CHAPTER 2. Early occurrence of neuropsychiatric manifestations in a large cohort of SLE patients
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1 CHAPTER 2 Early occurrence of neuropsychiatric manifestations in a large cohort of SLE patients G.M. Steup-Beekman 1, B.M.A. Gahrmann 1, B.J. Emmer 2, S.C.A. Steens 2, E.L.E.M. Bollen 3, M.A. van Buchem 2, T.W.J. Huizinga 1 Departments of 1 Rheumatology, 2 Radiology and 3 Neurology, Leiden University Medical Center, Leiden, the Netherlands European Journal of Clinical Investigation 2011 Submitted 31
2 Abstract Background For neuropsychiatric manifestations in systemic lupus erythematosus (NPSLE) different pathogenetic pathways have been proposed varying from damage induced by long-term disease to an immune-mediated pathway. However, exact pathogenetic mechanisms are unknown. Objective To describe the patient characteristics of a large cohort of SLE patients with neuropsychiatric manifestations in a single center and to assess whether these features fit an immune-mediated pathogenetic mechanism. Methods A total of 112 patients were identified because a magnetic resonance imaging (MRI) scan of the brain was ordered for suspected NPSLE. Data were collected from the medical records. neuropsychiatric syndromes were classified according to the American College of Rheumatology (ACR) nomenclature and case definitions. Results 155 Patients fulfilled the criteria for SLE. In 102 patients neuropsychiatric manifestations were attributed to lupus itself (primary NPSLE), whereas in the remaining patients the neuropsychiatric symptoms were due to other causes. Median age at the time of SLE diagnosis in primary NPSLE patients was 27.5 years and median duration until NPSLE was 2.8 years. Forty patients (39%) had a neuropsychiatric manifestation in the first year of disease. Cerebrovascular disease, cognitive dysfunction, seizures and headache were the most prevalent syndromes. In 47% of primary NPSLE patients, MRI scan of the brain showed no abnormalities. Conclusion A majority of neuropsychiatric manifestations in SLE occurred early in the disease course which is compatible with the concept of an immune-mediated pathogenesis. 32
3 Chapter 2 : Early occurrence of NP manifestations in SLE Introduction Overall prognosis for survival in systemic lupus erythematosus (SLE) has improved dramatically in the last decades, but neuropsychiatric complications remain a major cause of morbidity. 1,2 Prevalence of neuropsychiatric syndromes in SLE varies from 15 to 91%, depending on diagnostic criteria and patient selection. 3-5 Clinical symptoms arise from dysfunction of the central nervous system (CNS) as well as the peripheral nervous system (PNS) and vary from mild cognitive symptoms to severe neuropsychiatric disease. The imaging modality of choice in neuropsychiatric SLE (NPSLE) is magnetic resonance imaging (MRI). MRI abnormalities include small focal subcortical white matter lesions, cortical atrophy, periventricular white matter hyperintensities and infarcts, but are often non-specific. 6,7 In 1999 the American College of Rheumatology (ACR) Ad Hoc Committee published a consensus document defining diagnostic and exclusion criteria for 12 CNS syndromes and 7 PNS syndromes in SLE in order to facilitate research. 8 In about 60% of the cases neuropsychiatric disease can be attributed to lupus itself and is referred to as primary NPSLE. 9,10 In the other 40%, neuropsychiatric symptoms are the consequence of secondary causes indirectly related to SLE such as infections, side effects of drugs or metabolic derangement. No specific test exists to discriminate primary from secondary NPSLE. In primary NPSLE, pathogenesis of diffuse syndromes such as cognitive dysfunction and psychosis, still remains largely unclear. True vasculitis is observed only in a minority of histopathological cases. 11 Besides antiphospholipid (apl) antibodies, intracranial vasculopathy, cytokine and autoantibody-mediated neuronal dysfunction have been suggested as underlying processes. 12 The association between nervous system involvement and the presence of autoantibodies is addressed in several studies The integrity of the blood-brain barrier seems to play an important role in autoantibody-mediated CNS manifestations. 