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Erschienen in: Pediatric Rheumatology 1/2011

Open Access 01.12.2011 | Research

Clinical presentations and outcomes of Filipino juvenile systemic lupus erythematosus

verfasst von: Carien B Gulay, Leonila F Dans

Erschienen in: Pediatric Rheumatology | Ausgabe 1/2011

Abstract

Objective

Juvenile Systemic Lupus Erythematosus (SLE) varies by location and ethnicity. This study describes the clinical, laboratory profile and outcome of juvenile SLE seen at Philippine General Hospital (PGH) from 2004-2008.

Method

Medical charts of all Filipino Juvenile SLE cases admitted at PGH during the 5-year period were reviewed collecting demographic profile, clinical and laboratory manifestations and treatment during disease course.

Results

Seventy-eight cases of juvenile SLE were reviewed. There were 7 boys and 71 girls. The mean age at diagnosis was 14 years (SD 2.7) with a range of 8-18 years. Fever (52.5%) and malar rash (41.0%) were the most common features at disease onset. At the time of diagnosis, the most common features were malar rash (65.3%), renal involvement (62.8%) and photosensitivity (55.1%). Mucocutaneous (92.3%), renal (71.7%) and hematologic (69.2%) involvement were the most common features during the entire course of illness. Infection (34.5%) and neurologic (19.0%) complications were observed most frequently. Corticocosteroid treatment was given in most of the patients in the form of prednisone (97.4%) and concomitant methylprednisolone intravenous pulses (29.4%). Nine patients died during the study period. The overall 5-year mortality rate was 11.5%. Infection (77.0%) was the most frequent cause of death.

Conclusion

Malar rash was a common feature at disease onset and at diagnosis among Filipinos with juvenile SLE. Throughout the disease course, renal involvement occurs in 71.7% of patients. Infection was the leading cause of complication and death. The clinical presentations of Filipinos with juvenile SLE were similar to juvenile SLE in other countries.
Hinweise

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

CG and LD - substantial contribution to conception and design. Each of them participated sufficiently in preparation of this Manuscript. All authors read and approved the final manuscript.

Introduction

Systemic Lupus Erythematosus (SLE) is an autoimmune disease characterized by widespread inflammation of blood vessels and connective tissues and by the presence of antinuclear antibodies (ANAs), especially antibodies to native double stranded DNA (Anti dsDNA). Its clinical manifestation is variable and its natural history is unpredictable. Incidence of juvenile SLE varies by location and ethnicity. There is a wide range of variation in the natural history of SLE among different ethnic and geographical groups. Studies in juvenile SLE have estimated the incidence at 0.28 to 0.9/100,000 per year [13]. A previous study done by Brunner et al in 2008 among Caucasians suggests that patients with childhood-onset SLE have more active disease upon presentation and over time than adults. Children received more intensive drug therapy and accrue more damage [4]. Two significant factors with poor prognosis are female gender and development of end-stage renal disease (ESRD) [5]. Organ damage was significantly more likely to occur in patients who experienced neuropsychiatric manifestations upon diagnosis, had longer disease duration, and had received more intravenous pulses of cyclophosphamide [6]. Recurrent major infections significantly correlate with poorer long-term organ damage [7].
The actual prevalence of juvenile SLE among Filipinos is still unknown. With the review of the clinical manifestations of SLE cases and increased awareness of this condition in pediatric patients, this study hopes to be of value in ensuring early recognition and early institution of appropriate management of this often missed and mismanaged condition. We chose to review cases at the Philippine General Hospital (PGH), a tertiary government hospital located in Manila Philippines. It is the Filipino people's national university hospital and premier referral center. It caters more for low-income patients and it is the only institution in the country with a Pediatric Rheumatology training program.
This retrospective study aims to describe the clinical, laboratory profile and outcome of juvenile SLE seen at the PGH during a 5-year period from January 2004 to December 2008.

