Nazir, et al. Kesmas. 2023; 18 (Special Issue 1): 4-10
DOI: 10.21109/kesmas.v18i3.7039
Kesmas: Jurnal Kesehatan Masyarakat Nasional
(Kesmas: National Public Health Journal)
Clinical and Functional Outcomes of COVID-19 Survivors After
Hospitalization
Arnengsih Nazir1,2*, Salsabila S S Putri3, Muhammad Hasan Bashari4
1Department
of Physical and Rehabilitation Medicine, Dr. Hasan Sadikin General Hospital, Bandung, Indonesia, 2Department of Physical and
Rehabilitation Medicine, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia, 3Undergraduate Program of Medical Science, Faculty
of Medicine, Universitas Padjadjaran, Bandung, Indonesia, 4Departement of Biomedical Science, Faculty of Medicine, Universitas Padjadjaran,
Bandung, Indonesia
Abstract
Coronavirus disease 2019 (COVID-19) causes various clinical manifestations during acute infection and at the post-acute phase with persistent symptoms
called long COVID. It occurs in mild and moderate to severe cases which require hospitalization. In patients needing hospitalization, especially intensive care
unit admission, the risk of long COVID increases. Many hospitalized patients exhibited more symptoms in 60 days after the illness than non-hospitalized patients. This review aimed to identify the clinical and functional outcomes in COVID-19 survivors after hospitalization. The articles in the PubMed database published in 2019-2021 were reviewed and found 20 be eligible. The clinical outcomes were the appearance or persistence of general and multi-organ symptoms,
nutritional disorders, and decreased lung function. The functional outcomes found were decreased muscle strength, physical, psychological, and cognitive
functions, increased disability and dependencies, as well as decreased vocational status and quality of life. The incidence of each outcome could not be determined due to the variety of methods used to examine and present outcomes. To conclude, COVID-19 causes long-term clinical and functional outcomes
that need to be identified to prevent and manage long-term physical and functional disorders.
Keywords: COVID-19, hospitalization, post-acute COVID-19 syndrome, quality of life, survivor
Introduction
Coronavirus disease 2019 (COVID-19) causes
various clinical manifestations. The World Health Organization classifies the severity of this disease into mild,
moderate, severe, and critical. 1 The severity of the
disease increases the need for hospitalization, intensive
care unit (ICU) admission, and even mortality.2 People
with a comorbid for COVID-19 have a higher risk for
more severe disease.3 In addition to causing various
symptoms during acute infection, COVID-19 has longterm effects on survivors. This condition is called postacute sequelae of COVID-19 or long COVID-19 (LC).
The LC is a patient with signs and symptoms that persist
for about 4-12 weeks or appear after the acute phase
(≥12 weeks).4 Clinical outcomes (CO) and functional
outcomes (FO) of COVID-19 survivors can be affected.
A review by Hayes, et al.,5 found over 100 persistent
symptoms after COVID-19 infection. Reported symptoms include cardiovascular, pulmonary, respiratory,
fatigue, pain-related symptoms, generalized infection
symptoms, psychological disorders, cognitive impairment, sensory disturbances, skin problems, and impaired
function.5
A previous study have shown that LC not only occurs
in patients with moderate to severe cases which require
hospitalization but also in mild cases.6 However, the risk
of post-intensive care syndrome (PICS) was increased in
patients needing hospitalization, especially ICU admission.7 One systematic review found that a large proportion of hospitalized patients exhibited one or more
symptoms of LC at 60 days after the illness compared to
non-hospitalized patients.8 Thus, this review study aimed
to identify the CO and FO in COVID-19 survivors after
hospitalization to give the knowledge or to develop a
rehabilitation program for COVID-19 survivors.
Correspondence*: Arnengsih Nazir, Department of Physical and Rehabilitation
Medicine, Dr. Hasan Sadikin General Hospital, Pasteur Street No. 38, Bandung
40161, Indonesia, E-mail: arifssnt1@gmail.com, Phone: +62 (22) 255-1111/+62
819-3122-2414
Received : June 22, 2023
Accepted : July 21, 2023
Published : July 31, 2023
Method
Articles were searched in the PubMed database with
keywords ('functional' OR 'clinical') AND ('status' OR
'outcome') AND ('severe' OR 'critical') AND ('COVID19') AND ('survivor') for the period from September
2021 to October 2021. The article type was an original
article published from December 2019 to October 2021.
