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Published in: Arthritis Research & Therapy 2/2008

Open Access 01-04-2008 | Research article

Early atherosclerosis in systemic sclerosis and its relation to disease or traditional risk factors

Authors: Martha E Hettema, Dan Zhang, Karina de Leeuw, Ymkje Stienstra, Andries J Smit, Cees GM Kallenberg, Hendrika Bootsma

Published in: Arthritis Research & Therapy | Issue 2/2008

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Abstract

Introduction

Several systemic autoimmune diseases are associated with an increased prevalence of atherosclerosis which could not be explained by traditional risk factors alone. In systemic sclerosis (SSc), microvascular abnormalities are well recognized. Previous studies have suggested an increased prevalence of macrovascular disease as well. We compared patients with SSc to healthy controls for signs of early atherosclerosis by measuring intima-media thickness (IMT) of the common carotid artery in relation to traditional risk factors and markers of endothelial activation.

Methods

Forty-nine patients with SSc, of whom 92% had limited cutaneous SSc, and 32 healthy controls were studied. Common carotid IMT was measured by using B-mode ultrasound. Traditional risk factors for cardiovascular disease were assessed and serum markers for endothelial activation were measured.

Results

In patients with SSc, the mean IMT (median 0.69 mm, interquartile range [IQR] 0.62 to 0.79 mm) was not significantly increased compared with healthy controls (0.68 mm, IQR 0.56 to 0.75 mm; P = 0.067). Also, after correction for the confounders age, high-density lipoprotein (HDL) cholesterol, and low-density lipoprotein cholesterol (P = 0.328) or using a different model taking into account the confounders age, HDL cholesterol, and history of macrovascular disease (P = 0.474), no difference in IMT was present between SSc patients and healthy controls. Plaques were found in three patients and not in healthy controls (P = 0.274). In patients, no correlations were found between maximum IMT, disease-related variables, and markers of endothelial activation. Endothelial activation markers were not increased in SSc patients compared with controls.

