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Central neurological manifestations in a sample of
Syrian patients with systemic lupus erythematosus:
cross-sectional study
Maysoun Kudsia, Bassel Achmehc,*, Naram Khalayli, MDb, Karam Rabahe, Nour Rabahe, Lama Al_Darwishd,
Fatima Alzahraa Alghawe, MDc
Introduction: The authors aimed to study systemic lupus erythematosus (SLE) central neurological patterns and their correlations
with the disease activity.
Patients and methods: The authors’retrospective observational study was carried out on admitted SLE patients. The patients’
demographic data, clinical examinations, laboratory tests, imaging studies, and systemic lupus erythematosus disease activity index
(SLEDAI) were recorded.
Results: Thirty-six SLE patients had neurological manifestations from 203 patients, but 8 patients were excluded. 90.2% were
females. The age of neuro-lupus manifestation was 24.1 +2.9 years. Neurological manifestations were the initial presentation in 25%
of patients. General seizures were the frequent manifestation. SLEDAI was 29.51 ±18.43, while it was 18.3 ±9.2 among patients
without neuropsychiatric systemic lupus erythematosus (NPSLE). Twenty-five percent of patients had pleocytosis on cerebrospinal
fluid (CSF) analysis. Small lesions were seen in 57.1% of patients on brain MRIs, and large lesions were observed in 10.6%. These
findings were compatible with the disease activity.
Discussion: Central nervous system involvement ranged between 10 and 80%, and much more with active disease. The frequent
finding was general seizures. Psychosis and cognitive impairment were relatively frequent. Adult NPSLE manifestations had
developed before or around the time of SLE diagnosis and within the first year after diagnosis. These manifestations were directly
correlated to the disease activity. Abnormality in CSF is characterized by slight pleocytosis, and elevation of protein with normal
fructose. MRI is the neuroimaging test of choice for NPSLE in clinical practice.
Conclusion: Central neurological involvement in SLE was seen early in the course of the disease, and correlating to the disease
activity.
Keywords: cognitive impairment, neurological manifestation, neuro-lupus, SLE
Introduction
Systemic lupus erythematosus (SLE) is a systemic connective tis-
sue disease, that predominates in women, Asian and Hispanic
populations
[1]
.
Neurologic symptoms occur in 6–91%, either before the
diagnosis of SLE or during its course
[2–5]
, even without serologic
activity or disease clinical presentations
[6]
. This wide range of
prevalence is due to variable presentations, using different study
designs, different criteria, and different methods for
screening
[4,7]
. It involves both central and peripheral nervous
system
[5]
.
The neuro-manifestations of SLE is classified into primary,
which is related to the direct involvement of the neuro system, and
secondary, which is related to the disease complications and/or its
treatment
[4]
. The American College of Rheumatology (ACR) has
formulated the definition of neuro-lupus
[8]
.
HIGHLIGHTS
•Systemic lupus erythematosus (SLE) primarily affects
women, Asian, and Hispanic populations.
•Neurologic symptoms can occur in SLE cases and are
classified as primary or secondary involvement.
•Sixty percent of Syrian SLE patients experienced neuro-
lupus manifestations.
•The most common symptoms of neuro-lupus were head-
aches, seizures, and cognitive disorders.
•Patients with neuro-lupus had higher SLE disease activity
scores, and a significant association was found between
neuropsychiatric symptoms and anti-dsDNA antibodies.
Departments of
a
Rheumatology,
b
Psychiatry,
c
Faculty of Medicine, Damascus
University,
d
Sham Private University, Damascus and
e
Faculty of Medicine, Syrian
Private University, Daraa, Syria
Sponsorships or competing interests that may be relevant to content are disclosed at
the end of this article.
Published online 8 July 2024
*Corresponding author. Address. Bassel Achmeh, 36 Bab-Touma Street,
Damascus, Damascus, Governorate 20000, Syria. Tel.: +96 393 671 0885.
E-mail: basselachmeh@outlook.com (B. Achmeh).
Received 23 October 2023; Accepted 30 June 2024
Copyright © 2024 The Author(s). Published by Wolters Kluwer Health, Inc. This is an
open access article distributed under the Creative Commons Attribution-
NoDerivatives License 4.0, which allows for redistribution, commercial and non-
commercial, as long as it is passed along unchanged and in whole, with credit to the
author.
