EDITED BY
Reza Lashgari,
Shahid Beheshti University, Iran
REVIEWED BY
Maria Chiara Maccarone,
University Hospital of Padua, Italy
Massimiliano Mangone,
Sapienza University of Rome, Italy
Nenad Stojiljkovic,
University of Nis, Serbia
Alexandra Makai,
University of Pécs, Hungary
*CORRESPONDENCE
Kaja Teraž
RECEIVED 29 April 2023
ACCEPTED 10 July 2023
PUBLISHED 21 July 2023
CITATION
TeražK, ŠimuničB, Peskar M, Marusic U, Pišot S,
Šlosar L, Gasparini M and Pišot R (2023)
Functional characteristics and subjective
disease perception in patients with COVID-19
two months after hospital discharge.
Front. Rehabil. Sci. 4:1209900.
doi: 10.3389/fresc.2023.1209900
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© 2023 Teraž,Šimunič, Peskar, Marusic, Pišot,
Šlosar, Gasparini and Pišot. This is an open-
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The use, distribution or reproduction in other
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comply with these terms.
Functional characteristics and
subjective disease perception in
patients with COVID-19 two
months after hospital discharge
Kaja Teraž1,2*,Boštjan Šimunič1, Manca Peskar1,3, Uros Marusic1,4,
SašaPišot1, Luka Šlosar1,4, Malden Gasparini5and Rado Pišot1
1
Institute for Kinesiology Research, Science and Research Centre Koper, Koper, Slovenia,
2
Faculty of Sport,
University of Ljubljana, Ljubljana, Slovenia,
3
Biological Psychology and Neuroergonomics, Department of
Psychology and Ergonomics, Faculty V: Mechanical Engineering and Transport Systems, Technische
Universität Berlin, Berlin, Germany,
4
Department of Health Sciences, Alma Mater Europaea –ECM,
Maribor, Slovenia,
5
Department of General Surgery, General Hospital Izola, Izola, Slovenia
Introduction: Although early inpatient and post-hospital rehabilitation is recognized
as necessary, not all COVID-19 patients have access to rehabilitation. There are no
published reports in the literature that investigate the outcomes of patients who do
not receive rehabilitation after COVID-19. Our aim was to evaluate possible
improvements in determinate functional and psychological parameters in COVID-
19 patients two months after their hospital discharge.
Methods: On both time points various motor, cognitive, and clinical measurements
such as body composition, tensiomyography, blood pressure, spirometry, grip
strength test, Timed Up and Go test, gait speed, 30-second chair-stand test, and
Montreal Cognitive Assessment, were performed. Additionally, questionnaires such as
the SARC-CalF test, Edmonton frail scale, International Physical Activity questionnaire
andThe Mediterranean Lifestyle index were conducted to assess lifestyle characteristics.
Results: A total of 39 patients (87.2% male; mean age of 59.1 ± 10.3 years), who were
hospitalized due to COVID-19 at the Izola General Hospital (IGH), Slovenia between
December 2020 and April 2021, were included. Patients were assessed at two time
points (T
1
and T
2
): T
1
was taken after receiving a negative COVID-19 test and T
2
was
taken two months after T
1
. After two months of self-rehabilitation, we have detected
a BMI increase (p< .001), fat free mass increase (p<.001), better Edmonton frail
scale (p< .001), SARC-CalF score (p=.014)andMoCAscore(p= .014). There were
no detected changes in lifestyle habits nor in physical performance tests.
Discussion: It is already known that COVID-19 has long-term negative consequences
regardless of the stage of the disease. Our findings support the notion that patients
cannot fully regain all their functions within a two-month period without receiving
structured or supervised rehabilitation. Therefore, it is crucial to offer patients
comprehensive and structured rehabilitation that incorporates clinical, cognitive, and
motor exercises.
KEYWORDS
coronavirus, recovery, functional improvement, hospital stay, health perception
1. Introduction
In March 2020, the World Health Organization declared coronavirus disease 2019
(COVID-19) a pandemic (1). The first case of COVID-19 in Slovenia was reported on 04/
03/2020 (2). By 20/10/2022, more than 620 million confirmed cases had been reported
worldwide, with more than 5.5 million deaths (3). At that time, there were 1.2 million
confirmed cases in Slovenia, including 8,368 deaths (3).
TYPE Original Research
PUBLISHED 21 July 2023
|
DOI 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 01 frontiersin.org
The severity of COVID-19 disease ranges from no symptoms
to mild flu-like symptoms to severe pneumonia and acute
respiratory distress syndrome (ARDS) (4–6). Previous studies
have described details at admission, such as clinical
characteristics (e.g., fever, acute respiratory distress syndrome,
abnormal chest radiograph, shortness of breath, fever) (7–10),
demographics (a higher proportion of infected patients
comprised men, medical staff, and hospitalized patients)
(5,10–12), comorbidities (hypertension, obesity, and diabetes
(5,8,9), and laboratory parameters (e.g., higher plasma levels
of IL2, IL7, TNFα,etc(9). It is already known that the disease
can cause various types of damage to multiple organs,
particularly the brain (13). The inflammatory response that is
triggered by the infection can lead to long-term cognitive
decline, psychological distress, and musculoskeletal issues
(14–16). Moreover, patients who have survived severe
COVID-19 disease exhibit impaired balance and strength (17).
