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\begin{document}

\title{Does hospitalization of a patient in the intensive care unit cause
anxiety and does restriction of visiting cause depression for the
relatives of these patients during COVID-19 pandemic?}



\author[1]{Behiye Kosovali}%
\author[1]{Nevzat Mehmet Mutlu}%
\author[1]{Canan Cam Gonen}%
\author[1]{Tulay Tuncer Peker}%
\author[1]{Asiye Yavuz}%
\author[1]{Ozlem Balkiz Soyal}%
\author[1]{Esra Cakir}%
\author[1]{Belgin Akan}%
\author[1]{Derya Gokcinar}%
\author[1]{Deniz Erdem}%
\author[1]{Isil Ozkocak  Turan}%
\affil[1]{Ankara City Hospital}%


\vspace{-1em}



  
  \date{May 26, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Objectives: During the pandemic, anxiety, stress, and depression may
occur increasingly in the whole society. To evaluate the possible cause,
incidence and levels of anxiety and depression in the relatives of the
patients in the ICU in accordance with the patients' SARS-CoV-2 PCR
result. Materials and Method: The study was prospectively conducted on
relatives of patients admitted to tertiary ICU during COVID-19 pandemic.
Sociodemographic characteristics of the patients and their relatives
were recorded. ``The Turkish version of the Hospital Anxiety and
Depression Scale'' questionnaire was applied twice to the relatives of
120 patients to determine the symptoms of anxiety and depression in
accordance with the PCR results of the patients (PCR positive n=60, PCR
negative n=60). Results: The ratios above cut-off values for anxiety and
depression among relatives of the patients were 45,8\% and 67,5\% for
the first test and 46,7\% and 62,5\% for the second test respectively.
The anxiety and depression in the relatives of PCR positive patients was
more frequent than the PCR negative (p\textless{} 0,001 for HADS-A and
p=0,034 for HADS-D). The prevalence of anxiety and depression was
significantly higher in female participants (p=0,046 for HADS-A and
p=0,009 for HADS-A). There was no significant correlation between HADS
and age of the patient or education of the participants. The fact that
the patients were hospitalized in the ICU during the pandemic was an
independent risk factor for anxiety (AUC = 0.746) while restriction of
patient visiting in the ICU was found to be an independent risk factor
for depression (AUC= 0.703). Conclusion: While patient with positive PCR
and participant with female gender is responsible for both anxiety and
depression, hospitalization in the ICU due to COVID-19 is an independent
risk factor for anxiety and restriction of patient visiting in the ICU
is an independent risk factor for depression.%
\end{abstract}%



\sloppy


\textbf{Does hospitalization of a patient in the intensive care unit
cause anxiety and does restriction of visiting cause depression for the
relatives of these patients during COVID-19 pandemic?}

\textbf{Abstract:}

\textbf{Objectives:} During the pandemic, anxiety, stress, and
depression may occur increasingly in the whole society. To evaluate the
possible cause, incidence and levels of anxiety and depression in the
relatives of the patients in the ICU in accordance with the patients'
SARS-CoV-2 PCR result.

\textbf{Materials and Method:} The study was prospectively conducted on
relatives of patients admitted to tertiary intensive care units during
COVID-19 pandemic. Sociodemographic characteristics of the patients and
their relatives were recorded. ``The Turkish version of the Hospital
Anxiety and Depression Scale'' questionnaire was applied twice to the
relatives of 120 patients to determine the symptoms of anxiety and
depression in accordance with the PCR results of the patients (PCR
positive n=60, PCR negative n=60).

\textbf{Results:} The ratios above cut-off values for anxiety and
depression among relatives of the patients were 45.8\% and 67.5\% for
the first test and 46.7\% and 62.5\% for the second test respectively.
The anxiety and depression in the relatives of PCR positive patients was
more frequent than the PCR negative (p\textless{} 0.001 for HADS-A and
p=0.034 for HADS-D). The prevalence of anxiety and depression was
significantly higher in female participants (p=0.046 for HADS-A and
p=0.009 for HADS-A). There was no significant correlation between HADS
and age of the patient or education of the participants. The fact that
the patients were hospitalized in the ICU during the pandemic was an
independent risk factor for anxiety (AUC = 0.746) while restriction of
patient visiting in the ICU was found to be an independent risk factor
for depression (AUC= 0.703).

