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Saudi Journal of Kidney Diseases and Transplantation
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RENAL DATA FROM THE ARAB WORLD Table of Contents   
Year : 2008  |  Volume : 19  |  Issue : 6  |  Page : 1001-1008
Clinical and immunological manifestations of systemic lupus erythematosus: A study on 146 south Tunisian patients


1 Department of Internal Medicine, Hedi Chaker University Hospital, Sfax, Tunisia
2 Department of Nephrology, Hedi Chaker University Hospital, Sfax, Tunisia

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   Abstract 

The objective of this study was to determine the main clinical and laboratory features as well as the morbidity and mortality of systemic lupus erythematosus (SLE) in a population of patients predominantly from the south of Tunisia. A retrospective review of a well documented population of 146 patients with SLE was undertaken. All patients fulfilled four or more criteria defined by the American College of Rheumatology. The mean age at presentation was 29.2 years (range 6-55) and the mean duration of follow-up was 62 months (range 0.25-374). Musculoskeletal (84.2%) and mucocutaneous (75.3%) were the most frequent clinical mani­festations. Antinuclear antibodies were detected in 97.3%, anti-DNA antibodies in 69.2% and anti-Sm in 39.2% of the patients. Anti-cardiolipin antibodies and lupus anticoagulant were ob­served respectively in 71.6% and 37.8% of the patients. The five-year survival rate in our series was 92%. Renal involvement and thrombocytopenia were associated with poor prognosis (p< 0.05). The clinical and immunological characteristics of our SLE patients are largely comparable to most major studies. Main differences included prominent major organ damage and high pre­valence of anti-Sm and anti-cardiolipin antibodies.

Keywords: Systemic lupus erythematosus, Arab, African, Tunisia, Prognosis

How to cite this article:
Jallouli M, Frigui M, Hmida MB, Marzouk S, Kaddour N, Bahloul Z. Clinical and immunological manifestations of systemic lupus erythematosus: A study on 146 south Tunisian patients. Saudi J Kidney Dis Transpl 2008;19:1001-8

How to cite this URL:
Jallouli M, Frigui M, Hmida MB, Marzouk S, Kaddour N, Bahloul Z. Clinical and immunological manifestations of systemic lupus erythematosus: A study on 146 south Tunisian patients. Saudi J Kidney Dis Transpl [serial online] 2008 [cited 2019 May 23];19:1001-8. Available from: http://www.sjkdt.org/text.asp?2008/19/6/1001/43484

   Introduction Top


Systemic lupus erythematosus (SLE) is a multi­system autoimmune disease of unknown etio­logy characterized by the production of non­organ-specific autoantibodies directed to nuc­lear, cytoplasmic and cell surface antigens, which may lead to a wide range of tissue in­juries. The prevalence of clinical and immuno­logic manifestations varies significantly among different ethnic and geographical groups. Des­pite a large number of published reports, clini­cal and laboratory features are still an interes­ting matter of study, as there are important discrepancies. Few studies have been conducted on North Africans and Tunisians, in particular. In the current report; we present the main epidemiological, clinical and immunological features in a population essentially from the south of Tunisia. In addition, this investigation was meant to study the predictors of renal and neuropsychiatric involvement and to determine the impact of demographic factors, clinical manifestations, disease activity and serologic tests on survival.


   Patients and Methods Top


The patients included in this study were those attending the Department of Internal Medicine at the Hedi Chaker University Hospital, Sfax, Tunisia, from January 1996 to June 2006. All patients fulfilled four or more criteria for the diagnosis of SLE as defined by the American College of Rheumatology. Conventionally, the patients were seen at four monthly intervals. At each visit, the patient's history was re­viewed in addition to physical examination and routine laboratory tests.

The following data were collected: age, gender, age at onset of disease (defined as age at which the patient developed initial mani­festation(s) attributable to SLE) and age at diagnosis of SLE. The main clinical mani­festations were defined as described by the American Rheumatism Association glossary committee. Kidney biopsy results were docu­mented according to the World Health Orga­nization (WHO) classification system. Anti­nuclear antibodies (ANA) were evaluated by indirect immunofluorescence (IF) technique using either mouse liver or Hep-2 cells. Anti­DNA antibodies were assayed by IF using Crithidia luciliae as substrate and by enzyme linked immunosorbent assay (ELISA) if IF was negative. Anti-nucleosome antibodies and anti-extractible nuclear antigen antibodies (or anti-ENA: anti-Sm, anti-RNP, anti-SSA and anti-SSB) were detected by immunodot. Anti­cardiolipin antibodies were assessed by a stan­dardized ELISA technique. Complement and rheumatoid factor were assessed by nephe­lometry.

