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TYPE Original Research

PUBLISHED 12 June 2023
DOI 10.3389/fped.2023.1164099

Risk factors associated with

recurrence of Henoch–Schonlein
EDITED BY
Erkan Demirkaya,
Western University, Canada
purpura: a retrospective study
REVIEWED BY
Emanuele Micaglio,
Tongtong Cao, Hui-min Yang, Jing Huang and Yan Hu*
IRCCS San Donato Polyclinic, Italy Department of Traditional Chinese Medicine, Beijing Children’s Hospital, Capital Medical University,
David Piskin, National Center for Children’s Health, Beijing, China
Lawson Health Research Institute, Canada

*CORRESPONDENCE Background: Recurrence is considered a vital problem for assessing the prognosis
Yan Hu
of Henoch–Schonlein purpura (HSP). The objective of this study was to evaluate
[email protected]
factors affecting the recurrence in children with HSP.
RECEIVED 12 February 2023
Methods: We retrospectively reviewed records of 368 patients under the age of 16
ACCEPTED 18 May 2023
PUBLISHED 12 June 2023 years diagnosed with HSP from October 2019 to December 2020 in Beijing
Children’s Hospital. Patients were divided into a non-recurrence group and a
CITATION
Cao T, Yang H-m, Huang J and Hu Y (2023) Risk recurrence group according to whether there was a recurrence. Incidence of
factors associated with recurrence of Henoch– manifestation, possible cause, age, and treatment were retrospectively analyzed.
Schonlein purpura: a retrospective study. Univariate and multivariate logistic regression analyses were used to determine
Front. Pediatr. 11:1164099. the risk factors of recurrence in HSP.
doi: 10.3389/fped.2023.1164099
Results: Percentages of patients were 65.2% for the non-recurrence group and
COPYRIGHT
34.8% for the recurrence group. The percentage of patients with renal
© 2023 Cao, Yang, Huang and Hu. This is an
open-access article distributed under the terms involvement was significantly higher in the recurrence group (40.6%) than in the
of the Creative Commons Attribution License non-recurrence group (26.3%). Respiratory tract infection was the most frequent
(CC BY). The use, distribution or reproduction in trigger: 67.5% in the non-recurrence group and 66.4% in the recurrence group.
other forums is permitted, provided the original
author(s) and the copyright owner(s) are Recurrence was more likely to occur in patients aged >6 years (53.3% vs. 71.9%).
credited and that the original publication in this Logistic regression analysis revealed that hematuria plus proteinuria was an
journal is cited, in accordance with accepted independent risk factor for the recurrence of HSP. Conversely, animal protein,
academic practice. No use, distribution or
reproduction is permitted which does not exercise restriction, and age ≤6 years were independent favorable factors for the
comply with these terms. non-recurrence of HSP.
Conclusion: These results suggest that organ involvement, exercise, and diet
management during the initial episode of HSP should be strictly monitored for
children with HSP. Adequate clinical intervention for these risk factors may limit
or prevent HSP recurrence. Moreover, renal involvement is associated with the
long-term prognosis of HSP.

KEYWORDS

pediatric HSP, recurrence, risk factor, renal involvement, retrospective study

Background
Henoch–Schönlein purpura (HSP) is the most common vasculitis in children, with an
incidence of 20/100,000 children annually (1), and is diagnosed when palpable purpura is
present plus one of the following: biopsy showing predominant immunoglobulin A (IgA)
deposition, arthralgia/ arthritis, abdominal cramping pain, and hematuria/proteinuria (2).
HSP is considered a self-limiting disease. However, it is exceedingly subject to relapse and
its recurrence is difficult to prevent. Approximately 40%–50% of patients present renal
involvement and aggravate refractory HSP cases (3).
Though the exact pathogenic mechanisms of HSP are still obscure, previous studies focus
on the role of several factors in predicting the recurrence of HSP. According to the statistics,
approximately 30%–40% of patients with HSP have at least one recurrence during a 2-year

