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Environmental Science and Pollution Research (2022) 29:28062–28069

https://doi.org/10.1007/s11356-021-18384-4

RESEARCH ARTICLE

Circadian rhythm disorder and anxiety as mental health complications


in post‑COVID‑19
Dmytro I. Boiko1 · Andrii M. Skrypnikov1 · Anastasiia D. Shkodina2,3 · Mohammad Mehedi Hasan4 ·
Ghulam Md. Ashraf5,6 · Md. Habibur Rahman7,8 

Received: 23 November 2021 / Accepted: 24 December 2021 / Published online: 5 January 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022

Abstract
In 2020, the world gained dramatic experience of the development of the 2019 coronavirus disease pandemic (COVID-19)
caused by severe acute respiratory syndrome 2 (SARS-CoV-2). Recent researches notice an increasing prevalence of anxiety
and circadian rhythm disorders during COVID-19 pandemic. The aim of the study was describing clinical features of circa-
dian rhythm disorders and the level of anxiety in persons who have had COVID-19. We have conducted a cohort retrospec-
tive study that included 278 patients who were divided into 2 study groups according to medical history: group 1 includes
patients with a history of COVID-19; group 2 consists of patients who did not have clinically confirmed COVID-19 and are
therefore considered not to have had this disease. To objectify circadian rhythm disorders, they were verified in accordance
with the criteria of the International Classification of Sleep Disorders-3. The level of anxiety was assessed by the State-Trait
Anxiety Inventory. The most common circadian rhythm disorders were sleep phase shifts. We found that COVID-19 in the
anamnesis caused a greater predisposition of patients to the development of circadian rhythm disorders, in particular delayed
sleep phase disorder. In addition, it was found that after COVID-19 patients have increased levels of both trait and state
anxiety. In our study, it was the first time that relationships between post-COVID-19 anxiety and circadian rhythm disorders
had been indicated. Circadian rhythm disorders are associated with increased trait and state anxiety, which may indicate
additional ways to correct post-COVID mental disorders and their comorbidity with sleep disorders.

Keywords  COVID-19 · Circadian rhythm · Anxiety · Mood disorders · Sleep disorders · Cohort retrospective study

Responsible Editor: Lotfi Aleya

3
* Anastasiia D. Shkodina Neurological Department, Municipal Enterprise, “City
ad.shkodina@gmail.com Clinical Hospital of Poltava City Council”, Poltava, Ukraine
4
* Md. Habibur Rahman Department of Biochemistry and Molecular Biology, Faculty
pharmacisthabib@gmail.com of Life Science, MawlanaBhashani Science and Technology
University, Tangail, Bangladesh
Dmytro I. Boiko
5
bojko998@gmail.com Pre‑Clinical Research Unit, King Fahd Medical Research
Center, King Abdulaziz University, Jeddah, Saudi Arabia
Andrii M. Skrypnikov
6
skrypnikovandrii@gmail.com Department of Medical Laboratory Technology, Faculty
of Applied Medical Sciences, King Abdulaziz University,
Mohammad Mehedi Hasan
Jeddah, Saudi Arabia
mehedi.bmb.mbstu@gmail.com
7
Department of Pharmacy, Southeast University, Banani,
Ghulam Md. Ashraf
Dhaka 1213, Bangladesh
ashraf.gm@gmail.com
8
Department of Global Medical Science, Wonju College
1
Department of Psychiatry, Narcology and Medical of Medicine, Yonsei University, Wonju 26426, Gangwon‑do,
Psychology, Poltava State Medical University, Poltava, Korea
Ukraine
2
Department of Neurological Diseases With Neurosurgery
and Medical Genetics, Poltava State Medical University,
Poltava, Ukraine

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Environmental Science and Pollution Research (2022) 29:28062–28069 28063

