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Published in: Arthritis Research & Therapy 4/2010

Open Access 01-08-2010 | Research article

Atherosclerosis in early rheumatoid arthritis: very early endothelial activation and rapid progression of intima media thickness

Authors: Anna Södergren, Kjell Karp, Kurt Boman, Catharina Eriksson, Elisabet Lundström, Torgny Smedby, Lisbet Söderlund, Solbritt Rantapää-Dahlqvist, Solveig Wållberg-Jonsson

Published in: Arthritis Research & Therapy | Issue 4/2010

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Abstract

Introduction

In this study we aimed to investigate whether there are indications of premature atherosclerosis, as measured by endothelial dependent flow-mediated dilation (ED-FMD) and intima media thickness (IMT), in patients with very early RA, and to analyze its relation to biomarkers of endothelial dysfunction, taking inflammation and traditional cardiovascular disease (CVD) risk factors into account.

Methods

Patients from the three northern counties of Sweden diagnosed with early RA are followed in an ongoing prospective study of CVD co-morbidity. Of these, all patients aged ≤60 years were consecutively included in this survey of CVD risk factors (n = 79). Forty-four age and sex matched controls were included. IMT of common carotid artery and ED-FMD of brachial artery were measured using ultrasonography. Blood was drawn for analysis of lipids, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), plasminogen activator inhibitor-1 (PAI-1), tissue plasminogen activator (tPA)-mass, VonWillebrand factor (VWF), soluble intercellular adhesion molecule-1 (sICAM), soluble vascular cell adhesion molecule-1 (sVCAM), sE-selectin, sL-selectin and monocyte chemotactic protein-1 (MCP-1). In a subgroup of 27 RA patients and their controls the ultrasound measurements were reanalysed after 18 months.

Results

There were no significant differences between RA patients and controls in terms of IMT or ED-FMD at the first evaluation. However after 18 months there was a significant increase in the IMT among the patients with RA (P < 0.05). Patients with RA had higher levels of VWF, sICAM-1 (P < 0.05) and of MCP-1 (P = 0.001) compared with controls. In RA, IMT was related to some of the traditional CVD risk factors, tPA-mass, VWF (P < 0.01) and MCP-1 and inversely to sL-selectin (P < 0.05). In RA, ED-FMD related to sL-selectin (P < 0.01). DAS28 at baseline was related to PAI-1, tPA-mass and inversely to sVCAM-1 (P < 0.05) and sL-selectin (P = 0.001).

