
Lupus (2017) 26, 996–1001

journals.sagepub.com/home/lup

CONCISE REPORT

Outcomes of 847 childhood-onset systemic lupus erythematosus

patients in three age groups

SRM Lopes1, NWS Gormezano1, RC Gomes2, NE Aikawa1,2, RMR Pereira1, MT Terreri3, CS Magalhães4,
JC Ferreira2, EM Okuda5, AP Sakamoto3, AME Sallum2, S Appenzeller6, VPL Ferriani7, CM Barbosa8, S Lotufo9,
AA Jesus2, LEC Andrade3, LMA Campos2, E Bonfá1,*, CA Silva1,2,* and Brazilian Childhood-onset Systemic Lupus

Erythematosus Group**
1Division of Rheumatology, Faculdade de Medicina da Universidade de São Paulo, Brazil; 2Pediatric Rheumatology Unit, Children’s Institute,

Faculdade de Medicina da Universidade de São Paulo, Brazil; 3Pediatric Rheumatology Unit, Universidade Federal de São Paulo, Brazil;
4Pediatric Rheumatology Division, São Paulo State University (UNESP) – Faculdade de Medicina de Botucatu, Brazil; 5Pediatric Rheumatology
Unit, Irmandade da Santa Casa de Misericórdia de São Paulo, Brazil; 6Pediatric Rheumatology Unit, State University of Campinas (UNICAMP),
Brazil; 7Pediatric Rheumatology Unit, Ribeirão Preto Medical School – University of São Paulo, Brazil; 8Pediatric Rheumatology Unit, Hospital

Infantil Darcy Vargas, Brazil; and 9Pediatric Rheumatology Unit, Hospital Menino Jesus, Brazil

Objective: The objective of this study was to assess outcomes of childhood systemic lupus
erythematosus (cSLE) in three different age groups evaluated at last visit: group A early-onset
disease (<6 years), group B school age (�6 and <12 years) and group C adolescent (�12 and
<18 years). Methods: An observational cohort study was performed in ten pediatric rheuma-
tology centers, including 847 cSLE patients. Results: Group A had 39 (4%), B 395 (47%) and
C 413 (49%). Median disease duration was significantly higher in group A compared to
groups B and C (8.3 (0.1–23.4) vs 6.2 (0–17) vs 3.3 (0–14.6) years, p< 0.0001). The median
Systemic Lupus International Collaborating Clinics/American College of Rheumatology
Damage Index (SLICC/ACR-DI) (0 (0–9) vs 0 (0–6) vs 0 (0–7), p¼ 0.065) was comparable
in the three groups. Further analysis of organ/system damage revealed that frequencies of
neuropsychiatric (21% vs 10% vs 7%, p¼ 0.007), skin (10% vs 1% vs 3%, p¼ 0.002) and
peripheral vascular involvements (5% vs 3% vs 0.3%, p¼ 0.008) were more often observed in
group A compared to groups B and C. Frequencies of severe cumulative lupus manifestations
such as nephritis, thrombocytopenia, and autoimmune hemolytic anemia were similar in all
groups (p> 0.05). Mortality rate was significantly higher in group A compared to groups B
and C (15% vs 10% vs 6%, p¼ 0.028). Out of 69 deaths, 33/69 (48%) occurred within the first
two years after diagnosis. Infections accounted for 54/69 (78%) of the deaths and 38/54 (70%)
had concomitant disease activity. Conclusions: This large multicenter study provided evidence
that early-onset cSLE group had distinct outcomes. This group was characterized by higher
mortality rate and neuropsychiatric/vascular/skin organ damage in spite of comparable fre-
quencies of severe cumulative lupus manifestations. We also identified that overall death in
cSLE patients was an early event mainly attributed to infection associated with disease
activity. Lupus (2017) 26, 996–1001.

Correspondence to: CA Silva, Av. Dr Eneas Carvalho Aguiar, 647 –

Cerqueira César São Paulo, SP, Brazil.

