Skip to main content
Erschienen in: Clinical Neuroradiology 1/2017

13.05.2015 | Original Article

Global Cognitive Impairment in Systemic Lupus Erythematosus Patients: A Structural MRI Study

verfasst von: Nicolle Zimmermann, Diogo Goulart Corrêa, Tadeu Almodovar Kubo, Tania Maria Netto, Denis Batista Pereira, Rochele Paz Fonseca, Emerson Leandro Gasparetto

Erschienen in: Clinical Neuroradiology | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Objective

This study investigated differences in subcortical brain volumes of SLE patients with cognitive deficits (SLE-CD) and SLE patients with normal cognitive performance (SLE-CN), regardless of the presence of other neuropsychiatric symptoms.

Method

We studied 40 patients divided into two-matched groups (SLE-CD n = 20; SLE-CN n = 20), with age ranging from 21 to 63 years old (100 % female) and 14.73 ± 10.18 years of diagnosis. Magnetic resonance imaging exams were performed on a 1.5 T scanner. A neuropsychological flexible battery was applied individually, including reasoning/problem-solving, praxis, episodic and working memory, processing speed, language/fluency, executive functions (inhibition and flexibility), and sustained attention. Z score ≤ − 2.0 in any dimension was considered as a cut-off for being considered to possess cognitive deficits. One-way analyses of covariance (ANCOVA) were performed to compare the brain structure volumes between groups. The analyses were controlled for the effects of lupus-related neuropsychiatric disorders.

Results

SLE patients with cognitive deficits had significantly smaller volumes in the left hippocampus, amygdala, and the right hippocampus than SLE patients without cognitive deficits.