A descriptive analysis was performed with the aid of the SPSS program to analyze the frequency of the clinical manifestations, im­munological findings, and requirement of pharmacologic treatment during the course of disease. Qualitative differences between sub­groups were analyzed with the Chi-Square and Fisher Exact Test. The Student t-test was used to evaluate means with equal and unequal variance of the study variables. The signi­ficance level (< 0.05) was used for testing statistical difference of the hypotheses. Multi­variate analyses using logistic regression were performed to rule out possible indirect in­fluences.


   Results Top


A total of 146 patients with SLE were seen at our department during the study period. Of these, 126 (86.3%) were from the south of Tunisia. There were 125 females and 21 males, giving a sex ratio of 1:6. The mean age at presentation was 29.2 years with ages ranging between six and 55 years. Onset of the disease after the age of 50 years was uncommon (4.1%). The mean duration between the onset and the diagnosis of SLE was 16.8 months (range 1 week-18 years). The most prevalent initial manifestations were arthritis or arthral­gia (49.3%), fever (41.8%), cutaneous lesions (33%), hematological disorders (14.4%), sero­sitis (11%) and edema (7.5%). A triggering factor could be identified in 20 cases; it was mainly pregnancy, seen in 13 cases. [Table 1] gives the distribution of the cumulative clinical manifestations of the patients.

Articular manifestations were the most co­mmon clinical features seen in 84.2% of our patients. Arthritis occurred in 54.8% of cases while avascular necrosis was seen in eight patients (5.5%).

Cutaneous manifestations were also frequent (75.3%). Malar rash was seen in 52%, photo­sensitivity in 47.3% and oral ulcerations in 19.2% of the cases. Raynaud's phenomenon was observed in 7.5% of the patients.

Pleural effusion (28.8%) was the most co­mmon pulmonary manifestation. It was asso­ciated with the nephrotic syndrome in 14 cases. Three patients developed pulmonary hypertension. Pulmonary infarction was not observed in any patient.

Forty-one patients (28%) exhibited cardiac involvement at some stage of their illness. It consisted of pericarditis in 38 cases (26%), cardiomyopathy in seven patients (4.8%) and Libman Sacks endocarditis in one patient. Echocardiography was performed on 79 pa­tients (54.1%); it was abnormal in 51.9% of the cases. Venous thromboses were seen in 11 patients (7.5%) and arterial thromboses in five (3.4%).

Renal abnormalities were noted in 59% of our patients. Of these, 48.8% of the patients had microscopic hematuria, 40.7% had raised serum creatinine and 34.9% had the nephrotic syndrome. Renal biopsy specimens, obtained in 82 of the 86 patients with lupus nephritis (95.35%), showed diffuse proliferative glome­rulonephritis (GN) (WHO class IV) in 25 pa­tients, focal and segmental proliferative GN (WHO class III) in 27, moderate mesangial GN (WHO class II) in 18 and membranous GN (WHO class V) in five cases. A total of 31 patients underwent a second kidney biopsy. This procedure was performed in case of per­sistence or aggravation of the renal biological abnormalities despite treatment (73.3%) or in case of appearance of a renal flare up (26.7%).

Comparison of clinical and laboratory fea­tures of SLE patients, with and without renal involvement, showed that lupus nephritis was significantly associated with thrombocytopenia (p= 0.008), decreased C3 level (p = 0.003), arterial hypertension (p = 0.006), pleurisy (0.05) and leukopenia (0.009). In a multivariate ana­lysis, thrombocytopenia, decreased C3 level, hypertension and pleural effusion remained significant factors for the development of active renal disease.

A past or present neurological manifestation was observed in 28 cases (19.2%), mainly in the form of generalized tonic-clonic seizures, noted in 20 patients (13.7 %). Peripheral neu­ropathy occurred in four patients (2.75%). Comparison between patients with and without neurological manifestations showed that oral ulcerations (p = 0.003), pericarditis (p = 0.024), Raynaud's phenomenon (p = 0.037), thrombo­cytopenia (p = 0.003) and/or decreased C3 level (p = 0.017) were more commonly ob­served in patients with neurological manifes­tations. Of these variables, thrombocytopenia, pericarditis and oral ulcerations remained significant multivariate factors. Psychiatric features occurred in 26 patients (17.8%); they occurred before steroid therapy in nine pa­tients. The psychiatric manifestations essen­tially included depression (10 cases), acute confusional state (8 cases) and psychosis (6 cases).