Email: clovisaasilva@gmail.com

Received 23 June 2016; accepted 3 January 2017

*Both authors contributed equally with this manuscript.

**Collaborators of the Brazilian Childhood-onset Systemic Lupus

Erythematosus Group:

Children’s Institute, FMUSP—MF Silva, M Ferriani, VL Marques, G

Blay, GE Lube, JD Montoni, LP Coelho, LS Henriques, GV Novak,

BC Molinari, JB Brunelli, P Anuardo, M Verdier, K Kozu, SCL

Farhat, AC Pastorino, HH Marques, JC Rodrigues, A Watanabe,

BG Schvartsman, MH Vaisbich, WB Carvalho, M Carneiro-

Sampaio, V Odone-Filho; Division of Rheumatology, FMUSP—JA

Paupitz, GL Lima, APL Assad; UNIFESP—C Len, MOE Hilário,

AS Lopes, A Alencar, DP Piotto, G Faquin, G Clemente, OAB

Peracchi, V Bugni; UNESP—PR Aoki, JO Sato, SP Cardin, TAP

Fernandes; Irmandade da Santa Casa de Misericórdia de São

Paulo—A Guariento, MC dos Santos, SB Sacchetti; UNICAMP—M

Centeville, R Barbosa, R Marini; Ribeirão Preto Medical School,

FMUSP—PP Kahwage, G Pileggi, LM Carvalho, FH Gomes;

Hospital Infantil Darcy Vargas—J Libório, LTP Paulo; Hospital

Municipal Infantil Menino Jesus—TCM Castro; Pontifical Catholic

University of Sorocaba—VC Ramos.

! The Author(s), 2017. Reprints and permissions: http://www.sagepub.co.uk/journalsPermissions.nav 10.1177/0961203317690616

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Key words: Childhood-onset systemic lupus erythematosus; nephritis; outcome; death;
mortality and cumulative damage

Introduction

Early childhood-onset SLE (cSLE) is a rare auto-
immune disease that may lead to significant mor-
bidity and mortality.1–3 Recently, a large Brazilian
multicenter study reported distinct clinical and
laboratory profiles at cSLE diagnosis.1

Another recent large study comparing cSLE
with adult-onset SLE revealed a more aggressive
and worse outcome in the former group.4

However, analysis of age-related differences regard-
ing outcomes focused on pediatric patients and, in
particular, assessing early-onset cSLE patients (<6
years) has been limited to very small sample sizes,
precluding a definitive conclusion about the
findings.4–9

Thus, the aim of this large multicenter study was
to evaluate demographic data, cumulative clinical
and laboratory features, disease accrual damage,
and mortality rate in three different age groups of
cSLE assessed at last visit: group A—early-onset
disease (<6 years at diagnosis): group B—school
age (�6 and <12 years); and group C—adolescent
(�12 and <18 years).

Patients and methods

A retrospective multicenter cohort study
included 1017 consecutive cSLE patients fol-
lowed at ten pediatric rheumatology centers in
São Paulo state, Brazil. The charts were reviewed
from 2012-2014. One hundred and seventy
patients were excluded, due to the reasons previ-
ously reported.1 The remaining 847 cSLE patients
comprised the study group, and all patients ful-
filled the American College of Rheumatology
(ACR) criteria,10 with disease onset before 18
years of age.3

All investigators were trained in terms of proto-
col definitions of clinical parameters, disease activ-
ity, and damage scores.1 Patient’s medical charts
were meticulously reviewed according to a compre-
hensive standardized protocol for demographic
data, cumulative clinical features, laboratory find-
ings, treatments, and outcomes of cSLE evaluated
at last visit.