Conclusion

SLE patients with cognitive deficits appeared to have reduced temporal lobe structures when compared with SLE without cognitive deficits. These results corroborate a systems vulnerability model that investigated temporal lobe vulnerability during normal aging and in other neurological disorders.
Literatur
1.
Zurück zum Zitat ACR AC of RAHC. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 1999;42(4):599–608.CrossRef ACR AC of RAHC. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 1999;42(4):599–608.CrossRef
2.
Zurück zum Zitat Carlomagno S, Migliaresi S, Ambrosone L, Sannino M, Sanges G, Di Iorio G. Cognitive impairment in systemic lupus erythematosus: a follow-up study. J Neurol. 2000;247:273–9.CrossRefPubMed Carlomagno S, Migliaresi S, Ambrosone L, Sannino M, Sanges G, Di Iorio G. Cognitive impairment in systemic lupus erythematosus: a follow-up study. J Neurol. 2000;247:273–9.CrossRefPubMed
3.
Zurück zum Zitat Nowicka-Sauer K, Czuszyńska Z, Smoleńska Ż, Siebert J. Neuropsychological assessment in systemic lupus erythematosus patients: clinical usefulness of first-choice diagnostic tests in detecting cognitive impairment and preliminary diagnosis of neuropsychiatric lupus. Clin Exp Rheumatol. 2011;29:299–306.PubMed Nowicka-Sauer K, Czuszyńska Z, Smoleńska Ż, Siebert J. Neuropsychological assessment in systemic lupus erythematosus patients: clinical usefulness of first-choice diagnostic tests in detecting cognitive impairment and preliminary diagnosis of neuropsychiatric lupus. Clin Exp Rheumatol. 2011;29:299–306.PubMed
4.
Zurück zum Zitat Monastero R, Bettini P, Del E, Cottini E, Tincani A, Balestrieri G, Cattaneo R, Camarda R, Vignolo LA, Padovani A. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci. 2001;184:33–9.CrossRefPubMed Monastero R, Bettini P, Del E, Cottini E, Tincani A, Balestrieri G, Cattaneo R, Camarda R, Vignolo LA, Padovani A. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci. 2001;184:33–9.CrossRefPubMed
5.
Zurück zum Zitat Cagnoli P, Sundgren P, Kairys A, Graft C, Clauw D, Gebarski S, McCune WJ, Schmidt-Wilcke T. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol. 2012;29:959–67.CrossRef Cagnoli P, Sundgren P, Kairys A, Graft C, Clauw D, Gebarski S, McCune WJ, Schmidt-Wilcke T. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol. 2012;29:959–67.CrossRef
6.
Zurück zum Zitat Muscal E, Brey RL. Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol Clin. 2010;28(1):61–73 (Elsevier Ltd). Muscal E, Brey RL. Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol Clin. 2010;28(1):61–73 (Elsevier Ltd).
7.
Zurück zum Zitat Kozora E, Arciniegas DB, Filley CM, West SG, Brown M, Miller D, Grimm A, Devore MD, Wingrove C, Zhang L. Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Rheum. 2008;59(11):1639–46. Kozora E, Arciniegas DB, Filley CM, West SG, Brown M, Miller D, Grimm A, Devore MD, Wingrove C, Zhang L. Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Rheum. 2008;59(11):1639–46.
8.
Zurück zum Zitat Danchenko N, Satia J, Anthony M. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18. Danchenko N, Satia J, Anthony M. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18.
9.
Zurück zum Zitat Bruns A, Meyer O. Neuropsychiatric manifestations of systemic lupus erythematosus. Joint Bone Spine. 2006;73(6):639–45. Bruns A, Meyer O. Neuropsychiatric manifestations of systemic lupus erythematosus. Joint Bone Spine. 2006;73(6):639–45.
10.
Zurück zum Zitat Hanly JG. ACR classification criteria for systemic lupus erythematosus: limitations and revisions to neuropsychiatric variables. Lupus. 2004;13(11):861–4. Hanly JG. ACR classification criteria for systemic lupus erythematosus: limitations and revisions to neuropsychiatric variables. Lupus. 2004;13(11):861–4.
11.