Muscle contractile properties, assessed by tensiomyography
(TMG), were followed in Slovenian football players after
approximately 2 months of COVID-19 lockdown (18). When
compared post- to pre-, they reported a 6% and 50% increase
in contraction time in the vastus lateralis and biceps femoris,
respectively. Furthermore, this shift was not related to jump
performance but was associated with increased injury
incidence. However, TMG was not used in participants after
COVID-19 hospitalization. All of these consequences of
COVID-19 also lead to the development of frailty, sarcopenia,
and decreased quality of life, which can last for up to a year
after the disease has subsided (19).
The different functional and medical conditions of patients
before the onset of the disease, combined with the different
recovery rates after the disease, led to the development of several
guidelines and recommendations for the rehabilitation of patients
after COVID-19 (20). Although it is already well known that
early inpatient and post-hospital rehabilitation is necessary,
regular, systematic, and guided rehabilitation after COVID-19 is
not available to all patients. We did not find any reports in the
literature examining what happens to patients who are not
admitted to rehabilitation after COVID-19. In addition to the
guidelines for professional rehabilitation, many organizations
have published guidelines to promote self-rehabilitation after
COVID-19. The World Health Organization encouraged
individuals to be proactive by publishing guidelines for self-
rehabilitation after COVID-19 (21), although the literature
supporting this self-management practice among individuals
rehabilitating after COVID-19 is sparse (20). Therefore, we were
interested in investigating possible changes in some physiological
and psychological parameters in COVID-19 patients who were
not enrolled in specific rehabilitation programs after hospital
discharge. However, all patients received a general booklet with
recommendations and instructions for regular physical activity,
which was not specifically designed for patients with COVID-19.
It was assumed that most of the measured parameters would
improve two months after hospital discharge, despite the fact
that the patients were not enrolled in a specific rehabilitation
program.
2. Methods
We conducted a single-center prospective cohort study by
enrolling 43 consecutively hospitalized patients that were admitted
to the General Hospital Izola due to a complicated COVID-19
disease. Functional and clinical characteristics at hospital discharge
(T
1
) and 2-month follow-up (T
2
) were collected until 17/05/2021.
2.1. Participants
Initially, 43 participants were included in the study, but four of
them did not appear for the second measurement, leaving a total of
39 patients tested at both time points (T
1
and T
2
). Participants were
recruited from the pool of patients hospitalized at the Department
of Internal Medicine of the Izola General Hospital, Slovenia, due to
COVID-19 and its complications. Inclusion criteria for
participation in the study were: age ≥18 years, signed informed
consent, and hospitalization for COVID-19 disease [confirmed
with a positive polymerase chain reaction (PCR) nasal swab test
for SARS-CoV-2 virus]. Exclusion criteria were a positive PCR
test for the SARS-CoV-2 virus at the time of hospital discharge
and severe medical conditions (musculoskeletal, cardiovascular,
pulmonary, and neurological) that prevented patients from
performing all motor and cognitive tests. All patients were visited
by a dedicated physician during their hospitalization, and the
study protocol was discussed in detail with them. If the
participant agreed to participate in the study, written informed
consent was obtained prior to each examination. The clinical
trial protocol was registered on ClinicalTrials.gov under the
identifier number NCT04860206. All procedures were performed
in accordance with the Declaration of Helsinki, and the study
was ethically approved by the institutional ethical board of the
Izola General Hospital (application number: 1/21).
Patients participated in T
1
measurements on the condition of a
negative COVID-19 test, which was performed when one of the
following conditions was met: on the day of hospital discharge or
the 10th day after confirmation of the disease if discharged from
the hospital earlier. The time frame for recruiting patients for T
1
measurements was between 01/01/2021 and 18/03/2021. After
the T
1
assessment, the subject received a “Stay Active”brochure
(22) with general information on the beneficial effects of physical
activity and some comprehensive explanation of how different
exercises could be performed at home during the COVID-19
pandemic. The T
2
assessment was conducted 2 months after the
T
1
assessment (the time frame for T
2
measurements was between
11/03/2021 and 19/05/2021). All assessments were performed at
the Cardiac Rehabilitation Center of Izola General Hospital
during the morning hours.
2.2. Measurements
All assessments at T
1
and T
2
were performed by a trained
researcher in the same room and using the same equipment.