Inclusion criteria were original articles with the study
subjects of COVID-19 survivors after being discharged
from the hospital, written in English, and freely accessi-
Copyright @ 2023 Kesmas, p-ISSN: 1907-7505, e-ISSN: 2460-0601, SINTA-S1 accredited, http://journal.fkm.ui.ac.id/kesmas,
Licensed under Creative Commons Attribution-ShareAlike 4.0 International
Nazir, et al. Clinical and Functional Outcomes of COVID-19 Survivors After Hospitalization
ble in pdf or HTML format.
The identical articles were identified first, then
reviewed based on title, abstract, and keywords. Data
taken were the author(s), study design, total subject,
outcome assessment period, CO, and FO. Data were
synthesized narratively and displayed as a table and text.
The CO synthesized was based on symptoms, physical
examination, laboratory, and imaging findings, while FO
was determined based on functional impairment,
disability, and quality of life.
Results
A total of 1,053 articles based on keywords searched
and 40 articles matched with eligibility criteria. After
reading the full text, 27 articles explaining both CO and
FO were found. The study types were a prospective
cohort (n = 20), a retrospective cohort (n = 5), an ambidirectional cohort (n = 1), and a cross-sectional (n = 1)
study. Twenty prospective cohort studies were analyzed
as a final result. The Preferred Reporting Items for
Systema tic Reviews and Meta-Analyses (PRISMA)
flowchart for a systemic review (Figure 1) was used to
explain the results. The result summary is presented in
Table 1.
Discussion
Most studies were conducted in the first few months
of 2020. During this period, COVID-19 was known to
be caused by the original variant of severe acute respiratory system coronavirus 2 (SARS-CoV-2) with various
clinical and functional outcomes.
Clinical Outcomes of COVID-19
The Appearance or Persistence of General Symptoms
The most common symptoms reported by COVID-19
survivors after one month to one year after being
discharged from the hospital were shortness of breath
and fatigue. The presence of persistent symptoms in
COVID-19 survivors is caused by several mechanisms,
including the presence of SARS-CoV-2 and a persistent
inflammatory response in various tissues, reactivation of
neurotrophic pathogens when immune dysregulation
occurs, interactions of viruses with the microbiome or
virome of the host cell, blood coagulation problems,
Figure 1. PRISMA Flowchart for the Systematic Review
5
Kesmas. 2023; 18 (Special Issue 1): 4-10
Table 1a. Summary of Clinical and Functional Outcomes of COVID-19 Survivors After Hospitalization
Result
Author (s)
Total Subject
Clinical Outcome
Martillo, et al.9
45
Hall, et al.10
200
D'Cruz, et al.11
119
Cao, et al.12
62 at 1 month;
61 at 3 months
Monti, et al.13
39
Strumiliene, et al.14
51
Schandl, et al.15
113
Van Gassel, et al.16
46
González, et al.17
62
Todt, et al.18
251
De Lorenzo, et al.19
251
Rousseau, et al.20
32
Functional Outcome
Fatigue
• PICS
• Upper and lower extremity function abnormalities
• Minimal, mild, moderate, moderate-severe, severe depression,
PTSD, insomnia, anxiety
• Cognitive impairment
• Disability
• HRQoL: mobility, pain/discomfort, self-care, usual activities
• Dyspnea
• Increase exertional desaturation during 6MWT
• Impaired ventilation (FVC and DLCO)
• Depression, anxiety
• Fatigue, dyspnea with persistent cough and burdensome • Decreased four-minute gait speed
pain, especially in the shoulder, chest, lower extremity, • Decreased lower body muscular strength and endurance
and back, and sleep disturbance
• Increase exertional desaturation by ≥4% and to SpO2 ≤88%
during sit-to-stand test
• Depression, anxiety, PTSD
• Cognitive impairment
• Cough, dyspnea, fatigue
• 6MWT: decreased exertional capacity
• Impaired ventilation (FEV1, FVC, MVV under predict- • HRQoL: impaired domains of the physical or emotional role
ed value)
and social function
• Alteration in taste or smell, dyspnea at exertion
• Cognitive impairment
• Malnutrition, at risk for malnutrition
• Psychological disorders: anxiety and depression, PTSD, and
insomnia.
• Overall HRQoL showed no difficulty in mobility, self-care,
usual activities, and anxiety/depression. Moderate pain/dis
comfort by 41%.
