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Eur J Cardiothorac Surg 2004;25:578-584
© 2004 Elsevier Science NL

Arterial conduit shear stress following bypass grafting for intermediate coronary artery stenosis: a comparative study with saphenous vein grafts

Tsuyoshi Shimizua*, Shigeki Itoa, Yujiro Kikuchia, Masaharu Misakaa, Tetsuzo Hirayamaa, Shin Ishimarua, Akira Yamashinab

a Department of Surgery II, Tokyo Medical University, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan
b Department of Internal Medicine II, Tokyo Medical University, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan

Received 9 October 2003; received in revised form 7 December 2003; accepted 15 December 2003.

* Corresponding author. Tel.: +81-3-3342-6111x5077; fax: +81-3-3342-6193
e-mail: tshimizu-cvs{at}umin.ac.jp


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Objectives: Graft failure has been reported when the arterial conduit, such as the internal thoracic artery (ITA) or the right gastroepiploic artery (GEA), is grafted to a lower grade coronary artery stenosis. The shear stress as a significant factor affecting graft patency was compared between the arterial conduit and the saphenous vein graft (SVG) after surgery. Methods: In 101 patients, 40 ITAs, 27 GEAs and 34 SVGs were examined using a Doppler-tipped guide wire during postoperative angiography. The graft flow volume and shear stress were calculated from velocity and diameter data. The study grafts were classified according to the grade of native coronary artery stenosis: group L had more than 50 up to 75% stenosis, and group H had more than 75% stenosis. Group H consisted of 25 ITAs, 17 GEAs and 21 SVGs, while group L consisted of 15 ITAs, 10 GEAs and 13 SVGs. Results: In group H, graft flow volume did not significantly differ among the ITA (34±11 ml/min), GEA (36±16 ml/min) and SVG (41±15 ml/min), and graft shear stress significantly (ITA vs. GEA P<0.0001; GEA vs. SVG P<0.01) differed among the ITA (16.0±4.8 dyn/cm2), GEA (9.1±3.2 dyn/cm2) and SVG (4.8±1.6 dyn/cm2). In group L, flow volume was lower (P<0.001) in the ITA (18±6 ml/min) and GEA (13±8 ml/min) than in the SVG (35±16 ml/min), and shear stress was significantly (P<0.001) greater in the ITA (13.7±4.9 dyn/cm2) than the GEA (5.6±2.0 dyn/cm2) or SVG (4.6±2.0 dyn/cm2). Conclusions: These data suggest that shear stress of the ITA is superior and maintained despite the flow volume being reduced by flow competition. Lower shear stress of the GEA for intermediate stenosis may be associated with the development of conduit failure.

Key Words: Coronary artery bypass • Coronary artery disease • Internal thoracic artery • Gastroepiploic artery • Saphenous vein


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Based on its superior long-term patency rates, the internal thoracic artery (ITA) has been shown to be an excellent conduit for myocardial revascularization compared to the saphenous vein graft (SVG). The progression of intimal hyperplasia or the development of atherosclerosis is associated with late vein graft occlusion. On the other hand, the incidence of atherosclerosis is low in the ITA in patients undergoing coronary artery bypass for severe coronary artery disease [1]. Because of superior long-term patency rates, other arterial conduits, such as the radial artery or the gastroepiploic artery (GEA), are expected to achieve better long-term results. The GEA is an in situ arterial conduit, as is the ITA. The incidence of atherosclerosis is also rare in the GEA; however, it is slightly greater than in the ITA [2].

Wall shear stress has been thought to play an important role in the development of atherosclerosis. Shear stress increases the release of nitric oxide [3] and the production of prostacylin [4] by endothelial cells and inhibits smooth muscle cell proliferation [5]. In other words, low shear stress is associated with the development of atherosclerosis. Bach et al. [6] found that shear rates of the ITA were higher compared with the SVG, and they suggested these differences might have implications regarding the development of degenerative graft disease and long-term conduit patency. Indeed, endothelial cells in the ITA release more prostacylin [7] and nitric oxide [8] than those in the SVG.

