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\begin{document}

\title{The Effects of The COVID-19 Pandemic on Pediatric Cystic Fibrosis
Patients}



\author[1]{Omer Beser}%
\author[1]{Ebru Pelin Ugur Karaboga}%
\author[1]{EVRIM HEPKAYA}%
\author[2]{Ayse Ayzit Kilinc}%
\author[1]{Ahsen Donmez Turkmen}%
\author[1]{Tugce Damla Dilek}%
\author[3]{Haluk Cokugras}%
\author[1]{Fügen Çullu Çokuğraş}%
\affil[1]{Istanbul University-Cerrahpasa Cerrahpasa Faculty of Medicine}%
\affil[2]{Istanbul University Cerrahpasa Faculty of Medicine}%
\affil[3]{Istanbul Universitesi-Cerrahpasa}%


\vspace{-1em}



  
  \date{June 17, 2024}


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\selectlanguage{english}
\begin{abstract}
Objectives: To follow-up pediatric CF patients---in terms of health
status and nutritional status---via Telehealth services during the
COVID-19 pandemic. Additional aims were to measure the level of anxiety
in the patients and their parents, and to determine the COVID-19
transmission status in the CF patients. Materials and Methods: The CF
team supported the patients via remote contact, including dedicated
telephone lines. During Telehealth Services interviews, in addition to
obtaining information about the patients' anthropometric measurements,
health status, and CF-related complaints, the State-Trait Anxiety
Inventory (STAI) was administered to the patients and the Hospital
Anxiety and Depression Scale (HAD) was administered to their parents.
Results: The study included 144 pediatric CF patients (74 male and 70
female). Mean age of the patients was 8.9 years. In all, 42 (29.2\%) of
the patients were tested for COVID-19, of which 4 were positive. The
mean STAI score was significantly lower in the patient group than in the
control group (P \textless{} 0.001). The mean HAD anxiety score was
significantly higher in the parents of the CF patients, as compared to
the parents of the controls (P = 0.005). The mean HAD depression score
was also statistically higher in the parents of the CF patients (P
\textless{} 0.001). Conclusion: Telehealth is an innovative method for
providing healthcare services while maintaining social distancing,
avoiding the risk of exposure and spread of COVID-19. Telehealth
services reduce patients' and parents' anxiety, and increases their
confidence in managing CF-related complications.%
\end{abstract}%



\sloppy


\textbf{Introduction}

The COVID-19 pandemic caused by the novel coronavirus SARS-CoV-2 has
resulted in evolving public health crisis (1). Many studies have shown
that the clinical manifestations of COVID-19 are primarily related to
the respiratory system (2-4). Cystic fibrosis (CF) is a multi-systemic
disease and the main causes of morbidity and mortality in CF patients
are respiratory complications and comorbid chronic diseases (3). These
problems can cause a range of psychological symptoms in pediatric CF
patients and their parents (5-7). It is known that pediatric CF patients
and their parents have higher depression and anxiety scores than the
general population (8-10).

Viral respiratory tract infections cause more severe illness in children
with CF than in their healthy peers. The number of CF patients that have
been diagnosed with COVID-19 currently remains relatively low (11),
making it difficult to reach conclusions about the impact of the
COVID-19 infection on CF patients. In healthy individuals COVID-19 may
be mild, but in individuals with significant respiratory problems the
risk of more severe illness increases (11).

Respiratory infections can cause weight loss in CF patients and,
therefore, tracking their nutritional status is of critical importance
(12).

The present study aimed to monitor the health status and nutritional
status in pediatric CF patients during the pandemic. Additional aims
were to determine the level of anxiety in the patients and their parents
during the pandemic, and to determine the COVID-19 transmission status
among patients.

\textbf{Materials and Methods}

This prospective cross-sectional study included 144 pediatric CF
patients (patient group) and their parents, and 49 healthy (without any
chronic and acute disease) age- and gendered-matched children (control
group) and their patients. The study was performed at Istanbul
University-Cerrahpa\selectlanguage{polish}ş\selectlanguage{english}a, Cerrahpa\selectlanguage{polish}ş\selectlanguage{english}a School of Medicine, Department of
Pediatric Gastroenterology, Hepatology, and Nutrition, and Department of
Pediatric Pulmonology, Istanbul, Turkey. Inclusion criteria included a
diagnosis of CF and follow-up of [?]1 years at our clinics. Our center's
CF team supported the patients via remote contact, including central
email addresses and dedicated telephone lines. Regular CF appointments
were conducted via Medicare Telehealth Services during the COVID-19
pandemic. The inpatient team was on site, but only saw patients
face-to-face when absolutely necessary. Only caveat was that it has been
for MDs/dietitian/nurse only and their programmers on the list.

