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Published in: Clinical Rheumatology 7/2019

01-07-2019 | Systemic Sclerosis | Original Article

Neurosonological and cognitive screening for evaluation of systemic sclerosis patients

Authors: B. R. Sakr, R. E. Rabea, A. M. Aboulfotooh, N. A. Kishk

Published in: Clinical Rheumatology | Issue 7/2019

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Abstract

Objective

Assessment of cerebrovascular hemodynamics, third ventricle diameter (as a proxy of brain atrophy) by transcranial sonography (TCS), and screening of cognitive performance by the Symbol Digit Modalities Test (SDMT) in systemic sclerosis (SSc) patients.

Methods

A total of 38 SSc patients recruited from the outpatient clinic of the Rheumatology Department, Kasr Alainy Hospital, Cairo University, and 51, age- and sex-matched, healthy controls were included in the study. TCS was used to assess the mean flow velocity (MFV), pulsatility index (PI) of the anterior, middle, and posterior cerebral arteries bilaterally, and to measure the third ventricle diameter as a proxy of brain atrophy. Cognitive impairment was screened using the SDMT. p values < 0.05 were considered statistically significant.

Results

There was no significant difference between SSc patients and controls regarding either PI or MFV of the anterior, middle, and posterior cerebral arteries; also, there was no difference regarding the third ventricle diameter; however, limited SSc patients showed a significant increase in the PI of PCA and MFV of ACA as compared with diffuse SSc patients (p = 0.005, 0.004). There was a significant difference between SSc patients and controls regarding the SDMT (p = 0.016).

Conclusion

There is an evidence of increased cerebral vascular tone and resistance in limited SSc patients compared with diffuse SSc subgroup, without evidence of cerebral atrophy, suggesting early cerebrovascular affection even in asymptomatic limited SSc patients. There was also an evidence of cognitive impairment in SSc patients.
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Literature
1.
go back to reference Cerinic MM, Generini S, Pignone A, Casale R (1996) The nervous system in systemic sclerosis (scleroderma): clinical features and pathogenetic mechanisms. Rheum Dis Clin N Am 22(4):879–892CrossRef Cerinic MM, Generini S, Pignone A, Casale R (1996) The nervous system in systemic sclerosis (scleroderma): clinical features and pathogenetic mechanisms. Rheum Dis Clin N Am 22(4):879–892CrossRef
2.
go back to reference Roquer J, Segura T, Serena J, Castillo J (2009) Endothelial dysfunction, vascular disease and stroke: the ARTICO study. Cerebrovasc Dis 27(Suppl 1):25–37PubMedCrossRef Roquer J, Segura T, Serena J, Castillo J (2009) Endothelial dysfunction, vascular disease and stroke: the ARTICO study. Cerebrovasc Dis 27(Suppl 1):25–37PubMedCrossRef
3.
go back to reference Héron E, Fornes P, Rance A, Emmerich J, Bayle O, Fiessinger JN (1998) Brain involvement in scleroderma: two autopsy cases. Stroke 29(3):719–721PubMedCrossRef Héron E, Fornes P, Rance A, Emmerich J, Bayle O, Fiessinger JN (1998) Brain involvement in scleroderma: two autopsy cases. Stroke 29(3):719–721PubMedCrossRef
4.
go back to reference Bertinotti L, Mortilla M, Conforti ML, Colangelo N, Nacci F, Del Rosso A et al (2006) Proton magnetic resonance spectroscopy reveals central neuroaxonal impairment in systemic sclerosis. J Rheumatol 33(3):546–551PubMed Bertinotti L, Mortilla M, Conforti ML, Colangelo N, Nacci F, Del Rosso A et al (2006) Proton magnetic resonance spectroscopy reveals central neuroaxonal impairment in systemic sclerosis. J Rheumatol 33(3):546–551PubMed
5.
