(Circulation. 1997;96:2542-2544.)
© 1997 American Heart Association, Inc.
Articles |
Hyperhomocyst(e)inemia Is a Risk Factor for Arterial Endothelial Dysfunction in Humans
From the Department of Medicine, The Chinese University of Hong Kong (K.S.W., P.C., A.S.P.C., L.T.C., Y.Y.S., J.E.S.), the Department of Chemical Pathology (Y.I.L.), and the Department of Diagnostic Radiology and Organ Imaging (C.M.), Prince of Wales Hospital, Hong Kong; and the Department of Cardiology, Royal Prince Alfred Hospital (D.S.C.), Sydney, Australia.
Correspondence to Prof K.S. Woo, Department of Medicine, Prince of Wales Hospital, Shatin, Hong Kong.
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Abstract |
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Background Hyperhomocyst(e)inemia is associated with premature peripheral vascular, cerebrovascular, and coronary artery disease. Because homocysteine has been found to be damaging to endothelial cells in animal and cell culture studies, we evaluated the association between hyperhomocysteinemia and arterial endothelial dysfunction (a marker of early atherosclerosis) in asymptomatic adult subjects.
Methods and Results Using high-resolution ultrasound, we measured endothelium-dependent flow-mediated dilation (EDD) and endothelium-independent nitroglycerin-induced dilation (GTN) of the brachial artery in 14 prospectively defined hyperhomocysteinemic (mean plasma homocysteine, 34.8±8.5 µmol/L), nonsmoking, healthy subjects aged 53±9 years and 14 control subjects with low plasma homocysteine levels (9.9±3.2 µmol/L). The two groups were well matched for age; sex; body mass index; blood pressure, blood cholesterol, folate, and vitamin B12 levels; and vessel diameter. EDD was significantly lower in hyperhomocysteinemic subjects (6.5±1.7%) than in subjects with low homocysteine levels (10.8±1.7%) (P<.001). GTN responses were similar in the two subject groups (P=.90). Multivariate analysis confirmed homocysteine level as the strongest predictor for impaired EDD, independent of age, sex, body mass index, or blood pressure, folate, vitamin B12, and cholesterol levels.
Conclusions Hyperhomocysteinemia is an independent risk factor for arterial endothelial dysfunction in healthy middle-aged adults.
Key Words: risk factors • atherosclerosis • ultrasonics • endothelium-derived factors • hyperhomocysteinemia
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Introduction |
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Although many subjects with coronary artery disease have a history of cigarette smoking, hyperlipidemia, hypertension, or diabetes mellitus, a large proportion of subjects with clinical cardiovascular events do not have these "traditional" coronary risk factors present.1 Therefore, attention has recently focused on other potentially predisposing factors, such as hyperhomocysteinemia.1 2 In epidemiological studies, hyperhomocysteinemia has been associated with premature peripheral vascular, cerebrovascular, and coronary artery disease, independent of the effects of factors such as hyperlipidemia, cigarette smoking, and hypertension.3 4 Homocysteine is a highly reactive amino acid and is known to produce endothelial cell injury in both experimental animal and cell culture studies.5 6 The pathophysiological consequences of such endothelial injury may include impaired release of nitric oxide (NO),7 associated with significant alterations in vascular function.8 Because decreased bioavailability of NO may also result in abnormal reactions between the vessel wall, platelets, and macrophages,9 homocysteine-related endothelial dysfunction may be involved in the initiation and progression of atherogenesis and/or thrombosis.
We and others have recently described a noninvasive method for studying endothelium-dependent vasodilation related to NO release10 11 12 and have documented impaired endothelial function in children with very high plasma homocysteine levels due to homozygous homocystinuria.13 More recent studies, however, have emphasized the adverse cardiovascular outcomes related to mild to moderate hyperhomocysteinemia.3 4 14 Because in vivo studies of endothelial function in hyperhomocysteinemic adults have not been reported previously, such information may be important in defining vascular risk in otherwise apparently healthy subjects.
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Methods |
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Subjects
Data were analyzed from an ongoing community atherosclerosis study performed in the Prince of Wales Hospital, Hong Kong, on asymptomatic volunteers of both sexes aged 40 to 70 years. During the period November 1995 to August 1996, 81 Chinese subjects were recruited; none had any history of hyperlipidemia, hypertension, or diabetes mellitus or a family history of premature vascular disease. Approximately one quarter had a history of cigarette smoking; however, none had any clinical evidence of atherosclerosis, such as a history of angina, myocardial infarction, or previous stroke. All subjects were clinically well and taking no regular cardiovascular medications. All subjects gave informed consent, and the study was approved by our institutional committee on ethical practice.
