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Ann Thorac Surg 1997;63:1346-1352
© 1997 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Radial Artery Has Higher Receptor-Mediated Contractility but Similar Endothelial Function Compared With Mammary Artery

Division of Cardiothoracic Surgery, Department of Surgery, University of Hong Kong, Grantham Hospital, Aberdeen, Hong Kong, and Albert Starr Academic Center for Cardiac Surgery, St. Vincent Hospital, Portland, Oregon

Accepted for publication December 4, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
Background. The radial artery (RA) has been used as an alternative arterial graft for coronary artery bypass grafting, but this artery has been suggested to be spastic. Endothelin-1 (ET) and angiotensin II (AII) have been measured with increased plasma concentrations during cardiopulmonary bypass. However, whether RA is reactive to these two important receptor-mediated vasoconstrictors is unknown. Also unknown is the endothelial function of this arterial conduit. This study was designed to compare RA and the internal mammary artery regarding the contractile characteristics to ET-1 and AII and endothelial function.

Methods. Ring segments of the RA and internal mammary artery taken from patients undergoing coronary artery bypass grafting were studied in organ chambers at a physiologic pressure. The contractility was determined from the contraction induced by ET-1 and AII as contraction force and the force normalized by circumference (g/mm). The endothelium-dependent relaxation was induced by the calcium ionophore A23187, a nonreceptor agonist, and substance P, a receptor agonist for endothelium-derived relaxing factors. Nitroglycerin was used to study the endothelium-independent relaxation.

Results. Both ET-1 and AII induced a higher contraction force (9.0 ± 0.9 g, n = 12, versus 4.5 ± 0.4 g, n = 38, p < 0.0001 for ET and 6.5 ± 1.9 g, n = 7, versus 1.7 ± 0.3 g, n = 8, p = 0.015 for AII) and normalized force (0.95 ± 0.1 g/mm versus 0.66 ± 0.05 g/mm, p = 0.007 for ET-1 and 0.8 ± 0.2 g/mm versus 0.2 ± 0.05 g/mm, p < 0.01 for AII) in RA than in the internal mammary artery. There were no significant differences detected between these arteries with regard to either endothelium-dependent (to substance P and A23187) or endothelium-independent (to nitroglycerin) relaxation (p > 0.05).

Conclusions. We conclude that the human RA has a higher receptor-mediated contractility (to ET-1 and AII) but similar endothelial function compared to the internal mammary artery. The study reveals the nature of the more spastic characteristics of the RA, supports the necessity of a more active pharmacologic intervention to relieve spasm in the RA, and suggests that the similar endothelium-derived relaxing factor-mediated endothelial function of the RA compared with the internal mammary artery may be the basis for a satisfactory long-term patency.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
Various autologous arteries have been used as grafts for coronary artery bypass grafting. Because of the superior long-term results of the internal mammary artery (IMA) grafting [1], this graft has been used most frequently. In comparison with rather recently used arterial grafts such as gastroepiploic artery [2] and inferior epigastric artery [3], the radial artery (RA) was initially applied as a graft for coronary artery bypass grafting in 1971 [4]. However, it was soon abandoned because of reported high incidence of vasospasm and low patency rates [5]. With increased knowledge of spastic characteristics of this artery and of how to overcome the spasm using pharmacologic agents, this arterial graft is now again used [6]. However, despite large number of studies on biological characteristics of other arterial grafts such as IMA [7–14], gastroepiploic artery [15], and inferior epigastric artery [16], little has been known about the characteristics of RA [17].

