Advanced glycation endproducts are increased in rheumatoid arthritis patients with controlled disease

Arthritis Research and Therapy

Volumn 13, Issue 6, 2011, Pages

  de Groot, Lodewijk ^a   Hinkema, Helmy ^a   Westra, Johanna ^a   Smit, Andries J ^a   Kallenberg, Cees G M ^a   Bijl, Marc ^a   Posthumus, Marcel D ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Advanced glycation end products; Atherosclerosis; Endothelial cell activation; Endothelial dysfunction; Intima media thickness; Rheumatoid arthritis

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CHOLESTEROL; DISEASE MODIFYING ANTIRHEUMATIC DRUG; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; METHOTREXATE; THROMBOMODULIN; TRIACYLGLYCEROL; VASCULAR CELL ADHESION MOLECULE 1; VON WILLEBRAND FACTOR; BIOLOGICAL MARKER; C REACTIVE PROTEIN;

ADULT; AGED; ARTERIAL WALL THICKNESS; ARTHROPATHY; ARTICLE; ATHEROSCLEROSIS; AUTOFLUORESCENCE; BLOOD VESSEL PARAMETERS; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ACTIVITY; DISEASE CONTROL; DISEASE DURATION; DISEASE SEVERITY; ELASTICITY; ENDOTHELIAL DYSFUNCTION; FEMALE; GLUCOSE BLOOD LEVEL; HUMAN; HYPERTENSION; MALE; RHEUMATOID ARTHRITIS; SCORING SYSTEM; SEX DIFFERENCE; SMALL ARTERY ELASTICITY; SMOKING; TRIACYLGLYCEROL BLOOD LEVEL; BLOOD; CASE CONTROL STUDY; JOINT; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOLOGY; QUESTIONNAIRE; RISK FACTOR; SEVERITY OF ILLNESS INDEX; STATISTICAL MODEL; VASCULAR ENDOTHELIUM;

ADULT; AGED; ARTHRITIS, RHEUMATOID; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CAROTID INTIMA-MEDIA THICKNESS; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; ENDOTHELIUM, VASCULAR; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; JOINTS; LINEAR MODELS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; QUESTIONNAIRES; RISK FACTORS; SEVERITY OF ILLNESS INDEX; SEX FACTORS; THROMBOMODULIN; VASCULAR CELL ADHESION MOLECULE-1; VON WILLEBRAND FACTOR;

EID: 84855590107     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3538     Document Type: Article

References (55)