Measurements were taken in this order:
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 02 frontiersin.org
Body mass (kg) and height (m) were measured with a Libela
personal scale with a mounted stadiometer (Libela-Elsi Ltd.,
Slovenia), and the results were rounded to the nearest 0.1 kg and
0.5 cm, respectively. Body composition was measured using the
tetrapolar bioimpedance device BIA 101 Anniversary (Akern-Srl,
Florence, Italy) after the participants were in the supine position
for 30 min. The proportions of fat mass (FM in %) and muscle
mass (MM in %) were recorded from the assessment.
Tensiomyography measurements were performed in three
muscles of the right leg: the vastus lateralis (VL), the biceps
femoris (BF), and the gastrocnemius medialis (GM). All
measurements were made during electrically evoked maximal
isometric twitch contractions. For the VL, participants were in
the supine position with the knee angle at 30° of flexion (where
0° represents a fully extended knee joint). For the BF, they were
in the prone position with the knee at 5° of flexion, and for the
GM, they were prone with the ankle in a neutral position, as
previously reported (23–25). Foam pads were used for joint
support. A single 1-ms maximal monophasic electrical impulse
was used to elicit a twitch, which caused the muscle belly to
oscillate and enlarge. These oscillations were recorded using a
sensitive digital displacement sensor (TMG-BMC Ltd., Slovenia)
that was placed on the surface of the skin over the mid-belly of
the muscle of interest. If needed, the measurement point and
electrode positions were adjusted to obtain the maximum
amplitude (Dm) of the muscle belly response. Initially, the
stimulation amplitude was set just above the threshold and then
gradually increased until the Dm of the radial twitch
displacement did not increase any further. From two maximal
twitch responses, a contraction time (Tc), a delay time (Td), and
a transversal velocity (Vc) were calculated, and the average was
used for further analysis. Td was defined as the time from the
electrical impulse to 10% of Dm. Tc was defined as the time for
the amplitude to increase from 10% to 90% of Dm (25). Vc was
calculated as the ratio between Dm and the sum of Td and Tc (26).
During the tensiomyography assessment, participants were
interviewed to elucidate possible unhealthy lifestyle behaviors and
to estimate their risk for sarcopenia and frailty conditions. For
this purpose, we used the Slovenian version of the SARC-CalF
questionnaire (27), the Mediterranean Lifestyle Index (MEDLIFE)
(28), and the Edmonton frail scale questionnaire (29).
The SARC-CalF questionnaire is a screening tool for
sarcopenia in older adults. It addresses five domains: strength,
assistance in walking, rising from a chair, climbing stairs, and
falling (30), and also includes a calf circumference measurement
(31). Each answer is scored from 0 to 2 points according to the
reported difficulty in performing the task in question. For calf
circumference, zero represents normal muscle mass and 10
represents very low muscle mass. The sum of the points gives a
score that can range from 0 to 20, with zero indicating the best
result and 20 the worst. Individuals with a SARC-CalF score ≥11
are at increased risk for sarcopenia.
The Mediterranean Lifestyle index (MEDLIFE) is a tool that
measures the adherence of the individual to the principles of the
Mediterranean lifestyle (28). A total of 28 items are divided into
three blocks of questions (food consumption frequency,
Mediterranean dietary habits, and social habits). For each item, 1
point is awarded (28 points in total) if the answer meets certain
criteria. The final score of the MEDLIFE index ranges from 0
(the worst) to 28 (the best).
The Edmonton frail scale (EFS) is a brief, valid, and reliable
tool for assessing frailty. It can be administered by researchers
without special training in geriatric medicine. The EFS assesses
nine subscales: (1) cognition; (2) general health status; (3)
functional independence; (4) social support; (5) medication use;
(6) nutrition; (7) mood; (8) continence; and (9) functional
performance. The EFS scores range from zero to 17. Severe
frailty is defined as a score of 12–17, apparent frailty as a score
of 6–11, and absence of frailty as a score of 5 or less (29).
The level of physical activity was determined with the
Slovenian translation of the short version of the International
Physical Activity Questionnaire (IPAQ), which was assessed at T
2
(32,33). A total of seven items assess the frequency (days per
week), duration (time per day), and intensity (light, moderate, or
vigorous) of PA, which was performed during the previous week.
2.3. Clinical tests
Blood pressure and pulse wave velocity were measured using a
Vicorder (Vascular Model, SMT Medical Ltd., Germany). Prior to
measurement, participants were placed in the supine position in a
quiet room, with the head elevated to approximately 15°, so that
the skin and muscles over the carotid artery were relaxed, but not
too tense. Pulse wave velocity was measured with a cuff placed
over the right carotid artery and the right thigh. The length
between the common carotid artery (CCA) and the superficial
femoral artery (SFA) was measured between the suprasternal notch
and the midpoint of the thigh cuff. Measurements were taken until
pressure waveforms across the CCA and SFA were clear and
reproducible. During the FU, the same distance between the
measurement sites was used. Blood pressure was measured in the
sitting position with the cuff placed on the left upper arm.
Spirometry was performed with the participant comfortably
seated in a chair. A clip was used to close the nostrils.
