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\begin{document}

\title{Effect of COVID-19 Pandemic on Anxiety Levels of Children with Cystic
Fibrosis and Healthy Children}



\author[1]{Mürüvvet Cenk}%
\author[2]{Cansu Yılmaz Yegit}%
\author[1]{Almala  Ergenekon}%
\author[1]{Ayse Toksoy Aksoy}%
\author[1]{Gulcin Bilicen}%
\author[2]{Yasemin Gokdemir}%
\author[3]{Ela Erdem Eralp}%
\author[1]{Ayse Rodopman Arman}%
\author[3]{Fazilet Karakoc}%
\author[3]{Bulent Karadag}%
\affil[1]{Marmara University School of Medicine}%
\affil[2]{Marmara University}%
\affil[3]{Marmara University Faculty of Medicine}%


\vspace{-1em}



  
  \date{May 18, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Background Cystic fibrosis (CF) is a chronic disease causing recurrent
respiratory tract infections. Viral respiratory tract infections are
more severe in CF. The first case of COVID-19 was seen in Turkey on
March 11, 2020 and nationwide school closure and lockdown were
implemented. School closure and home confinement might have adverse
effects on children's physical and mental health. In this study, we
aimed to compare the effect of COVID-19 pandemic on psychological
reactions of CF patients and healthy controls. Methods This is a
controlled cross-sectional study including 7-18 year-old children with
CF. The survey included questions regarding family environment and peer
relations, self care and psychological reactions to COVID-19 pandemic.
The questionnaire was applied to children via telephone call under
parental supervision. Results We evaluated 132 CF patients and 135 their
healthy peers. Mean age was 11.5\selectlanguage{ngerman}±2.9 years in CF group and 11.8±3.2
years in control group (p=0.98). There were 55 girls (41.7\%) in CF
group and 81 girls (60\%) in control group (p=0.027). The socioeconomic
status of families was similar. CF patients was feeling less anxious
about the COVID-19 pandemic compared to controls (p=0.01). CF patients
were found to be less anxious for family members having the risk of
COVID-19, less upset for the school closure, less anxious about the
COVID-19 pandemic (p\textless{}0.001, 0.02, 0.01 respectively).
Conclusion CF patients seem to show more resilience in coping with the
pandemic. Appropriate psychological support should be provided to them
and resilience strategies in coping with the pandemic should be
nurtured.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


TITLE PAGE

\textbf{The Effect of COVID-19 Pandemic on Anxiety Levels of Children
with Cystic Fibrosis and Healthy Children}

Muruvvet Cenk\textsuperscript{1}, Cansu Yilmaz Yegit\textsuperscript{1},
Almala Pinar Ergenekon\textsuperscript{1}, Ayse Toksoy
Aksoy\textsuperscript{2}, Gulcin Bilicen\textsuperscript{3}, Yasemin
Gokdemir\textsuperscript{1}, Ela Erdem Eralp\textsuperscript{1}, Ayse
Rodopman Arman\textsuperscript{2}, Fazilet Karakoc\textsuperscript{1},
Bulent Karadag\textsuperscript{1}

\textsuperscript{1}Division of Pediatric Pulmonology; Marmara
University, School of Medicine, Istanbul, Turkey

\textsuperscript{2}Department of Child and Adolescent Psychiatry,
Marmara University, School of Medicine, Istanbul, Turkey

\textsuperscript{3}Marmara University, School of Medicine, Istanbul,
Turkey

Correspondence to: Muruvvet Cenk, MD

Kordonboyu mah Ankara cad No:147/196 Kartal/Istanbul

TURKIYE

Tel (mobile): +90 536 4191641

Email: \emph{muruvvetcenk@gmail.com}

\textbf{Abstract}

\textbf{Background}

Cystic fibrosis (CF) is a chronic disease causing recurrent respiratory
tract infections. Viral respiratory tract infections are more severe in
CF. The first case of COVID-19 was seen in Turkey on March 11, 2020 and
nationwide school closure and lockdown were implemented. School closure
and home confinement might have adverse effects on children's physical
and mental health. In this study, we aimed to compare the effect of
COVID-19 pandemic on psychological reactions of CF patients and healthy
controls.