Flow competition is a significant factor affecting arterial conduit morphology and patency. The string sign is an atrophic change in the arterial conduit and this phenomenon is due to competitive flow in grafts connected to only mildly stenosed coronary arteries. The fate of the string sign of the ITA is still controversial. In the GEA, patency rates seemed to be reduced by competitive flow. Suma et al. [9] reported that the 10 year patency rate of the GEA was 62.5%, and that anastomosis to a less critically stenosed coronary artery was one of the major causes of late graft occlusion. The flow characteristics of the GEA are yet to be fully clarified. The relationship between the SVG patency and native coronary artery stenosis has also been controversial, however, competitive flow may be a negligible factor in SVG graft patency.

The effect of flow competition on coronary artery bypass conduit shear stress is unknown. The ITA graft diameter has been shown to decrease when the native coronary artery stenosis is less [10]. Greater flow velocity and smaller vessel diameter increase shear stress. It may be beneficial for a bypass conduit to maintain conduit shear stress even if the conduit diameter is reduced by competitive flow.

An intravascular Doppler-tipped guide wire (DGW), developed as a coronary angioplasty guide wire, has been used for analysis of phasic flow velocity of ITA grafts and SVGs during postoperative angiography [6]. In the present study, flow velocity was detected in the ITA, GEA and SVG using a DGW. Shear stress was calculated from the graft flow velocity and diameter. Percent diameter stenosis was taken as an indicator showing native coronary flow. Intermediate coronary stenosis for coronary interventions was estimated between 50 and 75% [11]. The effect of native flow on conduit shear stress was investigated among the ITA, GEA and SVG.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
2.1. Study patients
Between 1996 and 1998, 101 patients (age 44–81 years; mean 63±10 years) who had had coronary artery bypass grafting using the ITA, GEA or SVG were examined during cardiac catheterization. The patients were investigated in the context of a postoperative angiographic follow-up study at intervals from 2 weeks to 8 years (mean 1.5 years) after surgery, and all were asymptomatic. Exclusion criteria were grafts with significant (>50%) stenosis or occlusion, sequential bypass grafts, composite grafts, patients with severe LV dysfunction (<30%), renal impairment, difficulty in introducing the guide wire to the anastomotic site, patients with abdominal aortic aneurysm or severe arterial occlusive disease. Informed consent was obtained from all patients.

Study grafts consisted of 40 ITA grafts (39 left and 1 right ITA), 27 GEA grafts and 34 SVGs. All ITA grafts were anastomosed to the left anterior descending artery. Of the 27 GEA grafts, 2 were placed to the left anterior descending artery, 15 were grafted to the right coronary system (14 to the posterior descending branch, 1 to the postero-lateral branch) and 10 were grafted to the left circumflex coronary artery. Of the 34 SVGs, 3 were grafted to the left anterior descending artery, 16 were grafted to the right coronary system (3 were grafted to the distal right coronary artery, 12 to the posterior descending branch and 1 to the postero-lateral branch), and 15 were grafted to the left circumflex coronary artery.

2.2. Coronary angiography and flow velocity measurement
Coronary angiography was performed by the standard femoral approach. After ITA, GEA or SVG angiography, a 5 or 6 F catheter was positioned in the origin of the grafts. A 0.015 or 0.018-in., 12-MHz DGW (Jomed Inc., Flowire) was connected to a velocitymeter (Jomed Inc., FloMap), and advanced through the catheter into the graft and introduced to the distal portion of the graft.

2.3. Graft flow volume and shear stress calculation
The graft diameter at the points of flow velocity measurement was determined by angiography using an automated edge-contour detection system (Cardio 500; Kontron Electronic AG, Eching, Germany).

Flow volume (Q ml/min) was calculated using the following equation as previously reported [12]:

where APV is the average peak velocity (cm/s) and R is the vessel radius (cm).

The SR (s-1) was calculated as:

where D is the graft diameter (cm).

The shear stress (SS dyn/cm2) was calculated using a modified Hagen–Paiseuille equation [13]:


where µ is the blood viscosity. We hypothesized that blood viscosity was constant at 0.0035 kg/m s [13].

2.4. Patient classification
The study patients/grafts were classified according to the grade of native coronary artery percent diameter stenosis at the time of postoperative angiography into group H, which had more than 75% stenosis and group L, which had more than 50% stenosis up to 75% stenosis.

