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Ann Thorac Surg 2006;81:125-131
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Comparative Effects of Tolazoline and Nitroprusside on Human Isolated Radial Artery

Önder Teskin, MD a , B. Sönmez Uydes-Dogan, PhD b , * , Yavuz Enç, MD a , F. Ilkay Alp, BS b , Deniz Kaleli, BS b , Süheyla Keser, MD a , Taner Iyigün, MD a , Fuat Bilgen, MD a , Sabri Dagsali, MD a , Osman Özdemir, PhD b

a Department of Cardiovascular Surgery, Siyami Ersek Thoracic and Cardiovascular Surgery Education and Research Hospital, Istanbul, Turkey
b Department of Pharmacology, Faculty of Pharmacy, Istanbul University, Istanbul, Turkey

Accepted for publication July 6, 2005.

* Address correspondence to Dr Uydes-Dogan, Istanbul University, Faculty of Pharmacy, Department of Pharmacology, Beyazit, 34116, Istanbul, Turkey (Email: sudogan{at}tr.net).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Notice From the American...
 References
 
BACKGROUND: The radial artery is increasingly being used in coronary revascularization as an alternative conduit to a saphenous vein graft. Its perfect endothelial capacity provides a high patency rate comparable with the internal mammary artery (IMA). However, its spastic characteristics cause difficulties during its intraoperative preparation and may lead to early postoperative graft failure. Thus, treatment and/or prevention of radial artery spasm with an effective vasodilator agent is essential for its longevity. Endogenous vasoconstrictors, including noradrenaline, endothelin-1, and thromboxane A2, are likely to play a role in the pathogenesis of graft spasm. In the present study, we evaluated the vasorelaxant effect of tolazoline, a nonselective alpha-adrenoceptor blocker, against the contractions induced by various spasmogenic agents in an isolated human radial artery.

METHODS: Tolazoline (10–9–10–4 M) or sodium nitroprusside (SNP, 10–9–10–4 M) were cumulatively applied on radial artery rings precontracted submaximally with noradrenaline, endothelin-1, thromboxane analogue, U46619, or potassium chloride. In addition, some rings were pretreated with tolazoline (4 x 10–6 M) for 30 minutes and the contractile response curve to noradrenaline was assessed in its presence.

RESULTS: Tolazoline effectively reversed noradrenaline-induced contractions in the radial artery, whereas it failed to produce remarkable relaxations on rings contracted with other spasmogenic agents, while SNP overcame the contractions induced by all spasmogens to a similar extent. In addition, brief pretreatment of radial artery rings with tolazoline significantly inhibited the contractions to noradrenaline.

CONCLUSIONS: Tolazoline is not as broadly effective as SNP against all spasmogens investigated; however, it may be effective in counteracting alpha-adrenoceptor-mediated vasospasm in human radial arteries.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Notice From the American...
 References
 
The radial artery was introduced as a conduit in coronary artery bypass operations by Carpentier and colleagues in the early 1970s [1]. However, its usage was abandoned shortly after because of its tendency for spasm leading to low patency rates [2]. Increasing interest in total arterial revascularization, due to the high obstruction rates with saphenous vein grafts and the development of new techniques for prevention or treatment of vasospasm, revived the use of the radial artery as a graft material [3].

Endogenous vasoconstrictors are among various stimuli likely to evoke graft spasm. Plasma levels of various spasmogens, including noradrenaline, endothelin-1, thromboxane A2, and angiotensin II have been reported to be elevated during cardiopulmonary bypass [4]. Propensity to spasm is an important issue during harvesting of the artery, and for the management of myocardial perfusion by the use of a vasoconstrictor, particularly a sympathomimetic agent [3]. Previous studies have shown a dominant alpha-adrenergic receptor activity in a human radial artery [5], and stronger contractions were obtained in response to alpha-receptor agonists compared with the internal mammary artery (IMA) [6, 7]. Hence, circulating catecholamines and exogenous sympathomimetics may profoundly predispose radial artery spasm during the perioperative and early postoperative periods. Use of an optimal vasodilator is important in order to counteract radial artery spasm and improve its longevity. However, occasional lack of efficiency of currently used vasodilators and their side effects limiting their usage stimulate the search for alternative vasodilator agents against this vasospasm [8].