\textbf{Methods}

This is a controlled cross-sectional study including 7-18 year-old
children with CF. The survey included questions regarding family
environment and peer relations, self care and psychological reactions to
COVID-19 pandemic. The questionnaire was applied to children via
telephone call under parental supervision.

\textbf{Results}

We evaluated 132 CF patients and 135 their healthy peers. Mean age was
11.5\selectlanguage{ngerman}±2.9 years in CF group and 11.8±3.2 years in control group (p=0.98).
There were 55 girls (41.7\%) in CF group and 81 girls (60\%) in control
group (p=0.027). The socioeconomic status of families was similar. CF
patients was feeling less anxious about the COVID-19 pandemic compared
to controls (p=0.01). CF patients were found to be less anxious for
family members having the risk of COVID-19, less upset for the school
closure, less anxious about the COVID-19 pandemic (p\textless{}0.001,
0.02, 0.01 respectively).

\textbf{Conclusion}

CF patients seem to show more resilience in coping with the pandemic.
Appropriate psychological support should be provided to them and
resilience strategies in coping with the pandemic should be nurtured.

\textbf{Key Words:} Cystic Fibrosis, COVID-19, Anxiety, Resilience,
Coping

\textbf{Introduction}

Cystic fibrosis (CF) is a chronic, life-shortening disease causing
recurrent respiratory tract infections and loss of lung functions
{[}1{]}. Previous meta-analyses and systematic reviews have shown that
adults and children with chronic diseases have higher risk of depression
and anxiety compared to community {[}2,3{]}. A number of studies
reported increased anxiety and depression in CF pateints compared to
healthy controls {[}4-6{]}. Facing a chronic disease such as CF on a
daily basis cause significant emotional burden which can be attributed
to large number of treatments, hospitalizations, multiple diagnostic
procedures, chronic respiratory symptoms, a lower body mass index
{[}6{]}.

Viral respiratory tract infections are more severe in patients with CF
compared to general population. Influenza pandemic in 2009, caused
significant morbidity in patients with CF and in a subgroup of patients
with severe lung disease, H1N1 infection was associated with respiratory
deterioration, intensive care admission and even death {[}7,8{]}.
Coronavirus disease-19 (COVID-19) has emerged in China and been
spreading all over the world since December 2019. The first case of
COVID-19 infection has been confirmed in Turkey as of March 11, 2020.
Although in most of the pediatric cases (\textgreater{}90\%) the disease
is asymptomatic or presented with signs of upper respiratory tract
infection symptoms, in a small number of children (\%0.6), the infection
may progress into critical disease causing respiratory insufficiency and
death {[}9{]}.

During COVID-19 pandemic people are likely to experience fear of falling
sick, dying or feelings of helplessness and a number of studies revealed
a wide range of psychosocial impacts on people {[}4{]}. In a study by
Wang et al, included 1210 respondents, psychological impact of the
outbreak was present in 53.8\%. Moderate to severe depression, anxiety
symptoms and stress levels were present in 16.5\%, 28.8\% and 8.1\% of
the participants respectively {[}10{]}. Another cross-sectional study in
7143 college students demonstrated that 21.3\% had mild and 3.6\% had
moderate-to-severe anxiety symptoms where economic effects on daily life
and delays in academic activities were positively associated with
anxiety symptoms {[}11{]}.

Although children seem to be less vulnerable than adults to COVID-19,
initial reports from China indicate that children and adolescents also
have been impacted psychologically, manifesting behavioral problem.
Previous studies suggested that when children are out of school (eg,
weekends and summer holidays), they are physically less active, have
longer screen time, irregular sleep patterns, and less favourable
feeding habits, resulting in weight gain and a loss of cardiorespiratory
fitness {[}12,13{]}.

Shuang-Jiang Zhou et al conducted a cross-sectional study including 8079
students aged 12--18 years during the COVID-19 pandemic period. The
prevalence of depressive symptoms, anxiety symptoms, and a combination
of depressive and anxiety symptoms was found 43.7\%, 37.4\%, and 31.3\%,
respectively {[}14{]}. Home confinement during pandemic appears to be
another factor in increasing stress levels in children. In 2013, Sprang
et al has been found that the post-traumatic stress scores of
quarantined children was four times higher than those who were not
quarantined {[}15{]}.

