Introduction: Many COVID-19 survivors suffer from persisting sequelae after acute disease. This is referred to as long COVID. The objectives of this study were to assess factors associated with long COVID and to analyze differences in persistent symptoms, findings on chest imaging, and pulmonary function between intensive care unit (ICU) and non-ICU hospitalized patients. Methods: We conducted a retrospective study including patients hospitalized with COVID-19. Patients were stratified into ICU patients and non-ICU patients. We analyzed the outcomes of patients who were in clinical follow-up 6 months after discharge with persistent symptoms, radiological and/or functional abnormalities. Logistic regression was used to examine the association between long COVID and patient characteristics. Results: A total of 549 patients were included. Eighty-one ICU patients (66%) and 146 (34%) non-ICU patients had persistent symptoms or abnormalities on chest imaging or lung function test minimally 6 months after discharge. Significantly more ICU patients had residual fibrotic abnormalities on chest CT and functional impairment. Female gender, myocardial infarction, OSAS, low PCO2 at admission, and longer hospital stay were associated with a higher risk of developing long COVID. Diabetes and treatment with tocilizumab were associated with a lower risk of developing long COVID. Conclusion: Of the patients hospitalized for COVID-19, 34–66% suffered from persistent symptoms, residual abnormalities on chest imaging, or reduced lung function at around 6 months after discharge. While persistent sequelae were more frequent in ICU patients, admission to the ICU was not found to be an independent risk factor for developing long COVID.

1.
World Health Organization
. WHO Coronavirus (COVID-19) Dashboard [cited 2022 Sept 12]. Available from: https://covid19.who.int.
2.
World Health Organization
. A clinical case definition of post COVID-19 condition by a Delphi consensus, 6 October 2021 [cited 2022 Sept 12]. Available from: https://www.who.int/teams/health-care-readiness/post-covid-19-condition.
3.
Comelli
A
,
Viero
G
,
Bettini
G
,
Nobili
A
,
Tettamanti
M
,
Galbussera
AA
, et al
.
Patient-reported symptoms and sequelae 12 Months after COVID-19 in hospitalized adults: a multicenter long-term follow-up study
.
Front Med
.
2022
;
9
:
834354
.
4.
Huang
L
,
Li
X
,
Gu
X
,
Zhang
H
,
Ren
L
,
Guo
L
, et al
.
Health outcomes in people 2 years after surviving hospitalisation with COVID-19: a longitudinal cohort study
.
Lancet Respir Med
.
2022
;
10
(
9
):
863
76
.
5.
Bek
LM
,
Berentschot
JC
,
Heijenbrok-Kal
MH
,
Huijts
S
,
van Genderen
ME
,
Vlake
JH
, et al
.
Symptoms persisting after hospitalisation for COVID-19: 12 months interim results of the CO-FLOW study
.
ERJ Open Res
.
2022
;
8
(
4
):
00355-2022
.
6.
Groff
D
,
Sun
A
,
Ssentongo
AE
,
Ba
DM
,
Parsons
N
,
Poudel
GR
, et al
.
Short-term and long-term rates of postacute sequelae of SARS-CoV-2 infection: a systematic review
.
JAMA Netw Open
.
2021
;
4
(
10
):
e2128568
.
7.
Pérez-González
A
,
Araújo-Ameijeiras
A
,
Fernández-Villar
A
,
Crespo
M
,
Poveda
E
;
Cohort COVID-19 of the Galicia Sur Health Research Institute
.
Long COVID in hospitalized and non-hospitalized patients in a large cohort in Northwest Spain, a prospective cohort study
.
Sci Rep
.
2022
;
12
(
1
):
3369
.
8.
Malik
P
,
Patel
K
,
Pinto
C
,
Jaiswal
R
,
Tirupathi
R
,
Pillai
S
, et al
.
Post-acute COVID-19 syndrome (PCS) and health-related quality of life (HRQoL)-A systematic review and meta-analysis
.
J Med Virol
.
2022
;
94
(
1
):
253
62
.
9.