Demographic data, cumulative clinical and
laboratory features, disease activity/damage,
and deaths in cSLE patients

Age at cSLE diagnosis, disease duration, and
gender were evaluated. Ethnic groups were divided
into four categories: White (patients with white
European ancestors), African–Latin Americans
(patients born in Latin America with at least one
African ancestor), Asian (patients with Asian
ancestors), and other/unknown.1

Descriptors and definitions of SLE Disease
Activity Index 2000 (SLEDAI-2K) were used to
score disease activity during the last visit,11 and
custom definitions as previously described.1

Neuropsychiatric lupus comprised 19 syndromes
according to ACR classification criteria.12

Antiphospholipid syndrome (APS) was diagnosed
according to the current criteria for the classifica-
tion of pediatric APS.13

Cumulative damage at the last visit was scored
using the Systemic Lupus International
Collaborating Clinics/ACR-Damage Index
(SLICC-ACR/DI).14 Cumulative treatment data
(prednisone, intravenous methylprednisolone,
chloroquine diphosphate, hydroxychloroquine sul-
fate, methotrexate, azathioprine, cyclosporine,
mycophenolate mofetil, intravenous cyclophospha-
mide, intravenous immunoglobulin, rituximab, and
plasmapheresis) were also recorded.

Statistical analysis
Statistical analyses were carried out according to
Statistical Package for the Social Sciences, version
13.0. Results were presented as a number (fre-
quency) for categorical variables and median
(range) or mean� standard deviation (SD) for con-
tinuous variables. Categorical variables were first
compared by Pearson �2 test, which necessitates
that at least 80% of the cells have an expected fre-
quency of� 5 and no cell must have an expected
frequency of< 1. If the subgroup analysis included
less than 300 subjects and the criteria for Pearson
�2 test was not met, then the Fisher–Freeman–
Halton exact test was used. The Kruskal–Wallis
test was used to compare continuous variables
with non-normal distribution involving the three
age groups (non-parametric one-way analysis of
variance (ANOVA)), followed by a post-hoc

Outcomes of 847 cSLE patients
SRM Lopes et al.

997

Lupus


analysis using Dunn’s multiple comparison test to
determine where the difference had occurred
between the three groups’ outcomes. The signifi-
cance level in all analyses was set at 5%.

Results

Patients were classified into three age groups: A 39
(4%), B 395 (47%), and C 413 (49%). Comparison
of demographic data, cumulative clinical manifest-
ations, and disease activity/damage scores at the
last visit in 847 cSLE patients in three age groups
are illustrated in Table 1. The median of disease
duration was significantly higher in group A com-
pared to groups B and C (8.3 (0.1–23.4) vs 6.2
(0–17) vs 3.3 (0–14.6) years, p< 0.0001), with simi-
lar frequencies of male gender (20% vs 16% vs
12%, p¼0.155) (Table 1).

Groups had distinct patterns of cumulative char-
acteristics. In group A, frequencies of cumulative
fever (82% vs 76% vs 61%, p< 0.0001), overall
reticuloendothelial manifestations (54% vs 48%
vs 32%, p< 0.0001), and pericarditis (41% vs
28% vs 22%, p¼ 0.011) were significantly higher
compared to groups B and C (Table 1).
Regarding therapy, cyclosporine use was also
more often observed in group A (24% vs 11% vs
8%, p¼ 0.007) (Table 2).

Mortality rate was significantly higher in group
A compared to groups B and C (15% vs 10% vs
6%, p¼ 0.028). The median disease duration
between cSLE diagnosis and death were similar in
the three age groups (2.9 (0.3–12.8) vs 3.6 (0.17–12)
vs 1.46 (0.6–15.3), p¼ 0.068) (Table 1). Of 69
deaths overall, 33/69 (48%) occurred during the
first two years after diagnosis and 8/33 (24%) in
the first month after diagnosis. Infections
accounted for 54/69 (78%) of overall deaths, with
38/54 (70%) having presented concomitant disease
activity. Other causes of death were nephritis (acute
kidney injury or chronic renal disease) in six (9%)
cSLE patients, alveolar hemorrhage in three (4%),
massive intracranial bleeding in one (1.4%), mul-
tiple thrombosis due to catastrophic APS in one
(1.4%), B-cell lymphoma in one (1.4%), and
unknown etiologies in three (4%).

