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August 14, 2001; 57 (3) Articles

The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus

H. Ainiala, J. Loukkola, J. Peltola, M. Korpela, A. Hietaharju
First published August 14, 2001, DOI: https://doi.org/10.1212/WNL.57.3.496
H. Ainiala
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J. Loukkola
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J. Peltola
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M. Korpela
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The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus
H. Ainiala, J. Loukkola, J. Peltola, M. Korpela, A. Hietaharju
Neurology Aug 2001, 57 (3) 496-500; DOI: 10.1212/WNL.57.3.496

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Abstract

Objective: To describe the prevalence of neuropsychiatric (NP) syndromes in a Finnish population of patients with systemic lupus erythematosus (SLE) and to classify them according to the recently developed American College of Rheumatology (ACR) nomenclature and case definitions for NPSLE.

Methods: Cross-sectional, population-based study covering an area with 440,000 people. A total of 58 patients with a definite diagnosis of SLE and aged 16 to 65 years were found in the computerized database of the area hospitals. Of these, 46 (79%) agreed to participate. The diagnosis of various NP syndromes was based on clinical impression (H.A.) following history, examination, review of medical records, and neuropsychologic testing.

Results: At least one NP syndrome was identified in 42 patients (91%). The most frequent manifestation was cognitive dysfunction (n = 37; 81%), followed by headache (n = 25; 54%) and mood disorder (n = 20; 43%). When mild NP syndromes (mild cognitive deficit, headache, mild depression, anxiety, electroneuromyography-negative polyneuropathy) were excluded, the prevalence of NPSLE dropped to 46%.

Conclusions: According to the ACR nomenclature, there is a high prevalence of NP manifestations in a population-based sample of patients with SLE. Most NP syndromes were classified as minor; if they were excluded, the 46% prevalence of NPSLE would be slightly less than estimated in previous studies.

A challenging problem in systemic lupus erythematosus (SLE) is the diagnosis and management of neuropsychiatric (NP) involvement. NPSLE may present with serious manifestations (e.g., acute confusional state, seizure disorder, and stroke), but more subtle deficits such as mild cognitive dysfunction have also been recognized.1,2⇓ The prevalence of NPSLE ranges widely between 14 and 75%, reflecting variable diagnostic criteria and differences in selection of patients for study.3,4⇓ A former definition for NPSLE in the 1982 revised American College of Rheumatology (ACR) criteria for SLE is inadequate because only two elements, psychosis and seizures, were included.5 The ACR has recently developed a standardized nomenclature system which provides case definitions for 19 NP syndromes seen in SLE, including reporting standards and recommendations for laboratory and imaging tests.6

We studied the prevalence of NP syndromes in a Finnish population-based cohort of patients with SLE and classified the syndromes according to the ACR nomenclature and case definitions.

Patients and methods.

Patient selection.

The study base was Pirkanmaa Health Care District located in southern Finland with a population of 440,000. The majority of new patients with SLE in the area are seen at Tampere University Hospital. We identified patients with SLE using the computerized databases of Tampere University Hospital, the three District Hospitals, and the local outpatient clinic. Medical records of both in- and outpatients coded for the diagnosis of SLE between January 1980 and December 1997 were examined to select patients who fulfilled four or more of the 1982 revised ACR criteria for the disease,5 were aged 16 to 65 years and of native Finnish origin, and resided in the study area. We excluded patients with another connective tissue disease.

We identified 110 patients with SLE. Of these,15 patients had died and 37 did not meet the inclusion criteria. The remaining 58 patients were contacted by mail, and 46 of them (79%) agreed to participate in the study. All participants gave written informed consent. The study protocol was approved by the local Ethics Committee.

Clinical and laboratory evaluation.

The diagnosis of various NP syndromes was based on clinical impression (H.A.) following history, examination, review of medical records, and neuropsychologic testing. All past and current NP syndromes were listed and classified according to the standardized ACR nomenclature and case definitions6 (table1). Individual disease activity was quantified by using the European Consensus Lupus Activity Measurement (ECLAM) scale.7 Current and previous use of steroid and other immunosuppressive medication was recorded. Cumulative lifetime dose of steroids (expressed as grams of prednisolone) was determined from the patients’ records. Electroneuromyography (ENMG) was performed on patients with clinical signs/symptoms suggesting polyneuropathy. Besides routine serological tests, IgG-type anticardiolipin antibodies (aCL) and B2-glycoprotein antibodies (B2GPAbG) were measured by ELISA (commercial kit).

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Table 1.

The neuropsychiatric syndromes in patients with systemic lupus erythematosus according to the American College of Rheumatology nomenclature and case definitions3

Neuropsychologic measures.

