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J Thorac Cardiovasc Surg 1998;116:454-458
© 1998 Mosby, Inc.

Surgery for Adult Cardiovascular Disease

Difference in acetylcholine-induced nitric oxide release of arterialand venous grafts in patients after coronary bypass operations

Hiroaki Nishioka, MD, Soichiro Kitamura, MD, Yoichi Kameda, MD, Shigeki Taniguchi, MD, Tetsuji Kawata, MD, Kazumi Mizuguchi, MD

From the Department of Surgery III, Nara Medical University, Nara,Japan.

Received for publication June 24, 1997. Revisions requested Sept. 24, 1997; revisions received March 9, 1998. Accepted for publication March 9, 1998. Address for reprints: Hiroaki Nishioka, MD, Department of Surgery III,Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634, Japan.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objectives: In vivo investigation ofnitric oxide release in coronary bypass grafts has not been reported. We studiedacetylcholine-induced nitric oxide release in vivo of coronary bypass grafts andvasomotor responses to acetylcholine of grafted coronary arteries in patientsafter coronary bypass grafting.
Methods:We examined 24 internal thoracic artery grafts and 16 saphenous vein grafts in39 patients. The mean ages of the patients were 65 years for the arterial graftsand 68 years for the venous grafts. Nitric oxide was measured as the plasmanitrite level by the Griess reaction. Before and after intragraft acetylcholineinfusion (5 µg), blood was sampled from the distal end of the graft, andangiograms were taken and analyzed by cine-densitometry.
Results: The plasma nitrite concentration afterstimulation with acetylcholine compared with the control value was 134%± 52% at 4 minutes (P = 0.05)and 184% ± 107% at 6 minutes (P =0.01) in the arterial grafts; in the venous grafts these values were 101%± 24% at 4 minutes (P  =0.96) and 108% ± 36% at 6 minutes (P =0.69). Low-dose acetylcholine dilated the coronary arteries supplied by arterialgrafts by 6.3% ± 16.6% whereas coronary arteries suppliedby venous grafts were reduced by 9.8% ± 11.8% in diameterand the vasoactive responses were different (P =0.01).
Conclusions: In vivo internalthoracic artery grafts had more endothelium-derived nitric oxide release inresponse to acetylcholine than did saphenous vein grafts after coronary bypassgrafting.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Arterial grafts, especially internal thoracic artery (ITA) grafts,recently have been used more often instead of saphenous vein grafts (SVGs) asthe first choice for coronary artery revascularization.Go 1 There are many reports that presentthe advantages of ITA grafts over venous grafts. First, ITA grafts haveexcellent patency and superior resistance to atherosclerotic changes over thelong-term postoperative period.Go 2Second, they adapt physiologically to the flow demands of coronary circulationGo 3 and adapt anatomically to physicaldevelopment in pediatric patients.Go 4These advantages are derived mainly from the viability of the ITA grafts.Go 5 In organ bath experiments,endothelial function in freshly harvested ITAs and saphenous veins in thegrafted or ungrafted state differed with respect to the release of nitric oxide(NO).Go Go 6-8In vivo investigation of NO release in implanted coronary bypass grafts,however, has not yet been reported. The purpose of this study was to compare theacetylcholine-induced endothelial NO release in bypass grafts between ITAs andsaphenous veins in patients after coronary artery bypass grafting and toevaluate the metabolic function of arterial and venous grafts.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Patients
In 39 patients (36 men and 3 women), 40 bypass grafts were studied duringpostoperative cardiac catheterization. Patients with any signs of ischemia,angina, heart failure, or stenosis of the bypass grafts were excluded from thestudy protocol. Patient profiles are shown in Table I. Themean age and mean postoperative period for the patients at the time of thisstudy were 65 ± 9 years (range 47 to 78 years) and 38 ±46 months (range 1 to 154 months), respectively, for the ITA graft group and 68 ±4 years (range 60 to 75 years) and 48 ± 50 months (range 1 to 152months), respectively, for the SVG group. There were no significant differencesbetween the two groups in age, gender, postoperative period, or coronary riskfactors including hypertension, diabetes mellitus, hyperlipidemia, and smokinghistory. All of the grafts were used as isolated grafts and all ITAs (19 leftITAs and 5 right ITAs) were used as in situ grafts. For the grafts bypassed tothe left circumflex coronary artery (LCX), there were also no significantdifferences between the two groups in clinical profiles including age,postoperative period, and coronary risk factors. All grafts wereangiographically patent with good run-off flow.


