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Published in: Arthritis Research & Therapy 1/2019

Open Access 01-12-2019 | Magnetic Resonance Imaging | Research article

Study of MRI brain findings and carotid US features in systemic sclerosis patients, relationship with disease parameters

Authors: Rania M. Gamal, Hanan Sayed M. Abozaid, Mohmed Zidan, Mohamed Aboel-Kassem F. Abdelmegid, Mohmed Raouf Abdel-Razek, Sahar Abdel-Rahman Alsayed, Amr F. Mourad, Nashwa Mostafa A. Azoz, Lobna Abdel-Wahid Mohram, Daniel E. Furst

Published in: Arthritis Research & Therapy | Issue 1/2019

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Abstract

Background/objectives

Systemic sclerosis (SSc) is an autoimmune disease associated with immune abnormalities and widespread vascular lesions, including increased intimal and medial thickness. These changes may be reflected in early atherosclerosis and cardiovascular risks. We aimed in this study to examine the carotid artery intima-media thickness and MRI brain findings in SSc patients and compared them to a group of normal controls. A relationship between these parameters and clinical measures in SSc was also sought.

Methods

Seventy-two SSc patients with no central nervous system (CNS) symptoms and 42 healthy controls were included. Clinical and laboratory measures, Medsger’s severity scale, and Doppler ultrasound common carotid artery intima-media thickness (CCA-IMT) were measured. Brain fluid-attenuated inversion recovery (FLAIR)-MRI and diffusion-weighted MRI (DWI) were also done.

Results

SSc patients had more CCA-IMT, higher CRP, and more brain MRI hyperintense lesions than controls (P < 0.05). Significant positive correlations existed between CCA-IMT and Medsger vascular (r = 0.7, P = 0.02). The FLAIR-MRI showed multiple hyperintense lesions in 24 patients (33%), ranging 0–36 lesions. SSc patients with more lesions (positive MRI) had longer disease duration (P = 0.001) and left and right carotid artery atheromata (P = 0.001, and 0.013, respectively) than SSc patients with negative MRIs; Medsger vascular score did not separate the SSc groups (P = 0.08).

