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Eur J Cardiothorac Surg 2006;29:473-478
© 2006 Elsevier Science NL

Flow dynamics and wall shear stress in the left internal thoracic artery: composite arterial graft versus single graft

Massimo Lemma a , * , Andrea Innorta a , Matteo Pettinari a , Andrea Mangini a , Guido Gelpi a , Manuela Piccaluga b , Paolo Danna b , Carlo Antona a

a Division of Cardiovascular Surgery, Luigi Sacco Hospital, Via Grassi 74, Milan 20157, Italy
b Division of Cardiology, Luigi Sacco Hospital, Via Grassi 74, Milan 20157, Italy

Received 23 September 2005; received in revised form 16 January 2006; accepted 20 January 2006.

* Corresponding author. Tel.: +39 02 39042333; fax: +39 02 39042652. (Email: m.lemma{at}hsacco.it).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 
Objective: Phasic blood flow dynamics and wall shear stress (WSS) have the potential to directly modulate endothelial responses, playing an important role in the development of bypass graft occlusion. This study compares phasic blood flow velocity patterns and WSS of the left internal thoracic artery (LITA) used as a composite Y-graft (27 patients, Y-group) and as a single graft (24 patients, S-group) on the left anterior descending (LAD) coronary artery. Methods: An intravascular Doppler-tipped guide wire was used for postoperative analysis of phasic blood flow velocity. Flow velocities were recorded proximally and distally into the LITA in both groups. Digitalized spectral velocities were acquired to compute systolic peak velocity, diastolic peak velocity, and average peak velocity. The ratio of diastolic to systolic peak velocity was computed (DSVR). WSS was calculated from graft flow velocity and vessel diameter. Results: Proximal LITA in Y-group had greater average peak velocity (APV) (p = 0.000), DSVR (p = 0.026), flow volume (p = 0.000), WSS (p = 0.02), and diameter (0.019) than S-group. There were not significant differences for the distal LITA between the two groups. Conclusions: The LITA shows a marked adaptability to flow dynamics. The proximal tract of the LITA in Y-group is able to match increased flow requirements, probably through the release of endothelial vasoactive mediators. Flow velocity spectra acquired in the proximal LITA in Y-group resemble the biphasic coronary artery pattern with a clear diastolic predominance. This pattern is probably consequence of the increase of blood flow due to the lower vascular resistance of the Y-graft system and to the active dilatation of the LITA.

Key Words: Myocardial revascularization • Left internal thoracic artery • Composite arterial grafts


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 
It is widely recognized that endothelial cells are the biosensors of fluid dynamic shear forces that reduce arterial diameter when blood flow rate decrease and enlarge the diameter when the flow rate increases [1]. The tractive force induced by blood flow acting on the endothelial cell surface is called wall shear stress (WSS). This force modulates the levels of two potent endothelium-derived vasoactive mediators, the vasodilator Nitric oxide (NO) [2] and the vasoconstrictor endothelin-1 (ET-1) [3]. Moreover, different flow patterns have different effects on endothelial cells proliferation and endothelial synthesis of vasoactive mediators [4].

The left internal thoracic artery (LITA) is currently the conduit of choice for myocardial revascularization because of superior graft patency, reduced cardiac events, and enhanced short-term and long-term results [5]. Exclusive use of arterial conduits is seen by many surgeons as a potential solution for the late failure of saphenous vein grafts. This can be achieved using the LITA as a composite Y- or T-graft, in order to extend as much as possible the number of distal anastomosis.

Previous reports have shown a consistent pattern of biphasic blood flow velocity into in situ LITA and significantly higher WSS along LITA conduits than in saphenous vein grafts [6]. This study compares phasic blood flow velocity patterns and WSS of the LITA used as a composite Y-graft and as a single graft on the left anterior descending coronary artery (LAD).


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 
2.1 Study patients and selection criteria
This study was carried out in accordance with the recommendations of the World Medical Associations Declarations of Helsinki [7] and was approved by the Research Committee of our Hospital. Written informed consent for the research protocol was obtained from each patient before cardiac catheterization.