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  		Table I. Patient profiles
 
Study protocol
The study protocol was approved by the Institutional Review Committee onHuman Research of Nara Medical University. Informed consent was obtained fromthe patients before the procedure and all the studies were completed withoutcomplications. Patients underwent cardiac catheterization while in a fastingstate without premedication, after interruption of all vasoactive drugs for morethan 24 hours. No patients received ß-adrenergic receptor blockers within48 hours before the study. After postoperative diagnostic catheterization, a 5FJudkins catheter for the right coronary artery was positioned at the ostium ofthe coronary bypass graft, and grafts were selectively cannulated to the distalanastomotic site with a 2.7F microcatheter (Tracker-18 infusion catheter, TargetTherapeutics) through a guiding catheter. Blood in the distal portion of thegraft was obtained through the microcatheter as a control. Blood was aspiratedthrough the microcatheter over about 60 to 90 seconds to avoid hemolysis. Fivemicrograms or 3 x 10-8 mol of acetylcholine solution wasthen infused into the graft through the guiding catheter for 30 seconds. Bloodsamples from the distal portion of the graft were obtained in the same manner asfor the control, at 4 and 6 minutes after the administration of acetylcholine.Eight minutes after the beginning of acetylcholine administration, angiographyof the grafts and the bypassed coronary arteries was performed. Angiograms werenot taken in the first five patients in the SVG group or in the first six in theITA group, but in the remaining patients angiographic investigations wereconsecutively performed and the diameters of grafts and coronary arteries atpoints about 1 cm upstream and downstream from the anastomotic site weremeasured by cine-densitometry. The electrocardiogram and arterial pressure weremonitored continuously during the procedures. Finally, 1 mg isosorbide dinitratewas injected into the graft through the guiding catheter to overcome theacetylcholine-induced vasoconstriction.

Assay of NO concentrations
Blood samples were obtained through the catheters with the use ofdisposable syringes and centrifuged as soon as possible at 3000 rpm for 5minutes at 4° C. Plasma was stored at –80° C until use. Plasmasamples were diluted 1:2 with deionized water and filtered through a 0.45µm microfilter. Plasma nitrite (NO2–) andnitrate (NO3–) concentrations were measured withan NOx analyzer (Eno10, Eicom, Kyoto, Japan) with high-performance liquidchromatography and the Griess reaction.Go Go 9,10 In brief, the samples were firstpassed through a column to separate NO3– from NO2–.Then the samples were passed through a second column containing copper-coatedcadmium to reduce the NO3– to NO2–.Next the NO2– was detected by reaction with theGriess reagent (0.03 mol/L sulfanilamide plus 0.15 mol/L HCl solution containing1.0 x 10-3 mol/L N-[1-naphthyl] ethylenediamine).Absorption was measured at 546 nm with use of a spectrophotometer. Thus theseparate NO2– and NO3–levels could be measured simultaneously. The detection limit of the assay was1.0 x 10-8 mol/L.