Conclusions

In systemic sclerosis patients without central nervous system symptoms, MRI lesion numbers correlated with CCA-IMT. MRI abnormalities were found more frequently if CRP was elevated, if the Medsger SSc Severity Scale was increased, or if there was thickened carotid IMT.
Literature
1.
go back to reference Kahalefp MB, Leroy EC. Autoimmunity and vascular involvement in systemic sclerosis (SSc). Autoimmunity. 1999;31(3):195–214.CrossRef Kahalefp MB, Leroy EC. Autoimmunity and vascular involvement in systemic sclerosis (SSc). Autoimmunity. 1999;31(3):195–214.CrossRef
2.
go back to reference Varga J, Trojanowska M, Kuwana M. Pathogenesis of systemic sclerosis: recent insights of molecular and cellular mechanisms and therapeutic opportunities. J Scleroderma Relat Disord. 2017;2(3):137–52.CrossRef Varga J, Trojanowska M, Kuwana M. Pathogenesis of systemic sclerosis: recent insights of molecular and cellular mechanisms and therapeutic opportunities. J Scleroderma Relat Disord. 2017;2(3):137–52.CrossRef
3.
go back to reference LeRoy EC. Systemic sclerosis: a vascular perspective. Rheum Dis Clin N Am. 1996;22(4):675–94.CrossRef LeRoy EC. Systemic sclerosis: a vascular perspective. Rheum Dis Clin N Am. 1996;22(4):675–94.CrossRef
4.
go back to reference Mackiewicz Z, et al. Increased but imbalanced expression of VEGF and its receptors has no positive effect on angiogenesis in systemic sclerosis skin. Clin Exp Rheumatol. 2002;20(5):641–6.PubMed Mackiewicz Z, et al. Increased but imbalanced expression of VEGF and its receptors has no positive effect on angiogenesis in systemic sclerosis skin. Clin Exp Rheumatol. 2002;20(5):641–6.PubMed
5.
go back to reference Ho M, et al. Macrovascular disease and systemic sclerosis. Ann Rheum Dis. 2000;59(1):39–43.CrossRef Ho M, et al. Macrovascular disease and systemic sclerosis. Ann Rheum Dis. 2000;59(1):39–43.CrossRef
6.
go back to reference Veale D, Collidge T, Belch J. Increased prevalence of symptomatic macrovascular disease in systemic sclerosis. Ann Rheum Dis. 1995;54(10):853–5.CrossRef Veale D, Collidge T, Belch J. Increased prevalence of symptomatic macrovascular disease in systemic sclerosis. Ann Rheum Dis. 1995;54(10):853–5.CrossRef
7.
go back to reference Gamal RM, Gamal WM, Ghandour AM, Abozaid HSM, Mohamed ME, Emad Y, Abdel Galeel A. Study of the osteoprotegerin/receptor activator of nuclear factor-kB ligand system association with inflammation and atherosclerosis in systemic sclerosis. Immunological investigations 2018;47(3):241–250CrossRef Gamal RM, Gamal WM, Ghandour AM, Abozaid HSM, Mohamed ME, Emad Y, Abdel Galeel A. Study of the osteoprotegerin/receptor activator of nuclear factor-kB ligand system association with inflammation and atherosclerosis in systemic sclerosis. Immunological investigations 2018;47(3):241–250CrossRef
8.
go back to reference Ngian G-S, et al. Cardiovascular disease in systemic sclerosis-an emerging association? Arthritis Res Ther. 2011;13(4):237.CrossRef Ngian G-S, et al. Cardiovascular disease in systemic sclerosis-an emerging association? Arthritis Res Ther. 2011;13(4):237.CrossRef
9.
go back to reference Alkaabi J, et al. Rheumatoid arthritis and macrovascular disease. Rheumatology. 2003;42(2):292–7.CrossRef Alkaabi J, et al. Rheumatoid arthritis and macrovascular disease. Rheumatology. 2003;42(2):292–7.CrossRef
10.
go back to reference El Sayed AM, et al. Insulin resistance as a risk factor for subclinical atherosclerosis in rheumatoid arthritis. Egypt Rheumatol. 2014;36(1):7–13.CrossRef El Sayed AM, et al. Insulin resistance as a risk factor for subclinical atherosclerosis in rheumatoid arthritis. Egypt Rheumatol. 2014;36(1):7–13.CrossRef
11.
