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J Thorac Cardiovasc Surg 1995;110:453-462
© 1995 Mosby, Inc.

SURGERY FOR ACQUIRED HEART DISEASE

LATE ENDOTHELIAL FUNCTION OF FREE AND PEDICLED INTERNAL MAMMARY ARTERY GRAFTS

Sudhir S. Kushwaha, MRCP, MDa, Mahmud Bustami, MBBSa, Samad Tadjkarimi, MD, FRCSb, Charles D. J. Ilsley, MRCPa, Andrew G. Mitchell, MRCPa, Magdi H. Yacoub, MD, FACCb


Harefield, United Kingdom

Received for publication Oct. 12, 1994. Accepted for publication Feb. 7 1995. Address for reprints: Sudhir Kushwaha, MD, MRCP, Cardiovascular Institute, The Mount Sinai Medical Center, One Gustav L. Levy Place, New York, NY 10029-6574.

Abstract

The internal mammary artery has greater long-term patency than the saphenous vein when used for coronary bypass grafting. Therefore, bilateral use of the internal mammary artery for grafting with the right internal mammary artery used as a "free" graft may result in improved graft survival. The study objectives were to compare the endothelial-dependent and -independent vasodilatory response in free and pedicled internal mammary artery grafts in patients who had previously undergone coronary surgery. Free (group 1, n = 8) and pedicled (group 2, n = 7) internal mammary artery grafts were studied by comparing the response to selective infusion of the endothelial-dependent vasodilator substance P (1.4 up to 22.4 pmol/min in doubling dose increments) followed by isosorbide dinitrate (2 mg over 2 minutes), in patients undergoing coronary angiography, 1 month to 6 years after coronary surgery. Maximal dilatory response to substance P was 8.7% ± 1.8% in pedicled grafts compared with 8.8% ± 2.3% in free grafts (p = not significant), with the dose response for both groups being similar. Infusion of isosorbide dinitrate produced only minimal further dilatation in both groups. No significant difference was found in endothelium-dependent and -independent vasodilatory response between free and pedicled internal mammary artery grafts, suggesting that the use of the free right internal mammary artery and other arterial grafts may enhance graft survival. (J THORAC CARDIOVASC SURG 1995;110:453-62)

The internal mammary artery (IMA) has been shown to have greater long-term patency for coronary artery bypass grafting when compared with the saphenous vein graft.Go Go 1,2 The vasodilator and antithrombotic properties of the vascular endothelium, which have been shown to be superior in the IMA compared with the saphenous vein grafts,Go 3 may be responsible for this greater long-term patency. The endothelium has been shown to modulate underlying vascular smooth muscle by the release of endothelium-derived relaxing factor,Go 4 which also reduces intraluminal platelet adhesionGo 5 and has potent antiaggregatory properties.Go 6 These antithrombotic properties may prevent the development of atherosclerosis, which develops with much greater frequency in saphenous vein grafts.

For this reason, interest has increased in the use of arterial conduits for coronary artery bypass grafting.Go 7 Bilateral use of the IMA for grafting has theoretical advantages over saphenous vein grafts.Go 8 One of the techniques is to use the right IMA as a "free" graft. The IMA is transected near the origin of the subclavian artery, with the proximal end being anastomosed to the aorta and the distal end to the coronary artery.Go 9 The advantages of this technique include the potential for grafting any branch of the coronary system and the possibility of using two or three segments of the same internal mammary vessel for grafting different vessels without resorting to sequential anastomosis. In addition, the technique can be used in patients with occlusive disease of the subclavian artery or accidental injury of the proximal IMA during dissection. Endothelial function of the IMA has been examined in vitro,Go 10 but endothelial-dependent and endothelial-independent vasodilatory abilities of the free graft have not been assessed in human subjects. Use of the free graft results in the denervation of the IMA with loss of the vasa vasorum and lymphatics, which may affect arterial vasodilatory ability, particularly in relation to flow mediated dilatationGo 11 as a result of increased myocardial demand. This study was carried out to examine and compare the endothelium-dependent and endothelial-independent vasodilatory response of free right and pedicled left IMA grafts in human subjects who had undergone coronary artery bypass grafting.

