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J Thorac Cardiovasc Surg 1999;117:906-911
© 1999 Mosby, Inc.

SURGERY FOR ADULT CARDIOVASCULAR DISEASE

NITROGLYCERIN IS SUPERIOR TO DILTIAZEM AS A CORONARY BYPASS CONDUIT VASODILATOR

Oz M. Shapira, MDa, Aiming Xu, PhDb, Joseph A. Vita, MDb, Gabriel S. Aldea, MDa, Nirav Shah, MDb, Richard J. Shemin, MDa, John F. Keaney, Jr, MDb

From the Department of Cardiothoracic Surgerya and Evans Department of Medicine,b Boston University School of Medicine, Boston, Mass.

This work was supported by grants from the American Heart Association, National Center (J.F.K), and the National Institute of Health (HL53398 and HL55993 to J.A.V. and HL59346 to J.F.K). J.A.V. is an Established Investigator of the American Heart Association, and J.F.K. is the recipient of a Clinical Investigator Development Award (HL03195) from the National Institutes of Health.

Received for publication July 28, 1998. Revisions requested Nov 5, 1998. Revisions received Jan 11, 1999. Accepted for publication Jan 12, 1999. Address for reprints: Oz M. Shapira, MD, Department of Cardiothoracic Surgery, Boston Medical Center, 88 E Newton St, Boston, MA 02118.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Background: Recent reports of improved radial artery patency have been attributed, in part, to routine use of diltiazem to prevent vasospasm. However, diltiazem is costly, and its use may be associated with negative inotropic and chronotropic side effects. This study compares the vasodilatory properties of diltiazem to those of nitroglycerin.
Methods: In vitro, with the use of organ chambers, the vasodilatory properties of diltiazem and nitroglycerin were compared in matched segments of radial artery, internal thoracic artery, and saphenous vein that were harvested from the same patients (n = 11). The vasodilatory response of the radial artery to intravenous diltiazem or nitroglycerin was compared in vivo (n = 10) with the use of ultrasonographic measurements of radial artery diameter.
Results: The maximum relaxation of radial artery (100% ± 4%), internal thoracic artery (96% ± 4%), and saphenous vein (100% ± 3%) to nitroglycerin were significantly greater than the response to diltiazem (33% ± 6%, 22% ± 7%, and 34% ± 5%, respectively; P < .001). The thromboxane mimetic, U46619, induced radial artery spasm with a median effective concentration of 3.7 ± 0.8 nmol/L. Physiologic concentrations of nitroglycerin (0.1 µmol/L) significantly inhibited the radial artery response to U46619 (median effective concentration, 6.2 ± 1.1 nmol/L; P = .046), whereas diltiazem (1 µmol/L) did not (median effective concentration, 3.7 ± 0.8 nmol/L; P = .64). In vivo, nitroglycerin increased radial artery diameter 22% ± 3%, which was significantly greater than diltiazem (3% ± 0.5%; P = .001).
Conclusion: Nitroglycerin is a superior conduit vasodilator and is more effective in preventing graft spasm than diltiazem. Nitroglycerin should be strongly considered as the drug of choice to prevent conduit spasm after coronary bypass grafting.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
The superior long-term patency rate of internal thoracic artery compared with saphenous vein for coronary artery bypass grafting (CABG) is well documented.Go 1 Improved patency rates have been shown to translate into improved long-term survival and cardiac event-free survival.Go 1 More recently the use of 2 internal thoracic grafts, particularly when used for 2 left-sided coronary arteries, further improves long-term results compared with use of a single internal thoracic artery.Go 2 These observations triggered the usage of multiple arterial conduits for CABG.Go 3

The radial artery was first introduced as an alternative arterial conduit in the early 1970s,Go 4 only to be abandoned shortly thereafter because of early graft failure related to accelerated intimal hyperplasia and vasospasm.Go 5 The use of the radial artery was recently rejuvenated with encouraging early results attributed to modifications in harvesting techniques and routine prolonged administration of antispasmodic agents, of which diltiazem is the most frequently used.Go Go 6-8 However, diltiazem is costly, and its use may be associated with negative inotropic and chronotropic side effects.Go 9 For example, we have shown that up to 40% of patients receiving diltiazem therapy require temporary cardiac pacing in the perioperative period, resulting in a longer intensive care unit stay.Go 10 In contrast, Gurevitch and colleaguesGo 11 have used long-acting nitrates as an alternative to diltiazem for prevention of composite arterial conduit spasm and reported satisfactory clinical results.