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Cao et al. 10.3389/fped.2023.1164099

period after the first outbreak (4). Numerous studies suggested that strenuous exercise until complete remission, including without
HSP might be associated with infection, whereas it has been stated rash, abdominal pain, or renal involvement.
that other factors, such as persistent rash, abdominal pain,
proteinuria, hematuria, and some pathogenic microorganism, are
significantly related to the recurrence of HSP (5). However, the Data collection and statistical analysis
prediction of recurrence in children has not been clearly
defined yet. We retrieved the data, including age, sex, onset seasons, family
history, diet history, infection, exercise, and organ involvement.
These data were obtained from the outpatient and inpatient
Methods department. Statistical analysis was performed with the Prism
software for personal computers. All continuous variables were
Patients tested for normality. Results were expressed as mean ± standard
deviation or as median and range or interquartile range (IQR) as
We retrospectively reviewed the records of 368 children with appropriate. Student’s t-test or Mann–Whitney U-test was used
HSP who were regularly consulted at Beijing Children’s Hospital to compare continuous variables and the χ 2 test for categorical
from October 2019 to December 2020. The patients had been variables. Multiple logistic regression analyses were conducted to
diagnosed with HSP according to the 2010 European League identify the independent predictors of recurrent HSP. A p-value
Against Rheumatism/Pediatric Rheumatology International Trials < 0.05 was considered statistically significant in all the calculations.
Organization/Pediatric Rheumatology European Society (EULAR/
PRINTO/PRES) criteria, were aged from 3 to 16 years and had
medical history >1 year included. Most cases were diagnosed
Results
with typical clinical manifestation based on the classical
diagnosis criteria, whereas some cases with HSP were confirmed Recurrent rate and clinical manifestations
by skin biopsy. Patients with skin rashes caused by other diseases
combined with severe organ damage were excluded. Cases with A total of 368 children aged <16 years with a diagnosis of HSP
missing key data were excluded. We conducted follow-up visits were enrolled in this retrospective study between October 2019 and
through outpatient visits and telephone contact. The follow-up December 2020. The clinical characteristics of all patients are
period was 1 year. Patients with renal involvement and urine summarized in Table 1. There were 171 girls and 197 boys. The
protein of more than 20 mg/kg/24 h and/or 20 red blood cells female-to-male ratio was 0.86 (46.5% female subjects and 53.5%
per high power field in the first onset were also excluded. male subjects). All patients were divided into non-recurrence and
Recurrence was defined as the presence of a fresh episode after at recurrence groups based on relapse/recurrence. The percentage of
least 3 months without signs or symptoms (6). No recurrence male/female patients showed no significant difference between
was defined as a patient previously diagnosed with HSP who was the two groups (Table 1).
in complete remission, including without rash, abdominal pain, The percentage of patients with non-recurrence was 65.2%
or renal involvement for six months from the previous episode. (240/368) for the non-recurrence group and 34.8% (128/368)
The patients with severe gastrointestinal involvement were given for the recurrence group. The percentage of patients with only
low-dose steroid treatment, and those with renal involvement skin lesions was 23.3% (56/240) for the non-recurrence group
were administered corresponding treatment. The patients were
provided with symptomatic and history support.
TABLE 1 Recurrence rate and clinical manifestations.
The epidemiological characteristics and demographic data,
including age, sex, onset seasons, family history, diet history, Total (n = 368) χ2 p-value
infection, exercise, and organ involvement, were retrieved.
NR R
Prescribed medications, including corticosteroids and (n = 240) (n = 128)
immunosuppressors, were also recorded. Joint involvement was Male sex 130 67 0.112 0.738
described as joint pain. Gastrointestinal involvement was defined Skin purpura only 56 21 2.421 0.120
as the presence of small bowel angina and postprandial Arthralgia/arthritis 94 32 7.855 0.005
abdominal pain in the context of the clinical duration of GI involvement 110 39 8.179 0.004
vasculitis. Edema and sub-mucosal and intramural hemorrhage Small bowel angina 103 35 8.638 0.003
Postprandial abdominal pain 34 11 2.416 0.120
under B-model ultrasonic were also defined as gastrointestinal
Edema and sub-mucosal 28 12 0.453 0.501
involvement. Renal involvement was defined as hematuria and/or and intramural hemorrhage
proteinuria. Hematuria was defined by the presence of at least Renal involvement 63 52 8.542 0.003
five red blood cells per high-power field. Proteinuria was defined Proteinuria 18 13 0.764 0.382
as protein loss of more than 0.3 g per 24 h. Diet restriction was Hematuria 8 6 0.418 0.518
prescribed; patients were recommended an animal protein-free Hematuria plus proteinuria 37 33 6.369 0.012
Renal plus GI 58 38 1.320 0.251
diet before the rash completely disappeared. Exercise restriction
was also prescribed; patients were recommended to avoid GI, gastrointestinal; NR, non-recurrence group; R, recurrent group.

