous lidocaine hydrochloride (1 mg/kg), bretylium tosylate (4 mg/kg), and propranolol (1 mg/body) were given to prevent ventricular arrhythmia and to reduce heart rate. A heart stabilizer (Mini-CABG; USSC, Norwalk, CT) was placed along the left anterior descending artery (LAD) distally to the first diagonal branch. Coronary arteriotomy was made and an intracoronary shunt of 1.5 or 2.0 mm in diameter (Anastaflo IVS-1512/2012; Baxter, Deerfield, IL) was placed to preserve distal perfusion. Then the LITA was anastomosed to the LAD on the beating heart without cardiopulmonary bypass. As the LITA graft was declamped, the LAD was ligated proximal to the first diagonal branch. An adjustable occluder (Vascular Occluder OC4; IVM, Healdsburg, CA) was put around the graft just proximal to the anastomosis, and a transit-time flow probe of 3 mm (H3 MB784; Transonic Inc, Ithaca, NY) was also placed on the proximal graft, at least 5 cm away from the occluder. A catheter (6F IM guiding catheter; Cordis, Miami, FL) was placed at the orifice of the LITA through the groin (Fig 1).



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  		Fig 1. Diagram of the procedure. The left internal thoracic artery (LITA) is anastomosed to the left anterior descending artery (LAD), which is occluded just proximal to the first diagonal branch. An adjustable occluder (Occ) and a flow probe (Pr) are placed on the graft.

 
Measurements
Before the start of the flow measurements, the status of the anastomosis was confirmed on angiography by the surgeon. The adjustable occluder, which does not give consistent stenosis, was inflated randomly and repeatedly by saline to create diverse degrees of stenosis until the heart lost its functional stability. At each situation, the graft flow was traced through a flowmeter (T-106; Transonic Inc) and recorded on a computer disk using a data acquisition software (Flowtrace 32; Transonic Inc), and was followed by angiography, at a 30-degree left anterior oblique view, which was also saved on the disk of a digital fluoroscopic unit (series 9600; OEC, Salt Lake City, UT). The mean blood pressure was maintained at 55 to 70 mm Hg throughout the procedure, and the heart rate during measurement was 90 to 110 beats/min.

Indicators
The flow parameters—total flow, systolic flow, diastolic flow, diastolic/total flow ratio (F-D/T), systolic peak flow (PF-S), diastolic peak flow (PF-D), systolic/diastolic peak flow index (PF-S/D; PF-S divided by PF-D), and pulsatility index (PI)—were measured or calculated. The PI is defined as the difference between PF-S and diastolic bottom flow divided by the mean flow. These values were obtained as an average of five consecutive stable wavelets in each situation using the program WINDAQ (DATAQ Instruments Inc, Akron, OH). The systolic period was defined as starting from the first upstroke on flow trace after the R wave on the electrocardiogram and ending before the first upstroke during the T wave. In the case of no obvious diastolic upstroke, the end point was set at the peak of the T wave.

Diagnosis
Three doctors blind to flow data reviewed the angiographic images. Images were divided into six grades as having 0 (no stenosis, baseline), 25 (less than 25), 50 (26 to 50), 75 (51 to 75), 90 (76 to 90), 99 (91 or higher) percent stenosis in diameter. Finally, the agreed value of two, or the central value of the three diagnosticians was adopted. Stenosis 0 and 25% were defined to be a successful grafting, and the others considered as failed.

Statistical analysis
All measurements of TTF were described in mean ± standard deviation. To analyze the variance among groups 25%, 50%, and 75%, mixed procedure (PROC MIXED; SAS Institute Inc, Cary, NC) was used. Then the measurements showing statistical significance (p < 0.05) in mixed procedure were analyzed with a probability test. The predicted diagnosis, successful (negative) or failed (positive), obtained was compared with the angiographic diagnosis, and then the sensitivity and the specificity were calculated on 50 cutoff points (every 2% of the highest value). The data were plotted into a receiver operating characteristic curve, and the area under the curve was calculated. All statistical analyses were performed using the SAS system.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
In all of the animals the LITA-LAD anastomosis did not have any stenosis as observed by the diagnosticians. Flow trace demonstrated systolic-dominant flow of the native (before division) LITA, significant diastolic flow after anastomosis, and disappearance of diastolic flow with severe stenosis. The measured values and p values in the mixed procedure are summarized in Table 1. In the mixed procedure among groups 25%, 50%, and 75%, diastolic flow (p = 0.028), F-D/T (p = 0.001), PF-D (p = 0.026), PF-S/D (p = 0.013), and PI (p = 0.039) showed significant variance, whereas total flow, systolic flow, and PF-S did not.