Han
Q
,
Zheng
B
,
Daines
L
,
Sheikh
A
.
Long-term sequelae of COVID-19: a systematic review and meta-analysis of one-year follow-up studies on post-COVID symptoms
.
Pathogens
.
2022
;
11
(
2
):
269
.
10.
Lopez-Leon
S
,
Wegman-Ostrosky
T
,
Perelman
C
,
Sepulveda
R
,
Rebolledo
PA
,
Cuapio
A
, et al
.
More than 50 long-term effects of COVID-19: a systematic review and meta-analysis
.
Sci Rep
.
2021
;
11
(
1
):
16144
.
11.
Heesakkers
H
,
van der Hoeven
JG
,
Corsten
S
,
Janssen
I
,
Ewalds
E
,
Simons
KS
, et al
.
Clinical outcomes among patients with 1-year survival following intensive care unit treatment for COVID-19
.
JAMA
.
2022
;
327
(
6
):
559
65
.
12.
Su
Y
,
Yuan
D
,
Chen
DG
,
Ng
RH
,
Wang
K
,
Choi
J
, et al
.
Multiple early factors anticipate post-acute COVID-19 sequelae
.
Cell
.
2022
;
185
(
5
):
881
95.e20
.
13.
Sigfrid
L
,
Drake
TM
,
Pauley
E
,
Jesudason
EC
,
Olliaro
P
,
Lim
WS
, et al
.
Long Covid in adults discharged from UK hospitals after Covid-19: a prospective, multicentre cohort study using the ISARIC WHO Clinical Characterisation Protocol
.
Lancet Reg Health Eur
.
2021
;
8
:
100186
.
14.
Yong
SJ
.
Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments
.
Infect Dis
.
2021
;
53
(
10
):
737
54
.
15.
Notarte
KI
,
Catahay
JA
,
Velasco
JV
,
Pastrana
A
,
Ver
AT
,
Pangilinan
FC
, et al
.
Impact of COVID-19 vaccination on the risk of developing long-COVID and on existing long-COVID symptoms: a systematic review
.
EClinicalMedicine
.
2022
;
53
:
101624
.
16.
Lee
JH
,
Yim
JJ
,
Park
J
.
Pulmonary function and chest computed tomography abnormalities 6-12 months after recovery from COVID-19: a systematic review and meta-analysis
.
Respir Res
.
2022
;
23
(
1
):
233
.
17.
Arnold
DT
,
Hamilton
FW
,
Milne
A
,
Morley
AJ
,
Viner
J
,
Attwood
M
, et al
.
Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort
.
Thorax
.
2021
;
76
(
4
):
399
401
.
18.
Buonsenso
D
,
Di Giuda
D
,
Sigfrid
L
,
Pizzuto
DA
,
Di Sante
G
,
De Rose
C
, et al
.
Evidence of lung perfusion defects and ongoing inflammation in an adolescent with post-acute sequelae of SARS-CoV-2 infection
.
Lancet Child Adolesc Health
.
2021
;
5
(
9
):
677
80
.
19.
Pretorius
E
,
Vlok
M
,
Venter
C
,
Bezuidenhout
JA
,
Laubscher
GJ
,
Steenkamp
J
, et al
.
Persistent clotting protein pathology in Long COVID/Post-Acute Sequelae of COVID-19 (PASC) is accompanied by increased levels of antiplasmin
.
Cardiovasc Diabetol
.
2021
;
20
(
1
):
172
.
20.
Zollner
A
,
Koch
R
,
Jukic
A
,
Pfister
A
,
Meyer
M
,
Rössler
A
, et al
.
Postacute COVID-19 is characterized by gut viral antigen persistence in inflammatory bowel diseases
.
Gastroenterology
.
2022
;
163
(
2
):
495
506.e8
.
21.
Phetsouphanh
C
,
Darley
DR
,
Wilson
DB
,
Howe
A
,
Munier
CML
,
Patel
SK
, et al
.
Immunological dysfunction persists for 8 months following initial mild-to-moderate SARS-CoV-2 infection
.