Conclusions

We found no signs of atherosclerosis in patients with newly diagnosed RA compared with controls. However, in patients with early RA, IMT and ED-FMD were, to a greater extent than in controls, related to biomarkers known to be associated with endothelial dysfunction and atherosclerosis. After 18 months, IMT had increased significantly in RA patients but not in controls.
Literature
1.
go back to reference Wållberg-Jonsson S, Öhman ML, Rantapää Dahlqvist S: Cardiovascular morbidity and mortality in patients with seropositive rheumatoid arthritis in northern Sweden. J Rheumatol. 1997, 24: 445-451.PubMed Wållberg-Jonsson S, Öhman ML, Rantapää Dahlqvist S: Cardiovascular morbidity and mortality in patients with seropositive rheumatoid arthritis in northern Sweden. J Rheumatol. 1997, 24: 445-451.PubMed
2.
go back to reference Wolfe F, Mitchell DM, Sibley JT, Fries JF, Bloch DA, Williams CA, Spitz PW, Haga M, Kleinheksel SM, Cathey MA: The mortality of rheumatoid arthritis. Arthritis Rheum. 1994, 37: 481-494. 10.1002/art.1780370408.CrossRefPubMed Wolfe F, Mitchell DM, Sibley JT, Fries JF, Bloch DA, Williams CA, Spitz PW, Haga M, Kleinheksel SM, Cathey MA: The mortality of rheumatoid arthritis. Arthritis Rheum. 1994, 37: 481-494. 10.1002/art.1780370408.CrossRefPubMed
3.
go back to reference Wållberg-Jonsson S, Johansson H, Öhman ML, Rantapää-Dahlqvist S: Extent of inflammation predicts cardiovascular disease and overall mortality in seropositive rheumatoid arthritis. A retrospective cohort study from disease onset. J Rheumatol. 1999, 26: 2562-2571.PubMed Wållberg-Jonsson S, Johansson H, Öhman ML, Rantapää-Dahlqvist S: Extent of inflammation predicts cardiovascular disease and overall mortality in seropositive rheumatoid arthritis. A retrospective cohort study from disease onset. J Rheumatol. 1999, 26: 2562-2571.PubMed
4.
go back to reference del Rincón 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.CrossRefPubMed del Rincón 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.CrossRefPubMed
5.
go back to reference Dessein PH, Joffe BI, Veller MG, Stevens BA, Tobias M, Reddi K, Stanwix AE: Traditional and nontraditional cardiovascular risk factors are associated with atherosclerosis in rheumatoid arthritis. J Rheumatol. 2005, 32: 435-442.PubMed Dessein PH, Joffe BI, Veller MG, Stevens BA, Tobias M, Reddi K, Stanwix AE: Traditional and nontraditional cardiovascular risk factors are associated with atherosclerosis in rheumatoid arthritis. J Rheumatol. 2005, 32: 435-442.PubMed
6.
go back to reference Nagata-Sakurai M, Inaba M, Goto H, Kumeda Y, Furumitsu Y, Inui K, Koyama H, Emoto M, Ishimura E, Shoji T, Nishizawa Y: Inflammation and bone resorption as independent factors of accelerated arterial wall thickening in patients with rheumatoid arthritis. Arthritis Rheum. 2003, 48: 3061-3067. 10.1002/art.11327.CrossRefPubMed Nagata-Sakurai M, Inaba M, Goto H, Kumeda Y, Furumitsu Y, Inui K, Koyama H, Emoto M, Ishimura E, Shoji T, Nishizawa Y: Inflammation and bone resorption as independent factors of accelerated arterial wall thickening in patients with rheumatoid arthritis. Arthritis Rheum. 2003, 48: 3061-3067. 10.1002/art.11327.CrossRefPubMed
7.
go back to reference Jonsson SW, Backman C, Johnson O, Karp K, Lundström E, Sundqvist KG, Dahlqvist SR: Increased prevalence of atherosclerosis in patients with medium term rheumatoid arthritis. J Rheumatol. 2001, 28: 2597-2602.PubMed Jonsson SW, Backman C, Johnson O, Karp K, Lundström E, Sundqvist KG, Dahlqvist SR: Increased prevalence of atherosclerosis in patients with medium term rheumatoid arthritis. J Rheumatol. 2001, 28: 2597-2602.PubMed