6.
go back to reference Sloan MA, Alexandrov AV, Tegeler CH, Spencer MP, Caplan LR, Feldmann E et al (2004) Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 62(9):1468–1481PubMedCrossRef Sloan MA, Alexandrov AV, Tegeler CH, Spencer MP, Caplan LR, Feldmann E et al (2004) Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 62(9):1468–1481PubMedCrossRef
7.
go back to reference Halpern EJ, Merton DA, Forsberg F (1998) Effect of distal resistance on Doppler US flow patterns. Radiology 206(3):761–766PubMedCrossRef Halpern EJ, Merton DA, Forsberg F (1998) Effect of distal resistance on Doppler US flow patterns. Radiology 206(3):761–766PubMedCrossRef
8.
go back to reference Naqvi J, Yap KH, Ahmad G, Ghosh J (2013) Transcranial Doppler ultrasound: a review of the physical principles and major applications in critical care. Int J Vasc Med 2013:629378PubMedPubMedCentral Naqvi J, Yap KH, Ahmad G, Ghosh J (2013) Transcranial Doppler ultrasound: a review of the physical principles and major applications in critical care. Int J Vasc Med 2013:629378PubMedPubMedCentral
9.
go back to reference Simon JH, Jacobs LD, Campion MK, Rudick RA, Cookfair DL, Herndon RM et al (1999) A longitudinal study of brain atrophy in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Neurology 53(1):139–148PubMedCrossRef Simon JH, Jacobs LD, Campion MK, Rudick RA, Cookfair DL, Herndon RM et al (1999) A longitudinal study of brain atrophy in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Neurology 53(1):139–148PubMedCrossRef
10.
go back to reference McNair S, Hategan A, Bourgeois JA, Losier B (2013) Neuropsychiatric symptoms in scleroderma. Psychosomatics 54(4):382–386PubMedCrossRef McNair S, Hategan A, Bourgeois JA, Losier B (2013) Neuropsychiatric symptoms in scleroderma. Psychosomatics 54(4):382–386PubMedCrossRef
11.
go back to reference Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R (2017) Multiple sclerosis outcome assessments consortium. validity of the symbol digit modalities test as a cognition performance outcome measure for multiple sclerosis. Mult Scler 23(5):721–733PubMedPubMedCentralCrossRef Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R (2017) Multiple sclerosis outcome assessments consortium. validity of the symbol digit modalities test as a cognition performance outcome measure for multiple sclerosis. Mult Scler 23(5):721–733PubMedPubMedCentralCrossRef
12.
go back to reference Silva PHR, Spedo CT, Barreira AA, Leoni RF (2018) Symbol Digit Modalities Test adaptation for magnetic resonance imaging environment: a systematic review and meta-analysis. Mult Scler Relat Disord 20:136–143PubMedCrossRef Silva PHR, Spedo CT, Barreira AA, Leoni RF (2018) Symbol Digit Modalities Test adaptation for magnetic resonance imaging environment: a systematic review and meta-analysis. Mult Scler Relat Disord 20:136–143PubMedCrossRef
13.
go back to reference Goverover Y, Genova HM, Hillary FG, DeLuca J (2007) The relationship between neuropsychological measures and the timed instrumental activities of daily living task in multiple sclerosis. Mult Scler 13(5):636–644PubMedCrossRef Goverover Y, Genova HM, Hillary FG, DeLuca J (2007) The relationship between neuropsychological measures and the timed instrumental activities of daily living task in multiple sclerosis. Mult Scler 13(5):636–644PubMedCrossRef
14.
go back to reference Shucard JL, Lee WH, Safford AS, Shucard DW (2011) The relationship between processing speed and working memory demand in systemic lupus erythematosus: evidence from a visual n-back task. Neuropsychology 25(1):45–52PubMedPubMedCentralCrossRef Shucard JL, Lee WH, Safford AS, Shucard DW (2011) The relationship between processing speed and working memory demand in systemic lupus erythematosus: evidence from a visual n-back task. Neuropsychology 25(1):45–52PubMedPubMedCentralCrossRef
15.