Zurück zum Zitat Unterman A, Nolte JES, Boaz M, Abady M, Shoenfeld Y, Zandman-Goddard G. Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum. 2011;41(1):1–11 Unterman A, Nolte JES, Boaz M, Abady M, Shoenfeld Y, Zandman-Goddard G. Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum. 2011;41(1):1–11
12.
Zurück zum Zitat Vogel A, Bhattacharya S, Larsen JL, Jacobsen S. Do subjective cognitive complaints correlate with cognitive impairment in systemic lupus erythematosus? A Danish outpatient study. Lupus. 2011;20(1):35–43. Vogel A, Bhattacharya S, Larsen JL, Jacobsen S. Do subjective cognitive complaints correlate with cognitive impairment in systemic lupus erythematosus? A Danish outpatient study. Lupus. 2011;20(1):35–43.
13.
Zurück zum Zitat Ainiala H, Hietaharju A, Loukkola J, Peltola J, Korpela M, Metsänoja R, Auvinen A. Validity of the New American College of Rheumatology Criteria for Neuropsychiatric Lupus Syndromes: a population-based evaluation. Arthritis Rheum. 2001 Oct;45(5):419-23.CrossRef Ainiala H, Hietaharju A, Loukkola J, Peltola J, Korpela M, Metsänoja R, Auvinen A. Validity of the New American College of Rheumatology Criteria for Neuropsychiatric Lupus Syndromes: a population-based evaluation. Arthritis Rheum. 2001 Oct;45(5):419-23.CrossRef
14.
Zurück zum Zitat Appenzeller S, Rondina JM, Li LM, Costallat LTL, Cendes F. Cerebral and corpus callosum atrophy in systemic lupus erythematosus. Arthritis Rheum. 2005;52(9):2783–9. Appenzeller S, Rondina JM, Li LM, Costallat LTL, Cendes F. Cerebral and corpus callosum atrophy in systemic lupus erythematosus. Arthritis Rheum. 2005;52(9):2783–9.
15.
Zurück zum Zitat Kozora E, Ellison MC, West S. Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum. 2004;51(5):810–8. Kozora E, Ellison MC, West S. Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum. 2004;51(5):810–8.
16.
Zurück zum Zitat Appenzeller S, Vasconcelos Faria A, Li LM, Costallat LTL, Cendes F. Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol. 2008;64(6):635–43. Appenzeller S, Vasconcelos Faria A, Li LM, Costallat LTL, Cendes F. Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol. 2008;64(6):635–43.
17.
Zurück zum Zitat Gauthier L, Dehaut F, Joanette Y. The Bells Test. Int J Clin Neuropsychol. 1989;6:48–54. Gauthier L, Dehaut F, Joanette Y. The Bells Test. Int J Clin Neuropsychol. 1989;6:48–54.
18.
Zurück zum Zitat Fonseca RP, Oliveira C, Gindri G, Zimmermann N, Reppold C. Teste Hayling: um instrumento de avaliação de componentes das funções executivas. In: Hutz C, editor. Avaliação psicológica e neuropsicológica de crianças e adolescentes. São Paulo: Casa do Psicólogo; 2010. pp. 337–64. Fonseca RP, Oliveira C, Gindri G, Zimmermann N, Reppold C. Teste Hayling: um instrumento de avaliação de componentes das funções executivas. In: Hutz C, editor. Avaliação psicológica e neuropsicológica de crianças e adolescentes. São Paulo: Casa do Psicólogo; 2010. pp. 337–64.
19.
Zurück zum Zitat Burgess PW, Shallice T. The Hayling and Brixton Tests. Thurston: Thames Valley Test Company; 1997. Burgess PW, Shallice T. The Hayling and Brixton Tests. Thurston: Thames Valley Test Company; 1997.
20.
Zurück zum Zitat AIT AITB. Army Individual Test Battery. Washington: War Department, Adjutant General’s Office; 1944. AIT AITB. Army Individual Test Battery. Washington: War Department, Adjutant General’s Office; 1944.
21.
Zurück zum Zitat Fonseca RP, Parente MA de MP, Côté H, Ska B, Joanette Y. Bateria Montréal de Avaliação da Comunicação—Bateria MAC. São Paulo: Pró-Fono; 2008. Fonseca RP, Parente MA de MP, Côté H, Ska B, Joanette Y. Bateria Montréal de Avaliação da Comunicação—Bateria MAC. São Paulo: Pró-Fono; 2008.
22.