Annals of Medicine & Surgery (2024) 86:5096–5100
http://dx.doi.org/10.1097/MS9.0000000000002361
’
Cross-sectional Study
5096
Studies have found that the frequent presentations were
headaches, seizures, cerebrovascular diseases, cranial neuro-
pathies, movement disorders, psychosis, cognitive disorders, and
others
[9,10]
.
The pathological etiologies are still obscure. Autoantibody
production, micro-angiopathy, intrathecal production of pro-
inflammatory cytokines, and premature atherosclerosis play a
role
[4,5,11]
.
This retrospective cohort study took place to evaluate the
frequency and characteristics of these manifestations, in a sample
of Syrian SLE patients and correlate them with the disease activity
since there have been no studies of NPSLE in Syria.
Patients and methods
Our retrospective observational study took place from
January.2015 to January. 2022. The hospital files of 203 SLE
patients were examined.
Inclusion criteria included SLE patients, diagnosed according
to the ACR criteria
[12]
, and the presence of SLE-related neuro-
logical symptoms, after signing the informed consent
[8]
.
Exclusion criteria included SLE patients with strokes, intra-
venous drug abuse, neurological infections, and encephalopathies
due to other causes, diabetes mellitus, hyperlipidemia, and elec-
trolyte disturbances.
We divided our cohort of patients into two groups. Group
A including patients with neuropsychiatric manifestations,
and Group B including those without neuropsychiatric
manifestations.
Demographic data, disease duration, clinical, labotorial, and
imaging findings of the disease were collected and analyzed.
Neuropsychiatric manifestations were reported from patients
medical records, including: Headaches, psychosis, seizures,
transient ischemic attacks, strokes, transverse myelitis, Cognitive
dysfunctions, chorea, cranial neuropathies and peripheral neu-
ropathies, based on ACR definition of neuro-SLE
[8]
.
Laboratory tests included: Complete blood count, erythrocyte
sedimentation rate, C-reactive protein, urea, creatinine, and liver
enzymes. All analyzed within 1 h after the collection of samples.
Immune profile included: Complement (C3, and 4), ANA,
Anti-Smith, anti-ds DNA, Lupus Anticoagulant, anti-cardiolipin,
anti-β2-glycoprotein 1 antibodies.
Urinalysis and 24 h proteinuria analysis, were performed.
Cerebrospinal fluid analysis was performed, when necessary.
Nerve conduction studies, electromyography, and electro-
encephalography if necessary were also performed. Conduction
velocity of action potential in meters per second was the used
criteria.
MRI of the brain was done using (3 Tesla) Siemens machine, in
addition to MR angiography when necessary.
The disease activity index of the SLEDAI contained 20 vari-
ables, and was used to evaluate the disease activity. Patients were
classified as: high (20), moderate (10–20), and mild/in remission
(<10)
[13]
.
Statistical analysis
Statistical Package for Social Sciences (SPSS) software version 23,
and Excel2010 were used. Data were presented as mean standard
deviations and percentiles. The t-student test, χ
2
test, and Fisher’s
exact test were utilized. The Kolmogorov–Smirnov was used to
verify the normality of variables distribution. Pvalueless than
0.05 was considered statically significant.
Our study is compatible with the STROCCS guidelines of the
annals of medicine and surgery journal
[14]
.
Results
As shown in Table 1, this study included 203 patients with SLE.
Thirty-six (17.73%) of SLE patients) had neurological manifes-
tations, and 167 patients without NPSLE. Eight patients were
excluded from neuropsychiatric systemic lupus erythematosus;
due to the presence of uremic encephalopathy resulting from
renal involvement by SLE (4 patients), hypertension-induced
intracranial hemorrhage (2 patients), meningitis (2 patients), and
the remaining were 28 patients. In 8 out of 28 patients (25%),
neurological manifestations were the initial presentation of SLE.
The mean age of group A was 27.4 ±7.7 (18–50), while it was
28.4 ±8.5 (18–52) years in group B. In group A, 26 (90.2%)
were females, and 2 (7.1%) were males, while in group B, 155
(92.81%)were females, and12 (7.1%) were males. The mean
duration of the disease was 5.9 ±3.8 years in group A, and
6.1 ±3.5 years in group B.