go back to reference Van Schependom J, D’hooghe MB, Cleynhens K, D’hooge M, Haelewyck MC, De Keyser J et al (2014) The Symbol Digit Modalities Test as sentinel test for cognitive impairment in multiple sclerosis. Eur J Neurol 21(9):1219–1225PubMedCrossRef Van Schependom J, D’hooghe MB, Cleynhens K, D’hooge M, Haelewyck MC, De Keyser J et al (2014) The Symbol Digit Modalities Test as sentinel test for cognitive impairment in multiple sclerosis. Eur J Neurol 21(9):1219–1225PubMedCrossRef
16.
go back to reference Pascoe M, Alamri Y, Dalrymple-Alford J, Anderson T, MacAskill M (2018) The Symbol-Digit Modalities Test in mild cognitive impairment: evidence from Parkinson’s disease patients. Eur Neurol 79(3–4):206–210PubMedCrossRef Pascoe M, Alamri Y, Dalrymple-Alford J, Anderson T, MacAskill M (2018) The Symbol-Digit Modalities Test in mild cognitive impairment: evidence from Parkinson’s disease patients. Eur Neurol 79(3–4):206–210PubMedCrossRef
17.
go back to reference Forn C, Belloch V, Bustamante JC, Garbin G, Parcet-Ibars MA, Sanjuan A et al (2009) A Symbol Digit Modalities Test version suitable for functional MRI studies. Neurosci Lett 456(1):11–14PubMedCrossRef Forn C, Belloch V, Bustamante JC, Garbin G, Parcet-Ibars MA, Sanjuan A et al (2009) A Symbol Digit Modalities Test version suitable for functional MRI studies. Neurosci Lett 456(1):11–14PubMedCrossRef
18.
go back to reference Randolph JJ, Arnett PA, Higginson CI (2001) Metamemory and tested cognitive functioning in multiple sclerosis. Clin Neuropsychol 15(3):357–368PubMedCrossRef Randolph JJ, Arnett PA, Higginson CI (2001) Metamemory and tested cognitive functioning in multiple sclerosis. Clin Neuropsychol 15(3):357–368PubMedCrossRef
19.
go back to reference Parmenter BA, Weinstock-Guttman B, Garg N, Munschauer F, Benedict RH (2007) Screening for cognitive impairment in multiple sclerosis using the Symbol Digit Modalities Test. Mult Scler 13(1):52–57PubMedCrossRef Parmenter BA, Weinstock-Guttman B, Garg N, Munschauer F, Benedict RH (2007) Screening for cognitive impairment in multiple sclerosis using the Symbol Digit Modalities Test. Mult Scler 13(1):52–57PubMedCrossRef
20.
go back to reference Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict RH (2009) Sensitivity of conventional memory tests in multiple sclerosis: comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Mult Scler 15(9):1077–1084PubMedCrossRef Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict RH (2009) Sensitivity of conventional memory tests in multiple sclerosis: comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Mult Scler 15(9):1077–1084PubMedCrossRef
21.
go back to reference Benedict RH, Smerbeck A, Parikh R, Rodgers J, Cadavid D, Erlanger D (2012) Reliability and equivalence of alternate forms for the Symbol Digit Modalities Test: implications for multiple sclerosis clinical trials. Mult Scler 18(9):1320–1325PubMedCrossRef Benedict RH, Smerbeck A, Parikh R, Rodgers J, Cadavid D, Erlanger D (2012) Reliability and equivalence of alternate forms for the Symbol Digit Modalities Test: implications for multiple sclerosis clinical trials. Mult Scler 18(9):1320–1325PubMedCrossRef
22.
go back to reference Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR et al (2012) Validity and reliability of a Persian translation of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Clin Neuropsychol 26(6):975–984PubMedCrossRef Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR et al (2012) Validity and reliability of a Persian translation of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Clin Neuropsychol 26(6):975–984PubMedCrossRef
23.