8.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
9.
go back to reference Gonzalez-Juanatey C, Llorca J, Testa A, Revuelta J, Garcia-Porrua C, Gonzalez-Gay MA: Increased prevalence of severe subclinical atherosclerotic findings in long-term treated rheumatoid arthritis patients without clinically evident atherosclerotic disease. Medicine (Baltimore). 2003, 82: 407-413. 10.1097/01.md.0000101572.76273.60.CrossRef Gonzalez-Juanatey C, Llorca J, Testa A, Revuelta J, Garcia-Porrua C, Gonzalez-Gay MA: Increased prevalence of severe subclinical atherosclerotic findings in long-term treated rheumatoid arthritis patients without clinically evident atherosclerotic disease. Medicine (Baltimore). 2003, 82: 407-413. 10.1097/01.md.0000101572.76273.60.CrossRef
10.
go back to reference Wendelhag I, Wiklund O, Wikstrand J: Atherosclerotic changes in the femoral and carotid arteries in familial hypercholesterolemia. Ultrasonographic assessment of intima-media thickness and plaque occurrence. Arterioscler Thromb. 1993, 13: 1404-1411.CrossRefPubMed Wendelhag I, Wiklund O, Wikstrand J: Atherosclerotic changes in the femoral and carotid arteries in familial hypercholesterolemia. Ultrasonographic assessment of intima-media thickness and plaque occurrence. Arterioscler Thromb. 1993, 13: 1404-1411.CrossRefPubMed
11.
go back to reference Iglesias del Sol A, Bots ML, Grobbee DE, Hofman A, Witteman JC: Carotid intima-media thickness at different sites: relation to incident myocardial infarction; The Rotterdam Study. Eur Heart J. 2002, 23: 934-940. 10.1053/euhj.2001.2965.CrossRefPubMed Iglesias del Sol A, Bots ML, Grobbee DE, Hofman A, Witteman JC: Carotid intima-media thickness at different sites: relation to incident myocardial infarction; The Rotterdam Study. Eur Heart J. 2002, 23: 934-940. 10.1053/euhj.2001.2965.CrossRefPubMed
12.
go back to reference O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK: Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999, 340: 14-22. 10.1056/NEJM199901073400103.CrossRefPubMed O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK: Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999, 340: 14-22. 10.1056/NEJM199901073400103.CrossRefPubMed
13.
go back to reference Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R: Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol. 2002, 39: 257-265. 10.1016/S0735-1097(01)01746-6.CrossRefPubMed Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R: Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol. 2002, 39: 257-265. 10.1016/S0735-1097(01)01746-6.CrossRefPubMed
14.
go back to reference Bonetti PO, Lerman LO, Lerman A: Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003, 23: 168-175. 10.1161/01.ATV.0000051384.43104.FC.CrossRefPubMed Bonetti PO, Lerman LO, Lerman A: Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003, 23: 168-175. 10.1161/01.ATV.0000051384.43104.FC.CrossRefPubMed
15.
go back to reference Gonzalez-Juanatey C, Testa A, Garcia-Castelo A, Garcia-Porrua C, Llorca J, Vidan J, Hajeer AH, Ollier WE, Mattey DL, Gonzalez-Gay MA: HLA-DRB1 status affects endothelial function in treated patients with rheumatoid arthritis. Am J Med. 2003, 114: 647-652. 10.1016/S0002-9343(03)00133-5.CrossRefPubMed Gonzalez-Juanatey C, Testa A, Garcia-Castelo A, Garcia-Porrua C, Llorca J, Vidan J, Hajeer AH, Ollier WE, Mattey DL, Gonzalez-Gay MA: HLA-DRB1 status affects endothelial function in treated patients with rheumatoid arthritis. Am J Med. 2003, 114: 647-652. 10.1016/S0002-9343(03)00133-5.CrossRefPubMed
16.