Introduction fear in an emotional response to a real or perceived immi-


nent threat. In addition, this term in the DSM-5 includes
In 2020, the world gained dramatic experience of the devel- an additional component, namely the cognitive aspects of
opment of the 2019 coronavirus disease pandemic (COVID- anxious expectation (Kupfer 2015). In the general popula-
19) caused by SARS-CoV-2. Based on previous studies, tion, anxiety disorders are usually chronic. To prevent and
SARS-CoV-2 penetrates the blood–brain barrier and can control chronic disease, timely treatment and management
directly affect the nervous tissue, which causes the develop- of chronic diseases are necessary, which can be achieved
ment of neurological and psychiatric symptoms (Hossain by identifying indicators of risk of chronicity (Ten Have
et al. 2020) (Sharma et al. 2021) (Rahman et al. 2020). At et al. 2021).
the same time, quarantine and social distancing have a sig- Environmental factors can affect the infectivity and sur-
nificant impact on the psychological state of the population. vival of the coronavirus. Several epidemiological and labo-
Separation from relatives, loss of freedom, uncertainty about ratory studies show that outbreaks of coronavirus disease
disease status, and boredom can sometimes have dramatic and the rate at which it spreads depend on climate, weather
effects. Serious socioeconomic losses can be a risk aspect for conditions and population density (Doğan et  al. 2020;
signs of mental disorders, in particular anxiety. Fear of infec- Shahzad et al. 2021). The seasons are considered to be a
tion, economic hardship, and stigma are important ingredi- significant environmental factor influencing the initiation
ents that lead to mental health problems during COVID-19 and further dynamics of mental disorders due to a number of
too (Akter et al. 2021)(Kaur et al. 2021). Despite the sig- heliometeorological factors determining biological rhythms
nificant amount of research on various aspects of the patho- such as the circadian functioning of the human body. It has
genesis and treatment of COVID-19, there are still many been established that there is a multi-vector network between
unresolved issues of the effectiveness of the therapy of such medico-biological phenomena and biorhythmological fea-
patients, especially the amount of psychosocial interventions tures of people suffered mental disorders (Zhyvotovska et al.
and predictors of long-term prognosis (Ivanova et al. 2020). 2017). Circadian rhythm disorders and sleep disorders are
Recently, there have been a growing number of reports conditions that under normal circumstances rarely attract
of symptoms that persist in the post-COVID period. the attention of doctors. However, it is important to keep in
Although studies of the classification of long-term effects mind that circadian rhythms are a factor in the optimization
remain at an early stage, researchers distinguish, among of the immune system. The most constitutive risk factors are
others, neurocognitive, psychological, and neurologi- genetic. The known association of affective disorders with
cal post-COVID syndromes, which are characterized by the functioning of circadian rhythms makes it possible to
involvement of the nervous system (Alsharif and Qurashi study clock genes as predictors of anxiety. Although clock
2021; Maltezou et al. 2021). genes have been implicated in regulating mood, the extent
In a research authored by Fernández-de-las-Peñas et al. to which they can influence affective disorders is not well
(2021b), the following classification for post-COVID symp- understood. The PER3 and BMAL1 genes, which influence
toms was proposed (Fernández-de-las-Peñas et al. 2021b): daytime mood, may be promising candidates (Landgraf et al.
2016; Liberman et al. 2017).
Transition phase: acute COVID-19 (up to 5 weeks); During the early period of the COVID pandemic, the
Phase 1: acute post-COVID symptoms (weeks 5–12); attention of researchers was drawn to non-pharmacological
Phase 2: long post-COVID symptoms (weeks 12–24); methods of treatment of this disease (Tagde et al., 2021)
Phase 3: persistent post-COVID symptoms (more than (Hussain et  al., 2021). Desynchronization of circadian
24 weeks). rhythm and immune system can lead to increased suscepti-
bility to infectious diseases and affect their course (Bryson
Meta-analysis of Xiong et al. (2020) shows an increase 2020). Circadian rhythm disorders and sleep disorders are
in the incidence of anxiety disorders from 6.3% to 50.9% closely related to changes in mental status and the devel-
after COVID-19 (Xiong et al. 2020). In addition, it is esti- opment of affective disorders, including anxiety syndrome
mated that anxiety symptoms persist in approximately 15% (Boiko et  al. 2017; Difrancesco et  al. 2019; Silva et  al.
of patients in the post-COVID period (Rogers et al. 2020), 2020). There is evidence of an association between certain
while 47% COVID-19 patients noticed experiencing anxi- polymorphisms of ‘internal clock’ genes, which are associ-
ety (Deng et al. 2021). It shows a great deal of anxiety in ated with chronotype features and disorders of the circa-
post-COVID syndrome, but exact range of its prevalence dian system, with the development of affective disorders,
remains unclear. including anxiety and depression (Partonen 2012; Sipilä
According to the definition from the DSM-5, anxiety et al. 2010). Animal models indicate circadian changes in
is the expectation of a future threat, which differs from serotonin secretion in rats with anxiety disorders (Bacqué-
Cazenave et al. 2020), which may be one of the common