go back to reference Spedo CT, Frndak SE, Marques VD, Foss MP, Pereira DA, Carvalho Lde F et al (2015) Cross-cultural adaptation, reliability, and validity of the BICAMS in Brazil. Clin Neuropsychol 29(6):836–846PubMedCrossRef Spedo CT, Frndak SE, Marques VD, Foss MP, Pereira DA, Carvalho Lde F et al (2015) Cross-cultural adaptation, reliability, and validity of the BICAMS in Brazil. Clin Neuropsychol 29(6):836–846PubMedCrossRef
24.
go back to reference Vanotti S, Smerbeck A, Benedict RH, Caceres F (2016) A new assessment tool for patients with multiple sclerosis from Spanish-speaking countries: validation of the Brief International Cognitive Assessment for MS (BICAMS) in Argentina. Clin Neuropsychol 30(7):1023–1031PubMedCrossRef Vanotti S, Smerbeck A, Benedict RH, Caceres F (2016) A new assessment tool for patients with multiple sclerosis from Spanish-speaking countries: validation of the Brief International Cognitive Assessment for MS (BICAMS) in Argentina. Clin Neuropsychol 30(7):1023–1031PubMedCrossRef
25.
go back to reference Hsieh SL, Tori CD (2007) Normative data on cross-cultural neuropsychological tests obtained from Mandarin-speaking adults across the life span. Arch Clin Neuropsychol 22(3):283–296PubMedCrossRef Hsieh SL, Tori CD (2007) Normative data on cross-cultural neuropsychological tests obtained from Mandarin-speaking adults across the life span. Arch Clin Neuropsychol 22(3):283–296PubMedCrossRef
26.
go back to reference Burggraaff J, Knol DL, Uitdehaag BMJ (2017) Regression-based norms for the Symbol Digit Modalities Test in the Dutch population: improving detection of cognitive impairment in multiple sclerosis? Eur Neurol 77(5–6):246–252PubMedCrossRef Burggraaff J, Knol DL, Uitdehaag BMJ (2017) Regression-based norms for the Symbol Digit Modalities Test in the Dutch population: improving detection of cognitive impairment in multiple sclerosis? Eur Neurol 77(5–6):246–252PubMedCrossRef
27.
go back to reference Arango-Lasprilla JC, Rivera D, Rodríguez G, Garza MT, Galarza-Del-Angel J, Rodríguez W et al (2015) Symbol Digit Modalities Test: normative data for the Latin American Spanish speaking adult population. NeuroRehabilitation 37(4):625–638PubMedCrossRef Arango-Lasprilla JC, Rivera D, Rodríguez G, Garza MT, Galarza-Del-Angel J, Rodríguez W et al (2015) Symbol Digit Modalities Test: normative data for the Latin American Spanish speaking adult population. NeuroRehabilitation 37(4):625–638PubMedCrossRef
28.
go back to reference Benedict RH, Amato MP, Boringa J, Brochet B, Foley F, Fredrikson S et al (2012) Brief International Cognitive Assessment for MS (BICAMS): international standards for validation. BMC Neurol 12:55PubMedPubMedCentralCrossRef Benedict RH, Amato MP, Boringa J, Brochet B, Foley F, Fredrikson S et al (2012) Brief International Cognitive Assessment for MS (BICAMS): international standards for validation. BMC Neurol 12:55PubMedPubMedCentralCrossRef
29.
go back to reference van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A et al (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755PubMedCrossRef van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A et al (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755PubMedCrossRef
30.
go back to reference Clements P, Lachenbruch P, Seibold JR, White B, Weiner S, Martin RW et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22:1281–1285PubMed Clements P, Lachenbruch P, Seibold JR, White B, Weiner S, Martin RW et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22:1281–1285PubMed
31.
go back to reference Walter U, Školoudík D (2014) Transcranial sonography (TCS) of brain parenchyma in movement disorders: quality standards, diagnostic applications and novel technologies. Ultraschall Med 35(4):322–331PubMedCrossRef Walter U, Školoudík D (2014) Transcranial sonography (TCS) of brain parenchyma in movement disorders: quality standards, diagnostic applications and novel technologies. Ultraschall Med 35(4):322–331PubMedCrossRef
33.