go back to reference Vaudo G, Marchesi S, Gerli R, Allegrucci R, Giordano A, Siepi D, Pirro M, Shoenfeld Y, Schillaci G, Mannarino E: Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity. Ann Rheum Dis. 2004, 63: 31-35. 10.1136/ard.2003.007740.PubMedCentralCrossRefPubMed Vaudo G, Marchesi S, Gerli R, Allegrucci R, Giordano A, Siepi D, Pirro M, Shoenfeld Y, Schillaci G, Mannarino E: Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity. Ann Rheum Dis. 2004, 63: 31-35. 10.1136/ard.2003.007740.PubMedCentralCrossRefPubMed
17.
go back to reference Hürlimann D, Forster A, Noll G, Enseleit F, Chenevard R, Distler O, Béchir M, Spieker LE, Neidhart M, Michel BA, Gay RE, Lüscher TF, Gay S, Ruschitzka F: Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation. 2002, 106: 2184-2187. 10.1161/01.CIR.0000037521.71373.44.CrossRefPubMed Hürlimann D, Forster A, Noll G, Enseleit F, Chenevard R, Distler O, Béchir M, Spieker LE, Neidhart M, Michel BA, Gay RE, Lüscher TF, Gay S, Ruschitzka F: Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation. 2002, 106: 2184-2187. 10.1161/01.CIR.0000037521.71373.44.CrossRefPubMed
18.
go back to reference Hafström I, Rohani M, Deneberg S, Wörnert M, Jogestrand T, Frostegård J: Effects of low-dose prednisolone on endothelial function, atherosclerosis, and traditional risk factors for atherosclerosis in patients with rheumatoid arthritis--a randomized study. J Rheumatol. 2007, 34: 1810-1816.PubMed Hafström I, Rohani M, Deneberg S, Wörnert M, Jogestrand T, Frostegård J: Effects of low-dose prednisolone on endothelial function, atherosclerosis, and traditional risk factors for atherosclerosis in patients with rheumatoid arthritis--a randomized study. J Rheumatol. 2007, 34: 1810-1816.PubMed
19.
go back to reference Hannawi S, Marwick TH, Thomas R: Inflammation predicts accelerated brachial arterial wall changes in patients with recent-onset rheumatoid arthritis. Arthritis Res Ther. 2009, 11: R51-10.1186/ar2668.PubMedCentralCrossRefPubMed Hannawi S, Marwick TH, Thomas R: Inflammation predicts accelerated brachial arterial wall changes in patients with recent-onset rheumatoid arthritis. Arthritis Res Ther. 2009, 11: R51-10.1186/ar2668.PubMedCentralCrossRefPubMed
20.
go back to reference Howard-Alpe GM, Sear JW, Foex P: Methods of detecting atherosclerosis in non-cardiac surgical patients; the role of biochemical markers. Br J Anaesth. 2006, 97: 758-769. 10.1093/bja/ael303.CrossRefPubMed Howard-Alpe GM, Sear JW, Foex P: Methods of detecting atherosclerosis in non-cardiac surgical patients; the role of biochemical markers. Br J Anaesth. 2006, 97: 758-769. 10.1093/bja/ael303.CrossRefPubMed
21.
go back to reference Tousoulis D, Antoniades C, Bosinakou E, Kotsopoulou M, Tsoufis C, Marinou K, Charakida M, Stefanadi E, Vavuranakis M, Latsios G, Stefanadis C: Differences in inflammatory and thrombotic markers between unstable angina and acute myocardial infarction. Int J Cardiol. 2007, 115: 203-207. 10.1016/j.ijcard.2006.03.011.CrossRefPubMed Tousoulis D, Antoniades C, Bosinakou E, Kotsopoulou M, Tsoufis C, Marinou K, Charakida M, Stefanadi E, Vavuranakis M, Latsios G, Stefanadis C: Differences in inflammatory and thrombotic markers between unstable angina and acute myocardial infarction. Int J Cardiol. 2007, 115: 203-207. 10.1016/j.ijcard.2006.03.011.CrossRefPubMed
22.
go back to reference Kusano KF, Nakamura K, Kusano H, Nishii N, Banba K, Ikeda T, Hashimoto K, Yamamoto M, Fujio H, Miura A, Ohta K, Morita H, Saito H, Emori T, Nakamura Y, Kusano I, Ohe T: Significance of the level of monocyte chemoattractant protein-1 in human atherosclerosis. Circ J. 2004, 68: 671-676. 10.1253/circj.68.671.CrossRefPubMed Kusano KF, Nakamura K, Kusano H, Nishii N, Banba K, Ikeda T, Hashimoto K, Yamamoto M, Fujio H, Miura A, Ohta K, Morita H, Saito H, Emori T, Nakamura Y, Kusano I, Ohe T: Significance of the level of monocyte chemoattractant protein-1 in human atherosclerosis. Circ J. 2004, 68: 671-676. 10.1253/circj.68.671.CrossRefPubMed