\textbf{Conclusion:} While patient with positive PCR and participant
with female gender is responsible for both anxiety and depression,
hospitalization in the ICU due to COVID-19 is an independent risk factor
for anxiety and restriction of patient visiting in the ICU is an
independent risk factor for depression.

\textbf{Keywords:} Anxiety, depression, hospital anxiety depression
scale, intensive care unit, COVID-19, family members

\textbf{What's known?}

\begin{itemize}
\tightlist
\item
  Anxiety and depression levels of individuals increased in COVID-19
  pandemic.
\item
  The high rate of COVID-19 transmission worries the whole world.
\item
  Worries are increasing for various reasons.
\end{itemize}

\textbf{What's new?}

We determined some of the causes of anxiety and depression in the
relatives of patients treated ICU due to the COVID-19 in pandemic.

A relative is in the intensive care unit due to COVID-19 is an
independent risk factor for anxiety and the restriction of visits in the
ICU is an independent risk factor for depression.

\textbf{1 \textbar{} INTRODUCTION:}

COVID-19 disease caused by SARS-CoV-2 virus, which was first isolated in
Wuhan, China in December 2019, spread all over the world and caused a
pandemic in a short time. The pandemic and its consequences still cause
serious problems affecting people all over the world.

The answers to many questions such as how long the pandemic will last
and when it will end, whether the vaccine will be effective are not yet
clear. These uncertainties added to restrictions applied due to the
epidemic also negate the socioeconomic status. In addition to all these,
when COVID-19 is suspected in their loved ones, even otherwise healthy
people may show symptoms of sleeping problems, stress, anxiety, and
depression along with behaviors such as fear, anger, and
denial.\textsuperscript{1}

In Turkey, after the first case detected on 10th March 2020, despite
intermittent quarantine practices and social isolation, COVID-19 cases
persist and even rise. \textsuperscript{2} While some of these patients
were treated at home, some were treated in hospital wards and intensive
care units (ICU). Due to the high risk of human-to-human transmission of
the SARS-CoV-2 virus, infected individuals must isolate themselves from
the society as well as the family members throughout their illness. In
our country, The Ministry of Health restricted patient visits,
especially in the pandemic intensive care units starting from the
beginning of the pandemic for the same reason. Relatives of these
patients cannot see, touch, or talk to them under these circumstances.
Another difference from the pre-pandemic period is that doctors report
their patients' progress through phone calls, not face-to-face.

Anxiety and depression are not rare among relatives of the patients in
the ICU.\textsuperscript{3} During the pandemic, visit and interview
restrictions are expected to increase these symptoms. Even without a
pandemic, we can say that being a relative of an intensive care patient
is a stress factor itself while it is much worse in a pandemic which has
many uncertainties.

Various studies have been conducted to measure the degree of anxiety and
depression caused by the pandemic and quarantine period in various
patient groups or healthy individuals since the beginning of the
pandemic.\textsuperscript{4,5} Post-traumatic stress disorder, anxiety
and depression levels in general population are shown to be higher in
China, where the pandemic started and then Italy, which is one of the
most affected European countries, respectively.\textsuperscript{6,7} We
did not encounter any study in the literature concerning anxiety and
depression levels in the relatives of the patient being treated in the
ICU due to COVID-19.

The aim of this study is to evaluate the anxiety and depression levels,
incidences and the reasons causing them in the relatives of the patients
treated in the ICU with positive or negative SARS-CoV-2 test results.

\textbf{2 \textbar{} MATERIAL AND METHODS:}

\textbf{2.1 \textbar{} Patient Data}

Our study was prospectively conducted on the relatives of the patients
who were admitted to the tertiary pandemic intensive care units of
Ankara City Hospital between May 15th and July 15th, 2020 after the
approval of the ethics committee (Ethics committee number: E1-20-526).

