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\begin{document}

\title{Childhood allergy symptoms increase the risk of behavioral problems: A
cross-sectional study}



\author[1]{Chikae Yamaguchi}%
\author[2]{Takeshi Ebara}%
\author[3]{Masaki Futamura}%
\author[4]{Yukihiro Ohya}%
\author[5]{Ｍidori Asano}%
\affil[1]{Nagoya City University Graduate School of Nursing}%
\affil[2]{Nagoya City University Graduate School of Medical Sciences and Medical School}%
\affil[3]{National Hospital Organization Nagoya Medical Center}%
\affil[4]{National Center for Child Health and Development}%
\affil[5]{Nagoya University Graduate School of Medicine}%


\vspace{-1em}



  
  \date{May 24, 2024}


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\selectlanguage{english}
\begin{abstract}
Background: Children with allergic symptoms tend to have behavioral or
emotional problems. However, previous studies on this association did
not control for factors such as parenting stress, demographic
characteristics, or allergy presentation. This study aimed to
investigate the relationship between childhood allergic symptoms and
behavioral problems, adjusted for confounders such as demographic
characteristics, parenting stress, and allergy-related variables.
Methods: We conducted an online cross-sectional survey among caregivers
of children aged 2-6 years (n=633). The Strengths and Difficulties
Questionnaire (SDQ) score was used as the primary measure of children's
behavioral characteristics. Data on history of wheezing, eczema, and
rhinitis were collected from the children's caregivers, using a
standardized questionnaire, based on the International Study of Asthma
and Allergies in Childhood. Associations were estimated using logistic
regression analyses with propensity score to adjust for confounding
factors. Results: Univariate analyses showed that history of wheezing
was associated with conduct problems, a behavioral component of the SDQ.
History of eczema was also associated with hyperactivity. Furthermore,
nose symptoms were associated with conduct and emotional problems. After
adjusting for potential confounders, history of wheezing (adjusted odds
ratio {[}OR{]}=1.69, 95\% confidence interval {[}CI{]}: 1.04-2.75) and
nose symptoms (adjusted OR=1.56, 95\% CI: 1.05-2.34) remained associated
with increased risk of conduct problems. Conclusions: This study
revealed that history of wheezing and rhinitis in children are
associated with increased risk of behavioral problems, in particular,
that of conduct problems. This evidence may inform future research into
childhood allergy symptoms and their behavioral problems.%
\end{abstract}%



\sloppy


\textbf{INTRODUCTION}

Allergy is a hypersensitivity reaction initiated by immunologic
mechanisms.\textsuperscript{1} The prevalence of allergic diseases is
increasing worldwide, including in Japan. The 1999 International Study
of Asthma and Allergies in Childhood (ISAAC) reported that the
prevalence of atopic dermatitis ranged from \textless{}2\% in Iran to
\textgreater{}16\% in Japan and Sweden among children aged 6-7
years.\textsuperscript{2} Phase III of the same study completed 7 years
later reported an increase in the prevalence of asthma,
rhinoconjunctivitis, and eczema in many countries; a decrease in
prevalence was reported only for asthma among adolescents aged 13-14
years.\textsuperscript{3}

Previous studies have reported a relationship between childhood
attention-deficit hyperactivity disorder (ADHD) as well as other mental
health problems and allergy. Studies have shown that children with
eczema or atopic dermatitis achieved higher scores on the Strengths and
Difficulties Questionnaire (SDQ), indicating that the presence of eczema
may be associated with worse mental health.\textsuperscript{4-7} Similar
findings have been reported for conditions such as ADHD and autism
spectrum disorders (ASD) among children with eczema. Children with
atopic dermatitis have been shown to be at increased risk of ADHD or
ASD. \textsuperscript{8-13}

Similar associations have been reported for asthma and
rhinitis\textsuperscript{5}. A systematic review has found that children
with ADHD had a higher rate of asthma than those without
ADHD.\textsuperscript{14} A separate meta-analysis suggested that
patients with asthma, particularly those with severe symptoms, should be
considered at higher risk of behavioral difficulties that may
necessitate psychosocial interventions.\textsuperscript{15} In a
nationwide population-based prospective study, Chen suggested that
asthma was a risk factor for further development of ADHD. In addition,
asthma in very early life has been shown to increase the risk of
developing ADHD during school years.\textsuperscript{16} Suwan reported
increased rates of allergic sensitization in ADHD
cases.\textsuperscript{17} The prevalence of allergic rhinitis among
children with ADHD has also been reported as higher than that among
children without ADHD.\textsuperscript{17} A study based on the Taiwan
National Health Insurance Research Database reported that allergic
disorders, in particular, bronchial asthma and allergic rhinitis, but
not atopic dermatitis, were risk factors for ADHD\textsuperscript{18}.