SLICC/ACR-DI score� 1 was observed in 249/
764 (33%) patients, with a similar frequency in all
groups (39% vs 36% vs 29%, p¼ 0.070). Likewise,
the median SLICC/ACR-DI (0 (0–9) vs 0 (0–6) vs 0
(0–7), p¼ 0.065) was low and comparable in the
three age groups (Table 1). Further analysis of
organ damage domain revealed that frequencies

of neuropsychiatric (21% vs 10% vs 7%,
p¼ 0.007), skin (10% vs 1% vs 3%, p¼ 0.002),
and peripheral vascular damage (5% vs 3% vs
0.3%, p¼ 0.008) were more often observed in
group A compared to groups B and C. The fre-
quencies of renal (8% vs 7% vs 8%, p¼ 0.912)
and musculoskeletal damage (10% vs 10% vs
10%, p¼ 0.989) were similar in all groups.

Group B had higher frequencies of cumulative
central nervous system involvements (46% vs
58% vs 41%, p< 0.0001) compared to groups A
and C (Table 1). The median of prednisone cumu-
lative dose was significantly higher in group B
versus groups A and C (20.6 (1.6–74.5) vs 21.7
(0.6–103.9) vs 17.6 (0.1–105.5) gm, p¼ 0.015)
(Table 2). Ocular damage was observed more
often in group B compared to groups A and C
(10% vs 13% vs 7%, p¼ 0.017) (Table 1).

Group C had no distinct characteristics com-
pared to groups A and B (Tables 1 and 2).

Discussion

We identified that cumulative clinical manifest-
ations and disease damage of cSLE patients
varied considerably according to patient’s age at
disease diagnosis, with distinct cumulative features
particularly in the early-onset cSLE group. We also
observed that death in cSLE patients was an early
outcome mainly attributed to infections associated
with disease activity.

With regard to the early-onset cSLE group, we
confirmed a previous observation of higher fre-
quency of deaths and identified that infection asso-
ciated with disease activity was the main cause
responsible for this outcome in this group of
patients.9 The reported disease severity related to
male gender6 did not seem to contribute to a higher
frequency of death in the early-onset cSLE, since
the male distribution was alike in the three age
groups analyzed. The predominant cumulative clin-
ical features in this age group was fever and reticu-
loendothelial manifestations, findings also reported
in Chinese patients of the same age group.5

One third of our cSLE patients had at least one
organ/system damaged, with a comparable fre-
quency in the three age groups, in spite of distinct
disease duration. This frequency of damage was
similar to the one observed in an international
study including 39 countries.15 The predominance
of neuropsychiatric damage in the early-onset cSLE
is worrisome, since it may affect health-related
quality of life and may induce learning disabilities.

Outcomes of 847 cSLE patients
SRM Lopes et al.

998

Lupus


In contrast to the early-onset cSLE group, the
prepubertal patients had a low frequency of cumu-
lative neuropsychiatric damage. The higher fre-
quency of glucocorticoid use in these patients
suggested that central nervous system lesions were
probably responsive to this therapy, and the latter
may explain the ocular damage observed in this
transitional group.16 Other studies, however, have
not evidenced a distinct pattern of manifestations
in this transition stage group.5,6

In spite of a report of an increased prevalence of
musculoskeletal manifestations in Italian cSLE

adolescents,6 a unique characteristic in this age
group was not observed here.

One of the advantages of the present study was
the standardized protocol,1,17–20 with established
clinical parameters evaluated during the disease
course, and disease activity/damage definitions for
quantitative scores. Additionally, a representative
large sample of cSLE patients was assessed, with a
substantial inclusion of the death figures and
accrued damage in the less frequent age group.5–7,9

Nevertheless, the main limitation of our study was
the missing data of some variables due to the

Table 1 Demographic data, cumulative clinical manifestations, disease activity/damage scores at last visit, and deaths in 847
childhood-onset systemic lupus erythematosus (cSLE) patients according to age groups at diagnosis