23.
go back to reference Martinovic I, Abegunewardene N, Seul M, Vosseler M, Horstick G, Buerke M, Darius H, Lindemann S: Elevated monocyte chemoattractant protein-1 serum levels in patients at risk for coronary artery disease. Circ J. 2005, 69: 1484-1489. 10.1253/circj.69.1484.CrossRefPubMed Martinovic I, Abegunewardene N, Seul M, Vosseler M, Horstick G, Buerke M, Darius H, Lindemann S: Elevated monocyte chemoattractant protein-1 serum levels in patients at risk for coronary artery disease. Circ J. 2005, 69: 1484-1489. 10.1253/circj.69.1484.CrossRefPubMed
24.
go back to reference Rainer TH: L-selectin in health and disease. Resuscitation. 2002, 52: 127-141. 10.1016/S0300-9572(01)00444-0.CrossRefPubMed Rainer TH: L-selectin in health and disease. Resuscitation. 2002, 52: 127-141. 10.1016/S0300-9572(01)00444-0.CrossRefPubMed
25.
go back to reference Johansson L, Jansson JH, Boman K, Nilsson TK, Stegmayr B, Hallmans G: Tissue plasminogen activator, plasminogen activator inhibitor-1, and tissue plasminogen activator/plasminogen activator inhibitor-1 complex as risk factors for the development of a first stroke. Stroke. 2000, 31: 26-32.CrossRefPubMed Johansson L, Jansson JH, Boman K, Nilsson TK, Stegmayr B, Hallmans G: Tissue plasminogen activator, plasminogen activator inhibitor-1, and tissue plasminogen activator/plasminogen activator inhibitor-1 complex as risk factors for the development of a first stroke. Stroke. 2000, 31: 26-32.CrossRefPubMed
26.
go back to reference Wållberg-Jonsson S, Öhman M, Rantapää-Dahlqvist S: Which factors are related to the presence of atherosclerosis in rheumatoid arthritis?. Scand J Rheumatol. 2004, 33: 373-379. 10.1080/03009740410010308.CrossRefPubMed Wållberg-Jonsson S, Öhman M, Rantapää-Dahlqvist S: Which factors are related to the presence of atherosclerosis in rheumatoid arthritis?. Scand J Rheumatol. 2004, 33: 373-379. 10.1080/03009740410010308.CrossRefPubMed
27.
go back to reference Dessein PH, Joffe BI, Singh S: Biomarkers of endothelial dysfunction, cardiovascular risk factors and atherosclerosis in rheumatoid arthritis. Arthritis Res Ther. 2005, 7: R634-643. 10.1186/ar1717.PubMedCentralCrossRefPubMed Dessein PH, Joffe BI, Singh S: Biomarkers of endothelial dysfunction, cardiovascular risk factors and atherosclerosis in rheumatoid arthritis. Arthritis Res Ther. 2005, 7: R634-643. 10.1186/ar1717.PubMedCentralCrossRefPubMed
28.
go back to reference Wållberg-Jonsson S, Caidahl K, Klintland N, Nyberg G, Rantapää-Dahlqvist S: Increased arterial stiffness and indication of endothelial dysfunction in long-standing rheumatoid arthritis. Scand J Rheumatol. 2008, 37: 1-5. 10.1080/03009740701633238.CrossRefPubMed Wållberg-Jonsson S, Caidahl K, Klintland N, Nyberg G, Rantapää-Dahlqvist S: Increased arterial stiffness and indication of endothelial dysfunction in long-standing rheumatoid arthritis. Scand J Rheumatol. 2008, 37: 1-5. 10.1080/03009740701633238.CrossRefPubMed
29.
go back to reference McEntegart A, Capell HA, Creran D, Rumley A, Woodward M, Lowe GD: Cardiovascular risk factors, including thrombotic variables, in a population with rheumatoid arthritis. Rheumatology (Oxford). 2001, 40: 640-644. 10.1093/rheumatology/40.6.640.CrossRef McEntegart A, Capell HA, Creran D, Rumley A, Woodward M, Lowe GD: Cardiovascular risk factors, including thrombotic variables, in a population with rheumatoid arthritis. Rheumatology (Oxford). 2001, 40: 640-644. 10.1093/rheumatology/40.6.640.CrossRef