Tolazoline is a competitive, nonselective alpha-adrenergic receptor blocker used in persistent pulmonary vasoconstriction and hypertension of the newborn, due to its selective vasodilator activity on the pulmonary vascular bed [9, 10]. Vasodilator effect of tolazoline is also demonstrated in traumatic arterial spasm; its intraarterial administration prevents stasis and thrombosis in the damaged area by increasing local blood flow [11]. Similarly, it was found effective against local arterial vasospasm due to catheterization in the newborn [12]. A recent study reported an excellent vasodilator effect in forearm and hand arteries as well as an improvement in blood flow after intraarterial administration of tolazoline during angiography of the hand [13]. In vitro studies demonstrating the vasorelaxant effect of tolazoline also supports its effectiveness against increased vascular tone [14, 15]. However, we have found no published report on the use of tolazoline to overcome arterial graft spasm.

In the present study, we aimed to investigate the antispasmodic effect of the nonselective alpha-adrenoreceptor antagonist tolazoline against contractions induced by various spasmogenic agents in isolated human radial artery rings, in comparison with a nitrovasodilator, sodium nitroprusside (SNP). The contractile responsiveness of radial artery rings to noradrenaline after a brief exposure to tolazoline was also assessed.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Notice From the American...
 References
 
Sampling and Preparation of Radial Artery
Radial artery samples were obtained from patients undergoing coronary artery bypass operations. Due to the limitations of graft length, only the patients in which radial artery grafts were to be used to bypass the first marginal branch of circumflex or intermediate coronary arteries (ramus intermedius) were enrolled. Use of discarded human radial artery segments was approved by the Institutional Review Board of Siyami Ersek Education and Research Hospital (March 8, 2003). Informed consent was obtained from all candidate patients prior to operation. Clinical characteristics of the patients are given in Table 1.


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  		Table 1. Clinical Characteristics of the Patients Undergoing Coronary Revascularization
 
Caution was exercised during harvesting of the vessel in order not to stretch and touch the endothelial surface. The sampled segment of radial artery, which is not exposed to any preparatory solution, was placed into cold (4°C) Krebs-Ringer bicarbonate solution, then immediately transferred to the laboratory. Composition of the solution was as follows (in mM): NaCl 118.5, KCl 4.8, KH2PO4 1.2, NaHCO3 25, MgSO4.7H2O 1.2, CaCl2 1.9, glucose 10.1, and disodium ethylenediaminetetraacetic acid 0.026.

Adherent connective tissues were removed and specimen was cut into rings of 3 to 4 mm in length. Rings were suspended between two stainless steel L-shaped hooks in a 10 mL jacketed organ bath containing Krebs-Ringer bicarbonate solution at 37°C and aerated with 95% O2 and 5% CO2. One hook was fixed at the bottom of the organ bath while the other was connected to a force displacement transducer (Grass Model FT03; Grass Telefactor, West Warwick, RI), which was fixed to a micrometric manipulator allowing adjustments in the resting tension of the rings. The optimal point of length-tension relation had been determined in our preliminary experiments by repeated exposure to noradrenaline (5 x 10–5 M) at different levels of resting tension. Four grams provided maximal noradrenaline responsiveness in radial arteries and this was used as the resting tension. Two to three rings were obtained from each artery specimen.

Experimental Protocol
After the equilibration period of 2 hours, viabilities of the vessel segments were checked by potassium chloride (40 mM) and preparations that produced a tension of less than 3 g were discarded. Two consecutive potassium chloride responses were obtained for each ring in order to standardize the reactivity of the preparations. All experiments were carried on endothelium intact rings of the radial artery, and the presence of endothelium was confirmed by functional relaxation of noradrenaline precontracted arteries in response to 10–5 M acetylcholine (92.51 ± 3.84%, n = 22).