Variables
Group A
(<6 yrs) n¼ 39

Group B
(�6 <12 yrs) n¼ 395

Group C
(�12 <18 yrs) n¼ 413 p

Demographic data

Age at cSLE diagnosis, years, n¼ 847 4.25 (0.25–5.9) 10 (6–11.9) 13.8 (12–17.8) <0.0001a

Disease duration, years, n¼ 842 8.3 (0.1–23.4) 6.2 (0–17) 3.3 (0–14.6) <0.0001a

Male gender, n¼ 847 8/39 (20) 63/395 (16) 50/413 (12) 0.155

Ethnic groups, n¼ 825 NA

White 28/37 (76) 278/383 (73) 282/405 (70) –

African–Latin American 9/37 (24) 101/383 (26) 115/405 (28) –

Asian 0/37 (0) 2/383 (0.5) 2/405 (0.5) –

Other/unknown 0/37 (0) 2/383 (0.5) 6/405 (1.5) –

Cumulative clinical manifestations

Fever, n¼ 843 32/39 (82) 298/394 (76) 251/410 (61) <0.0001

Reticuloendothelial manifestations, n¼ 844 21/39 (54) 187/393 (48) 130/412 (32) <0.0001

Mucocutaneous involvement, n¼ 846 38/39 (97) 365/395 (92) 381/412 (92) 0.505

Musculoskeletal involvement, n¼ 847 32/39 (82) 300/395 (76) 319/413 (77) 0.667

Serositis, n¼ 841 19/39 (49) 143/392 (36) 131/410 (32) 0.071

Pericarditis, n¼ 841 16/39 (41) 110/392 (28) 90/410 (22) 0.011

Nephritis, n¼ 842 25/39 (64) 275/393 (70) 254/410 (62) 0.055

Neuropsychiatric involvement, n¼ 844 18/39 (46) 229/395 (58) 173/410 (42) <0.0001

Autoimmune hemolytic anemia, n¼ 837 12/39 (31) 110/389 (28) 87/409 (21) 0.051

Thrombocytopenia, <100,000/mm3, n¼ 838 10/39 (26) 93/390 (24) 82/409 (20) 0.372

Current disease activity score at last visit

SLEDAI-2K, n¼ 839 6 (0–30) 4 (0–45) 4 (0–35) 0.615

SLEDAI-2K� 8, n¼ 839 16/39 (41) 96/390 (25) 86/410 (21) 0.015

Disease damage score at last visit

SLICC/ACR-DI, n¼ 764 0 (0–9) 0 (0–6) 0 (0–7) 0.065

SLICC/ACR-DI� 1, n¼ 764 15/38 (39) 130/362 (36) 104/364 (29) 0.070

Neuropsychiatric 8/38 (21) 36/362 (10) 24/364 (7) 0.007

Skin 4/38 (10) 5/362 (1) 10/364 (3) 0.002

Peripheral vascular 2/38 (5) 10/362 (3) 1/364 (0.3) 0.008

Ocular 4/38 (10) 48/362 (13) 25/364 (7) 0.017

Renal 3/38 (8) 25/362 (7) 28/364 (8) 0.912

Musculoskeletal 4/38 (10) 38/362 (10) 37/364 (10) 0.989

Cardiovascular 2/38 (5) 6/362 (2) 5/364 (1) 0.210

Deaths, n¼ 69/841 6/39 (15) 39/393 (10) 24/409 (6) 0.028

Disease duration between cSLE diagnosis and death, years 2.9 (0.3–12.8) 3.6 (0.17–12) 1.46 (0.6–15.3) 0.068

Infections, n¼ 54/69 5/6 (83) 29/39 (74) 20/24 (83) NA

Infections associated with disease activity, n¼ 38/54 3/5 (60) 20/29 (69) 15/20 (75) NA

Results are presented in n(%) and median (range).