18 Diamond and colleagues demonstrated that a subset of the antibodies to double stranded DNA (dsdna) in patients with SLE cross-reacts with subunits of the N-methyl-D-aspartate (NMDA) receptor on neuronal cells and can cause neuronal death by excito-toxicity and apoptosis. 19 In normal circumstances, the blood-brain barrier prevents these antibodies from causing neuronal damage. In a subsequent study in which these antibodies were induced in mice, neuronal damage occurred only when a breach in the integrity of the blood-brain barrier was present. 20,21 Recently a study suggested that this model might indeed be operative in patients with NPSLE whereas the presence of these antibodies in serum alone seems to have no direct effect on neuropsychiatric manifestations in SLE. 22,23 In clinical practice however, it is not known how frequent neuropsychiatric manifestations in patients with SLE are attributed to such an immune-mediated neuronal dysfunction. We expected to find neuropsychiatric symptoms occurring relatively early in the disease course in a substantial proportion of patients if an autoantibody mediated mechanism would be operative. If atherosclerotic damage would be the major pathogenetic pathway one would expect longer disease duration before neuropsychiatric symptoms occur. 33
4 The Leiden University Medical Center (LUMC) has been a referral center for NPSLE for over 20 years; this allowed us to retrospectively study features and time of occurrence ofneuropsychiatric disease in a large cohort of patients with suspected NPSLE. Methods The case records were evaluated of 212 patients who were referred for MRI scan of the brain because of possible NPSLE between January 1989 and January Patients were admitted to the departments of rheumatology, neurology and internal medicine of the LUMC, a tertiary referral center for the south-western part of the Netherlands, a region with a population of about three million inhabitants. This center also serves as a national referral center for NPSLE in the Netherlands (16 million inhabitants). SLE diagnosis was established, based on the presence of at least four of the ACR 1982 revised criteria for the classification of SLE. 24,25 Fifteen records showed insufficient clinical information and in 42 patients the SLE criteria were not met or a different diagnosis was made. These 57 patients were not evaluated in this study. The medical records of the 155 SLE patients were reviewed with particular attention to documented neuropsychiatric manifestations present at any time from the date of SLE diagnosis. The neuropsychiatric manifestations were classified retrospectively by a team of rheumatologists, according to the ACR nomenclature and case definitions for neuropsychiatric lupus syndromes. 8 Patients were categorized as primary NPSLE when symptoms were most likely attributed to lupus activity itself after extensive clinical evaluation and exclusion of other possible causes of neuropsychiatric symptoms. Secondary NPSLE was established when neuropsychiatric symptoms were the consequence of causes indirectly related to SLE such as infections, side effects of drugs or metabolic derangement due to damage to other organs. A single patient could have more than one neuropsychiatric syndrome and primary as well as secondary NPSLE could be established in the same patient. In case neuropsychiatric symptoms could not be related to SLE after thorough investigation, patients were classified as non-neuropsychiatric SLE. If patients did eventually not fulfill the classification criteria for SLE or if a different diagnosis was made, they were classified as other disease. Early onset NPSLE was defined as NPSLE diagnosis within one year after the diagnosis of SLE was recorded. Focal CNS, diffuse CNS and PNS manifestations were defined according to the 1999 ACR definitions. 8 All MRI scans were carried out on a Philips Gyroscan Intera ACS-NT 1.5T MR scanner (Philips Medical Systems, Best, the Netherlands). Axial T1-weighted images were acquired using a spin-echo sequence with an echo time (TE) of 20 ms, a repetition time (TR) of 600 ms, and a scanning time of 3 minutes 35 seconds. Axial proton-density (TR/TE: 2500/30 ms), T2-weighted (TR/TE 2500/120 ms), and fluid-attenuated inversion recovery (FLAIR; TR/TI/TE 8000 ms/2000 ms/120 ms) images were acquired with the following parameters: field of view (FOV) 220 mm, 34
