Lack of association between asymmetric dimethylarginine and in vivo microvascular and macrovascular endothelial function in patients with rheumatoid arthritis

Clinical and Experimental Rheumatology

Volumn 30, Issue 3, 2012, Pages 388-396

  Sandoo, Aamer ^a,b   Dimitroulas, Theodoros ^a   Veldhuijzen van Zanten, J J C S ^a,b   Smith, Jacqueline P ^a   Metsios, George S ^a   Nightingale, Peter ^c   Stavropoulos Kalinoglou, Antonios ^a   Kitas, George D ^a,d  

^a RUSSELLS HALL HOSPITAL   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

ADMA; Cardiovascular disease; Endothelial function; Rheumatoid arthritis

Indexed keywords

ACETYLCHOLINE; GLYCERYL TRINITRATE; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; NITROPRUSSIDE SODIUM;

ADULT; ARTERIAL STIFFNESS; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE DURATION; DISEASE SEVERITY; ENDOTHELIAL DYSFUNCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; IN VIVO STUDY; IONTOPHORESIS; LASER DOPPLER FLOWMETRY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; VASODILATATION;

ADULT; AGED; ARGININE; ARTHRITIS, RHEUMATOID; BIOLOGICAL MARKERS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MICROVESSELS; MIDDLE AGED; NITRIC OXIDE; RISK FACTORS; SEVERITY OF ILLNESS INDEX; VASCULAR DISEASES; VASCULAR STIFFNESS;