Biological characteristics of blood vessels include structure and function of endothelium and smooth muscle. Although it is still unclear what characteristics influence long-term patency, those factors may be related to (1) ability of the endothelium to release vasodilator and antiplatelet aggregation substances such as endothelium-derived nitric oxide and (2) spastic characteristics. However, the endothelial function with regard to the ability to release endothelium-derived nitric oxide and the smooth muscle function with regard to relaxant characteristics have not been well understood. The present study was designed to investigate vasoconstriction in the RA in response to the important vasoconstrictors endothelin-1 (ET-1) and angiotensin II (AII) and to compare them with those of the well-studied arterial graft-IMA.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
General
Human RA segments were collected from patients undergoing coronary artery bypass grafting using these grafts. In most of these patients, the operation was performed by Dr He. Approval to use discarded RA and IMA tissue was given by the Human Ethics Committee of the Grantham Hospital and the Institutional Review Board of the St. Vincent Hospital. After the arterial grafts were dissected, the required length was carefully measured. Any discarded segments of RA or IMA 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 [18]. 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

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
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 before [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, NJ) was used to determine the exponential line, pressure, and the 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 [8].

	Protocol

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
The sample of the RA and IMA used in this study was taken randomly from patients without regard to the preoperative drug therapy.

CONTRACTION.
After the normalization procedure, the vascular rings were equilibrated at least for 1 hour. K⁺ (100 mmol/L potassium chloride) was added to the organ bath and the contraction force was recorded. The ring was frequently washed to restore the baseline. Cumulative concentration–contraction curves were constructed in RA and IMA ring segments to endothelin-1 (ET-1) or angiotensin II (AII). The contraction was expressed three ways: (1) The first was contraction force (g). (2) The second expression was contraction force normalized by the circumference: Fn (normalized force) = Force (g)/C₁₀₀ (mm), where C₁₀₀ is the circumference at a pressure of 100 mm Hg and C₁₀₀ = x D₁₀₀ [11, 12]. This normalization procedure of the contraction force by using Fn between arteries with different diameters gives the force produced by 1 mm of circumference of the vessel. (3) The third expression was percentage of the contraction force induced by 100 mmol/L K⁺.

RELAXATION.
In this study, both the endothelium-dependent and endothelium-independent relaxation were compared in the RA and IMA. The relaxation was expressed as percentage relaxation of the precontraction induced by U46619 (10 nmol/L). The dose of U46619 was chosen because this concentration produced submaximal contraction (50% to 80%) determined from the logistic curve-fitting equation from previous studies for the IMA [7, 11–13, 16, 18] and from our pilot experiments for RA, which is also in accordance with a study by others [17].

The receptor-mediated endothelium-dependent relaxation was induced by substance P-a receptor-mediated endothelium-derived nitric oxide agonist. The nonreceptor-mediated endothelium-dependent relaxation was induced by calcium ionophore A23187 (calcimycin), a nonreceptor-mediated endothelium-derived nitric oxide agonist.

The endothelium-independent relaxation was induced by nitroglycerin.

	Data Analysis

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
The reactivity of RA and IMA was expressed as maximal contraction (or relaxation) and sensitivity. The sensitivity of the RA and IMA to vasoconstrictor (ET-1 and AII) or vasodilator (substance P, A23187, or nitroglycerin) agents is expressed by the effective concentration that induced 50% of the maximal effect (either contraction or relaxation). This is defined as EC₅₀. The EC₅₀ was calculated by a logistic, curve-fitting equation E = MA^p/(A^p + K^p) where E is response, M is maximum response, A is concentration, K is EC₅₀ concentration, and p is the slope parameter [18]. A computerized program was used for the curve fitting. From this fitted equation, the mean EC₅₀ value ± standard error of the mean was calculated in each group.

Two-way analysis of variance and unpaired Student's t test (two-tailed) was used to compare the contraction force or percentage relaxation for each vasoconstrictor, vasodilator, and the EC₅₀s between the RA and IMA. A p value less than 0.05 was considered significant.

"Reactivity" describes the range of response and is measured as the maximum contraction (contractility) to the vasoconstrictor substance or the maximum relaxation to the vasodilator substance as a percentage of the precontracted force [18]. "Sensitivity" is used throughout this article to describe the location of the concentration-response curve and is measured by the fitted EC₅₀ value [18].

	Drugs

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
Drugs used in this study and their resources were substance P, A23187, angiotensin II (Sigma, St. Louis, MO); U46619 (Cayman Chemical, Ann Arbor, MI); endothelin-1 (Peptides International, Louisville, KY); and nitroglycerin (SoloPak Laboratories, Franklin Park, IL). Stock solutions of endothelin-1, angiotensin II, and U46619 were held frozen until required.