This study included the native Turkish speaking relatives aged 18 and
over of 120 patients with clinical or radiological suspicion of COVID-19
on admission to ICU, half of whom received positive PCR results (n=60)
while the other half got negative PCR results (n=60). The consents of
the participants were obtained verbally during the phone call, due to
the pandemic and the Ministry of Health's restriction of the hospital
visits of the patient's relatives. The ``Hospital Anxiety and Depression
Scale (HADS)'' questionnaire was applied to the relative of the ICU
patient twice on phone by the intensive care doctor who followed the
patient and gave information. Before HADS questionnaire, 7 different
questions with 4-point scale ranging from 0 to 3 were asked to the
participants in order to determine the causes of anxiety and depression
(Table 1). HADS was first applied while the diagnosis of COVID-19 was
not yet clear, and then repeated when the PCR test results were
confirmed as positive or negative. Participants with previous or ongoing
psychiatric illness as well as the ones who refused to participate in
the study or cannot communicate and cooperate enough to complete the
questionnaires during phone call were excluded from the study. Patients
without confirmed PCR results were also excluded.

Gender, age, education (primary school, high school, university,
illiterate), marital status (married, single, divorced, widow) of the
patients and the participants were recorded. The patients were divided
into two groups according to the Acute Physiology and Chronic Health
Evaluation II (APACHE- II) score of the patient in the ICU as low
mortality risk ([?]20) and high mortality risk ([?]21) groups. Expected
mortality risks and PCR results were told to the participants on the
phone, before the second questionnaire was applied. According to World
Health Organization age classification, patients were divided into three
groups as 18-65 years, 66-80 years, 81-99 years.\textsuperscript{8} The
degree of kinship was evaluated in four groups including spouse, child,
relative or sibling. The occupations of the participants were classified
as private employee, civil servant, unemployed or student.

HADS questionnaire, found by Zigmond and Snaith and translated and
validated for the Turkish society by Aydemir et.al. was used to evaluate
the degree of anxiety and depression of the
participants.\textsuperscript{9,10} HADS consists of 14 questions with a
4-point scale ranging between 0-3 points. The general HADS score is the
total score of all the 14 questions asked (0-42 points) while anxiety
score (HADS-A) is calculated by adding up the 7 odd-numbered questions
(0-21 points) and the depression score (HADS-D) by adding up the 7
even-numbered questions (0-21 points). The HADS questionnaire was
administered to the participants on the phone and the score was
calculated using the answers recorded. According to the validation of
the HADS survey for the Turkish society, the values \textgreater{}10 and
\textgreater{}7 were considered as cut-off values for anxiety and
depression respectively (10). Participants were evaluated in 3 subgroups
for anxiety and depression as normal (0-10 for HADS-A and 0-7 for
HADS-D), moderate (11-15 for HADS-A and 8-10 for HADS-D) and high (16-21
for HADS-A and 11-21 for HADS-D).

\textbf{2.2 \textbar{} Statistical analysis:}

Statistical analysis of the data obtained in the study was evaluated
using the ``SPSS for windows 23.0'' statistical software. Continuous
variables were expressed as mean \selectlanguage{ngerman}± SD. After evaluating the conformity
of numerical data to normal distribution by Shapiro-Wilkins test,
student's t test was used to compare numerical data with normal
distribution and the result was evaluated according to the equality of
variances and Mann-Whitney U test was used to compare numerical data
without normal distribution. Categorical data was given as numbers.
Pearson Chi-Square test and Fisher Exact test were used to compare
categorical data. Paired t or Wilcoxon Rank test was used after
evaluating the compatibility of the difference to normal distribution in
the comparison of the first and second survey results. Logistic
regression analysis was performed to determine the factors associated
with the presence of depression and anxiety. ROC curves were drawn for
effective factors and the area under the curve (AUC) values were
calculated. \textless{}0.05 was considered significant.

Post hoc power analysis of the study was calculated with G-Power, the
power of the study was 86\% for the comparison made according to the PCR
result, 85\% for the comparison made according to the participant's
gender, 81\% for the comparison made according to the APACHE-II score
and the questions 1 and 3 obtained through logistic regression 88\% and
82\% respectively.

\textbf{3 \textbar{} RESULTS:}

The results of 120 out of 160 patients' relatives were included in the
statistical evaluation. Twenty two of the participants were excluded
because their patients were transferred to the ward from the ICU, before
the second test, 10 were excluded because their patients died before the
second test was performed, 7 were excluded because of unavailability
through phone, and 1 participant was excluded because the patient was
coming from a nursing home and the survey was taken by a staff, not a
relative.