Each subject made one visit to the hospital after a 14-hour fast, during which detailed medical and smoking histories were taken and physical examination, including measurement of supine resting blood pressure, was performed. Venous blood was sampled for fasting plasma cholesterol, creatinine, homocysteine, vitamin B12, and folate levels. For homocysteine analysis, blood was immediately put into a heparinized bottle on ice, protected from sunlight, and centrifuged within 10 minutes. Homocysteine was measured by isocratic reverse-phase high-performance liquid chromatography on a Hewlett Packard HP 1090 machine fitted with an HP 1049A fluorescence detector, as previously described by our laboratory.2 The assay was linear to a plasma homocysteine concentration of at least 100 µmol/L. The recoveries for homocysteine added to plasma to obtain concentrations of 20, 60, and 80 µmol/L were 103%, 91%, and 110% respectively. The within-batch imprecision (CV%) (n=16 for each) was 7.8%, 6.9%, and 3.7% at plasma homocysteine concentrations of 20, 60, and 80 µmol/L, respectively. The corresponding between-batch imprecision (n=16 for each) was 9.3%, 10.6% and 5.2%.
Arterial Reactivity Studies
For the studies of endothelium-dependent and
-independent arterial dilation, only nonsmoking subjects
were investigated because cigarette smoking is known to be associated
with significant impairment of endothelium-dependent
dilation.15 We investigated the 14 nonsmoking,
hyperhomocysteinemic adults whose fasting total plasma homocysteine was
above the 75th percentile for the entire group of 81 subjects
(homocysteine levels of 25 to 44 µmol/L). We then
selected 14 control nonsmokers from among those subjects with total
plasma homocysteine below the median for the entire group (homocysteine
levels of 5 to 14 µmol/L). A control subject was matched
for each hyperhomocysteinemic subject for sex and age (±5 years), and
these control subjects also had arterial reactivity studies
performed.
The ultrasound method for measuring endothelium-dependent and -independent arterial dilation was performed as described previously.10 11 In brief, arterial diameter was measured from B-mode ultrasound images at rest, in response to reactive hyperemia (with increased flow producing endothelium-dependent dilation, or EDD), again at rest, and after sublingual nitroglycerin (GTN, an endothelium-independent vasodilator). The condition of reactive hyperemia was induced by inflation of a pneumatic tourniquet placed around the forearm (distal to the segment of the artery being scanned) to a pressure of 250 mm Hg for 4.5 minutes, followed by release. Arterial diameter was measured with the use of an L10-5 (midfrequency of 7.5 MHz) linear-array transducer and a standard Advanced Technology Laboratories 3000 system. Arterial flow measurements were derived from the Doppler flow velocity signal, the vessel size, and the heart rate, as described previously.10 11 The accuracy, reproducibility, and low interobserver error for such measurements of arterial physiology have been demonstrated previously.16 EDD of the brachial artery is mainly due to NO release by the endothelium and correlates well with coronary endothelial function in the same subjects.12 17
Statistical Analysis
Descriptive data are expressed as mean±SD. Baseline
characteristics and responses of the hyperhomocysteinemic subjects were
compared with the control subjects by use of independent-samples
t tests. The prospectively defined primary end point of the
study was EDD; all other comparisons were adjusted for multiple tests
by use of Hochberg's modification of the Bonferroni
procedure.18 The determinants of EDD and GTN-induced
dilation were assessed by univariate and
multivariate linear regression analysis, with
age, sex, blood pressure, body mass index, total or LDL
cholesterol level, folate level, homocysteine level, and
vessel size entered as the independent variables. Statistical
significance was inferred at a two-tailed value of
P<.05.
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Results |
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Subjects were aged 41 to 69 years. The fasting total plasma homocysteine levels were 9.9±3.2 and 34.8±8.5 µmol/L (P=.005) in the control and high homocysteine groups, respectively, and plasma folate levels in both groups were normal or high compared with Western standards (49.6±21.3 and 33.0±10.7 nmol/L, respectively; P=.27).11 The control and hyperhomocysteinemic groups were well matched for other basal characteristics, including age, sex, body mass index, blood pressure, lipid profiles, vitamin B12, and vessel size (Table
). No subject had evidence of
vitamin deficiency; the folate level was >10 nmol/L and the
vitamin B12 level was >120 pmol/L in every
case.