	Results

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
Sixty-two RA rings and 107 IMA rings were studied. The diameter at a pressure of 100 mm Hg (D100) was 2.69 ± 0.09 mm for the RA and 2.31 ± 0.06 mm for the IMA (p < 0.01). This shows that the RA has a larger diameter than the IMA at the distal end from where the samples were taken. The transmural pressure at 0.9D100 (see Material and Methods) was 66.1 ± 1.7 mm Hg for the RA and 76.2 ± 0.7 mm Hg for the IMA. The resting force was 2.3 ± 0.2 g for the RA and 3.8 ± 0.2 g for the IMA (p < 0.05).

	Contraction

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
The ET-1 evoked 9.0 ± 0.9 g force in the RA (n = 12) and 4.5 ± 0.4 g in the IMA (n = 38, p < 0.0001). The normalized force by circumference (Fn) was significantly higher in the RA than in the IMA (0.95 ± 0.10 g /mm versus 0.66 ± 0.05 g /mm, p = 0.007). However, this contraction, if expressed as percentage of the contraction force induced by 100 mmol/L K⁺, was not significantly higher in the RA (n = 12) than in the IMA in which the contraction to 100 mmol/L K⁺ was tested (n = 12, 184.8% ± 23.4% versus 148.8% ± 17.4%, p = 0.23).

With regard to the sensitivity to ET-1, there was no difference between RA and IMA. EC₅₀ (-7.93 ± 0.16 log M versus -8.13 ± 0.06 log M, p = 0.18). The average concentration-contraction curves for these vasoconstrictors are shown in Figure 1.

View larger version (14K): [in this window] [in a new window]   Fig 1. . (A) Mean concentration (-log M)-contraction (force, g) curves for endothelin-1 in the radial artery (RA) and internal mammary artery (IMA). Symbols represent data averaged from 12 RA or 38 IMA rings. Vertical bars are 1 standard error of the mean at the maximum response. (B) Contraction force normalized by the circumference (Fn, g/mm); n = 12 for RA and n = 38 for IMA. (**p < 0.01; ***p < 0.001.)

View larger version (13K): [in this window] [in a new window]   Fig 2. . (A) Mean concentration (-log M)-contraction (force, g) curves for angiotensin II in the radial artery (RA) and internal mammary artery (IMA). Symbols represent data averaged from nine RA or eight IMA rings. Vertical bars are 1 standard error of the mean at the maximum response. (B) Contraction force normalized by the circumference (Fn, g/mm); n = 9 for RA and n = 8 for IMA. (*p < 0.05; **p < 0.01.)

View larger version (12K): [in this window] [in a new window]   Fig 3. . (A) Contraction force to 100 mmol/L K+ in the radial artery (RA) and the internal mammary artery (IMA); n = 12 for each artery (p = 0.09). (B) Contraction force normalized by the circumference (Fn, g/mm, n = 12 for each artery).

	Relaxation

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

View larger version (13K): [in this window] [in a new window]   Fig 4. . Mean concentration (-log M)-relaxation (percentage of precontraction) curves for substance P (A) or calcium ionophore A23187 (B). Symbols represent data averaged from 17 radial artery (RA) or 9 internal mammary artery (IMA) rings for substance P and from 14 RA or 26 IMA rings for A23187. The precontraction was induced by U46619 (10 nmol/L). Vertical bars are 1 standard error of the mean of the response at each concentration.

For the endothelium-independent relaxation, it is similar to the endothelium-dependent relaxation, there was no difference with regard to the endothelium-independent relaxation induced by nitroglycerin (99.2% ± 0.8% in the RA, n = 6, versus 96.8% ± 1.1%, n = 26) (p = 0.2, Fig 5).