This study was designed to compare the vasodilatory and antispasmodic properties of diltiazem to those of nitroglycerin. In vitro response was assessed with the use of organ-chamber methods, and in vivo response was assessed by the use of ultrasonographic measurement of radial artery vasodilation in patients with known coronary artery disease.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Patients
For the in vitro studies, matched segments of radial artery, internal thoracic artery, and saphenous vein that would otherwise be discarded were obtained from patients (n = 11) undergoing CABG at Boston Medical Center. Subjects were included in this study only if segments of all 3 conduits could be obtained. The study was approved by the Boston Medical Center Institutional Review Board. The vessels were harvested with the accompanying fat pedicle and placed in ice-cold physiologic salt solution (PSS) and prepared immediately for studies of vascular function. For the in vivo studies, subjects (n = 10) with angiographically documented coronary artery disease (at least one stenosis of more than 50%) were recruited for assessment of nitroglycerin- and diltiazem-induced dilation of the radial artery.

Materials
The PSS contained the following elements: NaCl, 118.3 mmol/L; KCl, 4.7 mmol/L; CaCl2, 2.5 mmol/L; MgSO4, 1.2 mmol/L; KH2PO4, 1.2 mmol/L; NaHCO3, 25 mmol/L; glucose, 11.1 mmol/L; Na2EDTA, 0.026 mmol/L; and indomethacin, 0.01 mmol/L. Nitroglycerin was obtained from Baxter Healthcare Corp (Deerfield, Ill). Diltiazem and U46619 were purchased from Sigma Chemical Co (St Louis, Mo).

Organ chamber methodology
The vessels were carefully dissected from their surrounding fat tissue and cut into 2 to 3 rings measuring 4 mm. The rings were placed in organ chambers (37°C) containing 10 mL PSS, suspended between 2 tungsten stirrups for the measurement of isometric tension as described,Go 12 and constantly aerated with 95% oxygen/5% carbon dioxide. Each vessel was then progressively stretched in 1-g increments to its optimal resting tension that produced a maximal response to 80 mEq of KCl. Vessels were then allowed to equilibrate for 1 hour before the introduction of vasoactive drugs as described.Go 13 Relaxation studies were performed after vessels were contracted with 0.1 to 1 µmol/L of U46619, such that contraction was 50% to 60% of the maximal KCl-induced contraction. Vessel segments were then exposed to increasing doses of nitroglycerin or diltiazem (10–9–10–5 mol/L), and dose-response curves were recorded. The ability to prevent radial artery spasm was assessed by dose-response curves to U46619 in baths containing PSS alone (control) or physiologic concentrations of nitroglycerin (0.1 µmol/L)Go 14 or diltiazem (1 µmol/L).Go 9

In vivo radial artery vasodilatory studies
The study was approved by the Boston Medical Center Institutional Review Board. Subjects were fasted overnight, calcium channel blockers were withheld for 48 hours before the study, and all other vasoactive medications were withheld for 24 hours. If applicable, patients were asked not to smoke overnight before the study. On the day of the study, images of the radial artery diameter 5 to 10 cm distal to the antecubital crease were recorded with an ultrasound system (Toshiba 140a; Toshiba, American Medical Systems, Tustin, Calif ) equipped with a 7.5 MHz linear array transducer. The transducer position was marked and used for subsequent scans. Serial 10-minute infusions of intravenous nitroglycerin (0.06–0.36 µmol/min) were then given into the contralateral arm vein with an infusion pump (Baxter Healthcare Corp, Irvine, Calif). At the end of each infusion, repeat ultrasound images of the radial artery were recorded. After a 2-hour period, the radial artery diameter was recorded, and patients were given a 0.25-mg/kg bolus of diltiazem over 2 minutes, followed by serial 20-minute diltiazem infusions (0.12-0.36 µmol/min). Radial artery diameter was determined with the use of customized image analysis softwareGo 15by personnel blinded to infused medication and image sequence.