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Cao et al. 10.3389/fped.2023.1164099

and 16.4% (21/128) for the recurrence group. The percentage of Renal involvement in different age groups
patients with arthralgia or arthritis was 39.2% (94/240) for the
non-recurrence group, but it decreased in the recurrence Table 3 shows similar proportions for age groups among 240
group (25%; 32/128). Gastrointestinal involvement was patients without renal involvement in the non-recurrence group
observed in 110 (110/240; 45.8%) patients in the non- (≤6 years old, 112/240, 46.6%; >6 years old, 128/240, 53.3%).
recurrence group, and it significantly decreased in the However, it showed recurrence is more frequent in older patients
recurrence group (39/128; 30.5%). The percentage of patients (≤6 years old, 36/128, 28.1%; >6 years old, 92/128, 71.9%).
with renal involvement was 26.3% (63/240) for the non- Furthermore, among 63 patients with renal involvement in the
recurrence group and 40.6% (52/128) for the recurrence group. non-recurrence group, older patients were more likely to have
More specifically, the percentage of patients with renal and renal involvement: ≤6 years old, 12/63, 19% and >6 years old,
gastrointestinal involvement was 24.2% (58/240) for the non- 51/63, 80.9%. There was a similar trend among 52 patients with
recurrence group and 29.6% (38/128) for the recurrence group; renal involvement in the recurrence group: ≤6 years old, 16/52,
there was no significant difference between the two groups 30.8% and >6 years old, 36/52, 69.2% (Table 3).
(Table 1).

Treatment
Possible cause
The treatment of HSP is shown in Table 4. Patients without
In the non-recurrence group, 144 (60%) patients occurred organ involvement were given symptomatic relief. The patients
with HSP in autumn and winter, and it was also high season with severe gastrointestinal involvement were administered low-
for the recurred patients (73/128; 57%) in the recurrence dose glucocorticoid treatment (1–2 mg/kg·day). Glucocorticoid
group). The upper respiratory tract infection (such as was administered to 99 patients (99/240; 41.2%) in the non-
pharyngalgia, fever, and cough) rate showed a similar pattern: recurrence group, and it was much less in the recurrence group
162/240; 67.5% in the non-recurrence group and 85/128 66.4% (45/128; 35.2%), but there was no statistical difference. In the
in the recurrence group. Moreover, it showed that pharyngalgia non-recurrence group, 10 patients (10/240; 4.2%) received
was the most frequent symptom of the upper respiratory tract immunoglobulin, but only 4 patients (4/128; 3.1%) with
among the two groups: 145/240; 60.4% in the non-recurrence recurrence were given this treatment.
group and 73/128; 57% in the recurrence group. Besides All patients were given a prescription for an animal protein-
respiratory tract infection,17 patients (17/240; 7%) had an restrictive diet and exercise restriction until the rash completely
allergy, 14 patients (14/240; 5.8%) had taken a vaccine, and 2 disappeared. There was better compliance with the animal
patients (2/240; 0.8%) had an injury in the non-recurrence protein restriction diet in the non-recurrence group (186/240;
group. In the recurrence group, 12 patients (12/128; 9.4%) had 77.5%) than in the recurrence group (53/128; 41.4%). The non-
an allergy, 8 patients (8/128; 6.3%) received vaccination, and no recurrence group also complied better with the exercise
patients had an injury. It was suggested to all patients that they restrictions (197/240; 82.1%) than the recurrence group (42/128;
avoid vaccination for at least 1 year after fully recovering. 32.8%).
However, unknown causes were found in 45 patients (45/240;
18.7%) in the non-recurrence group and in 23 patients (23/ TABLE 3 Renal involvement in different age groups for HSP.
128;17.9%) in the recurrence group. There were no significant
differences between the two groups for seasons and possible Without RI RI
causes (Table 2). NR R NR R
Age
≤6years 112 36 12 16
TABLE 2 Seasons and possible causes for HSP. >6years 128 92 51 36
χ2 11.937 2.215
NR (n = 240) R (n = 128) χ2 p-value p-value 0.001 0.145
Onset seasons NR, non-recurrence group; R, recurrent group; RI, renal involvement.
Autumn and winter 144 73 0.304 0.581
RI 162 85 0.045 0.832
Fever 14 8 0.026 0.872 TABLE 4 Treatment for HSP.
Cough 43 23 0.000 0.990
Pharyngalgia 144 73 0.304 0.581 NR (n = 240) R (n = 128) χ2 p-value
Allergy 17 12 0.604 0.437 APR 186 53 47.769 <0.001
Vaccination 14 8 0.026 0.872 ER 197 42 89.015 <0.001
Injury 2 0 0.000 1.000 GC 99 45 1.301 0.254
Unknown cause 45 23 0.034 0.854 IP 10 4 0.045 0.833

GI, gastrointestinal; NR, non-recurrence group; R, recurrent group; RI, respiratory NR, non-recurrence group; R, recurrent group; APR, animal protein restriction; ER,
tract infection. exercise restriction; GC, glucocorticoid; IP, immunoglobulin and plasma.