In patients of group A, malar rash was present in 78.5%
(n=22), photosensitivity in 64.2% (n=18). Serositis in 53.2%
(n=15) patients, arthralgia was noted in almost all patients
92.7% (n=26), articular arthritis was noted in 53.2% (n=15)
patients, hematological disorders in 42.5% (n=12), renal
involvement in 82.1% (n=23), cardiac manifestations in 6
(21.42%), pulmonary manifestations in 4 (14.28%), thrombotic
event in 5 (17.85%), fatigue in 18 (28%) patients, and fever in
28% (n=18) patients. While in group B, the malar rash was
present in 78.44% (n=131), photosensitivity in 59.88%
(n=100). Arthralgia was noted in almost all patients 98.20%
Table 1
Comparison between the studied groups according to
demographic data
Variable
Patients with
neuropsychiatric
manifestations
(group A) (n=28)
Patients without
neuropsychiatric
manifestations
(group B) (n=167) P
Age in years
(mean ±SD)
27.4 ±7.7 (18–50) 28.4 ±8.5 (18–52) NS
Sex, N(%)
Female 26 (90.2) 155 (92.81) NS
Male 2 (7.1) 12 (7.1)
Educational level, N(%)
Bachelor, or less 18 (64.28) 35 (20.95) NS
University 8 (28.57) 132 (79.04) <0.05
Marital status, N(%)
Single 10 (35.71) 54 (32.33) NS
Married 18 (64.28) 113 (67.66) NS
Work
Employed 18 (64.28) 100 (59.88) NS
Unemployed 10 (35.71) 67 (40.11) NS
Menstrual period
Normal 14 (50) 126 (75.44) <0.05
Abnormal 14 (50) 41 (24.55) <0.05
Disease duration 5.9 ±3.8 6.1 ±3.5 NS
Statistically significant P values are in bold.
NS, not specified.
Kudsi et al. Annals of Medicine & Surgery (2024)
5097
(n=164), articular arthritis was noted in 50.89% (n=85)
patients, hematological disorders in 47.90% (n=80), renal
involvement in 52.09% (n=87), and fever in 28.74% (n=48)
patients. Renal involvement was significantly higher in group A
patients compared to group B patients (P<0.05).
SLEDAI was 20.1 ±8.2 in group A patients and 13.9 ±6.9
(P<0.05) in group B patients.
Headaches had the highest percentage 28.57%, then seizures
21.42%, cognitive dysfunction 10.7%, and finally psychosis
10.7% (Table 2).
Generalized seizures in 5 out of 6 patients (83.33%), and 5 out
of 28 patients (17.85%) were the most frequent type of seizures.
One patient had a partial seizure in the form of epilepsy partials’
continuing to involve the facial muscles.
Persistent headache, not relieved by narcotics was present in 5
(17.85%) patients.
Cognitive impairment assessment of group A, by using the mean
Mini-Mental State Examination (MMSE)
[15]
score was 28.79 ±
1.98, while i t was 19.71 ±6.12(P<0.05) in group B patients.
Out of 28 patients studied, 25 (89.28%) had normal cognitive
function with an MMSE score between 24 and 30. Two patients
(7.1%) had mild cognitive impairment, with a score between 18 and
23, while one (3.57%) had severe cognitive impairment. (Table 3).
Laboratory findings at the presentation
As shown in Table 4, results of complete blood picture were
compared between both groups, with an evaluation of different
laboratory abnormalities found in patients of SLE as anemia,
leukopenia, lymphopenia, neutropenia and thrombocytopenia
and there was no significant difference between both groups.
However, regarding immunological profile, group A patients had
lower C3 and C4 levels, and more lupus anticoagulant level, ACL
level, and β2 GP 1 level.
Cerebral spinal fluid (CSF) analysis
CSF was performed and analyzed in 8 patients from group A.
Fifty-eight percent of the CSF analysis were completely normal,
25% revealed pleocytosis, 18% showed increased protein con-
tent, and 2% showed decreased glucose levels (Table 4).
Brain images in NPSLE patients
Among the 28 available brain MRIs, small lesions were seen in 16
(57.1%) brain MRIs, and large lesions were observed in two
(10.6%) MRIs. All abnormal MRIs revealed hyperintense lesions
in T2-weighted images, but only in 14 (50%), MRIs were cor-
responding hypointense lesions in T1-weighted images. These
characteristics were compatible with ischemic/demyelinating
lesions. Twelve patients had high disease activity (SLEDAI ≥20).