View larger version (19K): [in this window] [in a new window]   Fig 5. . Mean concentration (-log M)-relaxation (percentage of precontraction) curves for nitroglycerin. Symbols represent data averaged from 6 radial artery (RA) and 26 internal mammary artery (IMA) rings. The precontraction was induced by U46619 (10 nmol/L). Vertical bars are 1 standard error of the mean of the response at each concentration.

	Comment

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

Previous studies have demonstrated that the RA is reactive to norepinephrine, 5-hydroxytryptamine, and thromboxane A₂ mimetic U46619 [17]. However, important spasmogens for blood vessels may involve many vasoconstrictor substances. As demonstrated in other arterial grafts [14], these vasoconstrictors include (1) endothelium-derived contracting factors such as ET-1, (2) prostanoids such as thromboxane A₂ and prostaglandin F_2a, (3) circulating sympathomimetic substances (-adrenoceptor agonists) such as norepinephrine and synthetic ₁-adrenoceptor agonists (methoxamine or phenylephrine), (4) platelet-derived contracting substances such as 5-hydroxytryptamine and thromboxane A₂, (5) substances released from mast cells and basophils such as histamine, (6) muscarinic receptor agonists such as acetylcholine, (7) renin angiotensin system-related substances such as AII, and (8) depolarizing agent potassium ion.

Endothelin-1 has been proposed as the most potent vasoconstrictor known [19]. Elevated plasma levels have been measured during cardiopulmonary bypass [20]. Therefore, this vasoconstrictor may have a pathogenic significance in vasospasm related to cardiac operations. Similarly, the plasma level of AII has been measured to be elevated during [21] and after [22] cardiopulmonary bypass and presumed to be one of the factors responsible to postoperative hypertension [22]. These two vasoconstrictors, therefore, may have important pathologic significance in the vasospasm of the RA.

The long-term patency of a graft may be related to endothelial function. One of the possible causes for the early occlusion of the RA, as reported in the early 1970s, is that the endothelial function of this artery may be different compared with the well-established arterial graft-IMA. However, little has been known about the endothelial function of the RA [17]. In fact, endothelial function is rather complicated. Endothelium-dependent relaxation is often used as an index of endothelial function. Endothelium-dependent relaxation is composed of a few different mechanisms mediated by endothelium-derived relaxing factors including prostacyclin, nitric oxide, and endothelium-derived hyperpolarizing factor [23, 24]. With regard to the endothelium-derived relaxing factor mechanism, there are two major ways to stimulate the release-the receptor-mediated and nonreceptor-mediated mechanisms. The second part of our present study was designed on the basis of this knowledge. Substance P was used to stimulate the receptor-mediated endothelium-dependent relaxation and calcium ionophore (A23187), the nonreceptor-mediated endothelium-dependent relaxation.

In our study, we did not detect significant differences between the RA and IMA with regard to either the endothelium-dependent or endothelium-independent relaxation. Perhaps the difference seen clinically between these two arterial grafts (more spastic characteristic and higher incidence of narrowing or occlusion of the RA, as reported in the early experiences [5]) is not attributable to the endothelial function.

Chardigny and associates [17] have reported that the RA has increased reactivity to norepinephrine and serotonin. In our study we tested another two important vasoconstrictor substances: ET-1 and AII. Our results suggest that the RA has higher contractile response to both ET-1 and AII. This was shown by the observations that ET-1 induced a higher contraction force (9.0 g ) in the RA compared to the IMA (4.5 g , p < 0.0001). More important, this contraction force was also higher in the RA if normalized to the force developed per 1 mm circumference (0.95 ± 0.1 g /mm versus 0.66 ± 0.05 g /mm, p = 0.007). Similarly, both the maximal (6.5 ± 1.9 g versus 1.7 ± 0.3 g , p = 0.015) and the normalized (0.8 ± 0.2 g /mm versus 0.2 ± 0.05 g /mm, p < 0.01) contraction force to AII were higher in the RA than in the IMA (see Fig 2).