Participants were instructed to breathe normally for 10 s and
then to inhale as deeply as possible and exhale as quickly as
possible into a tube (microQuark, COSMED Ltd., Italy). The best
forced vital capacity (FVC) and forced expiratory volume
measurement in one second (FEV1) of the three tests performed
were used. An FEV1/FVC Tiffeneau-Pinelli index was calculated
automatically (34).
2.4. Physical performance measurements
The grip strength test (35) was performed using an analog
hydraulic handheld dynamometer (Jamar Dynamometer,
Sammons Preston, USA). During the measurement, participants
sat on a chair with no armrests. The dominant upper arm was
parallel to the torso, while the elbow was positioned at 90°
flexion. After two test attempts, participants performed three
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 03 frontiersin.org
consecutive handgrips with a 1-minute rest in between. The best
result was used for further analysis.
A“Timed Up and Go”test (36) was used to assess mobility at a
distance of three meters. Participants wore their regular walking
shoes. The test started with the participant sitting on a 46-cm-high
chair, then standing up, walking around a marked bar, returning
to the chair, and sitting on it. Each participant completed one test
trial and two trials without walking aids. The trial with the
shortest completion time was used for further analysis.
Gait speed was evaluated (37) at the self-selected speed and the
fastest speed over a distance of 4 meters using timed gates (Beam
Trainer timing system, Seedgrov d.o.o., Ljubljana, Slovenia). Two
meters were provided before and after the timed distance for
acceleration and deceleration. Each gait modality (self-selected
speed and fast speed) was assessed twice, and the best result was
used for further analysis.
A 30-second chair-stand test was used to assess the number of
stands a participant could complete in 30 s (38). Participants
initially sat on a 46-cm-high chair without armrests. They placed
their hands on the opposite shoulder, crossed at the wrists. Their
feet were flat on the floor, and their backs were straight. They
rose to a full standing position, then sat back down again and
repeated this for 30 s. Only completed repetitions were counted.
2.5. Cognitive tests
The Montreal Cognitive Assessment (MoCA) was used to
evaluate the general level of cognitive functioning and screen for
cognitive impairment (39). The MoCA test addresses several
cognitive domains, namely visuospatial ability, short-term
memory, executive function, attention, concentration, working
memory, language, and orientation to time and place. The final
score ranges from 0 to 30 points, with values ≥26 indicating no
cognitive impairment.
2.6. Qualitative assessments
A structured interview was used to assess the self-perceived
response to the COVID-19 experience in relation to functional,
mental, and mood states. The structured interview was used to
capture qualitative data. Patients were interviewed twice, at the
first measurement and then at the second measurement after
self-rehabilitation at an interval of 8 weeks. The interview was
conducted after the functional tests between the patient and the
researcher, who took notes on the answers.
The first structured interview included questions about the
subjective experience of being hospitalized for COVID-19, i.e.,
what was most distressing for the respondent besides the physical
problems: how did they help themselves or what helped them,
and what did they miss most? They also rated their physical and
mental states (in percentages) after the infection, assuming that
their pre-infection state was rated as 100%. At the end of the
interview, the patients were given a form to monitor their
symptoms or changes in well-being and were asked to bring it to
their post-rehabilitation follow-up appointment. Patients also
received a “Stay Home—Be Active”manual with instructions on
how to begin the exercise program designed for patients with
chronic lung disease.
At T
2
, patients were asked to compare their physical and
mental state and mood again, assuming that their pre-infection
state was rated as 100%. They were also asked to evaluate in
more detail what they found most difficult in coping with the
physical and mental stress, whether they were frustrated, what
thoughts came to mind during the recovery period, how they
helped themselves if necessary, and what they missed during the
recovery period or how it could have been more successful. They
also assessed their perception of what it would take to reach
100% physical, mental, and emotional health and when they
expected to achieve it. Finally, they were asked to hand over the
symptom monitoring form they received at the first
measurement, and if they did not bring it with them, they were
interviewed by the researcher to collect the data. They were also
asked if they had followed the advice in the manual and if they
had exercised according to its instructions.
2.7. Statistics
We used G-Power (40) to determine the required sample size.
Considering a two-sided α-value of 0.05 and a β-value of 0.20, and
a functional decline of less than −11% (indicating an effect size
greater than 0.9), we calculated that a sample size of 13
participants would be sufficient. All parameters are presented as
the mean and standard deviation (SD). The normal distribution
was confirmed by visual inspection using histograms and Q-Q
plots, and analytically using the Shapiro-Wilk test. Parameters of
the baseline (T
1
) and follow-up (T
2
) samples were assessed by a
paired samples t-test. All statistical analyses were performed using
IBM SPSS Statistics 22 (SAS Institute, Cary, NC, USA), with a
significance level of p< .05. Figures 1–3have been prepared using
Microsoft Office Excel (Microsoft Corporation, Washington, USA).