Since February 1999, a program of myocardial revascularization using either the right ITA or the radial artery (RA) in addition to LITA has been started in our Department. Arterial grafts were always harvested as a pedicle. Patients’ selection criteria for the different types of arterial grafting as well as operative technique and definitions of postoperative complications have been previously described [8]. Between March 2001 and February 2002, 40 patients receiving a composite arterial Y-graft (LITA–RA) gave their consent to predischarge cardiac catheterization comprising angiography and intravascular flow velocity measurements. Complete and reliable data could be taken only in 27 patients. In 13 patients flow velocity measurements and quantitative coronary angiography were not possible because of (1) failure to selectively and safely insert the guide catheter and/or the Doppler guide wire into the LITA, (2) poor quality signal, and (3) operator-dependent measurements errors. This group of patients is labeled as Y-excluded in the present paper, while the 27 patients with reliable data represent the Y-group. More recently also patients with complete arterial myocardial revascularization using the LITA as an in situ graft on the LAD and the RA in aorto-coronary position were asked to accept the same study protocol. Up to December 2004, 24 patients were enrolled. These patients represent the S-group in the present paper.

2.2 Predischarge cardiac catheterization and angiography
Patients were brought to the cardiac catheterization laboratory in a fasting state. All cardioactive medications were continued as clinically indicated. All the patients received midazolam (5–10 mg i.v.) as precatheterization medication. Coronary angiography was performed by standard femoral approach. Selective injection of the native coronary arteries and grafts was performed by diagnostic six French catheters. After injection of a single bolus of 5000 IU of heparin, selective angiography of the coronary arteries was performed first followed by grafts angiography. Evidence of a good angiographic result was the prerequisite to start the study protocol.

2.3 Intravascular flow velocity measurements
Intravascular blood flow velocity was measured using a 175-cm long, 0.014-in. (0.036 cm) diameter flexible steerable Doppler guide wire (FlowWire, Cardiometrics, Inc., Mountain View, CA, USA) part of a system coupled to a real-time spectrum analyzer, PAL videocassette recorder and video image printer. Simultaneous electrocardiogram, arterial blood pressure, and central venous pressure signals were also continuously recorded on a multichannel recorder. The tip of the Doppler guide wire was advanced into the LITA and stopped 3 cm after LITA take off from the left subclavian artery. The Doppler signal being dependent on the wire position relative to the flow stream within the vessel, the wire was manipulated until the best high-quality phasic signal of blood flow velocity was obtained. Intravascular flow velocity measurements were repeated as detailed above about 3 cm before the coronary anastomosis.

2.4 Quantitative biplane angiographic assessment
The segments of LITA investigated by the Doppler guide wire were analyzed and the vessel diameter was measured at end diastole by biplane quantitative coronary arteriography in two orthogonal views, usually but not exclusively 30° right anterior oblique projection and 60° left anterior oblique projection, using an electronic digital caliper (Thoshiba Corporation, Shimoishigami, Otawara-Shi, Tochigi-Ken, Japan or Philips Medical System, Italy) with the six French guiding catheters as a known reference diameter. The graft cross-sectional area was computed assuming the vessel as elliptical.

2.5 Flow velocity data analysis and flow volume calculation
Frequency analysis of the Doppler signal was carried out in real time by fast Fourier transformation with the use of a velocimeter (FlowMap, Cardiometrics, Inc.). Systolic peak velocity, diastolic peak velocity, the time–average peak velocity (APV) and the ratio between diastolic and systolic peak velocities (DSVR) were determined from phasic coronary blood flow recordings. Quantitative estimation of the flow volume in the proximal and distal LITA of both groups was computed considering the cross-sectional area and the APV, according to Doucette et al. [9], as follows:


Formula

where Q is the flow volume per minute and R is the vessel radius in cm.

2.6 Wall shear stress calculation
WSS was calculated using the modified Hagen–Poiseuille equation [10]:


Formula

where µ is the blood viscosity assumed to be constant at 0.0035 kg/ms and D is the vessel diameter.

2.7 Statistical analysis
All statistical analyses were performed using the SPSS® 11.0 software (SPSS Inc., Chicago, IL, USA). Continuous data were presented as mean ± standard deviation. Normal distribution was tested using both the Kolmogorov–Smirnov statistics with a Lilliefor's significance level and the Shapiro–Wilk statistics. Student's t-test and paired Student's t-test were used after evidence of normality.

Nominal data were analyzed using the {chi} 2-test. A probability value less than 0.05 was considered statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 
3.1 Clinical results
Clinical features of the 40 patients who received a composite arterial graft are reported in Table 1 . There were no differences between Y-excluded and Y-group. Preoperative clinical characteristics were not different between S-group and Y-group with the exception of female sex (Table 2 ).