1. van Halm VP, Peters MJ, Voskuyl AE, Boers M, Lems WF, Visser M, Stehouwer D, Spijkerman AM, Dekker JM, Nijpels G, Heine RJ, Bouter LM, Smulders YM, Dijkmans BA, Nurmohamed MT. Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease: a cross-sectional study, the CARRE investigation. Ann Rheum Dis 2009, 68:1395-1400. 10.1136/ard.2008.094151, 18697775.
2. Van Doornum S, McColl G, Wicks IP. Accelerated atherosclerosis: An extraarticular feature of rheumatoid arthritis?. Arthritis Rheum 2002, 46:862-873. 10.1002/art.10089, 11953961.
3. del Rincon 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, 44:2737-2745. 10.1002/1529-0131(200112)44:12<2737::AID-ART460>3.0.CO;2-#, 11762933.
4. Quyyumi AA. Inflamed joints and stiff arteries: Is rheumatoid arthritis a cardiovascular risk factor?. Circulation 2006, 114:1137-1139. 10.1161/CIRCULATIONAHA.106.648139, 16966595.
5. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999, 340:115-126. 10.1056/NEJM199901143400207, 9887164.
6. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation 2002, 105:1135-1143. 10.1161/hc0902.104353, 11877368.
7. Ridker PM, Hennekens CH, Roitman-Johnson B, Stampfer MJ, Allen J. Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 1998, 351:88-92. 10.1016/S0140-6736(97)09032-6, 9439492.
8. Van Doornum S, McColl G, Jenkins A, Green DJ, Wicks IP. Screening for atherosclerosis in patients with rheumatoid arthritis: Comparison of two in vivo tests of vascular function. Arthritis Rheum 2003, 48:72-80. 10.1002/art.10735, 12528106.
9. Duprez DA, De Buyzere ML, De Backer TL, Veire VD, Clement DL, Cohn JN. Relationship between arterial elasticity indices and carotid artery intima-media thickness. Am J Hypertens 2000, 13:1226-1232. 10.1016/S0895-7061(00)01203-6, 11078184.
10. Gerrits EG, Lutgers HL, Kleefstra N, Graaff R, Groenier KH, Smit AJ, Gans RO, Bilo HJ. Skin autofluorescence: a tool to identify type 2 diabetic patients at risk for developing microvascular complications. Diabetes Care 2008, 31:517-521.
11. Goh SY, Cooper ME. Clinical review: the role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 2008, 93:1143-1152. 10.1210/jc.2007-1817, 18182449.
12. Semba RD, Ferrucci L, Sun K, Beck J, Dalal M, Varadhan R, Walston J, Guralnik JM, Fried LP. Advanced glycation end products and their circulating receptors predict cardiovascular disease mortality in older community-dwelling women. Aging Clin Exp Res 2009, 21:182-190. 2684987, 19448391.
13. Mulder DJ, Water TV, Lutgers HL, Graaff R, Gans RO, Zijlstra F, Smit AJ. Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations. Diabetes Technol Ther 2006, 8:523-535. 10.1089/dia.2006.8.523, 17037967.
14. Sakata N, Imanaga Y, Meng J, Tachikawa Y, Takebayashi S, Nagai R, Horiuchi S. Increased advanced glycation end products in atherosclerotic lesions of patients with end-stage renal disease. Atherosclerosis 1999, 142:67-77. 10.1016/S0021-9150(98)00192-0, 9920507.
15. Nienhuis HL, de Leeuw K, Bijzet J, Smit A, Schalkwijk CG, Graaff R, Kallenberg CG, Bijl M. Skin autofluorescence is increased in systemic lupus erythematosus but is not reflected by elevated plasma levels of advanced glycation endproducts. Rheumatology (Oxford) 2008, 47:1554-1558.
16. Smit AJ, Lutgers HL. The clinical relevance of advanced glycation endproducts (AGE) and recent developments in pharmaceutics to reduce AGE accumulation. Curr Med Chem 2004, 11:2767-2784.
17. Pullerits R, Bokarewa M, Dahlberg L, Tarkowski A. Decreased levels of soluble receptor for advanced glycation end products in patients with rheumatoid arthritis indicating deficient inflammatory control. Arthritis Res Ther 2005, 7:R817-824. 10.1186/ar1749, 1175032, 15987483.
18. Goldstein RS, Bruchfeld A, Yang L, Qureshi AR, Gallowitsch-Puerta M, Patel NB, Huston BJ, Chavan S, Rosas-Ballina M, Gregersen PK, Czura CJ, Sloan RP, Sama AE, Tracey KJ. Cholinergic anti-inflammatory pathway activity and high mobility group box-1 (HMGB1) serum levels in patients with rheumatoid arthritis. Mol Med 2007, 13:210-215. 1899837, 17597834.
19. Sorensen MV, Pedersen S, Mogelvang R, Skov-Jensen J, Flyvbjerg A. Plasma high-mobility group box 1 levels predict mortality after ST-segment elevation myocardial infarction. JACC Cardiovasc Interv 2011, 4:281-286. 10.1016/j.jcin.2010.10.015, 21435605.