2.5. Statistical analysis
One-way analysis of variance (ANOVA) was used to compare three or six groups for continuous data. A Scheffe test was performed when the ANOVA showed significant differences. An unpaired t-test was used to compare two groups for continuous data. The {chi}2-test was used for nominal data.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 Appendix A. Conference...
 References
 
3.1. Baseline characteristics
The GEA group was significantly younger than the SVG group (P=0.0001). No significant differences were observed among the six groups in sex, body surface area, number of bypass grafts per patient, target coronary diameter, coronary risk factors, body mass index, or history of myocardial infarction (Table 1).


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  		Table 1. Baseline characteristics

 
3.2. Flow velocity spectra
Compared with the SVG, the transition between systole and diastole in the velocity spectra was obscure in the arterial conduits. In early systole, retrograde flow (flow reversal) was seen in the arterial conduit in group L, and appeared to be more apparent in the GEA than ITA (Fig. 1) .



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  		Fig. 1. Flow velocity spectra of the grafts for a coronary artery with 50–75% stenosis. (a) The left internal thoracic artery to the left anterior descending artery. (b) The right gastroepiploic artery to the postero-lateral branch of the left circumflex artery. (c) The saphenous vein graft to the postero-lateral branch of the left circumflex artery.

 
3.3. Hemodynamic data
3.3.1. Angiographic data
No significant differences were observed in left ventricular ejection fraction, end-diastolic volume and target coronary diameter. Graft diameter in group H significantly differed among the three conduits: ITA 2.3±0.3 mm; GEA 2.9±0.6 mm; SVG 3.7±0.6 mm (ITA vs. GEA P=0.017; ITA vs. SVG P<0.0001; GEA vs. SVG P<0.0001). In group L, graft diameter was greater (P<0.0001) in the SVG (3.6±0.4 mm) than the ITA (2.0±0.3 mm) or GEA (2.4±0.5 mm), but did not significantly differ between the ITA and GEA (P=0.0893). In the arterial conduits, graft diameter significantly differed between groups H and L (ITA P=0.0005; GEA P<0.0274), but did not differ in the SVG between groups H and L (P=0.6459) (Table 2).


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  		Table 2. Hemodynamic data

 
3.1.2. Catheterization data
Heart rate, aortic pressure and left ventricular end-diastolic pressure did not significantly differ among groups H and L.

3.1.3. Velocimetric and calculated data
Average peak velocity in group H significantly differed among the three conduits: ITA 26±7 cm/s; GEA 18±5 cm/s; SVG 12±4 cm/s (ITA vs. GEA P<0.0001; ITA vs. SVG P<0.0001; GEA vs. SVG P=0.013). In group L, average peak velocity was greater (ITA vs. GEA P<0.0001; ITA vs. SVG P=0.0015) in the ITA (19±6 cm/s) than the GEA (9±3 cm/s) or SVG (11±5 cm/s), but did not differ between the GEA and SVG (P=0.495). In the arterial conduits, average peak velocity significantly differed between groups H and L (ITA P=0.0022; GEA P<0.0001), but did not differ in the SVG between groups H and L (P=0.6141).

Flow volume in group H did not significantly differ among the three conduits: ITA 34±11 ml/min; GEA 35±16 ml/min; SVG 41±15 ml/min (ITA vs. GEA P=0.9786; ITA vs. SVG P<0.3370; GEA vs. SVG P<0.5179). In group L, flow volume was greater (P<0.0001) in the SVG (35±16 ml/min) than the ITA (18±6 ml/min) or GEA (13±8 ml/min), but did not significantly differ between the ITA and GEA (P=0.5776). In the arterial conduits, flow volume significantly differed between groups H and L (ITA P<0.0001; GEA P<0.0005), but did not differ in the SVG between groups H and L (P=0.4296).

Shear stress in group H significantly differed among the three conduits: ITA 16.0±4.8 dyn/cm2; GEA 9.1±3.2 dyn/cm2; SVG 4.8±1.6 dyn/cm2 (ITA vs. GEA P<0.0001; ITA vs. SVG P<0.0001; GEA vs. SVG P=0.002). In group L, shear stress was greater (P<0.0001) in the ITA (13.7±4.9 dyn/cm2) than the GEA (5.6±2.0 dyn/cm2) or SVG (4.6±2.0 dyn/cm2), but did not differ between the GEA and SVG (P=0.5832). Between groups H and L, shear stress significantly differed in the GEA (P=0.0041), but did not differ in the ITA (P=0.1354) or SVG (P=0.8021).