go back to reference Koh CL, Lu WS, Chen HC, Hsueh IP, Hsieh JJ, Hsieh CL (2011) Test-retest reliability and practice effect of the oral-format Symbol Digit Modalities Test in patients with stroke. Arch Clin Neuropsychol 26(4):356–363PubMedCrossRef Koh CL, Lu WS, Chen HC, Hsueh IP, Hsieh JJ, Hsieh CL (2011) Test-retest reliability and practice effect of the oral-format Symbol Digit Modalities Test in patients with stroke. Arch Clin Neuropsychol 26(4):356–363PubMedCrossRef
34.
go back to reference Chan YH (2003) Biostatistics 102: quantitative data--parametric & non-parametric tests. Singap Med J 44(8):391–396 Chan YH (2003) Biostatistics 102: quantitative data--parametric & non-parametric tests. Singap Med J 44(8):391–396
35.
go back to reference Chan YH (2003) Biostatistics 103: qualitative data - tests of independence. Singap Med J 44(10):498–503 Chan YH (2003) Biostatistics 103: qualitative data - tests of independence. Singap Med J 44(10):498–503
36.
go back to reference Chan YH (2003) Biostatistics 104: correlational analysis. Singap Med J 44(12):614–619 Chan YH (2003) Biostatistics 104: correlational analysis. Singap Med J 44(12):614–619
37.
go back to reference Kahaleh B (2008) Vascular disease in scleroderma: mechanisms of vascular injury. Rheum Dis Clin N Am 34(1):57–71CrossRef Kahaleh B (2008) Vascular disease in scleroderma: mechanisms of vascular injury. Rheum Dis Clin N Am 34(1):57–71CrossRef
39.
go back to reference Wollheim FA (2005) Classification of systemic sclerosis. Visions and reality. Rheumatology (Oxford) 44(10):1212–1216CrossRef Wollheim FA (2005) Classification of systemic sclerosis. Visions and reality. Rheumatology (Oxford) 44(10):1212–1216CrossRef
40.
go back to reference Timár O, Soltész P, Szamosi S, Dér H, Szántó S, Szekanecz Z et al (2008) Increased arterial stiffness as the marker of vascular involvement in systemic sclerosis. J Rheumatol 35(7):1329–1333PubMed Timár O, Soltész P, Szamosi S, Dér H, Szántó S, Szekanecz Z et al (2008) Increased arterial stiffness as the marker of vascular involvement in systemic sclerosis. J Rheumatol 35(7):1329–1333PubMed
41.
42.
go back to reference Youssef P, Brama T, Englert H, Bertouch J (1995) Limited scleroderma is associated with increased prevalence of macrovascular disease. J Rheumatol 22(3):469–472PubMed Youssef P, Brama T, Englert H, Bertouch J (1995) Limited scleroderma is associated with increased prevalence of macrovascular disease. J Rheumatol 22(3):469–472PubMed
43.
go back to reference Rodnan GP, Myerowitz RL, Justh GO (1980) Morphologic changes in the digital arteries of patients with progressive systemic sclerosis (scleroderma) and Raynaud phenomenon. Medicine (Baltimore) 59(6):393–408CrossRef Rodnan GP, Myerowitz RL, Justh GO (1980) Morphologic changes in the digital arteries of patients with progressive systemic sclerosis (scleroderma) and Raynaud phenomenon. Medicine (Baltimore) 59(6):393–408CrossRef
44.