This evidence notwithstanding, previous studies on the relationship
between allergic symptoms and childhood behavioral problems often failed
to consider the impact of parental factors associated with children's
psychosocial development. A study by Tokunaga et al. examined the impact
of parenting stress in this context and found that paternal stress was
significantly associated with the risk of child
hyperactivity/inattention, while maternal stress was significantly
associated with difficulties in peer relationships and emotional
symptoms.\textsuperscript{19} However, it is plausible that parenting
stress is the effect, not the cause, of childhood behavioral problems,
resulting in poorer SDQ scores.. It is also plausible that this
relationship is bi-directional.

This study aimed to investigate the relationship between allergic
symptoms and children's behavioral problems, adjusting for potential
confounding factors such as demographic characteristics, parenting
stress, and allergy-related variables.

\textbf{METHODS}

Study design and settings

This cross-sectional study was conducted in June 2019 as an online
survey of 2,215 candidates, registered at a private online research
firm, who raised preschool children; among them, 1,030 completed the
questionnaire (response rate 46.5\%). Participants were primary
caregivers of children aged 2-6 years.

Prior to answering the questionnaire, the website administrator provided
consent forms to respondents and informed them that completing the
questionnaire was equivalent to their agreement to study participation.
This study adhered to the Declaration of Helsinki, and was approved by
the ethics committee of Nagoya City University Graduate School of
Nursing (Approval No. 19014-2).

Outcomes, exposures, and covariates

The questionnaire collected data on SDQ domains used as a measure of
children's behavioral problems, demographic characteristics of children
and their caregivers, Parenting Stress Index short form (PSI-SF), and
ISAAC scores. SDQ is an instrument used to evaluate both positive and
negative infant, child, and adolescent behavior.\textsuperscript{20} It
includes 25 items scored on a 3-point Likert-type scale across 5
domains; emotional problems, conduct problems, hyperactivity, peer
problems, and prosocial behavior. The total difficulties score as
assessed in this study consisted of the 4 domains excluding prosocial
score, as that domain alone had a positive value.
\textsuperscript{20}The total difficulties score was used as an outcome
in this study. The Japanese SDQ, translated from the original version
developed in the United Kingdom, has been validated and is considered
applicable to children in Japan.\textsuperscript{21}

The PSI is a self-reported measure of stress associated with
childcare.\textsuperscript{22} The PSI-SF, which is an abbreviated
version of PSI, consists of 19 items scored on a 5-point Likert-type
scale. The Japanese PSI-SF has been validated and applied in this
study.\textsuperscript{23,24} Parenting stress was divided into parent-
and child-associated domains, and assessed comprehensively based on the
total score. Higher scores indicated higher stress levels.

Statistical Analysis

The primary outcome was total difficulties score for SDQ in each domain:
hyperactivity, emotional symptoms, conduct problems, and peer problems.
Each score can be interpreted as ``normal,'' ``borderline,'' and
``clinical,'' on a scale from the lowest to highest score. Matsuishi
proposed the total difficulties score classification as ``normal,''
``borderline,'' and ``clinical,'' corresponding to 0-12, 13-15, and
16-40 points, respectively. Matsuishi sets the ranges for the domains of
emotional problems, conduct problems, and peer problems as 0-3 for
``normal,'' 4 for ``borderline,'' and 5-10 for ``clinical''. The ranges
for the hyperactivity domain were defined as 0-5 for ``normal,'' 6 for
``borderline,'' and 7-10 for ``clinical''. In cases where the outcomes
were divided into binary results corresponding to non-occurrence or
occurrence, it is generally recommended that ``borderline'' results are
included in occurrence when high sensitivity is desired(normal vs.
borderline and clinical) , and excluded when high specificity is
desired(normal and borderline vs. clinical). \textsuperscript{20} We
have used the recommended borderline and clinical cutoff scores as
criteria for dichotomizing primary outcome variables.