When all patients evaluated, the average age was 70.22. Sixty (50\%)
patients were male with an average age of 66.48 and sixty (50\%) were
female with an average age of 73.95. Ninety two (76.7\%) of the patients
were married and 72 (60\%) of them were graduated from the primary
school. The average APACHE-II score was 17 and 34 (28\%) patients
required mechanical ventilator (Table 2).

When all participants were evaluated, the average age was 43.88. 72
(60\%) were male, 94 (78.3\%) were married, 54 (45\%) were graduated
from the university, 83 (69.2\%) were children of the patients, 53
(44.2\%) were private employee (Table 3).

While there was no difference in the averages of HADS, HADS-A and HADS-D
between the first and second surveys (p=0.572, p=0.974, p=0.190
respectively). Participants with HADS-A and HADS-D anxiety and
depression scale above the cut-off values were 45.8\% and 67.5\% for the
first test and 46.7\% and 62.5\% for the second test respectively (Table
4).

Although there was no statistically significant difference between the
averages of the first questionnaire according to the PCR results of the
patients (p=0.315), and the ratio of participants with PCR positive
patients who have higher survey scores then the cut-off values for
anxiety and depression were higher than the PCR negative patients both
in HADS-A (51.6\% for PCR positive, n=31 and 40\% for PCR negative,
n=24) and HADS-D (70 \% for PCR positive, n=41 and 65\% for PCR
negative, n=39) for the first questionnaire. When the results of the
second questionnaire were evaluated, HADS, HADS-A and HADS-D averages
were significantly higher (p=0.001, p\textless{}0.001, p=0.012
respectively), also the ratio of participants with PCR positive patients
who have higher survey scores then the cut-off values for anxiety and
depression were significantly higher than the PCR negative patients
(p\textless{}0.001 for HADS-A and p=0.034 for HADS-D) (Table 5).

When compared according to gender, the HADS and HADS-A scores of the
first questionnaire and the HADS-D scores of the first and second survey
were significantly higher in female then male participants (p=0.014,
0.046, 0.009, 0.049 respectively) (Table 6).

When HADS results were compared according to kinship, the HADS and
HADS-A results of the first questionnaire were significantly higher
among spouses of the patients than the other relatives (p=0.05 and
p=0.020 respectively) (Table 7).

When the first and second questionnaire HADS results were compared in
terms of APACHE-II score, there was no statistical difference (p=
0.919), but the HADS-D results of the second questionnaire were
significantly higher for patients with an APACHE-II score \selectlanguage{english}[?]21 (p= 0.042)
(Table 8).

The average HADS values of participants did not change according to age
of the patients, but the HADS average of the participants increased as
the age of the patients decreased and, although not statistically
significant, as the age of the patients increased, anxiety and
depression scales of the participants decreased (Table 9).

No significant relation was found between the education of the
participants and the HADS results (Table 10).

Logistic regression analysis was used to evaluate whether the answers to
the questions asked to the participants were independent risk factors
for anxiety and depression which showed patients' hospitalization in the
intensive care unit due to pandemic to be an independent risk factor for
anxiety among the participants while restrictions to visit patients in
the intensive care unit to be an independent risk factor for depression
(Table 11, Table 12). ROC curves were drawn. For anxiety in the
participants, AUC=0.746 for question 1 and for depression, AUC=0.703 for
question 3 (Figure 1, Figure 2).

Twenty five of the participants stated 10 different reasons for anxiety
and depression. Five of them feared death of their patient, 4 feared
infecting their families, 3 feared infecting other people, 3 feared the
length of time to recovery, 3 feared loss of their jobs or had financial
issues, 2 were upset about not getting convenient information through
regular calls, 1 was anxious about the education of his child, 1 was
anxious because he started working and could get infected, 1 expressed
concern about the general spread of the disease and the increasing
number of patients, while another expressed concern about the
insufficiency and unreliability of the data announced by the Ministry of
Health.