go back to reference Rizk A, et al. The impact of obesity in systemic lupus erythematosus on disease parameters, quality of life, functional capacity and the risk of atherosclerosis. Int J Rheum Dis. 2012;15(3):261–7.CrossRef Rizk A, et al. The impact of obesity in systemic lupus erythematosus on disease parameters, quality of life, functional capacity and the risk of atherosclerosis. Int J Rheum Dis. 2012;15(3):261–7.CrossRef
12.
go back to reference Fouda N, Abd-Elaziz H, Fouda EM. Assessment of subclinical carotid atherosclerosis in patients with primary osteoarthritis: correlation with disease severity and insulin resistance. Egypt Rheumatol. 2014;36(2):85–91.CrossRef Fouda N, Abd-Elaziz H, Fouda EM. Assessment of subclinical carotid atherosclerosis in patients with primary osteoarthritis: correlation with disease severity and insulin resistance. Egypt Rheumatol. 2014;36(2):85–91.CrossRef
13.
go back to reference Nowaczenko M, Sarzyńska-Długosz I, Członkowska A. Prevalence of carotid arteries atherosclerotic changes in ischemic stroke patients. Neurol Neurochir Pol. 2002;37(1):27–36. Nowaczenko M, Sarzyńska-Długosz I, Członkowska A. Prevalence of carotid arteries atherosclerotic changes in ischemic stroke patients. Neurol Neurochir Pol. 2002;37(1):27–36.
14.
go back to reference Cao JJ, et al. C-reactive protein, carotid intima-media thickness, and incidence of ischemic stroke in the elderly. Circulation. 2003;108(2):166–70.CrossRef Cao JJ, et al. C-reactive protein, carotid intima-media thickness, and incidence of ischemic stroke in the elderly. Circulation. 2003;108(2):166–70.CrossRef
15.
go back to reference Handa N, et al. Ischemic stroke events and carotid atherosclerosis. Stroke. 1995;26(10):1781–6.CrossRef Handa N, et al. Ischemic stroke events and carotid atherosclerosis. Stroke. 1995;26(10):1781–6.CrossRef
16.
go back to reference Hunt KJ, et al. Acoustic shadowing on B-mode ultrasound of the carotid artery predicts ischemic stroke. Stroke. 2001;32(5):1120–6.CrossRef Hunt KJ, et al. Acoustic shadowing on B-mode ultrasound of the carotid artery predicts ischemic stroke. Stroke. 2001;32(5):1120–6.CrossRef
17.
go back to reference Oliviero U, et al. Carotid atherosclerosis and ischemic stroke in young patients. Int Angiol. 2002;21(2):117.PubMed Oliviero U, et al. Carotid atherosclerosis and ischemic stroke in young patients. Int Angiol. 2002;21(2):117.PubMed
18.
go back to reference Ogihara T, et al. The Japanese Society of Hypertension guidelines for the management of hypertension (JSH 2009). Hypertens Res. 2009;32(1):3–107.PubMed Ogihara T, et al. The Japanese Society of Hypertension guidelines for the management of hypertension (JSH 2009). Hypertens Res. 2009;32(1):3–107.PubMed
19.
go back to reference Cifkova R, et al. Practice guidelines for primary care physicians: 2003 ESH/ESC hypertension guidelines. J Hypertens. 2003;21(10):1779–86.CrossRef Cifkova R, et al. Practice guidelines for primary care physicians: 2003 ESH/ESC hypertension guidelines. J Hypertens. 2003;21(10):1779–86.CrossRef
20.
go back to reference Bernick C, et al. Silent MRI infarcts and the risk of future stroke: the cardiovascular health study. Neurology. 2001;57(7):1222–9.CrossRef Bernick C, et al. Silent MRI infarcts and the risk of future stroke: the cardiovascular health study. Neurology. 2001;57(7):1222–9.CrossRef
21.
go back to reference Vermeer SE, et al. Silent brain infarcts and white matter lesions increase stroke risk in the general population. Stroke. 2003;34(5):1126–9.CrossRef Vermeer SE, et al. Silent brain infarcts and white matter lesions increase stroke risk in the general population. Stroke. 2003;34(5):1126–9.CrossRef
22.
go back to reference Fujikawa T, Yamawaki S, Touhouda Y. Background factors and clinical symptoms of major depression with silent cerebral infarction. Stroke. 1994;25(4):798–801.CrossRef Fujikawa T, Yamawaki S, Touhouda Y. Background factors and clinical symptoms of major depression with silent cerebral infarction. Stroke. 1994;25(4):798–801.CrossRef