2.7.1 Qualitative analysis
For research purposes, we developed an index of subjective
evaluation (of physical fitness, mental well-being, and mood) by
using index equations commonly used in monitoring economic
phenomena (measuring price changes) to show the extent of
relative changes in a phenomenon over time. Interpretative
phenomenological analysis (IPA) (41) was used to explore
participants’views of their own experiences of hospitalization
due to the COVID-19 infection. This type of individual personal
perception of the event as a phenomenon gave us the
opportunity to produce an objective statement of such an event
as the COVID-19 infection. Therefore, IPA can help us to
illuminate the subjective perceptual processes and understand
different responses to the same diagnosis.
Subjective assessment of physical and mental level was
analyzed by index (I), in percentage for the period after
hospitalization (T
1
) and after self-rehabilitation (T
2
) in relation
to the pre-infection state, considered 100%. The difference
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 04 frontiersin.org
between the two assessments was described by the index using the
following equation:
Equation 1:
I¼Yr
Yh
100
I—index of subjective assessment.
Yh—subjective assessment of physical or mental state after
hospitalization in %.
Yr—subjective assessment of physical or mental state after self-
rehabilitation in %.
An index above 100 means that the subjective state after self-
rehabilitation (Yr) is higher than after hospitalization (Yh), so
self-rehabilitation shows positive trends, while a value below 100
tells us that the post-self-rehabilitation state was estimated to be
lower than after hospitalization. A value around 100 shows no or
little change in the estimated state between Yh and Yr. The
difference is expressed in percentage points.
Additionally, descriptive analysis was used to report the most
common symptoms that patients had, which were assessed by
the Monitoring symptoms form. Such analysis gave us an answer
to “what happened”regarding the post-COVID-19 symptoms in
the period of 6-weeks of self-rehabilitation.
3. Results
In the study analysis, we included 39 participants with a mean
age of 59.1 ± 10.3 years (12.8% women) (Table 1).
Clinical, cognitive, and physical performance findings are
summarized in Table 2.ComparedtoT
1
, BMI increased by 2.9%
at T
2
(p< .001, Cohen’sd= 0.19), paralleled by a 4.8% increase in
fat-free mass (p< .001, Cohen’sd= 0.31). There were no changes
in other body characteristics or physical or clinical tests. The only
improvements we observed were in the Edmonton total symptom
score (p< .001, Cohen’sd= 0.64), the SARC-CalF score (p= .014,
Cohen’sd= 0.50), and the MoCA score (p=.014,Cohen’sd= 0.35).
Tensiomyographic data (Table 3)showedadecreaseinTc
in all three muscles at T
2
when compared to T
1
. Similarly,
Td decreased in VL and GM, whereas it was almost significant
in BF. Since Dm was unchanged, Vc increased, but only in BF.
On average, participants rated their physical condition 18.1
percentage points higher after self-rehabilitation (at T
2
) than
TABLE 1 Basic data of the study participants at the baseline assessment.
All
N39
Age (years), mean ± SD 59.1 ± 10.3
Height (cm) 175.9 ± 8.7
Body mass (kg) 98.9 ± 16.6
Body Mass Index (kg/m
2
) 31.5 ± 4.7
Fat mass (%) 30.0 ± 10.5
Fat-free mass (kg) 66.9 ± 10.4
Number of hospital days 7.5 ± 6.0
Physical activity (MET min/day) 312.8 ± 396.8
Sedentary behavior (min/day) 323.5 ± 181.6
Smoking status, n(%)
Current smoker 1 (2.6)
Former smoker 6 (15.4)
Comorbidities
Hypertension 17 (43.6)
Coronary heart disease 3 (7.7)
Heart failure 2 (5.1)
Atrial fibrillation 2 (5.1)
Asthma 2 (5.1)
COPD 1 (2.6)
Diabetes I 0
Diabetes II 8 (20.5)
COPD, Chronic obstructive pulmonary disease.
TABLE 2 Clinical, functional, and cognitive results at hospital discharge
(T
1
) and 2-month follow-up (T
2
).
T
1
T
2
Mean (SD) Mean (SD) p
TIME
(η
2
)
Body mass (kg) 98.9 (16.6) 98.7 (16.3) 0.774
Body Mass Index (kg/m
2
) 31.5 (4.7) 32.4 (5.0) <.001 (0.19)
Fat mass (%) 30.0 (10.5) 29.5 (11.5) 0.529
Fat-free mass (kg) 66.9 (10.4) 70.1 (11.5) <.001 (0.31)
30-sec Sit-to-stand test (n) 14.7 (4.7) 15.4 (4.1) 0.304
Timed Up and Go (s) 6.4 (1.6) 6.3 (1.4) 0.767
Self-selected gait speed (m/s) 1.31 (0.24) 1.33 (0.25) 0.443
Fast-paced gait speed (m/s) 1.82 (0.32) 1.80 (0.28) 0.610
Grip strength (kg) 41.6 (11.7) 41.8 (13.0) 0.732
Systolic blood pressure (mmHg) 143.8 (17.3) 148.6 (19.5) 0.263
Diastolic blood pressure (mmHg) 76.4 (11.1) 79.4 (11.1) 0.264
FEV1/FVC 0.80 (0.08) 0.8 (0.07) 0.424
MEDLIFE index 14.10 (4.1) 13.23 (4.3) 0.170
EDMONTON Scale 3.41 (2.5) 1.82 (2.2) <.001 (0.64)
SARC-CalF Score 1.45 (1.5) 0.7 (1.0) 0.014 (0.50)
MoCA Score 24.3 (2.9) 25.3 (3.2) 0.014 (0.35)
FEV1, forced expiratory volume in one second; FVC, forced vital capacity; MEDLIFE,
Mediterranean lifestyle; MoCA, Montreal Cognitive Assessment score.