Conclusion

SSc is not associated with an increased prevalence of early signs of atherosclerosis.
Appendix
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Literature
1.
go back to reference Kahaleh MB, LeRoy EC: Autoimmunity and vascular involvement in systemic sclerosis (SSc). Autoimmunity. 1999, 31: 195-214.CrossRefPubMed Kahaleh MB, LeRoy EC: Autoimmunity and vascular involvement in systemic sclerosis (SSc). Autoimmunity. 1999, 31: 195-214.CrossRefPubMed
2.
go back to reference LeRoy EC: Systemic sclerosis. A vascular perspective. Rheum Dis Clin North Am. 1996, 22: 675-694. 10.1016/S0889-857X(05)70295-7.CrossRefPubMed LeRoy EC: Systemic sclerosis. A vascular perspective. Rheum Dis Clin North Am. 1996, 22: 675-694. 10.1016/S0889-857X(05)70295-7.CrossRefPubMed
3.
go back to reference Mackiewicz Z, Sukura A, Povilenaité D, Ceponis A, Virtanen I, Hukkanen M, Konttinen YT: Increased but imbalanced expression of VEGF and its receptors has no positive effect on angiogenesis in systemic sclerosis skin. Clin Exp Rheumatol. 2002, 20: 641-646.PubMed Mackiewicz Z, Sukura A, Povilenaité D, Ceponis A, Virtanen I, Hukkanen M, Konttinen YT: Increased but imbalanced expression of VEGF and its receptors has no positive effect on angiogenesis in systemic sclerosis skin. Clin Exp Rheumatol. 2002, 20: 641-646.PubMed
4.
5.
6.
go back to reference Alkaabi JK, Ho M, Levison R, Pullar T, Belch JJF: Rheumatoid arthritis and macrovascular disease. Rheumatology. 2003, 42: 292-297. 10.1093/rheumatology/keg083.CrossRefPubMed Alkaabi JK, Ho M, Levison R, Pullar T, Belch JJF: Rheumatoid arthritis and macrovascular disease. Rheumatology. 2003, 42: 292-297. 10.1093/rheumatology/keg083.CrossRefPubMed
7.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
8.
go back to reference Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, Côte R, Grover SA, Fortin PR, Clarke AE, Senécal JL: Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2001, 44: 2331-2337. 10.1002/1529-0131(200110)44:10<2331::AID-ART395>3.0.CO;2-I.CrossRefPubMed Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, Côte R, Grover SA, Fortin PR, Clarke AE, Senécal JL: Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2001, 44: 2331-2337. 10.1002/1529-0131(200110)44:10<2331::AID-ART395>3.0.CO;2-I.CrossRefPubMed
9.
go back to reference Wallberg-Jonsson S, Ohman M, Rantapaa-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 Wallberg-Jonsson S, Ohman M, Rantapaa-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
10.
go back to reference Shoenfeld Y, Gerli R, Doria A, Matsuura E, Cerinic MM, Ronda N, Jara LJ, Abu-Shakra M, Meroni PL, Sherer Y: Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation. 2005, 112: 3337-3347. 10.1161/CIRCULATIONAHA.104.507996.CrossRefPubMed Shoenfeld Y, Gerli R, Doria A, Matsuura E, Cerinic MM, Ronda N, Jara LJ, Abu-Shakra M, Meroni PL, Sherer Y: Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation. 2005, 112: 3337-3347. 10.1161/CIRCULATIONAHA.104.507996.CrossRefPubMed
11.
go back to reference Ross R: Atherosclerosis – An inflammatory disease. N Engl J Med. 1999, 340: 115-126. 10.1056/NEJM199901143400207.CrossRefPubMed Ross R: Atherosclerosis – An inflammatory disease. N Engl J Med. 1999, 340: 115-126. 10.1056/NEJM199901143400207.CrossRefPubMed
12.
go back to reference Mayes MD, Lacey JV, Beebe-Dimmer J, Gillespie BW, Cooper B, Laing TJ, Schottenfeld D: Prevalence, incidence, survival, and disease characteristics of systemic sclerosis in a large US population. Arthritis Rheum. 2003, 48: 2246-2255. 10.1002/art.11073.CrossRefPubMed Mayes MD, Lacey JV, Beebe-Dimmer J, Gillespie BW, Cooper B, Laing TJ, Schottenfeld D: Prevalence, incidence, survival, and disease characteristics of systemic sclerosis in a large US population. Arthritis Rheum. 2003, 48: 2246-2255. 10.1002/art.11073.CrossRefPubMed
13.