• More than half of patients who were previously employed did
not return to their work.
• Fatigue, decreased physical activity, dyspnea at exertion, • 6MWT: decreased exertional capacity, increase exertional deasthenia, cough, arthralgia, hair loss, headache, insomnia
saturation
• Decrease pulmonary function test parameters (FVC,
• Decrease HRQoL score in all domains
FEV1, TLC, VC, DLCO)
• Psychological disorder: PTSD, anxiety, depression
• Impairment in all domains of HRQoL
• Decrease TLC and DLCO
• Decreased exertional capacity
• Returned to full-time work
• Fatigue
• Decreased exertional capacity
• Decreased DLCO
• Decreased HRQoL
• Muscle weakness, ICU-AW
• Anxiety and depression
• Cognitive impairment
• Dyspnea, muscle fatigue, cough
• HRQoL: decreased
• Decreased DLCO and TLC
• 6MWT: decreased exertional capacity
• Psychological disorder: anxiety and depression
Dyspnea
• Anxiety/depression
• Impairment in all domains of HRQoL
Tachypnea, dyspnea
• Anxiety, insomnia, PTSD
• Decreased HRQoL
Abnormal estimated glomerular filtration rate
• Decrease of peripheral muscle strength
• Poor sleep quality, PTSD
• Cognitive impairment
• Dependency
• Did not return to their previous level of activity
Notes: 6MWT = Six-minute Walk Test, DLCO = Diffusing Lung Capacity for Carbon Monoxide, FEV1 = Forced Expiratory Volume at 1 s, FVC = Forced Vital
Capacity, HRQoL = Health-Related Quality of Life, ICU-AW = Intensive Care Unit-Acquired Weakness, MVV = Maximal Voluntary Ventilation, PICS = Post-intensive Care Syndrome, PTSD = Post-traumatic Stress Disorder, TLC = Total Lung Capacity, VA = Alveolar Volume, VC = Vital Capacity.
dysfunction of vagal nerve signaling, abnormal cell metabolism, the presence of primitive immune cell activity,
and molecular mimicry leading to autoimmunity between
pathogens and host cells.29-30
6
The Appearance or Persistence of Multi-organ Symptoms
Angiotensin-converting enzyme 2 (ACE2), employed
by SARS-CoV-2 as a receptor to enter human cells, is
abundant in lung epithelial cells, especially in the alveoli.
However, ACE2 is also widespread in various organs,
Nazir, et al. Clinical and Functional Outcomes of COVID-19 Survivors After Hospitalization
Table 1b. Summary of Clinical and Functional Outcomes of COVID-19 Survivors After Hospitalization
Result
Author (s)
Total Subject
Sigfrid, et al.21
327
Latronico, et al.22
114 evaluated
at least once;
69 at least
twice; 43 three
times
Boari, et al.23
94
Bellan, et al.24
238
Guler, et al.25
66
Veenendaal, et al.26
50
Lombardo, et al.27
189
Bertolucci, et al.28
39
Clinical Outcome
Functional Outcome
Fatigue, dyspnea, sleeping problems, headache, limb weakness, myalgia, arthralgia or swelling, dizziness/lightheadedness, balance problems, swollen ankle, palpitations, seeing
problems, constipation, stomach pain, diarrhea, persistent
cough, chest pains, pain on breathing, anosmia, persistent
fever, ageusia, nausea/vomiting, swallowing problems, skin
rash, passing urine problems, hemiplegia/paresthesia, toe
lesions, weight loss
• Fatigue, ICU-AW
• At risk of malnutrition or being malnourished
• Decreased DLCO
• Anxiety/depression
• Disability in walking or mobility, memory, and concentration
• Decreased overall domains of HRQoL
• 6MWT: abnormal
• Decreased handgrip strength at 3 months, abnormal global
muscle strength at 3, 6, and 12 months
• Anxiety, depression, PTSD at 3 months
• Cognitive impairment
• Dependency at 3 and 6 months, and independency at 12
months
• Return to work at 3, 6, and 12 months, reduced effectiveness
at work at 3 and 6 months, not return to work at 3, 6, and 12
months
• Lamented fatigue, effort dyspnea, anorexia, dysgeusia or • Anxiety
anosmia, insomnia
• Alteration in DLCO
• Dyspnea, ageusia, anosmia, arthralgia, myalgia, cough,
• 2-minute walk test: 40.5% outside reference ranges of expectdiarrhea, chest pain
ed
• Decreased DLCO
• Mild, moderate, severe PTSD
• Mobility: limited
• Exertional dyspnea
6MWT: decreased exertional capacity, increase exertional desa• Had generally lower lung volumes, decreased DLCO
turation
• Fatigue, weakened condition, polyneuropathy, dyspnea, • Cognitive impairment
muscle weakness/stiffness, shoulder pain, restriction of • 10% no change in work, 13% reduced work rate, 10% occuextremities, difficulty sleeping, walking, impaired hand
pation change, 13% re-integration, and 43% too ill to work
function
• Weight loss
• Impaired ventilation (FEV1, FVC under predicted value),