Nat Immunol
.
2022
;
23
(
2
):
210
6
.
22.
Hilpert
K
,
Mikut
R
.
Is there a connection between gut microbiome dysbiosis occurring in COVID-19 patients and post-COVID-19 symptoms
.
Front Microbiol
.
2021
;
12
:
732838
.
23.
Vrettou
CS
,
Mantziou
V
,
Vassiliou
AG
,
Orfanos
SE
,
Kotanidou
A
,
Dimopoulou
I
.
Post-intensive care syndrome in survivors from critical illness including COVID-19 patients: a narrative review
.
Life
.
2022
;
12
(
1
):
107
.
24.
de Oliveira
JF
,
de Ávila
RE
,
de Oliveira
NR
,
da Cunha Severino Sampaio
N
,
Botelho
M
,
Gonçalves
FA
, et al
.
Persistent symptoms, quality of life, and risk factors in long COVID: a cross-sectional study of hospitalized patients in Brazil
.
Int J Infect Dis
.
2022
;
122
:
1044
51
.
25.
Legrand
M
,
Fong
N
,
Laouénan
C
,
Ghosn
J
,
Thill
B
,
Faure
K
, et al
.
Risk factors of long term symptoms and outcomes among patients discharged after covid-19: prospective, multicentre observational study
.
BMJ Med
.
2022
;
1
:
e000093
.
26.
Magdy
DM
,
Metwally
A
,
Tawab
DA
,
Hassan
SA
,
Makboul
M
,
Farghaly
S
.
Long-term COVID-19 effects on pulmonary function, exercise capacity, and health status
.
Ann Thorac Med
.
2022
;
17
(
1
):
28
36
.
27.
Mancuzo
EV
,
Marinho
CC
,
Machado-Coelho
GLL
,
Batista
AP
,
Oliveira
JF
,
Andrade
BH
, et al
.
Lung function of patients hospitalized with COVID-19 at 45 days after hospital discharge: first report of a prospective multicenter study in Brazil
.
J Bras Pneumol
.
2021
;
47
(
6
):
e20210162
.
28.
Becker
RC
.
COVID-19-associated vasculitis and vasculopathy
.
J Thromb Thrombolysis
.
2020
;
50
(
3
):
499
511
.
29.
Hama Amin
BJ
,
Kakamad
FH
,
Ahmed
GS
,
Ahmed
SF
,
Abdulla
BA
,
Mohammed
SH
, et al
.
Post COVID-19 pulmonary fibrosis; a meta-analysis study
.
Ann Med Surg
.
2022
;
77
:
103590
.
30.
Zou
JN
,
Sun
L
,
Wang
BR
,
Zou
Y
,
Xu
S
,
Ding
YJ
, et al
.
The characteristics and evolution of pulmonary fibrosis in COVID-19 patients as assessed by AI-assisted chest HRCT
.
PLoS One
.
2021
;
16
(
3
):
e0248957
.
31.
Han
X
,
Fan
Y
,
Alwalid
O
,
Li
N
,
Jia
X
,
Yuan
M
, et al
.
Six-month follow-up chest CT findings after severe COVID-19 pneumonia
.
Radiology
.
2021
;
299
(
1
):
E177
86
.
32.
Faverio
P
,
Luppi
F
,
Rebora
P
,
D’Andrea
G
,
Stainer
A
,
Busnelli
S
, et al
.
One-year pulmonary impairment after severe COVID-19: a prospective, multicenter follow-up study
.
Respir Res
.
2022
;
23
(
1
):
65
.
33.
Frésard
I
,
Genecand
L
,
Altarelli
M
,
Gex
G
,
Vremaroiu
P
,
Vremaroiu-Coman
A
, et al
.
Dysfunctional breathing diagnosed by cardiopulmonary exercise testing in “long COVID” patients with persistent dyspnoea
.
BMJ Open Respir Res
.
2022
;
9
(
1
):
e001126
.
34.
Asadi-Pooya
AA
,
Akbari
A
,
Emami
A
,
Lotfi
M
,
Rostamihosseinkhani
M
,
Nemati
H
, et al
.