Furthermore, our study demonstrates that this increased contractility in the RA is related to receptor-mediated mechanisms. This is demonstrated in our study by the observations that the contraction force to K⁺ (100 mmol/L) normalized by the circumference (Fn to K⁺) was similar in these two vessels (0.6 ± 0.1 g /mm versus 0.6 ± 0.07 g /mm, p = 0.7) (see Fig 3). It is well known that K⁺ contracts smooth muscle through depolarizing the smooth muscle membrane potential, whereas ET-1 and AII contract through receptor mechanisms.

Our study also demonstrates that although the RA contracts to ET-1 and AII to a higher force, there is no significant difference with regard to the sensitivity to these two vasoconstrictors between the RA and the IMA. This implies that although the RA contracts more strongly to ET-1 and AII than the IMA does, both RA and IMA respond at similar ranges of the increased plasma concentrations of these vasoconstrictors.

Although we have only tested two receptor agonists (ET-1 and AII) due to extreme sparsity of human tissue, a previous study has tested the reactivity of RA to norepinephrine and 5-hydroxytryptamine [17]. Our study adds information to the understanding of the biological characteristics of the RA.

Previous histologic studies [25] have demonstrated that the RA has a considerably thicker media and thus may be more prone to ischemia. This may partially account for the reported early failure of this graft. However, the histologic characteristics of the RA may not be changed by interventions during operation, but the higher contraction could be eliminated by pharmacologic agents. In fact, with the introduction of calcium antagonists, vasospasm of the RA is less encountered and the early results have been significantly improved [6], although the long-term results still remain to be determined. We have recently studied the effects of verapamil and nitroglycerin solution on the prevention of the contraction of the RA during operation [26]. The present study has demonstrated the necessity of the use of vasodilator solutions for the RA as this artery is particularly sensitive to some receptor agonists such as ET-1 and AII.

From the aforementioned, we believe that the difference seen clinically between the RA and the IMA, apart from the previously reported histologic difference, is at large related to the higher receptor-mediated contractility of the RA rather than endothelial function. Therefore, pharmacologic treatment (spasmolytic agents) is particularly important in the preparation and the postoperative treatment for coronary artery bypass grafting using the RA as a graft.

As recently suggested by us [13], arterial grafts may be functionally classified as type I (somatic arteries), type II (splanchnic arteries), and type III (limb arteries). The types II and III are more prone to vasospasm. In this classification, the IMA belongs to the type I and RA to the type III. The present study supports this functional classification and provides scientific evidence that the RA is more reactive to some receptor-mediated vasoconstrictor substances (such as ET-1 and AII).

In conclusion, the present study suggests that the human RA has a higher receptor-mediated contractility (to ET-1 and AII), but similar endothelial function compared to the IMA. The study reveals the nature of the more spastic characteristics of the RA, supports the necessity of a more active pharmacologic intervention to relieve spasm in the RA, and suggests that the similar endothelium-derived relaxing factor-mediated endothelial function of the RA compared with the IMA may be the basis for a satisfactory long-term patency.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
This study was supported by Committee of Research and Conference Grant (337/048/0018 and 335/048/0079) and Vice-Chancellor Grant (350/172/0/9), and Research Committee Grant (344/048/0001), University of Hong Kong, St. Vincent Medical Foundation, and Dant Equipment Funds of American Heart Association, Oregon Affiliate, Oregon. We gratefully acknowledge the assistance of Dr Anthony P. Furnary at St. Vincent Hospital and Dr Shui Wah Chiu at Grantham Hospital for providing some of the radial artery tissue for this study. We also thank Sister Sui Keng Hui, RN, and the nursing staff of the Operating Theater, Grantham Hospital, Hong Kong, Louise Garret and Bonnie Way, RN, and the nursing staff of St. Vincent Hospital for their technical assistance.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 
Address reprint requests to Prof He, Division of Cardiothoracic Surgery, University of Hong Kong, Grantham Hospital, 125 Wong Chuk Hang Rd, Aberdeen, Hong Kong (e-mail: gwhe{at}hkucc.hku.hk).

	References

Top Footnotes Abstract Introduction Material and Methods Organ Bath Technique Protocol Data Analysis Drugs Results Contraction Relaxation Comment Acknowledgments References

 

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