Although the mortality of COVID-19 infection was found higher in
patients with underlying diseases, until now, there is no evidence
suggesting that the course of COVID-19 is more severe in CF patients
compared to general population {[}16{]}. Clinical features of COVID-19
including dry cough, myalgia, and fever are quite distinct from the
symptoms of CF and recognisable. However it is possible that mild
disease might be labelled as within the normal spectrum of symptoms for
that individual. However, COVID-19 infection still might cause more
stress and anxiety in CF patients. To our knowledge there is only one
study evaluating anxiety of CF patients during COVID-19 pandemic.
Senkalfa et al compared the anxiety of 45 CF patients with 90 healthy
control group and revealed that healthy children, aged 13--18 years had
higher state anxiety scores than age-matched children with CF {[}17{]}.

In this study, our aim was to evaluate the effect of COVID-19 pandemic
on family environment and relations, self-care practises and peer
relations, psychological reactions including anxiety and coping of CF
patients and compare with healthy controls.

\textbf{Methods}

This is a controlled, cross-sectional, single center study including
7-18 year-old CF children who have been followed up in Selim Çöremen
Cystic Fibrosis Center in Marmara University Faculty of Medicine,
Division of Pediatric Pulmonology and their healthy peers.

Separate behavioral questionnaires for two different age groups (7-12
and 13-18 years), based on the child psychiatry mental health
examination references {[}18{]}, were formed by Marmara University
Faculty of Medicine Child and Adolescent Psychiatry Department.

The questionnaire included questions regarding family environment and
relations, self-care practises and peer relations during lockdown, and
psychological reactions regarding COVID-19 pandemic. Data regarding
presence of a health worker in the family, or a family member diagnosed
with COVID-19, current anxiety level, sleep disturbances, change in
appetite, activities in order to mitigate their anxiety (any attempt to
have a new hobby etc.) and seek for a psychological help were also
collected.

In CF patients, data regarding presence of pancreatic insufficiency,
colonisation of Pseudomonas Aeruginosa and level of forced expiratory
volume in second 1 (FEV\textsubscript{1}) were collected from patients'
medical records. Lung disease was categorised as mild, moderate and
severe according to their baseline FEV\textsubscript{1} measurements
(FEV\textsubscript{1} 70-89 mild lung disease, FEV\textsubscript{1} 40
to 69\% moderate lung disease, FEV\textsubscript{1} \textless{} 40\%
severe lung disease {[}19{]}.

The data was collected between 30th April, 2020 and 15 th of May, in
Turkey this time period was the peak of pandemic, schools were closed
and education was online. We conducted phone survey by asking questions
directly to the children under parental supervision. Children, younger
than 7 years of age or who refuse to answer the questions or children
with mental problems were excluded from the study.~\emph{Informed
consent was obtained from all parents following their agreement} to
participate the~\emph{phone survey} and the study was approved by the
medical ethics committee of Marmara University (Protocol number
09.2020.549).

Data were analyzed by using the SPSS Statistical Package for Windows
version 23.0. Numerical variables were expressed as mean±standart
deviation or median. Caterogical variables were compared using the
Chi-square test and expressed as numbers and percentages. A p value~of
less than 0.05 was considered statistically significant.

\textbf{Results}

This study included 132 CF patients and 135 healthy peers. The mean age
was 11.53±2.86 and 11.76±3.15 years respectively, in CF group and
control group (p=0.98). There were 55 girls (41.7\%) in CF group and 81
girls (60\%) in control group (p=0.027).

Of the 132 CF patients, 95 (72\%) had pancreatic insuffiency, 41
(31.1\%) were colonised with Pseudomonas Aeruginosa, 59 (44.7\%) had
normal FEV\textsubscript{1} value, 40 (30.3\%) had mild, 23 (17.4\%) had
moderate and 5 (3.8\%) of them had severe lung disease. There was no
statistically significant difference in terms of severity of the disease
and anxiety levels of CF patients (p \textgreater{}0.05). Comparison of
psychosocial and psychological findings between CF patients and control
group was presented in Table-1. CF patients were found to be less
anxious for family members having the risk of COVID-19, less upset for
the school closure, less anxious about the COVID-19 pandemic
(p\textless{}0.001, 0.02, 0.01 respectively). Control group was more
overthinking about the pandemic, and feeling sad, lonely or reluctant to
have playful time (p=0.03 and 0.02, respectively). Control group also
tried to have new hobbies more compared to CF group (p= 0.01).

