Maternal and Child Health Journal (2023) 27:1578–1588

https://doi.org/10.1007/s10995-023-03680-x

Health Related Quality of Life in Juvenile‑Onset Systemic Lupus

Erythematosus: A Questionnaire‑Based Study
Riham Eid1 · Ayman Hammad1 · Mai S. Korkor1 · Aya A. Fathy2 · Dena M. Abd El‑Ghafaar3 · Shaimaa Rakha4 ·
Nashwa Hamdy1

Accepted: 16 May 2023 / Published online: 12 June 2023

© The Author(s) 2023

Abstract
Objectives This study aimed to evaluate health related quality of life (HRQOL) in Egyptian children with systemic lupus
erythematosus (SLE) using 3 different tools.
Methods In this questionnaire-based study, 100 children with SLE were included. HRQOL was assessed using the Pediatric
Quality of Life Inventory Generic Core Scales (PedsQL™ 4.0 GCS), PedsQL™ 3.0 Rheumatology Module (PedsQL3-
RM) and the Simple Measure of the Impact of Lupus Erythematosus in Youngsters (SMILEY). SLE disease activity index
(SLEDAI) was used to evaluate activity and SLE International Collaborating Clinics/ American College of Rheumatology
Damage Index (SDI) was used to evaluate chronic damage.
Results All mean scores of ­PedsQLTM4.0 GCS domains in SLE patients were lower than published normative data and previ-
ously published results of Egyptian healthy controls (p < 0.001). All mean scores of PedsQL-3RM domains were significantly
lower than published normative data except for the treatment and pain and hurt domains (p = 0.1, 0.2 respectively). SMILEY
scores were low and the lowest domain scores was “Burden of SLE”. Longer duration of illness, higher cumulative steroid
doses, higher SLEDAI and SDI scores and presence of obesity were associated with lower scores for all 3 tools (p < 0.001).
Conclusion for Practice The Arabic copies of PedsQL™ 4.0 GCS, PedsQL3-RM and SMILEY are easily used for Arabic
speaking subjects and easily interpreted by physician and can be implemented for frequent monitoring of SLE HRQOL.
Controlling the disease activity and using lowest doses of steroids and other immunosuppressive drugs are the corner stone
strategies for improving HRQOL in SLE children.

Significance
This is the first study to evaluate HRQOL scores in Egyptian children with SLE which were found to be lower than pub-
lished data with long disease duration, high cumulative disease activity, use of steroids and presence of obesity are the main
influential factors related to low QoL scores. Generic and disease specific questionnaires are easily used for Arabic speaking
subjects and easily interpreted by physician and can be implemented for frequent monitoring of SLE HRQOL. Controlling

1
* Riham Eid Pediatric Nephrology Unit, Faculty of Medicine, Mansoura
[email protected] University Children’s Hospital, Mansoura University,
Mansoura 35561, Egypt
Ayman Hammad
2
[email protected] Public Health and Community Department, Faculty
of Medicine, Mansoura University, Mansoura, Egypt
Mai S. Korkor
3
[email protected] Rheumatology, Rehabilitation and Physical Medicine
Department, Faculty of Medicine, Mansoura University,
Aya A. Fathy
Mansoura, Egypt
[email protected]
4
Pediatric Cardiology Unit, Faculty of Medicine, Mansoura
Dena M. Abd El‑Ghafaar
University Children’s Hospital, Mansoura University,
[email protected]
Mansoura, Egypt
Shaimaa Rakha
[email protected]
Nashwa Hamdy
[email protected]

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Maternal and Child Health Journal (2023) 27:1578–1588 1579

the disease activity and using lowest doses of steroids and other immunosuppressive drugs are the corner stone strategies
for improving HRQOL in SLE children.

Keywords Children · Egypt · Lupus · Quality of life

Abbreviations Health- related quality of life (HRQOL) has been defined

ACR​ American college of rheumatology as a “multi-dimensional concept including physical, social
BMD Bone mineral density and psychological functioning related to a certain illness or
BMI Body mass index its treatment” (Miller et al., 2002). The physical, emotional,
CGCS Cumulative glucocorticoids and social effects of SLE drastically influence the QoL of
cSLE Childhood systemic lupus patients. This can be related to repeated hospitalizations,
erythematosus follow up visits, frequent laboratory monitoring, health-care
CNS Central nervous system. costs, and interference with daily activities (Hersh et al.,
eGFR Estimated Glomerular filtration rate 2009; Mina & Brunner, 2010). Research in adults with SLE
HRQOL Health related quality of life suggests that the disease has a significant negative impact on
JIA Juvenile idiopathic arthritis the patients’ HRQOL (Thumboo & Strand, 2007). Similar
LN Lupus nephritis research in children is lacking as there are few studies exam-
MMF Mycophenolate mofetil ining the HRQOL in small cSLE cohorts using standardized
QoL Quality of life instruments (Brunner et al., 2009; Moorthy et al., 2017).
PedsQL™ 4.0 GCS Pediatric Quality of Life Inventory So, evaluating the different domains of QoL of children
Generic Core Scales with SLE using pediatric specific tools have become critical
PedsQL3-RM PedsQL™ 3.0 Rheumatology determinants of the disease impact (Brunner & Giannini,
Module 2003; Moorthy et al., 2005; Ravelli et al., 2005). Consider-
SLE Systemic lupus erythematosus ing the paucity of information of QoL in cSLE in general,
SLEDAI Systemic lupus erythematosus and Egyptian children particularly, we conducted the present
disease activity index study. The objectives of our study were to assess the QoL
SDI SLE International Collaborat- in children aged 8–18 years with SLE using the Pediatric
ing Clinics/ American College of Quality of Life Inventory Generic Core Scales (PedsQL™
Rheumatology Damage Index 4.0 GCS), the PedsQL™ 3.0 Rheumatology Module (Ped-
SMILEY Simple Measure of the Impact sQL™ 3.0 RM) and the Simple Measure of the Impact of
of Lupus Erythematosus in Lupus Erythematosus in Youngsters (SMILEY), compare
Youngsters it to that of available cohorts; and assess the relationship of
QoL with SLE disease features, activity, and damage scores.

Introduction
Subjects and Methods
Childhood Systemic lupus erythematosus (cSLE) is char-
acterized by severe course, widespread organ involvement Participants
especially renal and central nervous systems (CNS) and high
mortality compared to adult-onset SLE (Ravelli et al., 2005). This questionnaire-based study was conducted in Mansoura
Young adults with SLE reported to have mortality rates 20- University Children’s Hospital in Egypt over the period of
times higher than general population (Brunner et al., 2008). 12 months. The study was approved by the local ethical com-
With the advances in treatment of cSLE, mortality rates mittee and all participants/ guardians gave their informed
decreased and life expectancy of the patients increased asso- consent prior to their inclusion in the study. A standardized
ciated with a wide-ranging spectrum of long-term morbidi- introduction on HRQOL was given to both patients and par-
ties which accumulates more quickly in cSLE compared to ents prior to fulfilment of the questionnaires.
adult-onset caused by higher rates of nephritis (Levy et al.,
2014), more aggressive course which increases the expo- Inclusion Criteria
sure to immunosuppressive medications over a longer dis-
ease duration and the impact of disease and medications side All included children were diagnosed to have SLE after ful-
effects on school performance and later on sexual and repro- filling the American College of Rheumatology (ACR) clas-
ductive lives of affected adolescents (Hersh et al., 2009). sification criteria (Hochberg, 1997) and with a duration of
illness of more than 1-year, normal kidney function, with no