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  		Table 1. Preoperative characteristics of the 40 patients receiving a composite arterial Y-graft
 

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  		Table 2. Preoperative characteristics of the study population
 
All the patients underwent elective operation without concomitant procedures. All the operations were performed using normothermic extracorporeal circulation. Mean cardiopulmonary bypass time (88 ± 17 min vs 92 ± 21 min; p = 0.6) and mean aortic cross clamp time (67 ± 30 min vs 69 ± 23 min; p = 0.8) were not different between Y-excluded and Y-group. Mean cardiopulmonary bypass time was not different between Y and S-group (92 ± 21 min vs 90 ± 20 min; p = 0.7) while aortic cross clamp time was significantly longer in Y-group (69 ± 23 min vs 56 ± 17 min; p = 0.046). The anastomosis between the LITA and the RA was always performed after coronary anastomoses and during ischemic time. Mean number of distal anastomoses was 3.6 ± 0.7 (range 2–5) for Y-group and 3.4 ± 0.5 (range 3–4) for S-group (Table 3 ). There was no difference in the characteristics of distal anastomoses between Y-excluded and Y-group (Table 4 ). Mean intensive care unit stay was 29 ± 13 h in Y-group and 27 ± 10 h in S-group (p = 0.5). There were neither deaths nor perioperative myocardial infarctions and none of the patients had major postoperative complications. Mean hospital stay was 7 ± 1 days.


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  		Table 3. Distal anastomosis in the study population
 

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  		Table 4. Distal anastomoses in the 40 patients receiving a composite arterial Y-graft
 
All patients underwent postoperative angiography and intravascular flow velocity measurements before hospital discharge, after a mean of 5 ± 1 days from the operation.

3.2 Flow velocity measurement results and flow volume estimation
Proximal APV was significantly higher in Y-group than in S-group (p = 0.000) (Tables 5 and 6 ). There was not significant difference for distal APV between the two groups. Proximal APV was also significantly higher than distal in Y-group (p = 0.005). There was not significant difference between proximal and distal APV in S-group.


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  		Table 5. Angiographic and flow measurements results (S-group vs Y-group)
 

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  		Table 6. Angiographic and flow measurements results (proximal vs distal)
 
Proximal DSVR was significantly higher in Y-group than in S-group (p = 0.026). There was not significant difference for distal DSVR between the two groups. DSVR increased significantly going from proximal to distal LITA in both groups of patients (S-group, p = 0.000; Y-group, p = 0.006).

Flow volume estimation in proximal LITA was significantly greater in Y-group than in S-group (p = 0.000). There was not significant flow difference in distal LITA between the two groups. Proximal LITA flow was significantly greater than distal in Y-group (p = 0.000). There was not significant difference between proximal and distal LITA flow in S-group.

3.3 Angiographic results and WSS calculation
Patency rate for all the grafts was 100% in both groups of patients.

Proximal LITA diameter was significantly greater in Y-group than in S-group (p = 0.019) (Tables 5 and 6). Distal LITA diameter was not significantly different between the two groups. Proximal LITA diameter was significantly greater than distal in Y-group (p = 0.000). There was not significant difference between the proximal and distal LITA diameter in S-group.

Proximal WSS was significantly greater in Y-group (p = 0.02). There was not difference in distal WSS between the two groups and between the proximal and distal part in each group.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 
The present study shows that the LITA has a marked adaptability to flow dynamics with a clear propension to adequate WSS and cross-sectional area to flow requirements. Proximal LITA in Y-group has higher blood flow, APV, WSS and greater diameter than S-group. There is no difference between the two groups for distal LITA. Furthermore proximal LITA flow velocity pattern in Y-group is different from S-group, being characterized by increased diastolic peak velocities and decreased systolic peak velocities (Table 5).

Two modifications take place into the proximal LITA in Y-group: (1) a ‘passive’ increase in blood flow and (2) and an ‘active’ increase of LITA diameter.

4.1 Passive increase in blood flow
Blood flows into vessels due to a pressure gradient and the relationships among flow, pressure, and resistance into the vascular system can be described using the Ohm's law:


Formula

where Q is the flow volume, {Delta}P is the pressure gradient and R is the vascular resistance. Being the pressure gradient (mean aortic pressure–right atrial pressure) alike in the two groups of patients (Table 2), the significant higher blood flow volume and velocity into the proximal LITA in Y-group can be explained by the lower resistance of the parallel vascular circuit represented by the composite Y-graft, as expressed by Kirchoff's 2nd law:


Formula

where R tot is the total system resistance, and R 1 and R 2 are the resistances of each vessel. In other words, the resistance of a composite Y-graft is given by the resistance of a single vessel divided by the number of all the vessels. This means that immediately after a Y-graft operation the proximal LITA passively receives more blood flow as a consequence of the low vascular resistance of the two branches of the composite graft.