Experiments were performed to evaluate the antispasmodic effect of tolazoline against various spasmogenic agents; namely, noradrenaline, endothelin-1, thromboxane analogue U46619, and potassium chloride, in comparison with sodium nitroprusside (SNP). For each agent, the concentration required to produce a similar contractile force (g) in radial artery graft was determined and this concentration was used for submaximal (60% to 80%) contraction. Vessel rings were contracted submaximally with noradrenaline (3 x 10–6–10–5 M), endothelin-1 (10–8 M), U-46619 (3 x 10–8 M), and potassium chloride (20–30 mM). Then, increasing concentrations of tolazoline (10–9–10–4 M) and SNP (10–9–10–4 M) were applied on radial artery rings precontracted with one of the contractile agents. At the end of each experiment, relaxation capacities of radial artery rings were tested with SNP, which was applied at maximal concentration (10–4 M). In parallel control experiments, the contractions induced by the spasmogenic agents were found stable enough for the period required to construct the cumulative-relaxation curves for tolazoline and SNP.

The preventive effect of tolazoline against noradrenaline-induced contractions was also evaluated. In these experiments, the cumulative concentration-response curves to noradrenaline (10–8–10–4 M) were obtained for radial artery rings. Thereafter, rings were pretreated with tolazoline for 30 minutes and concentration-response curves for noradrenaline were reproduced in the presence of tolazoline. Tolazoline was applied at 4 x 10–6 M, corresponding to the concentration providing 50% of maximal relaxant response (EC50) in the isolated radial artery.

Statistical Analysis
The results are given as mean ± standard error of the mean. The contractile responses to vasoconstrictor agonists are expressed as absolute (g) contractions. The maximal relaxations (Emax) with tolazoline and SNP are expressed as percent decreases of spasmogen-induced precontractions. The sensitivities of radial arteries to tolazoline, SNP, and contractile agonists are expressed as the effective concentration that elicited 50% (EC50) of the maximal response (either relaxation or contraction) and calculated separately for each concentration-response curve by probit regression analysis. A computerized program was used for the curve-fitting. The EC50 values are given as -log M. In all experiments n is the number of patients from whom the vessels were obtained. Statistical analyses were performed by using the Student's unpaired t test and one way analysis of variance (ANOVA), where appropriate. A p value less than 0.05 was considered significant.

Drugs
Tolazoline and endothelin-1 were obtained from Aldrich Chemical (Milwaukee, WI) and Peninsula Labs (Belmont, CA), respectively. All other agents were obtained from Sigma Chemical Co (St. Louis, MO). A stock solution of noradrenaline was prepared in 0.001 N HCl, and ascorbic acid (1 mg/mL) was added to prevent oxidation. Other drugs were prepared in distilled water and diluted in Krebs solution.


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Notice From the American...
 References
 
Reactivity to Spasmogens
Noradrenaline, endothelin-1, U46619, and potassium chloride produced concentration-dependent contractions in radial artery rings (Fig 1). The maximal contractile forces induced by these spasmogens were comparable (Emax: noradrenaline, 10.08 ± 0.92 g; endothelin-1, 10.67 ± 2.12 g; U46619, 13.62 ± 2.10 g; potassium chloride, 11.29 ± 2.19 g, n = 6–9, p > 0.05), whereas vessels were more sensitive to endothelin-1 and U46619 than noradrenaline and potassium chloride (EC50: endothelin-1, 8.31 ± 0.21; U46619, 7.79 ± 0.12; p < 0.001 vs noradrenaline, 5.78 ± 0.15; and potassium chloride, 1.82 ± 0.09).



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  		Fig 1. Concentration-dependent contractile responses to spasmogens: endothelin-1 ({diamondsuit}), a thromboxane analogue, U46619 ({blacktriangleup}), noradrenaline ({blacksquare}), or potassium chloride (•) in human radial artery rings (n = 6–9).

