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Eur J Cardiothorac Surg 2001;19:254-259
© 2001 Elsevier Science NL

Vasoactive response of different parts of human internal thoracic artery to isosorbide-dinitrate and nitroglycerin: an in-vitro study

Yosef Paza,b, Jacob Gurevitcha,b, Inna Frolkisa,b, Itzhak Shapiraa,b, Dimitri Pevnia,b, Amir Kramera,b, Chaim Lockera,b, Rephael Mohra,b

a Department of Thoracic and Cardiovascular Surgery, Tel Aviv Sourasky Medical Center, 6 Weizman Street, Tel-Aviv 64239, Israel
b The Sackler Faculty of Medicine, Tel Aviv University, Tel-Aviv, Israel

Received 27 June 2000; received in revised form 18 December 2000; accepted 8 January 2001.

Corresponding author. Tel.: +972-3-697-3322; fax: +972-3-697-4439
e-mail: shapiraiz{at}tasmc.health.gov.il


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 
Objective: The left internal thoracic artery (LITA) is the most important graft for coronary artery bypass grafting (CABG). Its distal region is, however, prone to vasospasm. The effect of nitroglycerin (NTG) and isosorbide-dinitrate (ISDN) on different segments of this region was studied. Methods: Rings of three segments of the LITA were studied: 6–9 mm proximal to the bifurcation (part A); 1–3 mm proximal to the bifurcation (part B); and 3–6 mm distal to the bifurcation (part C). After baseline, maximal contraction of the rings was achieved using 60 mmol/l of KCl, they were exposed to increasing doses of ISDN and NTG (10–100 µg/ml), and dose–response curves were recorded. Results: The contractile response of part A to KCl was significantly lower than that of parts B and C (1.87±0.25 versus 4.05±0.39 and 7.64±0.54 g, respectively; P<0.001). Both nitrates inhibited the contractile response in a concentration-dependent manner. The relaxing effects of both nitrates on part A was most pronounced (P<0.01), with the effect of ISDN being higher than that of NTG (P<0.01). Conclusions: The region 6–9 mm proximal to the LITA bifurcation is less prone to vasospasm, and has greater relaxation responses to ISDN and NTG than the more vasospastic distal parts of the LITA. We recommend avoiding the use of the very distal part of this artery during CABG, and to use high doses of ISDN rather than NTG as an anti-spastic measure.

Key Words: Human internal thoracic artery • Nitroglycerin • Isosorbide-dinitrate


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 References
 
There has been considerable and growing interest during the last few years in the use of arterial conduits in coronary artery bypass grafting (CABG), partly as a result of the well-documented, superior long-term patency rate of internal thoracic arteries (ITA) over the traditionally used saphenous vein bypass grafts [1], and of the increasing frequency of reoperative coronary bypass grafting in patients with occluded venous grafts [2]. The left internal thoracic artery (LITA) is the most common graft used in coronary artery bypass operations. Postoperative coronary angiography has proved that, like other arterial conduits, LITA is prone to arterial spasm [3].

Nitroglycerin (NTG) and isosorbide-dinitrate (ISDN) are widely used in treating patients with ischemic heart disease and congestive heart failure [4]. While these nitrates have a relaxing effect on all vessel types, the extent of this effect varies considerably between vessels from different anatomical regions and in different species [5].

Nitrates are converted enzymatically to nitric oxide (NO) in the vascular smooth muscle cells. NO stimulates soluble guanylate cyclase, causing an increase of cyclic GMP content that results in vasodilatation [6]. Several research groups have demonstrated that nitrates given perioperatively can prevent spasm of arterial grafts [7].

The length of the ITA is sometimes a limiting factor during CABG. A short LITA can leave the surgeon no choice but to use the entire length of the conduit. Knowing the vasoactive response of the distal region of the LITA and its reaction to anti-spastic treatment with nitrates will provide valuable information for optimal selection of the LITA segments for grafting.

The purpose of this in-vitro study was to compare the relaxation effect of NTG and ISDN on different segments of the distal human LITA.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 References
 
2.1. Preparation of vessels
The LITA was harvested in a skeletonized fashion from patients undergoing CABG. The skeletonized artery was isolated gently with scissors and silver clips, without cauterization. The most distal region of LITA bifurcates to the musculophrenic and gastroepiploic arteries (Fig. 1). We defined the segment 6–9 mm proximal to this bifurcation as part A, the region 1–3 mm proximal to the bifurcation as part B, and the proximal part of the superior-epigastric artery, 3–6 mm distal to the bifurcation, as part C.