23.
go back to reference Yanai I, et al. The 3-year course and outcome of patients with major depression and silent cerebral infarction. J Affect Disord. 1998;47(1):25–30.CrossRef Yanai I, et al. The 3-year course and outcome of patients with major depression and silent cerebral infarction. J Affect Disord. 1998;47(1):25–30.CrossRef
24.
go back to reference Gass A, et al. Diffusion-weighted MRI for the “small stuff”: the details of acute cerebral ischaemia. Lancet Neurol. 2004;3(1):39–45.CrossRef Gass A, et al. Diffusion-weighted MRI for the “small stuff”: the details of acute cerebral ischaemia. Lancet Neurol. 2004;3(1):39–45.CrossRef
25.
go back to reference Rovaris M, et al. The contribution of fast-FLAIR MRI for lesion detection in the brain of patients with systemic autoimmune diseases. J Neurol. 2000;247(1):29–33.CrossRef Rovaris M, et al. The contribution of fast-FLAIR MRI for lesion detection in the brain of patients with systemic autoimmune diseases. J Neurol. 2000;247(1):29–33.CrossRef
26.
go back to reference van den Hoogen F, et al. Classification criteria for systemic sclerosis: an ACR-EULAR collaborative initiative. Arthritis Rheum. 2013;65(11):2737.CrossRef van den Hoogen F, et al. Classification criteria for systemic sclerosis: an ACR-EULAR collaborative initiative. Arthritis Rheum. 2013;65(11):2737.CrossRef
27.
go back to reference LeROY EC, Medsger TA. Criteria for the classification of early systemic sclerosis. J Rheumatol. 2001;28(7):1573–6.PubMed LeROY EC, Medsger TA. Criteria for the classification of early systemic sclerosis. J Rheumatol. 2001;28(7):1573–6.PubMed
28.
go back to reference Furst DE, et al. The modified Rodnan skin score is an accurate reflection of skin biopsy thickness in systemic sclerosis. J Rheumatol. 1998;25(1):84–8.PubMed Furst DE, et al. The modified Rodnan skin score is an accurate reflection of skin biopsy thickness in systemic sclerosis. J Rheumatol. 1998;25(1):84–8.PubMed
29.
go back to reference Khanna D, et al. Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. J Scleroderma Relat Disord. 2017;2(1):11–8.CrossRef Khanna D, et al. Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. J Scleroderma Relat Disord. 2017;2(1):11–8.CrossRef
30.
go back to reference Medsger T, et al. Assessment of disease severity and prognosis. Clin Exp Rheumatol. 2003;21(3; SUPP/29):S42–6.PubMed Medsger T, et al. Assessment of disease severity and prognosis. Clin Exp Rheumatol. 2003;21(3; SUPP/29):S42–6.PubMed
31.
go back to reference Doria A, et al. Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis. 2003;62(11):1071–7.CrossRef Doria A, et al. Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis. 2003;62(11):1071–7.CrossRef
32.
go back to reference Blaszczyk M, et al. Progressive facial hemiatrophy: central nervous system involvement and relationship with scleroderma en coup de sabre. J Rheumatol. 2003;30(9):1997–2004.PubMed Blaszczyk M, et al. Progressive facial hemiatrophy: central nervous system involvement and relationship with scleroderma en coup de sabre. J Rheumatol. 2003;30(9):1997–2004.PubMed
33.
go back to reference Mohamed RH, Nassef AA. Brain magnetic resonance imaging findings in patients with systemic sclerosis. Int J Rheum Dis. 2010;13(1):61–7.CrossRef Mohamed RH, Nassef AA. Brain magnetic resonance imaging findings in patients with systemic sclerosis. Int J Rheum Dis. 2010;13(1):61–7.CrossRef
34.
go back to reference Stone J, et al. Scleroderma “en coup de sabre”: pathological evidence of intracerebral inflammation. J Neurol Neurosurg Psychiatry. 2001;70(3):382–5.CrossRef Stone J, et al. Scleroderma “en coup de sabre”: pathological evidence of intracerebral inflammation. J Neurol Neurosurg Psychiatry. 2001;70(3):382–5.CrossRef