Data analysis
Unless otherwise specified, all data are expressed as mean ± SEM. Vessel relaxation is expressed as percent reduction in tension induced by U46619. The median effective dose (EC50) represents the drug concentration producing 50% of maximum relaxation/contraction determined graphically by commercially available software (Origin; Microcal Inc, Northhampton, Mass). In vitro and in vivo dose-response curves for nitroglycerin, diltiazem, and U46619 were compared among the groups using 2-way analysis of variance (ANOVA) for repeated measures.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Study subjects
Vessel segments for the in vitro organ-chamber studies were obtained from 11 patients undergoing CABG. There were 9 men and 2 women, with a mean age of 56 ± 8 years (range, 39 to 64 years). No patient received intravenous nitroglycerin before the operation. A comparable group of 10 subjects were enrolled in the in vivo ultrasound studies. They were all men, with a mean age of 61 ± 7 years. The clinical profile of all the study subjects is depicted in Table I.


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  		Table I. Clinical profile of the study patients
 
In vitro vascular relaxation.
To determine the relative vasodilatory properties of diltiazem and nitroglycerin, matched segments of radial artery, internal thoracic artery, and saphenous vein were precontracted with U46619 and exposed to increasing doses of nitroglycerin or diltiazem in organ chambers. The maximum relaxation of the radial artery (100% ± 4%), internal thoracic artery (96% ± 4%), and saphenous vein (100% ± 3%) to nitroglycerin were each significantly greater than the response to diltiazem (33% ± 6%, 22% ± 7%, and 34% ± 5%, respectively; P < .001; Fig. 1).



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  		Fig. 1. Effect of nitroglycerin and diltiazem on radial artery (A), internal thoracic artery (B), and saphenous vein (C). Segments of radial artery, internal thoracic artery, and saphenous vein obtained from the same patients and contracted with 0.1 to 1 µmol/L U46619. Relaxation was recorded in response to the indicated doses of nitroglycerin and diltiazem as described in the text. Data are expressed as mean ± SEM and represent complete vessel sets derived from 11 patients. *P < .001.

 
In vitro prevention of radial artery spasm
To determine the antispasmodic properties of diltiazem and nitroglycerin, radial artery segments were placed in organ chambers containing PSS alone (control) or with physiologic concentrations of nitroglycerin or diltiazem and exposed to increasing doses U46619. The thromboxane mimetic, U46619, increased radial artery tone with an EC50 of 3.7 ± 0.8 nmol/L. Physiologic concentrations of nitroglycerin (0.1 µmol/L) significantly inhibited the radial artery response to U46619 (EC50, 6.2 ± 1.1; P = .046), whereas diltiazem (1 µmol/L) did not (EC50, 3.7 ± 0.8 nmol/L; P = .64; Fig. 2). These data suggest that nitroglycerin is not only a more potent vasodilator but that it is also more effective in preventing radial artery spasm than is diltiazem.



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  		Fig. 2. Prevention of radial artery vasospasm. A, Radial artery segments were exposed to the indicated concentrations of U46619 in organ chambers containing PSS alone ({circ}), 0.1 µmol/L nitroglycerin ({blacktriangleup}), or 1 µmol/L diltiazem ({triangledown}). Response to a maximal dose of U46619 was similar for all. B, However, the EC50 of the vasoconstrictor response to U46619 was significantly higher for nitroglycerin. Data are expressed as mean ± SEM and represent data obtained from 6 patients. *P = .046 versus control.