20. Nakashima A, Carrero JJ, Qureshi AR, Miyamoto T, Anderstam B, Barany P, Heimburger O, Stenvinkel P, Lindholm B. Effect of circulating soluble receptor for advanced glycation end products (sRAGE) and the proinflammatory RAGE ligand (EN-RAGE, S100A12) on mortality in hemodialysis patients. Clin J Am Soc Nephrol 2010, 5:2213-2219. 10.2215/CJN.03360410, 2994082, 20847094.
21. Lander HM, Tauras JM, Ogiste JS, Hori O, Moss RA, Schmidt AM. Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem 1997, 272:17810-17814. 10.1074/jbc.272.28.17810, 9211935.
22. Kume S, Takeya M, Mori T, Araki N, Suzuki H, Horiuchi S, Kodama T, Miyauchi Y, Takahashi K. Immunohistochemical and ultrastructural detection of advanced glycation end products in atherosclerotic lesions of human aorta with a novel specific monoclonal antibody. Am J Pathol 1995, 147:654-667. 1870970, 7545874.
23. Schleicher ED, Wagner E, Nerlich AG. Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest 1997, 99:457-468. 10.1172/JCI119180, 507819, 9022079.
24. de Leeuw K, Sanders JS, Stegeman C, Smit A, Kallenberg CG, Bijl M. Accelerated atherosclerosis in patients with Wegener's granulomatosis. Ann Rheum Dis 2005, 64:753-759. 10.1136/ard.2004.029033, 1755479, 15374854.
25. van der Heijde DM, 't Hof MA, van Riel PL, Theunisse LA, Lubberts EW, van Leeuwen MA, van Rijswijk MH, van de Putte LB. Judging disease activity in clinical practice in rheumatoid arthritis: First step in the development of a disease activity score. Ann Rheum Dis 1990, 49:916-920. 10.1136/ard.49.11.916, 1004262, 2256738.
26. Prevoo ML, '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 with rheumatoid arthritis. Arthritis Rheum 1995, 38:44-48. 10.1002/art.1780380107, 7818570.
27. Jacobsson LT, Hetland ML. New remission criteria for RA: 'modern times' in rheumatology--not a silent film, rather a 3D movie. Ann Rheum Dis 2011, 70:401-403. 10.1136/ard.2010.145607, 21292832.
28. Vita AJ, Terry RB, Hubert HB, Fries JF. Aging, health risks, and cumulative disability. N Engl J Med 1998, 338:1035-1041. 10.1056/NEJM199804093381506, 9535669.
29. van der Heijde DM. Plain X-rays in rheumatoid arthritis: Overview of scoring methods, their reliability and applicability. Baillieres Clin Rheumatol 1996, 10:435-453. 10.1016/S0950-3579(96)80043-4, 8876953.
30. Crilly MA, Kumar V, Clark HJ, Scott NW, Macdonald AG, Williams DJ. Arterial stiffness and cumulative inflammatory burden in rheumatoid arthritis: a dose-response relationship independent of established cardiovascular risk factors. Rheumatology (Oxford) 2009, 48:1606-1612.
31. Finkelstein SM, Cohn JN. First- and third-order models for determining arterial compliance. J Hypertens Suppl 1992, 10:S11-14. 10.1097/00004872-199204001-00003, 1432309.
32. Watt TB, Burrus CS. Arterial pressure contour analysis for estimating human vascular properties. J Appl Physiol 1976, 40:171-176.
33. de Groot E, Zwinderman AH, van der Steen AF, Ackerstaff RG, Montauban van Swijndregt AD, Bom N, Lie KI, Bruschke AV. Variance components analysis of carotid and femoral intima-media thickness measurements. REGRESS Study Group, Interuniversity Cardiology Institute of The Netherlands, Utrecht, The Netherlands. Regression Growth Evaluation Statin Study. Ultrasound Med Biol 1998, 24:825-832. 10.1016/S0301-5629(98)00037-4, 9740384.
34. Sramek A, Bosch JG, Reiber JH, Van Oostayen JA, Rosendaal FR. Ultrasound assessment of atherosclerotic vessel wall changes: reproducibility of intima-media thickness measurements in carotid and femoral arteries. Invest Radiol 2000, 35:699-706. 10.1097/00004424-200012000-00001, 11204795.
35. Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, Thorpe SR, Baynes JW, Gans ROB, Smit AJ. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 2004, 47:1324-1330.
36. Lutgers HL, Graaff R, Links TP, Ubink-Veltmaat LJ, Bilo HJ, Gans RO, Smit AJ. Skin autofluorescence as a noninvasive marker of vascular damage in patients with type 2 diabetes. Diabetes Care 2006, 29:2654-2659. 10.2337/dc05-2173, 17130200.
37. Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: A meta-analysis of observational studies. Arthritis Rheum 2008, 59:1690-1697. 10.1002/art.24092, 19035419.
38. Wolfe F, Mitchell DM, Sibley JT, Fries JF, Bloch DA, Williams CA, Spitz PW, Haga M, Kleinheksel SM, Cathy MA. The mortality of rheumatoid arthritis. Arthritis Rheum 1994, 37:481-494. 10.1002/art.1780370408, 8147925.
39. de Leeuw K, Graaff R, de Vries R, Dullaart RP, Smit AJ, Kallenberg CG, Bijl M. Accumulation of advanced glycation endproducts in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2007, 46:1551-1556.