Methodology

Patients diagnosed with juvenile SLE (met > 4 criteria of the 1997 revised American College of Rheumatology [ACR] classification criteria for SLE); age at onset <18 years according to the Paediatric Rheumatology International Trials Organization (PRINTO) [8] were included in the study. Patients were identified from the Out-patient and In-patient (wards and emergency room) service of General Pediatrics, Pediatric Rheumatology and Pediatric Nephrology sections of PGH. The institutional review board approved the study.
Medical charts were retrieved from the records section of PGH by the primary investigator (CG). These were reviewed from the date of the initial consult up to the last date of follow up. A data collection form was used to collect information on demographic profile, presenting features, clinical and laboratory manifestations and treatment during the course of the disease for each patient.
Clinical presentation at onset of disease was defined as the manifestations at the first 3 months of illness. The time of diagnosis was defined as the time when the patient fulfilled at least four ACR 1997 revised classification criteria for SLE.
Records of clinical and laboratory findings during the study period were collected as follows: Hemolytic anemia with reticulocytosis, leucocytopenia (< 4000 cells/mm3) and lymphopenia [absolute lymphocytic count (ALC) <1,500 cells/mm3 ] present in 2 or more occasions, thrombocytopenia (< 100,000 cells/mm3) in the absence of offending drugs, abnormal urinalysis (proteinuria 0.5 g/24 h or >3+ if quantitative evaluation was not done, and/or casts, hematuria >5 RBCs/HPF or pyuria >5 WBCs/HPF in the absence of infection), increased creatinine (> 1 mg/dl), low C3, increased erythrocyte sedimentation rate (ESR) (> 20 mm/hr). Pleuritis documented by history of pleuritic pain or rub heard by physician or evidence of pleural effusion and pericarditis documented by ECG, rub, or evidence of pericardial effusion. Growth failure is defined as the presence of at least 2 of the following 3 features: 1) height below the third percentile for age; 2) growth velocity over 6 months below the third percentile for age; 3) crossing at least 2 percentiles (5%,10%, 25%, 50%, 75%, 95%) on National Center for Health Statistics growth charts. Delayed puberty is defined as a delay in development of secondary sexual characteristics more than 2 SD below the mean for age by Tanner staging. Complications and causes of death were analyzed. Descriptive statistics which include mean, median, range and frequency were computed.

Results

Of the 84 children diagnosed with juvenile SLE seen in our institution, 78 of them (93.0%) had available medical records for review. The female to male ratio was 10:1 (71 girls, 7 boys). The overall mean age at diagnosis was 14.0 years (SD 2.7) (boys 13.7 years, girls 14.0 years), with a range of 8-18 years. The peak age group on diagnosis is 11 year old for male and 17 year old for female patients. Eight (10.2%) of our Filipino juvenile SLE patients are known to have history of SLE in the family. Six of them were first-degree relatives.

Clinical and Laboratory Features

Fever (52.5%), malar rash (41.0%), oral/nasopharyngeal ulcers (29.4%), alopecia and general fatigue (28.2%) were the most common features at disease onset (see Table 1).
Table 1
Presenting features at Disease Onset among 78 juvenile SLE patients
Manifestation
No.
%
Mucocutaneous
  
   Malar rash
32
41.0
   Oral/nasopharyngeal ulcers
23
29.4
   Alopecia
22
28.2
   Photosensitivity
19
24.0
   Punctate erythema
7
8.9
   Discoid rash
5
6.4
   Epistaxis
5
6.4
   Gumbleeding
2
2.5
Musculoskeletal
  
   Arthralgia
21
26.9
   Arthritis
14
17.9
Haematologic
  
   Pallor
16
20.5
Neuropsychiatric
  
   Seizures
3
3.8
   Psychiatric symptoms
2
2.5
Renal
  
   Gross hematuria
9
11.5
Gastrointestinal
  
   Abdominal pain
7
8.9
   Vomiting
7
8.9
Constitutional
  
   Fever
41
52.5
   General fatigue
22
28.2
   Weight loss
14
17.9
   Loss of appetite
7
8.9
At the time of diagnosis, the most common features were malar rash (65.3%), renal involvement (62.8%) and photosensitivity (55.1%) (see Table 2). Cardiovascular involvement was found in 17.0% of patients, pericardial effusion was noted in 15.3% and valvular anomaly 10.2%. They presented with tricuspid regurgitation (5), pulmonary regurgitation (2), mitral regurgitation (2) and moderate aortic regurgitation (1). Hematologic manifestations were as follows: 58.0% had anemia (hemoglobin range: 3.6-11.8; median: 9.35; mean 8.86 SD 2.02 g/dl), 8.9% with positive Coombs test, 15.3% with leukocytopenia (range: 2,950-3,900; median 3,800 cell/mm3), 21.7% with lymphocytopenia (ALC range: 325-1,431; median 1,034 cells/mm3), 14.1% with thrombocytopenia (platelet count range: 27,000-90,000; median 56,000 cells/mm3).
Table 2
Clinical and Laboratory Features among 78 juvenile SLE patients
Category
At the time of diagnosis
during the disease course
 