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The average degree of reactive hyperemia after cuff release was similar in both groups. In response to this increase in flow, arterial dilation was 10.8±1.7% (range, 7.3% to 13.5%) in the control group and 6.5±1.7% (range, 4.5% to 10%) in the hyperhomocysteinemic subjects (P<.001). By contrast, GTN-induced responses were similar in the two groups (P=.90). On univariate analysis, decreased EDD was significantly associated with high homocysteine level (r=-.63, P<.001) but not with folate level (r=.04, P=.85) nor with any of the other variables measured. On multivariate analysis, decreased EDD was still associated with high homocysteine levels (partial r=-.84, P<.001), independent of the effects of age, sex, body mass index, cholesterol level, folate level, vitamin B12 level, vessel size, or degree of hyperemia (P>.05 for all) (for this multivariate model, R2=.88, F=4.3, P=.008). When similar analyses were performed with GTN response as the dependent variable, neither homocysteine levels (P=.45) nor any other factors were correlated.
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Discussion |
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Homocysteine has been implicated as a pathogenetic factor in the development of arterial disease in a number of in vitro and experimental animal studies that have demonstrated an association between hyperhomocysteinemia and endothelial cell damage.5 6 7 8 In cell culture experiments, addition of homocysteine into the culture medium induces cell detachment from endothelial cell monolayers6 and functional abnormalities in the release of endothelium-derived NO.7 In nonhuman primates, a continuous homocysteine infusion for 3 months has resulted in patchy endothelial desquamation amounting to 10% of the aortic surface,5 and moderate hyperhomocysteinemia induced by methionine feeding has led to abnormal arterial vasomotor activity.8 In humans, homozygous homocystinuria is a rare disorder usually diagnosed in childhood, associated with markedly accelerated atherosclerosis and thrombosis and with endothelial dysfunction in children as young as 4 years old.13 Sporadic hyperhomocysteinemia, however, may be a much more frequent clinical problem because high homocysteine levels have been associated with premature arterial disease in adult life in several epidemiological studies.2 3 4 Despite this, a plausible biological link between spontaneous elevation in serum homocysteine and arterial damage in vivo has not been demonstrated previously.
In the present study of asymptomatic, middle-aged Chinese, we found impairment of arterial EDD in subjects with no identifiable vascular risk factors other than marked hyperhomocysteinemia. In this patient group, high homocysteine levels were not associated with deficiencies of folate or vitamin B12 or with renal failure and therefore probably represented levels at the upper end of a normal population distribution. Recent results from two other groups suggest that hyperhomocysteinemia may also be associated with early arterial injury in white adults.19 20 Because endothelial dysfunction is regarded as a key early event in atherogenesis21 and plays an important role in dynamic plaque behavior in the coronary circulation,22 these findings may have important pathophysiological and clinical implications. The mechanisms whereby hyperhomocysteinemia may account for impaired endothelium-dependent, NO-mediated vasodilatation in humans have not yet been elucidated. Possibilities include physical endothelial cell injury with desquamation,5 6 abnormal interactions between NO and the free thiol moiety of homocysteine,7 and homocysteine-related generation of reactive oxygen species,23 with consequent catabolism of endothelium-derived NO.
Therefore, in otherwise healthy adults, hyperhomocysteinemia may be associated with significant impairment of arterial EDD. Because high homocysteine levels may be treated by relatively simple interventions, such as oral folate, betaine, and/or pyridoxine therapy,24 25 these findings raise the possibility that such treatments may normalize endothelial function by lowering serum homocysteine, with potentially beneficial effects on the atherogenic process. Prospective studies to assess this possibility are currently under way in our institutions and may help elucidate the roles of screening for and treating hyperhomocysteinemia in populations at risk for atherosclerosis.
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Acknowledgments |
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We wish to thank Dr S.K. Kwong of Department of Medicine, the Prince of Wales Hospital in Hong Kong, for examining and helping with enrollment of volunteers.
Received February 24, 1997; revision received April 25, 1997; accepted May 15, 1997.