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  		Fig. 1. Rings of different parts of the distal region of the LITA were used (schema). Part A, 6–9 mm proximal to the bifurcation; part B, 1–4 mm proximal to bifurcation; and part C, proximal part of the superior-epigastric artery.

 
2.2. Organ bath technique
Arterial rings, 3 mm in length, were suspended on wire hooks in a 100-ml jacket glass bath, the temperature of which was maintained at 37°C. The modified Krebs–Henseleit (KH) buffer solution had the following composition: 118 mmol/l NaCl; 4.7 mmol/l KCl; 2.0 mmol/l CaCl; 1.2 mmol/l MgSO4.7H2O; 1.2 mmol/l KH2PO4; 11.1 mmol/l glucose; 25 mmol/l NaHCO3. The perfusate was bubbled continuously with 95% O2 and 5% CO2. The upper hook was connected to a force transducer (Instrument & Control LTD, Israel), and the lower hook was fixed on a Stalin leg. The amount of force was recorded on a Beckman Dynograph Recorder R611 (USA). Two organ bath arrangements were run simultaneously.

2.3. Protocol
After the rings were equilibrated without tension on the wire hooks for 1 h, a normalizing procedure was performed. The resting tension applied to each ring was equivalent to that required to stretch the ring to 90% of its internal circumference when distended with a transmural pressure of 100 mmHg [8]. After the normalizing procedure, the rings were left to rest for 30 min. A steady level of active contraction was then established by adding potassium chloride (KCl, 60 mmol/l). This concentration gave 60–80% of the maximal contraction of this agent on the LITA. Cumulative concentration–response curves for ISDN and NTG were obtained by adding the drugs in concentrations of 10–100 µg/ml to the organ chamber. Curves were obtained from ten different rings for a designated part of the LITA. A concentration–response curve was obtained only once for each ring.

In this study, we paid particular attention to carefully mount the LITA rings on the wire hooks in the organ bath in order to minimize damage to the endothelium. In all experiments, the presence of functional endothelium was confirmed by determining the relaxation response to 10-5 mol/l acetylcholine.

2.4. Drugs and chemicals
NTG was purchased from Taro Pharmaceutical Industries Ltd. (Israel), ISDN from Schwarz Farm AG (Monheim, Germany), and other chemicals were purchased from Sigma (St. Louis, MO).

2.5. Statistics
The results are presented as means±standard error. Statistical analysis was performed using the Student's unpaired t-test. Two-way analysis of variance (ANOVA) was used to calculate dose–responses and for comparison of groups. Significance was established at a P level of <0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 References
 
3.1. Contraction
Incubation of the rings with KCl resulted in different contractions of different parts of the LITA (Fig. 2). In the most proximal part (part A), KCl induced a significantly lower contractile force than it did in parts B and C (1.87±0.25 versus 4.05±0.93 and 7.64±0.54 g, respectively; part A versus part B, P<0.001; part A versus part C, P<0.001). KCl induced the most significant contractile force (P<0.001) in the most distal part (part C) compared with other parts.



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  		Fig. 2. Effect of KCl on different parts of the LITA. Contractile force (in grams) responses of parts: (A), A; (B), B; and (C), C of the LITA (n=10 in each group; see Fig. 1 for definitions). The contractile response of the proximal part A was significantly lower than that in parts B and C (P<0.001).

 
3.2. Relaxation
ISDN induced a more pronounced relaxation of the precontracted part A of LITA than did NTG (P<0.001, ANOVA; Figs. 3 and 4A). Specifically, the maximal relaxation induced by ISDN was 46.08±2.06%, whereas it was 20.45±1.82% by NTG (P<0.02). ISDN was more effective than NTG on the vasorelaxation of part B of the LITA (Fig. 4B; P<0.01, ANOVA). However, in part C, no differences between these nitrates were observed (Fig. 4C), and the maximal relaxations of the vessel rings of this part were relatively inconsequential (9.65±4.01% for ISDN and 10.7±4.23% for NTG).