EID: 84864777632     PISSN: 0392856X     EISSN: 1593098X     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Kitas Gd, Erb N: Tackling Ischaemic Heart disease in rheumatoid arthritis. Rheumatology 2003; 42: 607-13.
2. Douglas KMJ, Pace AV, Treharne GJ et al.: Excess Recurrent Cardiac Events in Rheumatoid Arthritis Patients with Acute Coronary Syndrome. Ann Rheum Dis 2005; 65: 348-53.
3. Panoulas VF, Metsios GS, Pace AV et al.: Hypertension in rheumatoid arthritis. Rheumatology 2008; 47: 1286-98.
4. Del Rincón ID, Williams K, Stern MP, Freeman GL, Escalante A: High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum 2001; 44: 2737-45.
5. Lutzky V, Hannawi S, Thomas R: Cells of the synovium in rheumatoid arthritis. Dendritic cells. Arthritis Res Ther 2007; 9: 219.
6. Sattar N, Mccarey DW, Capell H, Mcinnes IB: Explaining how "high-grade" systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 2003; 108: 2957-63.
7. Hannawi S, Marwick TH, Thomas R: Inflammation predicts accelerated brachial arterial wall changes in patients with recentonset rheumatoid arthritis. Arthritis Res Ther 2009; 11: R51.
8. Gonzalez-Gay MA, Gonzalez-Juanatey C, Martin J: Inflammation and endothelial dysfunction in rheumatoid arthritis. Clin Exp Rheumatol 2006; 24: 115-7.
9. Vaudo G, Marchesi S, Gerli R et al.: Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity. Ann Rheum Dis 2004; 63: 31-5.
10. Bergholm R, Leirisalo-Repo M, Vehkavaara S, Makimattila S, Taskinen MR, Yki-Jarvinen H: Impaired responsiveness to NO in newly diagnosed patients with rheumatoid arthritis. Arterioscler Thromb Vasc Biol 2002; 22: 1637-41.
11. Van Doornum S, Mccoll G, Jenkins A: Screening for atherosclerosis in patients with rheumatoid arthritis. Arthritis Rheum 2003; 48: 72-80.
12. Wallberg-Jonsson S, Caidahl K, Klintland N, Nyberg G, Rantapaadahlqvist S: Increased arterial stiffness and indication of endothelial dysfunction in long-standing rheumatoid arthritis. Scand J Rheumatol 2008; 37:1-5.
13. Klocke R, Cockcroft JR, Taylor GJ, Hall IR, Blake DR: Arterial stiffness and central blood pressure, as determined by pulse wave analysis, in rheumatoid arthritis. Ann Rheum Dis 2003; 62: 414-18.
14. Krzyzanowska K, Mittermayer F, Wolzt M, Schernthaner G: Asymmetric dimethylarginine predicts cardiovascular events in patients with type 2 diabetes. Diabetes Care 2007; 30: 1834-9.
15. Meinitzer A, Seelhorst U, Wellnitz B et al.: Asymmetrical dimethylarginine independently predicts total and cardiovascular mortality in individuals with angiographic coronary artery disease (the Ludwigshafen Risk and Cardiovascular Health study). Clin Chem 2007; 53: 273-83.
16. Kielstein JT, Böger RH, Bode-Böger SM et al.: Asymmetric dimethylarginine plasma concentrations differ in patients with endstage renal disease: relationship to treatment method and atherosclerotic disease. J Am Soc Nephrol 1999; 10: 594-600.
17. Surdacki A, Martens-Lobenhoffer J, Wloch A et al.: Elevated plasma asymmetric dimethyl-L-arginine levels are linked to endothelial progenitor cell depletion and carotid atherosclerosis in rheumatoid arthritis. Arthritis Rheum 2007; 56: 809-19.
18. Sari I, Kebapcilar L, Alacacioglu A et al.: Increased levels of asymmetric dimethylarginine (ADMA) in patients with ankylosing spondylitis. Intern Med 2009; 48: 1363-8.
19. Dimitroulas T, Giannakoulas G, Papadopoulou K et al.: Early detection of cardiacinvolvement in systemic sclerosis assessed by tissue-Doppler echocardiography: relationship with neurohormonal activation and endothelial dysfunction. J Rheumatol 2010; 37: 993-9.
20. Dimitroulas T, Giannakoulas G, Sfetsios T et al.: Asymmetrical dimethylarginine in systemic sclerosis-related pulmonary arterial hypertension. Rheumatology 2008; 47: 1682-1685.
21. Bultink IE, Teerlink T, Heijst JA, Dijkmans BA, Voskuyl AE: Raised plasma levels of asymmetric dimethylarginine are associated with cardiovascular events, disease activity, and organ damage in patients with systemic lupus erythematosus. Ann Rheum Dis 2005; 64: 1362-1365.