In CF group 71 (53.8\%) of patients were children and 61 (46.2\%) were
adolescents. Children were feeling more upset for the school closure
(p=0.01) and more anxiety about the COVID-19 pandemic (p=0.008), had
more appetite changes (p=0.03), expressed more reluctance of doing
homework for online education (p=0.03), engaging activities to decrease
their anxiety (p=0.01), tried to find new hobbies during lockdown
(p=0.005) and needed psychological help (p=0.059) more than adolescents.
Adolescents communicated with their friends via social media more than
children (p=0.005). Comparison of psychological and psychosocial
findings in CF group as children and adolescent was presented in
Table-2.

In control group, 79 (58.5\%) of them were children and 56 (41.5\%) of
them were adolescents. Although adolescents communicated with their
friends from social media more than children (p=0.003), children felt
happier for communicating online with their friends (p=0.02). Also
children engaged new activities and needed for psychological help more
than adolescents (p value 0.008 and 0.11 respectively). Comparison of
psychosocial and psychological findings in control group as children and
adolescent was presented in Table-3

In our country examinations for high school and university admission are
big stressors for adolescents. Twenty-four (39.4\%) of CF and 17
(30.4\%) of control group had admission examinations for high school or
university. We also asked these adolescents if the pandemic, school
closure and online education increased their anxiety. Although it was
not statistically significant (p=0.21), exam anxiety was higher in
control group compared to CF patients (46.4\% vs 24.6\%).

\textbf{Discussion}

The COVID-19 has spread all over the world since the first quarter of
2020 and the uncertainty about the personal and global effects of
COVID-19 in addition to psychological effect of quarantine caused fear
and anxiety. Previous studies have suggested that the outbreaks can have
many psychological effects like anxiety and depression {[}20,21{]}.
Although a number of studies evaluated psychological impact of COVID-19
pandemic in children and adults, data regarding the effect of pandemic
in patients with chronic disease is scarce {[}17{]}.

In this study we evaluated the psychological reactions, family and peer
relations, self-care practises and coping methods of CF patients during
pandemic and compared with healthy controls. Symptoms of anxiety were
unexpectedly higher in controls compared to CF patients. Almost 50\% of
the children in control group and 33\% of the CF patients were feeling
anxious about the COVID-19 pandemic. Feeling upset for school closure,
worries for a family member having the risk of COVID-19 infection,
feeling sad, lonely or reluctant to have playful time, overthinking
about pandemic are all more common psychological reactions regarding
pandemic in control group compared to CF patients.

Consistent to the results of current study, another study from Turkey,
Senkalfa et al also reported lower anxiety scores regarding COVID-19
pandemic in CF patients compared to age-matched healthy control group
{[}17{]}. Surprisingly lower anxiety scores in CF patients in both study
may be related with a number of factors.

Since the viral respiratory tract infections tend to be more severe in
CF patients with an increased risk of complications and a negative
impact on lung function, in the first days of pandemic, our patients and
their families were more concerned about the possible effect of COVID-19
infection. However until now, only few cases of COVID-19 infection in
people with CF were reported, which may probably related with the
efforts of families and patients to minimise social contacts {[}22{]}.
It should also worthwhile to emphasize that reported cases are mainly
adult CF patients and COVID-19 infection does not have an apparent
effect on CF disease severity. It is not possible to identify protective
factors and we need more data in order to determine the impact of
COVID-19 on patients with CF. In cooperation with national registries,
European Cystic Fibrosis Society (ECFS) Patient Registry has established
an international dataset to identify factors that predict severity of
COVID-19. However we assume that low numbers and mild course of COVID-19
infection caused a relieve in CF patients, which may partly explain
lower anxiety levels in our patients.

