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Systemic lupus erythematosus in the elderly

Article in Rheumatology International · May 2011

DOI: 10.1007/s00296-010-1744-3 · Source: PubMed

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Rheumatol Int (2012) 32:1225–1229
DOI 10.1007/s00296-010-1744-3
O R I G I N A L A R T I CL E
Systemic lupus erythematosus in the elderly
Achouak Achour · Amani Mankaï · Yosra Thabet · Wahiba Sakly ·
Fehmi Braham · Chedia Kechrid · Fethi Bahri · Elyès Bouajina ·
Sawssen Chouchène · Ons Haddad · Ibtissem Ghedira
Received: 10 August 2010 / Accepted: 30 December 2010 / Published online: 22 January 2011
© Springer-Verlag 2011
Abstract Onset of the disease above the age of 65 years
is unusual. This study was undertaken to determine retro-
spectively the clinical and laboratory features in SLE
patients aged over 65 years. It is a retrospective study about
18 elderly patients with SLE out of 342 diagnosed between
1994 and 2009 in the center of Tunisia. All patients had at
least 4 of 11 revised ACR criteria of SLE. The frequency of
SLE in the elderly was 5.3%. The median age was 70 years
(range 66 and 78 years). The sex ratio F/M was 5. The most
frequent clinical signs were anemia (83.3%), arthralgia
(55.5%), arthritis (38.9%), and malar rash (33.3%). The
proteinuria and the neuropsychiatric troubles were present
in 27.8% of cases. The pericarditis was present in 16.7% of
cases. Antibodies to double stranded DNA (anti-dsDNA)
A. Achour · A. Mankaï (&) · Y. Thabet · W. Sakly · F. Braham ·
I. Ghedira
Research unit (03/UR/07-02), Faculty of pharmacy,
Rue Avicenne, 5000 Monastir, Tunisia
e-mail: amani.mankai@yahoo.fr
C. Kechrid
Internal Medicine Department,
Sahloul Hospital, Sousse, Tunisia
F. Bahri
Internal Medicine Department,
Farhat Hached Hospital, Sousse, Tunisia
E. Bouajina
Rheumatology Department,
Farhat Hached Hospital, Sousse, Tunisia
S. Chouchène · O. Haddad · I. Ghedira
Laboratory of Immunology,
Farhat Hached Hospital, Sousse, Tunisia
were detected in 66.7%, anti-nucleosome in 50%, anti-SSA
and anti-RNP in 27.8%, anti-Sm in 22%, and anti-SSB in
11%. Elderly patients with SLE exhibit distinct clinical and
biological manifestations from the classic form. Thus,
greater attention should be given for this particular sub-
group of SLE patients to avoid delays in diagnosis or misdi-
agnosis.
Keywords Systemic lupus erythematosus · Elderly ·
Tunisia · Clinical and biological features
Introduction
Systemic lupus erythematosus (SLE) is a multisystem dis-
order that predominately aVects women of the reproductive
age. It is characterized by a broad range of clinical and lab-
oratory manifestations and is notable for a variable course,
prognosis, and response to treatment [1].
Etiopathogenetic factors, which can inXuence the devel-
opment of SLE, include, most of all, genetic background of
the patient, external environmental agents (e.g., superanti-
gens, viruses, UV radiation, drugs, chemicals), hormonal
factor, age, and probably also other factors that are as yet
unknown. The result is disturbance of the immunologic
homeostasis, with resultant induction and production of
auto-antibodies contributing to tissue damage [2].
The age of diagnosis of most SLE patients is between 10
and 50 years old [3]. However, some investigators reported
that the uncommon late-onset SLE patients have some
diVerences in clinical and laboratory features from the
younger patients. Late-onset SLE has been deWned as the
disease onset occurring at age older than 50 years [4–7].
Other studies have only described SLE in elderly (older
than 65 years) [8–10].
123
1226
SLE in the elderly is rare. The aim of our study was to
identify and analyze retrospectively clinical and serological
features of SLE in the elderly population in the center of
Tunisia.
Materials and methods
We retrospectively identiWed 18 SLE patients aged over
65 years and diagnosed between 1994 and 2009. The
median age was 70 years (range 66 and 78 years). There
were 15 women and 3 men (Table 1).
All SLE patients fulWlled at least four criteria of the 1997
American College of Rheumatology (ACR) updated crite-
ria for classiWcation of SLE [11]. The average number of
criteria was 4.55. In addition to the 11 criteria, some signiW-
cant organ involvement and laboratory data were further
used for the evaluation of clinical and serological features
of SLE. The SLE disease activity index (SLEDAI) and the
number of SLE criteria fulWlled were used for measuring
the severity of disease [12].
The study was approved by local Ethics Committee and
all patients gave their informed consent.
Laboratory assessment
Laboratory investigations included serological tests that
detect auto-antibodies. The antinuclear antibodies (ANA)
were determined using the indirect immuno-Xuorescence
technique (IIF) on sections of rat liver (frozen sections of 4
microns thick made in the laboratory) as described previ-
ously [13]. The anti-double stranded DNA antibodies (anti-
dsDNA) were detected by enzyme linked-immunoassay
(ELISA) (ORGENTEC®, Mainz, Germany) and IIF with
Crithidia luciliae (ORGENTEC®, Mainz, Germany) as sub-
strate. Antibodies to extractable nuclear antigens (anti-Sm,
anti-SSA, anti-SSB and anti-RNP antibodies) and anti-
nucleosome antibodies were detected also by ELISA
(ORGENTEC®, Mainz, Germany). Results are expressed in
international units.
Table 1 Basic demographics of systemic lupus erythematosus
patients
Elderly patients with SLE
(>65 years, n = 18)
Female 15
Male 3
Sex ratio F/M 5
Median age 70 years
Age range 66–78 years
123
Rheumatol Int (2012) 32:1225–1229
Statistical analysis
2 test was performed to compare frequencies of all cate-
gorical variables. P values <0.05 were considered signiW-
cant and all calculated P values are two tailed.
Results
Eighteen case records were analyzed. The patients origi-
nated all from the center of Tunisia. They comprised 15
females and 3 males (sex ratio F/M = 5). Seven SLE
patients were between the age of 66–68 years. Furthermore,
all patients between the ages 73–78 years are females
(Fig. 1). The frequency of SLE in the elderly was 5.3%
(18/342).
The most frequent clinical manifestations in our elderly
patients were arthralgia (55.5%), arthritis (38.9%), and
malar rash (33.3%). Three out of 18 SLE patients (16.7%)
had pericarditis and oral ulcer. The photosensitivity was
detected in 11% (2/18) of cases (Table 2). Fifteen patients
had anemia (83.3%). The frequency of thrombocytopenia
and lymphopenia, in our elderly patients, was 27.8 and
11%, respectively. Only 5 out of 18 SLE patients present
proteinuria (27.8%). Renal biopsy has not been done in the
Wve patients with proteinuria.
All patients had ANA (100%). The anti-dsDNA antibod-
ies were the most common auto-antibody detected. These
antibodies were present in 12 patients (66.7%), and fol-
lowed by the anti-nucleosome antibodies (50%). The anti-
SSA and the anti-RNP were found in 27.8%. The anti-Sm
was found in 22% and the anti-SSB in 11% (Table 3).
The frequencies of major clinical and serological mani-
festations of our patients, compared to other populations,
are represented in Table 4.
Fig. 1 Number of elderly SLE patients according to the sex and age
Rheumatol Int (2012) 32:1225–1229 1227