decreased DLCO under predictive value
Fatigue and weakness, myalgia and arthralgia, sleep disNeurocognitive impairments
orders, respiratory disorders, sensory alterations, gastrointestinal symptoms, movement impairments
Dysphagia, peripheral nervous system impairment
• Delirium
• Total Dependency
• Cannot walk
Notes: 6MWT = Six-minute Walk Test, DLCO = Diffusing Lung Capacity for Carbon Monoxide, FEV1 = Forced Expiratory Volume at 1 s, FVC = Forced Vital
Capacity, HRQoL = Health-Related Quality of Life, ICU-AW = Intensive Care Unit-Acquired Weakness, MVV = Maximal Voluntary Ventilation, PICS = Post-intensive Care Syndrome, PTSD = Post-traumatic Stress Disorder, TLC = Total Lung Capacity, VA = Alveolar Volume, VC = Vital Capacity.
such as the heart, intestines, and kidneys.31 Therefore,
the virus can persist and damage various organs,
resulting in other manifestations, both during the acute
phase and after the patient recovers. Autoimmunity is
also known to cause inflammation and damage in various
organs. 29 One study found an abnormal estimated
glomerular filtration rate.20 Acute kidney failure is one
of the complications due to COVID-19, which has a
prevalence of 17%, of which 77% have severe COVID19, and 5% of the total patients require renal replacement therapy.32 In addition to the kidneys, abnormal
results were found in cardiovascular organs, gastrointestinal, and neurological tissue.32
Decreased Lung Function
Various studies carried out pulmonary function tests
on COVID-19 survivors. They found that ventilation was
impaired through a decrease in forced vital capacity and
forced expiratory volume in one second, a decrease in
total lung capacity, and a decrease in diffusion capacity.10,12,14-17,22-26 COVID-19 survivors needed a long
period to recover due to lung fibrosis and other morphological changes fully. The recovery rate is affected by the
severity level, which is affected in turn by gender, obesity,
and the presence of comorbidities. 14 Predomi nant
impairment of lung function is a restrictive pattern with
7
Kesmas. 2023; 18 (Special Issue 1): 4-10
a reduction of diffusing capacity for carbon monoxide
(DLCO) value.14
Nutritional Disorders
Nutrition-related problems that arise in COVID-19
survivors, especially severe degrees of disease, are caused
by other related manifestations.33 Difficulty of swallowing and weakness can make it difficult for the patient to
eat. This condition is exacerbated by reduced appetite,
resulting in muscle wasting.33 In the end, survivors
reported a weight loss of >5% of their pre-illness body
weight.34 In other survivors, the diagnosis of malnutrition was established. Moderate to severe malnutrition is
the most common diagnosis.35
Functional Outcomes of COVID-19
Decreased Muscle Strength
Decreased muscle strength may occur due to chronic
skeletal muscle damage by SARS-CoV-2.36 In addition,
muscle weakness can be the result of immobility that
occurs during hospitalization.37 Prolonged ICU stay or
mechanical ventilation used increased the occurrence of
ICU-related muscle weakness.20,22
Decreased Physical Performance
The 6MWT was the most frequently used method to
determine decreased exercise capacity and increased
exertional desaturation post-COVID-19.10,12,14-17,22,25
Wong, et al., described that in patients who had exertional desaturation or hypoxemia (reduced SpO2 ≥4%),
45% had walking distance less than the lower limit of
normal on the 6-minute walking distance, and 100% had
DLCO less than the lower limit of normal.38 These
results suggest that desaturation during exercise is associated with pulmonary vascularity.38
Psychological Disorder
Anxiety and depression were the most frequently
reported psychological disorders in COVID-19 survivors,
especially those requiring hospitalization. 39 Mental
health disorders occur due to direct neuro-invasion by
viruses that cause nerve cell damage or due to immune
activation that causes an inflammatory response, especially in the brain.39 In addition, having to undergo
isolation makes it difficult to meet family and the inability
to carry out normal activities, as well as guilt toward
those closest to them because they have increased the
risk of exposure to disease, all of which become stressors
for the emergence of symptoms of anxiety and
depression.40
Cognitive Impairment
Not all literature describes methods for assessing the