5 Chapter 2 : Early occurrence of NP manifestations in SLE matrix 256 x 256, and 22 6mm slices with 0.6-mm slice gap. All scans were reviewed clinically by experienced neuroradiologists. The first MRI cerebrum made after the onset of neuropsychiatric symptoms was evaluated. White matter hyperintensities, infarctions, atrophy and all visible abnormalities were recorded. In case of suspected cognitive dysfunction, neuropsychological status was determined by means of an extensive neuropsychological battery, including the following domains as suggested by the 1999 ACR NPSLE nomenclature and case definition system, appendix C 8 : intelligence (Wechsler Adult Intelligence Scale (WAIS) -revised, Dutch version), attention and concentration (Wechsler memory scale-concentration, Knox Cube test, reaction time measurements), memory (Wechsler memory scale, 2 word learning list of 10 nouns, one presented orally and one visually), language and calculation skills (comprehension, word finding, naming pictures of the Object Naming Test, word fluency, reading and writing, 4 written calculations and 20 presented orally), constructional abilities (in addition to performance subtests of the WAIS, copying of perspective and geometric figures and drawings), gnosis and praxis and cognitive flexibility (Stroop Color and Word Test, Trail Making Test A and B, Wisconsin Modified Card sorting test). The presence of autoantibodies during the course of the disease was registered. An indirect immunofluorescent assay (Inova Diagnostics Inc, San Diego, CA, USA) using the hemoflagellate Crithidia Luciliae as a substrate was used to detect anti dsdna antibodies. Antinuclear antibodies (ANA) were also determined by indirect immune-fluorescence. The presence of antibodies against extractable nuclear antigen (anti-ena) was assessed using QUANTA Lite TM ENA 6 ELISA kit (Inova Diagnostics Inc, San Diego, CA, USA). Assays used for the detection of lupus anticoagulant (LAC) were lupus-aptt (activated partial thromboplastin time) and LA-screen and LA-confirm (Gradipore Inc, New York, USA). The presence of anticardiolipin antibodies (acl) IgM and IgG (phospholipid units per ml) was assessed using commercial ELISA kits (Pharmacia & Upjohn Diagnostics GmbH, Freiburg, Germany) in a procedure standard in our department of Rheumatology. The presence of the antiphospholipid syndrome was based on the preliminary classification criteria for definite APS. 26 To determine whether the NPSLE patients studied had a phenotype similar to the average SLE patient, the prevalence of the 1982 ACR criteria for SLE was listed and compared to the cohort used by the ACR as classical SLE patients. 24 Statistical analysis The statistical analyses were conducted using SPSS for Windows. To calculate 95% confidence intervals, the program CIA was used (Confidence Interval Analysis version 1.0, MJ Gardner and DG Altman, British Medical Journal 1989). 35
6 Results A total of 155 patients (90% female) fulfilled the criteria for SLE. Median age of SLE diagnosis was 29.7 years, IQR years). In 102 (66%) patients primary NPSLE was diagnosed (91% female) and neuropsychiatric manifestations secondary to SLE related problems were established in 15 patients (87% female). Four patients with primary NPSLE also developed secondary NPSLE during the course of their disease. In 42 SLE patients neuropsychiatric symptoms were not attributable to lupus (non- neuropsychiatric SLE). Median age of SLE diagnosis in this group was 34.9 years (IQR ). The age distribution at the time of SLE diagnosis and at the time of primary NPSLE diagnosis is shown in Figure 1. Median age at the time of SLE diagnosis in patients with primary NPSLE was 27.5 years (IQR years). Neuropsychiatric symptoms developed after median 2.8 years (IQR years). Early onset NPSLE was observed in 40 patients (39%). In 21 of these 40 patients, neuropsychiatric symptoms were the first manifestation of SLE. Median age at the time of SLE diagnosis in patients with secondary NPSLE was 23.3 years (IQR years). In these patients neuropsychiatric symptoms developed after median 1.3 years (IQR years). Neuropsychiatric