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Published in: Clinical Rheumatology 11/2009

01-11-2009 | Original Article

Subclinical atherosclerosis and endothelial dysfunction in young South-Asian patients with systemic lupus erythematosus

Authors: Parasar Ghosh, Amresh Kumar, Sudeep Kumar, Amita Aggarwal, Nakul Sinha, Ramnath Misra

Published in: Clinical Rheumatology | Issue 11/2009

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Abstract

Patients with systemic lupus erythematosus (SLE), especially Asian Indians, are at increased risk of developing premature atherosclerosis. To find out the prevalence and predictors of carotid intima-medial thickness (IMT) and brachial artery flow-mediated dilatation (FMD). Endothelial dysfunction was assessed by FMD in brachial artery and IMT was measured in common carotid artery in SLE patients and healthy controls. Sixty SLE patients (mean age 31 ± 9 years) and 38 healthy controls (mean age 34 ± 6 years) were included. The IMT was higher in SLE patients as compared to controls (0.49 ± 0.08 mm vs. 0.39 ± 0.05 mm, p < 0.0001). SLE and damage were independent predictors of abnormal IMT. FMD was impaired in SLE patients compared to controls (9.97% vs. 18.97%, p < 0.00001). None of the classical cardiovascular risk factors were predictors of FMD or abnormal IMT. Indian patients with SLE have higher prevalence of subclinical atherosclerosis and endothelial dysfunction. Presence of damage was associated with abnormal IMT in SLE patients.
Literature
1.
go back to reference Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA (1976) The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 60:221–225PubMedCrossRef Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA (1976) The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 60:221–225PubMedCrossRef
2.
go back to reference Bjornadal L, Yin L, Granath F, Klareskog L, Ekbom A (2004) Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: results from a Swedish population based study 1964–95. J Rheumatol 31:713–719PubMed Bjornadal L, Yin L, Granath F, Klareskog L, Ekbom A (2004) Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: results from a Swedish population based study 1964–95. J Rheumatol 31:713–719PubMed
3.
go back to reference Esdaile JM, Abrahamowicz M, Grodzicky T et al (2001) Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 44:2331–2337PubMedCrossRef Esdaile JM, Abrahamowicz M, Grodzicky T et al (2001) Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 44:2331–2337PubMedCrossRef
4.
go back to reference Manzi S, Meilahn EN, Rairie JE et al (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am J Epidemiol 145:408–415PubMed Manzi S, Meilahn EN, Rairie JE et al (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am J Epidemiol 145:408–415PubMed
5.
go back to reference Vita JA, Keaney JF Jr, Larson MG et al (2004) Brachial artery vasodilator function and systemic inflammation in the Framingham offspring study. Circulation 110:3604–3609PubMedCrossRef Vita JA, Keaney JF Jr, Larson MG et al (2004) Brachial artery vasodilator function and systemic inflammation in the Framingham offspring study. Circulation 110:3604–3609PubMedCrossRef
6.
go back to reference Vlachoyiannopoulos PG, Kanellopoulos PG, Ioannidis JP, Tektonidou MG, Mastorakou I, Moutsopoulos HM (2003) Atherosclerosis in premenopausal women with antiphospholipid syndrome and systemic lupus erythematosus: a controlled study. Rheumatology (Oxford) 42:645–651CrossRef Vlachoyiannopoulos PG, Kanellopoulos PG, Ioannidis JP, Tektonidou MG, Mastorakou I, Moutsopoulos HM (2003) Atherosclerosis in premenopausal women with antiphospholipid syndrome and systemic lupus erythematosus: a controlled study. Rheumatology (Oxford) 42:645–651CrossRef
7.
go back to reference de Leeuw K, Sanders JS, Stegeman C, Smit A, Kallenberg CG, Bijl M (2005) Accelerated atherosclerosis in patients with Wegener's granulomatosis. Ann Rheum Dis 64:753–759PubMedCrossRef de Leeuw K, Sanders JS, Stegeman C, Smit A, Kallenberg CG, Bijl M (2005) Accelerated atherosclerosis in patients with Wegener's granulomatosis. Ann Rheum Dis 64:753–759PubMedCrossRef
8.