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 A. Hassan, B. J. Hunt, M. O'Sullivan, R. Bell, R. D'Souza, S. Jeffery, J. M. Bamford, and H. S. Markus Homocysteine is a risk factor for cerebral small vessel disease, acting via endothelial dysfunction Brain, January 1, 2004; 127(1): 212 - 219. [Abstract] [Full Text] [PDF]
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 C. Sauvaget, J. Nagano, N. Allen, and K. Kodama Vegetable and Fruit Intake and Stroke Mortality in the Hiroshima/Nagasaki Life Span Study Stroke, October 1, 2003; 34(10): 2355 - 2360. [Abstract] [Full Text] [PDF]
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X. Zeng, J. Dai, D. G. Remick, and X. Wang Homocysteine Mediated Expression and Secretion of Monocyte Chemoattractant Protein-1 and Interleukin-8 in Human Monocytes Circ. Res., August 22, 2003; 93(4): 311 - 320. [Abstract] [Full Text] [PDF]
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A. Zulli, R. E. Widdop, D. L. Hare, B. F. Buxton, and M. J. Black High Methionine and Cholesterol Diet Abolishes Endothelial Relaxation Arterioscler Thromb Vasc Biol, August 1, 2003; 23(8): 1358 - 1363. [Abstract] [Full Text] [PDF]
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 P. A. Fischer, G. N. Dominguez, L. A. Cuniberti, V. Martinez, J. P. Werba, A. J. Ramirez, and L. D. Masnatta Hyperhomocysteinemia Induces Renal Hemodynamic Dysfunction: Is Nitric Oxide Involved? J. Am. Soc. Nephrol., March 1, 2003; 14(3): 653 - 660. [Abstract] [Full Text] [PDF]
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 M. Coffey, G. K. Crowder, and D. J. Cheek Reducing Coronary Artery Disease by Decreasing Homocysteine Levels Crit. Care Nurse, February 1, 2003; 23(1): 25 - 30. [Full Text] [PDF]
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A. Hassan, B. J. Hunt, M. O'Sullivan, K. Parmar, J. M. Bamford, D. Briley, M. M. Brown, D. J. Thomas, and H. S. Markus Markers of endothelial dysfunction in lacunar infarction and ischaemic leukoaraiosis Brain, February 1, 2003; 126(2): 424 - 432. [Abstract] [Full Text] [PDF]
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 K. Sydow, E. Schwedhelm, N. Arakawa, S. M. Bode-Boger, D. Tsikas, B. Hornig, J. C. Frolich, and R. H. Boger ADMA and oxidative stress are responsible for endothelial dysfunction in hyperhomocyst(e)inemia: effects of L-arginine and B vitamins Cardiovasc Res, January 1, 2003; 57(1): 244 - 252. [Abstract] [Full Text] [PDF]
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 U. Lim and P. A. Cassano Homocysteine and Blood Pressure in the Third National Health and Nutrition Examination Survey, 1988-1994 Am. J. Epidemiol., December 15, 2002; 156(12): 1105 - 1113. [Abstract] [Full Text] [PDF]
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 A. De Bree, W. M. M. Verschuren, D. Kromhout, L. A. J. Kluijtmans, and H. J. Blom Homocysteine Determinants and the Evidence to What Extent Homocysteine Determines the Risk of Coronary Heart Disease Pharmacol. Rev., December 1, 2002; 54(4): 599 - 618. [Abstract] [Full Text] [PDF]
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G. Schnyder, Y. Flammer, M. Roffi, R. Pin, and O. M. Hess Plasma homocysteine levels and late outcome after coronary angioplasty J. Am. Coll. Cardiol., November 20, 2002; 40(10): 1769 - 1776. [Abstract] [Full Text] [PDF]
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 U. Schwab, A. Torronen, L. Toppinen, G. Alfthan, M. Saarinen, A. Aro, and M. Uusitupa Betaine supplementation decreases plasma homocysteine concentrations but does not affect body weight, body composition, or resting energy expenditure in human subjects Am. J. Clinical Nutrition, November 1, 2002; 76(5): 961 - 967. [Abstract] [Full Text] [PDF]
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 K Jensen-Urstad, E Svenungsson, U de Faire, A Silveira, J L Witztum, A Hamsten, and J Frostegard Cardiac valvular abnormalities are frequent in systemic lupus erythematosus patients with manifest arterial disease Lupus, November 1, 2002; 11(11): 744 - 752. [Abstract] [PDF]
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 O. Stanger, H.-J. Semmelrock, W. Wonisch, U. Bos, E. Pabst, and T. C. Wascher Effects of Folate Treatment and Homocysteine Lowering on Resistance Vessel Reactivity in Atherosclerotic Subjects J. Pharmacol. Exp. Ther., October 1, 2002; 303(1): 158 - 162. [Abstract] [Full Text] [PDF]