In S-group proximal LITA blood flow velocity and volume are lower being greater the resistance of the series vascular circuit represented by the single left ITA on the LAD, as expressed by Kirchoff's 1st law:


Formula

4.2 Active increase of LITA diameter
Proximal LITA in Y-group has larger diameter than S-group. We can speculate that higher blood flow and APV could stimulate the synthetic and secretory functions of endothelial cells, modulating the production of NO and ET-1 to obtain LITA dilatation. On the basis of experimental evidence, it has been suggested that in physiological conditions WSS regulates the release of endothelial cell-derived vasoactive mediators to maintain vessel tone. Chronic alterations of physiological blood flow cause the arterial diameter to change so as to recover a physiological state of WSS (15 dyne/cm2) [1]. This should lead to similar WSS values between the two groups of patients. Proximal WSS is significantly greater in Y-group probably because at 5 ± 1 days from the operation the LITA is not completely adapted to the new flow volumes. However, it has already been shown that the ITA is able to adapt its dimension to flow demand in the late postoperative period [11].

Finally also the flow pattern could have a role in the production of vasoactive substances by vascular endothelial cells. Rapid oscillations of flow in magnitude and direction can affect endothelial cell synthesis and release of NO, contributing to vasoconstriction and cell proliferation. Bach et al. [6] have shown that the in situ LITA displays an unusual pattern of phasic blood flow with a transition from systolic-predominant to diastolic-predominant peak flow velocity shifting from the subclavian to the coronary end. We have confirmed this pattern in S-group but not in Y-group, where we have recorded a diastolic-predominant peak of flow velocity in the subclavian end. This peculiar flow patter is probably related to the reduced vascular resistance of the parallel vascular circuit represented by the Y-graft configuration. However, in both groups of patients, DSVR evaluation showed a gradual but significant transition to predominant diastolic peak velocity moving from the subclavian to the coronary end (Table 6).


   5. Limitation of the study
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
6. Conclusions
 Appendix A
 References
 
WSS was computed from blood velocity and graft diameter on the hypothesis of a constant blood viscosity. Blood is a non-Newtonian fluid but its viscosity has a relatively constant value for share rates above 100 s–1 [12]. Other authors have estimated WSS on this hypothesis in previous studies [13].

Inaccuracies in determination of the vessel cross-sectional area may contribute to the variability of the flow calculations. Vessel diameter was measured at end diastole by biplane quantitative angiography in two orthogonal views and the graft cross-sectional area was computed assuming the vessel as elliptical. Although these measurements should be more appropriate than considering the vessel having a circular cross section [14], inaccuracies in our estimation of the cross-sectional area may have occurred, limiting the reliability of clinical measurements.

The quality of the signal and the value of the peak velocity recorded are dependent on consistent and careful positioning of the wire. Operator-dependent measurement errors are possible, minimized but not excluded by analyzing only curves of good quality. In our experience, many data were cast off as inappropriate, reducing the amount of data available for analysis.

The number of patients enrolled is relatively small, due to both the complexity of the study protocol that make its acceptance low by the patient, and to the high cost of the whole procedure.

Cardioactive medications were continued as indicated throughout the study. These drugs could affect the reliability of measured parameters. However, all these patients had diltiazem to minimize the risk of arterial spasm and this drug has been shown not to invalidate the measurements of coronary flow [15].


   6. Conclusions
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
Appendix A
 References
 
Our study shows that in composite Y-graft the proximal LITA is able to actively adapt its dimension to the flow demand, probably through the release of endothelial vasoactive mediators, consequence of higher values of WSS. This process of adaptation begins immediately after the operation as a consequence of a passive increase of blood flow due to the lower vascular resistance of the Y-graft system. A significant increase in LITA diameter can be pointed out 5 days after myocardial revascularization.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
References
 
Conference discussion

Mr D. Wheatley (Glasgow, United Kingdom): Could we say the take-home message from this is that an anastomosis to an internal mammary artery is a very good thing? The proximal vessel tolerates this very well and responds well to this.

Dr Lemma : We see that the internal thoracic artery is able to adapt its diameter immediately after the operation because the vascular resistance in the proximal part is very low. Immediately after the operation the higher flow velocity stimulates the endothelium to produce nitric oxide, and after one week from the operation, the proximal part of the left internal thoracic artery is larger, and this is the initial phase of the chronic adaptation of the left internal thoracic artery to blood flow.

Mr Wheatley : And a more flippant comment, a take-home message for the cardiologists, is that the surgeon has a drug-eluting conduit now.