go back to reference Ioannidis JP, Vlachoyiannopoulos PG, Haidich AB, Medsger TA, Lucas M, Michet CJ, Kuwana M, Yasuoka H, Hoogen van den F, Te Boome L, van Laar JM, Verbeet NL, Matucci-Cerinic M, Georgountzos A, Moutsopoulos HM: Mortality in systemic sclerosis: an international meta-analysis of individual patient data. Am J Med. 2005, 118: 2-10. 10.1016/j.amjmed.2004.04.031.CrossRefPubMed Ioannidis JP, Vlachoyiannopoulos PG, Haidich AB, Medsger TA, Lucas M, Michet CJ, Kuwana M, Yasuoka H, Hoogen van den F, Te Boome L, van Laar JM, Verbeet NL, Matucci-Cerinic M, Georgountzos A, Moutsopoulos HM: Mortality in systemic sclerosis: an international meta-analysis of individual patient data. Am J Med. 2005, 118: 2-10. 10.1016/j.amjmed.2004.04.031.CrossRefPubMed
14.
go back to reference Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee: Preliminary criteria for the classification of systemic-sclerosis (scleroderma). Arthritis Rheum. 1980, 23: 581-590. 10.1002/art.1780230510.CrossRef Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee: Preliminary criteria for the classification of systemic-sclerosis (scleroderma). Arthritis Rheum. 1980, 23: 581-590. 10.1002/art.1780230510.CrossRef
15.
go back to reference LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA, Rowell N, Wollheim F: Scleroderma (systemic-sclerosis) – classification, subsets and pathogenesis. J Rheumatol. 1988, 15: 202-205.PubMed LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA, Rowell N, Wollheim F: Scleroderma (systemic-sclerosis) – classification, subsets and pathogenesis. J Rheumatol. 1988, 15: 202-205.PubMed
16.
go back to reference LeRoy EC, Medsger TA: Criteria for the classification of early systemic sclerosis. J Rheumatol. 2001, 28: 1573-1576.PubMed LeRoy EC, Medsger TA: Criteria for the classification of early systemic sclerosis. J Rheumatol. 2001, 28: 1573-1576.PubMed
17.
go back to reference Valentini G, Della Rossa A, Bombardieri S, Bencivelli W, Silman AJ, D'Angelo S, Cerinic MM, Belch JF, Black CM, Bruhlmann P, Czirják L, De Luca A, Drosos AA, Ferri C, Gabrielli A, Giacomelli R, Hayem G, Inanc M, McHugh NJ, Nielsen H, Rosada M, Scorza R, Stork J, Sysa A, Hoogen van den FH, Vlachoyiannopoulos PJ: European multicentre study to define disease activity criteria for systemic sclerosis. II. Identification of disease activity variables and development of preliminary activity indexes. Ann Rheum Dis. 2001, 60: 592-598. 10.1136/ard.60.6.592.PubMedCentralCrossRefPubMed Valentini G, Della Rossa A, Bombardieri S, Bencivelli W, Silman AJ, D'Angelo S, Cerinic MM, Belch JF, Black CM, Bruhlmann P, Czirják L, De Luca A, Drosos AA, Ferri C, Gabrielli A, Giacomelli R, Hayem G, Inanc M, McHugh NJ, Nielsen H, Rosada M, Scorza R, Stork J, Sysa A, Hoogen van den FH, Vlachoyiannopoulos PJ: European multicentre study to define disease activity criteria for systemic sclerosis. II. Identification of disease activity variables and development of preliminary activity indexes. Ann Rheum Dis. 2001, 60: 592-598. 10.1136/ard.60.6.592.PubMedCentralCrossRefPubMed
18.
go back to reference Valentini G, Bencivelli W, Bombardieri S, D'Angelo S, Della Rossa A, Silman AJ, Black CM, Czirjak L, Nielsen H, Vlachoyiannopoulos PG: European Scleroderma Study Group to define disease activity criteria for systemic sclerosis. III. Assessment of the construct validity of the preliminary activity criteria. Ann Rheum Dis. 2003, 62: 901-903. 10.1136/ard.62.9.901.PubMedCentralCrossRefPubMed Valentini G, Bencivelli W, Bombardieri S, D'Angelo S, Della Rossa A, Silman AJ, Black CM, Czirjak L, Nielsen H, Vlachoyiannopoulos PG: European Scleroderma Study Group to define disease activity criteria for systemic sclerosis. III. Assessment of the construct validity of the preliminary activity criteria. Ann Rheum Dis. 2003, 62: 901-903. 10.1136/ard.62.9.901.PubMedCentralCrossRefPubMed
19.