No.
%
No.
%
Mucocutaneous
Manifestations
71
91.0
72
92.3
   Malar rash
51
65.3
60
76.9
   Discoid rash
25
32.0
28
35.8
   Photosensitivity
43
55.1
57
73.0
   Oral ulcers
42
53.8
53
67.9
   Alopecia
31
39.7
41
52.5
Musculoskeletal
Involvement
32
41.0
42
53.8
   Arthritis
17
21.7
31
39.7
   Arthralgia
24
30.7
40
51.2
Pulmonary Involvement
11
14.1
17
21.7
   Pleuritis/Pleural effusion
11
14.1
16
20.5
Cardiac Involvement
13
16.6
17
21.7
Pericarditis/Pericardial
Effusion
12
15.3
14
20.5
Valvular anomaly on
Echocardiography
8
10.2
8
10.2
Ventricular/atrial
Hypertrophy
4
5.1
5
6.4
Renal involvement
49
62.8
56
71.7
   Hematuria
19
24.3
26
33.3
   Proteinuria
32
41.0
20
25.6
CNS involvement
24
30.7
25
32.0
   Seizure
12
15.3
15
19.2
   Behavioral changes
9
11.5
10
12.8
Hematologic
Involvement
37
47.4
54
69.2
Laboratory
    
   Cellular casts
11
14.1
22
28.2
   Increased creatinine
6
7.6
11
14.1
   Hemolytic anemia
7
8.9
8
10.2
   Leukocytopenia
12
15.3
25
32.0
   Lymphocytopenia
17
21.7
32
41.0
   Thrombocytopenia
11
14.1
20
25.6
   Low C3
7
8.9
7
8.9
Mucocutaneous (92.3%), renal (71.7%) and hematologic (69.2%) involvement were the most common features during the entire course of illness(see Table 2).
ANA was positive in 98.5% (n = 70/71) of our patients, mostly done using Indirect Immunofluorescence (IIF) technique using HEp-2 cells (70.0%). LE cell could be demonstrated in 25.6% of patients. Anti-dsDNA antibodies were detected by IIF on Crithidiae luciliae. It was done in only 21 patients and titers were significantly high among 18 of them.
The frequency of complications in our juvenile SLE patients is shown in Table 3. Infection (34.5%) followed by neurologic (19.0%) and musculoskeletal (8.7%) were observed most frequently.
Table 3
Complications among 78 juvenile SLE patients
Item
N
%
Infection
27
34.5
   Pneumonia
11
14.1
   Sepsis
8
10.2
   Tuberculosis (pulmonary, endotracheal, miliary)
6
7.7
   Cellulitis
2
2.5
Neurologic
15
19.0
   Seizure requiring therapy for 6 months
12
15.3
   Cerebral atrophy by imaging (Cranial CT scan)
2
2.5
   Lateral rectus palsy
1
1.2
Musculoskeletal
5
8.7
   Deforming or erosive arthritis
3
3.8
   Osteoporosis with fracture or vertebral collapse
2
2.5
   Osteomyelitis
1
1.2
   Muscle atrophy or weakness
1
1.2
Skin
4
5.0
   Scarring chronic alopecia
2
2.5
   Extensive scarring or panniculum other than scalp and pulp space
2
2.5
Gastrointestinal
2
2.0
   Autoimmune hepatitis by biopsy
2
2.0
Renal
2
2.5
   Estimated or measured glomerular filtration rate < 50%
2
2.5
Growth failure
4
5.1
Pubertal delay
2
2.5
Ocular
1
1.2
   Ischemic retinopathy
1
1.2
Pulmonary
1
1.2
   Pulmonary hypertension
1
1.2
Throughout the study period, 71.7% (56/78) of patients had renal involvement. Renal biopsy was done only among 24 of these patients. Evaluation was based on WHO classification for lupus nephritis. One was found to be of mixed type and was then classified under the dominant class. Renal histology showed class II nephritis in 25.0%, class III in 20.8%, class IV in 50.0% and class V in 4.1%.

Therapy

Corticosteroid treatment was given in most of the patients in the form of prednisone (97.4%) and Methylprednisolone IV pulses (29.4%). Hydroxychloroquine was used in 32.0%, Azathioprine in 23.0%, Cyclophosphamide intravenous pulses in 26.9%.