Quantitation of graft and coronary artery diameters
The diameters of the grafts and grafted coronary arteries were calculatedby cine-densitometry with a microcomputer analyzing program, Elk Cine-AngioSystem Cam-1000, produced by Nishimoto Sangyo, Osaka, Japan.Go 11

Statistical analysis
Measurements are expressed as mean plus or minus standard deviations(percentiles). Statistical analysis was performed with the SPSS version 6.1.3Jprogram (SPSS, Chicago, Ill.) on a personal computer (XL-590/Compaq Computer).The patient profile data were analyzed by the {chi}Go 2 or Mann-Whitney U test, and theplasma NO2 and NO3 concentration data were analyzed bythe Wilcoxon matched-pairs signed-rank test, Mann-Whitney U test, and analysisof variance (Pillai's multivariate test). Correlation coefficients werecalculated by the method of Pearson. All pvalues are two tailed.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Plasma NO2– and NO3–concentrations
For 40 grafts in 39 patients who had undergone coronary artery bypassgrafting, the plasma NO2 and NO3 concentrations in thedistal portion of the graft after acetylcholine administration are shown inTable II.Plasma NO2– concentration significantly increasedafter acetylcholine infusion in the ITA grafts (at 4 minutes,p = 0.05; at 6 minutes,p = 0.01), whereas there were nosignificant increases for the SVGs (at 4 minutes, p =0.96; at 6 minutes, p = 0.69). Theresponse in plasma NO2– levels after stimulationwith acetylcholine was different between ITA grafts and SVGs (at 4 minutes,p = 0.04; 6 minutes, p =0.03). The plasma concentration of total NO2– plusNO3– also responded differently to the stimulationof acetylcholine between the two groups (at 4 minutes, p =0.03; 6 minutes, p = 0.01). Significanceof the difference in plasma NO2– concentrationsbetween the ITA grafts and SVGs was statistically borderline by analysis ofvariance (p = 0.05). A significantrelation existed in the ratio of plasma level of NO2–to total NO2– plus NO3–6 minutes after stimulation with acetylcholine (p =0.05).


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  		Table II. Plasma nitrite and nitratelevels
 
Because the target coronary arteries of the ITA or SVG differed, and theITA was mainly used for the left anterior descending coronary artery and the SVGwas mainly used for the right coronary artery and LCX as shown in Table I, NO2–responses were compared in the bypass grafts for the LCX where both the ITA andSVG were used. The plasma NO2– concentration afterstimulation with acetylcholine compared with the control value was differentbetween the ITA and SVG (at 4 minutes, p = 0.04; at 6 minutes, p = 0.01) (Fig. 1). The increase in plasma NO2–levels after stimulation with acetylcholine in the ITAs did not reachstatistical significance.



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  		Fig. 1. Plasma NO2–concentration after stimulation with acetylcholine compared with control levelfor grafts bypassed to the LCX. For grafts to the LCX, plasma NO2–concentration after stimulation with acetylcholine compared with the controlvalue was significantly higher in ITA grafts than in SVGs at 4 minutes (p = 0.04) and at 6 minutes (p =0.01). This response was similar to the result for all study grafts, includinggrafts to other coronary arteries.

 
Time between the graft implantation and the study ranged from 1 to 154months for the ITA group and from 1 to 152 months for the SVG group. However, NOrelease induced by acetylcholine administration did not differ with regard tothe graft age. There were no significant correlations or significant differencesby regression analysis between the graft age and ratio of plasma NO2after stimulation with acetylcholine (Fig. 2).



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  		Fig. 2. The relation betweenthe change in nitrite level after acetylcholine infusion and the graft age(period between graft implantation and the study). There was no significantcorrelation by regression analysis between the change of plasma NO2–level after acetylcholine infusion and the graft age.

 
Vasomotor response to acetylcholine
Fig. 3 shows angiograms of an SVG implanted to the LCX in a 65-year-oldman 115 months after bypass grafting in the control condition and afterintragraft infusion of 5 µg acetylcholine. The native coronary artery wasconstricted after acetylcholine administration. Fig. 4 shows angiograms of anITA graft implanted to the left anterior descending artery in a 52-year-old man145 months after bypass grafting in the control condition and after intragraftinfusion of 5 µg acetylcholine. The native coronary artery was dilatedafter acetylcholine administration.



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  		Fig. 3. Angiograms of an SVGimplanted to the LCX in a 65-year-old man taken 115 months after the operationin the control condition (left) and afterintragraft infusion of 5 µg acetylcholine (right).The native coronary artery bypassed with an SVG constricted after acetylcholineadministration.