syndromes in all NPSLE patients are listed in Table 1. In 102 patients with primary NPSLE, 172 syndromes were established. Fifty-six patients (55%) had one neuropsychiatric syndrome. Two or more neuropsychiatric syndromes were diagnosed in 45% of the patients; 28 patients (28%) had 2 neuropsychiatric syndromes, 13 patients (13%) had 3 neuropsychiatric syndromes, 4 patients (4%) had 4 neuropsychiatric syndromes and 1 patient had 5 different neuropsychiatric syndromes during the course of the disease. CNS manifestations SLE (155) NPSLE (102) 15 Early onset NPSLE (40) *5-10 *10-15 *15-20 *20-25 *25-30 *30-35 *35-40 *40-45 *45-50 *50-55 *55-60 *60-65 *65-70 Figure 1. Numbers of patients, categorized according to age at the time of SLE,- and NPSLE diagnosis. 36
7 Chapter 2 : Early occurrence of NP manifestations in SLE Table 1. Neuropsychiatric syndromes according to the ACR definitions 8 in patients with primary and secondary NPSLE.* NPSLE syndromea 102 Primary NPSLE subjects with the diagnosis n (%) 15 Secondary NPSLE subjects b with the diagnosis n (%) Cerebrovascular disease 44 (43) 2 (13) Seizures 28 (28) 5 (33) Cognitive dysfunction 27 (27) 3 (20) Headache 23 (23) 5 (33) Mood disorder 8 (8) 2 (13) Acute confusional state 7 (7) 1 (7) Psychosis 6(6) 2 (13) Cranial neuropathy 6 (6) 1 (7) Myelopathy 6 (6) - Movement disorder 5 (5) - Aseptic meningitis 3 (3) - Mononeuropathy 3 (3) - Polyneuropathy 2 (2) - Plexopathy 2 (2) - Guillain Barré 1 (1) - Anxiety disorder 1 (1) 1 (7) Total * ACR, American College of Rheumatology; NPSLE, neuropsychiatric systemic lupus erythematosus. a Autonomic disorder, demyelinating syndrome and myasthenia gravis did not occur. b Note: four of these patients were also diagnosed with primary NPSLE. accounted for 92 % of the syndromes and PNS manifestations for 8%. Sixteen of the 19 established neuropsychiatric syndromes occurred at least once. The highest prevalence was found for cerebrovascular disease (CVD) (43%). High prevalence was also found for seizures (28%), cognitive dysfunction (27%) and headache (23%). In secondary NPSLE highest prevalence was for seizures (33%), headache (33%) and cognitive dysfunction (20%). The majority of secondary NPSLE manifestations were related to hypertension, which was related to lupus nephritis in two cases; one patient was diagnosed with papillary edema, four patients with headache and five patients with seizures, one had cerebral hemorrhage, and one had cerebral infarction. One patient was diagnosed with analgetics-related headache, two patients suffered from prednisone-induced psychosis and one patient developed an acute confusional state following septicemia during immunosuppression. Mood disorder caused by social deprivation related to SLE was diagnosed in two patients. Cognitive dysfunction was caused by seizures in two patients and prednisone-related in one other patient. The prevalence of the 11 different ACR 1982 criteria for SLE is listed in Table 2. The mean number of SLE criteria per patient was 6,3 (SD 1,6, median 6) exclusive of the neuropsychiatric symptoms. Antiphospholipid (apl) antibodies were present in 69% of patients with primary NPSLE (Table 3); 66% of the patients were positive for acl and 23% for LAC. The antiphospholipid syndrome was 37
8 Table 2. Revised ACR 1982 SLE criteria (cumulative) present in 102 primary NPSLE patients compared to ACR 1982 cohort.* 24 ACR 1982 criteria Primary NPSLE n = 102 % (95% c.i.) ACR 1982 cohort n = 177 % Malar rash 32 (23-41) 57 Discoid rash 35 (26-45) 18 Photosensitivity 28 (19-36) 43 Oral ulcers 25 (16-33) 27 Arthritis 76 (67-84) 86 Serositis 45 (35-55) 56 Renal disorder 43 (34-53) 51 Hematologic disorder 54 (44-64) 59 Immunologic disorder 91 (84-96) 84 Antinuclear antibody 96 (90-99) 98 * ACR, American College of Rheumatology; NPSLE, neuropsychiatric systemic lupus erythematosus. established in 25% of primary NPSLE patients. In patients with CVD, apl antibodies were found in 67%; 49% of these patients were diagnosed with the antiphospholipid syndrome. For the treatment of neuropsychiatric syndromes in this cohort physicians prescribed methylprednisolone intravenously or high dose oral prednisone in 69% of the patients, cyclophosphamide pulse therapy intravenously in 28%, azathioprine in 24%, aspirin in 22% and oral anticoagulants in 29% of the patients. MRI findings of 102 patients with primary NPSLE are listed in Table 4. In 48 patients (47%) the MRI scan of the brain showed no abnormalities, including 14 patients with stroke syndrome. In 22 patients with an abnormal MRI scan only aspecific abnormalities (white matter hyperintensities and atrophy) were found. This implies that in 70 patients with primary NPSLE (69%) the MRI scan showed no or aspecific abnormalities. Table 3. Prevalence of antiphospholipid antibodies.