35.
go back to reference Cypienė A, et al. The impact of systemic sclerosis on arterial wall stiffness parameters and endothelial function. Clin Rheumatol. 2008;27(12):1517–22.CrossRef Cypienė A, et al. The impact of systemic sclerosis on arterial wall stiffness parameters and endothelial function. Clin Rheumatol. 2008;27(12):1517–22.CrossRef
36.
go back to reference Nussinovitch U, Shoenfeld Y. Atherosclerosis and macrovascular involvement in systemic sclerosis: myth or reality. Autoimmun Rev. 2011;10(5):259–66.CrossRef Nussinovitch U, Shoenfeld Y. Atherosclerosis and macrovascular involvement in systemic sclerosis: myth or reality. Autoimmun Rev. 2011;10(5):259–66.CrossRef
37.
go back to reference Mohammed RHA, Sabry YY, Nasef AA. Brain MRI screening showing evidences of early central nervous system involvement in patients with systemic sclerosis. Rheumatol Int. 2011;31(5):667–71.CrossRef Mohammed RHA, Sabry YY, Nasef AA. Brain MRI screening showing evidences of early central nervous system involvement in patients with systemic sclerosis. Rheumatol Int. 2011;31(5):667–71.CrossRef
38.
go back to reference Sardanelli F, et al. White matter hyperintensities on brain magnetic resonance in systemic sclerosis. Ann Rheum Dis. 2005;64(5):777–9.CrossRef Sardanelli F, et al. White matter hyperintensities on brain magnetic resonance in systemic sclerosis. Ann Rheum Dis. 2005;64(5):777–9.CrossRef
39.
go back to reference Gussekloo J, et al. C-reactive protein is a strong but nonspecific risk factor of fatal stroke in elderly persons. Arterioscler Thromb Vasc Biol. 2000;20(4):1047–51.CrossRef Gussekloo J, et al. C-reactive protein is a strong but nonspecific risk factor of fatal stroke in elderly persons. Arterioscler Thromb Vasc Biol. 2000;20(4):1047–51.CrossRef
40.
go back to reference Rost NS, et al. Plasma concentration of C-reactive protein and risk of ischemic stroke and transient ischemic attack. Stroke. 2001;32(11):2575–9.CrossRef Rost NS, et al. Plasma concentration of C-reactive protein and risk of ischemic stroke and transient ischemic attack. Stroke. 2001;32(11):2575–9.CrossRef
41.
go back to reference Blackburn R, et al. Elevated C-reactive protein constitutes an independent predictor of advanced carotid plaques in dyslipidemic subjects. Arterioscler Thromb Vasc Biol. 2001;21(12):1962–8.CrossRef Blackburn R, et al. Elevated C-reactive protein constitutes an independent predictor of advanced carotid plaques in dyslipidemic subjects. Arterioscler Thromb Vasc Biol. 2001;21(12):1962–8.CrossRef
42.
go back to reference Moroni F, et al. Carotid atherosclerosis, silent ischemic brain damage and brain atrophy: a systematic review and meta-analysis. Int J Cardiol. 2016;223:681–7.CrossRef Moroni F, et al. Carotid atherosclerosis, silent ischemic brain damage and brain atrophy: a systematic review and meta-analysis. Int J Cardiol. 2016;223:681–7.CrossRef
43.
go back to reference Tyrrell PN, et al. Rheumatic disease and carotid intima-media thickness. Arterioscler Thromb Vasc Biol. 2010;30(5):1014–26.CrossRef Tyrrell PN, et al. Rheumatic disease and carotid intima-media thickness. Arterioscler Thromb Vasc Biol. 2010;30(5):1014–26.CrossRef
Metadata
Title
Study of MRI brain findings and carotid US features in systemic sclerosis patients, relationship with disease parameters
Authors
Rania M. Gamal
Hanan Sayed M. Abozaid
Mohmed Zidan
Mohamed Aboel-Kassem F. Abdelmegid
Mohmed Raouf Abdel-Razek
Sahar Abdel-Rahman Alsayed
Amr F. Mourad
Nashwa Mostafa A. Azoz
Lobna Abdel-Wahid Mohram
Daniel E. Furst
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2019
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-019-1877-z

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