Zurück zum Zitat Fonseca RP, Joanette Y, Côté H, Ska B, Giroux F, Fachel JM, Damasceno Ferreira G, Parente MA. Brazilian version of the Protocole Montréal d’Evaluation de la Communication (Protocole MEC): normative and reliability data. Span J Psychol. 2008;11:678–88.PubMed Fonseca RP, Joanette Y, Côté H, Ska B, Giroux F, Fachel JM, Damasceno Ferreira G, Parente MA. Brazilian version of the Protocole Montréal d’Evaluation de la Communication (Protocole MEC): normative and reliability data. Span J Psychol. 2008;11:678–88.PubMed
23.
Zurück zum Zitat do Nascimento E. Adaptação, validação e normatização do WAIS-III para uma amostra brasileira. In: Wechsler D, editor. WAIS III: manual para administração e avaliação. São Paulo: Casa do Psicólogo; 2004. do Nascimento E. Adaptação, validação e normatização do WAIS-III para uma amostra brasileira. In: Wechsler D, editor. WAIS III: manual para administração e avaliação. São Paulo: Casa do Psicólogo; 2004.
24.
Zurück zum Zitat de Figueiredo VLM, do Nascimento E. Desempenhos nas duas tarefas do subteste Dígitos do WISC-III e do WAIS-III. Psicol Teor e Pesqui. 2007;23(3):313–8.CrossRef de Figueiredo VLM, do Nascimento E. Desempenhos nas duas tarefas do subteste Dígitos do WISC-III e do WAIS-III. Psicol Teor e Pesqui. 2007;23(3):313–8.CrossRef
25.
Zurück zum Zitat Nascimento E, de Figueiredo VLM. WISC-III and WAIS-III: Alterations in the current American original versions of the adaptations for use in Brazil. Psicol Reflexão e Crítica. 2002;15:603–12.CrossRef Nascimento E, de Figueiredo VLM. WISC-III and WAIS-III: Alterations in the current American original versions of the adaptations for use in Brazil. Psicol Reflexão e Crítica. 2002;15:603–12.CrossRef
26.
Zurück zum Zitat Fonseca RP, de Salles JF, Parente MA de MP. Instrumento de Avaliação Neuropsicológica Breve NEUPSILIN. São Paulo: Vetor; 2009. Fonseca RP, de Salles JF, Parente MA de MP. Instrumento de Avaliação Neuropsicológica Breve NEUPSILIN. São Paulo: Vetor; 2009.
27.
Zurück zum Zitat Salgado JV, Malloy-Diniz LF, Abrantes SS, Moreira L, Schlottfeldt CG, Guimarães W, Freitas DM, Oliveira J, Fuentes D. Applicability of the Rey Auditory-Verbal Learning Test to an adult sample in Brazil. Rev Bras Psiquiatr. 2011;33(3):234–7.CrossRefPubMed Salgado JV, Malloy-Diniz LF, Abrantes SS, Moreira L, Schlottfeldt CG, Guimarães W, Freitas DM, Oliveira J, Fuentes D. Applicability of the Rey Auditory-Verbal Learning Test to an adult sample in Brazil. Rev Bras Psiquiatr. 2011;33(3):234–7.CrossRefPubMed
28.
Zurück zum Zitat Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex. 1976;12(4):313–24. Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex. 1976;12(4):313–24.
29.
Zurück zum Zitat Hatanpaa KJ, Raisanen JM, Herndon E, Burns DK, Foong C, Habib AA, White CL 3rd. Hippocampal subfields in dementia, epilepsy, and ischemic injury: differential vulnerability of hippocampal subfields. J Neuropathol Exp Neurol. 2014;73(2):136–42.CrossRefPubMedPubMedCentral Hatanpaa KJ, Raisanen JM, Herndon E, Burns DK, Foong C, Habib AA, White CL 3rd. Hippocampal subfields in dementia, epilepsy, and ischemic injury: differential vulnerability of hippocampal subfields. J Neuropathol Exp Neurol. 2014;73(2):136–42.CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Buckner RL, Krienen FM. The evolution of distributed association networks in the human brain. Trends Cogn Sci. 2013;17(12):648–65. Buckner RL, Krienen FM. The evolution of distributed association networks in the human brain. Trends Cogn Sci. 2013;17(12):648–65.
31.
Zurück zum Zitat Fjell AM, Amlien IK, Sneve MH, Grydeland H, Tamnes CK, Chaplin TA, Rosa MG, Walhovd KB. The roots of Alzheimer’s disease: are high-expanding cortical areas preferentially targeted? Cereb Cortex. 2014 Mar 21. [Epub ahead of print] Fjell AM, Amlien IK, Sneve MH, Grydeland H, Tamnes CK, Chaplin TA, Rosa MG, Walhovd KB. The roots of Alzheimer’s disease: are high-expanding cortical areas preferentially targeted? Cereb Cortex. 2014 Mar 21. [Epub ahead of print]