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 J. Gomez-Cerezo, J. J. Rios Blanco, I. Suarez Garcia, P. Moreno Anaya, P. Garcia Raya, E. Vazquez-Munoz, and F. J. Barbado Hernandez Noninvasive Study of Endothelial Function in White Coat Hypertension Hypertension, September 1, 2002; 40(3): 304 - 309. [Abstract] [Full Text] [PDF]
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 G. Schnyder, M. Roffi, Y. Flammer, R. Pin, and O. M. Hess Effect of Homocysteine-Lowering Therapy With Folic Acid, Vitamin B12, and Vitamin B6 on Clinical Outcome After Percutaneous Coronary Intervention: The Swiss Heart Study: A Randomized Controlled Trial JAMA, August 28, 2002; 288(8): 973 - 979. [Abstract] [Full Text] [PDF]
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F. F. Willems, W. R. M. Aengevaeren, G. H. J. Boers, H. J. Blom, and F. W. A. Verheugt Coronary endothelial function in hyperhomocysteinemia: improvement after treatment with folic acid and cobalamin in patients with coronary artery disease J. Am. Coll. Cardiol., August 21, 2002; 40(4): 766 - 772. [Abstract] [Full Text] [PDF]
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N. Weiss, C. Keller, U. Hoffmann, and J. Loscalzo Endothelial dysfunction and atherothrombosis in mild hyperhomocysteinemia Vascular Medicine, August 1, 2002; 7(3): 227 - 239. [Abstract] [PDF]
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 H Er, C Evereklioglu, T Cumurcu, Y Turkoz, E Ozerol, K Sahin, and S Doganay Serum homocysteine level is increased and correlated with endothelin-1 and nitric oxide in Behcet's disease Br J Ophthalmol, June 1, 2002; 86(6): 653 - 657. [Abstract] [Full Text] [PDF]
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Q. Zhang, X. Zeng, J. Guo, and X. Wang Oxidant stress mechanism of homocysteine potentiating Con A-induced proliferation in murine splenic T lymphocytes Cardiovasc Res, March 1, 2002; 53(4): 1035 - 1042. [Abstract] [Full Text] [PDF]
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J. E Roeters van Lennep, H.T. Westerveld, D.W. Erkelens, and E. E van der Wall Risk factors for coronary heart disease: implications of gender Cardiovasc Res, February 15, 2002; 53(3): 538 - 549. [Abstract] [Full Text] [PDF]
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 E. S Ford, S J. Smith, D. F Stroup, K. K Steinberg, P. W Mueller, and S. B Thacker Homocyst(e)ine and cardiovascular disease: a systematic review of the evidence with special emphasis on case-control studies and nested case-control studies Int. J. Epidemiol., February 1, 2002; 31(1): 59 - 70. [Abstract] [Full Text] [PDF]
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 H. Wang, X. Jiang, F. Yang, G. B. Chapman, W. Durante, N. E. S. Sibinga, and A. I. Schafer Cyclin A transcriptional suppression is the major mechanism mediating homocysteine-induced endothelial cell growth inhibition Blood, February 1, 2002; 99(3): 939 - 945. [Abstract] [Full Text] [PDF]
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N. Weiss, S. Heydrick, Y.-Y. Zhang, C. Bierl, A. Cap, and J. Loscalzo Cellular Redox State and Endothelial Dysfunction in Mildly Hyperhomocysteinemic Cystathionine {beta}-Synthase-Deficient Mice Arterioscler Thromb Vasc Biol, January 1, 2002; 22(1): 34 - 41. [Abstract] [Full Text] [PDF]
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C. H. Pullin, P. A. L. Ashfield-Watt, M. L. Burr, Z. E. Clark, M. J. Lewis, S. J. Moat, R. G. Newcombe, H. J. Powers, J. M. Whiting, and I. F. W. McDowell Optimization of dietary folate or low-dose folic acid supplements lower homocysteine but do not enhance endothelial function in healthy adults, irrespective of the methylenetetrahydrofolate reductase (C677T) genotype J. Am. Coll. Cardiol., December 1, 2001; 38(7): 1799 - 1805. [Abstract] [Full Text] [PDF]
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Q. Zhang, X. Zeng, J. Guo, and X. Wang Effects of homocysteine on murine splenic B lymphocyte proliferation and its signal transduction mechanism Cardiovasc Res, November 1, 2001; 52(2): 328 - 336. [Abstract] [Full Text] [PDF]
