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Ann Thorac Surg 1996;61:610-614
© 1996 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Use of Verapamil and Nitroglycerin Solution in Preparation of Radial Artery for Coronary Grafting

Department of Surgery, University of Hong Kong at The Grantham Hospital, Aberdeen, Hong Kong

Accepted for publication September 20, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. The radial artery (RA) has been used as an alternative arterial graft for coronary artery bypass grafting. This artery has been reported to be spastic; therefore, use of spasmolytic drugs (vasodilators) during the preparation of the RA is recommended. The combination of calcium antagonists and nitroglycerin (verapamil plus nitroglycerin, VG solution) has been suggested to be effective in other bypass grafts. This study was designed to investigate (1) the effect of the VG solution during preparation of the RA for coronary artery bypass grafting and (2) whether the effect would last for a prolonged period after topical use.

Methods. Ring segments of the RA taken from coronary artery bypass grafting patients were studied in organ chambers at a physiologic pressure. The relaxation effect of VG (30 µmol/L verapamil and 30 µmol/L nitroglycerin, n = 5) or papaverine (30 µmol/L, n = 5) was recorded in K⁺ (25 mmol/L potassium chloride)-precontracted RA segments. Other segments taken from the RA were treated (n = 5) or not treated (n = 20, as the control) with the VG solution for 45 minutes before used for coronary artery bypass grafting. Both the VG-treated and nontreated segments were immersed in oxygenated Krebs solution and stored in a refrigerator at 4°C for 24 hours. The contraction force to 100 mmol/L K⁺ was compared between the two groups.

Results. The VG solution induced more rapid relaxation than papaverine (p < 0.05 from the first to the ninth minute). After 10 minutes, both solutions induced full relaxation. The contraction to K⁺ (100 mmol/L) in rings treated with VG solution for 45 minutes during operation was almost abolished 24 hours later (0.86 ± 0.1 g). In contrast, the control segments (n = 20) taken from nontreated RA contracted with K⁺ to high force (5.0 ± 0.6 g; p < 0.001).

Conclusions. The present study suggests that the combination of verapamil and nitroglycerin may provide a rapid onset, a complete relaxation, and a long-lasting vasorelaxant effect when used to prepare the RA for grafting. This study adds a new method to prevent RA spasm during coronary artery bypass grafting.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Various autologous arteries have been used as grafts for coronary artery bypass grafting (CABG) since the wide use of the internal mammary artery grafting has gained superior long-term results [1]. However, unlike other arterial grafts such as the gastroepiploic artery [2] and the inferior epigastric artery [3], which were used only after the mid-1980s, the radial artery (RA) was initially applied as a graft for CABG in 1971 [4]. This artery was soon abandoned because of the high incidence of vasospasm [5, 6] and low patency rates [5–7], which are reportedly related to its spastic characteristics [5, 6].

The RA was recently reproposed to be used as a graft for CABG [8]. Preliminary reports have shown that the vasospasm of the RA may be treated by pharmacologic agents such as papaverine and calcium antagonists [8]. With the application of papaverine during [8, 9] and of diltiazem during and after CABG [8], the RA may be used with acceptable results. However, there is a lack of studies on the RA with regard to the effect of vasodilators.

Calcium antagonists provide vasoconstrictor-selective vasodilatation in the human arterial grafts [10–12]. Therefore, we proposed a mixture vasodilator solution (the VG solution) for usage in the grafts [13, 14], which is composed of verapamil and nitroglycerin (NTG). This solution combines advantages of both calcium antagonists (highly selective to voltage-dependent calcium channels and long-lasting effect) and NTG (rapid onset and nonvasoconstrictor-selective effect [15]) and has been demonstrated to be useful for CABG [13, 14]. In addition, this solution is neutral, which may be advantageous in the protection of the endothelium of grafts over papaverine, which is acidic.

The present study was designed to investigate (1) the effect of the VG solution during preparation of the RA for CABG and (2) whether the effect would last for a prolonged period after topical use.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
General
Human RA segments were collected from patients undergoing CABG using this graft. Approval to use discarded RA tissue was given by the Institutional Review Board. After the arterial grafts were dissected, the required length was carefully measured. Any discarded segments of RA were immediately collected and placed into a container with oxygenated physiologic (Krebs) solution maintained at 4°C, and then transferred to laboratory. The vessels were placed in a glass dish and dissected out from their surrounding connective tissue. The arteries were cut into 3-mm-long rings and then suspended on wires in organ baths [16, 17]. The number of rings provided by each patient varied from two to six. The Krebs solution had the following composition (in mmol/L): Na⁺ 144, K⁺ 5.9, Ca²⁺ 2.5, Mg²⁺ 1.2, Cl^- 128.7, HCO₃^- 25, SO₄^2- 1.2, H₂PO₄^- 1.2, and glucose 11. The solution was aerated with a gas mixture of 95% O₂–5% CO₂ at 37 ± 0.1°C.