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  		Table 1. Summary of Measured Values

 
Probability test was performed on the former five flow measures, and the receiver operating characteristic curves were depicted. Of these measures, F-D/T showed the highest area under the curve value (0.91, Fig 2A), followed by diastolic flow (0.85, Fig 2B), and PF-S/D (0.85), PF-D (0.81), and PI (0.76) showed the lowest. For 100% sensitivity, specificity ranged from 39% to 57%. At sensitivity levels of 90% and 85%, F-D/T showed higher specificity (82% and 86%, respectively) at each level (Table 2).



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  		Fig 2. Representative receiver operating characteristic curves. (A) Diastolic/total flow ratio, which showed the highest area under the curve (AUC) value. (B) Diastolic flow, which showed the second highest area under the curve value.

 

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  		Table 2. Area Under the Curve and Specificity of the Measurements at 100%, 90%, and 85% of Sensitivity

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
In off-pump CABG, the LITA-LAD anastomosis is performed on the beating heart through a full or partial sternotomy or small thoracotomy. Although off-pump CABG offers a shorter operative time and hospital stay with less costs, some surgeons suggest a possible risk of deteriorated graft patency due to reduced quality of the anastomosis [5, 6]. Because the long-term survival after coronary revascularization is mostly affected by the LITA-LAD graft patency [7], the anastomosis in off-pump CABG must be as patent as in a conventional procedure. Intraoperative angiography enables surgeons to correct the anastomosis if necessary. Surprisingly, the revision rate after intraoperative angiography is 20% to 33% [2, 3]. This is much higher than the acute graft occlusion rate of 5% [1] or early reoperation rate of 6% [8], as previously reported. However, performing angiography requires manpower, large instruments, and time. Another solution is flow measurements. Previous studies on electromagnetic flow measurements have demonstrated a correlation between the vein graft flow and patency [9]. No study, however, has clearly shown a similar correlation with arterial grafts. Electromagnetic flow measurements are dependent on hematocrit and need a suitable probe-to-vessel fit, both of which make the measured values unreliable. Other techniques such as Doppler flow measure flow velocity, not the exact flow volume. The accuracy of Doppler flow, as well as that of electromagnetic flow measurements, still remains undefined [10, 11].

Recently, TTF measurements became recognized as a useful modality for measuring blood flow with little variability and error [4]. The principle of TTF measurement is to measure the difference in transit time between the upstream and downstream signals through the targeted vessel. The TTF value is proportional to blood volume flow and is independent of hematocrit or vessel diameter. In 1994, Canver [12] and Matre [13] and their colleagues reported the clinical application of TTF measurement during CABG. They compared the flow volume measured by TTF with free flow of the internal thoracic artery or the flow volume of vein graft measured by Doppler, both resulting in an excellent correlation. Thus, the accuracy of TTF measurements with CABG was well established. No comparative study with angiography has been done, however, and the dividing line between successful and failed anastomoses remains unknown.

This study was designed to clarify the correlation between the TTF measurements and the angiographic degree of stenosis.

We analyzed eighth indicators (total flow, systolic flow, diastolic flow, PF-S, and PF-D measured directly from TTF tracing, and calculated F-D/T, PF-S/D, and PI), which can easily be obtained in the operating room. Because our objective was to distinguish between successful and failed anastomoses, the variance among 25%, 50%, and 75% stenosis was analyzed by mixed procedure. This procedure implements random effects in the statistical model and permits modeling the covariance structure of the data for analysis of repeatedly measured data [14]. Total flow, systolic flow, and PF-S did not show a proportional tendency with increased stenosis and were eliminated in subsequent analyses. This reflects the fact that the coronary blood flow is mostly delivered during diastole.

The next step was to perform a validation study on the measurements that showed significant variance in mixed procedure. The degrees of stenosis were divided into two groups, successful and failed, for the sake of convenience, although it might be controversial to classify 25% stenosis as successful. Area under the curve value, as well as the specificity at the sensitivity level of 90% or 85%, was the highest in F-D/T. The PI, which was taken for a predictor in a previously established article [15], showed the lowest area under the curve value and had only about 50% specificity at 90% and 85% sensitivity. We considered sensitivity more important than specificity in this study because a false-negative value (ie, a failed anastomosis) should be as small as possible, even if some patients with false-positive results have undergo unnecessary revision. This animal study suggests that F-D/T gives the most accurate diagnosis. However, further clarification may be needed, as the permissible sensitivity level is highly subjective; it is dependent on the surgeon’s definition of how much false-negative value is acceptable.