go back to reference Petri M, Lakatta C, Magder L, Goldman D (1994) Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med 96:254–259PubMedCrossRef Petri M, Lakatta C, Magder L, Goldman D (1994) Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med 96:254–259PubMedCrossRef
9.
go back to reference Roman MJ, Shanker BA, Davis A et al (2003) Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 349:2399–2406PubMedCrossRef Roman MJ, Shanker BA, Davis A et al (2003) Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 349:2399–2406PubMedCrossRef
10.
go back to reference Greenland P, Abrams J, Aurigemma GP et al (2000) Prevention Conference V: beyond secondary prevention: identifying the high-risk patient for primary prevention: noninvasive tests of atherosclerotic burden: Writing Group III. Circulation 101:E16–E22PubMed Greenland P, Abrams J, Aurigemma GP et al (2000) Prevention Conference V: beyond secondary prevention: identifying the high-risk patient for primary prevention: noninvasive tests of atherosclerotic burden: Writing Group III. Circulation 101:E16–E22PubMed
11.
go back to reference Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE (1997) Common carotid intima–media thickness and risk of stroke and myocardial infarction: the Rotterdam study. Circulation 96:1432–1437PubMed Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE (1997) Common carotid intima–media thickness and risk of stroke and myocardial infarction: the Rotterdam study. Circulation 96:1432–1437PubMed
12.
go back to reference Chambless LE, Heiss G, Folsom AR et al (1997) Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) study, 1987–1993. Am J Epidemiol 146:483–494PubMed Chambless LE, Heiss G, Folsom AR et al (1997) Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) study, 1987–1993. Am J Epidemiol 146:483–494PubMed
13.
go back to reference Hodis HN, Mack WJ, LaBree L et al (1998) The role of carotid arterial intima–media thickness in predicting clinical coronary events. Ann Intern Med 128:262–269PubMed Hodis HN, Mack WJ, LaBree L et al (1998) The role of carotid arterial intima–media thickness in predicting clinical coronary events. Ann Intern Med 128:262–269PubMed
14.
go back to reference O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr (1999) 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 340:14–22PubMedCrossRef O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr (1999) 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 340:14–22PubMedCrossRef
15.
go back to reference Manzi S, Selzer F, Sutton-Tyrrell K et al (1999) Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 42:51–60PubMedCrossRef Manzi S, Selzer F, Sutton-Tyrrell K et al (1999) Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 42:51–60PubMedCrossRef
16.
go back to reference Selzer F, Sutton-Tyrrell K, Fitzgerald SG et al (2004) Comparison of risk factors for vascular disease in the carotid artery and aorta in women with systemic lupus erythematosus. Arthritis Rheum 50:151–159PubMedCrossRef Selzer F, Sutton-Tyrrell K, Fitzgerald SG et al (2004) Comparison of risk factors for vascular disease in the carotid artery and aorta in women with systemic lupus erythematosus. Arthritis Rheum 50:151–159PubMedCrossRef
17.
go back to reference Piper MK, Raza K, Nuttall SL et al (2007) Impaired endothelial function in systemic lupus erythematosus. Lupus 16:84–88PubMedCrossRef Piper MK, Raza K, Nuttall SL et al (2007) Impaired endothelial function in systemic lupus erythematosus. Lupus 16:84–88PubMedCrossRef
18.
go back to reference Lima DS, Sato EI, Lima VC, Miranda F Jr, Hatta FH (2002) Brachial endothelial function is impaired in patients with systemic lupus erythematosus. J Rheumatol 29:292–297PubMed Lima DS, Sato EI, Lima VC, Miranda F Jr, Hatta FH (2002) Brachial endothelial function is impaired in patients with systemic lupus erythematosus. J Rheumatol 29:292–297PubMed
19.
go back to reference El-Magadmi M, Bodill H, Ahmad Y et al (2004) Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 110:399–404PubMedCrossRef El-Magadmi M, Bodill H, Ahmad Y et al (2004) Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 110:399–404PubMedCrossRef
20.
go back to reference Mohan V, Deepa R (2004) Risk factors for coronary artery disease in Indians. J Assoc Physicians India 52:95–97PubMed Mohan V, Deepa R (2004) Risk factors for coronary artery disease in Indians. J Assoc Physicians India 52:95–97PubMed
21.
