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      Brain MRI in patients with diffuse psychiatric/neuropsychological syndromes in systemic lupus erythematosus

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          Abstract

          Background

          Manifestations in neuropsychiatric systemic lupus erythematosus (NPSLE), especially active diffuse NPSLE syndromes, are some of the most difficult complications of the disease. For the evaluation and the diagnosis of central nervous system manifestations, including NPSLE, MRI is a very useful tool to detect the various abnormalities. However, the relationship between brain MRI findings and clinical variables has not yet been clarified in patients with diffuse NPSLE.

          Objectives

          The aim of this study is to investigate the pathogenesis of diffuse NPSLE, by comparing various parameters such as serum autoantibodies and cytokines in cerebrospinal fluid (CSF) with abnormal findings revealed on brain MRIs in patients with diffuse NPSLE.

          Methods

          Fifty-three patients with diffuse NPSLE admitted to our University Hospital from 1992 to 2012 were exhaustively enrolled in this study. Their medical charts and brain MRI scans were reviewed. The relationship of MRI abnormalities with various parameters was analysed.

          Results

          As many as 25 of 53 patients (47.2%) had abnormal MRI findings. MRI findings improved after treatment in 10 of 17 patients for whom follow-up studies were available. MRI abnormalities were not correlated with age at the onset of diffuse NPSLE. However, the disease duration of SLE was significantly longer in patients with abnormal MRI findings (p=0.0009). MRI abnormalities were not significantly associated with serum autoantibodies. However, there were significant elevations of the CSF protein level (p=0.0106) and the CSF interleukin 6 level (p=0.0225) in patients with abnormal MRI findings. Patients with MRI abnormalities showed significantly higher overall mortality (p=0.0348).

          Conclusions

          The results revealed that MRI abnormalities in diffuse NPSLE might be heterogeneous with regard to their reversibility. These data also indicate that patients with diffuse NPSLE and MRI abnormalities have more severe inflammation in the central nervous system related to the activity of diffuse NPSLE, as evidenced by poorer prognosis.

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          Most cited references23

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          Neuropsychiatric syndromes in lupus: prevalence using standardized definitions.

          M Navarrete, S Saklad, I Rodrigo-Rincon … (2002)
          The San Antonio Lupus Study of Neuropsychiatric Disease is a longitudinal study designed to characterize the spectrum of and important risk factors for specific neuropsychiatric systemic lupus erythematosus (NPSLE) syndromes. Subjects must meet criteria for SLE and must be at least 18 years of age. A standardized medical history, neurologic, rheumatologic, and psychiatric examinations, computerized neuropsychological evaluation, and serologic testing are performed. This report is based on the first 128 subjects (120 women and 8 men) who completed the initial study visit. Data from this initial study visit were evaluated for the prevalence of NPSLE using the American College of Rheumatology case definitions for 19 NPSLE syndromes. One or more NPSLE syndromes were present in 80% of subjects: cerebrovascular disease (2, 2%; ischemic stroke); headaches (73, 57%); mononeuropathy (9, 8%; median 8, ulnar 1); movement disorder (1, 1%; chorea); neuropathy, cranial (2, 2%; trigeminal); polyneuropathy (29, 22%; sensorimotor); seizures (21, 16%; partial); anxiety disorder (27, 24%); major depressive-like episode (37, 28%); mood disorder with depressive features (21, 19%); mood disorder with manic features (3, 3%); mood disorder with mixed features (1, 1%); psychosis (6, 5%). In a subset of 67 patients who received standardized neuropsychological testing, 21% had normal results. In the remainder, the following levels of impairment were seen: 43% mild, 30% moderate, and 6% severe. The prevalence of NPSLE was high in this cohort of unselected patients with SLE. Headaches, cognitive dysfunction, and psychiatric disorders were the most common NPSLE syndromes seen. These results will be easily comparable to other studies also using standardized diagnostic criteria. However, the lack of ethnicity and language-matched normative neuropsychological data may make comparisons of cognitive dysfunction in SLE populations difficult.
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            Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies.