30.
go back to reference Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, et al: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988, 31: 315-324. 10.1002/art.1780310302.CrossRefPubMed Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, et al: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988, 31: 315-324. 10.1002/art.1780310302.CrossRefPubMed
31.
go back to reference 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 with rheumatoid arthritis. Arthritis Rheum. 1995, 38: 44-48. 10.1002/art.1780380107.CrossRefPubMed 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 with rheumatoid arthritis. Arthritis Rheum. 1995, 38: 44-48. 10.1002/art.1780380107.CrossRefPubMed
32.
go back to reference Fries JF, Spitz P, Krainers RG, Holman HR: Measurement of patient outcome in arthritis. Arthritis Rheum. 1980, 23: 137-145. 10.1002/art.1780230202.CrossRefPubMed Fries JF, Spitz P, Krainers RG, Holman HR: Measurement of patient outcome in arthritis. Arthritis Rheum. 1980, 23: 137-145. 10.1002/art.1780230202.CrossRefPubMed
33.
go back to reference Rose GA: Cardiovascular survey methods. 1992, Geneva: World Health Organization. Albany. New York. WHO Publishing Centre, Monograph Series, 2 Rose GA: Cardiovascular survey methods. 1992, Geneva: World Health Organization. Albany. New York. WHO Publishing Centre, Monograph Series, 2
34.
go back to reference Nilsson TK, Boman K, Jansson JH, Thögersen AM, Berggren M, Broberg A, Granlund A: Comparison of soluble thrombomodulin, von Willebrand factor, tPA/PAI-1 complex, and high-sensitivity CRP concentrations in serum, EDTA plasma, citrated plasma, and acidified citrated plasma (Stabilyte) stored at -70 degrees C for 8-11 years. Thromb Res. 2005, 116: 249-254. 10.1016/j.thromres.2004.12.005.CrossRefPubMed Nilsson TK, Boman K, Jansson JH, Thögersen AM, Berggren M, Broberg A, Granlund A: Comparison of soluble thrombomodulin, von Willebrand factor, tPA/PAI-1 complex, and high-sensitivity CRP concentrations in serum, EDTA plasma, citrated plasma, and acidified citrated plasma (Stabilyte) stored at -70 degrees C for 8-11 years. Thromb Res. 2005, 116: 249-254. 10.1016/j.thromres.2004.12.005.CrossRefPubMed
35.
go back to reference Bergholm R, Leirisalo-Repo M, Vehkavaara S, Mäkimattila S, Taskinen MR, Yki-Järvinen H: Impaired responsiveness to NO in newly diagnosed patients with rheumatoid arthritis. Arterioscler Thromb Vasc Biol. 2002, 22: 1637-1641. 10.1161/01.ATV.0000033516.73864.4E.CrossRefPubMed Bergholm R, Leirisalo-Repo M, Vehkavaara S, Mäkimattila S, Taskinen MR, Yki-Järvinen H: Impaired responsiveness to NO in newly diagnosed patients with rheumatoid arthritis. Arterioscler Thromb Vasc Biol. 2002, 22: 1637-1641. 10.1161/01.ATV.0000033516.73864.4E.CrossRefPubMed
36.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
37.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
38.
go back to reference Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VL, Jacobsen SJ, Gabriel SE: Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum. 2005, 52: 402-411. 10.1002/art.20853.CrossRefPubMed Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VL, Jacobsen SJ, Gabriel SE: Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum. 2005, 52: 402-411. 10.1002/art.20853.CrossRefPubMed
39.