go back to reference Enas EA, Yusuf S, Mehta JL (1992) Prevalence of coronary artery disease in Asian Indians. Am J Cardiol 70:945–949PubMedCrossRef Enas EA, Yusuf S, Mehta JL (1992) Prevalence of coronary artery disease in Asian Indians. Am J Cardiol 70:945–949PubMedCrossRef
22.
go back to reference McKeigue PM, Miller GJ, Marmot MG (1989) Coronary heart disease in South Asians overseas: a review. J Clin Epidemiol 42:597–609PubMedCrossRef McKeigue PM, Miller GJ, Marmot MG (1989) Coronary heart disease in South Asians overseas: a review. J Clin Epidemiol 42:597–609PubMedCrossRef
23.
go back to reference Bhatt SP, Handa R, Gulati GS et al (2006) Atherosclerosis in Asian Indians with systemic lupus erythematosus. Scand J Rheumatol 35:128–132PubMedCrossRef Bhatt SP, Handa R, Gulati GS et al (2006) Atherosclerosis in Asian Indians with systemic lupus erythematosus. Scand J Rheumatol 35:128–132PubMedCrossRef
24.
go back to reference Grover S, Sinha RP, Singh U, Tewari S, Aggarwal A, Misra R (2006) Subclinical atherosclerosis in rheumatoid arthritis in India. J Rheumatol 33:244–247PubMed Grover S, Sinha RP, Singh U, Tewari S, Aggarwal A, Misra R (2006) Subclinical atherosclerosis in rheumatoid arthritis in India. J Rheumatol 33:244–247PubMed
25.
go back to reference Bahl VK, Sharma G (2001) Coping with syncope: tilt towards pacing. Indian Heart J 53:415–422PubMed Bahl VK, Sharma G (2001) Coping with syncope: tilt towards pacing. Indian Heart J 53:415–422PubMed
26.
go back to reference Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725PubMedCrossRef Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725PubMedCrossRef
27.
go back to reference Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640PubMedCrossRef Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640PubMedCrossRef
28.
go back to reference Gladman D, Ginzler E, Goldsmith C et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index for Systemic Lupus Erythematosus. Arthritis Rheum 39:363–369PubMedCrossRef Gladman D, Ginzler E, Goldsmith C et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index for Systemic Lupus Erythematosus. Arthritis Rheum 39:363–369PubMedCrossRef
29.
go back to reference Sidhu PS, Desai SR (1997) A simple and reproducible method for assessing intimal–medial thickness of the common carotid artery. Br J Radiol 70:85–89PubMed Sidhu PS, Desai SR (1997) A simple and reproducible method for assessing intimal–medial thickness of the common carotid artery. Br J Radiol 70:85–89PubMed
30.
go back to reference Corretti MC, Anderson TJ, Benjamin EJ et al (2002) 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 39:257–265PubMedCrossRef Corretti MC, Anderson TJ, Benjamin EJ et al (2002) 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 39:257–265PubMedCrossRef
31.
go back to reference Svenungsson E, Jensen-Urstad K, Heimburger M et al (2001) Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 104:1887–1893PubMedCrossRef Svenungsson E, Jensen-Urstad K, Heimburger M et al (2001) Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 104:1887–1893PubMedCrossRef
32.
go back to reference Reichlin M, Fesmire J, Quintero-Del-Rio AI, Wolfson-Reichlin M (2002) Autoantibodies to lipoprotein lipase and dyslipidemia in systemic lupus erythematosus. Arthritis Rheum 46:2957–2963PubMedCrossRef Reichlin M, Fesmire J, Quintero-Del-Rio AI, Wolfson-Reichlin M (2002) Autoantibodies to lipoprotein lipase and dyslipidemia in systemic lupus erythematosus. Arthritis Rheum 46:2957–2963PubMedCrossRef
33.
go back to reference Doria A, Shoenfeld Y, Wu R et al (2003) Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis 62:1071–1077PubMedCrossRef Doria A, Shoenfeld Y, Wu R et al (2003) Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis 62:1071–1077PubMedCrossRef
34.
