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(Circulation. 1997;95:2068-2074.)
© 1997 American Heart Association, Inc.


Articles

Biochemical Evidence for Impaired Nitric Oxide Synthesis in Patients With Peripheral Arterial Occlusive Disease

Rainer H. Böger, MD; Stefanie M. Bode-Böger, MD; Wolfgang Thiele; Wolfgang Junker; Klaus Alexander, MD; Jürgen C. Frölich, MD

From the Institute of Clinical Pharmacology and Department of Angiology (K.A.), Medical School, Hannover, Germany.

Background We studied urinary nitrate and cGMP excretion rates, indices of systemic NO formation, and plasma concentrations of L-arginine and the endogenous NO synthase inhibitor asymmetrical dimethylarginine (ADMA) and its inactive stereoisomer, symmetrical dimethylarginine, in 77 patients with peripheral arterial occlusive disease (PAOD) in Fontaine stages IIb through IV and in 47 young and 37 elderly healthy control subjects.

Methods and Results Urinary nitrate excretion was 182.0±11.4 µmol/mmol creatinine and cGMP excretion was 186.2±13.0 nmol/mmol creatinine in young healthy control subjects. In elderly control subjects, both excretion rates were slightly lower (nitrate, 156.0±7.8 µmol/mmol creatinine; cGMP, 150.0±8.3 nmol/mmol creatinine; P=NS). In PAOD patients, there was a significant, progressive reduction of urinary nitrate (IIb, 138.4±11.9; III, 128.6±11.3; and IV, 91.9±8.0 µmol/mmol creatinine; P<.05) and cGMP (IIb, 139.9±25.2; III, 115.6±13.1; and IV, 76.9±7.9 nmol/mmol creatinine; P<.05) excretion rates related to the Fontaine stage of PAOD. These changes were independent of changes in renal excretory function. Plasma L-arginine concentrations were not significantly different between the groups, but ADMA concentrations were elevated in PAOD patients (young control subjects, 1.25±0.11; elderly control subjects, 1.01±0.05 µmol/L; IIb, 2.62±0.24; III, 3.06±0.48; and IV, 3.49±0.26 µmol/L; P<.05 for PAOD versus control subjects). There was a significant linear correlation between urinary nitrate and cGMP excretion rates and a significant negative linear correlation between plasma ADMA concentrations and urinary nitrate excretion.

Conclusions In PAOD patients, there is a progressive reduction in urinary nitrate and cGMP excretion rates, which may be caused in part by accumulation of ADMA, an endogenous inhibitor of NO synthase.


Key Words: hypercholesterolemia • atherosclerosis • endothelium-derived factors • risk factors