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links in the pathogenesis between affective disorders and The study groups were representative by age and sex. The
circadian dysfunction. In addition, circadian rhythms are mean age of patients in group 1 was 39.6 ± 3.8 years, and in
reported to play a significant role in the regulation of meta- group 2—41.9 ± 4.6 years, which had no statistically signifi-
bolic processes and the metabolism of neurotransmitters cant differences (p = 0.643). The gender composition of all
(Tarianyk et al. 2021). Recent studies indicate a link between studied groups was equal and comparable without signifi-
sleep phase shift disorders and high levels of stress and anxi- cant differences between the groups (χ2 = 3,841, p = 0,504),
ety, which in combination with neurobiological components namely 82 (53.6 ± 4.03%) men and 71 (46.4 ± 4.03%) women
may presuppose comorbidity of these conditions (Gradisar in group 1 and 72 (57.6 ± 4.42%) and 53 (42.4 ± 4.42%) in
and Crowley 2013; Kivelä et al. 2018). group 2, respectively.
However, the severity of anxiety in circadian rhythm dis- During the examination of the patient, a clinical interview
orders on the background of COVID-19 has not been studied was conducted detailing the complaints and anamnestic data.
yet. The aim of the study was describing the prevalence of Collection of information on the clinical course of COVID-
circadian rhythm disorders and its links to the level of anxi- 19 was performed by analyzing both outpatient cards and
ety in persons who have had COVID-19. extracts from inpatient cards.

Circadian rhythm disorders

Materials and methods To objectify circadian rhythm disorders, they were verified


in accordance with the criteria of the International Clas-
Inclusion and exclusion criteria sification of Sleep Disorders-3, which includes advanced
sleep phase disorder, delayed sleep phase disorder, irregular
We have conducted a cohort retrospective study that included sleep phase disorder, non-24-h sleep–wake disorder, jet lag,
278 patients who consulted a family doctor for a preventive and shift work sleep disorders, others (not classified in other
examination during 2021. This has limited a certain number headings) (Berry 2012; Sateia 2014).
of patients in study groups. Criteria for inclusion in the study To assess the function of the circadian rhythm, we used
were age from 18 to 59 years, complaints of sleep disorders a sleep diary, which was filled in by the patient for 7 days
and anxiety, 5-day work schedule with peak activity in day- before the first visit, and data from daily thermometry, which
light. Exclusion criteria: age from 60 years, somatic pathol- was performed by the patient every 3 h.
ogy in the stages of sub- and decompensation, severe mental The following criteria were used to confirm circadian
disorders. The age was limited because younger people were rhythm disorders:
children and were treated in children’s hospitals. People aged a) persistent or recurring because of:
more than 60 years were elderly according to the WHO clas-
sification. It means that they have more accompanying ill- damage to the circadian rhythm system;
nesses with a brain injury that can cause anxiety. mismatch of internal rhythm and external factors;

b) lead to insomnia and/or excessive daytime sleepiness;