Clinical Outcomes

The follow-up period ranged from 0.1-6.4 years with a mean duration of 1.7 years (SD 1.8). About 34.6% of the Filipino juvenile SLE patients seen our institution are still attending our clinics, 21.7% were endorsed to adult rheumatology clinic, 6.4% transferred to other institution while 25.6% were lost to follow-up.
Nine patients died during the five-year study period. The causes of death were (1) active lupus (acute renal failure), (1) severe pulmonary hypertension and (7) infection. Identified pathogens on blood culture were Pseudomonas aeroginosa, Methicillin-resistant Staphylococcus epidermidis, Burkholderia mallei and Klebsiella pneumoniae. One had concomitant staphylococcal pneumonia and the other with osteomyelitis secondary to Salmonella sp (documented by synovial fluid culture).

Discussion

We compared the manifestations at diagnosis as well as the cumulative features of our juvenile SLE patients with the local data as well as from other countries (see Table 4 and 5). Available literatures with hospital-based data on juvenile SLE were included.
Table 4
Clinical And Laboratory Variables Of Children With SLE At Diagnosis Compared To Other Countries
 
Present Study
Wang, 20035
Balkaran, 200410
Bakr, 200511
Salah, 20099
Hamijoyo, 200912
No.of
Patients
78
153
33
52
207
147
Country
Philippines
Taiwan
Trinidad
Egypt
Egypt
Philippines
Follow-up, y
      
Mean
Range
1.7 ± 1.8
[0.1-6.4]
6.1 ± 9.0
 
1 ± 9.3
  
Age at diagnosis, y
Mean+SD
Range
14 ± 2.7
8 - 18
13.5 ± 5.5
5-17
11.9 ± 2.6
6-16
10 ± 2.7
2 - 16
12.29 ± 2.9
4 - 16
F:M ratio
10:1
5.9:1
6.6:1
12:1
2.69:1
11.2:1
Rash
      
   Malar
65.3
77.1
39
46.2
 
74.8
   Discoid
32.0
2.0
37
  
19.0
Photosensitivity
55.1
24.8
 
21,2
 
57.8
Oral ulcers
53.8
26.1
 
19.6
 
49.7
Alopecia
39.7
13.1
 
34.6
45.5
51.7
Musculoskeletal
53.8
 
69.7
65.4
  
   Arthritis
21.7
57.5
  
46.9
61.9
Neuropsychiatric
30.7
4.6
 
7.7
7.2
8.2
Serositis
26.9
15
   
14.3
Pleural
Effusion
14.1
   
6.3
 
Pericardial
Effusion
15.3
  
7.7
  
Nephritis
62.8
58.8
63.6
80.8
20.8
48.3
Hematologic
51.2
79.7
   
38.8
   Thrombocytopenia
14.1
19.6
 
29.2
  
Hemolytic
Anemia
8.9
44.4
  
17.0
 
   Leukocytopenia
15.3
34.6
 
27.5
  
Table 5
Cumulative Features Of Children With SLE Compared To Other Countries
Cumulative
Features
Present Study n = 78 (%)
Agcaoili
198613
n = 31(%)
Bahabri, 1997
n = 6014 (%)
Gedalia, 199915
n = 61 (%)
Pattaragarn, 200516
n = 82 (%)
Hiraki, 200817
n = 256 (%)
Salah, 20099
n = 207 (%)
Hoffman200918
n = 56(%)
Country
Philippines
Philippines
Saudi Arabia
African-America
Latin America
Thailand
Canada
Egypt
Europe
Rash
75.6
  