Exposure variables used in this study were history of allergic symptoms
such as wheezing, eczema, and nose symptoms since birth. The potential
confounding variables were age and sex (demographic characteristics),
PSI-SF scores (parents' psychological aspect), doctor's diagnosis, and
family history of allergic diseases such as atopic dermatitis, food
allergy, asthma, rhinoconjunctivitis, and hay fever, as well as other
items of the ISAAC.

We performed logistic regression analyses to estimate crude and adjusted
odds ratios (OR), accounting for propensity scores yielded by all
confounding variables. The items used to determine propensity scores are
shown in Supplementary Table 1. When integrating all confounders into
one variable as a propensity score and determining the propensity score
variables for each exposure, the variables relevant to the simultaneous
factors inducing collinearity, such as a history of diseases or period
prevalence, were excluded. The analyses applied a complete case
analysis. As the online survey prevented responders from submitting
their forms with missing values, the dataset involved no missing values.
All statistical analyses were performed using SPSS version 22.0.

\textbf{RESULTS}

Data from a total of 633 surveys were included in the analysis (valid
rate 61.5\%) (Figure 1). Participants were 633 primary caregivers. Of
these, 52.4\% were parents of boys, and 35.2\% had children with
physician-diagnosed atopic dermatitis (11.7\%), food allergy (9.6\%),
asthma (10.7\%), rhinoconjunctivitis (12.8\%), and hay fever (8.7\%). A
total of 221 children had general behavioral problems as measured by the
total difficulties score; 187(29.5\%) had conduct problems, 148(23.4\%)
had hyperactivity, 113(17.9\%) had emotional problems, and 171(27.0\%)
had peer problems. Participant characteristics and their SDQ scores are
presented in Table 1.

In crude logistic regression models, a higher risk of conduct problems
was observed among children with history of wheezing than among those
without (OR= 1.48, 95\% confidence interval {[}CI{]}: 1.01-2.16). A
similar association was observed between nose symptoms and conduct
problems, indicating a higher risk of conduct problems among children
with nose symptoms than among those without (OR=1.65, 95\% CI:
1.16-2.33). Additional associations were observed between history of
wheezing and peer problems (OR=0.59, 95\% CI: 0.38-0.91), that of rash
and hyperactivity (OR=1.62, 95\% CI: 1.02-2.57), and that of nose
symptoms and emotional problems (OR=1.62, 95\% CI: 1.06-2.45) (Table 2).

Adjusted ORs indicated that only history of wheezing (adjusted OR=1.69,
95\% CI: 1.04-2.75) and nose symptoms (adjusted OR=1.56, 95\% CI:
1.05-2.34) affected the risk of conduct problems. No other associations
between childhood allergic symptoms and behavioral problems were
detected after adjusting for propensity scores.

\textbf{DISCUSSION}

This study found that history of wheezing and rhinitis in children were
associated with increased risk of developmental problems, in particular,
that of conduct problems. Previous studies have investigated the
relationship between the presence of allergies and behavioral
characteristics of children. However, unlike previous studies, the
present study analyses included adjustments for potential confounding
factors such as demographic characteristics, parenting stress, and
allergy-related variables. Allergy-related variables included ISAAC
items, clinician's diagnosis of allergies, and family history of
allergies. To control for the impact of collinearity, which was likely
between the variables that represent similar concepts, we performed
adjustments using propensity scores.

Adjusted estimates indicated an association between history of wheezing
and that of nose symptoms and childhood conduct problems. This result is
consistent with that of previous studies, reporting that rhinitis and
asthma, but not eczema, were associated with increased risk of
ADHD.\textsuperscript{18} A separate cross-sectional study using SDQ as
an outcome measure and logistic regression analyses adjusted for gender,
age, and primary caregiver's educational level has shown that children
with current asthma symptoms were more likely to present with conduct
problems than those without.\textsuperscript{5} This study differed from
ours in that no significant association between conduct problems and
history of asthma or hay fever were observed. This discrepancy might be
due to between-study differences in definition of outcomes and
associated cutoff scores. For example, Hammer-Helmich et al. adopted the
``clinical'' value as a cutoff score, whereas we adopted the
``borderline'' value as the cutoff score. Goodman suggested that the
``borderline'' cutoff score be used in studies of high-risk samples
where false positives are not a major concern\textsuperscript{20};
however, we believe that using a highly sensitive threshold is
appropriate to reduce the danger of overlooking an association. Another
possible reason for between-study differences in findings is use of
different confounders for adjustment during analysis. The present study
adjusted for different types of confounders, using the propensity score
technique. Following these adjustments, our results indicate an
association between history of wheezing and/or nose symptoms in children
and conduct problems; this finding may inform selection of confounders
and support new perspectives in future studies.