TABLE 3 Tensiomyographic parameters of three skeletal muscles at
hospital discharge (T
1
) and 2-month follow-up (T
2
).
T
1
T
2
Mean (SD) Mean (SD) p
TIME
(η
2
)
Vastus lateralis
Delay time (ms) 24.6 (2.0) 23.6 (2.6) .014 (.150)
Contraction time (ms) 31.3 (6.3) 26.9 (5.2) <.001 (.358)
Amplitude (mm) 4.8 (2.1) 5.0 (1.8) .547
Radial velocity (mm/ms) .088 (.041) .099 (.036) .080
Biceps femoris
Delay time (ms) 47.4 (10.2) 43.4 (11.1) .091
Contraction time (ms) 29.8 (4.1) 27.8 (3.8) .007 (.178)
Amplitude (mm) 5.3 (3.1) 6.4 (2.9) .058
Radial velocity (mm/ms) .072 (.045) .091 (.040) .016 (.144)
Gastrocnemius medialis
Delay time (ms) 35.6 (8.3) 30.4 (8.3) <.001 (.381)
Contraction time (ms) 25.1 (3.1) 23.1 (2.1) <.001 (.313)
Amplitude (mm) 4.8 (1.6) 4.6 (1.8) .459
Radial velocity (mm/ms) .080 (.029) .086 (.029) .274
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 05 frontiersin.org
after hospitalization (at T
1
)(Figure 1), but the difference was not
statistically significant (p= .078). A total of 25 out of 28 patients
answered this question in the affirmative, reaching the pre-
infection level of 100% (while three patients reported that their
physical condition had further deteriorated at the 2-month
follow-up compared to the pre-infection period).
However, the mental state assessment index remained almost
unchanged. Participants rated their mental state 6.5 percentage
points higher at T
2
than at T
1
. Although most patients returned
to normal, five out of 28 patients still felt that they had not
returned to their pre-infection state (Figure 2).
3.1. Monitoring symptoms and changes
in well-being during self-rehabilitation
During the two-month self-rehabilitation period, patients were
asked to record any symptoms and changes in well-being. Only two
FIGURE 1
Average subjective assessment of physical status at the first and second measurements. *T
1
-first measurement; T
2
-second measurement.
FIGURE 2
Average subjective assessment of mental status at the first and second measurements. *T
1
-first measurement; T
2
-second measurement.
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 06 frontiersin.org
patients returned a completed form with symptoms recorded. In
addition, we were able to collect recalls of symptoms from 18
other patients at follow-up. Thus, in total, we recorded
symptoms and changes in well-being in half of the patients who
participated in the study (20 out of 40 participants) (Figure 3).
Our data also show that the most common symptoms after
COVID-19 are joint pain (10 patients), muscle pain, and cough
(seven patients), followed by irritability, sadness, shortness of
breath, and difficulty sleeping.
4. Discussion
In this study, we were interested in the clinical, functional, and
cognitive status of patients recovering from hospitalization for
COVID-19 who were not enrolled in an organized rehabilitation
program. Measurements of their performance were taken
immediately after hospital discharge and 2 months later. We
found differences between T
1
and T
2
in BMI, fat-free mass,
frailty score, muscle contractile properties, SARC-CalF, and
MoCA scores.
4.1. Lifestyle characteristics and quality
of life
We were interested in whether participants changed various
lifestyle characteristics between T
1
and T
2
. Nutritional and
physical activity patterns should be changed after the COVID-19
hospital discharged to overcome negative consequences of
disease. The self-reported amount of physical activity during self-
rehabilitation period, on average, 5.2 h peer day 5.4 h per day of
sitting. It has been suggested that COVID-19 may result in
physical inactivity, which in turn may become a long-lasting
symptom for individuals who have recovered from the virus (42).
On the other hand, regular physical activity can have an
important impact on different aspects of health, from
cardiovascular to mental health (43). Another behavioral factor
affecting COVID-19 rehabilitation is nutrition. Adequate
nutrition can play a protective and regenerative role, according to
COVID-19 (44). Because of its protective and preventive effects,
it has been suggested that the Mediterranean diet may represent
a positive approach against COVID-19 (45,46). In our sample,
we did not observe any changes in eating habits or lifestyle in
favor of a Mediterranean diet between T
1
and T
2
. Compared
with other studies (47), our population had a comparable
adherence to the Mediterranean lifestyle.