The shear rate in group H was 458±136 s-1 in the ITA, 261±93 s-1 in the GEA, and 137±46 s-1 in the SVG. In group L, the shear rate was 391±141 s-1 in the ITA, 159±56 s-1 in the GEA, and 130±57 s-1 in the SVG. Statistical differences in the shear stress among each group were the same as those for shear stress.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
Appendix A. Conference...
 References
 
Graft flow volume did not differ among the ITA, GEA and SVG for high-grade coronary stenosis, however, graft flow velocity was greatest in the ITA and lowest in the SVG grafting to the coronary artery with severe stenosis. In contrast, graft diameter was largest in the SVG and smallest in the ITA among the same groups. Our data suggest that the arterial conduits, the ITA and GEA, had higher shear stress than the SVG. Several investigators have reported in their intraoperative [14] or postoperative studies [6] that flow velocity of the ITA is greater than that of the SVG. Moreover, the present study also demonstrated that shear stress of the GEA is lower than that of the ITA. This may be due to the substantial differences in flow characteristics between the ITA and GEA, even when the target coronary vessels and vascular beds differ between these conduits. Tavilla et al. [15] reported no significant flow and diameter differences before takedown (17±6 cm/s, 2.8 mm) and after anostomosis of the GEA (19±10 cm/s, 2.8 mm). De Bono et al. [16] reported no significant difference in resting flow rates and the vessel diameter between grafted and ungrafted ITAs, although the flow velocity profiles of the grafted ITAs were distinct from those of the ungrafted ITAs. Their data suggested that the conduit flow velocity and shear rate are different between the ITA and GEA in in situ conditions before anastomosis, and that these flow profiles are reflected on the grafted conduit flow characteristics.

On the other hand, in the group with lower grade coronary stenosis, flow volume was lower in the arterial conduits than in the SVG. In other words, flow volume of the arterial conduits was reduced by native flow competition, however, the effect of competitive flow was not significant in the SVG. The patency of the SVG might be poorly associated with the native coronary stenosis. In contrast, the calculated shear stress of the ITA was also higher than that of the SVG, even when the grafts were anastomosed to the lower grade coronary stenosis, whereas shear stress of the GEA was as low as that of the SVG under flow competitive conditions. These results suggest that the ITA might have more flow adaptability to modulate arterial diameter to maintain flow velocity and shear stress, compared with the GEA. Graft narrowing of the ITA because of flow competition is generally reversible due to progression of native coronary artery stenosis. The string sign is considered to be an atrophic change in the ITA graft occurring with flow competition. It is unknown how long the non-functioning ITA graft maintains anatomical patency but we presume that the presence of the string sign in the GEA would not be prolonged, as this sign is relatively rare in a GEA graft with flow competition. This may be due to morphologic and anatomical differences between these grafts; the GEA is a muscular artery whereas the ITA is an elastic artery [17].

Ofili et al. [18] reported that the average peak velocity measured using a DGW is 23±11 cm/s in the distal LAD, 21±6 in the distal CX and 21±9 in the distal right coronary artery. The shear stress of the distal coronary artery near the anastomosis can be estimated using the formula used in the present study, producing a shear stress of approximately 15 dyn/cm2 (shear rate 420). This value is similar to the shear stress obtained in the distal portion of the ITA grafts in both groups H and L. On the other hand, the mean shear stress of the GEA near the anastomosis in group L was 5 dyn/cm2. This value seems to be too low for an arterial conduit grafted to the coronary artery.

Flow reversal in early systole was observed in the arterial conduits to the coronary artery with lower grade stenosis. The distance from the aortic root to the graft anastomosis causes a delay in the pressure wave of the graft, with the wave reaching the ITA or GEA after the coronary artery, which is much closer to the aorta. This is one of the reasons why the ITA graft shows the so called ‘to and fro pattern’ [19] or ‘swinging flow pattern’ [10] under high-grade competitive flow conditions. This delay might affect graft patency, and it is unlikely that such an effect would be beneficial under competitive flow conditions. Compared with the ITA, flow reversal seemed to be more apparent in the GEA, which is farther from the aorta. However, the long-term patency rate for coronary arteries with intermediate stenosis is likely to be better in ITA grafts than GEA grafts.