\textbf{4 \textbar{} DISCUSSION:}

Although there aren't any studies in the literature evaluating the
anxiety and depression in the relatives of the patients during the
pandemic, it has been reported before the pandemic that being a relative
of a hospitalized patient in the intensive care unit due to a
life-threatening disease is an important stress factor and may cause
anxiety and depression.\textsuperscript{11} Anxiety and depression rates
of relatives of patients in the ICU were evaluated by studies conducted
in different countries before the pandemic some of which are as follows:
69.1\% and 35.4\% in a multicenter trial in France, 71.8\% and 53.8\% in
a trial reported from Brazil, 60\% and 54\% in another trial from
Brazil, 35\% and 66\% in a trial from India, 35.9\% and 71.8\% in a
trial from Turkey respectively.\textsuperscript{11,12,13,14,15} As a
result of these trials preceding the pandemic, the anxiety levels in our
country is lower than France and Brazil, similar to India while
depression levels are higher than France, Brazil and India. When we
compare the rates of anxiety and depression in relatives of the patients
before the pandemic (35.9\% and 71.8\% respectively) by Kose et al. with
our study, we can roughly tell that anxiety levels rised (45.8-46.7\%)
while depression levels decreased (62.5-67.5\%) during the
pandemic.\textsuperscript{15}

Some of the studies showing the rates of anxiety and depression on the
general population during the pandemic are as follows: 29.83\% and
16.76\% in Russia, 35\% and 22\% in Austria, 28.8\% and 16.5\% in China,
and 45.1\% and 23.6\% in Turkey
respectively.\textsuperscript{16,17,18,19} In our country, the anxiety
rates in the general population were lower than Russia and Austria but
higher than China while depression rates were higher than the rest.
Apart from cultural differences, the differences in health care between
countries and the onset of the trials as the beginning or mid-pandemic
period or the level of awareness may be responsible for the results. One
of the reasons why the anxiety and depression rates in our study were
higher than China may be because in China, the study was carried out by
WHO as soon as the pandemic was declared while our study 3-6th months of
the pandemic in our country. The official onset of the pandemic was
different between countries as well.\textsuperscript{18} This later
onset of COVID-19 pandemic in our country may be cause of higher rates
of anxiety and depression because of the awareness of transmission
routes and speed as well as the mortality rates. National and social
media shares updated information about number of patients, deaths in the
country and the world which inclines day by day may also be responsible
for the anxiety and depression rates. Ozdin et al also conducted a study
concerning the anxiety and depression among healthy volunteers during
the pandemic.\textsuperscript{19} Depression rates of our study was
higher probably because of the population we chose.

In the literature, there is no similar study conducted with relatives of
patients hospitalized in ICU during pandemic. Our trial was started at
the beginning of the pandemic and all patients were admitted to ICU with
suspicion of COVID-19. The diagnosis was confirmed with PCR in addition
to clinical and radiological findings. The higher rates of anxiety and
depression in the relatives of patients with positive PCR test can be
explained by the serious concerns about the disease. A positive PCR also
eliminates the possibility of not having the disease and can incline
anxiety and depression.

In our study we found that symptoms of anxiety and depression are more
common in women during the pandemic, consistent with the studies prior
to pandemic showing female susceptibility to anxiety and
depression.\textsuperscript{20, 21} Studies from different countries
conducted in the general population since the beginning of the pandemic
also show tendency to anxiety and depression in female
gender.\textsuperscript{6,17,23,24} During the pandemic, female gender
was emphasized with regard to anxiety and depression in our country as
well.\textsuperscript{19} Hormonal changes during the menstrual cycle
can cause mood changes, which can cause women's reactions to events to
be more exaggerated or negative than men.\textsuperscript{25}Considering
that women have more posttraumatic stress symptoms such as negative
alteration of cognition and mood, re-experiencing and hyperarousal than
men in the COVID-19 epidemic, they are expected to have more anxiety and
depression symptoms due to both the pandemic and the anxiety they feel
for the wellbeing of their patients.\textsuperscript{23} Another factor
affecting depression is the role that societies attribute to genders
depending on cultural differences.\textsuperscript{22} Although the
study is carried out in the capital of our country, the cultural mosaic
in the city can reflect almost every region of our country since it is a
city that continues to receive immigrants from all over the country. In
some societies, the under-reacting of women to the events is regarded as
abnormal, while in some regions, the overreaction of men is abnormal.
Due to the place of men in society and the role assigned to them, men
can show their emotions less than women. The characteristics of the
regions where people come from, where they grow up, family and economic
structure may be factors that make the reactions of women and men
different from each other. Cultural characteristics and the acceptance
that the female gender may be emotionally reactive in life may explain
the higher frequency of anxiety and depression among females.