Grouping c) related to the disturbances in social, professional, and
other spheres of activity;
All patients included in the study gave informed consent. d) cannot be better explained by another sleep disorder,
The study was conducted in compliance with the basic provi- neurological or mental disorder, medication and substance
sions of the ‘Ethical principles of scientific medical research use.
involving human subjects,’ approved by the Declaration of
Helsinki (1964–2013), guidelines good clinical practice Level of anxiety measurement
(ICH GCP) (1996), orders of the Ministry of Health of
Ukraine № 690 dated 23.09.2009, № 944 dated 14.12.2009, The level of anxiety was assessed by the State-Trait Anxi-
№ 616 dated 03.08.2012. ety Inventory (STAI). It consists of 40 questions divided
Patients were divided into 2 study groups: into two blocks, the first of which is responsible for trait
anxiety, and the second—for state. The scale of trait anxi-
group 1 (n = 153)—patients with a history of COVID-19; ety describes anxiety as a characteristic permanent behav-
group 2 (n = 125)—patients who did not have clinically ioral trait, due to which a person perceives objectively safe
confirmed COVID-19 and are therefore considered not to things as a source of danger. At the same time, the state scale
have had this disease. characterizes the emotional reaction to the current situation.
Each of the 40 questions contains a Likert-scale answer in

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the form of a statement from 1 point (never) to 4 points contact with carriers and assumed the possibility of the
(very often). A separate sum of points is calculated for each disease development, another 48 (31.4 ± 3.7%) patients
block, which can vary from 20 to 80 points, whereby a larger considered having had no prior contact with infected per-
amount corresponds to a higher intensity of anxiety. It is sons, however, admitted the possibility of COVID onset,
considered that < 30 points are a low level of anxiety, 31–45 and 61 (39.9 ± 3.9%) patients were sure that they would
points—moderate, > 45 points—high (Julian 2011). not get sick.
According to the results of daily thermometry and entries
Statistical analysis in sleep diaries, we identified 118 (77.1 ± 3.39%) cases of
circadian rhythm disorders among patients of group 1 and
Statistical analysis was performed using EZR Statistics 67 (53.6 ± 4.46%) among patients of group 2, which are
v.1.13 and Microsoft Office Excel 2019. Qualitative vari- shown in Table 1. It was found that the presence of circa-
ables were presented in the form of absolute values (abs.) dian rhythm disorders is more typical for persons of group
and relative value (P) with the calculation of relative error 1 (χ2 = 16.06, p < 0.001). Among circadian rhythm disor-
(p). To compare qualitative data, χ2-Pearson with Yates ders in group 1, advanced sleep phase disorder was found
correction was used. To analyze the risk of comorbidity in 28 (23.7 ± 3.9%) patients, delayed sleep phase disorder
of nosologies, the calculation of the risk ratio with a 95% in 61 (51.7 ± 4.6%), irregular sleep phase disorders—in 18
confidence interval was used. The results were considered (15.3 ± 3.3%), non-24-h rhythm—in 8 (6.7 ± 2.3%), others—
statistically significant at p < 0.05. in 3 (2.5 ± 1.4%) patients.
Among the latter, 1 jetlag syndrome and 2 shift works
sleep disorders were identified. In group 2, advanced sleep
Results and discussion phase disorder was found in 19 (28.4 ± 5.5%) patients,
delayed sleep phase disorder—in 24 (35.8 ± 5.9%), irreg-
The mean period until the COVID-19 clinical onset from the ular sleep phase disorder—in 17 (25.4 ± 5.3%), non-24-h
time of examination in group 1 patients was 7.6 ± 1.1 weeks. rhythm—in 3 (4.5 ± 2.5%), others (shift work sleep disor-
Among them, 113 (73.8 ± 3.6%) people reported the pres- der)—in 2 patients.
ence of respiratory system symptoms, 96 (57.0 ± 4.01%)— We found that the history of COVID-19 was not associ-
nervous system symptoms, 67 (43.8 ± 4.02%)—hemato- ated with the risk of developing advanced sleep phase dis-
logical abnormalities, 26 (16.9 ± 3.04%)—cardiovascular order (RR = 0.84, 95% CI 0.51–1.38), irregular sleep phase
symptoms, 14 (9.15 ± 2.5%)—gastrointestinal disorders, disorders (RR = 0.61, 95% CI 0.33–1.09) and non-24-h cir-
and 4 (2.6 ± 1.3%)—urinary system disorders. Regarding the cadian rhythm (RR = 1.51, 95% CI 0.42–5.52). At the same
nervous system issues in particular, in accordance with med- time, the presence of a history of COVID-19 increased the
ical records in patients with COVID-19 there were olfactory risk of developing delayed sleep phase disorders by 1.5 times
disorders in 71 (73.9 ± 4.5%) patients, taste disturbances in (RR = 1.44, 95% CI 1.01–2.08). Other circadian rhythm dis-
64 (66.7 ± 4.8%) patients, ataxia in 11 (11.5 ± 3.3%) patients orders were relatively isolated, so they are not subject to
and peripheral nerve damage in 9 (9.4 ± 2.9%) patients. statistical analysis due to the lack of data.
Among patients who have had COVID-19, only 44 In group 1, low levels of trait anxiety were found in 64
(28.8 ± 3.7%) patients considered themselves to be in patients, moderate—in 65, and high—in 24, while in group