The Edmonton Frail scale and SARC-CalF test questionnaires
were used to measure changes related to frailty or sarcopenia
(27,29). COVID-19 patients tend to be more frail after hospital
discharge (48). Moreover, early detection of frailty and
sarcopenia may help in the future planning of specific
rehabilitation. We were interested in the frailty and sarcopenia
status of the enrolled participants after COVID-19. At T
1
measurements, two patients had severe frailty according to the
Edmonton scale of frailty, three patients had a moderate frailty
score, nine patients had a predisposition to frailty, and 25
patients showed no signs of frailty. The SARC-CalF test for
sarcopenia showed that one patient had potential sarcopenia on
T
1
measurements. Two months after discharge, the frailty results
improved, and no patient had severe frailty, while five patients
exhibited signs of moderate frailty, and the remaining patients
FIGURE 3
Types of symptoms and changes in well-being during self-rehabilitation. *a - joint pain; b - muscle pain, cough; c - irritability, sadness; d - shortness of
breath, difficulty sleeping, e - severe headache, nausea; f - indigestion (constipation), poor sense of smell, poor taste; g –no listed symptoms; h - anxiety;
i–fever, low appetite, increase appetite; j –other: tingling, impaired vision, fluctuating blood pressure.
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 07 frontiersin.org
were not at risk for frailty. The SARC-CalF test for sarcopenia after
two months showed that the patient no longer reported problems
suggestive of sarcopenia. Therefore, the screening instruments
(Edmonton Frail scale and SARC-CalF test), which are based on
self-reporting and self-assessment, showed improvement in
various aspects such as strength, assistance in walking, general
health status, and functional independence.
4.2. Physical health and performance tests
Despite positive results at T
2
for the Edmonton Frail scale and
the SARC-CalF test, we did not find improvements in physical
performance tests. As previously described in the literature,
patients may have impaired physical performance after hospital
discharge (49). Re-evaluation after two months of self-
rehabilitation showed that participants did not achieve the results
expected for a healthy population in selected functional
parameters such as the 30-sec Sit-to-stand test, TUG, gait speed,
grip strength, and clinical parameters such as systolic and
diastolic blood pressure and FEV1/FVC. Due to the complexity
of rehabilitation after COVID-19, bed exercises can be an
effective tool in the initial stages. An example of bed exercises is
the Full-body in-Bed Gym program (50,51), which allows the
difficulty of the exercises to be adjusted to the individual’s
physical and mental capabilities. Thermal water rehabilitation is
also a possible suggestion for an effective rehabilitation program
tailored to the individual. This type of rehabilitation can improve
the inspiratory muscles, which are typically weakened after
COVID-19 (52).
Patients had negatively deviated levels of some risk factors
compared with recommended levels shortly after discharge.
Factors such as increased BMI (53,54) and higher systolic blood
pressure (55,56) have been previously identified as factors that
may contribute to complications of COVID-19. In addition, it
has also been suggested that COVID-19 increases systolic and
diastolic blood pressure and may cause new-onset hypertension
(57), but we did not find correlations between previously
reported hypertension and elevated systolic blood pressure in our
patients. Therefore, we can assume that the elevated systolic
pressure in our patients is somehow related to the COVID-19
consequences.
4.2.1. Skeletal muscle contractile properties
A very consistent change after self-rehabilitation (T
2
) was a
decrease in temporal contractile parameters in three selected
muscles, when compared to hospital discharge values (T
1
).
Specifically, Tc decreased in all three muscles and Td decreased
in VL and GM, while BF showed an almost significant decrease.
Dm, which is related to muscle atrophy (58), remained
unchanged. Both Td and Tc were found to be related to muscle
MHC-I composition in VL muscle (25). This suggests a change
toward fast-twitch fibers in VL at T
2
when compared to T
1
.
Although this is true for the VL muscle, there is no reason to
believe that this would be similar in the other two observed
muscles (GM and BF). In fact, our team previously reported no
decrease in MHC VL proportions after 14 days of bed rest and
recovery in healthy 55–65-year-olds (59,60). Furthermore, the
above-mentioned studies confirmed CSA, force, and specific force
loss in only type I muscle fibers. Therefore, the explanation of
shorter Td and Tc must be sought at lower activation levels,
which are regularly found after short-term immobilization
studies (61).
4.3. Psycho-sociological characteristics and
subjective perceptions of illness
The literature also suggests changes in mental health status
after hospitalization for COVID-19. Despite the anxiety and fear
the respondents have experienced and, above all, the desire to
regain their pre-infection health status shown on the first
measurements at discharge from hospital care, two-thirds of the
patients showed no significant improvement in the measured
psychological parameters. At the T
1
measurements, like Brown
et al. (62), we noted a willingness to try anything to address
symptoms after COVID-19, as subjects showed interest in
exercising with the manual and in monitoring their health.