go back to reference Medsger TA, Bombardieri S, Czirjak L, Scorza R, Della Rossa A, Bencivelli W: Assessment of disease severity and prognosis. Clin Exp Rheumatol. 2003, 21: S42-S46.PubMed Medsger TA, Bombardieri S, Czirjak L, Scorza R, Della Rossa A, Bencivelli W: Assessment of disease severity and prognosis. Clin Exp Rheumatol. 2003, 21: S42-S46.PubMed
20.
go back to reference Blaauw J, van Pampus MG, van Doormaal JJ, Fokkema MR, Fidler V, Smit AJ, Aarnoudse JG: Increased intima-media thickness after early-onset preeclampsia. Obstet Gynecol. 2006, 107: 1345-1351.CrossRefPubMed Blaauw J, van Pampus MG, van Doormaal JJ, Fokkema MR, Fidler V, Smit AJ, Aarnoudse JG: Increased intima-media thickness after early-onset preeclampsia. Obstet Gynecol. 2006, 107: 1345-1351.CrossRefPubMed
21.
go back to reference Selzer RH, Hodis HN, Kwong-Fu H, Mack WJ, Lee PL, Liu CR, Liu CH: Evaluation of computerized edge tracking for quantifying intima-media thickness of the common carotid artery from B-mode ultrasound images. Atherosclerosis. 1994, 111: 1-11. 10.1016/0021-9150(94)90186-4.CrossRefPubMed Selzer RH, Hodis HN, Kwong-Fu H, Mack WJ, Lee PL, Liu CR, Liu CH: Evaluation of computerized edge tracking for quantifying intima-media thickness of the common carotid artery from B-mode ultrasound images. Atherosclerosis. 1994, 111: 1-11. 10.1016/0021-9150(94)90186-4.CrossRefPubMed
22.
go back to reference Lekakis J, Mavrikakis M, Papamichael C, Papazoglou S, Economou O, Scotiniotis I, Stamatelopoulos K, Vemmos C, Stamatelopoulos S, Moulopoulos S: Short-term estrogen administration improves abnormal endothelial function in women with systemic sclerosis and Raynaud's phenomenon. Am Heart J. 1998, 136: 905-912. 10.1016/S0002-8703(98)70137-1.CrossRefPubMed Lekakis J, Mavrikakis M, Papamichael C, Papazoglou S, Economou O, Scotiniotis I, Stamatelopoulos K, Vemmos C, Stamatelopoulos S, Moulopoulos S: Short-term estrogen administration improves abnormal endothelial function in women with systemic sclerosis and Raynaud's phenomenon. Am Heart J. 1998, 136: 905-912. 10.1016/S0002-8703(98)70137-1.CrossRefPubMed
23.
go back to reference Kaloudi O, Basta G, Perfetto F, Bartoli F, Del Rosso A, Miniati I, Conforti ML, Generini S, Guiducci S, Abbate R, Pignone A, Castellani S, Livi R, De Caterina R, Matucci-Cerinic M: Circulating levels of Nepsilon-(carboxymethyl)lysine are increased in systemic sclerosis. Rheumatology (Oxford). 2007, 46: 412-416. 10.1093/rheumatology/kel076.CrossRef Kaloudi O, Basta G, Perfetto F, Bartoli F, Del Rosso A, Miniati I, Conforti ML, Generini S, Guiducci S, Abbate R, Pignone A, Castellani S, Livi R, De Caterina R, Matucci-Cerinic M: Circulating levels of Nepsilon-(carboxymethyl)lysine are increased in systemic sclerosis. Rheumatology (Oxford). 2007, 46: 412-416. 10.1093/rheumatology/kel076.CrossRef
24.
go back to reference Bartoli F, Angotti C, Fatini C, Conforti ML, Guiducci S, Blagojevic J, Melchiorre D, Fiori G, Generini S, Damjanov N, Rednic S, Pignone A, Castellani S, Abbate R, Matucci Cerinic M: Angiotensin-converting enzyme I/D polymorphism and macrovascular disease in systemic sclerosis. Rheumatology (Oxford). 2007, 46: 772-775. 10.1093/rheumatology/kel433.CrossRef Bartoli F, Angotti C, Fatini C, Conforti ML, Guiducci S, Blagojevic J, Melchiorre D, Fiori G, Generini S, Damjanov N, Rednic S, Pignone A, Castellani S, Abbate R, Matucci Cerinic M: Angiotensin-converting enzyme I/D polymorphism and macrovascular disease in systemic sclerosis. Rheumatology (Oxford). 2007, 46: 772-775. 10.1093/rheumatology/kel433.CrossRef
25.
go back to reference Bartoli F, Blagojevic J, Bacci M, Fiori G, Tempestini A, Conforti ML, Guiducci S, Miniati I, Di Chicco M, Del Rosso A, Perfetto F, Castellani S, Pignone A, Cerinic MM: Flow-mediated vasodilation and carotid intima-media thickness in systemic sclerosis. Ann N Y Acad Sci. 2007, 1108: 283-290. 10.1196/annals.1422.030.CrossRefPubMed Bartoli F, Blagojevic J, Bacci M, Fiori G, Tempestini A, Conforti ML, Guiducci S, Miniati I, Di Chicco M, Del Rosso A, Perfetto F, Castellani S, Pignone A, Cerinic MM: Flow-mediated vasodilation and carotid intima-media thickness in systemic sclerosis. Ann N Y Acad Sci. 2007, 1108: 283-290. 10.1196/annals.1422.030.CrossRefPubMed
