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Long-Term N-Acetylcysteine and L-Arginine Administration Reduces Endothelial Activation and Systolic Blood Pressure in Hypertensive Patients with Type 2 Diabetes

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Long-Term N-Acetylcysteine and L-Arginine Administration Reduces Endothelial Activation and Systolic Blood Pressure in Hypertensive Patients with Type 2 Diabetes Emerging Treatments and Technologies ORIGINAL ARTICLE Long-Term N-Acetylcysteine and L-Arginine Administration Reduces Endothelial Activation and Systolic Blood Pressure in Hypertensive Patients With Type 2 Diabetes 1 1 VALENTINO MARTINA, MD PAOLA MASSARENTI, MD ardiovascular complications repre- 1 1 ANDI MASHA, MD FABIO SETTANNI, PHD sent 80% of the causes of death in 1 2 VALENTINA RAMELLA GIGLIARDI, MD LARA DELLA CASA, PHD 1 patients with type 2 diabetes. Several OREDANA ROCATO MD 2 C L B , STEFANIA BERGAMINI, PHD causes may explain this mortality excess. 3 2 ENZO MANZATO, MD, PHD NNA ANNONE MD, PHD 1 A I , Among these, the decreased availability of ARRIGO BERCHIO, MD nitric oxide (NO) has increasingly gained credit. In fact, reduced NO availability has been demonstrated not only in diabe- OBJECTIVE — Reactive oxygen and nitric oxide (NO) have recently been considered to be tes (1) but also in other diseases, such as involved in the cardiovascular complications of patients with type 2 diabetes, as NO is thought atherosclerosis and hypertension, known to lose its beneficial physiological effects in the presence of oxygen radicals. For this reason, we to be associated with increased mortality tested the effects of L-arginine (ARG) and N-acetylcysteine (NAC) administration in increasing due to cardiovascular causes (2,3). NO is NO bioavailability by reducing free radical formation. crucial for regulating the vascular tone RESEARCH DESIGN AND METHODS — A double-blind study was performed on 24 and maintaining the intrinsic thrombore- male patients with type 2 diabetes and hypertension divided into two groups of 12 patients that sistant and atheroprotective properties of randomly received either an oral supplementation of placebo or NAC ϩ ARG for 6 months. the vascular wall (4). NO production by constitutive NO RESULTS — The NAC ϩ ARG treatment caused a reduction of both systolic (P Ͻ 0.05) and synthase (cNOS) is mainly dependent on diastolic (P Ͻ 0.05) mean arterial blood pressure, total cholesterol (P Ͻ 0.01), LDL cholesterol the availability of L-arginine (ARG) (5). (P Ͻ 0.005), oxidized LDL (P Ͻ 0.05), high-sensitive C-reactive protein (P Ͻ 0.05), intracellular Several studies have demonstrated that adhesion molecule (P Ͻ 0.05), vascular cell adhesion molecule (P Ͻ 0.01), nitrotyrosine (P Ͻ ARG infusion is able to improve endothe- 0.01), fibrinogen (P Ͻ 0.01), and plasminogen activator inhibitor-1 (P Ͻ 0.05), and an improve- lial function in normal subjects and pa- ment of the intima-media thickness during endothelial postischemic vasodilation (P Ͻ 0.02). tients with coronary heart disease and Ͻ HDL cholesterol increased (P 0.05). No changes in other parameters studied were observed. hypertension (6), but the results, al- though encouraging, are not conclusive, CONCLUSIONS ϩ — NAC ARG administration seems to be a potential well-tolerated an- probably because of the short-term effects tiatherogenic therapy because it improves endothelial function in hypertensive patients with of ARG intravenous administration. Oral type 2 diabetes by improving NO bioavailability via reduction of oxidative stress and increase of NO production. Our study’s results give prominence to its potential use in primary and second- ARG has a longer half-life and longer- ary cardiovascular prevention in these patients. term effects than ARG given intra- arterially or intravenously so that in long- Diabetes Care 31:940–944, 2008 term health maintenance or symptoms management the oral route would be pre- ●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●● ferred. Unfortunately, studies in diabetic patients are not so widely positive, since From the 1Department of Internal Medicine, University of Torino, Torino, Italy; the 2Department of Bio- medical Sciences, University of Modena and Reggio Emilia, Modena, Italy; and the 3Department of Medical oral ARG does not improve endothelial and Surgical Sciences, University of Padova, Padova, Italy. function (7). Corresponding author: Valentino Martina, MD, Department of Internal Medicine, University of Torino, It is well known that thiols are active Corso Dogliotti 14, I-10121 Torino, Italy. E-mail: [email protected]. intermediates in the NO pathway (8). Ex- Received for publication 7 December 2007 and accepted in revised form 2 February 2008. Published ahead of print at http://care.diabetesjournals.org on 11 February 2008. DOI: 10.2337/dc07- isting data document an increased free 2251. radical production in diabetes and hyper- Abbreviations: ABP, arterial