Approval for telework was obtained after a painstaking week of back and
forth. The treatment team consisted of 2 pediatric gastroenterologists,
2 pediatric pulmonology specialists, 1 CF dietitian, and 1 nurse that
performed a mix of inpatient and outpatient work. The team was divided
into 2 sub teams that alternated weekly between on-site and telework.
The main responsibilities of the on-site dietitian was~complete initial
assessment and follow-up of patients that needed to be seen in person,
including re-checking lengths/etc., formula room/emergency service
discharge, daily check-ins with provider teams, and rounds [?]1 times each
week with service teams The main responsibilities of the dietitian
working from home were complete initial assessment and follow-up, unless
the patient required being seen in person, responding to pages,
notifying teams that they were teleworking, daily check-ins with
provider teams, discussing pending changes to diet orders/PN with teams,
contacting the on-site dietitian partner if a patient needed to be seen
in person so that they could complete the assessment and provision of
discharge instructions that could not be completed by a resident/RN.

As a decrease in the nutritional status in children with CF can be a
cause of a decline in health status, the patients' parent were asked
measure and their children's weight, which was then compared to the
z-scores last measured in the hospital. After measuring weight, height,
and length of each patient, 4 z-scores were calculated using the WHO
Anthro Program v.3.2.2 (January 2011) for children aged [?]5 years, as
follows; height-for-age (HFA); weight-for-age (WFA); weight-for-height
(WFH); body mass index-for-age (BMI). WFH in CF patients aged
\textless{}5 years and BMI in CF patients aged \textgreater{}5 years
were used to determine nutritional~status.

Via the Medicare Telehealth Services the pediatric CF patients and their
parents were administered a questionnaire that collected data on daily
life, clinical symptoms, and medical problems between March 11 and June
01 2020. Disease flare ups, problems getting to hospital and obtaining
medications, patient and family history of contact with confirmed
COVID-19 cases, screen time, exercise, adherence to diet, use of
vitamins, direct exposure to sunlight, and adherence to the 14 COVID-19
rules recommended by the Ministry of Health.

Medicare Health Services was used to administer the Hospital Anxiety and
Depression Scale (HAD) to the parents of the patients and controls. HAD
consists of 14 items, 7 of which assess anxiety and 7 of which assess
depression. Cut-off values are 10 for anxiety and 7 for depression.
Parents were considered positive if their score was higher than the
cut-off. HAD was adapted to Turkish by Aydemir (13), who demonstrated
that it is an appropriate instrument for use in Turkey. The Cronbach
alpha internal consistency coefficients were 0.8525 and 0.7784 for the
HAD anxiety and depression subscales, respectively. In addition, the
State-Trait Anxiety Inventory (STAI) was administered to the patient and
control groups to assess their mental health status. STAI was developed
by Spielberger et al. (14) to measure anxiety. STAI was adapted to
Turkish by Le Compte and \selectlanguage{ngerman}Öner (15). The test assesses anxiety via 2
subscales: the state anxiety subscale (STAI-S) (20 items) evaluates the
current state of anxiety and the trait anxiety subscale (STAI-T) (20
items) evaluates relatively stable aspects of the tendency for anxiety,
including general states of calmness, confidence, and security. The
range of scores for each subscale is 20-80, with higher scores
indicating greater anxiety. The cut-off point is 41 for STAI-S and 45
for STAI-T (Ercan et al. 2015). Patients were considered positive if
their score was higher than the cut-off. STAI scores in the patient and
control groups were compared. The Cronbach alpha internal consistency
coefficients were 0.8525 and 0.7784 for STAI-S and STAI-T, respectively
(13).

The correlations between the anxiety status in the CF patients and the
anxiety-depression status in their parents were statistically examined.
The same correlations were also analyzed in the controls and their
parents. All 98 pediatric CF patients had adequate intellectual ability
and education to complete STAI. The control group included 49 children
because we had 49 patients aged \textgreater{}8 years. The study
protocol was approved by the Istanbul University Cerrahpasa School of
Medicine Ethics Committee (approval no: 29430533-604).

