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Ann Thorac Surg 2002;73:1441-1445
© 2002 The Society of Thoracic Surgeons


Original article: cardiovascular

Effects of skeletonization on intraoperative flow and anastomosis diameter of internal thoracic arteries in coronary artery bypass grafting

Yoshiyuki Takami, MD*a, Hiroshi Ina, MDa

a Division of Cardiovascular Surgery, Kasugai Municipal Hospital, Kasugai, Japan

Accepted for publication February 2, 2002.

* Address reprint requests to Dr Takami, Division of Cardiovascular Surgery, Kasugai Municipal Hospital, 1-1-1 Takagi-cho, Kasugai, 486-8510 Japan
e-mail: cvs{at}hospital.kasugai.aichi.jp


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. We examined the hypothesis that complete skeletonization of an internal thoracic artery (ITA) results in increased diameter of the graft for anastomosis and therefore improves graft flow in coronary artery bypass grafting.

Methods. We studied 65 consecutive patients who underwent coronary artery bypass grafting, in which the left ITA was anastomosed to the left anterior descending artery. The first 20 consecutive ITA were harvested as a pedicle (group P) and later 45 consecutive ITAs were harvested as an ultrasonically skeletonized graft (group S). Intraoperative ITA graft mean flows were obtained with a transit-time flowmeter. Three diameters of the ITA graft were measured quantitatively in postoperative angiograms performed 14 ± 5 days after the coronary artery bypass grafting; D1, at the origin from the subclavian artery; D2, at the level of the second intercostal space; and D3, just proximal to the anastomosis.

Results. Intraoperative mean flow was significantly greater in group S than in group P (S: 42.6 ± 29.1 mL/min versus P: 26.4 ± 16.1 mL/min, p = 0.03). Although the diameters D1 and D2 were not significantly different between groups, D3 was significantly larger in group S than in group p (S: 1.77 ± 0.28 mm versus P: 1.57 ± 0.17 mm, p = 0.02).

Conclusions. Compared with pedicle harvesting, complete skeletonization of ITA may make it possible to anastomose an ITA with a larger diameter in coronary artery bypass grafting, which leads to increased graft flow by decreasing vascular resistance.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Internal thoracic arteries (ITA) have become the conduit of choice for coronary artery bypass grafting (CABG). Especially, a graft from the left ITA to the left anterior descending artery (LAD) has been demonstrated to result in superior long-term patency, longer survival, and reduced cardiac events [1, 2]. In addition, it has been reported that patients who received two ITA grafts have decreased risks of death, reoperation, and angioplasty than those who only receive one ITA [3]. Therefore, there has been extended use of ITA in CABG, including bilateral ITA, sequential, and free grafts, which are harvested as pedicle or skeletonized [4, 5]. Several studies have demonstrated the potential advantages of ITA skeletonization [610]. These include visual inspection of the vessel, increased effective length of the graft, higher free flow capacity, easy sequential anastomosis, and reduced incidence of sternal wound infection. The increased ITA length as a result of skeletonization might result in an anastomosis with increased diameter. To verify this hypothesis, we compared intraoperative flow and anastomosis diameter on the postoperative angiograms of skeletonized and pedicled ITA grafts.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Study patients and surgical technique
The present study included 65 consecutive patients (51 men and 14 women; mean age, 67.5 ± 8.0 years) who underwent CABG either with (n = 53) or without (n = 12) cardiopulmonary bypass. All patients had a left ITA grafted to the LAD. Two different techniques to harvest ITA were applied randomly. In the first 20 consecutive patients, the ITA were harvested in a pedicle fashion (group P). In the later consecutive 45 patients, the harvested ITA were completely skeletonized (group S). As demonstrated in Table 1, there was no significant difference in the clinical characteristics of the two patient groups, including gender, age, height, weight, body surface area, percentage of diabetic patients, and off-pump CABG. In addition, both groups of patients had no significant difference in the degree of stenosis in the LAD to be grafted, which is very influential on graft flow. In group P, the pedicled ITA conduit was harvested together with the surrounding veins, muscle, and fascia using electrocautery and small-sized hemoclips. In group S, the ITA was completely skeletonized using an ultrasonic scalpel (Harmonic Scalpel, Ethicon Endo-Surgery, Cincinnati, OH) and hemoclips. In both groups, the ITA was harvested from the bifurcation of the musculophrenic and superior epigastric arteries up to the upper margin of the first rib or higher. After systemic heparinization, the distal end of the ITA was cut and solutions, including diluted papaverine, were never injected into the ITA lumen (intraluminal no-touch technique). The distal anastomosis of the left ITA to the LAD was constructed with 7-0 polypropylene. Five stitches were made around the "heel" of the graft: two stitches on one side of the apex of the graft, one stitch through the apex, and two stitches on the opposite side. Until the stitches were in place, the graft was not connected to the coronary artery. The suture loops were pulled up to approximate the graft to the coronary artery. The anastomosis was completed by placing stitches around the toe of the graft in a counterclockwise direction. All procedures of ITA harvesting and anastomosis were performed by one surgeon (YT).