26.
go back to reference Cheng KS, Tiwari A, Boutin A, Denton CP, Black CM, Morris R, Hamilton G, Seifalian AM: Carotid and femoral arterial wall mechanics in scleroderma. Rheumatology (Oxford). 2003, 42: 1299-1305. 10.1093/rheumatology/keg371.CrossRef Cheng KS, Tiwari A, Boutin A, Denton CP, Black CM, Morris R, Hamilton G, Seifalian AM: Carotid and femoral arterial wall mechanics in scleroderma. Rheumatology (Oxford). 2003, 42: 1299-1305. 10.1093/rheumatology/keg371.CrossRef
27.
go back to reference Cheng KS, Tiwari A, Boutin A, Denton CP, Black CM, Morris R, Seifalian AM, Hamilton G: Differentiation of primary and secondary Raynaud's disease by carotid arterial stiffness. Eur J Vasc Endovasc Surg. 2003, 25: 336-341. 10.1053/ejvs.2002.1845.CrossRefPubMed Cheng KS, Tiwari A, Boutin A, Denton CP, Black CM, Morris R, Seifalian AM, Hamilton G: Differentiation of primary and secondary Raynaud's disease by carotid arterial stiffness. Eur J Vasc Endovasc Surg. 2003, 25: 336-341. 10.1053/ejvs.2002.1845.CrossRefPubMed
28.
go back to reference Szucs G, Tímár O, Szekanecz Z, Dér H, Kerekes G, Szamosi S, Shoenfeld Y, Szegedi G, Soltész P: Endothelial dysfunction precedes atherosclerosis in systemic sclerosis. Relevance for prevention of vascular complications. Rheumatology (Oxford). 2007, 46: 759-762. 10.1093/rheumatology/kel426.CrossRef Szucs G, Tímár O, Szekanecz Z, Dér H, Kerekes G, Szamosi S, Shoenfeld Y, Szegedi G, Soltész P: Endothelial dysfunction precedes atherosclerosis in systemic sclerosis. Relevance for prevention of vascular complications. Rheumatology (Oxford). 2007, 46: 759-762. 10.1093/rheumatology/kel426.CrossRef
29.
go back to reference Kang S, Wu Y, Li X: Effects of statin therapy on the progression of carotid atherosclerosis: a systematic review and meta-analysis. Atherosclerosis. 2004, 177: 433-442. 10.1016/j.atherosclerosis.2004.08.005.CrossRefPubMed Kang S, Wu Y, Li X: Effects of statin therapy on the progression of carotid atherosclerosis: a systematic review and meta-analysis. Atherosclerosis. 2004, 177: 433-442. 10.1016/j.atherosclerosis.2004.08.005.CrossRefPubMed
30.
go back to reference Kuwana M: Potential benefit of statins for vascular disease in systemic sclerosis. Curr Opin Rheumatol. 2006, 18: 594-600. 10.1097/01.bor.0000245720.02512.3e.CrossRefPubMed Kuwana M: Potential benefit of statins for vascular disease in systemic sclerosis. Curr Opin Rheumatol. 2006, 18: 594-600. 10.1097/01.bor.0000245720.02512.3e.CrossRefPubMed
31.
go back to reference Petri M, Lakatta C, Magder L, Goldman D: Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med. 1994, 96: 254-259. 10.1016/0002-9343(94)90151-1.CrossRefPubMed Petri M, Lakatta C, Magder L, Goldman D: Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med. 1994, 96: 254-259. 10.1016/0002-9343(94)90151-1.CrossRefPubMed
32.
go back to reference Doria A, Shoenfeld Y, Wu R, Gambari PF, Puato M, Ghirardello A, Gilburd B, Corbanese S, Patnaik M, Zampieri S, Peter JB, Favaretto E, Iaccarino L, Sherer Y, Todesco S, Pauletto P: Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis. 2003, 62: 1071-1077. 10.1136/ard.62.11.1071.PubMedCentralCrossRefPubMed Doria A, Shoenfeld Y, Wu R, Gambari PF, Puato M, Ghirardello A, Gilburd B, Corbanese S, Patnaik M, Zampieri S, Peter JB, Favaretto E, Iaccarino L, Sherer Y, Todesco S, Pauletto P: Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis. 2003, 62: 1071-1077. 10.1136/ard.62.11.1071.PubMedCentralCrossRefPubMed
33.