* Primary NPSLE (n = 102) n (%) Secondary NPSLE (n = 11) n (%) Non-NP SLE (n = 42) n = (%) apl 70 (69) 6 (55) 28 (62) acl 67 (66) 5 (45) 28 (62) acl_igm 11 (10) - 7 (16) acl_igg 26 (25) - 3 (7) acl_igm + IgG 30 (29) 5 (45) 18 (40) LAC 23 (23) 1 (9) 7 (16) LAC 3 (3) - - LAC + acl 20 (20) 1 (9) 7 (16) APS 26 (25) 2 (18) 6 (13) * NPSLE, neuropsychiatric systemic lupus erythematosus; apl, antiphospholipid antibodies; acl, anticardiolipin antibodies; LAC, lupus anticoagulant; APS, antiphospholipid syndrome. 38
9 Chapter 2 : Early occurrence of NP manifestations in SLE Table 4. Imaging findings in 102 primary NPSLE patients studied with brain MRI.* n (%) Normal MRI 48 (47) Abnormal MRI 54 (53) WMH 31 WMH + infarctions 4 Ischaemic infarctions 14 Multifocal infarctions 8 Atrophy 20 Other 8 * NPSLE, neuropsychiatric systemic lupus erythematosus; MRI, magnetic resonance imaging; WMH, white matter hyperintensities. Discussion In this study, features of a large group of NPSLE patients were evaluated. Main observations were that neuropsychiatric symptoms occurred early in the disease course and second, that a large proportion of patients had no abnormalities on MRI cerebrum. SLE was diagnosed at the age of median 27.5 years; this is compatible to general SLE populations. In patients with primary NPSLE, neuropsychiatric symptoms occurred after a mean of 2.8 years after SLE was diagnosed. Moreover, in 39% of the patients, neuropsychiatric symptoms were the presenting symptom or these symptoms developed within one year after the diagnosis of SLE. These numbers are in line with previous studies. 27,28 In a recent prospective analysis of a large inception cohort of patients with SLE, neuropsychiatric symptoms also frequently presented early in the disease course and 40% of the patients experienced at least one neuropsychiatric symptom within the first three years. Those events attributed to SLE and focal neuropsychiatric events had a better outcome. It was suggested that, as for rheumatoid arthritis, this may indicate a therapeutic window of opportunity when pathogenetic mediators are amenable to immunosuppressive treatment. 29 Some features in our study are compatible with the involvement of immune-mediated pathogenetic mechanisms of neuropsychiatric manifestations. First, the early onset of neuropsychiatric symptoms indicates that lupus specific mechanisms such as autoantibodies might be involved. In SLE, the specificity of autoreactive antibodies increases early in the development of the disease, and it is conceivable that antibodies that cross-react with brain tissue also develop during this process. 30 This is compatible with the fact that age of SLE diagnosis and age of occurrence of neuropsychiatric symptoms have a comparable distribution. Accelerated atherosclerosis, however, can be an important pathogenetic factor in elderly SLE patients expressing neuropsychiatric symptoms for the first time, and could explain the higher prevalence of neuropsychiatric symptoms in the group between 55 and 65 years old. 31 As atherosclerosis is a progressive disorder, a relation with young age is not expected. Second, the possible immunemediated pathogenesis is supported by the absence of abnormalities on conventional MRI scan 39