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Possible risk factors for recurrence The manifestation of recurrent HSP is quite variable in
childhood (10) and the exact incidence of the variable types in
After multivariate logistic regression analysis, animal protein- children with HSP is rarely reported. Some studies reported the
restrictive diet (OR = −0.439; 95% CI: 0.241–0.798; p = 0.007), percentage of recurrent HSP but rarely reported the exact types
exercise restriction (OR = 0.155; 95% CI: 0.086–0.280; p < 0.001), (11). Significant differences probably resulted from the recruited
age ≤ 6 years (OR = 0.483; 95% CI: 0.272–0.856; p = 0.013) were patients in different studies. We reviewed the patients with
the protective factors for the recurrence of HSP. Conversely, the various manifestations, including joint, gastrointestinal, and renal
initial onset with hematuria plus proteinuria was found to be an involvement. Renal involvement has been reported in 20%–50%
independent risk factor for the recurrence of HSP (OR = 10.342; of children with HSP. Our study suggested renal damage had a
95% CI: 3.772–28.354; p < 0.001) (Table 5). higher recurrence rate than other manifestations, such as rash,
arthralgia or arthritis, and gastrointestinal involvement. In the
present study, the frequency of HSP was concluded to be 40.6%
in the recurrence group and 26.3% in the non-recurrence group.
Discussion
Moreover, our results suggested that renal involvement recurred
more frequently relative to joint and gastrointestinal involvement.
HSP is an immune complex-mediated and self-limiting
In addition, our study indicated that renal involvement should be
vasculitis in childhood, which affects small vessels of the skin,
considered a crucial monitoring index in patients with HSP.
joints, gastrointestinal system, and kidneys. Patients with HSP may
At the time of the diagnosis of HSP, most patients presented with
exhibit different manifestations and organ involvement (7). Studies
skin lesions and additional symptoms, including joint,
have focused on the possible risk factors in patients with HSP and
gastrointestinal, and renal involvement. As opposed to the predictor
its recurrence. However, the exact risk factors in patients with
factors found, Prais D (12) reported that no clinical or laboratory
different organ involvement and the recurrence of HSP have not
characteristics were discovered to be a risk factor for predicting
been illustrated yet (8). Therefore, this study aimed to evaluate the
recurrence. This finding probably resulted from different definitions
characteristic type of HSP and the possible risk factor in the
of recurrence and recruited patient selection. In the present study,
recurrence of HSP. Moreover, it also assessed the relationship
initial onset with renal damage was an independent risk factor for the
between clinical features and the occurrence of HSP.
recurrence of HSP. It has also been reported that urine protein
Our recent study analyzed the recurrence risk factor by following
positivity is a risk factor for HSP recurrence (13). Therefore, there is a
up with 368 patients with HSP who were regularly consulted from
need for continuous monitoring and high attention in the case of
October 2019 to December 2020. Results showed that the
kidney damage occurrence. Consistent with previous data (14, 15),
infections were subjected to an obvious increase in patients with
the history of previous infections in our study was found to be related
HSP compared with other causes. Renal involvement has also
to the occurrence of HSP. We speculate that the reason may be that
been shown to be involved in the recurrence of HSP. In
children with upper respiratory tract infections produce a variety of
accordance with other studies, the present study showed similar
inflammatory mediators that change the immune balance of the
clinical characteristics of HSP with skin lesions.
body, easily leading to the occurrence of HSP.
Our study showed that, in the non-recurrence group, presentation
Moreover, exercise restriction was found to be a protective factor
with skin lesions only was 23.3%, skin plus joint was 39.2%, skin plus
for recurrent HSP. Histopathological features of HSP are leukocytic
gastrointestinal involvement was 45.8%, and renal involvement was
vasculitis of arterioles (16). Although few studies have focused on the
26.3%. The frequency of HSP patients with gastrointestinal and renal
relationship between exercise and HSP recurrence, it is not hard to
involvement was much higher in our study. It is probable that
speculate frequent and intense exercise accelerates the relaxation and
patients with HSP who presented skin lesions only usually received
contraction of small blood vessels between muscle tissues, increases
treatment in local hospitals, but patients with gastrointestinal or renal
the risk of capillary damage, and is prone to recurrence of HSP.
injuries attended our hospital for treatment. Thus, this might explain
Therefore, in the clinical treatment of HSP, children should also pay
the percentage of different types of HSP in our center. In this study,
attention to controlling their exercise intensity. However, excessive
the recurrence rate of HSP in children was 34.7% (128/368), which
restriction of physical activity will result in a decline in the immunity
was close to that reported in recent studies (33% recurrence rate),
of children and increase the susceptibility of the body. Therefore,
suggesting that the recurrence rate of HSP in children is high (9).
further research is needed to achieve a balance between exercise and
Therefore, it is beneficial to guide the clinical treatment of children,
immunity.
reduce the recurrence rate, and improve the prognosis.