84
81
    
   Malar
71.7
90.3
40
69
52
53.5
66
38.2
69.6
   Discoid
35.8
  
21
9
2
 
10.1
13.2
Photosensitivity
73
 
15
20
56
21.8
 
44
44.6
Oral ulcers
67.9
45.1
16
  
31.7
 
22.2
28.6
Musculoskeletal
Involvement
53.8
 
91.6
  
31.7
 
39.6
 
   Arthritis
39.7
74.1
 
79
75
 
67
 
59.3
Neuropsychiatric
32
32.2 psych
25.8 sz
27
31
40
20.8
27
24.2
 
Hematologic involvement
69.2
 
66.6
  
73.4
   
Hemolytic
anemia
10.2
  
18
12
  
19.3
38.5
Thromobocyto
penia
25.6
6.4
 
26
22
13.9
 
21.7
31.5
   Leukocytopenia
32
12.9
 
46
55
  
26
63.6
Serositis
26.9
        
   Carditis
17.9
32.26
 
28
16
   
16.7
   Pleuritis
20.5
25.81
 
36
24
    
Renal
Involvement
71.7
 
65
44
55
86.2
55
67
62.5
In our series, mean age at diagnosis was at 14.0 (SD 2.7) years old which is comparable to other studies (see Table 5). We reported 8 yr old as the youngest age at initial SLE diagnosis. This is relatively old compared to other series with reported youngest age at 2 to 7 years old [912]. Female preponderance, similar from reports of other countries, emphasizes the importance of hormonal factors in the clinical expression of the disease.
All local studies showed malar rash as the most common clinical feature at the time of diagnosis as well as during the entire course of illness [12, 13]. Our patients had fewer reports of arthritis but a significantly higher neuropsychiatric manifestations compared to the other local study done by Hamijoyo[12, 13] as well as with that of Taiwan [5] and Egypt [9]. The frequency of renal involvement in our study (62.8%) was comparable to the studies from Taiwan (58.8%) [5] and Trinidad (63.6%)[10]. Among the clinical features found throughout the entire clinical course, the cumulative frequency of hematologic (69.2%) and neuropsyschiatric (32%) involvement in our series is comparable to other studies [9, 1316]. However, arthritis still remained low throughout the course of illness in our patient population compared to other studies [13, 14, 16, 17]. The cumulative frequency of renal involvement in our series (71.7%) is comparable to studies involving Arab (65%) [14] and Egyptian (67%) [5] children but more common than in Canadian (55.0%) [17], European (62.5%) [18], African-American (44.0%) [15] and Latin American children (55%) [15]. Wide variations among different studies may be attributed to genetic differences or to referral bias, as some studies came from nephrology units and others from rheumatology units.
Most of our patients with lupus nephritis had pathological changes consistent with Class III and IV lupus nephritis (WHO classification). Report of nephritis was highest in Thailand (86.2%)[16] and lowest in African-American children(44%)[15]. These diverse presentations, disease course and outcome appear to be multifactorial. Environmental, socioeconomic, demographic, psychosocial, genetic (HLA-DRBl*0301, HLA-DRB1, FCGR gene family, IRF5, STAT4 and MECP2) [19], and clinical factors play an important role as determinants of the ethnic differences [20]. Further investigation is needed to elucidate the basis of these disparities.
One of the limitations of this study was that not all patients were able to have the complete antibody profile and kidney biopsy. This was primarily due to financial reasons as majority of our patients came from low income families.
Of the 9 patients who died the most common cause was infection (77%). The identified pathogens included were mostly gram negative bacteria. Nosocomial infection was the predominant type. This was similar in most studies on juvenile SLE, as infection has replaced renal failure as the leading cause of mortality among these patients [5, 2123]. Use of immunosuppressive therapy and inherent immune abnormalities in active lupus predisposes these children to infection. However, a major contributory factor which probably caused such high mortality in our institution could be that most of our patients belong to the low income families contributing to poor treatment compliance and adherence and poor follow-up. Another potential factor could be that our patients might have more severe disease spectrum since we are the biggest government institution with a referral center for children with rheumatologic diseases. Faced with such obstacles, a stronger awareness and recognition of this condition by other health professionals hopefully would assure early referral to the pediatric rheumatologist and other appropriate subspecialists. Emphasis in programs for health promotions among chronically ill patients and access support group for Filipino children suffering from lupus should also be advocated.

Conclusion

Malar rash was a common feature at disease onset and at diagnosis among Filipinos with juvenile SLE. Throughout the disease course, renal involvement occurs in 71.7% of patients. Infection was the leading cause of complication and death. The clinical presentations of Filipinos with juvenile SLE were similar to juvenile SLE in other countries.
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

CG and LD - substantial contribution to conception and design. Each of them participated sufficiently in preparation of this Manuscript. All authors read and approved the final manuscript.
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Metadaten
Titel
Clinical presentations and outcomes of Filipino juvenile systemic lupus erythematosus
verfasst von
Carien B Gulay
Leonila F Dans
Publikationsdatum
01.12.2011
Verlag
BioMed Central
Erschienen in
Pediatric Rheumatology / Ausgabe 1/2011
Elektronische ISSN: 1546-0096
DOI
https://doi.org/10.1186/1546-0096-9-7

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