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1580 Maternal and Child Health Journal (2023) 27:1578–1588

active infection and not admitted to the hospital at time of instruments/pediatric-quality-of-life-inventory# need _ this
enrolment in the study. _ questionnaire) provided by MAPI research institute, Lyon,
France]. This version of the questionnaire has been previ-
Exclusion Criteria ously used in the assessment of QoL in Egyptian children
with nephrotic syndrome (NS) (Eid et al., 2020). The Ped-
Children with disabilities, psychological problems or obesity sQL™ 3.0 RM was translated into Arabic by the authors,
that have been diagnosed before the onset of SLE and those and a professional English language expert. The Arabic copy
with mixed connective tissue diseases were excluded. of the questionnaire was approved by MAPI research insti-
During the period of the study and after applying tute, France and by professor James W. Varni. A free Arabic
inclusion and exclusion criteria, 123 cSLE patients were “for Egypt” copy of the SMILEY module was provided by
approached to participate of which 100 were enrolled (23 Professor Moorthy with the permission to use it.
patients not included as either refused to participate or
agreed initially then did not return completed questionnaire Measures
form).
All patients with clinically evident lupus nephritis (LN) PedsQL™4.0 Generic Core Scale
had ultrasound guided renal biopsy before starting treatment.
Total cumulative steroid dose was calculated for patients’ We used the children (8–12 years) and adolescents
weights and presented as g/kg according to which patients (13–18 years) copies of the questionnaire according to
were divided into 2 groups: high cumulative glucocorticoids patients’ age. A 5-point response scale was used from 0 to
(CGCS) dose (> 1 gm/kg) and low CGCS (< 1 gm /kg). Obe- 4. Items are reverse-scored and converted to a 0–100 scale
sity was defined as body mass index (BMI) above 95th per- so higher scores indicate better QoL. Scale scores are com-
centile for age. Bone complications included: pathological puted as the sum of the items divided by the number of items
fracture, avascular necrosis of femoral head and low bone answered (accounting for missing data). If more than 50% of
mineral density (BMD) diagnosed as BMD z-score < -2 (El- the items in the scale are missing, the scale score is not com-
Ziny et al., 2007). puted (Varni et al., 2001). This accounts for the differences
Current and previously reported disease activity [evalu- in sample sizes for scales reported in the results’ tables. The
ated by SLE Disease Activity Index 2000 (SLEDAI-2 K)] obtained results in all domains of PedsQL™ 4.0 were then
(Gladman et al., 2002) and disease related damage evalu- compared to its previously published normative data (Varni
ated by SLE International Collaborating Clinics/ American et al., 2003) and results of 100 healthy control Egyptian
College of Rheumatology Damage Index (SDI) were also children published in 2020 (Eid et al., 2020).
obtained. SDI is an instrument that allows evaluation of
accumulated damage in SLE patients including evaluation The PedsQL™ 3.0 RM
of 12 organ systems. Damage may be caused by previous
disease activity or by medications and should be ascertained We used the children (8–12 years) and adolescents
by clinical assessment and present for at least 6 months. A (13–18 years) copies of the questionnaire. The tool evaluates
higher SDI score indicates worsening disease damage (Glad- the QoL in 5 domains (pain and hurt, daily activities, treat-
man et al., 1996). For comparative purposes, we used cut- ment, worry, and communication). The format, instructions,
off values like published articles to group the patients with Likert scale, and scoring scheme are the same as the Ped-
greater disease activity and damage (cutoffs for SDI ≥ 2, sQL™ 4.0, with higher scores indicating better QoL (Varni
SLEDAI ≥ 12) (Moorthy et al., 2007, 2009, 2017). et al., 2001). For our study, we used PedsQL™ 3.0 RM
ratings of a cohort of 56 children with juvenile idiopathic
Procedures arthritis (JIA) as normative values for comparison which
was the first study to validate this rheumatology specific
All questionnaires were completed in paper form only. Ques- questionnaire in children with JIA being the most common
tionnaire forms were completed during clinic visits. Ques- pediatric rheumatology disorder (Brunner et al., 2004).
tionnaires were completed by the children, with only few
patients required some help from parents to understand some SMILEY
question (without guiding their answers).
Data were collected by a structured questionnaire using The SMILEY is the only disease-specific measure of
PedsQL™ 4.0 GCS, the PedsQL™ 3.0 RM, and the SMI- HRQOL in cSLE. We used child report of the SMILEY
LEY module. An “Arabic for Egypt” version (Language of measure. The SMILEY is a 26-item survey. The first 2 sur-
all participants) of the PedsQL™ 4.0 GCS is available for vey items are summary questions that are not included in the
free after registration at (https://​eprov​ide.​mapi trust.org/ final score. Item 1 relates to current HRQOL status and item

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2 relates to current SLE status. Responses are in the form of Table 1  Clinical and laboratory data of the patients
an illustrative 5-step scale with different facial expressions. Parameter Results
If more than 12 questions are not answered, SMILEY cannot
be scored. All items, including the first 2 summary ques- Sex male/female 21/79
tions, score from 1 to 5. The total score is transformed to a Age at diagnosis(years) mean ± SD 11.5 ± 2.6
1–100 scale (according to the scoring manual provided by Duration of illness (months) mean ± SD, 31.4 ± 19.9, 12–108
range
Professor Moorthy). Higher scores reflect better QoL. Being
Residence rural/urban 66/34
a disease specific tool, there are no normative values for the
School level 20/36/43/1
SMILEY questionnaire (Moorthy et al., 2006).
(primary/preparatory/secondary/non-
educated)
Statistical Analysis Family size range (3–9)
(Up to 5/above 5) 70/30
A sample size of 100 cSLE patients was chosen based on Source of medications:
the duration of the study, availability of cases that fulfil Self-purchased 3
inclusion criteria and collaboration of patients. Continu- Hospital 65
ous variables with normal distribution were expressed as Health insurance 7
means and standard deviation and compared using Student’s Mixed 25
t-test, whereas those not normally distributed were using Clinical manifestations (number/percentage):
Mann–Whitney U-test. Categorical variables were compared LN (class I, II, III, IV, V, VI) 70(8, 11, 23, 27, 1, 0)
using the Chi-square test or Fisher’s exact test. Subsequently, Skin manifestations 75
the association of demographic parameters, clinical features, CNS 11
and disease complications to QoL scores was investigated Arthritis 64
for SLE patients (Table 6) using Pearson correlation or t-test Serositis 18
(compare means) as relevant to the included variable. Cor- Number of hospital admissions (range), (0–9) 1.6 ± 1.6
relation between SMILEY scores and each of PedsQL™ mean ± SD
4.0 GCS and PedsQL™ 3.0 RM scores was conducted. Sta- SLEDAI score: mean ± SD
tistical analysis was done using Statistical Package for the At enrolment: 7.5 ± 4.6
Social Science software version 25.0 (SPSS Inc., Chicago, Cumulative: 8.3 ± 3.9
IL, USA). SDI: at enrolment: mean ± SD 0.42 ± 0.85
BMD Z-score mean ± SD − 0.65 ± 1.3
Medications
Results Steroid + hydroxychloroquine only 42
Cyclophosphamide (ever) 40
One hundred children with SLE participated in the study, MMF 12
79 females, and aged 14.04 ± 2.5 years at time of the study. Azathioprine 7
Characteristics of patients are summarized in Table 1. All CGCS: mean ± SD 0.84 ± 0.61
SLE children had normal kidney function at enrollment with High/low 37/63
eGFR 140.7 ± 25.8 ml/min/1.732. The number of medica- Complications
tions taken by each patient at enrolment ranged between 2 Decreased BMD (Z-score < -2) 19
and 5 medications including steroids, hydroxychloroquine, Pathological fracture/AVN 3
mycophenolate mofetil (MMF), cyclosporine, cyclophospha- Alopecia 47
mide, antihypertensives, calcium and vitamin supplementa- Cushingoid manifestations 35
tion. Due to presence of missing data and as described in Diabetes Miletus 2
methodology section, total scores of the 3 used measures Ocular complications 0
were calculated for 98 patients each. The mean scores for Obesity 33
each domain and summary score of the 3 scales are pre- Hypertension 15
sented in Tables 2 and 3. The mean scores for PedsQL™
SLE Systemic lupus erythematosus, SDI SLE damage index, SLEDAI
4.0 are compared to published normative data (Varni et al., SLE disease activity index, BMD bone mineral density, AVN avascu-
2003) and to the scores of 100 healthy Egyptian children lar necrosis, MMF Mycophenolate mofetil, SD standard deviation,
data published in 2020 (Eid et al., 2020) showing signifi- CNS central nervous system, LN lupus nephritis, CGCS cumulative
glucocorticoids
cantly lower scores for SLE patients in all domains. The
mean scores for PedsQL3-RM are compared to children
diagnosed with JIA as a comparative population.