TABLE 5 Possible risk factors for recurrence.

Risk factor β value SE value Wald value p-value OR value 95% CI

HPP 2.336 0.515 20.613 <0.001 10.342 3.772–28.354
Age ≤6 −0.729 0.293 6.196 0.013 0.483 0.272–0.856
APR −0.824 0.305 7.286 0.007 0.439 0.241–0.798
ER −1.865 0.302 38.205 <0.001 0.155 0.086–0.280

HPP, hematuria plus proteinuria; APR, animal protein restriction; ER, exercise restriction.

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In our experience of clinical treatment of purpura, an animal Ethics statement

protein restrictive diet is warranted, especially if a rash is present.
The cutoff point for animal protein restriction is usually suggested All data concerning personal information has been allowed for
until the rash completely disappears. Our study discovered better publication by all participants.
compliance with the animal protein-restrictive diet in the non-
recurrence group (186/240; 77.5%) than in the recurrence group
(53/128; 41.4%). Our results suggested that an animal protein-
restrictive diet was an independent protective factor for recurrent Author contributions
HSP. However, most of the recurrence patients did not follow the
doctor’s instructions. In addition, many parents chose to maintain TC collected the data and wrote the paper draft. YH and JH
the animal protein restrictive diet for a long time even after rashes corrected the draft. TC and H-mY completed the statistical
had disappeared, resulting in malnutrition. Moreover, there are analysis. TC was the first author. YH and JH were the
few studies on the relationship between diet and HSP recurrence. corresponding authors. All data were generated in-house, and no
We hope that further perspective multi-center studies will consider paper mill was used. All authors contributed to the article and
the role of diet management for patients with HSP. approved the submitted version.
In this study, the onset age was significantly higher in patients
aged over 6 years in the recurrence group. We discovered a small
proportion of HSP with renal involvement in patients aged <6
years. Furthermore, age ≤6 years was also an independent Funding
protective factor for recurrent HSP. Reasons for discrepancies in
patients with different age groups could be partially associated The authors disclosed receipt of the following financial support
with special immune states in different age groups. Therefore, it for the research, authorship, and/or publication of this article: the
is significant to research immunological mechanisms in different study was sponsored by Beijing Regional Traditional Chinese
age groups in patients with HSP. Medicine (Specialty) Diagnosis and Treatment Center
We included patients with various manifestations, including Construction Project (2018-7-12), Beijing Outstanding Talent
rash, joint pain, gastrointestinal involvement, and renal injury, in Backbone Project (2018000021469G276), and Beijing Traditional
the present study. However, several limitations might be seen in Chinese Medicine Science and Technology Development Fund
the present study. First, all cases came only from one center, so Project (JJ-2020-54).
the study population was a small sample size, and our center
received mostly patients with severe manifestations, hence
resulting in uneven case distribution. In addition, we suggested
that appropriate exercise and diet restrictions for patients with Conflict of interest
HSP could decrease the recurrence of HSP. However, we did not
determine how long the restriction should last; there is a need The authors declare that the research was conducted in the
for further prospective studies to define a specific point in time. absence of any commercial or financial relationships that could
We suggested renal involvement could be an independent risk be construed as a potential conflict of interest.
factor for the recurrence of HSP, and renal involvement recurred
more frequently than other types of HSP. This finding confirms
that patients with HSP need preventative treatment for renal
involvement. Further controlled clinical studies in a large Publisher’s note
population and multi-center follow-up should be considered.
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
Data availability statement organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
The original contributions presented in the study are included in the claim that may be made by its manufacturer, is not guaranteed
article, further inquiries can be directed to the corresponding author. or endorsed by the publisher.

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