Dr A. Moritz (Frankfurt, Germany): There are people taking these Y-grafts to revascularize all of the heart. I am somewhat reluctant, and I am asking you, do you know the total flow capacity, which is the most interesting thing? I mean, if you stress these patients, it should turn out if this graft is able to provide the full flow capacity you need in your coronaries. That is question one. And the second one is how different is the measured flow from the normal physiologic coronary flow? Do you reach with these Y-grafts a regular flow pattern in the target coronaries, in the circumflex or the LAD, or is this type of flow different from a normal physiologic flow?

Dr Lemma : About the first one, we published two years ago a paper in the European Journal of Cardiothoracic Surgery. We analyzed the flow capacity of the Y-graft postoperatively pacing the heart at 85% of the maximal heart rate for that patient, and we measured the flow before and after pacing, and we saw that the internal mammary artery is able to give all the blood flow the heart needs during maximal stress. We have shown that the internal thoracic artery is able to give all the blood the heart needs immediately after the operation.

About the second question, we didn’t record the flow velocity into the coronary vessels. We stopped about 3 cm before the distal anastomosis. So I can only tell you that the pattern of flow in the graft, in the left internal thoracic artery, is different between the left internal thoracic artery used as a single graft or as a Y-graft, in the sense that in the proximal part of the Y-graft we have a flow pattern with a predominant diastolic phase.

Dr Moritz : But you can correlate your data to the regular well-known standard data of coronary flow?

Dr Lemma : No, because we didn’t measure the flow into the coronary arteries.


   Footnotes
 
{star} Presented at the joint 19th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 13th Annual Meeting of the European Society of Thoracic Surgeons, Barcelona, Spain, September 25–28, 2005.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Limitation of the...
 6. Conclusions
 Appendix A
 References
 

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  3. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988;332(6163):411-415.[CrossRef][Medline]
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  5. Cameron A, Davis KB, Green G, Schaff HV. Coronary bypass surgery with internal-thoracic-artery grafts: effects on survival over a 15-year period. N Engl J Med 1996;334(4):216-219.[Abstract/Free Full Text]
  6. Bach RG, Kern MJ, Donohue TJ, Aguirre FV, Caracciolo EA. Comparison of phasic blood flow velocity characteristics of arterial and venous coronary artery bypass conduits. Circulation 1993;88(5 Pt 2):I133-I140.
  7. World Medical Association Declaration of Helsinki Recommendations guiding physicians in biomedical research involving humans subjects. Cardiovasc Res. 1997;35:2–3..
  8. Lemma M, Gelpi G, Mangini A, Vanelli P, Carro C, Condemi A, Antona C. Myocardial revascularization with multiple arterial grafts: comparison between the radial artery and the right internal thoracic artery. Ann Thorac Surg 2001;71(6):1969-1973.[Abstract/Free Full Text]
  9. Doucette JW, Corl PD, Payne HM, Flynn AE, Goto M, Nassi M, Segal J. Validation of a Doppler guide wire for intravascular measurement of coronary artery flow velocity. Circulation 1992;85:1899-1911.[Abstract/Free Full Text]
  10. Kute SM, Vorp DA. The effect of proximal artery flow on the hemodynamics at the distal anastomosis of a vascular bypass graft: computational study. J Biomech Eng 2001;123(3):277-283.[CrossRef][Medline]
  11. Gurne O, Chenu P, Polidori C, Lougagie Y, Buche M, Haxhe JP, Eucher P, Marchandise B, Schroeder E. Functional evaluation of internal Mammary artery bypass grafts in the early and late postoperative periods. J Am Coll Cardiol 1995;25:1120-1128.[Abstract]
  12. Doriot PA, Dorsaz PA, Dorsaz L, De Benedetti E, Chatelain P, Delafontaine P. In-vivo measurements of wall shear stress in human coronary arteries. Coron Artery Dis 2000;11:495-502.[CrossRef][Medline]
  13. Wentzel JJ, Krams R, Schuurbiers JC, Oomen JA, Kloet J, van Der Giessen WJ, Serruys PW, Slager CJ. Relationship between neointimal thickness and shear stress after Wallstent implantation in human coronary arteries. Circulation 2001;103:1740-1745.[Abstract/Free Full Text]
  14. Sakaguchi G, Tadamura E, Ohnaka M, Tambara K, Nishimura K, Komeda M. Composite arterial Y graft has less coronary flow reserve than independent grafts. Ann Thorac Surg 2002;74:493-496.[Abstract/Free Full Text]
  15. Rossen JD, Simonetti I, Marcus ML, Braun P, Winniford MD. The effect of diltiazem on coronary flow reserve in humans. Circulation 1989;80:1240-1246.[Abstract/Free Full Text]



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