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Table 2  Comparison of PedsQL™ 4.0 and PedsQL™ 3.0 RM results and normative data
Measure Normative data mean ± SD (N) SLE patients mean ± SD p-value
(N)
Published Normative Egyptian children

PedsQL™ 4.0 GCS

Summary score 82.9 ± 13.2(5972) 86.02 ± 6.1 (96) 71.3 ± 11.6(98) < 0.001** < 0.001***
Physical 86.9 ± 13.9(5962) 87.3 ± 8.6(99) 69.3 ± 13.5(99) < 0.001 < 0.001
Emotional 78.2 ± 18.6(5961) 87.3 ± 7.5 (99) 72.3 ± 13.7(98) 0.002 < 0.001
Social 84.0 ± 17.4(5948) 86.7 ± 7.7(99) 71.2 ± 12.9(99) < 0.001 < 0.001
School 79.9 ± 16.9(5908) 86.45 ± 7.9(99) 71.6 ± 11.9(97) < 0.001 < 0.001
PedsQL™ RM* Published normative (N = 56)
Summary score 84.4 ± 18 72.1 ± 9.9(98) < 0.0001
Daily activities 95.6 ± 11.1 71.9 ± 15.1(99) < 0.0001
Treatment 82.1 ± 16.3 78.4 ± 11.9(99) 0.1
Pain and hurt 77.8 ± 24.2 74.2 ± 14.2(97) 0.2
Communication 87.9 ± 16.3 73.2 ± 8.3(100) < 0.0001
Worry 83.6 ± 18.5 62.8 ± 9.8(98) < 0.0001

PedsQL™ 4 GCS Pediatric Quality of Life Inventory Generic Core Scales, PedsQL™ 3.0 RM the PedsQL™ 3.0 Rheumatology Module, SLE
systemic lupus erythematosus, SD standard deviation
*Source for PedsQL RM norms in 56 children with juvenile rheumatoid arthritis
**SLE patients vs published normative data
***SLE patients vs Egyptian children control data
Bold figures are the statistically significant values

(Brunner et al., 2004) (Table 2) and showed significantly (SDI < 2) (N = 92) or severe damage (SDI ≥ 2) (N = 8). The
lower scores for in SLE patients compared to controls in all mean scores for all domains of the 3 used scales for the 2
domains except for treatment and pain and hurt domains. groups (no/mild and severe severe) were calculated and com-
Being a disease specific scale, SMILEY has no normative pared in Table 5. Table 6 shows correlation of QoL scores
data, so we compared our results to published studies from of the 3 measures used and different clinical manifestations
different countries (Table 3). and revealed that longer duration of illness, high cumula-
As skin manifestations and LN are the most prevalent tive steroid doses, higher SLEDAI and SDI scores, presence
manifestations and LN being a leading cause of morbidi- of obesity and low BMD were associated with low QoL
ties and mortalities and a unique feature of cSLE compared scores for all 3 tools (p < 0.001). No significant differences
to other pediatric rheumatologic disorders and adult onset were reported between male and female patients scores of all
SLE, the total and domains’ scores for the used measures domains of 3 scales, disease activity or damage (p > 0.05 for
were compared between patients with and without LN and all). Spearman correlation showed that SMILEY total scores
showed that SMILEY total and domain scores were signifi- corelated more strongly with PedsQL3-RM (r = 0.917,
cantly lower in patients with LN compared to those with- p < 0.001) than PedsQL™ 4.0 (r = 0.753, p < 0.001).
out LN, while no significant differences in PedsQL™ 4.0
scores and only worry domain of PedsQL3-RM was signifi-
cantly lower in LN patients. Regarding skin manifestations, Discussion
no significant differences reported in total and all domain
scores of the 3 scales in patients with and without lupus skin The differences in cSLE regarding disease onset, pheno-
manifestations. Disease activity was evaluated by SLEDAI type, and outcomes between different ethnic groups is not
score according to which patients were classified as having fully elucidated (Massias et al., 2021). Additionally, differ-
no/mild (SLEDAI < 12) (N = 77) or severe disease activity ences in health care levels and attention to Qol also differ
(SLEDAI ≥ 12((N = 23). The mean scores for all domains between countries. In Egypt the overall estimated preva-
of the 3 scales for the 2 groups (mild and severe active dis- lence of cSLE is 1/100,000 population (0.24/100000 males
eases) were calculated and compared in Table 4. Disease and 1.8/100000 females). The age of onset and female pre-
related damage was evaluated by SDI according to which dominance are like other countries however, LN is more
patients were classified as having no or minimal damage common in Egypt compared to cSLE from other countries

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Table 3  Comparison of SMILEY scores of current study and published studies

Domain Study Results Current study results p-value
Mean ± SD(N) Mean ± SD(N) 95%CI