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J Am Coll CardiolHome page
R. H. Boger, S. M. Bode-Boger, P. S. Tsao, P. S. Lin, J. R. Chan, and J. P. Cooke
An endogenous inhibitor of nitric oxide synthase regulates endothelial adhesiveness for monocytes
J. Am. Coll. Cardiol., December 1, 2000; 36(7): 2287 - 2295.
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LupusHome page
P R J Ames, C Tommasino, J Alves, J D Morrow, L Iannaccone, G Fossati, S Caruso, F Caccavo, and V Brancaccio
Antioxidant susceptibility of pathogenic pathways in subjects with antiphospholipid antibodies: a pilot study
Lupus, November 1, 2000; 9(9): 688 - 695.
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J. Nutr.Home page
G. Wu and C. J. Meininger
Arginine Nutrition and Cardiovascular Function
J. Nutr., November 1, 2000; 130(11): 2626 - 2629.
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J. Thorac. Cardiovasc. Surg.Home page
G. Segarra, P. Medina, J. M. Vila, J. B. Martinez-Leon, R. M. Ballester, P. Lluch, and S. Lluch
Contractile effects of arginine analogues on human internal thoracic and radial arteries
J. Thorac. Cardiovasc. Surg., October 1, 2000; 120(4): 729 - 736.
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CirculationHome page
J. J. Jang, H.-K. V. Ho, H. H. Kwan, L. F. Fajardo, and J. P. Cooke
Angiogenesis Is Impaired by Hypercholesterolemia : Role of Asymmetric Dimethylarginine
Circulation, September 19, 2000; 102(12): 1414 - 1419.
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Arterioscler. Thromb. Vasc. Bio.Home page
J. P. Cooke
Does ADMA Cause Endothelial Dysfunction?
Arterioscler Thromb Vasc Biol, September 1, 2000; 20(9): 2032 - 2037.
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Arterioscler. Thromb. Vasc. Bio.Home page
A. Fard, C. H. Tuck, J. A. Donis, R. Sciacca, M. R. Di Tullio, H. D. Wu, T. A. Bryant, N.-T. Chen, M. Torres-Tamayo, R. Ramasamy, et al.
Acute Elevations of Plasma Asymmetric Dimethylarginine and Impaired Endothelial Function in Response to a High-Fat Meal in Patients With Type 2 Diabetes
Arterioscler Thromb Vasc Biol, September 1, 2000; 20(9): 2039 - 2044.
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Circ. Res.Home page
R. H. Boger, K. Sydow, J. Borlak, T. Thum, H. Lenzen, B. Schubert, D. Tsikas, and S. M. Bode-Boger
LDL Cholesterol Upregulates Synthesis of Asymmetrical Dimethylarginine in Human Endothelial Cells : Involvement of S-Adenosylmethionine-Dependent Methyltransferases
Circ. Res., July 21, 2000; 87(2): 99 - 105.
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Arterioscler. Thromb. Vasc. Bio.Home page
R. H. Boger, S. M. Bode-Boger, K. Sydow, D. D. Heistad, and S. R. Lentz
Plasma Concentration of Asymmetric Dimethylarginine, an Endogenous Inhibitor of Nitric Oxide Synthase, Is Elevated in Monkeys With Hyperhomocyst(e)inemia or Hypercholesterolemia
Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1557 - 1564.
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CirculationHome page
R. H. Boger, S. M. Bode-Boger, H. Matsuoka, H. Miyazaki, M. Usui, S. Ueda, S. Okuda, T. Imaizumi, and J. P. Cooke
Is Asymmetric Dimethylarginine a Novel Marker of Atherosclerosis? • Response
Circulation, April 11, 2000; 101 (14): e160 - e161.
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Arterioscler. Thromb. Vasc. Bio.Home page
J. R. Chan, R. H. Boger, S. M. Bode-Boger, O. Tangphao, P. S. Tsao, T. F. Blaschke, and J. P. Cooke
Asymmetric Dimethylarginine Increases Mononuclear Cell Adhesiveness in Hypercholesterolemic Humans
Arterioscler Thromb Vasc Biol, April 1, 2000; 20(4): 1040 - 1046.
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CirculationHome page
L. Vergnani, S. Hatrik, F. Ricci, A. Passaro, N. Manzoli, G. Zuliani, V. Brovkovych, R. Fellin, and T. Malinski
Effect of Native and Oxidized Low-Density Lipoprotein on Endothelial Nitric Oxide and Superoxide Production : Key Role of L-Arginine Availability
Circulation, March 21, 2000; 101(11): 1261 - 1266.
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CirculationHome page
N. Fujiwara, T. Osanai, T. Kamada, T. Katoh, K. Takahashi, and K. Okumura
Study on the Relationship Between Plasma Nitrite and Nitrate Level and Salt Sensitivity in Human Hypertension : Modulation of Nitric Oxide Synthesis by Salt Intake
Circulation, February 29, 2000; 101(8): 856 - 861.
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Cardiovasc ResHome page
K. J. Osterziel, S. M Bode-Boger, O. Strohm, A. E Ellmer, N. Bit-Avragim, D. Hanlein, M. B Ranke, R. Dietz, and R. H Boger
Role of nitric oxide in the vasodilator effect of recombinant human growth hormone in patients with dilated cardiomyopathy
Cardiovasc Res, January 14, 2000; 45(2): 447 - 453.
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ChestHome page
W. C. Hooper, C. Lally, H. Austin, J. Benson, A. Dilley, N. K. Wenger, C. Whitsett, P. Rawlins, and B. L. Evatt
The Relationship Between Polymorphisms in the Endothelial Cell Nitric Oxide Synthase Gene and the Platelet GPIIIa Gene With Myocardial Infarction and Venous Thromboembolism in African Americans
Chest, October 1, 1999; 116(4): 880 - 886.
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CirculationHome page
A. Ito, P. S. Tsao, S. Adimoolam, M. Kimoto, T. Ogawa, and J. P. Cooke
Novel Mechanism for Endothelial Dysfunction : Dysregulation of Dimethylarginine Dimethylaminohydrolase
Circulation, June 22, 1999; 99(24): 3092 - 3095.
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Arterioscler. Thromb. Vasc. Bio.Home page
T. Murohara, B. Witzenbichler, I. Spyridopoulos, T. Asahara, B. Ding, A. Sullivan, D. W. Losordo, and J. M. Isner
Role of Endothelial Nitric Oxide Synthase in Endothelial Cell Migration
Arterioscler Thromb Vasc Biol, May 1, 1999; 19(5): 1156 - 1161.
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CirculationHome page
H. Miyazaki, H. Matsuoka, J. P. Cooke, M. Usui, S. Ueda, S. Okuda, and T. Imaizumi
Endogenous Nitric Oxide Synthase Inhibitor : A Novel Marker of Atherosclerosis
Circulation, March 9, 1999; 99(9): 1141 - 1146.
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J. Am. Soc. Nephrol.Home page
J. T. KIELSTEIN, R. H. BÖGER, S. M. BODE-BÖGER, J. SCHÄFFER, M. BARBEY, K. M. KOCH, and J. C. FRÖLICH
Asymmetric Dimethylarginine Plasma Concentrations Differ in Patients with End-Stage Renal Disease: Relationship to Treatment Method andAtherosclerotic Disease
J. Am. Soc. Nephrol., March 1, 1999; 10(3): 594 - 600.
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CirculationHome page
R. H. Boger, S. M. Bode-Boger, A. Szuba, P. S. Tsao, J. R. Chan, O. Tangphao, T. F. Blaschke, and J. P. Cooke
Asymmetric Dimethylarginine (ADMA): A Novel Risk Factor for Endothelial Dysfunction : Its Role in Hypercholesterolemia
Circulation, November 3, 1998; 98(18): 1842 - 1847.
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J Am Coll CardiolHome page
R. H. Boger, S. M. Bode-Boger, W. Thiele, A. Creutzig, K. Alexander, and J.u. C. Frolich
Restoring vascular nitric oxide formation by L-arginine improves the symptoms of intermittent claudication in patients with peripheral arterial occlusive disease
J. Am. Coll. Cardiol., November 1, 1998; 32(5): 1336 - 1344.
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CirculationHome page
J. Mair, B. Puschendorf, R. H. Boger, and S. M. Bode-Boger
Is Measurement of Cyclic Guanosine Monophosphate in Plasma or Urine Suitable for Assessing In Vivo Nitric Oxide Production? • Response
Circulation, March 31, 1998; 97(12): 1209 - 1210.
[Full Text] [PDF]