Organ Bath Technique
A specially designed organ bath technique was used for this study. This technique allows normalization of vascular rings to a physiologic pressure in vitro comparable to in vivo. The details of the technique were published previously [16–18]. Briefly, each arterial ring was stretched-up in progressive steps to determine the individual length–tension curve. A computer iterative fitting program (VESTAND 2.1; Yang-Hui He, Princeton University, Princeton, NJ) was used to determine the exponential line, pressure, and internal diameter. When the transmural pressure on the rings reached 100 mm Hg, determined from their own length–tension curves, the stretch-up procedure was stopped and the rings were released to 90% of their internal circumference at 100 mm Hg. This degree of the passive tension was then maintained throughout the experiment.

Because of the importance of endothelium on vascular tone, we intentionally preserved the endothelium by cautiously dissecting and mounting the rings. Previously, we found that this technique allowed the experiments to be carried out with an intact endothelium, as determined by the functional relaxation response to acetylcholine [19].

Protocol
EFFECTS OF VERAPAMIL AND NITROGLYCERIN SOLUTION IN COMPARISON WITH PAPAVERINE.
After the normalization procedure, the vascular rings were equilibrated for at least 1 hour. K⁺ (potassium chloride, 25 mmol/L) was added to the organ bath. After the contraction reached stable level, VG (30 µmol/L verapamil and 30 µmol/L NTG) or papaverine (30 µmol/L) was added. The relaxation–time course was recorded. The force during relaxation was measured at 1-minute intervals and expressed as percentage of the force during precontraction. The relaxation was compared between VG solution and papaverine.

EXAMINATION OF ACTING DURATION AFTER TREATMENT WITH VERAPAMIL AND NITROGLYCERIN SOLUTION.
To examine whether the effect of VG solution would last for prolonged period after topical use, some segments were taken from the RA that was immersed in the VG solution before being used for CABG. The VG treatment time was 45 minutes. Control segments were taken from the RA that was not treated with VG solution. Both the VG-treated and nontreated segments were immersed in oxygenated Krebs solution and stored in a refrigerator at 4°C for 24 hours. The reason to store these vessels at 4°C rather than 37°C is to keep the viability of the vessels. These segments were then cut into 3-mm rings and mounted in the organ bath. The aforementioned normalization procedure was applied and the contraction to K⁺ (100 mmol/L) was established.

The components of the VG solution are as follows [13, 14]: verapamil hydrochloride, 5 mg; NTG, 2.5 mg; heparin, 500 units; 8.4% NaHCO₃, 0.2 mL; and Ringer's solution, 300 mL.

This solution gives a concentration of about 30 µmol/L of verapamil or NTG in an isotonic solution at pH 7.4.

Data Analysis
The relaxation of the RA to VG solution and papaverine was expressed as percentage of precontraction (to 25 mmol/L K⁺). The K⁺ (100 mmol/L)-induced contraction force in the VG treated and nontreated rings was compared.

Unpaired Student's t test was used to compare the contraction force or the percentage relaxation. A p value of less than 0.05 was considered significant.

Drugs
Drugs used in this study and their resources were verapamil (Sigma, St. Louis, MO), nitroglycerin (SoloPak Laboratories, Franklin Park, IL), and papaverine (Eli Lilly & Co, Indianapolis, IN). Other chemicals were purchased from Sigma.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Thirty-five RA rings were studied. The diameter at a pressure of 100 mm Hg (D₁₀₀) was 2.7 ± 0.7 mm. The transmural pressure at 0.9D₁₀₀ (see Methods) was 66.1 ± 1.7 mm Hg. The resting force was 2.3 ± 0.2 g.

Comparison of Verapamil and Nitroglycerin Solution and Papaverine
The VG solution induced more rapid relaxation than papaverine (p < 0.05 from the first to the ninth minute, n = 5 in each group). Figure 1 shows the different onset of these two vasodilator solutions. After 10 minutes, however, there was no statistical difference between the rings treated with VG solution and those treated with papaverine with regard to the magnitude of the relaxation. In fact, both solutions induced full relaxation.