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N. Weiss, Y.-Y. Zhang, S. Heydrick, C. Bierl, and J. Loscalzo Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction PNAS, October 12, 2001; (2001) 231428998. [Abstract] [Full Text] [PDF]
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A. Virdis, L. Ghiadoni, H. Cardinal, S. Favilla, P. Duranti, R. Birindelli, A. Magagna, G. Bernini, G. Salvetti, S. Taddei, et al. Mechanisms responsible for endothelial dysfunction induced by fasting hyperhomocystinemia in normotensive subjects and patients with essential hypertension J. Am. Coll. Cardiol., October 1, 2001; 38(4): 1106 - 1115. [Abstract] [Full Text] [PDF]
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 G. Targher, L. Zenari, L. Bertolini, G. Falezza, M. Muggeo, and G. Zoppini Plasma Total Homocysteine Levels Are Associated With von Willebrand Factor, Soluble Intercellular Adhesion Molecule-1, and Soluble Tumor Necrosis Factor-{alpha} Receptors in Young Type 1 Diabetic Patients Without Clinical Evidence of Macrovascular Complications Diabetes Care, August 1, 2001; 24(8): 1496 - 1497. [Full Text] [PDF]
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S. N. Doshi, I. F. W. McDowell, S. J. Moat, D. Lang, R. G. Newcombe, M. B. Kredan, M. J. Lewis, and J. Goodfellow Folate Improves Endothelial Function in Coronary Artery Disease : An Effect Mediated by Reduction of Intracellular Superoxide? Arterioscler Thromb Vasc Biol, July 1, 2001; 21(7): 1196 - 1202. [Abstract] [Full Text] [PDF]
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N. M. de Roos, M. L. Bots, and M. B. Katan Replacement of Dietary Saturated Fatty Acids by Trans Fatty Acids Lowers Serum HDL Cholesterol and Impairs Endothelial Function in Healthy Men and Women Arterioscler Thromb Vasc Biol, July 1, 2001; 21(7): 1233 - 1237. [Abstract] [Full Text] [PDF]
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J. Thambyrajah, M. J. Landray, H. J. Jones, F. J. McGlynn, D. C. Wheeler, and J. N. Townend A randomized double-blind placebo-controlled trial of the effect of homocysteine-lowering therapy with folic acid on endothelial function in patients with coronary artery disease J. Am. Coll. Cardiol., June 1, 2001; 37(7): 1858 - 1863. [Abstract] [Full Text] [PDF]
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P. Clausen, J. S. Jensen, G. Jensen, K. Borch-Johnsen, and B. Feldt-Rasmussen Elevated Urinary Albumin Excretion Is Associated With Impaired Arterial Dilatory Capacity in Clinically Healthy Subjects Circulation, April 10, 2001; 103(14): 1869 - 1874. [Abstract] [Full Text] [PDF]
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A. A Brown and F. B Hu Dietary modulation of endothelial function: implications for cardiovascular disease Am. J. Clinical Nutrition, April 1, 2001; 73(4): 673 - 686. [Abstract] [Full Text] [PDF]
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J. C. Chambers, L. Fusi, I. S. Malik, D. O. Haskard, M. De Swiet, and J. S. Kooner Association of Maternal Endothelial Dysfunction With Preeclampsia JAMA, March 28, 2001; 285(12): 1607 - 1612. [Abstract] [Full Text] [PDF]
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V. Gallai, V. Caso, M. Paciaroni, G. Cardaioli, E. Arning, T. Bottiglieri, and L. Parnetti Mild Hyperhomocyst(e)inemia : A Possible Risk Factor for Cervical Artery Dissection Stroke, March 1, 2001; 32(3): 714 - 718. [Abstract] [Full Text] [PDF]
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Z. Bagi, Z. Ungvari, L. Szollar, and A. Koller Flow-Induced Constriction in Arterioles of Hyperhomocysteinemic Rats Is Due to Impaired Nitric Oxide and Enhanced Thromboxane A2 Mediation Arterioscler Thromb Vasc Biol, February 1, 2001; 21(2): 233 - 237. [Abstract] [Full Text] [PDF]
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M. K. Al-Obaidi, P. J. Stubbs, P. Collinson, R. Conroy, I. Graham, and M. I. M. Noble Elevated homocysteine levels are associated with increased ischemic myocardial injury in acute coronary syndromes J. Am. Coll. Cardiol., October 1, 2000; 36(4): 1217 - 1222. [Abstract] [Full Text] [PDF]