Although they reported a severe experience with COVID-19, in
addition to anxiety and health concerns, their lifestyle habits did
not change after they went home, i.e., no systematic self-
rehabilitation was reported at the T2 measurements.
The subjects’self-assessment of physical and mental status
(index) showed mainly an improvement in physical status, where
the assessment of mental status remained unchanged, while some
patients (5%) still didn’t reach the pre-Covid state, which may
indicate that the mental (mood) consequences are lasting longer
what confirmed also by the MoCA test. Despite an average
higher MoCA score in the whole sample, 15 out of 39 patients
had worsened or remained unchanged at 2 months. Nevertheless,
patients’adherence appeared to be very low, as they admitted
that they did not follow the manual as advised at the initial
measurements. How to encourage patients to take a more active
approach to rehabilitation and how to increase adherence will
certainly be our future challenges.
Improvements in the MoCA test are indicative of recovery of
cognitive function in hospitalized COVID-19 patients at 2
months after hospital discharge. The original MoCA validation
study reported a test-retest consistency of 0.91 at 2 months, with
no significant learning effect (63); however, the indication of
improved performance following repeated MoCA administrations
(64) stresses the importance of interpreting the results with
caution. It has already been established that patients who are
critically ill or who have been treated in an intensive care unit
(ICU) are at risk of suffering from the long-term consequences
of COVID-19, such as impaired physical and cognitive function
and psychological disorders similar to post-intensive care
syndrome (PICS). Therefore, optimally selected rehabilitation
may be required to address these disabilities (65). In addition to
the significance of the results indicating overall recovery, it is
important not to overlook the 15 (38.5%) participants whose
cognitive status either worsened or remained unchanged from
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 08 frontiersin.org
post-hospitalization to 2-month follow-up. These participants
may be at higher risk or more susceptible to long-term post-
infection difficulties and may require additional attention during
recovery, if successful. A comprehensive report on the cognitive
status of the patients enrolled in this study has been published
previously (66).
4.4. Limitations
The single-center design and relatively small number of
patients are potential limitations of this study and may limit the
generalizability of the results. The severity of the infection was
not considered, and no assessment was performed before or
during the infection, so changes may not be solely attributable to
the infection.
5. Conclusions
COVID-19 has long-term negative consequences regardless of
the stage of the disease (67), making it all the more important that
patients have the opportunity for organized rehabilitation.
Although the subjects were provided with materials for self-
rehabilitation and entered the recovery phase with desire and
enthusiasm, this was not sufficient to engage in regular physical
activity that would constitute post-disease rehabilitation. This was
also reflected in the tests, as there was no visible improvement in
the physical performance tests. Our results confirm that patients
do not recover all functions within two months without
organized or guided rehabilitation. Rehabilitation treatment for
post-COVID-19 patients discharged from the hospital should be
tailored to each individual’s needs. This includes recovery from
muscular and neurological deficits, cardiorespiratory
reconditioning, improvement of cognitive symptoms, and
education on healthy lifestyles. Therefore, it is important to
provide patients with organized and guided complex
rehabilitation that includes clinical, cognitive, and motor exercises.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Ethics statement
The studies involving human participants were reviewed and
approved by Institutional Ethical board of the Izola General
Hospital (application number: 1/21). The patients/participants
provided their written informed consent to participate in this
study.
Author contributions
RP and MG developed the plan for the research. MG and UM
carried out cognitive and psychological evaluations. KT, BŠ,LŠ,SP,
MP, and UM collected the data. KT, SP, MP, and BŠanalyzed the
data, and BŠwrote the initial draft of the manuscript. KT was
responsible for writing the final version. All authors reviewed
and edited the manuscript, and ultimately approved the final
version for submission. All authors played a part in creating the
article and gave their approval for the final submitted version.
All authors contributed to the article and approved the
submitted version.
Funding
This study was financed within the ARRS Research Program
(P5-0381), Kinesiology of Quality of Life. MP and UM received
funding from the European Union’s Horizon 2020 research and
innovation program under grant agreement No. 952401
(TwinBrain—TWINning the BRAIN with Machine Learning for
Neuro-Muscular Efficiency).
Acknowledgments
We would like to express our gratitude to Dr. Bojan Novak,
who serves as the head of the COVID department at General
Hospital Izola, along with Dr. BlažBerger, Dr. Anita Bohinc,
Karmen Jakomin, and Jelena Prodić, for their assistance in
gathering biological human samples and connecting us with the
patients during their hospital stay. We would also like to extend
our thanks to all the participants who generously volunteered to
take part in the study and recognized the importance of
investigating the impacts of the SARS-CoV-2 infection.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.
Teražet al. 10.3389/fresc.2023.1209900
Frontiers in Rehabilitation Sciences 09 frontiersin.org
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