Total Moorthy et al. (2009)* 64 ± 12 (67) 58.8 ± 19.4(98) 0.05 (− 10.5 to 0.06)
Effect on self USA 64 ± 15(66) 63.5 ± 24.3(96) 0.9(− 7.1 to 6.1)
Mixed ethnicity
Limitations 63 ± 16(65) 58.3 ± 21.9(96) 0.14(− 10.9 to 1.56)
Effect on social life 81 ± 16(67) 73.3 ± 21.3(96) 0.01(− 13.7 to − 1.6)
Burden of SLE 58 ± 15(65) 53.7 ± 25.1(98) 0.22(− 11.1 to 2.5)
Total Moorthy et al. (2017)* 65 ± 14(182) 58.8 ± 19.4(98) 0.002(− 10.2 to − 2.2)
Effect on self North America 65 ± 17(181) 63.5 ± 24.3(96) 0.55(− 6.4 to 3.4)
Limitations 64 ± 17(182) 58.3 ± 21.9(96) 0.02(− 10.4 to − 1.02)
Effect on social life 82 ± 16(182) 73.3 ± 21.3(96) < 0.001(− 13.2 to − 4.2)
Burden of SLE 57 ± 17(182) 53.7 ± 25.1(98) 0.2(− 8.3 to 1.7)
Total Moorthy et al. (2017)* 67 ± 15(106) 58.8 ± 19.4(98) < 0.001(− 12.9 to − 3.4)
Effect on self South America 68 + 20(106) 63.5 ± 24.3(96) 0.15(− 10.7 to 1.7)
Limitations 66 ± 19(106) 58.3 ± 21.9(96) 0.008(− 13.3 to − 2.02)
Effect on social life 84 ± 15(106) 73.3 ± 21.3(96) < 0.0001(− 15.8 to − 5.6)
Burden of SLE 56 ± 19(106) 53.7 ± 25.1(98) 0.5(− 8.4 to 3.8)
Total Moorthy et al. (2017)* 68 ± 16(78) 58.8 ± 19.4(98) < 0.001(− 14.6 to − 3.8)
Effect on self Europe 68 ± 20(78) 63.5 ± 24.3(96) 0.19(− 11.3 to 2.3)
Limitations 66 ± 20(73) 58.3 ± 21.9(96) 0.02(− 14.2 to − 1.2)
Effect on social life 86 ± 15(77) 73.3 ± 21.3(96) < 0.0001(− 18.4 to − 7.03)
Burden of SLE 60 ± 18(78) 53.7 ± 25.1(98) 0.06(− 12.9 to 0.36)
Total Moorthy et al. (2017)* 72 ± 14(86) 58.8 ± 19.4(98) < 0.0001(− 18.2 to − 8.2)
Effect on self Asia 72 ± 17(87) 63.5 ± 24.3(96) 0.007(− 14.6 to − 2.3)
Limitations 71 ± 17(86) 58.3 ± 21.9(96) < 0.0001(− 18.5 to − 6.9)
Effect on social life 86 ± 14(86) 73.3 ± 21.3(96) < 0.0001(− 18.03 to − 7.4)
Burden of SLE 62 ± 19(78) 53.7 ± 25.1(98) 0.02(− 15.1 to − 1.5)
Total Moorthy et al. (2013)* 67 ± 16(93) 58.8 ± 19.4(98) 0.002(− 13.3 to − 3.1)
Effect on self Brazil 70 ± 20(93) 63.5 ± 24.3(96) 0.05 (− 12.9 to − 0.1)
Limitations 66 ± 20(93) 58.3 ± 21.9(96) 0.01(− 13.7 to − 1.7)
Effect on social life 85 ± 14(93) 73.3 ± 21.3(96) < 0.0001(− 16.9 to − 6.5)
Burden of SLE 57 ± 19(93) 53.7 ± 25.1(98) 0.3(− 9.6 to 3.1)

*First visit child report results only are included in comparison

SMILEY Simple Measure of the Impact of Lupus Erythematosus in Youngsters, SLE systemic lupus erythematosus
Bold figures are the statistically significant values

(Eesa et al., 2021) which is associated with use of more all the challenges they are facing. This was the motive for
immunosuppressives, frequent hospitalization and risk conducting the current study.
of deterioration of kidney functions. Youth with SLE in Multiple scales have been used to evaluate QoL in cSLE
Egypt face many challenges including late diagnosis, cost (Levy et al., 2014; Putera et al., 2020). Regarding generic
of diagnostic work up, and treatment. Moreover, pediat- questionnaires, Varni et al;(2001) reported that PedsQL™
ric rheumatology/nephrology service is available only in 4.0 summary score in SLE was significantly lower than
few centers in Egypt. Some medications including recent healthy children and that PedsQL™ 4.0 can differentiate
biologics are not available in Egypt which limit choices between healthy children and those with rheumatology
available for refractory cases. Cyclophosphamide is used disorder. Brunner et al; (2009) reported that CHQ-P50 and
in up to 50% of cSLE in Egyptian patients due to its avail- the PedsQL™ 4.0 scores of SLE children were lower than
ability and low cost despite being not preferred by the healthy children and that the 2 measures are responsive to
patients and families due to cosmetic and gonadal side clinically important changes in cSLE disease activity. In
effects (Eesa et al., 2021 and Elmougy et al., 2015). Qol the current study, all domains of the PedsQL™ 4.0 were
is not part of the care of youth with SLE in Egypt despite significantly lower in SLE children compared to published

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Table 4  Quality of life scores in patients with low versus high disease Table 5  Quality of life scores in patient with and without damage
activity
Measure Minimal or Damage (N = 23) p-value
Measure Low disease High disease P-value no damage
activity (N = 77) activity (N = 23) (N = 67)
SLEDAI < 12 SLEDAI ≥ 12 SDI ≤ 2 SDI > 2
Mean ± SD(N) Mean ± SD mean ± SD (N) mean ± SD(N)

PedsQL™ 4.0 GCS PedsQL™ 4.0 GCS

Summary score 73.7 ± 10.35(75) 63.8 ± 12.2(23) < 0.001 Summary score 72.2 ± 11.6(90) 61.4 ± 4.6(8) 0.01
Physical 71.5 ± 12.5(77) 61.3 ± 14.2(22) 0.002 Physical 70.7 ± 13.2(91) 53.4 ± 0.8(8) < 0.001
Emotional 74.9 ± 12.58(75) 64.04 ± 14.2(23) 0.001 Emotional 72.8 ± 13.9(90) 67.3 ± 10.8(8) 0.3
Social 73.3 ± 11.5(76) 64.13 ± 14.7(23) 0.002 Social 72.3 ± 12.7(91) 58.8 ± 6.4(8) < 0.001
School 73.6 ± 10.25(75) 65 ± 14.56(22) 0.002 School 72.1 ± 11.9(89) 66.9 ± 9.6(8) 0.2
PedsQL™ 3 RM* PedsQL™ 3 RM*
Summary score 73.86 ± 9.6(76) 65.87 ± 8.98(22) 0.001 Summary score 73.1 ± 9.8(90) 60.6 ± 3.1(8) 0.001
Daily activities 72.8 ± 16.1(77) 68.7 ± 11.1(22) 0.3 Daily activities 72.6 ± 15.5(91) 64.3 ± 6.7(8) 0.14
Treatment 80.3 ± 11.8(77) 71.8 ± 9.89(22) 0.003 Treatment 79.5 ± 11.6(91) 66.3 ± 8.3(8) 0.002
Pain and hurt 76.7 ± 13.1(75) 65.6 ± 14.7(22) 0.001 Pain and hurt 75.7 ± 13.9(89) 57.8 ± 3.2(8) < 0.001
Communication 75.1 ± 7.68(77) 67.1 ± 7.49(23) < 0.001 Communication 74.1 ± 7.9(92) 63.3 ± 4.8(8) < 0.001
Worry 64.4 ± 9.96(75) 57.8 ± 7.4(23) 0.004 Worry 63.6 ± 9.6(90) 51.5 ± 1.8(8) < 0.001
SMILEY SMILEY
Total 62.4 ± 18.59(76) 46.1 ± 16.79(22) < 0.001 Total 61.1 ± 18.5(90) 33.2 ± 3.6(8) < 0.001
Effect on self 67.4 ± 23.7(75) 50.2 ± 22.14(22) 0.003 Effect on self 66.2 ± 23.6(89) 33.5 ± 4.7(8) < 0.001
Limitations 62.5 ± 29.87(75) 43.5 ± 19.6(21) < 0.001 Limitations 60.4 ± 21.7(88) 35.3 ± 7.1(8) < 0.001
Effect on social life 77.09 ± 19.3(74) 60.68 ± 23.3(22) 0.001 Effect on social life 76.5 ± 19.2(88) 38.1 ± 8.4(8) < 0.001
Burden of SLE 57.4 ± 21.2(75) 41.86 ± 21.2(23) 0.009 Burden of SLE 56.1 ± 24.8(90) 27.5 ± 1.5(8) < 0.001