\textbf{Statistical analysis}

Data were analyzed using IBM SPSS Statistics for Windows v.21.0 (IBM
Corp., Armonk, NY, USA). Associations between the study variables were
measured via Pearson's chi-square test, the Mann-Whitney U test, and
Student's t-test. The level of statistical significance was set at P
\textless{} 0.05.

\textbf{Results}

\textbf{Descriptive findings}

The study included 144 pediatric patients (74 males and 70 female). Mean
age of the patients was 8.9 years. There was a mean 4.33 individuals per
patient household, with a mean age of 30.9 months. Among the patients,
15 had a decrease in appetite, of which 90\% had exacerbations and 80\%
were hospitalized. In total, 50\% of the patients (mean age: 8.81 years)
had no change in appetite and (30.5\%) (mean age: 10.42 years) had an
increase in appetite. There wasn't a significant difference between the
age groups based on Student's t-Test.

In all, 101 of the patients did not have any CF-related symptoms,
whereas 43 did, including cough (n = 16), fever (n = 12), wheezing and
shortness of breath (n = 8), nasal obstruction (n = 6), stomachache (n =
6), nausea (n = 6), diarrhea (n = 4), and constipation (n = 2).
Moreover, 22 of the patients reported via Telehealth Services that they
had greasy stool. Among the patients' parents, 98.02\% never considered
withdrawing their children's regular medications. Among the patients, 70
came to the hospital for face to face visits, during which time their
height and weight were recorded. Table 1 provides descriptive and
clinical characteristics of subjects.

\textbf{COVID-19-positive cases}

In total, 42 (29.2\%) of the CF patients were tested for COVID-19, of
which 4 were positive. Among those 42 patients, 28 were tested due to
COVID-19 positive cases in their family, of which only 3 were positive.
In all, 14 of the CF patients were tested for COVID-19 due to the
presence of COVID-19 symptoms; only 1 was positive, 3 quarantined at
home because they did not have any COVID-19 symptoms, and 1 was treated
in hospital due to clinical symptoms of COVID-19. The characteristics of
the COVID-19-positive CF patients are shown in Table 2.

\textbf{STAI and HAD}

STAI was administered to the 49 CF patients aged \textgreater{}8 years.
The STAI-S score in all 49 patients was above the cut-off value (normal
\textless{}45). The mean STAI-S score was significantly lower in the
patient group than in the control group (P \textless{} 0.001). STAI-S
scores were significantly higher in the male CF patients than in the
controls and female CF patients. STAI-S scores showed that adolescent
patients were more anxious than the younger CF patients and the
controls. In addition, adolescents with CF had a significantly higher
STAI-S score than their healthy peers and CF patients aged 8-14 years.
Similarly, STAI-T scores were higher in the control group than in the
patient group. In contrast to STAI-S findings, STAI-T scores did not
differ significantly according to age in the patient group. In addition,
there wasn't a significant difference in STAI-T scores between the
patients and controls. STAI findings are shown in Table 3.

HAD was administered to the parents of 144 CF patients and the parents
of 140 healthy controls. The mean HAD anxiety score in the patients'
parents was significantly higher than in the controls' parents.

The mean HAD anxiety score was significantly higher in the parents of
the patients, as compared to the parents of the controls (P = 0.005).
The mean HAD depression score was also significantly higher in the
patients' parents than in the controls' parents (P \textless{} 0.001).
Table 4 presents the HAD anxiety and depsression outcomes.

\textbf{Nutritional status}

The patients' BMI for age z-scores before and after the COVID-19
pandemic were compared. BMI for age and WFH z-scores in the CF patients
improved significantly during the pandemic (P = 0.002). In addition,
there was significant weight gain in the patients during the pandemic (P
= \textless{}0.001), as 74.3\% (n = 107) of the patients gained weight.
Moreover, 11.8\% of the patients maintained their current weight and
13.8\% lost \textgreater{}3\% of their weight; these patients reported
having CF-related symptoms.