All patients were submitted to a battery of standardized neuropsychologic tests to detect possible impairment in one or more of the subsequent cognitive domains: simple attention, complex attention, memory, visuo-spatial processing, language, reasoning/problem solving, psychomotor speed, and executive functions. The tests were administered by a trained psychologist. It took an average of 3 to 4 hours to complete the assessment. The individual test results were converted into standard scores, which were compared with the available normative data.8-12⇓⇓⇓⇓ Regarding any of the eight cognitive domains, subjects with a total score of two or more standard deviations (SD) below the normative value were considered to be impaired. Cognitive dysfunction was classified as mild if there were deficits in less than three dimensions, as moderate if there were deficits in three or four dimensions, and as severe if there were deficits in at least five dimensions.

Assessment of depression was based on clinical interview and the Beck Depression Inventory (BDI).13,14⇓ On BDI, scores from 10 to 17 were considered to indicate mild depression, from 18 to 24 moderate depression, and greater than 24 severe depression. However, the final grading of depression was based on a clinical interview by the psychologist. Anxiety was evaluated by the psychologist on clinical interview.

Statistical analysis.

Pearson exact χ2 test for cross-tabulated data, two-sample Student’s t-test, and Mann–Whitney U test were used to evaluate the association between occurrence of any NP manifestation and current or prior steroid use. The limit for significance was set equal to 0.05.

Results.

We studied 39 women and seven men, with a mean age of 45 ± 13 years (range 20 to 64). The mean disease duration since diagnosis of SLE was 14 ± 8 years (range 2 to 37). The mean number of ACR SLE criteria fulfilled was 5.5 ± 1.2 (range 4 to 9). The mean level of education was 13 ± 3 years (range 8 to 18). The mean ECLAM score was 1.6 (range 0 to 5), indicating a very mild disease activity. At the time of the study, 25 patients (54%) were using glucocorticoids, seven (15%) were on antimalarials, five (11%) on azathioprine, two (4%) on methotrexate, and one (2%) on cyclosporin. Nineteen patients (41%) were without specific medication. For those who had taken steroids, the mean cumulative lifetime dose of prednisolone was 26 g (range 1 to 89). A total of four patients (9%) had never used corticosteroids.

At least one NP syndrome was identified in 42 patients (91%). Five patients (11%) had one, 12 patients (26%) had two, 15 patients (33%) had three, four patients (9%) had four, four patients (9%) had five, and two patients (4%) had six NP syndromes, whereas only in four patients was no evidence of NP syndromes detected (table 2).

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Table 2.

Neuropsychiatric syndromes in 46 patients with systemic lupus erythematosus

The most frequent single manifestation was cognitive dysfunction, detected in 37 patients (81%). Memory dysfunction was the most affected domain registered in 20 patients (43%), followed by deficits in simple attention, visuospatial processing, and psychomotor speed, each in 12 patients (26%). Only 14 of 37 patients (38%) with cognitive dysfunction by testing had cognitive problems. Headache was diagnosed in 25 patients (54%). Depression, consisting of a major depressive-like episode of mostly mild severity in 18 and a mood disorder with mixed features in two patients, was detected in 43% of patients. Clinical findings possibly related to polyneuropathy were detected in 13 patients, but only four patients had subjective symptoms. ENMG findings consistent with polyneuropathy were present in only three of them. Seven patients (15%) had a history of cerebrovascular disease. No intracerebral hemorrhages were recorded. Mean time since the diagnosis of SLE to the occurrence of the first stroke or transient ischemic attack was 11 years (range 1 to 18). In four patients cerebrovascular disease was concomitant with systemic disease activity.

One patient (2%) had a demyelinating syndrome. The neurologic symptoms appeared with subacute onset 18 years after the diagnosis of SLE. In CSF examination, IgG index was elevated and eight oligoclonal bands were present, indicating intrathecal synthesis. Increased signal in periventricular white matter and at the level of corona radiata on T2-weighted MRI scans was observed. Both aCL (151 IgG phospholipid unit) and B2GPAbG (333 standard IgG anti-beta 2 GPI unit) levels were in the high positive range.

There was an association between history of headache and current steroid use (χ2 = 4.114; p = 0.043). Compared with other patients with SLE, those with a history of epileptic seizures (mean 65.0g vs 23.0g; t = 3.319, p = 0.002) or cerebrovascular disease (mean 45.4g vs 22.7g; t = 2.288, p = 0.028) had a higher cumulative lifetime dose of steroids. No other associations between occurrence of NP manifestation and steroid use were noticed.

Discussion.

In our study of 46 patients with SLE, 91% were identified to have at least one NP syndrome, whereas in previous studies, the prevalence of NPSLE was significantly lower, ranging from 14 to 75%.15-20⇓⇓⇓⇓⇓

The main explanation for the exceptionally high prevalence of NP involvement in our study is most likely that the ACR nomenclature system includes a wide array of different neurologic and psychiatric features as diagnostic elements. In most former studies the diagnosis of NPSLE was entirely based on major neurologic and psychiatric involvement, such as cerebrovascular event, neuropathy, movement disorder, transverse myelitis, seizure, meningitis, organic brain syndrome, and psychosis.15-16⇓ Patients with SLE also present with a number of minor neurologic and psychiatric problems such as headache, mild depression, anxiety, and cognitive complaints that have now been included in the new nomenclature system. If these minor manifestations and also ENMG-negative polyneuropathy were excluded, the prevalence of NPSLE in our series would be 46% instead of 91%.