10 of the brain in almost half of the patients. This might indicate subtle and more diffuse damage of brain tissue in a part of SLE patients with neuropsychiatric signs and symptoms. Though the presence of apl antibodies is correlated with focal syndromes such as stroke and seizures, these antibodies are also more frequently observed in SLE patients with diffuse neuropsychiatric manifestations, such as cognitive dysfunction. 16,17,32 MTR studies showed evidence for that fact that, apart from giving rise to macroscopic cerebral infarctions, acl antibodies may play a role in the pathogenesis of diffuse microscopic brain damage in NPSLE. 33 We also found significant correlation between the antiphospholipid syndrome and CVD, but in the group of NPSLE patients with CVD, MRI scan showed no abnormalities in a proportion of patients. CVD was diagnosed by neurological dysfunction which could be attributed to ischemia in brain tissue vascularized by a particular cerebral artery but was apparently not always caused by visible vascular occlusion or thrombosis. As new quantitative MRI techniques demonstrate more diffuse cerebral damage, further research in NPSLE patients without conventional MRI abnormalities is warranted. 34 In this study we describe the features of neuropsychiatric manifestations in patients referred for MRI scan of the brain because of suspected NPSLE. CVD, seizures, cognitive dysfunction and headache were the most common neuropsychiatric syndromes. Though the prevalence of neuropsychiatric syndromes in general SLE populations varies substantially in literature due to selection criteria and methodological issues, highest prevalence is often found for headache, cognitive dysfunction and mood disorder. 4 The ACR 1999 case definition system for neuropsychiatric symptoms in SLE provides a detailed guideline in describing neuropsychiatric manifestations in SLE. However, the assignment of the contribution of lupus activity to neuropsychiatric symptoms is often difficult to establish. In an unselected cohort of SLE patients, neuropsychiatric disease can be attributed to lupus activity itself (primary NPSLE) in roughly half of the cases. 9 Compared to literature we found a low number of patients with secondary NPSLE, especially infections. This could be caused by referral bias as many patients were referred to our clinic after careful evaluation in other departments or institutions. Selection of patients based on referral for MRI scan of the brain might also cause other bias. First, not all patients with neuropsychiatric symptoms are referred for MRI scan and probably more severe cases will be selected. This is also indicated by the observation that a high number of patients were treated with immunosuppressive agents and anticoagulants. Second, more CNS disease and less PNS disease will be observed. This could explain the higher number of patients with CVD and lower number of patients with PNS disorders than reported in literature. On the other hand, clear cases with cerebral infarctions, apl antibodies and compatible MRI abnormalities may have been referred less frequently and can therefore be underrepresented. As cognitive impairment was only evaluated in patients that complained of these symptoms, the real prevalence may be higher. We conclude that a large proportion of neuropsychiatric symptoms occur at a young age and early in the disease course of SLE patients. This observations is compatible with the concept of 40
11 Chapter 2 : Early occurrence of NP manifestations in SLE immune-mediated neuronal dysfunction. Furthermore, almost half of all MRI scans show no abnormalities in these patients. This might indicate subtle and more diffuse damage of brain tissue in a part of SLE patients with neuropsychiatric signs and symptoms. 41
12 References 1. Bresnihan B. Outcome and survival in systemic lupus erythematosus. Ann Rheum Dis 1989;48(6): Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003;82(5): Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A. The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 2001;57(3): Brey RL, Holliday SL, Saklad AR, Navarrete MG, Hermosillo-Romo D, Stallworth CL, et al. Neuropsychiatric syndromes in lupus: prevalence using standardized definitions. Neurology 2002;58(8): Jennekens FG, Kater L. The central nervous system in systemic lupus erythematosus. Part 1. Clinical syndromes: a literature investigation. Rheumatology (Oxford) 2002;41(6): Sibbitt WL, Jr., Sibbitt RR, Brooks WM. Neuroimaging in neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 1999;42(10): Ainiala H, Dastidar P, Loukkola J, Lehtimaki T, Korpela M, Peltola J, et al. Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: a population-based study. Scand J Rheumatol 2005;34(5): The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 1999;42(4): Hanly JG, McCurdy G, Fougere L, Douglas JA, Thompson K. Neuropsychiatric events in systemic lupus erythematosus: attribution and clinical significance. J Rheumatol 2004;31(11): Rood MJ, Breedveld FC, Huizinga TW. The accuracy of diagnosing neuropsychiatric systemic lupus erythematosus in a series of 49 hospitalized patients. Clin Exp Rheumatol 1999;17(1): Ellis SG, Verity MA. Central nervous system involvement in systemic lupus erythematosus: a review of neuropathologic findings in 57 cases, Semin Arthritis Rheum 1979;8(3): Hanly JG. Evaluation of patients with CNS involvement in SLE. Baillieres Clin Rheumatol 1998;12(3): Senecal JL, Raymond Y. The pathogenesis of neuropsychiatric manifestations in systemic lupus erythematosus: a disease in search of autoantibodies, or autoantibodies in search of a disease? J Rheumatol 2004;31(11): Omdal R, Brokstad K, Waterloo K, Koldingsnes W, Jonsson R, Mellgren SI. Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur J Neurol 2005;12(5): Hanly JG, Urowitz MB, Siannis F, Farewell V, Gordon C, Bae SC, et al. Autoantibodies and neuropsychiatric events at the time of systemic lupus erythematosus diagnosis: results from an international inception cohort study. Arthritis Rheum 2008;58(3): Brey RL. Antiphospholipid antibodies in young adults with stroke. J Thromb Thrombolysis 2005;20(2): Hanly JG, Hong C, Smith S, Fisk JD. A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis Rheum 1999;42(4): Abbott NJ, Mendonca LL, Dolman DE. The blood-brain barrier in systemic lupus erythematosus. Lupus 2003;12(12): DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B. A subset of lupus anti-dna antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 2001;7(11): Kowal C, DeGiorgio LA, Nakaoka T, Hetherington H, Huerta PT, Diamond B, et al. Cognition and immunity; antibody impairs memory. Immunity 2004;21(2): Huerta PT, Kowal C, DeGiorgio LA, Volpe BT, Diamond B. Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci U S A 2006;103(3): Emmer BJ, van der GJ, Steup-Beekman GM, Huizinga TW, van Buchem MA. Selective involvement of the amygdala in systemic lupus erythematosus. PLoS Med 2006;3(12):e
13 Chapter 2 : Early occurrence of NP manifestations in SLE 23. Harrison MJ, Ravdin LD, Lockshin MD. Relationship between serum NR2a antibodies and cognitive dysfunction in systemic lupus erythematosus. Arthritis Rheum 2006;54(8): Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25(11): Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997;40(9): Wilson WA, Gharavi AE, Koike T, Lockshin MD, Branch DW, Piette JC, et al. International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: report of an international workshop. Arthritis Rheum 1999;42(7): Shimojima Y, Matsuda M, Gono T, Ishii W, Ikeda SI. Relationship between clinical factors and neuropsychiatric manifestations in systemic lupus erythematosus. Clin Rheumatol 2005;24(5): Hanly JG, Urowitz MB, Sanchez-Guerrero J, Bae SC, Gordon C, Wallace DJ, et al. Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: an international inception cohort study. Arthritis Rheum 2007;56(1): Hanly JG, Urowitz MB, Su L, Bae SC, Gordon C, Wallace DJ, et al. Prospective analysis of neuropsychiatric events in an international disease inception cohort of SLE patients. Ann Rheum Dis 2010;69(3): Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003;349(16): Roman MJ, Crow MK, Lockshin MD, Devereux RB, Paget SA, Sammaritano L, et al. Rate and determinants of progression of atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2007;56(10): Mikdashi J, Handwerger B. Predictors of neuropsychiatric damage in systemic lupus erythematosus: data from the Maryland lupus cohort. Rheumatology (Oxford) 2004;43(12): Steens SC, Bosma GP, Steup-Beekman GM, le Cessie S, Huizinga TW, van Buchem MA. Association between microscopic brain damage as indicated by Magnetization Transfer Imaging and anticardiolipin antibodies in neuropsychiatric SLE. Arthritis Res Ther 2006;8(2):R Huizinga TW, Steens SC, van Buchem MA. Imaging modalities in central nervous system systemic lupus erythematosus. Curr Opin Rheumatol 2001;13(5):
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