            L Bertolaccini, Alessandro Mathieu, Munther A. Khamashta … (2003)
            To apply the new American College of Rheumatology nomenclature for neuropsychiatric systemic lupus erythematosus (NPSLE), determine the prevalence of the different neuropsychiatric (NP) syndromes, and evaluate which of these manifestations correlates with the presence of antiphospholipid antibodies (aPL). Methods. Clinical, serological, and imaging data of 323 consecutive patients with SLE were retrospectively reviewed. Neuropsychometric testing was applied by a neuropsychologist. Univariate and multivariate statistical analyses were applied to evaluate the association bewteen NP manifestations, magnetic resonance imaging (MRI) abnormalities, and aPL. In total, 185 patients (57.3%) had NP manifestations at any time during followup. Headache was the most frequent manifestation, present in 78 patients (24%). Cerebrovascular disease (CVD) was diagnosed in 47/323 patients (14.5%), with a total of 57 events. Mood disorders were found in 54 (16.7%), cognitive disorders in 35 (10.8%), and seizures in 27 patients (8.3%). Psychosis was diagnosed in 25 (7.7%), anxiety disorder in 24 (3.7%), and acute confusional state in 12 patients (3.7%). Less common manifestations were polyneuropathy, mononeuritis, myasthenia gravis, cranial neuropathy, myelopathy, chorea, demyelinating disease, and Guillain-Barré syndrome. The presence of aPL was associated with NP manifestations (p < 0.001). Multivariate analysis showed that aPL were independently associated with CVD (OR 6.17, 95% CI 2.94-12.9, p = 0.001), headache (OR 2.04, 95% CI 1.17-3.55, p = 0.01), and seizures (OR 2.89, 95% CI 1.18-7.10, p = 0.02). The presence of lupus anticoagulant (LAC) was independently associated with white matter hyperintensity lesions on MRI (OR 3.0, 95% CI 1.12-8.05, p = 0.027). The new ACR criteria for NPSLE are useful to define NP manifestations in SLE with accuracy. NP manifestations are significantly associated with aPL. CVD, headache, and seizures were independently associated with these antibodies.
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              Association of cerebrospinal fluid anti-NR2 glutamate receptor antibodies with diffuse neuropsychiatric systemic lupus erythematosus.

              Shunsei Hirohata, Yoshiyuki Arinuma, Tamiko Yanagida (2008)
              To explore the association of antibodies directed against N-methyl-D-aspartate receptor subunit NR2 (anti-NR2) in cerebrospinal fluid (CSF) with neuropsychiatric manifestations in systemic lupus erythematosus (NPSLE). Paired serum and CSF specimens were obtained from 56 patients with NPSLE (38 with diffuse psychiatric/neuropsychological syndromes [diffuse NPSLE] and 18 with neurologic syndromes or peripheral neuropathy [focal NPSLE]) and from 20 control patients with noninflammatory neurologic diseases. IgG anti-NR2 antibodies were measured by enzyme-linked immunosorbent assay using synthetic peptide containing the extracellular ligand-binding domain of NR2. The binding of affinity-purified anti-NR2 to human neuroblastoma cell line SK-N-MC was examined by flow cytometry. Purified anti-NR2 bound to the surface of SK-N-MC cells. Levels of anti-NR2 antibodies in CSF were significantly elevated in patients with diffuse NPSLE compared with levels in control patients or those with focal NPSLE, whereas there were no significant differences in serum anti-NR2 levels among the 3 groups. In 31 of the 38 patients with diffuse NPSLE (81.6%) and 8 of the 18 patients with focal NPSLE (44.4%), CSF anti-NR2 levels were more than 3 SD above the mean level in the control patients (P=0.0120 by chi-square test). These results indicate that anti-NR2 is a constituent of antineuronal antibodies and, more importantly, that anti-NR2 antibodies in CSF, but not in serum, are associated with diffuse NPSLE.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Lupus Sci Med
                Journal ID (iso-abbrev): Lupus Sci Med
                Journal ID (hwp): lupusscimed
                Journal ID (publisher-id): lupus
                Title: Lupus Science & Medicine
                Publisher: BMJ Publishing Group (BMA House, Tavistock Square, London, WC1H 9JR )
                ISSN (Electronic): 2053-8790
                Publication date Collection: 2014
                Publication date (Electronic): 3 November 2014
                Volume: 1
                Issue: 1
                Electronic Location Identifier: e000050
                Affiliations
                [1 ]Department of Rheumatology and Infectious Diseases, Kitasato University School of Medicine , Kanagawa, Japan
                [2 ]Department of Internal Medicine, Teikyo University School of Medicine , Tokyo, Japan
                [3 ]Department of Radiology, Teikyo University Hospital , Tokyo, Japan
                Author notes
                [Correspondence to ] Dr Yoshiyuki Arinuma; y-arinuma@ 123456med.kitasati-u.ac.jp
                Article
                Publisher ID: lupus-2014-000050
                DOI: 10.1136/lupus-2014-000050
                PMC ID: 4225739
                PubMed ID: 25396069
                SO-VID: 762bd812-ac29-428d-af9b-d4b8c6635e26
                Copyright © Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions
                License:

                This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/

                History
                Date received : 17 July 2014
                Date revision received : 24 September 2014
                Date accepted : 25 September 2014
                Categories
                Subject: Immunology and Inflammation
                Subject: 1506
                Subject: 2251

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