 
Relaxations in Response to Tolazoline and SNP
Tolazoline produced concentration-dependent relaxations on isolated radial arteries contracted with noradrenaline (Fig 2). However, very weak relaxant responses were observed in rings precontracted with endothelin-1 (11.69 ± 5.65%, n = 9), U46619 (8.56 ± 4.1%, n = 6), and potassium chloride (6.39 ± 2.73%, n = 6). The precontraction forces elicited by spasmogenic agents were similar (noradrenaline, 6.15 ± 0.94 g; endothelin-1, 6.25 ± 0.72 g; U46619, 6.30 ± 0.29 g, potassium chloride, 6.03 ± 0.70 g; n = 6–9, p > 0.05). On the other hand, SNP resulted in complete relaxations of radial artery rings precontracted with either of the contractile agents (Fig 2). In noradrenaline contracted rings, the maximal relaxation and the sensitivity to tolazoline (Emax: 91.18 ± 5.11%; EC50: 5.40 ± 0.14, n = 9) were close to, but significantly lower than that of SNP (Emax: 121.92 ± 3.84%; EC50: 6.87 ± 0.09, n = 9, p < 0.001 vs tolazoline).



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  		Fig 2. Comparative relaxation responses to tolazoline ({blacksquare}) and sodium nitroprusside ({blacktriangleup}) in human radial artery rings precontracted submaximally by noradrenaline (A), endothelin-1 (B), a thromboxane analogue, U46619 (C), or potassium chloride (D) (n = 6–9).

 
Noradrenaline Contractions After Tolazoline Pretreatment
Noradrenaline resulted in concentration-dependent contractions of radial artery rings. Pretreatment of the artery rings with tolazoline (4 x 10–6 M) for a brief period significantly decreased the maximal contraction and the sensitivity to noradrenaline (pretreated rings: Emax: 8.88 ± 2.29 g; EC50: 4.91 ± 0.15, n = 4 vs control rings: Emax: 11.15 ± 2.14 g, p < 0.05; EC50: 5.39 ± 0.14, n = 4, p < 0.05). Whereas in parallel control experiments, two consecutive cumulative contractions to noradrenaline were similar (Fig 3).



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  		Fig 3. Cumulative contraction curves to half-log molar increased concentrations of noradrenaline in vehicle (A) ({blacksquare} = control; {blacktriangleup} = vehicle) and tolazoline (B) ({blacksquare} = control; • = tolazoline) pretreated human radial artery rings. Tolazoline was applied at 4 x 10–6 M for 30 minutes, n = 4. *p < 0.05 compared to control.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Notice From the American...
 References
 
The radial artery is increasingly being used in coronary revascularization since its revival over the last 10 years. Angiographic studies and randomized trials clearly demonstrated that it has an excellent long-term patency rate superior to the saphenous vein and similar to the IMA [16, 17]. This advancing profile ultimately proposes the radial artery as a second conduit of choice after the IMA as well as an alternative to the saphenous vein. Unfortunately, spasm of the radial artery during harvesting and early postoperative period is a well-known phenomenon. Its greater tendency to spasm than the IMA is probably related to its muscular nature [18] and high reactivity to vasospastic agents [6, 7, 19]. In contrast, endothelial and vascular relaxation properties of the radial artery were found comparable to the IMA [19, 20].

The relief of vasospasm by using an appropriate vasodilator is important for the maintenance of early as well as long-term patency of the radial artery graft. In addition, a prosperous opposition of graft spasm during preparation is recommended in order to prevent the genesis of additional spasms in the perioperative and postoperative periods [21]. Various vasodilators acting by different mechanisms have been introduced for the management of radial artery spasm. However, all have some limitations, such as slow onset [21] and short duration [22, 23] of action, development of tolerance [24], possibility of endothelial damage [23, 25], variation of efficacy depending on the timing of application [26], sensitization to vasoconstrictors [27], low efficiency [28, 29], and hypotension [29, 30]. Thus, current vasodilators might be unsatisfactory in some circumstances and it is reasonable to consider alternative agents for the reversal or prevention of this vasospasm.