Table 1  Distribution of levels Circadian rhythm disorder Level of trait anxiety


of trait anxiety depending on
different types of circadian Group 1 (n = 153) Group 2 (n = 125)
rhythm disorders, taking
into account the presence of Type Yes/No Low Middle High Low Middle High
COVID-19 in the anamnesis,
DSPD Yes 9 (5.9%) 35 (22.9%) 17 (11.1%) 3 (2.4%) 5 (4.0%) 16 (12.8%)
abs. (P%)
No 55 (29.4%) 30 (19.6%) 7 (4.6%) 69 (55.2%) 29 (23.2%) 3 (2.4%)
ASPD Yes 9 (5.9%) 16 (5.9%) 3 (2.0%) 8 (6.4%) 6 (4.8%) 5 (4.0%)
No 55 (29.4%) 49 (32.0%) 21 (13.7%) 64 (51.2%) 28 (22.4%) 14 (11.2%)
ISPD Yes 4 (2.6%) 11 (7.2%) 3 (2.0%) 10 (8.0%) 4 (3.2%) 3 (2.4%)
No 61 (39.9%) 54 (35.3%) 21 (13.7%) 62 (49.6%) 30 (24.0%) 16 (12.8%)
Non-24-h rhythm Yes 1 (0.65%) 1 (0.65%) 6 (3.9%) 0 (0%) 2 (1.6%) 1 (0.8%)
No 63 (41.2%) 64 (41.8%) 18 (11.8%) 72 (57.6%) 32 (25.6%) 18 (14.4%)

Note. DSPD—delayed sleep phase disorder, ASPD—advanced sleep phase disorder, ISPD—irregular sleep
phase disorder