PedsQL™ 4 GCS Pediatric Quality of Life Inventory Generic Core PedsQL™ 4 GCS Pediatric Quality of Life Inventory Generic Core
Scales, PedsQL™ 3.0 RM the PedsQL™ 3.0 Rheumatology Module, Scales, PedsQL™ 3.0 RM the PedsQL™ 3.0 Rheumatology Module,
SLE systemic lupus erythematosus, SD standard deviation, SLEDAI SLE systemic lupus erythematosus, SD standard deviation, SDI sys-
SLE disease activity index temic lupus damage index
Bold figures are the statistically significant values Bold figures are the statistically significant values

normative data (Varni et al., 2003) and to a previously pub- good QoL score as stated by Varni et al; (2001), the score is
lished data of healthy Egyptian children (Eid et al., 2020) still significantly lower than normative data of children with
but with no difference in affection between domains which JIA (Brunner et al., 2004) with the worry domain scores
is also inconsistent with Rogers et al. who reported school being the lowest in our cohort. Comparing our results to the
domain to be the most affected (Rogers et al., 2017) and report by Stevens et al; (2019), total and all domain scores
also a report from USA (Stevens et al., 2019). Noticeably, of PedsQL™ 3.0 RM were significantly lower in our cohort.
all domains of PedsQL™ 4.0 of our patients are lower than Putera et al; (2020) reported PedsQL™ 3.0 RM scores to
scores of SLE children reported by Brunner et al., (2009), be much lower in children with LN during induction phase
Stevens et al; (2019) but not different from earlier reports as compared to maintenance phase. This again emphasis that
Varni et al; (2002) (except for social domain). The inconsist- that characteristics of patients at time of enrolment in the
ency of the results of the studies may be due to differences in study have great effect on the scores of HRQOL question-
selection criteria of patients, ethnic differences which mod- naires and could account for the inconsistency of results
ify disease presentation and severity, differences in patients’ between studies despite using same scales.
care between countries and the improvement of patients’ In pediatric rheumatology practice, outcome measures are
care over years. primarily concentrated on the impact of physical disability
Multiple rheumatology specific QoL questionnaires are pain on different aspects of life, as most of the children have
available and some of them have been used for SLE children JIA. QoL measures that have been developed for children
(Duffy, 2005; Duffy et al., 1997; Wright et al., 1994) with with chiefly musculoskeletal involvement may not ade-
PedsQL™ 3.0 RM introduced by Varni et al; (2002) being quately assess all aspects of illness in cSLE. Although physi-
the most popular. In the current work, despite having a total cal function is an important domain affected in SLE, a true
PedsQL™ 3.0 RM score above 70 which is recognized to be measure of SLE-related QoL must take into consideration

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Table 6  Analysis of possible associations of QoL Summary scores with different clinical and laboratory data of SLE patients
Parameter PedsQL™ 4.0 scores PedsQL™ 3.0 RM scores SMILEY
p-value, r* p-value, r p-value, r

Age at enrolment 0.004, − 0.288 0.009, − 0.262 0.004, − 0.286

Age at diagnosis 0.77, − 0.03 0.5, 0.065 0.8, − 0.023
Duration of illness < 0.001, − 0.527 < 0.001, − 0.606 < 0.001, − 0.539
Number of hospital admissions 0.3, − 0.108 0.08, − 0.175 0.004, − 0.289
Number of medications 0.4, − 0.094 0.007, − 0.284 0.002, − 0.32
SLEDAI score
Current 0.001, − 0.34 < 0.001, − 0.4 < 0.001, − 0.453
Cumulative 0.04, − 0.207 0.03, − 0.223 0.01, − 0.257
SDI score < 0.001, − 0.352 < 0.001, − 0.395 < 0.001, − 0.451
p-value (95% CI) p-value (95% CI) p-value (95% CI)
Sex: male vs female 0.2 (3.7 to 2.8) 0.09 (− 0.7- 9.1) 0.44 (− 5.7 to 13.6)
Geographic location: Rural vs urban 0.13 (− 8.6 to 1.13) 0.01 (− 9.5 to − 1.3) 0.008 (− 18.7 to − 2.9)
Family size: below 5 vs above 5 0.7 (− 4.02 to 6.2) 0.3 (2.2 to 2.2) 0.7(− 7.07 to 10)
Renal involvement: nephritis vs non-nephritis 0.5 (− 6.9 to 3.2) 0.2 (− 7.4 to 1.2) 0.01 (− 19.2 to − 2.3)
Arthritis: + ve vs − ve 0.4 (− 7.8 to 3.3) 0.4 (− 2.4 to 6.5) 0.2 (− 3.2 to 15)
CGCS: high vs low 0.002 (2.7 to 11.9) < 0.001 (5.8 to 13.2) 0.001 (5.7 to 21.1)
Obesity yes vs no 0.002 (− 12.3 to − 2.9) < 0.001 (− 13.4 to − 5.8) < 0.001 (− 22 to − 6.4)
Reduced BMD: + ve vs _ve < 0.001 (− 16.6 to − 5.4) < 0.001 (− 14.5 to − 4.8) < 0.001 (− 28.7 to − 10.7)
Alopecia yes vs no 0.9 (− 4.5 to 4.9) 0.7 (− 4.9 to 3.2) 0.02 (− 16.7 to − 1.4)
Hypertension: yes vs no 0.2 (− 9.4 to 2.2) 0.06 (− 9.9 to 0.29) 0.02 (− 21.8 to − 2.3)
Cyclophosphamide use (ever) yes vs no 0.6 (− 5.9 to 3.5) 0.08 (− 7.6 to 0.5) 0.01 (− 17.8 to − 2.4)