Risk factors associated with long COVID syndrome: a retrospective study
.
Iran J Med Sci
.
2021
;
46
(
6
):
428
36
.
35.
Fernández-de-Las-Peñas
C
,
de-la-Llave-Rincón
AI
,
Ortega-Santiago
R
,
Ambite-Quesada
S
,
Gómez-Mayordomo
V
,
Cuadrado
ML
, et al
.
Prevalence and risk factors of musculoskeletal pain symptoms as long-term post-COVID sequelae in hospitalized COVID-19 survivors: a multicenter study
.
Pain
.
2022
;
163
(
9
):
e989
96
.
36.
Yaksi
N
,
Teker
AG
,
Imre
A
.
Long COVID in hospitalized COVID-19 patients: a retrospective cohort study
.
Iran J Public Health
.
2022
;
51
(
1
):
88
95
.
37.
Bai
F
,
Tomasoni
D
,
Falcinella
C
,
Barbanotti
D
,
Castoldi
R
,
Mulè
G
, et al
.
Female gender is associated with long COVID syndrome: a prospective cohort study
.
Clin Microbiol Infect
.
2022
;
28
(
4
):
611.e9
611.e16
.
38.
Puntmann
VO
,
Carerj
ML
,
Wieters
I
,
Fahim
M
,
Arendt
C
,
Hoffmann
J
, et al
.
Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19)
.
JAMA Cardiol
.
2020
;
5
(
11
):
1265
73
.
39.
Mohamed
MO
,
Banerjee
A
.
Long COVID and cardiovascular disease: a learning health system approach
.
Nat Rev Cardiol
.
2022
;
19
(
5
):
287
8
.
40.
Laffey
JG
,
Kavanagh
BP
.
Hypocapnia
.
N Engl J Med
.
2002
;
347
(
1
):
43
53
.
41.
Swenson
ER
.
The unappreciated role of carbon dioxide in ventilation/perfusion matching
.
Anesthesiology
.
2019
;
131
(
2
):
226
8
.
42.
Hu
D
,
Li
J
,
Gao
R
,
Wang
S
,
Li
Q
,
Chen
S
, et al
.
Decreased CO2 levels as indicators of possible mechanical ventilation-induced hyperventilation in COVID-19 patients: a retrospective analysis
.
Front Public Health
.
2020
;
8
:
596168
.
43.
Dheir
H
,
Karacan
A
,
Sipahi
S
,
Yaylaci
S
,
Tocoglu
A
,
Demirci
T
, et al
.
Correlation between venous blood gas indices and radiological involvements of COVID-19 patients at first admission to emergency department
.
Rev Assoc Med Bras
.
2021
;
67
(
Suppl 1
):
51
6
.
44.
Gounidis
A
,
Evangeliou
AP
,
Kloura
C
,
Manganari
E
,
Parisi
C
,
Kourtidis
M
, et al
.
Baseline hypocapnia is associated with intubation in COVID-19 diagnosed patients
.
medRxiv
.
2021
.
45.
Kappelmann
N
,
Dantzer
R
,
Khandaker
GM
.
Interleukin-6 as potential mediator of long-term neuropsychiatric symptoms of COVID-19
.
Psychoneuroendocrinology
.
2021
;
131
:
105295
.
46.
Wynberg
E
,
van Willigen
HDG
,
Dijkstra
M
,
Boyd
A
,
Kootstra
NA
,
van den Aardweg
JG
, et al
.
Evolution of coronavirus disease 2019 (COVID-19) symptoms during the first 12 Months after illness onset
.
Clin Infect Dis
.
2022
;
75
(
1
):
e482
90
.
47.
Luger
AK
,
Sonnweber
T
,
Gruber
L
,
Schwabl
C
,
Cima
K
,
Tymoszuk
P
, et al
.
Chest CT of lung injury 1 year after COVID-19 pneumonia: the CovILD study
.
Radiology
.
2022
;
304
(
2
):
462
70
.
You do not currently have access to this content.