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Fig. 1  Level of trait anxiety in


patients who either have had
(group 1) or haven’t had (group
2) COVID-19

2, low levels were found in 72 people, moderate—in 34, and The levels of trait anxiety in patients with various forms
high—in 19, which is presented in Fig. 1. of circadian rhythm disorders, taking into account the
It was found that in the group of patients with COVID- presence of COVID-19 in the anamnesis, are presented in
19 in the anamnesis, a moderate level of trait anxiety pre- Table 1.
vailed, compared to the group 2, where a low level prevailed In group 1, the increase in the level of trait anxiety was
(χ2 = 8.02, p = 0.019). associated with the presence of a delayed sleep phase dis-
The level of state anxiety in group 1 was low in 46 people, order (χ2 = 32.67, p < 0.001), non-24-h rhythm (χ2 = 7.21,
moderate—in 48, and high—in 59, and in group 2 54 people p = 0.021) and a disorder of the irregular phase of sleep
had low levels, 47—moderate and in 24—high, which is (χ2 = 22.46, p < 0.001). At the same time, patients in group 1
presented in Fig. 2. who were diagnosed with advanced sleep phase disorder, no
It was determined that in patients who have had COVID- significant differences (χ2 = 5.87, p = 0.0542) in the severity
19, there is statistically significant higher intensity of state of personal anxiety compared with those who did not have
anxiety and its high level prevails, while in patients haven’t this disorder.
had COVID-19 low and moderate levels of anxiety were the Group 2 was characterized by an increase in per-
most common (χ2 = 12, 72, p = 0.002). sonal anxiety with the concurrent delayed sleep phase

Fig. 2  Level of state anxiety in


patients who either have had
(group 1) or haven’t had (group
2) COVID-19

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disorder (χ2 = 62.69, p < 0.001), but no differences were There are a variety of data on the frequency of their occur-
found between the level of anxiety while detecting disor- rence, which ranges from 16 to 45% (Chen et al. 2021;
ders of early (χ2 = 2.91, p = 0.234) and irregular (χ2 = 0.180, Fernández-de-las-Peñas et al. 2021a).
p = 0.091) phases of sleep or non-24-h rhythm (χ2 = 4.19, The most common circadian rhythm disorders were
p = 0.122). sleep phase shifts. We found that COVID-19 in the anam-
The distribution of levels of state anxiety in patients nesis caused a greater predisposition of patients to the
with various forms of circadian rhythm disorders, taking development of circadian rhythm disorders, in particular
into account the presence of COVID-19 in the anamnesis, delayed sleep phase disorder. In addition, it was found that
is presented in Table 2. after COVID-19 patients have increased levels of both trait
An increase in state anxiety in group 1 and group 2 and state anxiety. The prevalence of delayed sleep phase
was found in patients with delayed sleep phase disorder disorder may be due to both the neurotropic nature of the
(χ2 = 34.46, p < 0.001 and χ2 = 66.53, p < 0.001, respec- SARS-CoV-2 and the quarantine associated with COVID-
tively), irregular sleep phase disorders (χ2 = 31,89, p < 0.001 19 pandemic. Thus, the effect of a change in light expo-
and χ2 = 18.71, p < 0.001, respectively) and non-24-h sure under lockdown conditions on daily functioning was
rhythm (χ 2 = 31.85, p < 0.001 and χ2 = 20.79, p < 0.001, observed, namely a shift of the rhythm by 3 or more hours
respectively). The presence of advanced sleep phase disorder ahead. This has led to a decrease in exposure to natural
was not associated with more pronounced state anxiety in light, which affects the central circadian oscillator, which
both group 1 (χ2 = 0.72, p = 0.712) and group 2 (χ2 = 0.26, can also affect physical and nutritional activity (Bertrand
p = 0.881). It was not possible to estimate the differences et al. 2021; Leone et al. 2020). It was also noted that the
in the intensity of trait and state anxiety in patients with delay in sleep during a pandemic is associated with a
jet lag and shift work disorder due to the small number of worse quality of sleep and the psychological state of the
observations. respondents, and as a result, reduces the quality of their
Symptoms of respiratory and nervous system damage life and the degree of disability (Robillard et al. 2021).
predominated in patients who had COVID-19. Among the Some limitations of our study should be considered. In
latter, there were disturbances of smell and taste, ataxia and particular, it was conducted within one hospital. It will be
damage to peripheral nerves, which, in turn, may indicate useful to conduct similar studies in different countries in
the neurotoxicity of the SARS-CoV-2 virus. order to accumulate sufficient data. In addition, we were
On the other hand, the fact of coronavirus infection limited by clinical interviews without neurophysiological
itself could act as a psycho-traumatic factor that caused study of sleep structure or analysis of circadian biomark-
changes in the mental state of patients, as most of them ers. The study of these features may play an important role
considered themselves protected and insensitive to the in establishing a link between post-COVID-19 anxiety and
disease, i.e., did not expect the onset of COVID. In addi- circadian rhythm disorders. Furthermore, investigating of
tion, the long-term quarantine measures that have been the chronotype of patients may be useful, which is usu-
introduced due to the pandemic have affected both the ally considered as the middle of a sleep time on the free
mental and physical conditions of people. A high preva- day. It is intriguing in further research to study the role of
lence of anxiety disorders has been reported both in the chronotype in the formation of circadian rhythm disorders
acute period of COVID-19 and within 6–7 months after it. and increased post-COVID-19 anxiety.