A conventional magnetic resonance imaging scan performed in 30 patients was abnormal in 13 cases (43.3%). Cortical atrophy and small white matter hyperintensities were the most common findings (6 cases each).

Hematological manifestations (87%) were common in our series and included anemia in 78.75%, leukopenia in 47.9 %, lymphopenia in 47.3% and thrombocytopenia in 24.7% of the patients. Lymphadenopathy was observed in 34 patients (23.3%) and splenomegaly in 15 (10.3%).

Laboratory findings are presented in [Table 2]. Positive ANA were present in 97.3% of pa­tients, anti-DNA antibodies in 69.2%, anti-Sm antibodies in 39.2%, anti-cardiolipin antibodies in 71.6% and lupus anticoagulant in 37.8%. Fourteen patients (9.6%) met the diagnostic criteria for antiphospholipid syndrome. Anti­Sm antibodies were significantly associated with Raynaud's phenomenon (p = 0.027) and the presence of anti-RNP antibodies (p < 0.001). The presence of lupus anticoagulant was correlated with thrombocytopenia (p = 0.039).

After the diagnosis of SLE, 24 pregnancies in 15 women were followed-up. Nine women had only one pregnancy, three had two and three others had three pregnancies. The mean dura­tion of the disease before the onset of the first pregnancy was 56 months (range 9-132). Among the 24 pregnancies, 12 (50%) resulted in live births, seven (29.15%) in therapeutic abortion and five (20.8%) in spontaneous abortion.

At some stage of the disease, anti-malarial drugs and steroids were added respectively in 87.8% and 94.5% of our patients. High-dose steroid treatment was administered to 111 patients (76%). In addition, intravenous pulse cyclophosphamide was required in 39 cases (26.7%), the main indication being prolife­rative GN (87.2%). Only one patient received treatment with mycophenolate mofetil.

The mean duration of follow-up was 62 months (range 0.25-374). Complete clinical, biological and immunological remission was obtained in 15 cases (10.2%). Sixty-one pa­tients (41.8%) relapsed in an average time of 30 months. Fatality occurred in 11 cases. Nine patients died within five years after the diag­nosis of SLE was made. The cause of death included florid SLE (4 cases), infections (4 cases), complications of renal biopsy (2 cases) and pulmonary hypertension secondary to an associated systemic scleroderma (1 case). Re­nal involvement (p = 0.02), [nephrotic syn­drome (p = 0.04), raised creatinine (p = 0.02)], thrombocytopenia (p = 0.02) and the presence of anti-cardiolipin antibodies (p = 0.05) were associated with poor prognosis.

Sixty-six patients (45.2%) developed 169 infections during the study period (range 1- 11). The mean interval between the occurrence of infection and the diagnosis of SLE was 29 months (range 0-166 months). Infection in­volved the urinary tract (51 infections), the skin (30 infections) and the lung (17 infec­tions). Severe infections (18%) were observed in 29 patients (20%).


   Discussion Top


Important differences in clinical and immu­nological manifestations of SLE have been reported among various ethnic groups. Two previous studies on SLE in the Tunisian popu­lation have been reported earlier. [1],[12] Our series involved patients predominantly from the south of Tunisia.

As seen in our patients' records, SLE is generally a disease of patients in their third decade. The sex ratio in our series confirms the well-known female predominance in SLE. However, this ratio is different from that reported from Europe (10:1), [13] Japan (11:1) [4] or the United States (10:1). [5] The reason for this discrepancy was not obvious.

The frequency of major clinical and sero­logical manifestations in our patients, in com­parison to those of other populations is shown in [Table 3]. Articular and cutaneous manifes­tations were the most common clinical symp­toms in our patients as well as in the other reported series. Oral ulcers (19.2%) were seen more often when compared with patients in North Tunisia (4%). [1] However, the frequency was similar to that seen in the European, [3] African [6],[7] and Southeast American [5] cohorts (17-24%).