Elevated circulating levels of endogenous vasoconstrictors, including catecholamines, possibly play a role in the spasm of the radial artery. In addition, the risk of spasm is further increased when a vasoconstrictor substance, particularly a sympathomimetic agent, is used for the restoration of normal blood pressure and myocardial perfusion in patients who became hypotensive after extensive grafting [8]. Previous in vitro studies demonstrated that the radial artery has dominant alpha-adrenergic receptor activity [5] and displays stronger reactivity preferentially to noradrenaline as well as other vasoconstrictors compared with the IMA [6, 7, 19]. Among them, endothelin-1, thromboxane A2, and noradrenaline are classified as type I vasoconstrictors with high potency and strong contractile effects on human arteries, even in the presence of an intact endothelium [31]. In the present study, we observed profound contractions in radial artery rings in response to these spasmogens, with a higher sensitivity to endothelin-1 and thromboxane analogue than noradrenaline.

Although mainly its greater wall thickness accounts for the high responsiveness to vasoconstrictors, the preparation of the radial artery as a free graft may also contribute to the tendency for vasospasm. Likewise, it has been reported that denervation increases the expression of alpha-adrenoceptors in grafted vessels [32]. Thus, catecholamines and sympathomimetics may play a precise role in the development of radial artery spasm. Recently, phenoxybenzamine, an irreversible alpha-adrenoceptor antagonist, was reported as an effective and long acting antispasmodic agent for the prevention of radial artery vasospasm mediated by alpha-adrenergic stimuli [33]. This agent was suggested to have advantages over currently used vasodilators, such as having no harmful effects on endothelium in contrast to papaverine even at a high concentration and after a long exposure period [23]. Besides, a brief pretreatment with phenoxybenzamine was found highly effective in preventing contractions in response to alpha-adrenergic agonists in the radial artery, unlike papaverine which failed to attenuate the constriction responses [34] or produced relatively short-lived protective effects than phenoxybenzamine [22, 35]. However, it is not known whether the prolonged inhibitory effect of phenoxybenzamine on vascular reactivity may cause a problem in the clinical setting either by producing a refractory state to supportive vasopressor treatment after operation or by enhancing contractile reactivity to other possible spasmogens.

There are several reports evaluating the prevention as well as the reversal of the contractile tone in the arterial grafts by commonly used vasodilators [26, 36, 37]. Previous in vitro studies demonstrated that vasodilators may have different effectiveness on the reactivity of an arterial graft depending on the timing of their exposure, either before or after the contractile stimulus. This has been documented for glyceryl trinitrate [37] and milrinone [26]. Both of these agents were found to be more effective in reversing an already established contraction than preventing the generation of a contraction. Although the preventive effect of phenoxybenzamine in radial artery spasm has been demonstrated, the efficacy of alpha-adrenergic antagonists in reversing an established contraction has not, to our knowledge, been reported so far.

In the present study we demonstrated that competitive alpha-adrenoceptor antagonist tolazoline is effective in reversing radial artery spasm induced by noradrenaline under in vitro conditions. Increasing concentrations of tolazoline almost fully overcame the contractions induced by noradrenaline in radial artery rings, however only weakly inhibited the contractions produced by other potential spasmogens namely, endothelin-1, thromboxane A2 analogue, U46619, and potassium chloride. Current findings reinforce previous results of phenoxybenzamine pretreatment. In that study, phenoxybenzamine prevented the contractions induced by alpha-adrenergic agonists but it failed to inhibit contractions in response to other vasoconstrictor agents [35]. Our results suggest that tolazoline can effectively reverse vasospasm mediated by alpha-adrenergic activity in the radial artery graft. On the other hand, SNP was found effective in reversing both receptor and depolarizing agent-mediated contractions. In fact, nitrovasodilators are known as effective agents in reversing radial artery spasm regardless of the nature of the constrictor stimulus [6, 24]. In our study, the maximal responsiveness and the sensitivity of the radial artery to SNP were found somewhat higher than to tolazoline.