Table 2  Distribution of levels Circadian rhythm disorder Level of state anxiety


of state anxiety depending on
different types of circadian Group 1 (n = 153) Group 2 (n = 125)
rhythm disorders, taking
into account the presence of Type Yes\No Low Middle High Low Middle High
COVID-19 in the anamnesis,
DSPD Yes 9 (5.9%) 33 (21.6%) 19 (12.4%) 1 (0.8%) 7 (5.6%) 16 (12.8%)
abs. (P%)
No 55 (29.4%) 32 (20.9%) 5 (3.3%) 71 (56.8%) 27 (21.6%) 3 (2.4%)
ASPD Yes 13 (8.5%) 12 (7.8%) 3 (2.0%) 10 (8.0%) 6 (4.8%) 3 (2.4%)
No 51 (33.3%) 53 (34.6%) 21 (13.7%) 62 (49.6%) 28 (22.4%) 16 (12.8%)
ISPD Yes 3 (2.0%) 4 (2.6%) 11 (7.2%) 4 (3.2%) 12 (9.6%) 1 (0.8%)
No 61 (39.9%) 61 (39.9%) 13 (8.5%) 68 (54.4%) 22 (17.6%) 18 (14.4%)
Non-24-h rhythm Yes 0 (0%) 3 (2.0%) 5 (3.3%) 0 (0%) 0 (0%) 3 (2.4%)
No 64 (41.8%) 62 (40.5%) 19 (12.4%) 72 (57.6%) 34 (27.2%) 16 (12.8%)

Note. DSPD—delayed sleep phase disorder, ASPD—advanced sleep phase disorder, ISPD—irregular sleep
phase disorder

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The relationship between the severity of anxiety syn- Declarations 


drome and circadian rhythm disorders in the post-COVID
period has been established. Delayed sleep phase disor- Ethical approval  Not applicable.
der, irregular sleep phase disorder, and non-24-h rhythm
Consent to participate  Not Applicable.
had the most pronounced link to the increased levels of
anxiety. These conditions are accompanied by a process Consent to publish  Not Applicable.
of maladaptation due to an imbalance between the socially
Competing interest  Not Applicable.
acceptable work schedule and the daily functioning of the
patient.

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man performed conceptualization, methodology, and supervision; nyas.​14506
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Funding  This work was supported by the Deanship of Scientific Doğan B, Ben Jebli M, Shahzad K, Farooq TH, Shahzad U (2020)
Research (DSR), King Abdulaziz University, Jeddah, under Grant No. Investigating the Effects of Meteorological Parameters on
(DF-538–141-1441). The authors, therefore, gratefully acknowledge COVID-19: Case Study of New Jersey, United States. Environ
the DSR technical and financial support. Res, 191, 110148. Retrieved from https://d​ oi.o​ rg/1​ 0.1​ 016/j.e​ nvres.​
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