Another factor in which anxiety and depression rates were significantly
higher in our study was if the participant was the spouse of the
patient. After the spouses, the children, relatives, and siblings of the
patients followed the frequency of symptoms of anxiety and depression
among the relatives. The result of our study was consistent with
previous studies.\textsuperscript{15,27} Because the spouses share a
house, a life, and values, one's illness of affects the surviving spouse
both emotionally and socioeconomically. Therefore, we believe that it is
an expected result that the symptoms of anxiety and depression are more
common in spouses compared to other relatives of the ICU patients.

People aged 65 and over are more likely to have COVID-19 disease and
especially respiratory failure and the need for intensive care than
younger patients. However younger patients may also need treatment in
intensive care and death of these patients is more devastating for their
relatives. In our study, although the age of the patient did not
significantly affect the anxiety and depression levels of their
relatives, the rates of high anxiety and depression was higher in the
relatives of young patients than those of middle and elderly patients.
In this aspect, it was consistent with the results of other
studies.\textsuperscript{13,26} In the literature, there is no
difference between the anxiety and depression levels of the relatives of
ICU patients in terms of scores predicting mortality or the education
level of the patients' relatives.\textsuperscript{15,29,30} In our
study, we observed that learning the severity of the disease (high
APACHE-II score) by the relatives of the patients did not increase the
anxiety level, but it increased the depression. The higher incidence of
depression among the relatives of the patients in the ICU can be because
their patients are hospitalized in intensive care with the diagnosis of
COVID-19, knowing that their condition is more severe and possibly
lethal. Most of the participants in the study were university graduates,
and although the lowest anxiety and depression levels were found in this
group, and there was no significant relationship between the education
level of the participants and their anxiety or depression levels. This
suggests that education may be effective in the perception process and
acceptance of results, but still cannot fully control emotional
responses. Our study associates anxiety with COVID-19 as an independent
risk factor in accordance with to the answer given to the question ``How
concerning is your patient's hospitalization in the ICU due to an
epidemic?'' by the participants. A relative hospitalized in the ICU due
to an epidemic was found to be effective in the development of anxiety.

With the restrictions made to prevent transmission during the pandemic
period and the prohibition of daily patient visits, patients' relatives
could not visit their patients in the intensive care environment.
Therefore, we think that the lack of seeing, communicating and physical
contact in the ICU increases the curiosity and anxiety of the relatives
of the patients. Not being able to visit and see a patient was found to
be an independent risk factor for the development of depression in the
participants.

There may be many different factors that can cause anxiety and
depression on people during the pandemic period. Since we had only 25
participants who answered the question about other causes of anxiety and
depression, these answers were not evaluated statistically. From these
answers, which we have also stated in the findings section, we think
that 10 different reasons may cause anxiety in the relatives of the
patient during the pandemic process. We believe that these reasons
should be questioned in future studies investigating the causes of
anxiety and depression.

In conclusion, during the pandemic period, the fact that a relative is
in the intensive care unit due to COVID-19 is an independent risk factor
for anxiety and the restriction of visits in the ICU is an independent
risk factor for depression.

Limitations: Single center, the number of participants, taking the
questionnaire by phone are the limitations of our study.

\textbf{Author Contributions:}

Behiye Deniz Kosovali: Concept/design, Data analysis/interpretation,
Data collection, Drafting article

Nevzat Mehmet Mutlu: Concept/design, Data collection

Canan Cam Gonen: Data collection

Tulay Tuncer Peker: Data analysis/interpretation, Statistics

Asiye Yavuz: Data collection

Ozlem Balkiz Soyal: Data analysis/interpretation, Drafting article

Esra Cak\selectlanguage{polish}ı\selectlanguage{english}r: Data collection

Belgin Akan: Data collection

Derya Gokcinar: Data collection

Deniz Erdem: Data collection

Is\selectlanguage{polish}ı\selectlanguage{english}l Ozkocak Turan: Data collection

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