 
In vivo radial vasodilation
Because isolated vessels may not completely reflect events in vivo, the radial artery vasodilatory response to intravenous nitroglycerin or diltiazem was compared in vivo with the use of ultrasonographic measurements of radial artery diameter in subjects with documented coronary artery disease. Intravenous nitroglycerin produced dose-dependent radial artery vasodilation (P = .001), although intravenous diltiazem had no vasodilatory effect (P = .59; Fig. 3, A). Maximum increase in radial artery diameter in response to nitroglycerin (22% ± 3%) was much greater than to diltiazem (3% ± 0.5%; P = .001). Intravenous nitroglycerin (P = .001) and intravenous diltiazem (P = .001) both produced a dose-dependent fall in mean blood pressure (Fig. 3, GoB). The fall in blood pressure was significantly greater in response to nitroglycerin than in response to diltiazem (P = .03, by repeated-measurements ANOVA). The radial artery vasodilatory response to nitroglycerin and diltiazem in a representative subject is depicted in Fig. 4.



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  		Fig. 3. Effect of intravenous nitroglycerin and diltiazem on radial artery vasodilation and blood pressure (BP). Diltiazem () or nitroglycerin ({square}) was given intravenously at the indicated rates in 10 subjects. Vasodilation (A) and blood pressure (B) were recorded as described in the text. *P = .001 for dose-response by one-way repeated measures ANOVA. {dagger}P = .03 vs diltiazem by two-way ANOVA.

 


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  		Fig. 4. Representative two-dimensional ultrasound images of the radial artery in a volunteer subject exposed to intravenous infusion of nitroglycerin and diltiazem. A 31% increase in radial artery diameter is observed after nitroglycerin infusion (upper panels), whereas diltiazem had no measurable effect (lower panels).

 
The order of intravenous vasodilator administration in this study was not randomized because of the relatively long duration of diltiazem action. Even though radial artery diameter and systemic blood pressure returned to baseline between infusions, it is conceivable that the lack of radial artery dilation to diltiazem reflected some effect of the earlier nitroglycerin infusion. To address this concern, 6 patients returned for a repeat study of the response to diltiazem without previous nitroglycerin exposure. Diltiazem had no significant effect in these subjects, with a change in radial artery diameter of 0.7% ± 1.2%, 0.5% ± 2.1%, and –0.1% ± 1.3% in response to diltiazem infusions of 0.12, 0.24, and 0.36 µmol/min, respectively (P = .86, by repeated-measures ANOVA).


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
The use of the radial artery for coronary revascularization has been recently rejuvenated with improved early and midterm clinical results.Go Go 6-8 However, the radial artery propensity for vasospasm documented both clinically,Go Go Go Go 5,6,16-20 and in studies of isolated arterial segments with the use of organ-chamber methods,Go Go 21,22 is still worrisome. Chardigny and colleaguesGo 21 have shown that radial artery and gastroepiploic artery have greater contractile response to norepinephrine and serotonin compared with the internal thoracic artery. He and YangGo 22 reported that both endothelin I and angiotensin II induced significantly higher contraction force in the radial artery than in the internal thoracic artery. Most authors emphasize the necessity for pharmacologic intervention to prevent vasospasm when these conduits are used.Go Go Go Go Go 6-8,10,16-22 However, the drug of choice to prevent vasospasm is still a matter of controversy.