Another important difference compared with former studies is in patient selection. To our knowledge, no population-based study on the prevalence of NPSLE has been published so far. In the previous studies patients have been gathered from academic referral centers likely to be biased in terms of disease severity in comparison with the general population. Furthermore, much milder forms of the disease are now being recognized than a few decades ago.20

Cognitive impairment was the most frequent finding, occurring in 37 patients (80%). Previously reported prevalence rates have been lower, ranging from 21 to 66%.2,21-26⇓⇓⇓⇓⇓⇓ According to the ACR nomenclature, individual patients were defined as cognitively impaired if they demonstrated an impairment in one or more of eight areas of cognitive ability. In 70% of our patients with cognitive impairment, the dysfunction was classified as mild, implying that the impairment was established in only one or two cognitive domains. Eleven patients had three or more impaired areas, fulfilling the criteria for cognitive impairment used in other studies.21 Based on this definition, only 24% of our study population would have been classified as having a cognitive impairment. This figure is in accordance with prevalence rates of 21% in a study of 70 unselected patients with SLE21 and 26% in a study of 73 patients.22

In our study population, 25 patients (54%) had had headache, with lifetime prevalence of migraine and tension headache being 39 and 15%. The prevalence of tension headache in our study was actually slightly lower than in the healthy population.27-29⇓⇓

The reported prevalence rates of psychiatric manifestations in SLE have varied from 20 to 70%.22,30⇓ Recent reports have focused on the occurrence of milder psychiatric features such as depression and anxiety, whereas, in contrast to older studies, low prevalence of psychosis has been observed.20,22⇓ Our results corroborate this finding: 80% of patients with mood disorder had mild depression requiring no medication, whereas none had experienced any episode of psychosis.

Cerebrovascular disease was diagnosed in seven (15%) of our patients with SLE. In earlier studies, the frequency of stroke varied from 3 to 19%.15-19,31⇓⇓⇓⇓⇓ Patients with SLE who have had a stroke or transient ischemic attack are at high risk for recurrent cerebral ischemia.32 Two of our seven patients with cerebrovascular disease had a recurrence of stroke or transient ischemic attack, and one had a chronic multifocal disease. A significantly higher cumulative lifetime dose of steroids in patients with SLE with a history of cerebrovascular disease obviously reflects the severity of this subgroup.

A mild, symmetric distal sensory or sensorimotor neuropathy is the most common form of peripheral neuropathies in SLE.16 A 28% frequency of polyneuropathy in the current study is certainly overestimated, because the ACR nomenclature system does not demand an ENMG confirmation of polyneuropathy. The corresponding prevalence of ENMG-confirmed polyneuropathy in our series was 7%, in accordance with the previous studies.15-18,33-34⇓⇓⇓⇓⇓

One of the patients fulfilled the ACR nomenclature criteria for a demyelinating syndrome which may be reminiscent of MS.35-36⇓ Our patient had neurologic and MRI findings similar to MS, but a high positive titer of aCL together with the history of thrombocytopenia and deep venous thrombosis strongly favors the diagnosis of antiphospholipid syndrome. Oligoclonal banding has been described to occur in patients with secondary antiphospholipid syndrome caused by SLE.36 We suggest that future revisions of the ACR nomenclature system specifically exclude antiphospholipid syndrome in the diagnosis of a demyelinating syndrome.

The main weakness of the study is the small sample size, and therefore the results should to be interpreted with caution. As a cross-sectional study, the validity of disease history depends on the documentation of past disease episodes. We think that this is unlikely to have a substantial effect on the prevalence rates of the NP syndromes, but reliable discrimination between primary NPSLE, secondary NPSLE, and concurrent disease process becomes problematic. It has been estimated that two-thirds of NP manifestations in SLE are not directly related to NPSLE but are due to secondary causes such as drugs, infections, and metabolic complications of the disease.37,38⇓ Prospective analyses would help in discriminating between primary and secondary NPSLE.

Acknowledgments

Supported by the Medical Research Fund of Tampere University Hospital.

Acknowledgment

The authors thank Prof. Anssi Auvinen for helpful comments and critical review of the manuscript and Riina Metsänoja for statistical advice.

Footnotes

  • Additional material related to this article can be found on the Neurology Web site. Go to www.neurology.org and scroll down the Table of Contents for the August 14 issue to find the title link for this article.

  • Received October 17, 2000.
  • Accepted April 7, 2001.

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Letters: Rapid online correspondence

  • Reply to Letter to the Editor
    • Hanna Ainiala, Tampere University Hospital Tampere Finlandjukkaps@koti.tpo.fi
    Submitted March 15, 2002
  • The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus
    • Ignacio Casas Parera, Buenos Aires Argentinaescabio08@yahoo.com
    • Sara Malagold
    Submitted March 15, 2002
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