22. Turiel M, Atzeni F, Tomasoni L et al.: Non invasive assessment of coronary flow reserve and ADMA levels: a case-control study of early rheumatoid arthritis patients. Rheumatology 2009; 48: 834-9.
23. Arnett FC, Edworthy SM, Bloch DA et al.: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31: 315-24.
24. Prevoo ML, Van't Hof MA, Kuper HH, Van Leeuwen MA, Van De Putte LB, Van Riel PL: Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients withrheumatoid arthritis. Arthritis Rheum 1995; 38: 44-48.
25. Kirwan JR, Reeback JS: Stanford Health Assessment Questionnaire modified to assess disability in British patients with rheumatoid arthritis. Br J Rheumatol 1986; 25: 206-9.
26. Wilkinson IB, Hall IR, Maccallum H et al.: Pulse-wave analysis: clinical evaluation of a noninvasive, widely applicable method for assessing endothelial function. Arterioscler Thromb Vasc Biol 2002; 22: 147-2.
27. Turner J, Belch JJ, Khan F: Current concepts in assessment of microvascular endothelial function using laser Doppler imaging and iontophoresis. Trends Cardiovasc Med 2008; 18: 109-16.
28. Sandoo A, Veldhuijzen Van Zanten JJ, Metsios GS, Carroll D, Kitas GD: The endothelium and its role in regulating vascular tone. Open Cardiovasc Med J 2010; 4: 302-12.
29. Corretti MC, Anderson TJ, Benjamin EJ et al.: International Brachial Artery Reactivity Task Force. Guidelines for the ultrasound assessment of endothelial-dependent flowmediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39: 257-255.
30. Sydow K, Münzel T: ADMA and oxidative stress. Atheroscler Suppl 2003; 4: 41-51.
31. Böger RH, Sydow K, Borlak J et al.: LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosylmethionine-dependent methyltransferases. Circ Res 2000; 87: 99-105.
32. Ito A, Tsao PS, Adimoolam S, Kimoto M, Ogawa T, Cooke JP: Novel mechanism for endothelial dysfunction: dysregulation of dimethylarginine dimethylaminohydrolase. Circulation 1999; 99: 3092-5.
33. Millatt LJ, Whitley GS, LI D, Leiper JM, Siragy HM, Carey RM, Johns RA: Evidence for dysregulation of dimethylarginine dimethylaminohydrolase I in chronic hypoxia-induced pulmonary hypertension. Circulation 2003; 108: 1493-1498.
34. Middleton J, Americh L, Gayon R et al.: Endothelial cell phenotypes in the rheumatoid synovium: activated, angiogenic, apoptotic and leaky. Arthritis Res Ther 2004; 6: 60-72.
35. Turiel M, Tomasoni L, Sitia S et al.: Effects of long-term disease-modifying antirheumatic drugs on endothelial function in patients with early rheumatoid arthritis. Cardiovasc Ther 2010; 10: 1-12.
36. Toms TE, Panoulas VF, Douglas KM et al.: Statin use in rheumatoid arthritis in relation to actual cardiovascular risk: evidence for substantial undertreatment of lipid-associated cardiovascular risk? Ann Rheum Dis 2010; 69: 683-688.
37. Wagner AH, Köhler T, Rückschloss U, Just I, Hecker M: Improvement of nitric oxide-dependent vasodilatation by HMGCoA reductase inhibitors through attenuation of endothelial superoxide anion formation. Arterioscler Thromb Vasc Biol 2000; 20: 61-69.
38. Jiang JL, Wang S, Li NS, Zhang XH, Deng HW, Li YJ: The inhibitory effect of simvastatin on the ADMA-induced inflammatory reaction is mediated by MAPK pathways in endothelial cells. Biochem Cell Biol 2007; 85: 66-77.
39. Jiang JL, Jiang DJ, Tang YH, Li NS, Deng HW, Li YJ: Effect of simvastatin on endothelium-dependent vaso-relaxation and endogenous nitric oxide synthase inhibitor. Acta Pharmacol Sin 2004; 25: 893-901.
40. Päivä H, Laakso J, Lehtimäki T, Isomustajärvi M, Ruokonen I, Laaksonen R: Effect of high-dose statin treatment on plasma concentrations of endogenous nitric oxide synthase inhibitors. J Cardiovasc Pharmacol 2003; 41: 219-222.
41. Surdacki A, Nowicki M, Sandmann J et al.: Reduced urinary excretion of nitric oxide metabolites and increased plasma levels of asymmetric dimethylarginine in men with essential hypertension. J Cardiovasc Pharmacol 1999, 33: 652-658.