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  		Fig. 3. Original records of the relaxation of part A (6–9 mm proximal to the bifurcation) of the LITA. Rings were precontracted with 60 mmol/l of KCl, followed by the addition of increasing concentrations of ISDN or NTG (10–100 µg/ml). The contractile response to KCl started immediately after exposure to KCl (see KCl, arrow); relaxation to ISDN and NTG occurred at the points indicated by the ISDN arrow and the NTG arrow. The points on the ISDN and NTG curves indicate incubations with different concentrations of nitrates.

 


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  		Fig. 4. Effect of ISDN versus NTG on different parts of the distal LITA. The effect of ISDN and NTG on: (A), part A; (B), part B; and (C), part C of the LITA (n=10; see Fig. 1 for definitions). Rings were precontracted with 60 mmol/l of KCl, followed by the addition of increasing concentrations of ISDN or NTG (10–100 µg/ml). The relaxation effect of ISDN was significantly stronger than that of NTG on part A compared with parts B and C of the LITA (P<0.001 and P<0.01, respectively, ANOVA).

 
A comparison of the relaxation effects induced by ISDN on different parts of the LITA showed that the relaxation of part A was more pronounced than that of parts B and C (P<0.001, ANOVA; Fig. 5A). There were no differences between the relaxation induced by ISDN on parts B and C.



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  		Fig. 5. Relaxation response of the distal LITA to: (A), ISDN; and (B), NTG (n=10 in each group). Rings were precontracted with 60 mmol/l of KCl, followed by the addition of increasing concentrations of ISDN or NTG (10–100 µg/ml). ISDN caused a stronger relaxation of part A than that of parts B and C of the LITA (P<0.001, ANOVA; see Fig. 1 for definitions). Relaxation responses to NTG were more significant in part A than parts B and C of the LITA (P<0.001 and P<0.05, respectively, ANOVA). There was no difference between the degrees of relaxation of parts B and C when incubated with ISDN or NTG.

 
Similar results were obtained with NTG (Fig. 5B). Again, there was a significant increase in the relaxation of part A compared with parts B and C (P<0.001 and P<0.05, respectively), and there were no differences in relaxation between parts B and C.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
References
 
We demonstrated that the most proximal part of the distal LITA (Fig. 1, part A) is less susceptible to spasm than the more distal parts of the vessel, i.e. the parts located just before and beyond the bifurcation (Fig. 1, parts B and C, respectively). KCl produced the lowest contractile response in this part of the artery, where the relaxation response to the two nitrates used was also most prominent. Of these two nitrates, ISDN emerged as being superior to NTG by having a more pronounced relaxation effect.

Spasm of the conduits used for CABG [3] raises concern about their reactivity to circulating vasoconstrictors. Several substances, acting either in a synergistic or additive manner, might induce perioperative spasm.

He et al. demonstrated that contractile responses to norepinephrine and endothelin-1 were greater in rings taken from either branch of ITA bifurcation than in rings taken from the main portion of ITA [9].

The selection of KCl as the contracting agent in the present study was based on the relatively high concentrations of KCl in cardioplegic solutions used in our department during CABG. In our experiments, potassium ions served as membrane depolarizing agents to open voltage-operated calcium channels. KCl had a different contractile effect on different parts of the distal LITA: it produced the maximal contractile response in the more distal part (C), and the lowest contractile response in the more proximal part (A). Previous studies have also demonstrated such differences between different arteries, i.e. a pronounced increase in the contractile response of the radial artery to KCl when compared either with the ITA or gastroepiploic arteries [10], and in the canine coronary artery when compared with the ITA [11]. He et al. showed that in a segment of ITA placed 3–4 cm proximal to the bifurcation, the contractile force induced by U46619 and KCl was inversely correlated to the diameter of this segment [12]. This phenomenon might be explained by the differences in the densities of voltage-dependent channels of the smooth muscle cell membrane and by the sensitivity of the contractile apparatus to calcium, or by differences in the histological composition of the vessel walls. In their histological study, van Son et al. demonstrated that the two main branches after bifurcation of the ITA are muscular arteries, with rare elastic lamellae, and that the ITA is elastomuscular at its distal section before bifurcation [13].