Nerve conduction studies and electromyography revealed a
myogenic pattern in 3 (10.7%) patients; there was myositis and a
neurogenic pattern with conduction block in the patient with the
Guillain–Barre syndrome.
A treatment comparison between the two groups is revealed in
Table 5.
Table 2
The neuro-manifestations of SLE
Manifestation Frequency (percentage), N(%)
Headache 8 (28.57)
Seizure 6 (21.42)
Cognitive dysfunction 3 (10.7)
Psychosis 3 (10.7)
Cranial neuropathy 3 (10.7)
Peripheral neuropathy 2 (7.14)
Stroke 2 (7.14)
Aseptic meningitis 1 (3.57)
Table 3
MMSE score
Score Patients Percentage (%)
24–30 25 89.28
18–23 2 7.14
0–17 1 3.57
MMSE, Mini-Mental State Examination.
Table 4
Laboratory findings at the presentation of both groups
Laboratory parameter
NPSLE patients
(group A) (28), N(%)
SLE patients (group
B) (167), N(%) P
ANA 27 (96.42) 155 (92.8) NS
Anti-ds DNA 20 (71.42) 100 (59.88) <0.05
Anti-smith 4 (14.28) 27 (16.16) NS
C3 9 (32.14) 90 (53.89) <0.05
C4 7 (25) 82 (49.10)
Leukopenia 10 (35.71) 54 (32.33) NS
Lymphopenia 6 (21.42) 42 (25.14) NS
Thrombocytopenia 4 (14.28) 18 (10.77) NS
Lupus anticoagulant 4 (14.28%) 6 (4.7%) <0.05
ACL
Ig M 5 (17.85) 7 (4.19%) <0.05
Ig G 5 (17.85) 7 (4.19%) <0.05
Anti β2GP1
Ig M 2 (7.4%) 1 (0.59%) <0.05
Ig G 2 (7.4%) 1 (0.59%) <0.05
Statistically significant P values are in bold.
ACL anti-cardiolipin; ANA antinuclear antibody; Anti β2 GP 1 anti β2 glycoprotein I; Anti-dsDNA anti-
double stranded DNA antibodies; C3, complement 3; C4, complement 4; NPSLE, neuropsychiatric
systemic lupus erythematosus; NS, not specified; SLE, systemic lupus erythematosus.
Table 5
Treatment of both groups.
Drug
NPSLE patients
(group A), N(%)
SLE patients
(group B), N(%) P
Corticosteroids
<10 mg/day 7 (25) 42 (25.14) <0.05
10–20 10 (35.71) 82 (49.1)
20–30 8 (28.57) 26 (15.56)
>40 3 (10.71) 17 (10.17)
Methyleprednisolone 15 (53.57) 84 (50.29)
Hydroxychloroquine 24 (85.71) 142 (85.02)
Azathioprine 12 (42.85) 80 (47.90)
Cyclophosphamide 7 (25) 47 (28.14)
Mycophenolate mofetil 5 (17.85) 34 (20.35)
Rituximab 4 (14.28) 4 (2.3) <0.05
Statistically significant P values are in bold.
NPSLE, neuropsychiatric systemic lupus erythematosus; SLE, systemic lupus erythematosus.
Kudsi et al. Annals of Medicine & Surgery (2024) Annals of Medicine & Surgery
5098
Discussion
Nervous system involvement in SLE is frequent, serious, poten-
tially treatable, and affects both central nervous system (CNS)
and peripheral nervous system (PNS). Central involvement can
present as aseptic meningitis, cerebrovascular accidents, head-
aches, psychosis, and many others. It usually occurs during the
active disease
[1,2]
.
CNS involvement ranged between 10 and 80% (3), according
to studies, as in our one (17.73%). In this present study, head-
aches were the frequent presentation followed by seizures,
decreased level of consciousness, and weakness. This is compa-
tible with some other studies
[16,17]
. Meanwhile, seizures were a
frequent neurological feature in other studies that had occurred
during the disease course alone or with another neurological
manifestation
[1,18]
.
The frequency of headaches among SLE patients is (28–68%),
and it was 66%, which is compatible with studies
[15,19]
.
Studies have registered the frequency of cerebrovascular acci-
dents among SLE patients
[20]
. The frequency of a cerebrovascular
disease in our study was 35.6%, while it was less than that in the
studies of to Futrell and Milikan
[21]
. This may have been due to
their small-sized patients sample (105), and the study of risk
factors for stroke.