go back to reference Souza AW, Hatta FS, Miranda F Jr, Sato EI (2005) Atherosclerotic plaque in carotid arteries in systemic lupus erythematosus: frequency and associated risk factors. Sao Paulo Med J 123:137–142PubMedCrossRef Souza AW, Hatta FS, Miranda F Jr, Sato EI (2005) Atherosclerotic plaque in carotid arteries in systemic lupus erythematosus: frequency and associated risk factors. Sao Paulo Med J 123:137–142PubMedCrossRef
35.
go back to reference Jimenez S, Garcia-Criado MA, Tassies D et al (2005) Preclinical vascular disease in systemic lupus erythematosus and primary antiphospholipid syndrome. Rheumatology (Oxford) 44:756–761CrossRef Jimenez S, Garcia-Criado MA, Tassies D et al (2005) Preclinical vascular disease in systemic lupus erythematosus and primary antiphospholipid syndrome. Rheumatology (Oxford) 44:756–761CrossRef
36.
go back to reference Colombo BM, Murdaca G, Caiti M et al (2007) Intima–media thickness: a marker of accelerated atherosclerosis in women with systemic lupus erythematosus. Ann N Y Acad Sci 1108:121–126PubMedCrossRef Colombo BM, Murdaca G, Caiti M et al (2007) Intima–media thickness: a marker of accelerated atherosclerosis in women with systemic lupus erythematosus. Ann N Y Acad Sci 1108:121–126PubMedCrossRef
37.
go back to reference Sato H, Miida T, Wada Y et al (2007) Atherosclerosis is accelerated in patients with long-term well-controlled systemic lupus erythematosus (SLE). Clin Chim Acta 385:35–42PubMedCrossRef Sato H, Miida T, Wada Y et al (2007) Atherosclerosis is accelerated in patients with long-term well-controlled systemic lupus erythematosus (SLE). Clin Chim Acta 385:35–42PubMedCrossRef
38.
go back to reference Lopez LR, Salazar-Paramo M, Palafox-Sanchez C, Hurley BL, Matsuura E, Garcia-De La Torre I (2006) Oxidized low-density lipoprotein and beta2-glycoprotein in patients with systemic lupus erythematosus and increased carotid intima–media thickness: implications in autoimmune-mediated atherosclerosis. Lupus 15:80–86PubMedCrossRef Lopez LR, Salazar-Paramo M, Palafox-Sanchez C, Hurley BL, Matsuura E, Garcia-De La Torre I (2006) Oxidized low-density lipoprotein and beta2-glycoprotein in patients with systemic lupus erythematosus and increased carotid intima–media thickness: implications in autoimmune-mediated atherosclerosis. Lupus 15:80–86PubMedCrossRef
39.
go back to reference Wolak T, Todosoui E, Szendro G et al (2004) Duplex study of the carotid and femoral arteries of patients with systemic lupus erythematosus: a controlled study. J Rheumatol 31:909–914PubMed Wolak T, Todosoui E, Szendro G et al (2004) Duplex study of the carotid and femoral arteries of patients with systemic lupus erythematosus: a controlled study. J Rheumatol 31:909–914PubMed
40.
go back to reference Anderson TJ, Elstein E, Haber H, Charbonneau F (2000) Comparative study of ACE-inhibition, angiotensin II antagonism, and calcium channel blockade on flow-mediated vasodilation in patients with coronary disease (BANFF study). J Am Coll Cardiol 35:60–66PubMedCrossRef Anderson TJ, Elstein E, Haber H, Charbonneau F (2000) Comparative study of ACE-inhibition, angiotensin II antagonism, and calcium channel blockade on flow-mediated vasodilation in patients with coronary disease (BANFF study). J Am Coll Cardiol 35:60–66PubMedCrossRef
41.
go back to reference Ghiadoni L, Magagna A, Versari D et al (2003) Different effect of antihypertensive drugs on conduit artery endothelial function. Hypertension 41:1281–1286PubMedCrossRef Ghiadoni L, Magagna A, Versari D et al (2003) Different effect of antihypertensive drugs on conduit artery endothelial function. Hypertension 41:1281–1286PubMedCrossRef
42.