 


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  		Fig. 4. Angiograms of a leftITA graft implanted to the left anterior descending artery in a 52-year-old mantaken 145 months after the operation in the control condition(left) and after intragraft infusion of 5µg acetylcholine (right). The nativecoronary artery bypassed with an ITA graft dilated after acetylcholineadministration.

 
Low-dose acetylcholine dilated ITA grafts by 6.3% ± 11.6%whereas SVGs were reduced by 3.1% ± 8.9%. Vasomotorresponses of the grafts after acetylcholine administration were differentbetween the ITA grafts and SVGs (p = 0.02)(Fig. 5).



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  		Fig. 5. Vasomotor responses ofthe grafts to acetylcholine (ACH) infusion.Low-dose acetylcholine dilated ITA grafts whereas the SVGs were reduced indiameter (ITA vs SVG, p = 0.02).

 
Low-dose acetylcholine dilated the coronary arteries supplied by arterialgrafts by 6.3% ± 16.6% whereas coronary arteries suppliedby venous grafts were reduced by 9.8% ± 11.8% in diameter.Acetylcholine-induced vasoconstriction was significantly less in the coronaryarteries grafted with ITAs than in those with SVGs (p =0.01) (Fig. 6).



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  		Fig. 6. Vasomotor responses ofthe grafted coronary arteries to acetylcholine (ACH)infusion. Acetylcholine-induced vasoconstriction was significantly less in thecoronary arteries grafted with ITA grafts than in those grafted with SVGs (p = 0.01).

 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
Advantages of the ITA graft over the SVG are excellent patency, lowerincidence of graft disease in the long-term postoperative period, andphysiologic and anatomic adaptability.Go Go 12-16 These advantages are apparentlya result of the properties of the vessel, especially of the endothelium. Inorgan bath experiments, endothelial release of NO was different in ITAs and SVGsin the grafted or ungrafted states.Go Go 16-18 In this study, we demonstratedfor the first time a greater release of NO in the ITA graft than in the SVG inpatients 41 ± 47.3 months after coronary artery bypass grafting.

NO assay
NO cannot be easily or directly measured in biologic tissues or fluidsbecause it is rapidly metabolized. Instead, NO concentration is determined bymeasurement of NO2– and NO3–concentrations. Determination of total plasma NO2–plus NO3– concentrations as a measurement of NOconcentration has been previously described and is a well established method.Go Go 12,13Although NO2– and NO3–are metabolites of NO, the metabolic rate of conversion of NO to NO2or NO3 in the blood is not presently known. Plasma NO2–concentration is very low and previous assays rarely succeeded in themeasurement of isolated plasma NO2– level as ameasurement of NO production.Go 14Our measurements of separate plasma NO2 and NO3–concentrations were made with instrumentation incorporating high-performanceliquid chromatography and the Griess reaction, which enabled separate evaluationof changes in plasma NO2– and NO3–concentrations.Go Go 9,10

NO is released bidirectionally by the endothelium.Go 15 Extraluminal NO acts on theunderlying vascular smooth muscleGo 16and inhibits smooth muscle cell proliferation. Intraluminal NO is released intothe blood. The results of the concentration measurements of metabolites in thepresent study demonstrated that the ITA graft actually released NO into theblood in response to acetylcholine. The NO-releasing response to acetylcholinewas also better for the ITA grafts to the LCX as compared with that of the SVGfor the same arterial lesions. There seem to be no differences in the ability ofthe graft to produce NO regardless of which coronary artery is targeted.

NO plays an important role in many physiologic functions. NO inhibitsplatelet aggregation and promotes platelet disaggregation.Go 17 It also inhibits platelet andleukocyte adhesions to the endothelium,Go 18protecting the endothelium from injury induced by superoxide radicals; inaddition, intraluminally released NO may have a metabolic effect on thedownstream vascular beds.Go 19Therefore ITA grafts with NO-releasing endothelium may have anantiatherosclerotic effect on both grafts and grafted coronary arteries.