PedsQL™ 4 GCS Pediatric Quality of Life Inventory Generic Core Scales, PedsQL™ 3.0 RM the PedsQL™ 3.0 Rheumatology Module, SLE
systemic lupus erythematosus, SD standard deviation, SDI systemic lupus damage index. CGCs cumulative glucocorticoids, SLEDAI SLE dis-
ease activity index, BMD bone mineral density
*r Pearson correlation coefficient
Bold figures are the statistically significant values

other domains of HRQOL and adequately assess the impact Childhood SLE is more frequent in females which is also
of renal and CNS involvement, as well as the effect of medi- spotted in our study and consistent with previous reports
cations (Moorthy et al., 2005). So, SLE-specific QoL tool from our country and others (Brunner et al., 2009; Eid et al.,
titled ­(SMILEY©) was developed by Moorthy et al; (2006) 2021; Ruperto et al., 2004). Moorthy et al. reported female
and have been validated in different languages including gender to be associated with lower QoL scores (Moorthy
Arabic (Moorthy et al., 2006, 2007). Being a disease-spe- et al., 2017), which was not reported in our study. Patients
cific scale, SMILEY has no normative data, so we matched with LN showed lower scores for SMILEY scale compared
our results to previously published SMILEY results from to those without LN, but similar finding was not reported in
different countries as presented in Table 3 which showed the other 2 scales used. This supports the assumption that
variable results in the different domains. The comparatively SMILEY being disease specific has better ability to evalu-
high HRQOL among Asian patients could be due to cultural ate QoL of children with SLE. The relationship of HRQL
factors, family support, provider preferences related to medi- with renal manifestations, which are generally associated
cation choice that led to disease control or differences in with a worse clinical course and prognosis (Petty & Cassidy,
health care systems (Moorthy et al., 2017). Characteristics of 2001), may reflect a tendency for patients with a progressive
patients at time of enrolment in study is also a critical deter- disease to report lower HRQL, even if presented with non-
minant of the questionnaires’ scores. Moorthy et al. (2017) threatening manifestations. The poorer HRQOL in patients
reported the median SLEDAI and SDI scores significantly with renal and CNS involvement could be related to the
lower than our cohort. Also, the Brazilian cohort (Moorthy aggressive immunosuppressive regimens and higher doses of
et al., 2013) had a duration of illness 1–153 months and steroids which change body appearance and lead to impair-
median SLEDAI and SDI scores of 2 and zero respectively ment of self-confidence especially in adolescents (Ruperto
which are lower than the current study. et al., 2004). Patients who received cyclophosphamide had

13
1586 Maternal and Child Health Journal (2023) 27:1578–1588

significantly lower SMILEY score than those who didn’t work. Both generic and disease- or system-specific scales
receive it. These findings are coherent with report of Moor- can be used for its assessment. Collaborative efforts from
thy et al. of 456 children with SLE (Moorthy et al., 2017). pediatrician, rheumatologists, and psychiatrics are urgently
Arthritis which is a common feature in SLE was not associ- required to support those children.
ated with lower scores of the 3 scales used in the current
Supplementary Information The online version contains supplemen-
study. This is against Stevens et al. (2019) who reported tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 10995-0​ 23-0​ 3680-x.
arthritis to be the feature affecting all QoL domains. Syno-
vitis and arthritis are typical features of most pediatric rheu- Author Contribution RE: research hypothesis, obtained questionnaires’
matic disorders, but the localization and the extent of the permission to use, statistical analysis, wrote initial draft, revised, and
approved the final manuscript. AH, NH: research protocol, revised and
joints inflammation and erosions differs. Arthritis in SLE approved the final manuscript, provided medical care to all patients.
has short duration, good response to treatment, erosive MSK, SR: research protocol, guided the questionnaires fulfilment by
arthritis is unusual and only a minority of patients develop patients, revised final manuscript, cardiac assessment of all patients,
deformities which was not reported in any of our patients. revised and approved the final manuscript. AAF, DMAE: research
protocol, guided the questionnaires fulfilment by patients, statistical
Lower disease activity and damage were associated with analysis, and revised and approved final manuscript.
higher QoL scores of the 3 scales (except for daily activi-
ties domain of PedsQL™ 4.0). These findings are consist- Funding Open access funding provided by The Science, Technology &
ent with most of published studies (Brunner et al., 2009; Innovation Funding Authority (STDF) in cooperation with The Egyp-
tian Knowledge Bank (EKB). This research received no funding.
Moorthy et al., 2017; Ruperto et al., 2004) except Jones et al.
(2013) who reported no such correlation that was explained Data Availability Data and material are available upon request.
that traditional measures of cSLE activity do not capture
HRQOL outcomes adequately which may limit achievement Code Availability Non applicable.
of optimal health outcomes with cSLE. However, some fea-
tures and complications of the disease that may also occur
Declarations
in many other chronic illnesses correlated significantly with Conflict of interest The authors declared no potential conflicts of in-
QoL scores of all 3 scales as long duration of illness, high terest concerning the research, authorship, and/or publication of this
CGCS, obesity and decreased BMD. The main characteris- article.
tics and findings of available studies on HRQOL in children Ethical Approval All procedures performed in study were in accord-
with SLE are summarized in Supplementary Table 1. ance with the ethical standards of the institutional and/or national
This study explores for the first time HRQOL in Egyptian research committee and with the 1975 Helsinki declaration and its
children with SLE which was found to be low. Our next later amendments or comparable ethical standards. This study was
reviewed and approved by the local ethical committee (MFM-IRB)
step will be the evaluating parents view of their children (Code: R.21.08.1393).
life quality using the parents’ versions of the questionnaires
used in the study which will add to the overall understanding Informed Consent Informed consent was obtained from all individual
of cSLE Qol in Egyptian youth. Next, Qol assessment will participants included in the study.
be implemented as part of the routine care and follow up of Consent for Publication Not applicable.
those children with a psychiatric/ social worker added to
our pediatric rheumatology/nephrology care team for SLE Open Access This article is licensed under a Creative Commons Attri-
children. Focus should be towards controlling disease activ- bution 4.0 International License, which permits use, sharing, adapta-
ity using lowest doses and durations of medications, close tion, distribution and reproduction in any medium or format, as long
monitoring of organ involvements and life quality scores. as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
Limitations of the current work is being a single center were made. The images or other third party material in this article are
study, the lack of reference normative Egyptian data for the included in the article's Creative Commons licence, unless indicated
PedsQL™ 3.0 RM and the need for follow up evaluation of otherwise in a credit line to the material. If material is not included in
HRQOL scores changes over longer follow up duration and the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
the evaluation of family impact scores. need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.