Table 2 Clinical manifestations of systemic lupus erythematosus was 12 in our previous study in general lupus population
patients [13]. Borteli et al. [4] and Formiga et al. [6] found the
Elderly patients with SLE (n = 18) same result in SLE patients with disease onset after 50 years of
n (%) age. Nevertheless, in other studies, the sex ratio was
between 1.1 and 2.8 for patients older than 65 years
Malar rash 6 (33.3%) [8–10].
Photosensitivity 2 (11%) Regarding to the clinical manifestations, anemia was the
Discoid rash 1 (5.5%) most common sign with a rate of 83.3% which is well
Oral ulcer 3 (16.7%) above the rates recorded in other series. This diVerence
Arthralgia 10 (55.5%) could be explained, partly, by the fact that the results of
Arthritis 7 (38.9%) other series (10.5, 6, and 14.3%) [8–10] incorporates only
Pleurisy 1 (5.5%) hemolytic anemia while our results include all types of ane-
Pericarditis 3 (16.7%) mia observed in the SLE, whether hemolytic or inXamma-
Proteinuria 5 (27.8%) tory. Secondly, anemia aVects over 10% of the Tunisian
Pulmonary involvement 3 (16.7%) population over 49 years, which is linked to socio-eco-
Neuropsychiatric 5 (27.8%) nomic and nutritional habits.
SLEDAIa 6.7 In our study, the arthritis was found in 38.9% of patients.
a
SLEDAI Systemic lupus erytematosus disease activity index
Gaujard et al. [9] found of frequency of 47% for arthritis.
The malar rash, found in 33.3% of cases, was more com-
mon than in series of Goujard et al. and Carmen et al. (18
and 28%, respectively) [7, 9], but it was lower than that in
Table 3 Laboratory data of systemic lupus erythematosus patients the series of Chen et al. (42.1%) [8]. This Xuctuation may
Elderly patients with SLE (n = 18) be due to the higher levels of sunshine in Tunisia and China
n (%) compared to Europe.
Renal involvement was infrequent in our series with a
Hematologic disorders rate of 16.7%. This result was lower than those found in
Anemia 15 (83.3) other series on SLE in the elderly [8–10] (Table 4). In
Thrombocytopenia 5 (27.8) series of SLE patients including all ages, the rate of renal
Lymphopenia 2 (11) disease was 39 and 59% [13, 16]. The neuropsychiatric
Antibodies impairment was not encountered in our series. This could
Anti-nuclear antibodies 18 (100) be due to the diYculties in distinguishing causal links
Anti-dsDNA antibodies 12 (66.7) between neurological and psychiatric symptoms and lupus
Anti-nucleosome antibodies 9 (50) disease in this age. Besides, it has been reported that con-
Anti-SSA antibodies 5 (27.8) vulsions and psychosis were less frequent in patients with
Anti-RNP antibodies 5 (27.8) late-onset SLE [4, 8].
Anti-Sm antibodies 4 (22) The anti-dsDNA antibodies were positive in 66.7% of
Anti-SSB antibodies 2 (11) our patients. This result was consistent with data from the
previous studies. In fact, Chen et al. [8] and Pu et al. [10]
found a frequency of 63.2 and 52%, respectively. However,
these antibodies were detected in 82% of cases in the stud-
ies of Gaujard et al. [9]. The anti-nucleosome antibodies
Discussion were detected in 50% of our sera. Recently, it was proposed
that the nucleosome is the main auto-antigen in the patho-
In this study, we analyzed the clinical and laboratory data physiology of SLE, and that anti-nucleosome antibodies
of 18 patients aged over 65 years from a series of 342 were associated with organic damage. In fact, anti-nucleo-
patients with SLE diagnosed between 1994 and 2009 in some antibodies showed the highest correlation with dis-
four hospitals in the center of Tunisia. The percentage of ease activity, especially in patients negative for anti-
elderly in the lupus population was 5.3%. This frequency dsDNA antibodies. They also showed strong association
was similar to that found by Pu et al. [10], Cervera et al. with renal damage [17–19].
[14] and Dubois et al. [15]. About the anti-SSA and anti-RNP, their rates were
Female predominance appeared less marked in the 27.8%. In the previous studies, their rates were between 11
patients with older onset lupus than in younger group. In and 60%. Anti-Sm antibodies were present in 22% of our
fact, the sex ratio F/M was 5 in our current series; however, it cases and they varied between 6 and 24% in other studies