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K. S. Woo, P. Chook, H. C. Leong, X. S. Huang, and D. S. Celermajer The impact of heavy passive smoking on arterial endothelial function in modernized Chinese J. Am. Coll. Cardiol., October 1, 2000; 36(4): 1228 - 1232. [Abstract] [Full Text] [PDF]
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L. M. Title, P. M. Cummings, K. Giddens, J. J. Genest Jr, and B. A. Nassar Effect of folic acid and antioxidant vitamins on endothelial dysfunction in patients with coronary artery disease J. Am. Coll. Cardiol., September 1, 2000; 36(3): 758 - 765. [Abstract] [Full Text] [PDF]
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J. Thambyrajah, M. J. Landray, F. J. McGlynn, H. J. Jones, D. C. Wheeler, and J. N. Townend Does Folic Acid Decrease Plasma Homocysteine and Improve Endothelial Function in Patients With Predialysis Renal Failure? Circulation, August 22, 2000; 102(8): 871 - 875. [Abstract] [Full Text] [PDF]
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P. J. Stubbs, M. K. Al-Obaidi, R. M. Conroy, MusB, P. O. Collinson, MRCPath, I. M. Graham, FRCPI, and M. I. M. Noble Effect of Plasma Homocysteine Concentration on Early and Late Events in Patients With Acute Coronary Syndromes Circulation, August 8, 2000; 102(6): 605 - 610. [Abstract] [Full Text] [PDF]
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T. Omland, A. Samuelsson, M. Hartford, J. Herlitz, T. Karlsson, B. Christensen, and K. Caidahl Serum Homocysteine Concentration as an Indicator of Survival in Patients With Acute Coronary Syndromes Arch Intern Med, June 26, 2000; 160(12): 1834 - 1840. [Abstract] [Full Text] [PDF]
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J Thambyrajah and J.N Townend Homocysteine and atherothrombosis--mechanisms for injury Eur. Heart J., June 2, 2000; 21(12): 967 - 974. [PDF]
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A. Gottsater, I. Anwaar, K.-F. Eriksson, I. Mattiasson, F. Lindgarde, and A. Gottsater Homocysteine Is Related to Neopterin and Endothelin-1 in Plasma of Subjects with Disturbed Glucose Metabolism and Reference Subjects Angiology, June 1, 2000; 51(6): 489 - 497. [Abstract] [PDF]
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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. [Abstract] [Full Text] [PDF]
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D. W. Jacobsen Hyperhomocysteinemia and Oxidative Stress : Time for a Reality Check? Arterioscler Thromb Vasc Biol, May 1, 2000; 20(5): 1182 - 1184. [Full Text] [PDF]
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Z. Ungvari, E. Sarkadi-Nagy, Z. Bagi, L. Szollar, and A. Koller Simultaneously Increased TxA2 Activity in Isolated Arterioles and Platelets of Rats With Hyperhomocysteinemia Arterioscler Thromb Vasc Biol, May 1, 2000; 20(5): 1203 - 1208. [Abstract] [Full Text] [PDF]
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K. S. Woo, J. E. Sanderson, Y. Y. Sun, P. Chook, A. S. P. Cheung, L. T. Chan, C. Metreweli, Y. I. Lolin, and D. S. Celermajer Hyperhomocyst(e)inemia Is a Risk Factor for Arterial Endothelial Dysfunction in Humans Circulation, March 28, 2000; 101 (12): e116 - e116. [Full Text] [PDF]
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F. H. de Man, A. W. E. Weverling-Rijnsburger, A. van der Laarse, A. H. M. Smelt, J. W. Jukema, and G. J. Blauw Not Acute but Chronic Hypertriglyceridemia Is Associated With Impaired Endothelium-Dependent Vasodilation : Reversal After Lipid-Lowering Therapy by Atorvastatin Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 744 - 750. [Abstract] [Full Text] [PDF]
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C.-L. Chao, T.-L. Kuo, and Y.-T. Lee Effects of Methionine-Induced Hyperhomocysteinemia on Endothelium-Dependent Vasodilation and Oxidative Status in Healthy Adults Circulation, February 8, 2000; 101(5): 485 - 490. [Abstract] [Full Text] [PDF]
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 M. R. Rinder, R. J. Spina, and A. A. Ehsani Enhanced endothelium-dependent vasodilation in older endurance-trained men J Appl Physiol, February 1, 2000; 88(2): 761 - 766. [Abstract] [Full Text] [PDF]
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D. Lang, M. B. Kredan, S. J. Moat, S. A. Hussain, C. A. Powell, M. F. Bellamy, H. J. Powers, and M. J. Lewis Homocysteine-Induced Inhibition of Endothelium-Dependent Relaxation in Rabbit Aorta : Role for Superoxide Anions Arterioscler Thromb Vasc Biol, February 1, 2000; 20(2): 422 - 427. [Abstract] [Full Text] [PDF]