One of the limitations of this study was that the animals had normal coronary arteries, normal distal run-off, and no competitive flow from the native artery. Therefore, the absolute flow value and the peak flow value are not applicable to human beings. Application may also be affected by the difference in species, but indices such as F-D/T, PF-S/D, and PI have the possibility to predict anastomosis in humans. Another limitation arises from the flow measurement itself: graft kinking or dissection cannot be distinguished from anastomotic failure. These complications should be checked with direct vision.

In conclusion, in the setting of intentional hydraulic compression of the LITA graft on the swine model, among the indicators measured by TTF to predict significant stenosis after off-pump CABG, F-D/T was the most reliable, with satisfactory specificity and sensitivity values. Further evaluation on clinical cases is needed to eliminate angiography.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We thank Damian Craig, MS, for supporting statistical analysis. This study was funded by the Division of Cardiothoracic Surgery, Duke University Medical Center, through an unrestricted research grant from the United States Surgical Corporation, Norwalk, CT.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Moshkovitz Y., Lusky A., Mohr R. Coronary artery bypass without cardiopulmonary bypass: analysis of short-term and mid-term outcome in 220 patients. J Thorac Cardiovasc Surg 1995;110:979-987.[Abstract/Free Full Text]
  2. Lazzara R.R., McLellan B.A., Kidwell F.E., Combs D.T., Hanlon J.T., Young E.K. Intraoperative angiography during minimally invasive direct coronary artery bypass operations. Ann Thorac Surg 1997;64:1725-1727.[Abstract/Free Full Text]
  3. Barstad R.M., Fosse E., Vatne K., et al. Intraoperative angiography in minimally invasive direct coronary artery bypass grafting. Ann Thorac Surg 1997;64:1835-1839.[Abstract/Free Full Text]
  4. Lundell A., Bergqvist D., Mattsson E., Nilsson B. Volume blood flow measurements with a transit time flowmeter: an in vivo and in vitro variability and validation study. Clin Physiol 1993;13:547-557.[Medline]
  5. Ancalmo N.B. Minimally invasive coronary artery surgery: really minimal?. Ann Thorac Surg 1997;64:928-929.[Free Full Text]
  6. Reardon M.J., Espada R., Letsou G.V., Safi H.J., McCollum C.H., Baldwin J.C. Minimally invasive coronary artery surgery—a word of caution. J Thorac Cardiovasc Surg 1997;114:419-420.[Free Full Text]
  7. Cameron A., Davis G., Schaff H.V. Coronary bypass surgery with internal thoracic artery grafts: effects on survival over a 15-year period. N Engl J Med 1996;334:220-225.[Medline]
  8. Calafiore A.M., Giammarco G.D., Teodori G., et al. Midterm results after minimally invasive coronary surgery (LAST operation). J Thorac Cardiovasc Surg 1998;115:763-771.[Abstract/Free Full Text]
  9. Sharma G.V., Khuri S.F., Folland E.D., Barsamian E.M., Parisi A.F. Prognosis for aorta-coronary graft patency: a comparison of preoperative and intraoperative assessments. J Thorac Cardiovasc Surg 1983;85:570-576.[Abstract]
  10. Canver C.C., Ricotta J.J., Bhayana J.N., Fiedler R.C., Mentzer R.M. Use of duplex imaging to assess suitability of the internal mammary artery for coronary artery surgery. J Vasc Surg 1991;13:294-301.[Medline]
  11. Van Son J.A., Skotnicki S.H., Peters M.B., Pijls N.H., Noyez L., van Asten W.N. Noninvasive hemodynamic assessment of the internal mammary artery in myocardial revascularization. Ann Thorac Surg 1993;55:404-409.[Abstract/Free Full Text]
  12. Canver C.C., Dame N.A. Ultrasonic assessment of internal thoracic artery graft flow in the revascularized heart. Ann Thorac Surg 1994;58:135-138.[Abstract/Free Full Text]
  13. Matre K., Birkeland S., Hessevik I., Segadal L. Comparison of transit-time and Doppler ultrasound methods for measurement of flow in aortocoronary bypass grafts during cardiac surgery. Thorac Cardiovasc Surg 1994;42:170-174.[Medline]
  14. Littel R.C., Henry P.R., Ammerman C.B. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 1998;76:1216-1231.[Abstract/Free Full Text]
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