The second observation of our study is that the relaxation response to each of the two nitrates varied between different parts of the distal LITA. Both ISDN and NTG produced a more significant relaxation in the most proximal part (A) of the distal LITA than in the more distal parts (B and C). It is well-documented that the vasodilating properties of nitrates are heterogeneous. For example, the coronary arteries were found to be more sensitive to nitrates than were peripheral arteries [5]. These drugs preferentially dilate larger rather than smaller coronary arteries [14]. The sensitivity to the NO donor, SIN-1, was more pronounced in the gastroepiploic artery than in the internal mammary artery [15]. Venous vessels possess the greatest sensitivity to nitrates [16]. Interestingly, Lüscher et al. showed that endothelium-dependent relaxation was greater in the mammary artery than in the saphenous vein [17].

The third observation of this study is that ISDN produced a more pronounced relaxing effect than NTG on parts A and B of the LITA. Other studies have shown that nitrates differed in their actions on different vessel walls. For example, NTG was found to be more active than ISDN on the rabbit aorta [18]. Toyoda and associates [16] showed in the rabbit femoral vein, that the relaxation potency order of three commonly used nitrates was glyceryl-trinitrate>ISDN>isosorbide-5-mononitrate, and similar results were obtained when the rabbit renal vein was studied [19].

One possible explanation for the heterogeneous vasodilating effects of ISDN and NTG might be related to their metabolism. Differences in the chemical structure of the nitrates lead to differences in their metabolism. In order to exert pharmacological activities, nitrates must become metabolized to liberate NO. The metabolites of nitrates are pharmacologically active and induce vascular smooth muscle relaxation, which is less potent than their parent compounds [20]. It is possible, therefore, that the metabolism of nitrates to NO in the tissue or in structures adjacent to the vascular smooth muscle cells might make a significant contribution to the induction of the vasodilating effect.

The differences in the effects of ISDN and NTG observed in the current study might, therefore, be explained by different participation of several intracellular mechanisms in the action of nitrates. It is generally accepted that the intracellular second messenger, cGMP, mediates the vascular smooth muscle relaxation elicited by nitrates [6]. Tadjkarimi et al. [21] showed that glyceryl-trinitrate evoked a greater cGMP increase in the human ITA than in the saphenous vein, and that less cGMP per milligram of protein is required for maximal relaxation of this vein. In the rabbit aorta, ISDN induced maximal values of cGMP more rapidly than NTG [19].

The intracellular free calcium concentration plays a crucial role in the regulation of smooth muscle tension. Relaxation of vascular smooth muscles induced by cGMP is due to the reduction in cytosolic ionic calcium concentration. A decrease in the concentration of free intracellular calcium might be achieved by: a reduction of calcium influx across the plasma membrane; an increase in the binding of calcium to intracellular stores; reduction of the calcium release from these stores; and finally, an increase in outflow of calcium from the cells. Nitrates and other agents, which cause cGMP elevation, reduced the calcium concentration by all of these mechanisms [22].

Glyceryl-trinitrate, ISDN and isosorbide-5-mononitrate inhibit calcium release from intracellular stores more effectively in venous than in arterial preparations [23]. In our experiments, potassium ions served as a membrane depolarizing agent to open voltage-operated calcium channels and, in turn, to increase calcium influx. In this study, it was clearly shown that ISDN is more effective than NTG in inhibiting the contraction associated with voltage-operated channels.

Some reports have indicated that in the vascular smooth muscle cells, ISDN and NTG modulate the gating of two major potassium channels, ATP-sensitive and calcium-activated, which might play an important role in controlling vascular tone by changing the membrane potential [24].

The release of NO from coronary arteries and the conduit's endothelial cells is impaired following ischemia, and this might contribute to the vulnerability of the coronary and graft circulation to thrombus formation and vasospasm [11]. The results of a large number of experimental studies suggest that NO, NO precursors, and NO donors have a cardioprotective effect, and that they might preserve endothelial function and significantly decrease myocardial injury [25].

We conclude that the most proximal part of the distal LITA is less susceptible to spasm than the segments located just before and just after the bifurcation (superior-epigastric artery). This proximal part displayed the lowest contractile response to KCl. The relaxation response of this part to ISDN and NTG was most prominent when compared with more distal parts. ISDN was shown to be superior by having a more pronounced relaxation effect than NTG. We therefore recommend avoiding the use of the very distal part of the LITA, as well as the proximal part of the superior-epigastric artery, during CABG, and to use high doses of ISDN during this operation to avoid vasospasm.


   Acknowledgments
 
The authors thank Esther Eshkol for her editorial assistance.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 

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