go back to reference Gonzalez-Juanatey C, Llorca J, Garcia-Porrua C, Martin J, Gonzalez-Gay MA: Effect of anti-tumor necrosis factor alpha therapy on the progression of subclinical atherosclerosis in severe rheumatoid arthritis. Arthritis Rheum. 2006, 55: 150-153. 10.1002/art.21707.CrossRefPubMed Gonzalez-Juanatey C, Llorca J, Garcia-Porrua C, Martin J, Gonzalez-Gay MA: Effect of anti-tumor necrosis factor alpha therapy on the progression of subclinical atherosclerosis in severe rheumatoid arthritis. Arthritis Rheum. 2006, 55: 150-153. 10.1002/art.21707.CrossRefPubMed
40.
go back to reference Alizadeh Dehnavi R, Beishuizen ED, van de Ree MA, Le Cessie S, Huisman MV, Kluft C, Princen HM, Tamsma JT: The impact of metabolic syndrome and CRP on vascular phenotype in type 2 diabetes mellitus. Eur J Intern Med. 2008, 19: 115-121. 10.1016/j.ejim.2007.06.011.CrossRefPubMed Alizadeh Dehnavi R, Beishuizen ED, van de Ree MA, Le Cessie S, Huisman MV, Kluft C, Princen HM, Tamsma JT: The impact of metabolic syndrome and CRP on vascular phenotype in type 2 diabetes mellitus. Eur J Intern Med. 2008, 19: 115-121. 10.1016/j.ejim.2007.06.011.CrossRefPubMed
41.
go back to reference Rantapää-Dahlqvist S, Boman K, Tarkowski A, Hallmans G: Up regulation of monocyte chemoattractant protein-1 expression in anti-citrulline antibody and immunoglobulin M rheumatoid factor positive subjects precedes onset of inflammatory response and development of overt rheumatoid arthritis. Ann Rheum Dis. 2007, 66: 121-123. 10.1136/ard.2006.057331.PubMedCentralCrossRefPubMed Rantapää-Dahlqvist S, Boman K, Tarkowski A, Hallmans G: Up regulation of monocyte chemoattractant protein-1 expression in anti-citrulline antibody and immunoglobulin M rheumatoid factor positive subjects precedes onset of inflammatory response and development of overt rheumatoid arthritis. Ann Rheum Dis. 2007, 66: 121-123. 10.1136/ard.2006.057331.PubMedCentralCrossRefPubMed
42.
go back to reference Chung CP, Oeser A, Raggi P, Gebretsadik T, Shintani AK, Sokka T, Pincus T, Avalos I, Stein CM: Increased coronary-artery atherosclerosis in rheumatoid arthritis: relationship to disease duration and cardiovascular risk factors. Arthritis Rheum. 2005, 52: 3045-3053. 10.1002/art.21288.CrossRefPubMed Chung CP, Oeser A, Raggi P, Gebretsadik T, Shintani AK, Sokka T, Pincus T, Avalos I, Stein CM: Increased coronary-artery atherosclerosis in rheumatoid arthritis: relationship to disease duration and cardiovascular risk factors. Arthritis Rheum. 2005, 52: 3045-3053. 10.1002/art.21288.CrossRefPubMed
43.
go back to reference van Halm VP, Nielen MM, Nurmohamed MT, van Schaardenburg D, Reesink HW, Voskuyl AE, Twisk JW, van de Stadt RJ, de Koning MH, Habibuw MR, van der Horst-Bruinsma IE, Dijkmans BA: Lipids and inflammation: serial measurements of the lipid profile of blood donors who later developed rheumatoid arthritis. Ann Rheum Dis. 2007, 66: 184-188. 10.1136/ard.2006.051672.PubMedCentralCrossRefPubMed van Halm VP, Nielen MM, Nurmohamed MT, van Schaardenburg D, Reesink HW, Voskuyl AE, Twisk JW, van de Stadt RJ, de Koning MH, Habibuw MR, van der Horst-Bruinsma IE, Dijkmans BA: Lipids and inflammation: serial measurements of the lipid profile of blood donors who later developed rheumatoid arthritis. Ann Rheum Dis. 2007, 66: 184-188. 10.1136/ard.2006.051672.PubMedCentralCrossRefPubMed
Metadata
Title
Atherosclerosis in early rheumatoid arthritis: very early endothelial activation and rapid progression of intima media thickness
Authors
Anna Södergren
Kjell Karp
Kurt Boman
Catharina Eriksson
Elisabet Lundström
Torgny Smedby
Lisbet Söderlund
Solbritt Rantapää-Dahlqvist
Solveig Wållberg-Jonsson
Publication date
01-08-2010
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 4/2010
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar3116

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