Substance P is an 11 amino acid vasodilator neuropeptide. It is found in the peripheral nervous system in sensory neurons,Go 12 the vagus,Go 13 and some sympathetic ganglia.Go 14 It is a potent vasodilator in human beings, causing vasodilatation in the forearm when infused into the brachial arteryGo 15 and dilating epicardial coronary arteries when infused into the coronary circulation.Go 16 The vasodilator action of substance P has been shown to be endothelium dependent in most speciesGo 17 including man,Go Go 18,19 and its action in human coronary rings is inhibited by the nitric oxide synthesis inhibitor L-NG-monomethyl-arginine,Go 20 which is a specific inhibitor of nitric oxide from its precursor L-arginine. These findings suggest that substance P causes vasodilatation through the release of nitric oxide from the endothelium and, unlike acetylcholine,Go 21 has no vasoconstrictor action at higher doses and in coronary artery disease, making it suitable for the assessment of graft endothelial function in the present study population.

METHODS

A total of 15 patients were studied. Of these, seven had pedicled left IMA grafts and eight had free right IMA grafts in addition to left IMA grafts. In addition to receiving these grafts, all patients also had venous grafts, technical details of proximal and distal anastomoses are given in GoTable I, which also includes time of operation, location of coronary bypass grafts, and patency at angiography. In the patients with free IMA grafts, the free graft was used for the study. All IMA grafts that were studied were found to be patent with no angiographic evidence of atherosclerotic disease.


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  		Table I. Operative, angiographic, and clinical details of patients undergoing coronary angiography and bypass graft restudy with substance P infusion in free right and pedicled left IMA
 
Substance P infusion was carried out after left ventriculography and selective coronary angiography. Coronary arteriography was carried out with the Judkins technique. A baseline angiogram with iohexol radiopaque agent (Omnipaque 350) was performed in the projection best displaying the pedicled or free IMA graft as determined previously from the diagnostic films. This position was not altered throughout the course of the study. A high resolution 12.7 cm image intensifier (Optimus M200; Phillips Electronics, Sheldon, Conn.) was used. After a control angiogram, saline solution was infused at 1 ml/min for 2 minutes. This vehicle infusion was carried out before the infusions of substance P in all patients studied and was followed by an angiogram. Increasing concentrations of substance P were then infused at 1 ml/min for 2 minutes with a starting dose of 1.4 pmol/min and increasing in doubling increments up to a maximum dose of 22.4 pmol/min. Immediately after each infusion a coronary angiogram was performed. On completion of the substance P infusions, isosorbide dinitrate was infused at 1 mg/min for 2 minutes after which a final angiogram was taken.

Informed written consent was obtained from each patient, and the study was approved by the District Ethical Committee of Harefield Hospital.

Quantitative angiographic analysis.
Coronary artery luminal diameters were measured by an automated edge detection computer analysis system (Cardiovascular Angiography Analysis system, CAAS; Pie Data Medical, Neptune, N.J.). End-diastolic film frames were used for analysis, and specific segments of the IMA grafts were chosen. The size of the coronary catheter (8F in all cases) was used for calibration of the image in millimeters, and correction was made for radiographic pincushion distortion. In total 15 IMA segments were analyzed--seven pedicled and eight free IMA segments. Of the 15 films, 7 were reanalyzed by a second observer, and the measurement was highly reproducible: r = 0.95 and p = not significant between observations.

Data presentation.
Diameters of the grafts are expressed in millimeters or as percent diameter change from the control value. Mean ± 1 standard error of the mean is given for each dose of substance P. Responses were compared by means of repeated measures analysis of variance. A p value of <0.05 was taken to indicate significance.