go back to reference Mancini GB, Henry GC, Macaya C et al (1996) Angiotensin-converting enzyme inhibition with quinapril improves endothelial vasomotor dysfunction in patients with coronary artery disease. The TREND (trial on reversing endothelial dysfunction) study. Circulation 94:258–265PubMed Mancini GB, Henry GC, Macaya C et al (1996) Angiotensin-converting enzyme inhibition with quinapril improves endothelial vasomotor dysfunction in patients with coronary artery disease. The TREND (trial on reversing endothelial dysfunction) study. Circulation 94:258–265PubMed
43.
go back to reference Sudhir K, MacGregor JS, Gupta M et al (1993) Effect of selective angiotensin II receptor antagonism and angiotensin converting enzyme inhibition on the coronary vasculature in vivo. Intravascular two-dimensional and Doppler ultrasound studies. Circulation 87:931–938PubMed Sudhir K, MacGregor JS, Gupta M et al (1993) Effect of selective angiotensin II receptor antagonism and angiotensin converting enzyme inhibition on the coronary vasculature in vivo. Intravascular two-dimensional and Doppler ultrasound studies. Circulation 87:931–938PubMed
44.
go back to reference Kawamoto R, Ohtsuka N, Kusunoki T, Yorimitsu N (2008) An association between the estimated glomerular filtration rate and carotid atherosclerosis. Intern Med 47:391–398PubMedCrossRef Kawamoto R, Ohtsuka N, Kusunoki T, Yorimitsu N (2008) An association between the estimated glomerular filtration rate and carotid atherosclerosis. Intern Med 47:391–398PubMedCrossRef
45.
go back to reference Thambyrajah J, Landray MJ, McGlynn FJ, Jones HJ, Wheeler DC, Townend JN (2000) Abnormalities of endothelial function in patients with predialysis renal failure. Heart 83:205–209PubMedCrossRef Thambyrajah J, Landray MJ, McGlynn FJ, Jones HJ, Wheeler DC, Townend JN (2000) Abnormalities of endothelial function in patients with predialysis renal failure. Heart 83:205–209PubMedCrossRef
46.
go back to reference Hashimoto M, Eto M, Akishita M et al (1999) Correlation between flow-mediated vasodilatation of the brachial artery and intima–media thickness in the carotid artery in men. Arterioscler Thromb Vasc Biol 19:2795–2800PubMed Hashimoto M, Eto M, Akishita M et al (1999) Correlation between flow-mediated vasodilatation of the brachial artery and intima–media thickness in the carotid artery in men. Arterioscler Thromb Vasc Biol 19:2795–2800PubMed
47.
go back to reference Urowitz MB, Ibanez D, Gladman DD (2007) Atherosclerotic vascular events in a single large lupus cohort: prevalence and risk factors. J Rheumatol 34:70–75PubMed Urowitz MB, Ibanez D, Gladman DD (2007) Atherosclerotic vascular events in a single large lupus cohort: prevalence and risk factors. J Rheumatol 34:70–75PubMed
48.
go back to reference Petri M, Perez-Gutthann S, Spence D, Hochberg MC (1992) Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 93:513–519PubMedCrossRef Petri M, Perez-Gutthann S, Spence D, Hochberg MC (1992) Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 93:513–519PubMedCrossRef
49.
go back to reference Shah MA, Shah AM, Krishnan E (2009) Poor outcomes after acute myocardial infarction in systemic lupus erythematosus. J Rheumatol 36:570–575PubMedCrossRef Shah MA, Shah AM, Krishnan E (2009) Poor outcomes after acute myocardial infarction in systemic lupus erythematosus. J Rheumatol 36:570–575PubMedCrossRef
50.
go back to reference Urowitz MB, Gladman DD (2008) The SLICC inception cohort for atherosclerosis. Curr Rheumatol Rep 10:281–285PubMedCrossRef Urowitz MB, Gladman DD (2008) The SLICC inception cohort for atherosclerosis. Curr Rheumatol Rep 10:281–285PubMedCrossRef
Metadata
Title
Subclinical atherosclerosis and endothelial dysfunction in young South-Asian patients with systemic lupus erythematosus
Authors
Parasar Ghosh
Amresh Kumar
Sudeep Kumar
Amita Aggarwal
Nakul Sinha
Ramnath Misra
Publication date
01-11-2009
Publisher
Springer-Verlag
Published in
Clinical Rheumatology / Issue 11/2009
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-009-1228-6

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