Vasomotor response to acetylcholine
ITAs are usually free of atherosclerotic changesGo 20 and dilate in response to localadministration of acetylcholine as long as the endothelium is functional.Go 21 The results of the NO assay offeran explanation for the graft's response to acetylcholine. The endothelialrelease of NO in SVGs was insufficient to reverse the direct constrictive effectof acetylcholine. Here we have provided quantitative data comparing the responseto intragraft administration of low-dose acetylcholine of coronary arteriesgrafted with the ITA and SVG. The results are consistent with those of aprevious angiographic study that examined the vasomotor response of grafts andcoronary arteries grafted with ITAs to the administration of ergonovine orsubstance P.Go Go 22,23 However, high-dose acetylcholineadministration can uniformly induce a constrictive response of the coronaryartery, and a dilative response can be induced by an optimal dose ofacetylcholine.Go 24 Severalreasons for the dilation of the coronary arteries bypassed with ITA grafts inthis study can be considered. First, intraluminally released NO from the graftcan affect the downstream coronary arteries; second, endothelium-dependentNO-mediated dilation of the coronary artery occurs in response to acetylcholine;and third, flow-mediated vasodilation after the increased flow of the graftoccurs in response to acetylcholine or the angiographic procedures. Although wecannot exclude other mechanisms of coronary artery dilation such as aninvolvement of prostacyclinGo 25orendothelium-dependent hyperpolarization factor,Go 26 the results of the NO assay in thepresent study offer an explanation of the coronary artery response by theendothelium-derived NO from the grafts. The present angiographic results maysuggest that the ITA graft has a possible metabolic effect of protecting thegrafted coronary arteries from spasm and atherosclerosis.