go back to reference Carvalho D, Savage CO, Black CM, Pearson JD (1996) IgG antiendothelial cell autoantibodies from scleroderma patients induce leukocyte adhesion to human vascular endothelial cells in vitro. Induction of adhesion molecule expression and involvement of endothelium-derived cytokines. J Clin Invest 97(1):111–119PubMedPubMedCentralCrossRef Carvalho D, Savage CO, Black CM, Pearson JD (1996) IgG antiendothelial cell autoantibodies from scleroderma patients induce leukocyte adhesion to human vascular endothelial cells in vitro. Induction of adhesion molecule expression and involvement of endothelium-derived cytokines. J Clin Invest 97(1):111–119PubMedPubMedCentralCrossRef
45.
go back to reference Schachna L, Wigley FM (2002) Targeting mediators of vascular injury in scleroderma. Curr Opin Rheumatol 14:686–693PubMedCrossRef Schachna L, Wigley FM (2002) Targeting mediators of vascular injury in scleroderma. Curr Opin Rheumatol 14:686–693PubMedCrossRef
46.
47.
go back to reference Greene ER, Yonan KA, Sharrar JM, Sibbitt WL Jr, Roldan CA (2012) Middle cerebral artery resistivity and pulsatility indices in systemic lupus erythematosus: evidence for hyperperfusion. Lupus 21(4):380–385PubMedCrossRef Greene ER, Yonan KA, Sharrar JM, Sibbitt WL Jr, Roldan CA (2012) Middle cerebral artery resistivity and pulsatility indices in systemic lupus erythematosus: evidence for hyperperfusion. Lupus 21(4):380–385PubMedCrossRef
48.
go back to reference Oates JC, Shaftman SR, Self SE, Gilkeson GS (2008) Association of serum nitrate and nitrite levels with longitudinal assessments of disease activity and damage in systemic lupus erythematosus and lupus nephritis. Arthritis Rheum 58(1):263–272PubMedPubMedCentralCrossRef Oates JC, Shaftman SR, Self SE, Gilkeson GS (2008) Association of serum nitrate and nitrite levels with longitudinal assessments of disease activity and damage in systemic lupus erythematosus and lupus nephritis. Arthritis Rheum 58(1):263–272PubMedPubMedCentralCrossRef
49.
go back to reference Generini S, Matucci Cerinic M (1999) Raynaud’s phenomenon and vascular disease in systemic sclerosis. Adv Exp Med Biol 455:93–100PubMedCrossRef Generini S, Matucci Cerinic M (1999) Raynaud’s phenomenon and vascular disease in systemic sclerosis. Adv Exp Med Biol 455:93–100PubMedCrossRef
50.
go back to reference Bunker CB, Goldsmith PC, Leslie TA, Hayes N, Foreman JC, Dowd PM (1996) Calcitonin gene-related peptide, endothelin-1, the cutaneous microvasculature and Raynaud’s phenomenon. Br J Dermatol 134(3):399–406PubMedCrossRef Bunker CB, Goldsmith PC, Leslie TA, Hayes N, Foreman JC, Dowd PM (1996) Calcitonin gene-related peptide, endothelin-1, the cutaneous microvasculature and Raynaud’s phenomenon. Br J Dermatol 134(3):399–406PubMedCrossRef
51.
go back to reference Hennerici M, Rautenberg W, Sitzer G, Schwartz A (1987) Transcranial Doppler ultrasound for the assessment of intracranial arterial flow velocity--part 1. Examination technique and normal values. Surg Neurol 27(5):439–448PubMedCrossRef Hennerici M, Rautenberg W, Sitzer G, Schwartz A (1987) Transcranial Doppler ultrasound for the assessment of intracranial arterial flow velocity--part 1. Examination technique and normal values. Surg Neurol 27(5):439–448PubMedCrossRef
52.
go back to reference Macchi C, Catini C (1994) The measurement of the calibers and blood flow velocities of the arteries of the circle of Willis: a statistical investigation of 120 living subjects using transcranial color-Doppler ultrasonography. Ital J Anat Embryol 99(1):9–16PubMed Macchi C, Catini C (1994) The measurement of the calibers and blood flow velocities of the arteries of the circle of Willis: a statistical investigation of 120 living subjects using transcranial color-Doppler ultrasonography. Ital J Anat Embryol 99(1):9–16PubMed
53.