blood pressure; ABPM, ambulatory blood pressure monitoring; ADMA, tension with a consequent decrease in asymmetrical dimethyl-arginine; ARG, L-arginine; hs-CRP, high-sensitive C-reactive protein; sGC, soluble thiol levels. In this situation, NO reacts Ј Ј guanylyl cyclase; cGMP, intracellular guanosine 3 ,5 -cyclic monophosphate; GSH, glutathione; GSSG, with the superoxide anion and to a lesser oxidized glutathione; HPLC, high-performance liquid chromatography; ICAM, intercellular adhesion mol- ecule; IL-6, interleukin-6; IMT, intima-media thickness; ox-LDL, oxidized LDL; NAC, N-acetylcysteine; extent with thiols so that the beneficial cNOS, constitutive NO synthase; PAI-1, plasminogen activator inhibitor-1; ROS, reactive oxygen species; effects of NO are lost. We might suppose SDMA, symmetrical dimethyl-arginine; TNF-␣, tumor necrosis factor-␣; VCAM, vascular cell adhesion that in patients with diabetes, diminished molecule. NO availability and the failure to amelio- © 2008 by the American Diabetes Association. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby rate NO availability after oral ARG sup- marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. plementation could be attributed to this 940 DIABETES CARE, VOLUME 31, NUMBER 5, MAY 2008 Martina and Associates mechanism. Accordingly, we previously overlapping in terms of mean age (62.5 SDMA were determined using an HPLC demonstrated that, in type 2 diabetic pa- [95% CI 59.3–74.5] vs. 67.0 years [51.0– assay (Waters, Milford, MA). Normal sub- tients, a short-term intramuscular admin- 69.7]) and BMI (27.6 [23.6–38.9] vs. jects evaluated in a previous study istration of glutathione (GSH) is able to 28.5 kg/m2 [25.1–38.4]). Group A pa- showed the following mean values for increase NO availability (9). tients received placebo (compounds ARG, ADMA, and SDMA: 105 Ϯ 6.1, Based on these observations, we car- identical in appearance to ARG and NAC) 1.41 Ϯ 0.2, and 0.68 Ϯ 0.07 ␮mol/l, re- ried out a study where ARG and N-acetyl- for 6 months, while group B patients re- spectively (10). cysteine (NAC) were administered ceived NAC (600 mg Acetilcisteina, one Nitrites/nitrates were measured si- together in patients with type 2 diabetes tablet twice a day) plus ARG (1,200 mg multaneously: nitrates were first con- and hypertension: ARG was administered Zentrum, one vial a day) per os. Compli- verted to nitrites by means of enzymatic to enhance NO production while NAC ance was checked by pill and vial counts. conversion, then total nitrites were mea- was administered to ameliorate antioxi- No adverse effects were noted during the sured in the sample using the Griess re- dant defense and increase intracellular ni- treatment. There was one dropout in each agent. The concentration of nitrites in trosothiol concentration, thus increasing group, both not for medical reasons. samples was calculated by comparison NO availability. In all subjects, before and after 6 with a standard curve of sodium nitrite months of treatment/placebo, blood sam- (Sigma-Aldrich, Milan, Italy). Normal RESEARCH DESIGN AND ples were obtained in order to evaluate value Ϯ SEM was 20.1 Ϯ 4.3 mmol/l. METHODS — The study was ap- A1C, total, HDL, and LDL cholesterol, ox- GSH and GSSG in erythrocytes were proved by the ethics committee at our in- idized LDL (ox-LDL), triglycerides, ratio determined by HPLC after a derivatisa- stitution, and written informed consent was of reduced GSH to oxidized GSH (GSSG) tion of hemolysed samples using a fluo- obtained from all recruited subjects. It in erythrocytes, nitrites/nitrates, asym- rescence detector (Varian 9070). GSSG wasarandomized,double-blind,placebo- metrical and symmetrical dimethyl- was calculated as the difference between controlled small-scale study of 6 months. arginine (ADMA and SDMA, respec- total and reduced GSH. Male patients (n ϭ 24, median age 64 tively), nitrotyrosine, arginine, homocys- Plasma levels of nitrotyrosine were as- years [95% CI 51–74 ]) with type 2 dia- teine, high-sensitive C-reactive protein sessed by ELISA (HyCult Biotechnology); betes and hypertension treated with oral (hs-CRP), interleukin-6 (IL-6), tumor ne- the normal range was 0–120 ␮mol/l. hypoglycemic and antihypertensive crosis factor-␣ (TNF-␣), intercellular and Plasma levels of homocysteine were de- drugs were enrolled. All the subjects were vascular cell adhesion molecules (ICAM termined by EIA (Axis-Shield Diagnos- recruited from the outpatient clinic of the and VCAM, respectively), plasminogen ac- tics, Dundee, U.K.); the normal range was Diabetic Centre of the Division of Endo- tivator inhibitor-1 (PAI-1), and fibrinogen. 3–37 ␮mol/l. crinology of the University of Turin, Italy. Moreover, before and after 6 months of Serum levels of hs-CRP (ng/ml) were Only male subjects were selected to treatment, the patients underwent an ABPM measured with a high-sensitive ELISA avoid interferences on NO
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