In summary, the ITA graft is not only an excellent conduit with goodlong-term patency, but it also has a potential metabolic effect that protectsthe graft and the grafted coronary arteries from spasm and atherosclerosis. Thisis the first study to demonstrate in human subjects that in situ ITA grafts canproduce more NO compared with venous grafts after coronary bypass grafting. Thuscoronary artery bypass grafting with the ITA may have the salutary effect oftransplanting functional endothelial cells into the coronary circulation.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Loop FD, Lytle BW, Cosgrove DM, et al.Influence of the internal-mammary-artery graft on 10-year survival and othercardiac events. N Engl J Med 1986;314:1-5.[Abstract]
  2. Cameron A, Green GE, Brogno DA, Thornton J. Internalthoracic artery grafts: 20-year clinical follow-up. J Am Coll Cardiol 1995;25:188-92.[Abstract]
  3. Morita R, Kitamura S, Kawachi K, et al.Exercise coronary flow reserve of bilateral internal thoracic artery bypassgrafts. Ann Thorac Surg 1993;55:883-7.[Abstract]
  4. Kitamura S, Seki T, Kawachi K, Morita R,Kawata T. Excellent patency and growth potential of internal mammary arterygrafts in pediatric coronary bypass surgery: new evidence for a "live"conduit. Circulation 1989;78(Suppl):I29-39.
  5. Werner GS, Wuchwald A, Kreuzer H, Wiegant V.Evidence in vivo of an intact endothelial function in internal mammary arteriesbefore and after implantation as coronary grafts. Coron Artery Dis 1990;1:461-8.
  6. Lüscher TF, Diederich D, Siebenmann R, etal. Difference between endothelium-dependent relaxation in arterial and venouscoronary grafts. N Engl J Med 1988;319:462-7.[Abstract]
  7. Ku DD, Claufield JB, Kirklin JK.Endothelium-dependent response in long-term human coronary artery bypass grafts.Circulation 1991;83:402-11.[Abstract/Free Full Text]
  8. Ignarro LJ, Buga GM, Wood KS, Byrns RE,Chaudhuri G. Endothelium-derived relaxing factor produced and released fromartery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987;84:9265-9.[Abstract/Free Full Text]
  9. Green LC, Wagner DA, Grogowsk J, Skippers JS,Wishnock JS, Tannenbaum SR. Analysis of nitrate, nitrite and [15N] nitrate inbiological fluids. Anal Biochem 1982;126:131-8.[Medline]
  10. Muscara MN, de Nucci G. Simultaneousdetermination of nitrite and nitrate anion in plasma, urine and cell culturesupernatants by high-performance liquid chromatography with post-columnreactions. J Chromatogr B Biomed Sci Appl 1996;686:157-64.
  11. Seki T, Kitamura S, Kawachi K, et al. Aquantitative study of postoperative luminal narrowing of the internal thoracicartery graft in coronary artery bypass surgery. J Thorac Cardiovasc Surg 1992;104:1532-8.[Abstract]
  12. Marletta MA, Yoon PS, Iyengar R, Leaf CD,Wishnock JS. Macrophage oxidation of L-arginineto nitrite and nitrate: nitric oxide is an intermediate. Biochemistry 1988;27:8706-11.[Medline]
  13. Zaballos GA, Bernstein RB, Tompson CI, et al.Pharmacodynamics of plasma nitrate/nitrite as an indication of nitric oxideformation in conscious dog. Circulation 1995;91:2982-8.[Abstract/Free Full Text]
  14. Roth E, Steininger R, Winkler S, et al.L-Arginine deficiency after livertransplantation as an effect of arginase efflux from the graft. Transplantation 1994;57:665-9.[Medline]
  15. Pearson PJ, Evora PRB, Schaff HV. Bioassay ofEDRF from internal mammary arteries: implications for early and late bypassgraft patency. Ann Thorac Surg 1992;54:1078-84.[Abstract]
  16. Moncada S, Palmer RMJ, Higgs EA. Nitricoxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 1991;43:109-42.[Medline]
  17. Radomski MW, Palmer RMJ, Moncada S. Theanti-aggregating properties of vascular endothelium: interactions betweenprostacyclin and nitric oxide. Br J Pharmacol 1987;92:639-46.[Medline]
  18. Radomski MW, Palmer RMJ, Moncada S.Endogenous nitric oxide inhibits human platelet adhesion to vascularendothelium. Lancet 1987;2:1057-8.[Medline]
  19. Kalm M, Schrader J. Control of coronaryvascular tone by nitric oxide. Circ Res 1990;66:1561-75.[Abstract/Free Full Text]
  20. Kobayashi H, Kitamura S, Kawachi K, Morita R,Konishi Y, Tsutsumi M. A pathological and biological study of arteriosclerosisin the internal thoracic artery, a vessel commonly used as a graft in coronaryartery bypass surgery. Jpn J Surg 1993;23:697-703.
  21. Takeda T, Fujita M, Fudo T, et al. Responseof internal mammary artery to local administration of acetylcholine. Am JCardiol 1996;77:302-4.[Medline]
  22. Kitamura S, Morita R, Kanji K, et al.Different response of coronary and internal mammary artery bypass grafts toergonovine and nitroglycerin in variant angina. Ann Thorac Surg 1989;47:756-60.[Abstract]
  23. Kushwaha SS, Bastami M, Tadjkarimi S, IlsleyCDJ, Mitchell AG, Yacoub MH. Late endothelial function of free and pedicledinternal mammary artery grafts. J Thorac Cardiovasc Surg 1995;110:453-62.[Abstract/Free Full Text]
  24. Hanet C, Robert A, Wijins W. Vasomotorresponse to ergometrine and nitrates of saphenous vein grafts, internal mammaryartery grafts, and grafted coronary arteries late after bypass surgery.Circulation 1992;86(Suppl):II210-6.
  25. Forstermann U, Muggy A, Alheid U, Haverich A,Frolich JC. Selective attenuation of endothelium-mediated vasodilation inatherosclerotic human coronary artery. Circ Res 1988;62:185-90.[Abstract/Free Full Text]
  26. Horzmann S, Kikovetz WR, Windischhofer W,Paschke E, Graier WF. Pharmacologic differentiation between endotheliumdependent relaxations sensitive and resistant to nitro-L-argininein coronary arteries. J Cardiovasc Pharmacol 1994;23:747-56. [Medline]



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