32.
Zurück zum Zitat Jagust W. Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron. 2014;77(2):219–34.CrossRef Jagust W. Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron. 2014;77(2):219–34.CrossRef
33.
Zurück zum Zitat Kerchner GA, Bernstein JD, Fenesy MC, Deutsch GK, Saranathan M, Zeineh MM, Rutt BK. Shared vulnerability of two synaptically-connected medial temporal lobe areas to age and cognitive decline: a seven tesla magnetic resonance imaging study. J Neurosci. 2013;33(42):16666–72. Kerchner GA, Bernstein JD, Fenesy MC, Deutsch GK, Saranathan M, Zeineh MM, Rutt BK. Shared vulnerability of two synaptically-connected medial temporal lobe areas to age and cognitive decline: a seven tesla magnetic resonance imaging study. J Neurosci. 2013;33(42):16666–72.
34.
Zurück zum Zitat Toyota T, Akamatsu N, Tanaka A, Shouzaki T, Tsuji S, Saito K, Tanaka Y. Mesial temporal lobe epilepsy as a neuropsychiatric syndrome of systemic lupus erythematosus. Epilepsia. 2013;54(3):e33–6. Toyota T, Akamatsu N, Tanaka A, Shouzaki T, Tsuji S, Saito K, Tanaka Y. Mesial temporal lobe epilepsy as a neuropsychiatric syndrome of systemic lupus erythematosus. Epilepsia. 2013;54(3):e33–6.
35.
Zurück zum Zitat Xu J, Cheng Y, Chai P, Lu Z, Li H, Luo C, Li X, Li L, Zhou Q, Chen B, Cao J, Xu X, Shan B, Xu L, Wen J. White-matter volume reduction and the protective effect of immunosuppressive therapy in systemic lupus erythematosus patients with normal appearance by conventional magnetic resonance imaging. J Rheumatol. 2010;37(5):974–86. Xu J, Cheng Y, Chai P, Lu Z, Li H, Luo C, Li X, Li L, Zhou Q, Chen B, Cao J, Xu X, Shan B, Xu L, Wen J. White-matter volume reduction and the protective effect of immunosuppressive therapy in systemic lupus erythematosus patients with normal appearance by conventional magnetic resonance imaging. J Rheumatol. 2010;37(5):974–86.
36.
Zurück zum Zitat Appenzeller S, Carnevalle AD, Li LM, Costallat LTL, Cendes F. Hippocampal atrophy in systemic lupus erythematosus. Ann Rheum Dis. 2006;65(12):1585–9. Appenzeller S, Carnevalle AD, Li LM, Costallat LTL, Cendes F. Hippocampal atrophy in systemic lupus erythematosus. Ann Rheum Dis. 2006;65(12):1585–9.
37.
Zurück zum Zitat Ren T, Ho RC, Mak A. Dysfunctional cortico-basal ganglia-thalamic circuit and altered hippocampal-amygdala activity on cognitive set-shifting in non-neuropsychiatric systemic lupus erythematosus. Arthritis Rheum. 2012;64(12):4048–59. Ren T, Ho RC, Mak A. Dysfunctional cortico-basal ganglia-thalamic circuit and altered hippocampal-amygdala activity on cognitive set-shifting in non-neuropsychiatric systemic lupus erythematosus. Arthritis Rheum. 2012;64(12):4048–59.
38.
Zurück zum Zitat Cagnoli PC, Sundgren PC, Kairys A, Graft CC, Clauw DJ, Gebarski S, McCune WJ, Schmidt-Wilcke T. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol. 2012;39(5):959–67. Cagnoli PC, Sundgren PC, Kairys A, Graft CC, Clauw DJ, Gebarski S, McCune WJ, Schmidt-Wilcke T. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol. 2012;39(5):959–67.
Metadaten
Titel
Global Cognitive Impairment in Systemic Lupus Erythematosus Patients: A Structural MRI Study
verfasst von
Nicolle Zimmermann
Diogo Goulart Corrêa
Tadeu Almodovar Kubo
Tania Maria Netto
Denis Batista Pereira
Rochele Paz Fonseca
Emerson Leandro Gasparetto
Publikationsdatum
13.05.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Neuroradiology / Ausgabe 1/2017
Print ISSN: 1869-1439
Elektronische ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-015-0397-8

Weitere Artikel der Ausgabe 1/2017

Clinical Neuroradiology 1/2017 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.