RESULTS

All patients tolerated the study, and no complications occurred. No patients had symptoms of angina, although mild left-sided chest discomfort was experienced by patients undergoing studies of the pedicled IMA graft at the time of contrast injection. This was not severe enough to terminate the study.

Individual responses to substance P and isosorbide dinitrate are shown in GoTable II. There was no significant effect of saline infusion on vessel diameter. The mean dose response for pedicled and free IMA grafts are shown in Fig. 1. Maximal response to substance P at the highest dose used was 8.7% ± 1.8% in pedicled grafts compared with 8.8% ± 2.3% in free grafts (p = not significant). Infusion of isosorbide dinitrate produced only minimal further dilatation in both groups, and this effect was not significant. No significant difference was found between the maximal responses of free and pedicled IMA vessels during all doses of the substance P infusion, and no difference was found in the response to isosorbide dinitrate. Fig. 2, A and B shows a typical response in a free IMA graft before substance P infusion and after infusion of the maximal dose. Fig. 3, A and B similarly shows the appearance of the pedicled IMA in one of the patients before infusion of substance P and after infusion of the maximal dose.


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  		Table II. Absolute diameter and percent diameter change in free right IMA grafts and pedicled left IMA grafts
 


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  		Fig. 1. Mean dose response to increasing doses of substance P infusion followed by isosorbide dinitrate (2 mg over 2 minutes) in seven patients with pedicled left internal mammary artery grafts (Ped) and eight patients with free right internal mammary artery grafts (Free). ISDN, Isosorbide dinitrate.

 


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  		Fig. 2. A, Angiographic appearance of a free right internal mammary artery graft after control (saline 0.9%) infusion and before substance P infusion. B, Angiographic appearance of free right internal mammary artery graft shown in Fig. 2 after infusion of substance P at maximal dose (22.4 pmol/min for 2 minutes). Note apparent increase in diameter of vessel with vasodilatory effects of substance P on native circulation.

 


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  		Fig. 3. A, Angiographic appearance of a pedicled left internal mammary artery graft after control (saline 0.9%) infusion and before substance P infusion. B, Angiographic appearance of pedicled left internal mammary artery graft shown in A after infusion of substance P at maximal dose (22.4 pmol/min for 2 minutes). Note apparent increase in diameter of vessel with vasodilatory effects of substance P on native circulation.

 
DISCUSSION

This study shows that the dilatory ability of free and pedicled IMA grafts, through endothelial-dependent and -independent mechanisms, is comparable early and late after coronary artery bypass surgery. The dilatory ability of the right IMA as a free graft appears not to be affected by transection of this vessel near its point of origin. Therefore denervation, as well as the loss of the vasa vasorum and lymphatics, does not significantly affect endothelial function of the free IMA graft. These findings have important implications in terms of graft survival and long-term results after coronary artery bypass surgery.

Previous longitudinal studies have shown that the IMA graft has a substantially improved long-term patency when compared with saphenous vein grafts,Go 2 improves survival, and is associated with a decreased frequency of other cardiac events.Go Go 1,22 Morphologic studies have shown that although some fibrointimal proliferation does occur in IMA grafts atherosclerosis is extremely rare.Go 23 Although use of the IMA for coronary bypass surgery increases operative time,Go 24 it is unlikely that there is any increased surgical risk.Go 25 The inevitable fate of venous bypass grafts appears to be the development of atherosclerosis, severely limiting their long-term utility.Go Go 26,27

Therefore, the finding that the free IMA functions in an almost identical manner to the pedicled IMA suggests that it too will have an increased survival when compared with venous grafts and that it should be used more frequently for the treatment of coronary artery disease. Bilateral use of the IMA has already been shown to have a low operative risk with excellent long-term functional improvement and survivalGo 8 and may be particularly useful for myocardial revascularization in reoperationsGo Go 28,29 where survival and functional improvement may be comparable with those patients undergoing primary revascularizations with bilateral IMAs. The use of the right IMA as a pedicled graft may be more difficult because of inadequate length often limiting its use to grafting the right coronary artery.Go 9 In addition, freeing this vessel of endothoracic fascia, internal mammary veins, and lymphatics — a technique known as skeletonizationGo 30 — may provide greater length but still usually does not permit grafting of the left anterior descending coronary artery or its branches. Use of the right IMA as a free graft allows it to be used for potentially greater numbers of sites without the constraints of length if the vessel is pedicled.