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Table 1. Characteristics of Patients in the Two Groups

 
Intraoperative flow measurement
The graft flow tracing was obtained intraoperatively using a transit-time flowmeter (BF 2000; Medi-Stim AS, Oslo, Norway). A flow probe of 3 or 4 mm was placed around the ITA graft when the hemodynamic conditions were stable after the patient was weaned off cardiopulmonary bypass when using a standard CABG procedure, or when an anastomotic procedure was completed when the procedure was done off-pump. On the basis of the obtained flow profile, the following variables were calculated: mean graft flow (Qm, in milliliters per minute); pulsatility index ( ); percentage insufficiency ( ); and fast Fourier transformation (FFT) ratio (F0/H1, where F0 is a power of the fundamental frequency and H1 is a power of the first harmonic in FFT of the flow curve) [11, 12].

Postoperative quantitative graft angiography
Every patient underwent a postoperative cardiac catheterization 14 ± 5 days after CABG with a standard technique through the femoral or brachial route using a 5F or 4F catheter. A dose of 2 mg of isosorbide dinitrate was injected selectively in each bypass graft. All grafts were examined from at least three different views. Using a computer-assisted analyzing software (CCIP-310/W, CATHEX Co., Tokyo, Japan), three diameters of the ITA graft were measured quantitatively: D1, at the origin from the subclavian artery; D2, at the level of the second intercostal space; and D3, proximal to the anastomosis, as illustrated in Figure 1. The diameter of the LAD (D4) was also measured distal to the anastomosis with the ITA. Using optical magnification (2:1), an automatic edge-detection program determined the graft contours by assessing brightness along scan lines perpendicular to the center lines of the ITA by calibrating the diameter of the catheter used [1214].



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Fig 1. The three points for diameter measurements on the postoperative quantitative angiogram of the left internal thoracic artery (LITA) graft using an automatic edge-detection program calibrated with the diameter of the catheter used: D1, at the origin from the left subclavian artery; D2, at the level of the second intercostal space; and D3, just proximal to the anastomosis. The diameter of the left anterior descending artery (LAD) was also measured just distal to the anastomosis with the internal thoracic artery (D4).

 
Statistical analysis
All data were expressed as means ± standard deviation. Comparison of the data between the patent and nonpatent grafts was performed using Mann-Whitney’s test. Statistical correlation of variables was assessed by linear regression analysis. A p value of less than 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Intraoperative flow measurement
Typical recordings of a left ITA graft to the LAD, which was revealed to be patent in the postoperative angiogram, are shown in Figure 2. On the basis of physiology of coronary circulation, patent graft flow is predominantly diastolic, forming a trapezoid-shaped waveform with a short systolic peak. Intraoperative Qm was significantly greater in group S than in group P (S: 42.6 ± 29.1 mL/min versus P: 26.4 ± 16.1 mL/min; p = 0.03) (Table 2). The other flow-derived variables, PI, %Insuf, and FFT ratio, were not significantly different between the two groups.



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Fig 2. Results of the intraoperative transit-time flow measurement in a 67-year-old male patient who underwent an in-situ left internal thoracic artery grafting to the left anterior descending artery. His left internal thoracic artery graft was revealed to be patent postoperatively as demonstrated in Fig 1. (Upper panel) A left internal thoracic artery flow tracing; (lower panel) a fast Fourier transformation (FFT) of the flow curve. The mean flow was 132 mL/min, the pulsatility index was 1.6, the percent insufficiency was 0%, and the fast Fourier transformation ratio was 1.88. (F0 = power of the fundamental frequency; H1 = power of the first harmonic.)

 

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Table 2. Results of Intraoperative Transit-Time Flow Measurement

 
Clinical outcome and complications
There was no operative death in either group S or group P. One patient in group P suffered from mediastinitis after CABG; no sternomediastinitis occurred in group S (p = 0.71). In both groups, neither permanent nor transient phrenic nerve paralysis occurred.