During pandemic, consistent with international guidelines we recommended
self-isolation for our CF patients. Recommendations for preventive
measures such as using face masks and practising adequate hand hygiene
were reinforced. The CF team cancelled routine clinic appointments to
prevent unnecessary hospital visits and viral spread. Phone calls and
email contacts were used to monitor the clinical condition of patients
immediately after the lockdown. In a study from China, presence of
psychological problems were negatively associated with the level of
awareness of COVID-19 {[}14{]}. Wang et al revealed that wearing a mask
and practicing hand hygiene decreases the level of anxiety in children
older than 12 years old {[}10{]}. CF patients are used to follow
instructions for infection control guidelines' including wearing masks
and avoiding close in-person contact with other CF patients. The
awareness regarding respiratory tract infections and familiarity to
infection control measurements might be factors which decrease the level
of anxiety in CF patients.

Psychosocial maladjustment might be another reason for lower anxiety
levels in CF patients. Children with chronic physical disorders have
twice the risk of psychosocial maladjustment compared with healthy
children {[}23{]}. This maladjustment phenomenon might be an explanation
for CF patients to give fewer psychological reactions in our study group
in the case of pandemic, as they are already having longer times at
home, mostly detached from the school or peer relations.

CF patients always facing with a serious health problem and associated
anxiety symptoms, hovewer, healthy peers has been encountered fear of
disease for the first time in their life during pandemic which can also
partly explain relatively lower levels of anxiety in CF patients
compared to healthy controls.

Although no significant difference was found between CF and control
groups regarding family environment and relations or self care and peer
relations, it is important to emphasize that almost half of the children
were having apetite changes in both groups and incidence of sleeping
problem were 10\% in CF patients and 15\% in control group. In our
country, during disease outbreak, right after the school closure and
home confinement, home schooling plan has been implemented. In addition
to academic learning, age appropriate and attractive videos may motivate
children to have a healthy lifestyle at home by increasing physical
activities, having a balanced diet, regular sleep pattern, and good
personal hygiene.

Althoug CF patients had a lower tendency to need psychological help
compared to control group, children in CF group had more anxiety
symptoms compared to adolescents and required more psychological help
than adolescents in both groups. During pandemic children are constantly
exposed to pandemic-related news, so having direct conversations with
children about these issues could alleviate their anxiety. Home
confinement, with the right parenting approaches could be a good
opportunity to enhance family interactions and improve their
self-sufficiency skills of children {[}24{]}.

Resilience is the ability of properly adapt and react positively to
adversity, trauma, individual or society tragedies, including serious
health threats {[}25-26{]}. Coping responses mean the behaviours,
thoughts and feelings that individuals adopt to avoid being harmed by
life stressors {[}27{]}. In this study, we found that CF patients seem
more resilient and developed adaptive coping strategies with the
pandemic. Mental health of children and adolescents constitute the basis
for future adult mental health and related to quality of life,
productivity, and well-being as well as compliance to treatment in the
presence of a chronic health condition. Therefore, it is a vital effort
to understand the psychological reactions of CF patients during the
unusual period of pandemic, in addition to the chronic illness status.

Current study has a few limitations. First, although the CF and control
groups are aged-matched, they are not gender-matched. It has been shown
that girls experience more anxiety than boys in previous studies
{[}28-29{]}. Hovewer, since the anxiety levels of girls in our study
were similar in CF and control groups, we assumed that gender difference
has not been an important impact on our results.

Second, this was a phone survey and participants were recruited under
parental supervision. Since it was a self-report assessment, the
indicated levels of anxiety may not always be consistent with the
assessment of mental health by a professional.

Several studies reported increased anxiety and depression in CF pateints
compared to healthy controls and routine screening is strogly
recommended, {[}4-6{]}. In a recent unpublished study, before pandemic,
we revealed that moderate to severe depression and moderate anxiety was
peresent in 25.5\% and 17.6\% of 50 adolescent CF patients respectively
in our center {[}30{]}.

Current study revealed that CF patients had lower anxiety symptoms and
they were more resilient in coping during pandemic than their healthy
peers.

In conclusion, although acute events such as pandemics may not seem to
increase baseline anxiety and not associated with an important
physcological impact in CF patients compared to heathy population, lack
of psychological support in routine care may lead to higher levels of
anxiety and depression in long term.

\textbf{Conflict of Interest}

There is no conflict of interest.

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\end{enumerate}

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