\textbf{Discussion}

The burden of COVID-19 is increasing worldwide and is thought to be
greater in people with chronic diseases. On the other hand, it is
predicted that COVID-19 is more aggressive in patients with CF, as it is
thought that the virus affects the respiratory tract and can cause more
severe disease in those with a compromised immune system. The present
study aimed to monitor pediatric CF patients during the COVID-19
pandemic. The present findings show that statistically there were no
problems in the supply of CF drugs or their use during the pandemic (P =
\textless{}0.001 and P = 0.001, respectively). The present findings also
show that during the pandemic there was no increase in CF symptom
frequency or a decrease in appetite (P = 0.03 and P \textless{} 0.001,
respectively). Based on these findings, we think that pediatric CF
patients in Turkey are not affected by these problems during the
pandemic due to well-organized protocols, such as extending the health
reports of those with chronic diseases, delivering medicines to those
with chronic diseases, and regular patient contact.

Studies have shown that patients with other chronic diseases are not
infected to a greater degree during the COVID-19 pandemic than the
general population (16). In the present study only 4 (2.7\%) of 144
pediatric CF patients were COVID-19 positive. We think that the COVID-19
positivity rate was low because as the patients had a chronic disease
their parents were very careful about their isolation. Undoubtedly, we
did not have enough COVID-19 positive patients to compare with those who
did not; however, it was noted that among the 4 COVID-19 positive cases,
3 were infected via domestic contact and were asymptomatic. On the other
hand, it was observed that the 1 symptomatic patient had both a
significantly low BMI for age z-score and \emph{Pseudomonas
Aeruginosa}colonization.

It is clear that the COVID-19 pandemic affects individuals of all ages
psychologically, which is probably related to fear and anxiety (17-19).
Even though some studies have reported that patients with CF have higher
levels of anxiety than healthy controls (20), CF patients are born with
the disease, struggle with infections from an early age, routinely use
masks, and must take medicines daily without interruption; therefore,
the effects of the COVID-19 outbreak, such as wearing masks and
disinfecting hands, could be expected to affect children with CF less
than their healthy peers. In the present study STAI-S and STAI-T scores
in the CF patient group were significantly lower than in the control
group (P \textless{} 0.001 and P \textless{} 0.001, respectively), which
is in accordance with earlier reports (21).

Symptoms of anxiety are more common in adolescents and adults than in
the general population (22). In the present study anxiety scores were
significantly higher in the 14-18-year-old CF patients. Similarly, it
was reported that adolescents with non-CF bronchiectasis had higher
STAI-S scores than their healthy peers (23, 24). Children with CF
routinely experience exacerbation of lung symptoms, which can increase
their anxiety level during the COVID-19 pandemic; however, high anxiety
levels in healthy children may be due to the fact that they have not
encountered a serious illness prior to the COVID-19 pandemic. News that
Dornase alfa, which is used to treat CF, was an effective treatment for
COVID-19 may have calmed children with CF. In addition, STAI-T and
STAI-S scores in the present study's CF patients aged 8-14 years did not
differ from those in their healthy peers, which might have been due to
the fact that the patients were used to having lung problems.

In the present study HAD anxiety and HAD depression scores in the
parents of the CF patients were higher than in parents of controls, as
previously reported (25). As the presence of an accompanying chronic
illness that primarily affects the immune and respiratory systems would
likely increase the anxiety level to a greater degree in the parents of
healthy children, this was an expected finding (26).

Malnutrition is an important problem in CF patients. It was reported
that the degree of underweight in pediatric CF patients is an
independent factor that negatively affects survival, and more recently
short stature was identified as an independent risk factor for survival
(27, 28). Among the aims of the present study was to determine the
nutritional status of the CF patients via Telehealth Services and
intervene as necessary. The present findings show that the CF patients
improved their nutritional status during the COVID-19 pandemic (P =
0.002). There could be 2 reasons for this. The first is that the
patients attended school online due to the pandemic and spent more time
at home than usual; consequently, their parents could more easily
monitor their food intake. The other reason might be that the CF care
team canceled face-to-face appointments to avoid unnecessary risk for
the patients, but continued routine follow-up via teleconference, which
reduced the patients' and parents' anxiety and increases their
confidence in managing CF-related complications.

\textbf{Limitations}

Due to the COVID-19 pandemic, only some of the CF patients were
evaluated face to face, whereas the others were monitored via Telehealth
Services, which, considering the COVID-19 pandemic, was the ethical
choice, as it would have been unethical to schedule unnecessary face to
face evaluations due to the risk of COVID-19.

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