Postoperative quantitative graft angiography
The ITA grafts to the LAD were all patent. There was no significant difference in D1, D2, or D4 in either group. However, as shown in Table 3, D3 was greater in group S than in group P (S: 1.77 ± 0.28 mm versus P: 1.57 ± 0.17 mm; p = 0.02). The ratio D3/D1, which implies the degree of narrowing along the grafted ITA, was greater in group S than in group P (S: 0.71 ± 0.06 versus P: 0.66 ± 0.08; p = 0.04). The intraoperative Qm values correlated with the D3 values on the postoperative graft angiograms in both groups of patients (Qm = 23.6 x D3, R = 0.75; p < 0.05) (Fig 3).


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Table 3. Results of Postoperative Quantitative Graft Angiography

 


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Fig 3. Correlation of the intraoperative mean flow (Qm) with diameter just proximal to the anastomosis (D3) on the postoperative quantitative angiogram of the internal thoracic artery grafts. A correlation was present between Qm and D3 (Qm = 23.6 x D3, R = 0.75, p < 0.05), despite the harvesting techniques of internal thoracic arteries.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The present study showed, using two qualified modern modalities, that complete ITA skeletonization results in increased graft diameter for the anastomosis and, therefore, improves graft flow in CABG. One is the transit-time graft flow measurement. It is based on the principle that the time required for ultrasound to pass through blood is slightly longer upstream than downstream. Because the ultrasound beam is wider than the diameter of the vessel lumen, it is not necessary to know the vessel diameter or perform complex calibrating procedures. Therefore, transit-time flow measurements can be easily obtained in the operation room setting [11, 12]. Another method is quantitative coronary angiography with an edge detection algorithm. Currently, it has an established role in coronary intervention and post-CABG assessment [13, 14]. We could obtain the ITA diameter measurements more precisely by this modality than in the previous reports [6, 7]. There have been no reports describing the advantages of the ITA skeletonization over pedicle harvesting using intraoperative flow measurement and postoperative quantitative graft angiograms.

The benefits of ITA skeletonization are an anastomosis with a larger diameter and decrease in graft vascular resistance; these factors may prevent the hypoperfusion syndrome in CABG using ITA. This syndrome is a rare but life-threatening perioperative clinical syndrome manifested by low cardiac output, left ventricular failure, and cardiac arrest [15, 16]. The major contributory factor to ITA hypoperfusion is a disproportion between ITA flow and myocardial demand because of the small ITA size, overzealous use of sequential grafting, and severe left ventricular hypertrophy. Considering the current wide use of ITA, including sequential and bilateral, ITA skeletonization may be an efficient strategy to prevent perioperative hypoperfusion syndrome, especially in off-pump CABG without assisted circulation.

The intraoperative Qm values correlated with the D3 values on the postoperative graft angiograms for both groups P and S. Qm values are affected by the dynamic character of the variables, including blood pressure, heart rate, graft diameter, and coronary resistance. In this study, the LAD stenosis was of the same degree, as demonstrated in Table 1, and the LAD diameter at anastomosis was of the same size, as demonstrated in Table 3. Therefore, it is likely that the graft diameter at anastomosis (D3) may strongly affect the graft flow (Qm), as shown in Figure 3. To increase the ITA graft flow it is necessary to increase the diameter at the anastomosis by the complete skeletonization. We believe that ITA skeletonization may add perioperative benefits to the long-term excellent clinical results, which has already been achieved by many surgeons using pedicled ITA.

Previous studies have reported on the effect of free flow in skeletonized ITA [6, 7]. Choi and Lee [6] demonstrated that ITA skeletonization increases free flow as well as intraluminal papaverine injection for the pedicle ITA. Wendler and colleagues [7] described more improvement of free flow after injection of papaverine in the skeletonized ITA than in the pedicle ITA. Both studies revealed that papaverine increased the free flow capacity of skeletonized ITA. Our study demonstrated that skeletonization is sufficient and papaverine injection is not necessary to increase ITA graft flow. As previously reported [17], intraluminal application of acidic papaverine induces endothelial damage to the ITA. Therefore, we never use intraluminal papaverine on ITA. In our study, flow of the functioning ITA graft, rather than the free ITA flow, was measured after anastomosis in the hemodynamically stable condition. The flow of the functioning ITA may be clinically meaningful and appropriate because the hemodynamic variables and the run-off conditions of the ITA grafts (LAD stenosis and D4) were supposed to be almost equal between the two groups.