Biologically, allergy-sensitized children have elevated levels of
inflammatory cytokines. Studies in clinical psychiatry have shown that
levels of specific cytokines play a role in signaling the brain to
produce neurochemical, neuroendocrine, and neuroimmune responses that
correspond to behavioral changes. These responses may affect important
brain activities such as sleep, appetite, and neuroendocrine
regulation.\textsuperscript{25} Depending on the rate and amount at
which cytokines cross the blood brain barrier, diverse neuropsychiatric
symptoms may emerge, including low or depressed mood, anxiety, or
psychosis.\textsuperscript{26} This is not the case with eczema-related
findings; this study's findings were consistent with those of previous
studies on allergic symptoms\textsuperscript{25,26} and behavioral
problems in children.

In the present study, history of wheezing and rhinitis affected the risk
of conduct problems in children after adjustment for potential
confounders. Both wheezing and rhinitis cause respiratory symptoms,
which may lead to sleep disorders. Poor sleep quality can adversely
affect the behavior of children.\textsuperscript{27} In addition, a
previous systematic review revealed the presence of sleep disorders in
children with ADHD\textsuperscript{28}; a separate review reported that
associations between sleep and psychopathology are complex and likely
bidirectional.\textsuperscript{29} Therefore, additional studies are
needed to elucidate the association between ADHD-like behavioral
characteristics and sleep.

That is to say, given these findings, we believe that high impulsiveness
can be attributed in part to the psychological effect of elevated levels
of inflammatory cytokines that are triggered by allergic sensitization;
in addition, low quality of sleep is likely to play a role in tendency
toward behavioral irritation. However, further studies are needed to
confirm these associations.

This study has several strengths and limitations. This study is the
first to adjust for confounding factors, including participant
demographic characteristics, parenting stress, and allergy-related
variables. Study limitations are as follows. First, while we adjusted
for multifaceted confounders, we did not control for unmeasured or
residual confounding by factors such as sleep and psychopathological
characteristics. Second, as this was a cross-sectional study, the
presented findings preclude meaningful discussions of causality. Further
studies are warranted to confirm our findings; such studies should
involve a longitudinal design and a representative sample. Third, we did
not control for the impact of medication that could affect sleepiness or
mental health, such as antihistamines. Finally, caregivers may have
reported increased parenting stress due duties associated with care of
children with allergies; however, we could not account for this factor
in this study.

In conclusion, this study revealed that history of wheezing and rhinitis
in children is associated with increased risk of behavioral problems, in
particular, that of conduct problems.

\textbf{Author contributions: Chikae Yamaguchi:}
Conceptualization(lead); Data curation(lead); Formal analysis(lead);
Methodology(equal); Funding acquisition(lead); Writing-Original Draft
Preparation(lead); Writing-review and editing(lead). \textbf{Takeshi
Ebara:} Data curation(equal); Formal analysis(equal); Methodology(lead);
Writing-review and editing(equal).\textbf{Masaki Futamura:}
Conceptualization(equal); Writing-review and editing(equal).
\textbf{Yukihiro Ohya:} Writing-review and editing(equal).
\textbf{Midori Asano:} Conceptualization(supporting); Writing-review and
editing(equal).

\textbf{Acknowledgments:} The authors thank all study participants and
their families

\textbf{Key message:} This study revealed an association between
childhood history of wheezing and rhinitis and conduct problems. The
strength of this study is that it adjusted for confounding factors,
including demographic characteristics, parenting stress, and
allergy-related variables. In addition, to control for the impact of
collinearity, we adjusted for these factors using propensity scores,
increasing the reliability and validity of our findings.

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\textbf{Tables}\selectlanguage{english}
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\textbf{Figure legends:} Flow diagram of study data selection\selectlanguage{english}
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\textbf{Appendix:} Items used to estimate propensity scores\selectlanguage{english}
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