The calcium channel blocker diltiazem has been empirically selected by most surgeons.Go Go Go Go Go 6-8,10,16-19 However, diltiazem is costly and its use may be associated with negative inotropic and chronotropic side-effects.Go 9 Up to 30% to 40% of patients undergoing CABG and treated with diltiazem may experience hypotension, bradycardia, or heart block requiring lowering the dose, discontinuing the drug, or temporary pacing.Go Go 7,10 Moreover, use of diltiazem does not completely eliminate spasm. In early and midterm angiographic studies radial artery spasm was identified in 1% to 9.7% of cases.Go Go Go 6,16-20 Recently, Cable and colleaguesGo 23 demonstrated that diltiazem and verapamil had little effect on radial artery receptor-dependent and receptor-independent contraction, whereas nifedipine and nitroglycerin were much more effective. In another study,Go 24 the authors demonstrated that the use of verapamil and nitroglycerin solution to prepare radial artery grafts maximally preserves endothelial function. A systematic comparison of diltiazem to nitroglycerin has not been previously performed. With this information in mind, we sought to compare the vasodilatory response of the most commonly used coronary bypass conduits to nitroglycerin to that of diltiazem.

The data presented in this study demonstrate that the in vitro maximum relaxation of all 3 coronary bypass conduits to nitroglycerin is significantly greater than the response of these conduits to the calcium channel blocker diltiazem. We found diltiazem to be ineffective in vessels precontracted with U46619. Similar results were reported in radial arteries precontracted with potassium chloride or norepinephrine.Go 23 In our study, these in vitro observations were also found to be valid in vivo. Intravenous administration of nitroglycerin in patients with documented coronary artery disease induced significantly greater increase in radial artery diameter compared with diltiazem. Finally, within the therapeutic dose range, nitroglycerin was found to be much more effective in preventing U46619-induced radial artery spasm than was diltiazem. In accordance with our findings, Canver and colleaguesGo 25 have recently used ultrasonography and Doppler studies to document strong vasodilatory responses to oral nitroglycerin of both in situ and grafted internal thoracic arteries.

The clinical experience with the use of nitrates for the specific indication of prevention of arterial conduit spasm is limited, with only one published report.Go 11 Gurevitch and colleaguesGo 11 have used high-dose isosorbide dinitrate in patients undergoing myocardial revascularization with composite arterial grafts. They reported hospital mortality rates of 2.6%, postoperative hypoperfusion syndrome in 2.6% of patients, and a postoperative myocardial infarction rate of 1.3%. At a mean follow-up of 24 months, all hospital survivors were alive, with 97% being angina-free; 97% of the angiographically studied anastomoses were patent.Go 11

A major potential limitation of the use of nitrates is the development of tolerance.Go 26 The cause of tolerance is unclear and is a subject of intense investigation.Go 27 It is not related to altered pharmacokinetics, because drug plasma levels remain the same or even higher after prolonged use compared with the initial therapy.Go 28 Although there can be no doubt that loss of hemodynamic effects is a true phenomenon, it is also clear that some vascular effects of nitrate therapy persist during continued therapy and that cessation of treatment may be associated with withdrawal symptoms.Go 26 Similar to the variability of different vessel responses to nitroglycerin,Go Go 29,30 there are differences in the susceptibility of veins, arteries, and arterioles to develop nitrate tolerance and that arterial or arteriolar response may persist although venous tolerance exists.Go 30 To eliminate the tolerance effect as a confounding factor in the present study, none of the patients from whom vascular tissues were obtained for organ-chamber studies received intravenous nitroglycerin treatment, and oral nitroglycerin medications were withheld for 48 hours in subjects recruited for the in vivo studies. Undoubtedly, the mechanism and the clinical implications of tolerance in this treatment setting need to be further explored.

In conclusion, in this study nitroglycerin was found to be a superior arterial vasodilator and more effective in preventing radial artery spasm than diltiazem. Although a prospective randomized study comparing these agents clinically is clearly indicated, the data presented here strongly suggest that nitroglycerin should be considered as the drug of choice to prevent arterial conduit spasm after CABG.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

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  12. Keaney JF Jr, Xu A, Cunningham D, Jackson T, Frei B, Vita JA. Dietary probucol preserves endothelial function in cholesterol-fed rabbits by limiting vascular oxidative stress and superoxide generation. J Clin Invest 1995;95:2520-9.
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