Arterial grafts provide an alternative to venous bypass grafting and attention has also recently focused on the use of the gastroepiploic artery as an alternative arterial conduit. Endothelial function of this vessel has also been examined in vitro, and it has been shown that this vessel has a strong capacity to secrete endothelium-derived nitric oxide.Go 31 The L-arginine pathway in both vessels has been shown to be similar, although the gastroepiploic vessel may have a difference in prostaglandin metabolism compared with the IMAGo 32 and a greater capacity for vasodilatation.Go 33 Other arterial grafts which have recently been advocated include the inferior epigastricGo Go 34,35 and the radial artery.Go 36 However, it is probable that the IMA is more suited for use in coronary artery grafting because of its histologic structureGo 37 and the nature of its endothelial and smooth muscle function compared with other arteries which may be used for arterial grafts.

Although the endothelial vasodilatory capacity of the IMA as shown in the present study does not appear to be as great as the native coronary circulationGo 16 or the gastroepiploic artery,Go 31 a recent study examining Doppler flow in response to various stimuli including exercise showed that the blood flow in this vessel increases appropriately.Go 38 In addition an in vitro study in a canine IMA preparation showed release of endothelium-derived relaxing factor when the vessels were perfused with a physiologic salt solution,Go 39 suggesting that flow mediated dilation of this vessel occurs in the setting of increased myocardial oxygen consumption. The gastroepiploic artery showed a greater increase in flow on taking food.Go 38 Arterial grafts may be more physiologic for the treatment of coronary stenoses with a capacity for flow-dependent vasodilatationGo 11 and may therefore be able to respond appropriately to changes in myocardial oxygen consumption. Saphenous vein grafts, by comparison, probably only function as conduits and have been shown, in vivo, to have a limited response to nitrate infusionGo 40 and are therefore unlikely to be able to exhibit flow-mediated changes in diameter. These factors may be of importance in ischemia of microvascular origin.Go 41 Selective loss of acetylcholine-mediated relaxation in vein grafts has been observed in the early postoperative period and may have a role in eventual vein graft failure.Go 42

It is possible that the observed effect on the vessels studied may not be a direct effect, but the result of flow-mediated dilatationGo 11 as a result of increased blood flow caused by substance P in the distal coronary vascular bed.Go 16 If vessel dilatation occurred as a result of this effect, then it was observed in pedicled as well as free grafts suggesting that both function in a physiologic manner, with increases in flow causing an increase in diameter. This effect may be impaired in atherosclerosisGo 43 and because all patients underwent coronary bypass grafting for coronary artery disease, this mechanism of dilation may be impaired in both the groups studied. Nitrates are thought to have minimal effects on coronary blood flow and function as local smooth muscle vasodilators.Go 44 Because the infusion of isosorbide dinitrate did not cause further significant dilatation, it is most likely that the observed effect is a result of a local action of the substance P with maximal achievable dilatation due to this agent being observed.

In conclusion, we have shown that the right IMA, used as a free graft for grafting any of the coronary arteries, functions in the same way as a pedicled left IMA. Endothelial-dependent and endothelial-independent vasodilatory mechanisms are comparable in both types of graft and also suggest that these grafts may function in a more physiologic manner than vein grafts. Use of longer lasting arterial grafts for coronary revascularization, including greater numbers of free grafts, will improve the long-term beneficial effects of this procedure and prevent the need for reoperation because of venous graft failure,Go 45 which remains the main reason for symptomatic deterioration after bypass grafting.

Footnotes

From the Departments of Cardiologya and Cardiac Surgery, b Harefield Hospital and NHLI, Harefield, Middlesex, United Kingdom. Back

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