go back to reference Bartels E, Fuchs HH, Flugel KA (1995) Color Doppler imaging of cerebral arteries: normal reference values and clinical applications. Angiology 46:877–884PubMedCrossRef Bartels E, Fuchs HH, Flugel KA (1995) Color Doppler imaging of cerebral arteries: normal reference values and clinical applications. Angiology 46:877–884PubMedCrossRef
54.
go back to reference Farhoudi M, Kermani S, Sadeghi-Bazargani H (2010) Relatively higher norms of blood flow velocity of major intracranial arteries in North-West Iran. BMC Res Notes 3:174PubMedPubMedCentralCrossRef Farhoudi M, Kermani S, Sadeghi-Bazargani H (2010) Relatively higher norms of blood flow velocity of major intracranial arteries in North-West Iran. BMC Res Notes 3:174PubMedPubMedCentralCrossRef
55.
go back to reference Nobili F, Cutolo M, Sulli A, Vitali P, Vignola S, Rodriguez G (2002) Brain functional involvement by perfusion SPECT in systemic sclerosis and Behçet’s disease. Ann N Y Acad Sci 966:409–414PubMedCrossRef Nobili F, Cutolo M, Sulli A, Vitali P, Vignola S, Rodriguez G (2002) Brain functional involvement by perfusion SPECT in systemic sclerosis and Behçet’s disease. Ann N Y Acad Sci 966:409–414PubMedCrossRef
56.
go back to reference Sardanelli F, Iozzelli A, Cotticelli B, Losacco C, Cutolo M, Sulli A et al (2005) White matter hyperintensities on brain magnetic resonance in systemic sclerosis. Ann Rheum Dis 64(5):777–779PubMedPubMedCentralCrossRef Sardanelli F, Iozzelli A, Cotticelli B, Losacco C, Cutolo M, Sulli A et al (2005) White matter hyperintensities on brain magnetic resonance in systemic sclerosis. Ann Rheum Dis 64(5):777–779PubMedPubMedCentralCrossRef
57.
go back to reference Cutolo M, Nobili F, Sulli A, Pizzorni C, Briata M, Faelli F et al (2000) Evidence of cerebral hypo perfusion in scleroderma patients. Rheumatology (Oxford) 39(12):1366–1373CrossRef Cutolo M, Nobili F, Sulli A, Pizzorni C, Briata M, Faelli F et al (2000) Evidence of cerebral hypo perfusion in scleroderma patients. Rheumatology (Oxford) 39(12):1366–1373CrossRef
58.
go back to reference Seidel G, Kaps M, Gerrits T, Hutzelmann A (1995) Evaluation of the ventricular system in adults by transcranial duplex sonography. J Neuroimaging 5:105–108PubMedCrossRef Seidel G, Kaps M, Gerrits T, Hutzelmann A (1995) Evaluation of the ventricular system in adults by transcranial duplex sonography. J Neuroimaging 5:105–108PubMedCrossRef
59.
go back to reference Berg D, Mäurer M, Warmuth-Metz M, Rieckmann P, Becker G (2000) The correlation between ventricular diameter measured by transcranial sonography and clinical disability and cognitive dysfunction in patients with multiple sclerosis. Arch Neurol 57:1289–1292PubMedCrossRef Berg D, Mäurer M, Warmuth-Metz M, Rieckmann P, Becker G (2000) The correlation between ventricular diameter measured by transcranial sonography and clinical disability and cognitive dysfunction in patients with multiple sclerosis. Arch Neurol 57:1289–1292PubMedCrossRef
60.
go back to reference Giuliodori G, Fraticelli P, Bartolini M, Cagnetti C, Baruffaldi R, Rocchi MB et al (2009) Cognitive and cerebral hemodynamic impairment in scleroderma patients. Eur J Neurol 16(12):1285–1290PubMedCrossRef Giuliodori G, Fraticelli P, Bartolini M, Cagnetti C, Baruffaldi R, Rocchi MB et al (2009) Cognitive and cerebral hemodynamic impairment in scleroderma patients. Eur J Neurol 16(12):1285–1290PubMedCrossRef
61.