View larger version (14K): [in this window] [in a new window]   Fig 1. . Average relaxation response to verapamil (30 µmol/L) plus nitroglycerin (NTG) (30 µmol/L) in the human radial artery segments precontracted with potassium chloride (25 mmol/L). Average relaxation response to papaverine (30 µmol/L) was also compared. Symbols represent average data from five vessels. (a) Responses up to 85 minutes; (b) enlarged time scale for the first 15 minutes showing more rapid onset of the relaxation for the verapamil and nitroglycerin solution than papaverine.

View larger version (14K): [in this window] [in a new window]   Fig 2. . Comparison of contraction force to potassium chloride (100 mmol/L) in the human radial artery after being stored in oxygenated Krebs solution at 4°C for 24 hours between the artery treated with (VG-treated, n = 5) or without (control, n = 20) verapamil plus nitroglycerin (VG) for 45 minutes during operation. The vessels were then mounted in the organ bath at 37°C for the experiments. (*p < 0.001.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

Although the RA was first proposed to be used as a conduit for CABG in 1971 [4], the clinical application of this arterial graft has been eventful. This artery was soon abandoned as a graft because of a high incidence of narrowing or occlusion [6] that may be related to its spastic characteristics [5–7, 20] in accordance with clinical observations [5–7, 9, 20]. During dissection, the RA frequently develops detectable vasospasm so that pharmacologic agents (vasodilators) are required to relieve the spasm during operation. In our functional classification [21], the RA is a type III arterial graft that is more reactive to vasoconstrictors than somatic arteries located in the body wall (type I, such as the internal mammary artery and the inferior epigastric artery). Therefore, it is important to use vasodilators during the preparation of the RA.

The use of calcium antagonists during and after CABG with the RA has been suggested recently to be related to the better results for this arterial graft [8, 9]. The mechanism of vasorelaxant effects of calcium antagonists mainly involves the voltage-operated calcium channel (L-type calcium channel). This group of vasodilators selectively blocks the voltage-operated channel and inhibits calcium influx and therefore, is vasoconstrictor selective. These agents are more potent in inhibiting the depolarizing agent K⁺-induced vasoconstriction but less potent in inhibiting receptor-operated calcium channels [10]. The high vasoconstrictor selectivity of calcium antagonists is somewhat disadvantageous in the clinical use.

There have been many chemically diverse calcium antagonists used clinically. However, only diltiazem has been reported to have been applied for CABG using the RA [8]. The effect of three chemically different calcium antagonists [22]—dihydropyridine (nifedipine, for example), phenylalkylamines (such as verapamil), and benzothiazepines (such as diltiazem)—has been compared in the coronary artery and coronary bypass grafts [10, 16]. Among the three calcium antagonists (nifedipine, verapamil, and diltiazem), diltiazem is the least potent. For example, nifedipine is 15-fold more potent than diltiazem with regard to the vasorelaxant effect in the most commonly used human arterial coronary bypass graft—the internal mammary artery, as demonstrated in our previous study [10]. Verapamil is more potent than diltiazem in the canine internal mammary artery (EC₅₀,Au: spell out EC50 -5.73 versus -5.38 log M) and saphenous vein (-6.74 versus -6.30 log M) [16]. We have also found that in the human saphenous vein [13] diltiazem is significantly less potent than verapamil (EC₅₀, -6.62 versus -6.96 log mol/L). Taken together with the consideration of the complexity of the nature of the vasoconstriction [23] and the use of vasodilators [24] in arterial grafts, it is logical to test other calcium antagonists for use in the RA as a bypass graft.

In general, the advantages for calcium antagonists are (1) high potency to inhibit the voltage-operated calcium channel (L-type calcium channel), which is the primary mechanism for regulation of intracellular calcium concentration of vascular smooth muscle [25] and (2) long duration. The disadvantages, on the other hand, are (1) that high vasoconstrictor selectivity may limit their effect under some circumstances when a vessel is contracted through receptor mechanisms and (2) that relatively (compared to NTG) slower onset of the action, although the onset is more rapid than papaverine [16]. As demonstrated in the human internal mammary artery, a combination of calcium antagonists with NTG may combine the advantages of both.

The present study demonstrates such advantages for the combined vasodilator solution used for the human RA. Our experiments show that VG solution has a more rapid onset compared with papaverine. The relaxation is complete. Although we could only test depolarizing mechanism due to the sparsity of the RA tissue, as aforementioned, L-type calcium channel (related to the depolarizing mechanism) is the primary mechanism for vascular smooth muscle contraction. In addition, 24 hours later the RA was still in a plegic status with almost complete abolishment of the contraction to the depolarizing agent K⁺. In contrast, after the same period, in the control RA, a strong contraction still existed.