Although several benefits have been indicated, some surgeons are still concerned that skeletonization can cause vasospasm and mechanical irritation of the ITA. Immunohistochemical analysis showed preserved vessel wall integrity in the skeletonized ITA as well as in the pedicle ITA [18]. Thorough ultrasonic skeletonization, as used in the present study, may reduce this concern. Higami and colleagues [10] demonstrated that ultrasonic complete ITA skeletonization is safe and effective. We also experienced no vasospasm and mechanical damage of ITA by ultrasonic skeletonization. The Harmonic Scalpel uses two cutting mechanisms: longitudinal vibration enabling the scalpel to incise tissues and cavitational fragmentation disrupting low-density tissues and causing tissue planes to separate. The scalpel achieves ITA skeletonization with lower temperatures than electrocautery, which is safer because the dissecting procedures are always very close to the vessel.

In conclusion, the complete ultrasonic skeletonization of ITA, in comparison to pedicle harvesting, may make it possible to anastomose the ITA with a larger diameter in CABG, leading to increased perioperative graft flow by decreasing the vascular resistance.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Loop F.D., Lytle B.W., Cosgrove D.M., et al. Influence of the internal mammary artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314:1-6.[Abstract]
  2. Cameron A., Davis K.B., Green G.E. Coronary bypass surgery with internal thoracic artery grafts. Effects on survival over a 15-year period. N Engl J Med 1996;334:216-219.[Abstract/Free Full Text]
  3. Lytle B.W., Blackstone E.H., Loop F.D., et al. Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
  4. Pevni D., Kramer A., Paz Y., et al. Composite arterial grafting double skeletonized internal thoracic arteries. Eur J Cardio-thorac Surg 2001;20:299-304.[Abstract/Free Full Text]
  5. Dion R., Glineur D., Derouck D., et al. Long-term clinical and angiographic follow-up of sequential internal thoracic artery grafting. Eur J Cardio-thorac Surg 2000;17:407-414.[Abstract/Free Full Text]
  6. Choi J.B., Lee S.Y. Skeletonized and pedicled internal thoracic artery grafts: effects on free flow during bypass. Ann Thorac Surg 1996;61:909-913.[Abstract/Free Full Text]
  7. Wendler O., Tscholl D., Huang Q., Schäfers H.J. Free flow capacity of skeletonized versus pedicled internal thoracic artery grafts in coronary artery bypass grafts. Eur J Cardio-thorac Surg 1999;15:247-250.[Abstract/Free Full Text]
  8. Calafiore A.M., Vitolla G., Iaco A.L., et al. Bilateral internal mammary artery grafting: midterm results of pedicled versus skeletonized conduits. Ann Thorac Surg 1999;67:1637-1642.[Abstract/Free Full Text]
  9. Cohen A.J., Lockman J., Lorberboym M., et al. Assessment of sternal vascularity with single photon emission computed tomography after harvesting of the internal thoracic artery. J Thoracic Cardiovasc Surg 1999;118:496-502.[Abstract/Free Full Text]
  10. Higami T., Yamashita T., Nohara H., et al. Early results of coronary grafting using ultrasonically skeletonized internal thoracic arteries. Ann Thorac Surg 2001;71:1224-1228.[Abstract/Free Full Text]
  11. Takami Y., Ina H. A simple method to determine anastomotic quality of coronary artery bypass grafting in the operating room. Cardiovasc Surg 2001;9:68-72.[Medline]
  12. Takami Y., Ina H. Relation of intra-operative flow measurement with post-operative quantitative angiographic assessment of coronary artery bypass grafting. Ann Thorac Surg 2001;72:1270-1274.[Abstract/Free Full Text]
  13. Ormiston J.A., Stewart F.M., Roche A.H., et al. Late regression of the dilated site after coronary angioplasty: a 5-year quantitative angiographic study. Circulation 1997;96:468-474.[Abstract/Free Full Text]
  14. Poirier N.C., Carrier M., Lesperance J., et al. Quantitative angiographic assessment of coronary anastomoses performed without cardiopulmonary bypass. J Thorac Cardiovasc Surg 1999;117:292-297.[Abstract/Free Full Text]
  15. Jones E.L., Lattouf O.M., Weintraub W.S. Catastrophic consequences of internal mammary artery hypoperfusion. J Thorac Cardiovasc Surg 1989;98:902-907.[Abstract]
  16. Loop F., Thomas J. Hypoperfusion after arterial bypass grafting. Ann Thorac Surg 1993;56:812-813.[Medline]
  17. Noera G., Pensa P., Lodi R., Lammara M., Biagi B., Guelfi P. Influence of different harvesting techniques on the arterial wall of the internal mammary artery graft: microscopic analysis. Thorac Cardiovasc Surgeons 1993;41:16-20.
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