APS: antiphospholipid syndrome; SLEDAI-2K: Systemic Lupus Erythematosus Disease Activity Index 2000; NA: not applicable to assess Pearson

�2 test.
aPost-hoc analysis by Dunn’s multiple comparison test showed significant difference between all age groups (p< 0.001).

Outcomes of 847 cSLE patients
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retrospective study design. SLEDAI over time was
also not assessed. Therefore, a further inception
cohort study evaluating outcomes in a large Latin
America cSLE population will be necessary.

In conclusion, this large multicenter study pro-
vided evidence that the early-onset cSLE group had
distinct cumulative clinical features and outcomes.
This group was characterized by higher mortality
rate and neuropsychiatric/vascular/skin organ
damage. We also identified that overall death in
cSLE patients was an early outcome mainly attrib-
uted to infections associated with disease activity.

Acknowledgement

Our gratitude goes to Ulysses Doria-Filho for the
statistical analysis.

Declaration of conflicting interests

The authors declared no potential conflicts of inter-
est with respect to the research, authorship, and/or
publication of this article.

Funding

The authors disclosed receipt of the following finan-
cial support for the research, authorship, and/or pub-
lication of this article: grants from Conselho Nacional

de Desenvolvimento Cientı́fico e Tecnológico (CNPq
301805/2013-0 to RMRP, 303752/2015-7 to MTT,
301479/2015-1 to CSM, 305068/2014-8 to EB and
303422/2015-7 to CAS), Federico Foundation (to
EB, RMRP and CAS) and by Núcleo de Apoio à
Pesquisa ‘‘Saúde da Criança e do Adolescente’’ da
USP (NAP-CriAd) to CAS.

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Table 2 Cumulative treatments at last visit in 847 childhood-onset systemic lupus erythematosus (cSLE) patients according to age
groups at diagnosis

Cumulative treatments variables
Group A
(<6 yrs) n¼ 39

Group B
(�6 <12 yrs) n¼ 395

Group C
(�12 <18 yrs) n¼ 413 p

Nonsteroidal anti-inflammatory, n¼ 840 13/38 (34) 118/393 (30) 101/409 (25) 0.156

Prednisone, n¼ 838 38/38 (100) 384/390 (98) 403/410 (98) 0.717

Cumulative dose, gm, n¼ 711 20.6 (1.6–74.5) 21.7 (0.6–103.9) 17.6 (0.1–105.5) 0.015a

Intravenous methylprednisolone, n¼ 839 26/38 (68) 279/394 (71) 275/407 (68) 0.607

Cumulative dose, gm, n¼ 473 9 (1.4–78.6) 8.7 (0.2–138.5) 9 (0.5–111.7) 0.920

Total glucocorticoid dose, gm, n¼ 689 24.7 (1.6–111.6) 28.3 (0.5–205.5) 25.8 (0–2717) 0.687

Antimalarial drugs, n¼ 842 31/38 (82) 325/393 (82) 344/411 (83) 0.899

Immunosuppressive agents, n¼ 843 31/38 (81) 333/393 (85) 350/412 (85) 0.858

Azathioprine, n¼ 839 22/38 (58) 226/392 (58) 264/409 (64) 0.125

Cyclosporine, n¼ 837 9/38 (24) 43/390 (11) 22/409 (8) 0.007

Methotrexate, n¼ 837 10/38 (26) 100/389 (26) 80/410 (19) 0.097

Mycophenolate mofetil, n¼ 835 9/37 (24) 92/389 (23) 74/409 (18) 0.137

Intravenous cyclophosphamide, n¼ 842 17/38 (45) 186/393 (47) 149/411 (36) 0.006

Cumulative dose, gm, n¼ 309 6.8 (0.3–32) 7.8 (0.4–93) 6.4 (0.5–47) 0.373

Results are presented in n(%) and median (range).

ESR: erythrocyte sedimentation rate; CRP: C-reactive protein; NA: not applicable to assess Pearson �2 test.
aPost-hoc analysis by Dunn’s multiple comparison test showed significant differences between cumulative dose of prednisone between groups B vs

C (p< 0.05).

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