It has been speculated that increased shear stress might be one of the major factors affecting the patency of the saphenous vein after implantation into arterial circulation. Porter et al. [20] found that the arterial shear stress (9 dyn/cm2) inhibited the development of saphenous vein intimal hyperplasia more than venous shear stress (1 dyn/cm2). Zhu et al. [21] compared the expression levels of endothelin-1 and constitutional nitric oxide synthesis by the saphenous vein endothelial cells exposed to various shear stress (30, 6, 2, and 0 dyn/cm2) and found that the saphenous vein under 6 dyn/cm2 had the best endothelial function. Whether the calculated value (5 dyn/cm2) of SVG shear stress obtained in the present study can be estimated to be increased or decreased as a venous conduit grafted into coronary circulation remains unclear.

The present study has several limitations. First of all, shear stress was estimated from the graft diameter and velocity on the hypothesis that blood viscosity was constant. Although blood is a non-Newtonian fluid, blood viscosity has a relatively constant value for share rates above 100 s-1 [22]. Therefore, many investigators have estimated shear stress on this hypothesis in previous studies [23]. Secondly, percent diameter stenosis is not always the best predictor for native coronary flow. Therefore, it is difficult to define the degree of coronary stenosis required to keep the GEA graft patent.

Thirdly, the radial artery is a common arterial conduit for coronary revascularization, however, it had not been used in our institutes yet during the study period. Moreover, the radial artery, which might also be sensitive to competitive flow [24], seems to be unsuitable for this study because it is at high risk of spasm induced by a DGW. Fourthly, because the present study only determined the hemodynamic differences among the three kinds of bypass conduits, long-tem graft patency rates for lower grade stenosis should be considered to decide which conduit should be used to each target coronary artery. Our data suggest that the GEA is not necessarily feasible for lower grade coronary stenosis. When the right coronary artery system is a target vessel with lower grade coronary stenosis, the radial artery is also at high risk of failure [24]. Results of the right ITA to the posterior descending artery are not always acceptable [25]. The SVG to the right coronary artery system may be the best choice for coronary revascularization with native flow competition. When the circumflex branch is a target, the right ITA is often available via the transverse sinus while the left ITA to the circumflex and the right ITA to the left anterior descending artery are other options. In addition, prophylactic ITA anastomosis to the LAD without stenosis is still not recommended, although the present study showed superior shear stress of the ITA.

In conclusion, shear stress of the ITA was superior and maintained despite the flow volume being reduced by flow competition. These results suggest that the ITA has flow adaptability to modulate arterial diameter so as to maintain flow velocity, shear stress and graft patency. Lower shear stress of the GEA for less severe coronary stenosis may be associated with the development of conduit failure. Therefore, GEA grafting for intermediate stenosis should be avoided when the other conduits are appropriate.


   Footnotes
 
Presented at the Joint 17th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 11th Annual Meeting of the European Society of Thoracic Surgeons, Vienna, Austria, October 12–15, 2003.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
References
 
Dr B. Buxton (Heidelberg, Victoria, Australia): Your research provides a scientific basis for some of the findings that we see with arterial grafting. I know you corrected for diameter, but could diameter alone account for most of the low shear stress in the veins?

Dr Shimizu: Yes, it is occasionally correct. The diameter is very important to assess the shear stress. If the bypass conduits can provide the same flow volume, the flow velocity is lower when the diameter is greater. This is the reason why the gastroepiploic artery has low shear stress.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 

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M. A. Deja, K. S. Golba, M. Malinowski, S. Wos, M. Kolowca, J. Biernat, M. Kajor, and T. J. Spyt
Skeletonization of internal thoracic artery affects its innervation and reactivity
Eur. J. Cardiothorac. Surg., October 1, 2005; 28(4): 551 - 557.
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 Ann. Thorac. Surg.Home page
T. Shimizu, H. Suesada, M. Cho, S. Ito, K. Ikeda, and S. Ishimaru
Flow Capacity of Gastroepiploic Artery Versus Vein Grafts for Intermediate Coronary Artery Stenosis
Ann. Thorac. Surg., July 1, 2005; 80(1): 124 - 130.
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