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K. S. Woo, P. Chook, Y. I. Lolin, J. E. Sanderson, C. Metreweli, and D. S. Celermajer Folic acid improves arterial endothelial function in adults with hyperhomocystinemia J. Am. Coll. Cardiol., December 1, 1999; 34(7): 2002 - 2006. [Abstract] [Full Text] [PDF]
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J. C. Chambers, O. A. Obeid, and J. S. Kooner Physiological Increments in Plasma Homocysteine Induce Vascular Endothelial Dysfunction in Normal Human Subjects Arterioscler Thromb Vasc Biol, December 1, 1999; 19(12): 2922 - 2927. [Abstract] [Full Text] [PDF]
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V. Schachinger, M. B. Britten, M. Elsner, D. H. Walter, I. Scharrer, and A. M. Zeiher A Positive Family History of Premature Coronary Artery Disease Is Associated With Impaired Endothelium-Dependent Coronary Blood Flow Regulation Circulation, October 5, 1999; 100(14): 1502 - 1508. [Abstract] [Full Text] [PDF]
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K. J. Harjai Potential New Cardiovascular Risk Factors: Left Ventricular Hypertrophy, Homocysteine, Lipoprotein(a), Triglycerides, Oxidative Stress, and Fibrinogen Ann Intern Med, September 7, 1999; 131(5): 376 - 386. [Abstract] [Full Text] [PDF]
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G. W. de Valk-de Roo, C. D.A. Stehouwer, J. Lambert, C. G. Schalkwijk, M. J. van der Mooren, C. Kluft, and C. Netelenbos Plasma Homocysteine Is Weakly Correlated with Plasma Endothelin and von Willebrand Factor but not with Endothelium-dependent Vasodilatation in Healthy Postmenopausal Women Clin. Chem., August 1, 1999; 45(8): 1200 - 1205. [Abstract] [Full Text] [PDF]
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S. N. Doshi, J. Goodfellow, M. J. Lewis, and I. F.W. McDowell Homocysteine and endothelial function Cardiovasc Res, June 1, 1999; 42(3): 578 - 582. [Full Text] [PDF]
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B. Kristensen, J. Malm, T. K. Nilsson, J. Hultdin, B. Carlberg, G. Dahlen, and T. Olsson Hyperhomocysteinemia and Hypofibrinolysis in Young Adults With Ischemic Stroke Stroke, May 1, 1999; 30(5): 974 - 980. [Abstract] [Full Text] [PDF]
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J. C. Chambers, A. McGregor, J. Jean-Marie, O. A. Obeid, and J. S. Kooner Demonstration of Rapid Onset Vascular Endothelial Dysfunction After Hyperhomocysteinemia : An Effect Reversible With Vitamin C Therapy Circulation, March 9, 1999; 99(9): 1156 - 1160. [Abstract] [Full Text] [PDF]
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D. E. Gutstein and V. Fuster Pathophysiology and clinical significance of atherosclerotic plaque rupture Cardiovasc Res, February 1, 1999; 41(2): 323 - 333. [Abstract] [Full Text] [PDF]
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M.F. Bellamy, I.F.W. McDowell, M.W. Ramsey, M. Brownlee, C. Bones, R.G. Newcombe, and M.J. Lewis Hyperhomocysteinemia After an Oral Methionine Load Acutely Impairs Endothelial Function in Healthy Adults Circulation, November 3, 1998; 98(18): 1848 - 1852. [Abstract] [Full Text] [PDF]
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D. W. Jacobsen Homocysteine and vitamins in cardiovascular disease Clin. Chem., August 1, 1998; 44(8): 1833 - 1843. [Abstract] [Full Text] [PDF]
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A. R. Folsom, F. J. Nieto, P. G. McGovern, M. Y. Tsai, M. R. Malinow, J. H. Eckfeldt, D. L. Hess, and C. E. Davis Prospective Study of Coronary Heart Disease Incidence in Relation to Fasting Total Homocysteine, Related Genetic Polymorphisms, and B Vitamins : The Atherosclerosis Risk in Communities (ARIC) Study Circulation, July 21, 1998; 98(3): 204 - 210. [Abstract] [Full Text] [PDF]
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N. Weiss, Y.-Y. Zhang, S. Heydrick, C. Bierl, and J. Loscalzo Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction PNAS, October 23, 2001; 98(22): 12503 - 12508. [Abstract] [Full Text] [PDF]
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