The advantages of using VG solution over papaverine in the RA involve (1) more rapid onset and (2) neutral pH. Our experiments have shown a more rapid relaxation induced by the VG solution than papaverine within the first 10 minutes. Perhaps more important, VG solution is neutral (pH 7.4), whereas papaverine is acidic as measured by us (in the Ringer's solution, pH 4.4 at 2.5 mmol/L and pH 4.8 at 30 µmol/L [14]). Acidic solution has been shown to damage the endothelium [26]. This may be particularly important in the preparation of the RA because the vasodilator solution contacts the endothelium of the RA when the artery, as a free graft, is immersed in the solution before grafting. The long-term patency of a graft may be related to the preservation of the endothelium.

The present study also demonstrates that after 45 minutes of treatment with the VG solution, the vasorelaxant effect lasts for a prolonged period (ie, at 4°C the effect would last for at least 24 hours). In fact, in our experiment, even after 24 hours the vessel was still inactive in response to the vasoconstrictor K⁺. We realize that the 24-hour storage at 4°C is different from the clinical setting, in which the vascular graft is subject to 37°C and blood flow through the lumen. Under the experimental setting, the cold storage is necessary to keep the vessel biologically active as demonstrated in the control vessels. If the effect of VG solution lasts for more than 24 hours at 4°C, as demonstrated in our experiments, it is logical to speculate that at the body temperature it would last for at least a few hours. This is a critical period for the recovery of the patient as graft spasm normally develops in early postoperative period.

In this study, we cannot comment on the intravenous administration of diltiazem during and after operation as proposed by others [8]. In fact, the VG solution has been applied in our preliminary experience for the preparation of the RA in combination with intravenous administration of diltiazem and none of the patients had spasm of the RA perioperatively. Using the VG solution to prepare the RA during operation, the RA graft is completely relaxed before grafting. Our study has opened the discussion with regard to (1) the use of alternative vasodilators to overcome spasm of the RA during CABG and (2) the possibility that if the topical use of the VG solution during operation may effectively cover early postoperative period the systemic administration of vasodilators may be applied in reduced dosages or even unnecessary. However, further studies are required to clarify this.

In conclusion, the present study suggests that the combination of verapamil and NTG may provide a rapid onset, a complete relaxation, and a long-lasting vasorelaxant effect when used to prepare the RA for grafting. This study adds a new method to prevent RA spasm during CABG.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
This study was supported by Committee of Research and Conference Grant 337/048/0018 and Vice-Chancellor Grant 350/172/0/9, The University of Hong Kong.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Address reprint requests to Prof He, Division of Cardiothoracic Surgery, University of Hong Kong at The Grantham Hospital, 125 Wong Chuk Hang Rd, Aberdeen, Hong Kong.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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				G.-W. He and C.-Q. Yang Vasorelaxant effect of phosphodiesterase-inhibitor milrinone in the human radial artery used as coronary bypass graft J. Thorac. Cardiovasc. Surg., May 1, 2000; 119(5): 1039 - 1045. [Abstract] [Full Text]

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				G.-W. He and C.-Q. Yang COMPARATIVE STUDY ON CALCIUM CHANNEL ANTAGONISTS IN THE HUMAN RADIAL ARTERY: CLINICAL IMPLICATIONS J. Thorac. Cardiovasc. Surg., January 1, 2000; 119(1): 94 - 100. [Abstract] [Full Text] [PDF]

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				D. G. Cable, J. A. Caccitolo, E. A. Pfeifer, R. C. Daly, J. A. Dearani, C. J. Mullany, T. O'Brien, T. A. Orszulak, and H. V. Schaff Endothelial regulation of vascular contraction in radial and internal mammary arteries Ann. Thorac. Surg., April 1, 1999; 67(4): 1083 - 1090. [Abstract] [Full Text] [PDF]

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				G.-W. He Verapamil plus nitroglycerin solution maximally preserves endothelial function of the radial artery: Comparison with papaverine solution J. Thorac. Cardiovasc. Surg., June 1, 1998; 115(6): 1321 - 1325. [Abstract] [Full Text] [PDF]

				G.-W. He and C.-Q. Yang Characteristics of adrenoceptors in the human radial artery: Clinical implications J. Thorac. Cardiovasc. Surg., May 1, 1998; 115(5): 1136 - 1140. [Abstract] [Full Text] [PDF]

				G.-W. He and C.-Q. Yang Radial Artery Has Higher Receptor-Mediated Contractility but Similar Endothelial Function Compared With Mammary Artery Ann. Thorac. Surg., May 1, 1997; 63(5): 1346 - 1352. [Abstract] [Full Text]

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