42. Jiang JL, Zhu HQ, Chen Z, Xu HY, LI YJ: Angiotensin-converting enzyme inhibitors prevent LDL-induced endothelial dysfunction by reduction of asymmetric dimethylarginine level. Int J Cardiol 2005; 101: 153-155.
43. Sandoo A, Veldhuijzen Van Zanten JJ Metsios GS, Carroll D, Kitas GD: Vascular function and morphology in rheumatoid arthritis: a systematic review. Rheumatology (Oxford) 2011; 50: 2125-2139.
44. Kemény-Beke A, Gesztelyi R, Bodnár N et al.: Increased production of asymmetric dimethylarginine (ADMA) in ankylosing spondylitis: Association with other clinical and laboratory parameters. Joint Bone Spine 2011; 78: 184-187.
45. Antoniades C, Demosthenous M, Tousoulis D et al.: Role of asymmetrical dimethylarginine in inflammation-induced endothelial dysfunction in human atherosclerosis. Hypertension 2011; 58: 93-98.
46. Yilmaz MI, Sonmez A, Saglam M et al.: ADMA levels correlate with proteinuria, secondary amyloidosis, and endothelial dysfunction. J Am Soc Nephrol 2008; 19: 388-95.
47. Vladimirova-Kitova L, Deneva T, Angelova E, Nikolov F, Marinov B, Mateva N: Relationship of asymmetric dimethylarginine with flow-mediated dilatation in subjects with newly detected severe hypercholesterolemia. Clin Physiol Funct Imaging 2008; 28: 417-425.
48. Sibal L, Agarwal SC, Schwedhelm E, Lüneburg N, Böger RH, Home PD: A study of endothelial function and circulating asymmetric dimethylarginine levels in people with Type 1 diabetes without macrovascular disease or microalbuminuria. Cardiovasc Diabetol 2009; 8: 27.
49. Stamatelopoulos KS, Kitas GD, Papamichael CM et al.: Atherosclerosis in rheumatoid arthritis versus diabetes. a comparative study. Arterioscler Thromb Vasc Biol 2009; 29: 1702-1708.
50. Peters MJ, Van Halm VP, Voskuyl AE et al.: Does rheumatoid arthritis equal diabetes mellitus as an independent risk factor for cardiovascular disease? A prospective study. Arthritis Rheum 2009; 61: 1571-1579.
51. Perna M, Roman MJ, Alpert DR et al.: Relationship of asymmetric dimethylarginine and homocysteine to vascular aging in systemic lupus erythematosus patients. Arthritis Rheum 2010; 62: 1718-1722.
52. Kiani AN, Mahoney JA, Petri M: Asymmetric dimethylarginine is a marker of poor prognosis and coronary calcium in systemic lupus erythematosus. J Rheumatol 2007; 34: 1502-1505.
53. Mäki-Petäjä KM, Cheriyan J, Booth AD et al.: Inducible nitric oxide synthase activity is increased in patients with rheumatoid arthritis and contributes to endothelial dysfunction. Int J Cardiol 2008; 129: 399-405.
54. Gonzalez-Gay MA, Llorca J, Palominomorales R et al.: Influence of nitric oxide synthase gene polymorphisms on the risk of cardiovascular events in rheumatoid arthritis. Clin Exp Rheumatol 2009; 27: 116-119.
55. Brenol CV, Chies JA, Brenol JC, Xavier RM: Role of endothelial nitric oxide synthase (eNOS) polymorphisms in cardiovascular disease and rheumatoid arthritis. Clin Exp Rheumatol 2010; 28: 584; author reply 584-585.
56. García-Bermúdez M, González-Juanatey C, Rodríguez-Rodríguez L et al.: Lack of association of NAMPT rs9770242 and rs59744560 polymorphisms with disease susceptibility and cardiovascular risk in patients with rheumatoid arthritis. Clin Exp Rheumatol 2011; 29: 681-688.
57. Gonzalez-Gay MA, Gonzalez-Juanatey C, Rodriguez-Rodriguez L et al.: Lack of association between adipokines and ghrelin and carotid intima-media thickness in patients with severe rheumatoid arthritis. Clin Exp Rheumatol 2011; 29: 358-359.
58. Ter Avest E, Stalenhoef AF, De Graaf J: What is the role of non-invasive measurements of atherosclerosis in individual cardiovascular risk prediction? Clin Sci 2007; 112: 507-11.
59. Lundman P, Eriksson MJ, Stühlinger M, Cooke JP, Hamsten A, Tornvall P: Mild-to-moderate hypertriglyceridemia in young men is associated with endothelial dysfunction and increased plasma concentrations of asymmetric dimethylarginine. J Am Coll Cardiol 2001; 38: 111-116.