go back to reference Roman MJ, Shanker B, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE: Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003, 349: 2399-2406. 10.1056/NEJMoa035471.CrossRefPubMed Roman MJ, Shanker B, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE: Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003, 349: 2399-2406. 10.1056/NEJMoa035471.CrossRefPubMed
34.
go back to reference Folsom AR, Aleksic N, Catellier D, Juneja HS, Wu KK: C-reactive protein and incident coronary heart disease in the Atherosclerosis Risk In Communities (ARIC) study. Am Heart J. 2002, 144: 233-238. 10.1067/mhj.2002.124054.CrossRefPubMed Folsom AR, Aleksic N, Catellier D, Juneja HS, Wu KK: C-reactive protein and incident coronary heart disease in the Atherosclerosis Risk In Communities (ARIC) study. Am Heart J. 2002, 144: 233-238. 10.1067/mhj.2002.124054.CrossRefPubMed
35.
go back to reference Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH: Plasma concentration of C-reactive protein and risk of developing peripheral vascular disease. Circulation. 1998, 97: 425-428.CrossRefPubMed Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH: Plasma concentration of C-reactive protein and risk of developing peripheral vascular disease. Circulation. 1998, 97: 425-428.CrossRefPubMed
36.
go back to reference Kucharz EJ, Grucka-Mamczar E, Mamczar A, Brzezinska-Wcislo L: Acute-phase proteins in patients with systemic sclerosis. Clin Rheumatol. 2000, 19: 165-166. 10.1007/s100670050039.CrossRefPubMed Kucharz EJ, Grucka-Mamczar E, Mamczar A, Brzezinska-Wcislo L: Acute-phase proteins in patients with systemic sclerosis. Clin Rheumatol. 2000, 19: 165-166. 10.1007/s100670050039.CrossRefPubMed
37.
go back to reference Valentini G, Silman AJ, Veale D: Assessment of disease activity. Clin Exp Rheumatol. 2003, 21: S39-S41.PubMed Valentini G, Silman AJ, Veale D: Assessment of disease activity. Clin Exp Rheumatol. 2003, 21: S39-S41.PubMed
38.
go back to reference De Leeuw K, Freire B, Smit AJ, Bootsma H, Kallenberg CG, Bijl M: Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus. Lupus. 2006, 15: 675-682. 10.1177/0961203306069972.CrossRefPubMed De Leeuw K, Freire B, Smit AJ, Bootsma H, Kallenberg CG, Bijl M: Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus. Lupus. 2006, 15: 675-682. 10.1177/0961203306069972.CrossRefPubMed
39.
go back to reference Poredos P: Intima-media thickness: indicator of cardiovascular risk and measure of the extent of atherosclerosis. Vasc Med. 2004, 9: 46-54. 10.1191/1358863x04vm514ra.CrossRefPubMed Poredos P: Intima-media thickness: indicator of cardiovascular risk and measure of the extent of atherosclerosis. Vasc Med. 2004, 9: 46-54. 10.1191/1358863x04vm514ra.CrossRefPubMed
40.
go back to reference Simon A, Gariepy J, Chironi G, Megnien JL, Levenson J: Intima-media thickness: a new tool for diagnosis and treatment of cardiovascular risk. J Hypertens. 2002, 20: 159-169. 10.1097/00004872-200202000-00001.CrossRefPubMed Simon A, Gariepy J, Chironi G, Megnien JL, Levenson J: Intima-media thickness: a new tool for diagnosis and treatment of cardiovascular risk. J Hypertens. 2002, 20: 159-169. 10.1097/00004872-200202000-00001.CrossRefPubMed
41.
go back to reference Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M: Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007, 115: 459-467. 10.1161/CIRCULATIONAHA.106.628875.CrossRefPubMed Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M: Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007, 115: 459-467. 10.1161/CIRCULATIONAHA.106.628875.CrossRefPubMed
Metadata
Title
Early atherosclerosis in systemic sclerosis and its relation to disease or traditional risk factors
Authors
Martha E Hettema
Dan Zhang
Karina de Leeuw
Ymkje Stienstra
Andries J Smit
Cees GM Kallenberg
Hendrika Bootsma
Publication date
01-04-2008
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 2/2008
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar2408

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