Conclusion References
Quality of life assessment in Egyptian children with SLE is Brunner, H. I., & Giannini, E. H. (2003). Health-related quality of
not yet included as a part of the standard care provided to life in children with rheumatic diseases. Current Opinion in
these children despite being low as evaluated in the current

13
Maternal and Child Health Journal (2023) 27:1578–1588 1587

Rheumatology, 15(5), 602–612. https://​doi.​org/​10.​1097/​00002​ Gladman, D. D., Ibañez, D., & Urowitz, M. B. (2002). Systemic lupus
281-​20030​9000-​00014 erythematosus disease activity index 2000. The Journal of Rheu-
Brunner, H. I., Klein-Gitelman, M. S., Miller, M. J., Trombley, M., matology, 29(2), 288–291.
Baldwin, N., Kress, A., Johnson, A. L., Barron, A. C., Griffin, T. Hersh, A. O., von Scheven, E., Yazdany, J., Panopalis, P., Trupin, L.,
A., Passo, M. H., & Lovell, D. J. (2004). Health of children with Julian, L., Hersh, A. O., von Scheven, E., Yazdany, J., Panopalis,
chronic arthritis: Relationship of different measures and the qual- P., Trupin, L., Julian, L., Katz, P., Criswell, L. A., & Yelin, E.
ity of parent proxy reporting. Arthritis and Rheumatism, 51(5), (2009). Differences in long-term disease activity and treatment
763–773. https://​doi.​org/​10.​1002/​art.​20689 of adult patients with childhood- and adult-onset systemic lupus
Brunner, H. I., Gladman, D. D., Ibañez, D., Urowitz, M. D., & Sil- erythematosus. Arthritis and Rheumatism, 61(1), 13–20. https://​
verman, E. D. (2008). Difference in disease features between doi.​org/​10.​1002/​art.​24091
childhood-onset and adult-onset systemic lupus erythematosus. Hochberg, M. C. (1997). Updating the American College of Rheu-
Arthritis and Rheumatism, 58(2), 556–562. https://​doi.​org/​10.​ matology revised criteria for the classification of systemic lupus
1002/​art.​23204 erythematosus. Arthritis and Rheumatism, 40(9), 1725. https://​
Brunner, H. I., Higgins, G. C., Wiers, K., Lapidus, S. K., Olson, J. C., doi.​org/​10.​1002/​art.​17804​00928
Onel, K., Punaro, M., Ying, J., Klein-Gitelman, M. S., & Seid, M. Houghton, K. M., Tucker, L. B., Potts, J. E., & McKenzie, D. C. (2008).
(2009). Health-related quality of life and its relationship to patient Fitness, fatigue, disease activity, and quality of life in pediatric
disease course in childhood-onset systemic lupus erythematosus. lupus. Arthritis and Rheumatism, 59(4), 537–545. https://​doi.​org/​
The Journal of Rheumatology, 36(7), 1536–1545. https://​doi.​org/​ 10.​1002/​art.​23534
10.​3899/​jrheum.​081164 Jones, J. T., Nelson, S. L., Wootton, J., Liberio, B., Greenler, A. J.,
Duffy, C. M. (2005). Measurement of health status, functional status, Huggins, J. L., Huggins, J. L., Schanberg, L. E., & Brunner, H.
and quality of life in children with juvenile idiopathic arthritis: (2013). Level and Determinants of Health-Related Quality of Life
Clinical science for the pediatrician. Pediatric Clinics of North in Childhood-Onset Systemic Lupus Erythematosus, [Abstract
America, 52(2), 359–v. https://​doi.​org/​10.​1016/j.​pcl.​2005.​01.​009 844]: 2013 ACR/ARHP Annual Meeting.
Duffy, C. M., Arsenault, L., Duffy, K. N., Paquin, J. D., & Strawczyn- Levy, D. M., Peschken, C. A., Tucker, L. B., Chédeville, G., Huber, A.
ski, H. (1997). The juvenile arthritis quality of life questionnaire– M., Pope, J. E., Canadian Network for Improved Outcomes in SLE
development of a new responsive index for juvenile rheumatoid (CaNIOS) 1000 Faces Investigators, & Silverman, E. D. (2014).
arthritis and juvenile spondyloarthritides. The Journal of Rheu- Association of health-related quality of life in childhood-onset
matology, 24(4), 738–746. systemic lupus erythematosus with ethnicity: results from a mul-
Eesa, N. N., Abdel Nabi, H., Owaidy, R. E., Khalifa, I., Radwan, A. tiethnic multicenter Canadian cohort. Arthritis Care & Research,
R., NourEl-Din, A. M., Amer, M. A., ElShereef, R. R., Hassan, 66(12), 1767–1774. https://​doi.​org/​10.​1002/​acr.​22363
E., Ismail, F., El-Gazzar, I. I., Khalil, N. M., Moshrif, A. H., Massias, J. S., Smith, E. M., Al-Abadi, E., Armon, K., Bailey, K., Ciur-
Abualfadl, E., Tharwat, S., Fathi, H. M., Abd Elazeem, M. I., tin, C., Davidson, J., Gardner-Medwin, J., Haslam, K., Hawley,
El-Shebini, E., Samy, N., … Egyptian College of Rheumatology D. P., Leahy, A., Leone, V., McErlane, F., Mewar, D., Modgil,
(ECR) SLE Study Group. (2021). Systemic lupus erythematosus G., Moots, R., Pilkington, C., Ramanan, A. V., Rangaraj, S., …
children in Egypt: Homeland spectrum amid the global situation. Hedrich, C. M. (2021). Clinical and laboratory phenotypes in
Lupus, 30(13), 2135–2143. https://​doi.​org/​10.​1177/​09612​03321​ juvenile-onset systemic lupus erythematosus across ethnicities in
10430​10 the UK. Lupus, 30(4), 597–607. https://​doi.​org/​10.​1177/​09612​
Eid, R., Fathy, A. A., & Hamdy, N. (2020). Health-related quality 03320​984251
of life in Egyptian children with nephrotic syndrome. Quality Miller, M. L., LeBovidge, J., & Feldman, B. (2002). Health-related
of Life Research, 29(8), 2185–2196. https://​doi.​org/​10.​1007/​ quality of life in children with arthritis. Rheumatic Diseases
s11136-​020-​02438-0 Clinics of North America, 28(3), 493–vi. https://​doi.​org/​10.​1016/​
Eid, R., Hammad, A., Abdelsalam, M., Fathy, A. A., Abd-El Ghafaar, s0889-​857x(02)​00019-4
D. M., Elmarghany, E. B., El-Hanafy, A. A., Mostafa, N., Niazey, Mina, R., & Brunner, H. I. (2010). Pediatric lupus–are there differences
N. A., Korkor, M. S., & Hamdy, N. (2021). Tumor necrosis fac- in presentation, genetics, response to therapy, and damage accrual
tor receptor II and PTPN22 genes polymorphisms and the risk of compared with adult lupus? Rheumatic Diseases Clinics of North
systemic lupus erythematosus in Egyptian children. Lupus, 30(9), America, 36(1), 53–viii. https://d​ oi.o​ rg/1​ 0.1​ 016/j.r​ dc.2​ 009.1​ 2.0​ 12
1449–1458. https://​doi.​org/​10.​1177/​09612​03321​10203​59 Moorthy, L. N., Peterson, M., Onel, K. B., Harrison, M. J., & Lehman,
Elmougy, A., Sarhan, A., Hammad, A., El-Refaey, A., Zedan, M., Eid, T. J. (2005). Quality of life in children with systemic lupus erythe-
R., Laimon, W., Elrahman, A. A., Elhussieni, F., El-Sherbeny, matosus. Current Rheumatology Reports, 7(6), 447–452. https://​
E., & Bakr, A. (2015). Erratum to: Lupus nephritis in Egyptian doi.​org/​10.​1007/​s11926-​005-​0049-0
children: A 16-year experience. Journal of Nephrology, 28(1), Moorthy, L. N., Peterson, M. G., Baratelli, M., Harrison, M. J., Onel,
131. https://​doi.​org/​10.​1007/​s40620-​014-​0170-0 K. B., Chalom, E. C., Haines, K., Hashkes, P. J., & Lehman, T. J.
El-Ziny, M. A., Al-Tonbary, Y. A., Salama, O. S., Bakr, A., Al-Marsa- (2006). Simple Measure of The Impact of Lupus Erythematosus
fawy, H., & Elsharkawy, A. A. (2007). Low bone mass in children In Youngsters (SMILEY): Validity, internal consistency and test-
with malignant lymphoma. Pediatric Hematology and Oncology, retest reliability. Arthritis and Rheumatism, 54(9), S162.
24(8), 577–585. https://​doi.​org/​10.​1080/​08880​01070​16402​75 Moorthy, L. N., Peterson, M. G., Baratelli, M., Harrison, M. J., Onel,
Gladman, D., Ginzler, E., Goldsmith, C., Fortin, P., Liang, M., Urow- K. B., Chalom, E. C., Haines, K., Hashkes, P. J., & Lehman, T.
itz, M., Bacon, P., Bombardieri, S., Hanly, J., Hay, E., Isenberg, J. (2007). Multicenter validation of a new quality of life measure
D., Jones, J., Kalunian, K., Maddison, P., Nived, O., Petri, M., in pediatric lupus. Arthritis and Rheumatism, 57(7), 1165–1173.
Richter, M., Sanchez-Guerrero, J., Snaith, M., … Zoma, A. https://​doi.​org/​10.​1002/​art.​22988
(1996). The development and initial validation of the Systemic Moorthy, L. N., Peterson, M. G., Hassett, A. L., Baratelli, M., Chalom,
Lupus International Collaborating Clinics/American College of E. C., Hashkes, P. J., Hong, S., Reiff, A., & Lehman, T. J. (2009).
Rheumatology damage index for systemic lupus erythematosus. Relationship between health-related quality of life and SLE activ-
Arthritis and Rheumatism, 39(3), 363–369. https://​doi.​org/​10.​ ity and damage in children over time. Lupus, 18(7), 622–629.
1002/​art.​17803​90303 https://​doi.​org/​10.​1177/​09612​03308​101718