40. de Leeuw K, Nienhuis H, Smit A, Stegeman C, Kallenberg C, Bijl M. Increased accumulation of advanced glycation endproducts in patients with Wegener's granulomatosis. Ann Rheum Dis 2010, 69:625-627. 3133745, 20237121.
41. Carroll L, Hannawi S, Marwick T, Thomas R. Rheumatoid arthritis: links with cardiovascular disease and the receptor for advanced glycation end products. Wien Med Wochenschr 2006, 156:42-52. 10.1007/s10354-005-0242-9, 16465613.
42. Foster W, Carruthers D, Lip GY, Blann AD. Inflammatory cytokines, endothelial markers and adhesion molecules in rheumatoid arthritis: effect of intensive anti-inflammatory treatment. J Thromb Thrombolysis 2010, 29:437-442. 10.1007/s11239-009-0370-y, 19578810.
43. Pemberton PW, Ahmad Y, Bodill H, Lokko D, Hider SL, Yates AP, Walker MG, Laing I, Bruce IN. Biomarkers of oxidant stress, insulin sensitivity and endothelial activation in rheumatoid arthritis: a cross-sectional study of their association with accelerated atherosclerosis. BMC Res Notes 2009, 2:83. 10.1186/1756-0500-2-83, 2687454, 19426539.
44. Gonzalez-Juanatey C, Llorca J, Martin J, Gonzalez-Gay MA. Carotid intima-media thickness predicts the development of cardiovascular events in patients with rheumatoid arthritis. Semin Arthritis Rheum 2009, 38:366-371. 10.1016/j.semarthrit.2008.01.012, 18336869.
45. Georgiadis AN, Voulgari PV, Argyropoulou MI, Alamanos Y, Elisaf M, Tselepis AD, Drosos AA. Early treatment reduces the cardiovascular risk factors in newly diagnosed rheumatoid arthritis patients. Semin Arthritis Rheum 2008, 38:13-19. 10.1016/j.semarthrit.2007.09.008, 18191989.
46. Kumeda Y, Inaba M, Goto H, Nagata M, Henmi Y, Furumitsu Y, Ishimura E, Inui K, Yutani Y, Miki T, Shoji T, Nishizawa Y. Increased thickness of the arterial intima-media detected by ultrasonography in patients with rheumatoid arthritis. Arthritis Rheum 2002, 46:1489-1497. 10.1002/art.10269, 12115178.
47. Del Rincon I, Freeman GL, Haas RW, O'Leary DH, Escalante A. Relative contribution of cardiovascular risk factors and rheumatoid arthritis clinical manifestations to atherosclerosis. Arthritis Rheum 2005, 52:3413-3423. 10.1002/art.21397, 16255018.
48. Daza L, Aguirre M, Jimenez M, Herrera R, Bollain JJ. Common carotid intima-media thickness and von Willebrand factor serum levels in rheumatoid arthritis female patients without cardiovascular risk factors. Clin Rheumatol 2007, 26:533-537. 10.1007/s10067-006-0338-7, 16758372.
49. Park YB, Ahn CW, Choi HK, Lee SH, In BH, Lee HC, Nam CM, Lee SK. Atherosclerosis in rheumatoid arthritis: morphologic evidence obtained by carotid ultrasound. Arthritis Rheum 2002, 46:1714-1749. 10.1002/art.10359, 12124853.
50. Hannawi S, Haluska B, Marwick TH, Thomas R. Atherosclerotic disease is increased in recent-onset rheumatoid arthritis: a critical role for inflammation. Arthritis Res Ther 2007, 9:R116. 10.1186/ar2323, 2246234, 17986352.
51. Ma NH, Teh CL, Rapaee A, Lau KB, Fong AY, Hi S, Chang BC, Yew KL, Liew HB, Ang CK, Ong TK, Chua SK, Chin RW, Sim KH. Subclinical coronary artery disease in Asian rheumatoid arthritis patients who were in remission: a pilot study. Int J Rheum Dis 2010, 13:223-229.
52. Kallberg H, Ding B, Padyukov L, Bengtsson C, Ronnelid J, Klareskog L, Alfredsson L. Smoking is a major preventable risk factor for rheumatoid arthritis: estimations of risks after various exposures to cigarette smoke. Ann Rheum Dis 2011, 70:508-511. 10.1136/ard.2009.120899, 21149499.
53. Matsumoto T, Tsurumoto T, Baba H, Osaki M, Enomoto H, Yonekura A, Shindo H, Miyata T. Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysis-related spondyloarthropathy using non-invasive methods. Rheumatol Int 2007, 28:157-160. 10.1007/s00296-007-0408-4, 17653550.
54. Kageyama Y, Takahashi M, Nagafusa T, Torikai E, Nagano A. Etanercept reduces the oxidative stress marker levels in patients with rheumatoid arthritis. Rheumatol Int 2008, 28:245-251. 10.1007/s00296-007-0419-1, 17661050.
55. Soro-Paavonen A, Zhang WZ, Venardos K, Coughlan MT, Harris E, Tong DC, Brasacchio D, Paavonen K, Chin-Dusting J, Cooper ME, Kaye D, Thomas MC, Forbes JM. Advanced glycation end-products induce vascular dysfunction via resistance to nitric oxide and suppression of endothelial nitric oxide synthase. J Hypertens 2010, 28:780-788. 10.1097/HJH.0b013e328335043e, 20186099.