go back to reference Yilmaz N, Mollahasanoglu A, Gurvit H, Can M, Tuncer N, Inanc N et al (2012) Dysexecutive syndrome: a specific pattern of cognitive impairment in systemic sclerosis. Cogn Behav Neurol 25(2):57–62PubMedCrossRef Yilmaz N, Mollahasanoglu A, Gurvit H, Can M, Tuncer N, Inanc N et al (2012) Dysexecutive syndrome: a specific pattern of cognitive impairment in systemic sclerosis. Cogn Behav Neurol 25(2):57–62PubMedCrossRef
62.
go back to reference Golstein M, Meyer O, Bourgeois P, Palazzo E, Nicaise P, Labarre C et al (1993) Neurological manifestations of systemic lupus erythematosus: role of antiphospholipid antibodies. Clin Exp Rheumatol 11(4):373–379PubMed Golstein M, Meyer O, Bourgeois P, Palazzo E, Nicaise P, Labarre C et al (1993) Neurological manifestations of systemic lupus erythematosus: role of antiphospholipid antibodies. Clin Exp Rheumatol 11(4):373–379PubMed
63.
go back to reference Hanly J, Cassel K, Fisk J (1997) Cognitive functions in systemic lupus erythematosus: result of a 5-year prospective study. Arthritis Rheum 40:1542–1543PubMedCrossRef Hanly J, Cassel K, Fisk J (1997) Cognitive functions in systemic lupus erythematosus: result of a 5-year prospective study. Arthritis Rheum 40:1542–1543PubMedCrossRef
64.
go back to reference Sherer Y, Shoenfeld Y (2006) Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol 2:99–106PubMedCrossRef Sherer Y, Shoenfeld Y (2006) Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol 2:99–106PubMedCrossRef
65.
go back to reference Tiehuis AM, Vincken KL, van den Berg E, Hendrikse J, Manschot SM, Mali WP et al (2008) Cerebral perfusion in relation to cognitive function and type 2 diabetes. Diabetologia 51(7):1321–1326PubMedPubMedCentralCrossRef Tiehuis AM, Vincken KL, van den Berg E, Hendrikse J, Manschot SM, Mali WP et al (2008) Cerebral perfusion in relation to cognitive function and type 2 diabetes. Diabetologia 51(7):1321–1326PubMedPubMedCentralCrossRef
66.
go back to reference Rusinek H, Ha J, Yau PL, Storey P, Tirsi A, Tsui WH et al (2015) Cerebral perfusion in insulin resistance and type 2 diabetes. J Cereb Blood Flow Metab 35(1):95–102PubMedCrossRef Rusinek H, Ha J, Yau PL, Storey P, Tirsi A, Tsui WH et al (2015) Cerebral perfusion in insulin resistance and type 2 diabetes. J Cereb Blood Flow Metab 35(1):95–102PubMedCrossRef
67.
go back to reference Chung CC, Pimentel D, Jor’dan AJ, Hao Y, Milberg W, Novak V (2015) Inflammation associated declines in cerebral vasoreactivity and cognition in type 2 diabetes. Neurology 85(5):450–458PubMedPubMedCentralCrossRef Chung CC, Pimentel D, Jor’dan AJ, Hao Y, Milberg W, Novak V (2015) Inflammation associated declines in cerebral vasoreactivity and cognition in type 2 diabetes. Neurology 85(5):450–458PubMedPubMedCentralCrossRef
Metadata
Title
Neurosonological and cognitive screening for evaluation of systemic sclerosis patients
Authors
B. R. Sakr
R. E. Rabea
A. M. Aboulfotooh
N. A. Kishk
Publication date
01-07-2019
Publisher
Springer London
Published in
Clinical Rheumatology / Issue 7/2019
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-019-04468-7

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