13
1588 Maternal and Child Health Journal (2023) 27:1578–1588

Moorthy, L. N., Saad-Magalhães, C., Sato, J. O., Len, C. A., Vasco, erythematosus and its relationship to disease activity and dam-
M. B., Appenzeller, S., Marini, R., Oliveira, S. K., Rodrigues, age. Arthritis and Rheumatism, 51(3), 458–464. https://​doi.​org/​
M., Sztajnbok, F., Almeida, R. G., Jesus, A. A., Campos, L. M., 10.​1002/​art.​20412
Silva, C. A., Peterson, M. G., Hassett, A. L., Weiss, E., Verma, Stevens, B., Rodriguez, M., Rakestraw, A., & O’neil, K. (2019).
S., Dahodwala, M. Q., & Lehman, T. J. (2013). Validation of the SAT0477 quality of life in subjects with pre-pubertal onset
Portuguese Simple Measure of Impact of Lupus Erythematosus in systemic lupus erythematosus. Annals of the Rheumatic, 78,
Youngsters (SMILEY) in Brazil. Lupus, 22(2), 190–197. https://​ 1326–1327.
doi.​org/​10.​1177/​09612​03312​470185 Thumboo, J., & Strand, V. (2007). Health-related quality of life in
Moorthy, L. N., Baldino, M. E., Kurra, V., Puwar, D., Llanos, A., Peter- patients with systemic lupus erythematosus: An update. Annals of
son, M. G., Hassett, A. L., Lehman, T. J., International SMILEY© the Academy of Medicine, Singapore, 36(2), 115–122.
Collaborative group. (2017). Relationship between health-related Varni, J. W., Burwinkle, T. M., Seid, M., & Skarr, D. (2003). The Ped-
quality of life, disease activity and disease damage in a prospec- sQL 4.0 as a pediatric population health measure: feasibility, reli-
tive international multicenter cohort of childhood onset systemic ability, and validity. Ambulatory Pediatrics: the Official Journal of
lupus erythematosus patients. Lupus, 26(3), 255–265. https://​doi.​ the Ambulatory Pediatric Association, 3(6), 329–341. https://​doi.​
org/​10.​1177/​09612​03316​659546 org/​10.​1367/​1539-​4409(2003)​003%​3c0329:​tpaapp%​3e2.0.​co;2
Petty, R. E., & Cassidy, J. T. (2001). Systemic lupus erythematosus. In Varni, J. W., Seid, M., & Kurtin, P. S. (2001). PedsQL 4.0: reliability
J. T. Cassidy & R. E. Petty (Eds.), Textbook of pediatric rheuma- and validity of the pediatric quality of life inventory version 4.0
tology (4th ed., pp. 396–449). WB Saunders. generic core scales in healthy and patient populations. Medical
Putera, A. M., Irwanto, I., Maramis, M. M., Prasetyo, R. V., Soemyarso, Care, 39(8), 800–812. https://​doi.​org/​10.​1097/​00005​650-​20010​
N. A., & Noer, M. S. (2020). Effect of mental health problems on 8000-​00006
the quality of life in children with lupus nephritis. Neuropsychi- Varni, J. W., Seid, M., Smith Knight, T., Burwinkle, T., Brown, J., &
atric Disease and Treatment, 16, 1583–1593. https://​doi.​org/​10.​ Szer, I. S. (2002). The PedsQL in pediatric rheumatology: Reli-
2147/​NDT.​S2503​73 ability, validity, and responsiveness of the pediatric quality of life
Ravelli, A., Ruperto, N., & Martini, A. (2005). Outcome in juvenile inventory generic core scales and rheumatology module. Arthri-
onset systemic lupus erythematosus. Current Opinion in Rheu- tis and Rheumatism, 46(3), 714–725. https://​doi.​org/​10.​1002/​art.​
matology, 17(5), 568–573. https://​doi.​org/​10.​1097/​01.​bor.​00001​ 10095
69364.​69066.​1e Wright, F. V., Law, M., Crombie, V., Goldsmith, C. H., & Dent, P.
Rogers, J., Sagcal-Gironella, A. C. P., Rosillo, P., Ramirez, A. A., (1994). Development of a self-report functional status index for
Banuelos, R., & de Guzman, M. M. (2017). A single center review juvenile rheumatoid arthritis. The Journal of Rheumatology,
of health-related quality of life in children with systemic lupus 21(3), 536–544.
erythematosus using the pediatric quality of life inventory version
4.0 generic core scale. Arthritis & Rheumatology, 69(4), 223–224. Publisher's Note Springer Nature remains neutral with regard to
Ruperto, N., Buratti, S., Duarte-Salazar, C., Pistorio, A., Reiff, A., jurisdictional claims in published maps and institutional affiliations.
Bernstein, B., Maldonado-Velázquez, M. R., Beristain-Manter-
ola, R., Maeno, N., Takei, S., Falcini, F., Lepore, L., Spencer,
C. H., Pratsidou-Gertsi, P., Martini, A., & Ravelli, A. (2004).
Health-related quality of life in juvenile-onset systemic lupus

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