The prevalence of renal involvement in our study (59%) is among the highest reported, particularly when compared to the 39% preva­lence reported from the European population. [3] This frequency is lower than that reported from India (73%), [8] Senegal (74%) [7] or Curacao (78%). [9] Our renal biopsy findings were similar to that seen in studies reported by Cameron (72.5%), [10] Mery (68%) [11] and Le Thi Huong (54%). [12] We found that thrombocytopenia and arterial hypertension were significant predic­tors of the occurrence of lupus nephritis. Similar findings have been reported in the literature. [1],[12],[13],[14],[15] Although several previous stu­dies showed that renal involvement correlated with the presence of anti-DNA anti-bodies, [16],[17] we did not find any such association.

There is a major variation in the reported prevalence of patients with neuropsychiatric syndromes in association with SLE; they range from 18 to 69% in the literature. [18] Our cohort study included 42 patients with neuropsychia­tric manifestations. This was comparable with the populations from Europe (27%), [3] northern Tunisia (25%), [1] Senegal (32%), [7] South Ame­rica (26.35%), [19] Saudi Arabia (25.3%) [20] and India (28%). [21] In our study, the main risk fac­tors for the development of significant neuro­logical manifestations were pericarditis, oral ulcerations and thrombocytopenia. This is con­sistent with the results of Feinglass, [24] who showed a significant association between throm­bocytopenia and neuropsychiatric manifestations.

The main immunologic finding in our pa­tients was the high prevalence of anti-Sm antibodies (39.2%); this is in contrast to 10% prevalence reported among Europeans, [3] 16% among Puerto Ricans [25] and 13% among Southeast Americans. [5] A high prevalence was also observed in north Tunisia (61%), [1] South Africa (44.28%), [6] Martinique (37.1%) [26] and Saudi Arabia (40%). [20] In our series, the presence of anti-Sm antibodies was found more frequently in patients with Raynaud's phenomenon and anti-RNP antibodies. Asso­ciations between anti-Sm antibodies and Ray­naud's phenomenon have been reported pre­viously. [27],[28] On the other hand, the relation between anti-Sm antibodies and anti-RNP anti­bodies was demonstrated by Houman, Tickly and Molina. [1],[6],[29]

The level of anti-cardiolipin antibodies has been reported to be raised in 5-80% of patients with SLE. [1],[30] This large variation in the pre­valence of anti-cardiolipin antibodies can be explained by the difference in the assay kits used. We found anti-cardiolipin antibodies in 71.6% of our patients, probably the highest frequency observed in the literature. In con­trast, the antiphospholipid syndrome was found in only 9.6% versus 21% among Kuwaitis [31] and 32.4% among Afro-Caribbean. [26] Houman [1] and Mc Dounagh [32] have reported similar fre­quencies to those seen in our study, respec­tively 11 and 9%.

The treatment received by our patients co­rrelated well with the severity of their disease and the prevalence of major organ damage and, consequently, to the increased requirement of high dose steroids (76%) and immuno­suppressive drugs (26.7%).

Infections are common in SLE and affected 45.2% of our study patients. Most infections were mild (82%) involving principally the urinary tract and skin. Similar findings were observed in the literature. [33]

The survival of patients with SLE has clearly improved during the last four decades. Reports range from less than 50% survival in 1955 to more than 93% in the 1990's. Eleven patients (7.5%) died during follow-up in the present study. The five-year survival rate is 92% which is lower than that found in the European report (95%) but higher than that found in the north Tunisian report (86%). A bimodal distri­bution for SLE mortality was first described in 1976 by Urowitz et al. [34] Early deaths are largely due to active disease, while late deaths are associated with vascular events, infections and other complications not directly associated with lupus activity. In our series, active disease and infections were the two major causes of death and no patient died of cardiovascular complications or malignancies. These findings are comparable to those seen in northern Tuni­sians, [1] Chinese [41] and South Koreans. [35] Consis­tent with others studies, our data confirm an important increased risk of mortality among patients with renal involvement, [1],[36],[37],[38] thrombo­cytopenia [39],[40] and anti-cardiolipin antibodies. [1],[36]


   Conclusions Top


The clinical and immunological characteris­tics of our patients with SLE are largely com­parable to other study populations. In addition, the immunologic profile in our series is cha­racterized by the high prevalence of anti-Sm and anti-cardiolipin antibodies. Our data sug­gest that South Tunisian patients have more major organ damage such as renal and neuro­psychiatric disease.

 
   References Top

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Correspondence Address:
Moez Jallouli
Department of Internal Medicine, Hedi Chaker University Hospital, Sfax
Tunisia
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    Tables

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