Additionally, pretreatment of radial artery rings with tolazoline for a brief period significantly decreased the contractions to noradrenaline. In contrary with phenoxybenzamine, which fully depressed the responses to alpha-adrenoceptor agonists [23, 33, 34, 35], we found that tolazoline remarkably but incompletely inhibited the contractions induced by noradrenaline. This difference in efficacy pattern between tolazoline and phenoxybenzamine may be due to differences in receptor interaction and concentrations applied. In the present study, the duration of the inhibition of contractile response to noradrenaline was not assessed in tolazoline pretreated radial artery rings. Much shorter duration of action than that of phenoxybenzamine may be expected for tolazoline due to its different interaction profile with alpha-adrenoceptors, however this issue merits further investigation. It is suggested that prolonged inhibition of alpha-adrenoceptor mediated contraction by phenoxybenzamine may provide an advantage by extending the duration of protection against alpha-adrenergic stimuli to the early postoperative period [22, 35]. However, this may increase the risk for spasm by increasing the reactivity to other possible spasmogenic substances, in particular to angiotensin II, because of the cross talk between receptors [38]. Due to the sparsity of human tissue, pretreatment of radial arteries with SNP could not be assessed in this study. However, a recent study clearly demonstrated the significant attenuation of the contractile responses to alpha1-adrenoreceptor agonist phenylephrine in radial arteries pretreated with SNP [20].

Present findings suggest that tolazoline can be an effective vasodilator for the relief of radial artery spasm evoked by alpha-adrenoceptor activation. However, an additional relaxant agent seems to be needed in order to counteract the vasoconstriction initiated by other receptors in the graft. Our results and previous observations demonstrated that nitrovasodilators are highly effective agents in overcoming radial artery spasm induced by an extensive range of vasoconstrictors [20, 24, 28, 29]. The combined topical use of nitrovasodilators with calcium channel blockers has been established as the most appropriate strategy in overcoming radial artery vasospasm [21, 39]. Unlike nitrovasodilators, Ca++ channel blockers are not broadly effective and have limited effects in terms of preventing or reducing receptor-dependent contractions, including alpha-adrenoceptors, in the radial artery [28, 29]. Thus, in light of our findings, tolazoline may be introduced as an alternative local vasodilator to calcium channel blockers for use in combination with topical nitrovasodilators against radial artery vasospasm. In due time, this possibility needs to be exercised in clinical practice.

On the basis of the results of this in vitro study, tolazoline can be effective in the treatment as well as in the prevention of radial artery spasm evoked by alpha-adrenergic stimuli. Unlike SNP, tolazoline is not effective against all spasmogens evaluated. However, the use of selective receptor antagonists during the preparation of the radial artery is an encouraging and attractive strategy for the antispastic management of this graft. Notably, current results may provide evidence for the use of tolazoline as an effective topical antispasmodic agent during the preparation of the radial artery for grafting. Given the importance of increased sympathomimetic activity for the development of spasm, incorporation of alpha- adrenoceptor antagonist tolazoline into the vasodilator strategy may provide a novel therapeutic approach for the management of radial artery graft vasospasm.


   Notice From the American Board of Thoracic Surgery Regarding Trainees and Candidates for Certification Who Are Called to Military Service Related to the War on Terrorism
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 Notice From the American...
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The Board appreciates the concern of those who have received emergency calls to military service. They may be assured that the Board will exercise the same sympathetic consideration as was given to candidates in recognition of their special contributions to their country during the Vietnam conflict and the Persian Gulf conflict with regard to applications, examinations, and interruption of training. If you have any questions about how this might affect you, please call the Board office at (312) 202-5900.

Carolyn E. Reed, MD

Chair

The American Board of Thoracic Surgery


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Notice From the American...
 References
 

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S. Attaran, L. John, and A. El-Gamel
Clinical and Potential Use of Pharmacological Agents to Reduce Radial Artery Spasm in Coronary Artery Surgery
Ann. Thorac. Surg., April 1, 2008; 85(4): 1483 - 1489.
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