Acute meningitis and cranial nerve palsy are rare
[22]
, as in our
case. The use of non-steroidal anti-inflammatory treatment may
cause meningitis as a side effect
[1]
. We had one patient with this
manifestation.
In our study, psychosis and cognitive impairment were the
frequent presentations.
Psychosis and depression are frequent. Psychosis must be dif-
ferentiated from corticosteroid-induced psychosis
[4]
. Cognitive
impairment occurs frequently due to the diagnostic criteria
used
[1]
. Cognitive impairment was 10.7% in our series, and this is
in contrast with other results
[23,24]
. These variable differences
may be due to criteria selection, geographic region, and ethnicity.
In 8 patients (25%), neurological symptoms were the initial
presentation of SLE, moreover, it may be developed earlier and in
younger patients. Our results are compatible with some
studies
[1,5]
.
SLEDAI score was significantly higher in patients with group A
compared to those of group B. In addition, the neurological
manifestations were directly correlated to the disease activity
[24]
,
such as in our study.
CSF findings in neuro-lupus are pleocytosis, elevated protein,
and normal sugar level
[1]
, as 25% of our patients had elevated
white blood cells.
MRI is the best neuro-imagining tool for detecting NPSLE
[25]
.
Our results showed that small lesions were found in 57.1%, and
large ones were seen in 10.6%. Abnormal MRIs revealed hypo-
dense lesions in T1-weighted images, and hyperdense lesions in
T2-weighted images, which is compatible with previous
reports
[1,25]
.
EEG abnormalities were observed in patients with clinical
neuro-lupus, but it may be an indicator for subclinical neuro-
lupus
[1]
. In our study, electromyography revealed a myogenic
pattern in 3 (10.7%) patients; there was myositis and a neuro-
genic pattern, with conduction block in the patient with the
Guillain–Barre syndrome, like some other previous studies
[1,26]
.
The limitation to our study was the small sample size enrolled
in one center, when compared to the different neurological pub-
lished articles (Table 6).
Ethical approval/declaration of Helsinki
Approval of Ethical Board (NS: 2321) was credited, and in
accordance with the Declaration of Helsinki, the study was
performed.
Consent
Written informed consent was obtained from the patients for
publication and any accompanying images. A copy of the written
consent is available for review by the Editor-in-Chief of this
journal on request.
Source of funding
Not applicable.
Author contribution
M.K.: supervision, writing—review and editing. B.A.: con-
ceptualization, writing—original draft , writing—review and
editing. N.K.: data curation, writing—review and editing. K.R.:
writing—review and editing. N.R.: writing—review and editing.
L.A.D.: data curation, writing. F.A.A.: resources, review.
Table 6
The different neurological published articles
Study features Present study Robert et al.
[27]
Brey et al.
[28]
Sanna et al.
[29]
Khare et al.
[30]
No. patients included in the study 52 50 128 323 35
Nervous system involvement, N(%) 19 (36.54) 39 (78) 102 (80) 185 (57.3) 35 (100)
Cognitive dysfunction, N(%) 11 (57.89) 7 (17.95) 35 (10.8) 3 (9)
Seizure, N(%) 8 (42.1) 8 (20.51) 21 (16) 27 (8.3) 23 (66)
Acute confusional state, N(%) 6 (31.57) 6 (16.2) 12 (3.7) 7 (20)
Headache, N(%) 5 (26.31) 20 (55.6) 73 (57) 78 (24) 2 (6)
Depression, N(%) 5 (26.1) 37 (28)
Psychosis, N(%) 4 (21.05) 6 (16.2) 6 (5) 25 (7.7) 3 (9)
Polyneuropathy, N(%) 4 (21.05) 29 (22) 2 (6)
Cerebrovascular accident, N(%) NS 6 (16.2) 2 (2) 47 (14.5) 2 (6)
Movement disorder, N(%) NS 8 (20.51) 1 (1)
NS, not specified.
Kudsi et al. Annals of Medicine & Surgery (2024)
5099
Conflicts of interest disclosure
The authors declare no conflicts of interest.
Research registration unique identifying number
(UIN)
Researchregistry 9187
https://www.researchregistry.com/browse-the-registry#home/
Guarantor
Maysoun Kudsi.
Data availability statement
Not applicable.
Provenance and peer review
This paper is published solely and not invited.
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