123
1228 Rheumatol Int (2012) 32:1225–1229

Table 4 Frequencies of clinical

Chen et al. [8] Gaujard et al. [9] Pu SJ et al. [10] Our series
and laboratory features of SLE
patients among diVerent Patients number 19 17 21 18
ethnicities Sex ratio F/M 14/5 = 2.8 11/6 = 1.83 11/10 = 1.1 15/3 = 5

Most frequent manifestations

Arthritis 47.4% 35–47% 42.9 38.9%
Malar rash 42.1% 12–18% 19 33.3%
Nephritis 42.1% – 52.4 –
Mortality 31.6% – – –
Neuropsychiatric 15.8% 18% 4.8 27.8%
Photosensitivity 5.3% 6–18% 14.3 11%
SGS 5.3% 12–18% – 27.8%
Proteinuria – 41% – 27.8%
Oral ulcer 26.3% – 28.6 16.7%
Hematologic disorders 84.2% – 66.7 –
Anemia 10.5% 6% 14.3 83.3%
Lymphopenia 78.9% 82% 52.4 11%
Thrombocytopenia 26.3% 24% 33.3 27.8%
Serological manifestations
ANA 100% 100% 95.2 100%
Anti-dsDNA 63.2% 82% 52.4 66.7%
Anti-nucleosome – – – 50%
Anti-SSA 42.9% 38% – 27.8%
Anti-RNP 11.1% 13% – 27.8%
Anti-Sm 10.5% 6% – 22%
Anti-SSB 28.6% 13% – 11%

[7–9]. The use of various methods to measure these anti-
bodies, the small sample size of series, the diVerent genetic
background and the ethnic origin may explain these dis-
crepancies.
For the SLEDAI, a validated model of experienced clini-
cians’ global assessments of disease activity in lupus, it has
been reported that it was lower in elderly patients with SLE
[6, 8, 12].
In conclusion, our retrospective study showed that SLE
in elderly exhibit distinct clinical and biological manifesta-
tions from the classic form. Thus, greater attention should
be given for this particular subgroup of SLE patients to
avoid delays in diagnosis or misdiagnosis. So, prospective
studies involving a larger number of elderly patients with
SLE are needed.
Acknowledgments This study is supported by unité de recherche
Auto-Immunité et allergie (03/UR/07-02), Faculté de Pharmacie de
Monastir, Tunisie.
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