presence of cognitive impairment. However, in some
8
literature that explains this, the Montreal Cognitive
Assessment method was found to be the most widely
used method to assess cognitive impairment. Similar to
psychological disorders, cognitive impairment is also
caused by damage to neurological function and the
immune system.32,39 In addition, patients undergoing
treatment in hospitals do not receive stimulation and cognitive reorientation due to limited interactions between
humans.40 Cognitive symptoms that arise post-COVID19 include difficulty thinking and concentrating (brain
fog), decreased memory, and difficulty carrying out
executive functions.37 Any disturbances in physical,
mental health, and cognitive functions cause post-intensive care syndrome, seen in individuals who have had
treatment in an intensive care unit.7
Increased Disability and Dependency
Physical impairments that arise are related to the
treatment given in the acute phase.40 The more severe
the severity of the disease, the more complex the treatment given in the hospital. Severe disease increases the
likelihood of mechanical ventilation, sedation, and
neuromuscular blockade associated with prolonged
immobilization.40 Subsequent immobilization causes
muscle and joint contractures, making it difficult for the
patient to move. These disabilities make survivors dependent on carrying out daily activities. The Short Physical
Performance Battery test method can be used to measure
mobility ability through walking speed, Functional
Ambulatory Category for walking/ambulation ability,
and Barthel Index to determine individual dependence in
daily activities.40
Decreased Vocational Status
COVID-19 infection caused a significant reduction in
return to workability.13,15,20,22,26 Several studies found
that 50% to 87.5% of COVID-19 survivors did not
return to their previous work or activity.13,15,20 One
study found that 43% of COVID-19 survivors felt too ill
to work.26 Among survivors who returned to work, many
experienced a reduction of work capacity.22,26
Decreased Health-Related Quality of Life
Most studies found that all domains of HRQoL
decreased in COVID-19 survivors after hospitalization.12-19,21 Short-form 36 items and European Quality
of Life 5 Dimension were the most common HRQoL
assessment instruments.12-16,18,19,21 The decrease in
HRQoL was associated with symptoms, especially
shortness of breath and fatigue, decreased physical
performance, stress in family and work, and social
isolation.12-14,16 The decrease in physical performance
was associated with decreased pulmonary function.16
Nazir, et al. Clinical and Functional Outcomes of COVID-19 Survivors After Hospitalization
Conclusion
The CO identified in several studies is the appearance
or persistence of general symptoms, multi-organ
symptoms, decreased lung function, and nutritional
disorders, while the FO includes decreased muscle
strength and physical performance, psychological or
cognitive disorders, increased disability or dependency,
as well as decreased vocational status and HRQoL. With
various methods used to examine the CO and FO of
COVID-19 survivors after hospitalization and not all
literature being equipped with a percentage of each
outcome, the authors could not determine the incidence
of each outcome. Further studies need to elucidate the
incidence and differential outcomes associated with each
variant of SARS-CoV-2 and their specific mechanisms.
After knowing these outcomes, medical personnel are
expected to be able to assess the CO and FO of COVID19 patients to be used as a basis for carrying out rehabilitation management. Good cooperation between medical
per son nel and survivors is needed to improve the
HRQoL and prevent persistent anatomical and physiological damage to the body.
References
Abbreviations
COVID-19: coronavirus disease 2019; ICU: Intensive Care Unit; LC:
Long COVID, CO: Clinical Outcomes; FO: Functional Outcomes;
PICS: Post-intensive Care Syndrome; PRISMA: Preferred Reporting
Items for Systematic Reviews and Meta-Analyses; SARS-CoV-2: Severe
Acute Respiratory Syndrome Coronavirus 2; ACE2: AngiotensinConverting Enzyme 2; DLCO: Diffusing Lung Capacity for Carbon
Monoxide; 6MWT: Six-minute Walk Test; HRQoL: Health-Related
Quality of Life.
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The authors declares that there are no significant competing financial,
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